Role of IGF-1 in glucose regulation and cardiovascular disease

Expert Review of Cardiovascular Therapy

Volumn 6, Issue 8, 2008, Pages 1135-1149

  Abbas, Afrose ^a   Grant, Peter J ^a   Kearney, Mark T ^a  

^a UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Cardiovascular disease; Growth hormone; Growth hormone deficiency; Heart failure; IGF 1; Insulin resistance; Type 2 diabetes

Indexed keywords

ANGIOTENSIN II; C REACTIVE PROTEIN; CARDIOVASCULAR AGENT; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE TRANSPORTER 4; HEAT SHOCK PROTEIN 60; INSULIN; INSULIN RECEPTOR; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; NITRIC OXIDE; PHOSPHATIDYLINOSITOL 3 KINASE; PLACEBO; RECOMBINANT GROWTH HORMONE; RECOMBINANT SOMATOMEDIN BINDING PROTEIN 3; RECOMBINANT SOMATOMEDIN C; RESISTIN; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR; SOMATOSTATIN DERIVATIVE; UNCLASSIFIED DRUG;

APOPTOSIS; ATHEROSCLEROSIS; CARDIOMYOPATHY; CARDIOVASCULAR DISEASE; CARDIOVASCULAR RISK; CELL FUNCTION; CELL MIGRATION; CELL PROLIFERATION; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; DIABETES MELLITUS; DOWN REGULATION; DRUG POTENTIATION; DRUG SAFETY; ENZYME POLYMORPHISM; ENZYME REGULATION; GENE TRANSFER; GLUCONEOGENESIS; GLUCOSE METABOLISM; GLYCEMIC CONTROL; GROWTH HORMONE DEFICIENCY; HEART FAILURE; HEART FUNCTION; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART MUSCLE CELL; HUMAN; HYPOGLYCEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN SYNTHESIS; LOW DRUG DOSE; MONOTHERAPY; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PATHOPHYSIOLOGY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; RECEPTOR AFFINITY; REVIEW; SIGNAL TRANSDUCTION; SYSTEMIC VASCULAR RESISTANCE;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; BLOOD GLUCOSE; CARDIOVASCULAR DISEASES; DIABETIC ANGIOPATHIES; ENDOTHELIUM, VASCULAR; GROWTH HORMONE; HEART FAILURE; HUMANS; INSULIN RESISTANCE; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 1; INSULIN-LIKE GROWTH FACTOR I; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, CARDIAC; PANCREAS; RECEPTOR, IGF TYPE 1; STEM CELLS;

EID: 55249100997     PISSN: 14779072     EISSN: 17448344     Source Type: Journal    
DOI: 10.1586/14779072.6.8.1135     Document Type: Review

References (201)

1. Wilson PW. Diabetes mellitus and coronary heart disease. Am. J. Kidney Dis. 32(5 Suppl. 3), S89-S100 (1998).
2. Smith JW, Marcus FI, Serokman R. Prognosis of patients with diabetes mellitus after acute myocardial infarction. Am. J. Cardiol. 54(7), 718-721 (1984).
3. Stamler J, Vaccaro O, Neaton JD, Wentworth D. Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 16(2), 434-444 (1993).
4. 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. 28(5), 540-545 (2007).
5. Cubbon RM, Gale CP, Rajwani A et al. Aspirin and mortality in patients with diabetes mellitus sustaining acute coronary syndrome. Diabetes Care 31(2), 363-365 (2007).
6. Muniyappa R, Montagnani M, Koh KK, Quon MJ. Cardiovascular actions of insulin. Endocr. Rev. 28(5), 463-491 (2007).
7. Qatanani M, Lazar MA. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev. 21(12), 1443-1455 (2007).
8. Haffner SM, Stern MP, Hazuda HP, Mitchell BD, Patterson JK. Cardiovascular risk factors in confirmed prediabetic individuals. Does the clock for coronary heart disease start ticking before the onset of clinical diabetes? JAMA 263 (21), 2893-2898 (1990).
9. Bartnik M, Norhammar A, Ryden L. Hyperglycaemia and cardiovascular disease. J. Intern. Med. 262 (2), 145-156 (2007).
10. Hartge MM, Unger T, Kintscher U. The endothelium and vascular inflammation in diabetes. Diab. Vasc. Dis. Res. 4(2), 84-88 (2007).
11. Jansson PA. Endothelial dysfunction in insulin resistance and Type 2 diabetes. J. Intern. Med. 262(2), 173-183 (2007).
12. 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).
13. Grant PJ. Diabetes mellitus as a prothrombotic condition. J. Intern. Med. 262(2), 157-172 (2007).
14. Daughaday WH, Rotwein P. Insulin-like growth factors I and II. Peptide, messenger ribonucleic acid and gene structures, serum and tissue concentrations. Endocr. Rev. 10, 68-91 (1989).
15. Avruch J. Insulin and amino-acid regulation of mTOR signalling and kinase activity through the Rheb GTPase. Oncogene 25, 6361-6372 (2006).
16. Le Roith D. Seminars in medicine of the Beth Israel Deaconess Medical Center. Insulin-like growth factors. N. Engl. J. Med. 336(9), 633-640 (1997).
17. Riedemann J, Macaulay VM. IGF1R signalling and its inhibition. Endocr. Relat. Cancer 1, 533-543 (2006).
18. De Meyts P. Role of time factor in signalling specificity: application to mitogenic and metabolic signalling by the insulin and insulin-like growth factor-I receptor tyrosine kinases. Metabolism 44, 2-11 (1995).
19. Clemmons D. Involvement of insulin-like growth factor-I in the control of glucose homeostasis. Curr. Opin. Pharmacol. 6(6), 620-625 (2006).
