Interaction between insulin-like growth factor-1 and atherosclerosis and vascular aging

Frontiers of Hormone Research

Volumn 43, Issue , 2014, Pages 107-124

  Higashi, Yusuke ^a   Quevedo, Henry C ^a   Tiwari, Summit ^a   Sukhanov, Sergiy ^a   Shai, Shaw Yung ^a   Anwar, Asif ^a   Delafontaine, Patrice ^a  

^a TULANE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B; ELASTIN; LOW DENSITY LIPOPROTEIN; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN C; ANTIINFLAMMATORY AGENT; APOLIPOPROTEIN E; ENDOTHELIN 1; PPFIA1 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SOMATOMEDIN C RECEPTOR;

AGING; ANGIOGENESIS; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOPHOSPHORYLATION; CARDIOVASCULAR DISEASE; CELL ACTIVATION; CELL DEATH; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; HUMAN; HYPERTENSION; INFLAMMATION; MONOCYTE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TISSUE REGENERATION; VASCULAR DISEASE; VASCULAR SMOOTH MUSCLE CELL; ANIMAL; CELL AGING; CELL MOTION; DEFICIENCY; ENDOTHELIUM CELL; METABOLISM; MOUSE; PATHOPHYSIOLOGY; PHYSIOLOGY; PLAQUE, ATHEROSCLEROTIC; REGENERATION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGING; ANIMALS; ANTI-INFLAMMATORY AGENTS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELL AGING; CELL MOVEMENT; ENDOTHELIAL CELLS; ENDOTHELIN-1; HUMANS; HYPERTENSION; INSULIN-LIKE GROWTH FACTOR I; LIPOPROTEINS, LDL; MICE; MONOCYTES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OXIDATIVE STRESS; PLAQUE, ATHEROSCLEROTIC; RECEPTOR, IGF TYPE 1; REGENERATION;

EID: 84913525140     PISSN: 03013073     EISSN: 16623762     Source Type: Book Series    
DOI: 10.1159/000360571     Document Type: Article

References (135)

1. Cercek B, Fishbein MC, Forrester JS, Helfant RH, Fagin JA: Induction of insulin-like growth factor I messenger RNA in rat aorta after balloon denudation. Circ Res 1990; 66: 1755-1760.
2. Maile LA, Capps BE, Ling Y, Xi G, Clemmons DR: Hyperglycemia alters the responsiveness of smooth muscle cells to insulin-like growth factor-I. Endocrinology 2007; 148: 2435-2443.
3. Nabel EG, Yang Z, Liptay S, San H, Gordon D, Haudenschild CC, Nabel GJ: Recombinant plateletderived growth factor B gene expression in porcine arteries induce intimal hyperplasia in vivo. J Clin Invest 1993; 91: 1822-1829.
4. Soaje M, Deis RP: A modulatory role of endogenous opioids on prolactin secretion at the end of pregnancy in the rat. J Endocrinol 1994; 140: 97-102.
5. Zhang SH, Reddick RL, Piedrahita JA, Maeda N: Spontaneous hypercholesterolemia and arterial lesions in mice lacking apolipoprotein E. Science 1992; 258: 468-471.
6. Okura Y, Brink M, Itabe H, Scheidegger KJ, Kalangos A, Delafontaine P: Oxidized low-density lipoprotein is associated with apoptosis of vascular smooth muscle cells in human atherosclerotic plaques. Circulation 2000; 102: 2680-2686.
7. Kozaki K, Kaminski WE, Tang J, Hollenbach S, Lindahl P, Sullivan C, Yu JC, Abe K, Martin PJ, Ross R, Betsholtz C, Giese NA, Raines EW: Blockade of platelet-derived growth factor or its receptors transiently delays but does not prevent fibrous cap formation in ApoE null mice. Am J Pathol 2002; 161: 1395-1407.
8. Raines EW: PDGF and cardiovascular disease. Cytokine Growth Factor Rev 2004; 15: 237-254.
9. Frutkin AD, Otsuka G, Stempien-Otero A, Sesti C, Du L, Jaffe M, Dichek HL, Pennington CJ, Edwards DR, Nieves-Cintron M, Minter D, Preusch M, Hu JH, Marie JC, Dichek DA: TGF-[beta]1 limits plaque growth, stabilizes plaque structure, and prevents aortic dilation in apolipoprotein E-null mice. Arterioscler Thromb Vasc Biol 2009; 29: 1251-1257.
10. Sukhanov S, Higashi Y, Shai SY, Vaughn C, Mohler J, Li Y, Song YH, Titterington J, Delafontaine P: IGF-1 reduces inflammatory responses, suppresses oxidative stress, and decreases atherosclerosis progression in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 2007; 27: 2684-2690.
