Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T05:10:30.390Z Has data issue: false hasContentIssue false
  • English
  • Français

The importance of manganese in the cytoplasmic maturation of cattle oocytes: blastocyst production improvement regardless of cumulus cells presence during in vitro maturation

Published online by Cambridge University Press:  24 February 2015

Juan Patricio Anchordoquy ,
Juan Mateo Anchordoquy ,
Matias Angel Sirini ,
Juan Alberto Testa ,
Pilar Peral-García  and
Cecilia Cristina Furnus
Juan Patricio Anchordoquy
Affiliation:
Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina. Cátedra de Fisiología, Laboratorio de Nutrición Mineral, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina.
Juan Mateo Anchordoquy
Affiliation:
Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina. Cátedra de Fisiología, Laboratorio de Nutrición Mineral, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina.
Matias Angel Sirini
Affiliation:
Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina. Cátedra de Fisiología, Laboratorio de Nutrición Mineral, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina.
Juan Alberto Testa
Affiliation:
Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina. Cátedra de Fisiología, Laboratorio de Nutrición Mineral, Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina.
Pilar Peral-García
Affiliation:
Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina.
Cecilia Cristina Furnus*
Affiliation:
Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina. Cátedra de Citología, Histología y Embriología ‘A’, Facultad de Ciencias Médicas, Universidad Nacional de La Plata, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina.
*
All correspondence to: Cecilia Cristina Furnus. Instituto de Genética Veterinaria Prof. Fernando N. Dulout (IGEVET), Facultad de Ciencias Veterinarias, Universidad Nacional de La Plata – CONICET, calle 60 y 118 s/n, CP (1900), La Plata, Buenos Aires, Argentina. Tel:/Fax: +54 0221 421 1799. e-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Adequate dietary intake of manganese (Mn) is required for normal reproductive performance in cattle. This study was carried out to investigate the effect of Mn during in vitro maturation of bovine cumulus–oocyte complexes (COC) on apoptosis of cumulus cells, cumulus expansion, and superoxide dismutase (SOD) activity in the COC. The role of cumulus cells on Mn transport and subsequent embryo development was also evaluated. Early apoptosis decreased in cumulus cells matured with Mn compared with medium alone. Cumulus expansion did not show differences in COC matured with or without Mn supplementation. SOD activity was higher in COC matured with 6 ng/ml Mn than with 0 ng/ml Mn. Cleavage rates were higher in COC and denuded oocytes co-cultured with cumulus cells, either with or without Mn added to in vitro maturation (IVM) medium. Regardless of the presence of cumulus cells during IVM, the blastocyst rates were higher when 6 ng/ml Mn was supplemented into IVM medium compared with growth in medium alone. Blastocyst quality was enhanced when COC were matured in medium with Mn supplementation. The results of the present study indicated that Mn supplementation to IVM medium enhanced the ‘health’ of COC, and improved subsequent embryo development and embryo quality.

Keywords

Cumulus cellsCumulus expansionEmbryo developmentManganeseSuperoxide dismutase
Type
Research Article
Information
Zygote , Volume 24 , Issue 1 , February 2016 , pp. 139 - 148
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anchordoquy, J.P., Anchordoquy, J.M., Sirini, M.A., Mattioli, G., Picco, S.J. & Furnus, C.C. (2013). Effect of different manganese concentrations during in vitro maturation of bovine oocytes on DNA integrity of cumulus cells and subsequent embryo development. Reprod. Domest. Anim. 48, 905–11.CrossRefGoogle ScholarPubMed
