Hostname: page-component-7479d7b7d-68ccn Total loading time: 0 Render date: 2024-07-12T03:02:13.913Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular Mechanisms of Asymmetric Division in Oocytes

Published online by Cambridge University Press:  14 June 2013

Shao-Chen Sun  and
Nam-Hyung Kim
Shao-Chen Sun*
Affiliation:
College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China
Nam-Hyung Kim*
Affiliation:
Department of Animal Sciences, Chungbuk National University, Cheongju 361-763, Korea
*
*Corresponding author. E-mail: sunsc@njau.edu.cn
**Corresponding author. E-mail: nhkim@chungbuk.ac.kr
Get access

Abstract

In contrast to symmetric division in mitosis, mammalian oocyte maturation is characterized by asymmetric cell division that produces a large egg and a small polar body. The asymmetry results from oocyte polarization, which includes spindle positioning, migration, and cortical reorganization, and this process is critical for fertilization and the retention of maternal components for early embryo development. Although actin dynamics are involved in this process, the molecular mechanism underlying this remained unclear until the use of confocal microscopy and live cell imaging became widespread in recent years. Information obtained through a PubMed database search of all articles published in English between 2000 and 2012 that included the phrases “oocyte, actin, spindle migration,” “oocyte, actin, polar body,” or “oocyte, actin, asymmetric division” was reviewed. The actin nucleation factor actin-related protein 2/3 complex and its nucleation-promoting factors, formins and Spire, and regulators such as small GTPases, partitioning-defective/protein kinase C, Fyn, microRNAs, cis-Golgi apparatus components, myosin/myosin light-chain kinase, spindle stability regulators, and spindle assembly checkpoint regulators, play critical roles in asymmetric cell division in oocytes. This review summarizes recent findings on these actin-related regulators in mammalian oocyte asymmetric division and outlines a complete signaling pathway.

Keywords

oocytespindle migrationasymmetric divisionpolar body extrusionactin nucleationsmall GTPase
Type
Review Article
Information
Microscopy and Microanalysis , Volume 19 , Issue 4 , August 2013 , pp. 883 - 897
Copyright
Copyright © Microscopy Society of America 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aslan, J.E., Tormoen, G.W., Loren, C.P., Pang, J. & McCarty, O.J. (2011). S6K1 and mTOR regulate Rac1-driven platelet activation and aggregation. Blood 118(11), 3129–3136.Google Scholar
Azoury, J., Lee, K.W., Georget, V., Hikal, P. & Verlhac, M.H. (2011). Symmetry breaking in mouse oocytes requires transient F-actin meshwork destabilization. Development 138(14), 2903–2908.CrossRefGoogle ScholarPubMed
Azoury, J., Lee, K.W., Georget, V., Rassinier, P., Leader, B. & Verlhac, M.H. (2008). Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 18(19), 1514–1519.Google Scholar
Bernhardt, M.L., Kim, A.M., O'Halloran, T.V. & Woodruff, T.K. (2011). Zinc requirement during meiosis I-meiosis II transition in mouse oocytes is independent of the MOS-MAPK pathway. Biol Reprod 84(3), 526–536.CrossRefGoogle ScholarPubMed
Bielak-Zmijewska, A., Kolano, A., Szczepanska, K., Maleszewski, M. & Borsuk, E. (2008). Cdc42 protein acts upstream of IQGAP1 and regulates cytokinesis in mouse oocytes and embryos. Dev Biol 322(1), 21–32.Google Scholar