11. Higashi Y, Pandey A, Goodwin B, Delafontaine P: Insulin-like growth factor-1 regulates glutathione peroxidase expression and activity in vascular endothelial cells: implications for atheroprotective actions of insulin-like growth factor-1. Biochim Biophys Acta 2013; 1832: 391-399.
12. Clemmons DR: Metabolic actions of insulin-like growth factor-I in normal physiology and diabetes. Endocrinol Metab Clin North Am 2012; 41: 425-443, vii-viii.
13. Clemmons DR: Modifying IGF1 activity: an approach to treat endocrine disorders, atherosclerosis and cancer. Nat Rev Drug Discov 2007; 6: 821-833.
14. Jones JI, Clemmons DR: Insulin-like growth factors and their binding proteins: biological actions. Endocr Rev 1995; 16: 3-34.
15. Delafontaine P: Insulin-like growth factor I and its binding proteins in the cardiovascular system. Cardiovasc Res 1995; 30: 825-834.
16. Schneider MR, Lahm H, Wu M, Hoeflich A, Wolf E: Transgenic mouse models for studying the functions of insulin-like growth factor-binding proteins. FASEB J 2000; 14: 629-640.
17. Sakai K, Busby WH Jr, Clarke JB, Clemmons DR: Tissue transglutaminase facilitates the polymerization of insulin-like growth factor-binding protein-1 (IGFBP-1) and leads to loss of IGFBP-1's ability to inhibit insulin-like growth factor-I-stimulated protein synthesis. J Biol Chem 2001; 276: 8740-8745.
18. Ohta M, Hirao N, Mori Y, Takigami C, Eguchi M, Tanaka H, Ikeda M, Yamato H: Effects of bench step exercise on arterial stiffness in post-menopausal women: contribution of IGF-1 bioactivity and nitric oxide production. Growth Horm IGF Res 2012; 22: 36-41.
19. Jones JI, Gockerman A, Busby WH Jr, Wright G, Clemmons DR: Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the alpha 5 beta 1 integrin by means of its Arg-Gly-Asp sequence. Proc Natl Acad Sci USA 1993; 90: 10553-10557.
20. Le Roith D: The insulin-like growth factor system. Exp Diabesity Res 2003; 4: 205-212.
21. Tsuruzoe K, Emkey R, Kriauciunas KM, Ueki K, Kahn CR: Insulin receptor substrate 3 (IRS-3) and IRS-4 impair IRS-1-and IRS-2-mediated signaling. Mol Cell Biol 2001; 21: 26-38.
22. Saltiel AR, Kahn CR: Insulin signalling and the regulation of glucose and lipid metabolism. Nature 2001; 414: 799-806.
23. Stewart CE, Rotwein P: Growth, differentiation, and survival: multiple physiological functions for insulinlike growth factors. Physiol Rev 1996; 76: 1005-1026.
24. Higashi Y, Sukhanov S, Anwar A, Shai SY, Delafontaine P: Aging, atherosclerosis, and IGF-1. J Gerontol A Biol Sci Med Sci 2012; 67: 626-639.
25. Moxham CP, Duronio V, Jacobs S: Insulin-like growth factor I receptor beta-subunit heterogeneity. Evidence for hybrid tetramers composed of insulinlike growth factor I and insulin receptor heterodimers. J Biol Chem 1989; 264: 13238-13244.
26. 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.
27. Engberding N, San Martin A, Martin-Garrido A, Koga M, Pounkova L, Lyons E, Lassegue B, Griendling KK: 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: 408-415.
28. 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 2005; 146: 4690-4696.
29. Arnaldez FI, Helman LJ: Targeting the insulin growth factor receptor 1. Hematol Oncol Clin North Am 2012; 26: 527-542, vii-viii.
30. Colao A: The GH-IGF-I axis and the cardiovascular system: clinical implications. Clin Endocrinol (Oxf) 2008; 69: 347-358.
31. Berg C, Petersenn S, Lahner H, Herrmann BL, Buchfelder M, Droste M, Stalla GK, Strasburger CJ, Roggenbuck U, Lehmann N, Moebus S, Jockel KH, Mohlenkamp S, Erbel R, Saller B, Mann K: Cardiovascular risk factors in patients with uncontrolled and long-term acromegaly: comparison with matched data from the general population and the effect of disease control. J Clin Endocrinol Metab 2010; 95: 3648-3656.
32. Cannavo S, Almoto B, Cavalli G, Squadrito S, Romanello G, Vigo MT, Fiumara F, Benvenga S, Trimarchi F: Acromegaly and coronary disease: an integrated evaluation of conventional coronary risk factors and coronary calcifications detected by computed tomography. J Clin Endocrinol Metab 2006; 91: 3766-3772.
