Rac1 Is Essential for Basement Membrane-Dependent Epiblast Survival

REFERENCES

• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Etienne-Manneville, S., and A. Hall. 2002. Rho GTPases in cell biology. Nature 420:629–635.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Feller, S. M. 2001. Crk family adaptors—signalling complex formation and biological roles. Oncogene 20:6348–6371.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Franke, T. F., D. R. Kaplan, and L. C. Cantley. 1997. PI3K: downstream AKTion blocks apoptosis. Cell 88:435–437.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Halfter, W., M. Willem, and U. Mayer. 2005. Basement membrane-dependent survival of retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 46:1000–1009.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Matsuda, M., S. Ota, R. Tanimura, H. Nakamura, K. Matuoka, T. Takenawa, K. Nagashima, and T. Kurata. 1996. Interaction between the amino-terminal SH3 domain of CRK and its natural target proteins. J. Biol. Chem. 271:14468–14472.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• Murray, P., and D. Edgar. 2000. Regulation of programmed cell death by basement membranes in embryonic development. J. Cell Biol. 150:1215–1221.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Schmidt, A., and A. Hall. 2002. Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16:1587–1609.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck, B., and D. R. Alessi. 2000. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346:561–576.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMedGoogle Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMedGoogle Scholar