Bosch, M., Le, K.H., Bugyi, B., Correia, J.J., Renault, L. & Carlier, M.F. (2007). Analysis of the function of Spire in actin assembly and its synergy with formin and profilin. Mol Cell 28(4), 555–568.Google Scholar
Brockmann, C., Huarte, J., Dugina, V., Challet, L., Rey, E., Conne, B., Swetloff, A., Nef, S., Chaponnier, C. & Vassalli, J.D. (2011). Beta- and gamma-cytoplasmic actins are required for meiosis in mouse oocytes. Biol Reprod 85(5), 1025–1039.Google Scholar
Brunet, S., Maria, A.S., Guillaud, P., Dujardin, D., Kubiak, J.Z. & Maro, B. (1999). Kinetochore fibers are not involved in the formation of the first meiotic spindle in mouse oocytes, but control the exit from the first meiotic M phase. J Cell Biol 146(1), 1–12.Google Scholar
Brunet, S. & Verlhac, M.H. (2011). Positioning to get out of meiosis: The asymmetry of division. Hum Reprod Update 17(1), 68–75.CrossRefGoogle ScholarPubMed
Bugyi, B. & Carlier, M.F. (2010). Control of actin filament treadmilling in cell motility. Annu Rev Biophys 39, 449–470.Google Scholar
Campellone, K.G., Webb, N.J., Znameroski, E.A. & Welch, M.D. (2008). WHAMM is an Arp2/3 complex activator that binds microtubules and functions in ER to Golgi transport. Cell 134(1), 148–161.CrossRefGoogle ScholarPubMed
Campellone, K.G. & Welch, M.D. (2010). A nucleator arms race: Cellular control of actin assembly. Nat Rev Mol Cell Biol 11(4), 237–251.Google Scholar
Cao, Y.K., Zhong, Z.S., Chen, D.Y., Zhang, G.X., Schatten, H. & Sun, Q.Y. (2005). Cell cycle-dependent localization and possible roles of the small GTPase Ran in mouse oocyte maturation, fertilization and early cleavage. Reproduction 130(4), 431–440.Google Scholar
Chang, Y.F., Lee-Chang, J.S., Imam, J.S., Buddavarapu, K.C., Subaran, S.S., Sinha-Hikim, A.P., Gorospe, M. & Rao, M.K. (2012). Interaction between microRNAs and actin-associated protein Arpc5 regulates translational suppression during male germ cell differentiation. Proc Natl Acad Sci USA 109(15), 5750–5755.CrossRefGoogle ScholarPubMed
Chen, D., Zhang, Y., Yi, Q., Huang, Y., Hou, H., Zhang, Y., Hao, Q., Cooke, H.J., Li, L., Sun, Q. & Shi, Q. (2012a). Regulation of asymmetrical cytokinesis by cAMP during meiosis I in mouse oocytes. PLoS One 7(1), e29735. Google Scholar
Chen, L., Hu, X., Dai, Y., Li, Q., Wang, X., Li, Q., Xue, K., Li, Y., Liang, J., Wang, Y., Li, X. & Li, N. (2012b). MicroRNA-27a activity is not suppressed in porcine oocytes. Front Biosci (Elite Ed) 4, 2679–2685.Google Scholar
Choi, T., Fukasawa, K., Zhou, R., Tessarollo, L., Borror, K., Resau, J. & Vande Woude, G.F. (1996). The Mos/mitogen-activated protein kinase (MAPK) pathway regulates the size and degradation of the first polar body in maturing mouse oocytes. Proc Natl Acad Sci USA 93(14), 7032–7035.Google Scholar
Cui, X.S., Sun, S.C., Kang, Y.K. & Kim, N.H. (2013). Involvement of microRNA-335-5p in cytoskeleton dynamics in mouse oocytes. Reprod Fertil Dev 25(4), 691–699.Google Scholar
Dahlgaard, K., Raposo, A.A., Niccoli, T. & St Johnston, D. (2007). Capu and Spire assemble a cytoplasmic actin mesh that maintains microtubule organization in the Drosophila oocyte. Dev Cell 13(4), 539–553.Google Scholar
Dehapiot, B., Carriere, V., Carroll, J. & Halet, G. (2013). Polarized Cdc42 activation promotes polar body protrusion and asymmetric division in mouse oocytes. Dev Biol 377(1), 202–212.Google Scholar
De Matteis, M.A. & Luini, A. (2008). Exiting the Golgi complex. Nat Rev Mol Cell Biol 9(4), 273–284.CrossRefGoogle ScholarPubMed
