doi: 10.4161/cc.5.3.2395, Hanna, C. W., Taudt, A., Huang, J., Gahurova, L., Kranz, A., Andrews, S., et al. doi: 10.1093/molehr/gah009, Jones, K. T. (2011). Loss of the E2 SUMO-conjugating enzyme Ube2i in oocytes during ovarian folliculogenesis causes infertility in mice. (2007). doi: 10.1016/j.mce.2013.07.027, Akiyama, T., Kim, J. M., Nagata, M., and Aoki, F. (2004). The length of each phase can also change over . Biol. It should increase during ovulation and remain elevated when youre in the luteal phase. 277, 2574825755. Sci. doi: 10.1095/biolreprod.105.048553, Swain, J. E., Ding, J., Brautigan, D. L., Villa-Moruzzi, E., and Smith, G. D. (2007). Remember, it all starts in the ovary. Federal government websites often end in .gov or .mil. Activation of SIRT1 by resveratrol in vitro improves oocyte quality and embryo development in mice, pigs, and cows (Liu et al., 2013; Takeo et al., 2014; Wang et al., 2014; Itami et al., 2015; Li et al., 2016; Khan et al., 2017). Oocyte formation by mitotically-active germ cells purified from ovaries 120, 41174125. Cell-to-cell communication and ovulation. C-type natriuretic peptide: a link between hyperandrogenism and anovulation in a mouse model of polycystic ovary syndrome. Ovulation to implantation involves the journey of the oocyte through uterine tubes. Life Sci. An oocyte (UK: / o s a t /, US: / o o-/), ocyte, or ovocyte is a female gametocyte or germ cell involved in reproduction.In other words, it is an immature ovum, or egg cell.An oocyte is produced in a female fetus in the ovary during female gametogenesis.The female germ cells produce a primordial germ cell (PGC), which then undergoes mitosis, forming oogonia. Commun. 187, 383386. (2014). GnRH pulsatility, the pituitary response and reproductive dysfunction. Then, advances in the epigenetic aspects, such as histone acetylation, phosphorylation, methylation, glycosylation, ubiquitination, and SUMOylation related to the quality of oocyte maturation are reviewed. On the whole, HDAC8 is important for oocyte development and maturation, but the mechanisms of its action on oocytes needs further study. Genes Dev. doi: 10.1016/j.gde.2011.03.003, Wang, F., Tian, X., Zhang, L., He, C., Ji, P., Li, Y., et al. In addition, calcium signaling is involved in gonadotropin-induced oocyte maturation in many species (Veldhuis, 1987; Su et al., 1999; Zhang et al., 2007, 2009; Conti et al., 2012). 409, 194201. dominant follicle development) and precedes the Luteal phase (i.e. Both meiosis I and II consist of prophase, metaphase, anaphase and telophase. doi: 10.1126/science.1193573, Zhang, M., and Xia, G. (2012). Biochim. UBE2I (UBC9), a SUMO-conjugating enzyme, localizes to nuclear speckles and stimulates transcription in mouse oocytes. doi: 10.1530/rep.1.00824, Krege, J. H., Hodgin, J. doi: 10.1038/s41594-017-0013-5, Hao, X., Wang, Y., Kong, N., Zhang, Y., Zhao, Y., Xia, G., et al. doi: 10.1371/journal.pgen.1003377, Machaca, K. (2007). Endocrinology 146, 12361244. P. Sutovsky (New York, NY: Springer). U.S.A. 109, 27042704. 1975 Jan;64(1):37-47. doi: 10.1677/joe.0.0640037. 28 days. Commun. In bovine, the levels of MYST4 mRNA in both GV and MII oocytes are high. The hormones that stimulate ovulation are produced in the pituitary gland; these are known as the follicle-stimulating hormone and luteinizing hormone. (2002). Cell Dev. Rev. Moreover, the elevated calcium of cumulus granulosa cells inactivates NPR2, further decreasing the binding affinity of NPR2 for NPPC. Per each ovulation cycle, the average ovary loses 1,000 follicles to the process of selecting a dominant follicle that will be released. Commun. Genes Dev. 52, 99106. KDM5B is a master regulator of the H3K4-methylome in stem