A dual role for caveolin-1 in the regulation of fibronectin matrix assembly by uPAR

Journal of Cell Science

Volumn 121, Issue 22, 2008, Pages 3693-3703

  Monaghan Benson, Elizabeth ^a   Mastick, Cynthia Corley ^b   McKeown Longo, Paula J ^a  

^a ALBANY MEDICAL COLLEGE   (United States)

^b UNIVERSITY OF NEVADA   (United States)

Author keywords

Caveolin 1; Extracellular matrix; Fibronectin; Integrin; uPAR

Indexed keywords

CAVEOLIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; FIBRONECTIN; LIPID; METHYL BETA CYCLODEXTRIN; SMALL INTERFERING RNA; STEROID RECEPTOR COACTIVATOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; UROKINASE; VERY LATE ACTIVATION ANTIGEN 5;

ARTICLE; CELL STIMULATION; CONTROLLED STUDY; FOCAL ADHESION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN POLYMERIZATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SKIN FIBROBLAST;

ANIMALS; CAVEOLIN 1; CELLS, CULTURED; FIBROBLASTS; FIBRONECTINS; HUMANS; INTEGRINS; MICE; PHOSPHORYLATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, UROKINASE PLASMINOGEN ACTIVATOR; SIGNAL TRANSDUCTION;

EID: 59549100976     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.028423     Document Type: Article

References (68)

