Actin microfilaments guide the polarized transport of nuclear pore complexes and the cytoplasmic dispersal of Vasa mRNA during GVBD in the ascidian Halocynthia roretzi

Developmental Biology

Volumn 330, Issue 2, 2009, Pages 377-388

  Prodon, François ^a   Hanawa, Koichi ^b   Nishida, Hiroki ^b  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Actin microfilaments; Ascidian; GVBD; Nuclear pore; Oocyte; Polarity; Vasa mRNA

Indexed keywords

MESSENGER RNA; NUP153 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; ASCIDIACEA; CELL MATURATION; CENTROSOME; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FEMALE; FLUORESCENCE; GERMINAL VESICLE; HALOCYNTHIA RORETZI; MICROFILAMENT; NONHUMAN; NUCLEAR PORE COMPLEX; OOCYTE; PRIORITY JOURNAL;

ASCIDIA; HALOCYNTHIA RORETZI;

EID: 67349151774     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.04.006     Document Type: Article

References (49)

1. Bates W.R., and Nishida H. Developmental roles of nuclear complex factors released during oocyte maturation in the ascidians Halocynthia roretzi and Boltenia villosa. Zoolog. Sci. 15 (1998) 69-76
2. Bettinger B.T., Gilbert D.M., and Amberg D.C. Actin up in the nucleus. Nat. Rev. Mol. Cell. Biol. 5 5 (2004) 410-415 Review
3. Brown F.D., and Swalla B.J. Vasa expression in a colonial ascidian, Botrylloides violaceus. Evol. Dev. 9 2 (2007) 165-177
4. Conklin E.G. The organization and cell lineage of the ascidian egg. J. Acad. Nat. Sci. (Phila) 13 (1905) 1-119
5. Doree M., and Hunt T. From Cdc2 to Cdk1: when did the cell cycle kinase join its cyclin partner?. J. Cell. Sci. 115 (2002) 2461-2464
6. Fujimura M., and Takamura K. Characterization of an ascidian DEAD-box gene, Ci-DEAD1: specific expression in the germ cells and its mRNA localization in the posterior-most blastomeres in early embryos. Dev. Genes Evol. 210 (2000) 64-72
7. Gallo C.M., Munro E., Rasoloson D., Merritt C., and Seydoux G. Processing bodies and germ granules are distinct RNA granules that interact in C. elegans embryos. Dev. Biol. 16 (2008) [Electronic publication ahead of print]
8. Gohla A., Birkenfeld J., and Bokoch G.M. Chronophin, a novel HAD-type serine protein phosphatase, regulates cofilin-dependent actin dynamics. Nat. Cell Biol. 7 1 (2005) 21-29
9. Hibino T., Nishikata T., and Nishida H. Centrosome-attracting body: a novel structure closely related to unequal cleavages in the ascidian embryo. Dev. Growth Differ. 40 1 (1998) 85-95
10. Holaska J.M., Kowalski A.K., and Wilson K.L. Emerin caps the pointed end of actin filaments: evidence for an actin cortical network at the nuclear inner membrane. PLoS Biol. 2 9 (2004) E231
11. Iseto T., and Nishida H. Ultrastructural studies on the centrosome-attracting body: electron-dense matrix and its role in unequal cleavages in ascidian embryos. Dev. Growth Differ. 41 5 (1999) 601-609
12. Houston D.W., and King M.L. Germ plasm and molecular determinants of germ cell fate. Curr. Top Dev. Biol. 50 (2000) 155-181 Review
13. Kiseleva E., Drummond S.P., Goldberg M.W., Rutherford S.A., Allen T.D., and Wilson K.L. Actin- and protein-4.1-containing filaments link nuclear pore complexes to subnuclear organelles in Xenopus oocyte nuclei. J. Cell. Sci. 117 (2004) 2481-2490
14. Knaut H., Pelegri F., Bohmann K., Schwarz H., and Nüsslein-Volhard C. Zebrafish vasa RNA but not its protein is a component of the germ plasm and segregates asymmetrically before germline specification. J. Cell Biol. 149 4 (2000) 875-888
