Proteomic profiling of endothelial invasion revealed receptor for activated C kinase 1 (RACK1) complexed with vimentin to regulate focal adhesion kinase (FAK)

Journal of Biological Chemistry

Volumn 288, Issue 42, 2013, Pages 30720-30733

  Dave, Jui M ^a   Kang, Hojin ^a   Abbey, Colette A ^a   Maxwell, Steve A ^a   Bayless, Kayla J ^a  

^a TEXAS A M COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; FOCAL ADHESION KINASE; FOCAL ADHESIONS; INTERMOLECULAR COMPLEXES; PROTEOMIC PROFILING; VIMENTIN;

ADHESION; ENDOTHELIAL CELLS;

ENZYMES;

CHAPERONIN CONTAINING TCP1; FOCAL ADHESION KINASE; HEAT SHOCK PROTEIN 27; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 94B; LAMIN A; LAMIN B2; LAMIN C; LIPOCORTIN 2; LIPOCORTIN 5; OTUBAIN 1; PEROXIREDOXIN 1; PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; RECEPTOR FOR ACTIVATED C KINASE 1; STIMULATOR OF TAR RNA BINDING; TUMOR REJECTION ANTIGEN; UNCLASSIFIED DRUG; VIMENTIN;

ANGIOGENESIS; ARTICLE; CELL INVASION; COMPLEX FORMATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME REGULATION; FOCAL ADHESION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEOMICS; UPREGULATION;

ANGIOGENESIS; COLLAGEN; ENDOTHELIAL CELL; FOCAL ADHESION KINASE; MORPHOGENESIS; RACK1; VIMENTIN;

COLLAGEN; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; FOCAL ADHESION KINASE 1; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE KNOCKDOWN TECHNIQUES; GTP-BINDING PROTEINS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; LYSOPHOSPHOLIPIDS; MULTIPROTEIN COMPLEXES; NEOPLASM PROTEINS; NEOVASCULARIZATION, PHYSIOLOGIC; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN STABILITY; PROTEOMICS; RECEPTORS, CELL SURFACE; SIGNAL TRANSDUCTION; SPHINGOSINE; UP-REGULATION; VIMENTIN;

EID: 84886930695     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.512467     Document Type: Article

References (73)