33. Bogazzi F, Battolla L, Spinelli C, Rossi G, Gavioli S, Di Bello V, Cosci C, Sardella C, Volterrani D, Talini E, Pepe P, Falaschi F, Mariani G, Martino E: Risk factors for development of coronary heart disease in patients with acromegaly: a five-year prospective study. J Clin Endocrinol Metab 2007; 92: 4271-4277.
34. Palmeiro CR, Anand R, Dardi IK, Balasubramaniyam N, Schwarcz MD, Weiss IA: Growth hormone and the cardiovascular system. Cardiol Rev 2012; 20: 197-207.
35. Burgers AM, Biermasz NR, Schoones JW, Pereira AM, Renehan AG, Zwahlen M, Egger M, Dekkers OM: Meta-analysis and dose-response metaregression: circulating insulin-like growth factor I (IGF-I) and mortality. J Clin Endocrinol Metab 2011; 96: 2912-2920.
36. Andreassen M, Raymond I, Kistorp C, Hildebrandt P, Faber J, Kristensen LO: IGF1 as predictor of all cause mortality and cardiovascular disease in an elderly population. Eur J Endocrinol 2009; 160: 25-31.
37. Ruotolo G, Bavenholm P, Brismar K, Efendic S, Ericsson CG, de Faire U, Nilsson J, Hamsten A: 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 2000; 35: 647-654.
38. Conti E, Andreotti F, Sestito A, Riccardi P, Menini E, Crea F, Maseri A, Lanza GA: 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 2002; 89: 973-975.
39. Ruidavets JB, Luc G, Machez E, Genoux AL, Kee F, Arveiler D, Morange P, Woodside JV, Amouyel P, Evans A, Ducimetiere P, Bingham A, Ferrieres J, Perret B: Effects of insulin-like growth factor 1 in preventing acute coronary syndromes: the PRIME Study. Atherosclerosis 2011; 218: 464-469.
40. Harrela M, Qiao Q, Koistinen R, Tuomilehto J, Nissinen A, Seppala M, Leinonen P: High serum insulin-like growth factor binding protein-1 is associated with increased cardiovascular mortality in elderly men. Horm Metab Res 2002; 34: 144-149.
41. Wallander M, Norhammar A, Malmberg K, Ohrvik J, Ryden L, Brismar K: IGF binding protein 1 predicts cardiovascular morbidity and mortality in patients with acute myocardial infarction and type 2 diabetes. Diabetes Care 2007; 30: 2343-2348.
42. 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 Vasc Biol 1998; 18: 277-282.
43. Frystyk J: Utility of free IGF-I measurements. Pituitary 2007; 10: 181-187.
44. Boquist S, Ruotolo G, Skoglund-Andersson C, Tang R, Bjorkegren J, Bond MG, de Faire U, Brismar K, Hamsten A: Correlation of serum IGF-I and IGFBP-1 and-3 to cardiovascular risk indicators and early carotid atherosclerosis in healthy middle-aged men. Clin Endocrinol (Oxf) 2008; 68: 51-58.
45. Fischer F, Schulte H, Mohan S, Tataru MC, Kohler E, Assmann G, von Eckardstein A: Associations of insulin-like growth factors, insulin-like growth factor binding proteins and acid-labile subunit with coronary heart disease. Clin Endocrinol (Oxf) 2004; 61: 595-602.
46. Frystyk J: Free insulin-like growth factors-measurements and relationships to growth hormone secretion and glucose homeostasis. Growth Horm IGF Res 2004; 14: 337-375.
47. Brugts MP, Ranke MB, Hofland LJ, van der Wansem K, Weber K, Frystyk J, Lamberts SW, Janssen JA: Normal values of circulating insulin-like growth factor-I bioactivity in the healthy population: comparison with five widely used IGF-I immunoassays. J Clin Endocrinol Metab 2008; 93: 2539-2545.
48. Brugts MP, van den Beld AW, Hofland LJ, van der Wansem K, van Koetsveld PM, Frystyk J, Lamberts SW, Janssen JA: Low circulating insulin-like growth factor I bioactivity in elderly men is associated with increased mortality. J Clin Endocrinol Metab 2008; 93: 2515-2522.
49. Vaessen N, Heutink P, Janssen JA, Witteman JC, Testers L, Hofman A, Lamberts SW, Oostra BA, Pols HA, van Duijn CM: A polymorphism in the gene for IGF-I: functional properties and risk for type 2 diabetes and myocardial infarction. Diabetes 2001; 50: 637-642.
50. Bleumink GS, Schut AF, Sturkenboom MC, Janssen JA, Witteman JC, van Duijn CM, Hofman A, Stricker BH: A promoter polymorphism of the insulin-like growth factor-I gene is associated with left ventricular hypertrophy. Heart 2005; 91: 239-240.
