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Reactive oxygen species in reproduction: harmful, essential or both?

Published online by Cambridge University Press:  28 April 2020

M. Jamil Open the ORCID record for M. Jamil [Opens in a new window] ,
H. Debbarh ,
S. Aboulmaouahib ,
O. Aniq Filali ,
K. Mounaji ,
M. Zarqaoui ,
B. Saadani ,
N. Louanjli  and
R. Cadi
M. Jamil*
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology. Department of Biology, Ain Chock Faculty of Sciences, HASSAN II University, Casablanca, Morocco IVF Center IRIFIV, Iris Clinic, Casablanca, Morocco
H. Debbarh
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology. Department of Biology, Ain Chock Faculty of Sciences, HASSAN II University, Casablanca, Morocco
S. Aboulmaouahib
Affiliation:
Labomac IVF Center and Clinical Laboratory Medicine, Casablanca, Morocco
O. Aniq Filali
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology. Department of Biology, Ain Chock Faculty of Sciences, HASSAN II University, Casablanca, Morocco
K. Mounaji
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology. Department of Biology, Ain Chock Faculty of Sciences, HASSAN II University, Casablanca, Morocco
M. Zarqaoui
Affiliation:
IVF Center IRIFIV, Iris Clinic, Casablanca, Morocco
B. Saadani
Affiliation:
IVF Center IRIFIV, Iris Clinic, Casablanca, Morocco
N. Louanjli
Affiliation:
IVF Center IRIFIV, Iris Clinic, Casablanca, Morocco Labomac IVF Center and Clinical Laboratory Medicine, Casablanca, Morocco
R. Cadi
Affiliation:
Laboratory of Molecular Genetic Physiopathology and Biotechnology. Department of Biology, Ain Chock Faculty of Sciences, HASSAN II University, Casablanca, Morocco
*
Author for correspondence: M. Jamil. Laboratory of Molecular Genetic Physiopathology and Biotechnology. Department of Biology, Ain Chock Faculty of Sciences, HASSAN II University, Casablanca, Morocco. E-mail: [email protected]
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Summary

The process of embryonic development is crucial and radically influences preimplantation embryo competence. It involves oocyte maturation, fertilization, cell division and blastulation and is characterized by different key phases that have major influences on embryo quality. Each stage of the process of preimplantation embryonic development is led by important signalling pathways that include very many regulatory molecules, such as primary and secondary messengers. Many studies, both in vivo and in vitro, have shown the importance of the contribution of reactive oxygen species (ROS) as important second messengers in embryo development. ROS may originate from embryo metabolism and/or oocyte/embryo surroundings, and their effect on embryonic development is highly variable, depending on the needs of the embryo at each stage of development and on their environment (in vivo or under in vitro culture conditions). Other studies have also shown the deleterious effects of ROS in embryo development, when cellular tissue production overwhelms antioxidant production, leading to oxidative stress. This stress is known to be the cause of many cellular alterations, such as protein, lipid, and DNA damage. Considering that the same ROS level can have a deleterious effect on the fertilizing oocyte or embryo at certain stages, and a positive effect at another stage of the development process, further studies need to be carried out to determine the rate of ROS that benefits the embryo and from what rate it starts to be harmful, this measured at each key phase of embryonic development.

Keywords

Embryo developmentEmbryo qualityIn vitroOxidative stressReactive oxygen species
Type
Review Article
Information
Zygote , Volume 28 , Issue 4 , August 2020 , pp. 255 - 269
Copyright
© Cambridge University Press 2020

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References

Aboulghar, MA, Mansour, RT, Serour, GI, Amin, YA and Kamal, A (1996). Prospective controlled randomized study of in vitro fertilization versus intracytoplasmic sperm injection in the treatment of tubal factor infertility with normal semen parameters. Presented at the European Society of Human Reproduction and Embryo. Fertil Steril 66, 753–56.CrossRefGoogle Scholar
Adler, V, Yin, Z, Tew, KD and Ronai, Z (1999). Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18, 6104–11.CrossRefGoogle ScholarPubMed
Agarwal, A, Saleh, RA and Bedaiwy, MA (2003). Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 79, 829–43.CrossRefGoogle ScholarPubMed
Agarwal, A, Gupta, S and Sharma, RK (2005). Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 3, 1–21.CrossRefGoogle ScholarPubMed
Agarwal, A, Gupta, S and Sikka, S (2006a). The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol 18, 325–32.CrossRefGoogle ScholarPubMed
Agarwal, A, Said, TM, Bedaiwy, MA, Banerjee, J and Alvarez, JG (2006b). Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 86, 503–12.CrossRefGoogle Scholar
Ahelik, A, Mändar, R, Korrovits, P, Karits, P, Talving, E, Rosenstein, K, Jaagura, M, Salumets, A, and Kullisaar, T (2015). Systemic oxidative stress could predict assisted reproductive technique outcome. J Assist Reprod Genet 32, 699–704.CrossRefGoogle ScholarPubMed
Alam, H, Weck, J, Maizels, E, Park, Y, Lee, EJ, Ashcroft, M and Hunzicker-Dunn, M (2009). Role of the phosphatidylinositol-3-kinase and extracellular regulated kinase pathways in the induction of hypoxia-inducible factor (HIF)-1 activity and the HIF-1 target vascular endothelial growth factor in ovarian granulosa cells in response to follicle-stimulating hormone. Endocrinology 150, 915–28.CrossRefGoogle ScholarPubMed
Allen, GJ, Chu, SP, Harrington, CL, Schumacher, K, Hoffmann, T, Tang, YY, Grill, E and Schroeder, JI (2001). A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411(6841), 1053–7.CrossRefGoogle ScholarPubMed
Almeida, AM, Bertoncini, CR, Borecký, J, Souza-Pinto, NC and Vercesi, AE (2006). Mitochondrial DNA damage associated with lipid peroxidation of the mitochondrial membrane induced by Fe2+-citrate. An Acad Bras Cienc 78, 505–14.CrossRefGoogle ScholarPubMed
Amato, G, Conte, M, Mazziotti, G, Lalli, E, Vitolo, G, Tucker, AT, Bellastella, A, Carella, C and Izzo, A (2003). Serum and follicular fluid cytokines in polycystic ovary syndrome during stimulated cycles. Obstet Gynecol 101, 1177–82.Google ScholarPubMed
Apel, K and Hirt, H (2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Ann Rev Plant Biol 55, 373–99.CrossRefGoogle ScholarPubMed
Appasamy, M, Jauniaux, E, Serhal, P, Al-Qahtani, A, Groome, NP and Muttukrishna, S (2008). Evaluation of the relationship between follicular fluid oxidative stress, ovarian hormones, and response to gonadotropin stimulation. Fertil Steril 89, 912–21.CrossRefGoogle ScholarPubMed
Arat, S, Caputcu, AT, Çevik, M, Akkoc, T, Cetinkaya, G and Bagis, H (2016). Effect of growth factors on oocyte maturation and allocations of inner cell mass and trophectoderm cells of cloned bovine embryos. Zygote 24, 554–62.CrossRefGoogle ScholarPubMed
Artimani, T, Karimi, J, Mehdizadeh, M, Yavangi, M, Khanlarzadeh, E, Ghorbani, M, Asadi, S and Kheiripour, N (2018). Evaluation of pro-oxidant-antioxidant balance (PAB) and its association with inflammatory cytokines in polycystic ovary syndrome (PCOS). Gynecol Endocrinol 34, 148–52.CrossRefGoogle Scholar
Arya, BK, Haq, AU and Chaudhury, K (2012). Oocyte quality reflected by follicular fluid analysis in poly cystic ovary syndrome (PCOS): a hypothesis based on intermediates of energy metabolism. Med Hypotheses 78, 475–8.CrossRefGoogle ScholarPubMed
Augoulea, A, Mastorakos, G, Lambrinoudaki, I, Christodoulakos, G and Creatsas, G (2009). The role of the oxidative-stress in the endometriosis-related infertility. Gynecol Endocrinol 25, 75–81.CrossRefGoogle ScholarPubMed
Augoulea, A, Alexandrou, A, Creatsa, M, Vrachnis, N and Lambrinoudaki, I (2012). Pathogenesis of endometriosis: the role of genetics, inflammation and oxidative stress. Arch Gynecol Obstet 286, 99–103.CrossRefGoogle Scholar
Aurrekoetxea, I, Ruiz-Sanz, JI, del Agua, AR, Navarro, R, Hernández, ML, Matorras, R, Prieto, B and Ruiz-Larrea, MB (2010). Serum oxidizability and antioxidant status in patients undergoing in vitro fertilization. Fertil Steril 94, 1279–86.CrossRefGoogle ScholarPubMed
Babayev, E and Seli, E (2015). Oocyte mitochondrial function and reproduction. Curr Opin Obstet Gynecol 27, 175–81.CrossRefGoogle ScholarPubMed
Bain, NT, Madan, P and Betts, DH (2011). The early embryo response to intracellular reactive oxygen species is developmentally regulated. Reprod Fertil Dev 23, 561–75.CrossRefGoogle ScholarPubMed
Balaban, B, Urman, B, Ata, B, Isiklar, A, Larman, MG, Hamilton, R and Gardner, DK (2008). A randomized controlled study of human day 3 embryo cryopreservation by slow freezing or vitrification: vitrification is associated with higher survival, metabolism and blastocyst formation Hum Reprod 23, 1976–82.CrossRefGoogle ScholarPubMed
