Interaction of free radicals, matrix metalloproteinases and caveolin-1 impacts blood-brain barrier permeability

Frontiers in Bioscience - Scholar

Volumn 3 S, Issue 4, 2011, Pages 1216-1231

  Gu, Yong ^a   Dee, Cathleen Michelle ^b   Shen, Jiangang ^a,c  

^a THE UNIVERSITY OF HONG KONG   (Hong Kong)

^b UNIVERSITY OF HONG KONG   (Hong Kong)

^c UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Blood brain barrier; Caveolin 1; Cerebral ischemia; Free radicals; Nitric oxide; Reactive nitrogen species; Reactive oxygen species; Review

Indexed keywords

CAVEOLIN 1; CLAUDIN; ENZYME PRECURSOR; FREE RADICAL; GELATINASE A; GELATINASE B; JUNCTIONAL ADHESION MOLECULE A; MATRIX METALLOPROTEINASE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXYNITRITE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; TIGHT JUNCTION PROTEIN; XANTHINE OXIDASE;

ARTICLE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN DEATH; BRAIN EDEMA; BRAIN HEMORRHAGE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; BRAIN TISSUE; DOWN REGULATION; ELECTRON SPIN RESONANCE; ENCEPHALITIS; ENDOTHELIUM CELL; ENZYME ACTIVATION; EXTRACELLULAR MATRIX; INFLAMMATION; OXIDATIVE STRESS; POSITIVE FEEDBACK; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; REPERFUSION INJURY; SIGNAL TRANSDUCTION; SPIN TRAPPING; TRAUMATIC BRAIN INJURY; WILD TYPE; BIOLOGICAL MODEL; BIOSYNTHESIS; HUMAN; METABOLISM; PERMEABILITY; PHYSIOLOGY; REVIEW; TIGHT JUNCTION;

BLOOD-BRAIN BARRIER; CAVEOLIN 1; FREE RADICALS; HUMANS; MATRIX METALLOPROTEINASES; MODELS, BIOLOGICAL; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; OXIDATIVE STRESS; PERMEABILITY; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; REPERFUSION INJURY; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS;

EID: 80053121818     PISSN: 19450516     EISSN: 19450524     Source Type: Journal    
DOI: None     Document Type: Article

References (165)

1. Hensley, K., Robinson, K. A., Gabbita, S. P., S alsman, S. Floyd, R. A. Reactive oxygen species, cell signaling, and cell injury. Free Radic Biol Med, 28(10), 1456-62 (2000)
2. Droge, W. Free radicals in the physiological control of cell function. Physiol Rev, 82(1), 47-95 (2002)
3. Chan, P. H. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab, 21(1), 2-14 (2001)
4. Pun, P. B., Lu, J. Moochhala, S. Involvement of ROS in BBB dysfunction. Free Radic Res, 43(4), 348-64 (2009)
5. Gursoy-Ozdemir, Y., Bolay, H., Saribas, O. Dalkara, T. Role of endothelial nitric oxide generation and peroxynitrite formation in reperfusion injury after focal cerebral ischemia. Stroke, 31(8), 1974-80; discussion 1981 (2000)
6. Gursoy-Ozdemir, Y., Can, A. Dalkara, T. Reperfusioninduced oxidative/nitrative injury to neurovascular unit after focal cerebral ischemia. Stroke, 35(6), 1449-53 (2004)
7. Jasmin, J. F., Malhotra, S., Singh Dhallu, M., Mercier, I., Rosenbaum, D. M. Lisanti, M. P. Caveolin-1 deficiency increases cerebral ischemic injury. Circ Res, 100(5), 721-9 (2007)
8. Chow, A. K., Cena, J., El-Yazbi, A. F., Crawford, B. D., Holt, A., Cho, W. J., Daniel, E. E. Schulz, R. Caveolin-1 inhibits matrix metalloproteinase-2 activity in the heart. J Mol Cell Cardiol, 42(4), 896-901 (2007)
9. Shen, J., Ma, S., Chan, P., Lee, W., Fung, P. C., Cheung, R. T., Tong, Y. Liu, K. J. Nitric oxide down-regulates caveolin-1 expression in rat brains during focal cerebral ischemia and reperfusion injury. J Neurochem, 96(4), 1078-89 (2006)
10. Garcia-Cardena, G., Martasek, P., Masters, B. S., Skidd, P. M., Couet, J., Li, S., Lisanti, M. P. Sessa, W. C. 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), 25437-40 (1997)
11. Betz, A. L. Alterations in cerebral endothelial cell function in ischemia. Adv Neurol, 71, 301-11; discussion 311-3 (1996)
12. Gasche, Y., Soccal, P. M., Kanemitsu, M. Copin, J. C. Matrix metalloproteinases and diseases of the central nervous system with a special emphasis on ischemic brain. Front Biosci, 11, 1289-301 (2006)
13. Grossmann, J. Molecular mechanisms of "detachmentinduced apoptosis-Anoikis" . Apoptosis, 7(3), 247-60 (2002)
14. Mannello, F., Luchetti, F., Falcieri, E. Papa, S. Multiple roles of matrix metalloproteinases during apoptosis. Apoptosis, 10(1), 19-24 (2005)
15. Persidsky, Y ., Ramirez, S. H., Haorah, J. Kanmogne, G. D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol, 1(3), 223-36 (2006)
16. Sandoval, K. E. Witt, K. A. Blood-brain barrier tight junction permeability and ischemic stroke. Neurobiol Dis, 32(2), 200-19 (2008)
