Cdc42 controls vascular network assembly through protein kinase cι during embryonic vasculogenesis

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 8, 2011, Pages 1861-1870

  Qi, Yanmei ^a   Liu, Jie ^a   Wu, Xunwei ^b   Brakebusch, Cord ^c   Leitges, Michael ^d   Han, Yaling ^e   Corbett, Siobhan A ^a   Lowry, Stephen F ^a   Graham, Alan M ^a   Li, Shaohua ^a  

^a ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF OSLO   (Norway)

^e Shenyang Northern Hospital   (China)

Author keywords

angiogenesis; endothelium; signal transduction; vascular biology

Indexed keywords

GLYCOGEN SYNTHASE KINASE 3BETA; PROTEIN CDC42; PROTEIN KINASE C IOTA;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL JUNCTION; CELL MIGRATION; EMBRYO; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INACTIVATION; GENE EXPRESSION; MORPHOGENESIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION;

ADHERENS JUNCTIONS; ANIMALS; BLOOD VESSELS; CDC42 GTP-BINDING PROTEIN; CELL DIFFERENTIATION; CELL LINE; CELL MOVEMENT; EMBRYONIC STEM CELLS; ENDOTHELIAL CELLS; GLYCOGEN SYNTHASE KINASE 3; ISOENZYMES; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN KINASE C; SIGNAL TRANSDUCTION;

EID: 80051548128     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.230144     Document Type: Article

References (39)

