Fibronectin matrix turnover occurs through a caveolin-1-dependent process

Molecular Biology of the Cell

Volumn 16, Issue 2, 2005, Pages 757-768

  Sottile, Jane ^a   Chandler, Jennifer ^a  

^a UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CHLOROQUINE; COLLAGEN TYPE 1; FIBRONECTIN; RNA; SCLEROPROTEIN; THROMBOSPONDIN 1;

ANIMAL CELL; ARTICLE; DOWN REGULATION; ENDOCYTOSIS; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; INTERNALIZATION; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN STABILITY; RAT;

ADENOVIRIDAE; ANIMALS; BLOTTING, WESTERN; CAVEOLIN 1; CAVEOLINS; CELL LINE; CHLOROQUINE; COLLAGEN TYPE I; DOWN-REGULATION; EXTRACELLULAR MATRIX; FIBRONECTINS; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT ANTIBODY TECHNIQUE; FLUORESCENT DYES; GENE EXPRESSION REGULATION; HUMANS; IODINE; MICROSCOPY, CONFOCAL; MUSCLE, SMOOTH; PROTEIN BINDING; RATS; RNA, SMALL INTERFERING; THROMBOSPONDIN 1;

ANIMALIA;

EID: 12844269776     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-08-0672     Document Type: Article

References (100)

