Activation of Cdc42, Rac, PAK, and Rho-kinase in response to hepatocyte growth factor differentially regulates epithelial cell colony spreading and dissociation

Molecular Biology of the Cell

Volumn 11, Issue 5, 2000, Pages 1709-1725

  Royal, Isabelle ^a   Lamarche Vane, Nathalie ^b   Lamorte, Louie ^a,b   Kaibuchi, Kozo ^c   Park, Morag ^a,b  

^a MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

^b MCGILL UNIVERSITY   (Canada)

^c NARA INSTITUTE OF SCIENCE AND TECHNOLOGY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE; PROTEIN P21; PROTEIN TYROSINE KINASE; RAC PROTEIN; RHO KINASE; SCATTER FACTOR; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ARTICLE; CELL SPREADING; CELL STRAIN; CELL STRAIN COS1; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; EPITHELIUM CELL; LAMELLIPODIUM; MESENCHYME; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

EID: 0034108503     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.11.5.1709     Document Type: Article

References (72)

1. Adler, V., Franklin, C.C., and Kraft, A.S. (1992). Phorbol esters stimulate the phosphorylation of c-Jun but not v-Jun: regulation by the N-terminal ∂ domain. Proc. Natl. Acad. Sci. USA 89, 5341-5345.
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. Amano, M., Chihara, K., Kimura, K., Fukata, Y., Nakamura, N., Matsuura, Y., and Kaibuchi, K. (1997). Formation of actin stress fibers and focal adhesions enhanced by Rho-kinase. Science 275, 1308-1311.
4. Amano, M., Chihara, K., Nakamura, N., Fukata, Y., Yano, T., Shibata, M., Ikebe, M., and Kaibuchi, K. (1998). Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes Cells 3, 177-188.
5. Amano, M., Ito, M., Kimura, K., Fukata, Y., Chihara, K., Nakano, T., Matsuura, Y., and Kaibuchi, K. (1996). Phosphorylation and activation of myosin by Rho-associated kinase (Rho-kinase). J. Biol. Chem. 277, 20246-20249.
6. Aspenström, P. (1999). Effectors for the Rho GTPases. Curr. Opin. Cell Biol. 11, 95-102.
7. Aspenström, P., Lindberg, U., and Hall, A. (1996). Two GTPases, Cdc42 and Rac, bind directly to a protein implicated in the immunodeficiency disorder Wiskott Aldrich syndrome. Curr. Biol. 6, 70-75.
8. Bagrodia, S., Derijard, B., Davis, R.J., and Cerione, R.A. (1995a). Cdc42 and PAK-mediated signaling leads to Jun kinase and p38 mitogen-activated protein kinase activation. J. Biol. Chem. 270, 27995-27998.
9. Bagrodia, S., Taylor, S.J., Creasy, C.L., Chernoff, J., and Cerione, R.A. (1995b). Identification of a mouse p21Cdc42/Rac activated kinase. J. Biol. Chem. 270, 22731-22737.
10. Bardelli, A., Pugliese, L., and Comoglio, P.M. (1997). "Invasive-growth" signaling by the Met/HGF receptor: the hereditary renal carcinoma connection. Biochim. Biophys. Acta 1333, M41-M51.
11. Benard, V., Bohl, B.P., and Bokoch, G.M. (1999). Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274, 13198-13204.
12. Birchmeier, C., and Gherardi, E. (1998). Developmental roles of HGF/SF and its receptor, the c-Met tyrosine kinase. Trends Cell Biol. 10, 404-410.
13. Brown, J.L., Stowers, L., Baer, M., Trejo, J., Coughlin, S., and Chant, J. (1996). Human Ste20 homologue hPAK1 links GTPases to the JNK MAP kinase pathway. Curr. Biol. 6, 598-605.
14. Burridge, K. (1999). Crosstalk between Rac and Rho. Science 283, 2028-2029.
