AMP-activated protein kinase enhances the expression of muscle-specific ubiquitin ligases despite its activation of IGF-1/Akt signaling in C2C12 myotubes

Journal of Cellular Biochemistry

Volumn 108, Issue 2, 2009, Pages 458-468

  Tong, Jun F ^a   Yan, Xu ^a   Zhu, Mei J ^a   Du, Min ^a  

^a UNIVERSITY OF WYOMING   (United States)

Author keywords

AMP activated protein kinase; C2C12; FoxO; Insulin like growth factor 1; Protein degradation; Skeletal muscle; Ubiquitin ligase

Indexed keywords

ATROGIN 1; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MUSCLE RING FINGER 1 PROTEIN; PROTEIN KINASE B; SOMATOMEDIN C; TRANSCRIPTION FACTOR FKHRL1; UBIQUITIN PROTEIN LIGASE;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; ENZYME ACTIVATION; ENZYME INHIBITION; MOUSE; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ACETYL-COA CARBOXYLASE; ADENOSINE MONOPHOSPHATE; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CARRIER PROTEINS; CELL DIFFERENTIATION; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; INSULIN-LIKE GROWTH FACTOR I; MICE; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; MUSCLE, SKELETAL; PHOSPHOPROTEIN PHOSPHATASES; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; RIBONUCLEOSIDES; SIGNAL TRANSDUCTION; SIROLIMUS; SKP CULLIN F-BOX PROTEIN LIGASES; UBIQUITIN-PROTEIN LIGASES;

EID: 70349253984     PISSN: 07302312     EISSN: 10974644     Source Type: Journal    
DOI: 10.1002/jcb.22272     Document Type: Article

References (53)

