Oxidative stress activates protein tyrosine kinase and matrix metalloproteinases leading to blood-brain barrier dysfunction

Journal of Neurochemistry

Volumn 101, Issue 2, 2007, Pages 566-576

  Haorah, James ^a,b   Ramirez, Servio H ^a   Schall, Kathy ^a   Smith, Daniel ^a   Pandya, Rita ^a   Persidsky, Yuri ^a  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Blood brain barrier; Brain endothelial cell; Matrix metalloproteinases; Oxidative stress; Protein tyrosine kinase; Protein tyrosine phosphatase

Indexed keywords

GELATINASE A; GELATINASE B; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TISSUE INHIBITOR OF METALLOPROTEINASE 2;

ARTICLE; BASEMENT MEMBRANE; BLOOD BRAIN BARRIER; BRAIN DYSFUNCTION; CELL MEMBRANE PERMEABILITY; CELL MIGRATION; CONTROLLED STUDY; ENCEPHALITIS; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; MICROVASCULARIZATION; MONOCYTE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; STROKE; TIGHT JUNCTION;

BASEMENT MEMBRANE; BLOOD-BRAIN BARRIER; CELLS, CULTURED; CEREBRAL ARTERIES; CHEMOTAXIS, LEUKOCYTE; ENCEPHALITIS; ENDOTHELIAL CELLS; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; MATRIX METALLOPROTEINASES; NEURODEGENERATIVE DISEASES; OXIDATIVE STRESS; PROTEIN-TYROSINE KINASES; REACTIVE OXYGEN SPECIES; TIGHT JUNCTIONS; TISSUE INHIBITOR OF METALLOPROTEINASE-1; UP-REGULATION;

EID: 34047114464     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2006.04393.x     Document Type: Article

References (66)