17. Hawkins, B. T. Davis, T. P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev, 57(2), 173-85 (2005)
18. Simionescu, M., Simionescu, N. Palade, G. E. Segmental differentiations of cell junctions in the vascular endothelium. Arteries and veins. J Cell Biol, 68(3), 705-23 (1976)
19. Mitic, L. L. Anderson, J. M. Molecular architecture of tight junctions. Annu Rev Physiol, 60, 121-42 (1998)
20. Del Maschio, A., De Luigi, A., Martin-Padura, I., Brockhaus, M., Bartfai, T., Fruscella, P., Adorini, L., Martino, G., Furlan, R., De Simoni, M. G. Dejana, E. Leukocyte recruitment in the cerebrospinal fluid of mice withexperimental meningitis is inhibited by an antibody to junctional adhesion molecule (JAM). J Exp Med, 190(9), 1351-6 (1999)
21. Martin-Padura, I., Lostaglio, S., Schneemann, M., Williams, L., Romano, M., Fruscella, P., Panzeri, C., Stoppacciaro, A., Ruco, L., Villa, A., Simmons, D. Dejana, E. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol, 142(1), 117-27 (1998)
22. Yeung, D., Manias, J. L., Stewart, D. J. Nag, S. Decreased junctional adhesion molecule-A expression during blood-brain barrier breakdown. Acta Neuropathol, 115(6), 635-42 (2008)
23. Furuse, M., Hirase, T., Itoh, M., Nagafuchi, A., Yonemura, S. Tsukita, S. Occludin: a novel integral membrane protein localizing at tight junctions. J Cell Biol, 123(6 Pt 2), 1777-88 (1993)
24. Furuse, M., Itoh, M., Hirase, T., Nagafuchi, A., Yonemura, S. Tsukita, S. Direct association of occludin with ZO-1 and its possible involvement in the localization of occludin at tight junctions. J Cell Biol, 127(6 Pt 1), 1617-26 (1994)
25. Fanning, A. S., Jameson, B. J., Jesaitis, L. A. Anderson, J. M. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem, 273(45), 29745-53 (1998)
26. Balda, M. S., Whitney, J. A., Flores, C., Gonzalez, S., Cereijido, M. Matter, K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J Cell Biol, 134(4), 1031-49 (1996)
27. Balda, M. S., Flores-Maldonado, C., Cereijido, M. Matter, K. Multiple domains of occludin are involved in the regulation of paracellular permeability. J Cell Biochem, 78(1), 85-96 (2000)
28. Itoh, M., Furuse, M., Morita, K., Kubota, K., Saitou, M. Tsukita, S. Direct binding of three tight junction-associated MAGUKs, ZO-1, ZO-2, and ZO-3, with the COOH termini of claudins. J Cell Biol, 147(6), 1351-63 (1999)
29. Nitta, T., Hata, M., Gotoh, S., Seo, Y., Sasaki, H., Hashimoto, N., Furuse, M. Tsukita, S. Size-selective loosening of the blood-brain barrier in claudin-5- deficient mice. J Cell Biol, 161(3), 653-60 (2003)
30. del Zoppo, G. J. Milner, R. Integrin-matrix interactions in the cerebral microvasculature. Arterioscler Thromb Vasc Biol, 26(9), 1966-75 (2006)
31. Wang, C. X. Shuaib, A. Critical role of microvasculature basal lamina in ischemic brain injury. Prog Neurobiol, 83(3), 140-8 (2007)
32. Rosenberg, G. A. Yang, Y. Vasogenic edema due to tight junction disruption by matrix metalloproteinases in cerebral ischemia. Neurosurg Focus, 22(5), E4 (2007)
33. Massova, I., Kotra, L. P., Fridman, R. Mobashery, S. Matrix metalloproteinases: structures, evolution, and diversification. FASEB J, 12(12), 1075-95 (1998)
34. Yong, V. W., Krekoski, C. A., Forsyth, P. A., Bell, R. Edwards, D. R. Matrix metalloproteinases and diseases of the CNS. Trends Neurosci, 21(2), 75-80 (1998)
35. Clark, A. W., Krekoski, C. A., Bou, S. S., Chapman, K. R. Edwards, D. R. Increased gelatinase A (MMP-2) and gelatinase B (MMP-9) activities in human brain after focal ischemia. Neurosci Lett, 238(1-2), 53-6 (1997)
36. Montaner, J., Alvarez-Sabin, J., Molina, C. A., A ngles, A., Abilleira, S., Arenillas, J. Monasterio, J. Matrix metalloproteinase expression is related to hemorrhagic transformation after cardioembolic stroke. Stroke, 32(12), 2762-7 (2001)
37. Sato, H., Takino, T., Okada, Y., Cao, J., Shinagawa, A., Yamamoto, E. Seiki, M. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature, 370(6484), 61-5 (1994)
38. Strongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A. Goldberg, G. I. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem, 270(10), 5331-8 (1995)
39. Chang, D. I., Hosomi, N., Lucero, J., Heo, J. H., Abumiya, T., Mazar, A. P. del Zoppo, G. J. Activation systems for latent matrix metalloproteinase-2 are upregulated immediately after focal cerebral ischemia. J Cereb Blood Flow Metab, 23(12), 1408-19 (2003)
