Caveolae and caveolins in the cardiovascular system

Circulation Research

Volumn 94, Issue 11, 2004, Pages 1408-1417

  Gratton, Jean Philippe ^a   Bernatchez, Pascal ^b   Sessa, William C ^b  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Caveolaeo; Caveolins; Nitric oxide; Phenotypes; Signaling

Indexed keywords

ANTILIPEMIC AGENT; BETA 2 ADRENERGIC RECEPTOR; BRADYKININ RECEPTOR; CAVEOLIN; CAVEOLIN 1; CAVEOLIN 3; CHOLESTEROL; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LOW DENSITY LIPOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; N(G) NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE INHIBITOR; PROTEIN TYROSINE KINASE; STAT3 PROTEIN; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ATHEROSCLEROSIS; BLOOD VESSEL PERMEABILITY; CARDIOVASCULAR SYSTEM; CAVEOLA; CHOLESTEROL METABOLISM; ENDOTHELIUM CELL; FIBROBLAST; HEART HYPERTROPHY; HEART MUSCLE; HEART MUSCLE CELL; KNOCKOUT MOUSE; MECHANOTRANSDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REVIEW; SHEAR STRESS; SIGNAL TRANSDUCTION; VASCULAR SMOOTH MUSCLE;

ANIMALS; BIOLOGICAL TRANSPORT; CARDIOVASCULAR PHYSIOLOGY; CAVEOLAE; CAVEOLINS; CELL COMPARTMENTATION; CELLS, CULTURED; CHOLESTEROL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; HUMANS; MEMBRANE MICRODOMAINS; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCARDIUM; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; NITRIC OXIDE SYNTHASE TYPE III; PHENOTYPE; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION;

EID: 2942685631     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000129178.56294.17     Document Type: Review

References (123)

1. Stan RV. Structure and function of endothelial caveolae. Microsc Res Tech. 2002;57:350-364.
2. Munro S. Lipid rafts: elusive or illusive? Cell. 2003;115:377-388.
3. Parton RG, Richards AA. Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic. 2003;4: 724-738.
4. Carver LA, Schnitzer JE. Caveolae: mining little caves for new cancer targets. Nat Rev Cancer. 2003;3:571-581.
5. Razani B, Woodman SE, Lisanti MP. Caveolae: from cell biology to animal physiology. Pharmacol Rev. 2002;54:431-467.
6. Dvorak AM, Feng D. The vesiculo-vacuolar organelle (VVO). A new endothelial cell permeability organelle. J Histochem Cytochem. 2001; 49:419-432.
7. Schnitzer JE, Siflinger-Birnboim A, Del Vecchio PJ, Malik AB. Segmental differentiation of permeability, protein glycosylation, and morphology of cultured bovine lung vascular endothelium. Biochem Biophys Res Commun. 1994;199:11-19.
8. Peterson TE, Poppa V, Ueba H, Wu A, Yan C, Berk BC. Opposing effects of reactive oxygen species and cholesterol on endothelial nitric oxide synthase and endothelial cell caveolae. Circ Res. 1999;85:29-37.
9. Park H, Go YM, St John PL, Maland MC, Lisanti MP, Abrahamson DR, Jo H. Plasma membrane cholesterol is a key molecule in shear stress-dependent activation of extracellular signal-regulated kinase. J Biol Chem. 1998;273:32304-32311.
10. Boyd NL, Park H, Yi H, Boo YC, Sorescu GP, Sykes M, Jo H. Chronic shear induces caveolae formation and alters ERK and Akt responses in endothelial cells. Am J Physiol Heart Circ Physiol. 2003;285: H1113-H1122.
11. Simionescu M, Simionescu N, Palade GE. Morphometric data on the endothelium of blood capillaries. J Cell Biol. 1974;60:128-152.
12. Stewart PA. Endothelial vesicles in the blood-brain barrier: are they related to permeability? Cell Mol Neurobiol. 2000;20:149-163.
13. Schnitzer JE, Oh P, McIntosh DP. Role of GTP hydrolysis in fission of caveolae directly from plasma membranes. Science. 1996;274:239-242.
14. Oh P, McIntosh DP, Schnitzer JE. Dynamin at the neck of caveolae mediates their budding to form transport vesicles by GTP-driven fission from the plasma membrane of endothelium. J Cell Biol. 1998;141: 101-114.
15. Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol. 2001;3:473-483.
16. Severs NJ. Caveolae: static in pocketings of the plasma membrane, dynamic vesicles or plain artifact? J Cell Sci. 1988;90:341-348.
17. van Deurs B, Roepstorff K, Hommelgaard AM, Sandvig K. Caveolae: anchored, multifunctional platforms in the lipid ocean. Trends Cell Biol. 2003;13:92-100.
18. Foster LJ, De Hoog CL, Mann M. Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc Natl Acad Sci U S A. 2003;100:5813-5818.
19. Razani B, Lisanti MP. Caveolin-deficient mice: insights into caveolar function human disease. J Clin Invest. 2001;108:1553-1561.
20. Sargiacomo M, Sudol M, Tang Z, Lisanti MP. Signal transducing molecules and glycosyl-phosphatidylinositol-linked proteins form a caveolin-rich insoluble complex in MDCK cells. J Cell Biol. 1993;122: 789-807.
21. Moitier S, Parton RG, Vogel F, Behlke J, Henske A, Kurzchalia TV. VIP21-caveolin, a membrane protein constituent of the caveolar coat, oligomerizes in vivo and in vitro. Mol Biol Cell. 1995;6:911-927.
22. Smart EJ, Ying YS, Mineo C, Anderson RG. A detergent-free method for purifying caveolae membrane from tissue culture cells. Proc Natl Acad Sci U S A. 1995;92:10104-10108.
23. Song KS, Li S, Okamoto T, Quilliam LA, Sargiacomo M, Lisanti MP. Co-purification and direct interaction of Ras with caveolin, an integral membrane protein of caveolae microdomains. Detergent-free purification of caveolae microdomains. J Biol Chem. 1996;271:9690-9697.
24. 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 U S A. 1995;92:1759-1763.
25. von Haller PD, Donohoe S, Goodlett DR, Aebersold R, Watts JD. Mass spectrometric characterization of proteins extracted from Jurkat T cell detergent-resistant membrane domains. Proteomics. 2001;1:1010-1021.
26. Liu P, Rudick M, Anderson RG. Multiple functions of caveolin-1. J Biol Chem. 2002;277:41295-41298.
27. Michel CC, Curry FE. Microvascular permeability. Physiol Rev. 1999; 79:703-761.
28. Minshall RD, Tiruppathi C, Vogel SM, Malik AB. Vesicle formation and trafficking in endothelial cells and regulation of endothelial barrier function. Histochem Cell Biol. 2002;117:105-112.
29. McIntosh DP, Tan XY, Oh P, Schnitzer JE. Targeting endothelium and its dynamic caveolae for tissue-specific transcytosis in vivo: a pathway to overcome cell barriers to drug and gene delivery. Proc Natl Acad Sci U S A. 2002;99:1996-2001.
30. Okamoto T, Schlegel A, Scherer PE, Lisanti MP. Caveolins, a family of scaffolding proteins for organizing "preassembled signaling complexes" at the plasma membrane. J Biol Chem. 1998;273:5419-5422.
31. Vepa S, Scribner WM, Natarajan V. Activation of protein phosphorylation by oxidants in vascular endothelial cells: identification of tyrosine phosphorylation of caveolin. Free Radic Biol Med. 1997;22:25-35.
32. Volonte D, Galbiati F, Pestell RG, Lisanti MP. Cellular stress induces the tyrosine phosphorylation of caveolin-1 (Tyr(14)) via activation of p38 mitogen-activated protein kinase and c-Src kinase. Evidence for caveolae, the actin cytoskeleton, and focal adhesions as mechanical sensors of osmotic stress. J Biol Chem. 2001;276:8094-8103.
33. Rizzo V, Morton C, DePaola N, Schnitzer JE, Davies PF. Recruitment of endothelial caveolae into mechanotransduction pathways by flow conditioning in vitro. Am J Physiol Heart Circ Physiol. 2003;285: H1720-H1729.
34. Labrecque L, Royal I, Surprenant DS, Patterson C, Gingras D, Beliveau R. Regulation of vascular endothelial growth factor receptor-2 activity by caveolin-1 and plasma membrane cholesterol. Mol Biol Cell. 2003; 14:334-347.