1. Aguilar V, Alliouachene S, Sotiropoulos A, Sobering A, Athea Y, Djouadi F, Miraux S, Thiaudiere E, Foretz M, Viollet B, Diolez P, Bastin J, Benit P, Rustin P, Carling D, Sandri M, Ventura-Clapier R, Pende M. 2007. S6 kinase deletion suppresses muscle growth adaptations to nutrient availability by activating AMP kinase. Cell Metab 5:476-487. (Pubitemid 46825498)
2. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA. 1996. Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15:6541-6551. (Pubitemid 26413787)
3. Andjelkovic M, Jakubowicz T, Cron P, Ming XF, Han JW, Hemmings BA. 1996. Activation and phosphorylation of a pleckstrin homology domain containing protein kinase (RAC-PK/PKB) promoted by serum and protein phosphatase inhibitors. Proc Natl Acad Sci USA 93:5699-5704. (Pubitemid 26190743)
4. Barthel A, Schmoll D, Kruger KD, Roth RA, Joost HG. 2002. Regulation of the forkhead transcription factor FKHR (FOXO1a) by glucose starvation and AICAR, an activator of AMP-activated protein kinase. Endocrinology 143:3183-3186. (Pubitemid 34809893)
5. Bodine SC, Latres E, Baumhueter S, Lai VK, Nunez L, Clarke BA, Poueymirou WT, Panaro FJ, Na E, Dharmarajan K, Pan ZQ, Valenzuela DM, DeChiara TM, Stitt TN, Yancopoulos GD, Glass DJ. 2001. Identification of ubiquitin ligases required for skeletal muscle atrophy. Science 294:1704-1708. (Pubitemid 33104839)
6. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96:857-868. (Pubitemid 29165088)
7. Calnan DR, Brunet A. 2008. The FoxO code. Oncogene 27:2276-2288.
8. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J. 2009. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458:1056-1060.
9. Chan AY, Dyck JR. 2005. Activation of AMP-activated protein kinase (AMPK) inhibits protein synthesis: A potential strategy to prevent the development of cardiac hypertrophy. Can J Physiol Pharmacol 83:24-28.
10. Cross DA, Alessi DR, Cohen P, Andjelkovich M, Hemmings BA. 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378:785-789. (Pubitemid 26004411)
11. Doucet M, Russell AP, Leger B, Debigare R, Joanisse DR, Caron MA, LeBlanc P, Maltais F. 2007. Muscle atrophy and hypertrophy signaling in patients with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 176:261-269. (Pubitemid 47195876)
12. Du M, Shen QW, Zhu MJ, Ford SP. 2007. Leucine stimulates mammalian target of rapamycin signaling in C2C12 myoblasts in part through inhibition of adenosine monophosphate-activated protein kinase. J Anim Sci 85:919-927. (Pubitemid 46651831)
13. Engelman JA, Luo J, Cantley LC. 2006. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat Rev Genet 7:606-619. (Pubitemid 44100518)
14. Glass DJ. 2003. Signalling pathways that mediate skeletal muscle hypertrophy and atrophy. Nat Cell Biol 5:87-90.
15. Glass DJ. 2005. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem Cell Biol 37:1974-1984. (Pubitemid 41206815)
16. Greer EL, Oskoui PR, Banko MR, Maniar JM, Gygi MP, Gygi SP, Brunet A. 2007. The energy sensor AMP-activated protein kinase directly regulates the mammalian FOXO3 transcription factor. J Biol Chem 282:30107-30119. (Pubitemid 350035296)
17. Hardie DG. 2008. AMPK: A key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 32(Suppl 4): S7-S12.
18. Hay N, Sonenberg N. 2004. Upstream and downstream of mTOR. Genes Dev 18:1926-1945.
19. Hershko A, Ciechanover A. 1998. The ubiquitin system. Annu Rev Biochem 67:425-479.
20. Inoki K, Zhu T, Guan KL. 2003. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577-590. (Pubitemid 37506046)
21. Jagoe RT, Goldberg AL. 2001. What do we really know about the ubiquitin-proteasome pathway in muscle atrophy? Curr Opin Clin Nutr Metab Care 4:183-190.
22. Jakobsen SN, Hardie DG, Morrice N, Tornqvist HE. 2001. 5′-AMP-activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J Biol Chem 276:46912-46916. (Pubitemid 37373061)
23. Kido Y, Nakae J, Accili D. 2001. Clinical review 125: The insulin receptor and its cellular targets. J Clin Endocrinol Metab 86:972-979. (Pubitemid 32322967)
24. Kim JK, Fillmore JJ, Sunshine MJ, Albrecht B, Higashimori T, Kim DW, Liu ZX, Soos TJ, Cline GW, O'Brien WR, Littman DR, Shulman GI. 2004. PKC-theta knockout mice are protected from fat-induced insulin resistance. J Clin Invest 114:823-827. (Pubitemid 39578741)
25. Krawiec BJ, Nystrom GJ, Frost RA, Jefferson LS, Lang CH. 2007. AMP-activated protein kinase agonists increase mRNA content of the muscle-specific ubiquitin ligases MAFbx and MuRF1 in C2C12 cells. Am J Physiol Endocrinol Metab 292:E1555-E1567.
26. Lai KM, Gonzalez M, Poueymirou WT, Kline WO, Na E, Zlotchenko E, Stitt TN, Economides AN, Yancopoulos GD, Glass DJ. 2004. Conditional activation of akt in adult skeletal muscle induces rapid hypertrophy. Mol Cell Biol 24:9295-9304. (Pubitemid 39391668)
27. Latres E, Amini AR, Amini AA, Griffiths J, Martin FJ, Wei Y, Lin HC, Yancopoulos GD, Glass DJ. 2005. Insulin-like growth factor-1 (IGF-1) inversely regulates atrophy-induced genes via the phosphatidylinositol 3-kinase/Akt/mammalian target of rapamycin (PI3K/Akt/mTOR) pathway. J Biol Chem 280:2737-2744. (Pubitemid 40189380)
28. Lecker SH, Goldberg AL, Mitch WE. 2006. Protein degradation by the ubiquitin-proteasome pathway in normal and disease states. J Am Soc Nephrol 17:1807-1819. (Pubitemid 44036165)
