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Follicular structures of cows with cystic ovarian disease present altered expression of cytokines

Published online by Cambridge University Press:  15 August 2019

Antonela F. Stassi
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina
Natalia C. Gareis
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Argentina
Belkis E. Marelli
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Argentina
Valentina Matiller
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Argentina
Cristian J.M. Leiva
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina
Florencia Rey
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Argentina
Hugo H. Ortega
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Argentina
Natalia R. Salvetti
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina Facultad de Ciencias Veterinarias, Universidad Nacional del Litoral, Argentina
M. Eugenia Baravalle*
Affiliation:
Laboratorio de Biología Celular y Molecular Aplicada, Instituto de Ciencias Veterinarias del Litoral (ICiVet-Litoral), Consejo Nacional de Investigaciones Científicas y Técnicas, (CONICET) –Universidad Nacional del Litoral, Argentina
*
Address for correspondence: María Eugenia Baravalle. ICiVet-Litoral, Universidad Nacional del Litoral – CONICET, R.P. Kreder 2805. (3080) Esperanza, Santa Fe, Argentina. Tel: +54 3496 420639. Fax: +54 3496 426304. E-mail: [email protected]

Summary

Ovulation is considered an inflammatory, cytokine-mediated event. Cytokines, which are recognized as growth factors with immunoregulatory properties, are involved in many cellular processes at the ovarian level. In this sense, cytokines affect fertility and are involved in the development of different ovarian disorders such as bovine cystic ovarian disease (COD). Because it has been previously demonstrated that ovarian cells represent both sources and targets of cytokines, the aim of this study was to examine the expression of several cytokines, including IL-1β, IL-1RA, IL-1RI, IL-1RII, IL-4 and IL-8, in ovarian follicular structures from cows with spontaneous COD. The protein expression of these cytokines was evaluated by immunohistochemistry. Additionally, IL-1β, IL-4 and IL-8 concentrations in follicular fluid (FF) and serum were determined by enzyme-linked immunosorbent assay (ELISA). In granulosa and theca cells, IL-1RI, IL-1RII, IL-1RA and IL-4 expression levels were higher in cystic follicles than in the control dominant follicles. The serum and FF concentrations of IL-1β and IL-4 showed no differences between groups, whereas IL-8 concentration was detected only in FF of cysts from cows with COD. The FF and serum concentrations of IL-1β and IL-8 showed no significant differences, whereas IL-4 concentration was higher in FF than in serum in both the control and COD groups. These results evidenced an altered expression of cytokines in ovaries of cows with COD that could contribute to the pathogenesis of this disease.

Type
Research Article
Copyright
© Cambridge University Press 2019 

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References

Akdis, M, Aab, A, Altunbulakli, C, Azkur, K, Costa, RA, Crameri, R, et al. (2016) Interleukins (from IL-1 to IL-38), interferons, transforming growth factor β, and TNF-α: receptors, functions, and roles in diseases. J Allergy Clin Immunol 138, 9841010.CrossRefGoogle ScholarPubMed
