The transcription factor network associated with the amino acid response in mammalian cells

Advances in Nutrition

Volumn 3, Issue 3, 2012, Pages 295-306

  Kilberg, Michael S ^a   Balasubramanian, Mukundh ^a   Fu, Lingchen ^a   Shan, Jixiu ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR; AMINO ACID; CCAAT ENHANCER BINDING PROTEIN;

ANIMAL; CELL LINE; CELL NUCLEUS; DRUG EFFECT; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PROTEIN INTAKE; REVIEW; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTORS; AMINO ACIDS; ANIMALS; CCAAT-ENHANCER-BINDING PROTEINS; CELL LINE; CELL NUCLEUS; DIETARY PROTEINS; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; HUMANS; SIGNAL TRANSDUCTION;

EID: 84866783355     PISSN: 21618313     EISSN: 21565376     Source Type: Journal    
DOI: 10.3945/an.112.001891     Document Type: Review

References (121)

1. Gietzen DW, Rogers QR. Nutritional homeostasis and indispensable amino acid sensing:a new solution to an old puzzle. Trends Neurosci. 2006;29:91-9.
2. Koehnle TJ, Russell MC, Morin AS, Erecius LF, Gietzen DW. Diets deficient in indispensable amino acids rapidly decrease the concentration of the limiting amino acid in the anterior piriform cortex of rats. J Nutr. 2004;134:2365-71.
3. Hao S, Sharp JW, Ross-Inta CM, McDaniel BJ, Anthony TG, Wek RC, Cavener DR, McGrath BC, Rudell JB, Koehnle TJ, et al. Uncharged tRNA and sensing of amino acid deficiency in mammalian piriform cortex. Science. 2005;307:1776-8.
4. Maurin AC, Jousse C, Averous J, Parry L, Bruhat A, Cherasse Y, Zeng H, Zhang Y, Harding HP, Ron D, et al. The GCN2 kinase biases feeding behavior to maintain amino acid homeostasis in omnivores. Cell Metab. 2005;1:273-7.
5. Guo F, Cavener DR. The GCN2 eIF2alpha kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metab. 2007;5:103-14.
6. Endo Y, Fu Z, Abe K, Arai S, Kato H. Dietary protein quantity and quality affect rat hepatic gene expression. J Nutr. 2002;132:3632-7.
7. Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005;135:1382-6.
8. Kilberg MS, Shan J, Su N. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrinol Metab. 2009; 20:436-43.
9. Berlanga JJ, Santoyo J, De Haro C. Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2alpha kinase. Eur J Biochem. 1999;265:754-62.
10. Sood R, Porter AC, Olsen DA, Cavener DR, Wek RC. A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2. Genetics. 2000;154:787-801.
11. Zhang P,McGrath BC, Reinert J,Olsen DS, Lei L, Gill S, Wek SA, Vattem KM, Wek RC, Kimball SR, et al. The GCN2 eIF2alpha kinase is required for adaptation to amino acid deprivation in mice. Mol Cell Biol. 2002;22: 6681-8.
12. Kimball SR, Anthony TG, Cavener DR, Jefferson LS, editors. Nutrient signaling through mammalian GCN2. New York:Springer-Verlag; 2005.
13. Bunpo P, Dudley A, Cundiff JK, Cavener DR, Wek RC, Anthony TG. The GCN2 protein kinase is required to activate amino acid deprivation responses in mice treated with the anti-cancer agent, L-asparaginase. J Biol Chem. 2009;284:32742-9.
14. Kimball SR, Jefferson LS. Role of amino acids in the translational control of protein synthesis in mammals. Semin Cell Dev Biol. 2005;16:21-7.
15. Lee YY, Cevallos RC, Jan E. An upstream open reading frame regulates translation of GADD34 during cellular stresses that induce eIF2alpha phosphorylation. J Biol Chem. 2009;284:6661-73.
16. Novoa I, Zeng H, Harding HP, Ron D. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2. J Cell Biol. 2001;153:1011-22.
