Cellular and animal indispensable amino acid limitation responses and health promotion. Can the two be linked? A critical review

International Journal of Food Sciences and Nutrition

Volumn 64, Issue 3, 2013, Pages 300-311

  Sikalidis, Angelos K ^a,b  

^a Department of Obstetrics Gynecology   (United States)

^b ARISTOTLE UNIVERSITY MEDICAL SCHOOL   (Greece)

Author keywords

4E BP1; AMPK; EIF2 ; GCN2; Indispensable amino acids; Integrated stress response; MTOR

Indexed keywords

ESSENTIAL AMINO ACID; PROTEIN KINASE;

ANIMAL; APOPTOSIS; CELL SURVIVAL; CHRONIC DISEASE; GENE EXPRESSION REGULATION; GENETICS; HEALTH PROMOTION; HUMAN; METABOLISM; REVIEW; SIGNAL TRANSDUCTION;

AMINO ACIDS, ESSENTIAL; ANIMALS; APOPTOSIS; CELL SURVIVAL; CHRONIC DISEASE; GENE EXPRESSION REGULATION; HEALTH PROMOTION; HUMANS; PROTEIN KINASES; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA;

EID: 84876064381     PISSN: 09637486     EISSN: 14653478     Source Type: Journal    
DOI: 10.3109/09637486.2012.738649     Document Type: Review

References (74)