Barnhart, K, Dunsmoor-Su, R and Coutifaris, C (2002). Effect of endometriosis on in vitro fertilization. Fertil Steril 77, 1148–55.CrossRefGoogle ScholarPubMed
Barraud-Lange, V, Sifer, C, Pocaté, K, Ziyyat, A, Martin-Pont, B, Porcher, R, Hugues, JN and Wolf, JP (2008). Short gamete co-incubation during in vitro fertilization decreases the fertilization rate and does not improve embryo quality: a prospective auto controlled study. J Assist Reprod Genet 25, 305–10.CrossRefGoogle Scholar
Bedaiwy, MA, Falcone, T, Mohamed, MS, Aleem, AAN, Sharma, RK, Worley, SE, Thornton, J and Agarwal, A (2004). Differential growth of human embryos in vitro: role of reactive oxygen species. Fertil Steril 82, 593–600.CrossRefGoogle ScholarPubMed
Bedaiwy, MA, Mahfouz, RZ, Goldberg, JM, Sharma, R, Falcone, T, Abdel Hafez, MF and Agarwal, A (2010). Relationship of reactive oxygen species levels in day 3 culture media to the outcome of in vitro fertilization/intracytoplasmic sperm injection cycles. Fertil Steril 94, 2037–42.CrossRefGoogle ScholarPubMed
Beg, AA, T. S. Finco, TS, Nantermet, PV and Baldwin, AS (1993). Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκBα: a mechanism for NFκB activation. Mol Cell Biol 13, 3301–10.CrossRefGoogle Scholar
Behl, R and Pandey, RS (2002). FSH induced stimulation of catalase activity in goat granulosa cells in vitro. Anim Reprod Sci 70(3–4), 215–21.CrossRefGoogle ScholarPubMed
Bermejo-Álvarez, P, Lonergan, P, Rizos, D and Gutiérrez-Adan, A (2010). Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis. Reprod BioMed Online 20, 341–9.CrossRefGoogle ScholarPubMed
Berridge, MJ (2009). Inositol trisphosphate and calcium signalling mechanisms. Biochim Biophys Acta – Mol Cell Res 1793, 933–40.CrossRefGoogle ScholarPubMed
Berridge, MJ, Lipp, P and Bootman, MD (2000). The versatility and universality of calcium signalling. Nature Rev Mol Cell Biol 1, 11–21.CrossRefGoogle ScholarPubMed
Berridge, MJ, Bootman, MD and Roderick, HL (2003). Calcium signalling: dynamics, homeostasis and remodelling. Nature Rev Mol Cell Biol 4, 517–29.CrossRefGoogle ScholarPubMed
Betteridge, DJ (2000). What is oxidative stress?’ Metabalism 49(2 Suppl. 1), 3–8.CrossRefGoogle Scholar
Beydola, T, Sharma, RK and Agarwal, A (2014). Sperm preparation and selection techniques. In Medical and Surgical Management of Male Infertility (eds Rizk, BRMB, Aziz, N, Agarwal, A and E Sabanegh, Jr), pp. 244–51. New Delhi: Jaypee Brothers Medical Publishing.Google Scholar
Bhattacharya, S, Hamilton, MP, Shaaban, M, Khalaf, Y, Seddler, M, Ghobara, T, Braude, P, Kennedy, R, Rutherford, A, Hartshorne, G and Templeton, A (2001). Conventional in-vitro fertilisation versus intracytoplasmic sperm injection for the treatment of non-male-factor infertility: a randomised controlled trial. Lancet 357(9274), 2075–9.CrossRefGoogle ScholarPubMed
Blokhina, O, Virolainen, E and Fagerstedt, KV (2003). Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals Bot 91, 179–94.CrossRefGoogle ScholarPubMed
Boitier, E, Rea, R and Duchen, MR (1999). Mitochondria exert a negative feedback on the propagation of intracellular Ca2+ waves in rat cortical astrocytes. J Cell Biol 145, 795–808.CrossRefGoogle ScholarPubMed
Brennan, P and O’Neill, LAJ (1995). Effects of oxidants and antioxidants on nuclear factor κB activation in three different cell lines: evidence against a universal hypothesis involving oxygen radicals. BBA – Gene Struct Express 1260, 167–75.CrossRefGoogle ScholarPubMed
Brookes, PS, Yoon, Y, Robotham, JL, Anders, MW and Sheu, SS (2004). Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol – Cell Physiol 287, C817–33.CrossRefGoogle ScholarPubMed
Cadenas, E and Davies, KJA (2000). Mitochondrial Free Radical Generation, Oxidative Stress, and Aging. Free Radical Biol Med 29(3–4), 222–30.CrossRefGoogle ScholarPubMed
Camello-Almaraz, C, Salido, GM, Pariente, JA and Camello, PJ (2002). Role of mitochondria in Ca2+ oscillations and shape of Ca2+ signals in pancreatic acinar cells. Biochem Pharmacol 63, 283–92.CrossRefGoogle Scholar
Camello-Almaraz, C, Gomez-Pinilla, PJ, Pozo, MJ and Camello, PJ (2006a). Mitochondrial reactive oxygen species and Ca2+ signaling. Am J Physiol – Cell Physiol 291, 1082–88.CrossRefGoogle ScholarPubMed
Camello-Almaraz, MC, Pozo, MJ, Murphy, MP and Camello, PJ (2006b). Mitochondrial production of oxidants is necessary for physiological calcium oscillations. J Cell Physiol 206, 487–94.CrossRefGoogle ScholarPubMed
Carvalho, LF, Samadder, AN, Agarwal, A, Fernandes, LF and Abrão, MS (2012). Oxidative stress biomarkers in patients with endometriosis: systematic review. Arch Gynecol Obstet 286, 1033–40.CrossRefGoogle ScholarPubMed
Catt, JW and Henman, M (2000). Toxic effects of oxygen on human embryo development. Hum Reprod 15(Suppl. 2), 199–206.CrossRefGoogle ScholarPubMed
Cejas, P, Casado, E, Belda-Iniesta, C, De Castro, J, Espinosa, E, Redondo, A, Sereno, M, García-Cabezas, MA, Vara, JA, Domínguez-Cáceres, A, Perona, R and González-Barón, M (2004). Implications of oxidative stress and cell membrane lipid peroxidation in human cancer (Spain). Cancer Causes Control 15, 707–19.CrossRefGoogle Scholar
Celik, E, Celik, O, Kumbak, B, Yilmaz, E, Turkcuoglu, I, Simsek, Y, Karaer, A, Minareci, Y, Ozerol, E and Tanbek, K (2012). A comparative study on oxidative and antioxidative markers of serum and follicular fluid in GnRH agonist and antagonist cycles. J Assist Reprod Genet 29, 1175–83.CrossRefGoogle ScholarPubMed
Cetica, PD, Pintos, LN, Dalvit, GC and Beconi, MT (2001). Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51, 57–64.CrossRefGoogle ScholarPubMed
Chao, HT, Lee, SY, Lee, HM, Liao, TL, Wei, YH and Kao, SH (2005). Repeated ovarian stimulations induce oxidative damage and mitochondrial DNA mutations in mouse ovaries. Ann NY Acad Sci USA 1042, 148–56.CrossRefGoogle ScholarPubMed
Chattopadhayay, R, Ganesh, A, Samanta, J, Jana, SK, Chakravarty, BN and Chaudhury, K (2010). Effect of follicular fluid oxidative stress on meiotic spindle formation in infertile women with polycystic ovarian syndrome. Gynecol Obstet Invest 69, 197–202.CrossRefGoogle ScholarPubMed
Chaube, SK (2001). Role of meiotic maturation regulatory factors in developmental competence of mammalian oocytes. Health Popul Perspect Issues 24, 218–31.Google Scholar
Chen, Q, Vazquez, EJ, Moghaddas, S, Hoppel, CL and Lesnefsky, EJ (2003). Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278, 36027–31.CrossRefGoogle ScholarPubMed
Chen, Y, Lu, H, Liu, Q, Huang, G, Lim, CP, Zhang, L, Hao, A and Cao, X (2012). Function of GRIM-19, a mitochondrial respiratory chain complex I protein, in innate immunity. J Biol Chem 287, 27227–35.CrossRefGoogle ScholarPubMed
Choi, W, Banerjee, J, Agarwal, A, Falcone, T and Sharma, RK (2005). Can vitamin C supplementation reduce oxidative stress induced cytoskeleton damage of mouse oocyte? Fertil Steril 84, S452.CrossRefGoogle Scholar
Chronopoulou, E and Harper, JC (2015). IVF culture media: past, present and future. Hum Reprod Update 21, 39–55.CrossRefGoogle ScholarPubMed
Clark, AR, Stokes, YM, Lane, M and Thompson, JG (2006). Mathematical modelling of oxygen concentration in bovine and murine cumulus–oocyte complexes. Reproduction 131, 999–1006.CrossRefGoogle ScholarPubMed
Combelles, CMH, Gupta, S and Agarwal, A (2009). Could oxidative stress influence the in-vitro maturation of oocytes? Reprod BioMed Online 18, 864–80.CrossRefGoogle ScholarPubMed
Conti, M, Andersen, CB, Richard, FJ, Shitsukawa, K and Tsafriri, A (2002). Role of cyclic nucleotide signaling in oocyte maturation. Mol Cell Endocrinol 187(1–2), 153–9.CrossRefGoogle ScholarPubMed
Corrêa, GA, Rumpf, R, Mundim, TC, Franco, MM and Dode, MA (2008). Oxygen tension during in vitro culture of bovine embryos: effect in production and expression of genes related to oxidative stress. Anim Reprod Sci 104(2–4), 132–42.CrossRefGoogle ScholarPubMed
Coskun, S, Roca, GL, Elnour, AM, al Mayman, H, Hollanders, JM and Jaroudi, KA (1998). Effects of reducing insemination time in human in vitro fertilization and embryo development by using sibling oocytes. J Assist Reprod Genet 15, 605–8.CrossRefGoogle Scholar
Critchley, HO, Osei, J, Henderson, TA, Boswell, L, Sales, KJ, Jabbour, HN and Hirani, N (2006). Hypoxia-inducible factor-1 expression in human endometrium and its regulation by prostaglandin e-series prostanoid receptor 2 (EP2). Endocrinology 147, 744–53.CrossRefGoogle Scholar
Dai, SJ, Qiao, YH, Jin, HX, Xin, Z-M, Su, Y-C, Sun, Y-P and Chian, R-C (2012). Effect of coincubation time of sperm-oocytes on fertilization, embryonic development, and subsequent pregnancy outcome. Syst Biol Reprod Med 58, 348–53.CrossRefGoogle ScholarPubMed
Dalvit, GC, Cetica, PD, Pintos, LN and Beconi, MT (2005). Reactive oxygen species in bovine embryo in vitro production. Biocell 29, 209–12.CrossRefGoogle ScholarPubMed
