Hypoxia/aglycemia alters expression of occludin and actin in brain endothelial cells

Biochemical and Biophysical Research Communications

Volumn 327, Issue 4, 2005, Pages 1114-1123

  Brown, Rachel C ^a   Davis, Thomas P ^b  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Actin; Blood brain barrier; Hypoxic stress; Occludin; SKF 96365; Tight junction; ZO 1

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; ACTIN; CALCIUM CHANNEL BLOCKING AGENT; OCCLUDIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BRAIN CELL; CALCIUM TRANSPORT; CONTROLLED STUDY; CORRELATION ANALYSIS; ELECTRIC RESISTANCE; ENDOTHELIUM CELL; GLUCOSE BLOOD LEVEL; HYPOXIA; IN VITRO STUDY; MEMBRANE PERMEABILITY; MONOLAYER CULTURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STROKE; TIGHT JUNCTION;

ACTINS; ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CATTLE; CELL HYPOXIA; CELLS, CULTURED; CYTOSKELETON; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GLUCOSE; MEMBRANE PROTEINS; PHOSPHOPROTEINS; TIGHT JUNCTIONS;

EID: 12444249974     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2004.12.123     Document Type: Article

References (83)

1. D. Choi Ischemia-induced neuronal apoptosis Curr. Opin. Neurobiol. 6 1996 667 672
2. T. Broman Supravital analysis of disorders in the cerebrovascular permeability Acta Psyciatr. 25 1950 19 31
3. T. Broman, and A. Lindberg-Broman An experimental study of disorders in the permeability of the cerebral vessels ("the blood-brain barrier") produced by chemical and physico-chemical agents Acta Physiol. Scand. 10 1945 102 125
4. R. Goodale, B. Goetzman, and M. Visscher Hypoxia and iodacetic acid and alveolocapillary barrier permeability to albumin Am. J. Physiol. 219 1970 1226 1230
5. K.S. Mark, and T.P. Davis Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation Am. J. Physiol. Heart Circ. Physiol. 282 2002 H1485 H1494
6. R.C. Brown, K.S. Mark, R.D. Egleton, J.D. Huber, A. Burroughs, and T.P. Davis Protection against hypoxia-induced increase in blood-brain barrier permeability: role of tight junction proteins and NFκB J. Cell Sci. 116 Pt. 4 2003 693 700
7. T.J. Abbruscato, and T.P. Davis Combination of hypoxia/aglycemia compromises in vitro blood-brain barrier integrity J. Pharmacol. Exp. Ther. 289 1999 668 675
8. R.C. Brown, K.S. Mark, R.D. Egleton, and T.P. Davis Protection against hypoxia-induced blood-brain barrier disruption: changes in intracellular calcium Am. J. Physiol. Cell Physiol. 286 2004 C1045 C1052
9. J.D. Huber, R.D. Egleton, and T.P. Davis Molecular physiology and pathophysiology of tight junctions in the blood-brain barrier Trends Neurosci. 24 2001 719 725
10. M. Furuse, K. Fujita, T. Hiiragi, K. Fujimoto, and S. Tsukita Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin J. Cell Biol. 141 1998 1539 1550
11. M. Furuse, H. Sasaki, K. Fujimoto, and S. Tsukita A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts J. Cell Biol. 143 1998 391 401
12. S. Liebner, A. Fischmann, G. Rascher, F. Duffner, E.H. Grote, H. Kalbacher, and H. Wolburg Claudin-1 and claudin-5 expression and tight junction morphology are altered in blood vessels of human glioblastoma multiforme Acta Neuropathol. (Berl.) 100 2000 323 331
13. A. Lippoldt, U. Kniesel, S. Liebner, H. Kalbacher, T. Kirsch, H. Wolburg, and H. Haller Structural alterations of tight junctions are associated with loss of polarity in stroke-prone spontaneously hypertensive rat blood-brain barrier endothelial cells Brain Res. 885 2000 251 261