35. Lee H, Park DS, Wang XB, Scherer PE, Schwartz PE, Lisanti MP. Src-induced phosphorylation of caveolin-2 on tyrosine 19. Phosphocaveolin-2 (Tyr(P)19) is localized near focal adhesions, remains associated with lipid rafts/caveolae, but no longer forms a high molecular mass hetero-oligomer with caveolin-1. J Biol Chem. 2002;277: 34556-34567.
36. 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 U S A. 2003;100:6511-6516.
37. Murata M, Peranen J, Schreiner R, Wieland F, Kurzchalia TV, Simons K. VIP21/caveolin is a cholesterol-binding protein. Proc Natl Acad Sci U S A. 1995;92:10339-10343.
38. Uittenbogaard A, Shaul PW, Yuhanna IS, Blair A, Smart EJ. High density lipoprotein prevents oxidized low density lipoprotein-induced inhibition of endothelial nitric-oxide synthase localization and activation in caveolae. J Biol Chem. 2000;275:11278-11283.
39. Uittenbogaard A, Everson WV, Matveev SV, Smart EJ. Cholesteryl ester is transported from caveolae to internal membranes as part of a caveolin-annexin II lipid-protein complex. J Biol Chem. 2002;277: 4925-4931.
40. Everson WV, Smart EJ. Influence of caveolin, cholesterol, and lipoproteins on nitric oxide synthase: implications for vascular disease. Trends Cardiovasc Med. 2001;11:246-250.
41. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ. Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J Biol Chem. 1999;274:32512-32519.
42. Fielding CJ, Fielding PE. Cellular cholesterol efflux. Biochim Biophys Acta. 2001;1533:175-189.
43. Garcia-Cardena G, Oh P, Liu J, Schnitzer JE, Sessa WC. Targeting of nitric oxide synthase to endothelial cell caveolae via palmitoylation: implications for nitric oxide signaling. Proc Natl Acad Sci U S A. 1996; 93:6448-6453.
44. Shaul PW, Smart EJ, Robinson LJ, German Z, Yuhanna IS, Ying Y, Anderson RG, Michel T. Acylation targets endothelial nitric-oxide synthase to plasmalemmal caveolae. J Biol Chem. 1996;271: 6518-6522.
45. Liu J, Sessa WC. Identification of covalently bound amino-terminal myristic acid in endothelial nitric oxide synthase. J Biol Chem. 1994; 269:11691-11694.
46. Liu J, Garcia-Cardena G, Sessa WC. Biosynthesis and palmitoylation of endothelial nitric oxide synthase: mutagenesis of palmitoylation sites, cysteines-15 and/or -26, argues against depalmitoylation-induced translocation of the enzyme. Biochemistry. 1995;34:12333-12340.
47. Liu J, Garcia-Cardena G, Sessa WC. Palmitoylation of endothelial nitric oxide synthase is necessary for optimal stimulated release of nitric oxide: implications for caveolae localization. Biochemistry. 1996;35: 13277-13281.
48. Liu J, Hughes TE, Sessa WC. The first 35 amino acids and fatty acylation sites determine the molecular targeting of endothelial nitric oxide synthase into the Golgi region of cells: a green fluorescent protein study. J Cell Biol. 1997;137:1525-1535.
49. Sowa G, Pypaert M, Sessa WC. Distinction between signaling mechanisms in lipid rafts vs. caveolae. Proc Natl Acad Sci U S A. 2001;98: 14072-14077.
50. 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. 2001;293:2449-2452.
51. 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. 2001;276:38121-38138.
52. Feron O, Dessy C, Opel DJ, Arstall MA, Kelly RA, Michel T. Modulation of the endothelial nitric-oxide synthase-caveolin interaction in cardiac myocytes. Implications for the autonomic regulation of heart rate. J Biol Chem. 1998;273:30249-30254.
53. Smart EJ, Graf GA, McNiven MA, Sessa WC, Engelman JA, Scherer PE, Okamoto T, Lisanti MP. Caveolins, liquid-ordered domains, and signal transduction. Mol Cell Biol. 1999;19:7289-7304.
54. Garcia-Cardena G, Martasek P, Masters BS, Skidd PM, Couet J, Li S, Lisanti MP, Sessa WC. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem. 1997;272:25437-25440.
55. Ju H, Zou R, Venema VJ, Venema RC. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem. 1997;272:18522-18525.
56. Michel JB, Feron O, Sase K, Prabhakar P, Michel T. Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J Biol Chem. 1997;272:25907-25912.
