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Interleukin-1β and TNF-α systems in ovarian follicles and their roles during follicular development, oocyte maturation and ovulation

Published online by Cambridge University Press:  08 May 2020

José R.V. Silva Open the ORCID record for José R.V. Silva [Opens in a new window] ,
Francisco E.O. Lima ,
Ana L.P. Souza  and
Anderson W.B. Silva
José R.V. Silva*
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
Francisco E.O. Lima
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
Ana L.P. Souza
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
Anderson W.B. Silva
Affiliation:
Laboratory of Biotechnology and Physiology of Reproduction (LABIREP), Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil
*
Author for correspondence: J.R.V. Silva. Biotechnology Nucleus of Sobral - NUBIS, Federal University of Ceara, Av. Comandante Maurocélio Rocha Ponte 100, CEP 62041-040, Sobral, CE, Brazil. Tel:/Fax: +55 88 36118000. E-mail: [email protected]
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Summary

Tumour necrosis factor-α (TNF-α) and interleukin-1β (IL-1β) are cytokines that are involved in the development, proliferation and apoptosis of ovarian follicular cells in domestic mammals. The expression of these cytokines in various follicular compartments, depending on the stage of follicle development, demonstrates their involvement in the control of primordial follicle growth up to the preovulatory stage. The mechanism of action of these factors depends on the presence of their receptors that transduce their biological actions. This review shows the expression sites of TNF-α, IL-1β and their receptors in ovarian follicles, and discusses the mechanism of action of these cytokines during follicle development, oocyte maturation and ovulation in domestic animals.

Keywords

CytokinesDomestic mammalsFollicular developmentProtein expressionReceptors
Type
Review Article
Information
Zygote , Volume 28 , Issue 4 , August 2020 , pp. 270 - 277
Copyright
© Cambridge University Press 2020

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References

Abdo, M, Hisheh, S and Dharmarajan, A (2003). Role of tumor necrosis factor-alpha and the modulating effect of the caspases in rat corpus luteum apoptosis. Biol Reprod 68, 1241–8.CrossRefGoogle ScholarPubMed
Adashi, EY (1998). The potential role of interleukin-1 in the ovulatory process: An evolving hypothesis. Mol Cell Endocrinol 140, 77–81.CrossRefGoogle Scholar
Aggarwal, S, Takada, Y, Mhashilkar, AM, Sieger, K, Chada, S and Aggarwal, BB (2004). Melanoma differentiation-associated gene-7/IL-24 gene enhances NF-kappa B activation and suppresses apoptosis induced by TNF. J Immunol 173, 4368–76.CrossRefGoogle ScholarPubMed
Baeuerle, PA and Baltimore, D (1996). NF-κβ: Ten years after. Cell 87, 13–20.CrossRefGoogle Scholar
Barak, V, Yanai, P, Trevers, AJ, Roisman, I, Simón, A and Laufer, N (1992). Interleukin-1: local production and modulation of human granulosa luteal cells steroidogenesis. Fert Steril 58, 719–25.CrossRefGoogle ScholarPubMed
Baratta, M, Basini, G, Bussolati, S and Tamanini, C (1996). Effects of interleukin-1 beta fragment (163–171) on progesterone and estradiol-17 beta release by bovine granulosa cells from different size follicles. Regul Pept 67, 87–194.CrossRefGoogle ScholarPubMed
Basini, G, Baratta, M, Bussolati, S and Tamanini, C (1998). Interleukin-1 beta fragment (163–171) modulates bovine granulosa cell proliferation in vitro: dependence on size of follicle. J Reprod Immunol 37, 139–53.CrossRefGoogle ScholarPubMed
