Mitogen-activated protein kinase (MAPK) is a family of Ser/Thr protein kinases that are widely distributed in eukaryotic cells. Studies in the last decade revealed that MAPK cascade plays pivotal roles in regulating the meiotic cell cycle progression of oocytes. In mammalian species, activation of MAPK in cumulus cells is necessary for gonadotropin-induced meiotic resumption of oocytes, while MAPK activation is not required for spontaneous meiotic resumption. After germinal vesicle breakdown (GVBD), MAPK is involved in the regulation of microtubule organization and meiotic spindle assembly. The activation of this kinase is essential for the maintenance of metaphase II arrest, while its inactivation is a prerequisite for pronuclear formation after fertilization or parthenogenetic activation. MAPK cascade interacts extensively with other protein kinases such as maturation-promoting factor, protein kinase A, protein kinase C, and calmodulin-dependent protein kinase II, as well as with protein phosphatases in oocyte meiotic cell cycle regulation. The cross talk between MAPK cascade and other protein kinases is discussed. The review also addresses unsolved problems and discusses future directions.

https://bioone.org/journals/biology-of-reproduction/volume-70/issue-3/biolreprod.103.022830/Involvement-of-Mitogen-Activated-Protein-Kinase-Cascade-During-Oocyte-Maturation/10.1095/biolreprod.103.022830.pdf

Involvement of Mitogen-Activated Protein Kinase Cascade During Oocyte Maturation and Fertilization in Mammals

Oocyte meiotic maturation is one of the important physiological requirements for species survival. However, little is known about the detailed events occurring during this process. A number of studies have demonstrated that MAPK plays a pivotal role in the regulation of meiotic cell cycle progression in oocytes, but controversial findings have been reported in both lower vertebrates and mammals. In this review, we summarized the roles of MAPK cascade and related signal pathways in oocyte meiotic reinitiation in both lower vertebrates and mammals. We also tried to reconcile the paradoxical results and highlight the new findings concerning the function of MAPK in both oocytes and the surrounding follicular somatic cells. The unresolved questions and future research directions regarding the role of MAPK in meiotic resumption are addressed.

/pdf/mechanisms-regulating-oocyte-meiotic-resumption-roles-of-3j72pvrzqt.pdf

Mechanisms regulating oocyte meiotic resumption: roles of mitogen-activated protein kinase.

The role of androgen and androgen receptors (ARs) in males has been well established. This steroid and its receptor also exist in follicles, but their functions are still unclear. In this study, using a culture system containing a low dose of hypoxanthine, we revealed the positive contribution of testosterone to oocyte meiotic resumption. By performing ultracentrifugation to allow clear visualization of porcine germinal vesicles, our results provide evidence that mitogen-activated protein kinase (MAPK) in the oocyte itself but not in cumulus cells was activated before germinal vesicle breakdown (GVBD) after testosterone treatment. We further explored the signal cascade of testosterone-triggered GVBD and showed significant contributions of AR to testosterone-induced MAPK activation and GVBD. By using a potent and selective inhibitor of SRC and detecting activation of the kinase, we found that testosterone activated SRC in oocytes but not in cumulus cells and that SRC (as an essential upstream molecule of MAPK) mediated this testosterone- and AR-promoted reinitiation of meiosis. The present findings propose an undefined signaling pathway and suggest the potential competence of testosterone for meiotic resumption in mammalian oocytes.

Testosterone Potentially Triggers Meiotic Resumption by Activation of Intra-Oocyte SRC and MAPK in Porcine Oocytes

