Meal-related increases in microvascular vasomotion are impaired in obese individuals: A potential mechanism in the pathogenesis of obesity-related insulin resistance

Diabetes Care

Volumn 34, Issue SUPPL. 2, 2011, Pages

  Jonk, Amy M ^a   Houben, Alfons J ^a   Schaper, Nicolaas C ^a   De Leeuw, Peter W ^a   Serné, Erik H ^b   Smulders, Yvo M ^b   Stehouwer, Coen D ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; ENDOTHELIN 1; GLUCOSE; INSULIN; NITRIC OXIDE;

ADULT; BODY WEIGHT; CAPILLARY PERMEABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; DISEASE ASSOCIATION; DRINKING; DYNAMICS; ENERGY; FEMALE; GLUCOSE TRANSPORT; HOMEOSTASIS; HUMAN; HYPERINSULINEMIA; HYPERTENSION; INSULIN BLOOD LEVEL; INSULIN DEFICIENCY; INSULIN RESISTANCE; INSULIN SENSITIVITY; LEAN BODY WEIGHT; MALE; MEAL; MICROANGIOPATHY; MICROCIRCULATION; OBESITY; PATHOGENESIS; REVIEW; STEADY STATE; VASODILATATION; WAIST HIP RATIO; ARTICLE; BLOOD; CLINICAL TRIAL; CONTROLLED CLINICAL TRIAL; DRUG EFFECT; GLUCOSE BLOOD LEVEL; LASER DOPPLER FLOWMETRY; MICROVASCULATURE; PATHOPHYSIOLOGY; PHYSIOLOGY; RANDOMIZED CONTROLLED TRIAL;

BLOOD GLUCOSE; FEMALE; GLUCOSE; HUMANS; INSULIN; INSULIN RESISTANCE; LASER-DOPPLER FLOWMETRY; MALE; MICROVESSELS; OBESITY;

EID: 79959803809     PISSN: 01495992     EISSN: 19355548     Source Type: Journal    
DOI: 10.2337/dc11-s240     Document Type: Review

References (61)

