The role of IGF-1 resistance in obesity and type 2 diabetes-mellitus- related insulin resistance and vascular disease

Expert Opinion on Therapeutic Targets

Volumn 14, Issue 12, 2010, Pages 1333-1342

  Gatenby, Victoria K ^a   Kearney, Mark T ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

atherosclerosis; diabetes; IGF 1; insulin; nitric oxide

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; INSULIN; NITRIC OXIDE; PIOGLITAZONE; ROSIGLITAZONE; SOMATOMEDIN BINDING PROTEIN 1;

ATHEROSCLEROSIS; BIOAVAILABILITY; DISEASE COURSE; DRUG SAFETY; DYSLIPIDEMIA; HUMAN; HYPERCHOLESTEROLEMIA; HYPERCOAGULABILITY; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPERTENSION; INSULIN RESISTANCE; INSULIN SENSITIVITY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; REVIEW;

ANIMALS; ATHEROSCLEROSIS; CARDIOVASCULAR DISEASES; DIABETES MELLITUS, TYPE 2; ENDOTHELIUM, VASCULAR; HUMANS; HYPOGLYCEMIC AGENTS; INSULIN; INSULIN RESISTANCE; INSULIN-LIKE GROWTH FACTOR I; MALE; MOLECULAR TARGETED THERAPY; NITRIC OXIDE; OBESITY; RISK FACTORS; TREATMENT OUTCOME; VASCULAR DISEASES;

EID: 78249289434     PISSN: 14728222     EISSN: None     Source Type: Journal    
DOI: 10.1517/14728222.2010.528930     Document Type: Review

References (94)

