Dissociation between metabolic and vascular insulin resistance in aging

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 293, Issue 1, 2007, Pages

  Schulman, Ivonne Hernandez ^b   Zhou, Ming Sheng ^b   Jaimes, Edgar A ^b   Raij, Leopoldo ^a  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b NONE

Author keywords

Cell signaling; Endothelium; Metabolic syndrome; Nitric oxide

Indexed keywords

ACETYLCHOLINE; CAVEOLIN 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; INSULIN; INSULIN RECEPTOR SUBSTRATE 1; N(G) NITROARGININE METHYL ESTER; NITROPRUSSIDE SODIUM; PROTEIN KINASE (CALCIUM,CALMODULIN); PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; REGULATOR PROTEIN; SERINE; STRESS ACTIVATED PROTEIN KINASE 1;

AGING; ANIMAL MODEL; ANIMAL TISSUE; AORTA; ARTICLE; BLOOD VESSEL INJURY; CARDIOVASCULAR RISK; CARDIOVASCULAR SYSTEM; CONTROLLED STUDY; DISEASE PREDISPOSITION; ENZYME ACTIVITY; GLUCOSE BLOOD LEVEL; HYPERINSULINEMIA; INSULIN RESISTANCE; MALE; METABOLISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; STATISTICAL SIGNIFICANCE; SYSTOLIC BLOOD PRESSURE; VASCULAR ENDOTHELIUM; VASODILATATION;

AGING; ANIMALS; AORTA; ENDOTHELIUM, VASCULAR; INSULIN; INSULIN RESISTANCE; MALE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 34547093669     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00138.2007     Document Type: Article

References (50)