40. Rosenberg, G. A. Matrix metalloproteinases in neuroinflammation. Glia, 39(3), 279-91 (2002)
41. Yang, Y., Estrada, E. Y., Thompson, J. F., Liu, W. Rosenberg, G. A. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab, 27(4), 697-709 (2007)
42. Lee, C. Z., Xue, Z., Zhu, Y., Yang, G. Y. Young, W. L. Matrix metalloproteinase-9 inhibition attenuates vascular endothelial growth factor-induced intracerebral hemorrhage. Stroke, 38(9), 2563-8 (2007)
43. Gasche, Y., Copin, J. C., Sugawara, T., Fujimura, M. Chan, P. H. Matrix metalloproteinase inhibition prevents oxidative stress-associated blood-brain barrier disruption after transient focal cerebral ischemia. J Cereb Blood Flow Metab, 21(12), 1393-400 (2001)
44. Lu, A., Clark, J. F., Broderick, J. P., Pyne-Geithman, G. J., Wagner, K. R., Ran, R., Khatri, P., Tomsick, T. Sharp, F. R. Reperfusion activates metalloproteinases that contribute to neurovascular injury. Exp Neurol, 210( 2), 549-59 (2008)
45. Asahi, M., Wang, X., Mori, T., Sumii, T., Jung, J. C., Moskowitz, M. A., Fini, M. E. Lo, E. H. Effects of matrix metalloproteinase-9 gene knock-out on the proteolysis of blood-brain barrier and white matter components after cerebral ischemia. J Neurosci, 21(19), 7724-32 (2001)
46. Bauer, A. T., Burgers, H. F., Rabie, T. Marti, H. H. Matrix metalloproteinase-9 mediates hypoxia-induced vascular leakage in the brain via tight junction rearrangement. J Cereb Blood Flow Metab, 30(4), 837-48 (2010)
47. Fatokun, A. A., Stone, T. W. Smith, R. A. Oxidative stress in neurodegeneration and available means of protection. Front Biosci, 13, 3288-311 (2008)
48. Heo, J. H., Han, S. W. Lee, S. K. Free radicals as triggers of brain edema formation after stroke. Free Radic Biol Med, 39(1), 51-70 (2005)
49. Jian Liu, K. Rosenberg, G. A. Matrix metalloproteinases and free radicals in cerebral ischemia. Free Radic Biol Med, 39(1), 71-80 (2005)
50. Sheth, P., Basuroy, S., Li, C., Naren, A. P. Rao, R. K. Role of phosphatidylinositol 3-kinase in oxidative stressinduced disruption of tight junctions. J Biol Chem, 278(49), 49239-45 (2003)
51. Mertsch, K., Blasig, I. Grune, T. 4-Hydroxynonenal impairs the permeability of an in vitro rat blood-brain barrier. Neurosci Lett, 314(3), 135-8 (2001)
52. Shi, F., Cavitt, J. Audus, K. L. 21-aminosteroid and 2- (aminomethyl)chromans inhibition of arachidonic acidinduced lipid peroxidation and permeability enhancement in bovine brain microvessel endothelial cell monolayers. Free Radic Biol Med, 19(3), 349-57 (1995)
53. Hall, N. C., Carney, J. M., Plante, O. J., Cheng, M. Butterfield, D. A. Effect of 2-cyclohexene-1-one-induced glutathione diminution on ischemia/reperfusion-induced alterations in the physical state of brain synaptosomal membrane proteins and lipids. Neuroscience, 77(1), 283-90 (1997)
54. Emerich, D. F., Dean, R. L., 3rd Bartus, R. T. The role of leukocytes following cerebral ischemia: pathogenic variable or bystander reaction to emerging infarct? Exp Neurol, 173(1), 168-81 (2002)
55. Fabian, R. H. Kent, T. A. Superoxide anion production during reperfusion is reduced by an antineutrophil antibody after prolonged cerebral ischemia. Free Radic Biol Med, 26(3-4), 355-61 (1999)
56. Bannister, J. V., Bellavite, P., Davoli, A., Thornalley, P. J. Rossi, F. The generation of hydroxyl radicals following superoxide production by neutrophil NADPH oxidase. FEBS Lett, 150(2), 300-2 (1982)
57. Rathore, R., Zheng, Y. M., Niu, C. F., Liu, Q. H., Korde, A., Ho, Y. S. Wang, Y. X. Hypoxiaactivates NADPH oxidase to increase [ROS]i and [Ca2+]i through the mitochondrial ROS-PKCepsilon signaling axis in pulmonary artery smooth muscle cells. Free Radic Biol Med, 45(9), 1223-31 (2008)
58. Xu, H., Goettsch, C., Xia, N., Horke, S., Morawietz, H., Forstermann, U. Li, H. Differential roles of PKCalpha and PKCepsilon in controlling the gene expression of Nox4 in human endothelial cells. Free Radic Biol Med, 44(8), 1656-67 (2008)
59. Maier, C. M., Hsieh, L., Crandall, T., Narasimhan, P. Chan, P. H. A new approach for the investigation of reperfusion-related brain injury. Biochem Soc Trans, 34(Pt 6), 1366-9 (2006)
60. Morita-Fujimura, Y., Fujimura, M., Gasche, Y., Copin, J. C. Chan, P. H. Overexpression of copper and zinc superoxide dismutase in transgenic mice prevents the induction and activation of matrix metalloproteinases after cold injury-induced brain trauma. J Cereb Blood Flow Metab, 20(1), 130-8 (2000)