Best, CL and Hill, JA (1995). Interleukin-1 alpha and -beta modulation of luteinized human granulosa cell oestrogen and progesterone biosynthesis. Hum Reprod 10, 3206–10.CrossRefGoogle ScholarPubMed
Bonizzi, G and Karin, M (2004). The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol 25, 280–8.CrossRefGoogle ScholarPubMed
Boraschi, D and Tagliabue, A (2013). The interleukin-1 receptor family. Semin Immunol 25, 394–407.CrossRefGoogle ScholarPubMed
Brännström, M (2004). Potential role of cytokines in ovarian physiology: the case for interleukin 1. In The Ovary (eds Leung, PCK and Adash, EY), pp. 261–71. Elsevier-Academic Press.CrossRefGoogle Scholar
Brännström, M, Pascoe, V, Norman, RJ and McClure, N (1994). Localization of leukocyte subsets in the follicle wall and in the corpus luteum throughout the human menstrual cycle. Fertil Steril 61, 488–95.Google Scholar
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, 1–9.CrossRefGoogle ScholarPubMed
Cakmak, H, Franciosi, F, Zamah, AM, Cedars, MI and Conti, M (2016). Dynamic secretion during meiotic reentry integrates the function of the oocyte and cumulus cells. Proc Natl Acad Sci USA 113, 2424–9.CrossRefGoogle ScholarPubMed
Carlberg, M, Nejaty, J, Fröysa, B, Guan, Y, Söder, O and Bergqvist, A (2000). Elevated expression of tumor necrosis factor alpha in cultured granulosa cells from women with endometriosis. Hum Reprod 15, 1250–5.CrossRefGoogle ScholarPubMed
Chaubey, GK, Kumar, S, Kumar, M, Sarwalia, P, Kumaresan, A, De, S, Kumar, R and Datta, TK (2018). Induced cumulus expansion of poor quality buffalo cumulus oocyte complexes by Interleukin-1beta improves their developmental ability. J Cell Biochem 119, 5750–60.CrossRefGoogle ScholarPubMed
Chen, HL, Marcinkiewicz, JL, Sancho-Tello, M, Hunt, JS and Terranova, PF (1993). Tumor necrosis factor-α gene expression in mouse oocytes and follicular cells. Biol Reprod 48, 707–14.CrossRefGoogle ScholarPubMed
Cheng, Y, Yata, A, Klein, C, Cho, JH, Deguchi, M and Hsueh, AJW (2011). Oocyte-expressed interleukin 7 suppresses granulosa cell apoptosis and promotes oocyte maturation in rats. Biol Reprod 84, 707–14.CrossRefGoogle ScholarPubMed
Chun, SY and Hsueh, AJW (1998). Paracrine mechanisms of ovarian follicle apoptosis. Reprod Immunol 39, 63–75.CrossRefGoogle ScholarPubMed
Chun, SY, Eisenhauer, KM, Kubo, M and Hsueh, AJ (1995). Interleukin-1 suppresses apoptosis in rat ovarian follicles by increasing nitric oxide production. Endocrinology 136, 3120–7.CrossRefGoogle ScholarPubMed
Crespo, D, Mañanós, EL, Roher, N, Mackenzie, SA and Planas, JV (2012). Tumor necrosis factor alpha may act as an intraovarian mediator of luteinizing hormone-induced oocyte maturation in trout. Biol Reprod 86, 1–12.CrossRefGoogle ScholarPubMed
De Los Santos, MJ, Anderson, DJ, Racowsky, C, Simón, C and Hill, JA (1998). Expression of interleukin-1 system genes in human gametes. Biol Reprod 59, 1419–24.CrossRefGoogle ScholarPubMed
Deyerle, KL, Sims, JE, Dower, SK and Bothwell, MA (1992). Pattern of IL-1 receptor gene expression suggests role in noninflammatory processes. J Immunol 149, 1657–65.Google ScholarPubMed
Dinarello, CA (2010). Anti-inflammatory agents: present and future. Cell 140, 935–50.CrossRefGoogle ScholarPubMed
Duffy, DM, Ko, C, Jo, M, Brannstrom, M and Curry, TE (2019). Ovulation: parallels with inflammatory processes. Endocr Rev 40, 369–416.CrossRefGoogle ScholarPubMed
