RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis

FASEB Journal

Volumn 24, Issue 9, 2010, Pages 3186-3195

  Bryan, Brad A ^a,b,c   Dennstedt, Emily ^c   Mitchell, Dianne C ^a,b   Walshe, Tony E ^a,b   Noma, Kensuke ^d   Loureiro, Robyn ^a,b   Saint Geniez, Magali ^a,b   Campaigniac, Jean Paul ^c   Liao, James K ^d   D'Amore, Patricia A ^a,b  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c WORCESTER STATE UNIVERSITY   (United States)

^d BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

Endothelial cells; GTPase; Rho kinase; Vascular endothelial growth factor; Y 27632

Indexed keywords

4 (1 AMINOETHYL) N (4 PYRIDYL)CYCLOHEXANECARBOXAMIDE; PROTEIN; PROTEIN ROCK1; PROTEIN ROCK2; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CELL MOTILITY; CELL PROLIFERATION; CELL SURVIVAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; EXPLANT; HETEROZYGOTE; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

AMIDES; ANIMALS; APOPTOSIS; BLOTTING, WESTERN; CATTLE; CELLS, CULTURED; ENZYME ACTIVATION; HUMANS; MICE; MICROSCOPY, FLUORESCENCE; NEOVASCULARIZATION, PHYSIOLOGIC; PYRIDINES; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RHO-ASSOCIATED KINASES; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 77956639567     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-145102     Document Type: Article

References (64)

