5-Aminoimidazole-4-carboxamide-1-β-D-ribofuranoside (AICAR) effect on glucose production, but not energy metabolism, is independent of hepatic AMPK in vivo

Journal of Biological Chemistry

Volumn 289, Issue 9, 2014, Pages 5950-5959

  Hasenour, Clinton M ^a   Ridley, D Emerson ^a   Hughey, Curtis C ^f   James, Freyja D ^a   Donahue, E Patrick ^a   Shearer, Jane ^f   Viollet, Benoit ^c,d,e   Foretz, Marc ^a,b   Wasserman, David H ^a,b  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c INSTITUT COCHIN   (France)

^d CNRS   (France)

^e UNIVERSITÉ PARIS DESCARTES   (France)

^f UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE; AMP-ACTIVATED PROTEIN KINASE; ANTIDIABETIC AGENTS; ENERGY METABOLISM; GLUCOSE PRODUCTION; MITOCHONDRIAL FUNCTION; MITOCHONDRIAL OXIDATIVE PHOSPHORYLATION; MITOCHONDRIAL RESPIRATION;

BIOELECTRIC POTENTIALS; MAMMALS; METABOLISM; NUCLEOTIDES;

GLUCOSE;

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; FATTY ACID; HEPATIC NUCLEOTIDE MONOPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; ENERGY METABOLISM; ENZYME ACTIVATION; FATTY ACID BLOOD LEVEL; GLUCONEOGENESIS; GLUCOSE METABOLISM; IN VIVO STUDY; MALE; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN FOLDING; TRIACYLGLYCEROL BLOOD LEVEL;

AICAR; AMP; AMP KINASE; AMP-ACTIVATED KINASE (AMPK); ENERGY METABOLISM; FAT METABOLISM; IN VIVO; LIVER METABOLISM;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ENERGY METABOLISM; FATTY ACIDS; GLUCOSE; HYPOGLYCEMIC AGENTS; LIVER; MICE; MICE, KNOCKOUT; MITOCHONDRIA, LIVER; OXIDATIVE PHOSPHORYLATION; RIBONUCLEOTIDES; TRIGLYCERIDES;

EID: 84896826866     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.528232     Document Type: Article

References (63)