Anchordoquy, J.P., Anchordoquy, J.M., Picco, S.J., Sirini, M.A., Errecalde, A.L. & Furnus, C.C. (2014). Influence of manganese on apoptosis and glutathione content of cumulus cells during in vitro maturation in bovine oocytes. Cell. Biol. Int. 38, 246–53.CrossRefGoogle ScholarPubMed
Aschner, J.L. & Aschner, M. (2005). Nutritional aspects of manganese homeostasis. Mol. Aspects 26, 353–62.CrossRefGoogle ScholarPubMed
Aschner, M. & Gannon, M. (1994). Manganese (Mn) transport across the rat blood–brain barrier: saturable and transferrin-dependent transport mechanisms. Brain Res. Bull. 33, 345–9.CrossRefGoogle ScholarPubMed
Au, C., Benedetto, A. & Aschner, M. (2008). Manganese transport in eukaryotes: the role of DMT1. Neuro Toxicol. 29, 569–76.Google ScholarPubMed
Bentley, O.G. & Phillips, P.H. (1951). The effect of low manganese rations upon dairy cattle. J. Dairy Sci. 34, 396–403.CrossRefGoogle Scholar
Chen, L., Mao, S.J. & Larsen, W.J. (1992). Identification of a factor in fetal bovine serum that stabilizes the cumulus extracellular matrix. A role for a member of the inter-alpha-trypsin inhibitor family. J. Biol. Chem. 267, 12380–6.CrossRefGoogle ScholarPubMed
Chian, R.C., Niwa, K. & Sirard, M.A. (1994). Effect of cumulus cells on the male pronuclear formation and subsequent early development of bovine oocytes in vitro . Theriogenology 41, 1499–508.CrossRefGoogle ScholarPubMed
Chihuailaf, R., Contreras, P.A. & Wittwer, F. (2002). Patogénesis del estrés oxidativo: consecuencias y evaluación en salud animal. [Oxidative stress pathogenesis: consequences and animal health evaluation.] Vet. Méx. 33, 265–83.Google Scholar
Davidsson, L., Lonnerdal, B., Sandstrom, B., Kunz, C. & Keen, C.L. (1989). Identification of transferrin as the major plasma carrier protein for manganese introduced orally or intravenously or after in vitro addition in the rat. J. Nutr. 119, 1461–4.CrossRefGoogle ScholarPubMed
De Angelis, P.L. (1999). Hyaluronan synthases: fascinating glycosyltransferases from vertebrates, bacterial pathogens, and algal viruses. Cell Mol. Life Sci. 56, 670–82.CrossRefGoogle ScholarPubMed
de Matos, D.G., Furnus, C.C. & Moses, D.F. (1997). Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol. Reprod. 57, 1420–5.CrossRefGoogle ScholarPubMed
Dekel, N. & Beers, W. (1980). Development of the rat oocyte in vitro: inhibition and induction of maturation in the presence or absence of the cumulus oophorus. Dev. Biol. 75, 247–54.CrossRefGoogle ScholarPubMed
Edson, M.A., Nagaraja, A.K. & Matzuk, M.M. (2009). The mammalian ovary from genesis to revelation. Endocr. Rev. 30, 624–712.CrossRefGoogle ScholarPubMed
Epperly, M.W., Sikora, C.A., DeFilippi, S.J., Gretton, J.E., Zhan, Q., Kufe, D.W. & Greenberger, J.S. (2002). Manganese superoxide dismutase (SOD2) inhibits radiation-induced apoptosis by stabilization of the mitochondrial membrane. Radiat. Res. 157, 568–77.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1979). FSH stimulates hyaluronic acid synthesis by oocyte–cumulus cell complexes from mouse preovulatory follicles. Nature 281, 483–4.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1982). The relationship between cumulus cell oocyte coupling, oocyte meiotic maturation, and cumulus expansion. Dev. Biol. 89, 268–72.CrossRefGoogle ScholarPubMed
Eppig, J.J. (1991). Intercommunication between mammalian oocytes and companion somatic cells. Bioessays 13, 569–74.CrossRefGoogle ScholarPubMed
Eppig, J.J. & Downs, S.M. (1984). Chemical signals that regulate mammalian oocyte maturation. Biol. Reprod. 30, 1–11.CrossRefGoogle ScholarPubMed
