Identification of a novel amino acid response pathway triggering ATF2 phosphorylation in mammals

Molecular and Cellular Biology

Volumn 29, Issue 24, 2009, Pages 6515-6526

  Chaveroux, Cédric ^a   Jousse, Céline ^a   Cherasse, Yoan ^a   Maurin, Anne Catherine ^a   Parry, Laurent ^a   Carraro, Valérie ^a   Derijard, Benoit ^b   Bruhat, Alain ^a   Fafournoux, Pierre ^a  

^a INRA and University of Auvergne   (France)

^b UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 2; ACTIVATING TRANSCRIPTION FACTOR 3; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN CDC42; RAC1 PROTEIN; SMALL INTERFERING RNA; THREONINE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GCN2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MALNUTRITION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ACTIVATING TRANSCRIPTION FACTOR 2; ACTIVATING TRANSCRIPTION FACTOR 3; ADULT; AMINO ACIDS; ANIMALS; CDC42 GTP-BINDING PROTEIN; CELL LINE; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; GTP-BINDING PROTEIN ALPHA SUBUNITS, G12-G13; HUMANS; MAP KINASE KINASE 7; MAP KINASE KINASE KINASE 1; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 9; PHOSPHORYLATION; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; RAC1 GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STARVATION; TRANSCRIPTION FACTOR CHOP; TRANSCRIPTION FACTORS;

MAMMALIA;

EID: 71949084050     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00489-09     Document Type: Article

References (89)

1. Almeida, E. A., D. Ilic, Q. Han, C. R. Hauck, F. Jin, H. Kawakatsu, D. D. Schlaepfer, and C. H. Damsky. 2000. Matrix survival signaling: from fibronectin via focal adhesion kinase to c-Jun NH(2)-terminal kinase. J. Cell Biol. 149:741-754.
2. Averous, J., A. Bruhat, C. Jousse, V. Carraro, G. Thiel, and P. Fafournoux. 2004. Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J. Biol. Chem. 279:5288-5297.
3. Baan, B., H. van Dam, G. C. van der Zon, J. A. Maassen, and D. M. Ouwens. 2006. The role of c-Jun N-terminal kinase, p38, and extracellular signal-regulated kinase in insulin-induced Thr69 and Thr71 phosphorylation of activating transcription factor 2. Mol. Endocrinol. 20:1786-1795.
4. Baertl, J. M., R. P. Placko, and G. G. Graham. 1974. Serum proteins and plasma free amino acids in severe malnutrition. Am. J. Clin. Nutr. 27:733-742.
5. Barbosa-Tessmann, I. P., C. Chen, C. Zhong, F. Siu, S. M. Schuster, H. S. Nick, and M. S. Kilberg. 2000. Activation of the human asparagine synthetase gene by the amino acid response and the endoplasmic reticulum stress response pathways occurs by common genomic elements. J. Biol. Chem. 275:26976-26985.
6. Bennett, B. L., D. T. Sasaki, B. W. Murray, E. C. O'Leary, S. T. Sakata, W. Xu, J. C. Leisten, A. Motiwala, S. Pierce, Y. Satoh, S. S. Bhagwat, A. M. Manning, and D. W. Anderson. 2001. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. USA 98:13681-13686.
7. Bernard, F., and B. Andre. 2001. Genetic analysis of the signalling pathway activated by external amino acids in Saccharomyces cerevisiae. Mol. Microbiol. 41:489-502.
8. Bhoumik, A., and Z. Ronai. 2008. ATF2: a transcription factor that elicits oncogenic or tumor suppressor activities. Cell Cycle 7:2341-2345.
9. Bisson, N., M. Tremblay, F. Robinson, D. R. Kaplan, S. P. Trusko, and T. Moss. 2008. Mice lacking both mixed-lineage kinase genes Mlk1 and Mlk2 retain a wild type phenotype. Cell Cycle 7:909-916. (Pubitemid 351573786)
10. Boutros, T., E. Chevet, and P. Metrakos. 2008. Mitogen-activated protein (MAP) kinase/MAP kinase phosphatase regulation: roles in cell growth, death, and cancer. Pharmacol. Rev. 60:261-310.