1. Abulrob, A., Giuseppin, S., Andrade, M. F., McDermid, A., Moreno, M. and Stanimirovic, D. (2004). Interactions of EGFR and caveolin-1 in human glioblastoma cells: evidence that tyrosine phosphorylation regulates EGFR association with caveolae. Oncogene 23, 6967-6979.
2. Aguirre-Ghiso, J. A., Liu, D., Mignatti, A., Kovalski, K. and Ossowski, L. (2001). Urokinase receptor and fibronectin regulate the ERK(MAPK) to p38(MAPK) activity ratios that determine carcinoma cell proliferation or dormancy in vivo. Mol. Biol. Cell 12, 863-879.
3. Cao, D. J., Guo, Y. L. and Colman, R. W. (2004). Urokinase-type plasminogen activator receptor is involved in mediating the apoptotic effect of cleaved high molecular weight kininogen in human endothelial cells. Circ. Res. 94, 1227-1234.
4. Carlin, S. M., Resink, T. J., Tamm, M. and Roth, M. (2005). Urokinase signal transduction and its role in cell migration. FASEB J. 19, 195-202.
5. Cathcart, M. K. and Culp, L. A. (1979). Initial studies of the molecular organization of the cell-substrate adhesion site. Biochim. Biophys. Acta 556, 331-343.
6. Chaurasia, P., Aguirre-Ghiso, J. A., Liang, O. D., Gardsvoll, H., Ploug, M. and Ossowski, L. (2006). A region in urokinase plasminogen receptor domain III controlling a functional association with α5β1 integrin and tumor growth. J. Biol. Chem. 281, 14852-14863.
7. Christopher, R. A., Kowalczyk, A. P. and McKeown-Longo, P. J. (1997). Localization of fibronectin matrix assembly sites on fibroblasts and endothelial cells. J. Cell Sci. 110, 569-581.
8. Ciambrone, G. J. and McKeown-Longo, P. J. (1990). Plasminogen activator inhibitor type 1 stabilizes vitronectin- dependent adhesions in HT-1080 cells. J. Cell Biol. 111, 2183-2195.
9. Couet, J., Sargiacoma, M. and Lisanti, M. P. (1997). Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. J. Biol. Chem. 272, 30429-30438.
10. Degryse, B., Resnati, M., Czekay, R.-P., Loskutoff, D. J. and Blasi, F. (2005). Domain 2 of the urokinase receptor contains an integrin-interacting epitope with intrinsic signaling activity: generation of a new integrin inhibitor. J. Biol. Chem. 280, 24792-24803.
11. 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.
12. 1) antibodies. J. Cell Biol. 111, 699-708.
13. Garcia, A. J., Schwarzbauer, J. E. and Boettiger, D. (2002). Distinct activation states of α5β1 integrin show differential binding to RGD and synergy domains of fibronectin. Biochemistry 41, 9063-9069.
14. Gaus, K., Le Lay, S., Balasubramanian, N. and Schwartz, M. A. (2006). Integrin-mediated adhesion regulates membrane order. J. Cell Biol. 174, 725-734.
15. Hazlehurst, L. A. and Dalton, W. S. (2001). Mechanisms associated with cell adhesion mediated drug resistance (CAM-DR) in hematopoietic malignancies. Cancer Metastasis Rev. 20, 43-50.
16. He, Y., Liu, X. D., Chen, Z. Y., Zhu, J., Xiong, Y., Li, K., Dong, J. H. and Li, X. (2007). Interaction between cancer cells and stromal fibroblasts is required for activation of the uPAR-uPA-MMP-2 cascade in pancreatic cancer metastasis. Clin. Cancer Res. 13, 3115-3124.
17. 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.
18. Hocking, D. C., Sottile, J. and McKeown-Longo, P. J. (1994). Fibronectin's III-1 module contains a conformation-dependent binding site for the amino-terminal region of fibronectin. J. Biol. Chem. 269, 19183-19197.
19. Hocking, D. C., Smith, R. K. and McKeown-Longo, P. J. (1996). A novel role for the integrin-binding III-10 module in fibronectin matrix assembly. J. Cell Biol. 133, 431-444.
20. Iyer, A. K., Tran, K. T., Borysenko, C. W., Cascio, M., Camacho, C. J., Blair, H. C., Bahar, I. and Wells, A. (2007). Tenascin cytotactin epidermal growth factor-like repeat binds epidermal growth factor receptor with low affinity. J. Cell Physiol. 211, 748-758.
21. Iyer, A. K., Tran, K. T., Griffith, L. and Wells, A. (2008). Cell surface restriction by EGFR by a tenascin cytotactin-encoded EGF-like repeat is preferential for motility-related signaling. J. Cell Physiol. 214, 504-512.
22. Jo, M., Thomas, K. S., Takimoto, S., Gaultier, A., Hsieh, E. H., Lester, R. D. and Gonias, S. L. (2007). Urokinase receptor primes cells to proliferate in response to epidermal growth factor. Oncogene 26, 2585-2594.
23. Kaplan, J. M., Mardon, G., Bishop, J. M. and Varmus, H. E. (1988). The first seven amino acids encoded by the v-src oncogene act as a myristylation signal: lysine 7 is a critical determinant. Mol. Cell. Biol. 8, 2435-2441.
24. Kaplan, R. N., Rafii, S. and Lyden, D. (2006). Preparing the "soil": the premetastatic niche. Cancer Res. 66, 11089-11093.