61. Shinohara, M., Adachi, Y., Mitsushita, J., Kuwabara, M., Nagasawa, A., Harada, S., Furuta, S., Zhang, Y., Seheli, K., Miyazaki, H. Kamata, T. Reactive oxygen generated by NADPH oxidase 1 (Nox1) contributes to cell invasion by regulating matrix metalloprotease-9 production and cell migration. J Biol Chem, 285(7), 4481-8 (2010)
62. Liu, W., Sood, R., Chen, Q., Sakoglu, U., Hendren, J., Cetin, O., Miyake, M. Liu, K. J. Normobaric hyperoxia inhibits NADPH oxidase-mediated matrix metalloproteinase-9 induction in cerebral microvessels in experimental stroke. J Neurochem, 107(5), 1196-205 (2008)
63. Liu, W., Rosenberg, G. A., Shi, H., Furuichi, T., Timmins, G. S., Cunningham, L. A. Liu, K. J. Xanthine oxidase activates pro-matrix metalloproteinase-2 in cultured rat vascular smooth muscle cells through non-free radical mechanisms. Arch Biochem Biophys, 426(1), 11-7 (2004)
64. Schreibelt, G., Kooij, G., Reijerkerk, A., van Doorn, R., Gringhuis, S. I., van der Pol, S., Weksler, B. B., Romero, I. A., Couraud, P. O., Piontek, J., Blasig, I. E., Dijkstra, C. D., Ronken, E. de Vries, H. E. Reactive oxygen species alter brain endothelial tight junction dynamics via RhoA, PI3 kinase, and PKB signaling. FASEB J, 21(13), 3666-76 (2007)
65. Lee, H. S., Namkoong, K., Kim, D. H., Kim, K. J., Cheong, Y. H., Kim, S. S., Lee, W. B. Kim, K. Y. Hydrogen peroxide-induced alterations of tight junction proteins in bovine brain microvascular endothelial cells. Microvasc Res, 68(3), 231-8 (2004)
66. Rao, R. K., Basuroy, S., Rao, V. U., Karnaky Jr, K. J. Gupta, A. Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J, 368(Pt 2), 471-81 (2002)
67. Fischer, S., Wiesnet, M., Renz, D. Schaper, W. H2O2 induces paracellular permeability of porcine brain-derived microvascular endothelial cells by activation of the p44/42 MAP kinase pathway. Eur J Cell Biol, 84(7), 687-97 (2005)
68. Sheth, P., Samak, G., Shull, J. A., Seth, A. Rao, R. Protein phosphatase 2A plays a role in hydrogen peroxideinduced disruption of tight junctions in Caco-2 cell monolayers. Biochem J, 421(1), 59-70 (2009)
69. Faropoulos, K., Chroni, E., Assimakopoulos, S. F., Mavrakis, A. , Stamatopoulou, V., Toumpeki, C., Drainas, D., Grintzalis, K., Papapostolou, I., Georgiou, C. D. Konstantinou, D. Altered occludin expression in brain capillaries induced by obstructive jaundice in rats. Brain Res, 1325, 121-7 (2010)
70. Michel, T. Feron, O. Nitric oxide synthases: which, where, how, and why? J Clin Invest, 100(9), 2146-52 (1997)
71. Kuo, P. C. Schroeder, R. A. The emerging multifaceted roles of nitric oxide. Ann Surg, 221(3), 220-35 (1995)
72. Zhang, Z. G., Zhang, L., Jiang, Q., Zhang, R., Davies, K., Powers, C., Bruggen, N. Chopp, M. VEGF enhances angiogenesis and promotes blood-brain barrier leakage in the ischemic brain. J Clin Invest, 106(7), 829-38 (2000)
73. Bogdan, C., Rollinghoff, M. Diefenbach, A. Reactive oxygen and reactive nitrogen intermediates in innate and specific immunity. Curr Opin Immunol, 12(1), 64-76 (2000)
74. Fischer, A., Folkerts, G., Geppetti, P. Groneberg, D. A. Mediators of asthma: nitric oxide. Pulm Pharmacol Ther, 15(2), 73-81 (2002)
75. Lundberg, J. O., Weitzberg, E. Gladwin, M. T. The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov, 7(2), 156-67 (2008)
76. Kiss, J. P. Vizi, E. S. Nitric oxide: a novel link between synaptic and nonsynaptic transmission. Trends Neurosci, 24(4), 211-5 (2001)
77. Forstermann, U. Nitric oxide and oxidative stress in vascular disease. Pflugers Arch, 459(6), 923-39 (2010)
78. Conti, A., Miscusi, M., Cardali, S., Germano, A., Suzuki, H., Cuzzocrea, S. Tomasello, F. Nitric oxide in the injured spinal cord: synthases cross-talk, oxidative stress and inflammation. Brain Res Rev, 54(1), 205-18 (2007)
79. Moncada, S., Palmer, R. M. Higgs, E. A. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev, 43(2), 109-42 (1991)
80. Dalkara, T., Endres, M. Moskowitz, M. A. Mechanisms of NO neurotoxicity. Prog Brain Res, 118, 231-9 (1998)
81. Murphy, S. Gibson, C. L. Nitric oxide, ischaemia and brain inflammation. Biochem Soc Trans, 35(Pt 5), 1133-7 (2007)
82. Malinski, T., Bailey, F., Zhang, Z. G. Chopp, M. Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab, 13(3 ), 355-8 (1993)
83. Matsui, T., Nagafuji, T., Kumanishi, T. Asano, T. Role of nitric oxide in pathogenesis underlying ischemic cerebral damage. Cell Mol Neurobiol, 19(1), 177-89 (1999)
