Chronic restraint stress disturbs meiotic resumption through APC/C-mediated cyclin B1 excessive degradation in mouse oocytes

References

• Klonoff-Cohen H, Chu E, Natarajan L, et al. A prospective study of stress among women undergoing in vitro fertilization or gamete intrafallopian transfer. Fertil Steril. 2001;76:675–687.
   PubMed Web of Science ®Google Scholar
• Schroder AK, Katalinic A, Diedrich K, et al. Cumulative pregnancy rates and drop-out rates in a German IVF programme: 4102 cycles in 2130 patients. Reproductive Biomedicine Online. 2004;8:600–606.
   PubMed Web of Science ®Google Scholar
• Terzioglu F, Turk R, Yucel C, et al. The effect of anxiety and depression scores of couples who underwent assisted reproductive techniques on the pregnancy outcomes. Afr Health Sci. 2016;16:441–450.
   PubMed Web of Science ®Google Scholar
• Liang B, Wei DL, Cheng YN, et al. Restraint stress impairs oocyte developmental potential in mice: role of CRH-induced apoptosis of ovarian cells. Biol Reprod. 2013;89:64.
   PubMed Web of Science ®Google Scholar
• Ghizzoni L, Mastorakos G, Vottero A, et al. Corticotropin-releasing hormone (CRH) inhibits steroid biosynthesis by cultured human granulosa-lutein cells in a CRH and interleukin-1 receptor-mediated fashion. Endocrinology. 1997;138:4806–4811.
   PubMed Web of Science ®Google Scholar
• Dinopoulou V, Partsinevelos GA, Mavrogianni D, et al. The effect of CRH and its inhibitor, antalarmin, on in vitro growth of preantral mouse follicles, early embryo development, and steroidogenesis. Endocrinology. 2013;154:222–231.
   PubMed Web of Science ®Google Scholar
• Zhang SY, Wang JZ, Li JJ, et al. Maternal restraint stress diminishes the developmental potential of oocytes. Biol Reprod. 2011;84:672–681.
   PubMed Web of Science ®Google Scholar
• Zhou P, Lian HY, Cui W, et al. Maternal-restraint stress increases oocyte aneuploidy by impairing metaphase I spindle assembly and reducing spindle assembly checkpoint proteins in mice. Biol Reprod. 2012;86:83.
   PubMed Web of Science ®Google Scholar
• Divyashree S, Yajurvedi HN. Long-term chronic stress exposure induces PCO phenotype in rat. Reproduction. 2016;152:765–774.
   PubMed Web of Science ®Google Scholar
• Sirard MA, Desrosier S, Assidi M. In vivo and in vitro effects of FSH on oocyte maturation and developmental competence. Theriogenology. 2007;68 Suppl 1:S71–6.
   PubMed Web of Science ®Google Scholar
• Blondin P, Bousquet D, Twagiramungu H, et al. Manipulation of follicular development to produce developmentally competent bovine oocytes. Biol Reprod. 2002;66:38–43.
   PubMed Web of Science ®Google Scholar
• Homer H, Gui L, Carroll J. A spindle assembly checkpoint protein functions in prophase I arrest and prometaphase progression. Science. 2009;326:991–994.
   PubMed Web of Science ®Google Scholar
• Manandhar G, Schatten H, Sutovsky P. Centrosome reduction during gametogenesis and its significance. Biol Reprod. 2005;72:2–13.
   PubMed Web of Science ®Google Scholar
• Schuh M, Ellenberg J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell. 2007;130:484–498.
   PubMed Web of Science ®Google Scholar
• Keefe D, Liu L, Wang W, et al. Imaging meiotic spindles by polarization light microscopy: principles and applications to IVF. Reproductive Biomedicine Online. 2003;7:24–29.
   PubMedGoogle Scholar
• Wang WH, Keefe DL. Spindle observation in living mammalian oocytes with the polarization microscope and its practical use. Cloning and Stem Cells. 2002;4:269–276.
   PubMedGoogle Scholar
• Chen SU, Lien YR, Chao KH, et al. Effects of cryopreservation on meiotic spindles of oocytes and its dynamics after thawing: clinical implications in oocyte freezing–a review article. Mol Cell Endocrinol. 2003;202:101–107.
