Altered REDD1, myostatin, and Akt/mTOR/FoxO/MAPK signaling in streptozotocin-induced diabetic muscle atrophy

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 3, 2012, Pages 307-315

  Hulmi, Juha J ^a   Silvennoinen, Mika ^a   Lehti, Maarit ^b   Kivelä, Riikka ^a,c   Kainulainen, Heikki ^a  

^a UNIVERSITY OF JYVÄSKYLÄ   (Finland)

^b LIKES RESEARCH CENTER FOR SPORT AND HEALTH SCIENCES   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

Diabetes; Gene expression; Insulin; Myostatin; REDD1; Skeletal muscles

Indexed keywords

ADENOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MYOSTATIN; PROTEIN KINASE B; PROTEIN REDD1; REPRESSOR PROTEIN; STREPTOZOCIN; TRANSCRIPTION FACTOR FOXO; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC MUSCLE ATROPHY; DNA DAMAGE; DNA REPAIR; GASTROCNEMIUS MUSCLE; GENE EXPRESSION; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MICROARRAY ANALYSIS; MOUSE; MUSCLE ATROPHY; MUSCLE MASS; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; SIGNAL TRANSDUCTION; STREPTOZOCIN DIABETES; UBIQUITINATION; UNINDEXED SEQUENCE; WESTERN BLOTTING;

ANIMALS; DIABETES MELLITUS, TYPE 1; DNA REPAIR ENZYMES; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; MALE; MAP KINASE SIGNALING SYSTEM; MICE; MUSCLE, SKELETAL; MUSCULAR ATROPHY; MYOSTATIN; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SIZE; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RANDOM ALLOCATION; RNA, MESSENGER; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTORS; UBIQUITINATION;

EID: 84856166319     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00398.2011     Document Type: Article

References (52)