Field, SL, Dasgupta, T, Cummings, M and Orsi, NM (2014). Cytokines in ovarian folliculogenesis, oocyte maturation and luteinisation. Mol Reprod Dev 81, 284–314.CrossRefGoogle ScholarPubMed
Figueiredo, JR, Lima, LF, Silva, JRV and Santos, RR (2018). Control of growth and development of preantral follicle: insights from in vitro culture. Anim Reprod 15, 648–59.CrossRefGoogle Scholar
Fischer, R, Maier, O, Siegemund, M, Wajant, H, Scheurich, P and Pfizenmaier, K (2011). A TNF receptor 2 selective agonist rescues human neurons from oxidative stress-induced cell death. PLoS One 6, 1–11.CrossRefGoogle ScholarPubMed
Franciosi, F, Manandhar, S and Conti, M (2016). FSH regulates mRNA translation in mouse oocytes and promotes developmental competence. Endocrinology 157, 872–82.CrossRefGoogle ScholarPubMed
Fukuoka, M, Yasuda, K, Taii, S, Takakura, K, Mori, T (1989). Interleukin-1 stimulates growth and inhibits progesterone secretion in cultures of porcine granulosa cells. Endocrinology 124, 884–90.CrossRefGoogle ScholarPubMed
Gabay, C, Lamacchia, C and Palmer, G (2010). IL-1 pathways in inflammation and human diseases. Nat Rev Rheumatol 6, 232–41.CrossRefGoogle ScholarPubMed
Glister, C, Hatzirodos, N, Hummitzsch, K, Knight, PG and Rodgers, RJ (2014). The global effect of follicle-stimulating hormone and tumour necrosis factor α on gene expression in cultured bovine ovarian granulosa cells. BMC Genomics 15, 1–15.CrossRefGoogle ScholarPubMed
Gottschall, PE, Katsuura, G, Hoffmann, ST and Arimura, A (1988). Interleukin 1: an inhibitor of luteinizing hormone receptor formation in cultured rat granulosa cells. FASEB J 2, 2492–6.CrossRefGoogle ScholarPubMed
Hayden, MS and Ghosh, S (2004). Signalling to NF-κB. Genes Dev 18, 2195–224.CrossRefGoogle Scholar
Hsu, H, Xiong, J and Goeddel, DV (1995). The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell 81, 495–504.CrossRefGoogle ScholarPubMed
Hsueh, AJ, Kawamura, K, Cheng, Y and Fauser, BC (2015). Intraovarian control of early folliculogenesis. Endocr Rev 36, 1–24.CrossRefGoogle ScholarPubMed
Hurwitz, A, Ricciarelli, E, Botero, L, Rohan, RM, Hernandez, ER and Adashi, EY (1991). Endocrine- and autocrine-mediated regulation of rat ovarian (theca-interstitial) interleukin-1 beta gene expression: gonadotropin-dependent preovulatory acquisition. Endocrinology 129, 3427–9.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 (IL-1) system: highly compartmentalized and hormonally dependent regulation of the genes encoding IL-1, its receptor, and its receptor antagonist. J Clin Invest 89, 1746–54.CrossRefGoogle ScholarPubMed
Hurwitz, A, Finci-Yeheskel, Z, Dushnik, M, Milwidsky, A, Shimonovitz, S, Yagel, S, Adashi, EY and Mayer, M (1995). Interleukin-1-mediated regulation of plasminogen activation in pregnant mare serum gonadotropin-primed rat granulosa cells is independent of prostaglandin production. J Soc Gynecol Invest 2, 691–9.Google ScholarPubMed
Ingman, WV and Jones, RL (2008). Cytokine knockouts in reproduction: the use of gene ablation to dissect roles of cytokines in reproductive biology. Hum Reprod Update 14, 179–92.CrossRefGoogle ScholarPubMed
Javvaji, PK, Dhali, A, Francis, JR, Kolte, AP, Mech, A, Sathish, L and Roy, SC (2019). Interleukin-7 improves in vitro maturation of ovine cumulus–oocyte complexes in a dose dependent manner. Cytokine 113, 296–304.CrossRefGoogle ScholarPubMed
Johnson, ML, Murdoch, J, Van Kirk, EA, Kaltenbach, JE and Murdoch, WJ (1999). Tumor necrosis factor alpha regulates collagenolytic activity in preovulatory ovine follicles: relationship to cytokine secretion by the oocyte-cumulus cell complex. Biol Reprod 61, 1581–5.CrossRefGoogle ScholarPubMed
