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Current Vascular Pharmacology

Editor-in-Chief

ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

Review Article

Caveolin-1 in Stroke Neuropathology and Neuroprotection: A Novel Molecular Therapeutic Target for Ischemic-Related Injury

Author(s): Shanshan Wang and Brian P. Head*

Volume 17, Issue 1, 2019

Page: [41 - 49] Pages: 9

DOI: 10.2174/1570161116666180206112215

Price: $65

Abstract

Cardiovascular disease and associated cerebral stroke are a global epidemic attributed to genetic and epigenetic factors, such as diet, life style and an increasingly sedentary existence due to technological advances in both the developing and developed world. There are approximately 5.9 million stroke-related deaths worldwide annually. Current epidemiological data indicate that nearly 16.9 million people worldwide suffer a new or recurrent stroke yearly. In 2014 alone, 2.4% of adults in the United States (US) were estimated to experience stroke, which is the leading cause of adult disability and the fifth leading cause of death in the US There are 2 main types of stroke: Hemorrhagic (HS) and ischemic stroke (IS), with IS occurring more frequently. HS is caused by intra-cerebral hemorrhage mainly due to high blood pressure, while IS is caused by either embolic or thrombotic stroke. Both result in motor impairments, numbness or abnormal sensations, cognitive deficits, and mood disorders (e.g. depression). This review focuses on the 1) pathophysiology of stroke (neuronal cell loss, defective blood brain barrier, microglia activation, and inflammation), 2) the role of the membrane protein caveolin- 1 (Cav-1) in normal brain physiology and stroke-induced changes, and, 3) we briefly discussed the potential therapeutic role of Cav-1 in recovery following stroke.

Keywords: Hemorrhagic and ischemic stroke, blood brain barrier, inflammation, microglia, endothelial cell, gene therapy.

