Hyperglycaemia promotes cerebral barrier dysfunction through activation of protein kinase C-β

Diabetes, Obesity and Metabolism

Volumn 15, Issue 11, 2013, Pages 993-999

  Shao, B ^a   Bayraktutan, U ^a  

^a UNIVERSITY OF NOTTINGHAM   (United Kingdom)

Author keywords

Blood brain barrier; Hyperglycaemia; Occludin; Oxidative stress; Protein kinase C

Indexed keywords

APOCYNIN; GELATIN; GELATINASE A; GLUCOSE; OCCLUDIN; PROTEIN KINASE C BETA; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BLOOD BRAIN BARRIER; BLOOD BRAIN BARRIER DAMAGE; CENTRAL NERVOUS SYSTEM DISEASE; CONTROLLED STUDY; ELECTRIC RESISTANCE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; HYPERGLYCEMIA; IMMUNOBLOTTING; IN VITRO STUDY; MICROVASCULAR ENDOTHELIAL CELL; PROTEIN EXPRESSION; ZYMOGRAPHY;

BLOOD-BRAIN BARRIER; HYPERGLYCAEMIA; OCCLUDIN; OXIDATIVE STRESS; PROTEIN KINASE C;

ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN; CAPILLARY PERMEABILITY; CELLS, CULTURED; COCULTURE TECHNIQUES; DOWN-REGULATION; ELECTRIC IMPEDANCE; ENDOTHELIUM, VASCULAR; ENZYME ACTIVATION; HUMANS; HYPERGLYCEMIA; MATRIX METALLOPROTEINASE 2; MICROVESSELS; NADPH OXIDASE; OCCLUDIN; PERICYTES; PROTEIN KINASE C BETA; PROTEIN KINASE INHIBITORS; TIGHT JUNCTIONS;

EID: 84885299035     PISSN: 14628902     EISSN: 14631326     Source Type: Journal    
DOI: 10.1111/dom.12120     Document Type: Article

References (33)