Kaipia, A, Chun, SY, Eisenhauer, K and Hsueh, AJ (1996). Tumor necrosis factor-alpha and its second messenger, ceramide, stimulate apoptosis in cultured ovarian follicles. Endocrinology 137, 4864–70.CrossRefGoogle ScholarPubMed
Karakji, EG and Tsang, BK (1995). Regulation of rat granulosa cell plasminogen activator system: influence of interleukin-1 beta and ovarian follicular development. Biol Reprod 53, 1302–10.CrossRefGoogle ScholarPubMed
Karin, M and Ben-Neriah, Y (2000). Phosphorylation meets ubiquitination: the control of NF-κB activity. Annu Rev Immunol 18, 621–63.CrossRefGoogle Scholar
Kol, S, Donesky, BW, Ruutiainen-Altman, K, Ben-Shlomo, I, Irahara, M, Ando, M, Rohan, RM and Adashi, EY (1999). Ovarian interleukin-1 receptor antagonist in rats: gene expression, cellular localization, cyclic variation, and hormonal regulation of a potential determinant of interleukin-1 action. Biol Reprod 61, 274–82.CrossRefGoogle ScholarPubMed
Kong, QQ, Wang, J, Xiao, B, Lin, FH, Zhu, J, Sun, GY, Luo, MJ, Tan, JH (2018). Cumulus Cell-released tumor necrosis factor (TNF-α) promotes post-ovulatory aging of mouse oocytes. Aging (Albany) 26, 1745–57.CrossRefGoogle Scholar
Kool, M, Fierens, K and Lambrecht, BN (2012). Alum adjuvant: some of the tricks of the oldest adjuvant. J Med Microbiol 61, 927–34.CrossRefGoogle ScholarPubMed
Lima, F, Bezerra, F, Souza, GB, Matos, M, Van Den Hurk, R and Silva, J (2018). Influence of interleukin 1 beta and tumour necrosis factor alpha on the in vitro growth, maturation and mitochondrial distribution of bovine oocytes from small antral follicles. Zygote 26, 381–7.CrossRefGoogle ScholarPubMed
Ma, CH, Yan, LY, Qiao, J, Sha, W, Li, L, Chen, Y and Sun, QY (2010). Effects of tumor necrosis factor-alpha on porcine oocyte meiosis progression, spindle organization, and chromosome alignment. Fertil Steril 93, 920–6.CrossRefGoogle ScholarPubMed
Machelon, V and Emilie, D (1997). Production of ovarian cytokines and their role in ovulation in the mammalian ovary. Eur Cytokine Netw 8, 137–43.Google ScholarPubMed
Machelon, V, Nome, F, Durand-Gasselin, I and Emilie, D (1995). Macrophage and granulosa interleukin-1 beta mRNA in human ovulatory follicles. Hum Reprod 10, 2198–203.CrossRefGoogle ScholarPubMed
Manabe, N, Matsuda-Minehata, F, Goto, Y, Maeda, A, Cheng, Y, Nakagawa, S, Inoue, N, Wongpanit, K, Jin, H, Gonda, H and Li, J (2008). Role of cell death ligand and receptor system on regulation of follicular atresia in pig ovaries. Reprod Domest Anim 43, 268–72.CrossRefGoogle ScholarPubMed
Marcinkiewicz, JL, Krishna, A, Cheung, CM and Terranova, PF (1994). Oocytic tumor necrosis factor alpha: localization in the neonatal rat ovary and throughout follicular development in the adult rat. Biol Reprod 50, 1251–60.CrossRefGoogle ScholarPubMed
Martoriati, A, Lalmanach, AC, Goudet, G and Gérard, N (2002). Expression of interleukin-1 (IL-1) system genes in equine cumulus–oocyte complexes and influence of IL-1beta during in vitro maturation. Biol Reprod 67, 630–6.CrossRefGoogle ScholarPubMed
Martoriati, A, Caillaud, M, Goudet, G and Gérard, N (2003a). Inhibition of in vitro maturation of equine oocytes by interleukin 1 beta via specific IL-1 receptors. Reproduction 126, 509–15.CrossRefGoogle ScholarPubMed
Martoriati, A, Duchamp, G and Gérard, N (2003b). In vivo effect of epidermal growth factor, interleukin-1beta, and interleukin-1RA on equine preovulatory follicles. Biol Reprod 68, 1748–54.CrossRefGoogle ScholarPubMed
