Wu Y , Li M , Yang M .

             embryo development
             chromosome condensation

FIGURE 1. Overview of the main ubiquitination mechanisms during oocyte maturation and preimplantation embryo development. Ubiquitination regulates protein stability during almost all stages of oocyte maturation and embryo development. Initially, ubiquitin proteins accumulate at GV stage (Huo et al., 2004b). While whether and how ubiquitination regulates GVBD stage is unclear by now. In MI stage, SCFFboxo30-mediated SLBP degradation regulates the chromosome condensation and segregation through ubiquitination. After MI stage, ubiquitin-conjugating enzymes UBE2C and UBE2S play roles in the escape from MII arrest (Fujioka et al., 2018). They regulate first polar body extrusion and spindle arrangement via APC/CCDC20 and APC/CCDH1 complex. While substrates that are ubiquitinated by UBE2C and UBE2S remain elusive. Zygote stage is the beginning of embryo development, while how ubiquitination plays roles in this stage is lack of studies in mammals. In 2-cell stage, APC/CCDC20 ubiquitinates securin and regulates sister chromatid separation. During the 4-cell to marula stage, Rnf20 controls the expression of H2B through ubiquitination and is involved in regulating preimplantation embryo development by controlling gene expression. From 8-cell to morula, ubiquitination of Suv39H1 via CRL4DCAF13 is important to the genome reprogramming. In morula stage, as a member of the ubiquitin C-terminal hydrolase (UCH) of deubiquitinating enzymes, UCHL1 regulates the morula compaction (Mtango et al., 2012).

Akimov, UbiSite approach for comprehensive mapping of lysine and N-terminal ubiquitination sites. 2018, Pubmed

Akimov, UbiSite approach for comprehensive mapping of lysine and N-terminal ubiquitination sites. 2018, Pubmed
Baarends, Silencing of unpaired chromatin and histone H2A ubiquitination in mammalian meiosis. 2005, Pubmed
Bai, Biology of Poly(ADP-Ribose) Polymerases: The Factotums of Cell Maintenance. 2015, Pubmed
Behrends, Constructing and decoding unconventional ubiquitin chains. 2011, Pubmed
Besterman, Regulation of mouse preimplantation development: inhibitory effect of genistein, an inhibitor of tyrosine protein phosphorylation, on cleavage of one-cell embryos. 1990, Pubmed
Bui, Involvement of histone H3 (Ser10) phosphorylation in chromosome condensation without Cdc2 kinase and mitogen-activated protein kinase activation in pig oocytes. 2004, Pubmed
Cardozo, The SCF ubiquitin ligase: insights into a molecular machine. 2004, Pubmed
Chandrasekharan, Histone H2B ubiquitination and beyond: Regulation of nucleosome stability, chromatin dynamics and the trans-histone H3 methylation. 2010, Pubmed
Chen, Genome-wide analysis of translation reveals a critical role for deleted in azoospermia-like (Dazl) at the oocyte-to-zygote transition. 2011, Pubmed , Xenbase
Chen, PARP-1 promotes autophagy via the AMPK/mTOR pathway in CNE-2 human nasopharyngeal carcinoma cells following ionizing radiation, while inhibition of autophagy contributes to the radiation sensitization of CNE-2 cells. 2015, Pubmed
Cohen, The regulation of protein function by multisite phosphorylation--a 25 year update. 2000, Pubmed
Cohen, The origins of protein phosphorylation. 2002, Pubmed
Cohen-Kaplan, The ubiquitin-proteasome system and autophagy: Coordinated and independent activities. 2016, Pubmed
D'Amours, Poly(ADP-ribosyl)ation reactions in the regulation of nuclear functions. 1999, Pubmed
Das, Releasing prophase arrest in zebrafish oocyte: synergism between maturational steroid and Igf1. 2016, Pubmed
Di Bacco, The SUMO-specific protease SENP5 is required for cell division. 2006, Pubmed
Dikic, Proteasomal and Autophagic Degradation Systems. 2017, Pubmed
Ding, Bisphenol AF negatively affects oocyte maturation of mouse in vitro through increasing oxidative stress and DNA damage. 2017, Pubmed
Eifler, SUMOylation-Mediated Regulation of Cell Cycle Progression and Cancer. 2015, Pubmed
Endoh, Histone H2A mono-ubiquitination is a crucial step to mediate PRC1-dependent repression of developmental genes to maintain ES cell identity. 2012, Pubmed
Eskeland, Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. 2010, Pubmed
Faerge, Resumption of meiosis induced by meiosis-activating sterol has a different signal transduction pathway than spontaneous resumption of meiosis in denuded mouse oocytes cultured in vitro. 2001, Pubmed