1. Hajer GR, van Haeften TW, Visseren FL. Adipose tissue dysfunction in obesity, diabetes, and vascular diseases. Eur Heart J 2008;29:2959-2971
2. Jonk AM, Houben AJ, de Jongh RT, SernéEH, Schaper NC, Stehouwer CD. Microvascular dysfunction in obesity: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Physiology (Bethesda) 2007; 22:252-260
3. Serné EH, de Jongh RT, Eringa EC, IJzerman RG, Stehouwer CD. Microvascular dysfunction: a potential pathophysiological role in the metabolic syndrome. Hypertension 2007;50:204-211 (Pubitemid 46986042)
4. Levy BI, Ambrosio G, Pries AR, Struijker- Boudier HA. Microcirculation in hypertension: a newtarget for treatment? Circulation 2001;104:735-740
5. Clark MG. Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am J Physiol Endocrinol Metab 2008;295:E732-E750
6. Clark MG, Wallis MG, Barrett EJ, et al. Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab 2003;284:E241-E258 (Pubitemid 36120096)
7. Rattigan S, Clark MG, Barrett EJ. Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 1997;46:1381-1388 (Pubitemid 27369072)
8. Baron AD. Hemodynamic actions of insulin. Am J Physiol 1994;267:E187-E202
9. Yki-Järvinen H, Utriainen T. Insulininduced vasodilatation: physiology or pharmacology? Diabetologia 1998;41: 369-379
10. Clerk LH, Rattigan S, Clark MG. Lipid infusion impairs physiologic insulin-mediated capillary recruitment and muscle glucose uptake in vivo. Diabetes 2002;51:1138-1145 (Pubitemid 34438361)
11. Youd JM, Rattigan S, Clark MG. Acute impairment of insulin-mediated capillary recruitment and glucose uptake in rat skeletal muscle in vivo by TNF-alpha. Diabetes 2000;49:1904-1909
12. de Jongh RT, Serné EH, IJzerman RG, de Vries G, Stehouwer CD. Free fatty acid levels modulate microvascular function: relevance for obesity-associated insulin resistance, hypertension, andmicroangiopathy. Diabetes 2004;53:2873-2882 (Pubitemid 39425913)
13. Liu Z, Liu J, Jahn LA, Fowler DE, Barrett EJ. Infusing lipid raises plasma free fatty acids and induces insulin resistance in muscle microvasculature. J Clin Endocrinol Metab 2009;94:3543-3549
14. Newman JM, Dwyer RM, St-Pierre P, Richards SM, Clark MG, Rattigan S. Decreased microvascular vasomotion and myogenic response in rat skeletal muscle in association with acute insulin resistance. J Physiol 2009;587:2579-2588
15. Cardillo C, Nambi SS, Kilcoyne CM, et al. Insulin stimulates both endothelin and nitric oxide activity in the human forearm. Circulation 1999;100:820-825 (Pubitemid 29398879)
16. Eringa EC, Stehouwer CD, Merlijn T, Westerhof N, Sipkema P. Physiological concentrations of insulin induce endothelinmediated vasoconstriction during inhibition of NOS or PI3-kinase in skeletal muscle arterioles. Cardiovasc Res 2002;56:464-471 (Pubitemid 35351568)
17. Clark MG, Rattigan S, Barrett EJ, Vincent MA. Point: There is capillary recruitment in active skeletal muscle during exercise. J Appl Physiol 2008;104:889-891
18. Barlow TE, Haigh AL, Walder DN. Evidence for two vascular pathways in skeletal muscle. Clin Sci 1961;20:367-385
19. Eringa EC, Stehouwer CD, van Nieuw Amerongen GP, Ouwehand L, Westerhof N, Sipkema P. Vasoconstrictor effects of insulin in skeletal muscle arterioles are mediated by ERK1/2 activation in endothelium. Am J Physiol Heart Circ Physiol 2004;287:H2043-H2048 (Pubitemid 39430742)
20. Ursino M, Cavalcanti S, Bertuglia S, Colantuoni A. Theoretical analysis of complex oscillations in multibranched microvascular networks. Microvasc Res 1996;51: 229-249 (Pubitemid 26108051)
21. Meyer C, de Vries G, Davidge ST, Mayes DC. Reassessing the mathematical modeling of the contribution of vasomotion to vascular resistance. J Appl Physiol 2002; 92:888-889 (Pubitemid 34671062)
22. de Jongh RT, Clark AD, IJzerman RG, Serné EH, de Vries G, Stehouwer CD. Physiological hyperinsulinaemia increases intramuscular microvascular reactive hyperaemia and vasomotion in healthy volunteers. Diabetologia 2004;47:978-986 (Pubitemid 38918156)
23. Rossi M, Maurizio S, Carpi A. Skin blood flowmotion response to insulin iontophoresis in normal subjects. Microvasc Res 2005;70:17-22 (Pubitemid 41565405)
