The mechanisms of cerebral vascular dysfunction and neuroinflammation by MMP-mediated degradation of VEGFR-2 in alcohol ingestion

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 5, 2012, Pages 1167-1177

  Muneer, P M Abdul ^a   Alikunju, Saleena ^a   Szlachetka, Adam M ^a   Haorah, James ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Alcohol; Blood brain barrier; Matrix metalloproteinase; Vascular endothelial growth factor; Vascular endothelial growth factor R2; Vascular inflammation

Indexed keywords

GELATINASE B; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; STROMELYSIN; VASCULOTROPIN A; VASCULOTROPIN RECEPTOR 1;

ALCOHOLISM; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD BRAIN BARRIER; CELL INFILTRATION; CEREBROVASCULAR DISEASE; CHRONIC DISEASE; CONTROLLED STUDY; HUMAN; HUMAN CELL; IMMUNOCOMPETENT CELL; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT;

ALCOHOL DRINKING; ANIMALS; BLOOD-BRAIN BARRIER; BLOTTING, WESTERN; CELLS, CULTURED; CEREBROVASCULAR CIRCULATION; DISEASE MODELS, ANIMAL; ENDOTHELIUM, VASCULAR; HUMANS; MALE; MATRIX METALLOPROTEINASES; NEURODEGENERATIVE DISEASES; RATS; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-2;

EID: 84860215152     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.247668     Document Type: Article

References (46)

