Role of caveolin-1 in fibrotic diseases

Matrix Biology

Volumn 32, Issue 6, 2013, Pages 307-315

  Gvaramia, David ^a   Blaauboer, Marjolein E ^a,b   Hanemaaijer, Roeland ^b   Everts, Vincent ^a  

^a VU UNIVERSITY AMSTERDAM   (Netherlands)

^b TNO   (Netherlands)

Author keywords

Caveolin 1; CSD peptide; Fibrosis; Matrix remodeling; Mechanotransduction; TGF 1

Indexed keywords

ANTIFIBROTIC AGENT; CAVEOLIN 1; RECOMBINANT CAVEOLIN 1; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; FIBROSIS; HUMAN; MECHANICAL STRESS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SHORT SURVEY; TISSUE REPAIR;

EID: 84882616856     PISSN: 0945053X     EISSN: 15691802     Source Type: Journal    
DOI: 10.1016/j.matbio.2013.03.005     Document Type: Short Survey

References (97)

1. Annes J.P., Munger J.S., Rifkin D.B. Making sense of latent TGFbeta activation. J. Cell Sci. 2003, 116:217-224.
2. Arora P.D., Narani N., McCulloch C.A. The compliance of collagen gels regulates transforming growth factor-beta induction of alpha-smooth muscle actin in fibroblasts. Am. J. Pathol. 1999, 154:871-882.
3. Bai L., Deng X., Li J., Wang M., Li Q., An W., A.Deli, Cong Y.S. Regulation of cellular senescence by the essential caveolar component PTRF/Cavin-1. Cell Res. 2011, 21:1088-1101.
4. Bass M.D., Williamson R.C., Nunan R.D., Humphries J.D., Byron A., Morgan M.R., Martin P., Humphries M.J. A syndecan-4 hair trigger initiates wound healing through caveolin- and RhoG-regulated integrin endocytosis. Dev. Cell 2011, 21:681-693.
5. Bizet A.A., Liu K., Tran-Khanh N., Saksena A., Vorstenbosch J., Finnson K.W., Buschmann M.D., Philip A. The TGF-beta co-receptor, CD109, promotes internalization and degradation of TGF-beta receptors. Biochim. Biophys. Acta 2011, 1813:742-753.
6. Blaauboer M.E., Smit T.H., Hanemaaijer R., Stoop R., Everts V. Cyclic mechanical stretch reduces myofibroblast differentiation of primary lung fibroblasts. Biochem. Biophys. Res. Commun. 2011, 404:23-27.
7. Cerezo A., Guadamillas M.C., Goetz J.G., Sanchez-Perales S., Klein E., Assoian R.K., del Pozo M.A. The absence of caveolin-1 increases proliferation and anchorage-independent growth by a Rac-dependent, Erk-independent mechanism. Mol. Cell. Biol. 2009, 29:5046-5059.
8. Chen Y.G. Endocytic regulation of TGF-beta signaling. Cell Res. 2009, 19:58-70.
9. Chen C.L., Huang S.S., Huang J.S. Cellular heparan sulfate negatively modulates transforming growth factor-beta1 (TGF-beta1) responsiveness in epithelial cells. J. Biol. Chem. 2006, 281:11506-11514.
10. Chen C.L., Liu I.H., Fliesler S.J., Han X., Huang S.S., Huang J.S. Cholesterol suppresses cellular TGF-beta responsiveness: implications in atherogenesis. J. Cell Sci. 2007, 120:3509-3521.
11. Cho K.A., Ryu S.J., Oh Y.S., Park J.H., Lee J.W., Kim H.P., Kim K.T., Jang I.S., Park S.C. Morphological adjustment of senescent cells by modulating caveolin-1 status. J. Biol. Chem. 2004, 279:42270-42278.
12. Del Galdo F., Lisanti M.P., Jimenez S.A. Caveolin-1, transforming growth factor-beta receptor internalization, and the pathogenesis of systemic sclerosis. Curr. Opin. Rheumatol. 2008, 20:713-719.
13. del Pozo M.A., Balasubramanian N., Alderson N.B., Kiosses W.B., Grande-Garcia A., Anderson R.G., Schwartz M.A. Phospho-caveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 2005, 7:901-908.
14. Di Guglielmo G.M., Le Roy C., Goodfellow A.F., Wrana J.L. Distinct endocytic pathways regulate TGF-beta receptor signalling and turnover. Nat. Cell Biol. 2003, 5:410-421.
15. Drab M., Verkade P., Elger M., Kasper M., Lohn M., Lauterbach B., Menne J., Lindschau C., Mende F., Luft F.C., Schedl A., Haller H., Kurzchalia T.V. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001, 293:2449-2452.
