330
Views
14
CrossRef citations to date
0
Altmetric
Review

Insulin, insulin analogues and diabetic retinopathy

, &
Pages 54-62 | Received 24 Oct 2007, Accepted 08 Jan 2008, Published online: 10 Oct 2008

References

  • Aguilar E, Friedlander M, Gariano R F. Endothelial proliferation in diabetic retinal microaneurysms. Arch Ophthalmol 2003; 121: 740–741
  • Antonetti D A, Barber A J, Bronson S K, Freeman W M, Gardner T W, Jefferson L S, Kester M, Kimball S R, Krady J K, Lanoue K F, et al. Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 2006; 55: 2401–2411
  • Ashton N. Pathogenesis of diabetic retinopathy. Diabetic Retinopathy, H L Little, R L Jack, A Patz, P H Forsham. Thieme-Stratton Inc, New York 1983; 85–106
  • Bereket A, Lang C H, Wilson T A. Alterations in the growth homone-insulin-like growth factor axis in insulin dependent diabetes mellitus. Horm Metab Res 1999; 31: 172–181
  • Berger M R, Fink M, Feichter G E, Janetschek P. Effects of diazoxide-induced reversible diabetes on chemically induced autochthonus mammary carcinomas in Sprague-Dawley rats. Int J Cancer 1985; 35: 395–401
  • Bergman P B, Moravski C J, Edmondson S R, Russo V C, Bach L A, Wilkinson-Berka J L, Werther G A. Expression of the IGF system in normal and diabetic transgenic (mRen-2)27 rat eye. Invest Ophthalmol Vis Sci 2005; 46: 2708–2715
  • Brinchmann-Hansen O, Dahl-Jorgensen K, Hanssen K F, Sandvik L, the Oslo Study Group. Effect of intensified insulin treatment on various lesions of diabetic retinopathy. Am J Ophthalmol 1985; 100: 644–653
  • Buchbinder A, Miodovnik M, McElvy S, Rosenn B, Kranias G, Khoury J, Siddiqi T A. Is insulin lispro associated with the development or progression of diabetic retinopathy during pregnancy. Am J Obstet Gynecol 2000; 183: 1162–1165
  • Cassar J, Kohner E M, Hamilton A M, Gordon H, Joplin G F. Diabetic retinopathy and pregnancy. Diabetologia 1978; 15: 105–111
  • Chantelau E. Evidence that up-regulation of serum IGF-1 concentration can trigger acceleration of diabetic retinopathy. Br J Ophthalmol 1998; 82: 725–730
  • Chantelau E, Volaco A, Meyer-Schwickerath R. New insights into the pathogenesis of diabetic retinopathy—hormonal rather than metabolic factors are important. VASA 2004; 33: 205–210, (Erratum: VASA 2005;34:66)
  • Chao J R, Lai M Y, Azen S P, Klein R, Varma R, the Los Angeles Eye Study Group. Retinopathy in persons without diabetes: the Los Angeles Latino Eye Study. Invest Ophthalmol Vis Sci 2007; 48: 4019–4025
  • Chisalita S I, Arnqvist H J. Insulin-like growth factor I receptors are more abundant than insulin receptors in human micro- and macrovascular endothelial cells. Am J Physiol Endocrinol Metab 2004; 286: E896–E901
  • Chisalita S I, Nitert M D, Arnqvist H J. Characterisation of receptors for IGF-1 and insulin; evidence for hybrid insulin/IGF-1 receptor in human coronary artery endothelial cells. Growth Horm IGF Res 2006; 16: 258–266
  • Danis R P, Bingaman D P. Insulin-like growth factor-1 retinal microangiopathy in the pig eye. Ophthalmology 1997; 104: 1661–169
  • Davis M D, Beck R W, Home P D, Sandow J, Ferris F L. Early retinopathy progression in four randomized trials comparing insulin glargine and NPH insulin. Exp Clin Endocrinol Diabetes 2007; 115: 240–243, (Erratum in: Exp Clin Endocrinol Diabetes 2007;115:473)
  • De Bosch B J, Baur E, Deo B K, Hiraoka M, Kumagai A K. Effects of insulin-like growth factor-1 on retinal endothelial cell glucose transport and proliferation. J Neurochem 2001; 77: 1157–1167
  • Diabetes Control and Complications Trial Research Group. Early worsening of diabetic retinopathy in the Diabetes Control and Complications Trial. Arch Ophthalmol 1998; 116: 874–886, (Erratum: Arch Ophthalmol 1998;116:1469)
  • Diabetes Control and Complications Trial Research Group. The relationship of glycemic exposure (HbA1c) to the risk of development and progression of retinopathy in the Diabetes Control and Complications Trial. Diabetes 1995a; 44: 968–983
  • Diabetes Control and Complications Trial Research Group. Progression of retinopathy with intensive vs. conventional treatment in the Diabetes Control and Complications Trial. Ophthalmology 1995b; 102: 647–661
  • Diabetes Control and Complications Trial Research Group. The effect of intensive diabetes treatment on the progression of diabetic retinopathy in insulin-dependent diabetes mellitus. The DCCT Arch Ophthalmol 1995c; 113: 36–51
  • Eckel J. Insulin analogs revisited. Curr Med Chem Immunology, Endoc & Metab Agents 2005; 5: 475–484
  • Ekström K, Salemy J, Zachrisson I, Carlsson-Skwirut C, Örtqvist E, Bang P. Normalization of the IGF-IGFBP axis by sustained nightly insulinization in type-1 diabetes. Diabetes Care 2007; 30: 1357–1363
  • EMEA (European Medicines Agency). 2004a. EPARs for authorised medicinal product for human use-Actrapid, www.emea.europa.eu/humandocs/Humans/EPAR/actrapid/actrapid.htm (accessed September 2007).