Forrest, H.N. (1993). Ultratrace Minerals. In Shils, M.E., Olson, J.A. & Shike, M. (eds), Modern Nutrition in Health and Disease, 8th edn, pp. 269–86. Philadelphia: Lea & Febiger.Google Scholar
Furnus, C.C., de Matos, D.G. & Moses, D.F. (1998). Cumulus expansion during in vitro maturation of bovine oocytes: relationship with intracellular glutathione level and its role on subsequent embryo development. Mol. Reprod. Dev. 51, 76–83.3.0.CO;2-T>CrossRefGoogle ScholarPubMed
Gardner, D.K., Lane, M., Spitzer, A. & Batt, P.A. (1994). Enhanced rates of cleavage and development for sheep zygotes cultured to the blastocyst stage in vitro in the absence of serum and somatic cells: amino acids, vitamins, and culturing embryos in groups stimulate development. Biol. Reprod. 50, 390–400.CrossRefGoogle Scholar
Garrick, M.D., Dolan, K.G., Horbinski, C., Ghio, A.J., Higgins, D., Porubcin, M., Moore, E.G., Hainsworth, L.N., Umbreit, J.N., Conrad, M.E., Feng, L., Lis, A., Roth, J.A., Singleton, S., & Garrick, L.M. (2003). DMT1: a mammalian transporter for multiple metals. Biometals 16, 41–54.CrossRefGoogle ScholarPubMed
Ge, L., Han, D., Lan, G.C., Zhou, P., Liu, Y., Zhang, X., Sui, H.S. & Tan, J.H. (2008). Factors affecting the in vitro action of cumulus cells on the maturing mouse oocytes. Mol. Reprod. Dev. 75, 136–42.CrossRefGoogle ScholarPubMed
Gibbons, R.A., Dixon, S.N., Hallis, K., Russell, A.M., Sansom, B.F. & Symonds, H.W. (1976). Manganese metabolism in cows and goats. Biochim Biophys Acta 444, 1–10.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Ritter, L.J. & Armstrong, D.T. (2004). Oocyte–somatic cell interactions during follicle development in mammals. Anim. Reprod. Sci. 82, 431–46.CrossRefGoogle ScholarPubMed
Gilchrist, R.B., Lane, M. & Thompson, J.G. (2008). Oocyte-secreted factors: regulators of cumulus cell function and oocyte quality. Hum. Reprod. Update 14, 159–77.CrossRefGoogle ScholarPubMed
Glander, H.J. & Schaller, J. (1999). Binding of annexin V to plasma membranes of human spermatozoa: a rapid assay for detection of membrane changes after cryostorage. Mol. Hum. Reprod. 5, 109–15.CrossRefGoogle ScholarPubMed
Goud, P.T., Goud, A.P., Qian, C., Laverge, H., Van der Elst, J., De Sutter, P. & Dhont, M. (1998). In-vitro maturation of human germinal vesicle stage oocytes: role of cumulus cells and epidermal growth factor in the culture medium. Hum. Reprod. 13, 1638–44.CrossRefGoogle ScholarPubMed
Gunshin, H., Mackenzie, B., Berger, U.V., Gunshin, Y., Romero, M.F., Boron, W.F., Nussbeger, S., Gollan, J.L. & Hediger, M.A. (1997). Cloning and characterization of a mammalian proton-coupled metal–ion transporter. Nature 388 (6641), 482–8.CrossRefGoogle ScholarPubMed
Kincaid, R.L. (1999). Assessment of trace mineral status of ruminants: a review. Proc. Am. Soc. Anim. Sci. 1999, 1–10. Available at: http://www.org/jas/symposia/proceedings/0930.pdf.Google Scholar
Hampton, M.B. & Orrenius, S. (1997). Dual regulation of caspase activity by hydrogen peroxide: implications for apoptosis. FEBS Lett. 414, 552–6.CrossRefGoogle ScholarPubMed
Hansen, S.L., Spears, J.W., Lloyd, K.E. & Whisnant, C.S. (2006). Growth, reproductive performance, and manganese status of heifers fed varying concentrations of manganese. J. Anim. Sci. 84, 3375–80.CrossRefGoogle ScholarPubMed
He, L., Girijashanker, K., Dalton, T.P., Reed, J., Li, H., Soleimani, M. & Nerbert, D.W. (2006). ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol. Pharmacol. 70, 171–180.CrossRefGoogle ScholarPubMed
Himeno, S., Yanagiya, T. & Fujishiro, H. (2009). The role of zinc transporters in cadmium and manganese transport in mammalian cells. Biochimie. 91, 1218–22.CrossRefGoogle ScholarPubMed
Holley, A.K., Bakthavatchalu, V., Velez-Roman, J.M. & St Clair, D.K. (2011). Manganese superoxide dismutase: guardian of the powerhouse. Int. J. Mol. Sci. 12, 7114–62.CrossRefGoogle ScholarPubMed