Amweg, AN, Salvetti, NR, Stangaferro, ML, Paredes, AH, Lara, HH, Rodríguez, FM and Ortega, HH (2013) Ovarian localization of 11β-hydroxysteroid dehydrogenase (11βHSD): Effects of ACTH stimulation and its relationship with bovine cystic ovarian disease. Domest Anim Endocrinol 45, 126–40.CrossRefGoogle ScholarPubMed
Arend, WP (2002) The balance between IL-1 and IL-1Ra in disease. Cytokine Growth Factor Rev 13, 323–40.CrossRefGoogle Scholar
Baravalle, ME, Stassi, AF, Velázquez, MML, Belotti, EM, Rodríguez, FM, Ortega, HH and Salvetti, NR (2015) Altered expression of pro-inflammatory cytokines in ovarian follicles of cows with cystic ovarian disease. J Comp Pathol 153, 116–30.CrossRefGoogle ScholarPubMed
Bartolomé, JA, Thatcher, WW, Melendez, P, Risco, CA and Archbald, LF (2005) Strategies for the diagnosis and treatment of ovarian cysts in dairy cattle. J Am Vet Med Assoc 227, 1409–14.CrossRefGoogle ScholarPubMed
Belayet, HM, Kanayama, N, Khatun, S, Asahina, T, Okada, Y, Kitamura, K, Kobayashi, T and Terao, T (2000) Pharmacologic doses of interleukin 8 suppositories induce follicular maturation in rabbits. Cytokine 12, 361–7.CrossRefGoogle ScholarPubMed
Bello, NM, Steibel, JP and Pursley, JR (2006) Optimizing ovulation to first GnRH improved outcomes to each hormonal injection of ovsynch in lactating dairy cows. J Dairy Sci 89, 3413–24.CrossRefGoogle ScholarPubMed
Bonder, CS, Dickensheets, HL, Finlay-Jones, JJ, Donnelly, RP and Hart, PH (1998) Involvement of the IL-2 receptor gamma-chain (gammac) in the control by IL-4 of human monocyte and macrophage proinflammatory mediator production. J Immunol 160, 4048–56.Google ScholarPubMed
Bonecchi, R, Garlanda, C, Mantovani, A and Riva, F (2016) Cytokine decoy and scavenger receptors as key regulators of immunity and inflammation. Cytokine 87, 37–45.CrossRefGoogle ScholarPubMed
Bornstein, SR, Rutkowski, H and Vrezas, I (2004) Cytokines and steroidogenesis. Mol Cell Endocrinol 215, 135–41.CrossRefGoogle ScholarPubMed
Brännström, M (2004) Potential role of cytokines in ovarian physiology: the case for interleukin-1. In: The Ovary, 2nd edn, Leung, PCK, Adashi, EY, eds, Elsevier Academic Press, Vancouver, pp. 261–71.CrossRefGoogle Scholar
Brännström, M, Wang, L and Norman, RJ (1993) Ovulatory effect of interleukin-1 beta on the perfused rat ovary. Endocrinology 132, 399404.CrossRefGoogle ScholarPubMed
Braw-Tal, R and Yossefi, S (1997) Studies in-vivo and in-vitro on the initiation of follicle growth in the bovine ovary. J Reprod Fertil 109, 165–71.CrossRefGoogle ScholarPubMed
Bukulmez, O and Arici, A (2000) Leukocytes in ovarian function. Hum Reprod 6, 115.Google ScholarPubMed
Büscher, U, Chen, FC, Kentenich, H and Schmiady, H (1999) Cytokines in the follicular fluid of stimulated and non-stimulated human ovaries; is ovulation a suppressed inflammatory reaction? Hum Reprod 14, 162–6.CrossRefGoogle ScholarPubMed
Caillaud, M, Duchamp, G and Gérard, N (2005) In vivo effect of interleukin-1beta and interleukin-1RA on oocyte cytoplasmic maturation, ovulation, and early embryonic development in the mare. Reprod Biol Endocrinol 3, 19.CrossRefGoogle ScholarPubMed
Cattaneo, L, Signorini, ML, Bertoli, J, Bartolomé, JA, Gareis, NC, Díaz, PU, Bo, GA and Ortega, HH (2014) Epidemiological description of cystic ovarian disease in Argentine dairy herds: risk factors and effects on the reproductive performance of lactating cows. Reprod Domest Anim 49, 1028–33.CrossRefGoogle ScholarPubMed