  • EMEA (European Medicines Agency). 2004b. EPARs for authorised medicinal product for human use-Levemir, www.emea.europa.eu/humandocs/Humans/EPAR/levemir/levemir.htm (accessed September 2007).
  • EMEA (European Medicines Agency). 2004c. EPARs for authorised medicinal product for human use-NovoRapid, www.emea.europa.eu/humandocs/Humans/EPAR/novorapid/novorapid.htm (accessed September 2007).
  • EMEA (European Medicines Agency). 2005a. EPARs for authorised medicinal product for human use-Apidra, www.emea.europa.eu/humandocs/Humans/EPAR/apidra/apidra.htm (accessed September 2007).
  • EMEA (European Medicines Agency). 2005b. EPARs for authorised medicinal product for human use-Humalog, www.emea.europa.eu/humandocs/Humans/EPAR/humalog/humalog.htm (accessed September 2007).
  • EMEA (European Medicines Agency). 2005c. EPARs for authorised medicinal product for human use-Insuman, www.emea.europa.eu/humandocs/Humans/EPAR/insuman/insuman.htm (accessed September 2007).
  • EMEA (European Medicines Agency). 2005d. EPARs for authorised medicinal product for human use-Lantus, www.emea.europa.eu/humandocs/Humans/EPAR/lantus/lantus.htm (accessed September 2007).
  • Fischer F. Klinische Studie zur Retinitis diabetica proliferans (in German). Graefes Archiv für Ophthalmologie 1955; 156: 552–560
  • Frankfurter Allgemeine Zeitung. 2007. Aktie von Novo Nordisk eignet sich als defensives Investment, 12 September 2007.
  • Garg S K, Pennington M, Gottlieb P, Anderson J, Jenning K, Robinson J. Comparison of maternal and fetal outcome between human regular and Humalog® insulin treated pregnancies in type-1 diabetes (Abstract). Diabetes 1999; 48/Suppl.1: A61
  • Gariano R F, Gardner T W. Retinal angiogenesis in development and disease. Nature 2005; 438: 960–966
  • Grant M B, Mames R N, Fitzgerald C, Ellis E A, Aboufriekha M, Guy J. Insulin-like growth factor 1 acts as an angiogenic agent in rabbit cornea and retina: comparative studies with basic fibroblast growth factor. Diabetologia 1993; 36: 282–291
  • Hammes H P. Pericytes and the pathogenesis of diabetic retinopathy. Horm Metab Res 2005; 37/Suppl.1: 39–43
  • Hedman C A, Orre-Pettersson A C, Lindström T, Arnqvist H J. Treatment with insulin lispro changes the insulin profile but does not affect the plasma concentrations of IGF-1 and IGFBP-1 in type-1 diabetes. Clin Endocrinol 2001; 55: 107–112
  • Hellström A, Perruzzi C, Ju M, Engstrom E, Hard A L, Liu J L, Albertsson-Wikland K, Carlsson B, Niklasson A, Sjodell L, et al. Low IGF-1 suppresses VEGF-survival signaling in retinal endothelial cells: direct correlation with clinical retinopathy of prematurity. Proc Natl Acad Sci USA 2001; 98: 5804–5808
  • Hennige A M, Sartorius T, Tschritter O, Preissl H, Fritsche A, Ruth P, Häring H U. Tissue selectivity of insulin detemir action in vivo. Diabetologia 2006; 49: 1274–1282
  • Hennige A M, Strack V, Metzinger E, Seipke G, Häring HU,Kellerer M. Effects of new insulin analogues HMR1964(insulin glulisine) and HMR1423 on insulin receptors. Diabetologia 2005a; 48: 1891–1897
  • Hennige A M, Lehmann R, Weigert C, Moeschel K, Schäuble M, Metzinger E, Lammers R, Häring H U. Insulin Glulisine. Insulin receptor signaling characteristics in vivo. Diabetes 2005b; 54: 361–366
  • Home P D, Rosskamp R, Forjanic-Klapproth J, Dressler A. A randomized multicentre trial of insulin glargine compared with NPH insulin in people with type-1 diabetes. Diabetes Metab Rev Res 2005; 21: 545–553
  • Hussain M A, Studer K, Messmer E P, Froesch E R. Treatment with insulin-like growth factor I alters capillary permeability in skin and retina. Diabetes 1995; 44: 1209–1212
