Ran GTPase promotes oocyte polarization by regulating ERM (Ezrin/Radixin/Moesin) inactivation

Cell Cycle

Volumn 12, Issue 11, 2013, Pages 1672-1678

  Dehapiot, Benoit ^a,b   Halet, Guillaume ^a,b  

^a UNIVERSITÉ DE RENNES 1   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

Author keywords

Actin; Chromatin; Meiosis; Oocyte; Polarity GTPase

Indexed keywords

ACTIN; GUANOSINE TRIPHOSPHATASE; PROTEIN CDC42; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CAPPING PHENOMENON; CELL POLARITY; CHROMATIN; CHROMOSOME; CHROMOSOME CONDENSATION; CONFORMATION; DEPHOSPHORYLATION; GERMINAL VESICLE; MEIOSIS; METAPHASE; METAPHASE CHROMOSOME; MICROTUBULE; MICROVILLUS; MOUSE; NONHUMAN; OOCYTE; OOCYTE CORTEX; OOCYTE RETRIEVAL; PHOSPHORYLATION; POLARIZATION; PROTEIN EXPRESSION;

MAMMALIA;

EID: 84878540835     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.24901     Document Type: Article

References (47)

1. Brunet S, Verlhac MH. Positioning to get out of meiosis: the asymmetry of division. Hum Reprod Update 2011; 17:68-75; PMID:20833637; http://dx.doi.org/ 10.1093/humupd/dmq044
2. Li R, Albertini DF. The road to maturation: somatic cell interaction and self-organization of the mammalian oocyte. Nat Rev Mol Cell Biol 2013; 14:141-52; PMID:23429793; http://dx.doi.org/10.1038/nrm3531
3. Azoury J, Lee KW, Georget V, Rassinier P, Leader B, Verlhac MH. Spindle positioning in mouse oocytes relies on a dynamic meshwork of actin filaments. Curr Biol 2008; 18:1514-9; PMID:18848445; http://dx.doi.org/10.1016/j.cub.2008. 08.044
4. Schuh M, Ellenberg J. A new model for asymmetric spindle positioning in mouse oocytes. Curr Biol 2008; 18:1986-92; PMID:19062278; http://dx.doi. org/10.1016/j.cub.2008.11.022
5. Chaigne A, Verlhac MH, Terret ME. Spindle positioning in mammalian oocytes. Exp Cell Res 2012; 318:1442-7; PMID:22406266; http://dx.doi. org/10.1016/j.yexcr.2012.02.019
6. Connors SA, Kanatsu-Shinohara M, Schultz RM, Kopf GS. Involvement of the cytoskeleton in the movement of cortical granules during oocyte maturation, and cortical granule anchoring in mouse eggs. Dev Biol 1998; 200:103-15; PMID:9698460; http://dx.doi.org/10.1006/dbio.1998.8945
7. Longo FJ, Chen DY. Development of cortical polarity in mouse eggs: involvement of the meiotic apparatus. Dev Biol 1985; 107:382-94; PMID:4038667; http://dx.doi.org/10.1016/0012-1606(85)90320-3
8. Maro B, Johnson MH, Webb M, Flach G. Mechanism of polar body formation in the mouse oocyte: an interaction between the chromosomes, the cytoskeleton and the plasma membrane. J Embryol Exp Morphol 1986; 92:11-32; PMID:3723057
9. Van Blerkom J, Bell H. Regulation of development in the fully grown mouse oocyte: chromosomemediated temporal and spatial differentiation of the cytoplasm and plasma membrane. J Embryol Exp Morphol 1986; 93:213-38; PMID:3734683
10. Deng M, Suraneni P, Schultz RM, Li R. The Ran GTPase mediates chromatin signaling to control cortical polarity during polar body extrusion in mouse oocytes. Dev Cell 2007; 12:301-8; PMID:17276346; http://dx.doi.org/10.1016/j. devcel.2006.11.008
11. Dumont J, Petri S, Pellegrin F, Terret ME, Bohnsack MT, Rassinier P, et al. A centriole-and RanGTPindependent spindle assembly pathway in meiosis I of vertebrate oocytes. J Cell Biol 2007; 176:295-305; PMID:17261848; http://dx.doi.org/10.1083/jcb.200605199
12. Hao Y, Macara IG. Regulation of chromatin binding by a conformational switch in the tail of the Ran exchange factor RCC1. J Cell Biol 2008; 182:827-36; PMID:18762580; http://dx.doi.org/10.1083/jcb.200803110
13. Yi K, Unruh JR, Deng M, Slaughter BD, Rubinstein B, Li R. Dynamic maintenance of asymmetric meiotic spindle position through Arp2/3-complex-driven cytoplasmic streaming in mouse oocytes. Nat Cell Biol 2011; 13:1252-8; PMID:21874009; http://dx.doi.org/10.1038/ncb2320
