Restraint stress and elevation of corticotrophin-releasing hormone in female mice impair oocyte competence through activation of the tumour necrosis factor α (TNF- α) system
Xin-Yue Zhao A , Zhi-Bin Li A , Hong-Jie Yuan A , Xiao Han A , Jia-Shun Wu A , Xiu-Yun Feng A , Min Zhang A and Jing-He Tan
A B
+ Author Affiliations
- Author Affiliations
A Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention, College of Animal Science and Veterinary Medicine, Shandong Agricultural University, Tai’an City 271018, P. R. China.
B Corresponding author. Email: tanjh@sdau.edu.cn
Reproduction, Fertility and Development 32(9) 862-872 https://doi.org/10.1071/RD20002
Submitted: 4 January 2020 Accepted: 9 April 2020 Published: 28 May 2020
Abstract
Studies have observed that restraint stress (RS) and the associated elevation in corticotrophin-releasing hormone (CRH) impair oocyte competence by triggering apoptosis of ovarian cells but the underlying mechanisms are largely unclear. Although one study demonstrated that RS and CRH elevation triggered apoptosis in ovarian cells and oocytes via activating Fas/FasL signalling, other studies suggested that RS might damage cells by activating other pathways as well as Fas signalling. The objective of this study was to test whether RS and CRH elevation impairs oocytes by activating tumour necrosis factor α (TNF-α) signalling. Our in vivo experiments showed that RS applied during oocyte prematuration significantly increased expression of TNF-α and its receptor (TNFR1) while inducing apoptosis in both oocytes and mural granulosa cells (MGCs). In vitro treatment of MGCs with CRH significantly increased their apoptotic percentages and levels of TNF-α and TNFR1 expression. In vitro knockdown by interfering RNA, in vivo knockout of the TNF-α gene or injection of TNF-α antagonist etanercept significantly relieved the adverse effects of RS and CRH on apoptosis of MGCs and/or the developmental potential and apoptosis of oocytes. The results suggest that RS and CRH elevation in females impair oocyte competence through activating TNF-α signalling and that a TNF-α antagonist might be adopted to ameliorate the adverse effects of psychological stress on oocytes.
Additional keywords: apoptosis, psychological stress, TNF-α signaling.
References
Baigent, S. M., and Lowry, P. J. (2000). mRNA expression profiles for corticotrophin-releasing factor (CRF), urocortin, CRF receptors and CRF-binding protein in peripheral rat tissues. J. Mol. Endocrinol. 25, 43–52.| mRNA expression profiles for corticotrophin-releasing factor (CRF), urocortin, CRF receptors and CRF-binding protein in peripheral rat tissues.Crossref | GoogleScholarGoogle Scholar | 10915217PubMed |
Chie, K., Katsuo, N., Yoshiyuki, T., DenIchi, M., and Gen-Ichiro, S. (1994). Constitutive expression of TNF-alpha and -beta genes in mouse embryo: roles of cytokines as regulator and effector on development. Int. J. Biochem. 26, 111–119.
| Constitutive expression of TNF-alpha and -beta genes in mouse embryo: roles of cytokines as regulator and effector on development.Crossref | GoogleScholarGoogle Scholar |
Copper, R. L., Goldenberg, R. L., Das, A., Elder, N., Swain, M., Norman, G., Ramsey, R., Cotroneo, P., Collins, B. A., Johnson, F., Jones, P., and Meier, A. M. (1996). The preterm prediction study: maternal stress is associated with spontaneous preterm birth at less than thirty-five weeks’ gestation. Am. J. Obstet. Gynecol. 175, 1286–1292.
| The preterm prediction study: maternal stress is associated with spontaneous preterm birth at less than thirty-five weeks’ gestation.Crossref | GoogleScholarGoogle Scholar | 8942502PubMed |
Dawson, A. A., Diedrich, K., and Felberbaum, R. E. (2005). Why do couples refuse or discontinue ART? Arch. Gynecol. Obstet. 273, 3–11.
