Glucagon-like peptide 1 recruits microvasculature and increases glucose use in muscle via a nitric oxide-dependent mechanism

Diabetes

Volumn 61, Issue 4, 2012, Pages 888-896

  Chai, Weidong ^a   Dong, Zhenhua ^a,b   Wang, Nasui ^a,c   Wang, Wenhui ^b   Tao, Lijian ^c   Cao, Wenhong ^d   Liu, Zhenqi ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b SHANDONG UNIVERSITY   (China)

^c CENTRAL SOUTH UNIVERSITY   (China)

^d IL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INSULIN; NITRIC OXIDE SYNTHASE; PROTEIN KINASE B; SERINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD FLOW VELOCITY; BLOOD VOLUME; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; GLUCOSE UTILIZATION; HEART MUSCLE OXYGEN CONSUMPTION; INSULIN BLOOD LEVEL; INSULIN CLEARANCE; MALE; MICROVASCULAR BLOOD FLOW VELOCITY; MICROVASCULAR BLOOD VOLUME; MICROVASCULATURE; MUSCLE METABOLISM; NONHUMAN; OXYGEN SATURATION; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; AORTA; CATTLE; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DRUG ADMINISTRATION SCHEDULE; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HORMONES; INSULIN; MALE; MICROVESSELS; MUSCLE, SKELETAL; NG-NITROARGININE METHYL ESTER; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSTATIN;

EID: 84859529626     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db11-1073     Document Type: Article

References (46)