51. Schut AF, Janssen JA, Deinum J, Vergeer JM, Hofman A, Lamberts SW, Oostra BA, Pols HA, Witteman JC, van Duijn CM: Polymorphism in the promoter region of the insulin-like growth factor I gene is related to carotid intima-media thickness and aortic pulse wave velocity in subjects with hypertension. Stroke 2003; 34: 1623-1627.
52. Yazdanpanah M, Rietveld I, Janssen JA, Njajou OT, Hofman A, Stijnen T, Pols HA, Lamberts SW, Witteman JC, van Duijn CM: An insulin-like growth factor-I promoter polymorphism is associated with increased mortality in subjects with myocardial infarction in an elderly Caucasian population. Am J Cardiol 2006; 97: 1274-1276.
53. Yazdanpanah M, Sayed-Tabatabaei FA, Janssen JA, Rietveld I, Hofman A, Stijnen T, Pols HA, Lamberts SW, Witteman JC, van Duijn CM: IGF-I gene promoter polymorphism is a predictor of survival after myocardial infarction in patients with type 2 diabetes. Eur J Endocrinol 2006; 155: 751-756.
54. Allen NE, Davey GK, Key TJ, Zhang S, Narod SA: Serum insulin-like growth factor I (IGF-I) concentration in men is not associated with the cytosineadenosine repeat polymorphism of the IGF-I gene. Cancer Epidemiol Biomarkers Prev 2002; 11: 319-320.
55. Frayling TM, Hattersley AT, McCarthy A, Holly J, Mitchell SM, Gloyn AL, Owen K, Davies D, Smith GD, Ben-Shlomo Y: A putative functional polymorphism in the IGF-I gene: association studies with type 2 diabetes, adult height, glucose tolerance, and fetal growth in U.K. populations. Diabetes 2002; 51: 2313-2316.
56. Selman C, Lingard S, Choudhury AI, Batterham RL, Claret M, Clements M, Ramadani F, Okkenhaug K, Schuster E, Blanc E, Piper MD, Al-Qassab H, Speakman JR, Carmignac D, Robinson IC, Thornton JM, Gems D, Partridge L, Withers DJ: Evidence for lifespan extension and delayed age-related biomarkers in insulin receptor substrate 1 null mice. FASEB J 2008; 22: 807-818.
57. Kenyon CJ: The genetics of ageing. Nature 2010; 464: 504-512.
58. Suh Y, Atzmon G, Cho MO, Hwang D, Liu B, Leahy DJ, Barzilai N, Cohen P: Functionally significant insulin-like growth factor I receptor mutations in centenarians. Proc Natl Acad Sci USA 2008; 105: 3438-3442.
59. Fontana L, Partridge L, Longo VD: Extending healthy life span-from yeast to humans. Science 2010; 328: 321-326.
60. Holzenberger M, Dupont J, Ducos B, Leneuve P, Geloen A, Even PC, Cervera P, Le Bouc Y: IGF-1 receptor regulates lifespan and resistance to oxidative stress in mice. Nature 2003; 421: 182-187.
61. Bokov AF, Garg N, Ikeno Y, Thakur S, Musi N, De-Fronzo RA, Zhang N, Erickson RC, Gelfond J, Hubbard GB, Adamo ML, Richardson A: Does reduced IGF-1R signaling in Igf1r+/-mice alter aging? PLoS One 2011; 6:e26891.
62. Guevara-Aguirre J, Balasubramanian P, Guevara-Aguirre M, Wei M, Madia F, Cheng CW, Hwang D, Martin-Montalvo A, Saavedra J, Ingles S, de Cabo R, Cohen P, Longo VD: Growth hormone receptor deficiency is associated with a major reduction in proaging signaling, cancer, and diabetes in humans. Sci Transl Med 2011; 3: 70ra13.
63. Li H, Dimayuga P, Yamashita M, Yano J, Fournier M, Lewis M, Cercek B: Arterial injury in mice with severe insulin-like growth factor-1 (IGF-1) deficiency. J Cardiovasc Pharmacol Ther 2002; 7: 227-233.
64. Zhu B, Zhao G, Witte DP, Hui DY, Fagin JA: Targeted overexpression of IGF-I in smooth muscle cells of transgenic mice enhances neointimal formation through increased proliferation and cell migration after intraarterial injury. Endocrinology 2001; 142: 3598-3606.
65. Harrington SC, Simari RD, Conover CA: Genetic deletion of pregnancy-associated plasma protein-A is associated with resistance to atherosclerotic lesion development in apolipoprotein E-deficient mice challenged with a high-fat diet. Circ Res 2007; 100: 1696-1702.