1. World Health Organisation Facts and figures. Geneva, Switzerland: World Health Organization, 2010. Available from: http://www.who.int/diabetes/facts/en/ index.html [Last accessed 4 October 2010]
2. Booth GL, Kapral MK, Fung K, Tu JV. Relation between age and cardiovascular disease in men and women with diabetes compared with non-diabetic people: a population-based retrospective cohort study. Lancet 2006;368:29-36
3. Madala MC, Franklin BA, Chen AY, et al. Obesity and age of first non-ST-segment elevation myocardial infarction. J Am Coll Cardiol 2008;52:979-85
4. Cubbon RM, Rajwani A, Abbas A, et al. Hyperglycaemia, in relation to sex, and mortality after acute coronary syndrome. Eur J Cardiovasc Prev Rehabil 2007;14:666-71
5. Cubbon RM, Wheatcroft SB, Grant PJ, et al. Temporal trends in mortality of patients with diabetes mellitus suffering acute myocardial infarction: a comparison of over 3000 patients between 1995 and 2003. Eur Heart J 2007;28:540-5
6. Cubbon RM, Gale CP, Rajwani A, et al. Aspirin and mortality in patients with diabetes sustaining acute coronary syndrome. Diabetes Care 2008;31:363-5
7. Cubbon R, Abbas A, Wheatcroft SB, et al. Diabetes Mellitus and mortality after acute coronary syndrome as a first or recurrent cardiovascular event. PLoS ONE 2008;3: e3483
8. Gerstein HC, Miller ME, Byington RP, et al. Effects of intensive glucose lowering in type 2 diabetes. N Engl J Med 2008;358:2545-59 •• A study showing failure of intensive glucose lowering to reduce cardiovascular mortality in patients with type 2 diabetes.
9. Patel A, MacMahon S, Chalmers J, et al. Intensive blood glucose control and vascular outcomes in patients with type 2 diabetes. N Engl J Med 2008;358:2560-72 •• A study showing failure of intensive glucose lowering to reduce cardiovascular mortality in patients with type 2 diabetes.
10. Duckworth W, Abraira C, Moritz T, et al. Intensive glucose control and complications in American veterans with type 2 diabetes. N Engl J Med 2009;360:129-39
11. Wheatcroft SB, Williams IL, Shah AM, Kearney MT. Pathophysiological implications of insulin resistance on vascular endothelial function. Diabet Med 2003;20:255-68
12. Semenkovich CF. Insulin resistance and atherosclerosis. J Clin Invest 2006;116:1813-22
13. Fornengo P, Bosio A, Epifani G, et al. Prevalence of silent myocardial ischaemia in new-onset middle-aged type 2 diabetic patients without other cardiovascular risk factors. Diabet Med 2006;23:775-9
14. Pyorala M, Miettinen H, Halonen P, et al. Insulin resistance syndrome predicts the risk of coronary heart disease and stroke in healthy middle-aged men: the 22-year follow up of the Helsinki Policeman Study. Arteriosclerosis Thromb Vasc Biol 2000;20:538-44
15. Pyorala M, Miettinen H, Laakso M, et al. Hyperinsulinaemia predicts coronary artery disease risk in healthy middle-aged men: the 22-year follow up results of the Helsinki Policeman Study. Circulation 1998;98:398-404
16. Kahn CR, Chen L, Cohen SE. Unravelling the mechanism of action of thiazolidinediones. J Clin Invest 2000;106:1305-7
17. Dormandy JA, Charbonnei B, Eckland DJ, et al. Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial. Lancet 2005;366:1279-89 •• A study showing the effect of the thiazolidinedione pioglitazone on total and cardiovascular mortality in patients with type 2 diabetes.
18. Home PD, Pocock SJ, Beck-Nielsen H, et al. RECORD Study Team Rosiglitazone evaluated for cardiovascular outcomes in oral agent combination therapy for type 2 diabetes (RECORD): a multicentre, randomised, open-label trial. Lancet. 2009;373:2125-35 •• A study showing the effect of the thiazolidinedione roziglitazone on total and cardiovascular mortality in patients with type 2 diabetes.
19. Nissen SE, Wolski K. Effect of rosiglitazone on the risk of myocardial infarction and death from cardiovascular causes. N Engl J Med 2007;356:2457-71
20. van Genugten RE, van Raalte DH, Diamant M. Does glucagon-like peptide 1 receptor agonist therapy add value in the treatment of type 2 diabetes? focus on exanatide. Diabetes Res Clin Prac 2009; (Suppl 1): S26-34
21. ™) trial. Expert Rev Endocrinol Met 2009;4:119-29
22. Ross R. Atherosclerosis is an inflammatory disease. N Eng J Med 1999;340:115-26 ••A seminal description of the pathophysiology of atherosclerosis.
23. Rader D, Daugherty A. Translating molecular discoveries into new therapies for atherosclerosis. Nature 2008;451:904-13
24. Creager MA, Cooke JP, Mendelsohn ME, et al. Impaired vasodilation of forearm resistance vessels in hypercholesterolaemic humans. J Clin Invest 1990;86:228-34