Graphical Abstract

[1]
Garcia JH. The neuropathology of stroke. Hum Pathol 1975; 6: 583-98.
[2]
Chiras J, Bories J, Barth MO, Aymard A, Poirier B. Cerebral angiography in ischemic strokes. Neuroradiology 1985; 27: 521-38.
[3]
Yu AY, Coutts SB. Stroke: Risk assessment to prevent recurrence after mild stroke or TIA. Nat Rev Neurol 2015; 11: 131-3.
[4]
George PM, Steinberg GK. Novel stroke therapeutics: Unraveling stroke pathophysiology and its impact on clinical treatments. Neuron 2015; 87: 297-309.
[5]
McKevitt C, Fudge N, Redfern J, et al. Self-reported long-term needs after stroke. Stroke 2011; 42: 1398-403.
[6]
Chen S, Zeng L, Hu Z. Progressing haemorrhagic stroke: Categories, causes, mechanisms and managements. J Neurol 2014; 261: 2061-78.
[7]
Mayer SA, Sacco RL, Shi T, Mohr JP. Neurologic deterioration in noncomatose patients with supratentorial intracerebral hemorrhage. Neurology 1994; 44: 1379-84.
[8]
Sudlow CL, Warlow CP. Comparable studies of the incidence of stroke and its pathological types: Results from an international collaboration. International stroke incidence collaboration. Stroke 1997; 28: 491-9.
[9]
Qureshi AI, Mendelow AD, Hanley DF. Intracerebral haemorrhage. Lancet 2009; 373: 1632-44.
[10]
Xi G, Wagner KR, Keep RF, et al. Role of blood clot formation on early edema development after experimental intracerebral hemorrhage. Stroke 1998; 29: 2580-6.
[11]
Xi G, Reiser G, Keep RF. The role of thrombin and thrombin receptors in ischemic, hemorrhagic and traumatic brain injury: Deleterious or protective? J Neurochem 2003; 84: 3-9.
[12]
Martini WZ, Cortez DS, Dubick MA, Blackbourne LH. Different recovery profiles of coagulation factors, thrombin generation, and coagulation function after hemorrhagic shock in pigs. J Trauma Acute Care Surg 2012; 73: 640-7.
[13]
Ohnishi M, Katsuki H, Fujimoto S, Takagi M, Kume T, Akaike A. Involvement of thrombin and mitogen-activated protein kinase pathways in hemorrhagic brain injury. Exp Neurol 2007; 206: 43-52.
[14]
Xue M, Balasubramaniam J, Parsons KA, McIntyre IW, Peeling J, Del Bigio MR. Does thrombin play a role in the pathogenesis of brain damage after periventricular hemorrhage? Brain Pathol 2005; 15: 241-9.
[15]
Hua Y, Xi G, Keep RF, Hoff JT. Complement activation in the brain after experimental intracerebral hemorrhage. J Neurosurg 2000; 92: 1016-22.
[16]
Yang S, Nakamura T, Hua Y, et al. Intracerebral hemorrhage in complement C3-deficient mice. Acta Neurochir Suppl 2006; 96: 227-31.
[17]
Lim JS, Shin M, Kim HJ, Kim KS, Choy HE, Cho KA. Caveolin-1 mediates Salmonella invasion via the regulation of SopE-dependent Rac1 activation and actin reorganization. J Infect Dis 2014; 210: 793-802.
[18]
Chen D, Song MQ, Liu YJ, et al. Inhibition of complement C3 might rescue vascular hyporeactivity in a conscious hemorrhagic shock rat model. Microvasc Res 2016; 105: 23-9.
[19]
Xi G, Hua Y, Keep RF, Younger JG, Hoff JT. Brain edema after intracerebral hemorrhage: the effects of systemic complement depletion. Acta Neurochir Suppl 2002; 81: 253-6.
[20]
Haley MJ, Lawrence CB. The blood-brain barrier after stroke: Structural studies and the role of transcytotic vesicles. J Cereb Blood Flow Metab 2017; 37: 456-70.
[21]
Ronaldson PT, Davis TP. Blood-brain barrier integrity and glial support: Mechanisms that can be targeted for novel therapeutic approaches in stroke. Curr Pharm Des 2012; 18: 3624-44.
[22]
Willis CL, Leach L, Clarke GJ, Nolan CC, Ray DE. Reversible disruption of tight junction complexes in the rat blood-brain barrier, following transitory focal astrocyte loss. Glia 2004; 48: 1-13.
[23]
Willis CL, Camire RB, Brule SA, Ray DE. Partial recovery of the damaged rat blood-brain barrier is mediated by adherens junction complexes, extracellular matrix remodeling and macrophage infiltration following focal astrocyte loss. Neuroscience 2013; 250: 773-85.
[24]
Wagner KR, Xi G, Hua Y, et al. Lobar intracerebral hemorrhage model in pigs: Rapid edema development in perihematomal white matter. Stroke 1996; 27: 490-7.
[25]
Yang GY, Betz AL, Chenevert TL, Brunberg JA, Hoff JT. Experimental intracerebral hemorrhage: Relationship between brain edema, blood flow and blood-brain barrier permeability in rats. J Neurosurg 1994; 81: 93-102.
