Metabolism - Clinical and Experimental
Volume 44 , Pages 58-66 , October 1995

The insulin-like growth factor system in vascular smooth muscle: Interaction with insulin and growth factors

  • Hans J. Arnqvist

      Affiliations

    • Corresponding Author InformationAddress reprint requests to Hans J. Amgvist, MD, Department of Internal Medicine, University Hospital, S-58185 Linköping, Sweden.
    • Departments of Internal Medicine and Cell Biology, Faculty of Health Sciences, University of Linkbping, Linköping, Sweden
    • Department of Pathology, University of Washington, Seattle, WA, USA
  • ,
  • Karin E. Bornfeldt

      Affiliations

    • Departments of Internal Medicine and Cell Biology, Faculty of Health Sciences, University of Linkbping, Linköping, Sweden
    • Department of Pathology, University of Washington, Seattle, WA, USA
  • ,
  • Yun Chen

      Affiliations

    • Departments of Internal Medicine and Cell Biology, Faculty of Health Sciences, University of Linkbping, Linköping, Sweden
    • Department of Pathology, University of Washington, Seattle, WA, USA
  • ,
  • Torbjörn Lindström

      Affiliations

    • Departments of Internal Medicine and Cell Biology, Faculty of Health Sciences, University of Linkbping, Linköping, Sweden
    • Department of Pathology, University of Washington, Seattle, WA, USA

