Caveolin-1: A critical regulator of lung injury

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 300, Issue 2, 2011, Pages

  Jin, Yang ^a   Lee, Seon Jin ^a   Minshall, Richard D ^b   Choi, Augustine M K ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Apoptosis; Caveolae; Inflammation

Indexed keywords

BLEOMYCIN; CAVEOLIN 1;

ACUTE LUNG INJURY; ANTIGEN PRESENTATION; APOPTOSIS; AUTOPHAGY; CAPILLARY LEAK SYNDROME; CAVEOLA; CELL MIGRATION; ENDOCYTOSIS; ENDOTHELIUM CELL; HUMAN; IMMUNE RESPONSE; LUNG FIBROSIS; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW;

ACUTE LUNG INJURY; ANIMALS; BLEOMYCIN; CAVEOLIN 1; DISEASE MODELS, ANIMAL; HUMANS; INFLAMMATION MEDIATORS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MODELS, BIOLOGICAL; MODELS, MOLECULAR; RESPIRATORY DISTRESS SYNDROME, ADULT; SIGNAL TRANSDUCTION; TRANSCRIPTIONAL ACTIVATION;

EID: 79551531112     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00170.2010     Document Type: Review

References (124)

1. Alonso MA, Millán J. The role of lipid rafts in signalling and membrane trafficking in T lymphocytes. J Cell Sci 114: 3957-3965, 2001.
2. Benlimame N, Le PU, Nabi IR. Localization of autocrine motility factor receptor to caveolae and clathrin-independent internalization of its ligand to smooth endoplasmic reticulum. Mol Biol Cell 9: 1773-1786, 1998.
3. Bento-Abreu A, Velasco A, Polo-Hernández E, Lillo C, Kozyraki R, Tabernero A, Medina JM. Albumin endocytosis via megalin in astrocytes is caveola- and Dab-1 dependent and is required for the synthesis of the neurotrophic factor oleic acid. J Neurochem 111: 49-60, 2009.
4. Bist A, Fielding PE, Fielding CJ. Two sterol regulatory element-like sequences mediate up-regulation of caveolin gene transcription in response to low density lipoprotein free cholesterol. Proc Natl Acad Sci USA 94: 10693-10698, 1997.
5. Buckley S, Barsky L, Driscoll B, Weinberg K, Anderson KD, Warburton D. Apoptosis and DNA damage in type 2 alveolar epithelial cells cultured from hyperoxic rats. Am J Physiol Lung Cell Mol Physiol 274: L714-L720, 1998.
6. Cai QC, Jiang QW, Zhao GM, Guo Q, Cao GW, Chen T. Putative caveolin-binding sites in SARS-CoV proteins. Acta Pharmacol Sin 24: 1051-1059, 2003.
7. Chen ZH, Lam HC, Jin Y, Kim HP, Cao J, Lee SJ, Ifedigbo E, Parameswaran H, Ryter SW, Choi AM. Autophagy protein microtubule-associated protein 1 light chain-3B (LC3B) activates extrinsic apoptosis during cigarette smoke-induced emphysema. Proc Natl Acad Sci USA 107: 18880-18885, 2010.
8. Cho KA, Ryu SJ, Park JS, Jang IS, Ahn JS, Kim KT, Park SC. Senescent phenotype can be reversed by reduction of caveolin status. J Biol Chem 278: 27789-27795, 2003.
9. Cho WJ, Chow AK, Schulz R, Daniel EE. Matrix metalloproteinase-2, caveolins, focal adhesion kinase and c-Kit in cells of the mouse myocardium. J Cell Mol Med 11: 1069-1086, 2007. (Pubitemid 350037049)
10. Conrad PA, Smart EJ, Ying YS, Anderson RG, Bloom GS. Caveolin cycles between plasma membrane caveolae and the Golgi complex by microtubule-dependent and microtubule-independent steps. J Cell Biol 131: 1421-1433, 1995.
11. Couet J, Sargiacomo M, Lisanti MP. Interaction of a receptor tyrosine kinase, EGF-R, with caveolins. Caveolin binding negatively regulates tyrosine and serine/threonine kinase activities. J Biol Chem 272: 30429-30438, 1997.