15. Bussolino, F., Di Renzo, M.F., Ziche, M., Bocchietto, E., Olivero, M., Naldini, L., Gaudino, G., Tamagnone, L., Coffer, A., and Comoglio, P.M. (1992). Hepatocyte growth factor is a potent angiogenic factor which stimulates endothelial cell motility and growth. J. Cell Biol. 119, 629-641.
16. Cerione, R.A., and Zheng, Y. (1996). The Dbl family of oncogenes. Curr. Opin. Cell Biol. 8, 216-222.
17. Clark, E.A., King, W.G., Brugge, J.S., Symons, M., and Hynes, R.O. (1998). Integrin-mediated signals regulated by members of the Rho family of GTPases. J. Cell Biol. 142, 573-586.
18. Coso, O.A., Chiariello, M., Yu, J.-C., Teramoto, H., Crespo, P., Xu, N., Miki, T., and Gutkind, J.S. (1995). The small GTP-binding protein Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
19. Dharmawardhane, S., Sanders, L.C., Martin, S.S., Daniels, R.H., and Bokoch, G.M. (1997). Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J. Cell Biol. 138, 1265-1278.
20. D'Souza-Schorey, C., Boettner, B., and Van Aelst, L. (1998). Rac regulates integrin-mediated spreading and increased adhesion of T lymphocytes. Mol. Cell. Biol. 18, 3936-3946.
21. Frost, J.A., Khokhlatchev, A., Stippec, S., White, M.A., and Cobb, M.H. (1998). Differential effects of Pak1-activating mutations reveal activity-dependent and -independent effects on cytoskeletal regulation. J. Biol. Chem. 273, 28191-28198.
22. Fukata, Y., Oshiro, N., Kinoshita, N., Kawano, Y., Matsuoka, Y., Bennett, V., Matsuura, Y., and Kaibuchi, K. (1999). Phosphorylation of adducin by Rho-kinase plays a crucial role in cell motility. J. Cell Biol. 145, 347-361.
23. Grant, D.S., Kleinman, H.K., Goldberg, I.D., Bhargava, M.M., Nickoloff, B.J., Kinsella, J.L., Polverini, P., and Rosen, E.M. (1993). Scatter factor induces blood vessel formation in vivo. Proc. Natl. Acad. Sci. USA 90, 1937-1941.
24. Hall, A. (1998). Rho GTPases and the actin cytoskeleton. Science 279, 509-514.
25. Han, J., Luby-Phelps, K., Das, B., Shu, X., Xia, Y., Mosteller, R.D., Krishna, U.M., Falck, J.R., White, M.A., and Broek, D. (1998). Role of substrates and products of PI 3-kinase in regulating activation of Rac-related guanosine triphosphatases by Vav. Science 279, 558-560.
26. Hartmann, G., Weidner, K.M., Schwarz, H., and Birchmeier, W. (1994). The motility signal of scatter factor/hepatocyte growth factor mediated through the receptor tyrosine kinase Met requires intracellular action of Ras. J. Biol. Chem. 269, 21936-21939.
27. Hordijk, P.L., ten Klooster, J.P., van der Kammen, R.A., Michiels, F., Oomen, L.C.J.M., and Collard, J.G. (1997). Inhibition of invasion of epithelial cells by Tiam1-Rac signaling. Science 278, 1464-1466.
28. Ishizaki, T., et al. (1996). The small GTP-binding protein Rho binds to and activates a 160 kDa Ser/Thr protein kinase homologous to myotonic dystrophy kinase. EMBO J. 15, 1885-1893.
29. Ishizaki, T., Naito, M., Fujisawa, K., Maekawa, M., Watanabe, N., Saito, Y., and Narumiya, S. (1997). p160ROCK, a Rho-associated coiled-coil forming protein kinase, works downstream of Rho and induces focal adhesions. FEBS Lett. 404, 118-124.
30. Itoh, K., Yoshioka, K., Akedo, H., Uehata, M., Ishizaki, T., and Narumiya, S. (1999). An essential part for Rho-associated kinase in the transcellular invasion of tumor cells. Nat. Med. 5, 221-225.
31. Jeffers, M., Rong, S., and Vande Woude, G.F. (1996). Hepatocyte growth factor/scatter factor-Met signaling in tumorigenicity and invasion/metastasis. Mol. Med. 74, 505-513.