1. Carmeliet, P. (2003) Angiogenesis in health and disease. Nat. Med. 9, 653-660
2. Folkman, J., and D'Amore, P. A. (1996) Blood vessel formation: what is its molecular basis? Cell 87, 1153-1155
3. Adams, R. H., and Alitalo, K. (2007) Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478
4. Kalluri, R. (2003) Basement membranes: structure, assembly and role in tumour angiogenesis. Nat. Rev. Cancer, 3, 422-433
5. Iruela-Arispe, M. L., and Davis, G. E. (2009) Cellular and molecular mechanisms of vascular lumen formation. Dev. Cell 16, 222-231
6. Davis, G. E., and Camarillo, C. W. (1996) An α2β1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp. Cell Res. 224, 39-51
7. Egginton, S., and Gerritsen, M. (2003) Lumen formation: in vivo versus in vitro observations. Microcirculation 10, 45-61
8. Montesano, R., Pepper, M. S., Vassalli, J. D., and Orci, L. (1992) Modulation of angiogenesis in vitro. EXS 61, 129-136
9. Nicosia, R. F., and Villaschi, S. (1999) Autoregulation of angiogenesis by cells of the vessel wall. Int. Rev. Cytol. 185, 1-43
10. Vernon, R. B., and Sage, E. H. (1995) Between molecules and morphology. Extracellular matrix and creation of vascular form. Am. J. Pathol. 147, 873-883
11. Bayless, K. J., Kwak, H. I., and Su, S. C. (2009) Investigating endothelial invasion and sprouting behavior in three-dimensional collagen matrices. Nat. Protoc. 4, 1888-1898
12. Su, S. C., Maxwell, S. A., and Bayless, K. J. (2010) Annexin 2 regulates endothelial morphogenesis by controlling AKT activation and junctional integrity. J. Biol. Chem. 285, 40624-40634
13. Peters, S. L., and Alewijnse, A. E. (2007) Sphingosine-1-phosphate signaling in the cardiovascular system. Curr. Opin. Pharmacol. 7, 186-192
14. Rivera, J., Proia, R. L., and Olivera, A. (2008) The alliance of sphingosine- 1-phosphate and its receptors in immunity. Nat. Rev. Immunol. 8, 753-763
15. Rosen, H., and Goetzl, E. J. (2005) Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat. Rev. Immunol. 5, 560-570
16. Taha, T. A., Mullen, T. D., and Obeid, L. M. (2006) A house divided: ceramide, sphingosine, and sphingosine-1-phosphate in programmed cell death. Biochim. Biophys. Acta 1758, 2027-2036
17. Spiegel, S., and Milstien, S. (2003) Sphingosine-1-phosphate: an enigmatic signalling lipid. Nat. Rev. Mol. Cell Biol. 4, 397-407
18. McCahill, A., Warwicker, J., Bolger, G. B., Houslay, M. D., and Yarwood, S. J. (2002) The RACK1 scaffold protein: a dynamic cog in cell response mechanisms. Mol. Pharmacol. 62, 1261-1273
19. Sklan, E. H., Podoly, E., and Soreq, H. (2006) RACK1 has the nerve to act: structure meets function in the nervous system. Prog. Neurobiol. 78, 117-134
20. Chen, J. G., Ullah, H., Temple, B., Liang, J., Guo, J., Alonso, J. M., Ecker, J. R., and Jones, A. M. (2006) RACK1 mediates multiple hormone responsiveness and developmental processes in Arabidopsis. J. Exp. Bot. 57, 2697-2708
21. Guo, J., and Chen, J. G. (2008) RACK1 genes regulate plant development with unequal genetic redundancy in Arabidopsis. BMC Plant Biol. 8, 108
22. Wehner, P., Shnitsar, I., Urlaub, H., and Borchers, A. (2011) RACK1 is a novel interaction partner of PTK7 that is required for neural tube closure. Development 138, 1321-1327
23. Hermanto, U., Zong, C. S., Li, W., and Wang, L. H. (2002) RACK1, an insulin-like growth factor I (IGF-I) receptor-interacting protein, modulates IGF-I-dependent integrin signaling and promotes cell spreading and contact with extracellular matrix. Mol. Cell. Biol. 22, 2345-2365
24. Kiely, P. A., Baillie, G. S., Barrett, R., Buckley, D. A., Adams, D. R., Houslay, M. D., and O'Connor, R. (2009) Phosphorylation of RACK1 on tyrosine 52 by c-Abl is required for insulin-like growth factor I-mediated regulation of focal adhesion kinase. J. Biol. Chem. 284, 20263-20274
25. Kiely, P. A., Leahy, M., O'Gorman, D., and O'Connor, R. (2005) RACK1- mediated integration of adhesion and insulin-like growth factor I (IGF-I) signaling and cell migration are defective in cells expressing an IGF-I receptor mutated at tyrosines 1250 and 1251. J. Biol. Chem. 280, 7624- 7633
26. Kiely, P. A., Sant, A., and O'Connor, R. (2002) RACK1 is an insulin-like growth factor 1 (IGF-1) receptor-interacting protein that can regulate IGF-1-mediated Akt activation and protection from cell death. J. Biol. Chem. 277, 22581-22589
27. Neer, E. J., Schmidt, C. J., Nambudripad, R., and Smith, T. F. (1994) The ancient regulatory-protein family of WD-repeat proteins. Nature 371, 297-300
