Ranolazine recruits muscle microvasculature and enhances insulin action in rats

Journal of Physiology

Volumn 591, Issue 20, 2013, Pages 5235-5249

  Fu, Zhuo ^a   Zhao, Lina ^a   Chai, Weidong ^a   Dong, Zhenhua ^a,b   Cao, Wenhong ^c   Liu, Zhenqi ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b JINAN CENTRAL HOSPITAL AFFILIATED TO SHANDONG UNIVERSITY   (China)

^c IL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; INSULIN; INSULIN I 125; PHENYLEPHRINE; RANOLAZINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTERIOLE; ARTERY CONSTRICTION; ARTICLE; BLOOD VOLUME; CONTRAST ENHANCEMENT; ENZYME SYNTHESIS; EX VIVO STUDY; HYPERINSULINEMIA; MALE; MICROVASCULAR ENDOTHELIAL CELL; MICROVASCULATURE; MUSCLE BLOOD FLOW; MUSCLE BLOOD VESSEL; MUSCLE TONE; NONHUMAN; NUTRIENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; ULTRASOUND; VASODILATATION;

ACETANILIDES; ANIMALS; BLOOD GLUCOSE; CATTLE; CELLS, CULTURED; CYCLIC AMP; ENDOTHELIAL CELLS; INSULIN; MALE; MAP KINASE SIGNALING SYSTEM; MICROVESSELS; MUSCLE, SKELETAL; NITRIC OXIDE SYNTHASE TYPE III; PIPERAZINES; RATS; RATS, SPRAGUE-DAWLEY; REGIONAL BLOOD FLOW; VASODILATION;

EID: 84885406217     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.257246     Document Type: Article

References (51)

