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Regulatory Mechanism of Spindle Movements during Oocyte Meiotic Division
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 Title & Authors
Regulatory Mechanism of Spindle Movements during Oocyte Meiotic Division
Ai, Jun-Shu; Li, Mo; Schatten, Heide; Sun, Qing-Yuan;
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Female germ cell meiotic divisions are typically asymmetric, giving rise to two daughter cells with different sizes. Spindle movements including spindle migration from the oocyte center to the cortex and spindle rotation from parallel to perpendicular (typically in the mouse) at the cortex are crucial for these asymmetric divisions and therefore are crucial for gamete production. Different regulatory mechanisms for spindle movements have been determined in different species and a wide variety of different molecular components and processes that are involved in spindle movements have also been identified in different species. Here, we review the current state of knowledge as well as our understanding of mechanisms for spindle movements in different systems with focus on three main aspects: microtubules (MT), microfilaments (MF) and molecules associated with cytoskeletal organization as well as molecules that are not directly related to the cytoskeleton. How they might interact or function independently during female meiotic divisions in different species is discussed in detail.
Spindle Movement;Meiotic Division;Cytoskeleton;Oocyte;
 Cited by
Ai, J. S., Q. Wang, M. Li, L. H. Shi, S. I. Ola, B. Xiong, S. Yin, D. Y. Chen and Q. Y. Sun. 2008a. Roles of microtubules and microfilaments in spindle movements during rat oocyte meiosis. J. Reprod. Dev. 54:391-396 crossref(new window)

Ai, J. S., Q. Wang, S. Yin, L. H. Shi, B. Xiong, Y. C. Ouyang, Y. Hou, D. Y. Chen, H. Schatten and Q. Y. Sun. 2008b. Regulation of peripheral spindle movement and spindle rotation during mouse oocyte meiosis: New Perspectives. Microsc. Microanal. 14:349-356

Albertson, D. G. and J. N. Thomson. 1993. Segregation of holocentric chromosomes at meiosis in the nematode, Caenorhabditis elegans. Chromosome Res. 1:15-26 crossref(new window)

Alexandre, H., A. Van Cauwenberge and J. Mulnard. 1989. Involvement of microtubules and microfilaments in the control of the nuclear movement during maturation of mouse oocyte. Dev. Biol. 136:311-320 crossref(new window)

Bishop, A. L. and A. Hall. 2000. Rho GTPases and their effector proteins. Biochem. J. 348 Pt 2:241-255 crossref(new window)

Bresnick, A. R. 1999. Molecular mechanisms of nonmuscle myosin-II regulation. Curr. Opin. Cell Biol. 11:26-33 crossref(new window)

Calarco, P. G. 2005. The role of microfilaments in early meiotic maturation of mouse oocytes. Microsc. Microanal. 11:146-153

Carvalho, P., M. L. Gupta, Jr., M. A. Hoyt and D. Pellman. 2004. Cell cycle control of kinesin-mediated transport of Bik1 (CLIP-170) regulates microtubule stability and dynein activation. Dev. Cell 6:815-829 crossref(new window)

Cau, J., S. Faure, S. Vigneron, J. C. Labbe, C. Delsert and N. Morin. 2000. Regulation of Xenopus p21-activated kinase (XPAK2) by Cdc42 and maturation-promoting factor controls Xenopus oocyte maturation. J. Biol. Chem. 275:2367-2375 crossref(new window)

Chang, F., D. Drubin and P. Nurse. 1997. cdc12p, a protein required for cytokinesis in fission yeast, is a component of the cell division ring and interacts with profilin. J. Cell Biol. 137:169-182 crossref(new window)

Desai, A. and T. J. Mitchison. 1997. Microtubule polymerization dynamics. Annu. Rev. Cell Dev. Biol. 13:83-117 crossref(new window)

Ding, D. Q., Y. Chikashige, T. Haraguchi and Y. Hiraoka. 1998. Oscillatory nuclear movement in fission yeast meiotic prophase is driven by astral microtubules, as revealed by continuous observation of chromosomes and microtubules in living cells. J. Cell Sci. 111(Pt 6):701-712

Donaldson, J. G., D. Finazzi and R. D. Klausner. 1992. Brefeldin A inhibits Golgi membrane-catalysed exchange of guanine nucleotide onto ARF protein. Nature 360:350-352 crossref(new window)

Duchen, M. R. 2000. Mitochondria and calcium: from cell signalling to cell death. J. Physiol. 529 Pt 1:57-68 crossref(new window)