Deng, M., Kishikawa, H., Yanagimachi, R., Kopf, G.S., Schultz, R.M. & Williams, C.J. (2003). Chromatin-mediated cortical granule redistribution is responsible for the formation of the cortical granule-free domain in mouse eggs. Dev Biol 257(1), 166–176.Google Scholar
Deng, M., Suraneni, P., Schultz, R.M. & Li, R. (2007). The Ran GTPase mediates chromatin signaling to control cortical polarity during polar body extrusion in mouse oocytes. Dev Cell 12(2), 301–308.Google Scholar
Deng, M., Williams, C.J. & Schultz, R.M. (2005). Role of MAP kinase and myosin light chain kinase in chromosome-induced development of mouse egg polarity. Dev Biol 278(2), 358–366.Google Scholar
Dumont, J., Million, K., Sunderland, K., Rassinier, P., Lim, H., Leader, B. & Verlhac, M.H. (2007a). Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev Biol 301(1), 254–265.Google Scholar
Dumont, J., Petri, S., Pellegrin, F., Terret, M.E., Bohnsack, M.T., Rassinier, P., Georget, V., Kalab, P., Gruss, O.J. & Verlhac, M.H. (2007b). A centriole- and RanGTP-independent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol 176(3), 295–305.CrossRefGoogle ScholarPubMed
Duncan, F.E., Moss, S.B., Schultz, R.M. & Williams, C.J. (2005). PAR-3 defines a central subdomain of the cortical actin cap in mouse eggs. Dev Biol 280(1), 38–47.Google Scholar
Elbaz, J., Reizel, Y., Nevo, N., Galiani, D. & Dekel, N. (2010). Epithelial cell transforming protein 2 (ECT2) depletion blocks polar body extrusion and generates mouse oocytes containing two metaphase II spindles. Endocrinology 151(2), 755–765.CrossRefGoogle ScholarPubMed
Garcia-Lopez, J. & Del Mazo, J. (2012). Expression dynamics of microRNA biogenesis during preimplantation mouse development. Biochim Biophys Acta 1819(8), 847–854.Google Scholar
Georgiou, M., Marinari, E., Burden, J. & Baum, B. (2008). Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr Biol 18(21), 1631–1638.Google Scholar
Halet, G. & Carroll, J. (2007). Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 12(2), 309–317.Google Scholar
Higgs, H.N. & Pollard, T.D. (2001). Regulation of actin filament network formation through Arp2/3 complex: Activation by a diverse array of proteins. Annu Rev Biochem 70, 649–676.CrossRefGoogle ScholarPubMed
Homer, H.A., McDougall, A., Levasseur, M. & Herbert, M. (2005). Restaging the spindle assembly checkpoint in female mammalian meiosis I. Cell Cycle 4(5), 650–653.CrossRefGoogle ScholarPubMed
Huang, X., Ding, L., Pan, R., Ma, P.F., Cheng, P.P., Zhang, C.H., Shen, Y.T., Xu, L., Liu, Y., He, X.Q., Qi, Z.Q. & Wang, H.L. (2013). WHAMM is required for meiotic spindle migration and asymmetric cytokinesis in mouse oocytes. Histochem Cell Biol 139(4), 525–534.Google Scholar
Iden, S. & Collard, J.G. (2008). Crosstalk between small GTPases and polarity proteins in cell polarization. Nat Rev Mol Cell Biol 9(11), 846–859.Google Scholar
Jacinto, E., Loewith, R., Schmidt, A., Lin, S., Ruegg, M.A., Hall, A. & Hall, M.N. (2004). Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nat Cell Biol 6(11), 1122–1128.Google Scholar
Joukov, V., Groen, A.C., Prokhorova, T., Gerson, R., White, E., Rodriguez, A., Walter, J.C. & Livingston, D.M. (2006). The BRCA1/BARD1 heterodimer modulates ran-dependent mitotic spindle assembly. Cell 127(3), 539–552.CrossRefGoogle ScholarPubMed