17. Brush MH, Weiser DC, Shenolikar S. Growth arrest and DNA damageinducible protein GADD34 targets protein phosphatase 1 alpha to the endoplasmic reticulum and promotes dephosphorylation of the alpha subunit of eukaryotic translation initiation factor 2. Mol Cell Biol. 2003;23:1292-303.
18. Novoa I, Zhang Y, Zeng H, Jungreis R, Harding HP, Ron D. Stressinduced gene expression requires programmed recovery from translational repression. EMBO J. 2003;22:1180-7.
19. Wek RC, Jiang HY, Anthony TG. Coping with stress:eIF2 kinases and translational control. Biochem Soc Trans. 2006;34:7-11.
20. Harding HP, Zhang Y, Zeng H, Novoa I, Lu PD, Calfon M, Sadri N, Yun C, Popko B, Paules R, et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol Cell. 2003;11:619-33.
21. Dang Do AN, Kimball SR, Cavener DR, Jefferson LS. eIF2alpha kinases GCN2 and PERK modulate transcription and translation of distinct sets of mRNAs in mouse liver. Physiol Genomics. 2009;38: 328-41.
22. Gjymishka A, Palii SS, Shan J, Kilberg MS. Despite increased ATF4 binding at the C/EBP-ATF composite site following activation of the unfolded protein response, system A transporter 2 (SNAT2) transcription activity is repressed in HepG2 cells. J Biol Chem. 2008;283: 27736-47.
23. Zimmerman JA, Malloy V, Krajcik R, Orentreich N. Nutritional control of aging. Exp Gerontol. 2003;38:47-52.
24. Ooka H, Segall PE, Timiras PS. Histology and survival in age-delayed low-tryptophan-fed rats. Mech Ageing Dev. 1988;43:79-98.
25. Segall PE, Timiras PS. Patho-physiologic findings after chronic tryptophan deficiency in rats:a model for delayed growth and aging. Mech Ageing Dev. 1976;5:109-24.
26. Thissen JP, Ketelslegers JM, Underwood LE. Nutritional regulation of the insulin-like growth factors. Endocr Rev. 1994;15:80-101.
27. Smith WJ, Underwood LE, Clemmons DR. Effects of caloric or protein restriction on insulin-like growth factor-I (IGF-I) and IGF-binding proteins in children and adults. J Clin Endocrinol Metab. 1995;80: 443-9.
28. Averous J, Maurin AC, Bruhat A, Jousse C, Arliguie C, Fafournoux P. Induction of IGFBP-1 expression by amino acid deprivation of HepG2 human hepatoma cells involves both a transcriptional activation and an mRNA stabilization due to its 3'UTR. FEBS Lett. 2005;579: 2609-14.
29. Jousse C, Bruhat A, Ferrara M, Fafournoux P. Physiological concentration of amino acids regulates insulin-like-growth-factor-binding protein 1 expression. Biochem J. 1998;334:147-53.
30. Kanamoto R, Yokota T, Hayashi SI. Expressions of c-myc and insulinlike growth factor-1 mRNA in the liver of growing rats vary reciprocally in response to changes in dietary protein. J Nutr. 1994;124:2329-34.
31. Straus DS, Burke EJ, Marten NW. Induction of insulin-like growth factor binding protein-1 gene expression in liver of protein-restricted rats and in rat hepatoma cells limited for a single amino acid. Endocrinology. 1993;132:1090-100.
32. Takenaka A, Komori K, Morishita T, Takahashi SI, Hidaka T, Noguchi T. Amino acid regulation of gene transcription of rat insulin-like growth factor-binding protein-1. J Endocrinol. 2000;164:R11-6.
33. Figueras F, Gardosi J. Intrauterine growth restriction:new concepts in antenatal surveillance, diagnosis, and management. Am J Obstet Gynecol. 2011;204:288-300.
34. Imdad A, Bhutta ZA. Effect of balanced protein energy supplementation during pregnancy on birth outcomes. BMC Public Health. 2011; 11:Suppl 3:S17.
35. Brown LD, Green AS, Limesand SW, Rozance PJ. Maternal amino acid supplementation for intrauterine growth restriction. Front Biosci (Schol Ed). 2011;3:428-44.