| Why do couples refuse or discontinue ART?Crossref | GoogleScholarGoogle Scholar | 16080011PubMed |
Deb, G. K., Dey, S. R., Bang, J. I., Cho, S. J., Park, H. C., Lee, J. G., and Kong, I. K. (2011). 9-cis retinoic acid improves developmental competence and embryo quality during in vitro maturation of bovine oocytes through the inhibition of oocyte tumor necrosis factor-α gene expression. J. Anim. Sci. 89, 2759–2767.
| 9-cis retinoic acid improves developmental competence and embryo quality during in vitro maturation of bovine oocytes through the inhibition of oocyte tumor necrosis factor-α gene expression.Crossref | GoogleScholarGoogle Scholar | 21478451PubMed |
Dermitzaki, E., Tsatsanis, C., Gravanis, A., and Margioris, A. N. (2002). Corticotropin-releasing hormone induces Fas ligand production and apoptosis in PC12 cells via activation of p38 mitogen-activated protein kinase. J. Biol. Chem. 277, 12280–12287.
| Corticotropin-releasing hormone induces Fas ligand production and apoptosis in PC12 cells via activation of p38 mitogen-activated protein kinase.Crossref | GoogleScholarGoogle Scholar | 11790788PubMed |
Ebbesen, S. M., Zachariae, R., Mehlsen, M. Y., Thomsen, D., Højgaard, A., Ottosen, L., Petersen, T., and Ingerslev, H. J. (2009). Stressful life events are associated with a poor in vitro fertilization (IVF) outcome: a prospective study. Hum. Reprod. 24, 2173–2182.
| Stressful life events are associated with a poor in vitro fertilization (IVF) outcome: a prospective study.Crossref | GoogleScholarGoogle Scholar | 19465459PubMed |
Fu, J., Li, L., Qi, L., and Zhao, L. (2019). A randomized controlled trial of etanercept in the treatment of refractory recurrent spontaneous abortion with innate immune disorders. Taiwan. J. Obstet. Gynecol. 58, 621–625.
| A randomized controlled trial of etanercept in the treatment of refractory recurrent spontaneous abortion with innate immune disorders.Crossref | GoogleScholarGoogle Scholar | 31542082PubMed |
Glavin, G. B., Paré, W. P., Sandbak, T., Bakke, H. K., and Murison, R. (1994). Restraint stress in biomedical research: an update. Neurosci. Biobehav. Rev. 18, 223–249.
| Restraint stress in biomedical research: an update.Crossref | GoogleScholarGoogle Scholar | 8058215PubMed |
Greenfeld, C. R., Roby, K. F., Pepling, M. E., Babus, J. K., Terranova, P. F., and Flaws, J. A. (2007). Tumor necrosis factor (TNF) receptor type 2 is an important mediator of TNF alpha function in the mouse ovary. Biol. Reprod. 76, 224–231.
| Tumor necrosis factor (TNF) receptor type 2 is an important mediator of TNF alpha function in the mouse ovary.Crossref | GoogleScholarGoogle Scholar | 17065602PubMed |
Habib, K. E., Weld, K. P., Rice, K. C., Pushkas, J., Champoux, M., Listwak, S., Webster, E. L., Atkinson, A. J., Schulkin, J., Contoreggi, C., Chrousos, G. P., McCann, S. M., Suomi, S. J., Higley, J. D., and Gold, P. W. (2000). Oral administration of a corticotropin-releasing hormone receptor antagonist significantly attenuates behavioral, neuroendocrine, and autonomic responses to stress in primates. Proc. Natl. Acad. Sci. USA 97, 6079–6084.
| Oral administration of a corticotropin-releasing hormone receptor antagonist significantly attenuates behavioral, neuroendocrine, and autonomic responses to stress in primates.Crossref | GoogleScholarGoogle Scholar | 10823952PubMed |
Idriss, H. T., and Naismith, J. H. (2000). TNF alpha and the TNF receptor superfamily: structure–function relationship(s). Microsc. Res. Tech. 50, 184–195.