1. Anthony TG, McDaniel BJ, Byerley RL, McGrath BC, Cavener DR, McNurlan MA, Wek RC. 2004. Preservation of liver protein synthesis during dietary leucine deprivation occurs at the expense of skeletal muscle mass in mice deleted for eIF2 kinase GCN2. J Biol Chem 279:36553-36561.
2. Averous J, Bruhat A, Mordier S, Fafournoux P. 2003. Recent advances in the understanding of amino acid regulation of gene expression. J Nutr 133(Suppl. 1):2040S-2045S.
3. Avruch J, Long X, Ortiz-Vega S, Rapley J, Papageorgiou A, Dai N. 2009. Amino acid regulation of TOR complex 1. Am J Physiol Endocrinol Metab 296:592-602.
4. Buerger C, DeVries B, Stambolic V. 2006. Localization of Rheb to the endomembrane is critical for its signaling function. Biochem Biophys Res Commun 344:869-880.
5. Bunpo P, Dudley A, Cundiff JK, Cavener DR, Wek RC, Anthony TG. 2009. GCN2 protein kinase is required to activate amino acid deprivation responses in mice treated with the anticancer agent L-asparaginase. J Biol Chem 284:32742-32749.
6. Bunpo P, Cundiff JK, Reinert RB, Wek RC, Aldrich CJ, Anthony TG. 2010. The eIF2 kinase GCN2 is essential for the murine immune system to adapt to amino acid deprivation by asparaginase. J Nutr 140:2020-2027.
7. Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson M. 2010. Cellular stress responses, the hormesis paradigm and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal 13: 1763-1811.
8. Choo AY, Blenis J. 2009. Not all substrates are treated equally: implications for mTOR, rapamycin-resistance and cancer therapy. Cell Cycle 8:567-572.
9. Chotenchuang N, Azzout-Marniche D, Bos C, Chaumontent C, Gaussere's N, Steiler T, et al. 2009. mTOR, AMPK, and GCN2 coordinate the adaptation of hepatic energy metabolic pathways in response to protein intake in the rat. Am J Physiol Endocrinol Metab 297:1313-1323.
10. Dang Do AN, Kimball SR, Cavener DR, Jefferson LS. 2009. eIF2a kinases GCN2 and PERK modulate transcription and translation of distinct sets of mRNAs in mouse liver. Physiol Genomics 38:328-341.
11. De Marte ML, Enesco HE. 1986. Influence of low tryptophan diet on survival and organ growth in mice. Mech Ageing Dev 36: 161-171.
12. Deval C, Chaveroux C, Maurin AC, Cherasse Y, Parry L, Carraro V, et al. 2009. Amino acid limitation regulates the expression of genes involved in several specific biological processes through GCN2-dependent and GCN2-independent pathways. FEBS J 276:707-718.
13. Draznin B. 2006. Molecular mechanisms of insulin resistance: serine phosphorylation of insulin receptor substrate-1 and increased expression of p85alpha: the two sides of a coin. Diabetes 55: 2392-2397.
14. Gabauer F, Hentze M. 2004. Molecular mechanisms of translational control. Mol Cell Biol 5:827-834.
15. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913-963.
16. Goberdhan DC, Ogmundsdó ttir MH, Kazi S, Reynolds B, Visvalingam SM, Wilson C, Boyd CA. 2009. Amino acid sensing and mTOR regulation: inside or out? Biochem Soc Trans 37:248-252.
17. Guo F, Cavener DR. 2007. The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metab 5:103-114.
18. Haghighat A, Mader S, Pause A, Sonenberg N. 1995. Repression of cap-dependent translation by 4E-binding protein 1: competition with p220 for binding to eukaryotic initiation factor-4E. EMBO J 14:5701-5709.
19. Hao S, Sharp JW, Ross-Inta CM, McDaniel BJ, Anthony TG, Wek RC, et al. 2005. Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science 307: 1776-1778.
20. Harding HP, Novoa I, Zhang Y, Zeng H,Wek R, Schapira M, RonD. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol Cell 6:1099-1108.
21. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, et al. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell 11: 619-633.
22. Hinnebusch AG. 2005. Translational regulation of GCN4 and the general amino acid control of yeast. Annu Rev Microbiol 59: 407-450.
23. Hinnebusch AG. 2000. Mechanism and regulation of initiator methionyl-tRNA binding to ribosomes. In: Sonenberg N, Hershey JWB, Mathews MB, editors. Translational control of gene expression. Plainview, NY: Cold Springs Harbor Laboratory Press, pp 185-243.
24. Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318-327.
25. Jousse C, Deval C, Maurin AC, Parry L, Cherasse Y, Chaveroux C, et al. 2007. TRB3 inhibits the transcriptional activation of stress- regulated genes by a negative feedback on the ATF4 pathway. J Biol Chem 282:15851-15861.