16. Echarri A., Del Pozo M.A. Caveolae internalization regulates integrin-dependent signaling pathways. Cell Cycle 2006, 5:2179-2182.
17. Echarri A., Muriel O., Del Pozo M.A. Intracellular trafficking of raft/caveolae domains: insights from integrin signaling. Semin. Cell Dev. Biol. 2007, 18:627-637.
18. Eckes B., Nischt R., Krieg T. Cell-matrix interactions in dermal repair and scarring. Fibrogenesis Tissue Repair 2010, 3:4.
19. Engelman J.A., Chu C., Lin A., Jo H., Ikezu T., Okamoto T., Kohtz D.S., Lisanti M.P. Caveolin-mediated regulation of signaling along the p42/44 MAP kinase cascade in vivo. A role for the caveolin-scaffolding domain. FEBS Lett. 1998, 428:205-211.
20. Everts V., van der Zee E., Creemers L., Beertsen W. Phagocytosis and intracellular digestion of collagen, its role in turnover and remodelling. Histochem. J. 1996, 28:229-245.
21. Gauglitz G.G., Korting H.C., Pavicic T., Ruzicka T., Jeschke M.G. Hypertrophic scarring and keloids: pathomechanisms and current and emerging treatment strategies. Mol. Med. 2011, 17:113-125.
22. Gaus K., Le Lay S., Balasubramanian N., Schwartz M.A. Integrin-mediated adhesion regulates membrane order. J. Cell Biol. 2006, 174:725-734.
23. Gervasio O.L., Phillips W.D., Cole L., Allen D.G. Caveolae respond to cell stretch and contribute to stretch-induced signaling. J. Cell Sci. 2011, 124:3581-3590.
24. Goetz J.G. Bidirectional control of the inner dynamics of focal adhesions promotes cell migration. Cell Adhes. Migr. 2009, 3:185-190.
25. Goetz J.G., Joshi B., Lajoie P., Strugnell S.S., Scudamore T., Kojic L.D., Nabi I.R. Concerted regulation of focal adhesion dynamics by galectin-3 and tyrosine-phosphorylated caveolin-1. J. Cell Biol. 2008, 180:1261-1275.
26. Goetz J.G., Minguet S., Navarro-Lerida I., Lazcano J.J., Samaniego R., Calvo E., Tello M., Osteso-Ibanez T., Pellinen T., Echarri A., Cerezo A., Klein-Szanto A.J., Garcia R., Keely P.J., Sanchez-Mateos P., Cukierman E., Del Pozo M.A. Biomechanical remodeling of the microenvironment by stromal caveolin-1 favors tumor invasion and metastasis. Cell 2011, 146:148-163.
27. Goffin J.M., Pittet P., Csucs G., Lussi J.W., Meister J.J., Hinz B. Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J. Cell Biol. 2006, 172:259-268.
28. Grande-Garcia A., del Pozo M.A. Caveolin-1 in cell polarization and directional migration. Eur. J. Cell Biol. 2008, 87:641-647.
29. Grande-Garcia A., Echarri A., de Rooij J., Alderson N.B., Waterman-Storer C.M., Valdivielso J.M., del Pozo M.A. Caveolin-1 regulates cell polarization and directional migration through Src kinase and Rho GTPases. J. Cell Biol. 2007, 177:683-694.
30. Hardie W.D., Glasser S.W., Hagood J.S. Emerging concepts in the pathogenesis of lung fibrosis. Am. J. Pathol. 2009, 175:3-16.
31. Hinz B. Masters and servants of the force: the role of matrix adhesions in myofibroblast force perception and transmission. Eur. J. Cell Biol. 2006, 85:175-181.
32. Hinz B. Formation and function of the myofibroblast during tissue repair. J. Invest. Dermatol. 2007, 127:526-537.
33. Hinz B., Gabbiani G. Mechanisms of force generation and transmission by myofibroblasts. Curr. Opin. Biotechnol. 2003, 14:538-546.
34. Hinz B., Mastrangelo D., Iselin C.E., Chaponnier C., Gabbiani G. Mechanical tension controls granulation tissue contractile activity and myofibroblast differentiation. Am. J. Pathol. 2001, 159:1009-1020.
35. Hinz B., Phan S.H., Thannickal V.J., Galli A., Bochaton-Piallat M.L., Gabbiani G. The myofibroblast: one function, multiple origins. Am. J. Pathol. 2007, 170:1807-1816.
36. Hinz B., Phan S.H., Thannickal V.J., Prunotto M., Desmouliere A., Varga J., De Wever O., Mareel M., Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am. J. Pathol. 2012, 180:1340-1355.