cells, development and cancer. (2015). doi: 10.1016/j.domaniend.2011.09.003, Nathan, D., Ingvarsdottir, K., Sterner, D. E., Bylebyl, G. R., Dokmanovic, M., Dorsey, J. doi: 10.1371/journal.pone.0038807, Yang, F., Hu, L., Chen, C., Yu, J., OConnell, C. B., Khodjakov, A., et al. The follicular phase refers to that part of your menstrual cycle when an egg matures in your ovaries. doi: 10.1074/jbc.M111871200, Geister, K. A., Brinkmeier, M. L., Hsieh, M., Faust, S. M., Karolyi, I. J., Perosky, J. E., et al. Dev. Cell Differ. Regulation of mammalian oocyte meiosis by intercellular communication within the ovarian follicle. Reprod. This is further approved by the fact that estrogen-promoted NPPC expression in granulosa cells can be enhanced by interaction with FSH (Lee et al., 2013). Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity. PKA balances the activities of WEE1B/MYT1 kinase and CDC25 phosphatase, and thus regulates the activity of cyclin-dependent kinase 1 (CDK1). Dev. Mol. The importance of SUMOylation on oocytes maturation could be highlighted by the following facts. The COMPASS family of histone H3K4 methylases: mechanisms of regulation in development and disease pathogenesis. - Uses, Facts & Properties, Arrow Pushing Mechanism in Organic Chemistry, Working Scholars Bringing Tuition-Free College to the Community. Resveratrol improves the mitochondrial function and fertilization outcome of bovine oocytes. Dev. (2015). (2017). Novel signaling mechanisms in the ovary during oocyte maturation and ovulation. doi: 10.1038/nsmb.3204, Yuan, Y. F., Zhai, R., Liu, X. M., Khan, H. A., Zhen, Y. H., and Huo, L. J. Sirt6 depletion causes spindle defects and chromosome misalignment during meiosis of mouse oocyte. Interestingly, supplementary natriuretic peptide precursor type B (NPPB) and NPPC are effective at improving the developmental competence of oocytes recovered from small-sized antral follicles of porcine in vitro (Zhang W. et al., 2015; Zhang Y. et al., 2017). Cleveland Clinic is a non-profit academic medical center. (2006). HDAC11 is the only member of class IV, which is homologous to both classes I and II (Gao et al., 2002). doi: 10.1016/S0012-1606(03)00134-9, Houben, A., Demidov, D., Rutten, T., and Scheidtmann, K. H. (2005). Importantly, the phenotypes of conditional knockout of DPAGT1 in infertile mouse oocytes is consistent with those in humans (Li et al., 2020). In developing mouse oocytes, the level of H3K4me3 are elevated during the transition of chromatin configuration from the non-surrounded nucleolus (NSN) to surrounded nucleolus (SN) type (Yu et al., 2017), the latter of which have better developmental competence after fertilization (Ma et al., 2013; Zhang et al., 2019). The generations of Cx43 transgene mice driven by zona pellucida 3 (ZP3) crossed with Cx37-null mice are fertile due to the restoration of oocytegranulosa cell coupling, oocyte growth, and oocyte maturation (Li et al., 2007). Female germ cells enter and undergo the first meiotic progression during embryonic development, and arrest at the diplotene stage of prophase I before birth. (2006). Depleted SIRT6 results in disruption of spindle morphology and chromosome alignment in oocytes (Han et al., 2015). Menstrual cycle stages: Phase by phase - Medical News Today Notice I said 'egg' - singular? All other trademarks and copyrights are the property of their respective owners. In female mammals, meiosis of oocytes starts before birth and sustains at the dictyate stage of meiotic prophase I before gonadotropins-induced ovulation happens. Reprod. In mouse oocytes, transcriptional destruction, especially the transcripts of oxidative phosphorylation, energy production, and protein synthesis during the transition from GV to MII, is selective rather than promiscuous. Hormonal control of mammalian oocyte meiosis at diplotene stage. HDAC6 localizes in the cytoplasm of mouse GV oocytes. (2010). It helped me pass my exam and the test questions are very similar to the practice quizzes on Study.com. Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control. Having a long follicular phase doesnt mean youre less likely to become pregnant. 70, 18431851. PLoS One 10:e0126194. doi: 10.1016/j.ydbio.2008.04.011, Ma, P., and Schultz, R. M. (2013). These cells produce androgens which diffuse into the granulosa cells and convert to estrogen for follicular development. This transition enables granulosa cells to respond to LH levels and produce Progesterone. Luteinizing hormone action in human oocyte maturation and quality: signaling pathways, regulation, and clinical impact. Therefore, one of the key points to initiate oocyte meiosis depends on when to activate CDK1. All rights reserved. The alpha subunit is common to all glycoproteins including TSH (thyroid-stimulating hormone) and HCG (human chorionic gonadotropin hormone). The relationship between FSH and LH hormones is responsible for the process that induces follicular development, rupture, release, and endometrial reception or shedding. In addition, inhibition of HDAC6 in GV oocytes prevents PB1 extrusion later because of disrupted maturational progression and meiotic apparatus assembly (Zhou et al., 2017; Sui et al., 2020a). Finishing this lesson should enable you to: 20 chapters | Similarly, inhibition of SIRT2 during in vitro oocyte maturation or knockout of SIRT2 blocks the progression of oocyte development after GVBD (Riepsamen et al., 2015). (2005). Starting in your late 30s, your FSH levels may still increase during your follicular phase, but your LH levels may not spike as they did previously. PLoS One 6:e20696. 34, 96159627. NPPC actives NPR2, GTP is converted into cGMP, then cGMP enters the oocyte through CX37 gap junctions. Nat. Copyright 2023, StatPearls Publishing LLC. Retinoid signaling determines germ cell fate in mice. Menstrual cycle proliferative and follicular phase. Biol. Later, oocytes in fully grown follicles in response to gonadotropins stimulation possess the capability to resume meiosis and ovulate in vivo. Meiotic arrest of oocytes depends on cell-to-cell communication in the ovarian follicle. Annu. Reprod. Dev. Maternal mRNAs with distinct 3 UTRs define the temporal pattern of Ccnb1 synthesis during mouse oocyte meiotic maturation. Reproduction 128, 153162. Inhibition of HDAC11 by JB3-22 significantly interrupted mouse oocyte meiosis progress, possibly because of abnormal spindle organization and misaligned chromosomes, impaired kinetochore-microtubule attachment, and spindle assembly checkpoint function (Sui et al., 2020b). 9:149. doi: 10.1186/1477-7827-9-149, Liu, M., Sims, D., Calarco, P., and Talbot, P. (2003). Cell Biol. doi: 10.1093/nar/gkh252, Yang, Y., Yang, C. R., Han, S. J., Daldello, E. M., Cho, A., Martins, J. P. S., et al. Biol. Role of cyclic nucleotide signaling in oocyte maturation. Biol. Oncol. High level of C-type natriuretic peptide induced by hyperandrogen-mediated anovulation in polycystic ovary syndrome mice. FOIA Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Inhibition of HDAC8 in fully grown oocytes causes spindle defects and chromosome misalignment during oocyte meiotic maturation, accompanied by impaired kinetochore-microtubule attachments (Zhang K. et al., 2017). In addition, Yang et al. Biol. After GVBD, it starts to accumulate around the chromosomes, and shows a spindle pole-like localization pattern in both MI and MII. Mol. Germ-line deletion of either HDAC1 or HDAC2 