Cdc42 is required for cytoskeletal support of endothelial cell adhesion during blood vessel formation in mice

Development (Cambridge)

Volumn 142, Issue 17, 2015, Pages 3058-3070

  Barry, David M ^a   Xu, Ke ^b   Meadows, Stryder M ^c   Zheng, Yi ^d   Norden, Pieter R ^e   Davis, George E ^e   Cleaver, Ondine ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b HARVARD UNIVERSITY   (United States)

^c Tulane University   (United States)

^d UNIVERSITY OF CINCINNATI   (United States)

^e University of Missouri   (United States)

Author keywords

Blood vessel development; Cdc42; F actin; Filopodia; Vasculogenesis; VE cadherin

Indexed keywords

ANGIOPOIETIN RECEPTOR; CRE RECOMBINASE; F ACTIN; GUANOSINE TRIPHOSPHATASE; PODOCALYXIN; PROTEIN CDC42; SMALL INTERFERING RNA; VASCULAR ENDOTHELIAL CADHERIN; ACTIN; INTEGRASE; MYOSIN ADENOSINE TRIPHOSPHATASE; TEK PROTEIN, MOUSE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; AORTA ENDOTHELIUM; ARTICLE; BLOOD VESSEL; CELL ADHESION; CELL JUNCTION; CYTOSKELETON; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; FETUS MEMBRANE; FILOPODIUM; IN VITRO STUDY; IN VIVO STUDY; MORPHOGENESIS; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; RETINA BLOOD VESSEL; UMBILICAL VEIN ENDOTHELIAL CELL; YOLK SAC; ANIMAL; ANIMAL EMBRYO; AORTA; APOPTOSIS; BIOLOGICAL MODEL; CELL POLARITY; CELL PROLIFERATION; CELL SURVIVAL; CYTOLOGY; EMBRYOLOGY; EXTRACELLULAR MATRIX; FEMALE; GENE DELETION; GROWTH, DEVELOPMENT AND AGING; KNOCKOUT MOUSE; METABOLISM; PREGNANCY; PSEUDOPODIUM; VASCULARIZATION;

ACTINS; ACTOMYOSIN; ANIMALS; AORTA; APOPTOSIS; BLOOD VESSELS; CDC42 GTP-BINDING PROTEIN; CELL ADHESION; CELL POLARITY; CELL PROLIFERATION; CELL SURVIVAL; CYTOSKELETON; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; EXTRACELLULAR MATRIX; FEMALE; GENE DELETION; INTEGRASES; MICE, KNOCKOUT; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PHYSIOLOGIC; PREGNANCY; PSEUDOPODIA; RECEPTOR, TIE-2; RETINAL VESSELS; YOLK SAC;

EID: 84940785313     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.125260     Document Type: Article

References (59)

