Focal-adhesion targeting links caveolin-1 to a Rac1-degradation pathway

Journal of Cell Science

Volumn 123, Issue 11, 2010, Pages 1948-1958

  Nethe, Micha ^a   Anthony, Eloise C ^a   Fernandez Borja, Mar ^a   Dee, Rob ^a   Geerts, Dirk ^a   Hensbergen, Paul J ^b   Deelder, André M ^b   Schmidt, Gudula ^c   Hordijk, Peter L ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF FREIBURG   (Germany)

Author keywords

Adhesion; Caveolin 1; Rac1GTPase; Ubiquitylation

Indexed keywords

CAVEOLIN 1; FOCAL ADHESION KINASE; GUANOSINE TRIPHOSPHATE; RAC1 PROTEIN; SHORT HAIRPIN RNA; SMALL INTERFERING RNA; ACTIN; EHT 1864; PYRONE DERIVATIVE; QUINOLINE DERIVATIVE;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MIGRATION; ENDOTHELIUM CELL; EPITHELIUM CELL; FIBROBLAST; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UBIQUITINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL MOTION; CELL SURFACE; CONFOCAL MICROSCOPY; DRUG EFFECTS; FEEDBACK SYSTEM; FOCAL ADHESION; GENETICS; HELA CELL LINE; METABOLISM; PATHOLOGY;

ACTINS; ANIMALS; CAVEOLIN 1; CELL MOVEMENT; CELL SURFACE EXTENSIONS; FEEDBACK, PHYSIOLOGICAL; FIBROBLASTS; FOCAL ADHESIONS; HELA CELLS; HUMANS; MICE; MICROSCOPY, CONFOCAL; PYRONES; QUINOLINES; RAC1 GTP-BINDING PROTEIN; RNA, SMALL INTERFERING;

EID: 77953162073     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.062919     Document Type: Article

References (62)

