RhoA regulates initiation of invagination, but not convergent extension, during sea urchin gastrulation

Developmental Biology

Volumn 292, Issue 1, 2006, Pages 213-225

  Beane, Wendy S ^a   Gross, Jeffrey M ^b   McClay, David R ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

Brachyury; Convergent extension; Gastrulation; Invagination; RhoA; Sea urchin

Indexed keywords

RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; BRACHYURY PROTEIN; FETOPROTEIN; T BOX TRANSCRIPTION FACTOR;

ARTICLE; EXTRACELLULAR MATRIX; GASTRULATION; INTESTINE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; SEA URCHIN; ANIMAL; CYTOSKELETON; DRUG ANTAGONISM; GASTRULA; GENETICS; LYTECHINUS; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; PHYSIOLOGY; PRENATAL DEVELOPMENT; SEQUENCE ANALYSIS;

ECHINOIDEA; VERTEBRATA;

ANIMALS; CLONING, MOLECULAR; CYTOSKELETON; EXTRACELLULAR MATRIX; FETAL PROTEINS; GASTRULA; LYTECHINUS; MOLECULAR SEQUENCE DATA; RHOA GTP-BINDING PROTEIN; SEQUENCE ANALYSIS, PROTEIN; T-BOX DOMAIN PROTEINS;

EID: 33646444861     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2005.12.031     Document Type: Article

References (70)

