Regulation of fibronectin matrix assembly and capillary morphogenesis in endothelial cells by Rho family GTPases

Experimental Cell Research

Volumn 315, Issue 12, 2009, Pages 2092-2104

  Fernandez Sauze, Samantha ^a   Grall, Dominique ^a   Cseh, Botond ^a   Van Obberghen Schilling, Ellen ^a  

^a UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Endothelial cells; Fibronectin fibrillogenesis; Rho family GTPases; RNA interference

Indexed keywords

ACTIN; FIBRONECTIN; MYOSIN; PROTEIN CDC42; RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; RHOB GUANINE NUCLEOTIDE BINDING PROTEIN; RHOC GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5;

ANGIOGENESIS; ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; CAPILLARY; CELL INTERACTION; CONTROLLED STUDY; COW; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; GENETIC TRANSFECTION; IMMUNOFLUORESCENCE; MICROSCOPY; MORPHOGENESIS; NONHUMAN; NORTHERN BLOTTING; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FAMILY; REGULATORY MECHANISM; RETROVIRUS INFECTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

EID: 67349161798     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.03.017     Document Type: Article

References (53)

1. Francis S.E., Goh K.L., Hodivala-Dilke K., Bader B.L., Stark M., Davidson D., and Hynes R.O. Central roles of alpha5beta1 integrin and fibronectin in vascular development in mouse embryos and embryoid bodies. Arterioscler. Thromb. Vasc. Biol. 22 (2002) 927-933
2. George E.L., Georges-Labouesse E.N., Patel-King R.S., Rayburn H., and Hynes R.O. Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119 (1993) 1079-1091
3. Kim S., Bell K., Mousa S.A., and Varner J.A. Regulation of angiogenesis in vivo by ligation of integrin alpha5beta1 with the central cell-binding domain of fibronectin. Am. J. Pathol. 156 (2000) 1345-1362
4. Kalluri R. Angiogenesis: basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev., Cancer 3 (2003) 422-433
5. Kaspar M., Zardi L., and Neri D. Fibronectin as target for tumor therapy. Int. J. Cancer 118 (2006) 1331-1339
6. Jin H., Aiyer A., Su J., Borgstrom P., Stupack D., Friedlander M., and Varner J. A homing mechanism for bone marrow-derived progenitor cell recruitment to the neovasculature. J. Clin. Invest. 116 (2006) 652-662
7. Geiger B., Bershadsky A., Pankov R., and Yamada K.M. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev., Mol. Cell Biol. 2 (2001) 793-805
8. Mao Y., and Schwarzbauer J.E. Fibronectin fibrillogenesis, a cell-mediated matrix assembly process. Matrix Biol. 24 (2005) 389-399
9. Pankov R., Cukierman E., Katz B.Z., Matsumoto K., Lin D.C., Lin S., Hahn C., and Yamada K.M. Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J. Cell Biol. 148 (2000) 1075-1090
10. Katz B.Z., Zamir E., Bershadsky A., Kam Z., Yamada K.M., and Geiger B. Physical state of the extracellular matrix regulates the structure and molecular composition of cell-matrix adhesions. Mol. Biol. Cell 11 (2000) 1047-1060
11. Clark K., Pankov R., Travis M.A., Askari J.A., Mould A.P., Craig S.E., Newham P., Yamada K.M., and Humphries M.J. A specific alpha5beta1-integrin conformation promotes directional integrin translocation and fibronectin matrix formation. J. Cell. Sci. 118 (2005) 291-300
12. Zhang Q., Magnusson M.K., and Mosher D.F. Lysophosphatidic acid and microtubule-destabilizing agents stimulate fibronectin matrix assembly through Rho-dependent actin stress fiber formation and cell contraction. Mol. Biol. Cell 8 (1997) 1415-1425
13. Zhang Q., Peyruchaud O., French K.J., Magnusson M.K., and Mosher D.F. Sphingosine 1-phosphate stimulates fibronectin matrix assembly through a Rho-dependent signal pathway. Blood 93 (1999) 2984-2990