1. Beardsley, A., Fang, K., Mertz, H., Castranova, V., Friend, S. and Liu, J. (2005). Loss of caveolin-1 polarity impedes endothelial cell polarization and directional movement. J. Biol. Chem. 280, 3541-3547.
2. Bernards, A. and Settleman, J. (2004). GAP control: regulating the regulators of small GTPases. Trends Cell. Biol. 14, 377-385.
3. Bershadsky, A. D., Ballestrem, C., Carramusa, L., Zilberman, Y., Gilquin, B., Khochbin, S., Alexandrova, A. Y., Verkhovsky, A. B., Shemesh, T. and Kozlov, M. M. (2006). Assembly and mechanosensory function of focal adhesions: experiments and models. Eur. J. Cell Biol. 85, 165-173.
4. Bos, J. L., Rehmann, H. and Wittinghofer, A. (2007). GEFs and GAPs: critical elements in the control of small G proteins. Cell 129, 865-877.
5. -/- cells. Mol. Biol. Cell 17, 2489-2497.
6. Chen, Y., Yang, Z., Meng, M., Zhao, Y., Dong, N., Yan, H., Liu, L., Ding, M., Peng, H. B. and Shao, F. (2009). Cullin mediates degradation of RhoA through evolutionarily conserved BTB adaptors to control actin cytoskeleton structure and cell movement. Mol. Cell 35, 841-855.
7. Conrad, P. A., Smart, E. J., Ying, Y. S., Anderson, R. G. and Bloom, G. S. (1995). Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J. Cell Biol. 131, 1421-1433.
8. 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.
9. del Pozo, M. A., Balasubramanian, N., Alderson, N. B., Kiosses, W. B., Grande-Garcia, A., Anderson, R. G. and Schwartz, M. A. (2005). Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell. Biol. 7, 901-908.
10. DerMardirossian, C. and Bokoch, G. M. (2005). GDIs: central regulatory molecules in Rho GTPase activation. Trends Cell. Biol. 15, 356-363.
11. Dovas, A. and Couchman, J. R. (2005). RhoGDI: multiple functions in the regulation of Rho family GTPase activities. Biochem. J. 390, 1-9.
12. Doye, A., Mettouchi, A., Bossis, G., Clement, R., Buisson-Touati, C., Flatau, G., Gagnoux, L., Piechaczyk, M., Boquet, P. and Lemichez, E. (2002). CNF1 exploits the ubiquitin-proteasome machinery to restrict Rho GTPase activation for bacterial host cell invasion. Cell 111, 553-564. (Pubitemid 35356560)
13. Dull, T., Zufferey, R., Kelly, M., Mandel, R. J., Nguyen, M., Trono, D. and Naldini, L. (1998). A third-generation lentivirus vector with a conditional packaging system. J. Virol. 72, 8463-8471. (Pubitemid 28471781)
14. Enomoto, T. (1996). Microtubule disruption induces the formation of actin stress fibers and focal adhesions in cultured cells: possible involvement of the rho signal cascade. Cell Struct. Funct. 21, 317-326.
15. Flatau, G., Lemichez, E., Gauthier, M., Chardin, P., Paris, S., Fiorentini, C. and Boquet, P. (1997). Toxin-induced activation of the G protein p21 Rho by deamidation of glutamine. Nature 387, 729-733. (Pubitemid 27270616)
16. Gabert, J., Beillard, E., van der Velden, V. H., Bi, W., Grimwade, D., Pallisgaard, N., Barbany, G., Cazzaniga, G., Cayuela, J. M., Cave, H. et al. (2003). Standardization and quality control studies of 'real-time' quantitative reverse transcriptase polymerase chain reaction of fusion gene transcripts for residual disease detection in leukemia - a Europe Against Cancer program. Leukemia 17, 2318-2357.
17. Gaus, K., Le Lay, S., Balasubramanian, N. and Schwartz, M. A. (2006). Integrinmediated adhesion regulates membrane order. J. Cell Biol. 174, 725-734. (Pubitemid 44306728)
18. Gingras, D., Gauthier, F., Lamy, S., Desrosiers, R. R. and Beliveau, R. (1998). Localization of RhoA GTPase to endothelial caveolae-enriched membrane domains. Biochem. Biophys. Res. Commun. 247, 888-893. (Pubitemid 28418486)
19. Goetz, J. G., Joshi, B., Lajoie, P., Strugnell, S. S., Scudamore, T., Kojic, L. D. and Nabi, I. R. (2008). Concerted regulation of focal adhesion dynamics by galectin-3 and tyrosine-phosphorylated caveolin-1. J. Cell Biol. 180, 1261-1275. (Pubitemid 351468479)
20. Grande-Garcia, A., Echarri, A., de Rooij, J., Alderson, N. B., Waterman-Storer, C. M., Valdivielso, J. M. and del Pozo, M. A. (2007). Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 177, 683-694.
21. Gratton, J. P., Lin, M. I., Yu, J., Weiss, E. D., Jiang, Z. L., Fairchild, T. A., Iwakiri, Y., Groszmann, R., Claffey, K. P., Cheng, Y. C. et al. (2003). Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell 4, 31-39.