de los Santos, MJ, Gámiz, P, Albert, C, Galán, A, Viloria, T, Pérez, S, Romero, JL and Remohï, J (2013). Reduced oxygen tension improves embryo quality but not clinical pregnancy rates: a randomized clinical study into ovum donation cycles. Fertil Steril 100, 402–7.CrossRefGoogle Scholar
De Martin, H, Miranda, EP, Cocuzza, MS and Monteleone, PAA (2019). Density gradient centrifugation and swim-up for ICSI: useful, unsafe, or just unsuitable? J Assist Reprod Genet 36, 2421–3.CrossRefGoogle ScholarPubMed
De Munck, N, Janssens, R, Segers, I, Tournaye, H, Van De Velde, H, and Verheyen, G (2019). Influence of ultra-low oxygen (2%) tension on in-vitro human embryo development. Hum Reprod 34, 228–34.CrossRefGoogle ScholarPubMed
de Ziegler, D, Borghese, B and Chapron, C (2010). Endometriosis and infertility: pathophysiology and management. Lancet 376(9742), 730–8.CrossRefGoogle ScholarPubMed
Deguchi, R, Shirakawa, H, Oda, S, Mohri, T and Miyazaki, S (2000). Spatiotemporal analysis of Ca2+ waves in relation to the sperm entry site and animal-vegetal axis during Ca2+ oscillations in fertilized mouse eggs. Dev Biol 218, 299–313.CrossRefGoogle Scholar
Deleuze, S and Goudet, G (2010). Cysteamine supplementation of in vitro maturation media: a review. Reprod Domest Anim 45, 476–82.CrossRefGoogle ScholarPubMed
Dennery, PA (2007). Effects of oxidative stress on embryonic development. Birth Defects Res C Embryo Today 81, 155–62.CrossRefGoogle ScholarPubMed
Diamanti-Kandarakis, E, Paterakis, T, Alexandraki, K, Piperi, C, Aessopos, A, Katsikis, I, Katsilambros, N, Kreatsas, G and Panidis, D (2006). Indices of low-grade chronic inflammation in polycystic ovary syndrome and the beneficial effect of metformin. Hum Reprod 21, 1426–31.CrossRefGoogle ScholarPubMed
Diaz Vivancos, P, Wolff, T, Markovic, J, Pallardó, FV and Foyer, CH (2010). A nuclear glutathione cycle within the cell cycle. Biochem J 431, 169–78.CrossRefGoogle ScholarPubMed
DiLuigi, A, Weitzman, VN, Pace, MC, Siano, LJ, Maier, D and Mehlmann, LM (2008). Meiotic arrest in human oocytes is maintained by a Gs signaling pathway. Biol Reprod 78, 667–72.CrossRefGoogle ScholarPubMed
Dixon, SJ and Stockwell, BR (2014). The role of iron and reactive oxygen species in cell death. Nat Chem Biol 10, 9–17.CrossRefGoogle ScholarPubMed
Downs, SM, Hudson, ER and Hardie, DG (2002). A potential role for AMP-activated protein kinase in meiotic induction in mouse oocytes. Dev Biol 245, 200–12.CrossRefGoogle ScholarPubMed
Dröge, W (2002). Free radicals in the physiological control of cell function. Physiol Rev 82, 47–95.CrossRefGoogle ScholarPubMed
Duchen, MR (2000). Mitochondria and calcium: from cell signalling to cell death. J Physiol 529, 57–68.CrossRefGoogle ScholarPubMed
Ducibella, T and Fissore, R (2008). The roles of Ca2+, downstream protein kinases, and oscillatory signaling in regulating fertilization and the activation of development. Dev Biol 315, 257–79.CrossRefGoogle ScholarPubMed
Ducibella, T, Huneau, D, Angelichio, E, Xu, Z, Schultz, RM, Kopf, GS, Fissore, R, Madoux, S and Ozil, JP (2002). Egg-to-embryo transition is driven by differential responses to Ca2+ oscillation number. Dev Biol 250, 280–91.CrossRefGoogle Scholar
Duleba, AJ and Dokras, A (2012). Is PCOS an inflammatory process?’ Fertil Steril 97, 7–12.CrossRefGoogle Scholar
Dumollard, R, Hammar, K, Porterfield, M, Smith, PJ, Cibert, C, Rouvière, C and Sardet, C (2003). Mitochondrial respiration and Ca2+ waves are linked during fertilization and meiosis completion. Development 130, 683–92.CrossRefGoogle ScholarPubMed
Dumollard, R, Duchen, M and Sardet, C (2006). Calcium signals and mitochondria at fertilisation. Semin Cell Dev Biol 17, 314–23.CrossRefGoogle ScholarPubMed
Dumollard, R, Ward, Z, Carroll, J and Duchen, MR (2007). Regulation of redox metabolism in the mouse oocyte and embryo. Development 134, 455–65.CrossRefGoogle ScholarPubMed
Dumoulin, JCM (2000). Comparison of in-vitro development of embryos originating from either conventional in-vitro fertilization or intracytoplasmic sperm injection. Hum Reprod 15, 402–9.CrossRefGoogle ScholarPubMed
Dumoulin, JC, Meijers, CJ, Bras, M, Coonen, E, Geraedts, JP and Evers, JL (1999). Effect of oxygen concentration on human in vitro fertilization and embryo culture. Hum Reprod 14, 465–9.CrossRefGoogle Scholar
Edwards, LJ, Kind, KL, Armstrong, DT and Thompson, JG (2005). Effects of recombinant human follicle-stimulating hormone on embryo development in mice. Am J Physiol – Endocrinol Metab 288, 845–51.CrossRefGoogle ScholarPubMed
Enkhmaa, D, Kasai, T and Hoshi, K (2009). Long-time exposure of mouse embryos to the sperm produces high levels of reactive oxygen species in culture medium and relates to poor embryo development. Reprod Domest Anim 44, 634–7.CrossRefGoogle ScholarPubMed
Ertzeid, G (2001). The impact of ovarian stimulation on implantation and fetal development in mice. Hum Reprod 16, 221–5.CrossRefGoogle ScholarPubMed
Escobar-Morreale, HF, Luque-Ramírez, M and González, F (2011). Circulating inflammatory markers in polycystic ovary syndrome: a systematic review and metaanalysis. Fertil Steril 95, 1048.CrossRefGoogle ScholarPubMed
Fácio, CL, Previato, LF, Machado-Paula, LA, Matheus, PC and Filho, AE (2016). Comparison of two sperm processing techniques for low complexity assisted fertilization: sperm washing followed by swim-up and discontinuous density gradient centrifugation. J Brasil Reprod Assist 20, 206–11.CrossRefGoogle ScholarPubMed
Favero, TG, Zable, AC and Abramson, JJ (1995). Hydrogen peroxide stimulates the Ca2+ release channel from skeletal muscle sarcoplasmic reticulum. J Biol Chem 270, 25557–63.CrossRefGoogle ScholarPubMed
Feissner, RF, Skalska, J, Gaum, WE and Sheu, SS (2009). Crosstalk signaling between mitochondrial Ca2+ and ROS. Front Biosci 14, 1197–218.CrossRefGoogle ScholarPubMed
Feldman, B, Aizer, A, Brengauz, M, Dotan, K, Levron, J, Schiff, E and Orvieto, R (2017). Pre-implantation genetic diagnosis—should we use ICSI for all?’ J Assist Reprod Genet 34, 1179–83.CrossRefGoogle Scholar
Fenkci, V, Fenkci, S, Yilmazer, M and Serteser, M (2003). Decreased total antioxidant status and increased oxidative stress in women with polycystic ovary syndrome may contribute to the risk of cardiovascular disease. Fertil Steril 80, 123–7.CrossRefGoogle ScholarPubMed
Fernández-González, R, Laguna, R, Ramos-Ibeas, P, Pericuesta, E, Alcalde-Lopez, V, Perez-Cerezales, S, and Gutiérrez-Adan, A (2019). Successful ICSI in mice using caput epididymal spermatozoa. Front Cell Dev Biol 7, 1–5.CrossRefGoogle ScholarPubMed
Finkel, T (2011). Signal transduction by reactive oxygen species. J Cell Biol 194, 7–15.CrossRefGoogle ScholarPubMed
Fischer, B and Bavister, BD (1993). Oxygen tension in the oviduct and uterus of Rhesus monkeys, hamsters and rabbits. J Reprod Fertil 99, 673–9.CrossRefGoogle ScholarPubMed
Fujii, J, Iuchi, Y and Okada, F (2005). Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod Biol Endocrinol 3, 1–10.CrossRefGoogle ScholarPubMed
Fukui, Y, McGowan, LT, James, RW, Pugh, PA and Tervit, HR (1991). Factors affecting the in-vitro development to blastocysts of bovine oocytes matured and fertilized in vitro. J Reprod Fertil 92, 125–31.CrossRefGoogle ScholarPubMed
García-Martínez, S, Sánchez Hurtado, MA, Gutiérrez, H, Sánchez Margallo, FM, Romar, R, Latorre, R, Coy, P and López Albors, O (2018). Mimicking physiological O2 tension in the female reproductive tract improves assisted reproduction outcomes in pig. Mol Hum Reprod 24, 260–70.CrossRefGoogle ScholarPubMed
Gennarelli, G, Carosso, A, Canosa, S, Filippini, C, Cesarano, S, Scarafia, C, Brunod, N, Revelli, A and Benedetto, C (2019). ICSI versus conventional IVF in women aged 40 years or more and unexplained infertility: a retrospective evaluation of 685 cycles with propensity score model. J Clin Med 8, 1694.CrossRefGoogle ScholarPubMed
Gianaroli, L, Fiorentino, A, Cristina Magli, M, Ferraretti, AP and Montanaro, N (1996). Prolonged sperm-oocyte exposure and high sperm concentration affect human embryo viability and pregnancy rate. Hum Reprod 11, 2507–11.CrossRefGoogle ScholarPubMed
Giudice, LC (2010). Clinical practice. Endometriosis. N Engl J Med 362, 2389–99.CrossRefGoogle ScholarPubMed
Gius, D, Botero, A, Shah, S and Curry, HA (1999). Intracellular oxidation/reduction status in the regulation of transcription factors NF-κB and AP-1. Toxicol Lett 106(2–3), 93–106.CrossRefGoogle ScholarPubMed
Goel, P, Goel, AK, Bhatia, AK and Kharche, SD (2017). Influence of exogenous supplementation of IGF-I, cysteamine and their combination on in vitro caprine blastocyst development. Indian J Anim Sci 87, 171–4.Google Scholar
González, F, Rote, NS, Minium, J and Kirwan, JP (2006). Reactive oxygen species-induced oxidative stress in the development of insulin resistance and hyperandrogenism in polycystic ovary syndrome. J Clin Endocrinol Metab 91, 336–40.CrossRefGoogle ScholarPubMed