12. Dasari A, Bartholomew JN, Volonte D, Galbiati F. Oxidative stress induces premature senescence by stimulating caveolin-1 gene transcription through p38 mitogen-activated protein kinase/Sp1-mediated activation of two GC-rich promoter elements. Cancer Res 66: 10805-10814, 2006.
13. Del Galdo F, Lisanti MP, Jimenez SA. Caveolin-1, transforming growth factor-beta receptor internalization, and the pathogenesis of systemic sclerosis. Curr Opin Rheumatol 20: 713-719, 2008.
14. Dong F, Zhang X, Wold LE, Ren Q, Zhang Z, Ren J. Endothelin-1 enhances oxidative stress, cell proliferation and reduces apoptosis in human umbilical vein endothelial cells: role of ETB receptor, NADPH oxidase and caveolin-1. Br J Pharmacol 145: 323-333, 2005.
15. Drab M, Verkade P, Elger M, Kasper M, Lohn M, Lauterbach B, Menne J, Lindschau C, Mende F, Luft FC, Schedl A, Haller H, Kurzchalia TV. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293: 2449-2452, 2001.
16. Engelman JA, Chu C, Lin A, Jo H, Ikezu T, Okamoto T, Kohtz DS, Lisanti MP. Caveolin-mediated regulation of signaling along the p42/44 MAP kinase cascade in vivo. A role for the caveolin-scaffolding domain. FEBS Lett 428: 205-211, 1998. (Pubitemid 28319685)
17. Engelman JA, Lee RJ, Karnezis A, Bearss DJ, Webster M, Siegel P, Muller WJ, Windle JJ, Pestell RG, Lisanti MP. Reciprocal regulation of neu tyrosine kinase activity and caveolin-1 protein expression in vitro and in vivo. Implications for human breast cancer. J Biol Chem 273: 20448-20455, 1998.
18. Fang PK, Solomon KR, Zhuang L, Qi M, McKee M, Freeman MR, Yelick PC. Caveolin-1alpha and -1beta perform nonredundant roles in early vertebrate development. Am J Pathol 169: 2209-2222, 2006.
19. Fernández MA, Albor C, Ingelmo-Torres M, Nixon SJ, Ferguson C, Kurzchalia T, Tebar F, Enrich C, Parton RG, Pol A. Caveolin-1 is essential for liver regeneration. Science 313: 1628-1632, 2006.
20. Feron O. Endothelial nitric oxide synthase expression, and its functionality. Curr Opin Clin Nutr Metab Care 2: 291-296, 1999. (Pubitemid 129627829)
21. Feron O, Belhassen L, Kobzik L, Smith TW, Kelly RA, Michel T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 271: 22810-22814, 1996.
22. Fielding CJ, Fielding PE. Caveolae and intracellular trafficking of cholesterol. Adv Drug Deliv Rev 49: 251-264, 2001.
23. Franek WR, Horowitz S, Stansberry L, Kazzaz JA, Koo HC, Li Y, Arita Y, Davis JM, Mantell AS, Scott W, Mantell LL. Hyperoxia inhibits oxidant-induced apoptosis in lung epithelial cells. J Biol Chem 276: 569-575, 2001. (Pubitemid 32050353)
24. Frank PG, Lisanti MP. Caveolin-1 and caveolae in atherosclerosis: differential roles in fatty streak formation and neointimal hyperplasia. Curr Opin Lipidol 15: 523-529, 2004.
25. Fujimoto T, Kogo H, Nomura R, Une T. Isoforms of caveolin-1 and caveolar structure. J Cell Sci 113: 3509-3517, 2000.
26. Gadjeva M, Paradis-Bleau C, Priebe GP, Fichorova R, Pier GB. Caveolin-1 modifies the immunity to Pseudomonas aeruginosa. J Immunol 184: 296-302, 2010.
27. Galbiati F, Volonte D, Brown AM, Weinstein DE, Ben-Ze'ev A, Pestell RG, Lisanti MP. Caveolin-1 expression inhibits Wnt/beta-catenin/Lef-1 signaling by recruiting beta-catenin to caveolae membrane domains. J Biol Chem 275: 23368-23377, 2000.