1. Bagger JP, Botker HE, Thomassen A & Nielsen TT (1997). Effects of ranolazine on ischemic threshold, coronary sinus blood flow, and myocardial metabolism in coronary artery disease. Cardiovasc Drugs Ther 11, 479-484.
2. Barrett EJ, Eggleston EM, Inyard AC, Wang H, Li G, Chai W & 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.
3. Barrett EJ, Wang H, Upchurch CT & Liu Z (2011). Insulin regulates its own delivery to skeletal muscle by feed-forward actions on the vasculature. Am J Physiol Endocrinol Metab 301, E252-263.
4. Bertelsen M, Anggard EE & Carrier MJ (2001). Oxidative stress impairs insulin internalization in endothelial cells in vitro. Diabetologia 44, 605-613.
5. Chai W, Dong Z, Wang N, Wang W, Tao L, Cao W & 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.
6. Chai W, Wang W, Dong Z, Cao W & Liu Z (2011). Angiotensin II receptors modulate muscle microvascular and metabolic responses to insulin in vivo. Diabetes 60, 2939-2946.
7. Chai W, Wang W, Liu J, Barrett EJ, Carey RM, Cao W & Liu Z (2010). Angiotensin II type 1 and type 2 receptors regulate basal skeletal muscle microvascular volume and glucose use. Hypertension 55, 523-530.
8. Chaitman BR (2002). Measuring antianginal drug efficacy using exercise testing for chronic angina: improved exercise performance with ranolazine, a pFOX inhibitor. Curr Probl Cardiol 27, 527-555.
9. Chaitman BR (2004). Efficacy and safety of a metabolic modulator drug in chronic stable angina: review of evidence from clinical trials. J Cardiovasc Pharmacol Ther 9(Suppl 1), S47-64.
10. Chaitman BR, Pepine CJ, Parker JO, Skopal J, Chumakova G, Kuch J, Wang W, Skettino SL & Wolff AA (2004a). Effects of ranolazine with atenolol, amlodipine, or diltiazem on exercise tolerance and angina frequency in patients with severe chronic angina: a randomized controlled trial. JAMA 291, 309-316.
11. Chaitman BR, Skettino SL, Parker JO, Hanley P, Meluzin J, Kuch J, Pepine CJ, Wang W, Nelson JJ, Hebert DA & Wolff AA (2004b). Anti-ischemic effects and long-term survival during ranolazine monotherapy in patients with chronic severe angina. J Am Coll Cardiol 43, 1375-1382.
12. Chisholm JW, Goldfine AB, Dhalla AK, Braunwald E, Morrow DA, Karwatowska-Prokopczuk E & Belardinelli L (2010). Effect of ranolazine on A1C and glucose levels in hyperglycemic patients with non-ST elevation acute coronary syndrome. Diabetes Care 33, 1163-1168.
13. Chiu JD, Richey JM, Harrison LN, Zuniga E, Kolka CM, Kirkman E, Ellmerer M & Bergman RN (2008). Direct administration of insulin into skeletal muscle reveals that the transport of insulin across the capillary endothelium limits the time course of insulin to activate glucose disposal. Diabetes 57, 828-835.
14. 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, E732-750.
15. Clark MG, Wallis MG, Barrett EJ, Vincent MA, Richards SM, Clerk LH & Rattigan S (2003). Blood flow and muscle metabolism: a focus on insulin action. Am J Physiol Endocrinol Metab 284, E241-258.
16. Clarke B, Spedding M, Patmore L & McCormack JG (1993). Protective effects of ranolazine in guinea-pig hearts during low-flow ischaemia and their association with increases in active pyruvate dehydrogenase. Br J Pharmacol 109, 748-750.
17. Clerk LH, Rattigan S & Clark MG (2002). Lipid infusion impairs physiologic insulin-mediated capillary recruitment and muscle glucose uptake in vivo. Diabetes 51, 1138-1145.
18. 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.
19. Clerk LH, Vincent MA, Lindner JR, Clark MG, Rattigan S & Barrett EJ (2004). The vasodilatory actions of insulin on resistance and terminal arterioles and their impact on muscle glucose uptake. Diabetes Metab Res Rev 20, 3-12.
20. Coggins M, Lindner J, Rattigan S, Jahn L, Fasy E, Kaul S & Barrett E (2001). Physiologic hyperinsulinemia enhances human skeletal muscle perfusion by capillary recruitment. Diabetes 50, 2682-2690.
21. DeFronzo RA, Jacot E, Jequier E, Maeder E, Wahren J & Felber JP (1981). The effect of insulin on the disposal of intravenous glucose. Results from indirect calorimetry and hepatic and femoral venous catheterization. Diabetes 30, 1000-1007.
22. Deng CY, Kuang SJ, Rao F, Yang H, Fang XH, Shan ZX, Li XH, Zhou ZL, Lin QX, Yang M, Wu SL, Yu XY & Lin SG (2012). Effect of ranolazine on rat intrarenal arteries in vitro. Eur J Pharmacol 683, 211-216.
23. Dernovsek KD & Bar RS (1985). Processing of cell-bound insulin by capillary and macrovascular endothelial cells in culture. Am J Physiol Endocrinol Metab 248, E244-251.
24. Dhalla AK, Wang WQ, Dow J, Shryock JC, Belardinelli L, Bhandari A & Kloner RA (2009). Ranolazine, an antianginal agent, markedly reduces ventricular arrhythmias induced by ischemia and ischemia-reperfusion. Am J Physiol Heart Circ Physiol 297, H1923-1929.