will cause mouse embryo lethality (Montgomery et al., 2007; Leboeuf et al., 2010). The above results indicate that HDAC3 in both granulosa cells and oocytes plays important regulatory roles in oocyte maturation. According to the hypothalamus-pituitary-ovary axis feedback theory, an LH surge in response to a peak estrogen surge initiates oocytes meiosis in vivo through positive feedback regulation. Reprod. C. R. Biol. Biol. (2003). Fully grown oocytes in early antral and preovulatory follicles have the capability to resume meiosis before LH surge (Holt et al., 2010). As part of the MPF, cyclin B1 must be constantly degraded by a multi-subunit ubiquitin E3 ligase named the anaphase promoting complex (APC) to maintain meiosis arrest (Jaffe and Egbert, 2017). Interestingly, the remarkable increment in ATP levels and formation of J-aggregates at 06:30 (i.e., just prior to the release of eggs) prompted us to examine the status of the endocrine and growth factor axis during these sampling hours.As shown in Figure 1D, lhcgr expression showed a sharp increment from 05:00 (1 h) onwards when the oocytes underwent GV migration and GVBD. Mol. The release of a secondary oocyte from the ovaries is called ovulation. Pre-ovulatory LH/hCG surge decreases C-type natriuretic peptide secretion by ovarian granulosa cells to promote meiotic resumption of pre-ovulatory oocytes. Endocrinology 120, 445449. Pollut. Similarly, inhibition of UBE2I for GV-stage mouse oocytes disrupts meiotic maturation and causes defects in spindle organization (Yuan et al., 2014), while overexpression of UBE2I in meiotic incompetent oocytes stimulates gene transcription in vitro (Ihara et al., 2008). (2011). Cell Cycle 19, 354362. Reprod. doi: 10.4161/cc.24991, Ma, P., Hua, P., Montgomery, R. L., Olson, E. N., and Schultz, R. M. (2012). Reprod. 77, 21812197. Anaphase-promoting complex control in female mouse meiosis. Resveratrol protects against age-associated infertility in mice. 29, 20112020. doi: 10.1083/jcb.200303047, Kim, J., Singh, A. K., Takata, Y., Lin, K., Shen, J., Lu, Y., et al. SUMO-1 plays crucial roles for spindle organization, chromosome congression, and chromosome segregation during mouse oocyte meiotic maturation. Endocrinology 145, 16171624. 5, 10231025. Endocr. Also, due to the decreased glycosylation of ZP proteins, the mutant oocytes have a thin and fragile ZP layer and have poor developmental ability after in vitro fertilization. SIRT2 knockdown also affects spindle organization and chromosome alignment during meiosis (Zhang L. et al., 2014). Modulation of cell-to-cell communication in the cumulus-oocyte complex and the regulation of oocyte maturation by LH. Cell 30, 6172. doi: 10.1111/j.1748-1716.1990.tb08953.x, Tsafriri, A., Cao, X., Ashkenazi, H., Motola, S., Popliker, M., and Pomerantz, S. H. (2005). In vitro, O-glycosylation is elevated in bovine COCs exposed to glucosamine (Sutton-McDowall et al., 2006). Estrogen also has many other effects that are important for bone health and cardiovascular health in premenopausal patients, which will be discussed in another article. CW and YY revised the manuscript. Dev. Cell Dev. UBE2I is downregulated following meiotic resumption (Ihara et al., 2008). Channing CP, Schaerf FW, Anderson LD, Tsafriri A. It is clear that cAMP exerts its role by activating protein kinase A (PKA). Patterns 7, 657665. 