Hepatic insulin gene therapy prevents deterioration of vascular function and improves adipocytokine profile in STZ-diabetic rats

American Journal of Physiology - Endocrinology and Metabolism

Volumn 290, Issue 1, 2006, Pages

  Thulé, Peter M ^a,b   Campbell, Adam G ^a   Kleinhenz, Dean J ^a   Olson, Darin E ^a   Boutwell, Joshua J ^a   Sutliff, Roy L ^a   Hart, C Michael ^a  

^a EMORY UNIVERSITY   (United States)

^b ATLANTA VA MEDICAL CENTER   (United States)

Author keywords

Adenovirus; Adiponectin; Diabetes mellitus; Endothelium; Streptozotocin

Indexed keywords

ADENOVIRUS VECTOR; ADIPOCYTOKINE; ADIPONECTIN; BOVINE INSULIN; CHOLESTEROL; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FATTY ACID; GLUCAGON; GLUCOSE; HEMOGLOBIN; HUMAN INSULIN; INSULIN; ISOPHANE INSULIN; LEPTIN; LINPLANT; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; ACETYLCHOLINE; LIPID; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE SODIUM; NITROSYL HEMOGLOBIN; PEPTIDE HORMONE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL FUNCTION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DRUG EFFECT; ELECTRON SPIN RESONANCE; GLUCOSE BLOOD LEVEL; HOMEOSTASIS; HYPERGLYCEMIA; INSULIN RESISTANCE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STREPTOZOCIN DIABETES; VASCULAR RING; VASODILATATION; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; ADENOVIRUS; ANIMAL; AORTA; BLOOD; BODY WEIGHT; CARDIOVASCULAR FUNCTION; ERYTHROCYTE; EXPERIMENTAL DIABETES MELLITUS; GENE THERAPY; GENETICS; HUMAN; IN VITRO STUDY; INTRAVENOUS DRUG ADMINISTRATION; LIVER; METABOLISM; METHODOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ACETYLCHOLINE; ADENOVIRIDAE; ADIPONECTIN; ANIMALS; AORTA; BLOOD GLUCOSE; BODY WEIGHT; CARDIOVASCULAR PHYSIOLOGY; DIABETES MELLITUS, EXPERIMENTAL; ERYTHROCYTES; GENE THERAPY; GLUCAGON; HEMOGLOBINS; HUMANS; INJECTIONS, INTRAVENOUS; INSULIN; INSULIN RESISTANCE; LEPTIN; LIPIDS; LIVER; MALE; NITRIC OXIDE SYNTHASE; NITROPRUSSIDE; PEPTIDE HORMONES; RATS; RATS, SPRAGUE-DAWLEY; VASODILATION;

EID: 33644876113     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00134.2005     Document Type: Article

References (75)

