Protein kinase C activation modulates reversible increase in cortical blood-brain barrier permeability and tight junction protein expression during hypoxia and posthypoxic reoxygenation

Journal of Cerebral Blood Flow and Metabolism

Volumn 30, Issue 11, 2010, Pages 1847-1859

  Willis, Colin L ^a   Meske, Diana S ^a   Davis, Thomas P ^a  

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

Author keywords

blood brain barrier; ischemia; protein kinase C; tight junction; vascular permeability

Indexed keywords

CHELERYTHRINE; CLAUDIN 5; FLUORESCEIN ISOTHIOCYANATE DEXTRAN; IMMUNOGLOBULIN G; ISOENZYME; MEMBRANE PROTEIN; OCCLUDIN; OXYGEN; PROTEIN KINASE C; PROTEIN ZO1; TIGHT JUNCTION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN CORTEX; BRAIN HYPOXIA; CELL DISRUPTION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; FEMALE; HIPPOCAMPUS; MICROVASCULATURE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REOXYGENATION; SIGNAL TRANSDUCTION; TIGHT JUNCTION; WESTERN BLOTTING;

ANIMALS; ANOXIA; BENZOPHENANTHRIDINES; BLOOD-BRAIN BARRIER; CEREBRAL CORTEX; ENDOTHELIAL CELLS; ENZYME ACTIVATION; FEMALE; ISOENZYMES; MICROVESSELS; NERVE TISSUE PROTEINS; OXYGEN; PERMEABILITY; PROTEIN KINASE C; RATS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TIGHT JUNCTIONS; TIME FACTORS;

EID: 78049452265     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2010.119     Document Type: Article

References (40)

