Rab3A, Rab27A, and Rab35 regulate different events during mouse oocyte meiotic maturation and activation

Bustos MA, Lucchesi O, Ruete MC, Mayorga LS, Tomes CN (2012) Rab27 and Rab3 sequentially regulate human sperm dense-core granule exocytosis. Proc Natl Acad Sci USA 109(30):E2057–E2066 Chaigne A et al (2013) A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nat Cell Biol 15(8):958–966 Chen L et al (2014) TGN38 is required for the metaphase I/anaphase I transition and asymmetric cell division during mouse oocyte meiotic maturation. Cell Cycle 13(17):2723–2732 Chesneau L et al (2012) An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr Biol CB 22(2):147–153 Chevallier J et al (2009) Rab35 regulates neurite outgrowth and cell shape. FEBS Lett 583(7):1096–1101 Chua CEL, Lim YS, Tang BL (2010) Rab35-A vesicular traffic-regulating small GTPase with actin modulating roles. FEBS Lett 584(1):1–6 Clift D, Schuh M (2015) A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun 6:7217 Cran DG, Esper CR (1990) Cortical granules and the cortical reaction in mammals. J Reprod Fertil Suppl 42:177–188 Cuthbertson KS, Whittingham DG, Cobbold PH (1981) Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 294(5843):754–757 Desnos C et al (2003) Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 163(3):559–570 Estey MP, Di Ciano-Oliveira C, Froese CD, Bejide MT, Trimble WS (2010) Distinct roles of septins in cytokinesis: sEPT9 mediates midbody abscission. J Cell Biol 191(4):741–749 Fukuda M (2003) Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J Biol Chem 278(17):15373–15380 Gardner AJ, Evans JP (2006) Mammalian membrane block to polyspermy: new insights into how mammalian eggs prevent fertilisation by multiple sperm. Reprod Fertil Develop 18(1–2):53–61 Handley MTW, Haynes LP, Burgoyne RD (2007) Differential dynamics of Rab3A and Rab27A on secretory granules. J Cell Sci 120(6):973–984 Heytens E et al (2008) Effect of ionomycin on oocyte activation and embryo development in mouse. Reprod Biomed Online 17(6):764–771 Holubcova Z, Howard G, Schuh M (2013) Vesicles modulate an actin network for asymmetric spindle positioning. Nat Cell Biol 15(8):937–947 Jo YJ, Jang WI, Namgoong S, Kim NH (2015) Actin-capping proteins play essential roles in the asymmetric division of maturing mouse oocytes. J Cell Sci 128(1):160–170 Kim NH, Day BN, Lee HT, Chung KS (1996) Microfilament assembly and cortical granule distribution during maturation, parthenogenetic activation and fertilisation in the porcine oocyte. Zygote 4(2):145–149 Kimura K, Kimura A (2012) Rab6 is required for the exocytosis of cortical granules and the recruitment of separase to the granules during the oocyte-to-embryo transition in Caenorhabditis elegans. J Cell Sci 125(23):5897–5905 Kouranti I, Sachse M, Arouche N, Goud B, Echard A (2006) Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol CB 16(17):1719–1725 Li M et al (2009) Bub3 is a spindle assembly checkpoint protein regulating chromosome segregation during mouse oocyte meiosis. Plos One 4(11):e7701 Li S et al (2012) Septin 7 is required for orderly meiosis in mouse oocytes. Cell Cycle 11(17):3211–3218 Liu M (2011) The biology and dynamics of mammalian cortical granules. Reprod Biol Endocrinol RB&E 9:149 Liu XY et al (2005) Cortical granules behave differently in mouse oocytes matured under different conditions. Hum Reprod 20(12):3402–3413 Luo YB et al (2013) MBTD1 is associated with Pr-Set7 to stabilize H4K20me1 in mouse oocyte meiotic maturation. Cell Cycle 12(7):1142–1150 Ma RJ et al (2014) Rab5a is required for spindle length control and kinetochore-microtubule attachment during meiosis in oocytes. Faseb J 28(9):4026–4035 McGinnis LA, Lee HJ, Robinson DN, Evans JP (2015) MAPK3/1 (ERK1/2) and myosin light chain kinase in