Matsumi, H, Yano, T, Osuga, Y, Kugu, K, Tang, X, Xu, JP, Yano, N, Kurashima, Y, Ogura, T, Tsutsumi, O, Koji, T, Esumi, H and Taketani, Y (2000). Regulation of nitric oxide synthase to promote cytostasis in ovarian follicular development. Biol Reprod 63, 141–6.CrossRefGoogle ScholarPubMed
Micheau, O and Tschopp, J (2003). Induction of TNF receptor I-mediated apoptosis via two sequential signaling complexes. Cell 114, 181–90.CrossRefGoogle ScholarPubMed
Murdoch, WJ, Colgin, DC and Ellis, JA (1997). Role of tumor necrosis factor-alpha in the ovulatory mechanism of ewes. J Anim Sci 75, 1601–5.CrossRefGoogle ScholarPubMed
Muzio, M, Ni, J, Feng, P and Dixit, VM (1997). IRAK (Pelle) family member IRAK-2 and MyD88 as proximal mediators of IL-1 signaling. Science 278, 1612–5.CrossRefGoogle ScholarPubMed
Nakayama, M (2003). Changes in the expression of tumor necrosis factor (TNF), TNF receptor (TNFR) 2, and TNFR-associated factor 2 in granulosa cells during atresia in pig ovaries. Biol Reprod 68, 530–5.CrossRefGoogle ScholarPubMed
Naz, RK, Zhu, X and Menge, AC (1997). Expression of tumor necrosis factor-α and its receptors type I and type II in human oocytes. Mol Reprod Dev 47, 127–33.3.0.CO;2-O>CrossRefGoogle ScholarPubMed
Nilsson, EE, Stanfield, J and Skinner, MK (2006). Interactions between progesterone and tumor necrosis factor-α in the regulation of primordial follicle assembly. Reproduction 132, 877–86.CrossRefGoogle ScholarPubMed
Nishikori, M (2005). Classical and alternative NF-κβ activation pathways and their roles in lymphoid malignancies. J Clin Exp Hematophatol 45, 15–24.CrossRefGoogle Scholar
Passos, JRS, Costa, JJN, Cunha, EV, Silva, AWB, Ribeiro, RP, Souza, GB, Barroso, PAA, Dau, AMP, Saraiva, MVA, Gonçalves, PBD, Hurk, RVD and Silva, JRV (2016). Protein and messenger RNA expression of interleukin 1 system members in bovine ovarian follicles and effects of interleukin 1 on primordial follicle activation and survival in vitro. Domest Anim Endocrinol 54, 48–59.CrossRefGoogle ScholarPubMed
Paulino, LRFM, Cunha, EV, Silva, AWB, Souza, GB, Lopes, EPF, Donato, MAM, Peixoto, CA, Matos-Brito, BG, Van Den Hurk, R and Silva, JRV (2018). Effects of tumour necrosis factor-alpha and interleukin-1 on in vitro development of bovine secondary follicles. Reprod Domest Anim 53, 997–1005.CrossRefGoogle ScholarPubMed
Prange-Kiel, J, Kreutzkamm, C, Wehrenberg, U and Rune, GM (2001). Role of tumor necrosis factor in preovulatory follicles of swine. Biol Reprod 65, 928–35.CrossRefGoogle ScholarPubMed
Rauert, H, Wicovsky, A, Muller, N, Siegmund, D, Spindler, V, Waschke, J, Kneitz, NC and Wajant, H (2010). Membrane tumor necrosis factor (TNF) induces p100 processing via TNF receptor-2 (TNFR2). J Biol Chem 285, 7394–404.CrossRefGoogle Scholar
Rice, VM, Williams, VR, Limback, SD and Terranova, PF (1996). Tumor necrosis factor-α inhibits follicle stimulating hormone induced-granulosa cell oestradiol secretion in the human: dependence on size of follicles. Hum Reprod 11, 1256–61.CrossRefGoogle Scholar
Roby, KF and Terranova, PF (1989). Localization of tumor necrosis factor (TNF) in the rat and bovine ovary using immunocytochemistry and cell blot: evidence for granulosal production. In Growth Factors and the Ovary (ed. Hirshfield, AN), pp. 273–8. Boston, MA: Springer.CrossRefGoogle Scholar
Rothe, M, Sarma, V, Dixit, VM and Goeddel, DV (1995). TRAF2-mediated activation of NF-kappaB by TNF receptor 2 and CD40. Science 269, 1424–7.CrossRefGoogle ScholarPubMed