  • Janssen J AMJL, Lamberts S WJ. Circulating IGF-1 and its protective role in the pathogenesis of diabetic angiopathy. Clin Endocrinol (Oxf) 2000; 52: 1–9
  • Joussen A M, Fauser S, Krohne T U, Lemmen K D, Lang G E, Kirchhof B. Diabetic retinopathy. Pathophysiology and therapy of hypoxia-induced inflammation (in German). Ophthalmologe 2003; 100: 363–370
  • Jovanovic L, Pettitt D J. Treatment with insulin and its analogs in pregnancies complicated by diabetes. Diabetes Care 2007; 30/Suppl.2: S220–S224
  • Kern T S, Miller C M, Du Y, Zheng L, Mohr S, Ball S L, Kim M, Jamison J A, Bingaman D P. Topical administration of nepafenac inhibits diabetes-induced retinal microvascular disease and underlying abnormalities of retinal metabolism and physiology. Diabetes 2007; 56: 373–379
  • Kitamei H, Yokoi M, Kase M, Ohno S. Retinal neovascularization during treatment with IGF-1 for insulin resistance syndrome. Graefe's Arch Clin Exp Ophthalmol 2005; 243: 715–717
  • Kitzmiller J L, Main E, Ward B, Theiss T, Peterson D L. Insulin lispro and the development of proliferative diabetic retinopathy during pregnancy (Letter). Diabetes Care 1999; 22: 874–876
  • Kobayashi T, Puro D G. Loss of insulin-mediated vasoprotection: early effect of diabetes on pericyte-containing microvessels of the retina. Invest Ophthalmol Vis Sci 2007; 48: 2350–2355
  • Kohner E M, Patel V, Rassam S MB. Role of blood flow and impaired autoregulation in the pathogenesis of diabetic retinopathy. Diabetes 1995; 44: 603–607
  • Kondo T, Vicent D, Suzuma K, Yanagisawa M, King G L, Holzenberger M, Kahn R C. Knockout of insulin and IGF-1 receptors on vascular endothelial cells protect against retinal neo-vascularisation. J Clin Invest 2003; 111: 1835–1842
  • Kurtzhals P, Schäffer L, Sorensen A, Kristensen C, Jonassen I, Schmid C, Trüb T. Correlations of receptor binding and metabolic and mitogenic potencies of insulin analogs designed for clinical use. Diabetes 2000; 49: 999–1005
  • Laron Z. Laron syndrome (primary growth hormone resistance or insensitivity). The personal experience 1958–2003. J Clin Endocrinol Metab 2004; 89: 1031–1044
  • Lauritzen T, Frost-Larsen K, Larsen H W, Deckert T, Steno Study Group. Effect of 1 year of near-normal blood glucose levels on diabetic retinopathy in insulin-dependent diabetics. Lancet 1983; i: 200–204
  • Layton C J, Becker S, Osborne N N. The effect of insulin and glucose levels on retinal glial cell activation and pigment epithelium-derived fibroblast growth factor-2. Molecular Vision 2006; 12: 43–54
  • Leber T. Über die Erkrankungen des Augen bei Diabetes mellitus. Graefes Archiv für Ophthalmologie 1875; 21/III: 206–337
  • Lee H K, Suh K I, Koh C S, Min H K, Lee J H, Chung H. Effect of SMS 201-995 in rapidly progressive diabetic retinopathy (Letter). Diabetes Care 1988; 11: 441–443
  • Lee P D, Giudice L C, Conover C A, Powell D R. Insulin-like growth factor binding protein-1: recent findings and new directions. Proc Soc Exp Biol Med 1997; 216: 319–357
  • Loukovaara S, Immonen I, Teramo K A, Kaaja R. Progression of retinopathy during pregnancy in type-1 diabetic women treated with insulin lispro. Diabetes Care 2003; 26: 1193–1198
  • Martin X D, Zenobi P D. Type A syndrome of insulin resistance: anterior chamber anomalies of the eye and effects of insulin-like growth factor-1 on the retina. Ophthalmologica 2001; 215: 117–123
