GLP-1 at physiological concentrations recruits skeletal and cardiac muscle microvasculature in healthy humans

Clinical Science

Volumn 127, Issue 3, 2014, Pages 163-170

  Subaran, Sharmila C ^a   Sauder, Matthew A ^a   Chai, Weidong ^a   Jahn, Linda A ^a   Fowler, Dale E ^a   Aylor, Kevin W ^a   Basu, Ananda ^b   Liu, Zhenqi ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b MAYO CLINIC   (United States)

Author keywords

conduit artery; contrast ultrasonography; glucagon like peptide 1 (GLP 1); microvascular recruitment

Indexed keywords

GLUCAGON LIKE PEPTIDE 1; INSULIN;

ADULT; ARTICLE; BIOCHEMISTRY; BLOOD FLOW; BRACHIAL ARTERY; CLINICAL ARTICLE; FEMALE; FLOW RATE; GLUCAGON BLOOD LEVEL; HEART MUSCLE; HUMAN; INSULIN BLOOD LEVEL; MALE; MICROVASCULATURE; PRIORITY JOURNAL; SKELETAL MUSCLE; YOUNG ADULT;

ADOLESCENT; ADULT; BLOOD FLOW VELOCITY; BLOOD VOLUME; CORONARY VESSELS; GLUCAGON; GLUCAGON-LIKE PEPTIDE 1; HUMANS; INCRETINS; MICROVESSELS; MUSCLE, SKELETAL; REGIONAL BLOOD FLOW;

EID: 84898787394     PISSN: 01435221     EISSN: None     Source Type: Journal    
DOI: 10.1042/CS20130708     Document Type: Article

References (44)