20. Caro JF, Poulos J, Ittoop O, Pories WJ, Flickinger EG, Sinha MK. Insulin-like growth factor I binding in hepatocytes from human liver, human hepatoma, and normal, regenerating, and fetal rat liver. J. Clin. Invest. 81(4), 976-981 (1988).
21. Nitert MD, Chisalita SI, Olsson K, Bornfeldt KE, Arnqvist HJ. IGF-I/ insulin hybrid receptors in human endothelial cells. Mol. Cell. Endocrinol. 229(1-2), 31-37 (2005).
22. Soos MA, Field CE, Siddle K. Purified hybrid insulin/insulin-like growth factor-I receptors bind insulin-like growth factor-I, but not insulin, with high affinity. Biochem. J. 290(Pt 2), 419-426 (1993).
23. Bailyes EM, Nave BT, Soos MA, Orr SR, Hayward AC, Siddle K. Insulin receptor/IGF-I receptor hybrids are widely distributed in mammalian tissues: quantification of individual receptor species by selective immunoprecipitation and immunoblotting. Biochem. J. 327(Pt 1), 209-215 (1997).
24. Li G, Barrett EJ, Wang H, Chai W, Liu Z. 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 146 (11), 4690-4696 (2005).
25. Federici M, Porzio O, Lauro D et al. Increased abundance of insulin/insulin-like growth factor-I hybrid receptors in skeletal muscle of obese subjects is correlated with in vivo insulin sensitivity. J. Clin. Endocrinol. Metab. 83(8), 2911-2915 (1998).
26. Federici M, Porzio O, Zucaro L et al. Increased abundance of insulin/IGF-I hybrid receptors in adipose tissue from NIDDM patients. Mol. Cell Endocrinol. 135(1), 41-47 (1997).
27. Blakesley VA, Scrimgeour A, Esposito D, Le Roith D. Signaling via the insulin-like growth factor-I receptor: does it differ from insulin receptor signaling? Cytokine Growth Factor Rev. 7(2), 153-159 (1996).
28. Tsukahara H, Gordienko DV, Tonshoff B, Gelato MC, Goligorsky MS. Direct demonstration of insulin-like growth factor-I-induced nitric oxide production by endothelial cells. Kidney Int. 45(2), 598-604 (1994).
29. Klip A, Paquet MR. Glucose transport and glucose transporters in muscle and their metabolic regulation. Diabetes Care 13(3), 228-243 (1990).
30. Ross R. Atherosclerosis - an inflammatory disease. N. Engl. J. Med. 340(2), 115-126 (1999).
31. Wheatcroft SB, Williams IL, Shah AM, Kearney MT. Pathophysiological implications of insulin resistance on vascular endothelial function. Diabetic Medicine 20(4), 255-268 (2003).
32. Hsueh WA, Quinones MJ. Role of endothelial dysfunction in insulin resistance. Am. J. Cardiol. 92(4A), 10J-17J (2003).
33. Abe H, Yamada N, Kamata K et al. Hypertension, hypertriglyceridemia, and impaired endothelium-dependent vascular relaxation in mice lacking insulin receptor substrate-1. J. Clin. Invest. 101(8), 1784-1788 (1998).
34. Katakam PV, Ujhelyi MR, Hoenig ME, Miller AW. Endothelial dysfunction precedes hypertension in diet-induced insulin resistance. Am. J. Physiol. 275(3 Pt 2), R788-R792 (1998).
35. Merimee TJ, Zapf J, Froesch ER. Insulin-like growth factors in the fed and fasted states. J. Clin. Endocrinol. Metah. 55, 999-1002 (1982).
36. Underwood LE, Thissen JP, Lemozy S, Ketelslegers JM, Clemmons DR. Hormonal and nutritional regulation of IGF-I and its binding proteins. Horm. Res. 42(4-5), 145-151 (1994).
37. Guler HP, Zapf J, Froesch ER. Short-term metabolic effects of recombinant human insulin-like growth factor I in healthy adults. N. Engl. J. Med. 317(3), 137-140 (1987).
38. Jones JI, Clemmons DR. Insulin-like growth factors and their binding proteins: biological actions. Endocr. Rev. 16(1), 3-34 (1995).
39. Cusi K, DeFronzo R. Recombinant human insulin-like growth factor I treatment for 1 week improves metabolic control in Type 2 diabetes by ameliorating hepatic and muscle insulin resistance. J. Clin. Endocrinol. Metab. 85(9), 3077-3084 (2000).
40. Holt RI, Simpson HL, Sonksen PH. The role of the growth hormone-insulin-like growth factor axis in glucose homeostasis. Diabet. Med. 20(1), 3-15 (2003).
41. O'Connell T, Clemmons DR. IGF-I/IGF-binding protein-3 combination improves insulin resistance by GH-dependent and independent mechanisms. J. Clin. Endocrinol. Metab. 87(9), 4356-4360 (2002).
42. Yakar S. Inhibition of growth hormone action improves insulin sensitivity in liver IGF-1-deficient mice. J. Clin. Invest. 113, 96-105 (2004).
43. Dohm GL, Elton CW, Raju MS et al. IGF-I-stimulated glucose transport in human skeletal muscle and IGF-I resistance in obesity and NIDDM. Diabetes 39(9), 1028-1032 (1990).
44. Fernandez AM, Kim JK, Yakar S et al. Functional inactivation of the IGF-I and insulin receptors in skeletal muscle causes Type 2 diabetes. Genes. Dev. 15(15), 1926-1934 (2001).
45. Pennisi P, Gavrilova O, Setser-Portas J et al. Recombinant human insulin-like growth factor-I treatment inhibits gluconeogenesis in a transgenic mouse model of Type 2 diabetes mellitus. Endocrinology 147(6), 2619-2630 (2006).
46. Chang PY, Benecke H, Marchand-Brustel Y, Lawitts J, Moller DE. Expression of a dominant-negative mutant human insulin receptor in the muscle of transgenic mice. J. Biol. Chem. 269(23), 16034-16040 (1994).