1. Rubin LL, Staddon JM. The cell biology of the blood-brain barrier. Annu Rev Neurosci. 1999;22:11-28. (Pubitemid 29144879)
2. Hawkins BT, Davis TP. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev. 2005;57:173-185. (Pubitemid 41043883)
3. Fanning AS, Jameson BJ, Jesaitis LA, Anderson JM. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J Biol Chem. 1998;273:29745-29753. (Pubitemid 28509986)
4. Wardlaw JM, Doubal F, Armitage P, Chappell F, Carpenter T, Munoz Maniega S, Farrall A, Sudlow C, Dennis M, Dhillon B. Lacunar stroke is associated with diffuse blood-brain barrier dysfunction. Ann Neurol. 2009;65:194-202.
5. Fiala M, Liu QN, Sayre J, Pop V, Brahmandam V, Graves MC, Vinters HV. Cyclooxygenase-2-positive macrophages infiltrate the Alzheimer's disease brain and damage the blood-brain barrier. Eur J Clin Invest. 2002;32:360-371. (Pubitemid 36228397)
6. Persidsky Y, Heilman D, Haorah J, Zelivyanskaya M, Persidsky R, Weber GA, Shimokawa H, Kaibuchi K, Ikezu T. Rho-mediated regulation of tight junctions during monocyte migration across the blood-brain barrier in HIV-1 encephalitis (HIVE). Blood. 2006;107:4770-4780. (Pubitemid 43882628)
7. McCandless EE, Piccio L, Woerner BM, Schmidt RE, Rubin JB, Cross AH, Klein RS. Pathological expression of CXCL12 at the blood-brain barrier correlates with severity of multiple sclerosis. Am J Pathol. 2008;172:799-808. (Pubitemid 351354551)
8. Gaitan MI, Shea CD, Evangelou IE, Stone RD, Fenton KM, Bielekova B, Massacesi L, Reich DS. Evolution of the blood-brain barrier in newly forming multiple sclerosis lesions. Ann Neurol. 2011;70:22-29.
9. Haorah J, Schall K, Ramirez SH, Persidsky Y. Activation of protein tyrosine kinases and matrix metalloproteinases causes blood-brain barrier injury: novel mechanism for neurodegeneration associated with alcohol abuse. Glia. 2008;56:78-88. (Pubitemid 350172733)
10. Gursoy-Ozdemir Y, Qiu J, Matsuoka N, Bolay H, Bermpohl D, Jin H, Wang X, Rosenberg GA, Lo EH, Moskowitz MA. Cortical spreading depression activates and upregulates MMP-9. J Clin Invest. 2004;113:1447-1455. (Pubitemid 39071700)
11. Kim GW, Gasche Y, Grzeschik S, Copin JC, Maier CM, Chan PH. Neurodegeneration in striatum induced by the mitochondrial toxin 3-nitropropionic acid: role of matrix metalloproteinase-9 in early blood-brain barrier disruption? J Neurosci. 2003;23:8733-8742. (Pubitemid 37176654)
12. Machado LS, Kozak A, Ergul A, Hess DC, Borlongan CV, Fagan SC. Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 2006;7:56.
13. Rosell A, Alvarez-Sabin J, Arenillas JF, Rovira A, Delgado P, Fernandez-Cadenas I, Penalba A, Molina CA, Montaner J. A matrix metalloproteinase protein array reveals a strong relation between MMP-9 and MMP-13 with diffusion-weighted image lesion increase in human stroke. Stroke. 2005;36:1415-1420. (Pubitemid 40967504)
14. Rosell A, Ortega-Aznar A, Alvarez-Sabin J, Fernandez-Cadenas I, Ribo M, Molina CA, Lo EH, Montaner J. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke. 2006;37:1399-1406. (Pubitemid 44305716)
15. Carmeliet P. Angiogenesis in life, disease and medicine. Nature. 2005;438:932-936. (Pubitemid 43093958)
16. Shalaby F, Rossant J, Yamaguchi TP, Gertsenstein M, Wu XF, Breitman ML, Schuh AC. Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice. Nature. 1995;376:62-66.
17. Millauer B, Wizigmann-Voos S, Schnurch H, Martinez R, Moller NP, Risau W, Ullrich A. High affinity VEGF binding and developmental expression suggest Flk-1 as a major regulator of vasculogenesis and angiogenesis. Cell. 1993;72:835-846. (Pubitemid 23110226)
18. Neufeld G, Cohen T, Gengrinovitch S, Poltorak Z. Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 1999;13:9-22. (Pubitemid 29038270)
19. Baffert F, Le T, Sennino B, Thurston G, Kuo CJ, Hu-Lowe D, McDonald DM. Cellular changes in normal blood capillaries undergoing regression after inhibition of VEGF signaling. Am J Physiol Heart Circ Physiol. 2006;290:H547-H559.
20. Gerber HP, Hillan KJ, Ryan AM, Kowalski J, Keller GA, Rangell L, Wright BD, Radtke F, Aguet M, Ferrara N. VEGF is required for growth and survival in neonatal mice. Development. 1999;126:1149-1159. (Pubitemid 29182112)
21. Argaw AT, Gurfein BT, Zhang Y, Zameer A, John GR. VEGF-mediated disruption of endothelial CLN-5 promotes blood-brain barrier breakdown. Proc Natl Acad Sci USA. 2009;106:1977-1982.
22. Morin-Brureau M, Lebrun A, Rousset MC, Fagni L, Bockaert J, de Bock F, Lerner-Natoli M. Epileptiform activity induces vascular remodeling and zonula occludens 1 downregulation in organotypic hippocampal cultures: role of VEGF signaling pathways. J Neurosci. 2011;31:10677-10688.
23. Young PP, Fantz CR, Sands MS. VEGF disrupts the neonatal blood-brain barrier and increases life span after non-ablative BMT in a murine model of congenital neurodegeneration caused by a lysosomal enzyme deficiency. Exp Neurol. 2004;188:104-114. (Pubitemid 38748809)
24. Chi OZ, Hunter C, Liu X, Tan T, Weiss HR. Effects of VEGF on the blood-brain barrier disruption caused by hyperosmolarity. Pharmacology. 2008;82:187-192.