22. Haeusler, L. C., Blumenstein, L., Stege, P., Dvorsky, R. and Ahmadian, M. R. (2003). Comparative functional analysis of the Rac GTPases. FEBS Lett. 555, 556-560. (Pubitemid 37532610)
23. Haglund, K., Di Fiore, P. P. and Dikic, I. (2003). Distinct monoubiquitin signals in receptor endocytosis. Trends Biochem. Sci. 28, 598-603.
24. Hill, M. M., Scherbakov, N., Schiefermeier, N., Baran, J., Hancock, J. F., Huber, L. A., Parton, R. G. and Parat, M. O. (2007). Reassessing the role of phosphocaveolin-1 in cell adhesion and migration. Traffic 8, 1695-1705. (Pubitemid 350066682)
25. Ho, A., Schwarze, S. R., Mermelstein, S. J., Waksman, G. and Dowdy, S. F. (2001). Synthetic protein transduction domains: enhanced transduction potential in vitro and in vivo. Cancer Res. 61, 474-477.
26. Hope, T. J., Huang, X. J., McDonald, D. and Parslow, T. G. (1990). Steroid-receptor fusion of the human immunodeficiency virus type 1 Rev transactivator: mapping cryptic functions of the arginine-rich motif. Proc. Natl. Acad. Sci. USA 87, 7787-7791. (Pubitemid 20341802)
27. Joseph, G., Gorzalczany, Y., Koshkin, V. and Pick, E. (1994). Inhibition of NADPH oxidase activation by synthetic peptides mapping within the carboxyl-terminal domain of small GTP-binding proteins. Lack of amino acid sequence specificity and importance of polybasic motif. J. Biol. Chem. 269, 29024-29031. (Pubitemid 24983047)
28. Joshi, B., Strugnell, S. S., Goetz, J. G., Kojic, L. D., Cox, M. E., Griffith, O. L., Chan, S. K., Jones, S. J., Leung, S. P., Masoudi, H. et al. (2008). Phosphorylated caveolin-1 regulates Rho/ROCK-dependent focal adhesion dynamics and tumor cell migration and invasion. Cancer Res. 68, 8210-8220.
29. Jura, N., Scotto-Lavino, E., Sobczyk, A. and Bar-Sagi, D. (2006). Differential modification of Ras proteins by ubiquitination. Mol. Cell 21, 679-687. (Pubitemid 43290734)
30. Kanters, E., van Rijssel, J., Hensbergen, P. J., Hondius, D., Mul, F. P., Deelder, A. M., Sonnenberg, A., van Buul, J. D. and Hordijk, P. L. (2008). Filamin B mediates ICAM-1-driven leukocyte transendothelial migration. J. Biol. Chem. 283, 31830-31839.
31. Kraynov, V. S., Chamberlain, C., Bokoch, G. M., Schwartz, M. A., Slabaugh, S. and Hahn, K. M. (2000). Localized Rac activation dynamics visualized in living cells. Science 290, 333-337.
32. Lanning, C. C., Daddona, J. L., Ruiz-Velasco, R., Shafer, S. H. and Williams, C. L. (2004). The Rac1 C-terminal polybasic region regulates the nuclear localization and protein degradation of Rac1. J. Biol. Chem. 279, 44197-44210. (Pubitemid 39390727)
33. Lerm, M., Schmidt, G., Goehring, U. M., Schirmer, J. and Aktories, K. (1999) Identification of the region of rho involved in substrate recognition by Escherichia coli cytotoxic necrotizing factor 1 (CNF1). J. Biol. Chem. 274, 28999-29004.
34. Lin, M., DiVito, M. M., Merajver, S. D., Boyanapalli, M. and van Golen, K. L. (2005). Regulation of pancreatic cancer cell migration and invasion by RhoC GTPase and caveolin-1. Mol. Cancer 4, 21.
35. Lynch, E. A., Stall, J., Schmidt, G., Chavrier, P. and D'Souza-Schorey, C. (2006). Proteasome-mediated degradation of Rac1-GTP during epithelial cell scattering. Mol. Biol. Cell 17, 2236-2242.
36. Machleidt, T., Li, W. P., Liu, P. and Anderson, R. G. (2000). Multiple domains in caveolin-1 control its intracellular traffic. J. Cell Biol. 148, 17-28. (Pubitemid 30046779)
37. Modha, R., Campbell, L. J., Nietlispach, D., Buhecha, H. R., Owen, D. and Mott, H. R. (2008). The Rac1 polybasic region is required for interaction with its effector PRK1. J. Biol. Chem. 283, 1492-1500.
38. Mukherjee, S., Tessema, M. and Wandinger-Ness, A. (2006). Vesicular trafficking of tyrosine kinase receptors and associated proteins in the regulation of signaling and vascular function. Circ. Res. 98, 743-756. (Pubitemid 43755258)
39. Munro, P. and Lemichez, E. (2005). Bacterial toxins activating Rho GTPases. Curr. Top. Microbiol. Immunol. 291, 177-190. (Pubitemid 40674916)
40. Noritake, J., Fukata, M., Sato, K., Nakagawa, M., Watanabe, T., Izumi, N., Wang, S., Fukata, Y. and Kaibuchi, K. (2004). Positive role of IQGAP1, an effector of Rac1, in actin-meshwork formation at sites of cell-cell contact. Mol. Biol. Cell 15, 1065-1076. (Pubitemid 38324580)