36. Yung HW, Calabrese S, Hynx D, Hemmings BA, Cetin I, Charnock-Jones DS, Burton GJ. Evidence of placental translation inhibition and endoplasmic reticulum stress in the etiology of human intrauterine growth restriction. Am J Pathol. 2008;173:451-62.
37. Barker DJ. Adult consequences of fetal growth restriction. Clin Obstet Gynecol. 2006;49:270-83.
38. Gong L, Pan YX, Chen H. Gestational low protein diet in the rat mediates Igf2 gene expression in male offspring via altered hepatic DNA methylation. Epigenetics. 2010;5:619-26.
39. Kalantar-Zadeh K, Cano NJ, Budde K, Chazot C, Kovesdy CP, Mak RH, Mehrotra R, Raj DS, Sehgal AR, Stenvinkel P, et al. Diets and enteral supplements for improving outcomes in chronic kidney disease. Nat Rev Nephrol. 2011;7:369-84.
40. May PE, Barber A, D'Olimpio JT, Hourihane A, Abumrad NN. Reversal of cancer-related wasting using oral supplementation with a combination of beta-hydroxy-beta-methylbutyrate, arginine, and glutamine. Am J Surg. 2002;183:471-9.
41. Morley JE. Calories and cachexia. Curr Opin Clin Nutr Metab Care. 2009;12:607-10.
42. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N, Harding H, Novoa I, Varia M, Raleigh J, et al. ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J. 2005;24:3470-81.
43. Ye J, Kumanova M, Hart LS, Sloane K, Zhang H, DePanis DN, Bobrovnikova-Marjon E, Diehl A, Ron D, Koumenis C. The GCN2-ATF4 pathway is critical for tumor cell survival and proliferation in response to nutrient deprivation. EMBO J. 2010;29:2082-96.
44. Aslanian AM, Fletcher BS, Kilberg MS. Asparagine synthetase expression alone is sufficient to induce L-asparaginase resistance in MOLT-4 human leukaemia cells. Biochem J. 2001;357:321-8.
45. Su N, Pan YX, Zhou M, Harvey RC, Hunger SP, Kilberg MS. Correlation between asparaginase sensitivity and asparagine synthetase protein content, but not mRNA, in acute lymphoblastic leukemia cell lines. Pediatr Blood Cancer. 2008;50:274-9.
46. Pui CH, Relling MV, Downing JR. Acute lymphoblastic leukemia. N Engl J Med. 2004;350:1535-48.
47. Aslanian AM, Kilberg MS. Multiple adaptive mechanisms affect asparagine synthetase substrate availability in asparaginase-resistant MOLT-4 human leukaemia cells. Biochem J. 2001;358:59-67.
48. Lorenzi PL, Weinstein JN. Asparagine synthetase:a new potential biomarker in ovarian cancer. Drug News Perspect. 2009;22:61-4.
49. Anthony TG, McDaniel BJ, Byerley RL, McGrath BC, Cavener DR, McNurlan MA,Wek RC. 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. 2004;279: 36553-61.
50. Carraro V, Maurin AC, Lambert-Langlais S, Averous J, Chaveroux C, Parry L, Jousse C, Ord D, Ord T, Fafournoux P, et al. Amino acid availability controls TRB3 transcription in liver through the GCN2/eIF2alpha/ ATF4 pathway. PLoS ONE. 2010;5:e15716.
51. Siu F, Bain PJ, LeBlanc-Chaffin R, Chen H, Kilberg MS. ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J Biol Chem. 2002;277:24120-7.
52. Vattem KM, Wek RC. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc Natl Acad Sci U S A. 2004;101:11269-74.
53. Lu PD, Harding HP, Ron D. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J Cell Biol. 2004;167:27-33.
54. Wolfgang CD, Chen BP, Martindale JL, Holbrook NJ, Hai T. gadd153/Chop10, a potential target gene of the transcriptional repressor ATF3. Mol Cell Biol. 1997;17:6700-7.
55. Fawcett TW, Martindale JL, Guyton KZ, Hai T, Holbrook NJ. Complexes containing activating transcription factor (ATF)/cAMP-responsiveelement-binding protein (CREB) interact with the CCAATenhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem J. 1999;339:135-41.