Goto, Y, Noda, Y, Narimoto, K, Umaoka, Y and Mori, T (1992). Oxidative stress on mouse embryo development in vitro. Free Radical Biol Med 13, 47–53.CrossRefGoogle ScholarPubMed
Goto, Y, Noda, Y, Mori, T and Nakano, M (1993). Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radical Biol Med 15, 69–75.CrossRefGoogle ScholarPubMed
Gruber, I and Klein, M (2011). Embryo culture media for human IVF: which possibilities exist?. J Turk Ger Gynecol Assoc 12, 110–7.CrossRefGoogle ScholarPubMed
Guérin, P, El Mouatassim, S and Ménézo, Y (2001). Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 7, 175–89.CrossRefGoogle ScholarPubMed
Gunter, TE, Buntinas, L, Sparagna, G, Eliseev, R and Gunter, K (2000). Mitochondrial calcium transport: mechanisms and functions. Cell Calcium 28(5–6), 285–96.CrossRefGoogle ScholarPubMed
Gunter, TE, Yule, DI, Gunter, KK, Eliseev, RA and Salter, JD (2004). Calcium and mitochondria. FEBS Lett 567, 96–102.CrossRefGoogle ScholarPubMed
Gupta, MK, Uhm, SJ and Lee, HT (2010). Effect of vitrification and beta-mercaptoethanol on reactive oxygen species activity and in vitro development of oocytes vitrified before or after in vitro fertilization. Fertil Steril 93, 2602–7.CrossRefGoogle ScholarPubMed
Gupta, S, Agarwal, A, Krajcir, N and Alvarez, JG (2006). Role of oxidative stress in endometriosis. Reprod BioMed Online 13, 126–34.CrossRefGoogle ScholarPubMed
Gupta, S, Ghulmiyyah, J, Sharma, R, Halabi, J and Agarwal, A (2014). Power of proteomics in linking oxidative stress and female infertility. BioMed Res Int 2014, 916212.CrossRefGoogle ScholarPubMed
Häcker, H and Karin, M (2006). Regulation and function of IKK and IKK-related kinases. Signal Transduc Knowl Environ 2006, 357.Google ScholarPubMed
Hajnóczky, G, Robb-Gaspers, LD, Seitz, MB and Thomas, AP (1995). Decoding of cytosolic calcium oscillations in the mitochondria. Cell 82, 415–24.CrossRefGoogle ScholarPubMed
Halis, G and Arici, A (2004). Endometriosis and inflammation in infertility. Ann NY Acad Sci 1034, 300–15.CrossRefGoogle ScholarPubMed
Hammadeh, ME, Kühnen, A, Amer, AS, Rosenbaum, P and Schmidt, W (2001). Comparison of sperm preparation methods: effect on chromatin and morphology recovery rates and their consequences on the clinical outcome after in vitro fertilization embryo transfer. Inter J Androl 24, 360–8.CrossRefGoogle ScholarPubMed
Hansford, RG (1994). Physiological role of mitochondrial Ca2+ transport. J Biomembr Bioerg 26, 495–508.CrossRefGoogle ScholarPubMed
Hardy, K (1999). Apoptosis in the human embryo. Rev Reprod 4, 125–34.CrossRefGoogle ScholarPubMed
Harlev, A, Gupta, S and Agarwal, A (2015). Targeting oxidative stress to treat endometriosis. Expert Opin Ther Tar 19, 1447–64.CrossRefGoogle ScholarPubMed
Harvey, AJ, Kind, KL, Pantaleon, M, Armstrong, DT and Thompson, JG (2004). Oxygen-regulated gene expression in bovine blastocysts1. Biol Reprod 71, 1108–19.CrossRefGoogle Scholar
Hashimoto, S, Minami, N, Takakura, R, Yamada, M, Imai, H and Kashima, N (2000a). Low oxygen tension during in vitro maturation is beneficial for supporting the subsequent development of bovine cumulus–oocyte complexes. Mol Reprod Dev 57, 353–60.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Hashimoto, S, Minami, N, Yamada, M and Imai, H (2000b). Excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilization: relevance to intracellular reactive oxygen species and glutathione contents. Mol Reprod Dev 56, 520–6.3.0.CO;2-0>CrossRefGoogle ScholarPubMed
Henkel, RR and Schill, WB (2003). Sperm preparation for ART. Reprod Biol Endocrinol 1, 1–22.CrossRefGoogle ScholarPubMed
Hensley, K, Robinson, KA, Gabbita, SP, Salsman, S and Floyd, RA (2000). Reactive oxygen species, cell signaling, and cell injury. Free Radical Biol Me 28, 1456–62.CrossRefGoogle ScholarPubMed
Hockenbery, DM, Milliman, CL and Korsmeyer, SJ (1994). Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75, 241–51.CrossRefGoogle Scholar
Hoth, M, Fanger, CM and Lewis, RS (1997). Mitochondrial regulation of store-operated calcium signaling in T lymphocytes. J Cell Biol 137, 633–48.CrossRefGoogle ScholarPubMed
Huang, X, Wang, Q, Liu, T, Pei, T, Liu, D, Zhu, H and Huang, W (2019). Body fat indices as effective predictors of insulin resistance in obese/non-obese polycystic ovary syndrome women in the southwest of China. Endocrine 65, 81–5.CrossRefGoogle ScholarPubMed
Iwamoto, M, Onishi, A, Fuchimoto, D, Somfai, T, Takeda, K, Tagami, T, Hanada, H, Noguchi, J, Kaneko, H, Nagai, T and Kikuchi, K (2005). Low oxygen tension during in vitro maturation of porcine follicular oocytes improves parthenogenetic activation and subsequent development to the blastocyst stage. Theriogenology 63, 1277–89.CrossRefGoogle ScholarPubMed
Iwata, K, Yumoto, K, Sugishima, M, Mizoguchi, C, Kai, Y, Iba, Y and Mio, Y (2014). Analysis of compaction initiation in human embryos by using time-lapse cinematography. J Assist Reprod Genet 31, 421–26.CrossRefGoogle ScholarPubMed
Jackson, LW, Schisterman, EF, Dey-Rao, R, Browne, R and Armstrong, D (2005). Oxidative stress and endometriosis. Hum Reprod 20, 2014–20.CrossRefGoogle ScholarPubMed
Jayaraman, V, Upadhya, D, Narayan, PK and Adiga, SK (2012). Sperm processing by swim-up and density gradient is effective in elimination of sperm with DNA damage. J Assist Reprod Genet 29, 557–63.CrossRefGoogle ScholarPubMed
Jellerette, T, He, CL, Wu, H, Parys, JB and Fissore, RA (2000). Down-regulation of the inositol 1,4,5-trisphosphate receptor in mouse eggs following fertilization or parthenogenetic activation. Dev Biol 223, 238–50.CrossRefGoogle ScholarPubMed
Jeong, C-H and Joo, SH (2016). Downregulation of reactive oxygen species in apoptosis. J Cancer Prev 21, 13–20.CrossRefGoogle ScholarPubMed
Jones, DP (2008). Radical-free biology of oxidative stress. Am J Physiol Cell Physiol 295, C849–68.CrossRefGoogle ScholarPubMed
Jones, KT (1998). Protein kinase C action at fertilization: overstated or undervalued? Rev Reprod 3, 7–12.CrossRefGoogle ScholarPubMed
Kaminishi, T. and Kako, KJ (1989). Sensitivity to oxidants of mitochondrial and sarcoplasmic reticular calcium uptake in saponin-treated cardiac myocytes. Basic Res Cardiol 84, 282–90.CrossRefGoogle ScholarPubMed
Karagenc, L, Sertkaya, Z, Ciray, N, Ulug, U and Bahçeci, M (2004). Impact of oxygen concentration on embryonic development of mouse zygotes. Reprod BioMed Online 9, 409–17.CrossRefGoogle ScholarPubMed
Karin, M, Takahashi, T, Kapahi, P, Delhase, M, Chen, Y, Makris, C, Rothwarf, D, Baud, V, Natoli, G, Guido, F and Li, N (2001). Oxidative stress and gene expression: the AP-1 and NF-κB connections. BioFactors 15(2–4), 87–9.CrossRefGoogle ScholarPubMed
Karja, NW, Wongsrikeao, P, Murakami, M, Agung, B, Fahrudin, M, Nagai, T and Otoi, T (2004). Effects of oxygen tension on the development and quality of porcine in vitro fertilized embryos. Theriogenology 62, 1585–95.CrossRefGoogle ScholarPubMed
Karuputhula, NB, Chattopadhyay, R, Chakravarty, B and Chaudhury, K (2013). Oxidative status in granulosa cells of infertile women undergoing IVF. Syst Biol Reprod Med 59, 91–8.CrossRefGoogle ScholarPubMed
Kasterstein, E, Strassburger, D, Komarovsky, D, Bern, O, Komsky, A, Raziel, A, Friedler, S and Ron-El, R (2013). The effect of two distinct levels of oxygen concentration on embryo development in a sibling oocyte study. J Assist Reprod Genet 30, 1073–9.CrossRefGoogle Scholar
Kawamura, K, Kawamura, N, Fukuda, J, Kumagai, J, Hsueh, AJ and Tanaka, T (2007). Regulation of preimplantation embryo development by brain-derived neurotrophic factor. Dev Biol 311, 147–58.CrossRefGoogle ScholarPubMed
Ke, Q and Costa, M (2006). Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 70, 1469–80.CrossRefGoogle Scholar
Kea, B, Gebhardt, J, Watt, J, Westphal, LM, Lathi, RB, Milki, AA, and Behr, B (2007). Effect of reduced oxygen concentrations on the outcome of in vitro fertilization. Fertil Steril 87, 213–6.CrossRefGoogle ScholarPubMed
Keating, D, Cheung, S, Parrella, A, Xie, P, Rosenwaks, Z and Palermo, GD (2019). ICSI from the beginning to where we are today. Global Reprod Health 4, e35.CrossRefGoogle Scholar
Kelly, CC, Lyall, H, Petrie, JR, Gould, GW, Connell, JM and Sattar, N (2001). Low grade chronic inflammation in women with polycystic ovarian syndrome. J Clin Endocrinol Metab 86, 2453–5.CrossRefGoogle ScholarPubMed
Khansari, N, Shakiba, Y and Mahmoudi, M (2009). chronic inflammation and oxidative stress as a major cause of age-related diseases and cancer. Recent Pat Inflamm Allergy Drug Discov 3, 73–80.CrossRefGoogle ScholarPubMed
Khazaei, M and Aghaz, F (2017). Reactive oxygen species generation and use of antioxidants during in vitro maturation of oocytes. Int J Fertil Steril 11, 63–70.Google ScholarPubMed
