GLP-1 increases microvascular recruitment but not glucose uptake in human and rat skeletal muscle

American Journal of Physiology - Endocrinology and Metabolism

Volumn 306, Issue 4, 2014, Pages

  Sjøberg, Kim A ^a   Holst, Jens J ^b   Rattigan, Stephen ^c   Richter, Erik A ^a   Kiens, Bente ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Capillary recruitment; Incretin hormones; Insulin; Microcirculation

Indexed keywords

CAPILLARY RECRUITMENT; INCRETIN HORMONES; INSULIN; MICROCIRCULATION;

ADULT; ANIMALS; CAPILLARIES; FEMORAL ARTERY; GASTROINTESTINAL AGENTS; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE CLAMP TECHNIQUE; HUMANS; LEG; MALE; MUSCLE, SKELETAL; OCTREOTIDE; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84894034004     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00283.2013     Document Type: Article

References (39)

1. Ban K, Noyan-Ashraf MH, Hoefer J, Bolz SS, Drucker DJ, Husain M. Cardioprotective and vasodilatory actions of glucagon-like peptide 1 receptor are mediated through both glucagon-like peptide 1 receptordependent and-independent pathways. Circulation 117: 2340-2350, 2008.
2. Baron AD, Clark MG. Role of blood flow in the regulation of muscle glucose uptake. Annu Rev Nutr 17: 487-499, 1997.
3. Bullock BP, Heller RS, Habener JF. Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor. Endocrinology 137: 2968-2978, 1996.
4. Chai W, Dong Z, Wang N, Wang W, Tao L, Cao W, Liu Z. Glucagonlike peptide 1 recruits microvasculature and increases glucose use in muscle via a nitric oxide-dependent mechanism. Diabetes 61: 888-896, 2012.
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 295: E732-E750, 2008.
6. 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 angiogensin-converting enzyme inhibition. Am J Physiol Endocrinol Metab 293: E1804-E1809, 2007.
7. D'Alessio DA, Kahn SE, Leusner CR, Ensinck JW. Glucagon-like peptide 1 enhances glucose tolerance both by stimulation of insulin release and by increasing insulin-independent glucose disposal. J Clin Invest 93: 2263-2266, 1994.
8. DeFronzo RA, Tobin JD, Andres R. Glucose clamp technique: a method for quantifying insulin secretion and resistance. Am J Physiol Endocrinol Metab Gastrointest Physiol 237: E214-E223, 1979.
9. Delgado E, Luque MA, Alcantara A, Trapote MA, Clemente F, Galera C, Valverde I, Villanueva-Penacarrillo ML. Glucagon-like peptide-1 binding to rat skeletal muscle Peptides 16: 225-229, 1995.
10. Ding L, Zhang J. Glucagon-like peptide-1 activates endothelial nitric oxide synthase in human umbilical vein endothelial cells. Acta Pharmacol Sin 33: 75-81, 2012.
11. Falken Y, Hellstrom PM, Holst JJ, Naslund E. Changes in glucose homeostasis after Roux-en-Y gastric bypass surgery for obesity at day three, two months, and one year after surgery: role of gut peptides. J Clin Endocrinol Metab 96: 2227-2235, 2011.
12. Frosig C, Rose AJ, Treebak JT, Kiens B, Richter EA, Wojtaszewski JF. Effects of endurance exercise training on insulin signaling in human skeletal muscle: interactions at the level of phosphatidylinositol 3-kinase, Akt, and AS160. Diabetes 56: 2093-2102, 2007.
13. Furnsinn C, Ebner K, Waldhausl W. Failure of GLP-1(7-36)amide to affect glycogenesis in rat skeletal muscle. Diabetologia 38: 864-867, 1995.
14. 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 102: 81-86, 2001.
15. Gonzalez N, Acitores A, Sancho V, Valverde I, Villanueva-Penacarrillo ML. Effect of GLP-1 on glucose transport and its cell signalling in human myocytes. Regul Pept 126: 203-211, 2005.
16. Green CJ, Henriksen TI, Pedersen BK, Solomon TP. Glucagon like peptide-1-induced glucose metabolism in differentiated human muscle satellite cells is attenuated by hyperglycemia. PLoS One 7: e44284, 2012.
17. Gutniak M, Orskov C, Holst JJ, Ahren B, Efendic S. Antidiabetogenic effect of glucagon-like peptide-1 (7-36)amide in normal subjects and patients with diabetes mellitus. N Engl J Med 326: 1316-1322, 1992.