References 

  1. Schwartz SM, Heimark RL, Majesky MW. Developmental mechanisms underlying pathology of arteries. Physiol Rev. 1990;70:1177–1209
  2. Campbell GR, Campbell JH. Smooth muscle phenotypic changes in arterial wall homeostasis: Implications for the pathogenesis of atherosclerosis. Exp Mol Pathol. 1985;42:139–162
  3. Ross R. The pathogenesis of atherosclerosis: A perspective for the 1990s. Nature. 1993;362:801–809
  4. Nilsson J. Cytokines and smooth muscle cells in atherosclerosis. Cardiovasc Res. 1993;27:1184–1190
  5. Epstein SE, Speir E, Unger EF, et al.  The basis of molecular strategies for treating coronary restenosis after angioplasty. J Am Coll Cardiol. 1994;23:1278–1288
  6. Ferns GAA, Stewart-Lee AL, Änggård EE. Arterial response to mechanical injury: Balloon catheter de-endothelialization. Atherosclerosis. 1992;92:89–104
  7. Pauletteo P, Sarazani R, Rappelli A, et al.  Differentiation and growth of vascular smooth muscle cells in experimental hypertension. Am J Hypertens. 1994;7:661–674
  8. Bornfeldt KE, Arnqvist HJ, Dahlkvist HH, et al.  Characterization of receptors for insulin-like growth factor-I in plasma membranes isolated from bovine mesenteric arteries. Acta Endocrinol (Copenh). 1988;177:428–434
  9. Bornfeldt KE, Gidlöf R, Wastesson A, et al.  Binding and biological effects of insulin, insulin analogues and insulin-like growth factors in rat aortic smooth muscle cells. In: Comparison of maximal growth promoting activities. ed 2. Diabetologia. 34:1991;p. 307–313
  10. King GL, Goodman AD, Buzney S, et al.  Receptors and growth promoting effects of insulin and insulin-like growth factor on cells from bovine retinal capillaries and aorta. J Clin Invest. 1985;75:1028–1036
  11. Banskota NK, Taub R, Zehner K, et al.  Characterization of induction of protooncogene c-myc and cellular growth in human vascular smooth muscle cells by insulin and IGF-I. Diabetes. 1989;38:123–129
  12. Bornfeldt KE, Raines EW, Nakano T, et al.  Insulin-like growth factor-I and platelet derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signaling pathways that are distinct from those of proliferation. J Clin Invest. 1994;93:1266–1274
  13. Bornfeldt KE, Arnqvist HJ. Actions of insulin-like growth factor I and insulin in vascular smooth muscle: Receptor interaction and growth promoting effects. In:  Flyvbjerg A,  Ørskov H,  Alberti KGMM editor. Growth Hormone and Insulin-Like Growth Factor I in Human and Experimental Diabetes. Chichester, UK: Wiley; 1993;p. 159–191
  14. Jialal I, Crettaz M, Hachiya HL, et al.  Characterization of the receptors for insulin and insulin like growth factors on micro- and macrovascular tissues. Endocrinology. 1985;117:1222–1229
  15. Lee PDK, Hintz RL, Rosenfeldt RG, et al.  Presence of insulin like growth factor receptors and lack of insulin receptors on fetal bovine smooth muscle cells. In Vitro Cell Dev Biol. 1988;24:921–926
  16. De Meyts P. The structural basis of insulin and insulin-like growth factor-I receptor binding and negative co-operativity, and its relevance to mitogenic versus metabolic signalling. Diabetologia. 1994;37(suppl 2):S135–S148
  17. Christoffersen CT, Bornfeldt KE, Rotella CM, et al.  Negative cooperativity in the insulin-like growth factor-I receptor and a chimeric IGF-I/insulin receptor. Endocrinology. 1994;135:472–475
  18. Bornfeldt KE, Arnqvist HJ, Enberg B, et al.  Regulation of insulin-like growth factor-I and growth hormone receptor gene expression by diabetes and nutritional state in rat tissues. J Endocrinol. 1989;122:651–656
  19. Sarazani R, Brecher P, Chobanian AV. Growth factor expression in aorta of normotensive and hypertensive rats. J Clin Invest. 1989;83:1404–1408
  20. Murphy LJ, Ghahary A, Chakrabarti S. Insulin regulation of IGF-I expression in rat aorta. Diabetes. 1990;39:657–662
  21. Bornfeldt KE, Arnqvist HJ, Norstedt G. Regulation of insulin-like growth factor-I gene expression by growth factors in cultured vascular smooth muscle cells. J Endocrinol. 1990;125:381–386
  22. Delafontaine P, Bernstein KE, Alexander RW. Insulin-like growth factor I gene expression in vascular cells. Hypertension. 1991;17:693–699
  23. Clemmons DR, van Wyk JJ. Evidence for a functional role of endogenously produced somatomedinlike peptides in the regulation of DNA-synthesis in cultured human fibroblasts and porcine smooth muscle cells. J Clin Invest. 1985;75:1914–1918
  24. Clemmons DR. Variables controlling the secretion of a somatomedin-like peptide by cultured porcine smooth muscle cells. Circ Res. 1985;56:418–426
  25. Hoyt EC, Van Wyk JJ, Lund PK. Tissue and development specific regulation of a complex family of rat insulin-like growth factor-I messenger ribonucleic acids. Mol Endocrinol. 1988;22:1077–1086