1. Alberti G, Zimmet P, Shaw J, Bloomgarden Z, Kaufman F, Silink M, and Consensus Workshop G. Type 2 diabetes in the young: the evolving epidemic: the international diabetes federation consensus workshop. Diabetes Care 27: 1798-1811, 2004.
2. Alp N, Mussa S, Khoo J, Cai S, Guzik T, Jefferson A, Goh N, Rockett K, and Channon K. Tetrahydrobiopterin-dependent preservation of nitric oxide-mediated endothelial function in diabetes by targeted transgenic GTP cyclohydrolase I overexpression. J Clin Invest 112: 725-735, 2003.
3. Anderwald C, Muller G, Koca G, Furnsinn C, Waldhausl W, and Roden M. Short-term leptin-dependent inhibition of hepatic gluconeogenesis is mediated by insulin receptor substrate-2. Mol Endocrinol 16: 1612-1628, 2002.
4. Barzilai N and Rossetti L. Relationship between changes in body composition and insulin responsiveness in models of the aging rat. Am J Physiol Endocrinol Metab 269: E591-E597, 1995.
5. Beckman JA, Creager MA, and Libby P. Diabetes and atherosclerosis: epidemiology, pathophysiology, and management [see Comment]. JAMA 287: 2570-2581, 2002.
6. Berg AH, Combs TP, Du X, Brownlee M, and Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action [see Comment]. Nat Med 7: 947-953, 2001.
7. Buettner R, Newgard CB, Rhodes CJ, and O'Doherty RM. Correction of diet-induced hyperglycemia, hyperinsulinemia, and skeletal muscle insulin resistance by moderate hyperleptinemia. Am J Physiol Endocrinol Metab 278: E563-E569, 2000.
8. Carini M, Aldini G, Stefani R, Orioli M, and Facino RM. Nitrosylhemoglobin, an unequivocal index of nitric oxide release from nitroaspirin: in vitro and in vivo studies in the rat by ESR spectroscopy. J Pharm Biomed Anal 26: 509-518, 2001.
9. Ceddia RB, William WN, Lima FB, Flandin P, Curi R, and Giacobino JP. Leptin stimulates uncoupling protein-2 mRNA expression and Krebs cycle activity and inhibits lipid synthesis in isolated rat white adipocytes. Eur J Biochem 267: 5952-5958, 2000.
10. Chen H, Montagnani M, Funahashi T, Shimomura I, and Quon MJ. Adiponectin stimulates production of nitric oxide in vascular endothelial cells. J Biol Chem 278: 45021-45026, 2003.
11. Combs TP, Berg AH, Obici S, Scherer PE, and Rossetti L. Endogenous glucose production is inhibited by the adipose-derived protein Acrp30. J Clin Invest 108: 1875-1881, 2001.
12. Correia ML and Haynes WG. Obesity-related hypertension: is there a role for selective leptin resistance? Curr Hypertens Rep 6: 230-235, 2004.
13. Creager MA, Luscher TF, Cosentino F, and Beckman JA. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Circulation 108: 1527-1532, 2003.
14. Du X, Matsumura T, Edelstein D, Rossetti L, Zsengeller Z, Szabo C, and Brownlee M. Inhibition of GAPDH activity by poly(ADP-ribose) polymerase activates three major pathways of hyperglycemic damage in endothelial cells [see Comment]. J Clin Invest 112: 1049-1057, 2003.
15. Esposito K, Giugliano D, Nappo F, Marfella R, and Campanian Postprandial Hyperglycemia Study Group. Regression of carotid atherosclerosis by control of postprandial hyperglycemia in type 2 diabetes mellitus. Circulation 110: 214-219, 2004.
16. Fruhbeck G. Pivotal role of nitric oxide in the control of blood pressure after leptin administration. Diabetes 48: 903-908, 1999.
17. Gaede P, Vedel P, Larsen N, Jensen GVH, Parving HH, and Pedersen O. Multifactorial intervention and cardiovascular disease in patients with type 2 diabetes. N Engl J Med 348: 383-393, 2003.
18. Group RotDCaCTR. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329: 977-986, 1993.
19. Guzik TJ, Mussa S, Gastaldi D, Sadowski J, Ratnatunga C, Pillai R, and Channon KM. Mechanisms of increased vascular superoxide production in human diabetes mellitus: role of NAD(P)H oxidase and endothelial nitric oxide synthase. Circulation 105: 1656-1662, 2002.
