Caveolin-1 regulation of endothelial nitric oxide synthase function and oxidative stress in the endothelium

Systems Biology of Free Radicals and Antioxidants

Volumn , Issue , 2012, Pages 1343-1363

  Bonini, Marcelo G ^a   Dull, Randal O ^a   Minshall, Richard D ^a,b  

^a UNIVERSITY OF ILLINOIS HOSPITAL AND HEALTH SCIENCES SYSTEM   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Cardiovascular; Caveolae; Endothelial cell reprogramming; Endothelial dysfunction; Mechanotransduction; Nitric oxide; Peroxynitrite; Src kinase; Superoxide; Vascular disease

Indexed keywords

EID: 84929135591     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-3-642-30018-9_183     Document Type: Chapter

References (111)

1. Achcar RO, Demura Y et al (2006) Loss of caveolin and heme oxygenase expression in severe pulmonary hypertension. Chest 129(3):696-705
2. Alp NJ, McAteer MA et al (2004) Increased endothelial tetrahydrobiopterin synthesis by targeted transgenic GTP-cyclohydrolase I overexpression reduces endothelial dysfunction and atherosclerosis in ApoE-knockout mice. Arterioscler Thromb Vasc Biol 24(3):445-450
3. Arcaro A, Aubert M et al (2007) Critical role for lipid raft-associated Src kinases in activation of PI3K-Akt signalling. Cell Signal 19(5):1081-1092
4. Augusto O, Bonini MG et al (2002) Nitrogen dioxide and carbonate radical anion: two emerging radicals in biology. Free Radic Biol Med 32(9):841-859
5. Austin ED, Ma L et al (2012) Whole exome sequencing to identify a novel gene (caveolin-1) associated with human pulmonary arterial hypertension. Circ Cardiovasc Genet 5(3):336-343
6. Bakhshi F, Chen Z et al (2010) S-nitrosylation of caveolin-1 Cys156 regulates oligomer stability and caveolae trafficking. FASEB J (suppl.):D245 (abstract) Beckman JS, Beckman TW et al (1990) Apparent hydroxyl radical production by peroxynitrite: Implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 87(4):1620-1624
7. Belik J, McIntyre BA et al (2011) Pulmonary hypertension in the newborn GTP cyclohydrolase I-deficient mouse. Free Radic Biol Med 51(12):2227-2233
8. Bendall JK, Alp NJ et al (2005) Stoichiometric relationships between endothelial tetrahydrobiopterin, endothelial NO synthase (eNOS) activity, and eNOS coupling in vivo: insights from transgenic mice with endothelial-targeted GTP cyclohydrolase 1 and eNOS overexpression. Circ Res 97(9):864-871
9. Bernatchez P, Sharma A et al (2011) A noninhibitory mutant of the caveolin-1 scaffolding domain enhances eNOS-derived NO synthesis and vasodilation in mice. J Clin Invest 121(9):3747-3755
10. Bonini MG, Fernandes DC et al (2004) Albumin oxidation to diverse radicals by the peroxidase activity of Cu, Zn-superoxide dismutase in the presence of bicarbonate or nitrite: diffusible radicals produce cysteinyl and solvent-exposed and -unexposed tyrosyl radicals. Biochemistry 43(2):344-351
11. Bredt DS, Snyder SH (1990) Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc Natl Acad Sci USA 87(2):682-685
12. Browning EA, Chatterjee S et al (2012) Stop the flow: A paradigm for cell signaling mediated by reactive oxygen species in the pulmonary endothelium. Annu Rev Physiol 74:403-424
13. Bucci M, Gratton JP et al (2000) In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med 6(12):1362-1367
14. Buettner GR (1993) The pecking order of free radicals and antioxidants: lipid peroxidation, alpha-tocopherol, and ascorbate. Arch Biochem Biophys 300(2):535-543
15. Chang AC, Fu Y et al (2011) Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase. Dev Cell 21(2):288-300
16. Chen Z, Bakhshi FR et al (2012) Nitric oxide-dependent Src activation and resultant caveolin-1 phosphorylation promote eNOS/caveolin-1 binding and eNOS inhibition. Mol Biol Cell 23(7):1388-1398
17. Chester M, Seedorf G et al (2011) Cinaciguat, a soluble guanylate cyclase activator, augments cGMP after oxidative stress and causes pulmonary vasodilation in neonatal pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 301(5):L755-L764
18. Church JE, Qian J et al (2010) Inhibition of endothelial nitric oxide synthase by the lipid phosphatase PTEN. Vascul Pharmacol 52(5-6):191-198