Sakumoto, R and Okuda, K (2004). Possible actions of tumor necrosis factor-α in ovarian function. J Reprod Dev 50, 39–46.CrossRefGoogle ScholarPubMed
Salamonsen, LA, Hannan, NJ and Dimitriadis, E (2007). Cytokines and chemokines during human embryo implantation: roles in implantation and early placentation. Semin Reprod Med 25, 437–44.CrossRefGoogle ScholarPubMed
Samir, M, Glister, C, Mattar, D, Laird, M and Knight, PG (2017). Follicular expression of pro-inflammatory cytokines tumour necrosis factor-α (TNFα), interleukin 6 (IL6) and their receptors in cattle: TNFα, IL6 and macrophages suppress thecal androgen production in vitro. Reproduction 154, 35–49.CrossRefGoogle ScholarPubMed
Sancho-Tello, M, Tash, J, Roby, K and Terranova, PF (1993). Effects of lipopolysaccharide on ovarian function in the pregnant mare serum gonadotropin-treated immature rat. Endocr J 1, 503–11.Google Scholar
Sasson, R, Winder, N, Kees, S, and Amsterdam, A (2002). Induction of apoptosis in granulosa cells by TNF alpha and its attenuation by glucocorticoids involve modulation of Bcl-2. Biochem Biophys Res Commun 294, 51–9.CrossRefGoogle ScholarPubMed
Senftleben, U, Cao, Y, Xiao, G, Greten, FR, Krahn, G, Bonizzi, G, Chen, Y, Hu, Y, Fong, A, Sun, S-C and Karin, M (2001). Activation by IKKα of a second, evolutionary conserved, NF-κB signaling pathway. Science 293, 1995–9.CrossRefGoogle Scholar
Silva, JR, Figueiredo, JR and Van Den Hurk, R (2009). Involvement of growth hormone (GH) and insulin-like growth factor (IGF) system in ovarian folliculogenesis. Theriogenology 71, 1193–208.CrossRefGoogle ScholarPubMed
Silva, JRV, Van Den Hurk, R and Figueiredo, JR (2016). Ovarian follicle development in vitro and oocyte competence: advances and challenges for farm animals. Domest Anim Endocrinol 55, 123–35.CrossRefGoogle ScholarPubMed
Silva, AWB, Bezerra, FTG, Glanzner, WG, Dos Santos, JT, Dau, AMP, Rovani, MT, Ilha, GF, Costa, JJN, Cunha, EV, Donato, MAM, Peixoto, CA, Gonçalves, PBD, Bordignon, V and Silva, JRV (2017a). mRNA expression profile of the TNF-α system in LH-induced bovine preovulatory follicles and effects of TNF-α on gene expression, ultrastructure and expansion of cumulus–oocyte complexes cultured in vitro. Theriogenology 90, 1–10.CrossRefGoogle ScholarPubMed
Silva, AWB, Ribeiro, RP, Menezes, VG, Barberino, RS, Passos, JRS, Dau, AMP, Costa, JJN, Melo, LRF, Bezerra, FTG, Donato, MAM, Peixoto, CA, Matos, MHT, Gonçalves, PBD, Van Den Hurk, R, Silva, JRV (2017b). Expression of TNF-α system members in bovine ovarian follicles and the effects of TNF-α or dexamethasone on preantral follicle survival, development and ultrastructure in vitro. Anim Reprod Sci 182, 56–68.CrossRefGoogle ScholarPubMed
Simón, C, Frances, A, Piquette, G and Polan, ML (1994). Immunohistochemical localization of the interleukin-1 system in the mouse ovary during follicular growth, ovulation, and luteinization. Biol Reprod 50, 449–57.CrossRefGoogle ScholarPubMed
Sirotkin, AV (2011). Cytokines: signalling molecules controlling ovarian functions. Int J Biochem Cell Biol 43, 857–61.CrossRefGoogle ScholarPubMed
Solt, LA, Madge, LA, Orange, JS and May, MJ (2007). Interleukin-1-induced NF-κB activation is NEMO-dependent but does not require IKKβ. J Biol Chem 282, 8724–33.CrossRefGoogle Scholar
Spicer, LJ (1998). Tumor necrosis factor-α (TNF-α) inhibits steroidogenesis of bovine ovarian granulosa and thecal cells in vitro. Involvement of TNF-α receptors. Endocrine 8, 109–15.CrossRefGoogle ScholarPubMed