1. Wasserman, D. H. (2009) Four grams of glucose. Am. J. Physiol. Endocrinol. Metab. 296, E11-E21
2. Hu, F. B. (2011) Globalization of diabetes. The role of diet, lifestyle, and genes. Diabetes Care 34, 1249-1257
3. Kahn, B. B., Alquier, T., Carling, D., and Hardie, D. G. (2005) AMP-activated protein kinase. Ancient energy gauge provides clues into modern understanding of metabolism. Cell Metab. 1, 15-25 (Pubitemid 43960587)
4. Oakhill, J. S., Scott, J. W., and Kemp, B. E. (2012) AMPK functions as an adenylate charge-regulated protein kinase. Trends Endocrinol. Metab. 23, 125-132
5. Shaw, R. J., Lamia, K. A., Vasquez, D., Koo, S. H., Bardeesy, N., Depinho, R. A., Montminy, M., and Cantley, L. C. (2005) The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 310, 1642-1646 (Pubitemid 41780780)
6. Miller, R. A., Chu, Q., Xie, J., Foretz, M., Viollet, B., and Birnbaum, M. J. (2013) Biguanides suppress hepatic glucagon signaling by decreasing production of cyclic AMP. Nature 494, 256-260
7. Miller, R. A., Chu, Q., Le Lay, J., Scherer, P. E., Ahima, R. S., Kaestner, K. H., Foretz, M., Viollet, B., and Birnbaum, M. J. (2011) Adiponectin suppresses gluconeogenic gene expression in mouse hepatocytes independent of LKB1-AMPK signaling. J. Clin. Invest. 121, 2518-2528
8. Foretz, M., Hébrard, S., Leclerc, J., Zarrinpashneh, E., Soty, M., Mithieux, G., Sakamoto, K., Andreelli, F., and Viollet, B. (2010) Metformin inhibits hepatic gluconeogenesis in mice independently of LKB1/AMPK pathway via a decrease in hepatic energy state. J. Clin. Invest. 120, 2355-2369
9. Berglund, E. D., Lustig, D. G., Baheza, R. A., Hasenour, C. M., Lee-Young, R. S., Donahue, E. P., Lynes, S. E., Swift, L. L., Charron, M. J., Damon, B. M., and Wasserman, D. H. (2011) Hepatic glucagon action is essential for exercise-induced reversal of mouse fatty liver. Diabetes 60, 2720-2729
10. Berglund, E. D., Lee-Young, R. S., Lustig, D. G., Lynes, S. E., Donahue, E. P., Camacho, R. C., Meredith, M. E., Magnuson, M. A., Charron, M. J., and Wasserman, D. H. (2009) Hepatic energy state is regulated by glucagon receptor signaling in mice. J. Clin. Invest. 119, 2412-2422
11. Camacho, R. C., Donahue, E. P., James, F. D., Berglund, E. D., and Wasserman, D. H. (2006) Energy state of the liver during short-term and exhaustive exercise in C57BL/6J mice. Am. J. Physiol. Endocrinol. Metab. 290, E405-E408 (Pubitemid 43671684)
12. Yamauchi, T., Nio, Y., Maki, T., Kobayashi, M., Takazawa, T., Iwabu, M., Okada-Iwabu, M., Kawamoto, S., Kubota, N., Kubota, T., Ito, Y., Kamon, J., Tsuchida, A., Kumagai, K., Kozono, H., Hada, Y., Ogata, H., Tokuyama, K., Tsunoda, M., Ide, T., Murakami, K., Awazawa, M., Takamoto, I., Froguel, P., Hara, K., Tobe, K., Nagai, R., Ueki, K., and Kadowaki, T. (2007) Targeted disruption of AdipoR1 and AdipoR2 causes abrogation of adiponectin binding and metabolic actions. Nat. Med. 13, 332-339 (Pubitemid 46376688)
13. Kimball, S. R., Siegfried, B. A., and Jefferson, L. S. (2004) Glucagon represses signaling through the mammalian target of rapamycin in rat liver by activating AMP-activated protein kinase. J. Biol. Chem. 279, 54103-54109 (Pubitemid 40053145)
14. Foretz, M., Carling, D., Guichard, C., Ferré, P., and Foufelle, F. (1998) AMP-activated protein kinase inhibits the glucose-activated expression of fatty acid synthase gene in rat hepatocytes. J. Biol. Chem. 273, 14767-14771 (Pubitemid 28272762)
15. Hasenour, C. M., Berglund, E. D., and Wasserman, D. H. (2013) Emerging role of AMP-activated protein kinase in endocrine control of metabolism in the liver. Mol. Cell. Endocrinol. 366, 152-162
16. Guigas, B., Taleux, N., Foretz, M., Detaille, D., Andreelli, F., Viollet, B., and Hue, L. (2007) AMP-activated protein kinase-independent inhibition of hepatic mitochondrial oxidative phosphorylation by AICA riboside. Biochem. J. 404, 499-507 (Pubitemid 46953924)