47. Chen YH, Hung PF, Kao YH. IGF-I downregulates resistin gene expression and protein secretion. Am. J. Physiol. Endocrinol. Metab. 288(5), E1019-E1027 (2005).
48. Accili D. Lilly lecture 2003: the struggle for mastery in insulin action: from triumvirate to republic. Diabetes 53(7), 1633-1642 (2004).
49. Van Schravendijk CF, Foriers A, Van den Brande JL, Pipeleers DG. Evidence for the presence of Type I insulin-like growth factor receptors on rat pancreatic A and B cells. Endocrinology 121(5), 1784-1788 (1987).
50. van Haeften TW, Twickler TB. Insulin-like growth factors and pancreas β cells. Eur. J. Clin. Invest. 34(4), 249-255 (2004).
51. Rhodes CJ. IGF-I and GH post-receptor signaling mechanisms for pancreatic β-cell replication. J. Mol. Endocrinol. 24(3), 303-311 (2000).
52. Liu JL. Does IGF-I stimulate pancreatic islet cell growth? Cell Biochem. Biophys. 48(2-3), 115-125 (2007).
53. Lu Y, Herrera PL, Guo Y et al. Pancreatic-specific inactivation of IGF-I gene causes enlarged pancreatic islets and significant resistance to diabetes. Diabetes 53(12), 3131-3141 (2004).
54. Xuan S, Kitamura T, Nakae J et al. Defective insulin secretion in pancreatic {β} cells lacking Type 1 IGF receptor. J. Clin. Invest. 110(7), 1011-1019 (2002).
55. Kulkarni RN, Holzenberger M, Shih DQ et al. β-cell-specific deletion of the IGF1 receptor leads to hyperinsulinemia and glucose intolerance but does not alter β-cell mass. Nat. Genet. 31(1), 111-115 (2002).
56. Ueki K, Okada T, Hu J et al. Total insulin and IGF-I resistance in pancreatic β cells causes overt diabetes. Nat. Genet. 38(5), 583-588 (2006).
57. 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-1. J. Biol. Chem. 279(36), 38016-38024 (2004).
58. Clauson PG, Brismar K, Hall K, Linnarsson R, Grill V. Insulin-like growth factor-I and insulin-like growth factor binding protein-1 in a representative population of Type 2 diabetic patients in Sweden. Scand. J. Clin. Lab. Invest. 58(4), 353-360 (1998).
59. Frystyk J, Skjaerbaek C, Vestbo E, Fisker S, Orskov H. Circulating levels of free insulin-like growth factors in obese subjects: the impact of Type 2 diabetes. Diabetes Metab. Res. Rev. 15(5), 314-322 (1999).
60. Nam SY, Lee EJ, Kim KR et al. Effect of obesity on total and free insulin-like growth factor (IGF)-1, and their relationship to IGF-binding protein (BP)-1, IGFBP-2, IGFBP-3, insulin, and growth hormone. Int. J. Obes. Relat. Metab. Disord. 21(5), 355-359 (1997).
61. Sandhu MS, Heald AH, Gibson JM, Cruickshank JK, Dunger DB, Wareham NJ. Circulating concentrations of insulin-like growth factor-I and development of glucose intolerance: a prospective observational study. Lancet 359(9319), 1740-1745 (2002).
62. Tan K, Baxter RC. Serum insulin-like growth factor I levels in adult diabetic patients: the effect of age. J. Clin. Endocrinol. Metab. 63(3), 651-655 (1986).
63. Moses AC, Young SC, Morrow LA, O'Brien M, Clemmons DR. Recombinant human insulin-like growth factor I increases insulin sensitivity and improves glycemic control in Type 11 diabetes. Diabetes 45(1), 91-100 (1996).
64. Jabri N, Schalch DS, Schwartz SL et al. Adverse effects of recombinant human insulin-like growth factor I in obese insulin-resistant Type II diabetic patients. Diabetes 43(3), 369-374 (1994).
65. Carroll PV, Christ ER, Umpleby AM et al. IGF-I treatment in adults with Type 1 diabetes: effects on glucose and protein metabolism in the fasting state and during a hyperinsulinemic-euglycemic amino acid clamp. Diabetes 49(5), 789-796 (2000).
66. Morrow LA, O'Brien MB, Moller DE, Flier JS, Moses AC. Recombinant human insulin-like growth factor-I therapy improves glycemic control and insulin action in the Type A syndrome of severe insulin resistance. J. Clin. Endocrinol. Metab. 79(1), 205-210 (1994).
67. Acerini CL, Patton CM, Savage MO, Kernell A, Westphal O, Dunger DB. Randomised placebo-controlled trial of human recombinant insulin-like growth factor I plus intensive insulin therapy in adolescents with insulin-dependent diabetes mellitus. Lancet 350 (9086), 1199-1204 (1997).
68. Boulware SD, Tamborlane WV, Rennert NJ et al. Comparison of the metabolic effects of recombinant human insulin-like growth factor-I and insulin. Dose-response relationships in healthy young and middle-aged adults. J. Clin. Invest. 93 (3), 1131-1139 (1994).
69. Zenobi PD, Jaeggi-Groisman SE, Riesen WF et al. Insulin-like growth factor-I improves glucose and lipid metabolism in Type 2 diabetes mellitus. J. Clin. Invest. 90(6), 2234-2241 (1992).
70. Kuzuya H. Trial of insulin like growth factor I therapy for patients with extreme insulin resistance syndromes. Diabetes 42, 696-705 (1999).
71. RH in NIDDM Study Group, Evidence from a dose ranging study that recombinant insulin-like growth factor-1 (RhIGF-1) effectively and safely improves glycaemic control in non-insulin dependent diabetes mellitus. Diabetes 45 (Suppl. 2), 27A (1996).
