The cell adhesion-associated protein Git2 regulates morphogenetic movements during zebrafish embryonic development

Developmental Biology

Volumn 349, Issue 2, 2011, Pages 225-237

  Yu, Jianxin A ^a   Foley, Fiona C ^a   Amack, Jeffrey D ^a   Turner, Christopher E ^a  

^a State University of New York Upstate Medical University: College of Medicine   (United States)

Author keywords

Blebbistatin; Epiboly; FAK; Gastrulation; Git2; Non muscle Myosin II; Paxillin; Zebrafish

Indexed keywords

BLEBBISTATIN; CELL ADHESION MOLECULE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; MYOSIN II; MYOSIN LIGHT CHAIN; PROTEIN GIT2; PROTEIN GIT2A; PROTEIN GIT2B; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; LOSS OF FUNCTION MUTATION; MICROSCOPY; MIGRATION INHIBITION; MORPHOGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; TIME LAPSE IMAGING; ZEBRA FISH;

DANIO RERIO;

EID: 78650801821     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2010.10.027     Document Type: Article

References (49)

1. Bahri S.M., Choy J.M., Manser E., Lim L., Yang X. The Drosophila homologue of Arf-GAP GIT1, dGIT, is required for proper muscle morphogenesis and guidance during embryogenesis. Dev. Biol. 2009, 325:15-23.
2. Bokoch G.M. Biology of the p21-activated kinases. Annu. Rev. Biochem. 2003, 72:743-781.
3. Brown M.C., Turner C.E. Paxillin: adapting to change. Physiol. Rev. 2004, 84:1315-1339.
4. Brown M.C., Cary L.A., Jamieson J.S., Cooper J.A., Turner C.E. Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol. Biol. Cell 2005, 16:4316-4328.
5. Cheng J.C., Miller A.L., Webb S.E. Organization and function of microfilaments during late epiboly in zebrafish embryos. Dev. Dyn. 2004, 231:313-323.
6. Concha M.L., Adams R.J. Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development 1998, 125:983-994.
7. Crawford B.D., Henry C.A., Clason T.A., Becker A.L., Hille M.B. Activity and distribution of paxillin, focal adhesion kinase, and cadherin indicate cooperative roles during zebrafish morphogenesis. Mol. Biol. Cell 2003, 14:3065-3081.
8. Frank S.R., Adelstein M.R., Hansen S.H. GIT2 represses Crk- and Rac1-regulated cell spreading and Cdc42-mediated focal adhesion turnover. EMBO J. 2006, 25:1848-1859.
9. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell Biol. 2005, 6:622-634.
10. Hagel M., George E.L., Kim A., Tamimi R., Opitz S.L., Turner C.E., Imamoto A., Thomas S.M. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 2002, 22:901-915.
11. Hammerschmidt M., Wedlich D. Regulated adhesion as a driving force of gastrulation movements. Development 2008, 135:3625-3641.
12. Heisenberg C.P., Solnica-Krezel L. Back and forth between cell fate specification and movement during vertebrate gastrulation. Curr. Opin. Genet. Dev. 2008, 18:311-316.
13. Holloway B.A., de la Torre Gomez, Canny S., Ye Y., Slusarski D.C., Freisinger C.M., Dosch R., Chou M.M., Wagner D.S., Mullins M.C. A novel role for MAPKAPK2 in morphogenesis during zebrafish development. PLoS Genet. 2009, 5:e1000413.
14. Hynes R.O. The extracellular matrix: not just pretty fibrils. Science 2009, 326:1216-1219.
15. Iioka H., Iemura S., Natsume T., Kinoshita N. Wnt signaling regulates paxillin ubiquitination essential for mesodermal cell motility. Nat. Cell Biol. 2007, 9:813-821.
16. Ilic D., Furuta Y., Kanazawa S., Takeda N., Sobue K., Nakatsuji N., Nomura S., Fujimoto J., Okada M., Yamamoto T. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 1995, 377:539-544.
17. Jopling C., den Hertog J. Fyn/Yes and non-canonical Wnt signaling converge on RhoA in vertebrate gastrulation cell movement. EMBO Rep. 2005, 6:426-431.
18. Kai M., Heisenberg C.P., Tada M. Sphingosine-1-phosphate receptors regulate individual cell behaviours underlying the directed migration of prechordal plate progenitor cells during zebrafish gastrulation. Development 2008, 135:3043-3051.
19. Kane D.A., McFarland K.N., Warga R.M. Mutations in half baked/E-cadherin block cell behaviors that are necessary for teleost epiboly. Development 2005, 132:1105-1116.
20. Keller R. Cell migration during gastrulation. Curr. Opin. Cell Biol. 2005, 17:533-541.
21. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310.
22. Köppen M., Fernández B.G., Carvalho L., Jacinto A., Heisenberg C.P. Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila. Development 2006, 133:2671-2681.
23. Köster I., Jungwirth M.S., Steinbeisser H. xGit2 and xRhoGAP 11A regulate convergent extension and tissue separation in Xenopus gastrulation. Dev. Biol. 2010, 344:26-35.
24. Kovacs M., Toth J., Hetenyi C., Malnasi-Csizmadia A., Sellers J.R. Mechanism of blebbistatin inhibition of myosin II. J. Biol. Chem. 2004, 279:35557-35563.