14. Yi K, Li R. Actin cytoskeleton in cell polarity and asymmetric division during mouse oocyte maturation. Cytoskeleton (Hoboken) 2012; 69:727-37; PMID:22753278; http://dx.doi.org/10.1002/cm.21048
15. Yi K, Rubinstein B, Unruh JR, Guo F, Slaughter BD, Li R. Sequential actin-based pushing forces drive meiosis I chromosome migration and symmetry breaking in oocytes. J Cell Biol 2013; 200:567-76; PMID:23439682; http://dx.doi.org/10.1083/jcb.201211068
16. Dehapiot B, Carrière V, Carroll J, Halet G. Polarized Cdc42 activation promotes polar body protrusion and asymmetric division in mouse oocytes. Dev Biol 2013; 377:202-12; PMID:23384564; http://dx.doi. org/10.1016/j.ydbio.2013.01.029
17. Condeelis J. Life at the leading edge: the formation of cell protrusions. Annu Rev Cell Biol 1993; 9:411-44; PMID:8280467; http://dx.doi.org/10.1146/ annurev. cb.09.110193.002211
18. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112:453-65; PMID:12600310; http://dx.doi. org/10.1016/S0092-8674(03)00120-X
19. Halet G, Carroll J. Rac activity is polarized and regulates meiotic spindle stability and anchoring in mammalian oocytes. Dev Cell 2007; 12:309-17; PMID:17276347; http://dx.doi.org/10.1016/j.devcel. 2006.12.010
20. Yanagimachi R. Sperm-egg association in animals. Curr Top Dev Biol 1978; 12:83-105; PMID:352627; http://dx.doi.org/10.1016/S0070-2153(08)60594-3
21. Runge KE, Evans JE, He ZY, Gupta S, McDonald KL, Stahlberg H, et al. Oocyte CD9 is enriched on the microvillar membrane and required for normal microvillar shape and distribution. Dev Biol 2007; 304:317-25; PMID:17239847; http://dx.doi. org/10.1016/j.ydbio.2006.12.041
22. Jégou A, Ziyyat A, Barraud-Lange V, Perez E, Wolf JP, Pincet F, et al. CD9 tetraspanin generates fusion competent sites on the egg membrane for mammalian fertilization. Proc Natl Acad Sci USA 2011; 108:10946-51; PMID:21690351; http://dx.doi. org/10.1073/pnas.1017400108
23. Luo J, McGinnis LK, Kinsey WH. Fyn kinase activity is required for normal organization and functional polarity of the mouse oocyte cortex. Mol Reprod Dev 2009; 76:819-31; PMID:19363790; http://dx.doi. org/10.1002/mrd.21034
24. Yonemura S, Tsukita S, Tsukita S. Direct involvement of ezrin/radixin/moesin (ERM)-binding membrane proteins in the organization of microvilli in collaboration with activated ERM proteins. J Cell Biol 1999; 145:1497-509; PMID:10385528; http://dx.doi.org/10.1083/jcb.145.7.1497
25. Fehon RG, McClatchey AI, Bretscher A. Organizing the cell cortex: the role of ERM proteins. Nat Rev Mol Cell Biol 2010; 11:276-87; PMID:20308985; http://dx.doi.org/10.1038/nrm2866
26. Fievet BT, Gautreau A, Roy C, Del Maestro L, Mangeat P, Louvard D, et al. Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J Cell Biol 2004; 164:653-9; PMID:14993232; http://dx.doi. org/10.1083/jcb.200307032
27. Louvet S, Aghion J, Santa-Maria A, Mangeat P, Maro B. Ezrin becomes restricted to outer cells following asymmetrical division in the preimplantation mouse embryo. Dev Biol 1996; 177:568-79; PMID:8806832; http://dx.doi.org/10. 1006/dbio.1996.0186
28. Larson SM, Lee HJ, Hung PH, Matthews LM, Robinson DN, Evans JP. Cortical mechanics and meiosis II completion in mammalian oocytes are mediated by myosin-II and Ezrin-Radixin-Moesin (ERM) proteins. Mol Biol Cell 2010; 21:3182-92; PMID:20660156; http://dx.doi.org/10.1091/mbc. E10-01-0066
29. Brown MJ, Nijhara R, Hallam JA, Gignac M, Yamada KM, Erlandsen SL, et al. Chemokine stimulation of human peripheral blood T lymphocytes induces rapid dephosphorylation of ERM proteins, which facilitates loss of microvilli and polarization. Blood 2003; 102:3890-9; PMID:12907449; http://dx.doi.org/10.1182/ blood-2002-12-3807
30. Chen J, Cohn JA, Mandel LJ. Dephosphorylation of ezrin as an early event in renal microvillar breakdown and anoxic injury. Proc Natl Acad Sci USA 1995; 92:7495-9; PMID:7638219; http://dx.doi. org/10.1073/pnas.92.16.7495