1. Aguirre V, Uchida T, Yenush L, Davis R, White MF. The c-Jun NH2-terminal kinase promotes insulin resistance during association with insulin receptor substrate-1 and phosphorylation of Ser307. J Biol Chem 275: 9047-9054, 2000.
2. Andreozzi F, Laratta E, Sciacqua A, Perticone F, Sesti G. Angiotensin II impairs the insulin signaling pathway promoting production of nitric oxide by inducing phosphorylation of insulin receptor substrate-1 on Ser312 and Ser616 in human umbilical vein endothelial cells. Circ Res 94: 1211-1218, 2004.
3. Baron AD. Insulin and the vasculature-old actors, new roles. J Investig Med 44: 406-412, 1996.
4. Burritt JB, Quinn MT, Jutila MA, Bond CW, Jesaitis AJ. Topological mapping of neutrophil cytochrome b epitopes with phage-display libraries. J Biol Chem 270: 16974-16980, 1995.
5. Caglayan E, Blaschke F, Takata Y, Hsueh WA. Metabolic syndrome-interdependence of the cardiovascular and metabolic pathways. Curr Opin Pharmacol 5: 135-142, 2005.
6. Cohen AW, Combs TP, Scherer PE, Lisanti MP. Role of caveolin and caveolae in insulin signaling and diabetes. Am J Physiol Endocrinol Metab 285: E1151-E1160, 2003.
7. Cosentino F, Barker JE, Brand MP, Heales SJ, Werner ER, Tippins JR, West N, Channon KM, Volpe M, Luscher TF. Reactive oxygen species mediate endothelium-dependent relaxations in tetrahydrobiopterin-deficient mice. Arterioscler Thromb Vasc Biol 21: 496-502, 2001.
8. Cusi K, Maezono K, Osman A, Pendergrass M, Patti ME, Pratipanawatr T, DeFronzo RA, Kahn CR, Mandarino LJ. Insulin resistance differentially affects the PI 3-kinase- and MAP kinase-mediated signaling in human muscle. J Clin Invest 105: 311-320, 2000.
9. D'Angelo G, Elmarakby AA, Pollock DM, Stepp DW. Fructose feeding increases insulin resistance but not blood pressure in Sprague-Dawley rats. Hypertension 46: 806-811, 2005.
10. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399: 601-605, 1999.
11. Duerrschmidt N, Stielow C, Muller G, Pagano PJ, Morawietz H. NO-mediated regulation of NAD(P)H oxidase by laminar shear stress in human endothelial cells. J Physiol 576: 557-567, 2006.
12. Egashira K. Molecular mechanisms mediating inflammation in vascular disease: special reference to monocyte chemoattractant protein-1. Hypertension 41: 834-841, 2003.
13. Ford ES, Giles WH, Mokdad AH. Increasing prevalence of the metabolic syndrome among U.S. adults. Diabetes Care 27: 2444-2449, 2004.
14. Fornoni A, Raij L. Metabolic syndrome and endothelial dysfunction. Curr Hypertens Rep 7: 88-95, 2005.
15. Gorlach A, Brandes RP, Nguyen K, Amidi M, Dehghani F, Busse R. A gp91phox containing NADPH oxidase selectively expressed in endothelial cells is a major source of oxygen radical generation in the arterial wall. Circ Res 87: 26-32, 2000.
16. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 2: 275-281, 1998.
17. Hayakawa H, Raij L. The link among nitric oxide synthase activity, endothelial function, and aortic and ventricular hypertrophy in hypertension. Hypertension 29: 235-241, 1997.
18. Heymes C, Silvestre JS, Llorens-Cortes C, Chevalier B, Marotte F, Levy BI, Swynghedauw B, Samuel JL. Cardiac senescence is associated with enhanced expression of angiotensin II receptor subtypes. Endocrinology 139: 2579-2587, 1998.
19. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M, Hotamisligil GS. A central role for JNK in obesity and insulin resistance. Nature 420: 333-336, 2002.
20. Houstis N, Rosen ED, Lander ES. Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440: 944-948, 2006.
21. Huang PL, Huang ZH, Mashimo H, Bloch KD, Moskowitz MA, Bevan JA, Fishman MC. Hypertension in mice lacking the gene for endothelial nitric-oxide synthase. Nature 377: 239-242, 1995.
22. Jiang ZY, Lin YW, Clemont A, Feener EP, Hein KD, Igarashi M, Yamauchi T, White MF, King GL. Characterization of selective resistance to insulin signaling in the vasculature of obese Zucker (fa/fa) rats. J Clin Invest 104: 447-457, 1999.
23. Jones SA, O'Donnell VB, Wood JD, Broughton JP, Hughes EJ, Jones OT. Expression of phagocyte NADPH oxidase components in human endothelial cells. Am J Physiol Heart Circ Physiol 271: H1626-H1634, 1996.
24. Kamei N, Tobe K, Suzuki R, Ohsugi M, Watanabe T, Kubota N, Ohtsuka-Kowatari N, Kumagai K, Sakamoto K, Kobayashi M, Yamauchi T, Ueki K, Oishi Y, Nishimura S, Manabe I, Hashimoto H, Ohnishi Y, Ogata H, Tokuyama K, Tsunoda M, Ide T, Murakami K, Nagai R, Kadowaki T. Overexpression of monocyte chemoattractant protein-1 in adipose tissues causes macrophage recruitment and insulin resistance. J Biol Chem 281: 26602-26614, 2006.
25. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 113: 1888-1904, 2006.
26. Kobayashi T, Taguchi K, Yasuhiro T, Matsumoto T, Kamata K. Impairment of PI3-K/Akt pathway underlies attenuated endothelial function in aorta of type 2 diabetic mouse model. Hypertension 44: 956-962, 2004.
27. 2+ but requires phosphorylation by Akt at Ser(1179). J Biol Chem 276: 30392-30398, 2001.