14. T. Hirase, J.M. Staddon, M. Saitou, Y. Ando-Akatsuka, M. Itoh, M. Furuse, K. Fujimoto, S. Tsukita, and L.L. Rubin Occludin as a possible determinant of tight junction permeability in endothelial cells J. Cell Sci. 110 1997 1603 1613
15. M. Saitou, K. Fujimoto, Y. Doi, M. Itoh, T. Fujimoto, M. Furuse, H. Takano, T. Noda, and S. Tsukita Occludin-deficient embryonic stem cells can differentiate into polarized epithelial cells bearing tight junctions J. Cell Biol. 141 1998 397 408
16. J.M. Anderson, A.S. Fanning, L. Lapierre, and C.M. Van Itallie Zonula occludens (ZO)-1 and ZO-2: membrane-associated guanylate kinase homologues (MAGUKs) of the tight junction Biochem. Soc. Trans. 23 1995 470 475
17. J. Haskins, L. Gu, E.S. Wittchen, J. Hibbard, and B.R. Stevenson ZO-3, a novel member of the MAGUK protein family found at the tight junction, interacts with ZO-1 and occludin J. Cell Biol. 141 1998 199 208
18. M. Beatch, L.A. Jesaitis, W.J. Gallin, D.A. Goodenough, and B.R. Stevenson The tight junction protein ZO-2 contains three PDZ (Psd-95/Discs-large/ZO-1) domains and an alternatively spliced region J. Biol. Chem. 271 1996 25723 25726
19. M. Reichert, T. Muller, and W. Hunziker The PDZ domains of zonula occludens-1 induce an epithelial to mesenchymal transition of Madin-Darby canine kidney cells. Evidence for a role of beta-catenin/Tcf/Lef signaling J. Biol. Chem. 275 2000 9492 9500
20. A.S. Fanning, B.J. Jameson, L.A. Jesaitis, and J.M. Anderson The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton J. Biol. Chem. 273 1998 29745 29753
21. M. Itoh, M. Furuse, K. Morita, K. Kubota, M. Saitou, and S. Tsukita 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 1999 1351 1363
22. A.S. Yap, W.M. Brieher, and B.M. Gumbiner Molecular and functional analysis of cadherin-based adherens junctions Annu. Rev. Cell Dev. Biol. 13 1997 119 146
23. A. Avila-Flores, E. Rendon-Huerta, J. Moreno, S. Islas, A. Betanzos, M. Robles-Flores, and L. Gonzalez-Mariscal Tight-junction protein zonula occludens 2 is a target of phosphorylation by protein kinase C Biochem. J. 260 2001 295 304
24. G. Kale, A. Naren, P. Sheth, and R. Rao Tyrosine phosphorylation of occludin attenuates its interactions with ZO-1, ZO-2 and ZO-3 Biochem. Biophys. Res. Commun. 302 2003 324 329
25. S.K. Nigam, N. Denisenko, E. Rodriguez-Boulan, and S. Citi The role of phosphorylation in development of tight junctions in cultured renal epithelial (MDCK) cells Biochem. Biophys. Res. Commun. 181 1991 548 553
26. J.M. Staddon, K. Herrenknecht, C. Smales, and L.L. Rubin Evidence that tyrosine phosphorylation may increase tight junction permeability J. Cell Sci. 108 1995 609 619
27. T. Tsukamoto, and S.K. Nigam Role of tyrosine phosphorylation in the reassembly of occludin and other tight junction proteins Am. J. Physiol. 276 1999 F737 F750
28. V. Wong Phosphorylation of occludin correlates with occludin localization and function at the tight junction Am. J. Physiol. 273 1997 C1859 C1867
29. R.C. Brown, and T.P. Davis Calcium modulation of adherens and tight junction function: a potential mechanism for blood-brain barrier disruption after stroke Stroke 33 2002 1706 1711