1. Adams, A. E., Johnson, D. I., Longnecker, R. M., Sloat, B. F. and Pringle, J. R. (1990). CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111, 131-142.
2. Allen, W. E., Jones, G. E., Pollard, J. W. and Ridley, A. J. (1997). Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J. Cell Sci. 110, 707-720.
3. Bayless, K. J. and Davis, G. E. (2002). The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J. Cell Sci. 115, 1123-1136.
4. Bentley, K., Franco, C. A., Philippides, A., Blanco, R., Dierkes, M., Gebala, V., Stanchi, F., Jones, M., Aspalter, I. M., Cagna, G. et al. (2014). The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis. Nat. Cell Biol. 16, 309-321.
5. Bray, K., Brakebusch, C. and Vargo-Gogola, T. (2011). The Rho GTPase Cdc42 is required for primary mammary epithelial cell morphogenesis in vitro. Small GTPases 2, 247-258.
6. Broman, M. T., Mehta, D. and Malik, A. B. (2007). Cdc42 regulates the restoration of endothelial adherens junctions and permeability. Trends Cardiovasc. Med. 17, 151-156.
7. Bryant, D. M., Datta, A., Rodrı́guez-Fraticelli A. E., Peränen J., Martı́n- Belmonte, F., Mostov K. E. (2010). A molecular network for de novo generation of the apical surface and lumen. Nat. Cell Biol. 12, 1035-1045.
8. Casella, J. F., Flanagan, M. D. and Lin, S. (1981). Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293, 302-305.
9. Chauhan, B. K., Disanza, A., Choi, S.-Y., Faber, S. C., Lou, M., Beggs, H. E., Scita, G., Zheng, Y. and Lang, R. A. (2009). Cdc42- and IRSp53-dependent contractile filopodia tether presumptive lens and retina to coordinate epithelial invagination. Development 136, 3657-3667.
10. Chen, F., Ma, L., Parrini, M. C., Mao, X., Lopez, M., Wu, C., Marks, P. W., Davidson, L., Kwiatkowski, D. J., Kirchhausen, T. et al. (2000). Cdc42 is required for PIP2-induced actin polymerization and early development but not for cell viability. Curr. Biol. 10, 758-765.
11. Chong, D. C., Koo, Y., Xu, K., Fu, S. and Cleaver, O. (2011). Stepwise arteriovenous fate acquisition during mammalian vasculogenesis. Dev. Dyn. 240, 2153-2165.
12. Crosby, C. V., Fleming, P. A., Argraves, W. S., Corada, M., Zanetta, L., Dejana E. and Drake, C. J. (2005). VE-cadherin is not required for the formation of nascent blood vessels but acts to prevent their disassembly. Blood 105, 2771-2776.
13. Davis, G. E., Stratman, A. N., Sacharidou, A. and Koh, W. (2011). Molecular basis for endothelial lumen formation and tubulogenesis during vasculogenesis and angiogenic sprouting. Int. Rev. Cell Mol. Biol. 288, 101-165.
14. Derivery, E. and Gautreau, A. (2010). Generation of branched actin networks: assembly and regulation of the N-WASP and WAVE molecular machines. Bioessays 32, 119-131.
15. Downs, K. M., Temkin, R., Gifford, S. and McHugh, J. (2001). Study of the murine allantois by allantoic explants. Dev. Biol. 233, 347-364.
16. Ferkowicz, M. J. and Yoder, M. C. (2005). Blood island formation: longstanding observations and modern interpretations. Exp. Hematol. 33, 1041-1047.
17. Fukata, M., Watanabe, T., Noritake, J., Nakagawa, M., Yamaga, M., Kuroda, S., Matsuura, Y., Iwamatsu, A., Perez, F. and Kaibuchi, K. (2002). Rac1 and Cdc42 capture microtubules through IQGAP1 and CLIP-170. Cell 109, 873-885.
18. Fukuhara, A., Shimizu, K., Kawakatsu, T., Fukuhara, T. and Takai, Y. (2003). Involvement of nectin-activated Cdc42 small G protein in organization of adherens and tight junctions in Madin-Darby canine kidney cells. J. Biol. Chem. 278, 51885-51893.
19. Garvalov, B. K., Flynn, K. C., Neukirchen, D., Meyn, L., Teusch, N., Wu, X., Brakebusch, C., Bamburg, J. R. and Bradke, F. (2007). Cdc42 regulates cofilin during the establishment of neuronal polarity. J. Neurosci. 27, 13117-13129.
20. Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D. et al. (2003). VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161, 1163-1177.
