Role of protein kinase C in diabetic complications

Expert Review of Endocrinology and Metabolism

Volumn 5, Issue 1, 2010, Pages 77-88

  King, George L ^a,b   Das Evcimen, Net ^c  

^a HARVARD MEDICAL SCHOOL   (United States)

^b JOSLIN DIABETES CENTER   (United States)

^c ANKARA UNIVERSITY   (Turkey)

Author keywords

Diabetes mellitus; Diabetic complications; LY333531; PKC isoforms; Protein kinase C; Ruboxistaurin

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; ALPHA TOCOPHEROL; ANGIOTENSIN RECEPTOR ANTAGONIST; ANTISENSE OLIGONUCLEOTIDE; BISINDOLYLMALEIMIDE; DIACYLGLYCEROL; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEME OXYGENASE 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLOCARBAZOLE; INSULIN; MIDOSTAURIN; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PEPTIDE FRAGMENT; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN KINASE C; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA INHIBITOR; PROTEIN KINASE C BETA1; PROTEIN KINASE C BETA2; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN KINASE C GAMMA; ROTTLERIN; RUBOXISTAURIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULOTROPIN;

ANGIOGENESIS; ANTIOXIDANT ACTIVITY; ATHEROSCLEROSIS; BLOOD VESSEL PERMEABILITY; CARDIOVASCULAR DISEASE; CELL GROWTH; CELL PROLIFERATION; CORONARY ARTERY DISEASE; DIABETES MELLITUS; DIABETIC ANGIOPATHY; DIABETIC NEPHROPATHY; DIABETIC NEUROPATHY; DIABETIC RETINOPATHY; DOSE RESPONSE; DRUG EFFECT; DRUG EFFICACY; DRUG TARGETING; ENDOTHELIAL DYSFUNCTION; ENZYME ACTIVATION; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; HUMAN; HYPERGLYCEMIA; IC 50; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN RESISTANCE; LEUKOCYTE ADHERENCE; LIVER TOXICITY; LOW DRUG DOSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PATHOGENESIS; PERIPHERAL VASCULAR DISEASE; PRIMARY PREVENTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RISK FACTOR; SIGNAL TRANSDUCTION; UNSPECIFIED SIDE EFFECT;

EID: 77949803613     PISSN: 17446651     EISSN: None     Source Type: Journal    
DOI: 10.1586/eem.09.74     Document Type: Review

References (130)

1. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. The Diabetes Control and Complications Trial Research Group. N. Engl. J. Med. 329(14), 977-986 (1993).
2. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with Type 2 diabetes (UKPDS 33). UK Prospective Diabetes Study (UKPDS) Group. Lancet 352(9131), 837-853 (1998).
3. Koya D, King GL. Protein kinase C activation and the development of diabetic complications. Diabetes 47(6), 859-866 (1998).
4. Obrosova IG, Minchenko AG, Vasupuram R et al. Aldose reductase inhibitor fidarestat prevents retinal oxidative stress and vascular endothelial growth factor overexpression in streptozotocin-diabetic rats. Diabetes 52(3), 864-871 (2003).
5. Brownlee M. Biochemistry and molecular cell biology of diabetic complications. Nature 414(6865), 813-820 (2001).
6. Wendt T, Harja E, Bucciarelli L et al. RAGE modulates vascular inflammation and atherosclerosis in a murine model of Type 2 diabetes. Atherosclerosis 185(1), 70-77 (2006).
7. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258(5082), 607-614 (1992).
8. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J. 9(7), 484-496 (1995).
9. Keenan HA, Costacou T, Sun JK et al. Clinical factors associated with resistance to microvascular complications in diabetic patients of extreme disease duration: the 50-year medalist study. Diabetes Care 30(8), 1995-1997 (2007).
10. Mellor H, Parker PJ. The extended protein kinase C superfamily. Biochem. J. 332(Pt 2), 281-292 (1998).
11. Sheetz MJ, King GL. Molecular understanding of hyperglycemias adverse effects for diabetic complications. JAMA 288(20), 2579-2588 (2002).
12. Sajan MP, Standaert ML, Rivas J et al. Role of atypical protein kinase C in activation of sterol regulatory element binding protein-1c and nuclear factor kB (NFkB) in liver of rodents used as a model of diabetes, and relationships to hyperlipidaemia and insulin resistance. Diabetologia 52(6), 1197-1207 (2009).
13. Liscovitch M, Cantley LC. Lipid second messengers. Cell 77(3), 329-334 (1994).
14. Nakanishi H, Brewer KA, Exton JH. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 268(1), 13-16 (1993).
15. 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. 265(5 Pt 1), E783-E793 (1993).
16. Inoguchi T, Battan R, Handler E, Sportsman JR, Heath W, King GL. Preferential elevation of protein kinase C isoform b 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 89(22), 11059-11063 (1992).
17. Derubertis FR, Craven PA. Activation of protein kinase C in glomerular cells in diabetes. Mechanisms and potential links to the pathogenesis of diabetic glomerulopathy. Diabetes 43(1), 1-8 (1994).
18. Ishii H, Jirousek MR, Koya D et al. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC b inhibitor. Science 272(5262), 728-731 (1996).
19. Craven PA, Davidson CM, DeRubertis FR. Increase in diacylglycerol mass in isolated glomeruli by glucose from de novo synthesis of glycerolipids. Diabetes 39(6), 667-674 (1990).
20. Ido Y, McHowat J, Chang KC et al. Neural dysfunction and metabolic imbalances in diabetic rats. Prevention by acetyl-lcarnitine. Diabetes 43(12), 1469-1477 (1994).
21. Xia P, Inoguchi T, Kern TS, Engerman RL, Oates PJ, King GL. Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes 43(9), 1122-1129 (1994).
22. Ayo SH, Radnik R, Garoni JA, Troyer DA, Kreisberg JI. High glucose increases diacylglycerol mass and activates protein kinase C in mesangial cell cultures. Am. J. Physiol. 261(4 Pt 2), F571-F577 (1991).
23. Studer RK, Craven PA, DeRubertis FR. Role for protein kinase C in the mediation of increased fibronectin accumulation by mesangial cells grown in high-glucose medium. Diabetes 42(1), 118-126 (1993).
24. Konishi H, Tanaka M, Takemura Y et al. Activation of protein kinase C by tyrosine phosphorylation in response to H2O2. Proc. Natl Acad. Sci. USA 94(21), 11233-11237 (1997).
25. Nishikawa T, Edelstein D, Du XL et al. Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404(6779), 787-790 (2000).
26. Rolo AP, Palmeira CM. Diabetes and mitochondrial function: role of hyperglycemia and oxidative stress. Toxicol. Appl. Pharmacol. 212(2), 167-178 (2006).