66. Nichols TC, Busby WH Jr, Merricks E, Sipos J, Rowland M, Sitko K, Clemmons DR: Protease-resistant insulin-like growth factor (IGF)-binding protein-4 inhibits IGF-I actions and neointimal expansion in a porcine model of neointimal hyperplasia. Endocrinology 2007; 148: 5002-5010.
67. Razuvaev A, Henderson B, Girnita L, Larsson O, Axelson M, Hedin U, Roy J: The cyclolignan picropodophyllin attenuates intimal hyperplasia after rat carotid balloon injury by blocking insulin-like growth factor-1 receptor signaling. J Vasc Surg 2007; 46: 108-115.
68. Resch ZT, Simari RD, Conover CA: Targeted disruption of the pregnancy-associated plasma protein-A gene is associated with diminished smooth muscle cell response to insulin-like growth factor-I and resistance to neointimal hyperplasia after vascular injury. Endocrinology 2006; 147: 5634-5640.
69. Niu XL, Li J, Hakim ZS, Rojas M, Runge MS, Madamanchi NR: 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: 19808-19819.
70. Zadelaar S, Kleemann R, Verschuren L, de Vries-Van der Weij J, van der Hoorn J, Princen HM, Kooistra T: Mouse models for atherosclerosis and pharmaceutical modifiers. Arterioscler Thromb Vasc Biol 2007; 27: 1706-1721.
71. Adamo ML, Ma X, Ackert-Bicknell CL, Donahue LR, Beamer WG, Rosen CJ: Genetic increase in serum insulin-like growth factor-I (IGF-I) in C3H/HeJ compared with C57BL/6J mice is associated with increased transcription from the IGF-I exon 2 promoter. Endocrinology 2006; 147: 2944-2955.
72. Nichols TC, du Laney T, Zheng B, Bellinger DA, Nickols GA, Engleman W, Clemmons DR: Reduction in atherosclerotic lesion size in pigs by alphaVbeta3 inhibitors is associated with inhibition of insulin-like growth factor-I-mediated signaling. Circ Res 1999; 85: 1040-1045.
73. Ye P, D'Ercole J: Insulin-like growth factor I (IGF-I) regulates IGF binding protein-5 gene expression in the brain. Endocrinology 1998; 139: 65-71.
74. Sukhanov S, Higashi Y, Shai SY, Blackstock C, Galvez S, Vaughn C, Titterington J, Delafontaine P: Differential requirement for nitric oxide in IGF-1-induced anti-apoptotic, anti-oxidant and anti-atherosclerotic effects. FEBS Lett 2011; 585: 3065-3072.
75. Titterington JS, Sukhanov S, Higashi Y, Vaughn C, Bowers C, Delafontaine P: Growth hormone-releasing peptide-2 suppresses vascular oxidative stress in ApoE-/-mice but does not reduce atherosclerosis. Endocrinology 2009; 150: 5478-5487.
76. Andersson IJ, Ljungberg A, Svensson L, Gan LM, Oscarsson J, Bergstrom G: Increased atherosclerotic lesion area in apoE deficient mice overexpressing bovine growth hormone. Atherosclerosis 2006; 188: 331-340.
77. Payne JA, Reckelhoff JF, Khalil RA: Role of oxidative stress in age-related reduction of NO-cGMP-mediated vascular relaxation in SHR. Am J Physiol Regul Integr Comp Physiol 2003; 285:R542-R551.
78. Shai SY, Sukhanov S, Higashi Y, Vaughn C, Rosen CJ, Delafontaine P: Low circulating insulin-like growth factor I increases atherosclerosis in ApoEdeficient mice. Am J Physiol Heart Circ Physiol 2011; 300:H1898-H1906.
79. Khan AS, Sane DC, Wannenburg T, Sonntag WE: Growth hormone, insulin-like growth factor-1 and the aging cardiovascular system. Cardiovasc Res 2002; 54: 25-35.
80. Shai SY, Sukhanov S, Higashi Y, Vaughn C, Kelly J, Delafontaine P: Smooth muscle cell-specific insulinlike growth factor-1 overexpression in Apoe-/-mice does not alter atherosclerotic plaque burden but increases features of plaque stability. Arterioscler Thromb Vasc Biol 2010; 30: 1916-1924.
81. Willis PE, Chadan SG, Baracos V, Parkhouse WS: Restoration of insulin-like growth factor I action in skeletal muscle of old mice. Am J Physiol 1998; 275:E525-E530.
82. Cao JJ, Kurimoto P, Boudignon B, Rosen C, Lima F, Halloran BP: Aging impairs IGF-I receptor activation and induces skeletal resistance to IGF-I. J Bone Miner Res 2007; 22: 1271-1279.