20. Hackett N, El Sawy T, Lee L, Silva I, O'Leary J, Rosengart T, and Crystal R. Use of quantitative TaqMan real-time PCR to track the time-dependent distribution of gene transfer vectors in vivo. Mol Ther 2: 649-656, 2000.
21. Hammes HP, Du X, Edelstein D, Taguchi T, Matsumura T, Ju Q, Lin J, Bierhaus A, Nawroth P, Hannak D, Neumaier M, Bergfeld R, Giardino I, and Brownlee M. Benfotiamine blocks three major pathways of hyperglycemic damage and prevents experimental diabetic retinopathy. Nat Med 9: 294-299, 2003.
22. Hanefeld M, Fischer S, Julius U, Schulze J, Schwanebeck U, Schmechel H, Ziegelasch HJ, and Lindner J. Risk factors for myocardial infarction and death in newly detected NIDDM: the Diabetes Intervention Study, 11-year follow-up. Diabetologia 39: 1577-1583, 1996.
23. Harris M, Flegal K, Cowie C, and Eberhardt M. Glycemic control of adults with diagnosed diabetes in the US (Abstract). Diabetes 45, Suppl 2: 122A, 1996.
24. Herz J and Gerard RD. Adenovirus-mediated transfer of low density lipoprotein receptor gene acutely accelerates cholesterol clearance in normal mice. Proc Natl Acad Sci USA 90: 2812-2816, 1993.
25. Hink U, Li H, Mollnau H, Oelze M, Matheis E, Hartmann M, Skatchkov M, Thaiss F, Stahl RAK, Warnholtz A, Meinertz T, Griendling K, Harrison DG, Forstermann U, and Munzel T. Mechanisms underlying endothelial dysfunction in diabetes mellitus. Circ Res 88: 14e-22, 2001.
26. Hsueh WA, Lyon CJ, and Quinones MJ. Insulin resistance and the endothelium. Am J Med 117: 109-117, 2004.
27. Iossa S, Mollica MP, Lionetti L, Crescenzo R, Tasso R, and Liverini G. A possible link between skeletal muscle mitochondrial efficiency and age-induced insulin resistance. Diabetes 53: 2861-2866, 2004.
28. Irat AM, Aktan F, and Ozansoy G. Effects of L-carnitine treatment on oxidant/antioxidant state and vascular reactivity of streptozotocin-diabetic rat aorta. J Pharm Pharmacol 55: 1389-1395, 2003.
29. Kass-Eisler A, Falck-Pedersen EF, Elfenbein DH, Alvira M, Buttrick PM, and Leinwand LA. The impact of developmental stage, route of administration and the immune system on adenovirus-mediated gene transfer. Gene Ther 1: 395-402, 1994.
30. Kawashima S and Yokoyama M. Dysfunction of endothelial nitric oxide synthase and atherosclerosis. Arterioscler Thromb Vasc Biol 24: 998-1005, 2004.
31. Kimura K, Tsuda K, Baba A, Kawabe T, Boh-oka Si Ibata M, Moriwaki C, Hano T, and Nishio I. Involvement of nitric oxide in endothelium-dependent arterial relaxation by leptin. Biochem Biophys Res Commun 273: 745-749, 2000.
32. Kobayashi T and Kamata K. Effect of chronic insulin treatment on NO production and endothelium-dependent relaxation in aortae from established STZ-induced diabetic rats. Atherosclerosis 155: 313-321, 2000.
33. Lam NT, Lewis JT, Cheung AT, Luk CT, Tse J, Wang J, Bryer-Ash M, Kolls JK, and Kieffer TJ. Leptin increases hepatic insulin sensitivity and protein tyrosine phosphatase 1B expression. Mol Endocrinol 18: 1333-1345, 2004.
34. Landmesser U, Dikalov S, Price SR, McCann L, Fukai T, Holland SM, Mitch WE, and Harrison DG. Oxidation of tetrahydrobiopterin leads to uncoupling of endothelial cell nitric oxide synthase in hypertension. J Clin Invest 111: 1201-1209, 2003.
35. Lee HC, Kim JJ, Kim Ks Shin HC, and Yoon JW. Remission in models of type 1 diabetes by gene therapy using a single-chain insulin analogue. Nature 408: 483-488, 2000.
36. Lee HJ, Choi SS, Park MK, An YJ, Seo SY, Kim MC, Hong SH, Hwang TH, Kang DY, Garber AJ, and Kim DK. Fenofibrate lowers abdominal and skeletal adiposity and improves insulin sensitivity in OLETF rats*1. Biochem Biophys Res Commun 296: 293-299, 2002.
