AICAR treatment for 14 days normalizes obesity-induced dysregulation of TORC1 signaling and translational capacity in fasted skeletal muscle

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 299, Issue 6, 2010, Pages

  Drake, Joshua C ^a   Alway, Stephen E ^a   Hollander, John M ^a   Williamson, David L ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

AMP activated kinase; Eukaryotic initiation factor 4G; Mammalian target of rapamycin; ob ob

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ACETYL COCARBOXYLASE; COCARBOXYLASE; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INITIATION FACTOR 4F; INSULIN; MAMMALIAN TARGET OF RAPAMYCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR; TRANSDUCER OF REGULATED CAMP RESPONSE ELEMENT 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET RESTRICTION; GENE CONTROL; MALE; MOUSE; MUSCLE MASS; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RNA ANALYSIS; RNA TRANSLATION; SKELETAL MUSCLE; WEIGHT CHANGE;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANALYSIS OF VARIANCE; ANIMALS; BLOOD GLUCOSE; BLOTTING, WESTERN; EUKARYOTIC INITIATION FACTOR-4G; IMMUNOPRECIPITATION; INSULIN; MALE; MICE; MICE, OBESE; MUSCLE, SKELETAL; OBESITY; PHOSPHORYLATION; PROTEIN BIOSYNTHESIS; RIBONUCLEOTIDES; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 78649814492     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00337.2010     Document Type: Article

References (65)

1. Aguilar V, Alliouachene S, Sotiropoulos A, Sobering A, Athea Y, Djouadi F, Miraux S, Thiaudiere E, Foretz M, Voillet B, Diolez P, Bastin J, Benit P, Rustin P, Carling D, Sandri M, Ventura-Clapier R, Pende M. S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab 5: 476-487, 2007. (Pubitemid 46825498)
2. Alley DE, Chang VW. The changing relationship of obesity and disability, 1988-2004. JAMA 298: 2020-2027, 2007.
3. Augert G, Van de Werve G, Le Marchand-Brustel Y. Effect of work-induced hypertrophy on muscle glucose metabolism in lean and obese mice. Diabetologia 28: 295-301, 1985.
4. Benton CR, Han XX, Febbraio M, Graham TE, Bonen A. Inverse relationship between PGC-1α protein expression and triacylglycerol accumulation in rodent skeletal muscle. J Appl Physiol 100: 377-383, 2006.
5. Bentzinger CF, Romanino K, Cloetta D, Lin S, Mascarenhas JB, Oliveri F, Xia J, Casanova E, Costa CF, Brink M, Zorzato F, Hall MN, Ruegg MA. Skeletal muscle-specific ablation of raptor, but not of rictor, causes metabolic changes and results in muscle dystrophy. Cell Metab 8: 411-424, 2008.
6. Beretta L, Gingras AC, Svitkin YV, Hall MN, Sonenberg N. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J 15: 658-664, 1996.
7. Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. AMP-activated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J Biol Chem 277: 23977-23980, 2002.
8. Bolster DR, Kubica N, Crozier SJ, Williamson DL, Farrell PA, Kimball SR, Jefferson LS. Immediate response of mammalian target of rapamycin (mTOR)-mediated signalling following acute resistance exercise in rat skeletal muscle. J Physiol 553: 213-220, 2003. (Pubitemid 37483929)
9. Bolster DR, Vary TC, Kimball SR, Jefferson LS. Leucine regulates translation initiation in rat skeletal muscle via enhanced eIF4G phosphorylation. J Nutr 134: 1704-1710, 2004.
10. Burnett PE, Barrow RK, Cohen NA, Snyder SH, Sabatini DM. RAFT1 phosphorylation of the translational regulators p70 S6 kinase and 4E-BP1. Proc Natl Acad Sci USA 95: 1432-1437, 1998.
11. Campion DR, Purchas RW, Merkel RA, Romsos DR. Genetic obesity and the muscle satellite cell. Proc Soc Exp Biol Med 176: 143-147, 1984.
12. Chang GR, Chiu YS, Wu YY, Chen WY, Liao JW, Chao TH, Mao FC. Rapamycin protects against high fat diet-induced obesity in C57BL/6J mice. J Pharm Sci 109: 496-503, 2009.
13. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N. Dissecting the role of mTOR: lessons from mTOR inhibitors. Biochim Biophys Acta 1804: 433-439.
14. Durschlag RP, Layman DK. Skeletal muscle growth in lean and obese Zucker rats. Growth 47: 282-291, 1983.
15. Fluckey JD, Pohnert SC, Boyd SG, Cortright RN, Trappe TA, Dohm GL. Insulin stimulation of muscle protein synthesis in obese Zucker rats is not via a rapamycin-sensitive pathway. Am J Physiol Endocrinol Metab 279: E182-E187, 2000.
16. Gautsch TA, Anthony JC, Kimball SR, Paul GL, Layman DK, Jefferson LS. Availability of eIF-4E regulates skeletal muscle protein synthesis during recovery from exercise. Am J Physiol Cell Physiol 274: C406-C414, 1998.
17. Glazer HP, Osipov RM, Clements RT, Sellke FW, Bianchi C. Hypercholesterolemia is associated with hyperactive cardiac mTORC1 and mTORC2 signaling. Cell Cycle 8: 1738-1746, 2009.
18. Halseth AE, Ensor NJ, White TA, Ross SA, Gulve EA. Acute and chronic treatment of ob/ob and db/db mice with AICAR decreases blood glucose concentrations. Biochem Biophys Res Commun 294: 798-805, 2002.
19. Hardie DG. The AMP-activated protein kinase cascade: the key sensor of cellular energy status. Endocrinology 144: 5179-5183, 2003.
20. Hardie DG, Pan DA. Regulation of fatty acid synthesis and oxidation by the AMP-activated protein kinase. Biochem Soc Trans 30: 1064-1070, 2002. (Pubitemid 36002407)
21. Herbert TP, Tee AR, Proud CG. The extracellular signal-regulated kinase pathway regulates the phosphorylation of 4E-BP1 at multiple sites. J Biol Chem 277: 11591-11596, 2002.
22. Holz MK, Ballif BA, Gygi SP, Blenis J. mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123: 569-580, 2005.
23. Iglesias MA, Ye JM, Frangioudakis G, Saha AK, Tomas E, Ruderman NB, Cooney GJ, Kraegen EW. AICAR administration causes an apparent enhancement of muscle and liver insulin action in insulin-resistant high-fat-fed rats. Diabetes 51: 2886-2894, 2002.
24. Inoki K, Li Y, Zhu T, Wu J, Guan KL. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signalling. Nat Cell Biol 4: 648-657, 2002.
25. Kelly FJ, Jefferson LS. Control of peptide-chain initiation in rat skeletal muscle. Development of methods for preparation of native ribosomal subunits and analysis of the effect of insulin on formation of 40S initiation complexes. J Biol Chem 260: 6677-6683, 1985.
26. Kemp JG, Blazev R, Stephenson DG, Stephenson GM. Morphological and biochemical alterations of skeletal muscles from the genetically obese (ob/ob) mouse. Int J Obes (Lond) 33: 831-841, 2009.
27. Khamzina L, Veilleux A, Bergeron S, Marette A. Increased activation of the mammalian target of rapamycin pathway in liver and skeletal muscle of obese rats: possible involvement in obesity-linked insulin resistance. Endocrinology 146: 1473-1481, 2005.
28. Kim DH, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument- Bromage H, Tempst P, Sabatini DM. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110: 163-175, 2002.
29. Kubica N, Bolster DR, Farrell PA, Kimball SR, Jefferson LS. Resistance exercise increases muscle protein synthesis and translation of eukaryotic initiation factor 2Bε mRNA in a mammalian target of rapamycin-dependent manner. J Biol Chem 280: 7570-7580, 2005.
30. Kumar V, Pandey P, Sabatini D, Kumar M, Majumder PK, Bharti A, Carmichael G, Kufe D, Kharbanda S. Functional interaction between RAFT1/FRAP/mTOR and protein kinase Cδ in the regulation of cap-dependent initiation of translation. EMBO J 19: 1087-1097, 2000. (Pubitemid 30119833)
31. Lang CH. Elevated plasma free fatty acids decrease basal protein synthesis, but not the anabolic effect of leucine, in skeletal muscle. Am J Physiol Endocrinol Metab 291: E666-E674, 2006.