83. Elhadd TA, Abdu TA, Oxtoby J, Kennedy G, Mc-Laren M, Neary R, Belch JJ, Clayton RN: Biochemical and biophysical markers of endothelial dysfunction in adults with hypopituitarism and severe GH deficiency. J Clin Endocrinol Metab 2001; 86: 4223-4232.
84. Perticone F, Sciacqua A, Perticone M, Laino I, Miceli S, Care I, Galiano Leone G, Andreozzi F, Maio R, Sesti G: Low-plasma insulin-like growth factor-I levels are associated with impaired endothelium-dependent vasodilatation in a cohort of untreated, hypertensive Caucasian subjects. J Clin Endocrinol Metab 2008; 93: 2806-2810.
85. Fryburg DA: NG-monomethyl-L-arginine inhibits the blood flow but not the insulin-like response of forearm muscle to IGF-I: possible role of nitric oxide in muscle protein synthesis. J Clin Invest 1996; 97: 1319-1328.
86. Imrie H, Abbas A, Viswambharan H, Rajwani A, Cubbon RM, Gage M, Kahn M, Ezzat VA, Duncan ER, Grant PJ, Ajjan R, Wheatcroft SB, Kearney MT: Vascular insulin-like growth factor-I resistance and diet-induced obesity. Endocrinology 2009; 150: 4575-4582.
87. Holly JM, Amiel SA, Sandhu RR, Rees LH, Wass JA: The role of growth hormone in diabetes mellitus. J Endocrinol 1988; 118: 353-364.
88. Michell BJ, Griffiths JE, Mitchelhill KI, Rodriguez-Crespo I, Tiganis T, Bozinovski S, de Montellano PR, Kemp BE, Pearson RB: The Akt kinase signals directly to endothelial nitric oxide synthase. Curr Biol 1999; 9: 845-848.
89. Elzaouk L, Leimbacher W, Turri M, Ledermann B, Burki K, Blau N, Thony B: Dwarfism and low insulin-like growth factor-1 due to dopamine depletion in Pts-/-mice rescued by feeding neurotransmitter precursors and H4-biopterin. J Biol Chem 2003; 278: 28303-28311.
90. Tanaka J, Koshimura K, Murakami Y, Kato Y: Possible involvement of tetrahydrobiopterin in the trophic effect of insulin-like growth factor-1 on rat pheochromocytoma-12 (PC12) cells. Neurosci Lett 2002; 328: 201-203.
91. Bailey-Downs LC, Sosnowska D, Toth P, Mitschelen M, Gautam T, Henthorn JC, Ballabh P, Koller A, Farley JA, Sonntag WE, Csiszar A, Ungvari Z: Growth hormone and IGF-1 deficiency exacerbate high-fat diet-induced endothelial impairment in obese Lewis dwarf rats: implications for vascular aging. J Gerontol A Biol Sci Med Sci 2012; 67: 553-564.
92. Blankenberg S, Rupprecht HJ, Bickel C, Torzewski M, Hafner G, Tiret L, Smieja M, Cambien F, Meyer J, Lackner KJ: Glutathione peroxidase 1 activity and cardiovascular events in patients with coronary artery disease. N Engl J Med 2003; 349: 1605-1613.
93. Abbas A, Imrie H, Viswambharan H, Sukumar P, Rajwani A, Cubbon RM, Gage M, Smith J, Galloway S, Yuldeshava N, Kahn M, Xuan S, Grant PJ, Channon KM, Beech DJ, Wheatcroft SB, Kearney MT: The insulin-like growth factor-1 receptor is a negative regulator of nitric oxide bioavailability and insulin sensitivity in the endothelium. Diabetes 2011; 60: 2169-2178.
94. Li Y, Higashi Y, Itabe H, Song YH, Du J, Delafontaine P: Insulin-like growth factor-1 receptor activation inhibits oxidized LDL-induced cytochrome C release and apoptosis via the phosphatidylinositol 3 kinase/Akt signaling pathway. Arterioscler Thromb Vasc Biol 2003; 23: 2178-2184.
95. Hayashi K, Saga H, Chimori Y, Kimura K, Yamanaka Y, Sobue K: Differentiated phenotype of smooth muscle cells depends on signaling pathways through insulin-like growth factors and phosphatidylinositol 3-kinase. J Biol Chem 1998; 273: 28860-28867.
96. Liu ZP, Wang Z, Yanagisawa H, Olson EN: Phenotypic modulation of smooth muscle cells through interaction of Foxo4 and myocardin. Dev Cell 2005; 9: 261-270.
97. 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 1999; 19: 2119-2126.