1. Adamson P., Paterson H.F., and Hall A. Intracellular localization of the P21rho proteins. J. Cell Biol. 119 (1992) 617-627
2. Aktories K., Wilde C., and Vogelsgesang M. Rho-modifying C3-like ADP-ribosyltransferases. Rev. Physiol. Biochem. Pharmacol. 152 (2004) 1-22
3. Bakkers J., Kramer C., Pothof J., Quaedvlieg N.E., Spaink H.P., and Hammerschmidt M. Has2 is required upstream of Rac1 to govern dorsal migration of lateral cells during zebrafish gastrulation. Development 131 (2004) 525-537
4. Berg L.K., Chen S.W., and Wessel G.M. An extracellular matrix molecule that is selectively expressed during development is important for gastrulation in the sea urchin embryo. Development 122 (1996) 703-713
5. Bishop A.L., and Hall A. Rho GTPases and their effector proteins. Biochem. J. 348 Pt. 2 (2000) 241-255
6. Burridge K., and Wennerberg K. Rho and Rac take center stage. Cell 116 (2004) 167-179
7. Castellano L.E., Martinez-Cadena G., Lopez-Godinez J., Obregon A., and Garcia-Soto J. Subcellular localization of the GTP-binding protein Rho in the sea urchin sperm. Eur. J. Cell Biol. 74 (1997) 329-335
8. Covian-Nares F., Martinez-Cadena G., Lopez-Godinez J., Voronina E., Wessel G.M., and Garcia-Soto J. A Rho-signaling pathway mediates cortical granule translocation in the sea urchin oocyte. Mech. Dev. 121 (2004) 225-235
9. Cox K.H., Angerer L.M., Lee J.J., Davidson E.H., and Angerer R.C. Cell lineage-specific programs of expression of multiple actin genes during sea urchin embryogenesis. J. Mol. Biol. 188 (1986) 159-172
10. Croce J., Lhomond G., and Gache C. Expression pattern of Brachyury in the embryo of the sea urchin Paracentrotus lividus. Dev. Genes Evol. 211 (2001) 617-619
11. Croce, J., Duloquin, L., Lhomond, G., McClay, D.R., Gache, C., in press. Frizzled5/8 is required in secondary mesenchyme cells to initiate archenteron invagination during sea urchin development. Development.
12. Davidson E.H., Rast J.P., Oliveri P., Ransick A., Calestani C., Yuh C.H., Minokawa T., Amore G., Hinman V., Arenas-Mena C., Otim O., Brown C.T., Livi C.B., Lee P.Y., Revilla R., Rust A.G., Pan Z., Schilstra M.J., Clarke P.J., Arnone M.I., Rowen L., Cameron R.A., McClay D.R., Hood L., and Bolouri H. A genomic regulatory network for development. Science 295 (2002) 1669-1678
13. Davidson E.H., Rast J.P., Oliveri P., Ransick A., Calestani C., Yuh C.H., Minokawa T., Amore G., Hinman V., Arenas-Mena C., Otim O., Brown C.T., Livi C.B., Lee P.Y., Revilla R., Schilstra M.J., Clarke P.J., Rust A.G., Pan Z., Arnone M.I., Rowen L., Cameron R.A., McClay D.R., Hood L., and Bolouri H. A provisional regulatory gene network for specification of endomesoderm in the sea urchin embryo. Dev. Biol. 246 (2002) 162-190
14. Davies S.P., Reddy H., Caivano M., and Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351 (2000) 95-105
15. Etienne-Manneville S., and Hall A. Rho GTPases in cell biology. Nature 420 (2002) 629-635
16. Ettensohn C.A. Gastrulation in the sea urchin embryo is accompanied by the rearrangement of invaginating epithelial cells. Dev. Biol. 112 (1985) 383-390
17. Feig L.A. Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat. Cell Biol. 1 (1999) E25-E27
18. Fleming I.N., Elliott C.M., and Exton J.H. Differential translocation of rho family GTPases by lysophosphatidic acid, endothelin-1, and platelet-derived growth factor. J. Biol. Chem. 271 (1996) 33067-33073
19. Glotzer M. The molecular requirements for cytokinesis. Science 307 (2005) 1735-1739
20. Gross J.M., and McClay D.R. The role of Brachyury (T) during gastrulation movements in the sea urchin Lytechinus variegatus. Dev. Biol. 239 (2001) 132-147
21. Gross J.M., Peterson R.E., Wu S.Y., and McClay D.R. LvTbx2/3: a T-box family transcription factor involved in formation of the oral/aboral axis of the sea urchin embryo. Development 130 (2003) 1989-1999
22. Habas R., Kato Y., and He X. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107 (2001) 843-854
23. Habas R., Dawid I.B., and He X. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17 (2003) 295-309
24. Hacker U., and Perrimon N. DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev. 12 (1998) 274-284
25. Hardin J. Local shifts in position and polarized motility drive cell rearrangement during sea urchin gastrulation. Dev. Biol. 136 (1989) 430-445
26. Hardin J. The cellular basis of sea urchin gastrulation. Curr. Top Dev. Biol. 33 (1996) 159-262
27. Hardin J., and Cheng L. The mechanisms and mechanics of archenteron elongation during sea urchin gastrulation. Dev. Biol. 115 (1986) 490-501
28. Hardin J., and McClay D.R. Target recognition by the archenteron during sea urchin gastrulation. Dev. Biol. 142 (1990) 86-102
29. Hardin J., Coffman J.A., Black S.D., and McClay D.R. Commitment along the dorsoventral axis of the sea urchin embryo is altered in response to NiCl2. Development 116 (1992) 671-685
30. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., and Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405 (2000) 76-81
31. Keller R., Davidson L.A., and Shook D.R. How we are shaped: the biomechanics of gastrulation. Differentiation 71 (2003) 171-205
32. Kim G.H., and Han J.K. JNK and ROKalpha function in the noncanonical Wnt/RhoA signaling pathway to regulate Xenopus convergent extension movements. Dev. Dyn. 232 (2005) 958-968
33. Kimberly E.L., and Hardin J. Bottle cells are required for the initiation of primary invagination in the sea urchin embryo. Dev. Biol. 204 (1998) 235-250
34. Kominami T., and Takata H. Gastrulation in the sea urchin embryo: a model system for analyzing the morphogenesis of a monolayered epithelium. Dev. Growth Differ. 46 (2004) 309-326