32. Le Bacquer O, Petroulakis E, Paglialunga S, Poulin F, Richard D, Cianflone K, Sonenberg N. Elevated sensitivity to diet-induced obesity and insulin resistance in mice lacking 4E-BP1 and 4E-BP2. J Clin Invest 117: 387-396, 2007.
33. Lindstrom P. The physiology of obese-hyperglycemic mice [ob/ob mice]. Sci World J 7: 666-685, 2007.
34. Mayer J, Russell RE, Bates MW, Dickie MM. Metabolic, nutritional and endocrine studies of the hereditary obesity-diabetes syndrome of mice and mechanism of its development. Metabolism 2: 9-21, 1953.
35. Merrick WC, Hershey JWB. The pathway and mechanism of eukaryotic protein synthesis. In: Translational Control, edited by Hershey JWB, Mathews MB, Sonenberg N. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 1996, p. 31-69.
36. Miller AM, Brestoff JR, Phelps CB, Berk EZ, Reynolds TH. Rapamycin does not improve insulin sensitivity despite elevated mammalian target of rapamycin complex 1 activity in muscles of ob/ob mice. Am J Physiol Regul Integr Comp Physiol 295: R1431-R1438, 2008.
37. Ohne Y, Takahara T, Maeda T. Evaluation of mTOR function by a gain-of-function approach. Cell Cycle 8: 573-579, 2009.
38. Peterson JM, Bryner RW, Alway SE. Satellite cell proliferation is reduced in muscles of obese Zucker rats but restored with loading. Am J Physiol Cell Physiol 295: C521-C528, 2008.
39. Pold R, Jensen LS, Jessen N, Buhl ES, Schmitz O, Flyvbjerg A, Fujii N, Goodyear LJ, Gotfredsen CF, Brand CL, Lund S. Long-term AICAR administration and exercise prevents diabetes in ZDF rats. Diabetes 54: 928-934, 2005.
40. Purchas RW, Romsos DR, Allen RE, Merkel RA. Muscle growth and satellite cell proliferative activity in obese (ob/ob) mice. J Anim Sci 60: 644-651, 1985.
41. Pyronnet S, Dostie J, Sonenberg N. Suppression of cap-dependent translation in mitosis. Genes Dev 15: 2083-2093, 2001.
42. Pyronnet S, Imataka H, Gingras A, Fukunaga R, Hunter T, Sonenberg N. Human eukaryotic translation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E. EMBO J 18: 270-279, 1999.
43. Reynolds TH, Cinquino N, Anthony M, Phelps CB, Berk EZ. Insulin resistance without elevated mammalian target of rapamycin complex 1 activity in muscles of mice fed a high-fat diet. J Appl Physiol 107: 1479-1485, 2009.
44. Rivas DA, Yaspelkis BB, 3rd Hawley JA, Lessard SJ. Lipid-induced mTOR activation in rat skeletal muscle reversed by exercise and 5′- aminoimidazole-4-carboxamide-1β-D-ribofuranoside. J Endocrinol 202: 441-451, 2009.
45. Rolland Y, Lauwers-Cances V, Cristini C, Abellan van Kan G, Janssen I, Morley JE, Vellas B. Difficulties with physical function associated with obesity, sarcopenia, and sarcopenic-obesity in community-dwelling elderly women: the EPIDOS (EPIDemiologie de l'OSteoporose) Study. Am J Clin Nutr 89: 1895-1900, 2009.
46. Sarbassov DD, Ali SM, Sengupta S, Sheen JH, Hsu PP, Bagley AF, Markhard AL, Sabatini DM. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22: 159-168, 2006.
47. Shapira JF, Kircher I, Martin RJ. Indices of skeletal muscle growth in lean and obese Zucker rats. J Nutr 110: 1313-1318, 1980.
