Rac1 is essential for basement membrane-dependent epiblast survival

Molecular and Cellular Biology

Volumn 30, Issue 14, 2010, Pages 3569-3581

  He, Xiaowen ^a   Liu, Jie ^a   Qi, Yanmei ^a   Brakebusch, Cord ^b   Chrostek Grashoff, Anna ^c   Edgar, David ^d   Yurchenco, Peter D ^a   Corbett, Siobhan A ^a   Lowry, Stephen F ^a   Graham, Alan M ^a   Han, Yaling ^e   Li, Shaohua ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF VIRGINIA   (United States)

^d UNIVERSITY OF LIVERPOOL   (United Kingdom)

^e SHENYANG NORTHERN HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CRK ASSOCIATED SUBSTRATE PROTEIN; INTEGRIN; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; RAC1 PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; BASEMENT MEMBRANE; CELL ADHESION; CELL INTERACTION; CELL SURVIVAL; ECTODERM; EMBRYONIC STEM CELL; ENZYME ACTIVATION; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; ANTIGENS, CD29; APOPTOSIS; BASEMENT MEMBRANE; CELL LINE; CELL SURVIVAL; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; EPITHELIUM; GERM LAYERS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; MICE; NEUROPEPTIDES; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-CRK; RAC GTP-BINDING PROTEINS; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

MURINAE;

EID: 77954376980     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01366-09     Document Type: Article

References (49)