28. Galbiati F, Volonte D, Engelman JA, Watanabe G, Burk R, Pestell RG, Lisanti MP. Targeted downregulation of caveolin-1 is sufficient to drive cell transformation and hyperactivate the p42/44 MAP kinase cascade. EMBO J 17: 6633-6648, 1998.
29. Garrean S, Gao XP, Brovkovych V, Shimizu J, Zhao YY, Vogel SM, Malik AB. Caveolin-1 regulates NF-kappaB activation and lung inflammatory response to sepsis induced by lipopolysaccharide. J Immunol 177: 4853-4860, 2006.
30. Glenney JR Jr, Soppet D. Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc Natl Acad Sci USA 89: 10517-10521, 1992.
31. Goetz JG, Joshi B, Lajoie P, Strugnell SS, Scudamore T, Kojic LD, Nabi IR. Concerted regulation of focal adhesion dynamics by galectin-3 and tyrosine-phosphorylated caveolin-1. J Cell Biol 180: 1261-1275, 2008.
32. Gumbleton M, Abulrob AG, Campbell L. Caveolae: an alternative membrane transport compartment. Pharm Res 17: 1035-1048, 2000.
33. Han JM, Kim Y, Lee JS, Lee CS, Lee BD, Ohba M, Kuroki T, Suh PG, Ryu SH. Localization of phospholipase D1 to caveolin-enriched membrane via palmitoylation: implications for epidermal growth factor signaling. Mol Biol Cell 13: 3976-3988, 2002.
34. Hansen CG, Bright NA, Howard G, Nichols BJ. SDPR induces membrane curvature and functions in the formation of caveolae. Nat Cell Biol 11: 807-814, 2009.
35. Hansen CG, Nichols BJ. Exploring the caves: cavins, caveolins and caveolae. Trends Cell Biol 20: 177-186, 2010.
36. Heikkilä O, Susi P, Stanway G, Hyypiä T. Integrin alphaVbeta6 is a high-affinity receptor for coxsackievirus A9. J Gen Virol 90: 197-204, 2009.
37. Hill MM, Bastiani M, Luetterforst R, Kirkham M, Kirkham A, Nixon SJ, Walser P, Abankwa D, Oorschot VM, Martin S, Hancock JF, Parton RG. PTRF-Cavin, a conserved cytoplasmic protein required for caveola formation and function. Cell 132: 113-124, 2008.
38. Hill WG, Almasri E, Ruiz WG, Apodaca G, Zeidel ML. Water and solute permeability of rat lung caveolae: high permeabilities explained by acyl chain unsaturation. Am J Physiol Cell Physiol 289: C33-C41, 2005.
39. Hoetzel A, Schmidt R, Vallbracht S, Goebel U, Dolinay T, Kim HP, Ifedigbo E, Ryter SW, Choi AM. Carbon monoxide prevents ventilator-induced lung injury via caveolin-1. Crit Care Med 37: 1708-1715, 2009.
40. Hu G, Vogel SM, Schwartz DE, Malik AB, Minshall RD. Intercellular adhesion molecule-1-dependent neutrophil adhesion to endothelial cells induces caveolae-mediated pulmonary vascular hyperpermeability. Circ Res 102: e120-e131, 2008.
41. Hu G, Ye RD, Dinauer MC, Malik AB, Minshall RD. Neutrophil caveolin-1 expression contributes to mechanism of lung inflammation and injury. Am J Physiol Lung Cell Mol Physiol 294: L178-L186, 2008.
42. Ingbar DH. Mechanisms of repair and remodeling following acute lung injury. Clin Chest Med 21: 589-616, 2000.
43. Ito J, Kheirollah A, Nagayasu Y, Lu R, Kato K, Yokoyama S. Apolipoprotein A-I increases association of cytosolic cholesterol and caveolin-1 with microtubule cytoskeletons in rat astrocytes. J Neurochem 97: 1034-1043, 2006.
44. Jin Y, Kim HP, Cao J, Zhang M, Ifedigbo E, Choi AM. Caveolin-1 regulates the secretion and cytoprotection of Cyr61 in hyperoxic cell death. FASEB J 23: 341-350, 2009.