1. Ali, I. U., and Hynes, R. O. (1978). Role of disulfide bonds in the attachment and function of large, external, transformation-sensitive glycoprotein at the cell surface. Biochem. Biophys. Acta 510, 140-150.
2. Allen-Hoffmann, B. L., Crankshaw, C. L., and Mosher, D. F. (1988). Transforming growth factor beta increases cell surface binding and assembly of exogenous (plasma) fibronectin by normal human fibroblasts. Mol. Cell. Biol. 8, 4234-4242.
3. Allen-Hofrmann, L., and Mosher, D. F. (1987). Matrix assembly sites for exogenous fibronectin are decreased on human fibroblasts after treatment with agents which increase intracellular cAMP. J. Biol. Chem. 262, 14361-14365.
4. Bourdoulous, S., Orend, G., MacKenna, D. A., Pasqualini, R., and Ruoslahti, E. (1998). Fibronectin matrix regulates activation of RHO and CDC42 GTPases and cell cycle progression. J. Cell Biol. 143, 267-276.
5. Bretscher, M. S. (1989). Endocytosis and recycling of the fibronectin receptor in Chinese hamster ovary (CHO) cells. EMBO J. 8, 1341-1348.
6. Bretscher, M. S. (1992). Circulating integrins: alpha 5 beta 1, alpha 6 beta 4 and Mac-1, but not alpha 3 beta 1, alpha 4 beta 1 or LFA-1. EMBO J. 11, 405-410.
7. Burridge, K., Chrzanowska-Wodnicka, M., and Zhong, C. (1997). Focal adhesion assembly. Trends Cell Biol. 7, 342-347.
8. Cavalli, V., Corti, M., and Gruenberg, J. (2001). Endocytosis and signaling cascades: a close encounter. FEBS Lett. 498, 190-196.
9. Chen, H., Sottile, J., Strickland, D. K., and Mosher, D. F. (1996a). Binding and degradation of thrombospondin-1 mediated through heparan sulphate proteoglycans and low-density-lipoprotein receptor-related protein: localization of the functional activity to the trimeric N- terminal heparin-binding region of thrombospondin-1. Biochem. J. 318, 959-963.
10. Chen, H., Strickland, D. K., and Mosher, D. F. (1996b). Metabolism of thrombospondin 2. Binding and degradation by 3T3 cells and glycosaminoglycan- variant CHO cells. J. Biol. Chem. 271, 15993-15999.
11. Choi, M. G., and Hynes, R. O. (1979). Biosynthesis and processing of fibronectin in NIL8 hamster cells. J. Biol. Chem. 23, 12050-12055.
12. Christopher, R. A., Judge, S. R., Vincent, P. A., Higgins, P. J., and McKeown-Longo, P. J. (1999). The amino-terminal matrix assembly domain of fibronectin stabilizes cell shape and prevents cell cycle progression. J. Cell Sci. 112, 3225-3235.
13. Chung, C. Y., and Erickson, H. P. (1997). Glycosaminoglycans modulate fibronectin matrix assembly and are essential for matrix incorporation of tenascin-C. J. Cell Sci. 110, 1413-1419.
14. Clark, R. A. F. (1996). Wound repair: overview and general considerations. In: The Molecular and Cellular Biology of Wound Repair, ed. R. A. F. Clark, New York: Plenum Press, 3-50.
15. Clark, R. A. F., McCoy, G. A., Folkvord, J. M., and McPherson, J. M. (1997). TGF-β1 stimulates cultured human fibroblasts to proliferate and produce tissue-like fibroplasia: a fibronectin matrix-dependent event. J. Cell. Physiol. 170, 69-80.
16. Darribere, T., and Schwarzbauer, J. E. (2000). Fibronectin matrix composition and organization can regulate cell migration during amphibian development. Mech. Dev. 92, 239-250.
17. de Duve, C., de Barsy, T., Poole, B., Trouet, A., Tulkens, P., and Van Hoof, F. (1974). Commentary. Lysosomotropic agents. Biochem. Pharmacol. 23, 2495-2531.
18. Drab, M. et al. (2001). Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449-2452.
19. East, L., McCarthy, A., Wienke, D., Sturge, J., Ashworth, A., and Isacke, C. M. (2003). A targeted deletion in the endocytic receptor gene Endo180 results in a defect in collagen uptake. EMBO Rep. 4, 710-716.
20. Engelholm, L. H. et al. (2003). uPARAP/Endo180 is essential for cellular uptake of collagen and promotes fibroblast collagen adhesion. J. Cell Biol. 160, 1009-1015.
21. Fish, K. N., Schmid, S. L., and Damke, H. (2000). Evidence that dynamin-2 functions as a signal-transducing GTPase. J. Cell Biol. 150, 145-154.
22. Gleizes, P. E., Noaillac-Depeyre, J., Dupont, M. A., and Gas, N. (1996). Basic fibroblast growth factor (FGF-2) is addressed to caveolae after binding to the plasma membrane of BHK cells. Eur. J. Cell Biol. 71, 144-153.
23. Godyna, S., Liau, G., Popa, I., Stefansson, S., and Argraves, W. S. (1995a). Identification of the low density lipoprotein receptor-related protein (LRP) as an endocytic receptor for thrombospondin-1. J. Cell Biol. 129, 1403-1410.
24. Godyna, S., Mann, D. M., and Argraves, W. S. (1995b). A quantitative analysis of the incorporation of fibulin-1 into extracellular matrix indicates that fibronectin assembly is required. Matrix Biol. 14, 467-477.