84. Squadrito, G. L. Pryor, W. A. Oxidative chemistry of nitric oxide: the roles of superoxide, peroxynitrite, and carbon dioxide. Free Radic Biol Med, 25(4-5), 392-403 (1998)
85. Beckman, J. S., Ischiropoulos, H., Zhu, L., van der Woerd, M., Smith, C., Chen, J., Harrison, J., Martin, J. C. Tsai, M. Kinetics of superoxide dismutase- and ironcatalyzed nitration of phenolics by peroxynitrite. Arch Biochem Biophys, 298(2), 438-45 (1992)
86. Li, C. Jackson, R. M. Reactive species mechanisms of cellular hypoxia-reoxygenation injury. Am J Physiol Cell Physiol, 282(2), C227-41 (2002)
87. Huang, Z., Huang, P. L., Ma, J., Meng, W., Ayata, C., Fishman, M. C. Moskowitz, M. A. Enlarged infarcts in endothelial nitric oxide synthase knockout mice are attenuated by nitro-L-arginine. J Cereb Blood Flow Metab, 16(5), 981-7 (1996)
88. Huang, Z., Huang, P. L., Panahian, N., Dalkara, T., Fishman, M. C. Moskowitz, M. A. Effects of cerebral ischemia in mice deficient in neuronal nitric oxidesynthase. Science, 265(5180), 1883-5 (1994)
89. Hara, H., Huang, P. L., Panahian, N., Fishman, M. C. Moskowitz, M. A. Reduced brain edema and infarction volume in mice lacking the neuronal isoform of nitric oxide synthase after transient MCA occlusion. J Cereb Blood Flow Metab, 16(4), 605-11 (1996)
90. Sharma, H. S., Wiklund, L., Badgaiyan, R. D., Mohanty, S. Alm, P. Intracerebral administration of neuronal nitric oxide synthase antiserum attenuates traumatic brain injury-induced blood-brain barrier permeability, brain edema formation, and sensory motor disturbances in the rat. Acta Neurochir Suppl, 96, 288-94 (2006)
91. Park, E. M., Cho, S., Frys, K. A., Glickstein, S. B., Zhou, P., Anrather, J., Ross, M. E. Iadecola, C. Inducible nitric oxide synthase contributes to gender differences in ischemic brain injury. J Cereb Blood Flow Metab, 26(3), 392-401 (2006)
92. Chen, H. H. Wang, D. L. Nitric oxide inhibits matrix metalloproteinase-2 expression via the induction of activating transcription factor 3 in endothelial cells. Mol Pharmacol, 65(5), 1130-40 (2004)
93. Upchurch, G. R., Jr., Ford, J. W., Weiss, S. J., Knipp, B. S., Peterson, D. A., Thompson, R. W., Eagleton, M. J., Broady, A. J., Proctor, M. C. Stanley, J. C. Nitric oxide inhibition increases matrix metalloproteinase-9 expression by rat aortic smooth muscle cells in vitro. J Vasc Surg, 34(1), 76-83 (2001)
94. Jurasz, P., Sawicki, G., Duszyk, M., Sawicka, J., Miranda, C., Mayers, I. Radomski, M. W. Matrix metalloproteinase 2 in tumor cell-induced platelet aggregation: regulation by nitric oxide. Cancer Res, 61(1), 376-82 (2001)
95. Phillips, P. G. Birnby, L. M. Nitric oxide modulates caveolin-1 and matrix metalloproteinase-9 expression and distribution at the endothelial cell/tumor cell interface. Am J Physiol Lung Cell Mol Physiol, 286(5), L1055-65 (2004)
96. Eberhardt, W., Akool el, S., Rebhan, J., Frank, S., Beck, K. F., Franzen, R., Hamada, F. M. Pfeilschifter, J. Inhibition of cytokine-induced matrix metalloproteinase 9 expression by peroxisome proliferator-activated receptor alpha agonists is indirect and due to a NO-mediated reduction of mRNA stability. J Biol Chem, 277(36), 33518-28 (2002)
97. Gu, Z., Kaul, M., Yan, B., Kridel, S. J., Cui, J., Strongin, A., Smith, J. W., Liddington, R. C. Lipton, S . A. Snitrosylation of matrix metalloproteinases: signaling pathway to neuronal cell death. Science, 297(5584), 1186-90 (2002)
98. Szabo, C., Ischiropoulos, H. Radi, R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov, 6(8), 662-80 (2007)
99. Marla, S. S., Lee, J. Groves, J. T. Peroxynitrite rapidly permeates phospholipid membranes. Proc Natl Acad Sci U S A, 94(26), 14243-8 (1997)
100. Gobbel, G. T., Chan, T. Y. Chan, P. H. Nitric oxide- and superoxide-mediated toxicity in cerebral endothelial cells. J Pharmacol Exp Ther, 282(3), 1600-7 (1997)
101. Radi, R. Nitric oxide, oxidants, and protein tyrosine nitration. Proc Natl Acad Sci U S A, 101(12), 4003-8 (2004)
102. Moreno, J. J. Pryor, W. A. Inactivation of alpha 1- proteinase inhibitor by peroxynitrite. Chem Res Toxicol, 5(3), 425-31 (1992)
103. Endres, M., Wang, Z. Q., Namura, S., Waeber, C. Moskowitz, M. A. Ischemic brain injuryis mediated by the activation of poly(ADP-ribose)polymerase. J Cereb Blood Flow Metab, 17(11), 1143-51 (1997)
104. Eliasson, M. J., Huang, Z., Ferrante, R. J., Sasamata, M., Molliver, M. E., Snyder, S. H. Moskowitz, M. A. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci, 19(14), 5910-8 (1999)