40 Articles, This article is part of the Research Topic, Epigenetic Modification Involved Systematically in Oocytes Development and Maturation, https://doi.org/10.3389/fcell.2021.654028, Creative Commons Attribution License (CC BY). When oocytes are isolated from the antral follicles, the cAMP levels within the oocytes decrease and meiosis resumes spontaneously (Trnell et al., 1990). (2004). Disclosure: Megan Lord declares no relevant financial relationships with ineligible companies. Mitogen-activated protein kinase mediates luteinizing hormone-induced breakdown of communication and oocyte maturation in rat ovarian follicles. In a PDE3 knockout model, oocytes are permanently arrested at the GV stage and female mice are infertile (Vaccari et al., 2008). Test your knowledge. In contrast, HDAC2 in the nucleus increases between 5 and 12 days post-partum, and is relatively stable during the growing period of mice oocytes. suspensory ligament of the ovary), which carries the ovarian artery and vein. The SET1 complex selects actively transcribed target genes via multivalent interaction with CpG island chromatin. Along with the growth of activated follicles, the transcription of genes necessary for oocyte growth and meiosis resumption accumulate and are stored in the cytoplasm. doi: 10.1073/pnas.95.26.15677, Krieg, A. J., Mullinax, S. R., Grimstad, F., Marquis, K., Constance, E., Hong, Y., et al. Stage specific expression of histone deacetylase 4 (HDAC4) during oogenesis and early preimplantation development in mice. Different epidermal-like growth factors, such as amphiregulin (AREG), epiregulin (EREG), and beta-cellulin (BTC) are expressed in MGCs and CGCs in autocrine and paracrine manners through respective EGF receptors (EGFRs) (Tsafriri et al., 2005; Conti et al., 2006; Hsieh et al., 2007). Hum. Genome Res. About 90% of the maternal mRNA is degraded at the two-cell stage of early mice embryos (Schellander et al., 2007). The regulation of maturation promoting factor during prophase I arrest and meiotic entry in mammalian oocytes. Meiosis arrest female 1 (MARF1) has nuage-like function in mammalian oocytes. J. Acetylation of H3/4 leads to open chromatin configuration, enhances transcriptional activity, and thereby promotes transcription factor binding to DNA (Liu et al., 2011). Fertil. From here, it enters the uterine tube and begins its trek down towards the uterus, with the help of cilia along the walls of the tube, of course. Menopause signals a shift in your life when you no longer get your period. Genet. the follicular phase. (2017). doi: 10.1530/rep-06-0025, Kageyama, S.-I., Liu, H., Nagata, M., and Aoki, F. (2006). Baroreceptors Function & Location | What are Baroreceptors? Changes in endoplasmic reticulum structure during mouse oocyte maturation are controlled by the cytoskeleton and cytoplasmic dynein. doi: 10.1016/j.fertnstert.2007.07.1373, Kovo, M., Kandli-Cohen, M., Ben-Haim, M., Galiani, D., Carr, D. W., and Dekel, N. (2006). Although, the deletion of HDAC2 by ZP3-Cre did result in reduced fertility, but the follicular development was normal. We do not endorse non-Cleveland Clinic products or services. BMC Dev. Youre born with about a million eggs. doi: 10.1038/nrd2133, Bootman, M. D., Berridge, M. J., and Roderick, H. L. (2002). 27, 19141924. MH and TZ collected the information and wrote the manuscript. Cell Biol. Sci. Reprod. Inhibition of proteasomal proteolysis affects expression of extracellular matrix components and steroidogenesis in porcine oocyte-cumulus complexes. 