17. Foretz, M., Ancellin, N., Andreelli, F., Saintillan, Y., Grondin, P., Kahn, A., Thorens, B., Vaulont, S., and Viollet, B. (2005) Short-term overexpression of a constitutively active form of AMP-activated protein kinase in the liver leads to mild hypoglycemia and fatty liver. Diabetes 54, 1331-1339 (Pubitemid 40586661)
18. Cool, B., Zinker, B., Chiou, W., Kifle, L., Cao, N., Perham, M., Dickinson, R., Adler, A., Gagne, G., Iyengar, R., Zhao, G., Marsh, K., Kym, P., Jung, P., Camp, H. S., and Frevert, E. (2006) Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab. 3, 403-416 (Pubitemid 43811782)
19. Iglesias, M. A., Ye, J. M., Frangioudakis, G., Saha, A. K., Tomas, E., Ruderman, N. B., Cooney, G. J., and Kraegen, E. W. (2002) AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat fed rats. Diabetes 51, 2886-2894
20. Song, X. M., Fiedler, M., Galuska, D., Ryder, J. W., Fernström, M., Chibalin, A. V., Wallberg-Henriksson, H., and Zierath, J. R. (2002) 5-Aminoimi-dazole-4-carboxamide ribonucleoside treatment improves glucose homeostasis in insulin-resistant diabetic (ob/ob) mice. Diabetologia 45, 56-65 (Pubitemid 34118543)
21. Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., Musi, N., Hirshman, M. F., Goodyear, L. J., and Moller, D. E. (2001) Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108, 1167-1174 (Pubitemid 32995375)
22. Ayala, J. E., Bracy, D. P., McGuinness, O. P., and Wasserman, D. H. (2006) Considerations in the design of hyperinsulinemic-euglycemic clamps in the conscious mouse. Diabetes 55, 390-397 (Pubitemid 43343268)
23. Kang, L., Ayala, J. E., Lee-Young, R. S., Zhang, Z., James, F. D., Neufer, P. D., Pozzi, A., Zutter, M. M., and Wasserman, D. H. (2011) Diet-induced muscle insulin resistance is associated with extracellular matrix remodeling and interaction with integrin α2β1 in mice. Diabetes 60, 416-426
24. Bergeron, R., Previs, S. F., Cline, G. W., Perret, P., Russell, R. R., 3rd, Young, L. H., and Shulman, G. I. (2001) Effect of 5-aminoimidazole-4- carboxamide-1-β-D-ribofuranoside infusion on in vivo glucose and lipid metabolism in lean and obese Zucker rats. Diabetes 50, 1076-1082 (Pubitemid 32374538)
25. Bergeron, R., Russell, R. R., 3rd, Young, L. H., Ren, J. M., Marcucci, M., Lee, A., and Shulman, G. I. (1999) Effect ofAMPKactivation on muscle glucose metabolism in conscious rats. Am. J. Physiol. 276, E938-E944 (Pubitemid 29249614)
26. Morgan, C. R., and Lazarow, A. (1965) Immunoassay of pancreatic and plasma insulin following alloxan injection of rats. Diabetes 14, 669-671
27. Steele, R., Wall, J. S., De Bodo, R. C., and Altszuler, N. (1956) Measurement of the size and turnover rate of body glucose pool by the isotope dilution method. Am. J. Physiol. 187, 15-24
28. Romestaing, C., Piquet, M. A., Letexier, D., Rey, B., Mourier, A., Servais, S., Belouze, M., Rouleau, V., Dautresme, M., Ollivier, I., Favier, R., Rigoulet, M., Duchamp, C., and Sibille, B. (2008) Mitochondrial adaptations to steatohepatitis induced by a methionine- and choline-deficient diet. Am. J. Physiol. Endocrinol. Metab. 294, E110-E119
29. Hughey, C. C., Hittel, D. S., Johnsen, V. L., and Shearer, J. (2011) Respirometric oxidative phosphorylation assessment in saponin-permeabilized cardiac fibers. J. Vis. Exp. 48, 2431
30. Velasco, G., Geelen, M. J., and Guzmán, M. (1997) Control of hepatic fatty acid oxidation by 5 -AMP-activated protein kinase involves a malonyl-CoA-dependent and a malonyl-CoA-independent mechanism. Arch. Biochem. Biophys. 337, 169-175 (Pubitemid 27198179)
31. Corton, J. M., Gillespie, J. G., Hawley, S. A., and Hardie, D. G. (1995) 5-Aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229, 558-565