25. Drummond GB (2009). Reporting ethical matters in The Journal of Physiology: standards and advice. J Physiol 587, 713-719.
26. Fu Z, Zhang W, Zhen W, Lum H, Nadler J, Bassaganya-Riera J, Jia Z, Wang Y, Misra H & Liu D (2010). Genistein induces pancreatic β-cell proliferation through activation of multiple signaling pathways and prevents insulin-deficient diabetes in mice. Endocrinology 151, 3026-3037.
27. Hachiya HL, Halban PA & King GL (1988). Intracellular pathways of insulin transport across vascular endothelial cells. Am J Physiol Cell Physiol 255, C459-464.
28. Hachiya HL, Takayama S, White MF & King GL (1987). Regulation of insulin receptor internalization in vascular endothelial cells by insulin and phorbol ester. J Biol Chem 262, 6417-6424.
29. 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, 2457-2463.
30. Inyard AC, Clerk LH, Vincent MA & Barrett EJ (2007). Contraction stimulates nitric oxide independent microvascular recruitment and increases muscle insulin uptake. Diabetes 56, 2194-2200.
31. Karaki H, Ozaki H, Hori M, Mitsui-Saito M, Amano K, Harada K, Miyamoto S, Nakazawa H, Won KJ & Sato K (1997). Calcium movements, distribution, and functions in smooth muscle. Pharmacol Rev 49, 157-230.
32. 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, 1672-1677.
33. Li G, Barrett EJ, Barrett MO, Cao W & Liu Z (2007). Tumor necrosis factor-α induces insulin resistance in endothelial cells via a p38 mitogen-activated protein kinase-dependent pathway. Endocrinology 148, 3356-3363.
34. Li G, Barrett EJ, Wang H, Chai W & Liu Z (2005). 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 146, 4690-4696.
35. Liu Z (2007). Insulin at physiological concentrations increases microvascular perfusion in human myocardium. Am J Physiol Endocrinol Metab 293, E1250-1255.
36. Liu Z, Gardner LB & Barrett EJ (1993). Insulin and glucose suppress hepatic glycogenolysis by distinct enzymatic mechanisms. Metabolism 42, 1546-1551.
37. Liu Z, Liu J, Jahn LA, Fowler DE & Barrett EJ (2009). Infusing lipid raises plasma free fatty acids and induces insulin resistance in muscle microvasculature. J Clin Endocrinol Metab 94, 3543-3549.
38. Makielski JC & Valdivia CR (2006). Ranolazine and late cardiac sodium current-a therapeutic target for angina, arrhythmia and more Br J Pharmacol 148, 4-6.
39. McCormack JG, Stanley WC & Wolff AA (1998). Ranolazine: a novel metabolic modulator for the treatment of angina. Gen Pharmacol 30, 639-645.
40. Morrow DA, Scirica BM, Chaitman BR, McGuire DK, Murphy SA, Karwatowska-Prokopczuk E, McCabe CH & Braunwald E (2009). Evaluation of the glycometabolic effects of ranolazine in patients with and without diabetes mellitus in the MERLIN-TIMI 36 randomized controlled trial. Circulation 119, 2032-2039.
41. Nieminen T, Tavares CA, Pegler JR, Belardinelli L & Verrier RL (2011). Ranolazine injection into coronary or femoral arteries exerts marked, transient regional vasodilation without systemic hypotension in an intact porcine model. Circ Cardiovasc Interv 4, 481-487.
42. Ning Y, Zhen W, Fu Z, Jiang J, Liu D, Belardinelli L & Dhalla AK (2011). Ranolazine increases β-cell survival and improves glucose homeostasis in low-dose streptozotocin-induced diabetes in mice. J Pharmacol Exp Ther 337, 50-58.
43. Pollare T, Lithell H, Selinus I & Berne C (1988). Application of prazosin is associated with an increase of insulin sensitivity in obese patients with hypertension. Diabetologia 31, 415-420.
44. Rattigan S, Clark MG & Barrett EJ (1997). Hemodynamic actions of insulin in rat skeletal muscle: evidence for capillary recruitment. Diabetes 46, 1381-1388.
45. Na in guinea pig ventricular myocytes. J Cardiovasc Pharmacol 44, 192-199.
46. Stone PH, Gratsiansky NA, Blokhin A, Huang IZ & Meng L (2006). Antianginal efficacy of ranolazine when added to treatment with amlodipine: the ERICA (Efficacy of Ranolazine in Chronic Angina) trial. J Am Coll Cardiol 48, 566-575.
47. Timmis AD, Chaitman BR & Crager M (2006). Effects of ranolazine on exercise tolerance and HbA1c in patients with chronic angina and diabetes. Eur Heart J 27, 42-48.
48. Venkataraman R, Belardinelli L, Blackburn B, Heo J & Iskandrian AE (2009). A study of the effects of ranolazine using automated quantitative analysis of serial myocardial perfusion images. JACC Cardiovasc Imaging 2, 1301-1309.
49. 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, E123-129.
50. Vincent MA, Clerk LH, Lindner JR, Klibanov AL, Clark MG, Rattigan S & Barrett EJ (2004). Microvascular recruitment is an early insulin effect that regulates skeletal muscle glucose uptake in vivo. Diabetes 53, 1418-1423.
51. Zacharowski K, Blackburn B & Thiemermann C (2001). Ranolazine, a partial fatty acid oxidation inhibitor, reduces myocardial infarct size and cardiac troponin T release in the rat. Eur J Pharmacol 418, 105-110.