Log in

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

  • Original Paper
  • Published:
Histochemistry and Cell Biology Aims and scope Submit manuscript

Abstract

Rab family members play important roles in membrane trafficking, cell growth, and differentiation. Almost all components of the cell endomembrane system, the nucleus, and the plasma membrane are closely related to RAB proteins. In this study, we investigated the distribution and functions of three members of the Rab family, Rab3A, Rab27A, and Rab35, in mouse oocyte meiotic maturation and activation. The three Rab family members showed different localization patterns in oocytes. Microinjection of siRNA, antibody injection, or inhibitor treatment showed that (1) Rab3A regulates peripheral spindle and cortical granule (CG) migration, polarity establishment, and asymmetric division; (2) Rab27A regulates CG exocytosis following MII-stage oocyte activation; and (3) Rab35 plays an important role in spindle organization and morphology maintenance, and thus meiotic nuclear maturation. These results show that Rab proteins play important roles in mouse oocyte meiotic maturation and activation and that different members exert different distinct functions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chaigne A et al (2013) A soft cortex is essential for asymmetric spindle positioning in mouse oocytes. Nat Cell Biol 15(8):958–966

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chesneau L et al (2012) An ARF6/Rab35 GTPase cascade for endocytic recycling and successful cytokinesis. Curr Biol CB 22(2):147–153

    Article  CAS  PubMed  Google Scholar 

  • Chevallier J et al (2009) Rab35 regulates neurite outgrowth and cell shape. FEBS Lett 583(7):1096–1101

    Article  CAS  PubMed  Google Scholar 

  • Chua CEL, Lim YS, Tang BL (2010) Rab35-A vesicular traffic-regulating small GTPase with actin modulating roles. FEBS Lett 584(1):1–6

    Article  CAS  PubMed  Google Scholar 

  • Clift D, Schuh M (2015) A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat Commun 6:7217

    Article  PubMed  PubMed Central  Google Scholar 

  • Cran DG, Esper CR (1990) Cortical granules and the cortical reaction in mammals. J Reprod Fertil Suppl 42:177–188

    CAS  PubMed  Google Scholar 

  • Cuthbertson KS, Whittingham DG, Cobbold PH (1981) Free Ca2+ increases in exponential phases during mouse oocyte activation. Nature 294(5843):754–757

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Handley MTW, Haynes LP, Burgoyne RD (2007) Differential dynamics of Rab3A and Rab27A on secretory granules. J Cell Sci 120(6):973–984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heytens E et al (2008) Effect of ionomycin on oocyte activation and embryo development in mouse. Reprod Biomed Online 17(6):764–771

    Article  CAS  PubMed  Google Scholar 

  • Holubcova Z, Howard G, Schuh M (2013) Vesicles modulate an actin network for asymmetric spindle positioning. Nat Cell Biol 15(8):937–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jo YJ, Jang WI, Namgoong S, Kim NH (2015) Actin-cap** proteins play essential roles in the asymmetric division of maturing mouse oocytes. J Cell Sci 128(1):160–170

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M (2011) The biology and dynamics of mammalian cortical granules. Reprod Biol Endocrinol RB&E 9:149

    Article  CAS  Google Scholar 

  • Liu XY et al (2005) Cortical granules behave differently in mouse oocytes matured under different conditions. Hum Reprod 20(12):3402–3413

    Article  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Metchat A et al (2015) An actin-dependent spindle position checkpoint ensures the asymmetric division in mouse oocytes. Nat Commun 6:7784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Runft LL, Jaffe LA, Mehlmann LM (2002) Egg activation at fertilization: where it all begins. Dev Biol 245(2):237–254

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Salminen A, Novick PJ (1987) A ras-like protein is required for a post-Golgi event in yeast secretion. Cell 49(4):527–538

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2007) Rab GTPases at a glance. J Cell Sci 120(22):3905–3910

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10(8):513–525

    Article  CAS  PubMed  Google Scholar 

  • Sun QY (2003) Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs. Microsc Res Tech 61(4):342–348

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Sun SC et al (2011) Arp2/3 complex regulates asymmetric division and cytokinesis in mouse oocytes. PLoS One 6(4):e18392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szollosi D (1967) Development of cortical granules and the cortical reaction in rat and hamster eggs. Anat Rec 159(4):431–446

    Article  CAS  PubMed  Google Scholar 

  • Thery M et al (2005) The extracellular matrix guides the orientation of the cell division axis. Nat Cell Biol 7(10):947–953

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Wang F et al (2014) WASH complex regulates Arp2/3 complex for actin-based polar body extrusion in mouse oocytes. Sci Rep 4:5596

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We appreciate Yi Hou, Shi-Wen Li, and Li-Juan Wang’s help for their technical assistance. We also thank the other members in Dr. Sun’s laboratory for their kind discussions of these experiments. This study was supported by the National Basic Research Program of China (No. 2012CB944404).

Authors’ contribution

QYS and HHW helped with conception and design. QC, TZ, ZBW, YCOY, WS, JYM, and HS contributed to acquisition of data. QYS and HHW contributed to analysis and interpretation of data, and drafting the article. All authors approved the final version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Q. Y. Sun.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, H.H., Cui, Q., Zhang, T. et al. Rab3A, Rab27A, and Rab35 regulate different events during mouse oocyte meiotic maturation and activation. Histochem Cell Biol 145, 647–657 (2016). https://doi.org/10.1007/s00418-015-1404-5

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00418-015-1404-5

Keywords

Navigation