72. Schwartz SL. RHIGF1 co-therapy with Insulin Subgroup. RHIGF1 improves glucose control in insulin requiring Type 2 diabetes. Proceedings of the 5th Annual Meeting, of the American Diabetes Association, San Antonio, Texas, USA, 582 (1997).
73. Hussain MA, Schmitz O, Mengel A et al. Insulin-like growth factor-I stimulates lipid oxidation, reduces protein oxidation, and enhances insulin sensitivity in humans. J. Clin. Invest. 92(5), 2249-2256 (1993).
74. O'Connor R, Fennelly C, Krause D. Regulation of survival signals from the insulin-like growth factor-I receptor. Biochem. Soc. Trans. 28, 47-15 (2000).
75. Probst-Hensch NM. IGF-1, IGF-2 and IGFBP-3 in prediagnostic serum: association with colorectal cancer in a cohort of Chinese men in Shanghai. Br. J. Cancer 85, 1695-1699 (2001).
76. Hankinson SE. Circulating concentrations of insulin-like growth facior-I and risk of breast cancer. Lancet 351, 1393-1396 (1998).
77. Yu H. Plasma levels of insulin-like growth factor-I and lung cancer risk: a case-control analysis. J. Natl Cancer Inst. 91, 151-156 (1999).
78. Chan JM. Plasma insulin-like growth factor-I and prostate cancer risk: a prospective study. Science 279, 563-566 (1998).
79. Clemmons DR, Moses AC, Sommer A et al. RhIGF-I/rhIGFBP-3 administration to patients with Type 2 diabetes mellitus reduces insulin requirements while also lowering fasting glucose. Growth Horm. IGF Res. 15(4), 265-274 (2005).
80. Clemmons DR, Sleevi M, Allan G, Sommer A. Effects of combined recombinant insulin-like growth factor (IGF)-I and IGF binding protein-3 in Type 2 diabetic patients on glycemic control and distribution of IGF-I and IGF-II among serum binding protein complexes. J. Clin. Endocrinol. Metab. 92(7), 2652-2658 (2007).
81. Heald AH, Anderson SG, Ivison F, Laing I, Gibson JM, Cruickshank K. C-reactive protein and the insulin-like growth factor (IGF)-system in relation to risk of cardiovascular disease in different ethnic groups. Atherosclerosis 170(1), 79-86 (2003).
82. Colao A, Spiezia S, Di Somma C et al. Circulating insulin-like growth factor-I levels are correlated with the atherosclerotic profile in healthy subjects independently of age. J. Endocrinol. Invest. 28 (5), 440-448 (2005).
83. Ruotolo G, Bävenholm P, Brismar K et al. Serum insulin-like growth factor-I level is independently associated with coronary artery disease progression in young male survivors of myocardial infarction: beneficial effects of bezafibrate treatment. J. Am. Coll. Cardiol. 35(3), 647-654 (2000).
84. Wilson AM, Ryan MC, Boyle AJ. The novel role of C-reactive protein in cardiovascular disease: Risk marker or pathogen. Int. J. Cardiol. 106(3), 291-297 (2006).
85. Kaushal K, Heald AH, Siddals KW et al. The impact of abnormalities in IGF and inflammatory systems on the metabolic syndrome. Diabetes Care 27(11), 2682-2688 (2004).
86. Rajpathak SN, McGinn AP, Strickler HD et al. Insulin-like growth factor-(IGF)-axis, inflammation, and glucose intolerance among older adults. Growth Horm. IGF Res. 18(2), 166-173 (2007).
87. Du J, Delafontaine P. Inhibition of vascular smooth muscle cell growth through antisense transcription of a rat insulin-like growth factor I receptor cDNA. Circ. Res. 76(6), 963-972 (1995).
88. Arnqvist HJ, Bornfeldt KE, Chen Y, Lindstrom T. The insulin-like growth factor system in vascular smooth muscle: interaction with insulin and growth factors. Metabolism 44, 58-66 (1995).
89. Bennett MR, Evan GI, Schwartz SM. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J. Clin. Invest. 95(5), 2266-2274 (1995).
90. Johansson GS, Arnqvist HJ. Insulin and IGF-I action on insulin receptors, IGF-I receptors, and hybrid insulin/IGF-I receptors in vascular smooth muscle cells. Am. J. Physiol. Endocrinol. Metab. 291(5), E1124-E1130 (2006).
91. Du J, Peng T, Scheidegger KJ, Delafontaine P. 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. 19, 2119-2126 (1999).
92. Brink M, Chrast J, Price SR, Mitch WE, Delafontaine P. Angiontensin II stimulates gene expression of cardiac insulin-like growth factor I and its receptor through effects on blood pressure and food intake. Hypertension 34, 1053-1059 (1999).
93. Kirstein M, Aston C, Hintz R, Vlassara H. Receptor-specific induction of insulin-like growth factor I in human monocytes by advanced glycosylation end product-modified proteins. J. Clin. Invest. 90, 439-446 (1992).
94. Li H, Dimayuga P, Yamashita M et al. Arterial injury in mice with severe insulin-like growth factor-I (IGF-1) deficiency. J. Cardiovasc. Pharmacol. Ther. 7(4), 227-233 (2002).
95. Grant MB. Localization of insulin-like growth factor I and inhibition of coronary smooth muscle cell growth by somatostatin analogues in human coronary smooth muscle cells. A potential treatment for restenosis? Circulation 89, 1511-1517 (1994).
96. Hayry P. Stabile D-peptide analog of insulin-like growth factor-1 inhibits smooth muscle cell proliferation after carotid ballooning injury in the rat. FASEB J. 9, 1336-1344 (1995).
97. Wang J. Overexpression of insulin-like growth factor-binding protein-4 (IGFBP-4) in smooth muscle cells of transgenic mice through a smooth muscle α-actin-IGFBP-4 fusion gene induces smooth muscle hypoplasia. Endocrinology 139, 2605-2614 (1998).