11. Breitwieser, W., S. Lyons, A. M. Flenniken, G. Ashton, G. Bruder, M. Willington, G. Lacaud, V. Kouskoff, and N. Jones. 2007. Feedback regulation of p38 activity via ATF2 is essential for survival of embryonic liver cells. Genes Dev. 21:2069-2082. (Pubitemid 47267292)
12. Bruhat, A., Y. Cherasse, A. C. Maurin, W. Breitwieser, L. Parry, C. Deval, N. Jones, C. Jousse, and P. Fafournoux. 2007. ATF2 is required for amino acid-regulated transcription by orchestrating specific histone acetylation. Nucleic Acids Res. 35:1312-1321. (Pubitemid 46522981)
13. Bruhat, A., C. Jousse, V. Carraro, A. M. Reimold, M. Ferrara, and P. Fafournoux. 2000. Amino acids control mammalian gene transcription: activating transcription factor 2 is essential for the amino acid responsiveness of the CHOP promoter. Mol. Cell. Biol. 20:7192-7204.
14. Chen, H., Y. X. Pan, E. E. Dudenhausen, and M. S. Kilberg. 2004. 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. 279:50829-50839.
15. Chi, H., M. R. Sarkisian, P. Rakic, and R. A. Flavell. 2005. Loss of mitogen-activated protein kinase kinase kinase 4 (MEKK4) results in enhanced apoptosis and defective neural tube development. Proc. Natl. Acad. Sci. USA 102:3846-3851.
16. Conigrave, A. D., and D. R. Hampson. 2006. Broad-spectrum L-amino acid sensing by class 3 G-protein-coupled receptors. Trends Endocrinol. Metab. 17:398-407.
17. Coso, O. A., M. Chiariello, J. C. Yu, H. Teramoto, P. Crespo, N. Xu, T. Miki, and J. S. Gutkind. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81:1137-1146.
18. Cuenda, A., and D. S. Dorow. 1998. Differential activation of stress-activated protein kinase kinases SKK4/MKK7 and SKK1/MKK4 by the mixed-lineage kinase-2 and mitogen-activated protein kinase kinase (MKK) kinase-1. Biochem. J. 333:11-15. (Pubitemid 28342486)
19. Davies, S. P., H. Reddy, M. Caivano, and P. Cohen. 2000. Specificity and mechanism of action of some commonly used protein kinase inhibitors. Biochem. J. 351:95-105.
20. Davis, R. J. 2000. Signal transduction by the JNK group of MAP kinases. Cell 103:239-252.
21. Derijard, B., M. Hibi, I. H. Wu, T. Barrett, B. Su, T. Deng, M. Karin, and R. J. Davis. 1994. JNK1: a protein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76:1025-1037. (Pubitemid 24106383)
22. Derijard, B., J. Raingeaud, T. Barrett, I. H. Wu, J. Han, R. J. Ulevitch, and R. J. Davis. 1995. Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682-685.
23. Dermott, J. M., J. H. Ha, C. H. Lee, and N. Dhanasekaran. 2004. Differential regulation of Jun N-terminal kinase and p38MAP kinase by Galpha12. Oncogene 23:226-232.
24. Deval, C., C. Chaveroux, A. C. Maurin, Y. Cherasse, L. Parry, V. Carraro, D. Milenkovic, M. Ferrara, A. Bruhat, C. Jousse, and P. Fafournoux. 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.
25. Dickens, M., J. S. Rogers, J. Cavanagh, A. Raitano, Z. Xia, J. R. Halpern, M. E. Greenberg, C. L. Sawyers, and R. J. Davis. 1997. A cytoplasmic inhibitor of the JNK signal transduction pathway. Science 277:693-696. (Pubitemid 27373916)
26. Fafournoux, P., A. Bruhat, and C. Jousse. 2000. Amino acid regulation of gene expression. Biochem. J. 351:1-12. (Pubitemid 30781551)
27. Fanger, G. R., P. Gerwins, C. Widmann, M. B. Jarpe, and G. L. Johnson. 1997. MEKKs, GCKs, MLKs, PAKs, TAKs, and tpls: upstream regulators of the c-Jun amino-terminal kinases? Curr. Opin. Genet. Dev. 7:67-74.