25. Zuba D, Piekoszewski W, Pach J, Winnik L, Parczewski A. Concentration of ethanol and other volatile compounds in the blood of acutely poisoned alcoholics. Alcohol. 2002;26:17-22. (Pubitemid 34218999)
26. Deutch SR, Christian C, Hoyer S, Christensen EF, Dragsholt C, Hansen AC, Kristensen IB, Hougaard K. Drug and alcohol use among patients admitted to a Danish trauma centre: a prospective study from a regional trauma centre in Scandinavia. Eur J Emerg Med. 2004;11:318-322.
27. Haorah J, Knipe B, Gorantla S, Zheng J, Persidsky Y. Alcohol-induced blood-brain barrier dysfunction is mediated via inositol 1,4,5-triphosphate receptor (IP3R)-gated intracellular calcium release. J Neurochem. 2007;100:324-336. (Pubitemid 46010994)
28. Alikunju S, Abdul Muneer PM, Zhang Y, Szlachetka AM, Haorah J. The inflammatory footprints of alcohol-induced oxidative damage in neurovascular components. Brain Behav Immun. 2011;25(Suppl 1):S129-S136.
29. Li DQ, Meller D, Liu Y, Tseng SC. Overexpression of MMP-1 and MMP-3 by cultured conjunctivochalasis fibroblasts. Invest Ophthalmol Vis Sci. 2000;41:404-410. (Pubitemid 30080442)
30. Ramirez SH, Heilman D, Morsey B, Potula R, Haorah J, Persidsky Y. Activation of peroxisome proliferator-activated receptor gamma (PPARgamma) suppresses Rho GTPases in human brain microvascular endothelial cells and inhibits adhesion and transendothelial migration of HIV-1 infected monocytes. J Immunol. 2008;180:1854-1865.
31. Domingues I, Rino J, Demmers JA, de Lanerolle P, Santos SC. VEGFR2 translocates to the nucleus to regulate its own transcription. PLoS One. 2011;6:e25668.
32. Lampugnani MG, Orsenigo F, Gagliani MC, Tacchetti C, Dejana E. Vascular endothelial cadherin controls VEGFR-2 internalization and signaling from intracellular compartments. J Cell Biol. 2006;174:593-604. (Pubitemid 44231870)
33. Reijerkerk A, Kooij G, van der Pol SM, Khazen S, Dijkstra CD, de Vries HE. Diapedesis of monocytes is associated with MMP-mediated occludin disappearance in brain endothelial cells. FASEB J. 2006;20:2550-2552.
34. Raffetto JD, Khalil RA. Matrix metalloproteinases and their inhibitors in vascular remodeling and vascular disease. Biochem Pharmacol. 2008;75:346-359. (Pubitemid 350298459)
35. Bennett J, Basivireddy J, Kollar A, Biron KE, Reickmann P, Jefferies WA, McQuaid S. Blood-brain barrier disruption and enhanced vascular permeability in the multiple sclerosis model EAE. J Neuroimmunol. 2010;229:180-191.
36. Tsuji K, Aoki T, Tejima E, Arai K, Lee SR, Atochin DN, Huang PL, Wang X, Montaner J, Lo EH. Tissue plasminogen activator promotes matrix metalloproteinase-9 upregulation after focal cerebral ischemia. Stroke. 2005;36:1954-1959. (Pubitemid 41266533)
37. Turk BE, Huang LL, Piro ET, Cantley LC. Determination of protease cleavage site motifs using mixture-based oriented peptide libraries. Nat Biotechnol. 2001;19:661-667. (Pubitemid 32625438)
38. Tran ED, DeLano FA, Schmid-Schonbein GW. Enhanced matrix metalloproteinase activity in the spontaneously hypertensive rat: VEGFR-2 cleavage, endothelial apoptosis, and capillary rarefaction. J Vasc Res. 2010;47:423-431.
39. Lamy S, Lachambre MP, Lord-Dufour S, Beliveau R. Propranolol suppresses angiogenesis in vitro: inhibition of proliferation, migration, and differentiation of endothelial cells. Vascul Pharmacol. 2010;53:200-208.
40. Ugarte-Berzal E, Redondo-Munoz J, Eroles P, Del Cerro MH, Garcia-Marco JA, Terol MJ, Garcia-Pardo A. VEGF/VEGFR2 interaction downregulates matrix metalloproteinase-9 via STAT1 activation and inhibits B chronic lymphocytic leukemia cell migration. Blood. 2010;115:846-849.
41. Ito TK, Ishii G, Saito S, Yano K, Hoshino A, Suzuki T, Ochiai A. Degradation of soluble VEGF receptor-1 by MMP-7 allows VEGF access to endothelial cells. Blood. 2009;113:2363-2369.
42. Kanazawa M, Igarashi H, Kawamura K, Takahashi T, Kakita A, Takahashi H, Nakada T, Nishizawa M, Shimohata T. Inhibition of VEGF signaling pathway attenuates hemorrhage after tPA treatment. J Cereb Blood Flow Metab. 2011;31:1461-1474.
43. Heberlein A, Muschler M, Lenz B, Frieling H, Buchl C, Groschl M, Riera R, Kornhuber J, Bleich S, Hillemacher T. Serum levels of vascular endothelial growth factor A increase during alcohol withdrawal. Addict Biol. 2010;15:362-364.
44. Radek KA, Kovacs EJ, Gallo RL, DiPietro LA. Acute ethanol exposure disrupts VEGF receptor cell signaling in endothelial cells. Am J Physiol Heart Circ Physiol. 2008;295:H174-H184.
45. Deguchi T, Hashiguchi T, Horinouchi S, Uto T, Oku H, Kimura K, Makisumi K, Arimura K. Serum VEGF increases in diabetic polyneuropathy, particularly in the neurologically active symptomatic stage. Diabet Med. 2009;26:247-252.
46. Obermair A, Tempfer C, Hefler L, Preyer O, Kaider A, Zeillinger R, Leodolter S, Kainz C. Concentration of vascular endothelial growth factor (VEGF) in the serum of patients with suspected ovarian cancer. Br J Cancer. 1998;77:1870-1874. (Pubitemid 28254626)