  • Massi-Benedetti M, Humburg E, Dressler A, Ziemen M. A one-year, randomised, multicentre trial comparing insulin glargine with NPH insulin in combination with oral agents in patients with type-2 diabetes. Horm Metab Res 2003; 35: 189–196
  • Meyer-Schwickerath R, Pfeiffer A, Blum W F, Freyberger H, Klein M, Lösche C, Röllmann R, Schatz H. Vitreous levels of the insulin-like growth factorsI and II, and the insulin-like growth factor binding proteins 2 and 3, increase in neovascular eye disease. Studies in nondiabetic and diabetic subjects. J Clin Invest 1993; 92: 2620–2625
  • Min Shi, You-Min Feng. Studies on growth-promoting action of insulin: mitogenic activity of insulin and its analogues in mouse mammary tumor cells. Biochem Mol Biol Int 1997; 43: 705–711
  • Murata T, Nakagawa K, Khalil A, Ishibashi T, Inomata H, Sueishi K. The relation between expression of vascular endothelial growth factor and breakdown of the blood-retinal barrier in diabetic rat retinas. Lab Invest 1996; 74: 819–825
  • Patel J I, Hykin P G, Cree I A. Diabetic cataract removal: postoperative progression of maculopathy-growth factor and clinical analysis. Br J Ophthalmol 2006; 90: 697–701
  • Persson B, Swahn M L, Hjertberg R, Hanson U, Nord E, Nordlander E, Hansson L O. Insulin lispro therapy in pregnancies complicated by type-1 diabetes mellitus. Diabetes Res Clin Pract 2002; 58: 115–121
  • Peters K, Garg S K, Jackson W E, Mackenzie T, Queen J, Anil S, Chase P. Diabetic retinopathy in patients with type 1 diabetes treated with insulin glargine or NPH. Abstract. Diabetes 2001; 50/Suppl 2: A443
  • Pfeiffer A, Spranger J, Meyer-Schwickerath R, Schatz H. Growth factor alterations in advanced diabetic retinopathy. A possible role of blood retina barrier breakdown. Diabetes 1997; 46/Suppl. 2: S26–S30
  • Porta M, Townsend C, Clover G M, Nanson M, Alderson A R, McCraw A, Kohner E M. Evidence for functional endothelial cell damage in early diabetic retinopathy. Diabetologia 1981; 20: 597–601
  • Poulaki V, Qin W, Joussen A M, Hurlbut P, Wiegand S J, Rudge J, Yancopoulos G D, Adamis A P. Acute intensive insulin therapy exacerbates diabetic blood-retinal barrier breakdown via hypoxia-inducible factor 1 alpha and VEGF. J Clin Invest 2002; 109: 805–815
  • Poulaki V, Joussen A M, Mitsiades N, Mitsiades C S, Iliaki E F, Adamis A P. Insulin-like growth factor-1 plays a pathogenic role in diabetic retinopathy. Am J Pathol 2004; 165: 457–469
  • Quattrin T, Thrailkill K, Baker L, Kuntze J, Compton P, Martha P, rhIGF-1 Study Group. Improvement of HbA1c without increased hypoglycemia in adolescents and young adults with type-1 diabetes mellitus treated with recombinant human insulin-like growth factor-1 and insulin. rhIGF-1 in IDDM Study Group. J Pediatr Endocrinol Metab 2001; 14: 267–277
  • Rakatzi I, Ramrath S, Ledwig D, Dransfeld O, Bartels T, Seipke G, Eckel J. A novel insulin analog with unique properties. Diabetes 2003; 52: 2227–2238
  • Ratner R E, Hirsch I B, Neifing J L, Garg S K, Mecca T E, Wilson C A. Less hypoglycemia with insulin glargine in intensive insulin therapy for type-1 diabetes. US Study Group of Insulin Glargine in Type-1 Diabetes. Diabetes Care 2000; 23: 639–643
  • Reiter C E, Gardner T W. Functions of insulin and insulin receptor signaling in retina: possible implications for diabetic retinopathy. Prog Retin Eye Res 2003; 22: 545–562
  • Reiter C E, Wu X, Sandirasegarane L, Nakamura M, Gilbert K A, Singh R S, Fort P E, Antonetti D A, Gardner T W. Diabetes reduces basal retinal insulin receptor signaling: reversal with systemic and local insulin. Diabetes 2006; 55: 1148–1156