Ikeda, S., Imai, H. & Yamada, M. (2003). Apoptosis in cumulus cells during in vitro maturation of bovine cumulus-enclosed oocytes. Reproduction 125, 369–76.CrossRefGoogle ScholarPubMed
Keen, C.L., Ensunsa, J.L., Lönnerdal, , Zidenberg-Cherr, S. (2009). Manganese. In Caballero, B. (editor), Guide to Nutritional Supplements. Oxford, UK: Elsevier, pp. 256–63.Google Scholar
Keller, J.N., Kindy, M.S., Holtsberg, F.W., St Clair, D.K., Yen, H.C., Germeyer, A., Steiner, S.M., Bruce-Keller, A.J., Hutchins, J.B. & Mattson, M.P. (1998). Mitochondrial manganese superoxide dismutase prevents neural apoptosis and reduces ischemic brain injury: suppression of peroxynitrite production, lipid peroxidation, and mitochondrial dysfunction. J. Neurosci. 18, 687–97.CrossRefGoogle ScholarPubMed
Kim, J., Buckett, P.D. & Wessling-Resnick, M. (2013). Absorption of manganese and iron in a mouse model of hemochromatosis. PLoS One 8:e64944.CrossRefGoogle Scholar
Kim, S.K., Minami, N., Yamada, M. & Utsumi, K. (1996). Functional role of cumulus cells during maturation in development of in vitro matured and fertilized bovine oocytes. Theriogenology 45, 278.CrossRefGoogle Scholar
Kinoshita, M., Sakamoto, T., Kashio, A., Shimizu, T. & Yamasoba, T. (2013). Age-related hearing loss in Mn-SOD heterozygous knockout mice. Oxid. Med. Cell Longev. doi: 10.1155/2013/325702.CrossRefGoogle Scholar
Larsen, W.J. & Wert, S.E. (1988). Role of cell junctions in gametogenesis and in early embryonic development. Tiss. Cell. 20, 809–48.CrossRefGoogle ScholarPubMed
Larsen, W.J. (1989). Mechanisms of gap junction modulation. In Sperelakis, N. & Cole, W.C., Cell Interactions and Gap Junctions vol. I, pp. 3–27. Boca Raton, FL: CRC Press.Google Scholar
Lodde, V., Modina, S., Galbusera, C., Franciosi, F. & Luciano, A.M. (2007). Large-scale chromatin remodeling in germinal vesicle bovine oocytes: interplay with gap junction functionality and developmental competence. Mol. Reprod. Dev. 74, 740–9.CrossRefGoogle ScholarPubMed
Lonergan, P., Monaghan, P., Rizos, D., Boland, M.P. & Gordon, I. (1994). Effect of follicle size on bovine oocyte quality and developmental competence following maturation, fertilization, and culture in vitro . Mol. Reprod. Dev. 37, 48–53.CrossRefGoogle ScholarPubMed
Luciano, A.M., Lodde, V., Beretta, M.S., Colleoni, S., Lauria, A. & Modina, S. (2005). Developmental capability of denuded bovine oocyte in a co-culture system with intact cumulus–oocyte complexes: role of cumulus cells, cyclic adenosine 3′,5′-monophosphate, and glutathione. Mol. Reprod. Dev. 71, 389–97.CrossRefGoogle Scholar
Madison, V., Avery, B. & Greve, T. (1992). Selection of immature bovine oocytes for developmental potential in vitro . Anim. Reprod. Sci. 27, 1–11.CrossRefGoogle Scholar
Modina, S., Luciano, A.M., Vassena, R., Baraldi-Scesi, L., Lauria, A. & Gandolfi, F. (2001). Oocyte developmental competence after in vitro maturation depends on the persistence of cumulus–oocyte communications which are linked to the intracellular concentration of cAMP. Italian. J. Anat. Embryol. 106, 241–8.Google Scholar
Mohr, A., Buneker, C., Gough, R.P. & Zwacka, R.M. (2007). MnSOD protects colorectal cancer cells from TRAIL-induced apoptosis by inhibition of Smac/DIABLO release. Oncogene 27, 763–74.CrossRefGoogle ScholarPubMed
Paasch, U., Sharma, R.K., Gupta, A.K., Grunewald, S., Mascha, E.J., Thomas, A.J. Jr, Glander, H.J. & Agarwal, A. (2004). Cryopreservation and thawing is associated with varying extent of activation of apoptotic machinery in subsets of ejaculated human spermatozoa. Biol. Reprod. 71, 1828–37.CrossRefGoogle ScholarPubMed
Pangas, S.A. & Matzuk, M.M. (2005). The art and artifact of GDF9 activity: cumulus expansion and the cumulus expansion-enabling factor. Biol. Reprod. 73, 582–5.CrossRefGoogle ScholarPubMed