Fan, MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. 2009, Pubmed
Feitosa, Temporal and SUMO-specific SUMOylation contribute to the dynamics of Polo-like kinase 1 (PLK1) and spindle integrity during mouse oocyte meiosis. 2018, Pubmed
Flotho, Sumoylation: a regulatory protein modification in health and disease. 2013, Pubmed
Fodor, Mammalian Su(var) genes in chromatin control. 2010, Pubmed
Fuchs, RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. 2012, Pubmed
Fujioka, Contributions of UBE2C and UBE2S to meiotic progression of porcine oocytes. 2018, Pubmed
Galasinski, Global regulation of post-translational modifications on core histones. 2002, Pubmed
Garvin, The deSUMOylase SENP7 promotes chromatin relaxation for homologous recombination DNA repair. 2013, Pubmed
Gibson, New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. 2012, Pubmed
Goldknopf, Presence of protein A24 in rat liver nucleosomes. 1977, Pubmed
Gu, Distribution and expression of phosphorylated histone H3 during porcine oocyte maturation. 2008, Pubmed
Gutierrez, Tissue specificity of histone phosphorylation. 1967, Pubmed
Han, Deoxynivalenol exposure induces autophagy/apoptosis and epigenetic modification changes during porcine oocyte maturation. 2016, Pubmed
Hardwick, Cell cycle-dependent phosphorylation and regulation of cellular differentiation. 2018, Pubmed
Haren, Plk1-dependent recruitment of gamma-tubulin complexes to mitotic centrosomes involves multiple PCM components. 2009, Pubmed
Hayashi, Ubc9 is essential for viability of higher eukaryotic cells. 2002, Pubmed
Hendriks, A comprehensive compilation of SUMO proteomics. 2016, Pubmed
Hendzel, Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. 1997, Pubmed
Hickey, Function and regulation of SUMO proteases. 2012, Pubmed
Higuchi, Perturbation of maternal PIASy abundance disrupts zygotic genome activation and embryonic development via SUMOylation pathway. 2019, Pubmed
Hottiger, Nuclear ADP-Ribosylation and Its Role in Chromatin Plasticity, Cell Differentiation, and Epigenetics. 2015, Pubmed
Hou, Zearalenone exposure affects mouse oocyte meiotic maturation and granulosa cell proliferation. 2015, Pubmed
Hu, Plk1 negatively regulates PRC1 to prevent premature midzone formation before cytokinesis. 2012, Pubmed
Huang, Histone variant H3.3 and its functions in reprogramming. 2018, Pubmed
Huang, Maternal SENP7 programs meiosis architecture and embryo survival in mouse. 2017, Pubmed
Huo, Regulation of ubiquitin-proteasome pathway on pig oocyte meiotic maturation and fertilization. 2004, Pubmed
Huo, Ubiquitin-proteasome pathway modulates mouse oocyte meiotic maturation and fertilization via regulation of MAPK cascade and cyclin B1 degradation. 2004, Pubmed
Illingworth, The E3 ubiquitin ligase activity of RING1B is not essential for early mouse development. 2015, Pubmed
Imamura, Essential role for poly (ADP-ribosyl)ation in mouse preimplantation development. 2004, Pubmed
Jin, Fbxo30 regulates chromosome segregation of oocyte meiosis. 2019, Pubmed
Kang, Dynamics of histone H3 phosphorylation at threonine 3 during meiotic maturation in mouse oocytes. 2015, Pubmed
Kepkova, Transcriptomic analysis of in vivo and in vitro produced bovine embryos revealed a developmental change in cullin 1 expression during maternal-to-embryonic transition. 2011, Pubmed
King, A 20S complex containing CDC27 and CDC16 catalyzes the mitosis-specific conjugation of ubiquitin to cyclin B. 1995, Pubmed , Xenbase
Kraus, PARP goes transcription. 2003, Pubmed
Labas, Intact cell MALDI-TOF mass spectrometry on single bovine oocyte and follicular cells combined with top-down proteomics: A novel approach to characterise markers of oocyte maturation. 2018, Pubmed
Lan, Melatonin protects against defects induced by deoxynivalenol during mouse oocyte maturation. 2018, Pubmed
Lauberth, H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. 2013, Pubmed
Lee, Zygotic genome activation during the maternal-to-zygotic transition. 2014, Pubmed , Xenbase
Lee, The regulation of autophagy in porcine blastocysts: Regulation of PARylation-mediated autophagy via mammalian target of rapamycin complex 1 (mTORC1) signaling. 2016, Pubmed
Lee, Mutation of the polo-box disrupts localization and mitotic functions of the mammalian polo kinase Plk. 1998, Pubmed