Kirkegaard, K, Hindkjaer, JJ and Ingerslev, HJ (2013). Effect of oxygen concentration on human embryo development evaluated by time-lapse monitoring. Fertil Steril 99, 738–44.e4.CrossRefGoogle ScholarPubMed
Kitagawa, Y, Suzuki, K, Yoneda, A and Watanabe, T (2004). Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62, 1186–97.CrossRefGoogle Scholar
Kline, D and Kline, JT (1992). Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev Biol 149, 80–9.CrossRefGoogle ScholarPubMed
Kocaman, N (2019). Comparison of the effects of variables in sperm preparation techniques on pregnancy rates in intrauterine insemination. Annal Med Res 26, 2328.CrossRefGoogle Scholar
Koçyiğit, A, Çevik, M, Sen, U and Kuran, M (2015). The effect of macromolecule and growth factor combinations on in vitro development of bovine embryos. Turk J Vet Anim Sci 39, 308–13.CrossRefGoogle Scholar
Konc, J, Kanyó, K, Kriston, R, Somoski, B and Cseh, S (2014). Cryopreservation of embryos and oocytes in human assisted reproduction. BioMed Res Int 2014, 307268.CrossRefGoogle ScholarPubMed
Kono, T, Jones, KT, Bos-Mikich, A, Whittingham, DG and Carroll, J (1996). A cell cycle-associated change in Ca2+ releasing activity leads to the generation of Ca2+ transients in mouse embryos during the first mitotic division. J Cell Biol 132, 915–23.CrossRefGoogle ScholarPubMed
Kovačič, B (2012). Culture systems: low-oxygen culture. Methods Mol Biol 912, 249–72.Google ScholarPubMed
Kovačič, B and Vlaisavljević, V (2008). Influence of atmospheric versus reduced oxygen concentration on development of human blastocysts in vitro: a prospective study on sibling oocytes. Reprod BioMed Online 17, 229–36.CrossRefGoogle ScholarPubMed
Kovačič, B, Sajko, MC and Vlaisavljević, V (2010). A prospective, randomized trial on the effect of atmospheric versus reduced oxygen concentration on the outcome of intracytoplasmic sperm injection cycles. Fertil Steril 94, 511–9.CrossRefGoogle ScholarPubMed
Kowaltowski, AJ and Vercesi, AE (1999). Mitochondrial damage induced by conditions of oxidative stress. Free Radical Biol Med 26(3–4), 463–71.CrossRefGoogle ScholarPubMed
Kubiak, JZ, Ciemerych, MA, Hupalowska, A, Sikora-Polaczek, M and Polanski, Z (2008). On the transition from the meiotic to mitotic cell cycle during early mouse development. Int J Dev Biol 52(2–3), 201–17.CrossRefGoogle ScholarPubMed
Kurzawa, R, Glabowski, W, Baczkowski, T, Wiszniewska, B and Marchlewicz, M (2004). Growth factors protect in vitro cultured embryos from the consequences of oxidative stress. Zygote 12, 231–40.CrossRefGoogle ScholarPubMed
Kwon, HC, Yang, HW, Hwang, KJ, Yoo, JH, Kim, MS, Lee, CH, Ryu, HS and Oh, KS (1999). Effects of low oxygen condition on the generation of reactive oxygen species and the development in mouse embryos cultured in vitro. J Obstet Gynaecol Res 25, 359–66.CrossRefGoogle ScholarPubMed
Lambrinoudaki, IV, Augoulea, A, Christodoulakos, GE, Economou, EV, Kaparos, G, Kontoravdis, A, Papadias, C and Creatsas, G (2009). Measurable serum markers of oxidative stress response in women with endometriosis. Fertil Steril 91, 46–50.CrossRefGoogle ScholarPubMed
Lan, KC, Lin, YC, Chang, YC, Lin, HJ, Tsai, YR and Kang, HY (2019). Limited relationships between reactive oxygen species levels in culture media and zygote and embryo development. J Assist Reprod Genet 36, 325–34.CrossRefGoogle ScholarPubMed
Landolfi, B, Curci, S, Debellis, L, Pozzan, T and Hofer, AM (1998). Ca2+ Homeostasis in the agonist-sensitive internal store: functional interactions between mitochondria and the ER measured in situ in intact cells. J Cell Biol 142, 1235–43.CrossRefGoogle ScholarPubMed
Lane, M and Gardner, DK (2007). Embryo culture medium: which is the best?’ Best Prac Res: Clin Obstet Gynaecol 21, 83–100.CrossRefGoogle Scholar
Lane, M, O’Donovan, MK, Squires, EL, Seidel, GE and Gardner, DK (2001). Protection against reactive oxygen species during mouse preimplantation embryo development: role of edta, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol Reprod Dev 59, 44–53.Google Scholar
Latham, KE (2015). Endoplasmic reticulum stress signaling in mammalian oocytes and embryos: life in balance, vol. 316. Elsevier Ltd.Google Scholar
Layegh, P, Mousavi, Z, Farrokh Tehrani, D, Parizadeh, SM and Khajedaluee, M (2016). Insulin resistance and endocrine-metabolic abnormalities in polycystic ovarian syndrome: comparison between obese and non-obese PCOS patients. Int J Reprod BioMed 14, 263–70.Google ScholarPubMed
Lee, TH, Lee, MS, Liu, CH, Tsao, HM, Huang, CC and Yang, YS (2012). The association between microenvironmental reactive oxygen species and embryo development in assisted reproduction technology cycles. Reprod Sci 19, 725–32.CrossRefGoogle ScholarPubMed
Len, JS, Koh, WSD and Tan, SX (2019). The roles of reactive oxygen species and antioxidants in cryopreservation. Biosci Rep 39, BSR20191601.CrossRefGoogle ScholarPubMed
Lennicke, C, Rahn, J, Lichtenfels, R, Wessjohann, LA and Seliger, B (2015). Hydrogen peroxide – production, fate and role in redox signaling of tumor cells. Cell Commun Signal 13, 1–19.CrossRefGoogle ScholarPubMed
Leoni, GG, Rosati, I, Succu, S, Bogliolo, L, Bebbere, D, Berlinguer, F, Ledda, S and Naitana, S (2007). A low oxygen atmosphere during ivf accelerates the kinetic of formation of in vitro produced ovine blastocysts. Reprod Domest Anim 42, 299–304.CrossRefGoogle ScholarPubMed
Levi-Setti, PE, Patrizio, P and Scaravelli, G (2016). Evolution of human oocyte cryopreservation: slow freezing versus vitrification. Curr Opin Endocrinol, Diabetes Obesity 23, 445–50.CrossRefGoogle ScholarPubMed
Levine, AJ and Puzio-Kuter, AM (2010). The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330(6009), 1340–4.CrossRefGoogle ScholarPubMed
Lewis, A, Hayashi, T, Su, TP and Betenbaugh, MJ (2014). Bcl-2 family in inter-organelle modulation of calcium signaling; roles in bioenergetics and cell survival. J Bioenerg Biomembr 46, 1–15.CrossRefGoogle ScholarPubMed
Li, W, Llopis, J, Whitney, M, Zlokarnik, G and Tsien, RY (1998). Cell-permeant caged InsP3 ester shows that Ca2+ spike frequency can optimize gene expression. Nature 392(6679), 936–41.CrossRefGoogle ScholarPubMed
Lim, J and Luderer, U (2011). Oxidative damage increases and antioxidant gene expression decreases with aging in the mouse ovary. Biol Reprod 84, 775–82.CrossRefGoogle ScholarPubMed
Lincoln, AJ, Wickramasinghe, D, Stein, P, Schultz, RM, Palko, ME, De Miguel, MP, Tessarollo, L and Donovan, PJ (2002). Cdc25b phosphatase is required for resumption of meiosis during oocyte maturation. Nat Genet 30, 446–9.CrossRefGoogle ScholarPubMed
Liou, GY and Storz, P (2010). Reactive oxygen species in cancer. Free Radical Res 44, 479–96.CrossRefGoogle ScholarPubMed
Lopes, AS, Lane, M and Thompson, JG (2010). Oxygen consumption and ROS production are increased at the time of fertilization and cell cleavage in bovine zygotes. Hum Reprod 25, 2762–73.CrossRefGoogle ScholarPubMed
Luberda, Z (2005). The role of glutathione in mammalian gametes. Reprod Biol 5, 5–17.Google ScholarPubMed
Luna, M, Bigelow, C, Duke, M, Ruman, J, Sandler, B, Grunfeld, L and Copperman, AB (2011). Should ICSI be recommended routinely in patients with four or fewer oocytes retrieved? J Assist Reprod Genet 28, 911–5.CrossRefGoogle ScholarPubMed
Malcuit, C, Kurokawa, M and Fissore, RA (2006). Calcium oscillations and mammalian egg activation. J Cell Physiol 206, 565–73.CrossRefGoogle ScholarPubMed
Market-Velker, BA, Denomme, MM and Mann, MR (2012). Loss of genomic imprinting in mouse embryos with fast rates of preimplantation development in culture. Biol Reprod 86, 143–16.CrossRefGoogle ScholarPubMed
Martín-Romero, FJ, Miguel-Lasobras, EM, Domínguez-Arroyo, JA, González-Carrera, E and Alvarez, IS (2008). Contribution of culture media to oxidative stress and its effect on human oocytes. Reprod BioMed Online 17, 652–61.CrossRefGoogle ScholarPubMed
Maybin, JA, Critchley, HOD and Jabbour, HN (2011). Inflammatory pathways in endometrial disorders. Mol Cell Endocrinol 335, 42–51.CrossRefGoogle ScholarPubMed
Mehlmann, LM, Kalinowski, RR, Ross, LF, Parlow, AF, Hewlett, EL and Jaffe, LA (2006). Meiotic resumption in response to luteinizing hormone is independent of a Gi family G protein or calcium in the mouse oocyte. Dev Biol 299, 345–55.CrossRefGoogle ScholarPubMed
Mercurio, F and Manning, AM (1999). Multiple signals converging on NF-κB. Curr Opin Cell Biol 11, 226–32.CrossRefGoogle ScholarPubMed
Meyer, M, Schreck, R and Baeuerle, PA (1993). H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 12, 2005–15.CrossRefGoogle ScholarPubMed
Meyer, M, Pahl, HL and Baeuerle, PA (1994). Regulation of the transcription factors NF-κB and AP-1 by redox changes. Chem Biol Interact 91(2–3), 91–100.CrossRefGoogle ScholarPubMed
Mier-Cabrera, J, Jiménez-Zamudio, L, García-Latorre, E, Cruz-Orozco, O and Hernández-Guerrero, C (2011). Quantitative and qualitative peritoneal immune profiles, T-cell apoptosis and oxidative stress-associated characteristics in women with minimal and mild endometriosis. BJOG 118, 6–16.CrossRefGoogle ScholarPubMed