The oocyte quality remains as one of the major problems associated with poor in vitro fertilization (IVF) rate and assisted reproductive technology (ART) failure worldwide The oocyte quality is dependent on its meiotic maturation that begins inside the follicular microenvironment and gets completed at the time of ovulation in most of the mammalian species Follicular oocytes are arrested at diplotene stage of first meiotic prophase The resumption of meiosis from diplotene arrest, progression through metaphase-I (M-I) and further arrest at metaphase-II (M-II) are important physiological requirements for the achievement of meiotic competency in mammalian oocytes The achievement of meiotic competency is dependent upon cyclic stabilization/destabilization of maturation promoting factor (MPF) The mitogen-activated protein kinase3/1 (MAPK3/1) modulates stabilization/destabilization of MPF in oocyte by interacting either with signal molecules, transcription and post-transcription factors in cumulus cells or cytostatic factors (CSFs) in oocyte MPF regulates meiotic cell cycle progression from diplotene arrest to M-II arrest and directly impacts oocyte quality The MAPK3/1 activity is not reported during spontaneous meiotic resumption but its activity in cumulus cells is required for gonadotropin-induced oocyte meiotic resumption Although high MAPK3/1 activity is required for the maintenance of M-II arrest in several mammalian species, its cross-talk with MPF remains to be elucidated Further studies are required to find out the MAPK3/1 activity and its impact on MPF destabilization/stabilization during achievement of meiotic competency, an important period that decides oocyte quality and directly impacts ARTs outcome in several mammalian species including human J Cell Biochem 119: 123-129, 2018 © 2017 Wiley Periodicals, Inc

Role of Mitogen Activated Protein Kinase and Maturation Promoting Factor During the Achievement of Meiotic Competency in Mammalian Oocytes.

Cumulus cells (CCs) are of great importance in oocyte development and maturation in many species, but detailed influence of CCs has not been extensively examined, especially on rabbit. The present study was designed to investigate the effects of CCs and the elongation of in vitro maturation (IVM) time on rabbit oocyte nuclear and ooplasmic maturation and survival. Cumulus oocyte complexes (COCs) and naked oocytes (NOs) were recovered directly from rabbits super-ovulated with eCG. Corona-enclosed oocytes (COs) and denuded oocytes (DOs) were obtained from COCs after removing a part or whole of CCs. The oocytes were cultured in the following seven groups. (i) Cumulus cell enclosed oocytes (CEOs) were cultured alone (CEOs); (ii) COs were cultured alone (COs); (iii) DOs were cultured alone (DOs); (iv) NOs were cultured alone; (v) DOs were co-cultured with COCs [DOs(COCs)]; (vi) DOs were co-cultured with CCs [DOs(CCs)]; (vii) NOs were co-cultured with CCs [NOs(CCs)]. After the oocytes were cultured for 24 and 30 h, the nuclear maturation was evaluated by first polar body (PB1) extrusion while the ooplasmic maturation was evaluated by the cleavage rate after parthenogenetic activation. The results showed that the nuclear maturation rate of CEOs, COs, DOs(COCs) and DOs(CCs) after 24 h incubation were significantly different from each other (p or = 0.05). The cleavage rates in the first two groups were significantly higher than those of the others (p 0.05). The results suggest that rabbit CCs affect oocyte nuclear and ooplasmic maturation, and their survival. The prolongation of the culture time of rabbit oocyte from 24 to 30 h improves the nuclear and ooplasmic maturation differently in the present system. Rabbit oocytes free of CCs, especially NOs, show weak meiotic resumption potential and compromised viability, which cannot be improved by co-culture with dispersed CCs. The degeneration mostly happens at early time of IVM.

Effects of cumulus cells on rabbit oocyte in vitro maturation

Numerous studies have demonstrated that activation of the mitogen-activated protein (MAP) kinase is involved in the maturation of oocytes. In this study, the expression and phosphorylation of MAP kinase and p90rsk, one of the substrates of MAP kinase, during rabbit oocyte maturation were studied. The results showed that MAP kinase phosphorylation began to occur after germinal vesicle breakdown (GVBD) and the active form was maintained until metaphase II. p90rsk was also activated after GVBD following MAP kinase activation. Immunofluorescent analysis showed that p90rsk was enriched in the nuclear area after GVBD and was gradually localised to the spindle. When GVBD was inhibited by increased cAMP or decreased protein kinase C activity, the phosphorylation of both MAP kinase and p90rsk was blocked. Our data suggest that (1) MAP kinase/p90rsk activation is not necessary for GVBD, but plays an important role in the post-GVBD events including spindle assembly in rabbit oocytes; and (2) MAP kinase/p90rsk activation is down-regulated by cAMP and up-regulated by protein kinase C in cumulus-enclosed rabbit oocytes.

Phosphorylation of MAP kinase and p90rsk and its regulation during in vitro maturation of cumulus-enclosed rabbit oocytes.

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Phosphorylation of MAP kinase and p90rsk and its regulation during in vitro maturation of cumulus-enclosed rabbit oocytes.