37. Huang C., Ogawa R. Fibroproliferative disorders and their mechanobiology. Connect. Tissue Res. 2012, 53:187-196.
38. Ito T., Williams J.D., Fraser D.J., Phillips A.O. Hyaluronan regulates transforming growth factor-beta1 receptor compartmentalization. J. Biol. Chem. 2004, 279:25326-25332.
39. Karsdal M.A., Larsen L., Engsig M.T., Lou H., Ferreras M., Lochter A., Delaisse J.M., Foged N.T. Matrix metalloproteinase-dependent activation of latent transforming growth factor-beta controls the conversion of osteoblasts into osteocytes by blocking osteoblast apoptosis. J. Biol. Chem. 2002, 277:44061-44067.
40. Kasper M., Reimann T., Hempel U., Wenzel K.W., Bierhaus A., Schuh D., Dimmer V., Haroske G., Muller M. Loss of caveolin expression in type I pneumocytes as an indicator of subcellular alterations during lung fibrogenesis. Histochem. Cell Biol. 1998, 109:41-48.
41. Kim H.N., Chung H.S. Caveolin-1 inhibits membrane-type 1 matrix metalloproteinase activity. BMB Rep. 2008, 41:858-862.
42. Lafyatis R. Targeting fibrosis in systemic sclerosis. Endocr. Metab. Immune Disord. Drug Targets 2006, 6:395-400.
43. Le Lay S., Kurzchalia T.V. Getting rid of caveolins: phenotypes of caveolin-deficient animals. Biochim. Biophys. Acta 2005, 1746:322-333.
44. Le Roy C., Wrana J.L. Clathrin- and non-clathrin-mediated endocytic regulation of cell signalling. Nat. Rev. Mol. Cell Biol. 2005, 6:112-126.
45. Le Saux O., Teeters K., Miyasato S., Choi J., Nakamatsu G., Richardson J.A., Starcher B., Davis E.C., Tam E.K., Jourdan-Le Saux C. The role of caveolin-1 in pulmonary matrix remodeling and mechanical properties. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 295:L1007-L1017.
46. Lee E.K., Lee Y.S., Han I.O., Park S.H. Expression of caveolin-1 reduces cellular responses to TGF-beta1 through down-regulating the expression of TGF-beta type II receptor gene in NIH3T3 fibroblast cells. Biochem. Biophys. Res. Commun. 2007, 359:385-390.
47. Li S., Guan J.L., Chien S. Biochemistry and biomechanics of cell motility. Annu. Rev. Biomed. Eng. 2005, 7:105-150.
48. Margadant C., Sonnenberg A. Integrin-TGF-beta crosstalk in fibrosis, cancer and wound healing. EMBO Rep. 2010, 11:97-105.
49. Mayoral R., Valverde A.M., Llorente Izquierdo C., Gonzalez-Rodriguez A., Bosca L., Martin-Sanz P. Impairment of transforming growth factor beta signaling in caveolin-1-deficient hepatocytes: role in liver regeneration. J. Biol. Chem. 2010, 285:3633-3642.
50. Mercier I., Jasmin J.F., Pavlides S., Minetti C., Flomenberg N., Pestell R.G., Frank P.G., Sotgia F., Lisanti M.P. Clinical and translational implications of the caveolin gene family: lessons from mouse models and human genetic disorders. Lab. Invest. 2009, 89:614-623.
51. Miyasato S.K., Loeffler J., Shohet R., Zhang J., Lindsey M., Le Saux C.J. Caveolin-1 modulates TGF-beta1 signaling in cardiac remodeling. Matrix Biol. 2011, 30:318-329.
52. Mu D., Cambier S., Fjellbirkeland L., Baron J.L., Munger J.S., Kawakatsu H., Sheppard D., Broaddus V.C., Nishimura S.L. The integrin alpha(v)beta8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-beta1. J. Cell Biol. 2002, 157:493-507.
53. Nethe M., Hordijk P.L. A model for phospho-caveolin-1-driven turnover of focal adhesions. Cell Adh. Migr. 2011, 5:59-64.
54. Norambuena A., Schwartz M.A. Effects of integrin-mediated cell adhesion on plasma membrane lipid raft components and signaling. Mol. Biol. Cell 2011, 22:3456-3464.
55. Ohno-Iwashita Y., Shimada Y., Hayashi M., Inomata M. Plasma membrane microdomains in aging and disease. Geriatr. Gerontol. Int. 2010, 10(Suppl. 1):S41-S52.
56. Okamoto T., Schlegel A., Scherer P.E., Lisanti M.P. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J. Biol. Chem. 1998, 273:5419-5422.