30. L. Gonzalez-Mariscal, R.G. Contreras, J.J. Bolivar, A. Ponce, B. Chavez De amirez, and M. Cereijido Role of calcium in tight junction formation between epithelial cells Am. J. Physiol. 259 1990 C978 C986
31. 2+ in modulation of tight junction resistance in A6 cells Am. J. Physiol. 266 1994 F775 F784
32. 2+: a protein kinase C effect J. Membr. Biol. 149 1996 71 79
33. J. Ye, T. Tsukamoto, A. Sun, and S.K. Nigam A role for intracellular calcium in tight junction reassembly after ATP depletion-repletion Am. J. Physiol. Renal Physiol. 277 1999 F524 F532
34. K.L. Audus, and R.T. Borchardt Characterization of an in vitro blood-brain barrier model system for studying drug transport and metabolism Pharmacol. Res. 3 1986 81 87
35. E.A. Brownson, T.J. Abbruscato, T.J. Gillespie, V.J. Hruby, and T.P. Davis Effect of peptidases at the blood brain barrier on the permeability of enkephalin J. Pharmacol. Exp. Ther. 270 1994 675 680
36. S.J. Weber, T.J. Abbruscato, E.A. Brownson, A.W. Lipkowski, R. Polt, A. Misicka, R.C. Haaseth, H. Bartosz, V.J. Hruby, and T.P. Davis Assessment of an in vitro blood-brain barrier model using several [met5]enkephalin opioid analogs J. Pharmacol. Exp. Ther. 266 1993 1649 1655
37. T.P. Davis, T.J. Abbruscato, E. Brownson, and V.J. Hruby Conformationally constrained peptide drugs targeted at the blood-brain barrier NIDA Res. Monogr. 154 1995 47 60
38. A. Nusrat, J.A. Chen, C.S. Foley, T.W. Liang, J. Tom, M. Cromwell, C. Quan, and R.J. Mrsny The coiled-coil domain of occludin can act to organize structural and functional elements of the epithelial tight junction J. Biol. Chem. 275 2000 29816 29822
39. R.O. Stuart, and S.K. Nigam Regulated assembly of tight junctions by protein kinase C Proc. Natl. Acad. Sci. USA 92 1995 6072 6076
40. K.S. Mark, W.J. Trickler, and D.W. Miller Tumor necrosis factor-alpha induces cyclooxygenase-2 expression and prostaglandin release in brain microvessel endothelial cells J. Pharmacol. Exp. Ther. 297 2001 1051 1058
41. A.D. Mooradian Blood-brain barrier choline transport is reduced in diabetic rats Diabetes 36 1987 1094 1097
42. C.P. Hawkins, F. Mackenzie, P. Tofts, E.P. du Boulay, and W.I. McDonald Patterns of blood-brain barrier breakdown in inflammatory demyelination Brain Res. 114 1991 801 810
43. L.A. Stone, M.E. Smith, P.S. Albert, C.N. Bash, H. Maloni, J.A. Frank, and H.F. McFarland Blood-brain barrier disruption on contrast-enhanced MRI in patients with mild relapsing-remitting multiple sclerosis: relationship to course, gender, and age Neurology 45 1995 1122 1126
44. A.D. Mooradian Central nervous system complications of diabetes mellitus-a perspective from the blood-brain barrier Brain Res. Brain Res. Rev. 23 1997 210 218
45. J.D. Huber, K.A. Witt, S. Hom, R.D. Egleton, K.S. Mark, and T.P. Davis Inflammatory pain alters blood-brain barrier permeability and tight junctional protein expression Am. J. Physiol. Heart Circ. Physiol. 280 2001 H1241 H1248
46. V.H. Perry, D.C. Anthony, S.J. Bolton, and H.C. Brown The blood-brain barrier and the inflammatory response Mol. Med. Today 3 1997 335 341
47. A.A. Webb, and G.D. Muir The blood-brain barrier and its role in inflammation J. Vet. Intern. Med. 14 2000 399 411
48. C. Abraham, N. Harada, M. Deli, and M. Niwa Transient forebrain ischemia increases the blood-brain barrier permeability for albumin in stroke-prone spontaneously hypertensive rats Cell. Mol. Neurobiol. 22 2002 455 462