26. Kaufman RJ. 2004. Regulation of mRNA translation by protein folding in the endoplasmic reticulum. Trends Biochem Sci 29: 152-158.
27. Kilberg MS, Pan YX, Chen H, Leung-Pineda V. 2005. Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu Rev Nutr 25:59-85.
28. Kilberg MS, Shan J, Su N. 2009. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol Metab 20:436-443.
29. Kim E, Goraksha-Hicks P, Li L, Neufeld TP, Guan KL. 2008. Regulation of TORC1 by Rag GTPases in nutrient response. Nat Cell Biol 10:935-945.
30. Kimball SR, Antonetti DA, Brawley RM, Jefferson LS. 1991. Mechanism of inhibition of peptide chain initiation by amino acid deprivation in perfused rat liver. Regulation involving inhibition of eukaryotic initiation factor 2a phosphatase activity. J Biol Chem 266:1969-1976.
31. Kubica N, Jefferson LS, Kimball SR. 2006. Eukaryotic initiation factor 2B and its role in alterations in mRNA translation that occur under a number of pathophysiological and physiological conditions. Prog Nucleic Acid Res Mol Biol 81:271-296.
32. Lee J-I, Dominy JE, Jr, Sikalidis AK, Hirschberger LL, Wang W, Stipanuk MH. 2008. HepG2/C3A cells respond to cysteine deprivation by induction of the amino acid deprivation/ integrated stress response pathway. Physiol Genomics 33: 218-229.
33. Lu PD, Jousse C, Harding HP, Ron D. 2004a. Translation reinitiation at alternative open reading frames regulate gene expression in an integrated stress response. J Cell Biol 167: 27-33.
34. Lu PD, Jousse C, Marciniak SJ, Zhang Y, Novoa I, ScheunerD, et al. 2004b. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J 23:169-179.
35. Mader S, Lee H, Pause A, Sonenberg N. 1995. The translation initiation factor eIF-4E binds to a common motif shared by the translation factor eIF-4 gamma and the translational repressors 4E-binding proteins. Mol Cell Biol 15:4990-4997.
36. Martin B, Golden E, Egan JM, Mattson MP, Maudsley S. 2007. Reduced energy intake: the secret to a long and healthy life? IBS J Sci 2:35-39.
37. Masoro EJ. 1997. Hormesis and the antiaging action of dietary restriction. Exp Gerontol 33:61-66.
38. Masoro EJ. 2007. Role of hormesis in life extension by caloric restriction. Dose Response 5:163-173.
39. McCarty MF, Baroso-Aranda J, Contreras F. 2008. The lowmethionine content of vegan diets may make methionine restriction feasible as a life extension strategy. Med Hypotheses 72:125-128.
40. McCay CM, Crowell MF, Maynard LA. 1935. The effect of retarded growth upon the length of life span and upon the ultimate body size. J Nutr 10:63-79.
41. McCay CM, Maynard LA, Sperling G, Leroy Barnes L. 1939. Retarded growth, life span, ultimate body size and age changes in the albino rat after feeding diets restricted in calories. J Nutr 18: 1-13.
42. Milward DJ, Jackson AA. 2003. Protein/energy ratios of current diets in developed and developing countries compared with a safe protein/energy ratio: implications for recommended protein and amino acid intakes. Public Health Nutr 7:387-405.
43. Ooka H, Segall PE, Timiras PS. 1988. Histology and survival in agedelayed low-tryptophan-fed rats. Mech Ageing Dev 43:79-98.
44. Padyana AK, Qiu H, Roll-Mecak A, Hinnebusch AG, Burley SK. 2005. Structural basis for autoinhibition and mutational activation of eukaryotic initiation factor 2a protein kinase GCN2. J Biol Chem 280:29289-29299.
45. Pan YX, Chen H, Thiaville MM, Kilberg MS. 2007. Activation of the ATF3 gene through a co-ordinated amino acid-sensing response programme that controls transcriptional regulation of responsive genes following amino acid limitation. Biochem J 401: 299-307.
46. Poulin F, Gingras AC, Olsen H, Chevalier S, Sonenberg N. 1998. 4E-BP3, a new member of the eukaryotic initiation factor 4E-binding protein family. J Biol Chem 273:14002-14007.
47. Prévô t D, Darlix JL, Ohlmann T. 2003. Conducting the initiation of protein synthesis: the role of eIF4G. Biol Cell 95:141-156.
48. Raffaghello L, Lee C, Safdie FM, Wei M, Madia F, Bianchi G, Longo VD. 2008. Starvation-dependent differential stress resistance protects normal but not cancer cells against highdose chemotherapy. Proc Natl Acad Sci USA 105:8215-8220.
49. Ranganathan AC, Ojha S, Kourtidis A, Conklin DS, Aguirre-Ghiso JA. 2008. Dual function of pancreatic endoplasmic reticulum kinase in tumor cell growth arrest and survival. Cancer Res 68:3260-3268.
50. Rattan SIS. 2008. Hormesis in aging. Ageing Res Rev 7:63-78.