28. Montagnani M, Golovchenko I, Kim I, Koh GY, Goalstone ML, Mundhekar AN, Johansen M, Kucik DF, Quon MJ, Draznin B. Inhibition of phosphatidylinositol 3-kinase enhances mitogenic actions of insulin in endothelial cells. J Biol Chem 277: 1794-1799, 2002.
29. Ohashi Y, Kawashima S, Hirata K, Yamashita T, Ishida T, Inoue N, Sakoda T, Kurihara H, Yazaki Y, Yokoyama M. Hypotension and reduced nitric oxide-elicited vasorelaxation in transgenic mice overexpressing endothelial nitric oxide synthase. J Clin Invest 102: 2061-2071, 1998.
30. Park JL, Loberg RD, Duquaine D, Zhang HY, Deo BK, Ardanaz N, Coyle J, Atkins KB, Schin M, Charron MJ, Kumagai AK, Pagano PJ, Brosius FC. GLUT4 facilitative glucose transporter specifically and differentially contributes to agonist-induced vascular reactivity in mouse aorta. Arterioscler Thromb Vasc Biol 25: 1596-1602, 2005.
31. Park YW, Zhu S, Palaniappan L, Heshka S, Carnethon MR, Heymsfield SB. The metabolic syndrome: prevalence and associated risk factor findings in the US population from the Third National Health and Nutrition Examination Survey, 1988-1994. Arch Intern Med 163: 427-436, 2003.
32. Rueckschloss U, Galle J, Holtz J, Zerkowski HR, Morawietz H. Induction of NAD(P)H oxidase by oxidized low-density lipoprotein in human endothelial cells: antioxidative potential of hydroxymethylglutaryl coenzyme A reductase inhibitor therapy. Circulation 104: 1767-1772, 2001.
33. Schiffrin EL. Vascular stiffening and arterial compliance. Implications for systolic blood pressure. Am J Hypertens 17: 39S-48S, 2004.
34. Schulman IH, Zhou MS, Raij L. Interaction between nitric oxide and angiotensin II in the endothelium: role in atherosclerosis and hypertension. J Hypertens Suppl 24: S45-S50, 2006.
35. Schutzer WE, Reed JF, Mader SL. Decline in caveolin-1 expression and scaffolding of G protein receptor kinase-2 with age in Fischer 344 aortic vascular smooth muscle. Am J Physiol Heart Circ Physiol 288: H2457-H2464, 2005.
36. Shepherd PR, Kahn BB. Mechanisms of disease. Glucose transporters and insulin action. Implications for insulin resistance and diabetes mellitus. N Engl J Med 341: 248-257, 1999.
37. Shinozaki K, Ayajiki K, Nishio Y, Sugaya T, Kashiwagi A, Okamura T. Evidence for a causal role of the renin-angiotensin system in vascular dysfunction associated with insulin resistance. Hypertension 43: 255-262, 2004.
38. Sorensen H, Winzell MS, Brand CL, Fosgerau K, Gelling RW, Nishimura E, Ahren B. Glucagon receptor knockout mice display increased insulin sensitivity and impaired β-cell function. Diabetes 55: 3463-3469, 2006.
39. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD. Insulinmediated skeletal-muscle vasodilation is nitric-oxide dependent-a novel action of insulin to increase nitric-oxide release. J Clin Invest 94: 1172-1179, 1994.
40. Steinberg HO, Chaker H, Leaming R, Johnson A, Brechtel G, Baron AD. Obesity/insulin resistance is associated with endothelial dysfunction. Implications for the syndrome of insulin resistance. J Clin Invest 97: 2601-2610, 1996.
41. Sugita M, Sugita H, Kaneki M. Increased insulin receptor substrate 1 serine phosphorylation and stress-activated protein kinase/c-Jun N-terminal kinase activation associated with vascular insulin resistance in spontaneously hypertensive rats. Hypertension 44: 484-489, 2004.
42. Taddei S, Virdis A, Ghiadoni L, Salvetti G, Bernini G, Magagna A, Salvetti A. Age-related reduction of NO availability and oxidative stress in humans. Hypertension 38: 274-279, 2001.
43. Taniyama Y, Hitomi H, Shah A, Alexander RW, Griendling KK. Mechanisms of reactive oxygen species-dependent downregulation of insulin receptor substrate-1 by angiotensin II. Arterioscler Thromb Vasc Biol 25: 1142-1147, 2005.
44. van der Loo B, Labugger R, Skepper JN, Bachschmid M, Kilo J, Powell JM, Palacios-Callender M, Erusalimsky JD, Quaschning T, Malinski T, Gygi D, Ullrich V, Luscher TF. Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med 192: 1731-1744, 2000.
45. Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 27: 567-574, 1996.
46. Yang AL, Su CT, Lin KL, Chao JI, You HP, Lee SD. Exercise training improves insulin-induced and insulin-like growth factor-1-induced vasorelaxation in rat aortas. Life Sci 79: 2017-2021, 2006.
47. Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, Lin MI, Drab M, Kurzchalia TV, Stan RV, Sessa WC. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Invest 116: 1284-1291, 2006.
48. Zeng GY, Nystrom FH, Ravichandran LV, Cong LN, Kirby M, Mostowski H, Quon MJ. Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation 101: 1539-1545, 2000.
49. Zhou MS, Adam AG, Jaimes EA, Raij L. In salt-sensitive hypertension, increased superoxide production is linked to functional upregulation of angiotensin II. Hypertension 42: 945-951, 2003.
50. Zhou MS, Schulman IH, Pagano PJ, Jaimes EA, Raij L. Reduced NAD(P)H oxidase in low renin hypertension. Link among angiotensin II, atherogenesis, and blood pressure. Hypertension 47: 81-86, 2006.