49. S. Albayrak, Q. Zhao, B.K. Siesjo, and M.L. Smith Effect of transient focal ischemia on blood-brain barrier permeability in the rat: correlation to cell injury Acta Neuropathol. (Berl.) 94 1997 158 163
50. A.L. Betz, R.F. Keep, M.E. Beer, and X.D. Ren Blood-brain barrier permeability and brain concentration of sodium, potassium, and chloride during focal ischemia J. Cereb. Blood Flow Metab. 14 1994 29 37
51. S. Fischer, M. Wobben, H.H. Marti, D. Renz, and W. Schaper Hypoxia-induced hyperpermeability in brain microvessel endothelial cells involves VEGF-mediated changes in the expression of zonula occludens-1 Microvasc. Res. 63 2002 70 80
52. J.H. Park, N. Okayama, D. Gute, A. Krsmanovic, H. Battarbee, and J.S. Alexander Hypoxia/aglycemia increases endothelial permeability: role of second messengers and cytoskeleton Am. J. Physiol. Cell Physiol. 277 1999 C1066 C1074
53. S.J. Bolton, D.C. Anthony, and V.H. Perry Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo Neuroscience 86 1998 1245 1257
54. J.D. Huber, V.S. Hau, K.S. Mark, R.C. Brown, C.R. Campos, and T.P. Davis Viability of microvascular endothelial cells to direct exposure of formalin, lambda-carrageenan, and complete Freund's adjuvant Eur. J. Pharmacol. 450 2002 297 304
55. P. Farshori, and B. Kachar Redistribution and phosphorylation of occludin during opening and resealing of tight junctions in cultured epithelial cells J. Membr. Biol. 170 1999 147 156
56. U. Kayyali, C. Pennella, C. Trujillo, O. Villa, M. Gaestel, and P. Hassoun Cytoskeletal changes in hypoxic pulmonary endothelial cells are dependent on MAPK-activated protein kinase MK2 J. Biol. Chem. 277 2002 42596 42602
57. C.E. Patterson, H. Lum, K.L. Schaphorst, A.D. Verin, and J.G. Garcia Regulation of endothelial barrier function by the cAMP-dependent protein kinase Endothelium 7 2000 287 308
58. T. Sutton, H. Mang, and S. Atkinson Rho-kinase regulates myosin II activation in MDCK cells during recovery after ATP depletion Am. J. Physiol. Renal Physiol. 281 2001 F810 F818
59. T. Volberg, B. Geiger, S. Citi, and A.D. Bershadsky Effect of protein kinase inhibitor H-7 on the contractility, integrity, and membrane anchorage of the microfilament system Cell Motil. Cytoskeleton 29 1994 321 338
60. A. Andreeva, E. Krause, E. Muller, I.E. Blasig, and D. Utepbergenov Protein kinase C regulates the phosphorylation and cellular localization of occludin J. Biol. Chem. 276 2001 38480 38486
61. T. Ishizaki, H. Chiba, T. Kojima, M. Fujibe, T. Soma, H. Miyajima, K. Nagasawa, I. Wada, and N. Sawada Cyclic AMP induces phosphorylation of claudin-5 immunoprecipitates and expression of claudin-5 gene in blood-brain barrier endothelial cells via protein kinase A-dependent and -independent pathways Exp. Cell Res. 290 2003 275 288
62. P. Sheth, S. Basuroy, C. Li, A. Naren, and R. Rao Role of phosphatidylinositol 3-kinase in oxidative stress-induced disruption of tight junctions J. Biol. Chem. 278 2003 49239 49245
63. Y. Chen, Q. Lu, E.E. Schneeberger, and D.A. Goodenough Restoration of tight junction structure and barrier function by down-regulation of the mitogen-activated protein kinase pathway in Ras-transformed Madin-Darby canine kidney cells Mol. Biol. Cell 11 2000 849 862
64. M. Itoh, K. Morita, and S. Tsukita Characterization of ZO-2 as a MAGUK family member associated with tight as well as adherens junctions with a binding affinity to occludin and alpha catenin J. Biol. Chem. 274 1999 5981 5986