105. Xu, J., H e, L., Ahmed, S. H., Chen, S. W., Goldberg, M. P., Beckman, J. S. Hsu, C. Y. Oxygen-glucose deprivation induces inducible nitric oxide synthase and nitrotyrosine expression in cerebral endothelial cells. Stroke, 31(7), 1744-51 (2000)
106. Kidd, G. A., Hong, H., Majid, A., Kaufman, D. I. Chen, A. F. Inhibition of brain GTP cyclohydrolase I and tetrahydrobiopterin attenuates cerebral infarction via reducing inducible NO synthaseand peroxynitrite in ischemic stroke. Stroke, 36(12), 2705-11 (2005)
107. Suzuki, M., Tabuchi, M., Ikeda, M. Tomita, T. Concurrent formation of peroxynitrite with the expression of inducible nitric oxide synthase in the brain during middle cerebral artery occlusion and reperfusion in rats. Brain Res, 951(1), 113-20 (2 002)
108. Thiyagarajan, M., Kaul, C. L. Sharma, S. S. Neuroprotective efficacy and therapeutic time window of peroxynitrite decomposition catalysts in focal cerebral ischemia in rats. Br J Pharmacol, 142(5), 899-911 (2004)
109. Sharma, S. S., Munusamy, S., Thiyagarajan, M. Kaul, C. L. Neuroprotective effect of peroxynitrite decomposition catalyst and poly(adenosine diphosphate-ribose) polymerase inhibitor alone and in combination in rats with focal cerebral ischemia. J Neurosurg, 101(4), 669-75 (2004)
110. Tan, K. H., Harrington, S., Purcell, W. M. Hurst, R. D. Peroxynitrite mediates nitric oxide-induced blood-brain barrier damage. Neurochem Res, 29(3), 579-87 (2004)
111. Migita, K., Maeda, Y., Abiru, S., Komori, A., Yokoyama, T., Takii, Y., Nakamura, M., Yatsuhashi, H., Eguchi, K. Ishibashi, H. Peroxynitrite-mediated matrix metalloproteinase-2 activation in human hepatic stellate cells. FEBS Lett, 579(14), 3119-25 (2005)
112. Frears, E. R., Zhang, Z., Blake, D. R., O'Connell, J. P. Winyard, P. G. Inactivation of tissue inhibitor of metalloproteinase-1 by peroxynitrite. FEBS Lett, 381(1-2), 21-4 (1996)
113. Okamoto, T., Akaike, T., Nagano, T., Miyajima, S., Suga, M., Ando, M., Ichimori, K. Maeda, H. Activation of human neutrophil procollagenase by nitrogen dioxide and peroxynitrite: a novel mechanism for procollagenase activation involving nitric oxide. Arch Biochem Biophys, 342(2), 261-74 (1997)
114. Okamoto, T., Akaike, T., Sawa, T., Miyamoto, Y., van der Vliet, A. Maeda, H. Activation of matrix metalloproteinases by peroxynitrite-induced protein Sglutathiolation via disulfide S-oxide formation. J Biol C hem, 276(31), 29596-602 (2001)
115. Viappiani, S., Nicolescu, A. C., Holt, A., Sawicki, G., Crawford, B. D., Leon, H., van Mulligen, T. Schulz, R. Activation and modulation of 72k Da matrix metalloproteinase-2 by peroxynitrite and glutathione. Biochem Pharmacol, 77(5), 826-34 (2009)
116. Rajagopalan, S., Meng, X. P., Ramasamy, S., Harrison, D. G. Galis, Z. S. Reactiveoxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest, 98(11), 2572-9 (1996)
117. Donnini, S., Monti, M., Roncone, R., Morbidelli, L., Rocchigiani, M., Oliviero, S., Casella, L., Giachetti, A., Schulz, R. Ziche, M. Peroxynitrite inactivates human-tissue inhibitor of metalloproteinase-4. FEBS Lett, 582(7), 1135-40 (2008)
118. Wang, W., Sawicki, G. Schulz, R. Peroxynitrite-induced myocardial injury is mediated through matrix metalloproteinase-2. Cardiovasc Res, 53(1), 165-74 (2002)
119. Suofu, Y., Clark, J., Broderick, J., Wagner, K. R., Tomsick, T., Sa, Y. Lu, A. Peroxynitrite decomposition catalyst prevents matrix metalloproteinase activation and neurovascular injury after prolonged cerebral ischemia in rats. J Neurochem (2010)
120. Mazzon, E., De Sarro, A., Caputi, A. P. Cuzzocrea, S. Role of tight junction derangement in the endothelial dysfunction elicited by exogenous and endogenous peroxynitrite and poly(ADP-ribose) synthetase. Shock, 18(5), 434-9 (2002)
121. Bucolo, C., Ward, K. W., Mazzon, E., Cuzzocrea, S. Drago, F. Protective effects of a coumarin derivative in diabetic rats. Invest Ophthalmol Vis Sci, 50(8), 3846-52 (2009)
122. VanGilder, R. L., Kelly, K. A., Chua, M. D., Ptachcinski, R. L. Huber, J. D. Administration of sesamol improved blood-brain barrier function in streptozotocin-induced diabetic rats. Exp Brain Res, 197(1), 23-34 (20 09)
123. Anderson, R. G. The caveolae membrane system. Annu Rev Biochem, 67, 199-225 (1998)
124. Pelkmans, L. Secrets of caveolae- and lipid raftmediated endocytosis revealed by mammalian viruses. Biochim Biophys Acta, 1746(3), 295-304 (2005)
