Chronic activation of mTOR complex 1 by branched chain amino acids and organ hypertrophy

Amino Acids

Volumn 47, Issue 6, 2015, Pages 1167-1182

  Neishabouri, S Hallaj ^a   Hutson, S M ^b   Davoodi, J ^a,b  

^a UNIVERSITY OF TEHRAN   (Iran)

^b VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

Branched chain amino acids; Branched chain aminotransferase; mTORC1 signaling; Organ hypertrophy

Indexed keywords

AMINOTRANSFERASE; BRANCHED CHAIN AMINO ACID; MECHANISTIC TARGET OF RAPAMYCIN COMPLEX 1; MULTIPROTEIN COMPLEX; RAPAMYCIN; TARGET OF RAPAMYCIN KINASE;

ANIMAL; CARDIOMEGALY; CHEMICALLY INDUCED; GENETICS; KIDNEY DISEASE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; RAT; SPLENOMEGALY;

AMINO ACIDS, BRANCHED-CHAIN; ANIMALS; CARDIOMEGALY; KIDNEY DISEASES; MICE, KNOCKOUT; MULTIPROTEIN COMPLEXES; RATS; SIROLIMUS; SPLENOMEGALY; TOR SERINE-THREONINE KINASES; TRANSAMINASES;

EID: 84939986849     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-015-1944-y     Document Type: Article

References (67)