1. Baggio, L. L. and Drucker, D. J. (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 2131-2157.
2. Drucker, D. J. (2006) The biology of incretin hormones. Cell Metab. 3, 153-165.
3. Vilsboll, T., Krarup, T., Deacon, C. F., Madsbad, S. and Holst, J. J. (2001) Reduced postprandial concentrations of intact biologically active glucagon-like peptide 1 in type 2 diabetic patients. Diabetes 50, 609-613.
4. Toft-Nielsen, M.-B., Damholt, M. B., Madsbad, S., Hilsted, L. M., Hughes, T. E., Michelsen, B. K. and Holst, J. J. (2001) Determinants of the impaired secretion of glucagon-like peptide-1 in type 2 diabetic patients. J. Clin. Endocrinol. Metab. 86, 3717-3723.
5. Vilsboll, T., Krarup, T., Sonne, J., Madsbad, S., Volund, A., Juul, A. G. and Holst, J. J. (2003) 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. 88, 2706-2713.
6. Jones, I., Owens, D., Luzio, S., Williams, S. and Hayes, T. (1989) 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 32, 668-677.
7. Nauck, M. A., Heimesaat, M. M., Orskov, C., Holst, J. J., Ebert, R. and Creutzfeldt, W. (1993) Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J. Clin. Invest. 91, 301-307.
8. Nystrom, T. (2008) The potential beneficial role of glucagon-like peptide-1 in endothelial dysfunction and heart failure associated with insulin resistance. Horm. Metab. Res. 40, 593-606.
9. Nystr̈om, T., Gonon, A. T., Sj̈oholm, A. and Pernow, J. (2005) Glucagon-like peptide-1 relaxes rat conduit arteries via an endothelium-independent mechanism. Regul. Pept. 125, 173-177.
10. Nystrom, T., Gutniak, M. K., Zhang, Q., Zhang, F., Holst, J. J., Ahren, B. and Sjoholm, A. (2004) Effects of glucagon-like peptide-1 on endothelial function in type 2 diabetes patients with stable coronary artery disease. Am. J. Physiol. Endocrinol. Metab. 287, E1209-E1215.
11. Yu, M., Moreno, C., Hoagland, K. M., Dahly, A., Ditter, K., Mistry, M. and Roman, R. J. (2003) Antihypertensive effect of glucagon-like peptide 1 in Dahl salt-sensitive rats. J. Hypertens. 21, 1125-1135.
12. Basu, A., Charkoudian, N., Schrage, W., Rizza, R. A., Basu, R. and Joyner, M. J. (2007) Beneficial effects of GLP-1 on endothelial function in humans: dampening by glyburide but not by glimepiride. Am. J. Physiol. Endocrinol. Metab. 293, E1289-E1295.
13. Richter, G., Feddersen, O., Wagner, U., Barth, P., Goke, R. and Goke, B. (1993) GLP-1 stimulates secretion of macromolecules from airways and relaxes pulmonary artery. Am. J. Physiol. Lung Cell. Mol. Physiol. 265, L374-L381.
14. Golpon, H. A., Puechner, A., Welte, T., Wichert, P. V. and Feddersen, C. O. (2001) Vasorelaxant effect of glucagon-like peptide-(7-36)amide and amylin on the pulmonary circulation of the rat. Regul. Pept. 102, 81-86.
15. Chai, W., Dong, Z., Wang, N., Wang, W., Tao, L., Cao, W. and Liu, Z. (2012) Glucagon-like peptide 1 recruits microvasculature and increases glucose use in muscle via a nitric oxide-dependent mechanism. Diabetes 61, 888-896.
16. Dong, Z., Chai, W., Wang, W., Zhao, L., Fu, Z., Cao, W. and Liu, Z. (2013) Protein kinase A mediates glucagon-like peptide 1-induced nitric oxide production and muscle microvascular recruitment. Am. J. Physiol. Endocrinol. Metab. 304, E222-E228.
17. Erdogdu, ̈ O., Nathanson, D., Sj̈oholm, A., Nystr̈om, T. and Zhang, Q. (2010) Exendin-4 stimulates proliferation of human coronary artery endothelial cells through eNOS-, PKA- and PI3K/Akt-dependent pathways and requires GLP-1 receptor. Mol. Cell. Endocrinol. 325, 26-35.
18. Nikolaidis, L. A., Elahi, D., Hentosz, T., Doverspike, A., Huerbin, R., Zourelias, L., Stolarski, C., Shen, Y.-T. and Shannon, R. P. (2004) Recombinant glucagon-like peptide-1 increases myocardial glucose uptake and improves left ventricular performance in conscious dogs with pacing-induced dilated cardiomyopathy. Circulation 110, 955-961.
19. Barrett, E., Eggleston, E., Inyard, A., Wang, H., Li, G., Chai, W. and Liu, Z. (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.
20. Barrett, E. J., Wang, H., Upchurch, C. T. and Liu, Z. (2011) Insulin regulates its own delivery to skeletal muscle by feed-forward actions on the vasculature. Am. J. Physiol. Endocrinol. Metab. 301, E252-E263.
21. Liu, Z. (2007) Insulin at physiological concentrations increases microvascular perfusion in human myocardium. Am. J. Physiol. Endocrinol. Metab. 293, E1250-E1255.
22. Liu, Z., Liu, J., Jahn, L. A., Fowler, D. E. and Barrett, E. J. (2009) Infusing lipid raises plasma free fatty acids and induces insulin resistance in muscle microvasculature. J. Clin. Endocrinol. Metab. 94, 3543-3549.
23. Liu, J., Jahn, L. A., Fowler, D. E., Barrett, E. J., Cao, W. and Liu, Z. (2011) Free fatty acids induce insulin resistance in both cardiac and skeletal muscle microvasculature in humans. J. Clin. Endocrinol. Metab. 96, 438-446.
24. Sauder, M. A., Liu, J., Jahn, L. A., Fowler, D. E., Chai, W. and Liu, Z. (2012) Candesartan acutely recruits skeletal and cardiac muscle microvasculature in healthy humans. J. Clin. Endocrinol. Metab. 97, E1208-E1212.