98. Eriksen UH, Amtorp O, Bagger JP et al. Randomized double-blind Scandinavian trial of angiopeptin versus placebo for the prevention of clinical events and restenosis after coronary balloon angioplasty. Am. Heart J. 130(1), 1-8 (1995).
99. von Essen R, Ostermaier R, Grube E et al. Effects of octreotide treatment on restenosis after coronary angioplasty: results of the VERAS study. Verringerung der Restenoserate nach Angioplastie dutch ein Somatostatin-analogon. Circulation 96(5), 1482-1487 (1997).
100. Ling Y, Maile LA, Lieskovska J, Badley-Clarke J, Clemmons DR. Role of SHPS-1 in the regulation of insulin-like growth factor I-stimulated SHC and mitogen-activated protein kinase activation in vascular smooth muscle cells. Mol. Biol. Cell 16, 3353-3364 (2005).
101. Nichols TC. Reduction in atherosclerotic lesion size in pigs by αVα3 inhibitors is associated with inhibition of insulin-like growth factor-I-mediated signalling. Circ. Res. 85, 1040-1045 (1999).
102. Hers I. Insulin-like growth factor-1 potentiates platelet activation via the IRS/PI3K(α) pathway. Blood 110(13), 4243-4252 (2007).
103. Kim S, Garcia A, Jackson SP, Kunapuli SP. Insulin-like growth factor-1 regulates platelet activation through PI3-K{α} isoform. Blood 110(13), 4206-4213 (2007).
104. Walsh ME, Barazi M, Pete G et al. Insulin-like growth factor I diminishes in vivo and in vitro vascular contractility: role of vascular nitric oxide. Endocrinology 137(5), 1798-1803 (1996).
105. Izhar U, Hasdai D, Richardson DM, Cohen P, Lerman A. Insulin and insulin-like growth factor-I cause vasorelaxation in human vessels in vitro. Coron. Artery Dis. 11(1), 69-76 (2000).
106. Tivesten A, Bollano E, Andersson I et al. Liver-derived insulin-like growth factor-I is involved in the regulation of blood pressure in mice. Endocrinology 143(11), 4235-4242 (2002).
107. Patel VA, Zhang QJ, Siddle K et al. Defect in insulin-like growth factor-1 survival mechanism in atherosclerotic plaque-derived vascular smooth muscle cells is mediated by reduced surface binding and signaling. Circ. Res. 88(9), 895-902 (2001).
108. Okura Y, Brink M, Zahid AA, Anwar A, Delafontaine P. Decreased expression of insulin-like growth factor-1 and apoptosis of vascular smooth muscle cells in human atherosclerotic plaque, J. Mol. Cell Cardiol. 33(10), 1777-1789 (2001).
109. Bornfeldt KE, Arnqvist HJ, Dahlkvist HH, Skottner A, Wikberg JE. Receptors for insulin-like growth factor-I in plasma membranes isolated from bovine mesenteric arteries. Acta Endocrinol. (Copenh.) 117(4), 428-434 (1988).
110. Garg UC, Hassid A. Nitric oxide-generating vasodilators and 8-bromo-cyclic guanosine monophosphate inhibit mitogenesis and proliferation of cultured rat vascular smooth muscle cells. J. Clin. Invest. 83(5), 1774-1777 (1989).
111. Radomski MW, Palmer RM, Moncada S. An L-argirline/nitric oxide pathway present in human platelets regulates aggregation. Proc. Natl Acad. Sci. USA 87(13), 5193-5197 (1990).
112. Kubes P, Suzuki M, Granger DN. Nitric oxide: an endogenous modulator of leukocyte adhesion. Proc. Natl Acad. Sci. USA 88(11), 4651-4655 (1991).
113. Ignarro LJ, Buga. GM, Wood KS, Byrns RE, Chaudhuri G. Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide. Proc. Natl Acad. Sci. USA 84(24), 9265-9269 (1987).
114. Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature 327(6122), 524-526 (1987).
115. Petrie JR, Ueda S, Webb DJ, Elliott HL, Connell JM. Endothelial nitric oxide production and insulin sensitivity. A physiological link with implications for pathogenesis of cardiovascular disease. Circulation 93(7), 1331-1333 (1996).
116. Sowers JR. Insulin resistance and hypertension. Am. J. Physiol. Heart Circ. Physiol. 286(5), (2004).
117. Schini-Kerth VB. Dual effects of insulin-like growth factor-I on the constitutive and inducible nitric oxide (NO) synthase-dependent formation of NO in vascular cells. J. Endocrinol. Invest. 22(5 Suppl.), 82-88 (1999).
118. Vecchione C, Colella S, Fratta L et al. Impaired insulin-like growth factor I vasorelaxant effects in hypertension. Hypertension 37(6), 1480-1485 (2001).
119. Haylor J, Singh I, el Nahas AM. Nitric oxide synthesis inhibitor prevents vasodilation by insulin-like growth factor I. Kidney Int. 39(2), 333-335 (1991).
120. Copeland KC, Nair KS. Recombinant human insulin-like growth factor-I increases forearm blood flow. J. Clin. Endocrinol. Metab. 79(1), 230-232 (1994).
121. Schmidt-Lucke C, Rössig L, Fichtlscherer S et al. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation 111(22), 2981-2987 (2005).
122. Werner N, Kosiol S, Schiegl T et al. Circulating endothelial progenitor cells and cardiovascular outcomes. N. Engl. J. Med. 353(10), 999-1007 (2005).
123. Thum T, Hoeber S, Froese S et al. Age-dependent impairment of endothelial progenitor cells is corrected by growth-hormone-mediated increase of insulin-like growth-factor-1. Circ. Res. 100(3), 434-443 (2007).