57. Parat M.O. The biology of caveolae: achievements and perspectives. Int. Rev. Cell Mol. Biol. 2009, 273:117-162.
58. Parat M.O., Anand-Apte B., Fox P.L. Differential caveolin-1 polarization in endothelial cells during migration in two and three dimensions. Mol. Biol. Cell 2003, 14:3156-3168.
59. Park J.H., Han H.J. Caveolin-1 plays important role in EGF-induced migration and proliferation of mouse embryonic stem cells: involvement of PI3K/Akt and ERK. Am. J. Physiol. Cell Physiol. 2009, 297:C935-C944.
60. Parton R.G., Simons K. The multiple faces of caveolae. Nat. Rev. Mol. Cell Biol. 2007, 8:185-194.
61. Patel H.H., Murray F., Insel P.A. Caveolae as organizers of pharmacologically relevant signal transduction molecules. Annu. Rev. Pharmacol. Toxicol. 2008, 48:359-391.
62. Picardo N.E., Khan W.S. Advances in the understanding of the aetiology of Dupuytren's disease. Surgeon 2012, 10:151-158.
63. Radel C., Rizzo V. Integrin mechanotransduction stimulates caveolin-1 phosphorylation and recruitment of Csk to mediate actin reorganization. Am. J. Physiol. Heart Circ. Physiol. 2005, 288:H936-H945.
64. Razani B., Lisanti M.P. Caveolins and caveolae: molecular and functional relationships. Exp. Cell Res. 2001, 271:36-44.
65. Razani B., Engelman J.A., Wang X.B., Schubert W., Zhang X.L., Marks C.B., Macaluso F., Russell R.G., Li M., Pestell R.G., Di Vizio D., Hou H., Kneitz B., Lagaud G., Christ G.J., Edelmann W., Lisanti M.P. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J. Biol. Chem. 2001, 276:38121-38138.
66. Razani B., Zhang X.L., Bitzer M., von Gersdorff G., Bottinger E.P., Lisanti M.P. Caveolin-1 regulates transforming growth factor (TGF)-beta/SMAD signaling through an interaction with the TGF-beta type I receptor. J. Biol. Chem. 2001, 276:6727-6738.
67. Remacle A., Murphy G., Roghi C. Membrane type I-matrix metalloproteinase (MT1-MMP) is internalised by two different pathways and is recycled to the cell surface. J. Cell Sci. 2003, 116:3905-3916.
68. Rhudy R.W., McPherson J.M. Influence of the extracellular matrix on the proliferative response of human skin fibroblasts to serum and purified platelet-derived growth factor. J. Cell. Physiol. 1988, 137:185-191.
69. Sanguinetti A.R., Cao H., Corley Mastick C. Fyn is required for oxidative- and hyperosmotic-stress-induced tyrosine phosphorylation of caveolin-1. Biochem. J. 2003, 376:159-168.
70. Schor S.L. Cell proliferation and migration on collagen substrata in vitro. J. Cell Sci. 1980, 41:159-175.
71. Seals D.F., Courtneidge S.A. The ADAMs family of metalloproteases: multidomain proteins with multiple functions. Genes Dev. 2003, 17:7-30.
72. Serini G., Gabbiani G. Modulation of alpha-smooth muscle actin expression in fibroblasts by transforming growth factor-beta isoforms: an in vivo and in vitro study. Wound Repair Regen. 1996, 4:278-287.
73. Shi F., Sottile J. Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J. Cell Sci. 2008, 121:2360-2371.
74. Shi F., Harman J., Fujiwara K., Sottile J. Collagen I matrix turnover is regulated by fibronectin polymerization. Am. J. Physiol. Cell Physiol. 2010, 298:C1265-C1275.
75. Sinha B., Koster D., Ruez R., Gonnord P., Bastiani M., Abankwa D., Stan R.V., Butler-Browne G., Vedie B., Johannes L., Morone N., Parton R.G., Raposo G., Sens P., Lamaze C., Nassoy P. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011, 144:402-413.
76. Sottile J., Chandler J. Fibronectin matrix turnover occurs through a caveolin-1-dependent process. Mol. Biol. Cell 2005, 16:757-768.
77. Stehr M., Estrada C.R., Khoury J., Danciu T.E., Sullivan M.P., Peters C.A., Solomon K.R., Freeman M.R., Adam R.M. Caveolae are negative regulators of transforming growth factor-beta1 signaling in ureteral smooth muscle cells. J. Urol. 2004, 172:2451-2455.