125. Li, X. A., Everson, W. V. Smart, E. J. Caveolae, lipid rafts, and vascular disease. Trends Cardiovasc Med, 15(3), 92-6 (2005)
126. Rothberg, K. G., Heuser, J. E., Donzell, W. C., Ying, Y. S., Glenney, J. R. Anderson, R. G. Caveolin, a protein component of caveolae membrane coats. Cell, 68(4), 673-82 (1992)
127. Thyberg, J. Caveolin-1 and caveolae act as regulators of mitogenic signaling in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol, 23(9), 1481-3 (2003)
128. Peterson, T. E., Guicciardi, M. E., Gulati, R., Kleppe, L. S., Mueske, C. S., Mookadam, M., Sowa, G., Gores, G. J., Sessa, W. C. Simari, R. D. Caveolin-1 can regulate vascular smooth muscle cell fate by switching plateletderived growth factor signaling from a proliferative to an apoptotic pathway. Arterioscler Thromb Vasc Biol, 23(9), 1521-7 (2003)
129. Gargalovic, P. Dory, L. Cellular apoptosis is associated with increased caveolin-1 expression in macrophages. J Lipid Res, 44(9), 1622-32 (2003)
130. Fielding, C. J. Fielding, P. E. Caveolae and intracellular trafficking of cholesterol. Adv Drug Deliv Rev, 49(3), 251-64 (2001)
131. Burgermeister, E., Liscovitch, M., Rocken, C., Schmid, R. M. Ebert, M. P. Caveats of caveolin-1 in cancer progression. Cancer Lett, 268(2), 187-201 (2008)
132. Goetz, J. G., Lajoie, P., Wiseman, S. M. Nabi, I. R. Caveolin-1 in tumor progression: the good, the bad and the ugly. Cancer Metastasis Rev, 27(4), 715-35 (2008)
133. Frank, P. G., Hassan, G. S., Rodriguez-Feo, J. A. Lisanti, M. P. Caveolae and caveolin-1: novel potential targets for the treatment of cardiovascular disease. Curr Pharm Des, 13(17), 1761-9 (2007)
134. Sonveaux, P., Martinive, P., DeWever, J., Batova, Z., Daneau, G., Pelat, M., Ghisdal, P., Gregoire, V., Dessy, C., Balligand, J. L. Feron, O. Caveolin-1 expression is critical for vascular endothelial growth factor-induced ischemic hindlimb collateralization and nitric oxide-mediated angiogenesis. Circ Res, 95(2), 154-61 (2004)
135. Schubert, W., Frank, P. G., Woodman, S. E., Hyogo, H., Cohen, D. E., Chow, C. W. Lisanti, M. P. 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), 40091-8 (2002)
136. Sun, Y., Hu, G., Zhang, X. Minshall, R. D. Phosphorylation of caveolin-1 regulates oxidant-induced pulmonary vascular permeability via paracellular and transcellular pathways. Circ Res, 105(7), 676-85, 15 p following 685 (2009)
137. Miyawaki-Shimizu, K., Predescu, D., Shimizu, J., Broman, M., Predescu, S. Malik, A. B. siRNA-induced caveolin-1 knockdown in mice increases lung vascular permeability via the junctional pathway. Am J Physiol Lung Cell Mol Physiol, 290(2), L405-13 (2006)
138. Hatakeyama, T., Pappas, P. J., Hobson, R. W., 2nd, Boric, M. P., Sessa, W. C. Duran, W. N. Endothelial nitric oxide synthase regulates microvascular hyperpermeability in vivo. J Physiol, 574(Pt 1), 275-81 (2006)
139. Puyraimond, A., Fridman, R., Lemesle, M., Arbeille, B. Menashi, S. MMP-2 colocalizes with caveolae on the surface of endothelial cells. Exp Cell Res, 262(1), 28-36 (2001)
140. Han, F. Zhu, H. G. Caveolin-1 regulating the invasion and expression of matrix metalloproteinase (MMPs) in pancreatic carcinoma cells. J Surg Res, 159(1), 443-50 (2010)
141. Williams, T. M., Medina, F., Badano, I., Hazan, R. B., Hutchinson, J., Muller, W. J., Chopra, N. G., Scherer, P. E., Pestell, R. G. Lisanti, M. P. 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(49), 51630-46 (2004)
142. Kim, H. N. Chung, H. S. Caveolin-1 inhibits membrane-type 1 matrix metalloproteinase activity. BMB Rep, 41(12), 858-62 (2008)
143. Du, Z. M., Hu, C. F., Shao, Q., Huang, M. Y., Kou, C. W., Zhu, X. F., Zeng, Y. X. Shao, J. Y. Upregulation of caveolin-1 and CD147 expression in nasopharyngeal carcinoma enhanced tumor cell migration and correlated with poor prognosis of the patients. Int J Cancer, 125(8), 1832-41 (2009)
144. Yeh, D., Chen, C., Sun, M. Z., Shao, S., Hao, L., Song, Y., Gong, L., Hu, J. Wang, Q. Caveolin-1 is an important factor for the metastasis and proliferation of human small cell lung cancer NCI-H446 cell. Anat Rec (Hoboken), 292(10), 1584-92 (2009)
145. Lynch, R. D., Francis, S. A., McCarthy, K. M., Casas, E., Thiele, C. Schneeberger, E. E. Cholesterol depletion alters detergent-specific solubility profiles of selected tight junction proteins and the phosphorylation of occludin. Exp Cell Res, 313(12), 2597-610 (2007)