1. Aragno M, Mastrocola R, Catalano MG, Brignardello E, Danni O, Boccuzzi G. Oxidative stress impairs skeletal muscle repair in diabetic rats. Diabetes 53: 1082-1088, 2004.
2. Bodine SC, Stitt TN, Gonzalez M, Kline WO, Stover GL, Bauerlein R, Zlotchenko E, Scrimgeour A, Lawrence JC, Glass DJ, Yancopoulos GD. Akt/mTOR pathway is a crucial regulator of skeletal muscle hypertrophy and can prevent muscle atrophy in vivo. Nat Cell Biol 3: 1014-1019, 2001.
3. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, Witters LA, Ellisen LW, Kaelin WG Jr. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 18: 23: 2893-2904, 2004.
4. Burgering BM, Kops GJ. Cell cycle and death control: long live Forkheads. Trends Biochem Sci 27: 352-360, 2002.
5. Burkart V, Wang ZQ, Radons J, Heller B, Herceg Z, Stingl L, Wagner EF, Kolb H. Mice lacking the poly(ADP-ribose) polymerase gene are resistant to pancreatic beta-cell destruction and diabetes development induced by streptozocin. Nat Med 5: 314-319, 1999.
6. Dandona P, Thusu K, Cook S, Snyder B, Makowski J, Armstrong D, Nicotera T. Oxidative damage to DNA in diabetes mellitus. Lancet 347: 444-445, 1996.
7. Dominguez C, Ruiz E, Gussinye M, Carrascosa A. Oxidative stress at onset and in early stages of type 1 diabetes in children and adolescents. Diabetes Care 21: 1736-1742, 1998.
8. Ekladous D, Mehdi MZ, Costa M, Srivastava AK, Chiasson JL, Coderre L. Tissue- and fibre-specific modifications of insulin-signalling molecules in cardiac and skeletal muscle of diabetic rats. Clin Exp Pharmacol Physiol 35: 971-978, 2008.
9. Ellisen LW, Ramsayer KD, Johannessen CM, Yang A, Beppu H, Minda K, Oliner JD, McKeon F, Haber DA. REDD1, a developmentally regulated transcriptional target of p63 and p53, links p63 to regulation of reactive oxygen species. Mol Cell 10: 995-1005, 2002.
10. Favier FB, Costes F, Defour A, Bonnefoy R, Lefai E, Bauge S, Peinnequin A, Benoit H, Freyssenet D. Downregulation of Akt/mammalian target of rapamycin pathway in skeletal muscle is associated with increased REDD1 expression in response to chronic hypoxia. Am J Physiol Regul Integr Comp Physiol 298: R1659-R1666, 2010.
11. Fewell JG, Moerland TS. Responses of mouse fast and slow skeletal muscle to streptozotocin diabetes: myosin isoenzymes and phosphorous metabolites. Mol Cell Biochem 148: 147-154, 1995.
12. Flaim KE, Copenhaver ME, Jefferson LS. Effects of diabetes on protein synthesis in fast- and slow-twitch rat skeletal muscle. Am J Physiol Endocrinol Metab 239: E88-E95, 1980.
13. Frost RA, Huber D, Pruznak A, Lang CH. Regulation of REDD1 by insulin-like growth factor-I in skeletal muscle and myotubes. J Cell Biochem 108: 1192-1202, 2009.
14. Goodarzi MT, Navidi AA, Rezaei M, Babahmadi-Rezaei H. Oxidative damage to DNA and lipids: correlation with protein glycation in patients with type 1 diabetes. J Clin Lab Anal 24: 72-76, 2010.
15. Gordon CS, Serino AS, Krause MP, Campbell JE, Cafarelli E, Adegoke OA, Hawke TJ, Riddell MC. Impaired growth and force production in skeletal muscles of young partially pancreatectomized rats: a model of adolescent type 1 diabetic myopathy? PLoS One 5: e14032, 2010.
16. Hardie DG. New roles for the LKB1->AMPK pathway. Curr Opin Cell Biol 17: 167-173, 2005.
17. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG. Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 271: 27879-27887, 1996.
18. Hulmi JJ, Tannerstedt J, Selänne H, Kainulainen H, Kovanen V, Mero AA. Resistance exercise with whey protein ingestion affects mTOR signaling pathway and myostatin in men. J Appl Physiol 106: 1720-1729, 2009.
19. Hulmi JJ, Walker S, Ahtiainen JP, Nyman K, Kraemer WJ, Häkkinen K. Molecular signaling in muscle is affected by the specificity of resistance exercise protocol. Scand J Med Sci Sports 2010. Sep 9. doi: 10.1111/j.1600-0838.2010.01198.x. [Epub ahead of print].
20. Ishii S, Kamegai J, Tamura H, Shimizu T, Sugihara H, Oikawa S. Role of ghrelin in streptozotocin-induced diabetic hyperphagia. Endocrinology 143: 4934-4937, 2002.
21. Jakobsen J, Reske-Nielsen E. Diffuse muscle fiber atrophy in newly diagnosed diabetes. Clin Neuropathol 5: 73-77, 1986.
22. Johnston AP, Campbell JE, Found JG, Riddell MC, Hawke TJ. Streptozotocin induces G2 arrest in skeletal muscle myoblasts and impairs muscle growth in vivo. Am J Physiol Cell Physiol 292: C1033-C1040, 2007.
23. Kimball SR, Jefferson LS. New functions for amino acids: effects on gene transcription and translation. Am J Clin Nutr 83: 500S-507S, 2006.
24. Kimball SR, Jefferson LS, Fadden P, Haystead TA, Lawrence JC Jr. Insulin and diabetes cause reciprocal changes in the association of eIF-4E and PHAS-I in rat skeletal muscle. Am J Physiol Cell Physiol 270: C705-C709, 1996.
25. Kivelä R, Silvennoinen M, Touvra AM, Lehti TM, Kainulainen H, Vihko V. Effects of experimental type 1 diabetes and exercise training on angiogenic gene expression and capillarization in skeletal muscle. FASEB J 20: 1570-1572, 2006.