1. Vilsbøll T, Krarup T, Deacon CF, Madsbad S, Holst JJ. Reduced postprandial concentrations of intact biologically active glucagon-like peptide 1 in type 2 diabetic patients. Diabetes 2001;50:609-613 (Pubitemid 32195226)
2. Toft-Nielsen M-B, Damholt MB, Madsbad S, et al. Determinants of the impaired secretion of glucagon-like peptide-1 in type 2 diabetic patients. J Clin Endocrinol Metab 2001;86:3717-3723 (Pubitemid 32755966)
3. Vilsbøll T, Krarup T, Sonne J, et al. Incretin secretion in relation to meal size and body weight in healthy subjects and people with type 1 and type 2 diabetes mellitus. J Clin Endocrinol Metab 2003;88:2706-2713 (Pubitemid 36724446)
4. Jones IR, Owens DR, Luzio S, Williams S, Hayes TM. The glucose dependent insulinotropic polypeptide response to oral glucose and mixed meals is increased in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia 1989;32:668-677 (Pubitemid 19235993)
5. Drucker DJ. The biology of incretin hormones. Cell Metab 2006;3: 153-165
6. Ayala JE, Bracy DP, James FD, Julien BM, Wasserman DH, Drucker DJ. The glucagon-like peptide-1 receptor regulates endogenous glucose production and muscle glucose uptake independent of its incretin action. Endocrinology 2009;150:1155-1164
7. Nikolaidis LA, Elahi D, Hentosz T, et al. Recombinant glucagon-like peptide-1 increases myocardial glucose uptake and improves left ventricular performance in conscious dogs with pacing-induced dilated cardiomyopathy. Circulation 2004;110:955-961 (Pubitemid 39128621)
8. Nikolaidis LA, Elahi D, Shen Y-T, Shannon RP. Active metabolite of GLP-1 mediates myocardial glucose uptake and improves left ventricular performance in conscious dogs with dilated cardiomyopathy. Am J Physiol Heart Circ Physiol 2005;289:H2401-H2408 (Pubitemid 41698549)
9. Johnson KMS, Edgerton DS, Rodewald T, et al. Intraportal GLP-1 infusion increases nonhepatic glucose utilization without changing pancreatic hormone levels. Am J Physiol Endocrinol Metab 2007;293:E1085-E1091 (Pubitemid 47535841)
10. Zhao T, Parikh P, Bhashyam S, et al. Direct effects of glucagon-like peptide-1 on myocardial contractility and glucose uptake in normal and postischemic isolated rat hearts. J Pharmacol Exp Ther 2006;317:1106-1113 (Pubitemid 43764114)
11. Yu M, Moreno C, Hoagland KM, et al. Antihypertensive effect of glucagon-like peptide 1 in Dahl salt-sensitive rats. J Hypertens 2003;21:1125-1135 (Pubitemid 36667866)
12. Basu A, Charkoudian N, Schrage W, Rizza RA, Basu R, Joyner MJ. Beneficial effects of GLP-1 on endothelial function in humans: dampening by glyburide but not by glimepiride. Am J Physiol Endocrinol Metab 2007;293: E1289-E1295 (Pubitemid 350106596)
13. Nyström T, Gutniak MK, Zhang Q, et al. Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am J Physiol Endocrinol Metab 2004;287:E1209-E1215 (Pubitemid 39491964)
14. Richter G, Feddersen O, Wagner U, Barth P, Göke R, Göke B. GLP-1 stimulates secretion of macromolecules from airways and relaxes pulmonary artery. Am J Physiol 1993;265:L374-L381
15. Golpon HA, Puechner A, Welte T, Wichert PV, Feddersen CO. Vasorelaxant effect of glucagon-like peptide-(7-36)amide and amylin on the pulmonary circulation of the rat. Regul Pept 2001;102:81-86 (Pubitemid 33135568)
16. Barrett EJ, Eggleston EM, Inyard AC, et al. The vascular actions of insulin control its delivery to muscle and regulate the rate-limiting step in skeletal muscle insulin action. Diabetologia 2009;52:752-764
17. 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
18. Ko S-H, Cao W, Liu Z. Hypertension management and microvascular insulin resistance in diabetes. Curr Hypertens Rep 2010;12:243-251
19. 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
20. Keske MA, Clerk LH, Price WJ, Jahn LA, Barrett EJ. Obesity blunts microvascular recruitment in human forearm muscle after a mixed meal. Diabetes Care 2009;32:1672-1677
21. Inyard AC, Chong DG, Klibanov AL, Barrett EJ. Muscle contraction, but not insulin, increases microvascular blood volume in the presence of free fatty acid-induced insulin resistance. Diabetes 2009;58:2457-2463
22. Inyard AC, Clerk LH, Vincent MA, Barrett EJ. Contraction stimulates nitric oxide independent microvascular recruitment and increases muscle insulin uptake. Diabetes 2007;56:2194-2200 (Pubitemid 47358225)
23. Coggins M, Lindner J, Rattigan S, et al. Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes 2001;50:2682-2690 (Pubitemid 33733118)