1. Ferrara, N. (2000) Vascular endothelial growth factor and the regulation of angiogenesis. Recent Prog. Horm. Res. 55, 15-35; discussion 35-16
2. Lee, S., Chen, T. T., Barber, C. L., Jordan, M. C., Murdock, J., Desai, S., Ferrara, N., Nagy, A., Roos, K. P., and Iruela-Arispe, M. L. (2007) Autocrine VEGF signaling is required for vascular homeostasis. Cell 130, 691-703
3. Bryan, B. A., Walshe, T. E., Mitchell, D. C., Havumaki, J. S., Saint-Geniez, M., Maharaj, A. S., Maldonado, A. E., and D'Amore, P. A. (2008) Coordinated vascular endothelial growth factor expression and signaling during skeletal myogenic differentiation. Mol. Biol. Cell 19, 994-1006
4. Jin, K., Zhu, Y., Sun, Y., Mao, X. O., Xie, L., and Greenberg, D. A. (2002) Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc. Natl. Acad. Sci. U. S. A. 99, 11946-11950
5. Ferrara, N., Gerber, H. P., and LeCouter, J. (2003) The biology of VEGF and its receptors. Nat. Med. 9, 669-676
6. Zachary, I. (2003) VEGF signalling: integration and multitasking in endothelial cell biology. Biochem. Soc. Trans. 31, 1171-1177
7. Jaffe, A. B., and Hall, A. (2005) Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269
8. Zhao, Z. S., and Manser, E. (2005) PAK and other Rho-associated kinases-effectors with surprisingly diverse mechanisms of regulation. Biochem. J. 386, 201-214
9. Coleman, M. L., Sahai, E. A., Yeo, M., Bosch, M., Dewar, A., and Olson, M. F. (2001) Membrane blebbing during apoptosis results from caspase-mediated activation of ROCK I. Nat. Cell Biol. 3, 339-345
10. Sebbagh, M., Renvoize, C., Hamelin, J., Riche, N., Bertoglio, J., and Breard, J. (2001) Caspase-3-mediated cleavage of ROCK I induces MLC phosphorylation and apoptotic membrane blebbing. Nat. Cell Biol. 3, 346-352
11. Kaneko, T., Amano, M., Maeda, A., Goto, H., Takahashi, K., Ito, M., and Kaibuchi, K. (2000) Identification of calponin as a novel substrate of Rho-kinase. Biochem. Biophys. Res. Commun. 273, 110-116
12. Nakagawa, O., Fujisawa, K., Ishizaki, T., Saito, Y., Nakao, K., and Narumiya, S. (1996) ROCK-I and ROCK-II, two isoforms of Rho-associated coiled-coil forming protein serine/threonine kinase in mice. FEBS Lett. 392, 189-193
13. Wei, L., Roberts, W., Wang, L., Yamada, M., Zhang, S., Zhao, Z., Rivkees, S. A., Schwartz, R. J., and Imanaka-Yoshida, K. (2001) Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development 128, 2953-2962
14. Rikitake, Y., Oyama, N., Wang, C. Y., Noma, K., Satoh, M., Kim, H. H., and Liao, J. K. (2005) Decreased perivascular fibrosis but not cardiac hypertrophy in ROCK1+/- haploinsufficient mice. Circulation 112, 2959-2965
15. Shimizu, Y., Thumkeo, D., Keel, J., Ishizaki, T., Oshima, H., Oshima, M., Noda, Y., Matsumura, F., Taketo, M. M., and Narumiya, S. (2005) ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J. Cell Biol. 168, 941-953
16. Zhang, Y. M., Bo, J., Taffet, G. E., Chang, J., Shi, J., Reddy, A. K., Michael, L. H., Schneider, M. D., Entman, M. L., Schwartz, R. J., and Wei, L. (2006) Targeted deletion of ROCK1 protects the heart against pressure overload by inhibiting reactive fibrosis. FASEB J. 20, 916-925
17. Thumkeo, D., Keel, J., Ishizaki, T., Hirose, M., Nonomura, K., Oshima, H., Oshima, M., Taketo, M. M., and Narumiya, S. (2003) Targeted disruption of the mouse rho-associated kinase 2 gene results in intrauterine growth retardation and fetal death. Mol. Cell Biol. 23, 5043-5055
18. Thumkeo, D., Shimizu, Y., Sakamoto, S., Yamada, S., and Narumiya, S. (2005) ROCK-I and ROCK-II cooperatively regulate closure of eyelid and ventral body wall in mouse embryo. Genes Cells 10, 825-834
19. Connolly, J. O., Simpson, N., Hewlett, L., and Hall, A. (2002) Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell 13, 2474-2485
20. Hoang, M. V., Whelan, M. C., and Senger, D. R. (2004) Rho activity critically and selectively regulates endothelial cell organization during angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 101, 1874-1879
21. Park, H. J., Kong, D., Iruela-Arispe, L., Begley, U., Tang, D., and Galper, J. B. (2002) 3-hydroxy-3-methylglutaryl coenzyme A reductase inhibitors interfere with angiogenesis by inhibiting the geranylgeranylation of RhoA. Circ. Res. 91, 143-150
22. Ng, Y. S., Ramsauer, M., Loureiro, R. M., and D'Amore, P. A. (2004) Identification of genes involved in VEGF-mediated vascular morphogenesis using embryonic stem cell-derived cystic embryoid bodies. Lab. Invest. 84, 1209-1218