1. Abhari BA, Davoodi J (2008) A mechanistic insight into SMAC peptide interference with XIAP-Bir2 inhibition of executioner caspases. J Mol Biol 381(3):645-654. doi: 10.1016/j.jmb.2008.05.082
2. Ananieva EA, Patel CH, Drake CH, Powell JD, Hutson SM (2014) Cytosolic branched chain aminotransferase (BCATc) regulates mTORC1 signaling and glycolytic metabolism in CD4+ T cells. J Biol Chem 289(27):18793-18804. doi: 10.1074/jbc.M114.554113
3. Anthony JC, Anthony TG, Kimball SR, Vary TC, Jefferson LS (2000) Orally administered leucine stimulates protein synthesis in skeletal muscle of postabsorptive rats in association with increase eIF4F formation. J Nutr 130:139-145
4. Anthony TG, Anthony JC, Yoshizawa SR, Kimball SR, Jefferson LS (2001) Oral administration of leucine stimulates ribosomal protein mRNA translation but not global rates of protein synthesis in the liver of rats. J Nutr 131:1171-1176
5. Bixel MG, Hutson SM, Hamprecht B (1997) Cellular distribution of branched-chain amino acid aminotransferase isoenzymes among rat brain glial cells in culture. J Histochem Cytochem 45(5):685-694
6. Bruey JM, Ducasse C, Bonniaud P, Ravagnan L, Susin SA, Diaz-Latoud C, Gurbuxani S, Arrigo AP, Kroemer G, Solary E, Garrido C (2000) Hsp27 negatively regulates cell death by interacting with cytochrome c. Nat Cell Biol 2(9):645-652. doi: 10.1038/35023595
7. Cairns RA, Harris IS, Mak TW (2011) Regulation of cancer cell metabolism. Nat Rev Cancer 11(2):85-95. doi: 10.1038/nrc2981
8. Castellano S, Casarosa S, Sweatt AJ, Hutson SM, Bozzi Y (2007) Expression of cytosolic branched chain aminotransferase (BCATc) mRNA in the developing mouse brain. Gene Expr Patterns: GEP 7(4):485-490. doi: 10.1016/j.modgep.2006.10.010
9. Cen O, Longnecker R (2011) Rapamycin reverses splenomegaly and inhibits tumor development in a transgenic model of Epstein-Barr virus-related Burkitt's lymphoma. Mol Cancer Ther 10(4):679-686. doi: 10.1158/1535-7163.MCT-10-0833
10. Chiu MI, Katz H, Berlin V (1994) RAPT1, a mammalian homolog of yeast Tor, interacts with the FKBP12/rapamycin complex. Proc Natl Acad Sci USA 91(26):12574-12578
11. Choo AY, Blenis J (2009) Not all substrates are treated equally: implications for mTOR, rapamycin-resistance and cancer therapy. Cell Cycle 8(4):567-572
12. Choo AY, Yoon SO, Kim SG, Roux PP, Blenis J (2008) Rapamycin differentially inhibits S6Ks and 4E-BP1 to mediate cell-type-specific repression of mRNA translation. Proc Natl Acad Sci USA 105(45):17414-17419. doi: 10.1073/pnas.0809136105
13. Chou SD, Prince T, Gong J, Calderwood SK (2012) mTOR is essential for the proteotoxic stress response, HSF1 activation and heat shock protein synthesis. PLoS One 7(6):e39679. doi: 10.1371/journal.pone.0039679
14. Conway ME, Hutson SM (2000) Mammalian branched-chain aminotransferases. Methods Enzymol 324:355-365
15. Dann SG, Selvaraj A, Thomas G (2007) mTOR complex1-S6K1 signaling: at the crossroads of obesity, diabetes and cancer. Trends Mol Med 13:252-259
16. Davoodi J, Drown PM, Bledsoe RK, Wallin R, Reinhart GD, Hutson SM (1998) Overexpression and characterization of the human mitochondrial and cytosolic branched-chain aminotransferases. J Biol Chem 273(9):4982-4989
17. Gao XM, Wong G, Wang B, Kiriazis H, Moore XL, Su YD, Dart A, Du XJ (2006) Inhibition of mTOR reduces chronic pressure-overload cardiac hypertrophy and fibrosis. J Hypertens 24(8):1663-1670. doi: 10.1097/01.hjh.0000239304.01496.83
18. Garber AJ, Karl IE, Kipnis DM (1976) Alanine and glutamine synthesis and release from skeletal muscle. II. The precursor role of amino acids in alanine and glutamine synthesis. J Biol Chem 251(3):836-843
19. Ge Y, Chen J (2012) Mammalian target of rapamycin (mTOR) signaling network in skeletal myogenesis. J Biol Chem 287(52):43928-43935. doi: 10.1074/jbc.R112.406942
20. Gera JF, Mellinghoff IK, Shi Y, Rettig MB, Tran C, Hsu JH, Sawyers CL, Lichtenstein AK (2004) AKT activity determines sensitivity to mammalian target of rapamycin (mTOR) inhibitors by regulating cyclin D1 and c-myc expression. J Biol Chem 279(4):2737-2746. doi: 10.1074/jbc.M309999200
21. Gielchinsky Y, Laufer N, Weitman E, Abramovitch R, Granot Z, Bergman Y, Pikarsky E (2010) Pregnancy restores the regenerative capacity of the aged liver via activation of an mTORC1-controlled hyperplasia/hypertrophy switch. Genes Dev 24(6):543-548. doi: 10.1101/gad.563110
22. Gray S, Wang B, Orihuela Y, Hong E-G, Fisch S, Haldar S, Cline GW, Kim JK, Peroni OD, Kahn BB, Jain MK (2007) Regulation of gluconeogenesis by Kruppel-like factor 15. Cell Metab 5:305-312
23. 2+/CaM signaling to hVps34. Cell Metab 7(5):456-465. doi: 10.1016/j.cmet.2008.03.002