Parrish, J.J., Susko-Parrish, J., Leibfried-Rutledge, M.L., Critser, E.S., Eyestone, W.H. & First, N.F. (1986). Bovine in vitro fertilization with frozen–thawed semen. Theriogenology 25, 591–600.CrossRefGoogle ScholarPubMed
Racowsky, C. & Satterlie, R.A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during meiotic maturation in vivo and in vitro . Dev. Biol. 108, 191–202.CrossRefGoogle ScholarPubMed
Racowsky, C. (1985). Effect of forskolin on maintenance of meiotic arrest and stimulation of cumulus expansion, progesterone and cyclic AMP production by pig oocyte ± cumulus complexes. J. Reprod. Fertil. 74, 9–21.CrossRefGoogle ScholarPubMed
Rojas, M.A., Dyer, I.A. & Cassatt, W.A. (1965). Manganese deficiency in the bovine. J. Anim. Sci. 24, 664–7.CrossRefGoogle ScholarPubMed
Salustri, A. & Siracusa, G. (1983). Metabolic coupling, cumulus expansion and meiotic resumption in mouse cumuli oophori cultured in vitro in the presence of FSH or dcAMP, or stimulated in vivo by hCG. J. Reprod. Fertil. 68, 335–41.CrossRefGoogle ScholarPubMed
Schrantz, N., Blanchard, D.A., Mitenne, F., Auffredou, M.T., Vazquez, A. & Leca, G. (1999). Manganese induces apoptosis of human B cells: caspase-dependent cell death blocked by Bcl-2. Cell Death Diff. 6, 445–53.CrossRefGoogle Scholar
Shioya, Y., Kuwayama, M., Fukushima, M. & Iwasaki, S., (1988). In vitro fertilization and cleavage capability of bovine follicular oocytes classified by cumulus cells and matured in vitro . Theriogenology 30, 489–96.CrossRefGoogle ScholarPubMed
Sutton, M.L., Gilchrist, R.B., Thompson, J.G. (2003). Effects of in-vivo and in-vitro environments on the metabolism of the cumulus–oocyte complex and its influence on oocyte developmental capacity. Hum Reprod Update 9, 35–48.CrossRefGoogle Scholar
Sutton-McDowall, M.L., Gilchrist, R.B., Thompson, J.G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 39, 685–95.CrossRefGoogle Scholar
Tervit, H.R., Whittingham, D.G., Rowson, L.E.A. (1972). Successful culture in vitro of sheep and cattle ova. J Reprod Fertil. 30, 493–7.CrossRefGoogle ScholarPubMed
Underwood, E.J. & Suttle, N.F. (1999). The Mineral Nutrition of Livestock. London, UK: CABI Publishing.CrossRefGoogle Scholar
Van Remmen, H., Ikeno, Y., Hamilton, M., Pahlavani, M., Wolf, N., Thorpe, S.R., Alderson, N.L., Baynes, J.W., Epstein, C.J., Huang, T.T., Nelson, J., Strong, R. & Richardson, A. (2003). Life-long reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol. Genomics 16, 29–37.CrossRefGoogle Scholar
Vanderhyden, B.C. & Armstrong, D.T. (1989). Role of cumulus cells and serum on the in vitro maturation, fertilization, and subsequent development of rat oocytes. Biol. Reprod. 40, 720–8.CrossRefGoogle ScholarPubMed
Wang, J., Wang, Z.Y., Wang, Z.J., Liu, R., Liu, S.Q. & Wang, L. (2014). Effects of manganese deficiency on chondrocyte development in tibia growth plate of Arbor Acres chicks. J. Bone Miner. Metab. doi: 10.1007/s00774-014-0563-0. [Epub ahead of print]CrossRefGoogle Scholar
Wongsrikeao, P., Kaneshige, Y., Ooki, R., Taniguchi, M., Agung, B., Nii, M., & Otoi, T. (2005). Effect of the removal of cumulus cells on the nuclear maturation, fertilization and development of porcine oocytes. Reprod. Dom. Anim. 40, 166–170.CrossRefGoogle ScholarPubMed
Zhang, L., Jiang, S., Wozniak, P.J., Yang, X. & Godke, R.A. (1995). Cumulus cell function during bovine oocyte maturation, fertilization, and embryo development in vitro . Mol. Reprod. Dev. 40, 338–44.CrossRefGoogle ScholarPubMed
Zidenberg-Cherr, S., Keen, C.L., Lönnerdal, B. & Hurley, L.S. (1983). Superoxide dismutase activity and lipid peroxidation in the rat: developmental correlations affected by manganese deficiency. J. Nutr. 113, 2498– 504.CrossRefGoogle ScholarPubMed