51. Richie JP, Jr, Komninou D, Leutzinger Y, Kleinman W, Orentreich N, Malloy V, et al. 2001. Regulation of antioxidant metabolism by translation initiation factor 2alpha. Cell Biol 152: 997-1006.
52. Roth GS, Ingram DK, Lane MA. 2001. Caloric restriction in primates and relevance to humans. Ann NY Acad Sci 928: 305-315.
53. Salminen A, Kaarniranta K. 2010. ER stress and hormetic regulation of the aging process. Ageing Res Rev 9:211-217.
54. Sancak Y, Peterson TR, Shaul YD, Lindquist RA, Thoreen CC, Bar-Peled L, Sabatini DM. 2008. The Rag GTPases bind raptor and mediate amino acid signaling to mTORC1. Science 320:1496-1501.
55. Sanz A, Caro P, Ayala V, Portero-Otin M, Pamplona R, Barja G. 2006. Methionine restriction decreases mitochondrial oxygen radical generation and leak as well as oxidative damage to mitochondrial DNA and proteins. FASEB J 20:1064-1073.
56. Sarbassov DD, Sabatini DM. 2005. Redox regulation of the nutrient-sensitive raptor-mTOR pathway and complex. J Biol Chem 280:39505-39509.
57. Sato H, Nomura S, Maebara K, Sato K, Tamba M, Bannai S. 2004. Transcriptional control of cystine/glutamate transporter gene by amino acid deprivation. Biochem Biophys Res Commun 325: 109-116.
58. Schmelze T, Hall MN. 2000. TOR, a central controller of cell growth. Cell 103:253-262.
59. Shan J, Ord D, Ord T, Kilberg MS. 2009. Elevated ATF4 expression, in the absence of other signals, is sufficient for transcriptional induction via CCAATenhancer-binding proteinactivating transcription factor response elements. J Biol Chem 284:21241-21248.
60. Sikalidis AK, Stipanuk MH. 2010. Growing rats respond to a sulphur amino acid-deficient diet by phosphorylation of the alpha subunit of the eukaryotic initiation factor 2 heterotrimeric complex and induction of the adaptive components of the integrated stress response. J Nutr 140:1080-1085.
61. Sikalidis AK, Lee JI, Stipanuk MH. 2011. Gene expression and integrated stress response in HepG2/C3A cells cultured in amino acid deficient medium. Amino Acids 41:159-171.
62. Tan S, Somia N, Maher P, Schubert DJ. 2001. Regulation of antioxidant metabolism by translation initiation factor 2 alpha. Cell Biol 152:997-1006.
63. Tettweiler G, Miron M, Jenkins M, Sonenberg N, Lasko PF. 2005. Starvation and oxidative stress resistance in Drosophila are mediated through the eIF4e-binding protein d4E-BP. Genes Dev 19:1840-1843.
64. Thiaville MM, Pan YX, Gjymishka A, Zhong C, Kaufman RJ, Kilberg MS. 2008. MEK signaling is required for phosphorylation of eIF2alpha following amino acid limitation of HepG2 human hepatoma cells. J Biol Chem 283:10848-10857.
65. Watatani Y, Ichikawa K, Nakanishi N, Fujimoto M, Takeda H, Kimura N, et al. 2008. Stress-induced translation of ATF5 mRNA is regulated by the 50-untranslated region. J Biol Chem 283:2543-2553.
66. Wek RC, Jackson BM, Hinnebusch AG. 1989. Juxtaposition of domains homologous to protein kinases and histidyl-tRNA synthetases in GCN2 protein suggests a mechanism for coupling GCN4 expression to amino acid availability. Proc Natl Acad Sci USA 86:4579-4583.
67. Wek SA, Zhu S, Wek RC. 1995. The histidyl-tRNA synthetase-related sequence in the eIF-2a a protein kinase GCN2 interacts with tRNA and is required for activation in response to starvation for different amino acids. Mol Cell Biol 15: 4497-4506.
68. Wek RC, Jiang HY, Anthony TG. 2006. Coping with stress: eIF2 kinases and translational control. Biochem Soc Trans 34:7-11.
69. Xiao F, Huang Z, Li H, Yu J, Wang C, Chen S, et al. 2011. Leucine deprivation increases hepatic insulin sensitivity via GCN2/ mTOR/S6K1 and AMPK pathways. Diabetes 60:746-756.
70. Yamaguchi S, Ishihara H, Yamada T, Tamura A, Usui M, Tominaga R, et al. 2008. ATF4-mediated induction of 4E-BP1 contributes to pancreatic beta cell survival under endoplasmic reticulum stress. Cell Metab 7:269-276.
71. Ye J, Kumanova M, Hart LS, Sloane K, Zhang H, De Panis DN, et al. 2010. The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation. EMBO J 29:2082-2096.
72. Zhang P, McGrath BC, Reinert J, Olsen DS, Lei L, Gill S, et al. 2002. The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice. Mol Cell Biol 22:6681-6688.
73. Zimmerman JA. 2004. Tissue glutathione and cysteine levels in methionine-restricted rats. Nutrition 20:800-805.
74. Zimmerman JA, Malloy V, Krajcik R, Orentreich N. 2003. Nutritional control of aging. Exp Gerontol 38:47-52.