25. Grobmyer, S. R., Kuo, A., Orishimo, M., Okada, S. S., Cines, D. B., and Barnathan, E. S. (1993). Determinants of binding and internalization of tissue-type plasminogen activator by human vascular smooth muscle and endothelial cells. J. Biol. Chem. 268, 13291-13300.
26. Hausser, H., Ober, B., Quentin-Hoffmann, E., Schmidt, B., and Kresse, H. (1992). Endocytosis of different members of the small chondroitin/dermatan sulfate proteoglycan family. J. Biol. Chem. 267, 11559-11564.
27. Herz, J., Goldstein, J. L., Strickland, D. K., Ho, Y. K., and Brown, M. S. (1991). 39-kDa protein modulates binding of ligands to low density lipoprotein receptor-related protein/alpha 2-macroglobulin receptor. J. Biol. Chem. 266, 21232-21238.
28. Herz, J., and Strickland, D. K. (2001). LRP: a multifunctional scavenger and signaling receptor. J. Clin. Invest. 108, 779-784.
29. Hocking, D. C., and Chang, C. H. (2003). Fibronectin matrix polymerization regulates small airway epithelial cell migration. Am. J. Physiol. 285, L169-L179.
30. Hocking, D. C., and Kowalski, K. (2002). A cryptic fragment from fibronectin's III1 module localizes to lipid rafts and stimulates cell growth and contractility. J. Cell Biol. 158, 175-184.
31. Hocking, D. C., Sottile, J., and Langenbach, K. J. (2000). Stimulation of integrin-mediated cell contractility by fibronectin polymerization. J. Biol. Chem. 275, 10673-10682.
32. Holmbeck, K. et al. (1999). MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99, 81-92.
33. Hughes, P. E., Renshaw, M. W., Pfaff, M., Forsyth, J., Keivens, V. M., Schwartz, M. A., and Ginsberg, M. H. (1997). Supression of integrin activation: a novel function of a ras/raf-initiated MAP kinase pathway. Cell 88, 521-530.
34. Ignotz, R. A., and Massague, J. (1986). Transforming growth factor-β stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J. Biol. Chem. 261, 4337-4345.
35. Intengan, H. D., and Schiffrin, E. L. (2001). Vascular remodeling in hypertension: roles of apoptosis, inflammation, and fibrosis. Hypertension 38, 581-587.
36. Krishnaswamy, G., Kelley, J., Johnson, D., Youngberg, G., Stone, W., Huang, S. K., Bieber, J., and Chi, D. S. (2001). The human mast cell: functions in physiology and disease. Front. Biosci. 6, D1109-D1127.
37. Langenbach, K. J., and Sottile, J. (1999). Identification of protein disulfide isomerase activity in fibronectin. J. Biol. Chem. 274, 7032-7038.
38. Lazic, A., Dolmer, K., Strickland, D. K., and Gettins, P. G. (2003). Structural organization of the receptor associated protein. Biochemistry 42, 14913-14920.
39. Liu, J., Wang, X. B., Park, D. S., and Lisanti, M. P. (2002). Caveolin-1 expression enhances endothelial capillary tubule formation. J. Biol. Chem. 277, 10661-10668.
40. Liu, X., Wu, H., Byrne, M., Jeffrey, J., Krane, S., and Jaenisch, R. (1995). A targeted mutation at the known collagenase cleavage site in mouse type I collagen impairs tissue remodeling. J. Cell Biol. 130, 227-237.
41. McDonald, J. A., Kelley, D. G., and Broekelmann, T. J. (1982). Role of fibronectin in collagen deposition: Fab' to the gelatin-binding domain of fibronectin inhibits both fibronectin and collagen organization in fibroblast extracellular matrix. J. Cell Biol. 92, 485-492.
42. McKeown-Longo, P. J., Hanning, R., and Mosher, D. F. (1984). Binding and degradation of platelet thrombospondin by cultured fibroblasts. J. Cell Biol. 98, 22-28.
43. McKeown-Longo, P. J., and Mosher, D. F. (1984). Mechanism of formation of disulfide-bonded multimers of plasma fibronectin with the matrix-assembly receptor of fibroblasts. J. Biol. Chem. 259, 12210-12215.
44. 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.
45. Memmo, L. M., and McKeown-Longo, P. (1998). The alphavbeta5 integrin functions as an endocytic receptor for vitronectin. J. Cell Sci. 111, 425-433.
46. Miekka, S. I., Ingham, K. C., and Menache, D. (1982). Rapid methods for isolation of human plasma fibronectin. Thromb. Res. 27, 1-14.
47. Moolenaar, W. H., Kranenburg, O., Postma, F. R., and Zondag, G. C. (1997). Lysophosphatidic acid: G-protein signalling and cellular responses. Curr. Opin. Cell Biol. 9, 168-173.
48. Morla, A., Zhang, Z., and Ruoslahti, E. (1994). Superfibronectin is a functionally distinct form of fibronectin. Nature 367, 193-196.
49. Murphy-Ullrich, J. E., and Mosher, D. F. (1987). Interactions of thrombospondin with endothelial cells: receptor-mediated binding and degradation. J. Cell Biol. 105, 1603-1611.
50. Mutsaers, S. E., Bishop, J. E., McGrouther, G., and Laurent, G. J. (1997). Mechanisms of tissue repair: from wound healing to fibrosis. Int. J. Biochem. Cell Biol. 29, 5-17.