Ducibella, T., D. Huneau, E. Angelichio, Z. Xu, R. M. Schultz, G. S. Kopf, R. Fissore, S. Madoux and J. P. Ozil. 2002. Egg-toembryo transition is driven by differential responses to Ca(2+) oscillation number. Dev. Biol. 250:280-291

Dumollard, R., K. Hammar, M. Porterfield, P. J. Smith, C. Cibert, C. Rouviere and C. Sardet. 2003. Mitochondrial respiration and $Ca^{2+}$ waves are linked during fertilization and meiosis completion. Development 130:683-692 crossref(new window)

Dumollard, R., P. Marangos, G. Fitzharris, K. Swann, M. Duchen and J. Carroll. 2004. Sperm-triggered [Ca2+] oscillations and Ca2+ homeostasis in the mouse egg have an absolute requirement for mitochondrial ATP production. Development 131:3057-3067 crossref(new window)

Dumont, J., K. Million, K. Sunderland, P. Rassinier, H. Lim, B. Leader and M. H. Verlhac. 2007. Formin-2 is required for spindle migration and for the late steps of cytokinesis in mouse oocytes. Dev. Biol. 301:254-265 crossref(new window)

Duncan, F. E., S. B. Moss, R. M. Schultz and C. J. Williams. 2005. PAR-3 defines a central subdomain of the cortical actin cap in mouse eggs. Dev. Biol. 280:38-47 crossref(new window)

Ellis, G. C., J. B. Phillips, S. O'Rourke, R. Lyczak and B. Bowerman. 2004. Maternally expressed and partially redundant beta-tubulins in Caenorhabditis elegans are autoregulated. J. Cell Sci. 117:457-464 crossref(new window)

Endow, S. A. and D. J. Komma. 1997. Spindle dynamics during meiosis in Drosophila oocytes. J. Cell Biol. 137:1321-1336 crossref(new window)

Etienne-Manneville, S. and A. Hall. 2003. Cell polarity: Par6, aPKC and cytoskeletal crosstalk. Curr. Opin. Cell Biol. 15:67-72 crossref(new window)

Etienne-Manneville, S. and A. Hall. 2002. Rho GTPases in cell biology. Nature 420:629-635 crossref(new window)

Evangelista, M., D. Pruyne, D. C. Amberg, C. Boone and A. Bretscher. 2002. Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat. Cell Biol. 4:260-269 crossref(new window)

Fan, H. Y., L. J. Huo, X. Q. Meng, Z. S. Zhong, Y. Hou, D. Y. Chen and Q. Y. Sun. 2003. Involvement of calcium/calmodulin-dependent protein kinase II (CaMKII) in meiotic maturation and activation of pig oocytes. Biol. Reprod. 69:1552-1564 crossref(new window)

Feierbach, B. and F. Chang. 2001. Roles of the fission yeast formin for3p in cell polarity, actin cable formation and symmetric cell division. Curr. Biol. 11:1656-1665 crossref(new window)

Gard, D. L. 1992. Microtubule organization during maturation of Xenopus oocytes: assembly and rotation of the meiotic spindles. Dev. Biol. 151:516-530 crossref(new window)

Gard, D. L., B. J. Cha and A. D. Roeder. 1995. F-actin is required for spindle anchoring and rotation in Xenopus oocytes: a reexamination of the effects of cytochalasin B on oocyte maturation. Zygote 3:17-26

Gavin, R. H. 1997. Microtubule-microfilament synergy in the cytoskeleton. Int. Rev. Cytol. 173:207-242 crossref(new window)

Goldstein, B. 1995. Cell contacts orient some cell division axes in the Caenorhabditis elegans embryo. J. Cell Biol. 129:1071-1080 crossref(new window)

Gonczy, P. 2002. Mechanisms of spindle positioning: focus on flies and worms. Trends Cell Biol. 12:332-339 crossref(new window)

Grill, S. W., P. Gonczy, E. H. Stelzer and A. A. Hyman. 2001. Polarity controls forces governing asymmetric spindle positioning in the Caenorhabditis elegans embryo. Nature 409:630-633 crossref(new window)

Gueth-Hallonet, C., C. Antony, J. Aghion, A. Santa-Maria, I. Lajoie-Mazenc, M. Wright and B. Maro. 1993. gamma- Tubulin is present in acentriolar MTOCs during early mouse development. J. Cell Sci. 105(Pt 1):157-166 crossref(new window)

Gulyas, B. J. 1976. Ultrastructural observations on rabbit, hamster and mouse eggs following electrical stimulation in vitro. Am. J. Anat. 147:203-218 crossref(new window)

Gundersen, G. G. and A. Bretscher. 2003. Cell biology. Microtubule asymmetry. Science 300:2040-2041 crossref(new window)

