43
Views
0
CrossRef citations to date
0
Altmetric
Review

Role of protein kinase C inhibition in the development of diabetic microvascular complications

, &
Pages 321-329 | Published online: 10 Jan 2014

References

  • Wild S, Roglic G, Green A et al. Global prevalence of diabetes. Estimates for the year 2000 and projections for 2030. Diabetes Care27, 1047–1053 (2004).
  • King H, Aubert RE, Herman WH. Global burden of diabetes, 1995–2025: prevalence, numerical estimates, and projections. Diabetes Care21, 1414–1431 (1998).
  • Hedley AA, Ogden CL, Johnson CL et al. Prevalence of overweight and obesity among US children, adolescents, and adults, 1999–2002. JAMA291, 2847–2850 (2004).
  • Harris MI. Epidemiologic studies on the pathogenesis of non-insulin-dependent diabetes mellitus (NIDDM). Clin. Invest. Med.18, 231–239 (1995).
  • Centers for Disease Control and Prevention (CDC). Self-rated fair or poor health among adults with diabetes – United States,1996–2005. MMWR Morb. Mortal. Wkly Rep.55(45), 1224–1227 (2006).
  • Morgan CL, Currie CJ, Stott NC et al. The prevalence of multiple diabetes-related complications. Diabet. Med.17, 146–151 (2000).
  • Beckman JA, Creager MA, Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA287, 2570–2581 (2002).
  • Vinik AI, Milicevic Z. Preventive measures and treatment options for diabetic neuropathy. Contemp. Intern. Med.6(10), 41–42, 47–55 (1994).
  • Dyck PJ, Kratz KM, Karnes JL et al. The prevalence by staged severity of various types of diabetic neuropathy, retinopathy, and nephropathy in a population-based cohort: the Rochester Diabetic Neuropathy Study. Neurology43(4), 817–824 (1993).
  • Brown JB, Pedula KL, Bakst AW. The progressive cost of complications in Type 2 diabetes mellitus. Arch. Intern. Med.159(16), 1873–1880 (1999).
  • Williams R, Van Gaal L, Lucioni C. Assessing the impact of complications on the costs of Type 2 diabetes. Diabetologia352, 837–853 (2002).
  • Klein R, Klein BE, Moss SE. The Wisconsin Epidemiological Study of Diabetic Retinopathy: a review. Diabetes Metab. Rev.5, 559–570 (2002).
  • Kempen JH, O’Colmain BJ, Leske MC et al. The prevalence of diabetic retinopathy among adults in the United States. Arch. Ophthalmol.122, 552–563 (2004).
  • Blindness caused by diabetes: Massachusetts, 1987–1994. MMWR Morb. Mortal. Wkly Rep.45, 937–941 (1996).
  • Pirart J. Diabetes mellitus and its degenerative complications: a prospective study of 4,400 patients observed between 1947 and 1973. Diabetes Care1, 168–188 (1978).
  • Vinik AI, Park TS, Stansberry KB, Pittenger GL. Diabetic neuropathies. Diabetologia43, 957–973 (2000).
  • American Diabetes Association. Standards of medical care for patients with diabetes mellitus. Diabetes Care26(Suppl. 1), S33–S50 (2003).
  • US Renal Data System. USRDS 2002 Annual Data Report: Atlas of End-Stage Renal Disease in the United States. National Institute of Health, National Institute of Diabetes and Digestive and Kidney Diseases, Bethesda, MD (2002).
  • Girach A, Vignati L. Diabetic microvascular complications–can the presence of one predict the development of another? J. Diabetes Complications20(4), 228–237 (2006).
  • Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes and progression of long-term complications in insulin-dependent diabetes mellitus. N. Engl. J. Med.329, 977–986 (1993).
  • Diabetes Control and Complications Trial Research Group. The effect of intensive diabetes therapy on the development and progression of neuropathy. Ann. Int. Med.122, 561–568 (1995).
  • Diabetes Control and Complications Trial Research Group. The effect of intensive diabetes therapy on measures of autonomic nervous system function in the Diabetes Control and Complications Trial (DCCT). Diabetalogia41, 416–423 (1998).
  • Ohkubo Y, Kishikawa J, Araki E et al. Intensive insulin therapy prevents the progression of diabetic microvascular complication in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res Clin Pract.28, 103–117 (1995).