1. Andreeva AY, Krause E, Muller EC, Blasig IE, Utepbergen-ov DI (2001) Protein kinase C regulates the phosphor-ylation and cellular localization of occludin. J Biol Chem 276:38480-6
2. Angelow S, Zeni P, Hohn B, Galla H-J (2005) Phorbol ester induced short-and long-term permeabilization of blood-CSF barrier in vitro. Brain Res 1063:168-79
3. Avila-Flores A, Rendon-Huerta E, Moreno J, Islas S, Betanzos A, Robles-Flores M, Gonzalez-Mariscal L (2001) Tight-junction protein zonula occludens 2 is a target of phosphorylation by protein kinase C. Biochem J 360:295-304
4. Banan A, Fields JZ, Zhang LJ, Shaikh M, Farhadi A, Keshavarzian A (2003) The atypical zeta (z) isoform of protein kinase C prevents oxidant-induced NF-kB activation in the intestinal epithelium. J Pharmacol Exp Ther 307:53-66
5. Banan A, Zhang LJ, Fields JZ, Shaikh M, Farhadi A, Keshavarzian A (2004) Theta (y) isoform of PKC is required for alterations in microtubule cytoskeletal dynamics in intestinal epithelium: a novel function for PKC-y. Am J Physiol 287:C218-34
6. Banan A, Zhang LJ, Shaikh M, Fields JZ, Choudhary S, Forsyth CB, Farhadi A, Keshavarzian A (2007) y Isoform of protein kinase C alters barrier function in intestinal epithelium through modulation of distinct claudin isotypes: a novel mechanism for regulation of permeability. J Pharmacol Exp Ther 313:962-82
7. Banks WA (2009) Mouse models of neurological disorders: a view from the blood-brain barrier. Biochem Biophysia Acta (in press)
8. Brooks TA, Hawkins BT, Huber JD, Egleton RD, Davis TP (2005) Chronic inflammatory pain leads to increased blood-brain barrier permeability and tight junction protein alterations. Am J Physiol Heart Circ Physiol 289:H738-43
9. Butt AM, Jones HC, Abbott NJ (1990) Electrical-resistance across the blood-brain-barrier in anesthetized rats\-a developmental study. J Physiol 429:47-62
10. Dodane V, Kachar B (1996) Identification of isoforms of G proteins and PKC that colocalize with tight junctions. J Membr Biol 149:199-209
11. Fleegal MA, Hom S, Borg LK, Davis TP (2005) Activation of PKC modulates blood-brain barrier endothelial cell permeability changes induced by hypoxia and posthypoxic reoxygenation. Am J Physiol Heart Circ Physiol 289:2012-9
12. Furuse M, Fujita K, Hiiragi T, Fujimoto K, Tsukita S (1998) Claudin-1 and-2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin. J Cell Biol 141:1539-50
13. Furuse M, Hirase T, Itoh M, Nagafuchi A, Yonemura S, Tsukita S, Tsukita S (1993) Occludin\-a novel integral membrane-protein localizing at tight junctions. J Cell Biol 123:1777-88
14. Gonzalez-Mariscal L, Tapia R, Chamorro D (2008) Crosstalk of tight junction components with signalling pathways. Biochimica et Biophysica Acta 1778:729-56
15. Gopalakrishna R, Jaken S (2000) Protein kinase C signaling and oxidative stress. Free Rad Biol Med 28:1349-61
16. Herbert JM, Augereau JM, Gleye J, Maffrand JP (1990) Chelerythrine is a potent and specific inhibitor of protein kinase C. Biochem Biophys Res Comm 172:993-9
17. Himeda T, Hayakawa N, Tounai H, Sakuma M, Kato H, Araki T (2005) Alterations of interneurons of the gerbil hippocampus after transient cerebral ischemia: effect of pitavastatin. Neuropsychopharmacology 30: 2014-25
18. Hirase T, Staddon JM, Saitou M, Ando Akatsuka Y, Itoh M, Furuse M, Fujimoto K, Tsukita S, Rubin LL (1997) Occludin as a possible determinant of tight junction permeability in endothelial cells. J Cell Sci 110:1603-13
19. Kim J-H, Kim JH, Jun H-O, Yu YS, Kim K-W (2010a) Inhibition of protein kinase C d attenuates blood-retinal barrier breakdown in diabetic retinopathy. Am J Pathol 176:1517-24
20. Kim Y-A, Park SL, Kim M-Y, Lee SH, Baik EJ, Moon C-H, Jung Y-S (2010b) Role of PKCbII and PKCd in blood-brain barrier permeability during aglycemic hypoxia. Neurosci Letts 468:254-8
21. Mark KS, Davis TP (2002) Cerebral microvascular changes in permeability and tight junctions induced by hypoxia-reoxygenation. Am J Physiol Heart Circ Physiol 282: H1485-94
22. 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 (1998) Junctional adhesion molecule, a novel member of the immunoglo-bulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J Cell Biol 142:117-27
23. McCaffrey G, Willis CL, Staatz WD, Nametz N, Quigley CA, Hom S, Lochhead JJ, Davis TP (2009) Occludin oligomeric assembly at tight junctions of the blood-brain barrier are altered by hypoxia and reoxygenation. J Neurochem 110:58-71
24. Miettinen S, Roivainen R, Keinanen R, Hokfelt T, Koisti-naho J (1996) Specific induction of protein kinase C delta subspecies after transient middle cerebral artery occlusion in the rat brain: inhibition by MK-801. J Neurosci 16:6236-45
25. Petty MA, Lo EH (2002) Junctional complexes of the blood-brain barrier: permeability changes in neuroinflamma-tion. Prog Neurobiol 68:311-23
26. Ping P, Takano H, Zhang J, Tang X-L, Qiu Y, Li RCX, Banerjee S, Dawn B, Balafonova Z, Bolli R (1999) Isoform-selective activation of protein kinase C by nitric oxide in the heart of conscious rabbits: a signaling mechanism for both nitric oxide-induced and ischemia-induced preconditioning. Circ Res 84:587-604
27. Pulsinelli WA, Brierley JB, Plum F (1982) Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol 11:491-8
28. Rao RK, Basuroy S, Rao VU, Karnaky Jr KJ, Gupta A (2002) Tyrosine phosphorylation and dissociation of occludin-ZO-1 and E-cadherin-beta-catenin complexes from the cytoskeleton by oxidative stress. Biochem J 368:471-81
29. Ron D, Kazanietz MG (1999) New insights into the regulation of protein kinase C and novel phorbol ester receptors. FASEB J 13:1658-76
30. Schechtman D, Mochly-Rosen D (2001) Adaptor proteins in protein kinase C-mediated signal transduction. Oncogene 20:6339-47
31. Singhal AB, Wang X, Sumii T, Mori T, Lo EH (2002) Effects of normobaric hyperoxia in a rat model of focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 22:861-8
32. Steinberg SF (2008) Structural basis of protein kinase C isoform function. Physiol Rev 88:1341-78
33. Tamai I, Tsuji A (2000) Transporter-mediated permeation of drugs across the blood-brain barrier. J Pharm Sci 89: 1371-88
34. Willis CL, Leach L, Clarke GJ, Nolan CC, Ray DE (2004) Reversible disruption of tight junction complexes in the rat blood-brain barrier, following transitory focal astro-cyte loss. Glia 48:1-13
35. Witt KA, Mark KS, Hom S, Davis TP (2003) Effects of hypoxia-reoxygenation on rat blood-brain barrier permeability and tight junctional protein expression. Am J Physiol Heart Circ Physiol 285:H2820-31
36. Witt KA, Mark KS, Huber J, Davis TP (2005) Hypoxia-inducible factor and nuclear factor kappa-B activation in blood-brain barrier endothelium under hypoxic/ reoxygenation stress. J Neurochem 92:203-14
37. Witt KA, Mark KS, Sandoval KE, Davis TP (2008) Reoxygenation stress on blood-brain barrier paracellular permeability and edema in the rat. Microvascular Res 75:91-6
38. Yang T, Roder KE, Bhat GJ, Thekkumkara TJ, Abbruscato TJ (2006) Protein kinase C family members as a target for regulation of blood-brain barrier Na,K,2Cl-cotransporter during in vitro stroke conditions and nicotine exposure. Pharm Res 23:291-302
39. Yuan L, Seo J-S, Kang NS, Keinan S, Steele SE, Michelotti GA, Wetsel WC, Beratan DN, Gong Y-D, Lee TH, Hong J (2009) Identification of 3-hydroxy-2-(3-hydroxyphe-nyl)-4H-1-benzopyran-4-ones as isoform-selective PKC-z inhibitors and potential therapeutics for psychostimu-lant abuse. Mol BioSyst 5:927-30
40. Yuan SY (2002) Protein kinase signaling in the modulation of microvascular permeability. Vascul Pharmacol 39: 213-23