Enhancement of insulin-mediated rat muscle glucose uptake and microvascular perfusion by 5-aminoimidazole-4-carboxamide-1-β-d-ribofuranoside

Cardiovascular Diabetology

Volumn 14, Issue 1, 2015, Pages

  Bradley, Eloise A ^a   Zhang, Lei ^b   Genders, Amanda J ^c   Richards, Stephen M ^d   Rattigan, Stephen ^a   Keske, Michelle A ^a  

^a UNIVERSITY OF TASMANIA   (Australia)

^b GARVAN INSTITUTE OF MEDICAL RESEARCH   (Australia)

^c VICTORIA UNIVERSITY   (Australia)

^d UNIVERSITY OF TASMANIA   (Australia)

Author keywords

Glucose; Insulin; Microbubbles; Microcirculation; Muscle

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; GLUCOSE; INSULIN; LACTIC ACID; NITRIC OXIDE SYNTHASE; 5 AMINO 4 IMIDAZOLECARBOXAMIDE; AICA RIBONUCLEOTIDE; ANTIDIABETIC AGENT; CONTRAST MEDIUM; DEOXYGLUCOSE; RIBONUCLEOTIDE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VOLUME; CLAMP; CONTRAST ENHANCEMENT; CONTROLLED STUDY; ECHOGRAPHY; EUGLYCEMIC HYPERINSULINEMIC CLAMP; FEMORAL ARTERY FLOW; GASTROCNEMIUS MUSCLE; GLUCOSE BLOOD LEVEL; GLUCOSE INFUSION RATE; GLUCOSE TRANSPORT; HINDLIMB; IN VIVO STUDY; INFUSION RATE; INSULIN BLOOD LEVEL; LACTATE BLOOD LEVEL; MALE; MEAN ARTERIAL PRESSURE; MICROBUBBLE; MICROVASCULAR PERFUSION; MUSCLE CELL; MUSCLE MICROVASCULAR BLOOD VOLUME; NONHUMAN; PERFUSION; PLANTARIS MUSCLE; RAT; SOLEUS MUSCLE; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; BLOOD FLOW; BLOOD FLOW VELOCITY; DIAGNOSTIC IMAGING; DRUG EFFECTS; FAST MUSCLE FIBER; FEMORAL ARTERY; GLUCOSE CLAMP TECHNIQUE; METABOLISM; MICROCIRCULATION; MICROVASCULATURE; PHYSIOLOGY; SKELETAL MUSCLE; SLOW MUSCLE FIBER; TIME FACTOR; VASCULARIZATION; WISTAR RAT;

AMINOIMIDAZOLE CARBOXAMIDE; ANIMALS; BLOOD FLOW VELOCITY; CONTRAST MEDIA; DEOXYGLUCOSE; FEMORAL ARTERY; GLUCOSE CLAMP TECHNIQUE; HINDLIMB; HYPOGLYCEMIC AGENTS; INSULIN; LACTIC ACID; MALE; MICROBUBBLES; MICROCIRCULATION; MICROVESSELS; MUSCLE FIBERS, FAST-TWITCH; MUSCLE FIBERS, SLOW-TWITCH; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE; RATS, WISTAR; REGIONAL BLOOD FLOW; RIBONUCLEOTIDES; TIME FACTORS; ULTRASONOGRAPHY;

EID: 84937231483     PISSN: None     EISSN: 14752840     Source Type: Journal    
DOI: 10.1186/s12933-015-0251-y     Document Type: Article

References (54)