15. Kosaka K., Kawakami K., Sakamoto H., and Inoue K. Spatiotemporal localization of germ plasm RNAs during zebrafish oogenesis. Mech. Dev. 124 4 (2007) 279-289
16. Kumano G., and Nishida H. Ascidian embryonic development: an emerging model system for the study of cell fate specification in chordates. Dev. Dyn. 236 7 (2007) 1732-1747 Review
17. Leader B., Lim H., Carabatsos M.J., Harrington A., Ecsedy J., Pellman D., Maas R., and Leder P. Formin-2, polyploidy, hypofertility and positioning of the meiotic spindle in mouse oocytes. Nat. Cell Biol. 4 (2002) 921-928
18. Lénárt P., Bacher C.P., Daigle N., Hand A.R., Eils R., Terasaki M., and Ellenberg J. A contractile nuclear actin network drives chromosome congression in oocytes. Nature 436 (2005) 812-818
19. Libotte T., Zaim H., Abraham S., Padmakumar V.C., Schneider M., Lu W., Munck M., Hutchison C., Wehnert M., Fahrenkrog B., Sauder U., Aebi U., Noegel A.A., and Karakesisoglou I. Lamin A/C-dependent localization of Nesprin-2, a giant scaffolder at the nuclear envelope. Mol. Biol. Cell. 16 7 (2005) 3411-3424
20. Lohka M.J., Hayes M.K., and Maller J.L. Purification of maturation promoting factor, an intracellular regulator of early mitotic events. PNAS 85 (1988) 3009-3013
21. Machado R.J., Moore W., Hames R., Houliston E., Chang P., King M.L., and Woodland H.R. Xenopus Xpat protein is a major component of germ plasm and may function in its organisation and positioning. Dev. Biol. 287 (2005) 289-300
22. Margalit A., Vlcek S., Gruenbaum Y., and Foisner R. Breaking and making of the nuclear envelope. J. Cell. Biochem. 95 3 (2005) 454-465 Review
23. Masui Y., and Markert C.L. Cytoplasmic control of nuclear behavior during meiotic maturation in frog oocytes. J. Exp. Zool. 177 (1971) 129-146
24. Miyazaki A., Kato K.H., and Nemoto S. Role of microtubules and centrosomes in the eccentric relocation of the germinal vesicle upon meiosis reinitiation in sea-cucumber oocytes. Dev. Biol. 280 (2005) 237-247
25. Münter S., Enninga J., Vazquez-Martinez R., Delbarre E., David-Watine B., Nehrbass U., and Shorte S.L. Actin polymerisation at the cytoplasmic face of eukaryotic nuclei. BMC Cell Biol. 23 7 (2006) 23
26. Nakamura Y., Makabe K.W., and Nishida H. Localization and expression pattern of type I postplasmic mRNAs in embryos of the ascidian Halocynthia roretzi. Gene Expr. Patterns 3 (2003) 71-75
27. Nakamura Y., Makabe K.W., and Nishida H. POPK-1/Sad-1 kinase is required for the proper translocation of maternal mRNAs and putative germ plasm at the posterior pole of the ascidian embryo. Development 21 (2005) 4731-4742
28. Nishida H., and Sawada K. macho-1 encodes a localized mRNA in ascidian eggs that specifies muscle fate during embryogenesis. Nature 409 (2001) 724-729
29. Nishikata T., Hibino T., and Nishida H. The centrosome-attracting body, microtubule system, and posterior egg cytoplasm are involved in positioning of cleavage planes in the ascidian embryo. Dev. Biol. 209 (1999) 72-85
30. Numakunai T., and Hoshino Z. Periodic spawning of three types of ascidian, alocynthia roretzi (Drasche), under continuous light conditions. J. Exp. Zool. 212 (1980) 381-387
31. Patalano S., Pruliere G., Prodon F., Paix A., Dru P., Sardet C., and Chenevert J. The aPKC-PAR-6-PAR-3 cell polarity complex localizes to the centrosome attracting body, a macroscopic cortical structure responsible for asymmetric divisions in the early ascidian embryo. J. Cell. Sci. 119 (2006) 1592-1603