45. Jin Y, Kim HP, Chi M, Ifedigbo E, Ryter SW, Choi AM. Deletion of caveolin-1 protects against oxidative lung injury via up-regulation of heme oxygenase-1. Am J Respir Cell Mol Biol 39: 171-179, 2008.
46. Ju H, Zou R, Venema VJ, Venema RC. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 272: 18522-18525, 1997. (Pubitemid 27318186)
47. Kasper M, Barth K. Bleomycin and its role in inducing apoptosis and senescence in lung cells - modulating effects of caveolin-1. Curr Cancer Drug Targets 9: 341-353, 2009.
48. Kogo H, Aiba T, Fujimoto T. Cell type-specific occurrence of caveolin-1alpha and -1beta in the lung caused by expression of distinct mRNAs. J Biol Chem 279: 25574-25581, 2004.
49. Lee H, Woodman SE, Engelman JA, Volonté D, Galbiati F, Kaufman HL, Lublin DM, Lisanti MP. Palmitoylation of caveolin-1 at a single site (Cys-156) controls its coupling to the c-Src tyrosine kinase: targeting of dually acylated molecules (GPI-linked, transmembrane, or cytoplasmic) to caveolae effectively uncouples c-Src and caveolin-1 (TYR-14). J Biol Chem 276: 35150-35158, 2001.
50. Lee PJ, Alam J, Sylvester SL, Inamdar N, Otterbein L, Choi AM. Regulation of heme oxygenase-1 expression in vivo and in vitro in hyperoxic lung injury. Am J Respir Cell Mol Biol 14: 556-568, 1996.
51. Lee PJ, Alam J, Wiegand GW, Choi AM. Overexpression of heme oxygenase-1 in human pulmonary epithelial cells results in cell growth arrest and increased resistance to hyperoxia. Proc Natl Acad Sci USA 93: 10393-10398, 1996.
52. Lee PJ, Jiang BH, Chin BY, Iyer NV, Alam J, Semenza GL, Choi AM. Hypoxia-inducible factor-1 mediates transcriptional activation of the heme oxygenase-1 gene in response to hypoxia. J Biol Chem 272: 5375-5381, 1997.
53. Le PU, Nabi IR. Distinct caveolae-mediated endocytic pathways target the Golgi apparatus and the endoplasmic reticulum. J Cell Sci 116: 1059-1071, 2003.
54. Le Saux O, Teeters K, Miyasato S, Choi J, Nakamatsu G, Richardson JA, Starcher B, Davis EC, Tam EK, Jourdan-Le Saux C. The role of caveolin-1 in pulmonary matrix remodeling and mechanical properties. Am J Physiol Lung Cell Mol Physiol 295: L1007-L1017, 2008.
55. Le Saux CJ, Teeters K, Miyasato SK, Hoffmann PR, Bollt O, Douet V, Shohet RV, Broide DH, Tam EK. Down-regulation of caveolin-1, an inhibitor of transforming growth factor-beta signaling, in acute allergen-induced airway remodeling. J Biol Chem 283: 5760-5768, 2008.
56. Li L, Ren CH, Tahir SA, Ren C, Thompson TC. Caveolin-1 maintains activated Akt in prostate cancer cells through scaffolding domain binding site interactions with and inhibition of serine/threonine protein phosphatases PP1 and PP2A. Mol Cell Biol 24: 9389-9404, 2003.
57. Lim JS, Choy HE, Park SC, Han JM, Jang IS, Cho KA. Caveolae-mediated entry of Salmonella typhimurium into senescent nonphagocytotic host cells. Aging Cell 9: 243-251, 2010.
58. Linge A, Weinhold K, Bläsche R, Kasper M, Barth K. Downregulation of caveolin-1 affects bleomycin-induced growth arrest and cellular senescence in A549 cells. Int J Biochem Cell Biol 39: 1964-1974, 2007.
59. Lisanti MP, Scherer PE, Tang Z, Sargiacomo M. Caveolae, caveolin and caveolin-rich membrane domains: a signalling hypothesis. Trends Cell Biol 4: 231-235, 1994.
60. Lohse MJ, Blüml K, Danner S, Krasel C. Regulators of G-protein-mediated signalling. Biochem Soc Trans 24: 975-980, 1996.