19. Collins BM, Davis MJ et al (2012) Structure-based reassessment of the caveolin signaling model: do caveolae regulate signaling through caveolin-protein interactions? Dev Cell 23(1):11-20
20. Couet J, Li S et al (1997) Identification of peptide and protein ligands for the caveolin-scaffolding domain. Implications for the interaction of caveolin with caveolae-associated proteins. J Biol Chem 272(10):6525-6533
21. Crabtree MJ, Smith CL et al (2008) Ratio of 5,6,7,8-tetrahydrobiopterin to 7,8-dihydrobiopterin in endothelial cells determines glucose-elicited changes in NO vs. Superoxide production by eNOS. Am J Physiol Heart Circ Physiol 294(4):H1530-H1540
22. Delgado-Esteban M, Martin-Zanca D et al (2007) Inhibition of PTEN by peroxynitrite activates the phosphoinositide-3-kinase/Akt neuroprotective signaling pathway. J Neurochem 102(1):194-205
23. Diller GP, van Eijl S et al (2008) Circulating endothelial progenitor cells in patients with Eisenmenger syndrome and idiopathic pulmonary arterial hypertension. Circulation 117(23):3020-3030
24. Dimmeler S, Fleming I et al (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399(6736):601-605
25. Drab M, Verkade P et al (2001) Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293(5539):2449-2452
26. Dull RO, Dinavahi R et al (2003) Lung endothelial heparan sulfates mediate cationic peptideinduced barrier dysfunction: A new role for the glycocalyx. Am J Physiol Lung Cell Mol Physiol 285(5):L986-L995
27. Dull RO, Mecham I et al (2007) Heparan sulfates mediate pressure-induced increase in lung endothelial hydraulic conductivity via nitric oxide/reactive oxygen species. Am J Physiol Lung Cell Mol Physiol 292(6):L1452-L1458
28. Dull RO, Cluff M et al (2012) Lung heparan sulfates modulate K(fc) during increased vascular pressure: evidence for glycocalyx-mediated mechanotransduction. Am J Physiol Lung Cell Mol Physiol 302(9):L816-L828
29. Duplain H, Burcelin R et al (2001) Insulin resistance, hyperlipidemia, and hypertension in mice lacking endothelial nitric oxide synthase. Circulation 104(3):342-345
30. Farkas L, Gauldie J et al (2011) Pulmonary hypertension and idiopathic pulmonary fibrosis: A tale of angiogenesis, apoptosis, and growth factors. Am J Respir Cell Mol Biol 45(1):1-15
31. Fenouille N, Tichet Met al (2012) The epithelial-mesenchymal transition (EMT) regulatory factor SLUG (SNAI2) is a downstream target of SPARC and AKT in promoting melanoma cell invasion. PLoS One 7(7):e40378
32. Fernandes JL, Sampaio RO et al (2011) Comparison of inhaled nitric oxide versus oxygen on hemodynamics in patients with mitral stenosis and severe pulmonary hypertension after mitral valve surgery. Am J Cardiol 107(7):1040-1045
33. Feron O, Belhassen L et al (1996) Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem 271(37):22810-22814
34. Finkel T (2012) From sulfenylation to sulfhydration: what a thiolate needs to tolerate. Sci Signal 5(215):pe10
35. Florian JA, Kosky JR et al (2003) Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93(10):e136-e142
36. Garcia J, Sandi MJ et al (2012) Tie1 deficiency induces endothelial-mesenchymal transition. EMBO Rep 13(5):431-439
37. Garcia-Cardena G, Fan R et al (1996) Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem 271(44):27237-27240
38. Garcia-Cardena G, Martasek P et al (1997) Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 272(41):25437-25440
39. Ghosh S, Gachhui R et al (1998) Interaction between caveolin-1 and the reductase domain of endothelial nitric-oxide synthase. Consequences for catalysis. J Biol Chem 273(35):22267-22271
40. Gratton JP, Fontana J et al (2000) Reconstitution of an endothelial nitric-oxide synthase (eNOS), hsp90, and caveolin-1 complex in vitro. Evidence that hsp90 facilitates calmodulin stimulated displacement of eNOS from caveolin-1. J Biol Chem 275(29):22268-22272
41. Grille SJ, Bellacosa A et al (2003) The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines. Cancer Res 63(9):2172-2178