[26]
Takagi T, Imai T, Mishiro K, et al. Cilostazol ameliorates collagenase-induced cerebral hemorrhage by protecting the blood-brain barrier. J Cereb Blood Flow Metab 2017; 37: 123-39.
[27]
Manaenko A, Yang P, Nowrangi D, et al. Inhibition of stress fiber formation preserves blood-brain barrier after intracerebral hemorrhage in mice. J Cereb Blood Flow Metab 2018; 38(1): 87-102.
[28]
Kahles T, Luedike P, Endres M, et al. NADPH oxidase plays a central role in blood-brain barrier damage in experimental stroke. Stroke 2007; 38: 3000-6.
[29]
Chen S, Yang Q, Chen G, Zhang JH. An update on inflammation in the acute phase of intracerebral hemorrhage. Transl Stroke Res 2015; 6: 4-8.
[30]
Gelderblom M, Leypoldt F, Steinbach K, et al. Temporal and spatial dynamics of cerebral immune cell accumulation in stroke. Stroke 2009; 40: 1849-57.
[31]
Colton CA, Gilbert DL. Production of superoxide anions by a CNS macrophage, the microglia. FEBS Lett 1987; 223: 284-8.
[32]
Chen CJ, Raung SL, Liao SL, Chen SY. Inhibition of inducible nitric oxide synthase expression by baicalein in endotoxin/cytokine-stimulated microglia. Biochem Pharmacol 2004; 67: 957-65.
[33]
Kaur C, Sivakumar V, Zou Z, Ling EA. Microglia-derived proinflammatory cytokines tumor necrosis factor-alpha and interleukin-1beta induce Purkinje neuronal apoptosis via their receptors in hypoxic neonatal rat brain. Brain Struct Funct 2014; 219: 151-70.
[34]
Loftspring MC, McDole J, Lu A, Clark JF, Johnson AJ. Intracerebral hemorrhage leads to infiltration of several leukocyte populations with concomitant pathophysiological changes. J Cereb Blood Flow Metab 2009; 29: 137-43.
[35]
Pradilla G, Chaichana KL, Hoang S, Huang J, Tamargo RJ. Inflammation and cerebral vasospasm after subarachnoid hemorrhage. Neurosurg Clin N Am 2010; 21: 365-79.
[36]
Chaichana KL, Pradilla G, Huang J, Tamargo RJ. Role of inflammation (leukocyte-endothelial cell interactions) in vasospasm after subarachnoid hemorrhage. World Neurosurg 2010; 73: 22-41.
[37]
Durukan A, Tatlisumak T. Acute ischemic stroke: Overview of major experimental rodent models, pathophysiology, and therapy of focal cerebral ischemia. Pharmacol Biochem Behav 2007; 87: 179-97.
[38]
Kaithoju S. Ischemic stroke: Risk stratification, warfarin teatment and outcome measure. J Atr Fibrillation 2015; 8: 1144.
[39]
Chapuisat G, Dronne MA, Grenier E, Hommel M, Boissel JP. In silico study of the influence of intensity and duration of blood flow reduction on cell death through necrosis or apoptosis during acute ischemic stroke. Acta Biotheor 2010; 58: 171-90.
[40]
Memezawa H, Smith ML, Siesjo BK. Penumbral tissues salvaged by reperfusion following middle cerebral artery occlusion in rats. Stroke 1992; 23: 552-9.
[41]
Sims NR. Calcium, energy metabolism and the development of selective neuronal loss following short-term cerebral ischemia. Metab Brain Dis 1995; 10: 191-217.
[42]
Pilarczyk M, Krasinska-Czerlunczakiewicz H, Tynecka-Turowska M, Stelmasiak Z. General cerebral and systemic metabolic disturbances occurring in ischemic stroke with special emphasis on glucose and its metabolites. Neurol Neurochir Pol 1999; 32(Suppl. 6): 105-7.
[43]
Pilarczyk M, Krasinska-Czerlunczakiewicz H, Stelmasiak Z. Evaluation of lactic acid levels in blood of patients with ischemic stroke in the earliest stage of the disease. Neurol Neurochir Pol 1999; 32(Suppl. 6): 109-11.
[44]
Lampl Y, Paniri Y, Eshel Y, Sarova-Pinhas I. Cerebrospinal fluid lactate dehydrogenase levels in early stroke and transient ischemic attacks. Stroke 1990; 21: 854-7.
[45]
Brouns R, Sheorajpanday R, Wauters A, De Surgeloose D, Marien P, De Deyn PP. Evaluation of lactate as a marker of metabolic stress and cause of secondary damage in acute ischemic stroke or TIA. Clin Chim Acta 2008; 397: 27-31.
[46]
Nagafuji T, Koide T, Takato M. Neurochemical correlates of selective neuronal loss following cerebral ischemia: Role of decreased Na+,K(+)-ATPase activity. Brain Res 1992; 571: 265-71.
[47]
MacMillan V. Cerebral Na+,K+-ATPase activity during exposure to and recovery from acute ischemia. J Cereb Blood Flow Metab 1982; 2: 457-65.