1. Akhtar, N., and C. H. Streuli. 2006. Rac1 links integrin-mediated adhesion to the control of lactational differentiation in mammary epithelia. J. Cell Biol. 173:781-793. (Pubitemid 46165585)
2. Boudreau, N., C. J. Sympson, Z. Werb, and M. J. Bissell. 1995. Suppression of ICE and apoptosis in mammary epithelial cells by extracellular matrix. Science 267:891-893.
3. Brugnera, E., L. Haney, C. Grimsley, M. Lu, S. F. Walk, A. C. Tosello-Trampont, I. G. Macara, H. Madhani, G. R. Fink, and K. S. Ravichandran. 2002. Unconventional Rac-GEF activity is mediated through the Dock180-ELMO complex. Nat. Cell Biol. 4:574-582.
4. Cote, J. F., A. B. Motoyama, J. A. Bush, and K. Vuori. 2005. A novel and evolutionarily conserved PtdIns(3,4,5)P3-binding domain is necessary for DOCK180 signalling. Nat. Cell Biol. 7:797-807.
5. Cote, J. F., and K. Vuori. 2002. Identification of an evolutionarily conserved superfamily of DOCK180-related proteins with guanine nucleotide exchange activity. J. Cell Sci. 115:4901-4913.
6. Coucouvanis, E., and G. R. Martin. 1999. BMP signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development 126:535-546. (Pubitemid 29082040)
7. Coucouvanis, E., and G. R. Martin. 1995. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83:279-287.
8. del Pozo, M. A., L. S. Price, N. B. Alderson, X. D. Ren, and M. A. Schwartz. 2000. Adhesion to the extracellular matrix regulates the coupling of the small GTPase Rac to its effector PAK. EMBO J. 19:2008-2014.
9. Dolfi, F., M. Garcia-Guzman, M. Ojaniemi, H. Nakamura, M. Matsuda, and K. Vuori. 1998. The adaptor protein Crk connects multiple cellular stimuli to the JNK signaling pathway. Proc. Natl. Acad. Sci. U. S. A. 95:15394-15399.
10. Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature 420:629-635.
11. Farrelly, N., Y. J. Lee, J. Oliver, C. Dive, and C. H. Streuli. 1999. Extracellular matrix regulates apoptosis in mammary epithelium through a control on insulin signaling. J. Cell Biol. 144:1337-1348. (Pubitemid 29157309)
12. Fassler, R., M. Pfaff, J. Murphy, A. A. Noegel, S. Johansson, R. Timpl, and R. Albrecht. 1995. Lack of beta 1 integrin gene in embryonic stem cells affects morphology, adhesion, and migration but not integration into the inner cell mass of blastocysts. J. Cell Biol. 128:979-988.
13. Feller, S. M. 2001. Crk family adaptors-signalling complex formation and biological roles. Oncogene 20:6348-6371.
14. Fera, E., C. O'Neil, W. Lee, S. Li, and J. G. Pickering. 2004. Fibroblast growth factor-2 and remodeled type I collagen control membrane protrusion in human vascular smooth muscle cells: biphasic activation of Rac1. J. Biol. Chem. 279:35573-35582.
15. Franke, T. F., D. R. Kaplan, and L. C. Cantley. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88:435-437.
16. Gumienny, T. L., E. Brugnera, A. C. Tosello-Trampont, J. M. Kinchen, L. B. Haney, K. Nishiwaki, S. F. Walk, M. E. Nemergut, I. G. Macara, R. Francis, T. Schedl, Y. Qin, L. Van Aelst, M. O. Hengartner, and K. S. Ravichandran. 2001. CED-12/ELMO, a novel member of the CrkII/Dock180/Rac pathway, is required for phagocytosis and cell migration. Cell 107:27-41.
17. Halfter, W., M. Willem, and U. Mayer. 2005. Basement membrane-dependent survival of retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46:1000-1009.
18. Hasegawa, H., E. Kiyokawa, S. Tanaka, K. Nagashima, N. Gotoh, M. Shibuya, T. Kurata, and M. Matsuda. 1996. DOCK180, a major CRK-binding protein, alters cell morphology upon translocation to the cell membrane. Mol. Cell. Biol. 16:1770-1776.
19. Hernandez-Garcia, D., S. Castro-Obregon, S. Gomez-Lopez, C. Valencia, and L. Covarrubias. 2008. Cell death activation during cavitation of embryoid bodies is mediated by hydrogen peroxide. Exp. Cell Res. 314:2090-2099.
20. Ichiba, T., Y. Hashimoto, M. Nakaya, Y. Kuraishi, S. Tanaka, T. Kurata, N. Mochizuki, and M. Matsuda. 1999. Activation of C3G guanine nucleotide exchange factor for Rap1 by phosphorylation of tyrosine 504. J. Biol. Chem. 274:14376-14381.
21. Ichiba, T., Y. Kuraishi, O. Sakai, S. Nagata, J. Groffen, T. Kurata, S. Hattori, and M. Matsuda. 1997. Enhancement of guanine-nucleotide exchange activity of C3G for Rap1 by the expression of Crk, CrkL, and Grb2. J. Biol. Chem. 272:22215-22220.
22. Kiyokawa, E., Y. Hashimoto, S. Kobayashi, H. Sugimura, T. Kurata, and M. Matsuda. 1998. Activation of Rac1 by a Crk SH3-binding protein, DOCK180. Genes Dev. 12:3331-3336.
23. Kobayashi, S., T. Shirai, E. Kiyokawa, N. Mochizuki, M. Matsuda, and Y. Fukui. 2001. Membrane recruitment of DOCK180 by binding to PtdIns(3,4,5)P3. Biochem. J. 354:73-78.
24. Laurin, M., N. Fradet, A. Blangy, A. Hall, K. Vuori, and J. F. Cote. 2008. The atypical Rac activator Dock180 (Dock1) regulates myoblast fusion in vivo. Proc. Natl. Acad. Sci. U. S. A. 105:15446-15451.
25. Li, S., D. Edgar, R. Fassler, W. Wadsworth, and P. D. Yurchenco. 2003. The role of laminin in embryonic cell polarization and tissue organization. Dev. Cell 4:613-624.