Migdal, C and Serres, M (2011). Espèces réactives de l’oxygène et stress oxydant [Reactive oxygen species and oxidative stress]. Med Sci (Paris) 27, 405–12.CrossRefGoogle Scholar
Miyazaki, S (2006). Thirty years of calcium signals at fertilization. Semin Cell Dev Biol 17, 233–43.CrossRefGoogle ScholarPubMed
Morales, H, Tilquin, P, Rees, JF, Massip, A, Dessy, F and Van Langendonckt, A (1999). Pyruvate prevents peroxide-induced injury of in vitro preimplantation bovine embryos. Mol Reprod Dev 52, 149–57.3.0.CO;2-4>CrossRefGoogle ScholarPubMed
Morbeck, DE, Krisher, RL, Herrick, JR, Baumann, NA, Matern, D and Moyer, T (2014). Composition of commercial media used for human embryo culture. Fertil Steril 102, 759–66.e9.CrossRefGoogle ScholarPubMed
Morbeck, DE, Baumann, NA and Oglesbee, D (2017). Composition of single-step media used for human embryo culture. Fertil Steril 107, 1055–60.e1.CrossRefGoogle ScholarPubMed
Moreira da Silva, F, Marques, A and Chaveiro, A (2014). Reactive oxygen species: a double-edged sword in reproduction. Open Vet Sci J 4, 127–33.CrossRefGoogle Scholar
Motlík, J and Kubelka, M (1990). Cell-cycle aspects of growth and maturation of mammalian oocytes. Mol. Reprod. Dev 27, 366–75.CrossRefGoogle ScholarPubMed
Mukherjee, A, Malik, H, Saha, AP, Dubey, A, Singhal, DK, Boateng, S, Saugandhika, S, Kumar, S, De, S, Guha, SK and Malakar, D (2014). Resveratrol treatment during goat oocytes maturation enhances developmental competence of parthenogenetic and hand-made cloned blastocysts by modulating intracellular glutathione level and embryonic gene expression. J Assist Reprod Genet 31, 229–39.CrossRefGoogle ScholarPubMed
Murphy, MP (2009). How mitochondria produce reactive oxygen species. Biochem. J 417, 1–13.CrossRefGoogle ScholarPubMed
Murphy, MP (2016). Understanding and preventing mitochondrial oxidative damage. Biochem Soc Trans 44, 1219–26.CrossRefGoogle ScholarPubMed
Nanassy, L, Peterson, CA, Wilcox, AL, Peterson, CM, Hammoud, A and Carrell, DT (2010). Comparison of 5% and ambient oxygen during days 3–5 of in vitro culture of human embryos. Fertil Steril 93, 579–85.CrossRefGoogle ScholarPubMed
Nasr-Esfahani, MM and Johnson, MH (1991). The origin of reactive oxygen species in mouse embryos cultured in vitro. Development 113, 551–60.Google ScholarPubMed
Nastri, CO, Nóbrega, BN, Teixeira, DM, Amorim, J, Diniz, LMM, Barbosa, MWP, Giorgi, VSI, Pileggi, VN and Martins, WP (2016). Low versus atmospheric oxygen tension for embryo culture in assisted reproduction: a systematic review and meta-analysis. Fertil Steril 106, 95–104.e17.CrossRefGoogle ScholarPubMed
Nebreda, AR. and Ferby, I (2000). Regulation of the meiotic cell cycle in oocytes. Curr Opin Cell Biol 12, 666–75.CrossRefGoogle ScholarPubMed
Nejat, EJ, Zapantis, G, Rybak, EA, and Meier, UT (2011). It’s time to pay attention to the endometrium, including the nucleolar channel system. Fertil Steril 96, e165.CrossRefGoogle ScholarPubMed
Ng, KYB, Mingels, R, Morgan, H, Macklon, N and Cheong, Y (2018). In vivo oxygen, temperature and ph dynamics in the female reproductive tract and their importance in human conception: a systematic review. Hum Reprod Update 24, 15–34.CrossRefGoogle ScholarPubMed
Nishikimi, A, Mukai, J and Yamada, M (1999). Nuclear translocation of nuclear factor kappa B in early 1-cell mouse embryos. Biol Reprod 60, 1536–41.CrossRefGoogle ScholarPubMed
Nixon, VL, McDougall, A and Jones, KT (2000). Ca2+ Oscillations and the cell cycle at fertilisation of mammalian and ascidian eggs. Biol Cell 92(3–4), 187–96.CrossRefGoogle ScholarPubMed
Noda, Y, Matsumoto, H, Umaoka, Y, Tatsumi, K, Kishi, J and Mori, T (1991). Involvement of superoxide radicals in the mouse two-cell block. Mol. Reprod. Dev 28, 356–60.CrossRefGoogle ScholarPubMed
Noda, Y, Goto, Y, Umaoka, Y, Shiotani, M, Nakayama, T and Mori, T (1994). Culture of human embryos in alpha modification of eagle’s medium under low oxygen tension and low illumination. Fertil Steril 62, 1022–27.CrossRefGoogle ScholarPubMed
Norris, RP, Ratzan, WJ, Freudzon, M, Mehlmann, LM, Krall, J, Movsesian, MA, Wang, H, Ke, H, Nikolaev, VO and Jaffe, LA (2009). Cyclic GMP from the surrounding somatic cells regulates cyclic AMP and meiosis in the mouse oocyte. Development 136, 1869–78.CrossRefGoogle ScholarPubMed
Nothnick, WB (2001). Treating endometriosis as an autoimmune disease. Fertil Steril 76, 223–31.CrossRefGoogle ScholarPubMed
Ojeda-Ojeda, M, Murri, M, Insenser, M and Escobar-Morreale, H (2013). Mediators of low-grade chronic inflammation in polycystic ovary syndrome (PCOS). Curr Pharmaceut Design 19, 5775–91.CrossRefGoogle Scholar
Opuwari, CS and Henkel, RR (2016). An update on oxidative damage to spermatozoa and oocytes. BioMed Res Int 2016, 9540142.CrossRefGoogle ScholarPubMed
Ozil, JP, Markoulaki, S, Toth, S, Matson, S, Banrezes, B, Knott, JG, Schultz, RM, Huneau, D and Ducibella, T (2005). Egg activation events are regulated by the duration of a sustained Ca2+ Cyt signal in the mouse. Dev Biol 282, 39–54.CrossRefGoogle ScholarPubMed
Paciolla, M, Boni, R, Fusco, F, Pescatore, A, Poeta, L, Ursini, MV, Lioi, MB and Miano, MG (2011). Nuclear factor-kappa-B-inhibitor alpha (NFκBIA) Is a developmental marker of NF-κB/P65 activation during in vitro oocyte maturation and early embryogenesis. Hum Reprod 26, 1191–201.CrossRefGoogle Scholar
Pandey, AN, Tripathi, A, Premkumar, KV, Shrivastav, TG and Chaube, SK (2010). Reactive oxygen and nitrogen species during meiotic resumption from diplotene arrest in mammalian oocytes. J Cell Biochem 111, 521–8.CrossRefGoogle ScholarPubMed
Paria, BC and Dey, SK (1990). Preimplantation embryo development in vitro: cooperative interactions among embryos and role of growth factors. Proc Natl Acad Sci USA 87, 4756–60.CrossRefGoogle ScholarPubMed
Park, JI, Hong, JY, Yong, HY, Hwang, WS, Lim, JM and Lee, ES (2005). High oxygen tension during in vitro oocyte maturation improves in vitro development of porcine oocytes after fertilization. Anim Reprod Sci 87(1–2):133–41.CrossRefGoogle ScholarPubMed
Park, MK, Ashby, MC, Erdemli, G, Petersen, OH and Tepikin, AV (2001). Perinuclear, perigranular and sub-plasmalemmal mitochondria have distinct functions in the regulation of cellular calcium transport. EMBO J 20, 1863–74.CrossRefGoogle ScholarPubMed
Patergnani, S, Suski, JM, Agnoletto, C, Bononi, A, Bonora, M, De Marchi, E, Giorgi, C, Marchi, S, Missiroli, S, Poletti, F, Rimessi, A, Duszynski, J, Wieckowski, MR, and Pinton, P (2011). Calcium signaling around mitochondria associated membranes (MAMs). Cell Commun Signal 9, 1–10.CrossRefGoogle Scholar
Pawelczak, M, Rosenthal, J, Milla, S, Liu, Y-H and Shah, B (2014). Evaluation of the pro-inflammatory cytokine tumor necrosis factor-α in adolescents with polycystic ovary syndrome. PEDADO 27, 356–9.Google ScholarPubMed
Pomeroy, KO and Reed, M (2015). The effect of light on embryos and embryo culture. In (eds Elder, K, van den Bergh, M and Woodward, B), Troubleshooting and Problem-Solving in the IVF Laboratory, pp. 104–16. UK: Cambridge University Press.CrossRefGoogle Scholar
Practice Committees of the American Society for Reproductive Medicine and Society for Assisted Reproductive Technology (2012). Intracytoplasmic sperm injection (ICSI) for non-male factor infertility: a committee opinion. Fertil Steril 98, 1395–9.CrossRefGoogle Scholar
Prasad, S, Tiwari, M, Pandey, AN, Shrivastav, TG, and Chaube, SK (2016). Impact of stress on oocyte quality and reproductive outcome. J Biomed Sci 23, 19–23.CrossRefGoogle ScholarPubMed
Prieto, L, Quesada, JF, Cambero, O, Pacheco, A, Pellicer, A, Codoceo, R and Garcia-Velasco, JA (2012). Analysis of follicular fluid and serum markers of oxidative stress in women with infertility related to endometriosis. Fertil Steril 98, 126–30.CrossRefGoogle ScholarPubMed
Qu, F, Wang, FF, Lu, XE, Dong, MY, Sheng, JZ, Lv, PP, Ding, GL, Shi, BW, Zhang, D, and Huang, HF (2010). Altered aquaporin expression in women with polycystic ovary syndrome: hyperandrogenism in follicular fluid inhibits aquaporin-9 in granulosa cells through the phosphatidylinositol 3-kinase pathway. Hum Reprod 25, 1441–50.CrossRefGoogle ScholarPubMed
Rajani, S, Chattopadhyay, R, Goswami, SK, Ghosh, S, Sharma, S and Chakravarty, B (2012). Assessment of oocyte quality in polycystic ovarian syndrome and endometriosis by spindle imaging and reactive oxygen species levels in follicular fluid and its relationship with IVF-ET outcome. J Hum Reprod Sci 5, 187–93.CrossRefGoogle ScholarPubMed
Ray, PD, Huang, BW and Tsuji, Y (2012). Reactive oxygen species (ROS) homeostasis and redox regulation in cellular signaling. Cell Signal 24, 981–90.CrossRefGoogle ScholarPubMed