28. Forsberg, H., C. F. Gilstring, A. Zargari, P. Martinez, and P. O. Ljungdahl. 2001. The role of the yeast plasma membrane SPS nutrient sensor in the metabolic response to extracellular amino acids. Mol. Microbiol. 42:215-228.
29. Goldsmith, Z. G., and D. N. Dhanasekaran. 2007. G protein regulation of MAPK networks. Oncogene 26:3122-3142.
30. Gupta, S., D. Campbell, B. Derijard, and R. J. Davis. 1995. Transcription factor ATF2 regulation by the JNK signal transduction pathway. Science 267:389-393.
31. Harding, H. P., Y. Zhang, H. Zeng, I. Novoa, P. D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, R. Paules, D. F. Stojdl, J. C. Bell, T. Hettmann, J. M. Leiden, and D. Ron. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619-633.
32. Hartman, M. G., D. Lu, M. L. Kim, G. J. Kociba, T. Shukri, J. Buteau, X. Wang, W. L. Frankel, D. Guttridge, M. Prentki, S. T. Grey, D. Ron, and T. Hai. 2004. Role for activating transcription factor 3 in stress-induced β-cell apoptosis. Mol. Cell. Biol. 24:5721-5732.
33. Hashimoto, Y., C. Zhang, J. Kawauchi, I. Imoto, M. T. Adachi, J. Inazawa, T. Amagasa, T. Hai, and S. Kitajima. 2002. An alternatively spliced isoform of transcriptional repressor ATF3 and its induction by stress stimuli. Nucleic Acids Res. 30:2398-2406. (Pubitemid 34618991)
34. Hayakawa, J., S. Mittal, Y. Wang, K. S. Korkmaz, E. Adamson, C. English, M. Ohmichi, M. McClelland, and D. Mercola. 2004. Identification of promoters bound by c-Jun/ATF2 during rapid large-scale gene activation following genotoxic stress. Mol. Cell 16:521-535. (Pubitemid 39531876)
35. Heasman, S. J., and A. J. Ridley. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9:690-701.
36. Hirai, S., A. Kawaguchi, J. Suenaga, M. Ono, D. F. Cui, and S. Ohno. 2005. Expression of MUK/DLK/ZPK, an activator of the JNK pathway, in the nervous systems of the developing mouse embryo. Gene Expr. Patterns 5:517-523. (Pubitemid 40331391)
37. Hundal, H. S., and P. M. Taylor. 2009. Amino acid transceptors: gate keepers of nutrient exchange and regulators of nutrient signaling. Am. J. Physiol. Endocrinol Metab. 296:E603-E613.
38. Ichijo, H., E. Nishida, K. Irie, P. ten Dijke, M. Saitoh, T. Moriguchi, M. Takagi, K. Matsumoto, K. Miyazono, and Y. Gotoh. 1997. Induction of apoptosis by ASK1, a mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways. Science 275:90-94.
39. Itoh, R. E., E. Kiyokawa, K. Aoki, T. Nishioka, T. Akiyama, and M. Matsuda. 2008. Phosphorylation and activation of the Rac1 and Cdc42 GEF Asef in A431 cells stimulated by EGF. J. Cell Sci. 121:2635-2642.
40. Jackson, A. A., and M. S. Grimble. 1990. The malnourished child, vol.19. Raven Press, Vevey, Switzerland.
41. Jeevanandam, M., G. D. Horowitz, S. F. Lowry, and M. F. Brennan. 1984. Cancer cachexia and protein metabolism. Lancet i(8392):1423-1426.
42. Jiang, H. Y., and R. C. Wek. 2005. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2alpha) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J. Biol. Chem. 280:14189-14202.