[48]
Deb P, Sharma S, Hassan KM. Pathophysiologic mechanisms of acute ischemic stroke: An overview with emphasis on therapeutic significance beyond thrombolysis. Pathophysiology 2010; 17: 197-218.
[49]
Prass K, Dirnagl U. Glutamate antagonists in therapy of stroke. Restor Neurol Neurosci 1998; 13: 3-10.
[50]
Kauppinen RA, McMahon HT, Nicholls DG. Ca2+-dependent and Ca2+-independent glutamate release, energy status and cytosolic free Ca2+ concentration in isolated nerve terminals following metabolic inhibition: possible relevance to hypoglycaemia and anoxia. Neuroscience 1988; 27: 175-82.
[51]
Smith WS. Pathophysiology of focal cerebral ischemia: A therapeutic perspective. J Vasc Interv Radiol 2004; 15: 3-12.
[52]
Kumar VS, Gopalakrishnan A, Naziroglu M, Rajanikant GK. Calcium ion - The key player in cerebral ischemia. Curr Med Chem 2014; 21: 2065-75.
[53]
Vidale S, Consoli A, Arnaboldi M, Consoli D. Postischemic inflammation in acute stroke. J Clin Neurol 2017; 13: 1-9.
[54]
Sage JI, Van Uitert RL, Duffy TE. Early changes in blood brain barrier permeability to small molecules after transient cerebral ischemia. Stroke 1984; 15: 46-50.
[55]
Emsley HC, Smith CJ, Tyrrell PJ, Hopkins SJ. Inflammation in acute ischemic stroke and its relevance to stroke critical care. Neurocrit Care 2008; 9: 125-38.
[56]
Jin R, Liu L, Zhang S, Nanda A, Li G. Role of inflammation and its mediators in acute ischemic stroke. J Cardiovasc Transl Res 2013; 6: 834-51.
[57]
Krueger M, Hartig W, Reichenbach A, Bechmann I, Michalski D. Blood-brain barrier breakdown after embolic stroke in rats occurs without ultrastructural evidence for disrupting tight junctions. PLoS One 2013; 8: e56419.
[58]
Chen B, Friedman B, Whitney MA, et al. Thrombin activity associated with neuronal damage during acute focal ischemia. J Neurosci 2012; 32: 7622-31.
[59]
Bushi D, Chapman J, Katzav A, et al. Quantitative detection of thrombin activity in an ischemic stroke model. J Mol Neurosci 2013; 51: 844-50.
[60]
Thevenet J, Angelillo-Scherrer A, Price M, Hirt L. Coagulation factor Xa activates thrombin in ischemic neural tissue. J Neurochem 2009; 111: 828-36.
[61]
Stein ES, Itsekson-Hayosh Z, Aronovich A, et al. Thrombin induces ischemic LTP (iLTP): Implications for synaptic plasticity in the acute phase of ischemic stroke. Sci Rep 2015; 5: 7912.
[62]
Si QS, Nakamura Y, Kataoka K. Albumin enhances superoxide production in cultured microglia. Glia 1997; 21: 413-8.
[63]
Denes A, Vidyasagar R, Feng J, et al. Proliferating resident microglia after focal cerebral ischaemia in mice. J Cereb Blood Flow Metab 2007; 27: 1941-53.
[64]
Jin R, Yang G, Li G. Inflammatory mechanisms in ischemic stroke: Role of inflammatory cells. J Leukoc Biol 2010; 87: 779-89.
[65]
Kim E, Cho S. Microglia and monocyte-derived macrophages in stroke. Neurotherapeutics 2016; 13: 702-18.
[66]
Samdani AF, Dawson TM, Dawson VL. Nitric oxide synthase in models of focal ischemia. Stroke 1997; 28: 1283-8.
[67]
Kim JY, Park J, Chang JY, Kim SH, Lee JE. Inflammation after ischemic stroke: The role of leukocytes and glial cells. Exp Neurobiol 2016; 25: 241-51.
[68]
Kaushal V, Schlichter LC. Mechanisms of microglia-mediated neurotoxicity in a new model of the stroke penumbra. J Neurosci 2008; 28: 2221-30.
[69]
Price CJ, Menon DK, Peters AM, et al. Cerebral neutrophil recruitment, histology, and outcome in acute ischemic stroke: An imaging-based study. Stroke 2004; 35: 1659-64.
[70]
DeGraba TJ. The role of inflammation after acute stroke: Utility of pursuing anti-adhesion molecule therapy. Neurology 1998; 51: 62-8.
[71]
Lagowska-Lenard M, Bielewicz J, Raszewski G, Stelmasiak Z, Bartosik-Psujek H. Oxidative stress in cerebral stroke. Pol Merkur Lekarski 2008; 25: 205-8.
[72]
Alexandrova ML, Bochev PG, Markova VI, et al. Oxidative stress in the chronic phase after stroke. Redox Rep 2003; 8: 169-76.
[73]
Heo JH, Han SW, Lee SK. Free radicals as triggers of brain edema formation after stroke. Free Radic Biol Med 2005; 39: 51-70.
[74]
Chan PH. Reactive oxygen radicals in signaling and damage in the ischemic brain. J Cereb Blood Flow Metab 2001; 21: 2-14.