57. Ghosh S, Gachhui R, Crooks C, Wu C, Lisanti MP, Stuehr DJ. Interaction between caveolin-1 and the reductase domain of endothelial nitric-oxide synthase. Consequences for catalysis. J Biol Chem. 1998; 273:22267-22271.
58. Bucci M, Gratton JP, Rudic RD, Acevedo L, Roviezzo F, Cirino G, Sessa WC. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med. 2000;6: 1362-1367.
59. Gratton JP, Lin MI, Yu J, Weiss ED, Jiang ZL, Fairchild TA, Iwakiri Y, Groszmann R, Claffey KP, Cheng YC, Sessa WC. Selective inhibition of tumor microvascular permeability by cavtratin blocks tumor progression in mice. Cancer Cell. 2003;4:31-39.
60. Zhu L, Schwegler-Berry D, Castranova V, He P. Internalization of caveolin-1 scaffolding domain facilitated by Antennapedia homeodomain attenuates PAF-induced increase in microvessel permeability. Am J Physiol Heart Circ Physiol. 2003;28:H195-H201.
61. Brouet A, Sonveaux P, Dessy C, Balligand JL, Feron O. Hsp90 ensures the transition from the early Ca2+-dependent to the late phosphorylation-dependent activation of the endothelial nitric-oxide synthase in vascular endothelial growth factor-exposed endothelial cells. J Biol Chem. 2001;276:32663-32669.
62. Fulton D, Gratton JP, Sessa WC. Post-translational control of endothelial nitric oxide synthase: why isn't calcium/calmodulin enough? J Pharmacol Exp Ther. 2001;299:818-824.
63. Davies PF, Polacek DC, Shi C, Helmke BP. The convergence of haemodynamics, genomics, and endothelial structure in studies of the focal origin of atherosclerosis. Biorheology. 2002;39:299-306.
64. Rizzo V, McIntosh DP, Oh P, Schnitzer JE. In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. J Biol Chem. 1998;273:34724-34729.
65. Rizzo V, Sung A, Oh P, Schnitzer JE. Rapid mechanotransduction in situ at the luminal cell surface of vascular endothelium and its caveolae. J Biol Chem. 1998;273:26323-26329.
66. Liu J, Oh P, Horner T, Rogers RA, Schnitzer JE. Organized endothelial cell surface signal transduction in caveolae distinct from glycosylphosphatidylinositol-anchored protein microdomains. J Biol Chem. 1997;272:7211-7222.
67. Tiruppathi C, Song W, Bergenfeldt M, Sass P, Malik AB. Gp60 activation mediates albumin transcytosis in endothelial cells by tyrosine kinase-dependent pathway. J Biol Chem. 1997;272:25968-25975.
68. Feng Y, Venema VJ, Venema RC, Tsai N, Behzadian MA, Caldwell RB. VEGF-induced permeability increase is mediated by caveolae. Invest Ophthalmol Vis Sci. 1999;40:157-167.
69. Furuchi T, Anderson RG. Cholesterol depletion of caveolae causes hyperactivation of extracellular signal-related kinase (ERK). J Biol Chem. 1998;273:21099-21104.
70. 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. 1998;428:205-211.
71. Ushio-Fukai M, Hilenski L, Santanam N, Becker PL, Ma Y, Griendling KK, Alexander RW. Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J Biol Chem. 2001;276:48269-48275.
72. Wyse BD, Prior IA, Qian H, Morrow IC, Nixon S, Muncke C, Kurzchalia TV, Thomas WG, Parton RG, Hancock JF. Caveolin interacts with the angiotensin II type 1 receptor during exocytic transport but not at the plasma membrane. J Biol Chem. 2003;278:23738-23746.
73. Chun M, Liyanage UK, Lisanti MP, Lodish HF. Signal transduction of a G protein-coupled receptor in caveolae: colocalization of endothelin and its receptor with caveolin. Proc Natl Acad Sci U S A. 1994;91: 11728-11732.
74. de Weerd WF, Leeb-Lundberg LM. Bradykinin sequesters B2 bradykinin receptors and the receptor-coupled Galpha subunits Galphaq and Galphai in caveolae in DDT1 MF-2 smooth muscle cells. J Biol Chem. 1997;272:17858-17866.