43. Jiang, H. Y., S. A. Wek, B. C. McGrath, D. Lu, T. Hai, H. P. Harding, X. Wang, D. Ron, D. R. Cavener, and R. C. Wek. 2004. Activating transcription factor 3 is integral to the eukaryotic initiation factor 2 kinase stress response. Mol. Cell. Biol. 24:1365-1377.
44. Jousse, C., J. Averous, A. Bruhat, V. Carraro, S. Mordier, and P. Fafournoux. 2004. Amino acids as regulators of gene expression: molecular mechanisms. Biochem. Biophys. Res. Commun. 313:447-452.
45. Jousse, C., C. Deval, A. C. Maurin, L. Parry, Y. Cherasse, C. Chaveroux, R. Lefloch, P. Lenormand, A. Bruhat, and P. Fafournoux. 2007. TRB3 inhibits the transcriptional activation of stress-regulated genes by a negative feedback on the ATF4 pathway. J. Biol. Chem. 282:15851-15861.
46. Kawai, T., J. Fan, K. Mazan-Mamczarz, and M. Gorospe. 2004. Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell. Biol. 24:6773-6787.
47. Kilberg, M. S., Y. X. Pan, H. Chen, and V. Leung-Pineda. 2005. Nutritional control of gene expression: how mammalian cells respond to amino acid limitation. Annu. Rev. Nutr. 25:59-85.
48. Kim, E. K., K. T. Noh, J. H. Yoon, J. H. Cho, K. W. Yoon, G. Dreyfuss, and E. J. Choi. 2007. Positive regulation of ASK1-mediated c-Jun NH(2)-terminal kinase signaling pathway by the WD-repeat protein Gemin5. Cell Death Differ. 14:1518-1528.
49. Kroeze, W. K., D. J. Sheffler, and B. L. Roth. 2003. G-protein-coupled receptors at a glance. J. Cell Sci. 116:4867-4869.
50. Kurokawa, K., R. E. Itoh, H. Yoshizaki, Y. O. Nakamura, and M. Matsuda. 2004. Coactivation of Rac1 and Cdc42 at lamellipodia and membrane ruffles induced by epidermal growth factor. Mol. Biol. Cell 15:1003-1010.
51. Li, M. G., K. Katsura, H. Nomiyama, K. Komaki, J. Ninomiya-Tsuji, K. Matsumoto, T. Kobayashi, and S. Tamura. 2003. Regulation of the interleukin- 1-induced signaling pathways by a novel member of the protein phosphatase 2C family (PP2Cepsilon). J. Biol. Chem. 278:12013-12021.
52. Liao, X. H., A. Majithia, X. Huang, and A. R. Kimmel. 2008. Growth control via TOR kinase signaling, an intracellular sensor of amino acid and energy availability, with crosstalk potential to proline metabolism. Amino Acids 35:761-770.
53. Livingstone, C., G. Patel, and N. Jones. 1995. ATF-2 contains a phosphorylation-dependent transcriptional activation domain. EMBO J. 14:1785-1797.
54. Ljungdahl, P. O. 2009. Amino-acid-induced signalling via the SPS-sensing pathway in yeast. Biochem. Soc. Trans. 37:242-247.
55. Lopez, A. B., C. Wang, C. C. Huang, I. Yaman, Y. Li, K. Chakravarty, P. F. Johnson, C. M. Chiang, M. D. Snider, R. C. Wek, and M. Hatzoglou. 2007. A feedback transcriptional mechanism controls the level of the arginine/lysine transporter cat-1 during amino acid starvation. Biochem. J. 402:163-173.
56. Lu, P. D., H. P. Harding, and D. Ron. 2004. Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167:27-33.
57. Lu, P. D., C. Jousse, S. J. Marciniak, Y. Zhang, I. Novoa, D. Scheuner, R. J. Kaufman, D. Ron, and H. P. Harding. 2004. Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J. 23: 169-179. (Pubitemid 38165757)
58. Marciniak, S. J., C. Y. Yun, S. Oyadomari, I. Novoa, Y. Zhang, R. Jungreis, K. Nagata, H. P. Harding, and D. Ron. 2004. CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18:3066-3077.