Gunst, S. J. 2004. Actions by actin: reciprocal regulation of cortactin activity by tyrosine kinases and F-actin. Biochem. J. 380:e7-8 crossref(new window)

Halet, G. and J. Carroll. 2007. Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev. Cell 12:309-317 crossref(new window)

Hamaguchi, Y. 2001. Displacement of the mitotic apparatus which induces ectopic polar body formation or parthenogenetic cleavage in starfish oocytes. Dev. Biol. 239:364-375 crossref(new window)

Hartman, J. J., J. Mahr, K. McNally, K. Okawa, A. Iwamatsu, S. Thomas, S. Cheesman, J. Heuser, R. D. Vale and F. J. McNally. 1998. Katanin, a microtubule-severing protein, is a novel AAAATPase that targets to the centrosome using a WD40-containing subunit. Cell 93:277-287 crossref(new window)

Huisman, S. M. and M. Segal. 2005. Cortical capture of microtubules and spindle polarity in budding yeast - where's the catch? J. Cell Sci. 118:463-471 crossref(new window)

Hyman, A. A. 1989. Centrosome movement in the early divisions of Caenorhabditis elegans: a cortical site determining centrosome position. J. Cell Biol. 109:1185-1193 crossref(new window)

Hyman, A. A. and E. Karsenti. 1996. Morphogenetic properties of microtubules and mitotic spindle assembly. Cell 84:401-410 crossref(new window)

Ibanez, E., D. F. Albertini and E. W. Overstrom. 2003. Demecolcine-induced oocyte enucleation for somatic cell cloning: coordination between cell-cycle egress, kinetics of cortical cytoskeletal interactions, and second polar body extrusion. Biol. Reprod. 68:1249-1258 crossref(new window)

Ishizaki, T., Y. Morishima, M. Okamoto, T. Furuyashiki, T. Kato and S. Narumiya. 2001. Coordination of microtubules and the actin cytoskeleton by the Rho effector mDia1. Nat. Cell Biol. 3:8-14 crossref(new window)

Kaltschmidt, J. A., C. M. Davidson, N. H. Brown and A. H. Brand. 2000. Rotation and asymmetry of the mitotic spindle direct asymmetric cell division in the developing central nervous system. Nat. Cell Biol. 2:7-12 crossref(new window)

Kamm, K. E. and J. T. Stull. 2001. Dedicated myosin light chain kinases with diverse cellular functions. J. Biol. Chem. 276:4527-4530 crossref(new window)

Kim, N. H., S. K. Cho, S. H. Choi, E. Y. Kim, S. P. Park and J. H. Lim. 2000. The distribution and requirements of microtubules and microfilaments in bovine oocytes during in vitro maturation. Zygote 8:25-32 crossref(new window)

Kim, N. H., H. M. Chung, K. Y. Cha and K. S. Chung. 1998. Microtubule and microfilament organization in maturing human oocytes. Hum. Reprod. 13:2217-2222 crossref(new window)

Kline, D. and J. T. Kline. 1992. Repetitive calcium transients and the role of calcium in exocytosis and cell cycle activation in the mouse egg. Dev. Biol. 149:80-89 crossref(new window)

Kobielak, A., H. A. Pasolli and E. Fuchs. 2004. Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat. Cell Biol. 6:21-30 crossref(new window)

Kovar, D. R., J. R. Kuhn, A. L. Tichy and T. D. Pollard. 2003. The fission yeast cytokinesis formin Cdc12p is a barbed end actin filament capping protein gated by profilin. J. Cell Biol. 161:875-887 crossref(new window)

Kubiak, J., A. Paldi, M. Weber and B. Maro. 1991. Genetically identical parthenogenetic mouse embryos produced by inhibition of the first meiotic cleavage with cytochalasin D. Development 111:763-769

Kumakiri, J., S. Oda, K. Kinoshita and S. Miyazaki. 2003. Involvement of Rho family G protein in the cell signaling for sperm incorporation during fertilization of mouse eggs: inhibition by Clostridium difficile toxin B. Dev. Biol. 260:522-535 crossref(new window)

Labbe, J. C., E. K. McCarthy and B. Goldstein. 2004. The forces that position a mitotic spindle asymmetrically are tethered until after the time of spindle assembly. J. Cell Biol. 167:245-256 crossref(new window)

Leader, B., H. Lim, M. J. Carabatsos, A. Harrington, J. Ecsedy, D. Pellman, R. Maas and P. Leder. 2002. Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat. Cell Biol. 4:921-928 crossref(new window)