26. Li, S., D. Harrison, S. Carbonetto, R. Fassler, N. Smyth, D. Edgar, and P. D. Yurchenco. 2002. Matrix assembly, regulation, and survival functions of laminin and its receptors in embryonic stem cell differentiation. J. Cell Biol. 157:1279-1290.
27. Li, S., and P. D. Yurchenco. 2006. Matrix assembly, cell polarization, and cell survival: analysis of peri-implantation development with cultured embryonic stem cells. Methods Mol. Biol. 329:113-125.
28. Liu, J., X. He, S. A. Corbett, S. F. Lowry, A. M. Graham, R. Fassler, and S. Li. 2009. Integrins are required for the differentiation of visceral endoderm. J. Cell Sci. 122:233-242.
29. Mailleux, A. A., M. Overholtzer, T. Schmelzle, P. Bouillet, A. Strasser, and J. S. Brugge. 2007. BIM regulates apoptosis during mammary ductal morphogenesis, and its absence reveals alternative cell death mechanisms. Dev. Cell 12:221-234.
30. Matsuda, M., S. Ota, R. Tanimura, H. Nakamura, K. Matuoka, T. Takenawa, K. Nagashima, and T. Kurata. 1996. Interaction between the aminoterminal SH3 domain of CRK and its natural target proteins. J. Biol. Chem. 271:14468-14472.
31. Meller, N., M. Irani-Tehrani, W. B. Kiosses, M. A. Del Pozo, and M. A. Schwartz. 2002. Zizimin1, a novel Cdc42 activator, reveals a new GEF domain for Rho proteins. Nat. Cell Biol. 4:639-647.
32. Murray, P., and D. Edgar. 2000. Regulation of programmed cell death by basement membranes in embryonic development. J. Cell Biol. 150:1215-1221.
33. Nagashima, K., A. Endo, H. Ogita, A. Kawana, A. Yamagishi, A. Kitabatake, M. Matsuda, and N. Mochizuki. 2002. Adaptor protein Crk is required for ephrin-B1-induced membrane ruffling and focal complex assembly of human aortic endothelial cells. Mol. Biol. Cell 13:4231-4242.
34. Nguyen, N. M., D. G. Kelley, J. A. Schlueter, M. J. Meyer, R. M. Senior, and J. H. Miner. 2005. Epithelial laminin alpha5 is necessary for distal epithelial cell maturation, VEGF production, and alveolization in the developing murine lung. Dev. Biol. 282:111-125.
35. O'Brien, L. E., T. S. Jou, A. L. Pollack, Q. Zhang, S. H. Hansen, P. Yurchenco, and K. E. Mostov. 2001. Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly. Nat. Cell Biol. 3:831-838.
36. Pullan, S., J. Wilson, A. Metcalfe, G. M. Edwards, N. Goberdhan, J. Tilly, J. A. Hickman, C. Dive, and C. H. Streuli. 1996. Requirement of basement membrane for the suppression of programmed cell death in mammary epithelium. J. Cell Sci. 109:631-642.
37. Ramaswamy, S., N. Nakamura, F. Vazquez, D. B. Batt, S. Perera, T. M. Roberts, and W. R. Sellers. 1999. Regulation of G1 progression by the PTEN tumor suppressor protein is linked to inhibition of the phosphatidylinositol 3-kinase/Akt pathway. Proc. Natl. Acad. Sci. U. S. A. 96:2110-2115.
38. Reddien, P. W., and H. R. Horvitz. 2000. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat. Cell Biol. 2:131-136.
39. Schmidt, A., and A. Hall. 2002. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16:1587-1609.
40. Segal, N., F. Andriani, L. Pfeiffer, P. Kamath, N. Lin, K. Satyamurthy, C. Egles, and J. A. Garlick. 2008. The basement membrane microenvironment directs the normalization and survival of bioengineered human skin equivalents. Matrix Biol. 27:163-170.
41. Sher, I., S. Zisman-Rozen, L. Eliahu, J. M. Whitelock, N. Maas-Szabowski, Y. Yamada, D. Breitkreutz, N. E. Fusenig, E. Arikawa-Hirasawa, R. V. Iozzo, R. Bergman, and D. Ron. 2006. Targeting perlecan in human keratinocytes reveals novel roles for perlecan in epidermal formation. J. Biol. Chem. 281:5178-5187.
42. Smyth, N., H. S. Vatansever, P. Murray, M. Meyer, C. Frie, M. Paulsson, and D. Edgar. 1999. Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J. Cell Biol. 144:151-160.
43. Sugihara, K., N. Nakatsuji, K. Nakamura, K. Nakao, R. Hashimoto, H. Otani, H. Sakagami, H. Kondo, S. Nozawa, A. Aiba, and M. Katsuki. 1998. Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17:3427-3433.
44. Vanhaesebroeck, B., and D. R. Alessi. 2000. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346:561-576.
45. Wagner, E. F., and A. R. Nebreda. 2009. Signal integration by JNK and p38 MAPK pathways in cancer development. Nat. Rev. Cancer 9:537-549.
46. Wu, X., S. Li, A. Chrostek-Grashoff, A. Czuchra, H. Meyer, P. D. Yurchenco, and C. Brakebusch. 2007. Cdc42 is crucial for the establishment of epithelial polarity during early mammalian development. Dev. Dyn. 236:2767-2778.
47. Wu, Y. C., and H. R. Horvitz. 1998. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature 392:501-504.
48. Zheng, Y., S. Bagrodia, and R. A. Cerione. 1994. Activation of phosphoinositide 3-kinase activity by Cdc42Hs binding to p85. J. Biol. Chem. 269:18727-18730.
49. Zhou, Y. W., D. B. Thomason, D. Gullberg, and H. W. Jarrett. 2006. Binding of laminin alpha1-chain LG4-5 domain to alpha-dystroglycan causes tyrosine phosphorylation of syntrophin to initiate Rac1 signaling. Biochemistry 45:2042-2052.