32. Joneson, T., McDonough, M., Bar-Sagi, D., and Van Aelst, L. (1996). Rac regulation of actin polymerization and proliferation by a pathway distinct from Jun kinase. Science 274, 1374-1376.
33. Jou, T.-S., and Nelson, W.J. (1998). Effects of regulated expression of mutant RhoA and Rac1 small GTPases on the development of epithelial (MDCK) cell polarity. J. Cell Biol. 142, 85-100.
34. Khwaja, A., Lehmann, K., Marte, B., and Downward, J. (1998). Phosphoinositide 3-kinase induces scattering and tubulogenesis in epithelial cells through a novel pathway. J. Biol. Chem. 273, 18793-18801.
35. Kimura, K., et al. (1996). Regulation of myosin phosphatase by Rho and Rho-associated kinase (Rho-kinase). Science 273, 245-248.
36. Kiosses, W.B., Daniels, R.H., Otey, C., Bokoch, G.M., and Schwartz, M.A. (1999). A role for p21-activated kinase in endothelial cell migration. J. Cell Biol. 147, 831-843.
37. Kozma, R., Ahmed, S., Best, A., and Lim, L. (1995). The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15, 1942-1952.
38. Kuroda, S., Fukata, M., Fujii, K., Nakamura, T., Izawa, I., and Kaibuchi, K. (1997). Regulation of cell-cell adhesion of MDCK cells by Cdc42 and Rac1 small GTPases. Biochem. Biophys. Res. Commun. 240, 430-435.
39. Lamarche, N., and Hall, A. (1994). GAPs for rho-related GTPases. Trends Genet. 10, 436-440.
40. PAK and the JNK/SAPK MAP kinase cascade. Cell 87, 519-529.
41. Leung, T., Chen, X.-Q., Manser, E., and Lim, L. (1996). The p160 RhoA-binding kinase ROKa is a member of a kinase family and is involved in the reorganisation of the cytoskeleton. Mol. Cell. Biol. 36, 5313-5327.
42. Leung, T., Manser, E., Tan, L., and Lim, L. (1995). A novel serine/ threonine kinase binding the Ras-related RhoA GTPase which translocates the kinase to peripheral membranes. J. Biol. Chem. 270, 29051-29054.
43. Manser, E., Huang, H-Y., Loo, T.-H., Chen, X.-Q., Dong, J.-M., Leung, T., and Lim, L. (1997). Expression of constitutively active α-PAK reveals effects of the kinase on actin and focal complexes. Mol. Cell. Biol. 17, 1129-1143.
44. Manser, E., Leung, T., Salihuddin, H., Zhao, Z.S., and Lim, L. (1994). A brain serine/threonine protein kinase activated by Cdc42 and Rac1. Nature 367, 40-46.
45. Manser, E., Loo, T.-H., Koh, C.-G., Zhao, Z.-S., Chen, X.-Q., Tan, L., Tan, I., Leung, T., and Lim, L. (1998). Pak kinases are directly coupled to the Pix family of nucleotide exchange factors. Mol. Cell. 1, 183-192.
46. Martin, G.A., Bollag, G., McCormick, F., and Abo, A. (1995). A novel serine kinase activated by rac1/CDC42Hs-dependent autophosphorylation is related to PAK65 and STE20. EMBO J. 14, 1970-1978.
47. Matsui, T., Amano, M., Yamamoto, T., Chihara, K., Nakafuku, M., Ito, M., Nakano, T., Okawa, K., Iwamatsu, A., and Kaibuchi, K. (1996). Rho-associated kinase, a novel serine/threonine kinase, as a putative target for the small GTP binding protein Rho. EMBO J. 25, 2208-2216.
48. Matsumoto, K., and Nakamura, T. (1996). Emerging multipotent aspects of hepatocyte growth factor. J. Biochem. 119, 591-600.
49. Matsumoto, K., and Nakamura, T. (1997). Hepatocyte growth factor (HGF) as a tissue organizer for organogenesis and regeneration. Biochem. Biophys. Res. Commun. 239, 639-644.
50. Minden, A., Lin, A., Claret, F.-X., Abo, A., and Karin, M. (1995). Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157.