| TNF alpha and the TNF receptor superfamily: structure–function relationship(s).Crossref | GoogleScholarGoogle Scholar | 10891884PubMed |
Jin, L., Li, C., Li, R., Sun, Z., Fang, X., and Li, S. (2014). Corticotropin-releasing hormone receptors mediate apoptosis via cytosolic calcium-dependent phospholipase A2 and migration in prostate cancer cell RM-1. J. Mol. Endocrinol. 52, 255–267.
| Corticotropin-releasing hormone receptors mediate apoptosis via cytosolic calcium-dependent phospholipase A2 and migration in prostate cancer cell RM-1.Crossref | GoogleScholarGoogle Scholar | 24776847PubMed |
Kavurma, M. M., Tan, N. Y., and Bennett, M. R. (2008). Death receptors and their ligands in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 28, 1694–1702.
| Death receptors and their ligands in atherosclerosis.Crossref | GoogleScholarGoogle Scholar | 18669890PubMed |
Kiapekou, E., Zapanti, E., Mastorakos, G., and Loutradis, D. (2010). Update on the role of ovarian corticotropin-releasing hormone. Ann. N. Y. Acad. Sci. 1205, 225–229.
| Update on the role of ovarian corticotropin-releasing hormone.Crossref | GoogleScholarGoogle Scholar | 20840277PubMed |
Klonoff-Cohen, H., and Natarajan, L. (2004). The concerns during assisted reproductive technologies (CART) scale and pregnancy outcomes. Fertil. Steril. 81, 982–988.
| The concerns during assisted reproductive technologies (CART) scale and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 15066452PubMed |
Klonoff-Cohen, H., Chu, E., Natarajan, L., and Sieber, W. (2001). A prospective study of stress among women undergoing in vitro fertilization or gamete intrafallopian transfer. Fertil. Steril. 76, 675–687.
| A prospective study of stress among women undergoing in vitro fertilization or gamete intrafallopian transfer.Crossref | GoogleScholarGoogle Scholar | 11591398PubMed |
Kong, Q. Q., Wang, J., Xiao, B., Lin, F. H., Zhu, J., Sun, G. Y., Luo, M. J., and Tan, J. H. (2018). Cumulus cell-released tumor necrosis factor (TNF)-α promotes post-ovulatory aging of mouse oocytes. Aging (Albany NY) 10, 1745–1757.
| Cumulus cell-released tumor necrosis factor (TNF)-α promotes post-ovulatory aging of mouse oocytes.Crossref | GoogleScholarGoogle Scholar | 30048240PubMed |
Li, C. Y., Li, Z. B., Kong, Q. Q., Han, X., Xiao, B., Li, X., Chang, Z. L., and Tan, J. H. (2018). Restraint-induced corticotrophin-releasing hormone elevation triggers apoptosis of ovarian cells and impairs oocyte competence via activation of the Fas/FasL system. Biol. Reprod. 99, 828–837.
| Restraint-induced corticotrophin-releasing hormone elevation triggers apoptosis of ovarian cells and impairs oocyte competence via activation of the Fas/FasL system.Crossref | GoogleScholarGoogle Scholar | 29668880PubMed |
Liang, B., Wei, D. L., Cheng, Y. N., Yuan, H. J., Lin, J., Cui, X. Z., Luo, M. J., and Tan, J. H. (2013). Restraint stress impairs oocyte developmental potential in mice: role of CRH-induced apoptosis of ovarian cells. Biol. Reprod. 89, 64.
| Restraint stress impairs oocyte developmental potential in mice: role of CRH-induced apoptosis of ovarian cells.Crossref | GoogleScholarGoogle Scholar | 23884643PubMed |
Macklon, N. S., Stouffer, R. L., Giudice, L. C., and Fauser, B. C. (2006). The science behind 25 years of ovarian stimulation for in vitro fertilization. Endocr. Rev. 27, 170–207.
| The science behind 25 years of ovarian stimulation for in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 16434510PubMed |
Marcinkiewicz, J. L., Balchak, S. K., and Morrison, L. J. (2002). The involvement of tumor necrosis factor-alpha (TNF) as an intra-ovarian regulator of oocyte apoptosis in the neonatal rat. Front. Biosci. 7, d1997–d2005.
