TGFβ1 regulates endothelial cell spreading and hypertrophy through a Rac-p38-mediated pathway

Biology of the Cell

Volumn 100, Issue 9, 2008, Pages 537-550

  Varon, Christine ^a,b   Rottiers, Patricia ^a,b,c   Ezan, Jerome ^b,d,e   Reuzeau, Edith ^a,b,c   Basoni, Caroline ^a,b,f   Kramer, Ijsbrand ^a,b,c   Génot, Elisabeth ^a,b,c  

^a INSTITUT EUROPÉEN DE CHIMIE ET BIOLOGIE   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INSERM   (France)

^d U441   (France)

^e MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^f LAVAL UNIVERSITY   (Canada)

Author keywords

Cell spreading; Endothelial cell; Hypertrophy; p38; Rho GTPase; Transforming growth factor (TGF )

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; COLLAGEN TYPE 1; GUANOSINE TRIPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE P38; MUTANT PROTEIN; RAC1 PROTEIN; TRANSFORMING GROWTH FACTOR BETA1; ENZYME INHIBITOR; IMIDAZOLE DERIVATIVE; PROTEIN KINASE B; PYRIDINE DERIVATIVE;

ANIMAL CELL; AORTA; ARTICLE; ATHEROSCLEROSIS; CELL LINE; CELL SPREADING; CELL SURFACE; CELL SWELLING; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SWINE; VASCULAR ENDOTHELIUM; WOUND HEALING; ANIMAL; CELL SHAPE; CYTOLOGY; DRUG ANTAGONISM; HYPERTROPHY; METABOLISM; PATHOLOGY;

SUS;

ANIMALS; CELL LINE; CELL SHAPE; ENDOTHELIAL CELLS; ENZYME INHIBITORS; HYPERTROPHY; IMIDAZOLES; MAP KINASE SIGNALING SYSTEM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTO-ONCOGENE PROTEINS C-AKT; PYRIDINES; SWINE; TRANSFORMING GROWTH FACTOR BETA1;

EID: 50949127989     PISSN: 02484900     EISSN: None     Source Type: Journal    
DOI: 10.1042/BC20080021     Document Type: Article

References (57)

