Insulin-induced changes in skeletal muscle microvascular perfusion are dependent upon perivascular adipose tissue in women

Diabetologia

Volumn 58, Issue 8, 2015, Pages 1907-1915

  Meijer, Rick I ^a   Serné, Erik H ^a   Korkmaz, H Ibrahim ^a   van der Peet, Donald L ^b   de Boer, Michiel P ^a   Niessen, Hans W M ^a   van Hinsbergh, Victor W M ^a   Yudkin, John S ^a,c   Smulders, Yvo M ^a   Eringa, Etto C ^a  

^a VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Insulin resistance; Microcirculation; Microvascular recruitment; Perivascular adipose tissue

Indexed keywords

INSULIN;

ADIPOCYTE; ADIPOSE TISSUE; ADULT; ARTICLE; CELL SIZING (MEASUREMENT); CLINICAL ARTICLE; CONTRAST ENHANCED ULTRASOUND; CONTROLLED STUDY; DISEASE ASSOCIATION; EX VIVO STUDY; FEMALE; HISTOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; HYPERINSULINEMIA; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; LEAN BODY WEIGHT; MICROVASCULATURE; MUSCLE BIOPSY; MUSCLE PERFUSION; OBESITY; PRIORITY JOURNAL; SKELETAL MUSCLE; ULTRASOUND; VASOCONSTRICTION; VASODILATATION; ADOLESCENT; DRUG EFFECTS; INSULIN RESISTANCE; MIDDLE AGED; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOPHYSIOLOGY; PHYSIOLOGY; VASCULARIZATION; YOUNG ADULT;

ADIPOSE TISSUE; ADOLESCENT; ADULT; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; INSULIN; INSULIN RESISTANCE; MICROVESSELS; MIDDLE AGED; MUSCLE, SKELETAL; OBESITY; YOUNG ADULT;

EID: 84937513178     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-015-3606-8     Document Type: Article

References (38)