59. Maurin, A. C., C. Jousse, J. Averous, L. Parry, A. Bruhat, Y. Cherasse, H. Zeng, Y. Zhang, H. P. Harding, D. Ron, and P. Fafournoux. 2005. The GCN2 kinase biases feeding behavior to maintain amino acid homeostasis in omnivores. Cell Metab. 1:273-277. (Pubitemid 43960610)
60. Morton, S., R. J. Davis, and P. Cohen. 2004. Signalling pathways involved in multisite phosphorylation of the transcription factor ATF-2. FEBS Lett. 572:177-183. (Pubitemid 39092532)
61. Nicklin, P., P. Bergman, B. Zhang, E. Triantafellow, H. Wang, B. Nyfeler, H. Yang, M. Hild, C. Kung, C. Wilson, V. E. Myer, J. P. MacKeigan, J. A. Porter, Y. K. Wang, L. C. Cantley, P. M. Finan, and L. O. Murphy. 2009. Bidirectional transport of amino acids regulates mTOR and autophagy. Cell 136:521-534.
62. Nicola, C., P. K. Lala, and C. Chakraborty. 2008. Prostaglandin E2-mediated migration of human trophoblast requires RAC1 and CDC42. Biol. Reprod. 78:976-982.
63. Ogino, T., M. Ozaki, M. Hosako, M. Omori, S. Okada, and A. Matsukawa. 2009. Activation of c-Jun N-terminal kinase is essential for oxidative stress-induced Jurkat cell apoptosis by monochloramine. Leuk. Res. 33:151-158.
64. Ornatsky, O. I., D. M. Cox, P. Tangirala, J. J. Andreucci, Z. A. Quinn, J. L. Wrana, R. Prywes, Y. T. Yu, and J. C. McDermott. 1999. Post-translational control of the MEF2A transcriptional regulatory protein. Nucleic Acids Res. 27:2646-2654.
65. Ouwens, D. M., N. D. de Ruiter, G. C. van der Zon, A. P. Carter, J. Schouten, C. van der Burgt, K. Kooistra, J. L. Bos, J. A. Maassen, and H. van Dam. 2002. Growth factors can activate ATF2 via a two-step mechanism: phosphorylation of Thr71 through the Ras-MEK-ERK pathway and of Thr69 through RalGDS-Src-p38. EMBO J. 21:3782-3793.
66. Palii, S. S., H. Chen, and M. S. Kilberg. 2004. Transcriptional control of the human sodium-coupled neutral amino acid transporter system A gene by amino acid availability is mediated by an intronic element. J. Biol. Chem. 279:3463-3471.
67. Palii, S. S., C. E. Kays, C. Deval, A. Bruhat, P. Fafournoux, and M. S. Kilberg. 2009. Specificity of amino acid regulated gene expression: analysis of genes subjected to either complete or single amino acid deprivation. Amino Acids 37:79-88.
68. Pan, Y. X., H. Chen, M. M. Thiaville, and M. S. Kilberg. 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.
69. Peng, T., T. R. Golub, and D. M. Sabatini. 2002. The immunosuppressant rapamycin mimics a starvation-like signal distinct from amino acid and glucose deprivation. Mol. Cell. Biol. 22:5575-5584.
70. Prasad, M. V., J. M. Dermott, L. E. Heasley, G. L. Johnson, and N. Dhanasekaran. 1995. Activation of Jun kinase/stress-activated protein kinase by GTPase-deficient mutants of G alpha 12 and G alpha 13. J. Biol. Chem. 270:18655-18659.
71. Proud, C. G. 2007. Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem. J. 403:217-234.
72. Regard, J. B., I. T. Sato, and S. R. Coughlin. 2008. Anatomical profiling of G protein-coupled receptor expression. Cell 135:561-571.
73. Schiller, M. R. 2006. Coupling receptor tyrosine kinases to Rho GTPases - GEFs what's the link. Cell. Signal. 18:1834-1843.