Lee, Poly(ADP-ribosyl)ation is involved in pro-survival autophagy in porcine blastocysts. 2016, Pubmed
Li, Loss of Cdc20 causes a securin-dependent metaphase arrest in two-cell mouse embryos. 2007, Pubmed
Li, The ubiquitin ligase KBTBD8 regulates PKM1 levels via Erk1/2 and Aurora A to ensure oocyte quality. 2019, Pubmed
Lu, Cohesin acetyltransferase Esco2 regulates SAC and kinetochore functions via maintaining H4K16 acetylation during mouse oocyte meiosis. 2017, Pubmed
Lu, Phosphorylation of mitogen-activated protein kinase is regulated by protein kinase C, cyclic 3',5'-adenosine monophosphate, and protein phosphatase modulators during meiosis resumption in rat oocytes. 2001, Pubmed
Maison, SUMOylation promotes de novo targeting of HP1α to pericentric heterochromatin. 2011, Pubmed
Martello, Proteome-wide identification of the endogenous ADP-ribosylome of mammalian cells and tissue. 2016, Pubmed
Masutani, Poly(ADP-ribose) polymerase gene disruption conferred mice resistant to streptozotocin-induced diabetes. 1999, Pubmed
Mattson, Oogenesis: chromatin and microtubule dynamics during meiotic prophase. 1990, Pubmed
Ménissier de Murcia, Functional interaction between PARP-1 and PARP-2 in chromosome stability and embryonic development in mouse. 2003, Pubmed
Min, Protein Lysine Acetylation in Ovarian Granulosa Cells Affects Metabolic Homeostasis and Clinical Presentations of Women With Polycystic Ovary Syndrome. 2020, Pubmed
Motlik, Breakdown of the germinal vesicle in pig oocytes in vivo and in vitro. 1976, Pubmed
Mtango, Essential role of maternal UCHL1 and UCHL3 in fertilization and preimplantation embryo development. 2012, Pubmed
Nacerddine, The SUMO pathway is essential for nuclear integrity and chromosome segregation in mice. 2005, Pubmed
Nakamizo, Phosphorylation of Thr18 and Ser20 of p53 in Ad-p53-induced apoptosis. 2008, Pubmed
Narayanan, Computational studies of protein regulation by post-translational phosphorylation. 2009, Pubmed
Nishi, DYRK2 and GSK-3 phosphorylate and promote the timely degradation of OMA-1, a key regulator of the oocyte-to-embryo transition in C. elegans. 2005, Pubmed
Nowak, Phosphorylation of histone H3: a balancing act between chromosome condensation and transcriptional activation. 2004, Pubmed
Olsen, Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. 2010, Pubmed
Ooga, Involvement of histone H2B monoubiquitination in the regulation of mouse preimplantation development. 2015, Pubmed
Osada, PolyADP-ribosylation is required for pronuclear fusion during postfertilization in mice. 2010, Pubmed
Osman, Oocyte and Embryo Manipulation and Epigenetics. 2018, Pubmed
Pahlavan, Characterization of polo-like kinase 1 during meiotic maturation of the mouse oocyte. 2000, Pubmed
Patisaul, Long-term effects of environmental endocrine disruptors on reproductive physiology and behavior. 2009, Pubmed
Petronczki, Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. 2007, Pubmed
Prather, Transcriptional, post-transcriptional and epigenetic control of porcine oocyte maturation and embryogenesis. 2009, Pubmed
Prochazka, Mechanisms of FSH- and Amphiregulin-Induced MAP Kinase 3/1 Activation in Pig Cumulus-Oocyte Complexes During Maturation In Vitro. 2019, Pubmed
Qiao, The root of reduced fertility in aged women and possible therapentic options: current status and future perspects. 2014, Pubmed
Robajac, Preeclampsia transforms membrane N-glycome in human placenta. 2016, Pubmed
Romeo, The SENP7 SUMO-Protease Presents a Module of Two HP1 Interaction Motifs that Locks HP1 Protein at Pericentric Heterochromatin. 2015, Pubmed
Rosonina, Regulation of transcription factors by sumoylation. 2017, Pubmed
Ruan, PLK1 interacts and phosphorylates Axin that is essential for proper centrosome formation. 2012, Pubmed
Ruthenburg, Methylation of lysine 4 on histone H3: intricacy of writing and reading a single epigenetic mark. 2007, Pubmed
Samson, The specification and global reprogramming of histone epigenetic marks during gamete formation and early embryo development in C. elegans. 2014, Pubmed
Sang, A pannexin 1 channelopathy causes human oocyte death. 2019, Pubmed
Sassone-Corsi, Requirement of Rsk-2 for epidermal growth factor-activated phosphorylation of histone H3. 1999, Pubmed
Schwertman, Regulation of DNA double-strand break repair by ubiquitin and ubiquitin-like modifiers. 2016, Pubmed