25. Krens S.F., He S., Lamers G.E., Meijer A.H., Bakkers J., Schmidt T., Spaink H.P., Snaar-Jagalska B.E. Distinct functions for ERK1 and ERK2 in cell migration processes during zebrafish gastrulation. Dev. Biol. 2008, 319:370-383.
26. Krieg M., Arboleda-Estudillo Y., Puech P.H., Kafer J., Graner F., Muller D.J., Heisenberg C.P. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 2008, 10:429-436.
27. Latimer A., Jessen J.R. Extracellular matrix assembly and organization during zebrafish gastrulation. Matrix Biol. 2010, 29:89-96.
28. Llense F., Martin-Blanco E. JNK signaling controls border cell cluster integrity and collective cell migration. Curr. Biol. 2008, 18:538-544.
29. Lucanic M., Cheng H. A Rac/Cdc42-independent GIT/PIX/PAK signaling pathway mediates cell migration in C. elegans. PLoS Genet. 2008, 4:e1000269.
30. Martin A.C. Pulsation and stabilization: contractile forces that underlie morphogenesis. Dev. Biol. 2010, 341:114-125.
31. Matsumura F., Ono S., Yamakita Y., Totsukawa G., Yamashiro S. Specific localization of serine 19 phosphorylated Myosin II during cell locomotion and mitosis of cultured cells. J. Cell Biol. 1998, 140:119-129.
32. Mazaki Y., Hashimoto S., Tsujimura T., Morishige M., Hashimoto A., Aritake A., Yamada A., Nam J.M., Kiyonari H., Nakao K., Sabe H. Neutrophil direction sensing and superoxide production linked by the GTPase-activating protein GIT2. Nat. Immunol. 2006, 7:724-731.
33. Montero J.A., Kilian B., Chan J., Bayliss P.E., Heisenberg C.P. Phosphoinositide 3-kinase is required for process outgrowth and cell polarization of gastrulating mesendodermal cells. Curr. Biol. 2003, 13:1279-1289.
34. Nguyen D.H., Catling A.D., Webb D.J., Sankovic M., Walker L.A., Somlyo A.V., Weber M.J., Gonias S.L. Myosin light chain kinase functions downstream of Ras/ERK to promote migration of urokinase-type plasminogen activator-stimulated cells in an integrin-selective manner. J. Cell Biol. 1999, 146:149-164.
35. Pang J., Hoefen R., Pryhuber G.S., Wang J., Yin G., White R.J., Xu X., O'Dell M.R., Mohan A., Michaloski H., Massett M.P., Yan C., Berk B.C. G-protein-coupled receptor kinase interacting protein-1 is required for pulmonary vascular development. Circulation 2009, 119:1524-1532.
36. Postel R., Vakeel P., Topczewski J., Knoll R., Bakkers J. Zebrafish integrin-linked kinase is required in skeletal muscles for strengthening the integrin-ECM adhesion complex. Dev. Biol. 2008, 318:92-101.
37. Ridley A.J., Schwartz M.A., Burridge K., Firtel R.A., Ginsberg M.H., Borisy G., Parsons J.T., Horwitz A.R. Cell migration: integrating signals from front to back. Science 2003, 302:1704-1709.
38. Sanders L.C., Matsumura F., Bokoch G.M., de Lanerolle P. Inhibition of myosin light chain kinase by p21-activated kinase. Science 1999, 283:2083-2085.
39. Schulte-Merker S., Hammerschmidt M., Beuchle D., Cho K.W., De Robertis E.M., Nüsslein-Volhard C. Expression of zebrafish goosecoid and no tail gene products in wild-type and mutant no tail embryos. Development 1994, 120:843-852.
40. Steinberg M.S. Differential adhesion in morphogenesis: a modern view. Curr. Opin. Genet. Dev. 2007, 17:281-286.
41. Turner C.E., Brown M.C., Perrotta J.A., Riedy M.C., Nikolopoulos S.N., McDonald A.R., Bagrodia S., Thomas S., Leventhal P.S. Paxillin LD4 motif binds PAK and PIX through a novel 95-kD ankyrin repeat, ARF-GAP protein: a role in cytoskeletal remodeling. J. Cell Biol. 1999, 145:851-863.
42. Vitale N., Patton W.A., Moss J., Vaughan M., Lefkowwitz R.J., Premont R.T. GIT proteins, a novel family of phosphatidylinositol 3, 4, 5-trisphosphate-stimulated GTPase-activating proteins for ARF6. J. Biol. Chem. 2000, 275:13901-13906.
43. Warga R.M., Kimmel C.B. Cell movements during epiboly and gastrulation in zebrafish. Development 1990, 108:569-580.
44. Weiser D.C., Pyati U.J., Kimelman D. Gravin regulates mesodermal cell behavior changes required for axis elongation during zebrafish gastrulation. Genes Dev. 2007, 21:1559-1571.
45. Weiser D.C., Row R.H., Kimelman D. Rho-regulated myosin phosphatase establishes the level of protrusive activity required for cell movements during zebrafish gastrulation. Development 2009, 136:2375-2384.
46. Westerfield M. The zebrafish book 2000, University of Oregon Press, Eugene OR.
47. Yin G., Zheng Q., Yan C., Berk B.C. GIT1 is a scaffold for ERK1/2 activation in focal adhesions. J. Biol. Chem. 2005, 280:27705-27712.
48. Yu J.A., Deakin N.O., Turner C.E. Paxillin-kinase-linker tyrosine phosphorylation regulates directional cell migration. Mol. Biol. Cell 2009, 20:4706-4719.
49. Zhang H., Webb D.J., Asmussen H., Niu S., Horwitz A.F. A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J. Neurosci. 2005, 25:3379-3388.