41. Pop, M., Aktories, K. and Schmidt, G. (2004). Isotype-specific degradation of Rac activated by the cytotoxic necrotizing factor 1. J. Biol. Chem. 279, 35840-35848.
42. 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. (Pubitemid 28337528)
43. Price, L. S., Langeslag, M., ten Klooster, J. P., Hordijk, P. L., Jalink, K. and Collard, J. G. (2003). Calcium signaling regulates translocation and activation of Rac. J. Biol. Chem. 278, 39413-39421.
44. Razani, B., Woodman, S. E. and Lisanti, M. P. (2002). Caveolae: from cell biology to animal physiology. Pharmacol. Rev. 54, 431-467.
45. Ridley, A. J., Schwartz, M. A., Burridge, K., Firtel, R. A., Ginsberg, M. H., Borisy, G., Parsons, J. T. and Horwitz, A. R. (2003). Cell migration: integrating signals from front to back. Science 302, 1704-1709. (Pubitemid 37505725)
46. Root, D. E., Hacohen, N., Hahn, W. C., Lander, E. S. and Sabatini, D. M. (2006). Genome-scale loss-of-function screening with a lentiviral RNAi library. Nat. Methods 3, 715-719. (Pubitemid 44275739)
47. Rossman, K. L., Der, C. J. and Sondek, J. (2005). GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180. (Pubitemid 40215811)
48. Sahai, E., Garcia-Medina, R., Pouyssegur, J. and Vial, E. (2007). Smurf1 regulates tumor cell plasticity and motility through degradation of RhoA leading to localized inhibition of contractility. J. Cell Biol. 176, 35-42. (Pubitemid 46041678)
49. Schmidt, G., Sehr, P., Wilm, M., Selzer, J., Mann, M. and Aktories, K. (1997). Gln 63 of Rho is deamidated by Escherichia coli cytotoxic necrotizing factor-1. Nature 387, 725-729. (Pubitemid 27270615)
50. Shutes, A., Onesto, C., Picard, V., Leblond, B., Schweighoffer, F. and Der, C. J. (2007). Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of Rac family small GTPases. J. Biol. Chem. 282, 35666-35678. (Pubitemid 350277149)
51. ten Klooster, J. P. and Hordijk, P. L. (2007). Targeting and localized signalling by small GTPases. Biol. Cell 99, 1-12.
52. ten Klooster, J. P., Jaffer, Z. M., Chernoff, J. and Hordijk, P. L. (2006). Targeting and activation of Rac1 are mediated by the exchange factor beta-Pix. J. Cell Biol. 172, 759-769.
53. ten Klooster, J. P., Leeuwen, I., Scheres, N., Anthony, E. C. and Hordijk, P. L. (2007). Rac1-induced cell migration requires membrane recruitment of the nuclear oncogene SET. EMBO J. 26, 336-345.
54. van Hennik, P. B., ten Klooster, J. P., Halstead, J. R., Voermans, C., Anthony, E. C., Divecha, N. and Hordijk, P. L. (2003). The C-terminal domain of Rac1 contains two motifs that control targeting and signaling specificity. J. Biol. Chem. 278, 39166-39175.
55. Vastrik, I., Eickholt, B. J., Walsh, F. S., Ridley, A. and Doherty, P. (1999). Sema3A-induced growth-cone collapse is mediated by Rac1 amino acids 17-32. Curr. Biol. 9, 991-998. (Pubitemid 29456167)
56. Vicente-Manzanares, M., Webb, D. J. and Horwitz, A. R. (2005). Cell migration at a glance. J. Cell Sci. 118, 4917-4919.
57. Visvikis, O., Lores, P., Boyer, L., Chardin, P., Lemichez, E. and Gacon, G. (2008). Activated Rac1, but not the tumorigenic variant Rac1b, is ubiquitinated on Lys 147 through a JNK-regulated process. FEBS J. 275, 386-396.
58. Wang, H. R., Zhang, Y., Ozdamar, B., Ogunjimi, A. A., Alexandrova, E., Thomsen, G. H. and Wrana, J. L. (2003). Regulation of cell polarity and protrusion formation by targeting RhoA for degradation. Science 302, 1775-1779. (Pubitemid 37505743)
59. Ward, C. L., Omura, S. and Kopito, R. R. (1995). Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83, 121-127.
60. Wary, K. K., Mariotti, A., Zurzolo, C. and Giancotti, F. G. (1998). A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94, 625-634. (Pubitemid 28427581)
61. Worthylake, R. A. and Burridge, K. (2003). RhoA and ROCK promote migration by limiting membrane protrusions. J. Biol. Chem. 278, 13578-13584.
62. Zuluaga, S., Gutierrez-Uzquiza, A., Bragado, P., Alvarez-Barrientos, A., Benito, M., Nebreda, A. R. and Porras, A. (2007). p38alpha MAPK can positively or negatively regulate Rac-1 activity depending on the presence of serum. FEBS Lett. 581, 3819-3825. (Pubitemid 47102312)