24. Harrison DE, Strong R, Sharp ZD, Nelson JF, Astle CM, Flurkey K, Nadon NL, Wilkinson JE, Frenkel K, Carter CS, Pahor M, Javors MA, Fernandez E, Miller RA (2009) Rapamycin fed late in life extends lifespan in genetically heterogeneous mice. Nature 460(7253):392-395. doi: 10.1038/nature08221
25. Haymond MW, Miles JM (1982) Branched chain amino acids as a major source of alanine nitrogen in man. Diabetes 31(1):86-89
26. Howatson G, Hoad M, Goodall S, Tallent J, Bell PG, French DN (2012) Exercise-induced muscle damage is reduced in resistance-trained males by branched chain amino acids: a randomized, double-blind, placebo controlled study. J Int Soc Sports Nutr 9:20. doi: 10.1186/1550-2783-9-20
27. Hutson SM, Harper AE (1981) Blood and tissue branched-chain amino and alpha-keto acid concentrations: effect of diet, starvation, and disease. Am J Clin Nutr 34(2):173-183
28. Hutson SM, Cree TC, Harper AE (1978) Regulation of leucine and alpha-ketoisocaproate metabolism in skeletal muscle. J Biol Chem 253(22):8126-8133
29. Hutson SM, Wallin R, Hall TR (1992) Identification of mitochondrial branched chain aminotransferase and its isoforms in rat tissues. J Biol Chem 267(22):15681-15686
30. Hutson SM, Bledsoe RK, Hall TR, Dawson PA (1995) Cloning and expression of the mammalian cytosolic branched chain aminotransferase isoenzyme. J Biol Chem 270(51):30344-30352
31. Hutson SM, Sweatt AJ, Lanoue KF (2005) Branched-chain amino acid metabolism: implications for establishing safe intakes. J Nutr 135(6 Suppl):1557S-1564S
32. Ichihara A, Koyama E (1966) Transaminase of branched chain amino acids. I. Branched chain amino acids-alpha-ketoglutarate transaminase. J Biochem 59(2):160-169
33. Jefferies HB, Fumagalli S, Dennis PB, Reinhard C, Pearson RB, Thomas G (1997) Rapamycin suppresses 5′TOP mRNA translation through inhibition of p70s6k. EMBO J 16(12):3693-3704. doi: 10.1093/emboj/16.12.3693
34. Jewell JL, Russell RC, Guan KL (2013) Amino acid signalling upstream of mTOR. Nat Rev Mol Cell Biol 14(3):133-139. doi: 10.1038/nrm3522
35. Kawaguchi T, Shiraishi K, Ito T, Suzuki K, Koreeda C, Ohtake T, Iwasa M, Tokumoto Y, Endo R, Kawamura NH, Shiraki M, Habu D, Tsuruta S, Miwa Y, Kawaguchi A, Kakuma T, Sakai H, Kawada N, Hanai T, Takahashi SI, Kato A, Onji M, Takei Y, Kohgo Y, Seki T, Tamano M, Katayama K, Mine T, Sata M, Moriwaki H, Suzuki K (2013) Branched-chain amino acids prevent hepatocarcinogenesis and prolong survival of patients with cirrhosis. Clin Gastroenterol Hepatol Off Clin Prac J Am Gastroenterol Assoc. doi: 10.1016/j.cgh.2013.08.050
36. Kimball SR, Jefferson LS (2006) Signaling pathways and molecular mechanisms through which branched-chain amino acids mediate translational control of protein synthesis. J Nutr 136(1 Suppl):227S-231S
37. Kimball SR, Jefferson LS, Nguyen HV, Suryawan A, Bush JA, Davis TA (2000) Feeding stimulates protein synthesis in muscle and liver of neonatal pigs through an mTOR-dependent process. Am J Physiol Endocrinol Metab 279(5):E1080-E1087
38. Kolwicz SC Jr, Tian R (2011) Glucose metabolism and cardiac hypertrophy. Cardiovasc Res 90(2):194-201. doi: 10.1093/cvr/cvr071
39. 2+ influx and protein synthesis to improve skeletal muscle function. J Biol Chem 289(37):25556-25570. doi: 10.1074/jbc.M114.586289
40. Li C, Najafi H, Daikhin Y, Nissim IB, Collins HW, Yudkoff M, Matschinsky FM, Stanley CA (2003) Regulation of leucine-stimulated insulin secretion and glutamine metabolism in isolated rat islets. J Biol Chem 278:2853-2858
41. Liu Q, Chang JW, Wang J, Kang SA, Thoreen CC, Markhard A, Hur W, Zhang J, Sim T, Sabatini DM, Gray NS (2010) Discovery of 1-(4-(4-propionylpiperazin-1-yl)-3-(trifluoromethyl)phenyl)-9-(quinolin-3-yl)benz o[h][1,6]naphthyridin-2(1H)-one as a highly potent, selective mammalian target of rapamycin (mTOR) inhibitor for the treatment of cancer. J Med Chem 53(19):7146-7155. doi: 10.1021/jm101144f
42. Lo YC, Lee CF, Powell JD (2014) Insight into the role of mTOR and metabolism in T cells reveals new potential approaches to preventing graft rejection. Curr Opin Organ Transplant 19(4):363-371. doi: 10.1097/MOT.0000000000000098
43. Longo KA, Charoenthongtrakul S, Giuliana DJ, Govek EK, McDonagh T, Distefano PS, Geddes BJ (2010) The 24-hour respiratory quotient predicts energy intake and changes in body mass. Am J Physiol Regul Integr Comp Physiol 298(3):R747-R754. doi: 10.1152/ajpregu.00476.2009
44. Lynch CJ, Hutson SM, Patson BJ, Vaval A, Vary TC (2002) Tissue-specific effects of chronic dietary leucine and norleucine supplementation on protein synthesis in rats. Am J Physiol Endocrinol Metab 283:E824-E835
45. Malaisse WJ, Sener A, Malaisse-Lagae F, Welsh M, Matthews DE, Bier DM, Hellerstrom C (1982) The stimulus-secretion coupling of amino acid-induced insulin release. Metabolic response of pancreatic islets of l-glutamine and l-leucine. J Biol Chem 257(15):8731-8737