25. Meier, J. J., Gallwitz, B., Salmen, S., Goetze, O., Holst, J. J., Schmidt, W. E. and Nauck, M. A. (2003) Normalization of glucose concentrations and deceleration of gastric emptying after solid meals during intravenous glucagon-like peptide 1 in patients with type 2 diabetes. J. Clin. Endocrinol. Metab. 88, 2719-2725.
26. Hvidberg, A., Nielsen, M. T., Hilsted, J., Ørskov, C. and Holst, J. J. (1994) Effect of glucagon-like peptide-1 (proglucagon 78-107amide) on hepatic glucose production in healthy man. Metabolism 43, 104-108.
27. Coggins, M., Lindner, J., Rattigan, S., Jahn, L., Fasy, E., Kaul, S. and Barrett, E. (2001) Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes 50, 2682-2690.
28. Meijer, R. I., De Boer, M. P., Groen, M. R., Eringa, E. C., Rattigan, S., Barrett, E. J., Smulders, Y. M. and Serne, E. H. (2012) Insulin-induced microvascular recruitment in skin and muscle are related and both are associated with whole-body glucose uptake. Microcirculation 19, 494-500.
29. Katz, A., Nambi, S. S., Mather, K., Baron, A. D., Follmann, D. A., Sullivan, G. and Quon, M. J. (2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. J. Clin. Endocrinol. Metab. 85, 2402-2410.
30. Smushkin, G., Sathananthan, A., Man, C. D., Zinsmeister, A. R., Camilleri, M., Cobelli, C., Rizza, R. A. and Vella, A. (2012) Defects in GLP-1 response to an oral challenge do not play a significant role in the pathogenesis of prediabetes. J. Clin. Endocrinol. Metab. 97, 589-598.
31. Nikolaidis, L. A., Mankad, S., Sokos, G. G., Miske, G., Shah, A., Elahi, D. and Shannon, R. P. (2004) Effects of glucagon-like peptide-1 in patients with acute myocardial infarction and left ventricular dysfunction after successful reperfusion. Circulation 109, 962-965.
32. Moberly, S. P., Berwick, Z. C., Kohr, M., Svendsen, M., Mather, K. J. and Tune, J. D. (2012) Intracoronary glucagon-like peptide 1 preferentially augments glucose uptake in ischemic myocardium independent of changes in coronary flow. Exp. Biol. Med. 237, 334-342.
33. Sokos, G. G., Bolukoglu, H., German, J., Hentosz, T., Magovern, Jr, G. J., Maher, T. D., Dean, D. A., Bailey, S. H., Marrone, G., Benckart, D. H. et al. (2007) Effect of glucagon-like peptide-1 (GLP-1) on glycemic control and left ventricular function in patients undergoing coronary artery bypass grafting. Am. J. Cardiol. 100, 824-829.
34. Keske, M. A., Clerk, L. H., Price, W. J., Jahn, L. A. and Barrett, E. J. (2009) Obesity blunts microvascular recruitment in human forearm muscle after a mixed meal. Diabetes Care 32, 1672-1677.
35. Chai, W., Wang, W., Liu, J., Barrett, E. J., Carey, R. M., Cao, W. and Liu, Z. (2010) Angiotensin II type 1 and type 2 receptors regulate basal skeletal muscle microvascular volume and glucose use. Hypertension 55, 523-530.
36. Zhao, T., Parikh, P., Bhashyam, S., Bolukoglu, H., Poornima, I., Shen, Y.-T. and Shannon, R. P. (2006) Direct effects of glucagon-like peptide-1 on myocardial contractility and glucose uptake in normal and postischemic isolated rat hearts. J. Pharmacol. Exp. Ther. 317, 1106-1113.
37. Chai, W., Liu, J., Jahn, L. A., Fowler, D. E., Barrett, E. J. and Liu, Z. (2011) Salsalate attenuates free fatty acid-induced microvascular and metabolic insulin resistance in humans. Diabetes Care 34, 1634-1638.
38. Clerk, L. H., Vincent, M. A., Jahn, L. A., Liu, Z., Lindner, J. R. and Barrett, E. J. (2006) Obesity blunts insulin-mediated microvascular recruitment in human forearm muscle. Diabetes 55, 1436-1442.
39. Zhang, L., Vincent, M. A., Richards, S. M., Clerk, L. H., Rattigan, S., Clark, M. G. and Barrett, E. J. (2004) Insulin sensitivity of muscle capillary recruitment in vivo. Diabetes 53, 447-453.
40. Ayala, J. E., Bracy, D. P., James, F. D., Julien, B. M., Wasserman, D. H. and Drucker, D. J. (2009) The glucagon-like peptide-1 receptor regulates endogenous glucose production and muscle glucose uptake independent of its incretin action. Endocrinology 150, 1155-1164.
41. Rattigan, S., Clark, M. G. and Barrett, E. J. (1997) Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46, 1381-1388.
42. Randin, D., Vollenweider, P., Tappy, L., Jequier, E., Nicod, P. and Scherrer, U. (1994) Effects of adrenergic and cholinergic blockade on insulin-induced stimulation of calf blood flow in humans. Am. J. Physiol. Regul. Integrat. Comp. Physiol. 266, R809-R816.
43. Halbirk, M., Norrelund, H., Moller, N., Holst, J. J., Schmitz, O., Nielsen, R., Nielsen-Kudsk, J. E., Nielsen, S. S., Nielsen, T. T., Eiskjar, H. et al. (2010) Cardiovascular and metabolic effects of 48-h glucagon-like peptide-1 infusion in compensated chronic patients with heart failure. Am. J. Physiol. Heart Circ. Physiol. 298, H1096-H1102.
44. Nathanson, D., Ullman, B., Lofstrom, U., Hedman, A., Frick, M., Sjoholm, A. and Nystrom, T. (2012) Effects of intravenous exenatide in type 2 diabetic patients with congestive heart failure: a double-blind, randomised controlled clinical trial of efficacy and safety. Diabetologia 55, 926-935.