| 12161343PubMed |
Mekinian, A., Cohen, J., Alijotas-Reig, J., Carbillon, L., Nicaise-Roland, P., Kayem, G., Daraï, E., Fain, O., and Bornes, M. (2016). Unexplained recurrent miscarriage and recurrent implantation failure: is there a place for immunomodulation? Am. J. Reprod. Immunol. 76, 8–28.
| Unexplained recurrent miscarriage and recurrent implantation failure: is there a place for immunomodulation?Crossref | GoogleScholarGoogle Scholar | 26847715PubMed |
Neggers, Y., Goldenberg, R., Cliver, S., and Hauth, J. (2006). The relationship between psychosocial profile, health practices, and pregnancy outcomes. Acta Obstet. Gynecol. Scand. 85, 277–285.
| The relationship between psychosocial profile, health practices, and pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 16553174PubMed |
Ock, J., Lee, H., Kim, S., Lee, W. H., Choi, D. K., Park, E. J., Kim, S. H., Kim, I. K., and Suk, K. (2006). Induction of microglial apoptosis by corticotropin-releasing hormone. J. Neurochem. 98, 962–972.
| Induction of microglial apoptosis by corticotropin-releasing hormone.Crossref | GoogleScholarGoogle Scholar | 16893426PubMed |
Önalan, G., Tohma, Y. A., and Zeyneloğlu, H. B. (2018). Effect of etanercept on the success of assisted reproductive technology in patients with endometrioma. Gynecol. Obstet. Invest. 83, 358–364.
| Effect of etanercept on the success of assisted reproductive technology in patients with endometrioma.Crossref | GoogleScholarGoogle Scholar | 29208847PubMed |
Paré, W. P., and Glavin, G. B. (1986). Restraint stress in biomedical research: a review. Neurosci. Biobehav. Rev. 10, 339–370.
| Restraint stress in biomedical research: a review.Crossref | GoogleScholarGoogle Scholar | 3095718PubMed |
Polinder, S., Heijnen, E. M., Macklon, N. S., Habbema, J. D., Fauser, B. J., and Eijkemans, M. J. (2007). Cost-effectiveness of a mild compared with a standard strategy for IVF: a randomized comparison using cumulative term live birth as the primary endpoint. Hum. Reprod. 23, 316–323.
| Cost-effectiveness of a mild compared with a standard strategy for IVF: a randomized comparison using cumulative term live birth as the primary endpoint.Crossref | GoogleScholarGoogle Scholar | 18033807PubMed |
Song, J. P., Chen, X., Yang, G., and Geng, X. R. (2013). Corticotropin releasing hormone activates CD14+ cells to induce endothelial barrier dysfunction. Cell Biol. Int. 37, 1055–1060.
| Corticotropin releasing hormone activates CD14+ cells to induce endothelial barrier dysfunction.Crossref | GoogleScholarGoogle Scholar |
Soto, P., Natzke, R. P., and Hansen, P. J. (2003). Actions of tumor necrosis factor-alpha on oocyte maturation and embryonic development in cattle. Am. J. Reprod. Immunol. 50, 380–388.
| Actions of tumor necrosis factor-alpha on oocyte maturation and embryonic development in cattle.Crossref | GoogleScholarGoogle Scholar | 14750697PubMed |
Terranova, P. F., Hunter, V. J., Roby, K. F., and Hunt, J. S. (1995). Tumor necrosis factor-alpha in the female reproductive tract. Proc. Soc. Exp. Biol. Med. 209, 325–342.
| Tumor necrosis factor-alpha in the female reproductive tract.Crossref | GoogleScholarGoogle Scholar | 7638240PubMed |
Torres-Reverón, A., Rivera-Lopez, L. L., Flores, I., and Appleyard, C. B. (2018). Antagonizing the corticotropin releasing hormone receptor 1 with antalarmin reduces the progression of endometriosis. PLoS One 13, e0197698.