  • Renehan A G, Shalet S M. Diabetes, insulin therapy, and colorectal cancer. Br Med J 2005; 330: 551–552
  • Rosenstock J, Park G, Zimmerman J, US Insulin Glargine (HOE 901) Typ-1 Diabetes Investigator Group. Basal insulin glargine (HOE 901) versus NPH insulin in patients with type-1 diabetes on multiple daily insulin regimens. US Insulin Glargine (HOE) Type-1 Diabetes Investigator Group. Diabetes Care 2000; 23: 1137–1142
  • Ruberte J, Ayuso E, Navarro M, Carretero A, Nacher V, Haurigot V, George M, Llombart C, Casellas A, Costa C, et al. Increased ocular levels of IGF-1 in transgenic mice lead to diabetes-like eye disease. J Clin Invest 2004; 113: 1149–1157
  • Sasaoka T, Tsuneki H, Wada T. Comparison of intracellular signaling properties induced by the long-acting insulin analogues glargine and detemir in cultured cells (Abstract). Diabetologia 2007; 50/Suppl.1: S234
  • Shaw L C, Grant M B. Insulin like growth factor-1 and insulin-like growth factor binding proteins: their possible roles in both maintaining normal retinal vascular function and in promoting retinal pathology. Rev Endocr Metab Disord 2004; 5: 199–207
  • Shigetou M, Sagawa T, Ishibashi T, Nakashima N, Umeda F, Nawata H. Exacerbation of diabetic retinopathy following systemic insulin-like growth factor-1. Report of a case. Rinsho Ganka (Jpn J Clin Ophthalmol) 1997; 51: 1251–1255
  • Slawik M, Schories M, Busse Grawitz A, Reincke M, Petersen K G. Treatment with insulin glargine does not suppress serum IGF-1. Diabetic Med 2006; 23: 814–817
  • Slomiany M G, Rosenzweig S A. Hypoxia-inducible factor-1-dependent and -independent regulation of insulin-like growth factor-1 stimulated vascular endothelial growth factor secretion. J Pharmacol Exp Ther 2006; 318: 666–675
  • Smeeton F J, Shojaee-Moradie F, Jackson N, Jones R H, Umpleby A M, Russel-Jones D. Is insulin detemir hepatoselective when compared to NPH insulin using stable isotope methodology at plasma glucose concentrations of less than 4 mml/l? (Abstract). Diabetologia 2007; 50/Suppl.1: S24
  • Smith L EH. IGF-1 and retinopathy of prematurity in the preterm infant. Biol Neonate 2005; 88: 237–244
  • Sone H, Kawakami Y, Okuda Y, Sekine Y, Honmura S, Matsuo K, Segawa T, Suzuki H, Yamashita K. Ocular vascular endothelial growth factor levels in diabetic rats are elevated before observable retinal proliferative changes. Diabetologia 1997; 40: 726–730
  • Stammberger I, Seipke G, Bartels T. Insulin glulisine—a comprehensive preclinical evaluation. Int J Toxicol 2006; 25: 25–33
  • Suto C, Hori S, Kato S, Muraoka K, Kitano S. Effect of perioperative glycemic control in progression of diabetic retinopathy and maculopathy. Arch Ophthalmol 2006; 124: 38–45
  • The Kroc Collaborative Study Group. Diabetic retinopathy after 2 years of intensified insulin treatment. JAMA 1988; 260: 37–41
  • Treins C, Giorgetti-Peraldi S, Murdaca J, Semenza G L, Van Obberghen E. Insulin stimulates hypoxia-inducible factor 1 through a phosphatidylinositol 3-kinase/target of rapamycin-dependent signaling pathway. J Biol Chem 2002; 31: 27975–27981
  • Treins C, Giorgetti-Peraldi S, Murdaca J, Monthouel-Kartmann M N, Van Obberghen E. Regulation of hypoxia-inducible factor (HIF)-1 activity and expression of HIF hydroxylases in response to insulin-like growth factor 1. Mol Endocrinol 2005; 19: 1304–1317
  • Vigneri R, Belfiore A. Insulin and its receptor in growth promotion. Diabetes in the New Millenium, U DiMario, F Leonetti, G Pugliese, P Sbraccia, A Signore. John Wiley & Sons, Ltd, Chichester 2000; 151–160

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.