61. Lu Y, Liu DX, Tam JP. Lipid rafts are involved in SARS-CoV entry into Vero E6 cells. Biochem Biophys Res Commun 369: 344-349, 2008.
62. Lv XJ, Li YY, Zhang YJ, Mao M, Qian GS. Over-expression of caveolin-1 aggravate LPS-induced inflammatory response in AT-1 cells via up-regulation of cPLA2/p38 MAPK. Inflamm Res 59: 531-541, 2010.
63. Maniatis NA, Brovkovych V, Allen SE, John TA, Shajahan AN, Tiruppathi C, Vogel SM, Skidgel RA, Malik AB, Minshall RD. Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res 99: 870-877, 2006.
64. Mantell LL, Lee PJ. Signal transduction pathways in hyperoxia-induced lung cell death. Mol Genet Metab 71: 359-370, 2000.
65. Matute-Bello G, Frevert CW, Martin TR. Animal models of acute lung injury. Am J Physiol Lung Cell Mol Physiol 295: L379-L399, 2008.
66. Medina FA, Cohen AW, de Almeida CJ, Nagajyothi F, Braunstein VL, Teixeira MM, Tanowitz HB, Lisanti MP. Immune dysfunction in caveolin-1 null mice following infection with Trypanosoma cruzi (Tulahuen strain). Microbes Infect 9: 325-333, 2007.
67. Medina FA, de Almeida CJ, Dew E, Li J, Bonuccelli G, Williams TM, Cohen AW, Pestell RG, Frank PG, Tanowitz HB, Lisanti MP. Caveolin-1-deficient mice show defects in innate immunity and inflammatory immune response during Salmonella enterica serovar Typhimurium infection. Infect Immun 74: 6665-6674, 2006.
68. Medina FA, Williams TM, Sotgia F, Tanowitz HB, Lisanti MP. A novel role for caveolin-1 in B lymphocyte function and the development of thymus-independent immune responses. Cell Cycle 5: 1865-1871, 2006.
69. Mettouchi A, Klein S, Guo W, Lopez-Lago M, Lemichez E, Westwick JK, Giancotti FG. Integrin-specific activation of Rac controls progression through the G(1) phase of the cell cycle. Mol Cell 8: 115-127, 2001.
70. Meyrick B. Pathology of the adult respiratory distress syndrome. Crit Care Clin 2: 405-428, 1986.
71. Mirza MK, Yuan J, Gao XP, Garrean S, Brovkovych V, Malik AB, Tiruppathi C, Zhao YY. Caveolin-1 deficiency dampens Toll-like receptor 4 signaling through eNOS activation. Am J Pathol 176: 2344-2351, 2010.
72. Montesano R, Roth J, Robert A, Orci L. Non-coated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296: 651-653, 1982.
73. Mungunsukh O, Griffin AJ, Lee YH, Day RM. Bleomycin induces the extrinsic apoptotic pathway in pulmonary endothelial cells. Am J Physiol Lung Cell Mol Physiol 298: L696-L703, 2010.
74. Odajima N, Betsuyaku T, Nasuhara Y, Nishimura M. Loss of caveolin-1 in bronchiolization in lung fibrosis. J Histochem Cytochem 55: 899-909, 2007.
75. Ohnuma K, Uchiyama M, Hatano R, Takasawa W, Endo Y, Dang NH, Morimoto C. Blockade of CD26-mediated T cell costimulation with soluble caveolin-1-Ig fusion protein induces anergy in CD4+T cells. Biochem Biophys Res Commun 386: 327-332, 2009.
76. Ohnuma K, Uchiyama M, Yamochi T, Nishibashi K, Hosono O, Takahashi N, Kina S, Tanaka H, Lin X, Dang NH, Morimoto C. Caveolin-1 triggers T-cell activation via CD26 in association with CARMA1. J Biol Chem 282: 10117-10131, 2007.
77. Ohnuma K, Yamochi T, Uchiyama M, Nishibashi K, Iwata S, Hosono O, Kawasaki H, Tanaka H, Dang NH, Morimoto C. CD26 mediates dissociation of Tollip and IRAK-1 from caveolin-1 and induces upregulation of CD86 on antigen-presenting cells. Mol Cell Biol 25: 7743-7757, 2005.