Lei, Y. and R. Warrior. 2000. The Drosophila Lissencephaly1 (DLis1) gene is required for nuclear migration. Dev. Biol. 226:57-72 crossref(new window)

Lessman, C. A. 1987. Germinal vesicle migration and dissolution in Rana pipiens oocytes: effect of steroids and microtubule poisons. Cell Differ. 20:239-251 crossref(new window)

Liu, L., J. R. Trimarchi, R. Oldenbourg and D. L. Keefe. 2000. Increased birefringence in the meiotic spindle provides a new marker for the onset of activation in living oocytes. Biol. Reprod. 63:251-258 crossref(new window)

Longo, F. J. and D. Y. Chen. 1985. Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Dev. Biol. 107:382-394 crossref(new window)

Lu, C. and P. E. Mains. 2005. Mutations of a redundant alphatubulin gene affect Caenorhabditis elegans early embryonic cleavage via MEI-1/katanin-dependent and -independent pathways. Genetics 170:115-126 crossref(new window)

Lutz, D. A., Y. Hamaguchi and S. Inoue. 1988. Micromanipulation studies of the asymmetric positioning of the maturation spindle in Chaetopterus sp. oocytes: I. Anchorage of the spindle to the cortex and migration of a displaced spindle. Cell Motil. Cytoskeleton 11:83-96 crossref(new window)

Ma, C., H. A. Benink, D. Cheng, V. Montplaisir, L. Wang, Y. Xi, P. P. Zheng, W. M. Bement and X. J. Liu. 2006. Cdc42 activation couples spindle positioning to first polar body formation in oocyte maturation. Curr. Biol. 16:214-220 crossref(new window)

Ma, L., R. Rohatgi and M. W. Kirschner. 1998. The Arp2/3 complex mediates actin polymerization induced by the small GTP-binding protein Cdc42. Proc. Natl. Acad. Sci. USA 95:15362-15367 crossref(new window)

Machesky, L. M. and K. L. Gould. 1999. The Arp2/3 complex: a multifunctional actin organizer. Curr. Opin. Cell Biol. 11:117-121 crossref(new window)

Maro, B., S. K. Howlett and M. Webb. 1985. Non-spindle microtubule organizing centers in metaphase II-arrested mouse oocytes. J. Cell Biol. 101:1665-1672 crossref(new window)

Maro, B., M. H. Johnson, S. J. Pickering and G. Flach. 1984. Changes in actin distribution during fertilization of the mouse egg. J. Embryol. Exp. Morphol. 81:211-237

Maro, B., M. H. Johnson, M. Webb and G. Flach. 1986. Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane. J. Embryol. Exp. Morphol. 92:11-32

Maro, B. and M. H. Verlhac. 2002. Polar body formation: new rules for asymmetric divisions. Nat. Cell Biol. 4:E281-283 crossref(new window)

Matson, S., S. Markoulaki and T. Ducibella. 2006. Antagonists of myosin light chain kinase and of myosin II inhibit specific events of egg activation in fertilized mouse eggs. Biol. Reprod. 74:169-176 crossref(new window)

McCarter, J., B. Bartlett, T. Dang and T. Schedl. 1999. On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205:111-128 crossref(new window)

McGrail, M. and T. S. Hays. 1997. The microtubule motor cytoplasmic dynein is required for spindle orientation during germline cell divisions and oocyte differentiation in Drosophila. Development 124:2409-2419

Miller, M. A., V. Q. Nguyen, M. H. Lee, M. Kosinski, T. Schedl, R. M. Caprioli and D. Greenstein. 2001. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291:2144-2147 crossref(new window)

Miller, M. A., P. J. Ruest, M. Kosinski, S. K. Hanks and D. Greenstein. 2003. An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev. 17:187-200 crossref(new window)

Moore, C. A. and M. Zernicka-Goetz. 2005. PAR-1 and the microtubule-associated proteins CLASP2 and dynactin-p50 have specific localisation on mouse meiotic and first mitotic spindles. Reproduction 130:311-320 crossref(new window)

Motta, P. M., S. A. Nottola, S. Makabe and R. Heyn. 2000. Mitochondrial morphology in human fetal and adult female germ cells. Hum. Reprod. 15(Suppl 2):129-147

Mullins, R. D., J. A. Heuser and T. D. Pollard. 1998. The interaction of Arp2/3 complex with actin: nucleation, high affinity pointed end capping, and formation of branching networks of filaments. Proc. Natl. Acad. Sci. USA 95:6181-6186 crossref(new window)