37. Lefebvre PJ. Glucagon and its family revisited. Diabetes Care 18: 715-730, 1995.
38. Lembo G, Vecchione C, Fratta L, Marino G, Trimarco V, d'Amati G, and Trimarco B. Leptin induces direct vasodilation through distinct endothelial mechanisms. Diabetes 49: 293-297, 2000.
39. Luiken JJFP, Arumugam Y, Bell RC, Calles-Escandon J, Tandon NN, Glatz JFC, and Bonen A. Changes in fatty acid transport and transporters are related to the severity of insulin deficiency. Am J Physiol Endocrinol Metab 283: E612-E621, 2002.
40. Lundman P, Tornvall P, Nilsson L, and Pernow J. A triglyceride-rich fat emulsion and free fatty acids but not very low density lipoproteins impair endothelium-dependent vasorelaxation. Atherosclerosis 159: 35-41, 2001.
41. Luscher TF, Creager MA, Beckman JA, and Cosentino F. Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part II. Circulation 108: 1655-1661, 2003.
42. Matthews D, Hosker J, Rudenski A, Naylor B, Treacher D, and Turner R. Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28: 412-419, 1985.
43. McKeating J. Neutralization of virus. In: Practical Molecular Virology, edited by Collins MKL. Clifton, NJ: Humana, 1991, p. 89-93.
44. Menger MD, Vajkoczy P, Beger C, and Messmer K. Orientation of microvascular blood flow in pancreatic islet isografts. J Clin Invest 93: 2280-2285, 1994.
45. Minokoshi Y, Kim YB, Peroni OD, Fryer LG, Muller C, Carling D, and Kahn BB. Leptin stimulates fatty-acid oxidation by activating AMP-activated protein kinase [see Comment]. Nature 415: 339-343, 2002.
46. Murray MD and Kroenke K. Polypharmacy and medication adherence: small steps on a long road. J Gen Intern Med 16: 137-139, 2001.
47. NIDDK. National Diabetes Statistics Fact Sheet: General Information and National Estimates on Diabetes in the United States, 2003 (revised ed.). Bethesda, MD: US DHHS, NIH, 2004.
48. Olson D, Paveglio S, Huey P, Porter M, and Thule P. Glucose responsive hepatic insulin gene therapy of spontaneously diabetic BB/Wor rats. Hum Gene Ther 14: 1401-1413, 2003.
49. Orci L, Cook WS, Ravazzola M, Wang My Park BH, Montesano R, and Unger RH. Rapid transformation of white adipocytes into fat-oxidizing machines. Proc Natl Acad Sci USA 101: 2058-2063, 2004.
50. Ouchi N, Kobayashi H, Kihara S, Kumada M, Sato K, Inoue T, Funahashi T, and Walsh K. Adiponectin stimulates angiogenesis by promoting cross-talk between AMP-activated protein kinase and Akt signaling in endothelial cells. J Biol Chem 279: 1304-1309, 2004.
51. Peelman F, Waelput W, Iserentant H, Lavens D, Eyckerman S, Zabeau L, and Tavernier J. Leptin: linking adipocyte metabolism with cardiovascular and autoimmune diseases. Prog Lipid Res 43: 283-301, 2004.
52. Perez C, Fernandez-Galaz C, Fernandez-Agullo T, Arribas C, Andres A, Ros M, and Carrascosa JM. Leptin impairs insulin signaling in rat adipocytes. Diabetes 53: 347-353, 2004.
53. Perticone F, Ceravolo R, Pujia A, Ventura G, Iacopino S, Scozzafava A, Ferraro A, Chello M, Mastroroberto P, Verdecchia P, and Schillaci G. Prognostic significance of endothelial dysfunction in hypertensive patients. Circulation 104: 191-196, 2001.
54. Saydah SH, Fradkin J, and Cowie CC. Poor control of risk factors for vascular disease among adults with previously diagnosed diabetes. JAMA 291: 335-342, 2004.
55. Shinozaki K, Kashiwagi A, Nishio Y, Okamura T, Yoshida Y, Masada M, Toda N, and Kikkawa R. Abnormal biopterin metabolism is a major cause of impaired endothelium-dependent relaxation through nitric oxide/O2-imbalance in insulin-resistant rat aorta. Diabetes 48: 2437-2445, 1999.
56. Shiuchi T, Nakagami H, Iwai M, Takeda Y, Cui T, Chen R, Minokoshi Y, and Horiuchi M. Involvement of bradykinin and nitric oxide in leptin-mediated glucose uptake in skeletal muscle. Endocrinology 142: 608-612, 2001.