124. Janssen JA, Stolk RP, Pols HA, Grobbee DE, Lamberts SW Serum total IGF-I, free IGF-I, and IGFB-1 levels in an elderly population: relation to cardiovascular risk factors and disease. Arterioscler. Thromb. Vase. Biol. 18(2), 277-282 (1998).
125. Laughlin GA, Barrett-Connor E, Criqui MH, Kritz-Silverstein D. 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. 89(1), 114-120 (2004).
126. Juul A, Scheike T, Davidsen M, Gyllenborg J, Jorgensen T. Low serum insulin-like growth factor I is associated with increased risk of ischemic heart disease: a population-based case-control study. Circulation 106, 939-944 (2002).
127. Goodman-Gruen D, Barrett-Connor E, Rosen C. IGF-1 and ischemic heart disease in older people. J. Am. Geriatr. Soc. 48(7), 860-861 (2000).
128. Conti E, Andreotti F, Sciahbasi A et al. Markedly reduced insulin-like growth factor-1 in the acute phase of myocardial infarction'. J. Am. Coll. Cardiol. 38(1), 26-32 (2001).
129. Reeves I, Abribat T, Lararnee P, Jasmin G, Brazeau P. Age-related serum levels of insulin-like growth factor-I, -II and IGF-binding protein-3 following myocardial infarction. Growth Horm. IGF Res. 10(2), 78-84 (2000).
130. Conti E, Andreotti F, Sestito A et al. Reduced levels of insulin-like growth factor-1 in patients with angina pectoris, positive exercise stress test, and angiographically normal epicardial coronary arteries. Am. J Cardiol. 89 (8), 973-975(2002).
131. Johnsen SP, Hundborg HH, Sorensen HT et al. Insulin-like growth factor (IGF) I, -II, and IGF binding protein-3 and risk of ischemic stroke. J. Clin. Endocrinol. Metab. 90(11), 5937-5941 (2005).
132. van den Beld AW, Bots ML, Janssen, Pols HAP, Lamberts SWJ, Grobbee DE. Endogenous hormones and carotid atherosclerosis in elderly men. Am. J. Epidemiol. 157(1), 25-31 (2003)..
133. Spallarossa P, Brunelli C, Minuto F et al. Insulin-like growth factor-I and angiographically documented coronary artery disease. Am. J. Cardiol. 77(2), 200-202 (1996).
134. Kaplan RC, McGinn AP, Pollak MN et al. Association of total insulin-like growth factor-I, insulin-like growth factor binding protein-1 (IGFBP-1), and IGFBP-3 levels with incident coronary events and ischemic stroke. J. Clin. Endocrinol. Metab. 92(4), 1319-1325 (2007).
135. Vaessen N. A polymorphism in the gene for IGF1: functional properties and risk for Type 2 diabetes and myocardial infarction. Diabetes 50, 637-642 (2001).
136. Ito H, Hiroe M, Hirata Y et al. Insulin-like growth factor-I induces hypertrophy with enhanced expression of muscle-specific genes in cultured rat cardiomyocytes. Circulation 87(5), 1715-1721 (1993).
137. Torella D, Rota M, Nurzynska D et al. Cardiac stem cell and myocyte aging, heart failure, and insulin-like growth factor-1 overexpression. Circ. Res. 94(4), 514-524 (2004).
138. 2+ through a wortmannin-sensitive pathway: studies in rat and ferret isolated muscles. Circ. Res. 83(1), 50-59 (1998).
139. Duerr RL, McKirnan MD, Gim RD, Clark RG, Chien KR, Ross J. Cardiovascular effects of insulin-like growth factor-1 and growth hormone in chronic left ventricular failure in the rat. Circulation 93(12), 2188-2196 (1996).
140. Lee WL, Chen JW. Ting CT, Lin SJ, Wang PH. Changes of the insulin-like growth factor I system during acute myocardial infarction: implications on left ventricular remodeling. J. Clin. Endocrinol. Metab. 84(5), 1575-1581 (1999).
141. Wang PH. Roads to survival: insulin-like growth factor-1 signaling pathways in cardiac muscle. Circ. Res. 88(6), 552-554 (2001).
142. Buerke M, Murohara T, Skurk C, Nuss C, Tomaselli K, Lefer AM. Cardioprotective effect of insulin-like growth factor I in myocardial ischernia followed by reperfusion. Proc. Natl Acad. Sci. USA 92(17), 8031-8035 (1995).
143. Friehs I, Stamm C, Cao-Danh H, McGowan FX, del Nido PJ. Insulin-like growth factor-1 improves postischemic recovery in hypertrophied hearts. Ann. Thorac. Surg. 72(5), 1650-1656 (2001).
144. Otani H, Yamamura T, Nakao Y et al. Insulin-like growth factor-I improves recovery of cardiac performance during reperfusion in isolated rat heart by a wortmannin-sensitive mechanism. J. Cardiovasc. Pharmacol. 35(2), 275-281 (2000).
145. Wu W, Lee WL, Wu YY et al. Expression of constitutively active phosphaddylinositol 3-kinase inhibits activation of caspase 3 and apoptosis of cardiac muscle cells. J. Biol. Chem. 275(51), 40113-40119 (2000).
146. Fujio Y, Nguyen T, Wencker D, Kitsis RN, Walsh K. Akt promotes survival of cardionryocytes in vitro and protects against ischemia-reperfusion injury in mouse heart. Circulation 101(6), 660-667 (2000).
147. Parrizas M, Saltiel AR, LeRoith D. Insulin-like growth factor 1 inhibits apoptosis using the phosphatidylinosirol 3™-kinase and mitogen-activated protein kinase pathways. J. Biol. Chem. 272(1), 154-161 (1997).
148. Urbanek K, Rota M, Cascapera S et al. Cardiac stem cells possess growth factor-receptor systems that after activation regenerate the infarcred myocardium, improving ventricular function and long-term survival. Circ. Res. 97(7), 663-673 (2005).