42. Haddad F, Kudelko K et al (2011) Pulmonary hypertension associated with left heart disease: characteristics, emerging concepts, and treatment strategies. Prog Cardiovasc Dis 54(2):154-167
43. Huang J, Kaminski PM et al (2008) Pyrrolidine dithiocarbamate restores endothelial cell membrane integrity and attenuates monocrotaline-induced pulmonary artery hypertension. Am J Physiol Lung Cell Mol Physiol 294(6):L1250-L1259
44. Iwakiri Y, Satoh A et al (2006) Nitric oxide synthase generates nitric oxide locally to regulate compartmentalized protein S-nitrosylation and protein trafficking. Proc Natl Acad Sci USA 103(52):19777-19782
45. Jasmin JF, Mercier I et al (2004) Lung remodeling and pulmonary hypertension after myocardial infarction: pathogenic role of reduced caveolin expression. Cardiovasc Res 63(4):747-755
46. Ju H, Zou R et al (1997) Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 272(30):18522-18525
47. Jurasz P, Courtman D et al (2010) Role of apoptosis in pulmonary hypertension: from experimental models to clinical trials. Pharmacol Ther 126(1):1-8
48. Karuppiah K, Druhan LJ et al (2011) Suppression of eNOS-derived superoxide by caveolin-1: A biopterin-dependent mechanism. Am J Physiol Heart Circ Physiol 301(3):H903-H911
49. Kim P, Schini VB et al (1992) Reduced production of cGMP underlies the loss of endotheliumdependent relaxations in the canine basilar artery after subarachnoid hemorrhage. Circ Res 70(2):248-256
50. Kim JH, Bugaj LJ et al (2009) Arginase inhibition restores NOS coupling and reverses endothelial dysfunction and vascular stiffness in old rats. J Appl Physiol 107(4):1249-1257
51. Klinge CM, Wickramasinghe NS et al (2008) Resveratrol stimulates nitric oxide production by increasing estrogen receptor alpha-Src-caveolin-1 interaction and phosphorylation in human umbilical vein endothelial cells. FASEB J 22(7):2185-2197
52. Knepler JL Jr, Taher LN et al (2001) Peroxynitrite causes endothelial cell monolayer barrier dysfunction. Am J Physiol Cell Physiol 281(3):C1064-C1075
53. Krasuski RA, Devendra GP et al (2011) Response to inhaled nitric oxide predicts survival in patients with pulmonary hypertension. J Card Fail 17(4):265-271
54. Lancaster JR Jr, Gaston B (2004) NO and nitrosothiols: spatial confinement and free diffusion. Am J Physiol Lung Cell Mol Physiol 287(3):L465-L466
55. Lieberman EH, O'Neill S et al (1991) S-nitrosocysteine inhibition of human platelet secretion is correlated with increases in platelet cGMP levels. Circ Res 68(6):1722-1728
56. Linder AE, McCluskey LP et al (2005) Dynamic association of nitric oxide downstream signaling molecules with endothelial caveolin-1 in rat aorta. J Pharmacol Exp Ther 314(1):9-15
57. Maniatis NA, Shinin V et al (2008) Increased pulmonary vascular resistance and defective pulmonary artery filling in caveolin-1-/- mice. Am J Physiol Lung Cell Mol Physiol 294(5): L865-L873
58. Maniatis NA, Chernaya O et al (2012) Caveolins and lung function. Adv Exp Med Biol 729:157-179
59. Mao M, Sudhahar V et al (2012a) Nitroglycerin drives endothelial nitric oxide synthase activation via the phosphatidylinositol 3-kinase/protein kinase B pathway. Free Radic Biol Med 52(2):427-435
60. Mao M, Sudhahar V et al (2012b) Nitroglycerin-induced loss of caveolin-1 results in eNOS dysfunction and nitrate tolerance. Free Radic Biol Med 53:S182-S183, abstract
61. Marin N, Zamorano P et al (2012) S-nitrosation of beta-catenin and p120 catenin: A novel regulatory mechanism in endothelial hyperpermeability. Circ Res 111(5):553-563
62. Mason NA, Springall DR et al (1998) High expression of endothelial nitric oxide synthase in plexiform lesions of pulmonary hypertension. J Pathol 185(3):313-318
63. Mathew R (2010) Inflammation and pulmonary hypertension. Cardiol Rev 18(2):67-72
64. Mathew R, Huang J et al (2004) Disruption of endothelial-cell caveolin-1alpha/raft scaffolding during development of monocrotaline-induced pulmonary hypertension. Circulation 110(11):1499-1506
65. Medici D, Potenta S et al (2011) Transforming growth factor-beta2 promotes snail-mediated endothelial-mesenchymal transition through convergence of Smad-dependent and Smadindependent signalling. Biochem J 437(3):515-520