48. Shargill NS, Ohshima K, Bray GA, Chan TM. Muscle protein turnover in the perfused hindquarters of lean and genetically obese-diabetic (db/db) mice. Diabetes 33: 1160-1164, 1984. (Pubitemid 15176848)
49. Sitnick M, Bodine SC, Rutledge JC. Chronic high fat feeding attenuates load-induced hypertrophy in mice. J Physiol 587: 5753-5765, 2009.
50. Song XM, Fiedler M, Galuska D, Ryder JW, Fernstrom M, Chibalin AV, Wallberg-Henrikssen H, Zierath JR. 5-Aminoimidazole-4-carboxamide ribonucleoside treatment improves glucose homeostasis in insulin-resistant diabetic (ob/ob) mice. Diabetologia 45: 56-65, 2002.
51. Sparrow MP, Earl CA, Laurent GL, Everett AW. Turnover rates of muscle proteins in cardiac, skeletal, and smooth muscle: turnover rate related to muscle function. Recent Adv Stud Card Struct Metab 12: 29-34, 1976.
52. Stallone G, Infante B, Grandaliano G, Gesualdo L. Management of side effects of sirolimus therapy. Transplantation 87: S23-S26, 2009.
53. Stenholm S, Harris TB, Rantanen T, Visser M, Kritchevsky SB, Ferrucci L. Sarcopenic obesity: definition, cause and consequences. Curr Opin Clin Nutr Metab Care 11: 693-700, 2008.
54. Svanberg E, Jefferson LS, Lundholm K, Kimball SR. Postprandial stimulation of muscle protein synthesis is independent of changes in insulin. Am J Physiol Endocrinol Metab 272: E841-E847, 1997.
55. Svanberg E, Zachrisson H, Ohlsson C, Iresjo BM. Role of insulin and IGF-I in activation of muscle protein synthesis after oral feeding. Am J Physiol Endocrinol Metab 270: E614-E620, 1996.
56. Takano A, Usui I, Haruta T, Kawahara J, Uno T, Iwata M, Kobayashi M. Mammalian target of rapamycin pathway regulates insulin signaling via subcellular redistribution of insulin receptor substrate 1 and integrates nutritional signals and metabolic signals of insulin. Mol Cell Biol 21: 5050-5062, 2001.
57. Tremblay F, Gagnon A, Veilleux A, Sorisky A, Marette A. Activation of the mammalian target of rapamycin pathway acutely inhibits insulin signaling to Akt and glucose transport in 3T3 - L1 and human adipocytes. Endocrinology 146: 1328-1337, 2005.
58. Trostler N, Amin R, Shafrir E. Increased protease activity in muscles of obese (ob/ob) mice. Int J Obes 6: 557-566, 1982.
59. Tsika RW, Herrick RE, Baldwin KM. Time course adaptations in rat skeletal muscle isomyosins during compensatory growth and regression. J Appl Physiol 63: 2111-2121, 1987.
60. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G. Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431: 200-205, 2004.
61. von Manteuffel SR, Dennis PB, Pullen N, Gingras AC, Sonenberg N, Thomas G. The insulin-induced signalling pathway leading to S6 and initiation factor 4E binding protein 1 phosphorylation bifurcates at a rapamycin-sensitive point immediately upstream of p70s6k. Mol Cell Biol 17: 5426-5436, 1997.
62. Williamson DL, Bolster DR, Kimball SR, Jefferson LS. Time course changes in signaling pathways and protein synthesis in C2C12 myotubes following AMPK activation by AICAR. Am J Physiol Endocrinol Metab 291: E80-E89, 2006.
63. Williamson DL, Butler DC, Alway SE. AMPK inhibits myoblast differentiation through a PGC-1α-dependent mechanism. Am J Physiol Endocrinol Metab 297: E304-E314, 2009.
64. Williamson DL, Kubica N, Kimball SR, Jefferson LS. Exercise-induced alterations in extracellular signal-regulated kinases 1/2 and mammalian target of rapamycin (mTOR) to regulatory mechanisms of mRNA translation in mouse muscle. J Physiol 573: 497-510, 2006. (Pubitemid 43871062)
65. Williamson DL, Raue U, Slivka DR, Trappe S. Resistance exercise, skeletal muscle FOXO3A, and 85-year-old women. J Gerontol A Biol Sci Med Sci 65: 335-343, 2010.