1. Andriopoulou P., Navarro P., Zanetti A., Lampugnani M. G. and Dejana E. (1999) Histamine induces tyrosine phosphorylation of endothelial cell-to-cell adherens junctions. Arterioscler. Thromb. Vasc. Biol. 19, 2286-2297.
2. Antonetti D. A., Barber A. J., Hollinger L. A., Wolpert E. B. and Gardner T. W. (1999) Vascular endothelial growth factor induces rapid phosphorylation of tight junction proteins occludin and zonula occluden 1. A potential mechanism for vascular permeability in diabetic retinopathy and tumors. J. Biol. Chem. 274, 23 463-23 467.
3. Blasig I. E., Mertsch K. and Haseloff R. F. (2002) Nitronyl nitroxides, a novel group of protective agents against oxidative stress in endothelial cells forming the blood-brain barrier. Neuropharmacology 43, 1006-1014.
4. Boven L. A., Gomes L., Hery C., Gray F., Verhoef J., Portegies P., Tardieu M. and Nottet H. S. (1999) Increased peroxynitrite activity in AIDS dementia complex: implications for the neuropathogenesis of HIV-1 infection. J. Immunol. 162, 4319-4327.
5. Cernuda-Morollon E. and Ridley A. J. (2006) Rho GTPases and leukocyte adhesion receptor expression and function in endothelial cells. Circ. Res. 98, 757-767.
6. Chen C. H., Cheng T. H., Lin H. et al. (2006) Reactive oxygen species generation is involved in epidermal growth factor receptor transactivation through the transient oxidization of Src homology 2-containing tyrosine phosphatase in endothelin-1 signaling pathway in rat cardiac fibroblasts. Mol. Pharmacol. 69, 1347-1355.
7. Dejana E., Spagnuolo R. and Bazzoni G. (2001) Interendothelial junctions and their role in the control of angiogenesis, vascular permeability and leukocyte transmigration. Thromb. Haemost. 86, 308-315.
8. Du J., Peng T., Scheidegger K. J. and Delafontaine P. (1999) Angiotensin II activation of insulin-like growth factor 1 receptor transcription is mediated by a tyrosine kinase-dependent redox-sensitive mechanism. Arterioscler. Thromb. Vasc. Biol. 19, 2119-2126.
9. Fanning A. S., Jameson B. J., Jesaitis L. A. and Anderson J. M. (1998) The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273, 29 745-29 753.
10. Fiala M., Liu Q. N., Sayre J., Pop V., Brahmandam V., Graves M. C. and Vinters H. V. (2002) Cyclooxygenase-2-positive macrophages infiltrate the Alzheimer's disease brain and damage the blood-brain barrier. Eur. J. Clin. Invest. 32, 360-371.
11. Fukuda S., Fini C. A., Mabuchi T., Koziol J. A., Eggleston L. L. Jr and del Zoppo G. J. (2004) Focal cerebral ischemia induces active proteases that degrade microvascular matrix. Stroke 35, 998-1004.
12. Galli A., Svegliati-Baroni G., Ceni E. et al. (2005) Oxidative stress stimulates proliferation and invasiveness of hepatic stellate cells via a MMP2-mediated mechanism. Hepatology 41, 1074-1084.
13. Gasche Y., Fujimura M., Morita-Fujimura Y., Copin J. C., Kawase M., Massengale J. and Chan P. H. (1999) Early appearance of activated matrix metalloproteinase-9 after focal cerebral ischemia in mice: a possible role in blood-brain barrier dysfunction. J. Cereb. Blood Flow Metab. 19, 1020-1028.
14. Ghorpade A., Persidskaia R., Suryadevara R., Che M., Liu X. J., Persidsky Y. and Gendelman H. E. (2001) Mononuclear phagocyte differentiation, activation, and viral infection regulate matrix metalloproteinase expression: implications for human immunodeficiency virus type 1-associated dementia. J. Virol. 75, 6572-6583.
15. Grote K., Flach I., Luchtefeld M., Akin E., Holland S. M., Drexler H. and Schieffer B. (2003) Mechanical stretch enhances mRNA expression and proenzyme release of matrix metalloproteinase-2 (MMP-2) via NAD(P)H oxidase-derived reactive oxygen species. Circ. Res. 92, e80-e86.
16. Gursoy-Ozdemir Y., Qiu J., Matsuoka N., Bolay H., Bermpohl D., Jin H., Wang X., Rosenberg G. A., Lo E. H. and Moskowitz M. A. (2004) Cortical spreading depression activates and upregulates MMP-9. J. Clin. Invest. 113, 1447-1455.
17. Hanumegowda U. M., Copple B. L., Shibuya M., Malle E., Ganey P. E. and Roth R. A. (2003) Basement membrane and matrix metalloproteinases in monocrotaline-induced liver injury. Toxicol. Sci. 76, 237-246.
18. Haorah J., Knipe B., Leibhart J., Ghorpade A. and Persidsky Y. (2005a) Alcohol-induced oxidative stress in brain endothelial cells causes blood-brain barrier dysfunction. J. Leukoc. Biol. 78, 1223-1232.
19. Haorah J., Heilman D., Knipe B., Chrastil J., Leibhart J., Ghorpade A., Miller D. W. and Persidsky Y. (2005b) Ethanol-induced activation of myosin light chain kinase leads to dysfunction of tight junctions and blood-brain barrier compromise. Alcohol. Clin. Exp. Res. 29, 999-1009.
20. Haorah J. K. B., Gorantla S., Zheng J. and Persidsky Y. (2007) Alcohol-induced blood-brain barrier dysfunction is mediated via inositol 1,4,5-triphosphate receptor IP3R-gated intracellular calcium release. J. Neurochem. 100, 324-336.