25. Clapp BR, Hingorani AD, Kharbanda RK, et al. Inflammation-induced endothelial dysfunction involves reduced nitric oxide bioavailability and increased oxidant stress. Cardiovasc Res 2004;64:172-8
26. Tanner FC, Meier P, Greutert H, et al. Nitric oxide modulates expression of cell cycle regulatory proteins: a cytostatic strategy for inhibition of human vascular smooth muscle cell proliferation. Circulation 2000;101:1982-9
27. Monastyrskaya E, Folarin N, Malyshev, et al. Application of the nitric oxide donor SNAP to cardiomyocytes in culture provides protection against oxidative stress. Nitric Oxide 2002;7:127-31
28. Schafer A, Wiesmann F, Neubauer S, et al. Rapid regulation of platelet activation in vivo by nitric oxide. Circulation 2004;109:1819-22
29. Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 2000;101:1899-906
30. Bugiardini R, Manfrini O, Pizzi C, et al. Endothelial function predicts future development of coronary artery disease: a study of women with chest pain and normal coronary angiograms. Circulation 2004;109:2518-23
31. Imrie H, Abbas A, Kearney M. Insulin resistance lipotoxicity and endothelial dysfunction. Biochim Biophys Acta 2010;1801:320-6
32. Kearney MT, Duncan ER, Kahn M, Wheatcroft SB. Insulin resistance and endothelial cell dysfunction: studies in mammalian models. Exp Physiol 2008;93:158-63
33. Murphy C, Kanaganayagam GS, Jiang B, et al. Vascular dysfunction and reduced circulating endothelial progenitor cells in young healthy UK South Asian men. Arterioscler Thromb Vasc Biol 2007;27:936-42
34. Cubbon R, Murgatroyd SR, Ferguson C, et al. Human exercise induced circulating progenitor cell mobilisation is nitric oxide dependent and is blunted in South Asian Men. Arterioscler Thromb Vasc Biol 2010;30:878-84
35. Williams IL, Chowienczyk PJ, Wheatcroft SB, et al. Fat distribution and endothelial function in healthy humans diabetes obesity and metabolism. Diabetes Obes Metab 2006;8:296-301
36. Melikian N, Chowienczyk P, MacCarthy PA, et al. Determinants of endothelial function in asymptomatic subjects with and without the metabolic syndrome. Atherosclerosis 2008;197:375-82
37. Williams IL, Chowienczyk PJ, Wheatcroft S, et al. Endothelial function and weight loss in obese humans. Obes Surg 2005;15:1055-60
38. Melikian N, Shah AM, Thomas MR, et al. Independent determinants of coronary microvascular function in patients with metabolic syndrome and stable coronary artery disease. Eur Heart J 2008;29(Suppl 1): P625
39. Melikian N, Kearney MT, Thomas MR, et al. A simple thermodilution technique to assess coronary endothelium-dependent microvascular function in humans: validation and comparison with coronary flow reserve. Eur Heart J 2007;28:2188-94
40. Momin A, Melikian N, Wheatcroft SB, et al. The association between saphenous vein endothelial function, systemic inflammation, and statin therapy in patients undergoing coronary artery bypass surgery. J Thorac Cardiovasc Surg 2007;134:335-41
41. Steinberg HO, Chaker H, Leaming R, et al. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest 1996;97:2601-10
42. Laine H, Yki-Jarvinen H, Kirvela O, et al. Insulin resistance of glucose uptake in skeletal muscle cannot be ameliorated by enhancing endothelium-dependent blood flow in obesity. J Clin Invest 1998;101:1156-62
43. Tack CJ, Ong MK, Lutterman JA, Smits P. Insulin-induced vasodilatation and endothelial function in obesity/insulin resistance. Effects of troglitazone. Diabetologia 1998;41:569-76
44. Westerbacka J, Vehkavaara S, Bergholm R, et al. Marked resistance of the ability of insulin to decrease arterial stiffness characterizes human obesity. Diabetes 1999;48:821-7
45. Noronha BT, Li J-M, Wheatcroft SB, et al. Inducible nitric oxide synthase has divergent effects on vascular and metabolic function in obesity. Diabetes 2005;54:1082-9
46. Wheatcroft SB, Shah AM, Li J-M, et al. Preserved glucoregulation but attenuation of the vascular actions of insulin in mice heterozygous for knockout of the insulin receptor. Diabetes 2004;53:2645-52
47. Duncan ER, Walker SJ, Ezzat VA, et al. Accelerated endothelial dysfunction in mild prediabetic insulin resistance: the early role of reactive oxygen species. Am J Physiol Endocrinol Metab 2007;293: E1311-19
48. Moller DE, Yokota A, White MF, et al. A naturally occurring mutation of insulin receptor alanine 1134 impairs tyrosine kinase function and is associated with dominantly inherited insulin resistance. J Biol Chem 1990;265:14979-85