56. Shan J, Ord D, Ord T, Kilberg MS. Elevated ATF4 expression, in the absence of other signals, is sufficient for transcriptional induction via CCAAT enhancer-binding protein-activating transcription factor response elements. J Biol Chem. 2009;284:21241-8.
57. Ameri K, Harris AL. Activating transcription factor 4. Int J Biochem Cell Biol. 2008;40:14-21.
58. Thiaville MM, Dudenhausen EE, Zhong C, Pan YX, Kilberg MS. Deprivation of protein or amino acid induces C/EBP beta synthesis and binding to amino acid response elements, but its action is not an absolute requirement for enhanced transcription. Biochem J. 2008;410: 473-84.
59. Jiang HY, Wek SA, McGrath BC, Lu D, Hai TW, Harding HP, Wang XZ, Ron D, Cavener DR, Wek RC. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol Cell Biol. 2004;24:1365-77.
60. Pan YX, Chen H, Thiaville MM, Kilberg MS. 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. 2007;401:299-307.
61. Chérasse Y, Maurin AC, Chaveroux C, Jousse C, Carraro V, Parry L, Deval C, Chambon C, Fafournoux P, Bruhat A. The p300/CBP-associated factor (PCAF) is a cofactor of ATF4 for amino acid-regulated transcription of CHOP. Nucleic Acids Res. 2007;35:5954-65.
62. Chen H, Pan YX, Dudenhausen EE, Kilberg MS. Amino acid deprivation induces the transcription rate of the human asparagine synthetase gene through a timed program of expression and promoter binding of nutrient-responsive bZIP transcription factors as well as localized histone acetylation. J Biol Chem. 2004;279:50829-39.
63. Su N, Kilberg MS. C/EBP homology protein (chop) interacts with activating transcription factor 4 (ATF4) and negatively regulates the stress-dependent induction of the asparagine synthetase gene. J Biol Chem. 2008;283:35106-17.
64. Lopez AB,Wang C, Huang CC, Yaman I, Li Y, Chakravarty K, Johnson PF, Chiang CM, Snider MD, Wek RC, et al. A feedback transcriptional mechanism controls the level of the arginine/lysine transporter cat-1 during amino acid starvation. Biochem J. 2007;402:163-73.
65. Averous J, Bruhat A, Jousse C, Carraro V, Thiel G, Fafournoux P. Induction of CHOP Expression by Amino Acid Limitation Requires Both ATF4 Expression and ATF2 Phosphorylation. J Biol Chem. 2004;279:5288-97.
66. Bruhat A, Cherasse Y, Maurin AC, BreitwieserW, Parry L, Deval C, Jones N, Jousse C, Fafournoux P. ATF2 is required for amino acid-regulated transcription by orchestrating specific histone acetylation. Nucleic Acids Res. 2007;35:1312-21.
67. Chaveroux C, Jousse C, Cherasse Y, Maurin AC, Parry L, Carraro V, Derijard B, Bruhat A, Fafournoux P. Identification of a novel amino acid response pathway triggering ATF2 phosphorylation in mammals. Mol Cell Biol. 2009;29:6515-26.
68. Bruhat A, Jousse C, Carraro V, Reimold AM, Ferrara M, Fafournoux P. Amino acids control mammalian gene transcription:activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol Cell Biol. 2000;20:7192-204.
69. Fu L, Balasubramanian M, Shan J, Dudenhausen EE, Kilberg MS. Auto-activation of c-JUN gene by amino acid deprivation of hepatocellular carcinoma cells reveals a novel c-JUN-mediated signaling pathway. J Biol Chem. 2011;286:36724-38.
70. Gachon F, Devaux C, Mesnard JM. Activation of HTLV-I transcription in the presence of Tax is independent of the acetylation of CREB-2 (ATF-4). Virology. 2002;299:271-8.
71. Lassot I, Estrabaud E, Emiliani S, Benkirane M, Benarous R, Margottin-Goguet F. p300 modulates ATF4 stability and transcriptional activity independently of its acetyltransferase domain. J Biol Chem. 2005; 280:41537-45.