24. Chai W, Wang W, Liu J, et al. Angiotensin II type 1 and type 2 receptors regulate basal skeletal muscle microvascular volume and glucose use. Hypertension 2010;55:523-530
25. Nyström T. The potential beneficial role of glucagon-like peptide-1 in endothelial dysfunction and heart failure associated with insulin resistance. Horm Metab Res 2008;40:593-606
26. Li G, Barrett EJ, Wang H, Chai W, Liu Z. Insulin at physiological concentrations selectively activates insulin but not insulin-like growth factor I (IGF-I) or insulin/IGF-I hybrid receptors in endothelial cells. Endocrinology 2005;146:4690-4696 (Pubitemid 41446606)
27. Li G, Barrett EJ, Ko S-H, Cao W, Liu Z. Insulin and insulin-like growth factor-I receptors differentially mediate insulin-stimulated adhesion molecule production by endothelial cells. Endocrinology 2009;150:3475-3482
28. Vincent MA, Barrett EJ, Lindner JR, Clark MG, Rattigan S. Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 2003;285:E123-E129 (Pubitemid 36736369)
29. Wang N, Ko S-H, Chai W, et al. Resveratrol recruits rat muscle microvasculature via a nitric oxide-dependent mechanism that is blocked by TNFα. Am J Physiol Endocrinol Metab 2011;300:E195-E201
30. Vincent MA, Clerk LH, Lindner JR, et al. Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 2004;53:1418-1423 (Pubitemid 38697651)
31. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 2007;87: 1409-1439 (Pubitemid 350041474)
32. Zeleznik AJ, Roth J. Demonstration of the insulin receptor in vivo in rabbits and its possible role as a reservoir for the plasma hormone. J Clin Invest 1978;61:1363-1374 (Pubitemid 8324162)
33. Tolessa T, Gutniak M, Holst JJ, Efendic S, Hellström PM. Inhibitory effect of glucagon-like peptide-1 on small bowel motility. Fasting but not fed motility inhibited via nitric oxide independently of insulin and somatostatin. J Clin Invest 1998;102:764-774 (Pubitemid 28399609)
34. Chai W, Wang W, Dong Z, Cao W, Liu Z. Angiotensin II receptors modulate muscle microvascular and metabolic responses to insulin in vivo. Diabetes 2011;60:2939-2946
35. Honig CR, Odoroff CL, Frierson JL. Active and passive capillary control in red muscle at rest and in exercise. Am J Physiol 1982;243:H196-H206 (Pubitemid 12051554)
36. Vincent MA, Clerk LH, Lindner JR, et al. Mixed meal and light exercise each recruit muscle capillaries in healthy humans. Am J Physiol Endocrinol Metab 2006;290:E1191-E1197 (Pubitemid 43847903)
37. Scognamiglio R, Negut C, De Kreutzenberg SV, Tiengo A, Avogaro A. Postprandial myocardial perfusion in healthy subjects and in type 2 diabetic patients. Circulation 2005;112:179-184 (Pubitemid 40982299)
38. Hattori Y, Jojima T, Tomizawa A, et al. A glucagon-like peptide-1 (GLP-1) analogue, liraglutide, upregulates nitric oxide production and exerts anti-inflammatory action in endothelial cells. Diabetologia 2010;53:2256-2263
39. Ye J, Gao Z, Yin J, He Q. Hypoxia is a potential risk factor for chronic inflammation and adiponectin reduction in adipose tissue of ob/ob and dietary obese mice. Am J Physiol Endocrinol Metab 2007;293:E1118-E1128 (Pubitemid 47535846)
40. Hosogai N, Fukuhara A, Oshima K, et al. Adipose tissue hypoxia in obesity and its impact on adipocytokine dysregulation. Diabetes 2007;56:901-911 (Pubitemid 46525054)
41. Ye J. Emerging role of adipose tissue hypoxia in obesity and insulin resistance. Int J Obes (Lond) 2009;33:54-66
42. Yin J, Gao Z, He Q, Zhou D, Guo Z, Ye J. Role of hypoxia in obesity-induced disorders of glucose and lipid metabolism in adipose tissue. Am J Physiol Endocrinol Metab 2009;296:E333-E342
43. Kim JA, Koh KK, Quon MJ. The union of vascular and metabolic actions of insulin in sickness and in health. Arterioscler Thromb Vasc Biol 2005;25: 889-891 (Pubitemid 40627830)
44. Kim JA, Montagnani M, Koh KK, Quon MJ. Reciprocal relationships between insulin resistance and endothelial dysfunction: molecular and pathophysiological mechanisms. Circulation 2006;113:1888-1904 (Pubitemid 43739401)
45. Liu J, Jahn LA, Fowler DE, Barrett EJ, Cao W, Liu Z. Free fatty acids induce insulin resistance in both cardiac and skeletal muscle microvasculature in humans. J Clin Endocrinol Metab 2011;96:438-446
46. Holst JJ, Vilsbøll T, Deacon CF. The incretin system and its role in type 2 diabetes mellitus. Mol Cell Endocrinol 2009;297:127-136