46. Martin TD, Chen XW, Kaplan RE, Saltiel AR, Walker CL, Reiner DJ, Der CJ (2014) Ral and Rheb GTPase activating proteins integrate mTOR and GTPase signaling in aging, autophagy, and tumor cell invasion. Mol Cell 53(2):209-220. doi: 10.1016/j.molcel.2013.12.004
47. McMullen JR, Sherwood MC, Tarnavski O, Zhang L, Dorfman AL, Shioi T, Izumo S (2004) Inhibition of mTOR signaling with rapamycin regresses established cardiac hypertrophy induced by pressure overload. Circulation 109(24):3050-3055. doi: 10.1161/01.CIR.0000130641.08705.45
48. Muelly ER, Moore GJ, Bunce SC, Mack J, Bigler DC, Morton DH, Strauss KA (2013) Biochemical correlates of neuropsychiatric illness in maple syrup urine disease. J Clin Invest 123(4):1809-1820. doi: 10.1172/JCI67217
49. Putinski C, Abdul-Ghani M, Stiles R, Brunette S, Dick SA, Fernando P, Megeney LA (2013) Intrinsic-mediated caspase activation is essential for cardiomyocyte hypertrophy. Proc Natl Acad Sci USA 110(43):E4079-E4087. doi: 10.1073/pnas.1315587110
50. Reiter AK, Anthony TG, Anthony JC, Jefferson LS, Kimball SR (2004) The mTOR signaling pathway mediates control of ribosomal protein mRNA translation in rat liver. Int J Biochem Cell Biol 36(11):2169-2179
51. Segawa H, Fukasawa Y, Miyamoto K, Takeda E, Endou H, Kanai Y (1999) Identification and functional characterization of a Na+-independent neutral amino acid transporter with broad substrate selectivity. J Biol Chem 274(28):19745-19751
52. She P, Reid TM, Janket M, Bronson SK, Hutson SM, Lynch CJ (2006) Enhanced energy expenditure, insulin sensitivity and resistance to diet induced obesity in mice lacking BCATm. Diabetes 55S:A391
53. She P, Reid TM, Bronson SK, Vary TC, Hajnal A, Lynch CJ, Hutson SM (2007) Disruption of BCATm in mice leads to increased energy expenditure associated with the activation of a futile protein turnover cycle. Cell Metab 6:181-194
54. Shimobayashi M, Hall MN (2014) Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat Rev Mol Cell Biol 15(3):155-162. doi: 10.1038/nrm3757
55. Sr K, Lm S, Rl H, Ls J (1999) Leucine regulates translation of specific mRNAs in L6 myoblasts through mTOR-mediated changes in availability of eIF4E and phosphorylation of ribosomal protein S6. J Biol Chem 274(17):11647-11652
56. Suryawan A, Hawes JW, Harris RA, Shimomura Y, Jenkins AE, Hutson SM (1998) A molecular model of human branched-chain amino acid metabolism. Am J Clin Nutr 68(1):72-81
57. Takeshita Y, Takamura T, Kita Y, Ando H, Ueda T, Kato K, Misu H, Sunagozaka H, Sakai Y, Yamashita T, Mizukoshi E, Honda M, Kaneko S (2012) Beneficial effect of branched-chain amino acid supplementation on glycemic control in chronic hepatitis C patients with insulin resistance: implications for type 2 diabetes. Metabolism 61(10):1388-1394. doi: 10.1016/j.metabol.2012.03.011
58. Thalacker-Mercer AE, Petrella JK, Bamman MM (2009) Does habitual dietary intake influence myofiber hypertrophy in response to resistance training? A cluster analysis. Appl Physiol Nutr Metab 34(4):632-639. doi: 10.1139/H09-038
59. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, Reichling LJ, Sim T, Sabatini DM, Gray NS (2009) An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 284(12):8023-8032. doi: 10.1074/jbc.M900301200
60. Toko H, Minamino T, Komuro I (2008) Role of heat shock transcriptional factor 1 and heat shock proteins in cardiac hypertrophy. Trends Cardiovasc Med 18(3):88-93. doi: 10.1016/j.tcm.2008.01.003
61. Um SH, Frigerio F, Watanabe M, Picard F, Joaquin M, Sticker M, Fumagalli S, Allegrini PR, Kozma SC, Auwerx J, Thomas G (2004) Absence of S6K1 protects against age- and diet-induced obesity while enhancing insulin sensitivity. Nature 431(7005):200-205. doi: 10.1038/nature02866
62. Wallin R, Hall TR, Hutson SM (1990) Purification of branched chain aminotransferase from rat heart mitochondria. J Biol Chem 265:6019-6024
63. Wang T, Donahoe PK, Zervos AS (1994) Specific interaction of type I receptors of the TGF-beta family with the immunophilin FKBP-12. Science 265(5172):674-676
64. 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(9):4160-4168. doi: 10.1210/en.2006-0251
65. Wu G, Knabe DA (1994) Free and protein-bound amino acids in sow's colostrum and milk. J Nutr 124(3):415-424
66. Yang H, Rudge DG, Koos JD, Vaidialingam B, Yang HJ, Pavletich NP (2013) mTOR kinase structure, mechanism and regulation. Nature 497(7448):217-223. doi: 10.1038/nature12122
67. Yudkoff M, Daikhin Y, Nissim I, Horyn O, Luhovyy B, Lazarow A, Nissim I (2005) Brain amino acid requirements and toxicity: the example of leucine. J Nutr 135(6 Suppl):1531S-1538S