27. Inoguchi T, Xia P, Kunisaki M, Higashi S, Feener EP, King GL. Insulins effect on protein kinase C and diacylglycerol induced by diabetes and glucose in vascular tissues. Am. J. Physiol. 267(3 Pt 1), E369-E379 (1994).
28. Craven PA, DeRubertis FR. Protein kinase C is activated in glomeruli from streptozotocin diabetic rats. Possible mediation by glucose. J. Clin. Invest. 83(5), 1667-1675 (1989).
29. Whiteside CI, Dlugosz JA. Mesangial cell protein kinase C isozyme activation in the diabetic milieu. Am. J. Physiol. Renal Physiol. 282(6), F975-980 (2002).
30. Park JY, Takahara N, Gabriele A et al. Induction of endothelin-1 expression by glucose: an effect of protein kinase C activation. Diabetes 49(7), 1239-1248 (2000).
31. Toth C, Rong LL, Yang C et al. Receptor for advanced glycation end products (RAGEs) and experimental diabetic neuropathy. Diabetes 57(4), 1002-1017 (2008).
32. Rask-Madsen C, King GL. Proatherosclerotic mechanisms involving protein kinase C in diabetes and insulin resistance. Arterioscler. Thromb. Vasc. Biol. 25(3), 487-496 (2005).
33. Montagnani M, Chen H, Barr VA, Quon MJ. Insulin-stimulated activation of eNOS is independent of Ca2+ but requires phosphorylation by Akt at Ser(1179). J. Biol. Chem. 276(32), 30392-30398 (2001).
34. Kuboki K, Jiang ZY, Takahara N et al. Regulation of endothelial constitutive nitric oxide synthase gene expression in endothelial cells and in vivo: a specific vascular action of insulin. Circulation 101(6), 676-681 (2000).
35. Federici M, Pandolfi A, De Filippis EA et al. G972R IRS-1 variant impairs insulin regulation of endothelial nitric oxide synthase in cultured human endothelial cells. Circulation 109(3), 399-405 (2004).
36. Vicent D, Ilany J, Kondo T et al. The role of endothelial insulin signaling in the regulation of vascular tone and insulin resistance. J. Clin. Invest. 111(9), 1373-1380 (2003).
37. Jiang ZY, Lin YW, Clemont A et al. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J. Clin. Invest. 104(4), 447-457 (1999).
38. Cusi K, Maezono K, Osman A et al. Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J. Clin. Invest. 105(3), 311-320 (2000).
39. He Z, Opland DM, Way KJ et al. Regulation of vascular endothelial growth factor expression and vascularization in the myocardium by insulin receptor and PI3K/Akt pathways in insulin resistance and ischemia. Arterioscler. Thromb. Vasc. Biol. 26(4), 787-793 (2006).
40. Naruse K, Rask-Madsen C, Takahara N et al. Activation of vascular protein kinase C-b inhibits Akt-dependent endothelial nitric oxide synthase function in obesityassociated insulin resistance. Diabetes 55(3), 691-698 (2006).
41. Folli F, Kahn CR, Hansen H, Bouchie JL, Feener EP. Angiotensin II inhibits insulin signaling in aortic smooth muscle cells at multiple levels. A potential role for serine phosphorylation in insulin/angiotensin II crosstalk. J. Clin. Invest. 100(9), 2158-2169 (1997).
42. Geraldes P, Yagi K, Ohshiro Y et al. Selective regulation of heme oxygenase-1 expression and function by insulin through IRS1/phosphoinositide 3-kinase/Akt-2 pathway. J. Biol. Chem. 283(49), 34327-34336 (2008).
43. Farhangkhoee H, Khan ZA, Mukherjee S et al. Heme oxygenase in diabetesinduced oxidative stress in the heart. J. Mol. Cell Cardiol. 35(12), 1439-1448 (2003).
44. Hayashi K, Haneda M, Koya D, Maeda S, Isshiki K, Kikkawa R. Enhancement of glomerular heme oxygenase-1 expression in diabetic rats. Diabetes Res. Clin. Pract. 52(2), 85-96 (2001).
45. Cukiernik M, Mukherjee S, Downey D, Chakabarti S. Heme oxygenase in the retina in diabetes. Curr. Eye Res. 27(5), 301-308 (2003).
46. Abraham NG, Kushida T, McClung J et al. Heme oxygenase-1 attenuates glucose-mediated cell growth arrest and apoptosis in human microvessel endothelial cells. Circ. Res. 93(6), 507-514 (2003).
47. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat. Med. 9(6), 669-676 (2003).
48. Giordano FJ, Gerber HP, Williams SP et al. A cardiac myocyte vascular endothelial growth factor paracrine pathway is required to maintain cardiac function. Proc. Natl Acad. Sci. USA 98(10), 5780-5785 (2001).
