Transcriptional induction of the human asparagine synthetase gene during the unfolded protein response does not require the ATF6 and IRE1/XBP1 arms of the pathway

Biochemical Journal

Volumn 417, Issue 3, 2009, Pages 695-703

  Gjymishka, Altin ^a   Su, Nan ^a   Kilberg, Michael S ^a  

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

Author keywords

Activating transcription factor (ATF); Asparagine synthetase(ASNS); CCAAT enhancer binding protein (C EBP); Endoplasmic reticulum stress; Nutrient sensing; Unfolded protein response (UPR)

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR (ATF); ASPARAGINE SYNTHETASE(ASNS); CCAAT/ENHANCER-BINDING PROTEIN (C/EBP); ENDOPLASMIC RETICULUM STRESS; UNFOLDED PROTEIN RESPONSE (UPR);

ACTIVATION ANALYSIS; AMINATION; AMINES; AMINO ACIDS; CHEMICAL ACTIVATION; MAMMALS; NUCLEIC ACIDS; NUTRIENTS; ORGANIC ACIDS; RNA; SUGARS; TRANSCRIPTION FACTORS;

TRANSCRIPTION;

ACTIVATING TRANSCRIPTION FACTOR 3; ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA; ACTIVATING TRANSCRIPTION FACTOR 6 BETA; ASPARTATE AMMONIA LIGASE; CCAAT ENHANCER BINDING PROTEIN BETA; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PROTEIN IRE1; PROTEIN KINASE R; RNA POLYMERASE II; SMALL INTERFERING RNA; THAPSIGARGIN; TRANSCRIPTION FACTOR; TUNICAMYCIN; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1; ATF6 PROTEIN, HUMAN; DNA BINDING PROTEIN; ERN2 PROTEIN, HUMAN; MEMBRANE PROTEIN; PROTEIN SERINE THREONINE KINASE; REGULATORY FACTOR X TRANSCRIPTION FACTORS; RIBONUCLEASE;

AMINO ACID RESPONSE; ARTICLE; CELL STRAIN HEPG2; CELL STRESS; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM STRESS RESPONSE ELEMENT 1; ENDOPLASMIC RETICULUM STRESS RESPONSE ELEMENT 2; GENE EXPRESSION REGULATION; GENE SEQUENCE; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MAMMALIAN UNFOLDED PROTEIN RESPONSE ELEMENT; MUTAGENESIS; NUTRIENT SENSING RESPONSE ELEMENT 1; NUTRIENT SENSING RESPONSE ELEMENT 2; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; STEADY STATE; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ENDOPLASMIC RETICULUM; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; TUMOR CELL LINE;

EUKARYOTA; MAMMALIA;

ACTIVATING TRANSCRIPTION FACTOR 6; ASPARTATE-AMMONIA LIGASE; CELL LINE, TUMOR; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; ENDOPLASMIC RETICULUM; ENDORIBONUCLEASES; HUMANS; MEMBRANE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 59849090708     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20081706     Document Type: Article

References (46)