32. Pitt J.N., Schisa J.A., and Priess J.R. P granules in the germ cells of Caenorhabditis elegans adults are associated with clusters of nuclear pores and contain RNA. Dev. Biol. 219 2 (2000) 315-333
33. Prodon F., Dru P., Roegiers F., and Sardet C. Polarity of the ascidian egg cortex and relocalization of cER and mRNAs in the early embryo. J. Cell. Sci. 118 (2005) 2393-2404
34. Prodon F., Chenevert J., and Sardet C. Establishment of animal-vegetal polarity during maturation in ascidian oocytes. Dev. Biol. 290 (2006) 297-311
35. Prodon F., Yamada L., Shirae-Kurabayashi M., Nakamura Y., and Sasakura Y. Postplasmic/PEM RNAs: a class of localized maternal mRNAs with multiple roles in cell polarity and development in ascidian embryos. Dev. Dyn. 236 7 (2007) 1698-1715 Review
36. Prodon F., Sardet C., and Nishida H. Cortical and cytoplasmic flows driven by actin microfilaments polarize the cortical ER-mRNA domain along the a-v axis in ascidian oocytes. Dev. Biol. 313 2 (2008) 682-699
37. Riparbelli M.G., Gigliotti S., and Callaini G. The Drosophila nucleoporin gene nup154 is required for correct microfilament dynamics and cell death during oogenesis. Cell Motil. Cytoskelet. 64 8 (2007) 590-604
38. Romero S., Le Clainche C., Didry D., Egile C., Pantaloni D., and Carlier M.F. Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119 (2004) 419-429
39. Sardet C., Speksnijder J., Terasaki M., and Chang P. Polarity of the ascidian egg cortex before fertilization. Development 115 1 (1992) 221-237
40. Sardet C., Nishida H., Prodon F., and Sawada K. Maternal mRNAs of PEM and macho 1, the ascidian muscle determinant, associate and move with a rough endoplasmic reticulum network in the egg cortex. Development 130 23 (2003) 5839-5849
41. Sasakura Y., Ogasawara M., and Makabe K.W. Two pathways of maternal RNA localization at the posterior-vegetal cytoplasm in early ascidian embryos. Dev. Biol. 220 (2000) 365-378
42. Schetter A., Askjaer P., Piano F., Mattaj I., and Kemphues K. Nucleoporins NPP-1, NPP-3, NPP-4, NPP-11 and NPP-13 are required for proper spindle orientation in C. elegans. Dev. Biol. 289 2 (2006) 360-371
43. Shirae-Kurabayashi M., Nishikata T., Takamura K., Tanaka K.J., Nakamoto C., and Nakamura A. Dynamic redistribution of vasa homolog and exclusion of somatic cell determinants during germ cell specification in Ciona intestinalis. Development 133 14 (2006) 2683-2693
44. Sun Q.Y., and Schatten H. Regulation of dynamic events by microfilaments during oocyte maturation and fertilization. Reproduction 131 (2006) 193-205
45. Takamura K., Fujimura M., and Yamaguchi Y. Primordial germ cells originate from the endodermal strand cells in the ascidian Ciona intestinalis. Dev. Genes Evol. 212 (2002) 11-18
46. Vartiainen M.K., and Machesky L.M. The WASP-Arp2/3 pathway: genetic insights. Curr. Opin. Cell Biol. 16 2 (2004) 174-181 Review
47. Yamada L. Embryonic expression profiles and conserved localization mechanisms of pem/postplasmic mRNAs of two species of ascidian, Ciona intestinalis and Ciona savignyi. Dev. Biol. 296 (2006) 524-536
48. Zhou Y., and King M.L. Sending RNAs into the future: RNA localization and germ cell fate. IUBMB Life 56 1 (2004) 19-27 Review
49. Zigmond S.H. Beginning and ending an actin filament: control at the barbed end. Curr. Top Dev. Biol. 63 (2004) 145-188 Review