PKCβ promotes vascular inflammation and acceleration of atherosclerosis in diabetic ApoE null mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 8, 2013, Pages 1779-1787

  Kong, Linghua ^a   Shen, Xiaoping ^a   Lin, Lili ^a   Leitges, Michael ^b   Rosario, Rosa ^a   Zou, Yu Shan ^a   Yan, Shi Fang ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF OSLO   (Norway)

Author keywords

Antigens, CD11c; Atherosclerosis; Diabetes mellitus; Inflammation; PKC

Indexed keywords

APOLIPOPROTEIN E; CHEMOKINE; COMPLEMENT COMPONENT C3; INTERLEUKIN 1BETA; MITOGEN ACTIVATED PROTEIN KINASE 1; PROTEIN KINASE C BETA; SMALL INTERFERING RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA; AORTA SINUS; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DIABETES MELLITUS; GENE EXPRESSION PROFILING; IN VITRO STUDY; MACROPHAGE; MALE; MOLECULE; MONOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; STREPTOZOCIN DIABETES; VASCULITIS;

ANTIGENS, CD11C; ATHEROSCLEROSIS; DIABETES MELLITUS; INFLAMMATION; PKCΒ;

ANIMALS; ANTIGENS, CD11C; AORTITIS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; DIABETES MELLITUS, EXPERIMENTAL; DIABETIC ANGIOPATHIES; DISEASE MODELS, ANIMAL; GENE EXPRESSION; HUMANS; HYPERGLYCEMIA; HYPERLIPIDEMIAS; MACROPHAGES; MICE; MICE, KNOCKOUT; MONOCYTES; PROTEIN KINASE C; PROTEIN KINASE C BETA; SIGNAL TRANSDUCTION; U937 CELLS; VASCULITIS;

EID: 84881023410     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.301113     Document Type: Article

References (43)