Jurmeister, S., Baumann, M., Balwierz, A., Keklikoglou, I., Ward, A., Uhlmann, S., Zhang, J.D., Wiemann, S. & Sahin, O. (2012). MicroRNA-200c represses migration and invasion of breast cancer cells by targeting actin-regulatory proteins FHOD1 and PPM1F. Mol Cell Biol 32(3), 633–651.Google Scholar
Kim, D., Song, J., Kim, S., Park, H.M., Chun, C.H., Sonn, J. & Jin, E.J. (2012). MicroRNA-34a modulates cytoskeletal dynamics through regulating RhoA/Rac1 cross-talk in chondroblasts. J Biol Chem 287(15), 12501–12509.CrossRefGoogle ScholarPubMed
Kinoshita, T., Nohata, N., Watanabe-Takano, H., Yoshino, H., Hidaka, H., Fujimura, L., Fuse, M., Yamasaki, T., Enokida, H., Nakagawa, M., Hanazawa, T., Okamoto, Y. & Seki, N. (2012). Actin-related protein 2/3 complex subunit 5 (ARPC5) contributes to cell migration and invasion and is directly regulated by tumor-suppressive microRNA-133a in head and neck squamous cell carcinoma. Int J Oncol 40(6), 1770–1778.Google ScholarPubMed
Kutsuna, H., Suzuki, K., Kamata, N., Kato, T., Hato, F., Mizuno, K., Kobayashi, H., Ishii, M. & Kitagawa, S. (2004). Actin reorganization and morphological changes in human neutrophils stimulated by TNF, GM-CSF, and G-CSF: The role of MAP kinases. Am J Physiol Cell Physiol 286(1), C55–C64.Google Scholar
Kwon, S., Shin, H. & Lim, H.J. (2011). Dynamic interaction of formin proteins and cytoskeleton in mouse oocytes during meiotic maturation. Mol Hum Reprod 17(5), 317–327.Google Scholar
Lam, E.K., Wang, X., Shin, V.Y., Zhang, S., Morrison, H., Sun, J., Ng, E.K., Yu, J. & Jin, H. (2011). A microRNA contribution to aberrant Ras activation in gastric cancer. Am J Transl Res 3(2), 209–218.Google Scholar
Larson, S.M., Lee, H.J., Hung, P.H., Matthews, L.M., Robinson, D.N. & Evans, J.P. (2010). Cortical mechanics and meiosis II completion in mammalian oocytes are mediated by myosin-II and Ezrin-Radixin-Moesin (ERM) proteins. Mol Biol Cell 21(18), 3182–3192.Google Scholar
Leader, B., Lim, H., Carabatsos, M.J., Harrington, A., Ecsedy, J., Pellman, D., Maas, R. & Leder, P. (2002). Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat Cell Biol 4(12), 921–928.Google Scholar
Leblanc, J., Zhang, X., McKee, D., Wang, Z.B., Li, R., Ma, C., Sun, Q.Y. & Liu, X.J. (2011). The small GTPase Cdc42 promotes membrane protrusion during polar body emission via Arp2-nucleated actin polymerization. Mol Hum Reprod 17(5), 305–316.Google Scholar
Lee, S.E., Sun, S.C., Choi, H.Y., Uhm, S.J. & Kim, N.H. (2012). mTOR is required for asymmetric division through small GTPases in mouse oocytes. Mol Reprod Dev 79(5), 356–366.CrossRefGoogle ScholarPubMed
Levi, M., Maro, B. & Shalgi, R. (2010a). Fyn kinase is involved in cleavage furrow ingression during meiosis and mitosis. Reproduction 140(6), 827–834.Google Scholar
Levi, M., Maro, B. & Shalgi, R. (2010b). The involvement of Fyn kinase in resumption of the first meiotic division in mouse oocytes. Cell Cycle 9(8), 1577–1589.Google Scholar
Levi, M., Maro, B. & Shalgi, R. (2011). The conformation and activation of Fyn kinase in the oocyte determine its localisation to the spindle poles and cleavage furrow. Reprod Fertil Dev 23(7), 846–857.Google Scholar
Li, H., Guo, F., Rubinstein, B. & Li, R. (2008). Actin-driven chromosomal motility leads to symmetry breaking in mammalian meiotic oocytes. Nat Cell Biol 10(11), 1301–1308.Google Scholar
Lin, S.L., Qi, S.T., Sun, S.C., Wang, Y.P., Schatten, H. & Sun, Q.Y. (2010). PAK1 regulates spindle microtubule organization during oocyte meiotic maturation. Front Biosci (Elite Ed) 2, 1254–1264.Google Scholar