23. Ramsauer, M., and D'Amore, P. A. (2007) Contextual role for angiopoietins and TGFbeta1 in blood vessel stabilization. J. Cell Sci. 120, 1810-1817
24. Noma, K., Rikitake, Y., Oyama, N., Yan, G., Alcaide, P., Liu, P. Y., Wang, H., Ahl, D., Sawada, N., Okamoto, R., Hiroi, Y., Shimizu, K., Luscinskas, F. W., Sun, J., and Liao, J. K. (2008) ROCK1 mediates leukocyte recruitment and neointima formation following vascular injury. J. Clin. Invest. 118, 1632-1644
25. Rikitake, Y., Kim, H. H., Huang, Z., Seto, M., Yano, K., Asano, T., Moskowitz, M. A., and Liao, J. K. (2005) Inhibition of Rho kinase (ROCK) leads to increased cerebral blood flow and stroke protection. Stroke 36, 2251-2257
26. Im, E., Venkatakrishnan, A., and Kazlauskas, A. (2005) Cathepsin B regulates the intrinsic angiogenic threshold of endothelial cells. Mol. Biol. Cell 16, 3488-3500
27. Darland, D. C., and D'Amore, P. A. (2001) TGF beta is required for the formation of capillary-like structures in three-dimensional cocultures of 10T1/2 and endothelial cells. Angiogenesis 4, 11-20
28. Bryan, B. A., Li, D., Wu, X., and Liu, M. (2005) The Rho family of small GTPases: crucial regulators of skeletal myogenesis. Cell Mol. Life Sci. 62, 1547-1555
29. Van Nieuw Amerongen, G. P., Koolwijk, P., Versteilen, A., and van Hinsbergh, V. W. (2003) Involvement of RhoA/Rho kinase signaling in VEGF-induced endothelial cell migration and angiogenesis in vitro. Arterioscler. Thromb. Vasc. Biol. 23, 211-217
30. Vincent, L., Chen, W., Hong, L., Mirshahi, F., Mishal, Z., Mirshahi-Khorassani, T., Vannier, J. P., Soria, J., and Soria, C. (2001) Inhibition of endothelial cell migration by cerivastatin, an HMG-CoA reductase inhibitor: contribution to its antiangiogenic effect. FEBS Lett. 495, 159-166
31. Zeng, H., Zhao, D., and Mukhopadhyay, D. (2002) KDR stimulates endothelial cell migration through heterotrimeric G protein Gq/11-mediated activation of a small GTPase RhoA. J. Biol. Chem. 277, 46791-46798
32. Bobak, D., Moorman, J., Guanzon, A., Gilmer, L., and Hahn, C. (1997) Inactivation of the small GTPase Rho disrupts cellular attachment and induces adhesion-dependent and adhesion-independent apoptosis. Oncogene 15, 2179-2189
33. Fiorentini, C., Fabbri, A., Flatau, G., Donelli, G., Matarrese, P., Lemichez, E., Falzano, L., and Boquet, P. (1997) Escherichia coli cytotoxic necrotizing factor 1 (CNF1), a toxin that activates the Rho GTPase. J. Biol. Chem. 272, 19532-19537 (Pubitemid 27337754)
34. Giry, M., Popoff, M. R., von Eichel-Streiber, C., and Boquet, P. (1995) Transient expression of RhoA, -B, and -C GTPases in HeLa cells potentiates resistance to Clostridium difficile toxins A and B but not to Clostridium sordellii lethal toxin. Infect. Immun. 63, 4063-4071
35. Henning, S. W., Galandrini, R., Hall, A., and Cantrell, D. A. (1997) The GTPase Rho has a critical regulatory role in thymus development. EMBO J. 16, 2397-2407
36. Jimenez, B., Arends, M., Esteve, P., Perona, R., Sanchez, R., Ramon y Cajal, S., Wyllie, A., and Lacal, J. C. (1995) Induction of apoptosis in NIH3T3 cells after serum deprivation by overexpression of rho-p21, a GTPase protein of the ras superfamily. Oncogene 10, 811-816
37. Petrache, I., Crow, M. T., Neuss, M., and Garcia, J. G. (2003) Central involvement of Rho family GTPases in TNF-alpha-mediated bovine pulmonary endothelial cell apoptosis. Biochem. Biophys. Res. Commun. 306, 244-249
38. Lum, H., and Malik, A. B. (1996) Mechanisms of increased endothelial permeability. Can. J. Physiol. Pharmacol. 74, 787-800
39. Zeng, L., Xu, H., Chew, T. L., Eng, E., Sadeghi, M. M., Adler, S., Kanwar, Y. S., and Danesh, F. R. (2005) HMG CoA reductase inhibition modulates VEGF-induced endothelial cell hyperpermeability by preventing RhoA activation and myosin regulatory light chain phosphorylation. FASEB J. 19, 1845-1847
40. Croft, D. R., and Olson, M. F. (2006) The Rho GTPase effector ROCK regulates cyclin A, cyclin D1, and p27Kip1 levels by distinct mechanisms. Mol. Cell Biol. 26, 4612-4627
41. Pille, J. Y., Denoyelle, C., Varet, J., Bertrand, J. R., Soria, J., Opolon, P., Lu, H., Pritchard, L. L., Vannier, J. P., Malvy, C., Soria, C., and Li, H. (2005) Anti-RhoA and anti-RhoC siRNAs inhibit the proliferation and invasiveness of MDA-MB-231 breast cancer cells in vitro and in vivo. Mol. Ther. 11, 267-274
42. Kroll, J., and Waltenberger, J. (1997) The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells. J. Biol. Chem. 272, 32521-32527