Spicer, LJ (2001). Receptors for insulin-like growth factor-I and tumor necrosis factor-α are hormonally regulated in bovine granulosa and thecal cells. Anim Reprod Sci 3, 45–67.CrossRefGoogle Scholar
Sun, S-C and Ley, SC (2008). New insights into NF-κB regulation and function. Trends Immunol 29, 469–78.CrossRefGoogle ScholarPubMed
Tanaka, Y, Kuwahara, A, Ushigoe, K, Yano, Y, Taniguchi, Y, Yamamoto, Y, Matsuzaki, T, Yasui, T and Irahara, M (2017). Expression of cytokine-induced neutrophil chemoattractant suppresses tumor necrosis factor alpha expression and thereby prevents the follicles from undergoing atresia and apoptosis. Reprod Med Biol 16, 157–65.CrossRefGoogle ScholarPubMed
Terranova, PF and Rice, VM (1997). Review: cytokine involvement in ovarian processes. Am J Reprod Immunol 37, 50–63.CrossRefGoogle ScholarPubMed
Trundley, A and Moffett, A (2004). Human uterine leukocytes and pregnancy. Tissue Antigens 63, 1–12.CrossRefGoogle Scholar
Uri-Belapolsky, S, Shaish, A, Eliyahu, E, Grossman, H, Levi, M, Chuderland, D, Ninio-Many, L, Hasky, N, Shashar, D, Almog, T, Kandel-Kfi, M, Harats, D, Shalgi, R and Kamari, Y (2014). Interleukin-1 deficiency prolongs ovarian lifespan in mice. Proc Natl Acad Sci USA 111, 12492–7.CrossRefGoogle ScholarPubMed
Uri-Belapolsky, S, Miller, I, Shaish, A, Levi, M, Harats, D, Ninio-Many, L, Kamari, Y and Shalgi, R (2017). Interleukin 1-alpha deficiency increases the expression of follicle-stimulating hormone receptors in granulosa cells. Mol Reprod Dev 84, 460–7.CrossRefGoogle ScholarPubMed
Van Den Hurk, R and Zhao, J (2005). Formation of ovarian follicles and their growth, differentiation and maturation within ovarian follicles. Theriogenology 63, 1717–51.CrossRefGoogle ScholarPubMed
Veldhuis, JD, Garmey, JC, Urban, RJ, Demers, LM and Aggarwal, BB (1991). Ovarian actions of tumor necrosis factor-α (TNFα): pleiotropic effects of TNFα on differentiated functions of untransformed swine granulose cells. Endocrinology 129, 641–8.CrossRefGoogle Scholar
Wajant, H, Pfizenmaier, K and Scheurich, P (2003). Tumor necrosis factor signaling. Cell Death Differ 10, 45–65.CrossRefGoogle ScholarPubMed
Wang, LJ, Brännström, M, Cui, KH, Simula, AP, Hart, RP, Maddocks, S and Norman, RJ (1997). Localisation of mRNA for interleukin-1 receptor and interleukin-1 receptor antagonist in the rat ovary. J Endocrinol 152, 11–7.CrossRefGoogle ScholarPubMed
Wesche, H, Henzel, WJ, Shillinglaw, W, Li, S and Cao, Z (1997). MyD88: an adapter that recruits IRAK to the IL-1 receptor complex. Immunity 7, 837–47.CrossRefGoogle ScholarPubMed
Witty, JP, Bridgham, JT and Johnson, AL (1996). Induction of apoptotic cell death in hen granulosa cells by ceramide. Endocrinology 137, 5269–77.CrossRefGoogle ScholarPubMed
Wu, H and Arron, JR (2003). TRAF6, a molecular bridge spanning adaptive immunity, innate immunity and osteoimmunology. Bioessays 25, 1096–105.CrossRefGoogle ScholarPubMed
Wullaert, A, van Loo, G, Heyninck, K and Beyaert, R (2007). Hepatic tumor necrosis factor signaling and nuclear factor-kappaB: effects on liver homeostasis and beyond. Endocr Rev 28, 365–86.CrossRefGoogle ScholarPubMed
Yamamoto, Y, Kuwahara, A, Taniguchi, Y, Yamasaki, M, Tanaka, Y, Mukai, Y, Yamashita, M, Matsuzaki, T, Yasui, T and Irahara, M (2015). Tumor necrosis factor alpha inhibits ovulation and induces granulosa cell death in rat ovaries. Reprod Med Biol 14, 107–15.CrossRefGoogle ScholarPubMed
Zolti, M, Ben-Rafael, Z, Meirom, R, Shemesh, M, Bider, D, Mashiach, S and Apte, RN (1991). Cytokine involvement in oocytes and early embryos. Fertil Steril 56, 265–72.CrossRefGoogle ScholarPubMed