   PubMed Web of Science ®Google Scholar
• Wang WH, Meng L, Hackett RJ, et al. Limited recovery of meiotic spindles in living human oocytes after cooling-rewarming observed using polarized light microscopy. Hum Reproduction. 2001;16:2374–2378.
   PubMed Web of Science ®Google Scholar
• Moon JH, Hyun CS, Lee SW, et al. Visualization of the metaphase II meiotic spindle in living human oocytes using the Polscope enables the prediction of embryonic developmental competence after ICSI. Hum Reproduction. 2003;18:817–820.
   PubMed Web of Science ®Google Scholar
• Cristina Magli M, Capoti A, Resta S, et al. Prolonged absence of meiotic spindles by birefringence imaging negatively affects normal fertilization and embryo development. Reproductive Biomedicine Online. 2011;23:747–754.
   PubMed Web of Science ®Google Scholar
• Lenart P, Ellenberg J. Nuclear envelope dynamics in oocytes: from germinal vesicle breakdown to mitosis. Curr Opin Cell Biol. 2003;15:88–95.
   PubMed Web of Science ®Google Scholar
• Sanchez F, Romero S, De Vos M, et al. Human cumulus-enclosed germinal vesicle oocytes from early antral follicles reveal heterogeneous cellular and molecular features associated with in vitro maturation capacity. Hum Reproduction. 2015;30:1396–1409.
   PubMed Web of Science ®Google Scholar
• Luciano AM, Franciosi F, Modina SC, et al. Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol Reprod. 2011;85:1252–1259.
   PubMed Web of Science ®Google Scholar
• Gall L, De Smedt V, Crozet N, et al. Meiotically incompetent and competent goat oocytes: timing of nuclear events and protein phosphorylation. Theriogenology. 1996;46:825–835.
   PubMed Web of Science ®Google Scholar
• Higaki S, Kishi M, Koyama K, et al. Early germinal vesicle breakdown is a predictor of high preimplantation developmental competent oocytes in mice. Zygote. 2017;25:41–48.
   PubMed Web of Science ®Google Scholar
• Zeng HT, Ren Z, Guzman L, et al. Heparin and cAMP modulators interact during pre-in vitro maturation to affect mouse and human oocyte meiosis and developmental competence. Hum Reproduction. 2013;28:1536–1545.
   PubMed Web of Science ®Google Scholar
• Silva GM, Brito IR, Sales AD, et al. In vitro growth and maturation of isolated caprine preantral follicles: influence of insulin and FSH concentration, culture dish, coculture, and oocyte size on meiotic resumption. Theriogenology. 2017;90:32–41.
   PubMed Web of Science ®Google Scholar
• Eppig JJ, Schroeder AC. Capacity of mouse oocytes from preantral follicles to undergo embryogenesis and development to live young after growth, maturation, and fertilization in vitro. Biol Reprod. 1989;41:268–276.
   PubMed Web of Science ®Google Scholar
• Zuccotti M, Giorgi Rossi P, Martinez A, et al. Meiotic and developmental competence of mouse antral oocytes. Biol Reprod. 1998;58:700–704.
   PubMed Web of Science ®Google Scholar
• Holt JE, Tran SM, Stewart JL, et al. The APC/C activator FZR1 coordinates the timing of meiotic resumption during prophase I arrest in mammalian oocytes. Development. 2011;138:905–913.
   PubMed Web of Science ®Google Scholar
• Dedieu T, Gall L, Crozet N, et al. Mitogen-activated protein kinase activity during goat oocyte maturation and the acquisition of meiotic competence. Mol Reprod Dev. 1996;45:351–358.
   PubMed Web of Science ®Google Scholar
• Hirao Y, Miyano T, Kato S. Acquisition of maturational competence in in vitro grown mouse oocytes. J Exp Zool. 1993;267:543–547.
   PubMedGoogle Scholar
• Bui TTH, Belli M, Fassina L, et al. Cytoplasmic movement profiles of mouse surrounding nucleolus and not-surrounding nucleolus antral oocytes during meiotic resumption. Mol Reprod Dev. 2017;84:356–362.
   PubMed Web of Science ®Google Scholar
• Han SJ, Chen R, Paronetto MP, et al. Wee1B is an oocyte-specific kinase involved in the control of meiotic arrest in the mouse. Curr Biol. 2005;15:1670–1676.
