Selective insulin resistance and the development of cardiovascular diseases in diabetes: The 2015 Edwin Bierman Award Lecture

Diabetes

Volumn 65, Issue 6, 2016, Pages 1462-1471

  King, George L ^a   Park, Kyoungmin ^a   Li, Qian ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; INSULIN RECEPTOR; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VASCULOTROPIN; INSULIN;

ATHEROSCLEROSIS; AWARDS AND PRIZES; CARDIAC MUSCLE; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELLS; DISEASE ASSOCIATION; DISEASE COURSE; HEART BLOOD VESSEL; HUMAN; HYPERINSULINEMIA; INSULIN DEFICIENCY; INSULIN RESISTANCE; MACROPHAGE; MONOCYTE; PATHOPHYSIOLOGY; PERICYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; RODENT MODEL; SCIENTIST; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIUM; VASCULAR TISSUE; COMPLICATION; DIABETES MELLITUS; DIABETIC ANGIOPATHIES; DIABETIC CARDIOMYOPATHIES; HYPERINSULINISM; MASSACHUSETTS; METABOLISM; PHYSIOLOGY;

ATHEROSCLEROSIS; AWARDS AND PRIZES; BOSTON; DIABETES MELLITUS; DIABETIC ANGIOPATHIES; DIABETIC CARDIOMYOPATHIES; ENDOTHELIUM, VASCULAR; HUMANS; HYPERINSULINISM; INSULIN; INSULIN RESISTANCE; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84969820441     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db16-0152     Document Type: Review

References (69)