98. Tabet F, Schiffrin EL, Touyz RM: Mitogen-activated protein kinase activation by hydrogen peroxide is mediated through tyrosine kinase-dependent, protein kinase C-independent pathways in vascular smooth muscle cells: upregulation in spontaneously hypertensive rats. J Hypertens 2005; 23: 2005-2012.
99. Azar ZM, Mehdi MZ, Srivastava AK: Activation of insulin-like growth factor type-1 receptor is required for H 2 O 2-induced PKB phosphorylation in vascular smooth muscle cells. Can J Physiol Pharmacol 2006; 84: 777-786.
100. Gorlach A, Brandes RP, Bassus S, Kronemann N, Kirchmaier CM, Busse R, Schini-Kerth VB: Oxidative stress and expression of p22phox are involved in the up-regulation of tissue factor in vascular smooth muscle cells in response to activated platelets. FASEB J 2000; 14: 1518-1528.
101. Loh K, Deng H, Fukushima A, Cai X, Boivin B, Galic S, Bruce C, Shields BJ, Skiba B, Ooms LM, Stepto N, Wu B, Mitchell CA, Tonks NK, Watt MJ, Febbraio MA, Crack PJ, Andrikopoulos S, Tiganis T: Reactive oxygen species enhance insulin sensitivity. Cell Metab 2009; 10: 260-272.
102. Gardner CD, Eguchi S, Reynolds CM, Eguchi K, Frank GD, Motley ED: Hydrogen peroxide inhibits insulin signaling in vascular smooth muscle cells. Exp Biol Med (Maywood) 2003; 228: 836-842.
103. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR: Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med 2006; 12: 1075-1080.
104. Clarke MC, Littlewood TD, Figg N, Maguire JJ, Davenport AP, Goddard M, Bennett MR: Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res 2008; 102: 1529-1538.
105. 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 2001; 33: 1777-1789.
106. Wang J, Razuvaev A, Folkersen L, Hedin E, Roy J, Brismar K, Hedin U: The expression of IGFs and IGF binding proteins in human carotid atherosclerosis, and the possible role of IGF binding protein-1 in the regulation of smooth muscle cell proliferation. Atherosclerosis 2012; 220: 102-109.
107. Jia G, Cheng G, Gangahar DM, Agrawal DK: Insulin-like growth factor-1 and TNF-alpha regulate autophagy through c-jun N-terminal kinase and Akt pathways in human atherosclerotic vascular smooth cells. Immunol Cell Biol 2006; 84: 448-454.
108. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T: Ischemia-and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med 1999; 5: 434-438.
109. Rauscher FM, Goldschmidt-Clermont PJ, Davis BH, Wang T, Gregg D, Ramaswami P, Pippen AM, Annex BH, Dong C, Taylor DA: Aging, progenitor cell exhaustion, and atherosclerosis. Circulation 2003; 108: 457-463.
110. Thum T, Hoeber S, Froese S, Klink I, Stichtenoth DO, Galuppo P, Jakob M, Tsikas D, Anker SD, Poole-Wilson PA, Borlak J, Ertl G, Bauersachs J: Age-dependent impairment of endothelial progenitor cells is corrected by growth-hormone-mediated increase of insulin-like growth-factor-1. Circ Res 2007; 100: 434-443.
111. Tilki D, Hohn HP, Ergun B, Rafii S, Ergun S: Emerging biology of vascular wall progenitor cells in health and disease. Trends Mol Med 2009; 15: 501-509.
112. Degens H: The role of systemic inflammation in age-related muscle weakness and wasting. Scand J Med Sci Sports 2010; 20: 28-38.
113. Hammers DW, Matheny RW Jr, Sell C, Adamo ML, Walters TJ, Estep JS, Farrar RP: Impairment of IGF-I expression and anabolic signaling following ischemia/reperfusion in skeletal muscle of old mice. Exp Gerontol 2011; 46: 265-272.
114. Matata BM, Galinanes M: Peroxynitrite is an essential component of cytokines production mechanism in human monocytes through modulation of nuclear factor-kappa B DNA binding activity. J Biol Chem 2002; 277: 2330-2335.
115. Succurro E, Andreozzi F, Sciacqua A, Hribal ML, Perticone F, Sesti G: Reciprocal association of plasma IGF-1 and interleukin-6 levels with cardiometabolic risk factors in nondiabetic subjects. Diabetes Care 2008; 31: 1886-1888.
116. Jeschke MG, Herndon DN, Barrow RE: Insulin-like growth factor I in combination with insulin-like growth factor binding protein 3 affects the hepatic acute phase response and hepatic morphology in thermally injured rats. Ann Surg 2000; 231: 408-416.
117. Spies M, Wolf SE, Barrow RE, Jeschke MG, Herndon DN: Modulation of types I and II acute phase reactants with insulin-like growth factor-1/binding protein-3 complex in severely burned children. Crit Care Med 2002; 30: 83-88.