1. Andor, A., Trulzsch, K., Essler, M., Roggenkamp, A., Wiedemann, A., Heesemann, J. and Aepfelbacher, M. (2001) YopE of Yersinia, a GAP for Rho GTPases, selectively modulates Rac-dependent actin structures in endothelial cells. Cell Microbiol. 3, 301-310
2. Atfi, A., Djelloul, S., Chastre, E., Davis, R. and Gespach, C. (1997) Evidence for a role of Rho-like GTPases and stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK) in transforming growth factor beta-mediated signaling. J. Biol. Chem. 272, 1429-1432
3. Attisano, L. and Wrana, J.L. (2000) Smads as transcriptional co-modulators. Curr. Opin. Cell Biol. 12, 235-243
4. Bakin, A.V. , Rinehart, C., Tomlinson, A.K. and Arteaga, C.L. (2002) p38 mitogen-activated protein kinase is required for TGFβ-mediated fibroblastic transdifferentiation and cell migration. J. Cell Sci. 115, 3193-3206
5. Bhowmick, N.A., Ghiassi, M., Eakin, A., Aakre, M. , Lundquist, C.A., Engel, M.E., Arteaga, C.L. and Moses, H.L. (2001) Transforming growth factor-β1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell 12, 27-36
6. Carmona-Cuenca, I., Herrera, B., Ventura, J.J., Roncero, C., Fernandez, M. and Fabregat, I. (2006) EGF blocks NADPH oxidase activation by TGF-β in fetal rat hepatocytes, impairing oxidative stress, and cell death. J. Cell. Physiol. 207, 322-330
7. Chiu, C., Maddock, D.A., Zhang, Q., Souza, K.P., Townsend, A.R. and Wan, Y (2001) wTGF-β-induced p38 activation is mediated by Rac1-regulated generation of reactive oxygen species in cultured human keratinocytes. Int. J. Mol. Med. 8, 251-255
8. Conejo, R. and Lorenzo, M. (2001) Insulin signaling leading to proliferation, survival, and membrane ruffling in C2C12 myoblasts. J. Cell. Physiol. 187, 96-108
9. Davis, W., Stephens, L.R., Hawkins, P.T. and and Saklatvala, J. (1999) Synergistic activation of JNK/SAPK by interleukin-1 and platelet-derived growth factor is independent of Rac and Cdc42. Biochem. J. 338, 387-392
10. del Pozo, M.A., Alderson, N.B., Kiosses, W.B., Chiang, H.H., Anderson, R.G. and Schwartz, M.A. (2004) Integrins regulate Rac targeting by internalization of membrane domains. Science 303, 839-842
11. Edlund, S., Landstrom, M., Heldin, C.H. and Aspenstrom, P. (2002) Transforming growth factor-β-induced mobilization of actin cytoskeleton requires signaling by small GTPases Cdc42 and RhoA. Mol. Biol. Cell 13, 902-914
12. Engel, M.E., McDonnell, M.A., Law, B.K. and Moses, H.L. (1999) Interdependent SMAD and JNK signaling in transforming growth factor-beta-mediated transcription. J. Biol. Chem. 274, 37413-37420
13. 2+-mediated activation of Rap1 in human platelets. EMBO J. 16, 252-259
14. Gao, Y., Dickerson, J.B., Guo, F., Zheng, J. and Zheng, Y. (2004) Rational design and characterization of a Rac GTPase-specific small molecule inhibitor. Proc. Natl. Acad. Sci. U.S.A. 101, 7618-7623
15. Goldberg, P.L., MacNaughton, D.E., Clements, R.T, Minnear, F.L. and Vincent, P.A. (2002) p38 MAPK activation by TGF-β1 increases MLC phosphorylation and endothelial monolayer permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 282, L146-L154
16. Gregg, D., Rauscher, F.M. and Goldschmidt-Clermont, P.J. (2003) Rac regulates cardiovascular superoxide through diverse molecular interactions: more than a binary GTP switch. Am. J. Physiol. Cell Physiol. 285, C723-C734
17. Hall, A. (1998) Rho GTPases and the actin cytoskeleton. Science. 29, 509-514
18. Hedges, J.C., Dechert, M.A., Yamboliev, I.A., Martin, J.L., Hickey, E., Weber, L.A. and Gerthoffer, W.T. (1999) A role for p38(MAPK)/HSP27 pathway in smooth muscle cell migration. J. Biol. Chem. 274, 24211-24219
19. Hutchison, K.J. (1991) Endothelial cell morphology around graded stenoses of the dog common carotid artery. Blood Vessels 28, 396-406
20. Kim, H.P., Kim, T.Y., Lee, M.S., Jong, H.S., Lee, J.W. and Bang, Y.J. (2005) TGF-β1-mediated activations of c-Src and Rac1 modulate levels of cyclins and p27(Kip1) CDK inhibitor in hepatoma cells replated on fibronectin. Biochim. Biophys. Acta 1743, 151-161