35. Kranenburg O., Poland M., Gebbink M., Oomen L., and Moolenaar W.H. Dissociation of LPA-induced cytoskeletal contraction from stress fiber formation by differential localization of RhoA. J. Cell Sci. 110 Pt. 19 (1997) 2417-2427
36. Lai S.L., Chang C.N., Wang P.J., and Lee S.J. Rho mediates cytokinesis and epiboly via ROCK in zebrafish. Mol. Reprod. Dev. 71 (2005) 186-196
37. Lane M.C., Koehl M.A., Wilt F., and Keller R. A role for regulated secretion of apical extracellular matrix during epithelial invagination in the sea urchin. Development 117 (1993) 1049-1060
38. Lee J.J., Calzone F.J., Britten R.J., Angerer R.C., and Davidson E.H. Activation of sea urchin actin genes during embryogenesis. Measurement of transcript accumulation from five different genes in Strongylocentrotus purpuratus. J. Mol. Biol. 188 (1986) 173-183
39. Leptin M. Gastrulation movements: the logic and the nuts and bolts. Dev. Cell 8 (2005) 305-320
40. Logan C.Y., and McClay D.R. The allocation of early blastomeres to the ectoderm and endoderm is variable in the sea urchin embryo. Development 124 (1997) 2213-2223
41. Manser E. Small GTPases take the stage. Dev. Cell 3 (2002) 323-328
42. Manzo S., Martinez-Cadena G., Lopez-Godinez J., Pedraza-Reyes M., and Garcia-Soto J. A Rho GTPase controls the rate of protein synthesis in the sea urchin egg. Biochem. Biophys. Res. Commun. 310 (2003) 685-690
43. Marlow F., Topczewski J., Sepich D., and Solnica-Krezel L. Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12 (2002) 876-884
44. McClay D.R., Gross J.M., Range R., Peterson R.E., and Bradham C. Sea urchin gastrulation. In: Stern C.D. (Ed). Gastrulation: From Cells to Embryo (2004), Cold Spring Harbor Laboratory Press, New York 291-304
45. Miller R.N., Dalamagas D.G., Kingsley P.D., and Ettensohn C.A. Expression of S9 and actin CyIIa mRNAs reveals dorso-ventral polarity and mesodermal sublineages in the vegetal plate of the sea urchin embryo. Mech. Dev. 60 (1996) 3-12
46. Mlodzik M. Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation?. Trends Genet. 18 (2002) 564-571
47. Nakajima Y., and Burke R.D. The initial phase of gastrulation in sea urchins is accompanied by the formation of bottle cells. Dev. Biol. 179 (1996) 436-446
48. Nishimura Y., Nakano K., and Mabuchi I. Localization of Rho GTPase in sea urchin eggs. FEBS Lett. 441 (1998) 121-126
49. Nobes C.D., and Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81 (1995) 53-62
50. Range R.C., Venuti J.M., and McClay D.R. LvGroucho and nuclear beta-catenin functionally compete for Tcf binding to influence activation of the endomesoderm gene regulatory network in the sea urchin embryo. Dev. Biol. 279 (2005) 252-267
51. Rast J.P., Cameron R.A., Poustka A.J., and Davidson E.H. Brachyury target genes in the early sea urchin embryo isolated by differential macroarray screening. Dev. Biol. 246 (2002) 191-208
52. Ridley A.J. Rho family proteins: coordinating cell responses. Trends Cell Biol. 11 (2001) 471-477
53. Riento K., and Ridley A.J. Rocks: multifunctional kinases in cell behaviour. Nat. Rev., Mol. Cell Biol. 4 (2003) 446-456
54. Schatten G., Schatten H., Spector I., Cline C., Paweletz N., Simerly C., and Petzelt C. Latrunculin inhibits the microfilament-mediated processes during fertilization, cleavage and early development in sea urchins and mice. Exp. Cell Res. 166 (1986) 191-208
55. Schmitz A.A., Govek E.E., Bottner B., and Van Aelst L. Rho GTPases: signaling, migration, and invasion. Exp. Cell Res. 261 (2000) 1-12
56. Sekine A., Fujiwara M., and Narumiya S. Asparagine residue in the rho gene product is the modification site for botulinum ADP-ribosyltransferase. J. Biol. Chem. 264 (1989) 8602-8605
57. Sherwood D.R., and McClay D.R. LvNotch signaling mediates secondary mesenchyme specification in the sea urchin embryo. Development 126 (1999) 1703-1713
58. Sirotkin V., Seipel S., Krendel M., and Bonder E.M. Characterization of sea urchin unconventional myosins and analysis of their patterns of expression during early embryogenesis. Mol. Reprod. Dev. 57 (2000) 111-126
59. Solnica-Krezel L. Conserved patterns of cell movements during vertebrate gastrulation. Curr. Biol. 15 (2005) R213-R228
60. Tada M., and Smith J.C. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127 (2000) 2227-2238
61. Tada M., Concha M.L., and Heisenberg C.P. Non-canonical Wnt signalling and regulation of gastrulation movements. Semin. Cell Dev. Biol. 13 (2002) 251-260
62. Tahinci E., and Symes K. Distinct functions of Rho and Rac are required for convergent extension during Xenopus gastrulation. Dev. Biol. 259 (2003) 318-335
63. Wallingford J.B. Vertebrate gastrulation: polarity genes control the matrix. Curr. Biol. 15 (2005) R414-R416
64. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbacher U., Fraser S.E., and Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405 (2000) 81-85
65. Wallingford J.B., Fraser S.E., and Harland R.M. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2 (2002) 695-706
66. Wennerberg K., and Der C.J. Rho-family GTPases: it's not only Rac and Rho (and I like it). J. Cell Sci. 117 (2004) 1301-1312
67. Wikramanayake A.H., Peterson R., Chen J., Huang L., Bince J.M., McClay D.R., and Klein W.H. Nuclear beta-catenin-dependent Wnt8 signaling in vegetal cells of the early sea urchin embryo regulates gastrulation and differentiation of endoderm and mesodermal cell lineages. Genesis 39 (2004) 194-205
68. Wilde C., and Aktories K. The Rho-ADP-ribosylating C3 exoenzyme from Clostridium botulinum and related C3-like transferases. Toxicon 39 (2001) 1647-1660
69. Winter C.G., Wang B., Ballew A., Royou A., Karess R., Axelrod J.D., and Luo L. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105 (2001) 81-91
70. Zhu S., Liu L., Korzh V., Gong Z., and Low B.C. RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell Signal. 18 (2006) 359-372