   PubMed Web of Science ®Google Scholar
• Holt JE, Weaver J, Jones KT. Spatial regulation of APCCdh1-induced cyclin B1 degradation maintains G2 arrest in mouse oocytes. Development. 2010;137:1297–1304.
   PubMed Web of Science ®Google Scholar
• Sivakumar S, Gorbsky GJ. Spatiotemporal regulation of the anaphase-promoting complex in mitosis. Nat Rev Mol Cell Biol. 2015;16:82–94.
   PubMed Web of Science ®Google Scholar
• Herbert M, Levasseur M, Homer H, et al. Homologue disjunction in mouse oocytes requires proteolysis of securin and cyclin B1. Nat Cell Biol. 2003;5:1023–1025.
   PubMed Web of Science ®Google Scholar
• Durinzi KL, Saniga EM, Lanzendorf SE. The relationship between size and maturation in vitro in the unstimulated human oocyte. Fertil Steril. 1995;63:404–406.
   PubMed Web of Science ®Google Scholar
• Fair T, Hyttel P, Greve T. Bovine oocyte diameter in relation to maturational competence and transcriptional activity. Mol Reprod Dev. 1995;42:437–442.
   PubMed Web of Science ®Google Scholar
• Liu H, Aoki F. Transcriptional activity associated with meiotic competence in fully grown mouse GV oocytes. Zygote. 2002;10:327–332.
   PubMed Web of Science ®Google Scholar
• Zuccotti M, Ponce RH, Boiani M, et al. The analysis of chromatin organisation allows selection of mouse antral oocytes competent for development to blastocyst. Zygote. 2002;10:73–78.
   PubMed Web of Science ®Google Scholar
• Holt JE, Lane SI, Jennings P, et al. APC(FZR1) prevents nondisjunction in mouse oocytes by controlling meiotic spindle assembly timing. Mol Biol Cell. 2012;23:3970–3981.
   PubMed Web of Science ®Google Scholar
• Yang Y, Yang CR, Han SJ, et al. Maternal mRNAs with distinct 3ʹ UTRs define the temporal pattern of Ccnb1 synthesis during mouse oocyte meiotic maturation. Genes Dev. 2017;31:1302–1307.
   PubMed Web of Science ®Google Scholar
• Peters JM. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat Rev Mol Cell Biol. 2006;7:644–656.
   PubMed Web of Science ®Google Scholar
• Josefsberg LB, Galiani D, Dantes A, et al. The proteasome is involved in the first metaphase-to-anaphase transition of meiosis in rat oocytes. Biol Reprod. 2000;62:1270–1277.
   PubMed Web of Science ®Google Scholar
• Terret ME, Wassmann K, Waizenegger I, et al. The meiosis I-to-meiosis II transition in mouse oocytes requires separase activity. Curr Biol. 2003;13:1797–1802.
   PubMed Web of Science ®Google Scholar
• Kalich-Philosoph L, Roness H, Carmely A, et al. Cyclophosphamide triggers follicle activation and “burnout”; AS101 prevents follicle loss and preserves fertility. Sci Transl Med. 2013;5:185ra62.
   PubMed Web of Science ®Google Scholar
• Wu XF, Yuan HJ, Li H, et al. Restraint stress on female mice diminishes the developmental potential of oocytes: roles of chromatin configuration and histone modification in germinal vesicle stage oocytes. Biol Reprod. 2015;92:13.
   PubMed Web of Science ®Google Scholar
• Watanabe Y. Geometry and force behind kinetochore orientation: lessons from meiosis. Nat Rev Mol Cell Biol. 2012;13:370–382.
   PubMed Web of Science ®Google Scholar
• Qiu D, Hou X, Han L, et al. Sirt2-BubR1 acetylation pathway mediates the effects of advanced maternal age on oocyte quality. Aging Cell. 2018;17.
   Web of Science ®Google Scholar
• Han L, Wang H, Li L, et al. Melatonin protects against maternal obesity-associated oxidative stress and meiotic defects in oocytes via the SIRT3-SOD2-dependent pathway. J Pineal Res. 2017;63:e12431.