49. Duncan ER, Crossey P, Walker S, et al. The effect of endothelium specific insulin resistance on endothelial function in vivo. Diabetes 2008;57:3307-14
50. Wolff S, Ma H, Burch D, et al. SMK-1, an essential regulator of DAF-16-mediated longevity. Cell 2006;124:1039-53
51. Dillin A, Crawford DK, Kenyon C. Timing requirements for insulin/IGF-1 signaling in C. elegans. Science 2002;298:830-4
52. Wheatcroft SB, Kearney MT. IGF-dependent and IGF-independent actions of IGF-binding protein-1 and-2: implications for metabolic homeostasis. Trends Endocrinol Metab 2009;20:153-62
53. Juul A, Scheike T, Davidsen M, et al. Low serum insulin-like growth factor I is associated with increased risk of ischemic heart disease: a population-based casecontrol study. Circulation 2002;106:939-944
54. Laughlin G, Barrett-Connor E, Criqui MH, et al. The prospective association of serum insulin-like growth factor I (IGF-I) and IGF-binding protein-1 levels with all cause and cardiovascular disease mortality in older adults: The Rancho Bernardo Study. J Clin Endocrinol Metab 2004;89:114-20
55. Vaessen N, Heutlink P, Janssen JA, et al. A polymorphism in the gene for IGF-1: functional properties and risk for type 2 diabetes and myocardial infarction. Diabetes 2001;50:637-42 •• A study showing the effect of IGF-1 polymorphism on the development of diabetes and acute myocardial infarction.
56. Du J, Peng T, Scheidegger KJ, et al. Angiotensin II activation of insulin like growth factor 1 receptor transcription is mediated by a tyrosine kinase-dependent redox-sensitive mechanism. Arterioscler Thromb Vasc Biol 1999;19:2119-26
57. Okura Y, Brink M, Zahid AA, et al. Decreased expression of insulin-like growth factor-1 and apoptosis of vascular smooth muscle cells in human atherosclerotic plaque. J Mol Cell Cardiol 2001;33:1777-89
58. Niu XL, Hakim ZS, Rojas M, et al. Leukocyte antigen-related deficiency enhances insulin-like growth factor-1 signaling in vascular smooth muscle cells and promotes neointima formation in response to vascular injury. J Biol Chem 2007;282:19808-19
59. Sukhanov S, Higashi Y, Shai SY, et al. IGF-1 reduces inflammatory responses, suppresses oxidative stress, and decreases atherosclerosis progression in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 2007;27:2684-90
60. Chisalita SI, Arnquist HJ. Insulin-like growth factor 1 receptors are more abundant than insulin receptors in human micro-and macrovascular endothelial cells. Am J Physiol Endocrinol Metab 2004;286: E896-901
61. Zeng G, Quon MJ. Insulin-stimulated production of nitric oxide is inhibited by wortmannin. Direct measurement in vascular endothelial cells. J Clin Invest 1996;98:894-8 •• The first study, to our knowledge, showing the ability of insulin and IGF-1 to stimulate NO production in endothelial cells.
62. Copeland KC, Nair KS. Recombinant human insulin-like growth factor-1 increases forearm blood flow. J Clin Endocrinol Metab 1994;79:230-2
63. McCallum RW, Hamilton CA, Graham D, et al. Vascular responses to IGF-I and insulin are impaired in aortae of hypertensive rats. J Hypertens 2005;23:351-8
64. Hasdai D, Nielsen MF, Rizza RA, et al. Attenuated in vitro coronary arteriolar vasorelaxation to insulin-like growth factor-I in experimental hypercholesterolaemia. Hypertension 1999;34:89-95
65. Imrie H, Abbas A, Viswambharan H, et al. Vascular insulin-like growth factor-I resistance and diet-induced obesity. Endocrinology 2009;150:4575-82
66. Kim JJ, Accili D. Signalling through IGF-I and insulin receptors: where is the specificity? Growth Horm IGF Res 2002;12:84-90
67. Li G, Barrett EJ, Wang H, et al. Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/IGF-I hybrid receptors in endothelial cells. Endocrinology 2005;146:4690-6
68. Wang H, Liu Z, Li G, Barrett EJ. The vascular endothelial cell mediates insulin transport into skeletal muscle. Am J Physiol Endocrinol Metab 2006;291: E323-32
69. Wang H, Wang AX, Zhenqi Liu Z, Barrett EJ. Insulin signaling stimulates insulin transport by bovine aortic endothelial cells. Diabetes 2008;57:540-7
70. 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 2003;111:1373-80
71. Kondo T, Vicent D, Suzuma K, et al. Knockout of insulin and IGF-1 receptors on vascular endothelial cells protects against retinal neovascularization. J Clin Invest 2003;111:1835-42
72. Li G, Barrett EJ, Ko S-H, et al. Insulin and insulin-like growth factor-I receptors differentially mediate insulin-stimulated adhesion molecule production by endothelial cells. Endocrinology 2009;150:3475-82