78. Ohnuma K, Yamochi T, Uchiyama M, Nishibashi K, Yoshikawa N, Shimizu N, Iwata S, Tanaka H, Dang NH, Morimoto C. CD26 up-regulates expression of CD86 on antigen-presenting cells by means of caveolin-1. Proc Natl Acad Sci USA 101: 14186-14191, 2004.
79. Otterbein LE, Kolls JK, Mantell LL, Cook JL, Alam J, Choi AM. Exogenous administration of heme oxygenase-1 by gene transfer provides protection against hyperoxia-induced lung injury. J Clin Invest 103: 1047-1054, 1999.
80. Padhan K, Tanwar C, Hussain A, Hui PY, Lee MY, Cheung CY, Peiris JS, Jameel S. Severe acute respiratory syndrome coronavirus Orf3a protein interacts with caveolin. J Gen Virol 88: 3067-3077, 2007.
81. Palade GE. Fine structure of blood capillaries. J Appl Physiol 24: 1424, 1953.
82. Parat MO, Fox PL. Oxidative stress, caveolae and caveolin-1. Subcell Biochem 37: 425-441, 2004.
83. Ramirez MI, Pollack L, Millien G, Cao YX, Hinds A, Williams MC. The alpha-isoform of caveolin-1 is a marker of vasculogenesis in early lung development. J Histochem Cytochem 50: 33-42, 2002.
84. Razani B, Combs TP, Wang XB, Frank PG, Park DS, Russell RG, Li M, Tang B, Jelicks LA, Scherer PE, Lisanti MP. Caveolin-1-deficient mice are lean, resistant to diet-induced obesity, and show hypertriglyceridemia with adipocyte abnormalities. J Biol Chem 277: 8635-8647, 2002.
85. Razani B, Engelman JA, Wang XB, Schubert W, Zhang XL, Marks CB, Macaluso F, Russell RG, Li M, Pestell RG, Di Vizio D, Hou H Jr, Kneitz B, Lagaud G, Christ GJ, Edelmann W, Lisanti MP. Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276: 38121-38138, 2001.
86. Ravid D, Chuderland D, Landsman L, Lavie Y, Reich R, Liscovitch M. Filamin A is a novel caveolin-1-dependent target in IGF-I-stimulated cancer cell migration. Exp Cell Res 314: 2762-2773, 2008.
87. Rothberg KG, Heuser JE, Donzell WC, Ying YS, Glenney JR, Anderson RG. Caveolin, a protein component of caveolae membrane coats. Cell 68: 673-682, 1992.
88. Saqr HE, Omran OM, Oblinger JL, Yates AJ. TRAIL-induced apoptosis in U-1242 MG glioma cells. J Neuropathol Exp Neurol 65: 152-161, 2006.
89. Scherer PE, Tang Z, Chun M, Sargiacomo M, Lodish HF, Lisanti MP. Caveolin isoforms differ in their N-terminal protein sequence and subcellular distribution. Identification and epitope mapping of an isoform-specific monoclonal antibody probe. J Biol Chem 270: 16395-16401, 1995.
90. Schlott T, Eiffert H, Bohne W, Landgrebe J, Brunner E, Spielbauer B, Knight B. Chlamydia trachomatis modulates expression of tumor suppressor gene caveolin-1 and oncogene C-myc in the transformation zone of non-neoplastic cervical tissue. Gynecol Oncol 98: 409-419, 2005.
91. Schnitzer JE, Oh P. Aquaporin-1 in plasma membrane and caveolae provides mercury-sensitive water channels across lung endothelium. Am J Physiol Heart Circ Physiol 270: H416-H422, 1996.
92. Schnitzer JE, Oh P, Jacobson BS, Dvorak AM. Caveolae from luminal plasmalemma of rat lung endothelium: microdomains enriched in caveolin, Ca(2+)-ATPase, and inositol trisphosphate receptor. Proc Natl Acad Sci USA 92: 1759-1763, 1995.