Chun, SY, Eisenhauer, KM, Kubo, M and Hsueh, AJ (1995) Interleukin-1 beta suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology 136, 3120–7.CrossRefGoogle ScholarPubMed
Colotta, F, Re, F, Muzio, M, Polentarutti, N, Minty, A, Caput, D, Ferrara, P and Mantovani, A (1994) Interleukin-13 induces expression and release of interleukin-1 decoy receptor in human polymorphonuclear cells. J Biol Chem 269, 12403–6.Google ScholarPubMed
Colotta, F, Re, F, Muzio, M, Bertini, R, Polentarutti, N, Sironi, M, Giri, JG, Dower, SK, Sims, JE and Mantovani, A (1993) Interleukin-1 type II receptor: a decoy target for IL-1 that is regulated by IL-4. Science 61, 472–5.CrossRefGoogle Scholar
Colotta, F, Saccani, S, Giri, JG, Dower, SK, Sims, JE, Introna, M and Mantovani, A (1996) Regulated expression and release of the IL-1 decoy receptor in human mononuclear phagocytes. J Immunol 156, 2534–41.Google ScholarPubMed
Dang, X, Zhu, Q, He, Y, Wang, Y, Lu, Y, Li, X, Qi, J, Wu, H and Sun, Y (2017) IL-1β up-regulates StAR and progesterone production through the ERK1/2-and p38-mediated CREB signaling pathways in human granulosa-lutein cells. Endocrinology 158, 3281–91.CrossRefGoogle Scholar
Daun, JM, Ball, RW, Burger, HR and Cannon, JG (1999) Aspirin-induced increases in soluble IL-1 receptor type II concentrations in vitro and in vivo . J Leukoc Biol 65, 863–6.CrossRefGoogle ScholarPubMed
De, M, Sanford, T and Wood, G (1992) Interleukin-1, Interleukin-6, and tumor necrosis factor-α are produced in the mouse uterus during the estrous cycle and are induced by estrogen and progesterone. Dev Biol 151, 297305.Google ScholarPubMed
Dembic, Z (2015) Cytokines of the Immune System: Interleukins. In: The Cytokines of the Immune System 6, 143239.CrossRefGoogle Scholar
Deshpande, R, Chang, M, Chapman, J and Michael, S (2000) Alteration of cytokine production in follicular cystic ovaries induced in mice by neonatal estradiol injection. Am J Reprod Immunol 44, 80–8.CrossRefGoogle ScholarPubMed
Díaz, PU, Stangaferro, ML, Gareis, NC, Silvia, W, Matiller, V, Salvetti, NR, Rey, F, Barberis, F, Cattaneo, L and Ortega, HH (2015) Characterization of persistent follicles induced by prolonged treatment with progesterone in dairy cows: an experimental model for the study of ovarian follicular cysts. Theriogenology 84, 1149–60.CrossRefGoogle Scholar
Dickensheets, HL and Donnelly, RP (1997) IFN-gamma and IL-10 inhibit induction of IL-1 receptor type I and type II gene expression by IL-4 and IL-13 in human monocytes. J Immunol 159, 6226–33.Google ScholarPubMed
Dinarello, CA (2013) Overview of the interleukin-1 family of ligands and receptors. Semin Immunol 25, 389–93.CrossRefGoogle ScholarPubMed
Ebejer, K and Calleja-Agius, J (2013) The role of cytokines in polycystic ovarian syndrome. Gynecol Endocrinol 29, 536–40.CrossRefGoogle ScholarPubMed
Ellman, C, Corbett, JA, Misko, TP, McDaniel, M and Beckerman, KP (1993) Nitric oxide mediates interleukin-1-induced cellular cytotoxicity in the rat ovary. A potential role for nitric oxide in the ovulatory process. J Clin Invest 92, 3053–6.CrossRefGoogle ScholarPubMed
Field, SL, Dasgupta, T, Cummings, M and Orsi, NM (2014) Cytokines in ovarian folliculogenesis, oocyte maturation and luteinisation. Mol ReprodDev 81, 284314.CrossRefGoogle ScholarPubMed