51. Mitchison, T.J., and Cramer, L.P. (1996). Actin-based cell motility and cell locomotion. Cell 84, 371-379.
52. Montesano, R., Soriano, J.V., Pepper, M.S., and Orci, L. (1997). Induction of epithelial branching tubulogenesis in vitro. J. Cell Physiol. 173, 152-161.
53. Nobes, C.D., and Hall, A. (1995). Rho, Rac and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia and filopodia. Cell 81, 53-62.
54. Nobes, C.D., and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
55. Nobes, C.D., Hawkins, P., Stephens, L., and Hall, A. (1995). Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108, 225-233.
56. Obermeier, A., Ahmed, S., Manser, E., Yen, S.C., Hall, C., and Lim, L. (1998). PAK promotes morphological changes by acting upstream of Rac. EMBO J. 17, 4328-4339.
57. Olson, M.F., Ashworth, A., and Hall, A. (1995). An essential role for Rho, Rac and Cdc42 GTPases in cell cycle progression through G1. Science 269, 1270-1272.
58. Potempa, S., and Ridley, A.J. (1998). Activation of both MAP kinase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol. Biol. Cell 9, 2185-2200.
59. 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.
60. Ridley, A.J., Comoglio, P.M., and Hall, A. (1995). Regulation of scatter factor/hepatocyte growth factor responses by Ras, Rac, and Rho in MDCK cells. Mol. Cell. Biol. 15, 1110-1122.
61. Ridley, A.J., and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399.
62. 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.
63. Royal, I., and Park, M. (1995). Hepatocyte growth factor-induced scatter of MDCK cells requires phosphatidylinositol 3-kinase. J. Biol. Chem. 270, 27780-27787.
64. Sander, E.E., vanDelft, 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.
65. Sanders, L.C., Matsumura, F., Bokoch, G.M., and de Lanerolle, P. (1999). Inhibition of myosin light chain kinase by p21-activated kinase. Science 283, 2083-2085.
66. Sells, M.A., Knaus, U.G., Bagrodia, S., Ambrose, D.M., Bokoch, C.M., and Chernoff, J. (1997). Human p21-activated kinase (Pak1) regulates actin organization in mammalian cells. Curr. Biol. 7, 202-210.
67. Takaishi, K., Sasaki, T., Kotani, H., Nishioka, H., and Takai, Y. (1997). Regulation of cell-cell adhesion by Rac and Rho small G proteins in MDCK cells. J. Cell Biol. 139, 1047-1059.
68. Tu, H., and Wigler, M. (1999). Genetic evidence for Pak1 autoinhibition and its release by Cdc42. Mol. Cell. Biol. 19, 602-611.
69. Uehata, M., et al. (1997). Calcium sensitization of smooth muscle mediated by a Rho-associated protein kinase in hypertension. Nature 389, 990-994.
70. Wennstrom, S., Hawkins, P., Cooke, F., Hara, K., Yonezawa, K., Kasuga, M., Jackson, T., Claesson-Welsh, L., and Stephens, L. (1994). Activation of phosphoinositide 3-kinase is required for PDGF-stimulated membrane ruffling. Curr. Biol. 4, 385-393.
71. Zhao, Z.-S., Manser, E., Chen, X.-Q., Chong, C., Leung, T., and Lim, L. (1998). A conserved negative regulatory region in αPAK: inhibition of PAK kinases reveals their morphological roles downstream of Cdc42 and Rac1. Mol. Cell. Biol. 18, 2153-2163.
72. Zhu, H., Naujokas, M.A., and Park, M. (1994). Receptor chimeras indicate that the Met tyrosine kinase mediates the motility and morphogenic responses of hepatocyte growth factor/scatter factor. Cell Growth Differ. 5, 359-366.