  • UK Prospective Diabetes Study (UKPDS) Group. Intensive blood-glucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with Type 2 diabetes (UKPDS 33). Lancet352, 837–853 (1998).
  • Vaag AA. Glycemic control and prevention of microvascular and microvascular disease in the Steno 2 Study. Endocrine Practice12(S1), 89–92 (2006).
  • Dyck PJ, Davies JL, Wilson DM, Service FJ, Melton LJ III, O’Brien PC. Risk factors for severity of diabetic polyneuropathy: intensive longitudinal assessment of the Rochester Diabetic Neuropathy Study cohort. Diabetes Care22(9), 1479–1486 (1999).
  • Sheetz MJ, King GL. Molecular understanding of hyperglycemia’s adverse effects for diabetic complications. JAMA88(20), 2579–2588 (2002).
  • Hotta N, Toyota T, Matsuoka K et al. Clinical efficacy of fidarestat, a novel aldose reductase inhibitor, for diabetic peripheral neuropathy: a 52-week multicenter placebo-controlled double-blind parallel group study. The SNK-860 Diabetic Neuropathy Study Group. Diabetes Care24, 1776–1782 (2001).
  • King RH. The role of glycation in the pathogenesis of diabetic polyneuropathy. Mol. Pathol.54, 400–408 (2001).
  • Oates PJ. Polyol pathway and diabetic peripheral neuropathy. Int. Rev. Neurobiol.50, 325–392 (2002).
  • Reljanovic M, Reichel G, Rett K et al. Treatment of diabetic polyneuropathy with the antioxidant thiotic acid (α-lipoic acid): a two year multicentre randomized double-blind placebo-controlled trial (ALADIN II). Alpha Lipoic Acid in Diabetic Neuropathy. Free Radic. Res.31, 171–179 (1999).
  • Anand P, Terenghi G, Warner G et al. The role of endogenous nerve growth factor in human diabetic neuropathy. Nat. Med.2, 703–707 (1996).
  • Lee TS, Saltsman KA, Ohashi H, King GL. Activation of PKC by elevation of glucose concentration: proposal for a mechanism in the development of diabetic vascular complications. Proc. Natl Acad. Sci. USA86, 5141–5145 (1989).
  • Ways DK, Sheetz MJ. The role of protein kinase C in the development of the complications of diabetes. Vitam. Horm.60, 149–193 (2000).
  • Hamada Y, Araki N, Koh N, Nakamura J, Horiuchi S, Hotta N. Rapid formation of advanced glycation end products by intermediate metabolites of glycolytic pathway and polyol pathway. Biochem. Biophys. Res. Comm.228, 539–543 (1996).
  • Walaas SI, Greengard P. Protein phosphorylation and neuronal function. Pharmacol. Rev.43, 299–349 (1991).
  • Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science258, 607–614 (1992).
  • King GL, Brownlee M. The cellular and molecular mechanisms of diabetic complications. Endocrinol. Metab. Clin. North Am.25(2), 255–270 (1996).
  • Mellor H, Parker PJ. The extended protein kinase C superfamily. Biochem. J.332, 281–292 (1998).
  • Newton AC. Protein kinase C: structural and spatial regulation by phosphorylation, cofactors, and macromolecular interactions. Chem. Rev.101(8), 2353–2364 (2001).
  • Goekjian PG, Jirousek MR. Protein kinase C in the treatment of disease: signal transduction pathways, inhibitors, and agents in development. Curr. Med. Chem.6(9), 877–903 (1999).
  • Nishikawa T, Edelstein D, Brownlee M. The missing link: a single unifying mechanism for diabetic complications. Kidney. Int. Suppl.77, S26–S30 (2000).
  • Schechtman D, Mochly-Rosen D. Adaptor proteins in protein kinase C-mediated signal transduction. Oncogene20(44), 6339–6347 (2001).
  • Sipeki S, Bander E, Farkas G, Gujdar A, Ways DK, Farago A. Protein kinase C decreases the hepatocyte growth factor-induced activation of Erk1/Erk2 MAP kinases. Cell Signal.12(8), 549–555 (2000).
  • 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, 1480–1487 (1994).
  • Inoguchi T, Battan R, Handler E, Sportsman JR, Heath W, King GL. Preferential elevation of protein kinase C isoform β2 and diacylglycerol levels in the aorta and heart of diabetic rats: differential reversibility to glycemic control by islet cell transplantation. Proc. Natl Acad. Sci. USA89, 11059–11063 (1992).