51. Nabi, I. R., and Le, P. U. (2003). Caveolae/raft-dependent endocytosis. J. Cell Biol. 161, 673-677.
52. Newby, A. C., and Zaltsman, A. B. (2000). Molecular mechanisms in intimal hyperplasia. J. Pathol. 190, 300-309.
53. Ng, T., Shima, D., Squire, A., Bastiaens, P.I.H., Gschmeissner, S., Humphries, M. J., and Parker, P. J. (1999). PKCα regulates β1 integrin-dependent cell motility through association and control of integrin traffic. EMBO J. 18, 3909-3923.
54. Nichols, B. J. (2002). A distinct class of endosome mediates clathrin-independent endocytosis to the Golgi complex. Nat. Cell Biol. 4, 374-378.
55. Ozeri, V., Tovi, A., Burstein, I., Natanson-Yaron, S., Caparon, M. G., Yamada, K. M., Akiyama, S. K., Vlodavsky, I., and Hanski, E. (1996). A two-domain mechanism for group A streptococcal adherence through protein F to the extracellular matrix. EMBO J. 15, 989-998.
56. Paddison, P. J., Caudy, A. A., Bernstein, E., Hannon, G. J., and Conklin, D. S. (2002). Short hairpin RNAs (shRNAs) induce sequence-specific silencing in mammalian cells. Genes Dev. 16, 948-958,
57. Pang, H., Le, P. U., and Nabi, I. R. (2004). Ganglioside GM1 levels are a determinant of the extent of caveolae/raft-dependent endocytosis of cholera toxin to the Golgi apparatus. J. Cell Sci. 117, 1421-1430.
58. Park, D. S. et al. (2002), Caveolin-1/3 double-knockout mice are viable, but lack both muscle and non-muscle caveolae, and develop a severe cardiomyopathic phenotype. Am. J. Pathol. 160, 2207-2217.
59. Pelkmans, L., and Helenius, A. (2002). Endocytosis via caveolae. Traffic 3, 311-320.
60. Pelkmans, L., Kartenbeck, J., and Helenius, A. (2001). Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3, 473-483.
61. Pelkmans, L., Puntener, D., and Helenius, A. (2002). Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296, 535-539.
62. 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.
63. Peterson, T. E. et al. (2003). Caveolin-1 can regulate vascular smooth muscle cell fate by switching PDGF signaling from a proliferative to an apoptotic pathway. Arterioscler Thromb. Vasc. Biol. 23, 1521-1527.
64. Pijuan-Thompson, V., and Gladson, C. L. (1997). Ligation of integrin alpha5beta1 is required for intemalization of vitronectin by integrin alphavbeta3. J. Biol. Chem. 272, 2736-2743.
65. Prescott, M. F., Sawyer, W. K., Von Linden-Reed, J., Jeune, M., Chou, M., Caplan, S. L., and Jeng, A. Y. (1999). Effect of matrix metalloproteinase inhibition on progression of atherosclerosis and aneurysm in LDL receptor-deficient mice overexpresing MMP-3, MMP-12, and MMP-12 and on restenosis in rats after balloon injury. Ann. NY Acad. Sci. 878, 179-190.
66. Raub, T. J., and Kuentzel, S. L. (1989). Kinetic and morphological evidence for endocytosis of mammalian cell integrin receptors by using an anti-fibronectin receptor beta subunit monoclonal antibody. Exp. Cell Res. 184, 407-426.
67. Razani, B. et al. (2001). Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 276, 38121-38138.
68. Rebres, R. A., McKeown-Longo, P. J., Vincent, P. A., Cho, E., and Saba, T. M. (1995). Extracellular matrix incorporation of normal and NEM-alkylated fibronectin: liver and spleen deposition. Am. J. Physiol. 269, G902-G912.
69. Roman, J., and McDonald, J. A. (1993). Fibulin's organization into the extracellular matrix of fetal lung fibroblasts is dependent on fibronectin matrix assembly. Am. J. Respir. Cell Mol. Biol. 8, 538-545.
70. Rotundo, R. F., Vincent, P. A., McKeown-Longo, P. J., Blumenstock, F. A., and Saba, T. M. (1999). Hepatic fibronectin matrix turnover in rats: involvement of the asialoglycoprotein receptor. Am. J. Physiol. 277, G1189-G1199.
71. Salicioni, A. M., Mizelle, K. S., Loukinova, E., Mikhailenko, I., Strickland, D. K., and Gonias, S. L. (2002). The low density lipoprotein receptor-related protein mediates fibronectin catabolism and inhibits fibronectin accumulation on cell surfaces. J. Biol. Chem. 277, 16160-16166.
72. Sarkissian, M., and Lafyatis, R. (1998). Transforming growth factor-beta and platelet derived growth factor regulation of fibrillar fibronectin matrix formation by synovial fibroblasts. J. Rheumatol. 25, 613-622.
73. Sasaki, T., Wiedemann, H., Matzner, M., Chu, M.-L., and Timpl, R. (1996). Expression of fibulin-2 by fibroblasts and deposition with fibronectin into a fibrillar matrix. J. Cell Sci. 109, 2895-2904.
74. Schmid, S. L., McNiven, M. A., and De Camilli, P. (1998). Dynamin and its partners: a progress report. Curr. Opin. Cell Biol. 10, 504-512.