31. Kondo T, Takeuchi K, Doi Y, Yonemura S, Nagata S, Tsukita S. ERM (ezrin/radixin/moesin)-based molecular mechanism of microvillar breakdown at an early stage of apoptosis. J Cell Biol 1997; 139:749-58; PMID:9348291; http://dx.doi.org/10.1083/jcb.139.3.749
32. Nijhara R, van Hennik PB, Gignac ML, Kruhlak MJ, Hordijk PL, Delon J, et al. Rac1 mediates collapse of microvilli on chemokine-activated T lymphocytes. J Immunol 2004; 173:4985-93; PMID:15470041
33. Faure S, Salazar-Fontana LI, Semichon M, Tybulewicz VLJ, Bismuth G, Trautmann A, et al. ERM proteins regulate cytoskeleton relaxation promoting T cell-APC conjugation. Nat Immunol 2004; 5:272-9; PMID:14758359; http://dx.doi.org/10.1038/ni1039
34. Rossy J, Gutjahr MC, Blaser N, Schlicht D, Niggli V. Ezrin/moesin in motile Walker 256 carcinosarcoma cells: signal-dependent relocalization and role in migration. Exp Cell Res 2007; 313:1106-20; PMID:17292355; http://dx.doi.org/10.1016/j. yexcr.2006.12.023
35. Cernuda-Morollón E, Millán J, Shipman M, Marelli-Berg FM, Ridley AJ. Rac activation by the T-cell receptor inhibits T cell migration. PLoS ONE 2010; 5:e12393; PMID:20811629; http://dx.doi. org/10.1371/journal.pone. 0012393
36. Hao JJ, Liu Y, Kruhlak M, Debell KE, Rellahan BL, Shaw S. Phospholipase C-mediated hydrolysis of PIP2 releases ERM proteins from lymphocyte membrane. J Cell Biol 2009; 184:451-62; PMID:19204146; http://dx.doi.org/10.1083/jcb. 200807047
37. Halet G, Tunwell R, Balla T, Swann K, Carroll J. The dynamics of plasma membrane PtdIns(4,5) P(2) at fertilization of mouse eggs. J Cell Sci 2002; 115:2139-49; PMID:11973355
38. Roubinet C, Decelle B, Chicanne G, Dorn JF, Payrastre B, Payre F, et al. Molecular networks linked by Moesin drive remodeling of the cell cortex during mitosis. J Cell Biol 2011; 195:99-112; PMID:21969469; http://dx.doi.org/10.1083/ jcb.201106048
39. Takahashi K, Sasaki T, Mammoto A, Takaishi K, Kameyama T, Tsukita S, et al. Direct interaction of the Rho GDP dissociation inhibitor with ezrin/radixin/moesin initiates the activation of the Rho small G protein. J Biol Chem 1997; 272:23371-5; PMID:9287351; http://dx.doi.org/10.1074/jbc.272.37. 23371
40. Hamada K, Seto A, Shimizu T, Matsui T, Takai Y, Tsukita S, et al. Crystallization and preliminary crystallographic studies of RhoGDI in complex with the radixin FERM domain. Acta Crystallogr D Biol Crystallogr 2001; 57:889-90; PMID:11375519; http://dx.doi.org/10.1107/S090744490100556X
41. Sander EE, ten Klooster JP, van Delft S, van der Kammen RA, Collard JG. Rac downregulates Rho activity: reciprocal balance between both GTPases determines cellular morphology and migratory behavior. J Cell Biol 1999; 147:1009-22; PMID:10579721; http://dx.doi.org/10.1083/jcb.147.5.1009
42. Etienne-Manneville S, Hall A. Rho GTPases in cell biology. Nature 2002; 420:629-35; PMID:12478284; http://dx.doi.org/10.1038/nature01148
43. Vaughan EM, Miller AL, Yu HY, Bement WM. Control of local Rho GTPase crosstalk by Abr. Curr Biol 2011; 21:270-7; PMID:21295482; http://dx.doi.org/10. 1016/j.cub.2011.01.014
44. Valderrama F, Thevapala S, Ridley AJ. Radixin regulates cell migration and cell-cell adhesion through Rac1. J Cell Sci 2012; 125:3310-9; PMID:22467863; http://dx.doi.org/10.1242/jcs.094383
45. Raucher D, Sheetz MP. Cell spreading and lamellipodial extension rate is regulated by membrane tension. J Cell Biol 2000; 148:127-36; PMID:10629223; http://dx.doi.org/10.1083/jcb.148.1.127
46. Liu Y, Belkina NV, Park C, Nambiar R, Loughhead SM, Patino-Lopez G, et al. Constitutively active ezrin increases membrane tension, slows migration, and impedes endothelial transmigration of lymphocytes in vivo in mice. Blood 2012; 119:445-53; PMID:22106344; http://dx.doi.org/10.1182/blood-2011-07-368860
47. Kunda P, Rodrigues NTL, Moeendarbary E, Liu T, Ivetic A, Charras G, et al. PP1-mediated moesin dephosphorylation couples polar relaxation to mitotic exit. Curr Biol 2012; 22:231-6; PMID:22209527; http://dx.doi.org/10.1016/j.cub. 2011.12.016