  26. Cercek B, Fishbein MC, Forrester JS, et al.  Induction of insulin-like growth factor-I mRNA in rat aorta after balloon denudation. Circ Res. 1990;66:1755–1760
  27. Rom WN, Basset P, Fells GA, et al.  Alveolar macrophages release an insulin-like growth factor I-type molecule. J Clin Invest. 1988;82:1685–1693
  28. Kirstein M, Aston C, Hintz R, et al.  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
  29. Karey KP, Sirbasku DA. Human platelet-derived mitogens. II. Subcellular localization of insulin like growth factors I and II by purification and N-α amino acid analysis. Blood. 1989;74:1084–1092
  30. Shimasaki S, Ling N. Identification and molecular characterization of insulin-like growth factor binding proteins (IGFBP-1, -2, -3, -4, -5 and -6). Prog Growth Factor Res. 1991;3:243–266
  31. Sara VR, Hall K. Insulin-like growth factors and their binding proteins. Physiol Rev. 1990;70:591–614
  32. Chen Y, Bornfeldt KE, Arner A, et al.  Increase in insulin-like growth factor-I in hypertrophying smooth muscle. Am J Physiol. 1994;266:E224–E229
  33. Chen Y, Arnqvist HJ. Differential regulation of insulin-like growth factor binding protein-2 and -4 mRNA in muscle tissues and liver by diabetes or fasting. J Endocrinol. 1994;143:235–242
  34. McCusker RH, Camacho-Hubner C, Clemmons DR. Identification of the types of insulin-like growth factor-binding proteins that are secreted by muscle cells in vitro. J Biol Chem. 1989;264:7795–8000
  35. Kamyar A, Pirola CJ, Wang HM, et al.  Expression and insulin-like growth factor-dependent proteolysis of insulin-like growth factor-binding protein-4 are regulated by cell confluence in vascular smooth muscle cells. Circ Res. 1994;74:576–585
  36. Elgin RG, Busby WH, Clemmons DR. An insulin-like growth factor (IGF) binding protein enhances the response to IGF-I. In: ed 2. Proc Natl Acad Sci USA. 84:1987;p. 3254–3258
  37. Busby WH, Klapper DG, Clemmons DR. Purification of a 31,000-dalton insulin-like growth factor binding protein from human amniotic fluid: Isolation of two forms with different biological activities. J Biol Chem. 1988;263:14203–14210
  38. Clemmons DR. IGF binding proteins and their functions. Mol Reprod Dev. 1993;35:368–375
  39. Cohick WS, Gockerman A, Clemmons DR. Vascular smooth muscle cells synthesize two forms of insulin-like growth factor binding proteins which are regulated differentially by the insulin like growth factors. J Cell Physiol. 1993;157:52–60
  40. Jones JI, Gockerman A, Busby WH, et al.  Insulin-like growth factor binding protein 1 stimulates cell migration and binds to the α5β1 integrin by means of its Arg-Gly-Asp sequence. In: ed 2. Proc Natl Acad Sci USA. 90:1993;p. 10553–10557
  41. Tang XM, Rossi MJ, Masterson BJ, et al.  Insulin-like growth factor-I (IGF-I), IGF-I receptors, and IGF-I action in endometrial stromal and myometrial smooth muscle cells in vitro. Biol Reprod. 1994;50:1113–1122
  42. Davies RJ. The mitogen-activated protein kinase signal transduction pathway. J Biol Chem. 1993;268:14553–14556
  43. Myers MG, Sun X-J, White M. The IRS-1 signaling system. TIBS. 1994;19:289–293
  44. Mastick CC, Kato H, Robert CT, et al.  Insulin and insulin-like growth factor-I receptors similarly stimulate deoxyribonucleic acid synthesis despite differences in cellular protein tyrosine phosphorylation. Endocrinology. 1994;135:214–222
  45. Goldberg ID, Stemerman MB, Schnipper LE, et al.  Vascular smooth muscle cell kinetics: A new assay for studying patterns of cellular proliferation in vivo. Science. 1979;205:920–922
  46. Capron L, Jarnet J, Kazandjian S, et al.  Growth promoting effect of diabetes and insulin on arteries. Diabetes. 1986;35:973–978
  47. Bornfeldt KE, Arnqvist HJ, Capron L. In vivo proliferation of rat vascular smooth muscle in relation to diabetes mellitus, insulin-like growth factor I and insulin. Diabetologia. 1992;35:104–108
  48. Bornfeldt KE, Skottner A, Arnqvist HJ. In vivo regulation of messenger RNA encoding insulin-like growth factor-I (IGF-I) by diabetes, insulin and IGF-I in rat skeletal muscle, heart muscle and vascular smooth muscle. J Endocrinol. 1992;135:203–211
  49. Ridray S, Capron L, Heudes D, et al.  Effects of fasting and refeeding on the proliferative response of rat aorta to injury. Am J Physiol. 1991;261:H190–H195
  50. Grotendorst GR, Chang T, Seppä HEJ, et al.  Platelet-derived growth factor is a chemoattractant for vascular smooth muscle cells. J Cell Physiol. 1982;113:261–266
  51. Grant MB, Wargovich TJ, Ellis EA, et al.  Localization of insulin-like growth factor I and inhibition of coronary smooth muscle cell growth by somatostatin analogues in human coronary smooth muscle cells. In: A potential treatment for restenosis. ed 2. Circulation. 89:1994;p. 1511–1517