118. Roubenoff R, Parise H, Payette HA, Abad LW, D'Agostino R, Jacques PF, Wilson PW, Dinarello CA, Harris TB: Cytokines, insulin-like growth factor 1, sarcopenia, and mortality in very old community-dwelling men and women: the Framingham Heart Study. Am J Med 2003; 115: 429-435.
119. Serri O, Li L, Maingrette F, Jaffry N, Renier G: Enhanced lipoprotein lipase secretion and foam cell formation by macrophages of patients with growth hormone deficiency: possible contribution to increased risk of atherogenesis? J Clin Endocrinol Metab 2004; 89: 979-985.
120. Renier G, Clement I, Desfaits AC, Lambert A: Direct stimulatory effect of insulin-like growth factor-I on monocyte and macrophage tumor necrosis factor-alpha production. Endocrinology 1996; 137: 4611-4618.
121. Hochberg Z, Hertz P, Maor G, Oiknine J, Aviram M: Growth hormone and insulin-like growth factor-I increase macrophage uptake and degradation of low density lipoprotein. Endocrinology 1992; 131: 430-435.
122. 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 1992; 90: 439-446.
123. Fournier T, Riches DW, Winston BW, Rose DM, Young SK, Noble PW, Lake FR, Henson PM: Divergence in macrophage insulin-like growth factor-I (IGF-I) synthesis induced by TNF-alpha and prostaglandin E2. J Immunol 1995; 155: 2123-2133.
124. Kotsis V, Stabouli S, Karafillis I, Nilsson P: Early vascular aging and the role of central blood pressure. J Hypertens 2011; 29: 1847-1853.
125. Standley PR, Zhang F, Ram JL, Zemel MB, Sowers JR: Insulin attenuates vasopressin-induced calcium transients and a voltage-dependent calcium response in rat vascular smooth muscle cells. J Clin Invest 1991; 88: 1230-1236.
126. Galderisi M, Vitale G, Lupoli G, Barbieri M, Varricchio G, Carella C, de Divitiis O, Paolisso G: Inverse association between free insulin-like growth factor-1 and isovolumic relaxation in arterial systemic hypertension. Hypertension 2001; 38: 840-845.
127. Tivesten A, Bollano E, Andersson I, Fitzgerald S, Caidahl K, Sjogren K, Skott O, Liu JL, Mobini R, Isaksson OG, Jansson JO, Ohlsson C, Bergstrom G, Isgaard J: Liver-derived insulin-like growth factor-I is involved in the regulation of blood pressure in mice. Endocrinology 2002; 143: 4235-4242.
128. Vecchione C, Colella S, Fratta L, Gentile MT, Selvetella G, Frati G, Trimarco B, Lembo G: Impaired insulin-like growth factor I vasorelaxant effects in hypertension. Hypertension 2001; 37: 1480-1485.
129. Hongo K, Nakagomi T, Kassell NF, Sasaki T, Lehman M, Vollmer DG, Tsukahara T, Ogawa H, Torner J: Effects of aging and hypertension on endothelium-dependent vascular relaxation in rat carotid artery. Stroke 1988; 19: 892-897.
130. Hasdai D, Holmes DR Jr, Richardson DM, Izhar U, Lerman A: Insulin and IGF-I attenuate the coronary vasoconstrictor effects of endothelin-1 but not of sarafotoxin 6c. Cardiovasc Res 1998; 39: 644-650.
131. Duerrschmidt N, Wippich N, Goettsch W, Broemme HJ, Morawietz H: Endothelin-1 induces NAD(P)H oxidase in human endothelial cells. Biochem Biophys Res Commun 2000; 269: 713-717.
132. Li L, Fink GD, Watts SW, Northcott CA, Galligan JJ, Pagano PJ, Chen AF: Endothelin-1 increases vascular superoxide via endothelin(A)-NADPH oxidase pathway in low-renin hypertension. Circulation 2003; 107: 1053-1058.
133. Wedgwood S, McMullan DM, Bekker JM, Fineman JR, Black SM: Role for endothelin-1-induced superoxide and peroxynitrite production in rebound pulmonary hypertension associated with inhaled nitric oxide therapy. Circ Res 2001; 89: 357-364.
134. Frank HJ, Levin ER, Hu RM, Pedram A: Insulin stimulates endothelin binding and action on cultured vascular smooth muscle cells. Endocrinology 1993; 133: 1092-1097.
135. Kwok CF, Juan CC, Shih KC, Hwu CM, Jap TS, Ho LT: Insulin-like growth factor-1 increases endothelin receptor A levels and action in cultured rat aortic smooth muscle cells. J Cell Biochem 2005; 94: 1126-1134.