25. Khan, E. M., Heidinger, J. M., Levy, M., Lisanti, M. P., Ravid, T. and Goldkorn, T. (2006). Epidermal growth factor receptor exposed to oxidative stress undergoes Src-and caveolin-1-dependent perinuclear trafficking. J. Biol. Chem. 281, 14486-14493.
26. Konakova, M., Hucho, F. and Schleuning, W. D. (1998). Downstream targets of urokinase-type plasminogen-activator-mediated signal transduction. Eur. J. Biochem. 253, 421-429.
27. Lee, H., Volonte, D., Galbiati, F., Iyengar, P., Lublin, D. M., Bregman, D. B., Wilson, M. T., Campos-Gonzalez, R., Bouzahzah, B., Petell, R. G. et al. (2000). Constitutive and growth factor-regulated phosphorylation of caveolin-1 occurs at the same site (Tyr-14) in vivo: identification of a c-Src/Cav-1/Grb7 signaling cassette. Mol. Endocrinol. 14, 1750-1775.
28. Li, S., Couet, J. and Lisanti, M. P. (1996). Src tyrosine kinases, G alpha subunits, and H-Ras share a common membrane-anchored scaffolding protein, caveolin. Caveolin binding negatively regulates the auto-activation of Src tyrosine kinases. J. Biol. Chem. 271, 29182-29190.
29. Liu, D., Aguirre-Ghiso, J. A., Estrada, Y. and Ossowski, L. (2002). EGFR is a transducer of the urokinase receptor initiated signal that is required for in vivo growth of a human carcinoma. Cancer Cell 1, 445-457.
30. Madsen, C. D., Ferraris, G. M., Andolfo, A., Cunningham, O. and Sidenius, N. (2007). uPAR-induced cell adhesion and migration: vitronectin provides the key. J. Cell Biol. 177, 927-939.
31. Mandal, S. K., Iakhiaev, A., Pendurthi, U. R. and Rao, L. V. M. (2005). Acute cholesterol depletion impairs functional expression of tissue factor in fibroblasts: modulation of tissue factor activity by membrane cholesterol. Blood 105, 153-160.
32. Mao, Y. and Schwarzbauer, J. E. (2005). Stimulatory effects of a three-dimensional microenvironment on cell-mediated fibronectin fibrillogenesis. J. Cell Sci. 118, 4427-4436.
33. Mastick, C. C. and Saltiel, A. R. (1997). Insulin-stimulated tyrosine phosphorylation of caveolin is specific for the differentiated adipocyte phenotype in 3T3-L1 cells. J. Biol. Chem. 272, 20706-20714.
34. McKeown-Longo, P. J. and Mosher, D. F. (1985). Interaction of the 70,000-mol-wt amino-terminal fragment of fibronectin with the matrix-assembly receptor of fibroblasts. J. Cell Biol. 100, 364-374.
35. Mineo, C., Gill, G. N. and Anderson, R. G. (1999). Regulated migration of epidermal growth factor receptor from caveolae. J. Biol. Chem. 274, 30636-30643.
36. Monaghan, E., Gueorguiev, V., Wilkins-Port, C. and McKeown-Longo, P. J. (2004). The receptor for urokinase-type plasminogen activator regulates fibronectin matrix assembly in human skin fibroblasts. J. Biol. Chem. 279, 1400-1407.
37. Monaghan-Benson, E. and McKeown-Longo, P. J. (2006). Urokinase-type plasminogen activator receptor regulates a novel pathway of fibronectin matrix assembly requiring Src dependent transactivation of epidermal growth factor receptor. J. Biol. Chem. 281, 9450-9459.
38. Nguyen, D. H., Webb, D. J., Catling, A. D., Song, Q., Dhakephalkar, A., Weber, M. J., Ravichandran, K. S. and Gonias, S. L. (2000). Urokinase-type plasminogen activator stimulates the Ras/extracellular signal-regulated kinase (ERK) signaling pathway and MCF-7 cell migration by a mechanism that requires focal adhesion kinase, Src, and Shc. Rapid dissociation of GRB2/Sps-Shc complex is associated with the transient phosphorylation of ERK in urokinase-treated cells. J. Biol. Chem. 275, 19382-19388.
39. Nicholson, T. B. and Stanners, C. P. (2006). Specific inhibition of GPI-anchored protein function by homing and self-association of specific GPI anchors. J. Cell Biol. 175, 647-659.
40. Orlichenko, L., Huang, B., Krueger, E. and McNiven, M. A. (2006). Epithelial growth factor-induced phosphorylation of caveolin 1 at tyrosine 14 stimulates caveolae formation in epithelial cells. J. Biol. Chem. 281, 4570-4579.
41. Pereira, M., Rybarczyk, B. J., Odrljin, T. M., Hocking, D. C., Sottile, J. and Simpson-Haidaris, P. J. (2002). The incorporation of fibrinogen into extracellular matrix is dependent on active assembly of a fibronectin matrix. J. Cell Sci. 115, 609-617.
42. Ragno, P. (2006). The urokinase receptor: a ligand or a receptor? Story of a sociable molecule. Cell Mol. Life Sci. 63, 1028-1037.
43. Sanguinetti, A. R. and Mastick, C. C. (2003). c-Abl is required for oxidative stress-induced phosphorylation of caveolin-1 on tyrosine 14. Cell Signal. 15, 289-298.
44. Schwab, W., Gavlik, J. M., Beichler, T., Funk, R. H., Albrecht, S., Magdolen, V., Luther, T., Kasper, M. and Shakibaei, M. (2001). Expression of the urokinase-type plasminogen activator receptor in human articular chondrocytes: association with caveolin and β1 integrin. Histochem. Cell Biol. 115, 317-323.