[75]
Ishibashi N, Prokopenko O, Reuhl KR, Mirochnitchenko O. Inflammatory response and glutathione peroxidase in a model of stroke. J Immunol 2002; 168: 1926-33.
[76]
Inta I, Frauenknecht K, Dorr H, et al. Induction of the cytokine TWEAK and its receptor Fn14 in ischemic stroke. J Neurol Sci 2008; 275: 117-20.
[77]
Vila N, Castillo J, Davalos A, Chamorro A. Proinflammatory cytokines and early neurological worsening in ischemic stroke. Stroke 2000; 31: 2325-9.
[78]
Waje-Andreassen U, Krakenes J, Ulvestad E, et al. IL-6: An early marker for outcome in acute ischemic stroke. Acta Neurol Scand 2005; 111: 360-5.
[79]
Cojocaru IM, Cojocaru M, Tanasescu R, Iliescu I, Dumitrescu L, Silosi I. Expression of IL-6 activity in patients with acute ischemic stroke. Rom J Intern Med 2009; 47: 393-6.
[80]
Kwan J, Horsfield G, Bryant T, et al. IL-6 is a predictive biomarker for stroke associated infection and future mortality in the elderly after an ischemic stroke. Exp Gerontol 2013; 48: 960-5.
[81]
Richard Green A, Odergren T, Ashwood T. Animal models of stroke: Do they have value for discovering neuroprotective agents? Trends Pharmacol Sci 2003; 24: 402-8.
[82]
Zheng L, Ding J, Wang J, Zhou C, Zhang W. Effects and mechanism of action of inducible nitric oxide synthase on apoptosis in a rat model of cerebral ischemia-reperfusion injury. Anat Rec (Hoboken) 2016; 299: 246-55.
[83]
Meng S, Su Z, Liu Z, Wang N, Wang Z. Rac1 contributes to cerebral ischemia reperfusion-induced injury in mice by regulation of Notch2. Neuroscience 2015; 306: 100-14.
[84]
Murin R, Drgova A, Kaplan P, Dobrota D, Lehotsky J. Ischemia/Reperfusion-induced oxidative stress causes structural changes of brain membrane proteins and lipids. Gen Physiol Biophys 2001; 20: 431-8.
[85]
Sanderson TH, Reynolds CA, Kumar R, Przyklenk K, Huttemann M. Molecular mechanisms of ischemia-reperfusion injury in brain: Pivotal role of the mitochondrial membrane potential in reactive oxygen species generation. Mol Neurobiol 2013; 47: 9-23.
[86]
Chen XM, Chen HS, Xu MJ, Shen JG. Targeting reactive nitrogen species: A promising therapeutic strategy for cerebral ischemia-reperfusion injury. Acta Pharmacol Sin 2013; 34: 67-77.
[87]
Khan M, Jatana M, Elango C, Paintlia AS, Singh AK, Singh I. Cerebrovascular protection by various nitric oxide donors in rats after experimental stroke. Nitric Oxide 2006; 15: 114-24.
[88]
Matsui T, Nagafuji T, Kumanishi T, Asano T. Role of nitric oxide in pathogenesis underlying ischemic cerebral damage. Cell Mol Neurobiol 1999; 19: 177-89.
[89]
Eliasson MJ, Huang Z, Ferrante RJ, et al. Neuronal nitric oxide synthase activation and peroxynitrite formation in ischemic stroke linked to neural damage. J Neurosci 1999; 19: 5910-8.
[90]
Malinski T, Bailey F, Zhang ZG, Chopp M. Nitric oxide measured by a porphyrinic microsensor in rat brain after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 1993; 13: 355-8.
[91]
Uttara B, Singh AV, Zamboni P, Mahajan RT. Oxidative stress and neurodegenerative diseases: A review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 2009; 7: 65-74.
[92]
Crack PJ, Taylor JM. Reactive oxygen species and the modulation of stroke. Free Radic Biol Med 2005; 38: 1433-44.
[93]
Szocs K. Endothelial dysfunction and reactive oxygen species production in ischemia/reperfusion and nitrate tolerance. Gen Physiol Biophys 2004; 23: 265-95.
[94]
Schoknecht K, Prager O, Vazana U, et al. Monitoring stroke progression: In vivo imaging of cortical perfusion, blood-brain barrier permeability and cellular damage in the rat photothrombosis model. J Cereb Blood Flow Metab 2014; 34: 1791-801.
[95]
Palade GE. Fine structure of blood capillaries. J Appl Phys 1953; 24: 1424.
[96]
Yamada E. The fine structure of the gall bladder epithelium of the mouse. J Biophys Biochem Cytol 1955; 1: 445-58.
[97]
Shyng SL, Heuser JE, Harris DA. A glycolipid-anchored prion protein is endocytosed via clathrin-coated pits. J Cell Biol 1994; 125: 1239-50.
[98]
Head BP, Insel PA. Do caveolins regulate cells by actions outside of caveolae? Trends Cell Biol 2007; 17: 51-7.
[99]