146. Schwarz, B. T., Wang, F., Shen, L., Clayburgh, D. R., Su, L., Wang, Y., Fu, Y. X. Turner, J. R. LIGHT signals directly to intestinal epithelia to cause barrier dysfunction via cytoskeletal and endocytic mechanisms. Gastroenterology, 132(7), 2383-94 (2007)
147. Song, L., Ge, S. Pachter, J. S. Caveolin-1 regulates expression of junction-associated proteins in brain microvascular endothelial cells. Blood, 109(4), 1515-23 (2007)
148. Nag, S., Venugopalan, R. Stewart, D. J. Increased caveolin-1 expression precedes decreased expression of occludin and claudin-5 during blood-brain barrier breakdown. Acta Neuropathol, 114(5), 459-69 (2007)
149. Zhong, Y., Smart, E. J., Weksler, B., Couraud, P. O., Hennig, B. Toborek, M. Caveolin-1 regulates human immunodeficiency virus-1 Tat-induced alterations of tight junction protein expression via modulation of the Ras signaling. J Neurosci, 28(31), 7788-96 (2008)
150. Stamatovic, S. M., Keep, R. F., Wang, M. M., Jankovic, I. Andjelkovic, A. V. Caveolae-mediated internalization of occludin and claudin-5 during CCL2- induced tight junction remodeling in brain endothelial cells. J Biol Chem, 284(28), 19053-66 (2009)
151. Feron, O., Belhassen, L., Kobzik, L., Smith, T. W., Kelly, R. A. Michel, T. Endothelial nitric oxide synthase targeting to caveolae. Specific interactions with caveolin isoforms in cardiac myocytes and endothelial cells. J Biol Chem, 271(37), 22810-4 (1996)
152. Garcia-Cardena, G., Fan, R., Stern, D. F., Liu, J. Sessa, W. C. Endothelial nitric oxide synthase is regulated by tyrosine phosphorylation and interacts with caveolin-1. J Biol Chem, 271(44), 27237-40 (1996)
153. Michel, J. B., Feron, O., Sacks, D. Michel, T. Reciprocal regulation of endothelial nitric-oxide synthase by Ca2+-calmodulin and caveolin. J Biol Chem, 272(25), 15583-6 (1997)
154. Michel, J. B., Feron, O., Sase, K., Prabhakar, P. Michel, T. Caveolin versus calmodulin. Counterbalancing allosteric modulators of endothelial nitric oxide synthase. J Biol Chem, 272(41), 25907-12 (1997)
155. Ju, H., Zou, R., Venema, V. J. Venema, R. C. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem, 272(30), 18522-5 (1997)
156. Felley-Bosco, E., Bender, F. C., Courjault-Gautier, F., Bron, C. Quest, A. F. Caveolin-1 down-regulates inducible nitric oxide synthase via the proteasome pathway in human colon carcinoma cells. Proc Natl Acad Sci U S A, 97( 26), 14334-9 (2000)
157. Bucci, M., Gratton, J. P., Rudic, R. D., Acevedo, L., Roviezzo, F., Cirino, G. Sessa, W. C. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med, 6(12), 1362-7 (2000)
158. Sato, Y., Sagami, I. Shimizu, T. Identification of caveolin-1-interacting sites in neuronal nitric-oxide synthase. Molecular mechanism for inhibition of NO formation. J Biol Chem, 279(10), 8827-36 (2004)
159. Shah, V., Toruner, M., Haddad, F., Cadelina, G., Papapetropoulos, A., Choo, K., Sessa, W. C. Groszmann, R. J. Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology, 117(5), 1222-8 (1999)
160. Hare, J. M., Lofthouse, R. A., Juang, G. J., Colman, L., Ricker, K. M., Kim, B., Senzaki, H., Cao, S., Tunin, R. S. Kass, D. A. Contribution of caveolin protein abundance to augmented nitric oxide signaling in conscious dogs with pacing-induced heart failure. Circ Res, 86(10), 1085-92 (2000)
161. Feron, O., Saldana, F., Michel, J. B. Michel, T. The endothelial nitric-oxide synthase-caveolin regulatory cycle. J Biol Chem, 273(6), 3125-8 (1998)
162. Fernandez-Hernando, C., Yu, J., Suarez, Y., Rahner, C., Davalos, A., Lasuncion, M. A. Sessa, W. C. Genetic evidence supporting a critical role of endothelial caveolin-1 during the progression of atherosclerosis. Cell Metab, 10(1), 48-54 (2009)
163. Navarro-Lerida, I., Portoles, M. T., Barrientos, A. A., Gavilanes, F., Bosca, L. Rodriguez-Crespo, I. Induction of nitric oxide synthase-2 proceeds with the concomitant downregulation of the endogenous caveolin levels. J Cell Sci, 117(Pt 9), 1687-97 (2004)
164. Shen, J., Lee, W., Li, Y., Lau, C. F., Ng, K. M., Fung, M. L. Liu, K. J. Interaction of caveolin-1, nitric oxide, and nitric oxide synthases in hypoxic human SKN- MC neuroblastoma cells. J Neurochem, 107(2), 478-87 (2008)
165. Chanvorachote, P., Nimmannit, U., Lu, Y., Talbott, S., Jiang, B. H. Rojanasakul, Y. Nitric oxide regulates lung carcinoma cell anoikis through inhibition of ubiquitinproteasomal degradation of caveolin-1. J Biol Chem, 284(41), 28476-84 (2009)