43. Marshall, C. J. (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185
44. 2+ in VEGF- and FGF-induced choroidal endothelial cell proliferation. Am. J. Physiol. Cell Physiol. 281, C1448-C1456
45. Abecassis, I., Olofsson, B., Schmid, M., Zalcman, G., and Karniguian, A. (2003) RhoA induces MMP-9 expression at CD44 lamellipodial focal complexes and promotes HMEC-1 cell invasion. Exp. Cell. Res. 291, 363-376
46. Wang, H., and Keiser, J. A. (1998) Vascular endothelial growth factor upregulates the expression of matrix metalloproteinases in vascular smooth muscle cells: role of flt-1. Circ. Res. 83, 832-840
47. Yin, L., Morishige, K., Takahashi, T., Hashimoto, K., Ogata, S., Tsutsumi, S., Takata, K., Ohta, T., Kawagoe, J., Takahashi, K., and Kurachi, H. (2007) Fasudil inhibits vascular endothelial growth factor-induced angiogensis in vitro and in vivo. Mol. Cancer Ther. 6, 1517-1525
48. Hata, Y., Miura, M., Nakao, S., Kawahara, S., Kita, T., and Ishibashi, T. (2008) Antiangiogenic properties of fasudil, a potent Rho-Kinase inhibitor. Jpn. J. Ophthalmol. 52, 16-23
49. Ghosh, K., Thodeti, C. K., Dudley, A. C., Mammoto, A., Klagsbrun, M., and Ingber, D. E. (2008) Tumor-derived endothelial cells exhibit aberrant Rho-mediated mechanosensing and abnormal angiogenesis in vitro. Proc. Natl. Acad. Sci. U. S. A. 105, 11305-11310
50. Kroll, J., Epting, D., Kern, K., Dietz, C. T., Feng, Y., Hammes, H. P., Weiland, T., Augustin, H. G. (2009) Inhibition of Rho-dependent kinases ROCK 1/II activates VEGF-driven retinal neovascularization and sprouting angiogenesis. Am. J. Physiol. Heart Circ. Physiol. 269, 893-899
51. Im, E., and Kazlauskas, A. (2007) Src family kinases promote vessel stability by antagonizing the Rho/ROCK pathway. J. Biol. Chem. 282, 29122-29129
52. Mavria, G., Vercoulen, Y., Yeo, M., Paterson, H., Karasarides, M., Marais, R., Bird, D., and Marshall, C. J. (2006) ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9, 33-44
53. Yoshida, A., Anand-Apte, B., and Zetter, B. R. (1996) Differential endothelial migration and proliferation to basic fibroblast growth factor and vascular endothelial growth factor. Growth Factors 13, 57-64
54. Cleaver, O., and Krieg, P. A. (1998) VEGF mediates angioblast migration during development of the dorsal aorta in Xenopus. Development 125, 3905-3914
55. Bryan, B. A., and D'Amore, P. A. (2007) What tangled webs they weave: Rho-GTPase control of angiogenesis. Cell. Mol. Life Sci. 64, 2053-2065
56. Clauss, M., Gerlach, M., Gerlach, H., Brett, J., Wang, F., Familletti, P. C., Pan, Y. C., Olander, J. V., Connolly, D. T., and Stern, D. (1990) Vascular permeability factor: a tumor-derived polypeptide that induces endothelial cell and monocyte procoagulant activity, and promotes monocyte migration. J. Exp. Med. 172, 1535-1545
57. Ratajska, A., Torry, R. J., Kitten, G. T., Kolker, S. J., and Tomanek, R. J. (1995) Modulation of cell migration and vessel formation by vascular endothelial growth factor and basic fibroblast growth factor in cultured embryonic heart. Dev. Dyn. 203, 399-407
58. Raftopoulou, M., and Hall, A. (2004) Cell migration: Rho GTPases lead the way. Dev. Biol. 265, 23-32
59. Titus, B., Schwartz, M. A., and Theodorescu, D. (2005) Rho proteins in cell migration and metastasis. Crit. Rev. Eukaryot. Gene Expr. 15, 103-114
60. Watanabe, T., Noritake, J., and Kaibuchi, K. (2005) Regulation of microtubules in cell migration. Trends Cell Biol. 15, 76-83
61. Birukova, A. A., Adyshev, D., Gorshkov, B., Bokoch, G. M., Birukov, K. G., and Verin, A. D. (2006) GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am. J. Physiol. Lung Cell Mol. Physiol. 290, L540-548
62. Holinstat, M., Mehta, D., Kozasa, T., Minshall, R. D., and Malik, A. B. (2003) Protein kinase Calpha-induced p115RhoGEF phosphorylation signals endothelial cytoskeletal rearrangement. J. Biol. Chem. 278, 28793-28798
63. Mehta, D., Rahman, A., and Malik, A. B. (2001) Protein kinase C-alpha signals rho-guanine nucleotide dissociation inhibitor phosphorylation and rho activation and regulates the endothelial cell barrier function. J. Biol. Chem. 276, 22614-22620
64. Hasmim, M., Bieler, G., and Ruegg, C. (2007) Zoledronate inhibits endothelial cell adhesion, migration and survival through the suppression of multiple, prenylation-dependent signaling pathways. J. Thromb. Haemost. 5, 166-173