72. Greene LA, Lee HY, Angelastro JM. The transcription factor ATF5: role in neurodevelopment and neural tumors. J Neurochem. 2009; 108:11-22.
73. Al Sarraj J, Vinson C, Thiel G. Regulation of asparagine synthetase gene transcription by the basic region leucine zipper transcription factors ATF5 and CHOP. Biol Chem. 2005;386:873-9.
74. Watatani Y, Ichikawa K, Nakanishi N, Fujimoto M, Takeda H, Kimura N, Hirose H, Takahashi S, Takahashi Y. Stress-induced translation of ATF5 mRNA is regulated by the 5'-untranslated region. J Biol Chem. 2008;283:2543-53.
75. Zhou D, Palam LR, Jiang L, Narasimhan J, Staschke KA, Wek RC. Phosphorylation of eIF2 directs ATF5 translational control in response to diverse stress conditions. J Biol Chem. 2008;283:7064-73.
76. Yamazaki T, Ohmi A, Kurumaya H, Kato K, Abe T, Yamamoto H, Nakanishi N, Okuyama R, Umemura M, Kaise T, et al. Regulation of the human CHOP gene promoter by the stress response transcription factor ATF5 via the AARE1 site in human hepatoma HepG2 cells. Life Sci. 2010;87:294-301.
77. Li G, Li W, Angelastro JM, Greene LA, Liu DX. Identification of a novel DNA binding site and a transcriptional target for activating transcription factor 5 in c6 glioma and mcf-7 breast cancer cells. Mol Cancer Res. 2009;7:933-43.
78. Rousseau J, Gagne V, Labuda M, Beaubois C, Sinnett D, Laverdiere C, Moghrabi A, Sallan SE, Silverman LB, Neuberg D, et al. ATF5 polymorphisms influence ATF function and response to treatment in children with childhood acute lymphoblastic leukemia. Blood. 2011; 118:5883-90.
79. Hai T, Wolford CC, Chang YS. ATF3, a hub of the cellular adaptiveresponse network, in the pathogenesis of diseases:is modulation of inflammation a unifying component? Gene Expr. 2010;15:1-11.
80. Thompson MR, Xu D, Williams BR. ATF3 transcription factor and its emerging roles in immunity and cancer. J Mol Med. 2009;87: 1053-60.
81. Pan YX, Chen H, Siu F, Kilberg MS. Amino acid deprivation and endoplasmic reticulum stress induce expression of multiple ATF3 mRNA species which, when overexpressed in HepG2 cells, modulate transcription by the human asparagine synthetase promoter. J Biol Chem. 2003;278:38402-12.
82. Pan Y, Chen H, Kilberg MS. Interaction of RNA-binding proteins HuR and AUF1 with the human ATF3 mRNA 3'-untranslated region regulates its amino acid limitation-induced stabilization. J Biol Chem. 2005;280:34609-16.
83. Yaman I, Fernandez J, Sarkar B, Schneider RJ, Snider MD, Nagy LE, Hatzoglou M. Nutritional control of mRNA stability is mediated by a conserved AU-rich element that binds the cytoplasmic shuttling protein HuR. J Biol Chem. 2002;277:41539-46.
84. Wolfgang CD, Liang G, Okamoto Y, Allen AE, Hai T. Transcriptional autorepression of the stress-inducible gene ATF3. J Biol Chem. 2000; 275:16865-70.
85. Zhou D, Zhang Y, Pan YX, Chen H. Dickkopf homolog 1, a Wnt signaling antagonist, is transcriptionally up-regulated via an ATF4-independent and MAPK/ERK-dependent pathway following amino acid deprivation. Biochim Biophys Acta. 2011;1809:306-15.
86. Descombes P, Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell. 1991;67:569-79.
87. Calkhoven CF, Muller C, Leutz A. Translational control of C/EBPalpha and C/EBPbeta isoform expression. Genes Dev. 2000;14:1920-32.
88. Kimball SR, Jefferson LS. Molecular mechanisms through which amino acids mediate signaling through the mammalian target of rapamycin. Curr Opin Clin Nutr Metab Care. 2004;7:39-44.