24. Gavin TP, Stallings HW 3rd, Zwetsloot KA, et al. Lower capillary density but no difference in VEGF expression in obese vs. lean young skeletal muscle in humans. J Appl Physiol 2005;98:315-321 (Pubitemid 40041262)
25. CardilloC,CampiaU, IantornoM, Panza JA. Enhanced vascular activity of endogenous endothelin-1 in obese hypertensive patients. Hypertension 2004;43:36-40 (Pubitemid 38031908)
26. 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 1996;97:2601-2610
27. de Jongh RT, Serné EH, IJzerman RG, Jørstad HT, Stehouwer CD. Impaired local microvascular vasodilatory effects of insulin and reduced skin microvascular vasomotion in obese women. Microvasc Res 2008;75:256-262 (Pubitemid 351240937)
28. de Jongh RT, Serné EH, IJzerman RG, de Vries G, Stehouwer CD. Impaired microvascular function in obesity: implications for obesity-associated microangiopathy, hypertension, and insulin resistance. Circulation 2004;109:2529-2535 (Pubitemid 38720552)
29. Arcaro G, Zamboni M, Rossi L, et al. Body fat distribution predicts the degree of endothelial dysfunction in uncomplicated obesity. Int JObes RelatMetabDisord 1999; 23:936-942 (Pubitemid 29423936)
30. Clerk LH, Vincent MA, Jahn LA, Liu Z, Lindner JR, Barrett EJ. Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 2006;55:1436-1442 (Pubitemid 44195384)
31. Caballero AE. Endothelial dysfunction, inflammation, and insulin resistance: a focus on subjects at risk for type 2 diabetes. Curr Diab Rep 2004;4:237-246 (Pubitemid 39173548)
32. Ziccardi P, Nappo F, Giugliano G, et al. Reduction of inflammatory cytokine concentrations and improvement of endothelial functions in obese women after weight loss over one year. Circulation 2002;105: 804-809 (Pubitemid 34174919)
33. Kim F, PhamM, Maloney E, et al. Vascular inflammation, insulin resistance, and reduced nitric oxide production precede the onset of peripheral insulin resistance. Arterioscler Thromb Vasc Biol 2008;28: 1982-1988
34. Lesniewski LA, Donato AJ, Behnke BJ, et al. Decreased NO signaling leads to enhanced vasoconstrictor responsiveness in skeletal muscle arterioles of the ZDF rat prior to overt diabetes and hypertension. Am J Physiol Heart Circ Physiol 2008; 294:H1840-H1850 (Pubitemid 351490614)
35. Inyard AC, Chong DG, Klibanov AL, Barrett EJ. Muscle contraction, but not insulin, increases microvascular blood volume in the presence of free fatty acidinduced insulin resistance. Diabetes 2009; 58:2457-2463
36. Wallace TM, Levy JC, Matthews DR. Use and abuse of HOMA modeling. Diabetes Care 2004;27:1487-1495 (Pubitemid 38680001)
37. Shimabukuro M, Chinen I, Higa N, Takasu N, Yamakawa K, Ueda S. Effects of dietary composition on postprandial endothelial function and adiponectin concentrations in healthy humans: a crossover controlled study. Am J Clin Nutr 2007;86: 923-928 (Pubitemid 47538291)
38. Holowatz LA, Thompson-Torgerson CS, Kenney WL. The human cutaneous circulation as a model of generalized microvascular function. J Appl Physiol 2008;105: 370-372
39. Lang CH. Rates and tissue sites of noninsulinand insulin-mediated glucose uptake in diabetic rats. Proc Soc Exp BiolMed 1992;199: 81-87
40. Serné EH, Gans RO, ter Maaten JC, ter Wee PM, Donker AJ, Stehouwer CD. Capillary recruitment is impaired in essential hypertension and relates to insulin's metabolic and vascular actions. Cardiovasc Res 2001;49:161-168
41. Steinberg HO, Paradisi G, Hook G, Crowder K, Cronin J, Baron AD. Free fatty acid elevation impairs insulin-mediated vasodilation and nitric oxide production. Diabetes 2000;49:1231-1238 (Pubitemid 30439100)
42. Tripathy D, Mohanty P, Dhindsa S, et al. Elevation of free fatty acids induces inflammation and impairs vascular reactivity in healthy subjects. Diabetes 2003;52: 2882-2887 (Pubitemid 37466856)
43. Zhang L, Wheatley CM, Richards SM, Barrett EJ, Clark MG, Rattigan S. TNFalpha acutely inhibits vascular effects of physiological but not high insulin or contraction. Am J Physiol Endocrinol Metab 2003;285:E654-E660 (Pubitemid 37010846)