75. Escriche M, Burgueno J, Ciruela F, Canela EI, Mallol J, Enrich C, Lluis C, Franco R. Ligand-induced caveolae-mediated internalization of A1 adenosine receptors: morphological evidence of endosomal sorting and receptor recycling. Exp Cell Res. 2003;285:72-90.
76. Rapacciuolo A, Suvarna S, Barki-Harrington L, Luttrell LM, Cong M, Lefkowitz RJ, Rockman HA. Protein kinase A and G protein-coupled receptor kinase phosphorylation mediates beta-1 adrenergic receptor endocytosis through different pathways. J Biol Chem. 2003;278: 35403-35411.
77. Dessy C, Kelly RA, Balligand JL, Feron O. Dynamin mediates caveolar sequestration of muscarinic cholinergic receptors and alteration in NO signaling. EMBO J. 2000;19:4272-4280.
78. Ostrom RS, Gregorian C, Drenan RM, Xiang Y, Regan JW, Insel PA. Receptor number and eaveolar co-localization determine receptor coupling efficiency to adenylyl cyclase. J Biol Chem. 2001;276: 42063-42069.
79. Ju H, Venema VJ, Liang H, Harris MB, Zou R, Venema RC. Bradykinin activates the Janus-activated kinase/signal transducers and activators of transcription (JAK/STAT) pathway in vascular endothelial cells: localization of JAK/STAT signalling proteins in plasmalemmal caveolae. Biochem J. 2000;351:257-264.
80. Xiang Y, Rybin VO, Steinberg SF, Kobilka B. Caveolar localization dictates physiologic signaling of beta 2-adrenoceptors in neonatal cardiac myocytes. J Biol Chem. 2002;277:34280-34286.
81. Song KS, Scherer PE, Tang Z, Okamoto T, Li S, Chafel M, Chu C, Kohtz DS, Lisanti MP. Expression of caveolin-3 in skeletal, cardiac, and smooth muscle cells. Caveolin-3 is a component of the sarcolemma and co-fractionates with dystrophin and dystrophin-associated glycoproteins. J Biol Chem. 1996;271:15160-15165.
82. Murthy KS, Makhlouf GM. Heterologous desensitization mediated by G protein-specific binding to caveolin. J Biol Chem. 2000;275: 30211-30219.
83. Chatterjee S, Cao S, Peterson TE, Simari RD, Shah V. Inhibition of GTP-dependent vesicle trafficking impairs internalization of plasmalemmal eNOS and cellular nitric oxide production. J Cell Sci. 2003;116: 3645-3655.
84. Oh P, Schnitzer JE. Segregation of heterotrimeric G proteins in cell surface microdomains. G(q) binds caveolin to concentrate in caveolae, whereas G(i) and G(s) target lipid rafts by default. Mol Biol Cell. 2001;12:685-698.
85. Huang C, Hepler JR, Chen LT, Gilman AG, Anderson RG, Mumby SM. Organization of G proteins and adenylyl cyclase at the plasma membrane. Mol Biol Cell. 1997;8:2365-2378.
86. Li S, Okamoto T, Chun M, Sargiacomo M, Casanova JE, Hansen SH, Nishimoto I, Lisanti MP. Evidence for a regulated interaction between heterotrimeric G proteins and caveolin. J Biol Chem. 1995;270: 15693-15701.
87. Galbiati F, Volonte D, Chu JB, Li M, Fine SW, Fu M, Bermudez J, Pedemonte M, Weidenheim KM, Pestell RG, Minetti C, Lisanti MP. Transgenic overexpression of caveolin-3 in skeletal muscle fibers induces a Duchenne-like muscular dystrophy phenotype. Proc Natl Acad Sci U S A. 2000;97:9689-9694.
88. Aravamudan B, Volonte D, Ramani R, Gursoy E, Lisanti MP, London B, Galbiali F. Transgenic overexpression of caveolin-3 in the heart induces a cardiomyopathic phenotype. Hum Mol Genet. 2003;12: 2777-2788.
89. Park DS, Cohen AW, Frank PG, Razani B, Lee H, Williams TM, Chandra M, Shirani J, De Souza AP, Tang B, Jelicks LA, Factor SM, Weiss LM, Tanowitz HB, Lisanti MP. Caveolin-1 null (-/-) mice show dramatic reductions in life span. Biochemistry. 2003;42:15124-15131.
90. Hagiwara Y, Sasaoka T, Araishi K, Imamura M, Yorifuji H, Nonaka I, Ozawa E, Kikuchi T. Caveolin-3 deficiency causes muscle degeneration in mice. Hum Mol Genet. 2000;9:3047-3054.