1. Rutkowski, D. T. and Kaufman, R. J. (2004) A trip to the ER: coping with stress. Trends Cell Biol. 14, 20-28
2. van Anken, E. and Braakman, I. (2005) Endoplasmic reticulum stress and the making of a professional secretory cell. Crit. Rev. Biochem. Mol. Biol. 40, 269-283
3. Schroder, M. and Kaufman, R. J. (2005) The mammalian unfolded protein response. Annu. Rev. Biochem. 74, 739-789
4. Guo, F. and Cavener, D. R. (2007) The GCN2 eIF2a kinase regulates fatty-acid homeostasis in the liver during deprivation of an essential amino acid. Cell Metab. 5, 103-114
5. Ron, D. (2002) Translational control in the endoplasmic reticulum stress response. J. Clin. Invest. 110, 1383-1388
6. Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. and Mori, K. (2001) XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881-891
7. Romisch, K. (2005) Endoplasmic reticulum-associated degradation. Annu. Rev. Cell Dev. Biol. 21, 435-456
8. Sriburi, R., Jackowski, S., Mori, K. and Brewer, J. W. (2004) XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167, 35-41
9. Ma, Y., Brewer, J. W., Diehl, J. A. and Hendershot, L. M. (2002) Two distinct stress signaling pathways converge upon the CHOP promoter during the mammalian unfolded protein response. J. Mol. Biol. 318, 1351-1365
10. Pirot, P., Ortis, F., Cnop, M., Ma, Y., Hendershot, L. M., Eizirik, D. L. and Cardozo, A. K. (2007) Transcriptional regulation of the endoplasmic reticulum stress gene chop in pancreatic insulin-producing cells. Diabetes 56, 1069-1077
11. Yoshida, H., Haze, K., Yanagi, H., Yura, T. and Mori, K. (1998) Identification of the cis-acting endoplasmic reticulum stress response element responsible for transcriptional induction of mammalian glucose-regulated proteins. J. Biol. Chem. 273, 33741-33749
12. Yoshida, H., Okada, T., Haze, K., Yanagi, H., Yura, T., Negishi, M. and Mori, K. (2000) ATF6 activated by proteolysis binds in the presence of NF-Y (CBF) directly to the cis-acting element responsible for the mammalian unfolded protein response. Mol. Cell. Biol. 20, 6755-6767
13. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H. and Ron, D. (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904
14. Vattem, K. M. and Wek, R. C. (2004) Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 101, 11269-11274
15. Lu, P. D., Harding, H. P. and Ron, D. (2004) Translation reinitiation at alternative open reading frames regulates gene expression in an integrated stress response. J. Cell Biol. 167, 27-33
16. Ameri, K. and Harris, A. L. (2008) Activating transcription factor 4. Int. J. Biochem. Cell Biol. 40, 14-21
17. Wek, R. C. and Cavener, D. R. (2007) Translational control and the unfolded protein response. Antioxid. Redox Signaling. 9, 2357-2371
18. Dong, J., Qiu, H., Garcia-Barrio, M., Anderson, J. and Hinnebusch, A. G. (2000) Uncharged tRNA activates GCN2 by displacing the protein kinase moiety from a bipartite tRNA-binding domain. Mol. Cell 6, 269-279
19. Berlanga, J. J., Santoyo, J. and De Haro, C. (1999) Characterization of a mammalian homolog of the GCN2 eukaryotic initiation factor 2a kinase. Eur. J. Biochem. 265, 754-762
20. Sood, R., Porter, A. C., Olsen, D. A., Cavener, D. R. and Wek, R. C. (2000) A mammalian homologue of GCN2 protein kinase important for translational control by phosphorylation of eukaryotic initiation factor-2α. Genetics 154, 787-801
21. Barbosa-Tessmann, I. P., Chen, C., Zhong, C., Siu, F., Schuster, S. M., Nick, H. S. and Kilberg, M. S. (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
22. Zhong, C., Chen, C. and Kilberg, M. S. (2003) Characterization of the nutrient sensing response unit in the human asparagine synthetase promoter. Biochem. J. 372 603-609
23. Wolfgang, C. D., Chen, B. P., Martindale, J. L., Holbrook, N. J. and Hai, T. (1997) gadd153/Chop10, a potential target gene of the transcriptional repressor ATF3. Mol. Cell. Biol. 17, 6700-6707
24. Siu, F. Y., Chen, C., Zhong, C. and Kilberg, M. S. (2001) CCAAT/ enhancer-binding protein beta (C/EBPb) is a mediator of the nutrient sensing response pathway that activates the human asparagine synthetase gene. J. Biol. Chem. 276, 48100-48107
25. Siu, F., Bain, P. J., LeBlanc-Chaffin, R., Chen, H. and Kilberg, M. S. (2002) ATF4 is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J. Biol. Chem. 277, 24120-24127
26. Lopez, A. B., Wang, C., Huang, C. C., Yaman, I., Li, Y., Chakravarty, K., Johnson, P. F., Chiang, C. M., Snider, M. D., Wek, R. C. and Hatzoglou, M. (2007) A feedback transcriptional mechanism controls the level of the arginine/lysine transporter cat-1 during amino acid starvation. Biochem. J. 402, 163-173
