Methotrexate promotes glucose uptake and lipid oxidation in skeletal muscle via AMPK activation

Diabetes

Volumn 64, Issue 2, 2015, Pages 360-369

  Pirkmajer, Sergej ^a   Kulkarni, Sameer S ^a   Tom, Robby Z ^a   Ross, Fiona A ^b   Hawley, Simon A ^b   Hardie, D Grahame ^b   Zierath, Juleen R ^a   Chibalin, Alexander V ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; GLUCOSE TRANSPORTER 4; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; METHOTREXATE; PALMITIC ACID; SMALL INTERFERING RNA; GLUCOSE; NUCLEIC ACID SYNTHESIS INHIBITOR; PROTEIN SUBUNIT;

ANIMAL EXPERIMENT; ARTICLE; CELL LYSATE; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVATION; GENE SILENCING; GLUCOSE TRANSPORT; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; LIPID OXIDATION; METABOLIC ACTIVITY ASSAY; MOUSE; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PURINE SYNTHESIS; SKELETAL MUSCLE; SOLEUS MUSCLE; CELL LINE; CHEMISTRY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LIPID PEROXIDATION; METABOLISM; PHYSIOLOGY; PROTEIN SUBUNIT;

AMP-ACTIVATED PROTEIN KINASES; CELL LINE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; HUMANS; LIPID PEROXIDATION; METHOTREXATE; MUSCLE, SKELETAL; NUCLEIC ACID SYNTHESIS INHIBITORS; PROTEIN SUBUNITS;

EID: 84921897035     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db14-0508     Document Type: Article

References (49)