49. Jiang ZY, He Z, King BL et al. Characterization of multiple signaling pathways of insulin in the regulation of vascular endothelial growth factor expression in vascular cells and angiogenesis. J. Biol. Chem. 278(34), 31964-31971 (2003).
50. Poulaki V, Qin W, Joussen AM et al. Acute intensive insulin therapy exacerbates diabetic blood-retinal barrier breakdown via hypoxia-inducible factor-1a and VEGF. J. Clin. Invest. 109(6), 805-815 (2002).
51. Miele C, Rochford JJ, Filippa N, Giorgetti-Peraldi S, Van Obberghen E. Insulin and insulin-like growth factor-I induce vascular endothelial growth factor mRNA expression via different signaling pathways. J. Biol. Chem. 275(28), 21695-21702 (2000).
52. Chou E, Suzuma I, Way KJ et al. Decreased cardiac expression of vascular endothelial growth factor and its receptors in insulin-resistant and diabetic states: a possible explanation for impaired collateral formation in cardiac tissue. Circulation 105(3), 373-379 (2002).
53. Yoon YS, Uchida S, Masuo O et al. Progressive attenuation of myocardial vascular endothelial growth factor expression is a seminal event in diabetic cardiomyopathy: restoration of microvascular homeostasis and recovery of cardiac function in diabetic cardiomyopathy after replenishment of local vascular endothelial growth factor. Circulation 111(16), 2073-2085 (2005).
54. Pandolfi A, Solini A, Pellegrini G et al. Selective insulin resistance affecting nitric oxide release but not plasminogen activator inhibitor-1 synthesis in fibroblasts from insulin-resistant individuals. Arterioscler. Thromb. Vasc. Biol. 25(11), 2392-2397 (2005).
55. Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocr. Rev. 28(5), 463-491 (2007).
56. Morisco C, Marrone C, Trimarco V et al. Insulin resistance affects the cytoprotective effect of insulin in cardiomyocytes through an impairment of MAPK phosphatase-1 expression. Cardiovasc. Res. 76(3), 453-464 (2007).
57. Oliver FJ, de la Rubia G, Feener EP et al. Stimulation of endothelin-1 gene expression by insulin in endothelial cells. J. Biol. Chem. 266(34), 23251-23256 (1991).
58. Arcaro G, Cretti A, Balzano S et al. Insulin causes endothelial dysfunction in humans: sites and mechanisms. Circulation 105(5), 576-582 (2002).
59. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J. Clin. Invest. 97(11), 2601-2610 (1996).
60. Rask-Madsen C, Ihlemann N, Krarup T et al. Insulin therapy improves insulinstimulated endothelial function in patients with Type 2 diabetes and ischemic heart disease. Diabetes 50(11), 2611-2618 (2001).
61. Rask-Madsen C, King GL. Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat. Clin. Pract. Endocrinol. Metab. 3(1), 46-56 (2007).
62. Standaert ML, Bandyopadhyay G, Kanoh Y, Sajan MP, Farese RV. Insulin and PIP3 activate PKC-zeta by mechanisms that are both dependent and independent of phosphorylation of activation loop (T410) and autophosphorylation (T560) sites. Biochemistry 40(1), 249-255 (2001).
63. Christiansen JS, Gammelgaard J, Frandsen M, Parving HH. Increased kidney size, glomerular filtration rate and renal plasma flow in short-term insulindependent diabetics. Diabetologia 20(4), 451-456 (1981).
64. Ditzel J, Schwartz M. Abnormally increased glomerular filtration rate in short-term insulin-treated diabetic subjects. Diabetes 16(4), 264-267 (1967).
65. Hostetter TH, Troy JL, Brenner BM. Glomerular hemodynamics in experimental diabetes mellitus. Kidney Int. 19(3), 410-415 (1981).
66. Viberti GC. Early functional and morphological changes in diabetic nephropathy. Clin. Nephrol. 12(2), 47-53 (1979).
67. ODonnell MP, Kasiske BL, Keane WF. Glomerular hemodynamic and structural alterations in experimental diabetes mellitus. FASEB J. 2(8), 2339-2347 (1988).
68. Ruan X, Arendshorst WJ. Role of protein kinase C in angiotensin II-induced renal vasoconstriction in genetically hypertensive rats. Am. J. Physiol. 270(6 Pt 2), F945-F952 (1996).