74. Sinha, S., and W. Yang. 2008. Cellular signaling for activation of Rho GTPase Cdc42. Cell. Signal. 20:1927-1934.
75. Siu, F., P. J. Bain, R. LeBlanc-Chaffin, H. Chen, and M. S. Kilberg. 2002. ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J. Biol. Chem. 277:24120-24127.
76. Suzuki, N., N. Hajicek, and T. Kozasa. 2009. Regulation and physiological functions of G12/13-mediated signaling pathways. Neurosignals 17:55-70.
77. Szczepankiewicz, B. G., C. Kosogof, L. T. Nelson, G. Liu, B. Liu, H. Zhao, M. D. Serby, Z. Xin, M. Liu, R. J. Gum, D. L. Haasch, S. Wang, J. E. Clampit, E. F. Johnson, T. H. Lubben, M. A. Stashko, E. T. Olejniczak, C. Sun, S. A. Dorwin, K. Haskins, C. Abad-Zapatero, E. H. Fry, C. W. Hutchins, H. L. Sham, C. M. Rondinone, and J. M. Trevillyan. 2006. Aminopyridine-based c-Jun N-terminal kinase inhibitors with cellular activity and minimal cross-kinase activity. J. Med. Chem. 49:3563-3580.
78. Thiaville, M. M., Y. X. Pan, A. Gjymishka, C. Zhong, R. J. Kaufman, and M. S. Kilberg. 2008. MEK signaling is required for phosphorylation of eIF2alpha following amino acid limitation of HepG2 human hepatoma cells. J. Biol. Chem. 283:10848-10857.
79. Tournier, C., A. J. Whitmarsh, J. Cavanagh, T. Barrett, and R. J. Davis. 1997. Mitogen-activated protein kinase kinase 7 is an activator of the c-Jun NH2-terminal kinase. Proc. Natl. Acad. Sci. USA 94:7337-7342.
80. van Dam, H., D. Wilhelm, I. Herr, A. Steffen, P. Herrlich, and P. Angel. 1995. ATF-2 is preferentially activated by stress-activated protein kinases to mediate c-jun induction in response to genotoxic agents. EMBO J. 14:1798-1811.
81. Vattem, K. M., and R. C. Wek. 2004. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. USA 101:11269-11274.
82. Vlahopoulos, S. A., S. Logotheti, D. Mikas, A. Giarika, V. Gorgoulis, and V. Zoumpourlis. 2008. The role of ATF-2 in oncogenesis. Bioessays 30:314-327.
83. Wang, X., A. Beugnet, M. Murakami, S. Yamanaka, and C. G. Proud. 2005. Distinct signaling events downstream of mTOR cooperate to mediate the effects of amino acids and insulin on initiation factor 4E-binding proteins. Mol. Cell. Biol. 25:2558-2572.
84. Wang, X., A. Destrument, and C. Tournier. 2007. Physiological roles of MKK4 and MKK7: insights from animal models. Biochim. Biophys. Acta 1773:1349-1357.
85. Whitmarsh, A. J. 2006. The JIP family of MAPK scaffold proteins. Biochem. Soc. Trans. 34:828-832.
86. Wolfe, R. R., F. Jahoor, and W. H. Hartl. 1989. Protein and amino acid metabolism after injury. Diabetes Metab. Rev. 5:149-164.
87. Xu, Z., N. V. Kukekov, and L. A. Greene. 2003. POSH acts as a scaffold for a multiprotein complex that mediates JNK activation in apoptosis. EMBO J. 22:252-261. (Pubitemid 36119431)
88. Zhao, M., L. New, V. V. Kravchenko, Y. Kato, H. Gram, F. di Padova, E. N. Olson, R. J. Ulevitch, and J. Han. 1999. Regulation of the MEF2 family of transcription factors by p38. Mol. Cell. Biol. 19:21-30.
89. Ziegler, T. R., C. Gatzen, and D. W. Wilmore. 1994. Strategies for attenuating protein-catabolic responses in the critically ill. Annu. Rev. Med. 45: 459-480.