Redding, GP, Bronlund, JE and Hart, AL (2007). Mathematical modelling of oxygen transport-limited follicle growth. Reproduction 133, 1095–1106.CrossRefGoogle ScholarPubMed
Ren, SS, Sun, GH, Ku, CH, Chen, DC and Wu, GJ (2004). Comparison of four methods for sperm preparation for IUI. Arch Androl 50, 139–43.CrossRefGoogle ScholarPubMed
Reuter, S, Gupta, SC, Chaturvedi, MM and Aggarwal, BB (2010). Oxidative stress, inflammation, and cancer: how are they linked?’ Free Radical Biol Med 49, 1603–16.CrossRefGoogle Scholar
Rhee, SG (2006). H2O2, a necessary evil for cell signaling. Science 312(5782), 1882–3.CrossRefGoogle ScholarPubMed
Rhee, SG, Kang, SW, Jeong, W, Chang, TS, Yang, KS and Woo, HA (2005). Intracellular messenger function of hydrogen peroxide and its regulation by peroxiredoxins. Curr Opin Cell Biol 17, 183–9.CrossRefGoogle ScholarPubMed
Ricci, G, Perticarari, S, Boscolo, R, Montico, M, Guaschino, S and Presani, G (2009). Semen preparation methods and sperm apoptosis: swim-up versus gradient-density centrifugation technique. Fertil Steril 91, 632–8.CrossRefGoogle ScholarPubMed
Rivera-Egea, R, Garrido, N and Varghese, AC (2019) Sperm processing in assisted reproductive technology. In Nagy, Z, Varghese, A and Agarwal, A (eds) In Vitro Fertilization, pp. 299–312. Springer, Cham.CrossRefGoogle Scholar
Rizzo, A, Roscino, MT, Binetti, F and Sciorsci, RL (2012). Roles of reactive oxygen species in female reproduction. Reprod Domest Anim 47, 344–52.CrossRefGoogle ScholarPubMed
Roderick, HL and Bootman, MD (2003). Bi-directional signalling from the InsP3 receptor: regulation by calcium and accessory factors. Biochem Soc Trans 31, 950–3.CrossRefGoogle ScholarPubMed
Runft, LL, Jaffe, LA and Mehlmann, LM (2002). Egg activation at fertilization: where it all begins. Dev Biol 245, 237–54.CrossRefGoogle ScholarPubMed
Sabatini, L, Wilson, C, Lower, A, Al-Shawaf, T, and Grudzinskas, JG (1999). Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization. Fertil Steril 72, 1027–34.CrossRefGoogle ScholarPubMed
Saito, H, Seino, T, Kaneko, T, Nakahara, K, Toya, M and Kurachi, H (2002). Endometriosis and oocyte quality. Gynecol Obstet Invest 53(Suppl. 1), 46–51.CrossRefGoogle ScholarPubMed
Sakkas, D, Manicardi, GC, Tomlinson, M, Mandrioli, M, Bizzaro, D, Bianchi, PG, and Bianchi, U (2000). The use of two density gradient centrifugation techniques and the swim-up method to separate spermatozoa with chromatin and nuclear DNA anomalies. Hum Reprod 15, 1112–6.CrossRefGoogle ScholarPubMed
Santella, L, Lim, D, and Moccia, F (2004). Calcium and fertilization: the beginning of life. Trends Biochem Sci 29, 400–8.CrossRefGoogle ScholarPubMed
Santiago-Moreno, J, Esteso, MC, Castaño, C, Toledano-Díaz, A, Delgadillo, JA and López-Sebastián, A (2017). Seminal plasma removal by density-gradient centrifugation is superior for goat sperm preservation compared with classical sperm washing. Anim Reprod Sci 181, 141–50.CrossRefGoogle ScholarPubMed
Santos, MA, Kuijk, EW and Macklon, NS (2010). The impact of ovarian stimulation for IVF on the developing embryo. Reproduction 139, 23–34.CrossRefGoogle ScholarPubMed
Saragusty, J and Arav, A (2011). Current progress in oocyte and embryo cryopreservation by slow freezing and vitrification. Reproduction 141, 1–19.CrossRefGoogle ScholarPubMed
Sasaki, H, Hamatani, T, Kamijo, S, Iwai, M and Kobanawa, M (2019). Impact of oxidative stress on age-associated decline in oocyte developmental competence. Front Endocrinol (Lausanne) 10, 811.CrossRefGoogle ScholarPubMed
Sauer, H, Wartenberg, M and Hescheler, J (2001). Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol Biochem 11, 173–86.CrossRefGoogle ScholarPubMed
Schieber, M and Chandel, NS (2014). ROS function in redox signaling and oxidative stress. Curr Biol 24, R453–62.CrossRefGoogle ScholarPubMed
Schoonbroodt, S, Ferreira, V, Best-Belpomme, M, Boelaert, JR, Legrand-Poels, S, Korner, M and Piette, J (2000). Crucial role of the amino-terminal tyrosine residue 42 and the carboxyl-terminal pEST Domain of IκBα in NF-κB activation by an oxidative stress. J Immunol 164, 4292–300.CrossRefGoogle ScholarPubMed
Schreck, R, Rieber, P and Baeuerle, PA (1991). Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-κB transcription factor and HIV-1. EMBO J 10, 2247–58.CrossRefGoogle ScholarPubMed
Schultz, RM and Kopf, GS (1995). Molecular basis of mammalian egg activation. Curr Topics Dev Biol 30(C), 21–62.CrossRefGoogle ScholarPubMed
Seino, T, Saito, H, Kaneko, T, Takahashi, T, Kawachiya, S and Kurachi, H (2002). Eight-hydroxy-2′-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization-embryo transfer program. Fertil Steril 77, 1184–90.CrossRefGoogle Scholar
Shekarriz, M, DeWire, DM, Thomas, AJ and Agarwal, A (1995). A method of human semen centrifugation to minimize the latrogenic sperm injuries caused by reactive oxygen species. Eur Urol 28, 31–5.CrossRefGoogle Scholar
Shuai, HL, Ye, Q, Huang, YH and Xie, BG (2015). Comparison of conventional in vitro fertilisation and intracytoplasmic sperm injection outcomes in patients with moderate oligoasthenozoospermia. Andrologia 47, 499–504.CrossRefGoogle ScholarPubMed
Shulga, N and Pastorino, JG (2012). GRIM-19-mediated translocation of STAT3 to mitochondria is necessary for TNF-induced necroptosis. J Cell Sci 125, 2995–3003.CrossRefGoogle ScholarPubMed
Simpson, PB (2000). The local control of cytosolic Ca2+ as a propagator of CNS communication – integration of mitochondrial transport mechanisms and cellular responses. J Bioenerg Biomembr 32, 5–13.CrossRefGoogle ScholarPubMed
Singh, AK, Chattopadhyay, R, Chakravarty, B and Chaudhury, K (2013). Markers of oxidative stress in follicular fluid of women with endometriosis and tubal infertility undergoing IVF. Reprod Toxicol 42, 116–24.CrossRefGoogle ScholarPubMed
Singh, B, Mal, G, Gautam, SK and Mukesh, M (2019). Cryopreservation of oocytes and embryos. In: Advances in Animal Biotechnology, pp. 97–108. Cham: Springer.CrossRefGoogle Scholar
Sirard, MA, Richard, F and Mayes, M (1998). Controlling meiotic resumption in bovine oocytes: a review. Theriogenology 49, 483–97.CrossRefGoogle ScholarPubMed
Somfai, T, Ozawa, M, Noguchi, J, Kaneko, H, Karja, NWK, Farhudin, M, Dinnyés, A, Nagai, T and Kikuchi, K (2007). Developmental competence of in vitro-fertilized porcine oocytes after in vitro maturation and solid surface vitrification: effect of cryopreservation on oocyte antioxidative system and cell cycle stage. Cryobiology 55, 115–26.CrossRefGoogle ScholarPubMed
Sovernigo, TC, Adona, PR, Monzani, PS, Guemra, S, Barros, FDA, Lopes, FG and Leal, CLV (2017). Effects of supplementation of medium with different antioxidants during in vitro maturation of bovine oocytes on subsequent embryo production. Reprod Domest Anim 52, 561–9.CrossRefGoogle ScholarPubMed
Spanos, S, Becker, DL, Winston, RML and Hardy, K (2000). Anti-apoptotic action of insulin-like growth factor-i during human preimplantation embryo development. Biol Reprod 63, 1413–20.CrossRefGoogle ScholarPubMed
Stimpfel, M, Jancar, N, Vrtacnik-Bokal, E and Virant-Klun, I (2019). Conventional IVF improves blastocyst rate and quality compared to icsi when used in patients with mild or moderate teratozoospermia. Syst Biol Reprod Med 65, 458–64.CrossRefGoogle ScholarPubMed
Stricker, SA (1999). Comparative biology of calcium signaling during fertilization and egg activation in animals. Dev Biol 211, 157–76.CrossRefGoogle ScholarPubMed
Su, YQ and Eppig, JJ (2002). Evidence that multifunctional calcium/calmodulin-dependent protein kinase II (CaM KII) participates in the meiotic maturation of mouse oocytes. Mol Reprod Dev 61, 560–9.CrossRefGoogle ScholarPubMed
Sun, Z and Andersson, R (2002). NF-κB activation and inhibition: a review. Shock 18, 99–106.CrossRefGoogle ScholarPubMed
Suzuki, T and Perry, ACF (2018). Intracytoplasmic sperm injection (ICSI): applications and insights. In (eds Palermo, GD and Sills, ES) Intracytoplasmic Sperm Injection: Indications, Techniques and Applications, pp. 169–81. SpringerCrossRefGoogle Scholar
Swann, K and Yu, Y (2008). The dynamics of calcium oscillations that activate mammalian eggs. Int J Dev Biol 52(5–6), 585–94.CrossRefGoogle ScholarPubMed
Swenson, K, Check, JH, Summers-Chase, D, Choe, JK and Check, ML (2000). A randomized study comparing the effect of standard versus short incubation of sperm and oocyte on subsequent pregnancy and implantation rates following in vitro fertilization embryo transfer. Arch Androl 45, 73–7.Google ScholarPubMed
Szczepańska, M, Koźlik, J, Skrzypczak, J and Mikołajczyk, M (2003). Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 79, 1288–93.CrossRefGoogle ScholarPubMed
Takada, Y, Mukhopadhyay, A, Kundu, GC, Mahabeleshwar, GH, Singh, S and Aggarwal, BB (2003). Hydrogen peroxide activates NF-κB through tyrosine phosphorylation of IκBα and serine phosphorylation of p65: evidence for the involvement of IκBα kinase and Syk protein-tyrosine kinase. J Biol Chem 278, 24233–41.CrossRefGoogle ScholarPubMed