1. Ruderman NB, Gupta S, Sussman I. Hyperglycemia, diabetes and vascular disease: an overview. In: Ruderman N, Williamson J, Brownlee M, eds. Hyperglycemia, Diabetes and Vascular Disease. New York, NY: Oxford University Press; 1992: 3-20.
2. Kannel WB, McGee DL. Diabetes and cardiovascular disease. The Framingham Study. JAMA. 1979;241: 2035-2038.
3. Ferreiro JL, Angiolillo DJ. Diabetes and antiplatelet therapy in acute coronary syndrome. Circulation. 2011;123: 798-813.
4. Lüscher TF, Creager MA, Beckman JA, Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: Part II. Circulation. 2003;108: 1655-1661.
5. Haffner SM, Mykkänen L, Festa A, Burke JP, Stern MP. Insulin-resistant prediabetic subjects have more atherogenic risk factors than insulinsensitive prediabetic subjects: implications for preventing coronary heart disease during the prediabetic state. Circulation. 2000;101: 975-980.
6. 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 U S A. 1992;89: 11059-11063.
7. Danis RP, Sheetz MJ. Ruboxistaurin: PKC-beta inhibition for complications of diabetes. Expert Opin Pharmacother. 2009;10: 2913-2925.
8. Kelly DJ, Zhang Y, Hepper C, Gow RM, Jaworski K, Kemp BE, Wilkinson-Berka JL, Gilbert RE. Protein kinase C beta inhibition attenuates the progression of experimental diabetic nephropathy in the presence of continued hypertension. Diabetes. 2003;52: 512-518.
9. Aiello LP. The potential role of PKC beta in diabetic retinopathy and macular edema. Surv Ophthalmol. 2002;47 (suppl 2):S263-S269.
10. Harja E, Chang JS, Lu Y, Leitges M, Zou YS, Schmidt AM, Yan SF. Mice deficient in PKCbeta and apolipoprotein E display decreased atherosclerosis. FASEB J. 2009;23: 1081-1091.
11. Yan SF, Lu J, Zou YS, Soh-Won J, Cohen DM, Buttrick PM, Cooper DR, Steinberg SF, Mackman N, Pinsky DJ, Stern DM. Hypoxia-associated induction of early growth response-1 gene expression. J Biol Chem. 1999;274: 15030-15040.
12. Yan SF, Lu J, Zou YS, Kisiel W, Mackman N, Leitges M, Steinberg S, Pinsky D, Stern D. Protein kinase C-beta and oxygen deprivation. A novel Egr-1-dependent pathway for fibrin deposition in hypoxemic vasculature. J Biol Chem. 2000;275: 11921-11928.
13. Fujita T, Asai T, Andrassy M, Stern DM, Pinsky DJ, Zou YS, Okada M, Naka Y, Schmidt AM, Yan SF. PKCbeta regulates ischemia/reperfusion injury in the lung. J Clin Invest. 2004;113: 1615-1623.
14. Yan SF, Fujita T, Lu J, Okada K, Shan Zou Y, Mackman N, Pinsky DJ, Stern DM. Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med. 2000;6: 1355-1361.
15. Harja E, Bucciarelli LG, Lu Y, Stern DM, Zou YS, Schmidt AM, Yan SF. Early growth response-1 promotes atherogenesis: mice deficient in early growth response-1 and apolipoprotein E display decreased atherosclerosis and vascular inflammation. Circ Res. 2004;94: 333-339.
16. Park L, Raman KG, Lee KJ, Lu Y, Ferran LJ Jr, Chow WS, Stern D, Schmidt AM. Suppression of accelerated diabetic atherosclerosis by the soluble receptor for advanced glycation endproducts. Nat Med. 1998;4: 1025-1031.
17. Bucciarelli LG, Wendt T, Qu W, Lu Y, Lalla E, Rong LL, Goova MT, Moser B, Kislinger T, Lee DC, Kashyap Y, Stern DM, Schmidt AM. RAGE blockade stabilizes established atherosclerosis in diabetic apolipoprotein E-null mice. Circulation. 2002;106: 2827-2835.
18. Bu DX, Rai V, Shen X, Rosario R, Lu Y, D'Agati V, Yan SF, Friedman RA, Nuglozeh E, Schmidt AM. Activation of the ROCK1 branch of the transforming growth factor-beta pathway contributes to RAGE-dependent acceleration of atherosclerosis in diabetic ApoE-null mice. Circ Res. 2010;106: 1040-1051.
19. Tomkin GH. Atherosclerosis, diabetes and lipoproteins. Expert Rev Cardiovasc Ther. 2010;8: 1015-1029.
20. Kanter JE, Johansson F, LeBoeuf RC, Bornfeldt KE. Do glucose and lipids exert independent effects on atherosclerotic lesion initiation or progression to advanced plaques? Circ Res. 2007;100: 769-781.
21. Mazzone T, Chait A, Plutzky J. Cardiovascular disease risk in type 2 diabetes mellitus: insights from mechanistic studies. Lancet. 2008; 371: 1800-1809.