1. Toms TE, Panoulas VF, John H, Douglas KM, Kitas GD. Methotrexate therapy associates with reduced prevalence of the metabolic syndrome in rheumatoid arthritis patients over the age of 60-more than just an anti-inflammatory effect? A cross sectional study. Arthritis Res Ther 2009;11:R110
2. Solomon DH, Massarotti E, Garg R, Liu J, Canning C, Schneeweiss S. Association between disease-modifying antirheumatic drugs and diabetes risk in patients with rheumatoid arthritis and psoriasis. JAMA 2011;305:2525-2531
3. Russo GT, Minutoli L, Bitto A, et al. Methotrexate increases skeletal muscle GLUT4 expression and improves metabolic control in experimental diabetes. J Nutr Metab 2012;2012:132056
4. De Oliveira CC, Acedo SC, Gotardo EM, et al. Effects of methotrexate on inflammatory alterations induced by obesity: an in vivo and in vitro study. Mol Cell Endocrinol 2012;361:92-98
5. Mathews CK. DNA synthesis as a therapeutic target: the first 65 years. FASEB J 2012;26:2231-2237
6. Cronstein BN, Naime D, Ostad E. The antiinflammatory mechanism of methotrexate. Increased adenosine release at inflamed sites diminishes leukocyte accumulation in an in vivo model of inflammation. J Clin Invest 1993;92:2675-2682
7. Svenson KL, Pollare T, Lithell H, Hällgren R. Impaired glucose handling in active rheumatoid arthritis: relationship to peripheral insulin resistance. Metabolism 1988;37:125-130
8. Hoes JN, Van Der Goes MC, Van Raalte DH, et al. Glucose tolerance, insulin sensitivity and β-cell function in patients with rheumatoid arthritis treated with or without low-to-medium dose glucocorticoids. Ann Rheum Dis 2011;70:1887-1894
9. Dhalla AK, Wong MY, Voshol PJ, Belardinelli L, Reaven GM. A1 adenosine receptor partial agonist lowers plasma FFA and improves insulin resistance induced by high-fat diet in rodents. Am J Physiol Endocrinol Metab 2007;292:E1358-E1363
10. Xu B, Berkich DA, Crist GH, La Noue KF. A1 adenosine receptor antagonism improves glucose tolerance in Zucker rats. Am J Physiol 1998;274:E271-E279
11. Chabner BA, Allegra CJ, Curt GA, et al. Polyglutamation of methotrexate. Is methotrexate a prodrug? J Clin Invest 1985;76:907-912
12. Marie S, Heron B, Bitoun P, Timmerman T, Van Den Berghe G, Vincent MF. AICA-ribosiduria: a novel, neurologically devastating inborn error of purine biosynthesis caused by mutation of ATIC. Am J Hum Genet 2004;74:1276-1281
13. Luhby AL, Cooperman JM. Aminoimidazolecarboxamide excretion in vitamin-B12 and folic-acid deficiencies. Lancet 1962;2:1381-1382
14. Corton JM, Gillespie JG, Hawley SA, Hardie DG. 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 1995;229:558-565
15. Hardie DG, Ross FA, Hawley SA. AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 2012;13:251-262
16. Day P, Sharff A, Parra L, et al. Structure of a CBS-domain pair from the regulatory gamma1 subunit of human AMPK in complex with AMP and ZMP. Acta Crystallogr D Biol Crystallogr 2007;63:587-596
17. Hawley SA, Ross FA, Chevtzoff C, et al. Use of cells expressing gamma subunit variants to identify diverse mechanisms of AMPK activation. Cell Metab 2010;11:554-565
18. Fogarty S, Hardie DG. Development of protein kinase activators: AMPK as a target in metabolic disorders and cancer. Biochim Biophys Acta 2010;1804:581-591
19. Long YC, Zierath JR. AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 2006;116:1776-1783
20. Hardie DG. AMPK: a target for drugs and natural products with effects on both diabetes and cancer. Diabetes 2013;62:2164-2172
21. Sabina RL, Kernstine KH, Boyd RL, Holmes EW, Swain JL. Metabolism of 5-amino-4-imidazolecarboxamide riboside in cardiac and skeletal muscle. Effects on purine nucleotide synthesis. J Biol Chem 1982;257:10178-10183
22. Bønsdorff T, Gautier M, Farstad W, Rønningen K, Lingaas F, Olsaker I. Mapping of the bovine genes of the de novo AMP synthesis pathway. Anim Genet 2004;35:438-444
23. Narkar VA, Downes M, Yu RT, et al. AMPK and PPARdelta agonists are exercise mimetics. Cell 2008;134:405-415
24. Song XM, Fiedler M, Galuska D, et al. 5-Aminoimidazole-4-carboxamide ribonucleoside treatment improves glucose homeostasis in insulin-resistant diabetic (ob/ob) mice. Diabetologia 2002;45:56-65
25. Merrill GF, Kurth EJ, Hardie DG, Winder WW. AICA riboside increases AMPactivated protein kinase, fatty acid oxidation, and glucose uptake in rat muscle. Am J Physiol 1997;273:E1107-E1112
26. Dixon R, Gourzis J, McDermott D, Fujitaki J, Dewland P, Gruber H. AICAriboside: safety, tolerance, and pharmacokinetics of a novel adenosine-regulating agent. J Clin Pharmacol 1991;31:342-347