Lippi, G., Steinert, J.R., Marczylo, E.L., D'Oro, S., Fiore, R., Forsythe, I.D., Schratt, G., Zoli, M., Nicotera, P. & Young, K.W. (2011). Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology. J Cell Biol 194(6), 889–904.Google Scholar
Liu, H., Cao, Y.D., Ye, W.X. & Sun, Y.Y. (2010). Effect of microRNA-206 on cytoskeleton remodelling by downregulating Cdc42 in MDA-MB-231 cells. Tumori 96(5), 751–755.Google Scholar
Liu, L., Chen, L., Chung, J. & Huang, S. (2008). Rapamycin inhibits F-actin reorganization and phosphorylation of focal adhesion proteins. Oncogene 27(37), 4998–5010.CrossRefGoogle ScholarPubMed
Logue, J.S., Whiting, J.L. & Scott, J.D. (2011). Sequestering Rac with PKA confers cAMP control of cytoskeletal remodeling. Small GTPases 2(3), 173–176.Google Scholar
Longo, F.J. & Chen, D.Y. (1985). Development of cortical polarity in mouse eggs: Involvement of the meiotic apparatus. Dev Biol 107(2), 382–394.Google Scholar
Luo, J., McGinnis, L.K. & Kinsey, W.H. (2009). Fyn kinase activity is required for normal organization and functional polarity of the mouse oocyte cortex. Mol Reprod Dev 76(9), 819–831.Google Scholar
Luo, J., McGinnis, L.K. & Kinsey, W.H. (2010). Role of Fyn kinase in oocyte developmental potential. Reprod Fertil Dev 22(6), 966–976.Google Scholar
Ma, C., Benink, H.A., Cheng, D., Montplaisir, V., Wang, L., Xi, Y., Zheng, P.P., Bement, W.M. & Liu, X.J. (2006). Cdc42 activation couples spindle positioning to first polar body formation in oocyte maturation. Curr Biol 16(2), 214–220.Google Scholar
Ma, J., Flemr, M., Stein, P., Berninger, P., Malik, R., Zavolan, M., Svoboda, P. & Schultz, R.M. (2010). MicroRNA activity is suppressed in mouse oocytes. Curr Biol 20(3), 265–270.Google Scholar
Maritzen, T., Zech, T., Schmidt, M.R., Krause, E., Machesky, L.M. & Haucke, V. (2012). Gadkin negatively regulates cell spreading and motility via sequestration of the actin-nucleating Arp2/3 complex. Proc Natl Acad Sci USA 109(26), 10382–10387.Google Scholar
Maro, B. & Verlhac, M.H. (2002). Polar body formation: New rules for asymmetric divisions. Nat Cell Biol 4(12), E281–E283.Google Scholar
Mattan, L., Ruth, K.K. & Ruth, S. (2011). Regulation of division in mammalian oocytes: Implications for polar body formation. Mol Hum Reprod 17(5), 328–334.Google Scholar
McGinnis, L.K., Albertini, D.F. & Kinsey, W.H. (2007). Localized activation of Src-family protein kinases in the mouse egg. Dev Biol 306(1), 241–254.Google Scholar
McGinnis, L.K., Kinsey, W.H. & Albertini, D.F. (2009). Functions of Fyn kinase in the completion of meiosis in mouse oocytes. Dev Biol 327(2), 280–287.Google Scholar
Mehlmann, L.M. & Jaffe, L.A. (2005). SH2 domain-mediated activation of an SRC family kinase is not required to initiate Ca2+ release at fertilization in mouse eggs. Reproduction 129(5), 557–564.CrossRefGoogle Scholar
Mendoza, M.C., Er, E.E., Zhang, W., Ballif, B.A., Elliott, H.L., Danuser, G. & Blenis, J. (2011). ERK-MAPK drives lamellipodia protrusion by activating the WAVE2 regulatory complex. Mol Cell 41(6), 661–671.Google Scholar
Meng, L., Luo, J., Li, C. & Kinsey, W.H. (2006). Role of Src homology 2 domain-mediated PTK signaling in mouse zygotic development. Reproduction 132(3), 413–421.Google Scholar
Michaut, M.A., Williams, C.J. & Schultz, R.M. (2005). Phosphorylated MARCKS: A novel centrosome component that also defines a peripheral subdomain of the cortical actin cap in mouse eggs. Dev Biol 280(1), 26–37.Google Scholar