14. Zhong C., Chrzanowska-Wodnicka M., Brown J., Shaub A., Belkin A.M., and Burridge K. Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141 (1998) 539-551
15. Olorundare O.E., Peyruchaud O., Albrecht R.M., and Mosher D.F. Assembly of a fibronectin matrix by adherent platelets stimulated by lysophosphatidic acid and other agonists. Blood 98 (2001) 117-124
16. Vouret-Craviari V., Boulter E., Grall D., Matthews C., and Van Obberghen-Schilling E. ILK is required for the assembly of matrix-forming adhesions and capillary morphogenesis in endothelial cells. J. Cell. Sci. 117 (2004) 4559-4569
17. Boulter E., Grall D., Cagnol S., and Van Obberghen-Schilling E. Regulation of cell-matrix adhesion dynamics and Rac-1 by integrin linked kinase. FASEB J. 20 (2006) 1489-1491
18. Filipenko N.R., Attwell S., Roskelley C., and Dedhar S. Integrin-linked kinase activity regulates Rac- and Cdc42-mediated actin cytoskeleton reorganization via alpha-PIX. Oncogene 24 (2005) 5837-5849
19. Lu H., Fedak P.W., Dai X., Du C., Zhou Y.Q., Henkelman M., Mongroo P.S., Lau A., Yamabi H., Hinek A., Husain M., Hannigan G., and Coles J.G. Integrin-linked kinase expression is elevated in human cardiac hypertrophy and induces hypertrophy in transgenic mice. Circulation 114 (2006) 2271-2279
20. Kiss E., Muranyi A., Csortos C., Gergely P., Ito M., Hartshorne D.J., and Erdodi F. Integrin-linked kinase phosphorylates the myosin phosphatase target subunit at the inhibitory site in platelet cytoskeleton. Biochem. J. 365 (2002) 79-87
21. Muranyi A., MacDonald J.A., Deng J.T., Wilson D.P., Haystead T.A., Walsh M.P., Erdodi F., Kiss E., Wu Y., and Hartshorne D.J. Phosphorylation of the myosin phosphatase target subunit by integrin-linked kinase. Biochem. J. 366 (2002) 211-216
22. Wilson D.P., Sutherland C., Borman M.A., Deng J.T., Macdonald J.A., and Walsh M.P. Integrin-linked kinase is responsible for Ca2+-independent myosin diphosphorylation and contraction of vascular smooth muscle. Biochem. J. 392 (2005) 641-648
23. Bayless K.J., and Davis G.E. The Cdc42 and Rac1 GTPases are required for capillary lumen formation in three-dimensional extracellular matrices. J. Cell. Sci. 115 (2002) 1123-1136
24. Cascone I., Giraudo E., Caccavari F., Napione L., Bertotti E., Collard J.G., Serini G., and Bussolino F. Temporal and spatial modulation of Rho GTPases during in vitro formation of capillary vascular network. Adherens junctions and myosin light chain as targets of Rac1 and RhoA. J. Biol. Chem. 278 (2003) 50702-50713
25. Connolly J.O., Simpson N., Hewlett L., and Hall A. Rac regulates endothelial morphogenesis and capillary assembly. Mol. Biol. Cell 13 (2002) 2474-2485
26. Vouret-Craviari V., Grall D., and Van Obberghen-Schilling E. Modulation of Rho GTPase activity in endothelial cells by selective proteinase-activated receptor (PAR) agonists. J. Thromb. Haemost. 1 (2003) 1103-1111
27. Mammoto A., Mammoto T., and Ingber D.E. Rho signaling and mechanical control of vascular development. Curr. Opin. Hematol. 15 (2008) 228-234
28. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., and Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411 (2001) 494-498
29. Sahai E., Garcia-Medina R., Pouyssegur J., and Vial E. Smurf1 regulates tumor cell plasticity and motility through degradation of RhoA leading to localized inhibition of contractility. J. Cell Biol. 176 (2007) 35-42
30. Deroanne C., Vouret-Craviari V., Wang B., and Pouyssegur J. EphrinA1 inactivates integrin-mediated vascular smooth muscle cell spreading via the Rac/PAK pathway. J. Cell. Sci. 116 (2003) 1367-1376
31. Deroanne C.F., Hamelryckx D., Ho T.T., Lambert C.A., Catroux P., Lapiere C.M., and Nusgens B.V. Cdc42 downregulates MMP-1 expression by inhibiting the ERK1/2 pathway. J. Cell. Sci. 118 (2005) 1173-1183