66. Michel JB (1997) Role of endothelial nitric oxide in the regulation of arterial tone. Rev Prat 47(20):2251-2256
67. Mihira H, Suzuki HI et al (2012) TGF-beta-induced mesenchymal transition of MS-1 endothelial cells requires Smad-dependent cooperative activation of Rho signals and MRTF-A. J Biochem 151(2):145-156
68. Milovanova T, Chatterjee S et al (2008) Caveolae are an essential component of the pathway for endothelial cell signaling associated with abrupt reduction of shear stress. Biochim Biophys Acta 1783(10):1866-1875
69. Murata T, Lin MI et al (2007) Reexpression of caveolin-1 in endothelium rescues the vascular, cardiac, and pulmonary defects in global caveolin-1 knockout mice. J Exp Med 204(10):2373-2382
70. Olesen SP, Clapham DE et al (1988) Haemodynamic shear stress activates a K+ current in vascular endothelial cells. Nature 331(6152):168-170
71. O'Riordan E, Mendelev N et al (2007) Chronic NOS inhibition actuates endothelial-mesenchymal transformation. Am J Physiol Heart Circ Physiol 292(1):H285-H294
72. Pahakis MY, Kosky JR et al (2007) The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun 355(1):228-233
73. Park H, Go YM et al (1998) Plasma membrane cholesterol is a key molecule in shear stressdependent activation of extracellular signal-regulated kinase. J Biol Chem 273(48):32304-32311
74. Patel HH, Zhang S et al (2007) Increased smooth muscle cell expression of caveolin-1 and caveolae contribute to the pathophysiology of idiopathic pulmonary arterial hypertension. FASEB J 21(11):2970-2979
75. Place AT, Chen Z et al (2011) Cooperative role of caveolin-1 and C-terminal Src kinase binding protein in C-terminal Src kinase-mediated negative regulation of c-Src. Mol Pharmacol 80(4):665-672
76. Pryor WA, Stone K (1993) Oxidants in cigarette smoke. Radicals, hydrogen peroxide, peroxynitrate, and peroxynitrite. Ann N Y Acad Sci 686:12-27, discussion 27-18
77. Razani B, Engelman JA et al (2001) Caveolin-1 null mice are viable but show evidence of hyperproliferative and vascular abnormalities. J Biol Chem 276(41):38121-38138
78. Repetto S, Salani B et al (2005) Insulin and IGF-I phosphorylate eNOS in HUVECs by a caveolin-1 dependent mechanism. Biochem Biophys Res Commun 337(3):849-852
79. Rivero-Vilches FJ, de Frutos S et al (2003) Differential relaxing responses to particulate or soluble guanylyl cyclase activation on endothelial cells: A mechanism dependent on PKG-I alpha activation by NO/cGMP. Am J Physiol Cell Physiol 285(4):C891-C898
80. Rizzo V, McIntosh DP et al (1998) In situ flow activates endothelial nitric oxide synthase in luminal caveolae of endothelium with rapid caveolin dissociation and calmodulin association. J Biol Chem 273(52):34724-34729
81. Sakao S, Tatsumi K et al (2010) Reversible or irreversible remodeling in pulmonary arterial hypertension. Am J Respir Cell Mol Biol 43(6):629-634
82. Schermuly RT, Ghofrani HA et al (2011) Mechanisms of disease: pulmonary arterial hypertension. Nat Rev Cardiol 8(8):443-455
83. Schubert W, Frank PG et al (2002) Microvascular hyperpermeability in caveolin-1 (-/-) knockout mice. Treatment with a specific nitric-oxide synthase inhibitor, L-NAME, restores normal microvascular permeability in Cav-1 null mice. J Biol Chem 277(42):40091-40098
84. Schulz E, Jansen T et al (2008) Nitric oxide, tetrahydrobiopterin, oxidative stress, and endothelial dysfunction in hypertension. Antioxid Redox Signal 10(6):1115-1126
85. Sehgal PB, Lee JE (2011) Protein trafficking dysfunctions: role in the pathogenesis of pulmonary arterial hypertension. Pulm Circ 1(1):17-32
86. Shesely EG, Maeda N et al (1996) Elevated blood pressures in mice lacking endothelial nitric oxide synthase. Proc Natl Acad Sci USA 93(23):13176-13181
87. Shinin V, Temple AL et al (2010) Caveolin-1 regulates notch signaling-dependent pulmonary endothelial tip cell specification during angiogenesis. Proc Amer Thorac Soc (suppl.):A5230 (abstract)
88. Siddiqui MR, Komarova YA et al (2011) Caveolin-1-eNOS signaling promotes p190RhoGAP-A nitration and endothelial permeability. J Cell Biol 193(5):841-850