Miles, J.R., McDaneld, T.G., Wiedmann, R.T., Cushman, R.A., Echternkamp, S.E., Vallet, J.L. & Smith, T.P. (2012). MicroRNA expression profile in bovine cumulus-oocyte complexes: Possible role of let-7 and miR-106a in the development of bovine oocytes. Anim Reprod Sci 130(1-2), 16–26.Google Scholar
Na, J. & Zernicka-Goetz, M. (2006). Asymmetric positioning and organization of the meiotic spindle of mouse oocytes requires CDC42 function. Curr Biol 16(12), 1249–1254.Google Scholar
Nance, J. & Zallen, J.A. (2011). Elaborating polarity: PAR proteins and the cytoskeleton. Development 138(5), 799–809.Google Scholar
Pang, R.T., Liu, W.M., Leung, C.O., Ye, T.M., Kwan, P.C., Lee, K.F. & Yeung, W.S. (2011). miR-135A regulates preimplantation embryo development through down-regulation of E3 ubiquitin ligase Seven In Absentia Homolog 1A (SIAH1A) expression. PLoS One 6(11), e27878. Google Scholar
Parsons, J.T., Horwitz, A.R. & Schwartz, M.A. (2010). Cell adhesion: Integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 11(9), 633–643.Google Scholar
Payne, C. & Schatten, G. (2003). Golgi dynamics during meiosis are distinct from mitosis and are coupled to endoplasmic reticulum dynamics until fertilization. Dev Biol 264(1), 50–63.Google Scholar
Pechlivanis, M., Samol, A. & Kerkhoff, E. (2009). Identification of a short Spir interaction sequence at the C-terminal end of formin subgroup proteins. J Biol Chem 284(37), 25324–25333.Google Scholar
Petronczki, M., Glotzer, M., Kraut, N. & Peters, J.M. (2007). Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev Cell 12(5), 713–725.Google Scholar
Pfender, S., Kuznetsov, V., Pleiser, S., Kerkhoff, E. & Schuh, M. (2011). Spire-type actin nucleators cooperate with Formin-2 to drive asymmetric oocyte division. Curr Biol 21(11), 955–960.Google Scholar
Pollard, T.D. (2007). Regulation of actin filament assembly by Arp2/3 complex and formins. Annu Rev Biophys Biomol Struct 36, 451–477.Google Scholar
Pollard, T.D. & Borisy, G.G. (2003). Cellular motility driven by assembly and disassembly of actin filaments. Cell 112(4), 453–465.CrossRefGoogle ScholarPubMed
Quinlan, M.E., Heuser, J.E., Kerkhoff, E. & Mullins, R.D. (2005). Drosophila Spire is an actin nucleation factor. Nature 433(7024), 382–388.Google Scholar
Quinlan, M.E., Hilgert, S., Bedrossian, A., Mullins, R.D. & Kerkhoff, E. (2007). Regulatory interactions between two actin nucleators, Spire and Cappuccino. J Cell Biol 179(1), 117–128.Google Scholar
Rosales-Nieves, A.E., Johndrow, J.E., Keller, L.C., Magie, C.R., Pinto-Santini, D.M. & Parkhurst, S.M. (2006). Coordination of microtubule and microfilament dynamics by Drosophila Rho1, Spire and Cappuccino. Nat Cell Biol 8(4), 367–376.Google Scholar
Sabatel, C., Malvaux, L., Bovy, N., Deroanne, C., Lambert, V., Gonzalez, M.L., Colige, A., Rakic, J.M., Noel, A., Martial, J.A. & Struman, I. (2011). MicroRNA-21 exhibits antiangiogenic function by targeting RhoB expression in endothelial cells. PLoS One 6(2), e16979. Google Scholar
Schatten, H. & Sun, Q.Y. (2011). Centrosome dynamics during mammalian oocyte maturation with a focus on meiotic spindle formation. Mol Reprod Dev 78(10-11), 757–768.Google Scholar
Schonichen, A. & Geyer, M. (2010). Fifteen formins for an actin filament: A molecular view on the regulation of human formins. Biochim Biophys Acta 1803(2), 152–163.Google Scholar