44. IJzerman RG, Voordouw JJ, Van Weissenbruch MM, et al. TNF-alpha levels are associated with skin capillary recruitment in humans: a potential explanation for the relationship between TNFalpha and insulin resistance. Clin Sci (Lond) 2006;110:361-368 (Pubitemid 43341639)
45. Kim F, Tysseling KA, Rice J, et al. Free fatty acid impairment of nitric oxide production in endothelial cells is mediated by IKKbeta. Arterioscler Thromb Vasc Biol 2005;25:989-994 (Pubitemid 40627844)
46. Plomgaard P, Bouzakri K, Krogh-Madsen R, Mittendorfer B, Zierath JR, Pedersen BK. Tumor necrosis factor-alpha induces skeletal muscle insulin resistance in healthy human subjects via inhibition of Akt substrate 160 phosphorylation. Diabetes 2005; 54:2939-2945 (Pubitemid 41401090)
47. Wang XL, Zhang L, YoukerK, et al. Free fatty acids inhibit insulin signaling-stimulated endothelial nitric oxide synthase activation through upregulating PTEN or inhibiting Akt kinase. Diabetes 2006;55:2301-2310 (Pubitemid 44743628)
48. Ogihara T, Asano T, Katagiri H, et al. Oxidative stress induces insulin resistance by activating the nuclear factor-kappa B pathway and disrupting normal subcellular distribution of phosphatidylinositol 3-kinase. Diabetologia 2004;47:794-805 (Pubitemid 38756991)
49. Eringa E.C. Stehouwer C.D.A. Walburg K. Clark A.D. Van Nieuw A. G.P.
50. Eringa EC, Stehouwer CD, Walburg K, et al. Physiological concentrations of insulin induce endothelin-dependent vasoconstriction of skeletal muscle resistance arteries in the presence of tumor necrosis factor-alpha dependence on c-Jun N-terminal kinase. Arterioscler Thromb Vasc Biol 2006;26:274-280 (Pubitemid 43732187)
51. Mohamed F, Monge JC, Gordon A, Cernacek P, Blais D, Stewart DJ. Lack of role for nitric oxide (NO) in the selective destabilization of endothelial NO synthase mRNA by tumor necrosis factoralpha. Arterioscler Thromb Vasc Biol 1995; 15:52-57
52. Bourgoin F, Bachelard H, Badeau M, et al. Endothelial and vascular dysfunctions and insulin resistance in rats fed a high-fat, high-sucrose diet. Am J Physiol Heart Circ Physiol 2008;295:H1044-H1055
53. Yan G, You B, Chen SP, Liao JK, Sun J. Tumor necrosis factor-alpha downregulates endothelial nitric oxide synthase mRNA stability via translation elongation factor 1-alpha 1. Circ Res 2008;103:591-597
54. Yudkin JS, Eringa E, Stehouwer CD. "Vasocrine" signalling from perivascular fat: amechanismlinking insulin resistance to vascular disease. Lancet 2005;365:1817-1820 (Pubitemid 40744663)
55. Eringa EC, Bakker W, Smulders YM, Serné EH, Yudkin JS, Stehouwer CD. Regulation of vascular function and insulin sensitivity by adipose tissue: focus on perivascular adipose tissue. Microcirculation 2007;14:389-402 (Pubitemid 47050030)
56. Sarzani R, Salvi F, Dessì-Fulgheri P, Rappelli A. Renin-angiotensin system, natriuretic peptides, obesity, metabolic syndrome, and hypertension: an integrated view in humans. J Hypertens 2008;26: 831-843 (Pubitemid 351540757)
57. Velloso LA, Folli F, Sun XJ, White MF, Saad MJ, Kahn CR. Cross-talk between the insulin and angiotensin signaling systems. Proc Natl Acad Sci U S A 1996;93:12490-12495 (Pubitemid 26367171)
58. Wei Y, Sowers JR, Nistala R, et al. Angiotensin II-induced NADPH oxidase activation impairs insulin signaling in skeletal muscle cells. J BiolChem2006;281:35137-35146 (Pubitemid 46036553)
59. Clerk LH, Vincent MA, Barrett EJ, Lankford MF, Lindner JR. Skeletal muscle capillary responses to insulin are abnormal in late-stage diabetes and are restored by angiotensin-converting enzyme inhibition. Am J Physiol Endocrinol Metab 2007;293: E1804-E1809 (Pubitemid 350255135)
60. Harte AL, McTernan PG, McTernan CL, et al. Insulin increases angiotensinogen expression in human abdominal subcutaneous adipocytes. Diabetes Obes Metab 2003;5: 462-467 (Pubitemid 37483609)
61. Goossens GH, Jocken JW, Blaak EE, Schiffers PM, Saris WH, van Baak MA. Endocrine role of the renin-angiotensin system in human adipose tissue and muscle: effect of beta-adrenergic stimulation. Hypertension 2007;49:542-547