27. Boon H, Bosselaar M, Praet SF, et al. Intravenous AICAR administration reduces hepatic glucose output and inhibits whole body lipolysis in type 2 diabetic patients. Diabetologia 2008;51:1893-1900
28. Barnes BR, Marklund S, Steiler TL, et al. The 59-AMP-activated protein kinase gamma3 isoform has a key role in carbohydrate and lipid metabolism in glycolytic skeletal muscle. J Biol Chem 2004;279:38441-38447
29. Woods A, Salt I, Scott J, Hardie DG, Carling D. The alpha1 and alpha2 isoforms of the AMP-activated protein kinase have similar activities in rat liver but exhibit differences in substrate specificity in vitro. FEBS Lett 1996;397:347-351
30. Hawley SA, Fullerton MD, Ross FA, et al. The ancient drug salicylate directly activates AMP-activated protein kinase. Science 2012;336:918-922
31. Bökkerink JP, Bakker MA, Hulscher TW, De Abreu RA, Schretlen ED. Purine de novo synthesis as the basis of synergism of methotrexate and 6-mercaptopurine in human malignant lymphoblasts of different lineages. Biochem Pharmacol 1988;37:2321-2327
32. Beckers A, Organe S, Timmermans L, et al. Methotrexate enhances the antianabolic and antiproliferative effects of 5-aminoimidazole-4-carboxamide riboside. Mol Cancer Ther 2006;5:2211-2217
33. Kaminskas E, Nussey AC. Effects of methotrexate and of environmental factors on glycolysis and metabolic energy state in cultured Ehrlich ascites carcinoma cells. Cancer Res 1978;38:2989-2996
34. Oakhill JS, Steel R, Chen ZP, et al. AMPK is a direct adenylate chargeregulated protein kinase. Science 2011;332:1433-1435
35. Davies SP, Helps NR, Cohen PT, Hardie DG. 59-AMP inhibits dephosphorylation, as well as promoting phosphorylation, of the AMP-activated protein kinase. Studies using bacterially expressed human protein phosphatase-2C alpha and native bovine protein phosphatase-2AC. FEBS Lett 1995;377:421-425
36. Mahlapuu M, Johansson C, Lindgren K, et al. Expression profiling of the gamma-subunit isoforms of AMP-activated protein kinase suggests a major role for gamma3 in white skeletal muscle. Am J Physiol Endocrinol Metab 2004;286:E194-E200
37. Scott JW, Van Denderen BJ, Jorgensen SB, et al. Thienopyridone drugs are selective activators of AMP-activated protein kinase beta1-containing complexes. Chem Biol 2008;15:1220-1230
38. Wojtaszewski JF, Birk JB, Frøsig C, Holten M, Pilegaard H, Dela F. 5'AMP activated protein kinase expression in human skeletal muscle: effects of strength training and type 2 diabetes. J Physiol 2005;564:563-573
39. Cuthbertson DJ, Babraj JA, Mustard KJ, et al. 5-aminoimidazole-4-carboxamide 1-beta-D-ribofuranoside acutely stimulates skeletal muscle 2-deoxyglucose uptake in healthy men. Diabetes 2007;56:2078-2084
40. Cheung PC, Salt IP, Davies SP, Hardie DG, Carling D. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem J 2000;346:659-669
41. Birk JB, Wojtaszewski JF. Predominant alpha2/beta2/gamma3 AMPK activation during exercise in human skeletal muscle. J Physiol 2006;577:1021-1032
42. Garcia-Roves PM, Osler ME, Holmström MH, Zierath JR. Gain-of-function R225Q mutation in AMP-activated protein kinase gamma3 subunit increases mitochondrial biogenesis in glycolytic skeletal muscle. J Biol Chem 2008;283:35724-35734
43. Wang YC, Chiang EP. Low-dose methotrexate inhibits methionine Sadenosyltransferase in vitro and in vivo. Mol Med 2012;18:423-432
44. Martínez-Chantar ML, Vázquez-Chantada M, Garnacho M, et al. Sadenosylmethionine regulates cytoplasmic HuR via AMP-activated kinase. Gastroenterology 2006;131:223-232
45. Hornik P, Vyskocilová P, Friedecký D, Adam T. Diagnosing AICA-ribosiduria by capillary electrophoresis. J Chromatogr B Analyt Technol Biomed Life Sci 2006;843:15-19
46. Holmes BF, Kurth-Kraczek EJ, Winder WW. Chronic activation of 59-AMPactivated protein kinase increases GLUT-4, hexokinase, and glycogen in muscle. J Appl Physiol (1985) 1999;87:1990-1995
47. Sugita T, Aya H, Ueno M, Ishizuka T, Kawashima K. Characterization of molecularly cloned human 5-aminoimidazole-4-carboxamide ribonucleotide transformylase. J Biochem 1997;122:309-313
48. Chan ES, Montesinos MC, Fernandez P, et al. Adenosine A (2A) receptors play a role in the pathogenesis of hepatic cirrhosis. Br J Pharmacol 2006;148:1144-1155
49. Worm J, Kirkin AF, Dzhandzhugazyan KN, Guldberg P. Methylationdependent silencing of the reduced folate carrier gene in inherently methotrexateresistant human breast cancer cells. J Biol Chem 2001;276:39990-40000