21. Gomes, E. R., Jani, S. and Gundersen, G. G. (2005). Nuclear movement regulated by Cdc42, MRCK, myosin, and actin flow establishes MTOC polarization in migrating cells. Cell 121, 451-463.
22. Hoelzle, M. K. and Svitkina, T. (2012). The cytoskeletal mechanisms of cell-cell junction formation in endothelial cells. Mol. Biol. Cell 23, 310-323.
23. Hu, G. D., Chen, Y. H., Zhang, L., Tong, W. C., Cheng, Y. X., Luo, Y. L., Cai, S. X. and Zhang, L. (2011). The generation of the endothelial specific cdc42-deficient mice and the effect of cdc42 deletion on the angiogenesis and embryonic development. Chin. Med. J. 124, 4155-4159.
24. Jin, Y., Liu, Y., Lin, Q., Li, J., Druso, J. E., Antonyak, M. A., Meininger, C. J., Zhang, S. L., Dostal, D. E., Guan, J.-L. et al. (2013). Deletion of Cdc42 enhances ADAM17-mediated vascular endothelial growth factor receptor 2 shedding and impairs vascular endothelial cell survival and vasculogenesis. Mol. Cell. Biol. 33, 4181-4197.
25. Johnson, D. I. and Pringle, J. R. (1990). Molecular characterization of CDC42, a Saccharomyces cerevisiae gene involved in the development of cell polarity. J. Cell Biol. 111, 143-152.
26. Jones, E. A. V. (2011). The initiation of blood flow and flow induced events in early vascular development. Semin. Cell Dev. Biol. 22, 1028-1035.
27. Katayama, K.-i., Imai, F., Campbell, K., Lang, R. A., Zheng, Y. and Yoshida, Y. (2013). RhoA and Cdc42 are required in pre-migratory progenitors of the medial ganglionic eminence ventricular zone for proper cortical interneuron migration. Development 140, 3139-3145.
28. Kesavan, G., Sand, F.W., Greiner, T. U., Johansson, J. K., Kobberup, S., Wu, X., Brakebusch, C. and Semb, H. (2009). Cdc42-mediated tubulogenesis controls cell specification. Cell 139, 791-801.
29. Koh, W., Mahan, R. D. and Davis, G. E. (2008). Cdc42- and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J. Cell Sci. 121, 989-1001.
30. Kouklis, P., Konstantoulaki, M., Vogel, S., Broman, M. and Malik, A. B. (2004). Cdc42 regulates the restoration of endothelial barrier function. Circ. Res. 94, 159-166.
31. Kuč era, T., Strilić B., Regener K., Schubert M., Laudet V. and Lammert E. (2009). Ancestral vascular lumen formation via basal cell surfaces. PLoS ONE 4, e4132.
32. Martin-Belmonte, F. and Mostov K. (2007). Phosphoinositides control epithelial development. Cell Cycle 6, 1957-1961.
33. Mattila, P. K. and Lappalainen, P. (2008). Filopodia: molecular architecture and cellular functions. Nat. Rev. Mol. Cell Biol. 9, 446-454.
34. Meadows, S. M., Fletcher, P. J., Moran, C., Xu, K., Neufeld, G., Chauvet, S., Mann, F., Krieg, P. A. and Cleaver, O. (2012). Integration of repulsive guidance cues generates avascular zones that shape mammalian blood vessels. Circ. Res. 110, 34-46.
35. Melendez, J., Grogg, M. and Zheng, Y. (2011). Signaling role of Cdc42 in regulating mammalian physiology. J. Biol. Chem. 286, 2375-2381.
36. Neumann, J. C., Dovey, J. S., Chandler, G. L., Carbajal, L. and Amatruda, J. F. (2009). Identification of a heritable model of testicular germ cell tumor in the zebrafish. Zebrafish 6, 319-327.
37. Peng, J., Wallar, B. J., Flanders, A., Swiatek, P. J. and Alberts, A. S. (2003). Disruption of the Diaphanous-related formin Drf1 gene encoding mDia1 reveals a role for Drf3 as an effector for Cdc42. Curr. Biol. 13, 534-545.
38. Qi, Y., Liu, J., Wu, X., Brakebusch, C., Leitges, M., Han, Y., Corbett, S. A., Lowry, S. F., Graham, A. M. and Li, S. (2011). Cdc42 controls vascular network assembly through protein kinase Ciota during embryonic vasculogenesis. Arterioscler. Thromb. Vasc. Biol. 31, 1861-1870.
39. Reginensi, A., Scott, R. P., Gregorieff, A., Bagherie-Lachidan, M., Chung, C., Lim, D.-S., Pawson, T., Wrana, J. and McNeill, H. (2013). Yap- and Cdc42-dependent nephrogenesis and morphogenesis during mouse kidney development. PLoS Genet. 9, e1003380.