28. Onishi, I., Lin, P. J., Diering, G. H., Williams, W. P., and Numata, M. (2007) RACK1 associates with NHE5 in focal adhesions and positively regulates the transporter activity. Cell. Signal. 19, 194-203
29. Adams, D. R., Ron, D., and Kiely, P. A. (2011) RACK1, a multifaceted scaffolding protein: structure and function. Cell Commun. Signal. 9, 22
30. Berns, H., Humar, R., Hengerer, B., Kiefer, F. N., and Battegay, E. J. (2000) RACK1 is up-regulated in angiogenesis and human carcinomas. FASEB J. 14, 2549-2558
31. Kwak, H. I., Kang, H., Dave, J. M., Mendoza, E. A., Su, S. C., Maxwell, S. A., and Bayless, K. J. (2012) Calpain-mediated vimentin cleavage occurs upstream of MT1-MMP membrane translocation to facilitate endothelial sprout initiation. Angiogenesis 15, 287-303
32. Burgstaller, G., Gregor, M., Winter, L., and Wiche, G. (2010) Keeping the vimentin network under control: cell-matrix adhesion-associated plectin 1f affects cell shape and polarity of fibroblasts. Mol. Biol. Cell 21, 3362-3375
33. Tsuruta, D., and Jones, J. C. (2003) The vimentin cytoskeleton regulates focal contact size and adhesion of endothelial cells subjected to shear stress. J. Cell Sci. 116, 4977-4984
34. Romer, L. H., Birukov, K. G., and Garcia, J. G. (2006) Focal adhesions: paradigm for a signaling nexus. Circ. Res. 98, 606-616
35. Petit, V., and Thiery, J. P. (2000) Focal adhesions: structure and dynamics. Biol. Cell 92, 477-494
36. Martin, G. M. (1996) Fak and focal adhesions. Jpn. J. Cancer Res. 87, inside front cover
37. Burridge, K., Chrzanowska-Wodnicka, M., and Zhong, C. (1997) Focal adhesion assembly. Trends Cell Biol. 7, 342-347
38. Burridge, K., and Chrzanowska-Wodnicka, M. (1996) Focal adhesions, contractility, and signaling. Annu. Rev. Cell Dev. Biol. 12, 463-518
39. Mitra, S. K., and Schlaepfer, D. D. (2006) Integrin-regulated FAK-Src signaling in normal and cancer cells. Curr. Opin. Cell Biol. 18, 516-523
40. Guan, J. L. (2010) Integrin signaling through FAK in the regulation of mammary stem cells and breast cancer. IUBMB Life. 62, 268-276
41. Arold, S. T. (2011) How focal adhesion kinase achieves regulation by linking ligand binding, localization and action. Curr. Opin. Struct. Biol. 21, 808-813
42. Braren, R., Hu, H., Kim, Y. H., Beggs, H. E., Reichardt, L. F., and Wang, R. (2006) Endothelial FAK is essential for vascular network stability, cell survival, and lamellipodial formation. J. Cell Biol. 172, 151-162
43. Hakim, Z. S., DiMichele, L. A., Doherty, J. T., Homeister, J. W., Beggs, H. E., Reichardt, L. F., Schwartz, R. J., Brackhan, J., Smithies, O., Mack, C. P., and Taylor, J. M. (2007) Conditional deletion of focal adhesion kinase leads to defects in ventricular septation and outflow tract alignment. Mol. Cell. Biol. 27, 5352-5364
44. Peng, X., Wu, X., Druso, J. E., Wei, H., Park, A. Y., Kraus, M. S., Alcaraz, A., Chen, J., Chien, S., Cerione, R. A., and Guan, J. L. (2008) Cardiac developmental defects and eccentric right ventricular hypertrophy in cardiomyocyte focal adhesion kinase (FAK) conditional knockout mice. Proc. Natl. Acad. Sci. U.S.A. 105, 6638-6643
45. Shen, T. L., Park, A. Y., Alcaraz, A., Peng, X., Jang, I., Koni, P., Flavell, R. A., Gu, H., and Guan, J. L. (2005) Conditional knockout of focal adhesion kinase in endothelial cells reveals its role in angiogenesis and vascular development in late embryogenesis. J. Cell Biol. 169, 941-952
46. Kaslow, H. R., and Burns, D. L. (1992) Pertussis toxin and target eukaryotic cells: binding, entry, and activation. FASEB J. 6, 2684-2690
47. Kiely, P. A., O'Gorman, D., Luong, K., Ron, D., and O'Connor, R. (2006) Insulin-like growth factor I controls a mutually exclusive association of RACK1 with protein phosphatase 2A and 1 integrin to promote cell migration. Mol. Cell. Biol. 26, 4041-4051
48. Serrels, A., Canel, M., Brunton, V. G., and Frame, M. C. (2011) Src/FAKmediated regulation of E-cadherin as a mechanism for controlling collective cell movement: insights from in vivo imaging. Cell. Adh. Migr. 5, 360-365
49. Kiely, P. A., Baillie, G. S., Lynch, M. J., Houslay, M. D., and O'Connor, R. (2008) Tyrosine 302 in RACK1 is essential for insulin-like growth factor- I-mediated competitive binding of PP2A and β1 integrin and for tumor cell proliferation and migration. J. Biol. Chem. 283, 22952-22961
50. Burridge, K., Fath, K., Kelly, T., Nuckolls, G., and Turner, C. (1988) Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4, 487-525
51. Bayless, K. J., Davis, G. E., and Meininger, G. A. (1997) Isolation and biological properties of osteopontin from bovine milk. Protein Expr. Purif. 9, 309-314