mammalian eggs affect myosin-II Function and regulate the metaphase II State in a calcium- and zinc-dependent manner. Biol Reprod 92(6):146 Metchat A et al (2015) An actin-dependent spindle position checkpoint ensures the asymmetric division in mouse oocytes. Nat Commun 6:7784 Miyara F et al (2003) Multiparameter analysis of human oocytes at metaphase II stage after IVF failure in non-male infertility. Hum Reprod 18(7):1494–1503 O’Neill GT, Rolfe LR, Kaufman MH (1991) Developmental potential and chromosome constitution of strontium-induced mouse parthenogenones. Mol Reprod Dev 30(3):214–219 Petersen CG et al (2011) Evaluation of zona pellucida birefringence intensity during in vitro maturation of oocytes from stimulated cycles. Reprod Biol Endocrinol RB&E 9:53 Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245(2):237–254 Rupnik M et al (2007) Distinct role of Rab3A and Rab3B in secretory activity of rat melanotrophs. Am J Physiol Cell Physiol 292(1):C98–C105 Sakisaka T, Meerlo T, Matteson J, Plutner H, Balch WE (2002) Rab-alpha GDI activity is regulated by a Hsp90 chaperone complex. EMBO J 21(22):6125–6135 Salminen A, Novick PJ (1987) A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49(4):527–538 Sato M, Grant BD, Harada A, Sato K (2008a) Rab11 is required for synchronous secretion of chondroitin proteoglycans after fertilization in Caenorhabditis elegans. J Cell Sci 121(19):3177–3186 Sato M et al (2008b) Regulation of endocytic recycling by C. elegans Rab35 and its regulator RME-4, a coated-pit protein. EMBO J 27(8):1183–1196 Schuh M, Ellenberg J (2007) Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130(3):484–498 Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2007) Rab GTPases at a glance. J Cell Sci 120(22):3905–3910 Shibata Y et al (2012) An oocyte-specific astacin family protease, alveolin, is released from cortical granules to trigger egg envelope hardening during fertilization in medaka (Oryzias latipes). Dev Biol 372(2):239–248 Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513–525 Sun QY (2003) Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs. Microsc Res Tech 61(4):342–348 Sun QY et al (2001) Dynamic events are differently mediated by microfilaments, microtubules, and mitogen-activated protein kinase during porcine oocyte maturation and fertilization in vitro. Biol Reprod 64(3):879–889 Sun SC et al (2011) Arp2/3 complex regulates asymmetric division and cytokinesis in mouse oocytes. PLoS One 6(4):e18392 Szollosi D (1967) Development of cortical granules and the cortical reaction in rat and hamster eggs. Anat Rec 159(4):431–446 Thery M et al (2005) The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7(10):947–953 Tsuboi T, Fukuda M (2006) Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J Cell Sci 119(Pt 11):2196–2203 Wang F et al (2014) WASH complex regulates Arp2/3 complex for actin-based polar body extrusion in mouse oocytes. Sci Rep 4:5596 Wessel GM, Conner SD, Berg L (2002) Cortical granule translocation is microfilament mediated and linked to meiotic maturation in the sea urchin oocyte. Development 129(18):4315–4325 Wilson SM et al (2000) A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc Natl Acad Sci USA 97(14):7933–7938 Woolner S, O’Brien LL, Wiese C, Bement WM (2008) Myosin-10 and actin filaments are essential for mitotic spindle function. J Cell Biol 182(1):77–88 Yi K et al (2013a) Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J Cell Biol 200(5):567–576 Yi K, Rubinstein B, Li R (2013b) Symmetry breaking and polarity establishment during mouse oocyte maturation. Philos Trans R Soc Lond B Biol Sci 368(1629):20130002 Zhang J, Fonovic M, Suyama K, Bogyo M, Scott MP (2009) Rab35 controls actin bundling by recruiting fascin as an effector protein. Science 325(5945):1250–1254