Sowa G. Regulation of cell signaling and function by endothelial caveolins: Implications in disease. Transl Med (Sunnyvale) 2012; Suppl 8: 001.
[100]
Virgintino D, Robertson D, Errede M, et al. Expression of caveolin-1 in human brain microvessels. Neuroscience 2002; 115: 145-52.
[101]
Cameron PL, Ruffin JW, Bollag R, Rasmussen H, Cameron RS. Identification of caveolin and caveolin-related proteins in the brain. J Neurosci 1997; 17: 9520-35.
[102]
Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci 2006; 7: 41-53.
[103]
Gurnik S, Devraj K, Macas J, et al. Angiopoietin-2-induced blood-brain barrier compromise and increased stroke size are rescued by VE-PTP-dependent restoration of Tie2 signaling. Acta Neuropathol 2016; 131: 753-73.
[104]
Zhao YL, Song JN, Zhang M. Role of caveolin-1 in the biology of the blood-brain barrier. Rev Neurosci 2014; 25: 247-54.
[105]
Gu Y, Dee CM, Shen J. Interaction of free radicals, matrix metalloproteinases and caveolin-1 impacts blood-brain barrier permeability. Front Biosci (Schol Ed) 2011; 3: 1216-31.
[106]
Lakhan SE, Kirchgessner A, Tepper D, Leonard A. Matrix metalloproteinases and blood-brain barrier disruption in acute ischemic stroke. Front Neurol 2013; 4: 32.
[107]
Liu J, Jin X, Liu KJ, Liu W. Matrix metalloproteinase-2-mediated occludin degradation and caveolin-1-mediated claudin-5 redistribution contribute to blood-brain barrier damage in early ischemic stroke stage. J Neurosci 2012; 32: 3044-57.
[108]
Salgado IK, Serrano M, Garcia JO, et al. SorLA in glia: Shared subcellular distribution patterns with caveolin-1. Cell Mol Neurobiol 2012; 32: 409-21.
[109]
Takeuchi S, Matsuda W, Tooyama I, Yasuhara O. Kainic acid induces expression of caveolin-1 in activated microglia in rat brain. Folia Histochem Cytobiol 2013; 51: 25-30.
[110]
Head BP, Peart JN, Panneerselvam M, et al. Loss of caveolin-1 accelerates neurodegeneration and aging. PLoS One 2010; 5: e15697.
[111]
Niesman IR, Zemke N, Fridolfsson HN, et al. Caveolin isoform switching as a molecular, structural, and metabolic regulator of microglia. Mol Cell Neurosci 2013; 56: 283-97.
[112]
Head BP, Hu Y, Finley JC, et al. Neuron-targeted caveolin-1 protein enhances signaling and promotes arborization of primary neurons. J Biol Chem 2011; 286: 33310-21.
[113]
Head BP, Patel HH, Tsutsumi YM, et al. Caveolin-1 expression is essential for N-methyl-D-aspartate receptor-mediated Src and extracellular signal-regulated kinase 1/2 activation and protection of primary neurons from ischemic cell death. FASEB J 2008; 22: 828-40.
[114]
Shiroto T, Romero N, Sugiyama T, et al. Caveolin-1 is a critical determinant of autophagy, metabolic switching, and oxidative stress in vascular endothelium. PLoS One 2014; 9: e87871.
[115]
Yun JH, Park SJ, Jo A, et al. Caveolin-1 is involved in reactive oxygen species-induced SHP-2 activation in astrocytes. Exp Mol Med 2011; 43: 660-8.
[116]
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: 22810-4.
[117]
Michel JB, Feron O, Sacks D, Michel T. Reciprocal regulation of endothelial nitric-oxide synthase by Ca2+-calmodulin and caveolin. J Biol Chem 1997; 272: 15583-6.
[118]
Xu HL, Galea E, Santizo RA, Baughman VL, Pelligrino DA. The key role of caveolin-1 in estrogen-mediated regulation of endothelial nitric oxide synthase function in cerebral arterioles in vivo. J Cereb Blood Flow Metab 2001; 21: 907-13.
[119]
Shen J, Ma S, Chan P, et al. Nitric oxide down-regulates caveolin-1 expression in rat brains during focal cerebral ischemia and reperfusion injury. J Neurochem 2006; 96: 1078-89.
[120]
Bucci M, Gratton JP, Rudic RD, et al. In vivo delivery of the caveolin-1 scaffolding domain inhibits nitric oxide synthesis and reduces inflammation. Nat Med 2000; 6: 1362-7.
[121]
Shen J, Lee W, Li Y, et al. Interaction of caveolin-1, nitric oxide, and nitric oxide synthases in hypoxic human SK-N-MC neuroblastoma cells. J Neurochem 2008; 107: 478-87.
[122]
Gao L, Chen X, Peng T, et al. Caveolin-1 protects against hepatic ischemia/reperfusion injury through ameliorating peroxynitrite-mediated cell death. Free Radic Biol Med 2016; 95: 209-15.
[123]