  52. Kundra V, Escobedo JA, Kazlauskas A, et al.  Regulation of chemotaxis by the platelet-derived growth factor-BB. Nature. 1994;367:474–476
  53. Stossel TP. On the crawling on animal cells. Science. 1993;260:1086–1094
  54. Clemmons DR. Exposure to platelet-derived growth factor modulates the porcine aortic smooth muscle cell response to somatomedin-C. Endocrinology. 1985;117:77–83
  55. Pfeifle B, Boeder H, Ditschuneit H. Interactions of receptors for insulin-like growth factor I, platelet-derived growth factor, and fibroblast growth factor in rat aortic cells. Endocrinology. 1987;120:2251–2258
  56. Giannella-Neto D, Kamyar A, Sharifi B, et al.  Platelet-derived growth factor isoforms decrease insulin-like growth factor I gene expression in rat vascular smooth muscle cells and selectively stimulate the biosynthesis of insulin-like growth factor binding protein 4. Circ Res. 1992;71:646–656
  57. Ko Y, Stiebler H, Nuckenig G, et al.  Synergistic action of angiotensin II, insulin-like growth factor-I and transforming growth-factor-β on platelet-derived growth factor-BB, basic fibroblast growth factor, and epidermal growth factor-induced DNA synthesis in vascular smooth muscle cells. Am J Hypertens. 1993;6:496–499
  58. Hovis JG, Meyer T, Teasdale RM, et al.  Intracellular calcium regulates insulin-like growth factor-I messenger ribonucleic acid levels. Endocrinology. 1993;132:1931–1938
  59. Delafontaine P, Bernstein KE, Alexander RW. Insulin-like growth factor-I gene expression in vascular cells. Hypertension. 1991;17:693–699
  60. Mathews LS, Norstedt G, Palmiter RD. Regulation of insulin-like growth factor I gene expression by growth hormone. In: ed 2. Proc Natl Acad Sci USA. 83:1986;p. 9343–9347
  61. Delafontaine P, Lou H. Angiotensin II regulates insulin-like growth factor I gene expression in vascular smooth muscle cells. J Biol Chem. 1993;268:16866–16870
  62. Ververis JJ, Ku L, Delafontaine P. Regulation of insulin-like growth factor-I receptors on vascular smooth muscle cells by growth factors and phorbol esters. Circ Res. 1993;72:1285–1292
  63. Rubini M, Werner H, Gandini E, et al.  Platelet-derived growth factor increases the activity of the promoter of the insulin-like growth factor-I (IGF-I) receptor gene. Exp Cell Res. 1994;211:374–379
  64. Bornfeldt K, Arnqvist HJ. Effect of insulin-like growth factor I (IGF-I) on metabolism in bovine mesenteric arteries. Acta Physiol Scand. 1987;131:563–568
  65. Tamaroglio TA, Lo CS. Regulation of fibronectin by insulin-like growth factor-I in cultured rat thoracic aortic smooth muscle cells and glomerular mesangial cells. Exp Cell Res. 1994;215:338–346
  66. Rich CB, Ewton DZ, Martin BM, et al.  IGF-regulation of elastogenesis: Comparison of aortic and lung cells. Am J Physiol. 1992;263:L276–L282
  67. Wolfe BL, Rich CB, Goud HD, et al.  Insulin-like growth factor-I regulates transcription of the elastin gene. J Biol Chem. 1993;268:12418–12426
  68. Fath KA, Alexander RW, Delafontaine P. Abdominal coarctation increases insulin-like growth factor I mRNA levels in rat aorta. Circ Res. 1993;72:271–277
  69. Anwar A, Delafontaine P. Hypertension increases insulin-like growth factor binding protein-4 mRNA levels in rat aorta. Hypertension. 1994;24:679–685
  70. Chen Y, Bornfeldt KE, Arner A, et al.  Different regulation of gene expression encoding insulin-like growth factor-I, insulin-like growth factor-binding protein-2 and -4 during smooth muscle hypertrophy. Growth Regul. 1995;5:45–52
  71. Hansson H-A, Jennische E, Skottner A. IGF-I expression in blood vessels varies with vascular load. Acta Physiol Scand. 1987;129:165–169
  72. DeVol DL, Rotwein P, Sadow JL, et al.  Activation of insulin-like growth factor gene expression during work induced skeletal muscle growth. Am J Physiol. 1990;259:E89–E95
  73. Wåhlander H, Isgaard J, Jennische E, et al.  Left ventricular insulin-like growth factor I increases in early renal hypertension. Hypertension. 1992;19:25–32
  74. Russell-Jones DL, Leach RM, Ward JPT, et al.  Insulin-like growth factor-I gene expression is increased in the right ventricular hypertrophy induced by chronic hypoxia in the rat. J Mol Endocrinol. 1993;10:99–102
  75. Flyvbjerg A, Bornfeldt KE, Ørskov H, et al.  Effect of insulin-like growth factor I infusion on renal hypertrophy in experimental diabetes in rats. Diabetologia. 1991;34:715–720
  76. Drejer K, Kruse V, Larsen UD, et al.  Receptor binding and tyrosine kinase activation by insulin analogues with extreme affinities studied in human hepatoma HepG2 cells. Diabetes. 1991;40:1488–1495