Gaafar, TM, Hanna, MOF, Hammady, MR, Amr, HM, Osman, OM, Nasef, A and Osman, AM (2014) Evaluation of cytokines in follicular fluid and their effect on fertilization and pregnancy outcome. Immunol Invest 43, 572–84.CrossRefGoogle ScholarPubMed
Garcia-Velasco, JA and Arici, A (1998) Chemokines and human reproduction. Fertil Steril 71, 983–93.CrossRefGoogle Scholar
Garlanda, C, Dinarello, CA and Mantovani, A (2013) The interleukin-1 family: back to the future. Immunity 39, 1003–18.CrossRefGoogle ScholarPubMed
Garverick, HA (1997) Ovarian follicular cysts in dairy cows. J Dairy Sci 80, 9951004.CrossRefGoogle ScholarPubMed
Hatler, TB, Hayes, SH, Ray, DL, Reames, PS and Silvia, WJ (2008) Effect of subluteal concentrations of progesterone on luteinizing hormone and ovulation in lactating dairy cows. Vet J 177, 360–8.CrossRefGoogle ScholarPubMed
Hurwitz, A, Loukides, J, Ricciarelli, E, Botero, L, Katz, E, McAllister, JM, Garcia, JE, Rohan, R, Adashi, EY and Hernandez, ER (1992) Human intraovarian interleukin-1 (IL1) system: highly compartmentalized and hormonally dependent regulation of the genes encoding IL1, its receptor, and its receptor antagonist. J Clin Invest 89, 17461754.CrossRefGoogle Scholar
Hurwitz, A, Dushnik, M, Solomon, H, Ben-Chetrit, A, Finci-Yeheskel, Z, Milwidsky, A, Mayer, M, Adashi, EY and Yagel, S (1993) Cytokine-mediated regulation of rat ovarian function: interleukin-1 stimulates the accumulation of a 92-kilodalton gelatinase. Endocrinology 132, 2709–14.CrossRefGoogle ScholarPubMed
Isobe, N, Kitabayashi, M and Yoshimura, Y (2005) Microvascular distribution and vascular endothelial growth factor expression in bovine cystic follicles. Domest Anim Endocrinol 29, 634–45.CrossRefGoogle ScholarPubMed
Isobe, N, Kitabayashi, M and Yoshimura, Y (2008) Expression of vascular endothelial growth factor receptors in bovine cystic follicles. Reprod Domest Anim 43, 267–71.CrossRefGoogle ScholarPubMed
Jiemtaweeboon, S, Shirasuna, K, Nitta, A, Kobayashi, A, Schuberth, H, Shimizu, T and Miyamoto, A (2011) Evidence that polymorphonuclear neutrophils infiltrate into the developing corpus luteum and promote angiogenesis with interleukin-8 in the cow. Reprod Biol Endocrinol 8, 979.Google Scholar
Kalliolias, GD, Gordon, RA and Ivashkiv, LB (2010) Suppression of TNF-alpha and IL-1 signaling identifies a mechanism of homeostatic regulation of macrophages by IL-27. J Immunol 185, 7047–56.CrossRefGoogle ScholarPubMed
Kitaya, K and Yamada, H (2011) Pathophysiological roles of chemokines in human reproduction: an overview. Am J Reprod Immunol 65, 449–59.CrossRefGoogle ScholarPubMed
Koch, AE, Polverini, PJ, Kunkel, SL, Harlow, LA, DiPietro, LA, Elner, VM, Elner, SG and Strieter, RM (1992) Interleukin 8 as a macrophage derived mediator of angiogenesis. Science 258, 1798–801.CrossRefGoogle ScholarPubMed
Kuhn, PH, Marjaux, E, Imhof, A, De Strooper, B, Haass, C and Lichtenthaler, SF (2007) Regulated intramembrane proteolysis of the intereukin-1 receptor II by alpha-, beta-, and gamma-secretase. J Biol Chem 282, 11982–95.CrossRefGoogle Scholar
Leo, CP, Pisarska, MD and Hsueh, AJ (2001) DNA array analysis of changes in preovulatory gene expression in the rat ovary. Biol Reprod 65, 269–76.CrossRefGoogle ScholarPubMed