1. Rattigan S, Clark MG, Barrett EJ (1997) Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46(9):1381-1388
2. Vincent MA, Dawson D, Clark AD, Lindner JR, Rattigan S, Clark MG et al (2002) Skeletal muscle microvascular recruitment by physiological hyperinsulinemia precedes increases in total blood flow. Diabetes 51(1):42-48
3. Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S et al (2004) Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53(6):1418-1423
4. Vincent MA, Barrett EJ, Lindner JR, Clark MG, Rattigan S (2003) Inhibiting NOS blocks microvascular recruitment and blunts muscle glucose uptake in response to insulin. Am J Physiol Endocrinol Metab 285(1):E123-E129
5. Rodnick KJ, Henriksen EJ, James DE, Holloszy JO (1992) Exercise training, glucose transporters, and glucose transport in rat skeletal muscles. Am J Physiol 262:C9-C14
6. Stephens JM, Pilch PF (1995) The metabolic regulation and vesicular transport of GLUT4, the major insulin-responsive glucose transporter. Endocr Rev 16:529-546
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(5):1436-1442
8. Keske MA, Clerk LH, Price WJ, Jahn LA, Barrett EJ (2009) Obesity blunts microvascular recruitment in human forearm muscle after a mixed meal. Diabetes Care 32(9):1672-1677
9. Sjoberg KA, Rattigan S, Hiscock NJ, Richter EA, Kiens B (2011) 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(2):H450-H458
10. Vincent MA, Clerk LH, Lindner JR, Price WJ, Jahn LA, Leong-Poi H et al (2006) Mixed meal and light exercise each recruit muscle capillaries in healthy humans. Am J Physiol Endocrinol Metab 290(6):E1191-E1197
11. Kubota T, Kubota N, Kumagai H, Yamaguchi S, Kozono H, Takahashi T et al (2011) Impaired insulin signaling in endothelial cells reduces insulin-induced glucose uptake by skeletal muscle. Cell Metab 13(3):294-307
12. 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(1):28-36
13. St Pierre P, Genders AJ, Keske MA, Richards SM, Rattigan S (2010) Loss of insulin-mediated microvascular perfusion in skeletal muscle is associated with the development of insulin resistance. Diabetes Obes Metab 12(9):798-805
14. Wallis MG, Wheatley CM, Rattigan S, Barrett EJ, Clark AD, Clark MG (2002) Insulin-mediated hemodynamic changes are impaired in muscle of zucker obese rats. Diabetes 51(12):3492-3498
15. Clark MG (2008) Impaired microvascular perfusion: a consequence of vascular dysfunction and a potential cause of insulin resistance in muscle. Am J Physiol Endocrinol Metab 295(4):E732-E750
16. Scherrer U, Randin D, Vollenweider P, Vollenweider L, Nicod P (1994) Nitric oxide release accounts for insulin's vascular effects in humans. J Clin Invest 94(6):2511-2515
17. Steinberg HO, Brechtel G, Johnson A, Fineberg N, Baron AD (1994) Insulin-mediated skeletal muscle vasodilation is nitric oxide dependent. A novel action of insulin to increase nitric oxide release. J Clin Invest. 94:1172-1179
18. Bradley EA, Richards SM, Keske MA, Rattigan S (2013) Local NOS inhibition impairs vascular and metabolic actions of insulin in rat hindleg muscle in vivo. Am J Physiol Endocrinol Metab 305(6):E745-E750
19. Natali A, Quinones GA, Pecori N, Sanna G, Toschi E, Ferrannini E (1998) Vasodilation with sodium nitroprusside does not improve insulin action in essential hypertension. Hypertension 31(2):632-636
20. Mahajan H, Richards SM, Rattigan S, Clark MG (2004) Local methacholine but not bradykinin potentiates insulin-mediated glucose uptake in muscle in vivo by augmenting capillary recruitment. Diabetologia 47(12):2226-2234
21. Clark MG, Wallis MG, Barrett EJ, Vincent MA, Richards SM, Clerk LH et al (2003) Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab 284(2):E241-E258