89. Wilson FA, Suryawan A, Gazzaneo MC, Orellana RA, Nguyen HV, Davis TA. Stimulation of muscle protein synthesis by prolonged parenteral infusion of leucine is dependent on amino acid availability in neonatal pigs. J Nutr. 2010;140:264-70.
90. Li Y, Bevilacqua E, Chiribau CB, Majumder M, Wang C, Croniger CM, Snider MD, Johnson PF, Hatzoglou M. Differential control of the CCAAT/ enhancer-binding protein beta (C/EBPbeta) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J Biol Chem. 2008;283: 22443-56.
91. Chiribau CB, Gaccioli F, Huang CC, Yuan CL, Hatzoglou M. Molecular symbiosis of CHOP and C/EBP beta isoform LIP contributes to endoplasmic reticulum stress-induced apoptosis. Mol Cell Biol. 2010;30:3722-31.
92. Zinszner H, Kuroda M, Wang XZ, Batchvarova N, Lightfoot RT, Remotti H, Stevens JL, Ron D. CHOP is implicated in programmed cell death in response to impaired function of the endoplasmic reticulum. Genes Dev. 1998;12:982-95.
93. Price BD, Calderwood SK. Gadd45 and Gadd153 messenger RNA levels are increased during hypoxia and after exposure of cells to agents which elevate the levels of the glucose-regulated proteins. Cancer Res. 1992;52:3814-7.
94. Jousse C, Bruhat A, Harding HP, Ferrara M, Ron D, Fafournoux P. Amino acid limitation regulates CHOP expression through a specific pathway independent of the unfolded protein response. FEBS Lett. 1999;448:211-6.
95. Bruhat A, Jousse C, Wang XZ, Ron D, Ferrara M, Fafournoux P. Amino acid limitation induces expression of CHOP, a CCAAT/enhancer binding protein-related gene, at both transcriptional and post-transcriptional levels. J Biol Chem. 1997;272:17588-93.
96. Abcouwer SF, Schwarz C, Meguid RA. Glutamine deprivation induces the expression of GADD45 and GADD153 primarily by mRNA stabilization. J Biol Chem. 1999;274:28645-51.
97. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J. 2005;24:1243-55.
98. Pohjanpelto P, Holtta E. Deprivation of a single amino acid induces protein synthesis-dependent increases in c-jun, c-myc, and ornithine decarboxylase mRNAs in Chinese hamster ovary cells. Mol Cell Biol. 1990;10:5814-21.
99. Li J, Liu J, Song J, Wang X, Weiss HL, Townsend CM Jr., Gao T, Evers BM. mTORC1 inhibition increases neurotensin secretion and gene expression through activation of the MEK/ERK/c-Jun pathway in the human endocrine cell line BON. Am J Physiol Cell Physiol. 2011; 301:C213-26.
100. Gietzen DW, Ross CM, Hao S, Sharp JW. Phosphorylation of eIF2alpha is involved in the signaling of indispensable amino acid deficiency in the anterior piriform cortex of the brain in rats. J Nutr. 2004;134:717-23.
101. Shan J, Lopez MC, Baker HV, Kilberg MS. Expression profiling after activation of the amino acid deprivation response in HepG2 human hepatoma cells. Physiol Genomics. 2010;41:315-27.
102. Lopez-Bergami P, Lau E, Ronai Z. Emerging roles of ATF2 and the dynamic AP1 network in cancer. Nat Rev Cancer. 2010;10:65-76.
103. van Dam H, Duyndam M, Rottier R, Bosch A, de Vries-Smits L, Herrlich P, Zantema A, Angel P, van der Eb AJ. Heterodimer formation of cJun and ATF-2 is responsible for induction of c-jun by the 243 amino acid adenovirus E1A protein. EMBO J. 1993;12:479-87.
104. Morooka H, Bonventre JV, Pombo CM, Kyriakis JM, Force T. Ischemia and reperfusion enhance ATF-2 and c-Jun binding to cAMP response elements and to an AP-1 binding site from the c-jun promoter. J Biol Chem. 1995;270:30084-92.