  77. Sara V, Hall K. Insulin-like growth factors and their binding proteins. Physiol Rev. 1990;70:591–614
  78. Clemmons DR, Underwood LE. Nutritional regulation of IGF-I and IGF binding proteins. Annu Rev Nutr. 1991;11:393–412
  79. Möller C, Arner P, Sonnenfeld T, et al.  Quantitative comparison of insulin-like growth factor mRNA levels in human and rat tissues analyzed by a solution hybridization assay. J Mol Endocrinol. 1991;7:213–222
  80. Brismar K, Fernquist-Forbes E, Wahren J, et al: Effect of insulin on the hepatic secretion of IGFBP-1 and IGF-I in insulin dependent diabetes. J Clin Endocrinol Metab (in press)
  81. Pyörälä K. Relationship of glucose intolerance and plasma insulin to the incidence of coronary heart disease: Results from two population studies in Finland. Diabetes Care. 1979;2:131–141
  82. Welborn TA, Wearne K. Coronary heart disease incidence and cardiovascular mortality in Busselton with reference to glucose and insulin concentrations. Diabetes Care. 1979;2:154–160
  83. Fontbonne A, Tchobroutsky G, Eschwege E, et al.  Coronary heart disease mortality risk: Plasma insulin level is a more sensitive marker than hypertension or abnormal glucose tolerance in overweight males: The Paris Prospective Study. Int J Obes. 1988;12:557–565
  84. Rönnemaa T, Laakso M, Pyörälä K, et al.  High fasting plasma insulin is an indicator of coronary heart disease in non-insulin-dependent diabetic patients and nondiabetic subjects. Arterioscler Thromb. 1991;11:80–90
  85. Pyörälä K, Laakso M, Uusitupa M. Diabetes and atherosclerosis: An epidermiologic view. Diabetes Metab Rev. 1987;3:463–524
  86. Standl E, Janka HU. High serum insulin concentrations in relation to other cardiovascular risk factors in macrovascular disease of type 2 diabetes. Horm Metab Res. 1985;15:46–51 (suppl)
  87. Bierman E. Atherogenesis in diabetes. Arterioscler Thromb. 1992;12:647–656
  88. Jarrett RJ. Risk factors for coronary heart disease in diabetes mellitus. Diabetes. 1992;41(suppl 2):1–3
  89. Stout RW. Insulin and atheroma—20-yr perspective. Diabetes Care. 1990;13:631–654
  90. Welin L, Eriksson H, Larsson B, et al.  Hyperinsulinaemia is not a major coronary risk factor in elderly men. In: The study of men born in 1913. ed 2. Diabetologia. 35:1992;p. 766–770
  91. Jarrett RJ. In defence of insulin: A critique of syndrome X. Lancet. 1992;340:469–471
  92. Liu QZ, Knowler WC, Nelson RG, et al.  Insulin treatment, endogenous insulin concentration, and ECG abnormalities in diabetic Pima Indians: Cross-sectional and prospective analyses. Diabetes. 1992;41:1141–1150
  93. Lindström T, Arnqvist HJ, von Schenck HH. Effect of conventional and intensified insulin therapy on free-insulin profiles and glycemic control in NIDDM. Diabetes Care. 1992;15:27–34
  94. Lindström T, Arnqvist HJ, Olsson AG. Effect of different insulin regimens on plasma lipoprotein and apolipoprotein concentrations in patients with non-insulin-dependent diabetes mellitus. Atherosclerosis. 1990;81:137–144
  95. Taskinen M-R, Kuusi T, Helve E, et al.  Insulin therapy induces antiatherogenic changes of serum lipoproteins in noninsulin-dependent diabetes. Arteriosclerosis. 1988;8:168–177
  96. Lindström T, Olsson AG, von Schenck aH, et al.  Insulin treatment improves microalbuminuria and other cardiovascular risk factors in patients with type 2 diabetes mellitus. J Int Med. 1994;235:253–261
  97. Lindström T, Eriksson P, Olsson AG, et al.  Long-term improvement of glycemic control by insulin treatment in NIDDM patients with secondary failure. Diabetes Care. 1994;17:719–721
  98. Jain SK, Nagi DK, Slavin BM, et al.  Insulin therapy in type 2 diabetic subjects suppresses plasminogen activator inhibitor (PAI-1) activity and proinsulin-like molecules independently of glycaemic control. Diabetic Med. 1993;10:27–32
  99. Malmberg K. Myocardial infarction and diabetes mellitus. In: ed 2. Doctoral thesis. Stockholm, Sweden: University of Stockholm; 1994;
  100. Nagi DK, Hendra TJ, Ryle AJ, et al.  The relationships of concentrations of insulin, intact proinsulin and 32–33 split proinsulin with cardiovascular risk factors in type 2 (non-insulin-dependent) diabetic subjects. Diabetologia. 1990;33:532–537
  101. Polonsky KS, Rubenstein AH. C-peptide as a measure of the secretion and hepatic extraction of insulin-Pitfalls and limitations. Diabetes. 1984;33:486–494
  102. Lindström T, Arnqvist HJ, Ludvigsson J, et al.  C-peptide profiles in patients with non-insulin-dependent diabetes mellitus before and during insulin treatment. Acta Endocrinol (Copenh). 1992;126:477–483

PII: 0026-0495(95)90222-8

Metabolism - Clinical and Experimental
Volume 44 , Pages 58-66 , October 1995