Tamura, H, Takasaki, A, Miwa, I, Taniguchi, K, Maekawa, R, Asada, H, Taketani, T, Matsuoka, A, Yamagata, Y, Shimamura, K, Morioka, H, Ishikawa, H, Reiter, RJ, and Sugino, N (2008). Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 44, 280–7.CrossRefGoogle ScholarPubMed
Tannus, S, Son, WY, Gilman, A, Younes, G, Shavit, T and Dahan, MH (2017). The role of intracytoplasmic sperm injection in non-male factor infertility in advanced maternal age. Hum Reprod 32, 119–24.Google ScholarPubMed
Tatemoto, H, Sakurai, N and Muto, N (2000). Protection of porcine oocytes against apoptotic cell death caused by oxidative stress during in vitro maturation: role of cumulus cells. Biol Reprod 63, 805–10.CrossRefGoogle ScholarPubMed
Thannickal, VJ and Fanburg, BL (2000). Invited review reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279, 1005–28.CrossRefGoogle Scholar
Thisse, B and Thisse, C (2005). Functions and regulations of fibroblast growth factor signaling during embryonic development. Dev Biol 287, 390–402.CrossRefGoogle ScholarPubMed
Thomas, M, Jain, S, Kumar, GP and Laloraya, M (1997). A programmed oxyradical burst causes hatching of mouse blastocysts. J Cell Sci 110, 1597–602.Google ScholarPubMed
Thongkittidilok, C, Tharasanit, T, Songsasen, N, Sananmuang, T, Buarpung, S and Techakumphu, M (2015). Epidermal growth factor improves developmental competence and embryonic quality of singly cultured domestic cat embryos. J Reprod Dev 61, 269–76.CrossRefGoogle ScholarPubMed
Tiwari, M, Prasad, S, Shrivastav, TG and Chaube, SK (2017). Calcium signaling during meiotic cell cycle regulation and apoptosis in mammalian oocytes. J Cell Physiol 232, 976–81.CrossRefGoogle ScholarPubMed
Tournaye, H, Verheyen, G, Albano, C, Camus, M, Van Landuyt, L, Devroey, P and Van Steirteghem, A (2002). Intracytoplasmic sperm injection versus in vitro fertilization: a randomized controlled trial and a meta-analysis of the literature. Fertil Steril 78, 1030–7.CrossRefGoogle Scholar
Tranguch, S, Steuerwald, N and Huet-Hudson, YM (2003). Nitric oxide synthase production and nitric oxide regulation of preimplantation embryo development. Biol Reprod 68, 1538–44.CrossRefGoogle ScholarPubMed
Tripathi, A, Kumar, KVP and Chaube, SK (2010). Meiotic cell cycle arrest in mammalian oocytes. J. Cell. Physiol. 223, 592–600.Google ScholarPubMed
Truong, T and Gardner, DK (2017). Antioxidants improve IVF outcome and subsequent embryo development in the mouse. Hum Reprod 32, 2404–13.CrossRefGoogle ScholarPubMed
Uhlén, P and Fritz, N (2010). Biochemistry of calcium oscillations. Biochem Biophys Res Commun 396, 28–32.CrossRefGoogle ScholarPubMed
Vaccari, S, Weeks, JL, Hsieh, M, Menniti, FS and Conti, M (2009). Cyclic GMP signaling is involved in the luteinizing hormone-dependent meiotic maturation of mouse oocytes. Biol Reprod 81, 595–604.CrossRefGoogle ScholarPubMed
van den Berg, R, Haenen, GRMM, van den Berg, H and Bast, A (2001). Transcription factor NF-κB as a potential biomarker for oxidative stress. Br J Nutr 86(S1), S121–27.CrossRefGoogle ScholarPubMed
van der Westerlaken, L, Helmerhorst, F, Dieben, S and Naaktgeboren, N (2005). Intracytoplasmic sperm injection as a treatment for unexplained total fertilization failure or low fertilization after conventional in vitro fertilization. Fertil Steril 83, 612–7.CrossRefGoogle ScholarPubMed
Van Langendonckt, A, Casanas-Roux, F and Donnez, J (2002). Oxidative stress and peritoneal endometriosis. Fertil Steril 77, 861–70.CrossRefGoogle ScholarPubMed
Van Montfoort, APA, Arts, EGJM, Wijnandts, L, Sluijmer, A, Pelinck, M-J, Land, JA and Van Echten-Arends, J (2020). Reduced oxygen concentration during human ivf culture improves embryo utilization and cumulative pregnancy rates per cycle. Hum Reprod Open 2020, hoz036.CrossRefGoogle ScholarPubMed
Vanden Meerschaut, F, Nikiforaki, D, Heindryckx, B and De Sutter, P (2014). Assisted oocyte activation following ICSI fertilization failure. Reprod BioMed Online 28, 560–71.CrossRefGoogle ScholarPubMed
Veal, EA, Day, AM and Morgan, BA (2007). Hydrogen peroxide sensing and signaling. Mol Cell 26, 1–14.CrossRefGoogle ScholarPubMed
Verit, FF, Erel, O and Celik, H (2008). Paraoxonase-1, activity in patients with hyperemesis gravidarum. Redox Report 13, 134–8.CrossRefGoogle ScholarPubMed
Victor, VM, Rocha, M, Bañuls, C, Sanchez-Serrano, M, Sola, E, Gomez, M and Hernandez-Mijares, A (2009). Mitochondrial complex I impairment in leukocytes from polycystic ovary syndrome patients with insulin resistance. J Clin Endocrinol Metab 94, 3505–12.CrossRefGoogle ScholarPubMed
Volpes, A, Sammartano, F, Rizzari, S, Gullo, S, Marino, A and Allegra, A (2016). The pellet swim-up is the best technique for sperm preparation during in vitro fertilization procedures. J Assist Reprod Genet 33, 765–70.CrossRefGoogle ScholarPubMed
Wallingford, JB, Ewald, AJ, Harland, RH and Fraser, SE (2001). Calcium signaling during convergent extension in Xenopus. Curr Biol 11, 652–61.CrossRefGoogle ScholarPubMed
Wang, J, Deng, X, Yang, Y, Yang, X, Kong, B and Chao, L (2016). Expression of GRIM-19 in adenomyosis and its possible role in pathogenesis. Fertil Steril 105, 1093–101.CrossRefGoogle ScholarPubMed
Whitaker, M (2006). Calcium at fertilization and in early development. Physiol Rev 86, 25–88.CrossRefGoogle ScholarPubMed
Wong, KM, Mastenbroek, S and Repping, S (2014). Cryopreservation of human embryos and its contribution to in vitro fertilization success rates. Fertil Steril 102, 19–26.CrossRefGoogle ScholarPubMed
Yamanaka, M, Tomita, K, Hashimoto, S, Matsumoto, H, Satoh, M, Kato, H, Hosoi, Y, Inoue, M, Nakaoka, Y and Morimoto, Y (2016). Combination of density gradient centrifugation and swim up method effectively decreases morphogically abnormal sperms. J Reprod Dev 62, 599–606.CrossRefGoogle Scholar
Yang, D, Shahata, MA, al-Bader, M, al-Natsha, SD, al-Flamerzia, M and al-Shawaf, T (1996). Intracytoplasmic sperm injection improving embryo quality comparison of the sibling oocytes of non-male-factor couples. J Assist Reprod Genet 13, 351–5.CrossRefGoogle ScholarPubMed
Yang, HW, Hwang, KJ, Kwon, HC, Kim, HS, Choi, KW and Oh, KS (1998). Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod 13, 998–1002.CrossRefGoogle ScholarPubMed
Yilmaz, N, Inal, HA, Gorkem, U, Sargin Oruc, A, Yilmaz, S and Turkkani, A (2016). Follicular fluid total antioxidant capacity levels in PCOS. J Obstet Gynaecol 36, 654–7.CrossRefGoogle ScholarPubMed
Younglai, EV, Holt, D, Brown, P, Jurisicova, A and Casper, RF (2001). Sperm swim-up techniques and DNA fragmentation. Hum Reprod 16, 1950–3.CrossRefGoogle ScholarPubMed
Younis, A, Clower, C, Nelsen, D, Butler, W, Carvalho, A, Hok, E and Garelnabi, M (2012). The relationship between pregnancy and oxidative stress markers on patients undergoing ovarian stimulations. J Assist Reprod Genet 29, 1083–9.CrossRefGoogle ScholarPubMed
Yu, B, Zhou, H, Liu, M, Zheng, T, Jiang, L, Zhao, M, Xu, X and Huang, Z (2015). Epigenetic alterations in density selected human spermatozoa for assisted reproduction. PLoS ONE 10, 1–16.CrossRefGoogle ScholarPubMed
Yuan, YQ, Van Soom, A, Coopman, FOJ, Mintiens, K, Boerjan, ML, Van Zeveren, A, De Kruif, A and Peelman, LJ (2003). Influence of oxygen tension on apoptosis and hatching in bovine embryos cultured in vitro. Theriogenology 59, 1585–96.CrossRefGoogle ScholarPubMed
Zalba, G, San José, G, Moreno, MU, Fortuño, MA, Fortuño, A, Beaumont, FJ and Díez, J (2001). Oxidative stress in arterial hypertension role of NAD(P)H oxidase. Hypertension 38, 1395–9.CrossRefGoogle ScholarPubMed
Zeeshan, HM, Lee, GH, Kim, HR and Chae, HJ (2016). Endoplasmic reticulum stress and associated ROS. Int J Mol Sci 17, 1–20.CrossRefGoogle ScholarPubMed
Zhang, J, Wang, X, Vikash, V, Ye, Q, Wu, D, Liu, Y and Dong, W (2016). ROS and ROS-mediated cellular signaling. Oxid Med Cell Longev 2016, 4350965.CrossRefGoogle ScholarPubMed
Zhang, M, Ouyang, H and Xia, G (2009). The signal pathway of gonadotrophins-induced mammalian oocyte meiotic resumption. Mol Hum Reprod 15, 399–409.CrossRefGoogle ScholarPubMed
Zhang, XD, Liu, JX, Liu, WW, Gao, Y, Han, W, Xiong, S and Wu, LH (2013). Time of insemination culture and outcomes of in vitro fertilization : a systematic review and meta-analysis. Human Reprod Update 19, 685–95.CrossRefGoogle ScholarPubMed
Zhao, Y, Zhang, C, Huang, Y, Yu, Y, Li, R, Li, M, Liu, N, Liu, P and Qiao, J (2015). Upregulated expression of Wnt5a increases inflammation and oxidative stress via PI3K/AKT/NFκB signaling in the granulosa cells of PCOS patients. J Clin Endocrinol Metab 100, 201–11.CrossRefGoogle Scholar
Zribi, N, Feki Chakroun, N, El Euch, H, Gargouri, J, Bahloul, A and Ammar Keskes, L (2010). Effects of cryopreservation on human sperm deoxyribonucleic acid integrity. Fertil Steril 93, 159–66.CrossRefGoogle ScholarPubMed