40. Risau, W. and Flamme, I. (1995). Vasculogenesis. Annu. Rev. Cell Dev. Biol. 11, 73-91.
41. Rohatgi, R., Ma, L., Miki, H., Lopez, M., Kirchhausen, T., Takenawa, T. and Kirschner, M. W. (1999). The interaction between N-WASP and the Arp2/3 complex links Cdc42-dependent signals to actin assembly. Cell 97, 221-231.
42. Sacharidou, A., Stratman, A. N. and Davis, G. E. (2012). Molecular mechanisms controlling vascular lumen formation in three-dimensional extracellular matrices. Cells Tissues Organs 195, 122-143.
43. Sachdev, S., Bu, Y. and Gelman, I. H. (2009). Paxillin-Y118 phosphorylation contributes to the control of Src-induced anchorage-independent growth by FAK and adhesion. BMC Cancer 9, 12.
44. Sato, T. N., Qin, Y., Kozak, C. A. and Audus, K. L. (1993). Tie-1 and tie-2 define another class of putative receptor tyrosine kinase genes expressed in early embryonic vascular system. Proc. Natl. Acad. Sci. USA 90, 9355-9358.
45. Stalmans, I., Ng, Y.-S., Rohan, R., Fruttiger, M., Bouché A., Ÿuce A., Fujisawa H., Hermans B., Shani M., Jansen S. et al. (2002). Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109, 327-336.
46. Stratman, A. N. and Davis, G. E. (2012). Endothelial cell-pericyte interactions stimulate basement membrane matrix assembly: influence on vascular tube remodeling, maturation, and stabilization. Microsc. Microanal. 18, 68-80.
47. Stratman, A. N., Davis, M. J. and Davis, G. E. (2011). VEGF and FGF prime vascular tube morphogenesis and sprouting directed by hematopoietic stem cell cytokines. Blood 117, 3709-3719.
48. Strilić B., Kuč era, T., Eglinger J., Hughes, M. R., McNagny, K. M., Tsukita S., Dejana E., Ferrara N. ., Lammert E. (2009). The molecular basis of vascular lumen formation in the developing mouse aorta. Dev. Cell 17, 505-515.
49. Sumi, T., Matsumoto, K., Takai, Y. and Nakamura, T. (1999). Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42- activated LIM-kinase 2. J. Cell Biol. 147, 1519-1532.
50. Tang, N., Marshall, W. F., McMahon, M., Metzger, R. J. and Martin, G. R. (2011). Control of mitotic spindle angle by the RAS-regulated ERK1/2 pathway determines lung tube shape. Science 333, 342-345.
51. Villasenor, A., Chong, D. C. and Cleaver, O. (2008). Biphasic Ngn3 expression in the developing pancreas. Dev. Dyn. 237, 3270-3279.
52. Wang, Y., Nakayama, M., Pitulescu, M. E., Schmidt, T. S., Bochenek, M. L., Sakakibara, A., Adams, S., Davy, A., Deutsch, U., Lüthi U. et al. (2010). Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486.
53. Wilkinson, S., Paterson, H. F. and Marshall, C. J. (2005). Cdc42-MRCK and Rho- ROCK signalling cooperate in myosin phosphorylation and cell invasion. Nat. Cell Biol. 7, 255-261.
54. Wirtz, D. and Khatau, S. B. (2010). Protein filaments: bundles from boundaries. Nat. Mater. 9, 788-790.
55. Xu, K., Chong, D. C., Rankin, S. A., Zorn, A. M. and Cleaver, O. (2009). Rasip1 is required for endothelial cell motility, angiogenesis and vessel formation. Dev. Biol. 329, 269-279.
56. Yang, L., Wang, L. and Zheng, Y. (2006). Gene targeting of Cdc42 and Cdc42GAP affirms the critical involvement of Cdc42 in filopodia induction, directed migration, and proliferation in primary mouse embryonic fibroblasts. Mol. Biol. Cell 17, 4675-4685.
57. Yang, L., Wang, L., Geiger, H., Cancelas, J. A., Mo, J. and Zheng, Y. (2007a). Rho GTPase Cdc42 coordinates hematopoietic stem cell quiescence and niche interaction in the bone marrow. Proc. Natl. Acad. Sci. USA 104, 5091-5096.
58. Yang, L., Wang, L., Kalfa, T. A., Cancelas, J. A., Shang, X., Pushkaran, S., Mo, J., Williams, D. A. and Zheng, Y. (2007b). Cdc42 critically regulates the balance between myelopoiesis and erythropoiesis. Blood 110, 3853-3861.
59. Zeng, Q., Lagunoff, D., Masaracchia, R., Goeckeler, Z., Cote, G. and Wysolmerski, R. (2000). Endothelial cell retraction is induced by PAK2 monophosphorylation of myosin II. J. Cell Sci. 113, 471-482.