22. Butcher MJ, Galkina EV. Phenotypic and functional heterogeneity of macrophages and dendritic cell subsets in the healthy and atherosclerosisprone aorta. Front Physiol. 2012;3:44.
23. Randolph GJ. The fate of monocytes in atherosclerosis. J Thromb Haemost. 2009;7 (suppl 1): 28-30.
24. Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis (*). Annu Rev Immunol. 2009;27: 165-197.
25. Cho HJ, Shashkin P, Gleissner CA, Dunson D, Jain N, Lee JK, Miller Y, Ley K. Induction of dendritic cell-like phenotype in macrophages during foam cell formation. Physiol Genomics. 2007;29: 149-160.
26. Sadhu C, Ting HJ, Lipsky B, Hensley K, Garcia-Martinez LF, Simon SI, Staunton DE. CD11c/CD18: novel ligands and a role in delayed-type hypersensitivity. J Leukoc Biol. 2007;81: 1395-1403.
27. Wu H, Gower RM, Wang H, Perrard XY, Ma R, Bullard DC, Burns AR, Paul A, Smith CW, Simon SI, Ballantyne CM. Functional role of CD11c+ monocytes in atherogenesis associated with hypercholesterolemia. Circulation. 2009;119: 2708-2717.
28. Paulson KE, Zhu SN, Chen M, Nurmohamed S, Jongstra-Bilen J, Cybulsky MI. Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Circ Res. 2010;106: 383-390.
29. Manthey HD, Zernecke A. Dendritic cells in atherosclerosis: functions in immune regulation and beyond. Thromb Haemost. 2011;106: 772-778.
30. McCaffrey TA, Fu C, Du B, Eksinar S, Kent KC, Bush H Jr, Kreiger K, Rosengart T, Cybulsky MI, Silverman ES, Collins T. High-level expression of Egr-1 and Egr-1-inducible genes in mouse and human atherosclerosis. J Clin Invest. 2000;105: 653-662.
31. Rokosh G. Heme Egr-1: new partners in atherosclerotic progression? Circ Res. 2008;102: 6-8.
32. Xu Y, Toure F, Qu W, Lin L, Song F, Shen X, Rosario R, Garcia J, Schmidt AM, Yan SF. Advanced glycation end product (AGE)-receptor for AGE (RAGE) signaling and up-regulation of Egr-1 in hypoxic macrophages. J Biol Chem. 2010;285: 23233-23240.
33. Andrassy M, Belov D, Harja E, Zou YS, Leitges M, Katus HA, Nawroth PP, Yan SD, Schmidt AM, Yan SF. Central role of PKCbeta in neointimal expansion triggered by acute arterial injury. Circ Res. 2005;96: 476-483.
34. Huang C, Chang JS, Xu Y, Li Q, Zou YS, Yan SF. Reduction of PKCbetaII activity in smooth muscle cells attenuates acute arterial injury. Atherosclerosis. 2010;212: 123-130.
35. López-Cabrera M, Nueda A, Vara A, García-Aguilar J, Tugores A, Corbí AL. Characterization of the p150,95 leukocyte integrin alpha subunit (CD11c) gene promoter. Identification of cis-acting elements. J Biol Chem. 1993;268: 1187-1193.
36. Nelken NA, Coughlin SR, Gordon D, Wilcox JN. Monocyte chemoattractant protein-1 in human atheromatous plaques. J Clin Invest. 1991;88: 1121-1127.
37. Wu H, Perrard XD, Wang Q, Perrard JL, Polsani VR, Jones PH, Smith CW, Ballantyne CM. CD11c expression in adipose tissue and blood and its role in diet-induced obesity. Arterioscler Thromb Vasc Biol. 2010;30: 186-192.
38. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 1993;362: 801-809.
39. Moyer CF, Sajuthi D, Tulli H, Williams JK. Synthesis of IL-1 alpha and IL-1 beta by arterial cells in atherosclerosis. Am J Pathol. 1991;138: 951-960.
40. Kleemann R, Zadelaar S, Kooistra T. Cytokines and atherosclerosis: a comprehensive review of studies in mice. Cardiovasc Res. 2008;79: 360-376.
41. Rezzonico R, Chicheportiche R, Imbert V, Dayer JM. Engagement of CD11b and CD11c beta2 integrin by antibodies or soluble CD23 induces IL-1beta production on primary human monocytes through mitogen-activated protein kinase-dependent pathways. Blood. 2000;95: 3868-3877.
42. Javey G, Schwartz SG, Flynn Jr HW, Aiello LP, Sheetz M. Ruboxistaurin: Review of safety and efficacy in the treatment of diabetic retinopathy. Clinical Medical Insights: Therapeutics. 2010;2:625-631
43. Clarke M, Dodson PM. PKC inhibition and diabetic microvascular complications. Best Pract Res Clin Endocrinol Metab. 2007;21: 573-586.