32. Holland, W. L., Miller, R. A., Wang, Z. V., Sun, K., Barth, B. M., Bui, H. H., Davis, K. E., Bikman, B. T., Halberg, N., Rutkowski, J. M., Wade, M. R., Tenorio, V. M., Kuo, M. S., Brozinick, J. T., Zhang, B. B., Birnbaum, M. J., Summers, S. A., and Scherer, P. E. (2011) Receptor-mediated activation of ceramidase activity initiates the pleiotropic actions of adiponectin. Nat. Med. 17, 55-63
33. Kim, Y. D., Park, K. G., Lee, Y. S., Park, Y. Y., Kim, D. K., Nedumaran, B., Jang, W. G., Cho, W. J., Ha, J., Lee, I. K., Lee, C. H., and Choi, H. S. (2008) Metformin inhibits hepatic gluconeogenesis through AMP-activated protein kinase-dependent regulation of the orphan nuclear receptor SHP. Diabetes 57, 306-314
34. Iglesias, M. A., Furler, S. M., Cooney, G. J., Kraegen, E. W., and Ye, J. M. (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, 1649-1654 (Pubitemid 38857020)
35. Buhl, E. S., Jessen, N., Pold, R., Ledet, T., Flyvbjerg, A., Pedersen, S. B., Pedersen, O., Schmitz, O., and Lund, S. (2002) Long-term AICAR administration reduces metabolic disturbances and lowers blood pressure in rats displaying features of the insulin resistance syndrome. Diabetes 51, 2199-2206 (Pubitemid 34729025)
36. Fryer, L. G., Parbu-Patel, A., and Carling, D. (2002) The Anti-diabetic drugs rosiglitazone and metformin stimulate AMP-activated protein kinase through distinct signaling pathways. J. Biol. Chem. 277, 25226-25232 (Pubitemid 34951829)
37. Vincent, M. F., Erion, M. D., Gruber, H. E., and Van den Berghe, G. (1996) Hypoglycaemic effect of AICAriboside in mice. Diabetologia 39, 1148-1155 (Pubitemid 26319937)
38. Vincent, M. F., Marangos, P. J., Gruber, H. E., and Van den Berghe, G. (1991) Inhibition by AICA riboside of gluconeogenesis in isolated rat hepatocytes. Diabetes 40, 1259-1266
39. Mihaylova, M. M., Vasquez, D. S., Ravnskjaer, K., Denechaud, P. D., Yu, R. T., Alvarez, J. G., Downes, M., Evans, R. M., Montminy, M., and Shaw, R. J. (2011) Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145, 607- 621
40. Shirai, T., Inoue, E., Ishimi, Y., and Yamauchi, J. (2011) AICAR response element binding protein (AREBP), a key modulator of hepatic glucose production regulated by AMPK in vivo. Biochem. Biophys. Res. Commun. 414, 287-291
41. Chanda, D., Kim, S. J., Lee, I. K., Shong, M., and Choi, H. S. (2008) Sodium arsenite induces orphan nuclear receptor SHP gene expression via AMPactivated protein kinase to inhibit gluconeogenic enzyme gene expression. Am. J. Physiol. Endocrinol. Metab. 295, E368-E379
42. Koo, S. H., Flechner, L., Qi, L., Zhang, X., Screaton, R. A., Jeffries, S., Hedrick, S., Xu, W., Boussouar, F., Brindle, P., Takemori, H., and Montminy, M. (2005) The CREB coactivator TORC2 is a key regulator of fasting glucose metabolism. Nature 437, 1109-1111
43. Yamauchi, T., Kamon, J., Minokoshi, Y., Ito, Y., Waki, H., Uchida, S., Yamashita, S., Noda, M., Kita, S., Ueki, K., Eto, K., Akanuma, Y., Froguel, P., Foufelle, F., Ferre, P., Carling, D., Kimura, S., Nagai, R., Kahn, B. B., and Kadowaki, T. (2002) Adiponectin stimulates glucose utilization and fattyacid oxidation by activating AMP-activated protein kinase. Nat. Med. 8, 1288-1295 (Pubitemid 35373562)
44. Lochhead, P. A., Salt, I. P., Walker, K. S., Hardie, D. G., and Sutherland, C. (2000) 5-Aminoimidazole-4-carboxamide riboside mimics the effects of insulin on the expression of the 2 key gluconeogenic genes PEPCK and glucose-6-phosphatase. Diabetes 49, 896-903 (Pubitemid 30349410)
45. Andreelli, F., Foretz, M., Knauf, C., Cani, P. D., Perrin, C., Iglesias, M. A., Pillot, B., Bado, A., Tronche, F., Mithieux, G., Vaulont, S., Burcelin, R., and Viollet, B. (2006) Liver adenosine monophosphate-activated kinase-α2 catalytic subunit is a key target for the control of hepatic glucose production by adiponectin and leptin but not insulin. Endocrinology 147, 2432-2441
46. Krebs, H. (1964) The Croonian Lecture, 1963. Gluconeogenesis. Proc. R. Soc. Lond. B. Biol. Sci. 159, 545-564
47. Atkinson, D. E. (1968) The energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochemistry 7, 4030-4034