Song, Induction of autophagy during in vitro maturation improves the nuclear and cytoplasmic maturation of porcine oocytes. 2014, Pubmed
Song, Induction of autophagy promotes preattachment development of bovine embryos by reducing endoplasmic reticulum stress. 2012, Pubmed
Su, Mitogen-activated protein kinase activity in cumulus cells is essential for gonadotropin-induced oocyte meiotic resumption and cumulus expansion in the mouse. 2002, Pubmed
Sun, Regulation of mitogen-activated protein kinase phosphorylation, microtubule organization, chromatin behavior, and cell cycle progression by protein phosphatases during pig oocyte maturation and fertilization in vitro. 2002, Pubmed
Swain, Proper chromatin condensation and maintenance of histone H3 phosphorylation during mouse oocyte meiosis requires protein phosphatase activity. 2007, Pubmed
Swatek, Ubiquitin modifications. 2016, Pubmed
Tan, Phosphorylation of p90rsk during meiotic maturation and parthenogenetic activation of rat oocytes: correlation with MAP kinases. 2001, Pubmed
Tetzlaff, Defective cardiovascular development and elevated cyclin E and Notch proteins in mice lacking the Fbw7 F-box protein. 2004, Pubmed
Tong, Polo-like kinase-1 is a pivotal regulator of microtubule assembly during mouse oocyte meiotic maturation, fertilization, and early embryonic mitosis. 2002, Pubmed
Trounson, Oocyte maturation. 1998, Pubmed
Van Hooser, Histone H3 phosphorylation is required for the initiation, but not maintenance, of mammalian chromosome condensation. 1998, Pubmed
Verlhac, Mos activates MAP kinase in mouse oocytes through two opposite pathways. 2000, Pubmed
Vermeulen, Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. 2007, Pubmed
Villeneuve, Ecotoxicogenomics to support ecological risk assessment: a case study with bisphenol A in fish. 2012, Pubmed
Vlastaridis, Estimating the total number of phosphoproteins and phosphorylation sites in eukaryotic proteomes. 2017, Pubmed
Wang, Rab23/Kif17 regulate meiotic progression in oocytes by modulating tubulin acetylation and actin dynamics. 2019, Pubmed
Wang, The SUMO pathway functions in mouse oocyte maturation. 2010, Pubmed
Wang, Histone phosphorylation and pericentromeric histone modifications in oocyte meiosis. 2006, Pubmed
Wang, HDAC3 maintains oocyte meiosis arrest by repressing amphiregulin expression before the LH surge. 2019, Pubmed
Webster, Mechanisms of Aneuploidy in Human Eggs. 2017, Pubmed
Wei, Phosphorylation of histone H3 at serine 10 is correlated with chromosome condensation during mitosis and meiosis in Tetrahymena. 1998, Pubmed
Wei, Functions of PARylation in DNA Damage Repair Pathways. 2016, Pubmed
Wei, Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. 1999, Pubmed
Xie, Poly(ADP-ribose) mediates asymmetric division of mouse oocyte. 2018, Pubmed
Xu, Effects of E2 binding enzyme UBC9 on porcine oocyte maturation, apoptosis and embryo development. 2020, Pubmed
Xuan, Inhibition of PSMD4 alters ZP1 ubiquitination state and sperm-oocyte-binding ability in pigs. 2018, Pubmed
Xue, Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. 2013, Pubmed
Yan, Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. 2013, Pubmed
Yang, Inhibition of neddylation causes meiotic arrest in mouse oocyte. 2019, Pubmed
Yartseva, The Maternal-to-Zygotic Transition During Vertebrate Development: A Model for Reprogramming. 2015, Pubmed
Yokoi, Non-radioisotopic quantitative RT-PCR to detect changes in mRNA levels during early mouse embryo development. 1993, Pubmed
Zhang, Inhibition of protein kinase D disrupts spindle formation and actin assembly during porcine oocyte maturation. 2018, Pubmed
Zhang, DCAF13 promotes pluripotency by negatively regulating SUV39H1 stability during early embryonic development. 2018, Pubmed
Zhang, RAB35 depletion affects spindle formation and actin-based spindle migration in mouse oocyte meiosis. 2019, Pubmed
Zheng, Structure of the Cul1-Rbx1-Skp1-F boxSkp2 SCF ubiquitin ligase complex. 2002, Pubmed
Zhou, AMPK mediates a pro-survival autophagy downstream of PARP-1 activation in response to DNA alkylating agents. 2013, Pubmed
Zhu, Toxic effects of HT-2 toxin on mouse oocytes and its possible mechanisms. 2016, Pubmed
Zhu, Effect of mycotoxin-containing diets on epigenetic modifications of mouse oocytes by fluorescence microscopy analysis. 2014, Pubmed
Zhu, MISP is a novel Plk1 substrate required for proper spindle orientation and mitotic progression. 2013, Pubmed