93. Schubert W, Frank PG, Razani B, Park DS, Chow CW, Lisanti MP. Caveolae-deficient endothelial cells show defects in the uptake and transport of albumin in vivo. J Biol Chem 276: 48619-48622, 2001.
94. Schubert W, Frank PG, Woodman SE, Hyogo H, Cohen DE, Chow CW, Lisanti MP. Microvascular hyperpermeability in caveolin-1 (-/-) knock-out mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem 277: 40091-40098, 2002.
95. Schwab W, Galbiati F, Volonte D, Hempel U, Wenzel KW, Funk RH, Lisanti MP, Kasper M. Characterisation of caveolins from cartilage: expression of caveolin-1, -2 and -3 in chondrocytes and in alginate cell culture of the rat tibia. Histochem Cell Biol 112: 41-49, 1999.
96. Shack S, Wang XT, Kokkonen GC, Gorospe M, Longo DL, Holbrook NJ. Caveolin-induced activation of the phosphatidylinositol 3-kinase/Akt pathway increases arsenite cytotoxicity. Mol Cell Biol 23: 2407-2414, 2003.
97. Smart EJ, Ying YS, Conrad PA, Anderson RG. Caveolin moves from caveolae to the Golgi apparatus in response to cholesterol oxidation. J Cell Biol 127: 1185-1197, 1994.
98. Sowa G, Pypaert M, Fulton D, Sessa WC. The phosphorylation of caveolin-2 on serines 23 and 36 modulates caveolin-1-dependent caveolae formation. Proc Natl Acad Sci USA 100: 6511-6516, 2003.
99. Sowa G, Pypaert M, Sessa WC. Distinction between signaling mechanisms in lipid rafts vs. caveolae. Proc Natl Acad Sci USA 98: 14072-14077, 2001.
100. Sun Y, Hu G, Zhang X, Minshall RD. Phosphorylation of caveolin-1 regulates oxidant induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ Res 105: 676-685, 2009.
101. Sundivakkam PC, Kwiatek AM, Sharma TT, Minshall RD, Malik AB, Tiruppathi C. Caveolin-1 scaffold domain interacts with TRPC1 and IP3R3 to regulate Ca2+ store release-induced Ca2+ entry in endothelial cells. Am J Physiol Cell Physiol 296: C403-C413, 2009.
102. Thomas CM, Smart EJ. Caveolae structure and function. J Cell Mol Med 12: 796-809, 2008.
103. Tourkina E, Richard M, Gööz P, Bonner M, Pannu J, Harley R, Bernatchez PN, Sessa WC, Silver RM, Hoffman S. Antifibrotic properties of caveolin-1 scaffolding domain in vitro and in vivo. Am J Physiol Lung Cell Mol Physiol 294: L843-L861, 2008.
104. Tourkina E, Richard M, Oates J, Hofbauer A, Bonner M, Gööz P, Visconti R, Zhang J, Znoyko S, Hatfield CM, Silver RM, Hoffman S. Caveolin-1 regulates leucocyte behaviour in fibrotic lung disease. Ann Rheum Dis 69: 1220-1226, 2010.
105. Tiruppathi C, Shimizu J, Miyawaki-Shimizu K, Vogel S, Bair AM, Minshall RD, Predescu D, Malik AB. Role of NF-κB dependent caveolin-1 expression in the menchanism of increased endothelial permeability induced by LPS. J Biol Chem 283: 4210-4218, 2008.
106. van den Heuvel AP, Schulze A, Burgering BM. Direct control of caveolin-1 expression by FOXO transcription factors. Biochem J 385: 795-802, 2005.
107. Vassilieva EV, Ivanov AI, Nusrat A. Flotillin-1 stabilizes caveolin-1 in intestinal epithelial cells. Biochem Biophys Res Commun 379: 460-465, 2009.
108. Volonte D, Zhang K, Lisanti MP, Galbiati F. Expression of caveolin-1 induces premature cellular senescence in primary cultures of murine fibroblasts. Mol Biol Cell 13: 2502-2517, 2002.
109. Wallach-Dayan SB, Izbicki G, Cohen PY, Gerstl-Golan R, Fine A, Breuer R. Bleomycin initiates apoptosis of lung epithelial cells by ROS but not by Fas/FasL pathway. Am J Physiol Lung Cell Mol Physiol 290: L790-L796, 2006.