149. Vasan RS, Sullivan LM, D'Agostino RB et al. Serum insulin-like growth factor I and risk for heart failure in elderly individuals without a previous myocardial infarction: the Framingham Heart Study. Ann. Intern. Med. 139(8), 642-648 (2003).
150. Ren J, Samson WK, Sowers JR. Insulin-like growth factor I as a cardiac hormone: physiological and pathophysiological implications in heart disease. J. Mol. Cell Cardiol. 31(11), 2049-2061 (1999).
151. Anker SD, Volterrani M, Pflaum CD et al. Acquired growth hormone resistance in patients with chronic heart failure: implications for therapy with growth hormone. J. Am. Coll. Cardiol. 38(2), 443-452 (2001).
152. Niebauer J, Pflaum CD, Clark AL et al. Deficient insulin-like growth factor I in chronic heart failure predicts altered body composition, anabolic deficiency, cytokine and neurohormonal activation. J. Am. Coll. Cardiol. 32(2), 393-397 (1998).
153. Musaro A, Giacinti C, Borsellino G et al. Stem cell-mediated muscle regeneration is enhanced by local isoform of insulin-like growth factor 1. Proc. Natl Acad. Sci. USA 101(5), 1206-1210 (2004).
154. 2+-dependent positive inotropic effects in failing human myocardium. Circ. Res. 92(2), 169-176 (2003).
155. Donath MY, Satsch G, Yan XW et al. Acute cardiovascular effects of insulin-like growth factor I in patients with chronic heart failure. J. Clin. Endocrinol. Metab. 83 (9), 3177-3183 (1998).
156. Osterziel KJ, Blum WF, Strohm O, Dietz R. The severity of chronic heart failure due to coronary artery disease predicts the endocrine effects of short-term growth hormone administration. J. Clin. Endocrinol, Metab. 85(4), 1533-1539 (2000).
157. Napoli R, Guardasole V, Angelini V et al. Acute effects of growth hormone on vascular function in human subjects. J. Clin. Endocrinol. Metab. 88(6), 2817-2820 (2003).
158. Volterrani M, Desenzani P, Lorusso R, d'Aloia A, Manelli F, Giustina A. Haemodynamic effects of intravenous growth hormone in congestive heart failure. Lancet 349 (9058), 1067-1068 (1997).
159. Fazio S, Sabatini D, Capaldo B et al. A preliminary study of growth hormone in the treatment of dilated cardiornyopathy. N. Engl. J. Med. 334(13), 809-814 (1996).
160. Jose VJ, Zechariah TU, George P, Jonathan V. Growth hormone therapy in patients with dilated cardiomyopathy: preliminary observations of a pilot study. Indian Heart J. 51(2), 183-185 (1999).
161. Perrot A, Ranke MB, Dietz R, Osterziel KJ. Growth hormone treatment in dilated cardiomyopathy. J. Card. Surg. 16(2), 127-131 (2001).
162. Frustaci A, Gentiloni N, Russo MA. Growth hormone in the treatment of dilated cardiomyopathy. N. Engl. J. Med. 335(9), 672-673 (1996).
163. Acevedo M, Corbalan R, Chamorro G et al. Administration of growth hormone to patients with advanced cardiac heart failure: effects upon left ventricular function, exercise capacity, and neurohormonal status. Int. J. Cardiol. 87(2-3), 185-191 (2003).
164. Isgaard J, Bergh CH, Caidahl K, Lomsky M, Hjalmarson A, Bengtsson BA. A placebo-controlled study of growth hormone in patients with congestive heart failure. Eur. Heart J. 19(11), 1704-1711 (1998).
165. Spallarossa P, Rossettin P, Minuto F et al. Evaluation of growth hormone administration in patients with chronic heart failure secondary to coronary artery disease. Am. J. Cardiol. 84(4), 430-433 (1999).
166. Le Corvoisier P, Hittinger L, Chanson P, Montagne O, Macquin-Mavier I, Maison P. Cardiac effects of growth hormone treatment in chronic heart failure: a meta-analysis. J. Clin. Enaocrinol. Metab. 92(1), 180-185 (2007).
167. Bates AS, VantHoff W, Jones PJ, Clayton RN. The effecc of hypopituitarism on life expectancy. J. Clin. Endocrinol. Metab. 81(3), 1169-1172 (1996).
168. Tomlinson JW, Holden N, Hills RK et al. Association between premature mortality and hypopituitarism. Lancet 357(9254), 425-431 (2001).
169. Rosen T, Bengtsson BA. Premature mortality due to cardiovascular-disease in hypopitunarism. Lancet 336(8710), 285-288 (1990).
170. Elhadd TA, Abdu TAM, Clayton R. Hypopituitarism and atherosclerosis. Ann. Med. 33(7), 477-485 (2001).
171. Maison P, Griffin S, Nicoue-Beglah M, Haddad N, Balkau B, Chanson P. Impact of growth hormone (GH) treatment on cardiovascular risk factors in GH-deficient adults: a meta-analysis of blinded, randomized, placebo-controlled trials. J. Clin. Endocrinol. Metab. 89 (5), 2192-2199 (2004).
172. Yuen KC, Frystyk J, White DK et al. Improvement in insulin sensitivity without concomitant changes in body composition and cardiovascular risk markers following fixed administration of a very low growth hormone (GH) dose in adults with severe GH deficiency. Clin. Endocrinol. (Oxf) 63(4), 428-436 (2005).
173. Capaldo B, Guardasoie V, Pardo F et al. Abnormal vascular reactivity in growth hormone de6ciency. Circulation 103(4), 520-524 (2001).
174. Amato G, Carella C, Fazio S et al. Body composition, bone metabolism, and heart structure and function in growth hormone (GH)-deficient adults before and after GH replacement therapy at low doses. J. Clin. Endocrinol. Metab. 77(6), 1671-1676 (1993).