Li, A, Varney, ML, Valasek, J, Godfrey, M, Dave, BJ and Singh, RK (2005) Autocrine role of interleukin-8 in induction of endothelial cell proliferation, survival, migration and MMP-2 production and angiogenesis. Angiogenesis 8, 6371.CrossRefGoogle ScholarPubMed
Lorenzen, I, Lokau, J, Düsterhöft, S, Trad, A, Garbers, C, Scheller, J, Rose-John, S and Grötzinger, J (2012) The membrane-proximal domain of A disintegrin and metalloprotease 17 (ADAM17) is responsible for recognition of the interleukin-6 receptor and interleukin-1 receptor II. FEBS Lett 586, 1093–100.CrossRefGoogle ScholarPubMed
Marelli, BE, Díaz, PU, Salvetti, NR, Rey, F and Ortega, HH (2014) mRNA expression pattern of gonadotropin receptors in bovine follicular cysts. Biol Reprod 4, 276–81.CrossRefGoogle Scholar
Matiller, V, Stangaferro, ML, Díaz, PU, Ortega, HH, Rey, F, Huber, E and Salvetti, NR (2014) Altered expression of transforming growth factor beta isoforms in bovine cystic ovarian disease. Reprod Domest Anim 49, 813–23.CrossRefGoogle ScholarPubMed
Mu, Y, Liu, J, Wang, B, Wen, Q, Wang, J, Yan, J, Zhou, S, Ma, X and Cao, Y (2010) Interleukin 1 beta (IL-1β) promoter C [-511] T polymorphism but not C [+3953] T polymorphism is associated with polycystic ovary syndrome. Endocrine 37, 71–5.CrossRefGoogle Scholar
Niu, Z, Ye, Y, Xia, L, Fengm, Y and Zhang, A (2017) Follicular fluid cytokine composition and oocyte quality of polycystic ovary syndrome patients with metabolic syndrome undergoing in vitro fertilization. Cytokine 91, 180–6.CrossRefGoogle ScholarPubMed
Oakley, OR, Kim, H, El-Amouri, I, Lin, PC, Cho, J, Bani-Ahmad, M and Ko, C (2010) Periovulatory leukocyte infiltration in the rat ovary. Endocrinology 151, 4551–9.CrossRefGoogle ScholarPubMed
Orsi, NM (2008) Cytokine networks in the establishment and maintenance of pregnancy. Hum Fertil 11, 222–30.CrossRefGoogle ScholarPubMed
Orsi, NM and Tribe, RM (2008) Cytokine networks and the regulation of uterine function in pregnancyand parturition. Neuroendocrinology 20, 462–9.CrossRefGoogle Scholar
Ortega, HH, Díaz, PU, Salvetti, NR, Hein, GJ, Marelli, BE, Rodríguez, FM, Stassi, AF and Rey, F (2016) Follicular cysts: a single sign and different diseases. a view from comparative medicine. Curr Pharm Des 22, 5634–45.CrossRefGoogle Scholar
Ortega, HH, Rey, F, Velázquez, MML and Padmanabhan, V (2010) Developmental programming: effect of prenatal steroid excess on intraovarian components of insulin signaling pathway and related proteins in sheep. Biol Reprod 82, 1065–75.CrossRefGoogle Scholar
Ou, HL, Sun, D, Peng, YC and Wu, YL (2016) Novel effects of the cyclooxygenase-2-selective inhibitor NS-398 on IL-1β-induced cyclooxygenase-2 and IL-8 expression in human ovarian granulosa cells. Innate Immun 22, 452–65.CrossRefGoogle ScholarPubMed
Passos, JRS, Costa, JJN, da Cunha, EV, Silva, AWB, Ribeiro, RP, de Souza, GB, Barroso, PA, Dau, AM, Saraiva, MV, Gonçalves, PB, van den Hurk, R and Silva, JR (2016) Protein and messenger RNA expression of interleukin 1 system members in bovine ovarian follicles and effects of interleukin 1b on primordial follicle activation and survival in vitro . Domest Anim Endocrinol 54, 4859.CrossRefGoogle Scholar
Peter, AT (2004) An update on cystic ovarian degeneration in cattle. Reprod Domest Anim 39, 17.CrossRefGoogle ScholarPubMed
Probo, M, Comin, A, Mollo, A, Cairoli, F, Stradaioli, G and Veronesi, MC (2011) Reproductive performance of dairy cows with luteal or folicular ovarian cysts after treatment with buserelin. Anim Reprod Sci 127, 135–9.CrossRefGoogle ScholarPubMed