1. Drake CJ. Embryonic and adult vasculogenesis. Birth Defects Res C Embryo Today. 2003;69:73-82. (Pubitemid 37238417)
2. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, O'Shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature. 1996;380:439-442. (Pubitemid 26102720)
3. Shalaby F, Ho J, Stanford WL, Fischer KD, Schuh AC, Schwartz L, Bernstein A, Rossant J. A requirement for Flk1 in primitive and definitive hematopoiesis and vasculogenesis. Cell. 1997;89:981-990. (Pubitemid 27513524)
4. Fong GH, Rossant J, Gertsenstein M, Breitman ML. Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature. 1995;376:66-70.
5. Vittet D, Buchou T, Schweitzer A, Dejana E, Huber P. Targeted nullmutation in the vascular endothelial-cadherin gene impairs the organization of vascular-like structures in embryoid bodies. Proc Natl Acad Sci USA. 1997;94:6273-6278. (Pubitemid 27270674)
6. Bloch W, Forsberg E, Lentini S, Brakebusch C, Martin K, Krell HW, Weidle UH, Addicks K, Fassler R. 1 Integrin is essential for teratoma growth and angiogenesis. J Cell Biol. 1997;139:265-278. (Pubitemid 27444097)
7. Carlson TR, Hu H, Braren R, Kim YH, Wang RA. Cell-autonomous requirement for 1 integrin in endothelial cell adhesion, migration and survival during angiogenesis in mice. Development. 2008;135: 2193-2202. (Pubitemid 352015153)
8. Tzima E. Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ Res. 2006;98:176-185.
9. Broman MT, Kouklis P, Gao X, Ramchandran R, Neamu RF, Minshall RD, Malik AB. Cdc42 regulates adherens junction stability and endothelial permeability by inducing catenin interaction with the vascular endothelial cadherin complex. Circ Res. 2006;98:73-80. (Pubitemid 43970205)
10. Tzima E, Del Pozo MA, Kiosses WB, Mohamed SA, Li S, Chien S, Schwartz MA. Activation of Rac1 by shear stress in endothelial cells mediates both cytoskeletal reorganization and effects on gene expression. EMBO J. 2002;21:6791-6800. (Pubitemid 36014551)
11. Bayless KJ, Davis GE. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J Cell Sci. 2002;115:1123-1136. (Pubitemid 34272478)
12. Aspenstrom P, Fransson A, Saras J. Rho GTPases have diverse effects on the organization of the actin filament system. Biochem J. 2004;377: 327-337. (Pubitemid 38142188)
13. Koh W, Mahan RD, Davis GE. Cdc42-and Rac1-mediated endothelial lumen formation requires Pak2, Pak4 and Par3, and PKC-dependent signaling. J Cell Sci. 2008;121:989-1001. (Pubitemid 351639418)
14. Wu X, Li S, Chrostek-Grashoff A, Czuchra A, Meyer H, Yurchenco PD, Brakebusch C. Cdc42 is crucial for the establishment of epithelial polarity during early mammalian development. Dev Dyn. 2007;236:2767-2778. (Pubitemid 47613239)
15. Bandyopadhyay G, Standaert ML, Sajan MP, Kanoh Y, Miura A, Braun U, Kruse F, Leitges M, Farese RV. Protein kinase C-αknockout in embryonic stem cells and adipocytes impairs insulin-stimulated glucose transport. Mol Endocrinol. 2004;18:373-383. (Pubitemid 38183936)
16. Li S, Yurchenco PD. Matrix assembly, cell polarization, and cell survival: analysis of peri-implantation development with cultured embryonic stem cells. Methods Mol Biol. 2006;329:113-125.
17. Kearney JB, Kappas NC, Ellerstrom C, DiPaola FW, Bautch VL. The VEGF receptor flt-1 (VEGFR-1) is a positive modulator of vascular sprout formation and branching morphogenesis. Blood. 2004;103: 4527-4535. (Pubitemid 38745980)
18. Li S, Chow LH, Pickering JG. Cell surface-bound collagenase-1 and focal substrate degradation stimulate the rear release of motile vascular smooth muscle cells. J Biol Chem. 2000;275:35384-35392.
19. Risau W, Sariola H, Zerwes HG, Sasse J, Ekblom P, Kemler R, Doetschman T. Vasculogenesis and angiogenesis in embryonic-stem-cellderived embryoid bodies. Development. 1988;102:471-478. (Pubitemid 18084930)
20. Jakobsson L, Kreuger J, Claesson-Welsh L. Building blood vessels-stem cell models in vascular biology. J Cell Biol. 2007;177:751-755. (Pubitemid 46873082)
21. Ruhrberg C, Gerhardt H, Golding M, Watson R, Ioannidou S, Fujisawa H, Betsholtz C, Shima DT. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 2002;16:2684-2698.
22. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161:1163-1177. (Pubitemid 36870177)
23. Martin P, Wood W. Epithelial fusions in the embryo. Curr Opin Cell Biol. 2002;14:569-574. (Pubitemid 35247739)
24. Etienne-Manneville S, Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKC-. Cell. 2001; 106:489-498. (Pubitemid 32786992)
25. Kovac J, Oster H, Leitges M. Expression of the atypical protein kinase C (aPKC) isoforms-/-and during mouse embryogenesis. Gene Expr Patterns. 2007;7:187-196. (Pubitemid 44712739)
26. Etienne-Manneville S, Hall A. Cdc42 regulates GSK-3 and adenomatous polyposis coli to control cell polarity. Nature. 2003;421:753-756. (Pubitemid 36227627)
27. Harwood AJ. Regulation of GSK-3: a cellular multiprocessor. Cell. 2001; 105:821-824. (Pubitemid 32635083)
28. Chen F, Ma L, Parrini MC, Mao X, Lopez M, Wu C, Marks PW, Davidson L, Kwiatkowski DJ, Kirchhausen T, Orkin SH, Rosen FS, Mayer BJ, Kirschner MW, Alt FW. Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr Biol. 2000;10:758-765. (Pubitemid 30466938)
29. Sugihara K, Nakatsuji N, Nakamura K, Nakao K, Hashimoto R, Otani H, Sakagami H, Kondo H, Nozawa S, Aiba A, Katsuki M. Rac1 is required for the formation of three germ layers during gastrulation. Oncogene. 1998;17:3427-3433. (Pubitemid 29050677)
30. Tan W, Palmby TR, Gavard J, Amornphimoltham P, Zheng Y, Gutkind JS. An essential role for Rac1 in endothelial cell function and vascular development. FASEB J. 2008;22:1829-1838. (Pubitemid 351811460)
31. Joberty G, Petersen C, Gao L, Macara IG. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat Cell Biol. 2000; 2:531-539.
32. Lin D, Edwards AS, Fawcett JP, Mbamalu G, Scott JD, Pawson T. A mammalian PAR-3-PAR-6 complex implicated in Cdc42/Rac1 and aPKC signalling and cell polarity. Nat Cell Biol. 2000;2:540-547.
33. Hirano Y, Yoshinaga S, Takeya R, Suzuki NN, Horiuchi M, Kohjima M, Sumimoto H, Inagaki F. Structure of a cell polarity regulator, a complex between atypical PKC and Par6 PB1 domains. J Biol Chem. 2005;280: 9653-9661. (Pubitemid 40409663)
34. Khasar SG, Lin YH, Martin A, Dadgar J, McMahon T, Wang D, Hundle B, Aley KO, Isenberg W, McCarter G, Green PG, Hodge CW, Levine JD, Messing RO. A novel nociceptor signaling pathway revealed in protein kinase C-mutant mice. Neuron. 1999;24:253-260. (Pubitemid 29466163)
35. Leitges M, Sanz L, Martin P, Duran A, Braun U, Garcia JF, Camacho F, Diaz-Meco MT, Rennert PD, Moscat J. Targeted disruption of the PKC gene results in the impairment of the NF-αB pathway. Mol Cell. 2001; 8:771-780. (Pubitemid 33030211)
36. Wu X, Quondamatteo F, Lefever T, Czuchra A, Meyer H, Chrostek A, Paus R, Langbein L, Brakebusch C. Cdc42 controls progenitor cell differentiation and catenin turnover in skin. Genes Dev. 2006;20: 571-585. (Pubitemid 43345323)
37. Goode N, Hughes K, Woodgett JR, Parker PJ. Differential regulation of glycogen synthase kinase-3-by protein kinase C isotypes. J Biol Chem. 1992;267:16878-16882.
38. Liu J, He X, Corbett SA, Lowry SF, Graham AM, Fassler R, Li S. Integrins are required for the differentiation of visceral endoderm. J Cell Sci. 2009;122:233-242.
39. Zovein AC, Luque A, Turlo KA, Hofmann JJ, Yee KM, Becker MS, Fassler R, Mellman I, Lane TF, Iruela-Arispe ML. 1 Integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism. Dev Cell. 2010;18:39-51.