Schuh, M. (2012). An actin-dependent mechanism for long-range vesicle transport. Nat Cell Biol 13(12), 1431–1436.Google Scholar
Schuh, M. & Ellenberg, J. (2008). A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 18(24), 1986–1992.Google Scholar
Schuldt, A. (2005). Spire: A new nucleator for actin. Nat Cell Biol 7(2), 107.Google Scholar
Sette, C., Paronetto, M.P., Barchi, M., Bevilacqua, A., Geremia, R. & Rossi, P. (2002). Tr-kit-induced resumption of the cell cycle in mouse eggs requires activation of a Src-like kinase. Embo J 21(20), 5386–5395.Google Scholar
Sharif, B., Na, J., Lykke-Hartmann, K., McLaughlin, S.H., Laue, E., Glover, D.M. & Zernicka-Goetz, M. (2010). The chromosome passenger complex is required for fidelity of chromosome transmission and cytokinesis in meiosis of mouse oocytes. J Cell Sci 123(Pt 24), 4292–4300.Google Scholar
Simerly, C., Nowak, G., de Lanerolle, P. & Schatten, G. (1998). Differential expression and functions of cortical myosin IIA and IIB isotypes during meiotic maturation, fertilization, and mitosis in mouse oocytes and embryos. Mol Biol Cell 9(9), 2509–2525.Google Scholar
Sossey-Alaoui, K., Downs-Kelly, E., Das, M., Izem, L., Tubbs, R. & Plow, E.F. (2011). WAVE3, an actin remodeling protein, is regulated by the metastasis suppressor microRNA, miR-31, during the invasion-metastasis cascade. Int J Cancer 129(6), 1331–1343.Google Scholar
Suh, N., Baehner, L., Moltzahn, F., Melton, C., Shenoy, A., Chen, J. & Blelloch, R. (2010). MicroRNA function is globally suppressed in mouse oocytes and early embryos. Curr Biol 20(3), 271–277.Google Scholar
Sun, Q.Y. & Schatten, H. (2006). Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131(2), 193–205.Google Scholar
Sun, S.C. & Kim, N.H. (2011). GM130: New insights into oocyte asymmetric division. Cell Cycle 10(15), 2419. Google Scholar
Sun, S.C. & Kim, N.H. (2012). Spindle assembly checkpoint and its regulators in meiosis. Hum Reprod Update 18(1), 60–72.Google Scholar
Sun, S.C., Liu, H.L. & Sun, Q.Y. (2012). Survivin regulates Plk1 localization to kinetochore in mouse oocyte meiosis. Biochem Biophys Res Commun 421(4), 797–800.Google Scholar
Sun, S.C., Sun, Q.Y. & Kim, N.H. (2011a). JMY is required for asymmetric division and cytokinesis in mouse oocytes. Mol Hum Reprod 17(5), 296–304.CrossRefGoogle ScholarPubMed
Sun, S.C., Wang, Z.B., Xu, Y.N., Lee, S.E., Cui, X.S. & Kim, N.H. (2011b). Arp2/3 complex regulates asymmetric division and cytokinesis in mouse oocytes. PLoS One 6(4), e18392. Google Scholar
Sun, S.C., Wei, L., Li, M., Lin, S.L., Xu, B.Z., Liang, X.W., Kim, N.H., Schatten, H., Lu, S.S. & Sun, Q.Y. (2009). Perturbation of survivin expression affects chromosome alignment and spindle checkpoint in mouse oocyte meiotic maturation. Cell Cycle 8(20), 3365–3372.Google Scholar
Sun, S.C., Xu, Y.N., Li, Y.H., Lee, S.E., Jin, Y.X., Cui, X.S. & Kim, N.H. (2011c). WAVE2 regulates meiotic spindle stability, peripheral positioning and polar body emission in mouse oocytes. Cell Cycle 10(11), 1853–1860.Google Scholar
Suzuki, A. & Ohno, S. (2006). The PAR-aPKC system: Lessons in polarity. J Cell Sci 119(Pt 6), 979–987.Google Scholar
Tong, C., Fan, H.Y., Chen, D.Y., Song, X.F., Schatten, H. & Sun, Q.Y. (2003). Effects of MEK inhibitor U0126 on meiotic progression in mouse oocytes: Microtuble organization, asymmetric division and metaphase II arrest. Cell Res 13(5), 375–383.Google Scholar