27. Sheng, S., Moraga, D. A., Van Heeke, G. and Schuster, S. M. (1992) High-level expression of human asparagine synthetase and production of monoclonal antibodies for enzyme purification. Protein Expression Purif. 3, 337-346
28. Chen, H., Pan, Y. X., Dudenhausen, E. E. and Kilberg, M. S. (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
29. Thomas, M. C. and Chiang, C. M. (2006) The general transcription machinery and general cofactors. Crit. Rev. Biochem. Mol. Biol. 41, 105-178
30. Sato, S., Tomomori-Sato, C., Parmely, T. J., Florens, L., Zybailov, B., Swanson, S. K., Banks, C. A., Jin, J., Cai, Y. and Washburn, M. P. et al. (2004) A set of consensus mammalian mediator subunits identified by multidimensional protein identification technology. Mol. Cell 14, 685-691
31. Takagi, Y. and Kornberg, R. D. (2006) Mediator as a general transcription factor. J. Biol. Chem. 281, 80-89
32. Fan, X., Chou, D. M. and Struhl, K. (2006) Activator-specific recruitment of Mediator in vivo. Nat. Struct. Mol. Biol. 13, 117-120
33. Andrau, J. C., van de Pasch, L., Lijnzaad, P., Bijma, T., Koerkamp, M. G., van de Peppel, J., Werner, M. and Holstege, F. C. (2006) Genome-wide location of the coactivator mediator: binding without activation and transient Cdk8 interaction on DNA. Mol. Cell 22, 179-192
34. Zhu, X., Wiren, M., Sinha, I., Rasmussen, N. N., Linder, T., Holmberg, S., Ekwall, K. and Gustafsson, C. M. (2006) Genome-wide occupancy profile of mediator and the Srb8-11 module reveals interactions with coding regions. Mol. Cell 22, 169-178
35. Novoa, I., Zhang, Y., Zeng, H., Jungreis, R., Harding, H. P. and Ron, D. (2003) Stress-induced gene expression requires programmed recovery from translational repression. EMBO J. 22, 1180-1187
36. Cui, H., Darmanin, S., Natsuisaka, M., Kondo, T., Asaka, M., Shindoh, M., Higashino, F., Hamuro, J., Okada, F., Kobayashi, M. et al. (2007) Enhanced expression of asparagine synthetase under glucose-deprived conditions protects pancreatic cancer cells from apoptosis induced by glucose deprivation and cisplatin. Cancer Res. 67, 3345-3355
37. Barbosa-Tessmann, I. P., Chen, C., Zhong, C., Schuster, S. M., Nick, H. S. and Kilberg, M. S. (1999) Activation of the unfolded protein response pathway induces human asparagine synthetase gene expression. J. Biol. Chem. 274, 31139-31144
38. Yoshida, H., Matsui, T., Hosokawa, N., Kaufman, R. J., Nagata, K. and Mori, K. (2003) A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 4, 265-271
39. Yamamoto, K., Sato, T., Matsui, T., Sato, M., Okada, T., Yoshida, H., Harada, A. and Mori, K. (2007) Transcriptional induction of mammalian ER quality control proteins is mediated by single or combined action of ATF6a and XBP1. Dev. Cell 13, 365-376
40. Ma, Y. and Hendershot, L. M. (2004) Herp is dually regulated by both the endoplasmic reticulum stress-specific branch of the unfolded protein response and a branch that is shared with other cellular stress pathways. J. Biol. Chem. 279, 13792-13799
41. Lee, A. H., Iwakoshi, N. N. and Glimcher, L. H. (2003) XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23, 7448-7459
42. Chen, C., Dudenhausen, E. E., Pan, Y., Zhong, C. and Kilberg, M. S. (2004) Human CCAAT/enhancer-binding protein β (C/EBPβ) gene expression is activated by endoplasmic reticulum stress through an unfolded protein response element downstream of the protein coding sequence. J. Biol. Chem. 279, 27948-27956
43. Fernandez, J., Lopez, A. B., Wang, C., Mishra, R., Zhou, L., Yaman, I., Snider, M. D. and Hatzolgou, M. (2003) Transcriptional control of the arginine/lysine transporter, cat-1, by physiological stress. J. Biol. Chem. 278, 50000-50009
44. Kilberg, M. S., Pan, Y. X., Chen, H. and Leung-Pineda, V. (2005) Nutritional control of gene expression: How mammalian cells respond to amino acid limitation. Annu. Rev. Nutr. 25, 59-85
45. Bruhat, A., Averous, J., Carraro, V., Zhong, C., Reimold, A. M., Kilberg, M. S. and Fafournoux, P. (2002) Differences in the molecular mechanisms involved in the transcriptional activation of the CHOP and asparagine synthetase genes in response to amino acid deprivation or activation of the unfolded protein response. J. Biol. Chem. 277, 48107-48114
46. Jousse, C., Bruhat, A., Harding, H. P., Ferrara, M., Ron, D. and Fafournoux, P. (1999) Amino acid limitation regulates CHOP expression through a specific pathway independent of the unfolded protein response. FEBS Lett. 448, 211-216