65. M. Itoh, A. Nagafuchi, S. Moroi, and S. Tsukita Involvement of ZO-1 in cadherin-based cell adhesion through its direct binding to alpha catenin and actin filaments J. Cell Biol. 138 1997 181 192
66. J. Mankertz, S. Tavalali, H. Schmitz, A. Mankertz, E.O. Riecken, M. Fromm, and J.D. Schulzke Expression from the human occludin promoter is affected by tumor necrosis factor alpha and interferon gamma J. Cell Sci. 113 2000 2085 2090
67. J. Mankertz, J.S. Waller, B. Hillenbrand, S. Tavalali, P. Florian, T. Schoneberg, M. Fromm, and J.D. Schulzke Gene expression of the tight junction protein occludin includes differential splicing and alternative promoter usage Biochem. Biophys. Res. Commun. 298 2002 657 666
68. J. Ikenouchi, M. Matsuda, M. Furuse, and S. Tsukita Regulation of tight junctions during the epithelium-mesenchyme transition: direct repression of the gene expression of claudins/occludin by Snail J. Cell Sci. 116 2003 1959 1967
69. T. Ohkubo, and M. Ozawa The transcription factor snail downregulates the tight junction components independently of E-cadherin downregulation J. Cell Sci. 117 2004 1675 1685
70. G.L. Semenza, F. Agani, G. Booth, J. Forsythe, N. Iyer, B.H. Jiang, S. Leung, R. Roe, C. Wiener, and A. Yu Structural and functional analysis of hypoxia-inducible factor 1 Kidney Int. 51 1997 553 555
71. M. Bergeron, A.Y. Yu, K.E. Solway, G.L. Semenza, and F.R. Sharp Induction of hypoxia-inducible factor-1 (HIF-1) and its target genes following focal ischaemia in rat brain Eur. J. Neurosci. 11 1999 4159 4170
72. J. Nedelcu, M.A. Klein, A. Aguzzi, P. Boesiger, and E. Martin Biphasic edema after hypoxic-ischemic brain injury in neonatal rats reflects early neuronal and late glial damage Pediatr. Res. 46 1999 297 304
73. G.Y. Yang, and A.L. Betz Reperfusion-induced injury to the blood-brain barrier after middle cerebral artery occlusion in rats Stroke 25 1994 1658 1664 (Discussion 1664-1655)
74. A. Easton, and N. Abbott Bradykinin increases permeability by calcium and 5-lipoxygenase in the ECV304/C6 cell culture model of the blood-brain barrier Brain Res. 953 2002 157 169
75. 2+ concentration without production of nitric oxide and von Willebrand factor Cell Calcium 20 1996 501 508
76. 2+ entry Naunyn Schmiedebergs Arch. Pharmacol. 359 1999 92 101
77. Y. Leung, C. Kwan, and T. Loh Dual effects of SK&F 96365 in human leukemic HL-60 cells Biochem. Pharmacol. 51 1996 605 612
78. S. Li, Q. Jiang, and P.K. Stys Important role of reverse Na(+)-Ca(2+) exchange in spinal cord white matter injury at physiological temperature J. Neurophysiol. 84 2000 1116 1119
79. D. Guerini The significance of the isoforms of plasma membrane calcium ATPase Cell Tissue Res. 292 1998 191 197
80. 2+ entry in human pulmonary artery endothelial cells Am. J. Physiol. Lung Cell. Mol. Physiol. 285 2003 L1233 L1245
81. D.S. Bredt Endogenous nitric oxide synthesis: Biological functions and pathophysiology Free Radic. Res. 31 1999 577 596
82. I. Fleming, and R. Busse Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase Am. J. Physiol. Regul. Integr. Comp. Physiol. 284 2003 R1 R12
83. K.S. Mark, A. Burroughs, R.C. Brown, J.D. Huber, and T.P. Davis Nitric oxide mediates hypoxia-induced changes in paracellular permeability of cerebral microvasculature Am. J. Physiol. Heart Circ. Physiol. 286 2004 H174 H180