21. Hawkins B. T. and Davis T. P. (2005) The blood-brain barrier/ neurovascular unit in health and disease. Pharmacol. Rev. 57, 173-185.
22. Hemmerlein B., Johanns U., Halbfass J., Bottcher T., Heuser M., Radzun H. J. and Thelen P. (2004) The balance between MMP-2/-9 and TIMP-1/-2 is shifted towards MMP in renal cell carcinomas and can be further disturbed by hydrogen peroxide. Int. J. Oncol. 24, 1069-1076.
23. van Horssen J., Schreibelt G., Bo L., Montagne L., Drukarch B., van Muiswinkel F. L. and de Vries H. E. (2006) NAD(P)H:quinone oxidoreductase 1 expression in multiple sclerosis lesions. Free Radic. Biol. Med. 41, 311-317.
24. Ilzecka J. (1996) The structure and function of blood-brain barrier in ischaemic brain stroke process. Ann. Univ. Mariae Curie Sklodowska [Med.] 51, 123-127.
25. Kale G., Naren A. P., Sheth P. and Rao R. K. (2003) Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2, and ZO-3. Biochem. Biophys. Res. Commun. 302, 324-329.
26. Kim Y. M., Jang J. W., Lee O. H., Yeon J., Choi E. Y., Kim K. W., Lee S. T. and Kwon Y. G. (2000) Endostatin inhibits endothelial and tumor cellular invasion by blocking the activation and catalytic activity of matrix metalloproteinase. Cancer Res. 60, 5410-5413.
27. Kim Y. M., Hwang S., Kim Y. M., Pyun B. J., Kim T. Y., Lee S. T., Gho Y. S. and Kwon Y. G. (2002) Endostatin blocks vascular endothelial growth factor-mediated signaling via direct interaction with KDR/Flk-1. J. Biol. Chem. 277, 27872-27879.
28. Kim G. W., Gasche Y., Grzeschik S., Copin J. C., Maier C. M. and Chan P. H. (2003) Neurodegeneration in striatum induced by the mitochondrial toxin 3-nitropropionic acid: role of matrix metalloproteinase-9 in early blood-brain barrier disruption J. Neurosci. 23, 8733-8742.
29. Kouwenhoven M., Carlstrom C., Ozenci V. and Link H. (2001) Matrix metalloproteinase and cytokine profiles in monocytes over the course of stroke. J. Clin. Immunol. 21, 365-375.
30. Liu B., Hackshaw K. V. and Whisler R. L. (1996) Calcium signals and protein tyrosine kinases are required for the induction of c-jun in Jurkat cells stimulated by the T cell-receptor complex and oxidative signals. J. Interferon Cytokine Res. 16, 77-90.
31. Lohmann C., Krischke M., Wegener J. and Galla H. J. (2004) Tyrosine phosphatase inhibition induces loss of blood-brain barrier integrity by matrix metalloproteinase-dependent and -independent pathways. Brain Res. 995, 184-196.
32. Lu Y. and Wahl L. M. (2005) Oxidative stress augments the production of matrix metalloproteinase-1, cyclooxygenase-2, and prostaglandin E2 through enhancement of NF-kappa B activity in lipopolysaccharide-activated human primary monocytes. J. Immunol. 175, 5423-5429.
33. Lucchesi P. A., Sabri A., Belmadani S. and Matrougui K. (2004) Involvement of metalloproteinases 2/9 in epidermal growth factor receptor transactivation in pressure-induced myogenic tone in mouse mesenteric resistance arteries. Circulation 110, 3587-3593.
34. Machado L. S., Kozak A., Ergul A., Hess D. C., Borlongan C. V. and Fagan S. C. (2006) Delayed minocycline inhibits ischemia-activated matrix metalloproteinases 2 and 9 after experimental stroke. BMC Neurosci. 7, 56.
35. Matsumoto K., Minamitani T., Orba Y., Sato M., Sawa H. and Ariga H. (2004) Induction of matrix metalloproteinase-2 by tenascin-X deficiency is mediated through the c-Jun N-terminal kinase and protein tyrosine kinase phosphorylation pathway. Exp. Cell Res. 297, 404-414.
36. Meng T. C., Fukada T. and Tonks N. K. (2002) Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399.
37. Meyer T. N., Schwesinger C., Ye J., Denker B. M. and Nigam S. K. (2001) Reassembly of the tight junction after oxidative stress depends on tyrosine kinase activity. J. Biol. Chem. 276, 22 048-22 055.
38. Millan J., Williams L. and Ridley A. J. (2006) An in vitro model to study the role of endothelial rho GTPases during leukocyte transendothelial migration. Methods Enzymol. 406, 643-655.
39. Moosmann B. and Behl C. (2002) Antioxidants as treatment for neurodegenerative disorders. Expert Opin. Investig. Drugs 11, 1407-1435.
40. Morgan A. R., Rerkasem K., Gallagher P. J. et al. (2004) Differences in matrix metalloproteinase-1 and matrix metalloproteinase-12 transcript levels among carotid atherosclerotic plaques with different histopathological characteristics. Stroke 35, 1310-1315.
41. Morganti-Kossmann M. C., Rancan M., Stahel P. F. and Kossmann T. (2002) Inflammatory response in acute traumatic brain injury: a double-edged sword. Curr. Opin. Crit. Care 8, 101-105.
42. Mun-Bryce S. and Rosenberg G. A. (1998) Gelatinase B modulates selective opening of the blood-brain barrier during inflammation. Am. J. Physiol. 274, R1203-R1211.
43. Nakashima I., Kato M., Akhand A. A., Suzuki H., Takeda K., Hossain K. and Kawamoto Y. (2002) Redox-linked signal transduction pathways for protein tyrosine kinase activation. Antioxid. Redox Signal. 4, 517-531.