1. Rask-Madsen C, King GL. Vascular complications of diabetes: mechanisms of injury and protective factors. Cell Metab 2013;17:20-33
2. Kitada M, Zhang Z, Mima A, King GL. Molecular mechanisms of diabetic vascular complications. J Diabetes Investig 2010;1:77-89
3. The Diabetes Control and Complications Trial/Epidemiology of Diabetes Interventions and Complications Research Group. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. N Engl J Med 2000;342:381-389
4. Patel A, MacMahon S, Chalmers J, et al.; ADVANCE Collaborative Group. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 2008;358:2560-2572
5. Gerstein HC, Miller ME, Ismail-Beigi F, et al.; ACCORD Study Group. Effects of intensive glycaemic control on ischaemic heart disease: analysis of data from the randomised, controlled ACCORD trial. Lancet 2014;384:1936-1941
6. Duckworth W, Abraira C, Moritz T, et al.; VADT Investigators. Glucose control and vascular complications in veterans with type 2 diabetes. N Engl J Med 2009;360:129-139
7. Laakso M. Cardiovascular disease in type 2 diabetes from population to man to mechanisms: the Kelly West Award Lecture 2008. Diabetes Care 2010; 33:442-449
8. Livingstone SJ, Looker HC, Hothersall EJ, et al. Risk of cardiovascular disease and total mortality in adults with type 1 diabetes: Scottish registry linkage study. PLoS Med 2012;9:e1001321
9. Libby P, Ridker PM, Hansson GK. Progress and challenges in translating the biology of atherosclerosis. Nature 2011;473:317-325
10. Després JP, Lamarche B, Mauriège P, et al. Hyperinsulinemia as an independent risk factor for ischemic heart disease. N Engl J Med 1996;334:952-957
11. de Ferranti SD, de Boer IH, Fonseca V, et al. Type 1 diabetes mellitus and cardiovascular disease: a scientific statement from the American Heart Association and American Diabetes Association. Diabetes Care 2014;37:2843-2863
12. Gerstein HC, Bosch J, Dagenais GR, et al.; ORIGIN Trial Investigators. Basal insulin and cardiovascular and other outcomes in dysglycemia. N Engl J Med 2012;367:319-328
13. Rask-Madsen C, Buonomo E, Li Q, et al. Hyperinsulinemia does not change atherosclerosis development in apolipoprotein E null mice. Arterioscler Thromb Vasc Biol 2012;32:1124-1131
14. King GL, Johnson SM. Receptor-mediated transport of insulin across endothelial cells. Science 1985;227:1583-1586
15. Rask-Madsen C, King GL. Mechanisms of disease: endothelial dysfunction in insulin resistance and diabetes. Nat Clin Pract Endocrinol Metab 2007;3:46-56
16. Jialal I, Crettaz M, Hachiya HL, et al. Characterization of the receptors for insulin and the insulin-like growth factors on micro- and macrovascular tissues. Endocrinology 1985;117:1222-1229
17. Soos MA, Siddle K. Immunological relationships between receptors for insulin and insulin-like growth factor I. Evidence for structural heterogeneity of insulin-like growth factor I receptors involving hybrids with insulin receptors. Biochem J 1989;263:553-563
18. Virkamäki A, Ueki K, Kahn CR. Protein-protein interaction in insulin signaling and the molecular mechanisms of insulin resistance. J Clin Invest 1999;103:931-943
19. 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 2008;283:34327-34336
20. 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 2003;278:31964-31971
21. 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 2000;101:676-681
22. Rask-Madsen C, Li Q, Freund B, et al. Loss of insulin signaling in vascular endothelial cells accelerates atherosclerosis in apolipoprotein E null mice. Cell Metab 2010;11:379-389
23. Oliver FJ, de la Rubia G, Feener EP, et al. Stimulation of endothelin-1 gene expression by insulin in endothelial cells. J Biol Chem 1991;266:23251-23256
24. Nagai M, Kamide K, Rakugi H, et al. Role of endothelin-1 induced by insulin in the regulation of vascular cell growth. Am J Hypertens 2003;16:223-228
25. Schneider DJ, Absher PM, Ricci MA. Dependence of augmentation of arterial endothelial cell expression of plasminogen activator inhibitor type 1 by insulin on soluble factors released from vascular smooth muscle cells. Circulation 1997;96:2868-2876
26. Ward CW, Gough KH, Rashke M, Wan SS, Tribbick G, Wang J. Systematic mapping of potential binding sites for Shc and Grb2 SH2 domains on insulin receptor substrate-1 and the receptors for insulin, epidermal growth factor, platelet-derived growth factor, and fibroblast growth factor. J Biol Chem 1996; 271:5603-5609
27. 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 1999;104:447-457
28. Barrett EJ, Liu Z. The endothelial cell: an "early responder" in the development of insulin resistance. Rev Endocr Metab Disord 2013;14:21-27
29. Wang H, Wang AX, Barrett EJ. Caveolin-1 is required for vascular endothelial insulin uptake. Am J Physiol Endocrinol Metab 2011;300:E134-E144
30. Wang H, Wang AX, Aylor K, Barrett EJ. Caveolin-1 phosphorylation regulates vascular endothelial insulin uptake and is impaired by insulin resistance in rats. Diabetologia 2015;58:1344-1353
31. 2+ but requires phosphorylation by Akt at Ser(1179). J Biol Chem 2001;276:30392-30398
32. King GL, Buzney SM, Kahn CR, et al. Differential responsiveness to insulin of endothelial and support cells from micro- and macrovessels. J Clin Invest 1983; 71:974-979
33. Wilhelm K, Happel K, Eelen G, et al. FOXO1 couples metabolic activity and growth state in the vascular endothelium. Nature 2016;529:216-220
34. Huang PL. eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol Metab 2009;20:295-302
35. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 1987;327: 524-526
36. Furchgott RF, Zawadzki JV. The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature 1980;288:373-376