32. Gadea G., Lapasset L., Gauthier-Rouviere C., and Roux P. Regulation of Cdc42-mediated morphological effects: a novel function for p53. EMBO J. 21 (2002) 2373-2382
33. Pankov R., Endo Y., Even-Ram S., Araki M., Clark K., Cukierman E., Matsumoto K., and Yamada K.M. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170 (2005) 793-802
34. Etienne-Manneville S., and Hall A. Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106 (2001) 489-498
35. Small J.V., Rottner K., Kaverina I., and Anderson K.I. Assembling an actin cytoskeleton for cell attachment and movement. Biochim. Biophys. Acta 1404 (1998) 271-281
36. Zamir E., and Geiger B. Molecular complexity and dynamics of cell-matrix adhesions. J. Cell. Sci. 114 (2001) 3583-3590
37. Small J.V., and Kaverina I. Microtubules meet substrate adhesions to arrange cell polarity. Curr. Opin. Cell Biol. 15 (2003) 40-47
38. Giry M., Popoff M.R., von Eichel-Streiber C., and Boquet P. 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 (1995) 4063-4071
39. Ho T.T., Merajver S.D., Lapiere C.M., Nusgens B.V., and Deroanne C.F. RhoA-GDP regulates RhoB protein stability. Potential involvement of RhoGDIalpha. J. Biol. Chem. 283 (2008) 21588-21598
40. Davis G.E., and Senger D.R. Extracellular matrix mediates a molecular balance between vascular morphogenesis and regression. Curr. Opin. Hematol. 15 (2008) 197-203
41. Fiorentini C., Gauthier M., Donelli G., and Boquet P. Bacterial toxins and the Rho GTP-binding protein: what microbes teach us about cell regulation. Cell Death Differ. 5 (1998) 720-728
42. Jaffe A.B., and Hall A. Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21 (2005) 247-269
43. Bishop A.L., and Hall A. Rho GTPases and their effector proteins. Biochem. J. 348 Pt 2 (2000) 241-255
44. Wierzbicka-Patynowski I., and Schwarzbauer J.E. Regulatory role for SRC and phosphatidylinositol 3-kinase in initiation of fibronectin matrix assembly. J. Biol. Chem. 277 (2002) 19703-19708
45. Ilic D., Kovacic B., Johkura K., Schlaepfer D.D., Tomasevic N., Han Q., Kim J.B., Howerton K., Baumbusch C., Ogiwara N., Streblow D.N., Nelson J.A., Dazin P., Shino Y., Sasaki K., and Damsky C.H. FAK promotes organization of fibronectin matrix and fibrillar adhesions. J. Cell. Sci. 117 (2004) 177-187
46. Totsukawa G., Yamakita Y., Yamashiro S., Hartshorne D.J., Sasaki Y., and Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J. Cell Biol. 150 (2000) 797-806
47. Leiss M., Beckmann K., Giros A., Costell M., and Fassler R. The role of integrin binding sites in fibronectin matrix assembly in vivo. Curr. Opin. Cell Biol. 20 (2008) 502-507
48. Geiger B., and Bershadsky A. Assembly and mechanosensory function of focal contacts. Curr. Opin. Cell Biol. 13 (2001) 584-592
49. Zamir E., Katz B.Z., Aota S., Yamada K.M., Geiger B., and Kam Z. Molecular diversity of cell-matrix adhesions. J. Cell. Sci. 112 (1999) 1655-1669
50. Somlyo A.V., Bradshaw D., Ramos S., Murphy C., Myers C.E., and Somlyo A.P. Rho-kinase inhibitor retards migration and in vivo dissemination of human prostate cancer cells. Biochem. Biophys. Res. Commun. 269 (2000) 652-659
51. Uchida S., Watanabe G., Shimada Y., Maeda M., Kawabe A., Mori A., Arii S., Uehata M., Kishimoto T., Oikawa T., and Imamura M. The suppression of small GTPase rho signal transduction pathway inhibits angiogenesis in vitro and in vivo. Biochem. Biophys. Res. Commun. 269 (2000) 633-640
52. Hoang M.V., Whelan M.C., and Senger D.R. Rho activity critically and selectively regulates endothelial cell organization during angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 1874-1879
53. Mavria G., Vercoulen Y., Yeo M., Paterson H., Karasarides M., Marais R., Bird D., and Marshall C.J. ERK-MAPK signaling opposes Rho-kinase to promote endothelial cell survival and sprouting during angiogenesis. Cancer Cell 9 (2006) 33-44