69. Craven PA, Caines MA, DeRubertis FR. Sequential alterations in glomerular prostaglandin and thromboxane synthesis in diabetic rats: relationship to the hyperfiltration of early diabetes. Metabolism 36(1), 95-103 (1987).
70. Perico N, Benigni A, Gabanelli M et al. Atrial natriuretic peptide and prostacyclin synergistically mediate hyperfiltration and hyperperfusion of diabetic rats. Diabetes 41(4), 533-538 (1992).
71. Feke GT, Buzney SM, Ogasawara H et al. Retinal circulatory abnormalities in Type 1 diabetes. Invest. Ophthalmol. Vis. Sci. 35(7), 2968-2975 (1994).
72. Bursell SE, Clermont AC, Kinsley BT, Simonson DC, Aiello LM, Wolpert HA. Retinal blood flow changes in patients with insulin-dependent diabetes mellitus and no diabetic retinopathy. Invest. Ophthalmol. Vis. Sci. 37(5), 886-897 (1996).
73. Clermont AC, Brittis M, Shiba T, McGovern T, King GL, Bursell SE. Normalization of retinal blood flow in diabetic rats with primary intervention using insulin pumps. Invest. Ophthalmol. Vis. Sci. 35(3), 981-990 (1994).
74. Kohner EM, Patel V, Rassam SM. Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 44(6), 603-607 (1995).
75. Aiello LP, Avery RL, Arrigg PG et al. Vascular endothelial growth factor in ocular fluid of patients with diabetic retinopathy and other retinal disorders. N. Engl. J. Med. 331(22), 1480-1487 (1994).
76. Cameron NE, Cotter MA. Metabolic and vascular factors in the pathogenesis of diabetic neuropathy. Diabetes 46(Suppl. 2), S31-S37 (1997).
77. Uehara K, Yamagishi S, Otsuki S, Chin S, Yagihashi S. Effects of polyol pathway hyperactivity on protein kinase C activity, nociceptive peptide expression, and neuronal structure in dorsal root ganglia in diabetic mice. Diabetes 53(12), 3239-3247 (2004).
78. Nakamura J, Kato K, Hamada Y et al. A protein kinase C-b-selective inhibitor ameliorates neural dysfunction in streptozotocin-induced diabetic rats. Diabetes 48(10), 2090-2095 (1999).
79. Haneda M, Kikkawa R, Horide N et al. Glucose enhances type IV collagen production in cultured rat glomerular mesangial cells. Diabetologia 34(3), 198-200 (1991).
80. Fumo P, Kuncio GS, Ziyadeh FN. PKC and high glucose stimulate collagen a 1 (IV) transcriptional activity in a reporter mesangial cell line. Am. J. Physiol. 267(4 Pt 2), F632-F638 (1994).
81. Yamamoto T, Nakamura T, Noble NA, Ruoslahti E, Border WA. Expression of transforming growth factor b is elevated in human and experimental diabetic nephropathy. Proc. Natl Acad. Sci. USA 90(5), 1814-1818 (1993).
82. Shankland SJ, Scholey JW, Ly H, Thai K. Expression of transforming growth factor-b 1 during diabetic renal hypertrophy. Kidney Int. 46(2), 430-442 (1994).
83. Edwards AS, Faux MC, Scott JD, Newton AC. Carboxyl-terminal phosphorylation regulates the function and subcellular localization of protein kinase C bII. J. Biol. Chem. 274(10), 6461-6468 (1999).
84. Chiu R, Boyle WJ, Meek J, Smeal T, Hunter T, Karin M. The c-Fos protein interacts with c-Jun/AP-1 to stimulate transcription of AP-1 responsive genes. Cell 54(4), 541-552 (1988).
85. Ohshiro Y, Ma RC, Yasuda Y et al. Reduction of diabetes-induced oxidative stress, fibrotic cytokine expression, and renal dysfunction in protein kinase Cb-null mice. Diabetes 55(11), 3112-3120 (2006).
86. Oliver JA. Adenylate cyclase and protein kinase C mediate opposite actions on endothelial junctions. J. Cell Physiol. 145(3), 536-542 (1990).
87. Lynch JJ, Ferro TJ, Blumenstock FA, Brockenauer AM, Malik AB. Increased endothelial albumin permeability mediated by protein kinase C activation. J. Clin. Invest. 85(6), 1991-1998 (1990).
88. Nagpala PG, Malik AB, Vuong PT, Lum H. Protein kinase C b 1 overexpression augments phorbol ester-induced increase in endothelial permeability. J. Cell Physiol. 166(2), 249-255 (1996).
89. Wolf BA, Williamson JR, Easom RA, Chang K, Sherman WR, Turk J. Diacylglycerol accumulation and microvascular abnormalities induced by elevated glucose levels. J. Clin. Invest. 87(1), 31-38 (1991).
90. Xia P, Aiello LP, Ishii H et al. Characterization of vascular endothelial growth factors effect on the activation of protein kinase C, its isoforms, and endothelial cell growth. J. Clin. Invest. 98(9), 2018-2026 (1996).