Ranefall, P, Wester, K, Andersson, AC, Busch, C and Bengtsson, E (1998) Automatic quantification of immunohistochemically stained cell nuclei based on standard reference cells. Anal Cell Pathol 17, 111–23.CrossRefGoogle ScholarPubMed
Rashid, N, Nigam, A, Saxena, P, Jain, SK and Wajid, S (2017) Association of IL-1β, IL-1Ra and FABP1 gene polymorphisms with the metabolic features of polycystic ovary syndrome. Inflamm Res 66, 621–36.CrossRefGoogle ScholarPubMed
Re, F, Muzio, M, De Rossi, M, Polentarutti, N, Giri, JG, Mantovani, A and Colotta, F (1994) The type II ‘‘receptor’ as a decoy target for interleukin 1 in polymorphonuclear leukocytes: characterization of induction by dexamethasone and ligand binding properties of the released decoy receptor. J Exp Med 179, 739–43.CrossRefGoogle ScholarPubMed
Re, F, Sironi, M, Muzio, M, Matteucci, C, Introna, M, Orlando, S, Penton-Rol, G, Dower, SK, Sims, JE, Colotta, F and Mantovani, A (1996) Inhibition of interleukin-1 responsiveness by type II receptor gene transfer: a surface ‘receptor’ with anti-interleukin-1 function. J Exp Med 183, 1841–50.CrossRefGoogle ScholarPubMed
Richards, JS, Liu, Z and Shimada, M (2008) Immune-like mechanisms in ovulation. Trends Endocrinol Metab 19, 191–6.CrossRefGoogle ScholarPubMed
Richards, JS and Pangas, SA (2010) The ovary: basic biology and clinical implications. J Clin Invest 120, 963–72.CrossRefGoogle ScholarPubMed
Rizzo, A, Campanile, D, Mutinati, M, Minoia, G, Spedicato, M and Sciorsci, RL (2011) Epidural vs intramuscular administration of lecirelin, a GnRH analogue, for the resolution of follicular cysts in dairy cows. Anim Reprod Sci 126, 1922.Google ScholarPubMed
Rodgers, RJ and Irving-Rodgers, HF (2010) Morphological classification of bovine ovarian follicles. Reproduction 139, 309–18.CrossRefGoogle ScholarPubMed
Salvetti, NR, Müller, LA, Acosta, JC, Gimeno, JE and Ortega, HH (2007) Estrogen receptors a and b and progesterone receptors in ovarian follicles of cows with cystic ovarian disease. Vet Pathol 44, 373–8.CrossRefGoogle Scholar
Salvetti, NR, Stangaferro, ML, Palomar, MM, Alfaro, NS, Rey, F, Gimeno, EJ and Ortega, HH (2010) Cell proliferation and survival mechanisms underlying the abnormal persistence of folicular cysts in bovines with cystic ovarian disease induced by ACTH. Anim Reprod Sci 122, 98110.CrossRefGoogle Scholar
Schadendorf, D, Moller, A, Algermissen, B, Worm, M, Sticherling, M and Czarnetzki, BM (1993) IL-8 produced by human malignant melanoma cells in vitro is an essential autocrine growth factor. J Immunol 151, 26672675.Google ScholarPubMed
Scherzer, WJ, Ruutiainen-Altman, KS, Putowski, LT, Kol, S, Adashi, EY and Rohan, RM (1996) Detection and in vivo hormonal regulation of rat ovarian type I and type II interleukin-I receptor mRNAs: increased expression during the periovulatory period. J Soc Gynecol Invest 3, 131–9.Google ScholarPubMed
Shimizu, T, Imamura, E, Magata, F, Murayama, C and Miyamoto, A (2013) Interleukin-8 stimulates progesterone production via the MEK pathway in ovarian theca cells. Mol Cell Biochem 374, 157–61.CrossRefGoogle ScholarPubMed
Shimizu, T, Kaji, A, Murayama, C, Magata, F, Shirasuna, K, Wakamiya, K, Okuda, K and Miyamoto, A (2012) Effects of interleukin-8 on estradiol and progesterone production by bovine granulosa cells from large follicles and progesterone production by luteinizing granulosa cells in culture. Cytokine 57, 175–81.CrossRefGoogle ScholarPubMed