57. Son SM, Whalin MK, Harrison DG, Taylor WR, and Griendling KK. Oxidative stress and diabetic vascular complications. Curr Diabetes Rep 4: 247-252, 2004.
58. Steinberg HO and Baron AD. Vascular function, insulin resistance and fatty acids [see Comment]. Diabetologia 45: 623-634, 2002.
59. Stuehr D, Pou S, and Rosen GM. Oxygen reduction by nitric-oxide synthases. J Biol Chem 276: 14533-14536, 2001.
60. Sutliff RL, Dikalov S, Weiss D, Parker J, Raidel S, Racine AK, Russ R, Haase CP, Taylor WR, and Lewis W. Nucleoside reverse transcriptase inhibitors impair endothelium-dependent relaxation by increasing superoxide. Am J Physiol Heart Circ Physiol 283: H2363-H2370, 2002.
61. Thule PM, Liu J, and Phillips LS. Glucose regulated production of human insulin in rat hepatocytes. Gene Ther 7: 205-214, 2000.
62. Thule PM and Liu JM. Regulated hepatic insulin gene therapy of STZ-diabetic rats. Gene Ther 7: 1744-1752, 2000.
63. Tomas E, Tsao TS, Saha AK, Murrey HE, Zhang Cc Itani SI, Lodish HF, and Ruderman NB. Enhanced muscle fat oxidation and glucose transport by ACRP30 globular domain: acetyl-CoA carboxylase inhibition and AMP-activated protein kinase activation. Proc Natl Acad Sci USA 99: 16309-16313, 2002.
64. Tripathy D, Mohanty P, Dhindsa S, Syed T, Ghanim H, Aljada A, and Dandona P. Elevation of free fatty acids induces inflammation and impairs vascular reactivity in healthy subjects. Diabetes 52: 2882-2887, 2003.
65. Vecchione C, Aretini A, Maffei A, Marino G, Selvetella G, Poulet R, Trimarco V, Frati G, and Lembo G. Cooperation between insulin and leptin in the modulation of vascular tone. Hypertension 42: 166-170, 2003.
66. Vik SA, Maxwell CJ, and Hogan DB. Measurement, correlates, and health outcomes of medication adherence among seniors. Ann Pharmacother 38: 303-312, 2004.
67. Wallace T, Levy J, and Matthews D. Use and abuse of HOMA modeling. Diabetes Care 27: 1487-1495, 2004.
68. Wang CCL, Goalstone ML, and Draznin B. Molecular mechanisms of insulin resistance that impact cardiovascular biology. Diabetes 53: 2735-2740, 2004.
69. Wever RM, van Dam T, van Rijn HJ, de Groot F, and Rabelink TJ. Tetrahydrobiopterin regulates superoxide and nitric oxide generation by recombinant endothelial nitric oxide synthase. Biochem Biophys Res Commun 237: 340-344, 1997.
70. Wu X, Motoshima H, Mahadev K, Stalker TJ, Scalia R, and Goldstein BJ. Involvement of AMP-activated protein kinase in glucose uptake stimulated by the globular domain of adiponectin in primary rat adipocytes. Diabetes 52: 1355-1363, 2003.
71. Yamagishi Si Edelstein D, Du Xl Kaneda Y, Guzman M, and Brownlee M. Leptin induces mitochondrial superoxide production and monocyte chemoattractant protein-1 expression in aortic endothelial cells by increasing fatty acid oxidation via protein kinase A. J Biol Chem 276: 25096-25100, 2001.
72. Yamauchi T, Kamon J, Waki H, Imai Y, Shimozawa N, Hioki K, Uchida S, Ito Y, Takakuwa K, Matsui J, Takata M, Eto K, Terauchi Y, Komeda K, Tsunoda M, Murakami K, Ohnishi Y, Naitoh T, Yamamura K, Ueyama Y, Froguel P, Kimura S, Nagai R, and Kadowaki T. Globular adiponectin protected ob/ob mice from diabetes and ApoE-deficient mice from atherosclerosis. J Biol Chem 278: 2461-2468, 2003.
73. Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, and Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity [see Comment]. Nat Med 7: 941-946, 2001.
74. Yamaza H, Komatsu T, Chiba T, Toyama H, To K, Higami Y, and Shimokawa I. A transgenic dwarf rat model as a tool for the study of calorie restriction and aging. Exp Gerontol 39: 269-272, 2004.
75. Zar J. Biostatistical Analysis. Englewood Cliffs, NJ: Prentice-Hall, 1984.