| Antagonizing the corticotropin releasing hormone receptor 1 with antalarmin reduces the progression of endometriosis.Crossref | GoogleScholarGoogle Scholar | 30427841PubMed |
Verhaak, C. M., Smeenk, J. M., van Minnen, A., Kremer, J. A., and Kraaimaat, F. W. A. (2005). Longitudinal, prospective study on emotional adjustment before, during and after consecutive fertility treatment cycles. Hum. Reprod. 20, 2253–2260.
| Longitudinal, prospective study on emotional adjustment before, during and after consecutive fertility treatment cycles.Crossref | GoogleScholarGoogle Scholar | 15817584PubMed |
Verhaak, C. M., Smeenk, J. M., Evers, A. W., Kremer, J. A., Kraaimaat, F. W., and Braat, D. D. (2007). Women’s emotional adjustment to IVF: a systematic review of 25 years of research. Hum. Reprod. Update 13, 27–36.
| Women’s emotional adjustment to IVF: a systematic review of 25 years of research.Crossref | GoogleScholarGoogle Scholar | 16940360PubMed |
Xiao, B., Li, X., Feng, X. Y., Gong, S., Li, Z. B., Zhang, J., Yuan, H. J., and Tan, J. H. (2019). Restraint stress of male mice induces apoptosis in spermatozoa and spermatogenic cells: role of the FasL/Fas system. Biol. Reprod. 101, 235–247.
| Restraint stress of male mice induces apoptosis in spermatozoa and spermatogenic cells: role of the FasL/Fas system.Crossref | GoogleScholarGoogle Scholar | 31066896PubMed |
Yuan, H. J., Li, Z. B., Zhao, X. Y., Sun, G. Y., Wang, G. L., Zhao, Y. Q., Zhang, M., and Tan, J. H. (2020). Glucocorticoids impair oocyte competence and trigger apoptosis of ovarian cells via activating the TNF-α system. Reprod. , .
| Glucocorticoids impair oocyte competence and trigger apoptosis of ovarian cells via activating the TNF-α system.Crossref | GoogleScholarGoogle Scholar |
Zhang, S. Y., Wang, J. Z., Li, J. J., Wei, D. L., Sui, H. S., Zhang, Z. H., Zhou, P., and Tan, J. H. (2011). Maternal restraint stress diminishes the developmental potential of oocytes. Biol. Reprod. 84, 672–681.
| Maternal restraint stress diminishes the developmental potential of oocytes.Crossref | GoogleScholarGoogle Scholar | 21123817PubMed |
Zhang, Y., Liu, W., Ma, C., Geng, J., Li, Y., Li, S., Yu, F., Zhang, X., and Cong, B. (2012). Endoplasmic reticulum stress contributes to CRH-induced hippocampal neuron apoptosis. Exp. Cell Res. 318, 732–740.
| Endoplasmic reticulum stress contributes to CRH-induced hippocampal neuron apoptosis.Crossref | GoogleScholarGoogle Scholar | 22285133PubMed |
Zheng, L. L., Tan, X. W., Cui, X. Z., Yuan, H. J., Li, H., Jiao, G. Z., Ji, C. L., and Tan, J. H. (2016). Preimplantation maternal stress impairs embryo development by inducing oviductal apoptosis with activation of the Fas system. Mol. Hum. Reprod. 22, 778–790.
| Preimplantation maternal stress impairs embryo development by inducing oviductal apoptosis with activation of the Fas system.Crossref | GoogleScholarGoogle Scholar | 27475493PubMed |
Zhou, P., Lian, H. Y., Cui, W., Wei, D. L., Li, Q., Liu, Y. X., Liu, X. Y., and Tan, J. H. (2012). Maternal-restraint stress increases oocyte aneuploidy by impairing metaphase I spindle assembly and reducing spindle assembly checkpoint proteins in mice. Biol. Reprod. 86, 83.
| Maternal-restraint stress increases oocyte aneuploidy by impairing metaphase I spindle assembly and reducing spindle assembly checkpoint proteins in mice.Crossref | GoogleScholarGoogle Scholar | 22133696PubMed |