105. van Dam H, Wilhelm D, Herr I, Steffen A, Herrlich P, Angel P. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 1995;14: 1798-811.
106. Aronheim A, Zandi E, Hennemann H, Elledge SJ, Karin M. Isolation of an AP-1 repressor by a novel method for detecting protein-protein interactions. Mol Cell Biol. 1997;17:3094-102.
107. Jin C, Ugai H, Song J, Murata T, Nili F, Sun K, Horikoshi M, Yokoyama KK. Identification of mouse Jun dimerization protein 2 as a novel repressor of ATF-2. FEBS Lett. 2001;489:34-41.
108. Jin C, Li H, Murata T, Sun K, Horikoshi M, Chiu R, Yokoyama KK. JDP2, a repressor of AP-1, recruits a histone deacetylase 3 complex to inhibit the retinoic acid-induced differentiation of F9 cells. Mol Cell Biol. 2002;22:4815-26.
109. Chérasse Y, Chaveroux C, Jousse C, Maurin AC, Carraro V, Parry L, Fafournoux P, Bruhat A. Role of the repressor JDP2 in the amino acid-regulated transcription of CHOP. FEBS Lett. 2008;582:1537-41.
110. Weidenfeld-Baranboim K, Hasin T, Darlyuk I, Heinrich R, Elhanani O, Pan J, Yokoyama KK, Aronheim A. The ubiquitously expressed bZIP inhibitor, JDP2, suppresses the transcription of its homologue immediate early gene counterpart, ATF3. Nucleic Acids Res. 2009; 37:2194-203.
111. Weidenfeld-Baranboim K, Bitton-Worms K, Aronheim A. TREdependent transcription activation by JDP2-CHOP10 association. Nucleic Acids Res. 2008;36:3608-19.
112. Matsukawa T, Inoue Y, Oishi Y, Kato H, Noguchi T. Up-regulation of upstream stimulatory factors by protein malnutrition and its possible role in regulation of the IGF-binding protein-1 gene. Endocrinology. 2001;142:4643-51.
113. Kokkinakis DM, Liu X, Chada S, Ahmed MM, Shareef MM, Singha UK, Yang S, Luo J. Modulation of gene expression in human central nervous system tumors under methionine deprivation-induced stress. Cancer Res. 2004;64:7513-25.
114. Jiang HY, Wek SA, McGrath BC, Scheuner D, Kaufman RJ, Cavener DR, Wek RC. Phosphorylation of the alpha subunit of eukaryotic initiation factor 2 is required for activation of NF-kappaB in response to diverse cellular stresses. Mol Cell Biol. 2003;23:5651-63.
115. Jiang HY, Wek RC. GCN2 phosphorylation of eIF2alpha activates NF-kappaB in response to UV irradiation. Biochem J. 2005;385: 371-80.
116. Kaestner KH, Knochel W, Martinez DE. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 2000;14:142-6.
117. Imae M, Inoue Y, Fu Z, Kato H, Noguchi T. Gene expression of the three members of hepatocyte nuclear factor-3 is differentially regulated by nutritional and hormonal factors. J Endocrinol. 2000;167: R1-5.
118. Su N, Thiaville MM, Awad K, Gjymishka A, Brant JO, Yang TP, Kilberg MS. Protein or amino acid deprivation differentially regulates the hepatic forkhead box protein A (FOXA) genes through an activating transcription factor-4-independent pathway. Hepatology. 2009;50: 282-90.
119. Deval C, Chaveroux C, Maurin AC, Cherasse Y, Parry L, Carraro V, Milenkovic D, Ferrara M, Bruhat A, Jousse C, et al. Amino acid limitation regulates the expression of genes involved in several specific biological processes through GCN2-dependent and GCN2-independent pathways. FEBS J. 2009;276:707-18.
120. Taylor PM. Amino acid transporters:éminences grises of nutrient signalling mechanisms?. Biochem Soc Trans. 2009;37:237-41.
121. Conigrave AD, Hampson DR. Broad-spectrum L-amino acid sensing by class 3 G-protein-coupled receptors. Trends Endocrinol Metab. 2006;17:398-407.