52. Tonnesen, M. G., Feng, X., and Clark, R. A. (2000) Angiogenesis in wound healing. J. Investig. Dermatol. Symp. Proc. 5, 40-46
53. Zhao, J., Singleton, P. A., Brown, M. E., Dudek, S. M., and Garcia, J. G. (2009) Phosphotyrosine protein dynamics in cell membrane rafts of sphingosine-1-phosphate-stimulated human endothelium: role in barrier enhancement. Cell. Signal. 21, 1945-1960
54. Chang, B. Y., Harte, R. A., and Cartwright, C. A. (2002) RACK1: a novel substrate for the Src protein-tyrosine kinase. Oncogene 21, 7619-7629
55. Yaka, R., Thornton, C., Vagts, A. J., Phamluong, K., Bonci, A., and Ron, D. (2002) NMDA receptor function is regulated by the inhibitory scaffolding protein, RACK1. Proc. Natl. Acad. Sci. U.S.A. 99, 5710-5715
56. Koehler, J. A., and Moran, M. F. (2001) RACK1, a protein kinase C scaffolding protein, interacts with the PH domain of p120GAP. Biochem. Biophys. Res. Commun. 283, 888-895
57. Rodriguez, M. M., Ron, D., Touhara, K., Chen, C. H., and Mochly-Rosen, D. (1999) RACK1, a protein kinase C anchoring protein, coordinates the binding of activated protein kinase C and select pleckstrin homology domains in vitro. Biochemistry 38, 13787-13794
58. Usacheva, A., Tian, X., Sandoval, R., Salvi, D., Levy, D., and Colamonici, O. R. (2003) The WD motif-containing protein RACK-1 functions as a scaffold protein within the type I IFN receptor-signaling complex. J. Immunol. 171, 2989-2994
59. Liliental, J., and Chang, D. D. (1998) Rack1, a receptor for activated protein kinase C, interacts with integrin β subunit. J. Biol. Chem. 273, 2379-2383
60. Lee, H. S., Millward-Sadler, S. J., Wright, M. O., Nuki, G., Al-Jamal, R., and Salter, D. M. (2002) Activation of integrin-RACK1/PKCα signalling in human articular chondrocyte mechanotransduction. Osteoarthritis Cartilage 10, 890-897
61. Rigas, A. C., Ozanne, D. M., Neal, D. E., and Robson, C. N. (2003) The scaffolding protein RACK1 interacts with androgen receptor and promotes cross-talk through a protein kinase C signaling pathway. J. Biol. Chem. 278, 46087-46093
62. Helfand, B. T., Chou, Y. H., Shumaker, D. K., and Goldman, R. D. (2005) Intermediate filament proteins participate in signal transduction. Trends Cell Biol. 15, 568-570
63. Ivaska, J., Pallari, H. M., Nevo, J., and Eriksson, J. E. (2007) Novel functions of vimentin in cell adhesion, migration, and signaling. Exp. Cell Res. 313, 2050-2062
64. Oriolo, A. S., Wald, F. A., Ramsauer, V. P., and Salas, P. J. (2007) Intermediate filaments: a role in epithelial polarity. Exp. Cell Res. 313, 2255-2264
65. Bershadsky, A. D., Tint, I. S., and Svitkina, T. M. (1987) Association of intermediate filaments with vinculin-containing adhesion plaques of fibroblasts. Cell Motil. Cytoskeleton 8, 274-283
66. Gonzales, M., Weksler, B., Tsuruta, D., Goldman, R. D., Yoon, K. J., Hopkinson, S. B., Flitney, F. W., and Jones, J. C. (2001) Structure and function of a vimentin-associated matrix adhesion in endothelial cells. Mol. Biol. Cell 12, 85-100
67. Ilić, D., Furuta, Y., Kanazawa, S., Takeda, N., Sobue, K., Nakatsuji, N., Nomura, S., Fujimoto, J., Okada, M., and Yamamoto, T. (1995) Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377, 539-544
68. Owens, L. V., Xu, L., Dent, G. A., Yang, X., Sturge, G. C., Craven, R. J., and Cance, W. G. (1996) Focal adhesion kinase as a marker of invasive potential in differentiated human thyroid cancer. Ann. Surg. Oncol. 3, 100-105
69. Tremblay, L., Hauck, W., Aprikian, A. G., Begin, L. R., Chapdelaine, A., and Chevalier, S. (1996) Focal adhesion kinase (pp125FAK) expression, activation and association with paxillin and p50CSK in human metastatic prostate carcinoma. Int. J. Cancer 68, 164-171
70. Al-Reefy, S., and Mokbel, K. (2010) The role of RACK1 as an independent prognostic indicator in human breast cancer. Breast Cancer Res. Treat. 123, 911
71. Cao, X. X., Xu, J. D., Xu, J. W., Liu, X. L., Cheng, Y. Y., Wang, W. J., Li, Q. Q., Chen, Q., Xu, Z. D., and Liu, X. P. (2010) RACK1 promotes breast carcinoma proliferation and invasion/metastasis in vitro and in vivo. Breast Cancer Res. Treat. 123, 375-386
72. Singh, S., Sadacharan, S., Su, S., Belldegrun, A., Persad, S., and Singh, G. (2003) Overexpression of vimentin: role in the invasive phenotype in an androgen-independent model of prostate cancer. Cancer Res. 63, 2306- 2311
73. Alfonso, P., Núñez, A., Madoz-Gurpide, J., Lombardia, L., Sanchez, L., and Casal, J. I. (2005) Proteomic expression analysis of colorectal cancer by two-dimensional differential gel electrophoresis. Proteomics 5, 2602- 2611