Verlhac, M.H. & Dumont, J. (2008). Interactions between chromosomes, microfilaments and microtubules revealed by the study of small GTPases in a big cell, the vertebrate oocyte. Mol Cell Endocrinol 282(1-2), 12–17.Google Scholar
Verlhac, M.H., Lefebvre, C., Guillaud, P., Rassinier, P. & Maro, B. (2000). Asymmetric division in mouse oocytes: With or without Mos. Curr Biol 10(20), 1303–1306.Google Scholar
Vinot, S., Le, T., Maro, B. & Louvet-Vallee, S. (2004). Two PAR6 proteins become asymmetrically localized during establishment of polarity in mouse oocytes. Curr Biol 14(6), 520–525.Google Scholar
Vizcarra, C.L., Kreutz, B., Rodal, A.A., Toms, A.V., Lu, J., Zheng, W., Quinlan, M.E. & Eck, M.J. (2011). Structure and function of the interacting domains of Spire and Fmn-family formins. Proc Natl Acad Sci USA 108(29), 11884–11889.Google Scholar
Wang, J.B., Sonn, R., Tekletsadik, Y.K., Samorodnitsky, D. & Osman, M.A. (2009a). IQGAP1 regulates cell proliferation through a novel CDC42-mTOR pathway. J Cell Sci 122(Pt 12), 2024–2033.Google Scholar
Wang, L., Wang, Z.B., Zhang, X., Fitzharris, G., Baltz, J.M., Sun, Q.Y. & Liu, X.J. (2008). Brefeldin A disrupts asymmetric spindle positioning in mouse oocytes. Dev Biol 313(1), 155–166.Google Scholar
Wang, S., Hu, J., Guo, X., Liu, J.X. & Gao, S. (2009b). ADP-ribosylation factor 1 regulates asymmetric cell division in female meiosis in the mouse. Biol Reprod 80(3), 555–562.Google Scholar
Wu, Y.G., Zhou, P., Lan, G.C., Gao, D., Li, Q., Wei, D.L., Wang, H.L. & Tan, J.H. (2010). MPF governs the assembly and contraction of actomyosin rings by activating RhoA and MAPK during chemical-induced cytokinesis of goat oocytes. PLoS One 5(9), e12706. Google Scholar
Xu, Y.W., Wang, B., Ding, C.H., Li, T., Gu, F. & Zhou, C. (2011). Differentially expressed microRNAs in human oocytes. J Assist Reprod Genet 28(6), 559–566.Google Scholar
Yi, K., Unruh, J.R., Deng, M., Slaughter, B.D., Rubinstein, B. & Li, R. (2011). Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 13(10), 1252–1258.Google Scholar
Yu, D., Zhang, H., Blanpied, T.A., Smith, E. & Zhan, X. (2010). Cortactin is implicated in murine zygotic development. Exp Cell Res 316(5), 848–858.CrossRefGoogle ScholarPubMed
Zeidan, A., Hunter, J.C., Javadov, S. & Karmazyn, M. (2011). mTOR mediates RhoA-dependent leptin-induced cardiomyocyte hypertrophy. Mol Cell Biochem 352(1-2), 99–108.Google Scholar
Zhang, C.H., Wang, Z.B., Quan, S., Huang, X., Tong, J.S., Ma, J.Y., Guo, L., Wei, Y.C., Ouyang, Y.C., Hou, Y., Xing, F.Q. & Sun, Q.Y. (2011). GM130, a cis-Golgi protein, regulates meiotic spindle assembly and asymmetric division in mouse oocyte. Cell Cycle 10(11), 1861–1870.Google Scholar
Zhang, Q.H., Qi, S.T., Wang, Z.B., Yang, C.R., Wei, Y.W., Chen, L., Ouyang, Y.C., Hou, Y., Schatten, H. & Sun, Q.Y. (2012). Localization and function of the Ska complex during mouse oocyte meiotic maturation. Cell Cycle 11(5), 909–916.Google Scholar
Zhang, X., Ma, C., Miller, A.L., Katbi, H.A., Bement, W.M. & Liu, X.J. (2008). Polar body emission requires a RhoA contractile ring and Cdc42-mediated membrane protrusion. Dev Cell 15(3), 386–400.Google Scholar
Zhong, Z.S., Huo, L.J., Liang, C.G., Chen, D.Y. & Sun, Q.Y. (2005). Small GTPase RhoA is required for ooplasmic segregation and spindle rotation, but not for spindle organization and chromosome separation during mouse oocyte maturation, fertilization, and early cleavage. Mol Reprod Dev 71(2), 256–261.Google Scholar