Young LH, Ikeda Y, Lefer AM. Caveolin-1 peptide exerts cardioprotective effects in myocardial ischemia-reperfusion via nitric oxide mechanism. Am J Physiol Heart Circ Physiol 2001; 280: H2489-95.
[124]
Seiler C, Hess OM, Buechi M, Suter TM, Krayenbuehl HP. Influence of serum cholesterol and other coronary risk factors on vasomotion of angiographically normal coronary arteries. Circulation 1993; 88: 2139-48.
[125]
Reddy KG, Nair RN, Sheehan HM, Hodgson JM. Evidence that selective endothelial dysfunction may occur in the absence of angiographic or ultrasound atherosclerosis in patients with risk factors for atherosclerosis. J Am Coll Cardiol 1994; 23: 833-43.
[126]
Creager MA, Cooke JP, Mendelsohn ME, et al. Impaired vasodilation of forearm resistance vessels in hypercholesterolemic humans. J Clin Invest 1990; 86: 228-34.
[127]
Flavahan NA. Atherosclerosis or lipoprotein-induced endothelial dysfunction. Potential mechanisms underlying reduction in EDRF/nitric oxide activity. Circulation 1992; 85: 1927-38.
[128]
Casino PR, Kilcoyne CM, Quyyumi AA, Hoeg JM, Panza JA. The role of nitric oxide in endothelium-dependent vasodilation of hypercholesterolemic patients. Circulation 1993; 88: 2541-7.
[129]
Feron O, Dessy C, Moniotte S, Desager JP, Balligand JL. Hypercholesterolemia decreases nitric oxide production by promoting the interaction of caveolin and endothelial nitric oxide synthase. J Clin Invest 1999; 103: 897-905.
[130]
Charles S, Raj V, Arokiaraj J, Mala K. Caveolin1/protein arginine methyltransferase1/sirtuin1 axis as a potential target against endothelial dysfunction. Pharmacol Res 2017; 119: 1-11.
[131]
Gu Y, Zheng G, Xu M, et al. Caveolin-1 regulates nitric oxide-mediated matrix metalloproteinases activity and blood-brain barrier permeability in focal cerebral ischemia and reperfusion injury. J Neurochem 2012; 120: 147-56.
[132]
Choi KH, Kim HS, Park MS, et al. Regulation of caveolin-1 expression determines early brain edema after experimental focal cerebral ischemia. Stroke 2016; 47: 1336-43.
[133]
Thomsen MS, Routhe LJ, Moos T. The vascular basement membrane in the healthy and pathological brain. J Cereb Blood Flow Metab 2017; 37(10): 3300-17.
[134]
Horng S, Therattil A, Moyon S, et al. Astrocytic tight junctions control inflammatory CNS lesion pathogenesis. J Clin Invest 2017; 127: 3136-51.
[135]
Xu L, Wang L, Wen Z, et al. Caveolin-1 is a checkpoint regulator in hypoxia-induced astrocyte apoptosis via Ras/Raf/ERK pathway. Am J Physiol Cell Physiol 2016; 310: 903-10.
[136]
Fu S, Gu Y, Jiang JQ, et al. Calycosin-7-O-beta-D-glucoside regulates nitric oxide /caveolin-1/matrix metalloproteinases pathway and protects blood-brain barrier integrity in experimental cerebral ischemia-reperfusion injury. J Ethnopharmacol 2014; 155: 692-701.
[137]
Isshiki M, Ando J, Yamamoto K, Fujita T, Ying Y, Anderson RG. Sites of Ca(2+) wave initiation move with caveolae to the trailing edge of migrating cells. J Cell Sci 2002; 115: 475-84.
[138]
Isshiki M, Ying YS, Fujita T, Anderson RG. A molecular sensor detects signal transduction from caveolae in living cells. J Biol Chem 2002; 277: 43389-98.
[139]
Brazer SC, Singh BB, Liu X, Swaim W, Ambudkar IS. Caveolin-1 contributes to assembly of store-operated Ca2+ influx channels by regulating plasma membrane localization of TRPC1. J Biol Chem 2003; 278: 27208-15.
[140]
Ge S, Pachter JS. Caveolin-1 knockdown by small interfering RNA suppresses responses to the chemokine monocyte chemoattractant protein-1 by human astrocytes. J Biol Chem 2004; 279: 6688-95.
[141]
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 2009; 296: C403-13.
[142]
Drab M, Verkade P, Elger M, et al. Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 2001; 293: 2449-52.
[143]
Xiong Y, Wang XM, Zhong M, et al. Alterations of caveolin-1 expression in a mouse model of delayed cerebral vasospasm following subarachnoid hemorrhage. Exp Ther Med 2016; 12: 1993-2002.
[144]
Wan D, Zhou Y, Wang K, Hou Y, Hou R, Ye X. Resveratrol provides neuroprotection by inhibiting phosphodiesterases and regulating the cAMP/AMPK/SIRT1 pathway after stroke in rats. Brain Res Bull 2016; 121: 255-62.
[145]