26. +/- and streptozotocininduced Type 1 diabetic models. J Appl Physiol 106: 1650-1659, 2009.
27. Kraynak AR, Storer RD, Jensen RD, Kloss MW, Soper KA, Clair JH, DeLuca JG, Nichols WW, Eydelloth RS. Extent and persistence of streptozotocin-induced DNA damage and cell proliferation in rat kidney as determined by in vivo alkaline elution and BrdUrd labeling assays. Toxicol Appl Pharmacol 135: 279-286, 1995.
28. Lecker SH, Solomon V, Price SR, Kwon YT, Mitch WE, Goldberg AL. Ubiquitin conjugation by the N-end rule pathway and mRNAs for its components increase in muscles of diabetic rats. J Clin Invest 104: 1411-1420, 1999.
29. Lehti TM, Silvennoinen M, Kivelä R, Kainulainen H, Komulainen J. Effects of streptozotocin-induced diabetes and physical training on gene expression of extracellular matrix proteins in mouse skeletal muscle. Am J Physiol Endocrinol Metab 290: E900-E907, 2006.
30. Mas A, Montane J, Anguela XM, Munoz S, Douar AM, Riu E, Otaegui P, Bosch F. Reversal of type 1 diabetes by engineering a glucose sensor in skeletal muscle. Diabetes 55: 1546-1553, 2006.
31. McGhee NK, Jefferson LS, Kimball SR. Elevated corticosterone associated with food deprivation upregulates expression in rat skeletal muscle of the mTORC1 repressor, REDD1. J Nutr 139: 828-834, 2009.
32. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-beta superfamily member. Nature 387: 83-90, 1997.
33. Pain VM, Albertse EC, Garlick PJ. Protein metabolism in skeletal muscle, diaphragm, and heart of diabetic rats. Am J Physiol Endocrinol Metab 245: E604-E610, 1983.
34. Proud CG. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403: 217-234, 2007.
35. Proud CG. Regulation of protein synthesis by insulin. Biochem Soc Trans 34: 213-216, 2006.
36. Ramm G, Larance M, Guilhaus M, James DE. A role for 14-3-3 in insulin-stimulated GLUT4 translocation through its interaction with the RabGAP AS160. J Biol Chem 281: 29174-29180, 2006.
37. Regazzetti C, Bost F, Le Marchand-Brustel Y, Tanti JF, nd Giorgetti-Peraldi S. Insulin induces REDD1 expression through hypoxia-inducible factor 1 activation in adipocytes. J Biol Chem 285: 5157-5164, 2010.
38. Reisz-Porszasz S, Bhasin S, Artaza JN, Shen R, Sinha-Hikim I, Hogue A, Fielder TJ, Gonzalez-Cadavid NF. Lower skeletal muscle mass in male transgenic mice with muscle-specific overexpression of myostatin. Am J Physiol Endocrinol Metab 285: E876-E888, 2003.
39. Riddell MC, Iscoe KE. Physical activity, sport, and pediatric diabetes. Pediatr Diabetes 7: 60-70, 2006.
40. Riu E, Mas A, Ferre T, Pujol A, Gros L, Otaegui P, Montoliu L, Bosch F. Counteraction of type 1 diabetic alterations by engineering skeletal muscle to produce insulin: insights from transgenic mice. Diabetes 51: 704-711, 2002.
41. Rodgers BD, Strack AM, Dallman MF, Hwa L, Nicoll CS. Corticosterone regulation of insulin-like growth factor I, IGF-binding proteins, and growth in streptozotocin-induced diabetic rats. Diabetes 44: 1420-1425, 1995.
42. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307: 1098-1101, 2005.
43. Shoshani T, Faerman A, Mett I, Zelin E, Tenne T, Gorodin S, Moshel Y, Elbaz S, Budanov A, Chajut A, Kalinski H, Kamer I, Rozen A, Mor O, Keshet E, Leshkowitz D, Einat P, Skaliter R, Feinstein E. Identification of a novel hypoxia-inducible factor 1-responsive gene, RTP801, involved in apoptosis. Mol Cell Biol 22: 2283-2293, 2002.
44. Sofer A, Lei K, Johannessen CM, Ellisen LW. Regulation of mTOR and cell growth in response to energy stress by REDD1. Mol Cell Biol 25: 5834-5845, 2005.
45. Takasu N, Komiya I, Asawa T, Nagasawa Y, Yamada T. Streptozocinand alloxan-induced H2O2 generation and DNA fragmentation in pancreatic islets. H2O2 as mediator for DNA fragmentation. Diabetes 40: 1141-1145, 1991.
46. Trendelenburg AU, Meyer A, Rohner D, Boyle J, Hatakeyama S, Glass DJ. Myostatin reduces Akt/TORC1/p70S6K signaling, inhibiting myoblast differentiation and myotube size. Am J Physiol Cell Physiol 296: C1258-C1270, 2009.
47. Unterman TG, Jentel JJ, Oehler DT, Lacson RG, Hofert JF. Effects of glucocorticoids on circulating levels and hepatic expression of insulin-like growth factor (IGF)-binding proteins and IGF-I in the adrenalectomized streptozotocin-diabetic rat. Endocrinology 133: 2531-2539, 1993.
48. Welle S, Burgess K, Thornton CA, Tawil R. Relation between extent of myostatin depletion and muscle growth in mature mice. Am J Physiol Endocrinol Metab 297: E935-E940, 2009.
49. Whitney ML, Jefferson LS, Kimball SR. ATF4 is necessary and sufficient for ER stress-induced upregulation of REDD1 expression. Biochem Biophys Res Commun 379: 451-455, 2009.
50. Wieteska-Skrzeczynska W, Grzelkowska-Kowalczyk K, Jank M, Maciejewski H. Transcriptional dysregulation of skeletal muscle protein metabolism in streptozotocin-diabetic mice. J Physiol Pharmacol 60, Suppl 1: 29-36, 2009.
51. 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.
52. 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.