91. Gamou S, Shimizu N. Calphostin-C stimulates epidermal growth factor receptor phosphorylation and internalization via light-dependent mechanism. J. Cell Physiol. 158(1), 151-159 (1994).
92. Katsura Y, Okano T, Noritake M et al. Hepatocyte growth factor in vitreous fluid of patients with proliferative diabetic retinopathy and other retinal disorders. Diabetes Care 21(10), 1759-1763 (1998).
93. Pfeiffer A, Schatz H. Diabetic microvascular complications and growth factors. Exp. Clin. Endocrinol. Diabetes 103(1), 7-14 (1995).
94. Koya D, Jirousek MR, Lin YW, Ishii H, Kuboki K, King GL. Characterization of protein kinase C b isoform activation on the gene expression of transforming growth factor-b, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J. Clin. Invest. 100(1), 115-126 (1997).
95. Jirousek MR, Gillig JR, Gonzalez CM et al. (S)-13-[(dimethylamino)methyl] - 10,11,14,15-tetrahydro-4,9:16, 21-dimetheno-1H, 13H-dibenzo[e,k] pyrrolo[3,4-h][1,4,13] oxadiazacyclohexadecene-1,3(2H)-d ione (LY333531) and related analogues: isozyme selective inhibitors of protein kinase C b. J. Med. Chem. 39(14), 2664-2671 (1996).
96. Bursell SE, King GL. Can protein kinase C inhibition and vitamin E prevent the development of diabetic vascular complications? Diabetes Res. Clin. Pract. 45(2-3), 169-182 (1999).
97. Orr JW, Keranen LM, Newton AC. Reversible exposure of the pseudosubstrate domain of protein kinase C by phosphatidylserine and diacylglycerol. J. Biol. Chem. 267(22), 15263-15266 (1992).
98. McKay RA, Miraglia LJ, Cummins LL, Owens SR, Sasmor H, Dean NM. Characterization of a potent and specific class of antisense oligonucleotide inhibitor of human protein kinase C-a expression. J. Biol. Chem. 274(3), 1715-1722 (1999).
99. Ron D, Luo J, Mochly-Rosen D. C2 region-derived peptides inhibit translocation and function of b protein kinase C in vivo. J. Biol. Chem. 270(41), 24180-24187 (1995).
100. Dorn GW 2nd, Souroujon MC, Liron T et al. Sustained in vivo cardiac protection by a rationally designed peptide that causes e protein kinase C translocation. Proc. Natl Acad. Sci. USA 96(22), 12798-12803 (1999).
101. Parmer TG, Ward MD, Hait WN. Effects of rottlerin, an inhibitor of calmodulin-dependent protein kinase III, on cellular proliferation, viability, and cell cycle distribution in malignant glioma cells. Cell Growth Differ. 8(3), 327-334 (1997).
102. Kunisaki M, Bursell SE, Clermont AC et al. Vitamin E prevents diabetes-induced abnormal retinal blood flow via the diacylglycerol-protein kinase C pathway. Am. J. Physiol. 269(2 Pt 1), E239-E246 (1995).
103. Bursell SE, Takagi C, Clermont AC et al. Specific retinal diacylglycerol and protein kinase C b isoform modulation mimics abnormal retinal hemodynamics in diabetic rats. Invest. Ophthalmol. Vis. Sci. 38(13), 2711-2720 (1997).
104. Bursell SE, Clermont AC, Aiello LP et al. High-dose vitamin E supplementation normalizes retinal blood flow and creatinine clearance in patients with Type 1 diabetes. Diabetes Care 22(8), 1245-1251 (1999).
105. Yusuf S, Dagenais G, Pogue J, Bosch J, Sleight P. Vitamin E supplementation and cardiovascular events in high-risk patients. The Heart Outcomes Prevention Evaluation Study Investigators. N. Engl. J. Med. 342(3), 154-160 (2000).
106. Economides PA, Khaodhiar L, Caselli A et al. The effect of vitamin E on endothelial function of micro- and macrocirculation and left ventricular function in Type 1 and Type 2 diabetic patients. Diabetes 54(1), 204-211 (2005).
107. Bowling N, Walsh RA, Song G et al. Increased protein kinase C activity and expression of Ca2+-sensitive isoforms in the failing human heart. Circulation, 99(3), 384-391 (1999).
108. McGill JB, King GL, Berg PH et al. Clinical safety of the selective PKC-b inhibitor, ruboxistaurin. Expert Opin. Drug Saf. 5(6), 835-845 (2006).
109. Nonaka A, Kiryu J, Tsujikawa A et al. PKC-b inhibitor (LY333531) attenuates leukocyte entrapment in retinal microcirculation of diabetic rats. Invest. Ophthalmol. Vis. Sci. 41(9), 2702-2706 (2000).