37. Wang H, Wang AX, Liu Z, Chai W, Barrett EJ. The trafficking/interaction of eNOS and caveolin-1 induced by insulin modulates endothelial nitric oxide production. Mol Endocrinol 2009;23:1613-1623
38. Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocr Rev 2007;28:463-491
39. King GL, Goodman AD, Buzney S, Moses A, Kahn CR. Receptors and growth-promoting effects of insulin and insulinlike growth factors on cells from bovine retinal capillaries and aorta. J Clin Invest 1985;75:1028-1036
40. Begum N, Sandu OA, Duddy N. Negative regulation of rho signaling by insulin and its impact on actin cytoskeleton organization in vascular smooth muscle cells: role of nitric oxide and cyclic guanosine monophosphate signaling pathways. Diabetes 2002;51:2256-2263
41. Takeya K, Wang X, Sutherland C, et al. Involvement of myosin regulatory light chain diphosphorylation in sustained vasoconstriction under pathophysiological conditions. J Smooth Muscle Research 2014;50:18-28
42. Yokota T, Ma RC, Park JY, et al. Role of protein kinase C on the expression of platelet-derived growth factor and endothelin-1 in the retina of diabetic rats and cultured retinal capillary pericytes. Diabetes 2003;52:838-845
43. Hopfner RL, Hasnadka RV, Wilson TW, McNeill JR, Gopalakrishnan V. Insulin increases endothelin-1-evoked intracellular free calcium responses by increased ET(A) receptor expression in rat aortic smooth muscle cells. Diabetes 1998;47:937-944
44. Fujita N, Furukawa Y, Du J, et al. Hyperglycemia enhances VSMC proliferation with NF-κB activation by angiotensin II and E2F-1 augmentation by growth factors. Mol Cell Endocrinol 2002;192:75-84
45. Geraldes P, Hiraoka-Yamamoto J, Matsumoto M, et al. Activation of PKC-δ and SHP-1 by hyperglycemia causes vascular cell apoptosis and diabetic retinopathy. Nat Med 2009;15:1298-1306
46. Mita T, Azuma K, Goto H, et al. IRS-2 deficiency in macrophages promotes their accumulation in the vascular wall. Biochem Biophys Res Commun 2011; 415:545-550
47. Han S, Liang CP, DeVries-Seimon T, et al. Macrophage insulin receptor deficiency increases ER stress-induced apoptosis and necrotic core formation in advanced atherosclerotic lesions. Cell Metab 2006;3:257-266
48. Abel ED, O'Shea KM, Ramasamy R. Insulin resistance: metabolic mechanisms and consequences in the heart. Arterioscler Thromb Vasc Biol 2012;32:2068-2076
49. Jia G, DeMarco VG, Sowers JR. Insulin resistance and hyperinsulinaemia in diabetic cardiomyopathy. Nat Rev Endocrinol 2016;12:144-153
50. Gray S, Kim JK. New insights into insulin resistance in the diabetic heart. Trends Endocrinol Metab 2011;22:394-403
51. Belke DD, Betuing S, Tuttle MJ, et al. Insulin signaling coordinately regulates cardiac size, metabolism, and contractile protein isoform expression. J Clin Invest 2002;109:629-639
52. 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 2006;26:787-793
53. 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 2002;105:373-379
54. Khamaisi M, Katagiri S, Keenan H, et al. PKCδ inhibition normalizes the wound-healing capacity of diabetic human fibroblasts. J Clin Invest 2016;126:837-853
55. Sun XJ, Goldberg JL, Qiao LY, Mitchell JJ. Insulin-induced insulin receptor substrate-1 degradation is mediated by the proteasome degradation pathway. Diabetes 1999;48:1359-1364
56. Hirashima Y, Tsuruzoe K, Kodama S, et al. Insulin down-regulates insulin receptor substrate-2 expression through the phosphatidylinositol 3-kinase/Akt pathway. J Endocrinol 2003;179:253-266
57. Haruta T, Uno T, Kawahara J, et al. A rapamycin-sensitive pathway down-regulates insulin signaling via phosphorylation and proteasomal degradation of insulin receptor substrate-1. Mol Endocrinol 2000;14:783-794
58. White MF. IRS proteins and the common path to diabetes. Am J Physiol Endocrinol Metab 2002;283:E413-E422
59. Maeno Y, Li Q, Park K, et al. Inhibition of insulin signaling in endothelial cells by protein kinase C-induced phosphorylation of p85 subunit of phosphatidylinositol 3-kinase (PI3K). J Biol Chem 2012;287:4518-4530
60. Kubota T, Kubota N, Kumagai H, et al. Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab 2011;13:294-307
61. Park K, Li Q, Rask-Madsen C, et al. Serine phosphorylation sites on IRS2 activated by angiotensin II and protein kinase C to induce selective insulin resistance in endothelial cells. Mol Cell Biol 2013;33:3227-3241
62. Boden G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM. Diabetes 1997;46:3-10
63. Nakatani Y, Kaneto H, Kawamori D, et al. Modulation of the JNK pathway in liver affects insulin resistance status. J Biol Chem 2004;279: 45803-45809
64. Solinas G, Naugler W, Galimi F, Lee MS, Karin M. Saturated fatty acids inhibit induction of insulin gene transcription by JNK-mediated phosphorylation of insulin-receptor substrates. Proc Natl Acad Sci U S A 2006;103:16454-16459
65. Gual P, Grémeaux T, Gonzalez T, Le Marchand-Brustel Y, Tanti JF. MAP kinases and mTOR mediate insulin-induced phosphorylation of insulin receptor substrate-1 on serine residues 307, 612 and 632. Diabetologia 2003;46:1532-1542
66. Fernández-Hernando C, Ackah E, Yu J, et al. Loss of Akt1 leads to severe atherosclerosis and occlusive coronary artery disease. Cell Metab 2007;6:446-457
67. Tsuchiya K, Tanaka J, Shuiqing Y, et al. FoxOs integrate pleiotropic actions of insulin in vascular endothelium to protect mice from atherosclerosis. Cell Metab 2012;15:372-381
68. Kong L, Shen X, Lin L, et al. PKCβ promotes vascular inflammation and acceleration of atherosclerosis in diabetic ApoE null mice. Arterioscler Thromb Vasc Biol 2013;33:1779-1787
69. Li Q, Park K, Li C, et al. Induction of vascular insulin resistance and endothelin-1 expression and acceleration of atherosclerosis by the overexpression of protein kinase C-β isoform in the endothelium. Circ Res 2013; 113:418-427