  • Ishii H, Jirousek MR, Koya D et al. Amelioration of vascular dysfunctions in diabetic rats by an oral PKC β inhibitor. Science272, 728–731 (1996).
  • Craven PA, DeRubertis FR. Protein kinase C is activated in glomeruli from streptozotocin diabetic rats. Possible mediation by glucose. J. Clin. Invest.83, 1667–1675 (1989).
  • 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, F571–F577 (1991).
  • 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, E783–E793 (1993).
  • Congdon N, O’Colmain B, Klaver CC et al. Causes and prevalence of visual impairment among adults in the United States. Arch. Ophthalmol.122, 477–485 (2004).
  • Moss SE, Klein R, Klein BE. The 14-year incidence of visual loss in a diabetic population. Ophthalmology105, 998–1003 (1998).
  • Fong DS, Aiello LP, Ferris FL III, Klein R. Diabetic retinopathy. Diabetes Care27(S1), S84–S87 (2004).
  • Gardner TW, Antonetti DA, Barber AJ, LaNoue KF, Lewison SW. Diabetic retinopathy: more than meets the eye. Surv. Ophtalmol.47(Suppl. 2), S253–S262 (2004).
  • Comer GM, Ciulla TA. Current and future pharmacological intervention for diabetic retinopathy. Expert Opin. Emerg. Drugs10(2), 441–455 (2005).
  • Ciulla TA, Amador AG, Zinman B. Diabetic retinopathy and diabetic macular edema: pathophysiology, screening, and novel therapies. Diabetes Care26(9), 2653–2664 (2003).
  • Xia P, Inoguchi T, Kern T, Engerman RL, Oates PJ, King GL. Characterization of the mechanism for the chronic activation of diacylglycerol-protein kinase C pathway in diabetes and hypergalactosemia. Diabetes43, 1122–1129 (1994).
  • Wetsel WC, Khan WA, Merchenthaler I et al. Tissue and cellular distribution of the extended family of protein kinase C isoenzymes. J. Cell Biol.117, 121–133 (1992).
  • Williams B, Gallacher B, Patel H, Orme C. Glucose-induced protein kinase C activation regulates vascular permeability factor mRNA expression and peptide production by human vascular smooth muscle cells in vitro. Diabetes46, 1497–1503 (1997).
  • Mathews MK, Merges C, McLeod DS, Lutty GA. Vascular endothelial growth factor and vascular permeability changes in human diabetic retinopathy. Invest. Ophthalmol. Vis. Sci.38, 2729–2741 (1997).
  • Adamis AP, Shima DT, Tolentino MJ et al. Inhibition of vascular endothelial growth factor prevents retinal ischemia-associated iris neovascularization in a nonhuman primate. Arch. Ophthalmol.114, 66–71 (1996).
  • Kowluru RA, Jirousek MR, Stramm L, Farid N, Engerman RL, Kern TS. Abnormalities of retinal metabolism in diabetes or experimental galactosemia. V. Relationship between protein kinase C and ATPases. Diabetes47, 464–469 (1998).
  • Aiello LP, Bursell SE, Clermont A et al. Vascular endothelial growth factor-induced retinal permeability is mediated by protein kinase C in vivo and suppressed by an orally effective β-isoform-selective inhibitor. Diabetes46, 1473–1480 (1997).
  • Danis RP, Bingaman DP, Jirousek M, Yang Y. Inhibition of intraocular neovascularization caused by retinal ischemia in pigs by PKC-β inhibition with LY333531. Invest. Ophthalmol. Vis. Sci.39, 171–179 (1998).
  • McGill JB, King GL, Berg PH et al. Clinical safety of the selective PKC-β inhibitor, ruboxistaurin. Expert Opin. Drug Saf.5(6), 835–845 (2006).
  • Aiello LP, Clermont A, Arora V, Davis MD, Sheetz MJ, Bursell SE. Inhibition of PKC β 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).
  • PKC-DRS Study Group. The effect of ruboxistaurin on visual loss in patients with moderately severe to very severe nonproliferative diabetic retinopathy. Diabetes54, 2188–2197 (2005).
  • PKC DRS2 Study Group. Effect of ruboxistaurin on visual loss in patients with diabetic retinopathy. Ophthalmology113(12), 2221–2230 (2006).