89. Song LB, Li J et al (2009) The polycomb group protein Bmi-1 represses the tumor suppressor PTEN and induces epithelial-mesenchymal transition in human nasopharyngeal epithelial cells. J Clin Invest 119(12):3626-3636
90. Sun Y, Hu G et al (2009) Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ Res 105(7):676-685
91. Thomas DD, Liu X et al (2001) The biological lifetime of nitric oxide: implications for the perivascular dynamics of NO and O2. Proc Natl Acad Sci USA 98(1):355-360
92. Tie L, Li XJ et al (2009) Endothelium-specific GTP cyclohydrolase I overexpression accelerates refractory wound healing by suppressing oxidative stress in diabetes. Am J Physiol Endocrinol Metab 296(6):E1423-E1429
93. Urakami T, Jarvinen TA et al (2011) Peptide-directed highly selective targeting of pulmonary arterial hypertension. Am J Pathol 178(6):2489-2495
94. van Meeteren LA, ten Dijke P (2012) Regulation of endothelial cell plasticity by TGF-beta. Cell Tissue Res 347(1):177-186
95. Vasquez-Vivar J, Kalyanaraman B et al (1998) Superoxide generation by endothelial nitric oxide synthase: The influence of cofactors. Proc Natl Acad Sci USA 95(16):9220-9225
96. Vasquez-Vivar J, Martasek P et al (2002) The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study. Biochem J 362(Pt 3):733-739
97. Vasquez-Vivar J, Kalyanaraman B et al (2003) The role of tetrahydrobiopterin in superoxide generation from eNOS: enzymology and physiological implications. Free Radic Res 37(2):121-127
98. Wang XL, Zhang L et al (2006) Free fatty acids inhibit insulin signaling-stimulated endothelial nitric oxide synthase activation through upregulating PTEN or inhibiting Akt kinase. Diabetes 55(8):2301-2310
99. Wang H, Quah SY et al (2007) PRL-3 down-regulates PTEN expression and signals through PI3K to promote epithelial-mesenchymal transition. Cancer Res 67(7):2922-2926
100. Wang H, Wang AX et al (2009) The trafficking/interaction of eNOS and caveolin-1 induced by insulin modulates endothelial nitric oxide production. Mol Endocrinol 23(10):1613-1623
101. Wenzel P, Schulz E et al (2008) AT1-Receptor blockade by telmisartan upregulates GTPcyclohydrolase I and protects eNOS in diabetic rats. Free Radic Biol Med 45(5):619-626
102. Whitsett J, Martasek P et al (2006) Endothelial cell superoxide anion radical generation is not dependent on endothelial nitric oxide synthase-serine 1179 phosphorylation and endothelial nitric oxide synthase dimer/monomer distribution. Free Radic Biol Med 40(11):2056-2068
103. Wood PM (1988) The potential diagram for oxygen at pH 7. Biochem J 253(1):287-289
104. Wunderlich C, Schober K et al (2006) Disruption of caveolin-1 leads to enhanced nitrosative stress and severe systolic and diastolic heart failure. Biochem Biophys Res Commun 340(2):702-708
105. Wunderlich C, Schmeisser A et al (2008a) Chronic NOS inhibition prevents adverse lung remodeling and pulmonary arterial hypertension in caveolin-1 knockout mice. Pulm Pharmacol Ther 21(3):507-515
106. Wunderlich C, Schober K et al (2008b) The adverse cardiopulmonary phenotype of caveolin-1 deficient mice is mediated by a dysfunctional endothelium. J Mol Cell Cardiol 44(5):938-947
107. Yang X, Long L et al (2011) Expression of mutant BMPR-II in pulmonary endothelial cells promotes apoptosis and a release of factors that stimulate proliferation of pulmonary arterial smooth muscle cells. Pulm Circ 1(1):103-110
108. Yue L, Bian JT et al (2012) Apolipoprotein E enhances endothelial-NO production by modulating caveolin 1 interaction with endothelial NO synthase. Hypertension 60(4):1040-1046
109. Zeisberg EM, Tarnavski O et al (2007) Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 13(8):952-961
110. Zhao YY, Liu Y et al (2002) Defects in caveolin-1 cause dilated cardiomyopathy and pulmonary hypertension in knockout mice. Proc Natl Acad Sci USA 99(17):11375-11380
111. Zhao YY, Zhao YD et al (2009) Persistent eNOS activation secondary to caveolin-1 deficiency induces pulmonary hypertension in mice and humans through PKG nitration. J Clin Invest 119(7):2009-2018