   Web of Science ®Google Scholar
• Machtinger R, Combelles CM, Missmer SA, et al. The association between severe obesity and characteristics of failed fertilized oocytes. Hum Reproduction. 2012;27:3198–3207.
   PubMed Web of Science ®Google Scholar
• Miao Y, Zhou C, Bai Q, et al. The protective role of melatonin in porcine oocyte meiotic failure caused by the exposure to benzo(a)pyrene. Hum Reproduction. 2018;33:116–127.
   PubMed Web of Science ®Google Scholar
• Zhang M, Miao Y, Chen Q, et al. BaP exposure causes oocyte meiotic arrest and fertilization failure to weaken female fertility. FASEB J. 2018;32:342–352.
   PubMed Web of Science ®Google Scholar
• Liu YX, Cheng YN, Miao YL, et al. Psychological stress on female mice diminishes the developmental potential of oocytes: a study using the predatory stress model. PloS One. 2012;7:e48083.
   PubMed Web of Science ®Google Scholar
• Marangos P, Carroll J. The dynamics of cyclin B1 distribution during meiosis I in mouse oocytes. Reproduction. 2004;128:153–162.
   PubMed Web of Science ®Google Scholar
• Hinchcliffe EH, Thompson EA, Miller FJ, et al. Nucleo-cytoplasmic interactions that control nuclear envelope breakdown and entry into mitosis in the sea urchin zygote. J Cell Sci. 1999;112(Pt 8):1139–1148.
   PubMed Web of Science ®Google Scholar
• Takizawa CG, Morgan DO. Control of mitosis by changes in the subcellular location of cyclin-B1-Cdk1 and Cdc25C. Curr Opin Cell Biol. 2000;12:658–665.
   PubMed Web of Science ®Google Scholar
• Reis A, Chang HY, Levasseur M, et al. APCcdh1 activity in mouse oocytes prevents entry into the first meiotic division. Nat Cell Biol. 2006;8:539–540.
   PubMed Web of Science ®Google Scholar
• Marangos P, Carroll J. Securin regulates entry into M-phase by modulating the stability of cyclin B. Nat Cell Biol. 2008;10:445–451.
   PubMed Web of Science ®Google Scholar
• Ogushi S, Fulka J Jr., Miyano T. Germinal vesicle materials are requisite for male pronucleus formation but not for change in the activities of CDK1 and MAP kinase during maturation and fertilization of pig oocytes. Dev Biol. 2005;286:287–298.
   PubMed Web of Science ®Google Scholar
• Inoue A, Nakajima R, Nagata M, et al. Contribution of the oocyte nucleus and cytoplasm to the determination of meiotic and developmental competence in mice. Hum Reproduction. 2008;23:1377–1384.
   PubMed Web of Science ®Google Scholar
• Lee HS, Yin XJ, Jin YX, et al. Germinal vesicle chromatin configuration and meiotic competence is related to the oocyte source in canine. Anim Reprod Sci. 2008;103:336–347.
   PubMed Web of Science ®Google Scholar
• Kumar S, Kumar M, Dholpuria S, et al. Transient arrest of germinal vesicle breakdown improved in vitro development potential of buffalo (Bubalus Bubalis) oocytes. J Cell Biochem. 2018;119:278–289.
   PubMed Web of Science ®Google Scholar
• Shu YM, Zeng HT, Ren Z, et al. Effects of cilostamide and forskolin on the meiotic resumption and embryonic development of immature human oocytes. Hum Reproduction. 2008;23:504–513.
   PubMed Web of Science ®Google Scholar
• Ola SI, Wang Q, Ai JS, et al. Meiotic competence and acetylation pattern of UV light classified mouse antral oocytes after meiotic arrest with isobutylmethylxanthine. Mol Reprod Dev. 2007;74:591–599.
   PubMed Web of Science ®Google Scholar
• Monti M, Redi CA. Isolation and characterization of mouse antral oocytes based on nucleolar chromatin organization. J Vis Exp. 2016;107:e53616.
   PubMed Web of Science ®Google Scholar
• Ami D, Mereghetti P, Natalello A, et al. FTIR spectral signatures of mouse antral oocytes: molecular markers of oocyte maturation and developmental competence. Biochim Biophys Acta. 2011;1813:1220–1229.
   PubMed Web of Science ®Google Scholar