Cui X, Chopp M, Zacharek A, et al. Endothelial nitric oxide synthase regulates white matter changes via the BDNF/TrkB pathway after stroke in mice. PLoS One 2013; 8: e80358.
[146]
Qi D, Ouyang C, Wang Y, et al. HO-1 attenuates hippocampal neurons injury via the activation of BDNF-TrkB-PI3K/Akt signaling pathway in stroke. Brain Res 2014; 1577: 69-76.
[147]
Yang Y, Ma Z, Hu W, et al. Caveolin-1/-3: Therapeutic targets for myocardial ischemia/reperfusion injury. Basic Res Cardiol 2016; 111: 45.
[148]
Das M, Gherghiceanu M, Lekli I, Mukherjee S, Popescu LM, Das DK. Essential role of lipid raft in ischemic preconditioning. Cell Physiol Biochem 2008; 21: 325-34.
[149]
Kang JW, Lee SM. Impaired expression of caveolin-1 contributes to hepatic ischemia and reperfusion injury. Biochem Biophys Res Commun 2014; 450: 1351-7.
[150]
Flick M, Albrecht M, Oei GT, et al. Helium postconditioning regulates expression of caveolin-1 and -3 and induces RISK pathway activation after ischaemia/reperfusion in cardiac tissue of rats. Eur J Pharmacol 2016; 791: 718-25.
[151]
Patel HH, Tsutsumi YM, Head BP, et al. Mechanisms of cardiac protection from ischemia/reperfusion injury: A role for caveolae and caveolin-1. FASEB J 2007; 21: 1565-74.
[152]
Das M, Cui J, Das DK. Generation of survival signal by differential interaction of p38MAPKalpha and p38MAPKbeta with caveolin-1 and caveolin-3 in the adapted heart. J Mol Cell Cardiol 2007; 42: 206-13.
[153]
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 2006; 34: 434-42.
[154]
Pavlides S, Tsirigos A, Vera I, et al. Loss of stromal caveolin-1 leads to oxidative stress, mimics hypoxia and drives inflammation in the tumor microenvironment, conferring the “reverse Warburg effect”: A transcriptional informatics analysis with validation. Cell Cycle 2010; 9: 2201-19.
[155]
Mandyam CD, Schilling JM, Cui W, et al. Neuron-targeted caveolin-1 improves molecular signaling, plasticity, and behavior dependent on the hippocampus in adult and aged mice. Biol Psychiatry 2017; 81: 101-10.
[156]
Egawa J, Schilling JM, Cui W, et al. Neuron-specific caveolin-1 overexpression improves motor function and preserves memory in mice subjected to brain trauma. FASEB J 2017; 31: 3403-11.
[157]
Egawa J, Zemljic-Harpf AE, Mandyam CD, et al. Neuron-targeted caveolin-1 promotes ultrastructural and functional hippocampal synaptic plasticity. Cereb Cortex 2018; 28(9): 3255-66.
[158]
Li HQ, Li Y, Chen ZX, et al. Electroacupuncture exerts neuroprotection through caveolin-1 mediated molecular pathway in intracerebral hemorrhage of rats. Neural Plast 2016; 2016: 7308261.
[159]
Sonveaux P, Martinive P, DeWever J, et al. Caveolin-1 expression is critical for vascular endothelial growth factor-induced ischemic hindlimb collateralization and nitric oxide-mediated angiogenesis. Circ Res 2004; 95: 154-61.
[160]
Griffoni C, Spisni E, Santi S, Riccio M, Guarnieri T, Tomasi V. Knockdown of caveolin-1 by antisense oligonucleotides impairs angiogenesis in vitro and in vivo. Biochem Biophys Res Commun 2000; 276: 756-61.
[161]
Chang SH, Feng D, Nagy JA, Sciuto TE, Dvorak AM, Dvorak HF. Vascular permeability and pathological angiogenesis in caveolin-1-null mice. Am J Pathol 2009; 175: 1768-76.
[162]
Tahir SA, Park S, Thompson TC. Caveolin-1 regulates VEGF-stimulated angiogenic activities in prostate cancer and endothelial cells. Cancer Biol Ther 2009; 8: 2286-96.
[163]
Jasmin JF, Malhotra S, Singh Dhallu M, Mercier I, Rosenbaum DM, Lisanti MP. Caveolin-1 deficiency increases cerebral ischemic injury. Circ Res 2007; 100: 721-9.
[164]
Gao Y, Zhao Y, Pan J, et al. Treadmill exercise promotes angiogenesis in the ischemic penumbra of rat brains through caveolin-1/VEGF signaling pathways. Brain Res 2014; 1585: 83-90.
[165]
Pang Q, Zhang H, Chen Z, et al. Role of caveolin-1/vascular endothelial growth factor pathway in basic fibroblast growth factor-induced angiogenesis and neurogenesis after treadmill training following focal cerebral ischemia in rats. Brain Res 2017; 1663: 9-19.
[166]
Zhao Y, Pang Q, Liu M, et al. Treadmill exercise promotes neurogenesis in ischemic rat brains via caveolin-1/VEGF signaling pathways. Neurochem Res 2017; 42: 389-97.

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