73. Holzenberger M, Dupont J, Ducos B, et al. IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 2003;421:182-7 •• A study showing the effect of the IGF-1 receptor deficiency on longevity in mice.
74. Suh Y, Atzmon G, Cho MO, et al. Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci USA 2008;105:3438-42 •• A study showing the effect of the IGF-1 receptor deficiency on longevity in humans.
75. De Meyts P, Whittaker J. Structural biology of insulin and IGF1 receptors: implications for drug design Nat. Rev Drug Disc 2002;1:769-83
76. Federici M, Porzio O, Lauro D, et al. Increased abundance of insulin/insulinlike growth factor-I hybrid receptors in skeletal muscle of obese subjects is correlated with in vivo insulin sensitivity. J Clin Endocrinol Metab 1998;83:2911-15
77. Chisalita SI, Nitert MD, Arnqvist HJ. IGF-I/insulin hybrid receptors in human endothelial cells. Growth Horm IGF Res 2006;16:258-66
78. Nitert MD, Chisalita SI, Olsson K, et al. IGF-I/insulin hybrid receptors in human endothelial cells. Mol Cell Endocrinol 2005;229:31-7 • A study showing thepresence of IGF-1/insulin receptor hybrids in endothelial cells.
79. Chisalita SI, Arnqvist HJ. Insulin-like growth factor I receptors are more abundant than insulin receptors in human micro-and macrovascular endothelial cells. Am J Physiol Endocrinol Metab 2004;286: E896-901
80. Ward CW, Lawrence MC, Streltsov VA, et al. The insulin and IGF receptor structures: new insights into ligand-induced receptor activation. Trends Biochem Sci 2007;32:129-37
81. Fulzele K, DiGirolamo DJ, Liu Z, et al. Disruption of the insulin-like growth factor type 1 receptor in osteoblasts enhances insulin signaling and action. J Biol Chem 2007;282:25649-58
82. Zhang H, Pelzer AM, Kiang DT, Yee D. Down-regulation of type I insulin-like growth factor receptor increases sensitivity of breast cancer cells to insulin. Cancer Res 2007;67:391-7
83. Entingh-Pearsall A, Kahn CR. Differential roles of the insulin and insulin-like growth factor-I (IGF-I) receptors in response to insulin and IGF-I. J Biol Chem 2004;279:38016-24
84. Engberding N, San Martín A, Martin-Garrido A, et al. Insulin-like growth factor-1 receptor expression masks the antiinflammatory and glucose uptake capacity of insulin in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol 2009;29:408-15 • A study showing the ability of the IGF-1 receptor deficiency to enhance insulin sensitivity in vascular smooth muscle cells.
85. Raile K, Schneider A, Keller A, et al. Clinical and functional characteristics of the human Arg59Ter insulin-like growth factor 1 receptor (IGF1R) mutation: implications for a gene dosage effect of the human IGF1R. J Clin Endocrinol Metab 2006;91:2264-71 • A study showing the effect of a polymorphism leading to IGF-1 receptor deficiency on insulin sensitivity in humans.
86. RHIGF-1 In NIDDM Study Group. Evidence from a dose ranging study that recombinant insulin like growth factor-1 (IGF-1) effectively and safely improves glycaemic control in type II diabetes. Diabetes 1996;45: (Suppl 2) 27A
87. Moses AC, Young SC, Morrow LA, et al. Recombinant human insulin like growth factor 1 increases insulin sensitivity and improves glycaemic control in type II diabetes. Diabetes 1996;45:91-100 • A study showing the effect of IGF-1 on insulin sensitivity in patients with type 2 diabetes.
88. Schwartz SL. RHIGF1 co-therapy with insulin Subgroup. RHIGF1 improves glucose control in insulin requiring type 2 diabetes (abstract 582.). Proc 5th Annu Meeting Am Diabetes Assoc. San Antonio Texas, USA; 1997
89. Clemmons DR, Moses AC, Sommer A, et al. Rh/IGF-1/rhIGFBP-3 administration to patients with type 2 diabetes mellitus reduces insulin requirements while also lowering fasting glucose. Growth Horm IGF Res 2005;15:265-74
90. Wheatcroft SB, Kearney MT, Shah AM, et al. Vascular endothelial function and blood pressure homeostasis in mice overexpressing IGF binding protein-1. Diabetes 2003;52:2075-82
91. Pollak M. Targeting insulin and insulin-like growth factor signalling in oncology. Curr Opin Pharmacol 2008;8:384-92
92. Bahr C, Groner B. The insulin like growth factor-1 receptor (IGF-1R) as a drug target: novel approaches to cancer therapy. Growth Horm IGF-1 Res 2004;14:287-95
93. Yee D. Targeting insulin-like growth factor pathways. Br J Cancer 2006;94:465-8
94. Abbas A, Imrie H, Viswambharan H, et al. IGF-1 Receptor and insulin receptor stoichiometry is a critical determinant of nitric oxide bioavailablity in-vivo. Circulation 2009;120: S1161