21. Kramer, I.M., Patel, R., Spargo, D. and Riley, P. (1994) Initiation of growth inhibition by TGFβ1 is unlikely to occur in G1. J. Cell Sci. 107, 3469-3475
22. Lamouille, S. and Derynck, R. (2007) Cell size and invasion in TGF-β induced epithelial to mesenchymal transition is regulated by activation of the mTOR pathway. J. Cell Biol. 178, 437-451
23. Larsson, J., Goumans, M.J., Sjostrand, L.J., van Rooijen, M.A., Ward, D., Leveen, R, Xu, X., ten Dijke, P., Mummery, C.L. and Karlsson, S. (2001) Abnormal angiogenesis but intact hematopoietic potential in TGF-β type I receptor-deficient mice. EMBO J. 20, 1663-1673
24. Leeuwen, F.N., Kain, H.E., Kammen, R.A., Michiels, F., Kranenburg, O.W. and Collard, J.G. (11997) The guanine nucleotide exchange factor Tiam1 affects neuronal morphology; opposing roles for the small GTPases Rac and Rho. J. Cell Biol. 139, 797-807
25. Lim, J.Y, Park, S.J., Hwang, H.Y, Park, E.J., Nam, J.H., Kim, J. and Park, S.I. (2005) TGF-β1 induces cardiac hypertrophic responses via PKC-depenclent ATF-2 activation. J. Mol. Cell. Cardiol. 39, 627-636
26. Madri, J.A., Pratt, B. M. and Yannariello-Brown, J. (1988) Matrix-driven cell size change modulates aortic endothelial cell proliferation and sheet migration. Am. J. Pathol. 132, 18-27
27. Madri, J.A., Reidy, M.A., Kocher, O. and Bell, L. (1989) Endothelial cell behavior after denudation injury is modulated by transforming growth factor-beta1 and fibronectin. Lab. Invest. 60, 755-765
28. Marchuk, D.A., Srinivasan, S., Squire, T.L. and Zawistowski, J.S. (2003) Vascular morphogenesis: tales of two syndromes. Hum. Mol. Genet. 12, R97-R112
29. Massague, J. and Wotton, D. (2000) Transcriptional control by the TGF-β/ Smad signaling system. EMBO J. 19, 1745-1754
30. Mazharian, A., Roger, S., Maurice, P., Berrou, E., Popoff, M.R., Hoylaerts, M.F., Fauvel-Lafeve, F., Bonnefoy, A. and Bryckaert, M. (2005) Differential Involvement of ERK2 and p38 in platelet adhesion to collagen. J. Biol. Chem. 280, 26002-26010
31. Meriane, M., Charrasse, S., Comunale, F., Mery, A., Fort, P., Roux, P. and Gauthier-Rouviere, C. (2002) Participation of small GTPases Rac1 and Cdc42Hs in myoblast transformation. Oncogene 21, 2901-2907
32. Merrilees, M.J. and Sodek, J. (1992) Synthesis of TGF-β1 by vascular endothelial cells is correlated with cell spreading. J. Vasc. Res. 29, 376-384
33. Miettinen, P.J., Ebner, R., Lopez, A.R. and Derynck, R. (1994) TGF-β induced transdifferentiation of mammary epithelial cells to mesenchymal cells: involvement of type I receptors. J. Cell Biol. 127, 2021-2036
34. Newton, L.K., Yung, W.K., Pettigrew, L.C. and Steck, P.A. (1990) Growth regulatory activities of endothelial extracellular matrix: mediation by transforming growth factor-beta. Exp. Cell Res. 190, 127-132
35. Ogura, M. and Kitamura, M. (1998) Oxidant stress incites spreading of macrophages via extracellular signal-regulated kinases and p38 mitogen-activated protein kinase. J. Immunol. 161, 3569-3574
36. Pepper, M.S. (1997) Transforming growth factor-beta: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 8, 21-43
37. Pepper, M.S., Vassalli, J.D., Orci, L. and Montesano, R. (1993) Biphasic effect of transforming growth factor-β1 on in vitro angiogenesis. Exp. Cell Res. 204, 356-363
38. Pertovaara, L., Sistonen, L., Bos, T.J., Vogt, P.K., Keski-Oja, J. and Alitalo, K. (1989) Enhanced jun gene expression is an early genomic response to transforming growth factor beta stimulation. Mol. Cell. Biol. 9, 1255-1262
39. Pettersson, A., Nagy, J.A., Brown, L.F, Sundberg, C., Morgan, E., Jungles, S., Carter, R., Krieger, J.E., Manseau, E.J., Harvey, V.S., Eckelhoefer, I.A., Feng, D., Dvorak, A.M., Mulligan, R.C. and Dvorak, H.F. (2000) Heterogeneity of the angiogenic response induced in different normal adult tissues by vascular permeability factor/vascular endothelial growth factor. Lab. Invest. 80, 99-115