45. Sechler, J. L. and Schwarzbauer, J. E. (1998). Control of cell cycle progression by fibronectin matrix architecture. J. Biol. Chem. 273, 25533-25536.
46. Sechler, J. L., Corbett, S. A. and Schwarzbauer, J. E. (1997). Modulatory roles for integrin activation and the synergy site of fibronectin during matrix assembly. Mol. Biol. Cell 8, 2563-2573.
47. Simon, D. I., Weis, Y., Zhang, L., Rao, N. K., Xu, H., Chen, Z., Liu, Q., Rosenberg, S. and Chapman, H. A. (2000). Identification of a urokinase receptor-integrin interaction site. J. Biol. Chem 275, 10228-10234.
48. Sottile, J. and Hocking, D. C. (2002). Fibronectin polymerization regulates the composition and stability of extracellular matrix fibrils and cell-matrix adhesions. Mol. Biol. Cell 13, 3546-3559.
49. Sottile, J. and Chandler, J. (2005). Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol. Biol. Cell 16, 757-768.
50. Sottile, J., Hocking, D. C. and Swiatek, P. J. (1998). Fibronectin matrix assembly enhances adhesion-dependent cell growth. J. Cell Sci. 111, 2933-2943.
51. Stahl, A. and Mueller, B. M. (1995). The urokinase-type plasminogen activator receptor, a GPI-linked protein is localized in caveolae. J. Cell Biol. 129, 335-344.
52. Syme, C. A., Zhang, L. and Bisello, A. (2006). Caveolin-1 regulates cellular trafficking and function of the glucagon-like Peptide 1 receptor. Mol. Endocrinol. 20, 3400-3411.
53. Tarui, T., Mazar, A. P., Cines, D. B. and Takada, Y. (2001). Urokinase-type plasminogen activator receptor (CD87) is a ligand for integrins and mediates cell-cell interaction. J. Biol. Chem 276, 3983-3990.
54. Tomasini-Johansson, B. R., Annis, D. S. and Mosher, D. F. (2006). The N-terminal 70-κDa fragment of fibronectin binds to cell surface fibronectin assembly sites in the absence of intact fibronectin. Matrix Biol. 25, 282-293.
55. van der Pluijm, G., Sijmons, B., Vloedgraven, H., van der Bent, C., Drijfhout, J. W., Verheijen, J., Quax, P., Karperien, M., Papapoulos, S. and Lowik, C. (2001). Urokinase-receptor/integrin complexes are functionally involved in adhesion and progression of human breast cancer in vivo. Am. J. Pathol. 159, 971-982.
56. Velling, T., Risteli, J., Wennerberg, K., Mosher, D. F. and Johansson, S. (2002). Polymerization of type I and III collagens is dependent on fibronectin and enhanced by integrins α11β1 and α2β1. J. Biol. Chem 277, 37377-37381.
57. Vial, D., Monaghan-Benson, E. and McKeown-Longo, P. J. (2006). Coordinate regulation of fibronectin matrix assembly by the plasminogen activator system and vitronectin in human osteosarcoma cells. Cancer Cell Int. 6, 8.
58. 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.
59. Wei, Y., Lukashev, M., Simon, D. I., Bodary, S. C., Rosenberg, S., Doyle, M. V. and Chapman, H. A. (1996). Regulation of integrin function by the urokinase receptor. Science 273, 1551-1555.
60. Wei, Y., Yang, X., Liu, Q., Wilkins, J. A. and Chapman, H. A. (1999). A role for caveolin and the urokinase receptor in integrin-mediated adhesion and signaling. J. Cell Biol. 144, 1285-1294.
61. Wei, Y., Eble, J. A., Wang, Z., Kreidberg, J. A. and Chapman, H. A. (2001). Urokinase receptors promote β1 integrin function through interactions with integrin α3β1. Mol. Biol. Cell 12, 2975-2986.
62. Wei, Y., Czekay, R.-P., Robillard, L., Kugler, M. C., Zhang, F., Kim, K. K., Xiong, J. P., Humphries, M. J. and Chapman, H. A. (2005). Regulation of α5β1 integrin conformation and function by urokinase receptor binding. J. Cell Biol. 168, 501-511.
63. Wei, Y., Tang, C. H., Kim, Y., Robillard, L., Zhang, F., Kugler, M. C. and Chapman, H. A. (2007). Urokinase receptors are required for α5β1 integrin-mediated signaling in tumor cells. J. Biol. Chem. 282, 3929-3939.
64. Wierzbicka-Patynowski, I. and Schwarzbauer, J. E. (2003). The ins and outs of fibronectin matrix assembly. J. Cell Sci. 116, 3269-3276.
65. Wu, C., Keivens, V. M., O'Toole, T. E., McDonald, J. A. and Ginsberg, M. H. (1995). Integrin activation and cytoskeletal interaction are essential for the assembly of a fibronectin matrix. Cell 83, 715-724.
66. Yu, J. L., Coomber, B. L. and Kerbel, R. S. (2002). A paradigm for therapy-induced microenvironmental changes in solid tumors leading to drug resistance. Differentiation 70, 599-609.
67. Zhang, F., Tom, C. C., Kugler, M. C., Ching, T. T., Kreidberg, J. A., Wei, Y. and Chapman, H. A. (2003). Distinct ligand binding sites in integrin α3β1 regulate matrix adhesion and cell-cell contact. J. Cell Biol. 163, 177-188.
68. Zheng, M. and McKeown-Longo, P. J. (2002). Regulation of HEF1 expression and phosphorylation by TGF-β1 and cell adhesion. J. Biol. Chem. 277, 39599-39608.