75. Schubert, W., Frank, P. G., Razani, B., Park, D. S., Chow, C. W., and Lisanti, M. P. (2001). Caveolae-defident endothelial cells show defects in the uptake and transport of albumin in vivo. J. Biol. Chem. 276, 48619-48622.
76. Sechler, J. L., and Schwarzbauer, J. E. (1998). Control of cell cycle progression by fibronectin matrix architecture. J. Biol. Chem 273, 25533-25536.
77. Smart, E. J., and Anderson, R. G. (2002). Alterations in membrane cholesterol that affect structure and function of caveolae. Methods Enzymol. 353, 131-139.
78. Sommers, C. E., and Mosher, D. F. (1993). PKC modulation of fibronectin matrix assembly. J. Biol. Chem. 268, 22277-22280.
79. 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.
80. Sottile, J., Hocking, D. C., and Langenbach, K. J. (2000). Fibronectin polymerization stimulates cell growth by RGD-dependent and -independent mechanisms. J. Cell Sci. 113, 4287-4299.
81. Sottile, J., Hocking, D. C., and Swiatek, P. (1998). Fibronectin matrix assembly enhances adhesion-dependent cell growth. J. Cell Sci. 111, 2933-2943.
82. 1 module. Biochem. J. 323, 51-60.
83. Sottile, J., and Wiley, S. (1994). Assembly of amino-terminal fibronectin dimers into the extracellular matrix. J. Biol. Chem. 269, 17192-17198.
84. Streuli, C. (1999). Extracellular matrix remodelling and cellular differentiation. Curr. Opin. Cell Biol. 11, 634-640.
85. Tchougounova, E., Forsberg, E., Angelborg, G., Kjellen, L., and Pejler, G. (2000). Altered processing of fibronectin in mice lacking heparin. A role for heparin-dependent mast cell chymase in fibronectin degradation. J. Biol. Chem. 276, 3772-3777.
86. Tomasini-Johansson, B. R., Kaugman, N. R., Ensenberger, M. G., Ozeri, V., Hanski, E., and Mosher, D. F. (2001). Peptide from adhesin F1 inhibits fibronectin matrix assembly. J. Biol. Chem. 276, 23430-23439.
87. Towbin, H. T., Staehlin, T., and Grodon, J. (1979). Electrophoretic transfer of protein from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350-4354.
88. Upla, P., Marjomaki, V., Kankaanpaa, P., Ivaska, J., Hyypia, T., Van Der Goot, F. G., and Heino, J. (2004). Clustering induces a lateral redistribution of alpha 2 beta 1 integrin from membrane rafts to caveolae and subsequent PKC-dependent internalization. Mol. Biol. Cell 15, 625-636.
89. Van Nhieu, G. T., Krukonis, E. S., Reszka, A. A., Horwitz, A. F., and Isberg, R. R. (1996). Mutations in the cytoplasmic domain of the integrin beta1 chain indicate a role for endocytosis factors in bacterial intemalization. J. Biol. Chem. 271, 7665-7672.
90. 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 alpha 11beta 1 and alpha 2beta 1. J. Biol. Chem. 277, 37377-37381.
91. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J.A., Hanahan, D., Shapiro, S. D., Senior, R. M., and Werb, Z. (1998). MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422.
92. Wienke, D., MacFadyen, J. R., and Isacke, C.M. (2003). Identification and characterization of the endocytic transmembrane glycoprotein Endo180 as a novel collagen receptor. Mol. Biol. Cell 14, 3592-3604.
93. Wojciechowski, K., Chang, C. H., and Hocking, D. C. (2004). Expression, production, and characterization of full-length vitronectin in Escherichia coli. Protein Expr. Purif. 36, 131-138.
94. Wu, C., Keightley, S. Y., Leung-Hagesteijn, C., Radeva, G., Coppolino, M., Goicoechea, S., McDonald, J. A., and Dedhar, S. (1998). Integrin-linked protein kinase regulates fibronectin matrix assembly, E-cadherin expression and tumorigenicity. J. Biol. Chem. 273, 528-536.
95. Yanagishita, M., and Hascall, V. C. (1984). Metabolism of proteoglycans in rat ovarian glanulosa cell culture. Multiple intracellular degradative pathways and the effect of chloroquine. J. Biol. Chem. 259, 10270-10283.
96. Yatohgo, T., Izumi, M., Kashiwagi, H., and Hayashi, M. (1988). Novel purification of vitronectin from human plasma by heparin affinity. Cell Struct. Funct. 13, 281-292.
97. Yong, L. C. (1997). The mast cell: origin, morphology, distribution, and function. Exp. Toxicol. Pathol. 49, 409-424.
98. Zeisberg, M., Strutz, F., and Muller, G. A. (2000). Role of fibroblast activation in inducing interstitial fibrosis. J. Nephrol. 13(Suppl 3), S111-S120.
99. Zhang, Q., Magnusson, M. K., and Mosher, D. F. (1997). Lysophosphatidic acid and microtuble-destabilizing agents stimulate fibronectin matrix assembly through rho-dependent actin stress fiber formation and cell contraction. Mol. Biol. Cell 8, 1415-1425.
100. Zhong, C., Chrzanowska-Wodnicka, M., Brown, J., Shaub, A., Belkin, A. M., and Burridge, K. (1998). Rho-mediated contractility exposes a cryptic site in fibronectin and induces fibronectin matrix assembly. J. Cell Biol. 141, 539-551.