2014;1154:145-69. doi: 10.1007/978-1-4939-0659-8_7. Sustained activity of the EGF receptor is an absolute requisite for LH-induced oocyte maturation and cumulus expansion. doi: 10.1111/j.1432-1033.1973.tb02664.x, Brici, D., Zhang, Q., Reinhardt, S., Dahl, A., Hartmann, H., Schmidt, K., et al. Biol. From there cell division continues. In: StatPearls [Internet]. With the initiation of meiotic resumption, not only does the transcription in oocytes cease because of staining agglutination, but the maternal mRNAs stored in oocytes are degraded and gradually consumed. Histone sumoylation is a negative regulator in saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. For instance, LH inhibits Cx43 translation and breaks down GJs to prevent cAMP and cGMP diffusion into the oocyte, which results in PKA inactivation and triggers the initiation of oocyte maturation (Kalma et al., 2004; Edry et al., 2006; Sela-Abramovich et al., 2006). Natl. CBP-CITED4 is required for luteinizing hormone-triggered target gene expression during ovulation. doi: 10.1111/j.1432-1033.1985.tb08650.x, Huo, L. J., Fan, H. Y., Liang, C. G., Yu, L. Z., Zhong, Z. S., Chen, D. Y., et al. (2013). 25, 7382. 12, 271276. Enrolling in a course lets you earn progress by passing quizzes and exams. For instance, cytoplasmic polyadenylation of the 3-untranslated region (3-UTR) is closely related to mRNA stability and mRNA translational activation, which plays an important role in oocyte maturation (Yang et al., 2017). doi: 10.1093/humrep/der282, Khan, I., Kim, S. W., Lee, K. L., Song, S. H., Mesalam, A., Chowdhury, M. M. R., et al. Sci. Mol. doi: 10.1371/journal.pbio.1000453, Arroyo, A., Kim, B., and Yeh, J. The production of EGFs activates EGFR signaling and elevates the level of calcium in cumulus granulosa cells to further inactivate NPR2. Reprod. 226, 167179. Mol. In recent years, due to the rapid development and popularization of technologies like the genetic modification of animal models, molecular biology, and biochemistry, researchers have gained a better understanding of oocyte GV arrest and meiosis I resumption. Biochem. 8:597498. doi: 10.3389/fcell.2020.597498, Shilatifard, A. Cell Physiol. doi: 10.1095/biolreprod.109.081547, Sutton-McDowall, M. L., Mitchell, M., Cetica, P., Dalvit, G., Pantaleon, M., Lane, M., et al. Protein O-glycosylation plays a small role in oocyte maturation. Mol. Cell. cGMP production in CGCs relies on the coordination of MGCs-secreted NPPC conjugating with its receptor, guanylyl cyclase NPR2 which is found on the membrane of CGCs. (2017). 31, 137138. Struct. Specifically, inhibition of PDE3 elevates cAMP level and prevents oocyte spontaneous maturation simultaneously in cultured cumulus-oocyte-complexes (COCs) or denuded oocytes (DOs) (Kovanci et al., 2008). Histone modifications during mammalian oocyte maturation: dynamics, regulation and functions. Hum. 38, 12671277. Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. Gap junctions in the ovary: expression, localization and function. doi: 10.1007/s10815-018-1151-3, Leboeuf, M., Terrell, A., Trivedi, S., Sinha, S., Epstein, J. maintenance of corpus luteum) that progresses to either endometrial shedding or implantation. Follicular Phase of the Ovarian Cycle | Overview & Stages, The Pros & Cons of Day Care: Characteristics & Outcomes. In the female reproductive system, a large number of proteins, including FSH, LH, GDF9, BMP15, and AMH are glycosylated (Saito et al., 2008; Bousfield and Harvey, 2019). Translational regulation during oogenesis and early development: the cap-poly(A) tail relationship. doi: 10.1126/science.1214680, Su, Y.-Q., Sun, F., Handel, M. A., Schimenti, J. C., and Eppig, J. J. CNP/NPR2 signaling maintains oocyte meiotic arrest in early antral follicles and is suppressed by EGFR-mediated signaling in preovulatory follicles. doi: 10.1242/jcs.01328, Sasseville, M., Ct, N., Guillemette, C., and Richard, F. J. Biol. Development 144, 21652174. Trace the path of an oocyte from ovary to fertilization The female, or ovarian, reproductive system functions to produce gametes and reproductive hormones, just like the male reproductive system; however, it also has the additional task of supporting the developing fetus and delivering it to the outside world.