  • The PKC-DMES Study Group. Effect of ruboxistaurin, a PKC isoform-selective inhibitor, in patients with diabetic macular edema: 30-month results of the randomized PKC-DMES clinical trial. Arch. Ophthalmol. (2007) (In Press).
  • Boulton AJ. Treatment of symptomatic diabetic neuropathy. Diabetes Metab. Res. Rev.19(Suppl. 1), S16–S21 (2003).
  • Vinik AI, Mehrabyan A. Diagnosis and management of diabetic autonomic neuropathy. Compr. Ther.29(2–3), 130–145 (2003).
  • Boulton AJ, Malik RA, Arezzo JC, Sosenko JM. Diabetic somatic neuropathies. Diabetes Care27(6), 1458–1486 (2004).
  • Boulton AJ. Guidelines for diagnosis and outpatient management of diabetic peripheral neuropathy. European Association for the Study of Diabetes, Neurodiab. Diabetes Metab.24(Suppl. 3), 55–65 (1998).
  • Sugimoto K, Murakawa Y, Sima AA. Diabetic neuropathy – a continuing enigma. Diabetes Metab. Res. Rev.16(6), 408–433 (2000).
  • Dyck PJ, Giannini C. Pathological alterations in the diabetic neuropathies of humans: a review. Neuropathol. Exp. Neurol.55(12), 1181–1193 (1996).
  • Cameron NE, Eaton SE, Cotter MA, Tesfaye S. Vascular factors and metabolic interactions in the pathogenesis of diabetic neuropathy. Diabetologia44(11), 1973–1988 (2001).
  • Cameron NE, Cotter MA, Low PA. Nerve blood flow in early experimental diabetes in rats: relation to conduction deficits. Am. J. Physiol.261(24), El–E8 (1991).
  • Cotter MA, Jack AM, Cameron NE. Effects of the protein kinase C β inhibitor LY333531 on neural and vascular function in rats with streptozotocin-induced diabetes. Clinical Science103, 311–321 (2002).
  • Nakamura J, Kato K, Hamada Y et al. A protein kinase C-β-selective inhibitor ameliorates neural dysfunction in streptozotocin-induced diabetic rats. Diabetes48, 2090–2095 (1999).
  • Vinik AI, Bril V, Kempler P et al. Treatment of symptomatic diabetic peripheral neuropathy with the protein kinase C β-inhibitor ruboxistaurin mesylate during a 1-year, randomized, placebo-controlled, double blind clinical trial. Clin. Ther.27, 1164–1180 (2005).
  • Tandan R, Skljarevski V, Price KL, Kles KA, Bastyr EJ; for the Ruboxistaurin Treatment of DPN Study Group. Neuropathy Progression in Patients with Symptomatic Diabetic Peripheral Neuropathy: Experience from Phase 3 Ruboxistaurin Clinical Trials. Neurology66(5) (Suppl. 2), A191 (2006).
  • Tuttle KR, Anderson PW. A novel potential therapy for diabetic nephropathy and vascular complications: protein kinase C-β inhibition. Am. J. Kidney Dis.42(3), 456–465 (2003).
  • American Diabetes Association. Standards of Medical Care in Diabetes. Diabetes Care28(S1), S4–S36 (2005).
  • Williams ME, Tuttle KR. The next generation of diabetic nephropathy therapies: an update. Adv. Chronic Kidney Dis.12(2), 212–222 (2005).
  • Williams B, Schrier RW. Glucose-induced protein kinase C activity regulates arachidonic acid release and eicosanoid production by cultured glomerular mesangial cells. J. Clin. Invest.92(6), 2889–2896 (1993).
  • Craven PA, Studer RK, DeRubertis FR. Impaired nitric oxide-dependent cyclic guanosine monophosphate generation in glomeruli from diabetic rats. Evidence for protein kinase C-mediated suppression of the cholinergic response. J. Clin. Invest.93(1), 311–320 (1994).
  • Sharma K, Ziyadeh FN. Hyperglycemia and diabetic kidney disease. The case for transforming growth factor-β as a key mediator. Diabetes44, 1139–1146 (1995).
  • Koya D, Haneda M, Nakagawa H et al. Amelioration of accelerated diabetic mesangial expansion by treatment with a PKC β inhibitor in diabetic db/db mice, a rodent model for Type 2 diabetes. FASEB J.14, 439–447 (2000).
  • Tuttle KR, Bakris GL, Toto RD, McGill JB, Hu K, Anderson PW. The effect of ruboxistaurin on nephropathy in Type 2 diabetes. Diabetes Care28, 2686–2690 (2005).

Websites

  • Centers for Disease Control (CDC) www.cdc.gov/diabetes/statistics/index.htm
  • World Health Organization www.who.int/hpr/gs.fs.diabetes.shtml

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.