Silvia, WJ, Alter, TB, Nugent, AM and Laranja da Fonseca, LF (2002) Ovarian follicular cysts in dairy cows: an abnormality in folliculogenesis. Domest Anim Endocrinol 23, 167–77.CrossRefGoogle ScholarPubMed
Silvia, WJ, McGinnis, AS and Hatler, TB (2005) A comparison of adrenal gland function in lactating dairy cows with or without ovarian follicular cysts. Biol Reprod 5, 1929.Google ScholarPubMed
Sims, JE, Giri, JG and Dower, SK (1994) The two interleukin-1 receptors play different roles in IL-1 actions. Clin Immunol Immunopathol 72, 914.CrossRefGoogle ScholarPubMed
Sirotkin, A (2011) Cytokines: signalling molecules controlling ovarian functions. Int J Biochem Cell Biol 43, 857–61.CrossRefGoogle ScholarPubMed
Smith, DE, Hanna, R, Della Friend Moore, H, Chen, H, Farese, AM, MacVittie, TJ, Virca, GD and Sims, JE (2003) The soluble form of IL-1 receptor accessory protein enhances the ability of soluble type II IL-1 receptor to inhibit IL-1 action. Immunity 18, 8796.CrossRefGoogle ScholarPubMed
Smolikova, K, Mlynarcikova, A and Scsukova, S (2012) Role of interleukins in the regulation of ovarian functions. Endocr Regul 46, 237–53.CrossRefGoogle ScholarPubMed
Spriggs, MK, Nevens, PJ, Grabstein, K, Dower, SK, Cosman, D, Armitage, RJ and McMahan, CJ, Sims, JE (1992) Molecular characterization of the interleukin-1 receptor (IL-1R) on monocytes and polymorphonuclear cells. Cytokine 4, 90–5.CrossRefGoogle ScholarPubMed
Stassi, AF, Baravalle, ME, Belotti, EM, Amweg, AN, Angeli, E, Velázquez, MML, Rey, F, Salvetti, NR and Ortega, HH (2018) Altered expression of IL-1β, IL-1RI, IL-1RII, IL-1RA and IL-4 could contribute to anovulation and follicular persistence in cattle. Theriogenology 110, 6173.CrossRefGoogle ScholarPubMed
Stassi, AF, Baravalle, ME, Belotti, EM, Rey, F, Gareis, NC, Díaz, PU, Rodríguez, FM, Leiva, CJ, Ortega, HH and Salvetti, NR (2017) Altered expression of cytokines IL-1α, IL-6, IL-8 and TNF-α in bovine follicular persistence. Theriogenology 97, 104–12.CrossRefGoogle ScholarPubMed
Terranova, P and Rice, V (1997) Cytokine involvement in ovarian processes. Am J Reprod Immunol 37, 5063.CrossRefGoogle ScholarPubMed
Ujioka, T, Matsukawa, A, Tanaka, N, Matsuura, K, Yoshinaga, M and Okamura, H (1998) Interleukin-8 as an essential factor in the human chorionic gonadotropin-induced rabbit ovulatory process: interleukin-8 induces neutrophil accumulation and activation in ovulation. Biol Reprod 58, 526–30.CrossRefGoogle ScholarPubMed
Vanholder, T, Opsomer, G and de Kruif, A (2006) Etiology and pathogenesis of cystic ovarian follicles in dairy cattle: a review. Reprod Nut Dev 46, 105–19.CrossRefGoogle ScholarPubMed
Volpert, OV, Fong, T, Koch, AE, Peterson, JD, Waltenbaugh, C, Tepper, RI and Bouck, NP (1998) Inhibition of angiogenesis by interleukin 4. J Exp Med 188, 1039–46.CrossRefGoogle ScholarPubMed
Wang, CJ, Zhou, ZG, Holmqvist, A, Zhang, H, Li, Y, Adell, G and Sun, XF (2009) Survivin expression quantified by Image Pro-Plus compared with visual assessment. Appl Immunohistochem Mol Morphol 17, 530–5.CrossRefGoogle ScholarPubMed
Woods, AM and Judd, AM (2008) Interleukin-4 increases cortisol release and decreases adrenal androgen release from bovine adrenal cells. Domest Anim Endocrinol 34, 372–82.CrossRefGoogle ScholarPubMed