40. Price, L.S., Leng, J., Schwartz, M.A. and Bokoch, G.M. (1998) Activation of Rac and Cdc42 by integrins mediates cell spreading. Mol. Biol. Cell 9, 1863-1871
41. Ren, X.D., Kiosses, W.B. and Schwartz, M.A. (1999) Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18, 578-585
42. Repin, V.S., Dolgov, V.V., Zaikina, O.E., Novikov, I.D., Antonov, A.S., Nikolaeva, M.A. and Smirnov, V.N. (1984) Heterogeneity of endothelium in human aorta, A quantitative analysis by scanning electron microscopy. Atherosclerosis 50, 35-52
43. Ridley, A.J., Paterson, H.F, Johnston, C.L., Diekmann, D. and Hall, A. (1992) The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70, 401-410
44. Sakai, H., Chen, Y., Itokawa, T., Yu, K.P., Zhu, M.L. and Insogna, K. (2006) Activated c-Fms recruits Vav and Rac during CSF-1-induced cytoskeletal remodeling and spreading in osteoclasts. Bone 39, 1290-1301
45. Sander, E.E., van Delft, S., ten Klooster, J.P., Reid, T, van der Kammen, R.A., Michiels, F. and Collard, J.G. (1998) Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143, 1385-1398
46. Ueda, Y., Wang, S., Dumont, N., Yi, J.Y., Koh, Y and Arteaga, C.L. (2004) Overexpression of HER2 (erbB2) in human breast epithelial cells unmasks transforming growth factor beta-induced cell motility. J. Biol. Chem. 279, 24505-24513
47. van Leeuwen, F.N., van Delft, S., Kain, H.E., van der Kammen, R.A. and Collard, J.G. (1999) Rac regulates phosphorylation of the myosin-II heavy chain, actinomyosin disassembly and cell spreading. Nat, Cell Biol. 1, 242-248
48. van Wetering, S., van den Berk, N., van Buul, J.D., Mul, F.P., Lommerse, I., Mous, R., ten Klooster, J.P., Zwaginga, J.J. and Hordijk, P.L. (2003) VCAM-1-mediated Rac signaling controls endothelial cell-cell contacts and leucocyte transmigration. Am. J. Physiol. Cell Physiol. 285, C343-C352
49. Varon, C., Basoni, C., Reuzeau, E., Moreau, V., Kramer, I.J. and Genot, E. (2006a) TGFbeta1-induced aortic endothelial morphogenesis requires signaling by small GTPases Rac1 and RhoA. Exp. Cell Res. 312, 3604-3619
50. Varon, C., Tatin, F., Moreau, V., Van Obberghen-Schilling, E., Fernandez-Sauze, S., Reuzeau, E., Kramer, I. and Genot, E. (2006b) Transforming growth factor beta induces rosettes of podosomes in primary aortic endothelial cells. Mol. Cell. Biol. 26, 3582-3594
51. Vouret-Craviari, V., Bourcier, C., Boulter, E. and vanObberghen-Schilling, E. (2002) Distinct signals via Rho GTPases and Src drive shape changes by thrombin and sphingosine-1-phosphate in endothelial cells. J. Cell Sci. 115, 2475-2484
52. Watkins, S.J., Jonker, L. and Arthur, H.M. (2006) A direct interaction between TGFbeta activated kinase 1 and the TGFbeta type II receptor: implications for TGFbeta signalling and cardiac hypertrophy. Cardiovasc Res. 69, 432-439
53. Welch, H., Eguinoa, A., Stephens, L.R. and Hawkins, P.T. (1998) Protein kinase B and rac; are activated in parallel within a phosphatidylinositide 3OH-kinase-controlled signaling pathway. J. Biol. Chem. 273, 11248-11256
54. Wilkes, M.C., Murphy, S.J., Garamszegi, N. and Leof, E.B. (2003) Cell-type-specific activation of PAK2 by transforming growth factor beta independent of Smad2 and Smad3. Mol. Cell. Biol. 23, 8878-8889
55. Wojciak-Stothard, B. and Ridley, A.J. (2002) Rho GTPases and the regulation of endothelial permeability. Vascul. Pharmacol. 39, 187-199
56. Zhou, K., Wang, Y, Gorski, J.L., Nomura, N., Collard, J. and Bokoch, G. M. (1998) Guanine nucleotide exchange factors regulate specificity of downstream signaling from Rac and Cdc42. J. Biol. Chem. 273, 16782-16786
57. Zicha, D., Genot, E., Dunn, G.A. and Kramer, I.M. (1999) TGFß1 induces a cell-cycle-dependent increase in motility of epithelial cells. J. Cell Sci. 112, 447-454