91. Galbiati F, Engelman JA, Volonte D, Zhang XL, Minetti C, Li M, Hou H, Jr., Kneitz B, Edelmann W, Lisanti MP. Caveolin-3 null mice show a loss of caveolae, changes in the microdomain distribution of the dystrophin-glycoprotein complex, and t-tubule abnormalities. J Biol Chem. 2001;276:21425-21433.
92. Razani B, Wang XB, Engelman JA, Battista M, Lagaud G, Zhang XL, Kneitz B, Hou H, Jr., Christ GJ, Edelmann W, Lisanti MP. Caveolin-2-deficient mice show evidence of severe pulmonary dysfunction without disruption of caveolae. Mol Cell Biol. 2002;22:2329-2344.
93. 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. 2002;277:40091- 40098.
94. Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, Buerk DG, Huang PL, Jain RK. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci U S A. 2001;98:2604-2609.
95. Liu J, Wang XB, Park DS, Lisanti MP. Caveolin-1 expression enhances endothelial capillary tubule formation. J Biol Chem. 2002;277: 10661-10668.
96. Liu J, Razani B, Tang S, Terman BI, Ware JA, Lisanti MP. Angiogenesis activators and inhibitors differentially regulate caveolin-1 expression and caveolae formation in vascular endothelial cells. Angiogenesis inhibitors block vascular endothelial growth factor-induced down-regulation of caveolin-1. J Biol Chem. 1999;274:15781-15785.
97. Woodman SE, Ashton AW, Schubert W, Lee H, Williams TM, Medina FA, Wyckoff JB, Combs TP, Lisanti MP. Caveolin-1 knockout mice show an impaired angiogenic response to exogenous stimuli. Am J Pathol. 2003;162:2059-2068.
98. Murohara T, Asahara T, Silver M, Bauters C, Masuda H, Kalka C, Kearney M, Chen D, Symes JF, Fishman MC, Huang PL, Isner JM. Nitric oxide synthase modulates angiogenesis in response to tissue ischemia. J Clin Invest. 1998;101:2567-2578.
99. Segal SS, Brett SE, Sessa WC. Codistribution of NOS and caveolin throughout peripheral vasculature and skeletal muscle of hamsters. Am J Physiol. 1999;277:H1167-H1177.
100. Thyberg J, Roy J, Tran PK, Blomgren K, Dumitrescu A, Hedin U. Expression of caveolae on the surface of rat arterial smooth muscle cells is dependent on the phenotypic state of the cells. Lab Invest. 1997;77: 93-101.
101. Thyberg J. Caveolae and cholesterol distribution in vascular smooth muscle cells of different phenotypes. J Histochem Cytochem. 2002;50: 185-195.
102. Thyberg J. Caveolin-1 and caveolae act as regulators of mitogenic signaling in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2003;23:1481-1483.
103. Peterson TE, Guicciardi ME, Gulati R, Kleppe LS, Mueske CS, Mookadam M, Sowa G, Gores GJ, Sessa WC, Simari RD. Caveolin-1 can regulate vascular smooth muscle cell fate by switching platelet-derived growth factor signaling from a proliferative to an apoptotic pathway. Arterioscler Thromb Vasc Biol. 2003;23:1521-1527.
104. Lohn M, Furstenau M, Sagach V, Elger M, Schulze W, Luft FC, Haller H, Gollasch M. Ignition of calcium sparks in arterial and cardiac muscle through caveolae. Circ Res. 2000;87:1034-1039.
105. Je HD, Gallant C, Leavis PC, Morgan KG. Caveolin-1 Regulates Contractility in Differentiated Vascular Smooth Muscle. Am J Physiol Heart Circ Physiol. 2003;286:H91-H8.
106. Graf GA, Matveev SV, Smart EJ. Class B scavenger receptors, caveolae and cholesterol homeostasis. Trends Cardiovasc Med. 1999;9:221-225.
107. Feron O, Dessy C, Desager JP, Balligand JL. Hydroxy- methylglutarylcoenzyme A reductase inhibition promotes endothelial nitric oxide synthase activation through a decrease in caveolin abundance. Circulation. 2001;103:113-118.