Mullins, R. D., W. F. Stafford and T. D. Pollard. 1997. Structure, subunit topology, and actin-binding activity of the Arp2/3 complex from Acanthamoeba. J. Cell Biol. 136:331-343 crossref(new window)

Na, J. and M. Zernicka-Goetz. 2006. Asymmetric positioning and organization of the meiotic spindle of mouse oocytes requires CDC42 function. Curr. Biol. 16:1249-1254 crossref(new window)

Natale, D. R. and A. J. Watson. 2002. Rac-1 and IQGAP are potential regulators of E-cadherin-catenin interactions during murine preimplantation development. Mech. Dev. 119(Suppl 1):S21-26 crossref(new window)

Navara, C. S., N. L. First and G. Schatten. 1994. Microtubule organization in the cow during fertilization, polyspermy, parthenogenesis, and nuclear transfer: the role of the sperm aster. Dev. Biol. 162:29-40 crossref(new window)

Navarro, P. A., L. Liu, J. R. Trimarchi, R. A. Ferriani and D. L. Keefe. 2005. Noninvasive imaging of spindle dynamics during mammalian oocyte activation. Fertil. Steril. 83(Suppl 1):1197-1205 crossref(new window)

Nishimura, Y. and I. Mabuchi. 2003. An IQGAP-like protein is involved in actin assembly together with Cdc42 in the sea urchin egg. Cell Motil. Cytoskeleton 56:207-218 crossref(new window)

Palazzo, A. F., T. A. Cook, A. S. Alberts and G. G. Gundersen. 2001. mDia mediates Rho-regulated formation and orientation of stable microtubules. Nat. Cell Biol. 3:723-729 crossref(new window)

Palazzo, R. E., E. Vaisberg, R. W. Cole and C. L. Rieder. 1992. Centriole duplication in lysates of Spisula solidissima oocytes. Science 256:219-221 crossref(new window)

Pearson, C. G. and K. Bloom. 2004. Dynamic microtubules lead the way for spindle positioning. Nat. Rev. Mol. Cell Biol. 5:481-492 crossref(new window)

Pellegrin, S. and H. Mellor. 2005. The Rho family GTPase Rif induces filopodia through mDia2. Curr. Biol. 15:129-133 crossref(new window)

Pellestor, F., T. Anahory and S. Hamamah. 2005. Effect of maternal age on the frequency of cytogenetic abnormalities in human oocytes. Cytogenet. Genome Res. 111:206-212 crossref(new window)

Phillips, J. B., R. Lyczak, G. C. Ellis and B. Bowerman. 2004. Roles for two partially redundant alpha-tubulins during mitosis in early Caenorhabditis elegans embryos. Cell Motil. Cytoskeleton 58:112-126 crossref(new window)

Pollard, T. D., L. Blanchoin and R. D. Mullins. 2000. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29:545-576 crossref(new window)

Pruyne, D., M. Evangelista, C. Yang, E. Bi, S. Zigmond, A. Bretscher and C. Boone. 2002. Role of formins in actin assembly: nucleation and barbed-end association. Science 297:612-615 crossref(new window)

Reinsch, S. and P. Gonczy. 1998. Mechanisms of nuclear positioning. J. Cell Sci. 111(Pt 16):2283-2295 crossref(new window)

Rizzuto, R., P. Bernardi and T. Pozzan. 2000. Mitochondria as allround players of the calcium game. J. Physiol. 529(Pt 1):37-47 crossref(new window)

Sagot, I., S. K. Klee and D. Pellman. 2002. Yeast formins regulate cell polarity by controlling the assembly of actin cables. Nat. Cell Biol. 4:42-50

Sardet, C., F. Prodon, R. Dumollard, P. Chang and J. Chenevert. 2002. Structure and function of the egg cortex from oogenesis through fertilization. Dev. Biol. 241:1-23 crossref(new window)

Sathananthan, A. H. 1997. Ultrastructure of the human egg. Hum. Cell 10:21-38

Sathananthan, A. H. and A. O. Trounson. 2000. Mitochondrial morphology during preimplantational human embryogenesis. Hum. Reprod. 15(Suppl 2):148-159 crossref(new window)

Schaerer-Brodbeck, C. and H. Riezman. 2000. Interdependence of filamentous actin and microtubules for asymmetric cell division. Biol. Chem. 381:815-825 crossref(new window)

Schirenbeck, A., T. Bretschneider, R. Arasada, M. Schleicher and J. Faix. 2005. The Diaphanous-related formin dDia2 is required for the formation and maintenance of filopodia. Nat. Cell Biol. 7:619-625 crossref(new window)

Schuh, M. and J. Ellenberg. 2007. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130:484-498 crossref(new window)