1. Levy BI, Schiffrin EL, Mourad JJ et al (2008) Impaired tissue perfusion: a pathology common to hypertension, obesity, and diabetes mellitus. Circulation 118:968–976
2. Laine H, Knuuti MJ, Ruotsalainen U et al (1998) Preserved relative dispersion but blunted stimulation of mean flow, absolute dispersion, and blood volume by insulin in skeletal muscle of patients with essential hypertension. Circulation 97:2146–2153
3. de Boer MP, Meijer RI, Wijnstok NJ et al (2012) Microvascular dysfunction: a potential mechanism in the pathogenesis of obesity-associated insulin resistance and hypertension. Microcirculation 19:5–18
4. Barrett EJ, Eggleston EM, Inyard AC et al (2009) The vascular actions of insulin control its delivery to muscle and regulate the rate-limiting step in skeletal muscle insulin action. Diabetologia 52:752–764
5. Meijer RI, de Boer MP, Groen MR et al (2012) Insulin-induced microvascular recruitment in skin and muscle are related and both are associated with whole body glucose uptake. Microcirculation 19:494–500
6. Premilovac D, Bradley EA, Ng HL, Richards SM, Rattigan S, Keske MA (2013) Muscle insulin resistance resulting from impaired microvascular insulin sensitivity in Sprague Dawley rats. Cardiovasc Res 98:28–36
7. Clerk LH, Vincent MA, Jahn LA, Liu Z, Lindner JR, Barrett EJ (2006) Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 55:1436–1442
8. Keske MA, Clerk LH, Price WJ, Jahn LA, Barrett EJ (2009) Obesity blunts microvascular recruitment in human forearm muscle following a mixed meal. Diabetes Care 32:1672–1677
9. Yudkin JS, Eringa E, Stehouwer CD (2005) "Vasocrine" signalling from perivascular fat: a mechanism linking insulin resistance to vascular disease. Lancet 365:1817–1820
10. Meijer RI, Serne EH, Smulders YM, van Hinsbergh VWM, Yudkin JS, Eringa EC (2011) Perivascular adipose tissue and its role in type 2 diabetes and cardiovascular disease. Curr Diab Rep 11:211–217
11. Meijer RI, Bakker W, Alta CL et al (2013) Perivascular adipose tissue control of insulin-induced vasoreactivity in muscle is impaired in db/db mice. Diabetes 62:590–598
12. Greenstein AS, Khavandi K, Withers SB et al (2009) Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 119:1661–1670
13. Withers SB, Agabiti-Rosei C, Livingstone DM et al (2011) Macrophage activation is responsible for loss of anticontractile function in inflamed perivascular fat. Arterioscler Thromb Vasc Biol 31:908–913
14. Galvez-Prieto B, Somoza B, Gil-Ortega M et al (2012) Anticontractile effect of perivascular adipose tissue and leptin are reduced in hypertension. Front Pharmacol 6:1–8
15. Owen MK, Witzmann FA, McKenney ML et al (2013) Perivascular adipose tissue potentiates contraction of coronary vascular smooth muscle: influence of obesity. Circulation 128:9–18
16. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112:1796–1808
17. Omar A, Chatterjee TK, Tang Y, Hui DY, Weintraub NL (2014) Proinflammatory phenotype of perivascular adipocytes. Arterioscler Thromb Vasc Biol 34:1631–1636
18. de Jongh RT, Clark AD, Ijzerman RG, Serne EH, de Vries G, Stehouwer CD (2004) Physiological hyperinsulinaemia increases intramuscular microvascular reactive hyperaemia and vasomotion in healthy volunteers. Diabetologia 47:978–986
19. Mitchell WK, Phillips BE, Williams JP et al (2013) Development of a new Sonovue contrast-enhanced ultrasound approach reveals temporal and age-related features of muscle microvascular responses to feeding. Physiol Rep 1, e00119
20. Barrett EJ, Rattigan S (2012) Muscle perfusion: its measurement and role in metabolic regulation. Diabetes 61:2661–2668
21. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
22. Preacher KJ, Hayes AF (2008) Asymptotic and resampling strategies for assessing and comparing indirect effects in multiple mediator models. Behav Res Methods 40:879–891
23. Rittig K, Staib K, Machann J et al (2008) Perivascular fatty tissue at the brachial artery is linked to insulin resistance but not to local endothelial dysfunction. Diabetologia 51:2093–2099
24. Aghamohammadzadeh R, Greenstein AS, Yadav R et al (2013) The effects of bariatric surgery on human small artery function: evidence for reduction in perivascular adipocyte inflammation, and the restoration of normal anticontractile activity despite persistent obesity. J Am Coll Cardiol 62:128–135
25. Bhattacharya I, Dragert K, Albert V et al (2013) Rictor in perivascular adipose tissue controls vascular function by regulating inflammatory molecule expression. Arterioscler Thromb Vasc Biol 33:2105–2111
26. Hirata Y, Tabata M, Kurobe H et al (2011) Coronary atherosclerosis is associated with macrophage polarization in epicardial adipose tissue. J Am Coll Cardiol 58:248–255
27. Chatterjee TK, Stoll LL, Denning GM et al (2009) Proinflammatory phenotype of perivascular adipocytes influence of high-fat feeding. Circ Res 104:541–549
28. Cotillard A, Poitou C, Torcivia A et al (2014) Adipocyte size threshold matters: link with risk of type 2 diabetes and improved insulin-resistance after gastric bypass. J Clin Endocrinol Metab 99:E1466–E1470
29. Michaud A, Boulet MM, Veilleux A, Noel S, Paris G, Tchernof A (2014) Abdominal subcutaneous and omental adipocyte morphology and its relation to gene expression, lipolysis and adipocytokine levels in women. Metabolism 63:372–381
30. Cardillo C, Nambi SS, Kilcoyne CM et al (1999) Insulin stimulates both endothelin and nitric oxide activity in the human forearm. Circulation 100:820–825
31. Eringa EC, Stehouwer CD, Merlijn T, Westerhof N, Sipkema P (2002) Physiological concentrations of insulin induce endothelin-mediated vasoconstriction during inhibition of NOS or PI3-kinase in skeletal muscle arterioles. Cardiovasc Res 56:464–471
32. Eringa EC, Stehouwer CD, van Nieuw Amerongen GP, Ouwehand L, Westerhof N, Sipkema P (2004) Vasoconstrictor effects of insulin in skeletal muscle arterioles are mediated by ERK1/2 activation in endothelium. Am J Physiol Heart Circ Physiol 287:H2043–H2048
33. Mendizabal Y, Llorens S, Nava E (2013) Vasoactive effects of prostaglandins from the perivascular fat of mesenteric resistance arteries in WKY and SHROB rats. Life Sci 93:1023–1032
34. Virdis A, Duranti E, Rossi C et al (2015) Tumour necrosis factor-alpha participates on the endothelin-1/nitric oxide imbalance in small arteries from obese patients: role of perivascular adipose tissue. Eur Heart J 36:784–794
35. Zhao L, Chai W, Fu Z et al (2013) Globular adiponectin enhances muscle insulin action via microvascular recruitment and increased insulin delivery. Circ Res 112:1263–1271
36. Margaritis M, Antonopoulos AS, Digby J et al (2013) Interactions between vascular wall and perivascular adipose tissue reveal novel roles for adiponectin in the regulation of endothelial nitric oxide synthase function in human vessels. Circulation 127:2209–2221
37. Antonopoulos AS, Margaritis M, Coutinho P et al (2014) Adiponectin as a link between type 2 diabetes mellitus and vascular NADPH-oxidase activity in the human arterial wall: the regulatory role of perivascular adipose tissue. Diabetes. doi:10.2337/db14-1011
38. Segal SS, Duling BR (1986) Communication between feed arteries and microvessels in hamster striated muscle: segmental vascular responses are functionally coordinated. Circ Res 59:283–290