108. Brouet A, Sonveaux P, Dessy C, Moniotte S, Balligand JL, Feron O. Hsp90 and caveolin are key targets for the proangiogenic nitric oxide-mediated effects of statins. Circ Res. 2001;89:866-873.
109. Pelat M, Dessy C, Massion P, Desager JP, Feron O, Balligand JL. Rosuvastatin decreases caveolin-1 and improves nitric oxide-dependent heart rate and blood pressure variability in apolipoprotein E-/- mice in vivo. Circulation. 2003;107:2480-2486.
110. Frank PG, Lee H, Park DS, Tandon NN, Scherer PE, Lisanti MP. Genetic ablation of caveolin-1 confers protection against atherosclerosis. Arterioscler Thromb Vasc Biol. 2003;24:98-105.
111. Febbraio M, Podrez EA, Smith JD, Hajjar DP, Hazen SL, Hoff HF, Sharma K, Silverstein RL. Targeted disruption of the class B scavenger receptor CD36 protects against atherosclerotic lesion development in mice. J Clin Invest. 2000;105:1049-1056.
112. Podrez EA, Febbraio M, Sheibani N, Schmitt D, Silverstein RL, Hajjar DP, Cohen PA, Frazier WA, Hoff HF, Hazen SL. Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species. J Clin Invest. 2000;105: 1095-1108.
113. 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. 1996;271:22810-22814.
114. Venema VJ, Ju H, Zou R, Venema RC. Interaction of neuronal nitric-oxide synthase with caveolin-3 in skeletal muscle. Identification of a novel caveolin scaffolding/inhibitory domain. J Biol Chem. 1997; 272:28187-28190.
115. Barouch LA, Harrison RW, Skaf MW, Rosas GO, Cappola TP, Kobeissi ZA, Hobai IA, Lemmon CA, Burnett AL, O'Rourke B, Rodriguez ER, Huang PL, Lima JA, Berkowitz DE, Hare JM. Nitric oxide regulates the heart by spatial confinement of nitric oxide synthase isoforms. Nature. 2002;416:337-339.
116. Massion PB, Balligand JL. Modulation of cardiac contraction, relaxation and rate by the endothelial nitric oxide synthase (eNOS): lessons from genetically modified mice. J Physiol. 2003;546:63-75.
117. Woodman SE, Park DS, Cohen AW, Cheung MW, Chandra M, Shirani J, Tang B, Jelicks LA, Kitsis RN, Christ GJ, Factor SM, Tanowitz HB, Lisanti MP. Caveolin-3 knock-out mice develop a progressive cardiomyopathy and show hyperactivation of the p42/44 MAPK cascade. J Biol Chem. 2002;277:38988-38997.
118. Zhao YY, Liu Y, Stan RV, Fan L, Gu Y, Dalton N, Chu PH, Peterson K, Ross J, Jr., Chien KR. Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc Natl Acad Sci U S A. 2002;99:11375-11380.
119. Cohen AW, Park DS, Woodman SE, Williams TM, Chandra M, Shirani J, Pereira de Souza A, Kitsis RN, Russell RG, Weiss LM, Tang B, Jelicks LA, Factor SM, Shtutin V, Tanowitz HB, Lisanti MP. Caveolin-1 null mice develop cardiac hypertrophy with hyperactivation of p42/44 MAP kinase in cardiac fibroblasts. Am J Physiol Cell Physiol. 2003; 284:C457-C474.
120. Park DS, Woodman SE, Schubert W, Cohen AW, Frank PG, Chandra M, Shirani J, Razani B, Tang B, Jelicks LA, Factor SM, Weiss LM, Tanowitz HB, Lisanti MP. 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. 2002;160:2207-2217.
121. Rybin VO, Xu X, Steinberg SF. Activated protein kinase C isoforms target to cardiomyocyte caveolae: stimulation of local protein phosphorylation. Circ Res. 1999;84:980-988.
122. Rybin VO, Xu X, Lisanti MP, Steinberg SF. Differential targeting of beta -adrenergic receptor subtypes and adenylyl cyclase to cardiomyocyte caveolae. A mechanism to functionally regulate the cAMP signaling pathway. J Biol Chem. 2000;275:41447-41457.
123. Rybin VO, Pak E, Alcott S, Steinberg SF. Developmental changes in beta2-adrenergic receptor signaling in ventricular myocytes: the role of Gi proteins and caveolae microdomains. Mol Pharmacol. 2003;63: 1338-1348.