110. Wang XM, Kim HP, Song R, Choi AM. Caveolin-1 confers antiinflammatory effects in murine macrophages via the MKK3/p38 MAPK pathway. Am J Respir Cell Mol Biol 34: 434-442, 2006.
111. Wang XQ, Yan Q, Sun P, Liu JW, Go L, McDaniel SM, Paller AS. Suppression of epidermal growth factor receptor signaling by protein kinase C-alpha activation requires CD82, caveolin-1, and ganglioside. Cancer Res 67: 9986-9995, 2007.
112. Wang XM, Zhang Y, Kim HP, Zhou Z, Feghali-Bostwick CA, Liu F, Ifedigbo E, Xu X, Oury TD, Kaminski N, Choi AM. Caveolin-1: a critical regulator of lung fibrosis in idiopathic pulmonary fibrosis. J Exp Med 203: 2895-2906, 2006.
113. Wary KK, Mariotti A, Zurzolo C, Giancotti FG. A requirement for caveolin-1 and associated kinase Fyn in integrin signaling and anchorage-dependent cell growth. Cell 94: 625-634, 1998.
114. Williams TM, Medina F, Badano I, Hazan RB, Hutchinson J, Muller WJ, Chopra NG, Scherer PE, Pestell RG, Lisanti MP. Caveolin-1 gene disruption promotes mammary tumorigenesis and dramatically enhances lung metastasis in vivo. Role of Cav-1 in cell invasiveness and matrix metalloproteinase (MMP-2/9) secretion. J Biol Chem 279: 51630-51646, 2004.
115. Xie Z, Zeng X, Waldman T, Glazer RI. Transformation of mammary epithelial cells by 3-phosphoinositide-dependent protein kinase-1 activates beta-catenin and c-Myc, and down-regulates caveolin-1. Cancer Res 63: 5370-5375, 2003.
116. Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol 1: 445-458, 1955.
117. Yang G, Park S, Cao G, Goltsov A, Ren C, Truong LD, Demayo F, Thompson TC. MMTV promoter-regulated caveolin-1 overexpression yields defective parenchymal epithelia in multiple exocrine organs of transgenic mice. Exp Mol Pathol 89: 9-19, 2010.
118. Yang G, Timme TL, Naruishi K, Fujita T, Fattah el MA, Cao G, Rajagopalan K, Troung LD, Thompson TC. Mice with cav-1 gene disruption have benign stromal lesions and compromised epithelial differentiation. Exp Mol Pathol 84: 131-140, 2008.
119. Zaas DW, Swan ZD, Brown BJ, Li G, Randell SH, Degan S, Sunday ME, Wright JR, Abraham SN. Counteracting signaling activities in lipid rafts associated with the invasion of lung epithelial cells by Pseudomonas aeruginosa. J Biol Chem 284: 9955-9964, 2009.
120. Zaher TE, Miller EJ, Morrow DM, Javdan M, Mantell LL. Hyperoxia-induced signal transduction pathways in pulmonary epithelial cells. Free Radic Biol Med 42: 897-908, 2007.
121. Zhao X, Liu Y, Ma Q, Wang X, Jin H, Mehrpour M, Chen Q. Caveolin-1 negatively regulates TRAIL-induced apoptosis in human hepatocarcinoma cells. Biochem Biophys Res Commun 378: 21-26, 2009.
122. Zhao YY, Malik AB. A novel insight into the mechanism of pulmonary hypertension involving caveolin-1 deficiency and endothelial nitric oxide synthase activation. Trends Cardiovasc Med 19: 238-242, 2009.
123. Zhang M, Lin L, Lee SJ, Mo L, Cao J, Ifedigbo E, Jin Y. Deletion of caveolin-1 protects hyperoxia-induced apoptosis via survivin-mediated pathways. Am J Physiol Lung Cell Mol Physiol 297: L945-L953, 2009.
124. Zundel W, Swiersz LM, Giaccia A. Caveolin 1-mediated regulation of receptor tyrosine kinase-associated phosphatidylinositol 3-kinase activity by ceramide. Mol Cell Biol 20: 1507-1514, 2000.