1. Dejana E. Endothelial cell-cell junctions: happy together. Nat Rev Mol Cell Biol 2004; 5: 261-270.
2. Furuse M, Sasaki H, Fujimoto K, Tsukita S. A single gene product, claudin-1 or -2, reconstitutes tight junction strands and recruits occludin in fibroblasts. J Cell Biol 1998; 143: 391-401.
3. Baird TA, Parsons MW, Barber PA et al. The influence of diabetes mellitus and hyperglycaemia on stroke incidence and outcome. J Clin Neurosci 2002; 9: 618-626.
4. Bayraktutan U. Free radicals, diabetes and endothelial dysfunction. Diabetes Obes Metab 2002; 4: 224-238.
5. Inoguchi T, Battan R, Handler E, Sportsman JR, Heath W, King GL. Preferential elevation of protein kinase C isoform beta II and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc Natl Acad Sci USA 1992; 89: 11059-11063.
6. Shiba T, Inoguchi T, Sportsman JR, Heath WF, Bursell S, King GL. Correlation of diacylglycerol level and protein kinase C activity in rat retina to retinal circulation. Am J Physiol 1993; 265: E783-E793.
7. Aiello LP, Clermont A, Arora V, Davis MD, Sheetz MJ, Bursell SE. Inhibition of PKC beta by oral administration of ruboxistaurin is well tolerated and ameliorates diabetes-induced retinal hemodynamic abnormalities in patients. Invest Ophthalmol Vis Sci 2006; 47: 86-92.
8. Kelly DJ, Zhang Y, Hepper C et al. Protein kinase C beta inhibition attenuates the progression of experimental diabetic nephropathy in the presence of continued hypertension. Diabetes 2003; 52: 512-518.
9. Allen CL, Bayraktutan U. Antioxidants attenuate hyperglycaemia-mediated brain endothelial cell dysfunction and blood-brain barrier hyperpermeability. Diabetes Obes Metab 2009; 11: 480-490.
10. Inoguchi T, Li P, Umeda F et al. High glucose level and free fatty acid stimulate reactive oxygen species production through protein kinase C-dependent activation of NAD(P)H oxidase in cultured vascular cells. Diabetes 2000; 49: 1939-1945.
11. Li L, Mamputu JC, Wiernsperger N, Renier G. Signaling pathways involved in human vascular smooth muscle cell proliferation and matrix metalloproteinase-2 expression induced by leptin: inhibitory effect of metformin. Diabetes 2005; 54: 2227-2234.
12. Yang Y, Estrada EY, Thompson JF, Liu W, Rosenberg GA. Matrix metalloproteinase-mediated disruption of tight junction proteins in cerebral vessels is reversed by synthetic matrix metalloproteinase inhibitor in focal ischemia in rat. J Cereb Blood Flow Metab 2007; 27: 697-709.
13. Yang Y, Rosenberg GA. MMP-mediated disruption of claudin-5 in the blood-brain barrier of rat brain after cerebral ischemia. Methods Mol Biol 2011; 762: 333-345.
14. Rosell A, Ortega-Aznar A, Alvarez-Sabín J et al. Increased brain expression of matrix metalloproteinase-9 after ischemic and hemorrhagic human stroke. Stroke 2006; 37: 1399-1406.
15. Allen C, Srivastava K, Bayraktutan U. Small GTPase RhoA and its effector rho kinase mediate oxygen glucose deprivation-evoked in vitro cerebral barrier dysfunction. Stroke 2010; 41: 2056-2063.
16. Birchall AM, Bishop J, Bradshaw D et al. Ro 32-0432, a selective and orally active inhibitor of protein kinase C prevents T-cell activation. J Pharmacol Exp Ther 1994; 268: 922-929.
17. Davies SP, Reddy H, Caivano M, Cohen P. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem J 2000; 351: 95-105.
18. Park JY, Takahara N, Gabriele A et al. Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes 2000; 49: 1239-1248.
19. Cipolla MJ, Huang Q, Sweet JG. Inhibition of protein kinase C β reverses increased blood-brain barrier permeability during hyperglycemic stroke and prevents edema formation in vivo. Stroke 2011; 42: 3252-3257.
20. Kowluru RA. Diabetes-induced elevations in retinal oxidative stress, protein kinase C and nitric oxide are interrelated. Acta Diabetol 2001; 38: 179-185.
21. Fujita T, Asai T, Andrassy M et al. PKCbeta regulates ischemia/reperfusion injury in the lung. J Clin Invest 2004; 113: 1615-1623.
22. Kunt T, Forst T, Kazda C et al. The beta-specific protein kinase C inhibitor ruboxistaurin (LY333531) suppresses glucose-induced adhesion of human monocytes to endothelial cells in vitro. J Diabetes Sci Technol 2007; 1: 929-935.
23. Nonaka A, Kiryu J, Tsujikawa A et al. PKC-beta inhibitor (LY333531) attenuates leukocyte entrapment in retinal microcirculation of diabetic rats. Invest Ophthalmol Vis Sci 2000; 41: 2702-2706.
24. Martini SR, Kent TA. Hyperglycemia in acute ischemic stroke: a vascular perspective. J Cereb Blood Flow Metab 2007; 27: 435-451.
25. Kusaka I, Kusaka G, Zhou C et al. Role of AT1 receptors and NAD(P)H oxidase in diabetes-aggravated ischemic brain injury. Am J Physiol Heart Circ Physiol 2004; 286: H2442-H2451.
26. Bayraktutan U. Nitric oxide synthase and NAD(P)H oxidase modulate coronary endothelial cell growth. J Mol Cell Cardiol 2004; 36: 277-286.
27. Fontayne A, Dang PM, Gougerot-Pocidalo MA, El-Benna J. Phosphorylation of p47phox sites by PKC alpha, beta II, delta, and zeta: effect on binding to p22phox and on NADPH oxidase activation. Biochemistry 2002; 41: 7743-7750.
28. Raad H, Paclet MH, Boussetta T et al. Regulation of the phagocyte NADPH oxidase activity: phosphorylation of gp91phox/NOX2 by protein kinase C enhances its diaphorase activity and binding to Rac2, p67phox, and p47phox. FASEB J 2009; 23: 1011-1022.
29. Gopalakrishna R, Jaken S. Protein kinase C signaling and oxidative stress. Free Radic Biol Med 2000; 28: 1349-1361.
30. Kamada H, Yu F, Nito C, Chan PH. Influence of hyperglycemia on oxidative stress and matrix metalloproteinase-9 activation after focal cerebral ischemia/reperfusion in rats: relation to blood-brain barrier dysfunction. Stroke 2007; 38: 1044-1049.
31. Wang HH, Hsieh HL, Wu CY, Yang CM. Oxidized low-density lipoprotein-induced matrix metalloproteinase-9 expression via PKC-delta/p42/p44 MAPK/Elk-1 cascade in brain astrocytes. Neurotox Res 2010; 17: 50-65.
32. Hawkins BT, Lundeen TF, Norwood KM, Brooks HL, Egleton RD. Increased blood-brain barrier permeability and altered tight junctions in experimental diabetes in the rat: contribution of hyperglycaemia and matrix metalloproteinases. Diabetologia 2007; 50: 202-211.
33. Kim JH, Jun HO, Yu YS, Kim KW. Inhibition of protein kinase C delta attenuates blood-retinal barrier breakdown in diabetic retinopathy. Am J Pathol 2010; 176: 1517-1524.