29. Lin CF, Chen CL, Chiang CW, Jan MS, Huang WC, Lin YS. 2007. GSK-3beta acts downstream of PP2A and the PI 3-kinase-Akt pathway, and upstream of caspase-2 in ceramide-induced mitochondrial apoptosis. J Cell Sci 120:2935-2943.
30. Lopez JM, Santidrian AF, Campas C, Gil J. 2003. 5-Aminoimidazole-4- carboxamide riboside induces apoptosis in Jurkat cells, but the AMP-activated protein kinase is not involved. Biochem J 370:1027-1032. (Pubitemid 36399097)
31. Matsuzaki H, Daitoku H, Hatta M, Tanaka K, Fukamizu A. 2003. Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Proc Natl Acad Sci USA 100:11285-11290. (Pubitemid 37205927)
32. McClung JM, Kavazis AN, Whidden MA, DeRuisseau KC, Falk DJ, Criswell DS, Powers SK. 2007. Antioxidant administration attenuates mechanical ventilation-induced rat diaphragm muscle atrophy independent of protein kinase B (PKB Akt) signalling. J Physiol 585:203-215.
33. McKinnell IW, Rudnicki MA. 2004. Molecular mechanisms of muscle atrophy. Cell 119:907-910.
34. Mitch WE, Goldberg AL. 1996. Mechanisms of muscle wasting. The role of the ubiquitin-proteasome pathway. N Engl J Med 335:1897-1905.
35. Nakae J, Kitamura T, Ogawa W, Kasuga M, Accili D. 2001. Insulin regulation of gene expression through the forkhead transcription factor Foxo1 (Fkhr) requires kinases distinct from Akt. Biochemistry 40:11768-11776. (Pubitemid 32906038)
36. Nakashima K, Yakabe Y. 2007. AMPK activation stimulates myofibrillar protein degradation and expression of atrophy-related ubiquitin ligases by increasing FOXO transcription factors in C2C12 myotubes. Biosci Biotechnol Biochem 71:1650-1656. (Pubitemid 47358716)
37. Nystrom GJ, Lang CH. 2008. Sepsis and AMPK activation by AICAR differentially regulate FoxO-1, -3 and -4 mRNA in striated muscle. Int J Clin Exp Med 1:50-63.
38. Oldham S, Hafen E. 2003. Insulin/IGF and target of rapamycin signaling: A TOR de force in growth control. Trends Cell Biol 13:79-85. (Pubitemid 36135889)
39. O'Reilly KE, Rojo F, She QB, Solit D, Mills GB, Smith D, Lane H, Hofmann F, Hicklin DJ, Ludwig DL, Baselga J, Rosen N. 2006. mTOR inhibition induces upstream receptor tyrosine kinase signaling and activates Akt. Cancer Res 66:1500-1508. (Pubitemid 43259931)
40. Reiter AK, Bolster DR, Crozier SJ, Kimball SR, Jefferson LS. 2005. Repression of protein synthesis and mTOR signaling in rat liver mediated by the AMPK activator aminoimidazole carboxamide ribonucleoside. Am J Physiol Endocrinol Metab 288:E980-E988.
41. Sakoda H, Ogihara T, Anai M, Fujishiro M, Ono H, Onishi Y, Katagiri H, Abe M, Fukushima Y, Shojima N, Inukai K, Kikuchi M, Oka Y, Asano T. 2002. Activation of AMPK is essential for AICAR-induced glucose uptake by skeletal muscle but not adipocytes. Am J Physiol Endocrinol Metab 282:E1239-E1244. (Pubitemid 34654692)
42. Sandri M, Sandri C, Gilbert A, Skurk C, Calabria E, Picard A, Walsh K, Schiaffino S, Lecker SH, Goldberg AL. 2004. Foxo transcription factors induce the atrophy-related ubiquitin ligase atrogin-1 and cause skeletal muscle atrophy. Cell 117:399-412. (Pubitemid 38534545)
43. Skurk C, Izumiya Y, Maatz H, Razeghi P, Shiojima I, Sandri M, Sato K, Zeng L, Schiekofer S, Pimentel D, Lecker S, Taegtmeyer H, Goldberg AL, Walsh K. 2005. The FOXO3a transcription factor regulates cardiac myocyte size downstream of AKT signaling. J Biol Chem 280:20814-20823. (Pubitemid 40776786)
44. Stein SC, Woods A, Jones NA, Davison MD, Carling D. 2000. The regulation of AMP-activated protein kinase by phosphorylation. Biochem J 345(Pt 3):437-443. (Pubitemid 30099070)
45. Stitt TN, Drujan D, Clarke BA, Panaro F, Timofeyva Y, Kline WO, Gonzalez M, Yancopoulos GD, Glass DJ. 2004. The IGF-1/PI3K/Akt pathway prevents expression of muscle atrophy-induced ubiquitin ligases by inhibiting FOXO transcription factors. Mol Cell 14:395-403. (Pubitemid 38591410)
46. Tesseraud S, Metayer-Coustard S, Boussaid S, Crochet S, Audouin E, Derouet M, Seiliez I. 2007. Insulin and amino acid availability regulate atrogin-1 in avian QT6 cells. Biochem Biophys Res Commun 357:181-186. (Pubitemid 46584647)
47. Towler MC, Hardie DG. 2007. AMP-activated protein kinase in metabolic control and insulin signaling. Circ Res 100:328-341. (Pubitemid 46272405)
48. Wan X, Harkavy B, Shen N, Grohar P, Helman LJ. 2007. Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene 26:1932-1940. (Pubitemid 46474636)
49. Wang X, Hu Z, Hu J, Du J, Mitch WE. 2006. Insulin resistance accelerates muscle protein degradation: Activation of the ubiquitin-proteasome pathway by defects in muscle cell signaling. Endocrinology 147:4160-4168. (Pubitemid 44268367)
50. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D. 2005. Ca2+/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2:21-33. (Pubitemid 43239822)
51. Wray CJ, Mammen JM, Hershko DD, Hasselgren PO. 2003. Sepsis upregulates the gene expression of multiple ubiquitin ligases in skeletal muscle. Int J Biochem Cell Biol 35:698-705.
52. Wullschleger S, Loewith R, Hall MN. 2006. TOR signaling in growth and metabolism. Cell 124:471-484.
53. Zhu MJ, Ford SP, Means WJ, Hess BW, Nathanielsz PW, Du M. 2006. Maternal nutrient restriction affects properties of skeletal muscle in offspring. J Physiol 575:241-250. (Pubitemid 44178141)