48. Longuet, C., Sinclair, E. M., Maida, A., Baggio, L. L., Maziarz, M., Charron, M. J., and Drucker, D. J. (2008) The glucagon receptor is required for the adaptive metabolic response to fasting. Cell Metab. 8, 359-371
49. Brunmair, B., Staniek, K., Gras, F., Scharf, N., Althaym, A., Clara, R., Roden, M., Gnaiger, E., Nohl, H., Waldhäusl, W., and Fürnsinn, C. (2004) Thiazolidinediones, like metformin, inhibit respiratory complex I. A common mechanism contributing to their antidiabetic actions? Diabetes 53, 1052-1059 (Pubitemid 38436618)
50. El-Mir, M. Y., Nogueira, V., Fontaine, E., Avéret, N., Rigoulet, M., and Leverve, X. (2000) Dimethylbiguanide inhibits cell respiration via an indirect effect targeted on the respiratory chain complex I. J. Biol. Chem. 275, 223-228 (Pubitemid 30038975)
51. Taketa, K., and Pogell, B. M. (1965) Allosteric inhibition of rat liver fructose 1,6-diphosphatase by adenosine 5 -monophosphate. J. Biol. Chem. 240, 651-662
52. Pencek, R. R., Shearer, J., Camacho, R. C., James, F. D., Lacy, D. B., Fueger, P. T., Donahue, E. P., Snead, W., and Wasserman, D. H. (2005) 5-Aminoimidazole-4-carboxamide-1-β-D-ribofuranoside causes acute hepatic insulin resistance in vivo. Diabetes 54, 355-360
53. Wasserman, D. H., and Cherrington, A. D. (1991) Hepatic fuel metabolism during muscular work. Role and regulation. Am. J. Physiol. 260, E811-E824
54. Miller, R. A., and Birnbaum, M. J. (2010) An energetic tale of AMPK-independent effects of metformin. J. Clin. Invest. 120, 2267-2270
55. Vincent, M. F., Bontemps, F., and Van den Berghe, G. (1992) Inhibition of glycolysis by 5-amino-4-imidazolecarboxamide riboside in isolated rat hepatocytes. Biochem. J. 281, 267-272
56. Mukhtar, M. H., Payne, V. A., Arden, C., Harbottle, A., Khan, S., Lange, A. J., and Agius, L. (2008) Inhibition of glucokinase translocation by AMP-activated protein kinase is associated with phosphorylation of both GKRP and 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase. Am. J. Physiol. Regul. Integr. Comp. Physiol. 294, R766-R774 (Pubitemid 351346952)
57. Guigas, B., Bertrand, L., Taleux, N., Foretz, M., Wiernsperger, N., Vertommen, D., Andreelli, F., Viollet, B., and Hue, L. (2006) 5-Aminoimidazole-4-carboxamide-1-β-D-ribofuranoside and metformin inhibit hepatic glucose phosphorylation by an AMP-activated protein kinase-independent effect on glucokinase translocation. Diabetes 55, 865-874 (Pubitemid 44100158)
58. Hunter, R. W., Treebak, J. T., Wojtaszewski, J. F., and Sakamoto, K. (2011) Molecular mechanism by which AMP-activated protein kinase activation promotes glycogen accumulation in muscle. Diabetes 60, 766-774
59. García-Villafranca, J., Guillén, A., and Castro, J. (2008) Ethanol consumption impairs regulation of fatty acid metabolism by decreasing the activity of AMP-activated protein kinase in rat liver. Biochimie 90, 460-466 (Pubitemid 351232118)
60. Muoio, D. M., Seefeld, K., Witters, L. A., and Coleman, R. A. (1999) AMP-activated kinase reciprocally regulates triacylglycerol synthesis and fatty acid oxidation in liver and muscle. Evidence that sn-glycerol-3-phosphate acyltransferase is a novel target. Biochem. J. 338, 783-791 (Pubitemid 29140087)
61. Li, Y., Xu, S., Mihaylova, M. M., Zheng, B., Hou, X., Jiang, B., Park, O., Luo, Z., Lefai, E., Shyy, J. Y., Gao, B., Wierzbicki, M., Verbeuren, T. J., Shaw, R. J., Cohen, R. A., and Zang, M. (2011) AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in dietinduced insulin-resistant mice. Cell Metab. 13, 376-388
62. Carling, D., Zammit, V. A., and Hardie, D. G. (1987) A common bicyclic protein kinase cascade inactivates the regulatory enzymes of fatty acid and cholesterol biosynthesis. FEBS Lett. 223, 217-222
63. Hardie, D. G., and Hawley, S. A. (2001) AMP-activated protein kinase. The energy charge hypothesis revisited. Bioessays 23, 1112-1119