110. Arikawa E, Ma RC, Isshiki K et al. Effects of insulin replacements, inhibitors of angiotensin, and PKCbs actions to normalize cardiac gene expression and fuel metabolism in diabetic rats. Diabetes 56(5), 1410-1420 (2007).
111. Campochiaro PA. Reduction of diabetic macular edema by oral administration of the kinase inhibitor PKC412. Invest. Ophthalmol. Vis. Sci. 45(3), 922-931 (2004).
112. Barber AJ, Lieth E, Khin SA, Antonetti DA, Buchanan AG, Gardner TW. Neural apoptosis in the retina during experimental and human diabetes. Early onset and effect of insulin. J. Clin. Invest. 102(4), 783-791 (1998).
113. Aiello LP, Clermont A, Arora V, Davis MD, Sheetz MJ, Bursell SE. Inhibition of PKC b by oral administration of ruboxistaurin is well tolerated and ameliorates diabetes-induced retinal hemodynamic abnormalities in patients. Invest. Ophthalmol. Vis. Sci. 47(1), 86-92 (2006).
114. Aiello LP, Davis MD, Girach A et al. Effect of ruboxistaurin on visual loss in patients with diabetic retinopathy. Ophthalmology 113(12), 2221-2230 (2006).
115. Sarnak MJ, Levey AS, Schoolwerth AC et al. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 108(17), 2154-2169 (2003).
116. Ismail N, Becker B, Strzelczyk P, Ritz E. Renal disease and hypertension in non-insulin-dependent diabetes mellitus. Kidney Int. 55(1), 1-28 (1999).
117. Parving HH, Hommel E, Mathiesen E et al. Prevalence of microalbuminuria, arterial hypertension, retinopathy and neuropathy in patients with insulin dependent diabetes. Br. Med. J. (Clin. Res. Ed.) 296(6616), 156-160 (1988).
118. Tuttle KR, Bakris GL, Toto RD, McGill JB, Hu K, Anderson PW. The effect of ruboxistaurin on nephropathy in Type 2 diabetes. Diabetes Care 28(11), 2686-2690 (2005).
119. Calver A, Collier J, Vallance P. Inhibition and stimulation of nitric oxide synthesis in the human forearm arterial bed of patients with insulin-dependent diabetes. J. Clin. Invest. 90(6), 2548-2554 (1992).
120. De Vriese AS, Verbeuren TJ, Van de Voorde J, Lameire NH, Vanhoutte PM. Endothelial dysfunction in diabetes. Br. J. Pharmacol. 130(5), 963-974 (2000).
121. McVeigh GE, Brennan GM, Johnston GD et al. Impaired endothelium-dependent and independent vasodilation in patients with Type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 35(8), 771-776 (1992).
122. Beckman JA, Goldfine AB, Gordon MB, Garrett LA, Creager MA. Inhibition of protein kinase Cb prevents impaired endothelium-dependent vasodilation caused by hyperglycemia in humans. Circ. Res. 90(1), 107-111 (2002).
123. Hink U, Li H, Mollnau H et al. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ. Res. 88(2), E14-E22 (2001).
124. Zou MH, Cohen R, Ullrich V. Peroxynitrite and vascular endothelial dysfunction in diabetes mellitus. Endothelium 11(2), 89-97 (2004).
125. Cosentino F, Eto M, De Paolis P et al. High glucose causes upregulation of cyclooxygenase-2 and alters prostanoid profile in human endothelial cells: role of protein kinase C and reactive oxygen species. Circulation 107(7), 1017-1023 (2003).
126. Cardillo C, Campia U, Bryant MB, Panza JA. Increased activity of endogenous endothelin in patients with Type II diabetes mellitus. Circulation 106(14), 1783-1787 (2002).
127. Mehta NN, Sheetz M, Price K et al. Selective PKC b inhibition with ruboxistaurin and endothelial function in Type-2 diabetes mellitus. Cardiovasc. Drugs Ther. 23(1), 17-24 (2009).
128. Harja E, Chang JS, Lu Y et al. Mice deficient in PKCb and apolipoprotein E display decreased atherosclerosis. FASEB J. 23(4), 1081-1091 (2009).
129. Balafanova Z, Bolli R, Zhang J et al. Nitric oxide (NO) induces nitration of protein kinase Ce (PKCe), facilitating PKCe translocation via enhanced PKCe -RACK2 interactions: a novel mechanism of no-triggered activation of PKCe. J. Biol. Chem. 277(17), 15021-15027 (2002).
130. Nagareddy PR, Soliman H, Lin G et al. Selective inhibition of protein kinase C b(2) attenuates inducible nitric oxide synthase-mediated cardiovascular abnormalities in streptozotocin-induced diabetic rats. Diabetes 58(10), 2355-2364 (2009).