44. Nourshargh S., Krombach F. and Dejana E. (2006) The role of JAM-A and PECAM-1 in modulating leukocyte infiltration in inflamed and ischemic tissues. J. Leukoc. Biol. 80, 714-718.
45. Nyberg P., Heikkila P., Sorsa T., Luostarinen J., Heljasvaara R., Stenman U. H., Pihlajaniemi T. and Salo T. (2003) Endostatin inhibits human tongue carcinoma cell invasion and intravasation and blocks the activation of matrix metalloprotease-2, -9, and -13. J. Biol. Chem. 278, 22 404-22 411.
46. Opdenakker G., Nelissen I. and Van Damme J. (2003) Functional roles and therapeutic targeting of gelatinase B and chemokines in multiple sclerosis. Lancet Neurol. 2, 747-756.
47. Parathath S. R., Parathath S. and Tsirka S. E. (2006) Nitric oxide mediates neurodegeneration and breakdown of the blood-brain barrier in tPA-dependent excitotoxic injury in mice. J. Cell. Sci. 119, 339-349.
48. Pardridge W. M. (1983) Brain metabolism: a perspective from the bloodbrain barrier. Physiol. Rev. 63, 1481-1535.
49. Persidsky Y., Heilman D., Haorah J., Zelivyanskaya M., Persidsky R., Weber G. A., Shimokawa H., Kaibuchi K. and Ikezu T. (2006) Rho-mediated regulation of tight junctions during monocyte migration across the blood-brain barrier in HIV-1 encephalitis (HIVE). Blood 107, 4770-4780.
50. Poulet R., Gentile M. T., Vecchione C. et al. (2006) Acute hypertension induces oxidative stress in brain tissues. J. Cereb. Blood Flow Metab. 26, 253-262.
51. Rascher G., Fischmann A., Kroger S., Duffner F., Grote E. H. and Wolburg H. (2002) Extracellular matrix and the blood-brain barrier in glioblastoma multiforme: spatial segregation of tenascin and agrin. Acta Neuropathol. (Berl.) 104, 85-91.
52. Romanic A. M., White R. F., Arleth A. J., Ohlstein E. H. and Barone F. C. (1998) Matrix metalloproteinase expression increases after cerebral focal ischemia in rats: inhibition of matrix metalloproteinase-9 reduces infarct size. Stroke 29, 1020-1030.
53. Rosell A., Alvarez-Sabin J., Arenillas J. F., Rovira A., Delgado P., Fernandez-Cadenas I., Penalba A., Molina C. A. and Montaner J. (2005) 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 36, 1415-1420.
54. Rosell A., Ortega-Aznar A., Alvarez-Sabin J., Fernandez-Cadenas I., Ribo M., Molina C. A., Lo E. H. and Montaner J. (2006) Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 37, 1399-1406.
55. Rubin L. L. and Staddon J. M. (1999) The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22, 11-28.
56. Sanchez-del-Rio M. and Reuter U. (2004) Migraine aura: new information on underlying mechanisms. Curr. Opin. Neurol. 17, 289-293.
57. Schmidt A., Wenzel D., Thorey I., Werner S., Fleischmann B. K. and Bloch W. (2005) Endostatin down-regulates soluble guanylate cyclase (sGC) in endothelial cells in vivo: influence of endostatin on vascular endothelial growth factor (VEGF) signaling. Endothelium 12, 251-257.
58. Sluijter J. P., de Kleijn D. P. and Pasterkamp G. (2006) Vascular remodeling and protease inhibition-bench to bedside. Cardiovasc. Res. 69, 595-603.
59. Staddon J. M., Herrenknecht K., Smales C. and Rubin L. L. (1995) Evidence that tyrosine phosphorylation may increase tight junction permeability. J. Cell. Sci. 108, 609-619.
60. Tao Q., Spring S. C. and Terman B. I. (2005) Comparison of the signaling mechanisms by which VEGF, H2O2, and phosphatase inhibitors activate endothelial cell ERK1/2 MAP-kinase. Microvasc. Res. 69, 36-44.
61. Urbich C., Reissner A., Chavakis E., Dernbach E., Haendeler J., Fleming I., Zeiher A. M., Kaszkin M. and Dimmeler S. (2002) Dephosphorylation of endothelial nitric oxide synthase contributes to the anti-angiogenic effects of endostatin. FASEB J. 16, 706-708.
62. Valentin F., Bueb J. L., Kieffer P., Tschirhart E. and Atkinson J. (2005) Oxidative stress activates MMP-2 in cultured human coronary smooth muscle cells. Fundam. Clin. Pharmacol. 19, 661-667.
63. Vos C. M., Gartner S., Ransohoff R. M., McArthur J. C., Wahl L., Sjulson L., Hunter E. and Conant K. (2000) Matrix metalloprotease-9 release from monocytes increases as a function of differentiation: implications for neuroinflammation and neurodegeneration. J. Neuroimmunol. 109, 221-227.
64. Wang S., Lee S. R., Guo S. Z., Kim W. J., Montaner J., Wang X. and Lo E. H. (2006) Reduction of tissue plasminogen activator-induced matrix metalloproteinase-9 by simvastatin in astrocytes. Stroke 37, 1910-1912.
65. Whisler R. L., Newhouse Y. G., Beiqing L., Karanfilov B. K., Goyette M. A. and Hackshaw K. V. (1994) Regulation of protein kinase enzymatic activity in Jurkat T cells during oxidative stress uncoupled from protein tyrosine kinases: role of oxidative changes in protein kinase activation requirements and generation of second messengers. Lymphokine Cytokine Res. 13, 399-410.
66. Zalewska T., Ziemka-Nalecz M., Sarnowska A. and Domanska-Janik K. (2003) Transient forebrain ischemia modulates signal transduction from extracellular matrix in gerbil hippocampus. Brain Res. 977, 62-69.