22. Montagnani M, Ravichandran LV, Chen H, Esposito DL, Quon MJ (2002) Insulin receptor substrate-1 and phosphoinositide-dependent kinase-1 are required for insulin-stimulated production of nitric oxide in endothelial cells. Mol Endocrinol 16(8):1931-1942
23. Vincent MA, Montagnani M, Quon MJ (2003) Molecular and physiologic actions of insulin related to production of nitric oxide in vascular endothelium. CurrDiabRep 3(4):279-288
24. Bradley EA, Clark MG, Rattigan S (2007) Acute effects of wortmannin on insulin's hemodynamic and metabolic actions in vivo. Am J Physiol Endocrinol Metab 292(3):E779-E787
25. Bradley EA, Eringa EC, Stehouwer CD, Korstjens I, Nieuw Amerongen GP, Musters R et al (2010) Activation of AMP-activated protein kinase by 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside in the muscle microcirculation increases nitric oxide synthesis and microvascular perfusion. Arterioscler Thromb Vasc Biol 30(6):1137-1142
26. Bergeron R, Russell RR III, Young LH, Ren JM, Marcucci M, Lee A et al (1999) Effect of AMPK activation on muscle glucose metabolism in conscious rats. Am J Physiol 276(5 Pt 1):E938-E944
27. Fisher JS, Gao J, Han DH, Holloszy JO, Nolte LA (2002) Activation of AMP kinase enhances sensitivity of muscle glucose transport to insulin. Am J Physiol Endocrinol Metab 282(1):E18-E23
28. Bergeron R, Previs SF, Cline GW, Perret P, Russell RR III, Young LH et al (2001) Effect of 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside infusion on in vivo glucose and lipid metabolism in lean and obese Zucker rats. Diabetes 50(5):1076-1082
29. Wei K, Jayaweera AR, Firoozan S, Linka A, Skyba DM, Kaul S (1998) Quantification of myocardial blood flow with ultrasound-induced destruction of microbubbles administered as a constant venous infusion. Circulation 97(5):473-483
30. Inyard AC, Clerk LH, Vincent MA, Barrett EJ (2007) Contraction stimulates nitric oxide independent microvascular recruitment and increases muscle insulin uptake. Diabetes 56(9):2194-2200
31. Wynants J, Petrov B, Nijhof J, Van Belle H (1987) Optimization of a high-performance liquid chromatographic method for the determination of nucleosides and their catabolies. Application to cat and rabbit heart perfusates. J Chromatogr 386:297-308
32. Laughlin MH, Armstrong RB (1983) Rat muscle blood flows as a function of time during prolonged slow treadmill exercise. Am J Physiol 244:H814-H824
33. Morrow VA, Foufelle F, Connell JM, Petrie JR, Gould GW, Salt IP (2003) Direct activation of AMP-activated protein kinase stimulates nitric oxide synthesis in human aortic endothelial cells. J Biol Chem 278(34):31629-31639
34. Iglesias MA, Ye JM, Frangioudakis G, Saha AK, Tomas E, Ruderman NB et al (2002) AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat-fed rats. Diabetes 51(10):2886-2894
35. Iglesias MA, Furler SM, Cooney GJ, Kraegen EW, Ye JM (2004) AMP-activated protein kinase activation by AICAR increases both muscle fatty acid and glucose uptake in white muscle of insulin-resistant rats in vivo. Diabetes 53(7):1649-1654
36. Ai H, Ihlemann J, Hellsten Y, Lauritzen HP, Hardie DG, Galbo H et al (2002) Effect of fiber type and nutritional state on AICAR- and contraction-stimulated glucose transport in rat muscle. Am J Physiol Endocrinol Metab 282(6):E1291-E1300
37. Putman CT, Martins KJ, Gallo ME, Lopaschuk GD, Pearcey JA, MacLean IM et al (2007) Alpha-catalytic subunits of 5'AMP-activated protein kinase display fiber-specific expression and are upregulated by chronic low-frequency stimulation in rat muscle. Am J Physiol Regul Integr Comp Physiol 293(3):R1325-R1334. doi: 10.1152/ajpregu.00609.2006
38. Pencek RR, Shearer J, Camacho RC, James FD, Lacy DB, Fueger PT et al (2005) 5-Aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside causes acute hepatic insulin resistance in vivo. Diabetes 54(2):355-360