78. Tatti O., Vehvilainen P., Lehti K., Keski-Oja J. MT1-MMP releases latent TGF-beta1 from endothelial cell extracellular matrix via proteolytic processing of LTBP-1. Exp. Cell Res. 2008, 314:2501-2514.
79. Tomasek J.J., Gabbiani G., Hinz B., Chaponnier C., Brown R.A. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 2002, 3:349-363.
80. Tourkina E., Richard M., Gooz P., Bonner M., Pannu J., Harley R., Bernatchez P.N., Sessa W.C., Silver R.M., Hoffman S. Antifibrotic properties of caveolin-1 scaffolding domain in vitro and in vivo. Am. J. Physiol. Lung Cell. Mol. Physiol. 2008, 294:L843-L861.
81. Tourkina E., Richard M., Oates J., Hofbauer A., Bonner M., Gooz P., Visconti R., Zhang J., Znoyko S., Hatfield C.M., Silver R.M., Hoffman S. Caveolin-1 regulates leucocyte behaviour in fibrotic lung disease. Ann. Rheum. Dis. 2010, 69:1220-1226.
82. Vassilieva E.V., Gerner-Smidt K., Ivanov A.I., Nusrat A. Lipid rafts mediate internalization of beta1-integrin in migrating intestinal epithelial cells. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 295:G965-G976.
83. Vaughan M.B., Howard E.W., Tomasek J.J. Transforming growth factor-beta1 promotes the morphological and functional differentiation of the myofibroblast. Exp. Cell Res. 2000, 257:180-189.
84. Volonte D., Galbiati F. Polymerase I and transcript release factor (PTRF)/cavin-1 is a novel regulator of stress-induced premature senescence. J. Biol. Chem. 2011, 286:28657-28661.
85. Volonte D., Zhang K., Lisanti M.P., Galbiati F. Expression of caveolin-1 induces premature cellular senescence in primary cultures of murine fibroblasts. Mol. Biol. Cell 2002, 13:2502-2517.
86. Wang X.M., Zhang Y., Kim H.P., Zhou Z., Feghali-Bostwick C.A., Liu F., Ifedigbo E., Xu X., Oury T.D., Kaminski N., Choi A.M. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J. Exp. Med. 2006, 203:2895-2906.
87. Wang Y., Maciejewski B.S., Drouillard D., Santos M., Hokenson M.A., Hawwa R.L., Huang Z., Sanchez-Esteban J. A role for caveolin-1 in mechanotransduction of fetal type II epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 2010, 298:L775-L783.
88. Wary K.K., Mariotti A., Zurzolo C., Giancotti F.G. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 1998, 94:625-634.
89. Wheaton K. Caveolar vesicles generate DNA damage and perpetuate cellular aging. Cell Res. 2011, 21:993-994.
90. Wight T.N., Potter-Perigo S. The extracellular matrix: an active or passive player in fibrosis?. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 301:G950-G955.
91. Williams T.M., Lisanti M.P. The caveolin proteins. Genome Biol. 2004, 5:214.
92. Wynn T.A. Common and unique mechanisms regulate fibrosis in various fibroproliferative diseases. J. Clin. Invest. 2007, 117:524-529.
93. Xia H., Diebold D., Nho R., Perlman D., Kleidon J., Kahm J., Avdulov S., Peterson M., Nerva J., Bitterman P., Henke C. Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis. J. Exp. Med. 2008, 205:1659-1672.
94. Xia H., Khalil W., Kahm J., Jessurun J., Kleidon J., Henke C.A. Pathologic caveolin-1 regulation of PTEN in idiopathic pulmonary fibrosis. Am. J. Pathol. 2010, 176:2626-2637.
95. Yu J., Bergaya S., Murata T., Alp I.F., Bauer M.P., Lin M.I., Drab M., Kurzchalia T.V., Stan R.V., Sessa W.C. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J. Clin. Invest. 2006, 116:1284-1291.
96. Zhang X.L., Topley N., Ito T., Phillips A. Interleukin-6 regulation of transforming growth factor (TGF)-beta receptor compartmentalization and turnover enhances TGF-beta1 signaling. J. Biol. Chem. 2005, 280:12239-12245.
97. Zhang G.Y., Yu Q., Cheng T., Liao T., Nie C.L., Wang A.Y., Zheng X., Xie X.G., Albers A.E., Gao W.Y. Role of caveolin-1 in the pathogenesis of tissue fibrosis by keloid-derived fibroblasts in vitro. Br. J. Dermatol. 2011, 164:623-627.