18. Hansen BF, Jensen P, Nepper-Christensen E, Skjolstrup B. Effects of glucagon-like peptide-1 (7-36)amide on insulin stimulated rat skeletal muscle glucose transport. Acta Diabetol 35: 101-103, 1998.
19. Hansen L, Hartmann B, Mineo H, Holst JJ. Glucagon-like peptide-1 secretion is influenced by perfusate glucose concentration and by a feedback mechanism involving somatostatin in isolated perfused porcine ileum. Regul Pept 118: 11-18, 2004.
20. Hare KJ, Vilsboll T, Asmar M, Deacon CF, Knop FK, Holst JJ. The glucagonostatic and insulinotropic effects of glucagon-like peptide 1 contribute equally to its glucose-lowering action. Diabetes 59: 1765-1770, 2010.
21. Hoeg LD, Sjoberg KA, Jeppesen J, Jensen TE, Frosig C, Birk JB, Bisiani B, Hiscock N, Pilegaard H, Wojtaszewski JF, Richter EA, Kiens B. Lipid-induced insulin resistance affects women less than men and is not accompanied by inflammation or impaired proximal insulin signaling. Diabetes 60: 64-73, 2011.
22. Holst JJ. The physiology of glucagon-like peptide 1. Physiol Rev 87: 1409-1439, 2007.
23. Hvidberg A, Nielsen MT, Hilsted J, Orskov C, Holst JJ. Effect of glucagon-like peptide-1 (proglucagon 78-107amide) on hepatic glucose production in healthy man. Metabolism 43: 104-108, 1994.
24. Keske MA, Clerk LH, Price WJ, Jahn LA, Barrett EJ. Obesity blunts microvascular recruitment in human forearm muscle after a mixed meal. Diabetes Care 32: 1672-1677, 2009.
25. Knop FK, Vilsboll T, Larsen S, Hojberg PV, Volund A, Madsbad S, Holst JJ, Krarup T. Increased postprandial responses of GLP-1 and GIP in patients with chronic pancreatitis and steatorrhea following pancreatic enzyme substitution. Am J Physiol Endocrinol Metab 292: E324-E330, 2007.
26. 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 96: 438-446, 2011.
27. 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 94: 3543-3549, 2009.
28. Nystrom T, Gonon AT, Sjoholm A, Pernow J. Glucagon-like peptide-1 relaxes rat conduit arteries via an endothelium-independent mechanism. Regul Pept 125: 173-177, 2005.
29. Orskov C, Rabenhoj L, Wettergren A, Kofod H, Holst JJ. Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans. Diabetes 43: 535-539, 1994.
30. Pehmoller C, Brandt N, Birk JB, Hoeg LD, Sjoberg KA, Goodyear LJ, Kiens B, Richter EA, Wojtaszewski JF. Exercise alleviates lipid-induced insulin resistance in human skeletal muscle-signaling interaction at the level of TBC1 domain family member 4. Diabetes 61: 2743-2752, 2012.
31. Rattigan S, Clark MG, Barrett EJ. Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46: 1381-1388, 1997.
32. Sjoberg KA, Rattigan S, Hiscock N, Richter EA, Kiens B. A new method to study changes in microvascular blood volume in muscle and adipose tissue: real-time imaging in humans and rat. Am J Physiol Heart Circ Physiol 301: H450-H458, 2011.
33. Tesauro M, Schinzari F, Adamo A, Rovella V, Martini F, Mores N, Barini A, Pitocco D, Ghirlanda G, Lauro D, Campia U, Cardillo C. Effects of GLP-1 on forearm vasodilator function and glucose disposal during hyperinsulinemia in the metabolic syndrome. Diabetes Care 36: 683-689, 2012.
34. Toft-Nielson M, Madsbad S, Holst JJ. The effect of glucagon-like peptide I (GLP-I) on glucose elimination in healthy subjects depends on the pancreatic glucoregulatory hormones. Diabetes 45: 552-556, 1996.
35. Villanueva-Penacarrillo ML, Alcantara AI, Clemente F, Delgado E, Valverde I. Potent glycogenic effect of GLP-1(7-36)amide in rat skeletal muscle. Diabetologia 37: 1163-1166, 1994.
36. Vilsboll T, Krarup T, Sonne J, Madsbad S, Volund A, Juul AG, Holst JJ. 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, 2003.
37. 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 285: E123-E129, 2003.
38. Wei K, Jayaweera AR, Firoozan S, Linka A, Skyba DM, Kaul S. Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97: 473-483, 1998.
39. Wei Y, Mojsov S. Tissue-specific expression of the human receptor for glucagon-like peptide-I: brain, heart and pancreatic forms have the same deduced amino acid sequences. FEBS Lett 358: 219-224, 1995.