39. Camacho RC, Pencek RR, Lacy DB, James FD, Donahue EP, Wasserman DH (2005) Portal venous 5-aminoimidazole-4-carboxamide-1-beta-d-ribofuranoside infusion overcomes hyperinsulinemic suppression of endogenous glucose output. Diabetes 54(2):373-382
40. Camacho RC, Lacy DB, James FD, Donahue EP, Wasserman DH (2005) 5-Aminoimidazole-4-carboxamide-1-{beta}-d-ribofuranoside renders glucose output by the liver of the dog insensitive to a pharmacological increment in insulin. Am J Physiol Endocrinol Metab 289(6):E1039-E1043
41. Kurth-Kraczek EJ, Hirshman MF, Goodyear LJ, Winder WW (1999) 5' AMP-activated protein kinase activation causes GLUT4 translocation in skeletal muscle. Diabetes 48(8):1667-1671
42. Merrill GF, Kurth EJ, Hardie DG, Winder WW (1997) AICA riboside increases AMP-activated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol 273(6 Pt 1):E1107-E1112
43. Holmes BF, Kurth-Kraczek EJ, Winder WW (1999) Chronic activation of 5'-AMP-activated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle. J Appl Physiol 87(5):1990-1995
44. Winder WW (2000) AMP-activated protein kinase: possible target for treatment of type 2 diabetes. Diabetes Technol Ther 2(3):441-448
45. Atkinson LL, Kozak R, Kelly SE, Onay Besikci A, Russell JC, Lopaschuk GD (2003) Potential mechanisms and consequences of cardiac triacylglycerol accumulation in insulin-resistant rats. Am J Physiol Endocrinol Metab 284(5):E923-E930. doi: 10.1152/ajpendo.00360.2002
46. Halse R, Fryer LG, McCormack JG, Carling D, Yeaman SJ (2003) Regulation of glycogen synthase by glucose and glycogen: a possible role for AMP-activated protein kinase. Diabetes 52(1):9-15
47. Hue L, Beauloye C, Marsin AS, Bertrand L, Horman S, Rider MH (2002) Insulin and ischemia stimulate glycolysis by acting on the same targets through different and opposing signaling pathways. J Mol Cell Cardiol 34(9):1091-1097
48. Longnus SL, Wambolt RB, Parsons HL, Brownsey RW, Allard MF (2003) 5-Aminoimidazole-4-carboxamide 1-beta-d-ribofuranoside (AICAR) stimulates myocardial glycogenolysis by allosteric mechanisms. Am J Physiol Regul Integr Comp Physiol 284(4):R936-R944
49. Jung CH, Lee MJ, Kang YM, Lee YL, Yoon HK, Kang SW et al (2014) Vaspin inhibits cytokine-induced nuclear factor-kappa B activation and adhesion molecule expression via AMP-activated protein kinase activation in vascular endothelial cells. Cardiovasc Diabetol 13:41. doi: 10.1186/1475-2840-13-41
50. Anil TM, Harish C, Lakshmi MN, Harsha K, Onkaramurthy M, Sathish Kumar V et al (2014) CNX-012-570, a direct AMPK activator provides strong glycemic and lipid control along with significant reduction in body weight; studies from both diet-induced obese mice and db/db mice models. Cardiovasc Diabetol 13:27. doi: 10.1186/1475-2840-13-27
51. Clerk LH, Rattigan S, Clark MG (2002) Lipid infusion impairs physiologic insulin-mediated capillary recruitment and muscle glucose uptake in vivo. Diabetes 51(4):1138-1145
52. Wheatley CM, Rattigan S, Richards SM, Barrett EJ, Clark MG (2004) Skeletal muscle contraction stimulates capillary recruitment and glucose uptake in insulin-resistant obese Zucker rats. Am J Physiol Endocrinol Metab 287(4):E804-E809
53. Inyard AC, Chong DG, Klibanov AL, Barrett EJ (2009) Muscle contraction, but not insulin, increases microvascular blood volume in the presence of free fatty acid-induced insulin resistance. Diabetes 58(11):2457-2463
54. Lee-Young RS, Bonner JS, Mayes WH, Iwueke I, Barrick BA, Hasenour CM et al (2013) AMP-activated protein kinase (AMPK)alpha2 plays a role in determining the cellular fate of glucose in insulin-resistant mouse skeletal muscle. Diabetologia 56(3):608-617. doi: 10.1007/s00125-012-2787-7