175. Longobardi S, Cuocolo A, Merola B et al. Left ventricular function in young adults with childhood and adulthood onset growth hormone deficiency. Clin. Endocrinol. (Oxf) 48(2), 137-143 (1998).
176. Merola B, Cittadini A, Colao A et al. Cardiac-structural and functional abnormalities in adult patients with growth hormone deficiency. J. Clin. Endocrinol. Metab. 77(6), 1658-1661 (1993).
177. Maison P, Chanson P. Cardiac effects of growth hormone in adults with growth hormone deficiency: a meta-analysis. Circulation 108(21), 2648-2652 (2003).
178. Sesmilo G, Biller BMK, Llevadot J et al. Effects of growth hormone administration on inflammatory and other cardiovascular risk markers in men with growth hormone deficiency - a randomized, controlled clinical trial. Ann. Intern. Med. 133(2), 111-122 (2000).
179. Klibanski A. Growth hormone and cardiovascular risk markers. Growth Horm. IGF Res. 13, S109-S115 (2003).
180. Kalina-Faska B, Kalina M, Koehler B. Effects of recombinant growth hormone therapy on thyroid hormone concentrations. Int. J. Clin. Pharmacol. Ther. 42(1), 30-34 (2004).
181. Agha A, Monson JP. Modulation of glucocorticoid metabolism by the growth hormone - IGF-1 axis. Clin. Endocrinol. 66(4), 459-465 (2007).
182. Verhelst J, Abs R. Long-term growth hormone replacement therapy in hypopituitary adults. Drugs 62(16), 2399-2412 (2002).
183. Fein FS. Diabetic cardiomyopathy. Diabetes Care 13(11), 1169-1179 (1990).
184. Bell D. Heart Failure: The frequent, forgotten, and often fatal complication of diabetes. Diabetes Care 26(8), 2433-2441 (2003).
185. Shan YX, Liu TJ, Su HF, Samsamshariat A, Mestril R, Wang PH. Hsp10 and Hsp60 modulate Bcl-2 family and mitochondria apoptosis signaling induced by doxorubicin in cardiac muscle cells. J. Mol. Cell. Cardiol. 35(9), 1135-1143 (2003).
186. Fazio S, Palmieri EA, Biondi B, Cittadini A, Saccá L. The role of the GH-IGF-I axis in the regulation of myocardial growth: from experimental models to human evidence. Eur. J. Endocrinol. 142(3), 211-216 (2000).
187. Shan YX, Yang TL, Mestril R, Wang PH Hsp10 and Hsp60 suppress ubiquirination of insulin-like growth factor-1 receptor and augment insulin-like growth factor-1 receptor signaling in cardiac muscle: implications on decreased myocardial protection in diabetic cardiomyopathy. J. Biol. Chem. 278(46), 45492-45498 (2003).
188. Schafler AE, Kirmattoglou K, Balbach J, Pecher P, Hannekum A, Schumacher B. The expression of heat shock protein 60 in myocardium of patients with chronic atrial fibrillation. Basic Res. Cardiol. 97(3), 258-261 (2002).
189. Lin KM, Lin B, Lian IY, Mestril R, Scheffler IE, Dillmann WH. Combined and individual mitochondrial HSP60 and HSP10 expression in cardiac myocyres protects mitochondrial function and prevents apoptotic cell deaths induced by simulated ischemia-reoxygenation. Circulation 103(13), 1787-1792 (2001).
190. Chen HS, Shan YX, Yang TL et al. Insulin deficiency downregulated heat shock protein 60 and IGF-1 receptor signalling in diabetic myocardium. Diabetes 54(1), 175-181 (2005).
191. Lai HC, Liu TJ, Ting CT et al. Regulation of IGF-1 receptor signalling in diabetic cardiac muscle: dysregulation of cytosolic and mitochondria HSP60. Am. J. Physiol. Fndocrinol. Metab. 292(1), E292-E297 (2007).
192. Lowell B, Shulman G. Mitochondrial dysfunction and Type 2 diabetes. Science 307(5708), 384-387 (2005).
193. Dann SG, Selvaraj A, Thomas G. mTOR complex1-S6K1 signalling: at the crossroads of obesity, diabetes and cancer. Trends Mol. Med. 13, 252-259 (2007).
194. Kaspar BK, Lladó J, Sherkat N, Rothstein JD, Gage FH. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 301(5634), 839-842 (2003).
195. Chao W, Matsui T, Novikov MS et al. Strategic advantages of insulin-like growth factor-1 expression for cardioprotection. J. Gene Med. 5(4), 277-286 (2003).
196. Slieker LJ. Modifications in the B10 and B26-30 regions of the B chain of human insulin alter affinity for the human IGF1 receptor more than for the insulin receptor. Diabetal, 40, S54-S61 (1997).
197. Hua QX. Mini-proinsulin and mini-IGF1: homologous protein sequences encoding non-homologous structures. J. Mol. Biol. 277, 103-118 (1998).
198. Pell JM, Hill RA, Stewart CE, Weston CR, Flick-Smith HC. Enhancement of insulin-like growth factor I activity by novel antisera: potential structure/function interactions. Endocrinology 141(2), 741-751 (2000).
199. Fan W. Insulin-like growth factor 1/insulin signalling activates androgen signalling through direct interactions of Foxol with androgen receptor. J. Biol. Chem. 282, 7329-7338 (2007).
200. Elliot SJ. Smoking induces glomerulosclerosis in aging oestrogen-deficient mice through crosstalk between TGF-β and IGR1 signalling pathways. J. Am. Soc. Nephrol. 17, 3315-3324 (2006).
201. Sisci D, Surmacz E. Crosstalk between IGF signalling and steroid hormone receptors in breast cancer. Curr. Pharm. Des. 13, 705-717 (2007).