Drosophila melanogaster activating transcription factor 4 regulates glycolysis during endoplasmic reticulum stress

G3: Genes, Genomes, Genetics

Volumn 5, Issue 4, 2015, Pages 667-675

  Lee, Ji Eun ^a   Oney, McKenna ^a   Frizzell, Kimberly ^a   Phadnis, Nitin ^a   Hollien, Julie ^a  

^a UNIVERSITY OF UTAH   (United States)

Author keywords

Atf4; Endoplasmic reticulum stress; Glycolysis metabolism; Unfolded protein response

Indexed keywords

GLYCOLYTIC ENZYME; LACTATE DEHYDROGENASE; LACTIC ACID; OCTAMER TRANSCRIPTION FACTOR 4; 6 PHOSPHOFRUCTOKINASE; ACTIVATING TRANSCRIPTION FACTOR 4; DOUBLE STRANDED RNA; DROSOPHILA PROTEIN; MULTIENZYME COMPLEX; OXYGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBON METABOLISM; CELL PROLIFERATION; CITRIC ACID CYCLE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; DROSOPHILA MELANOGASTER; FEMALE; GENE EXPRESSION; GLUCOSE METABOLISM; GLYCOLYSIS; MALE; NEOPLASM; NONHUMAN; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PROMOTER REGION; RESPIRATORY CHAIN; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BINDING SITE; ENDOPLASMIC RETICULUM STRESS; GENETICS; METABOLISM; PHYSIOLOGY; RNA INTERFERENCE;

DROSOPHILA MELANOGASTER;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; BINDING SITES; CITRIC ACID CYCLE; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM STRESS; GLYCOLYSIS; L-LACTATE DEHYDROGENASE; LACTIC ACID; MULTIENZYME COMPLEXES; OXYGEN; PHOSPHOFRUCTOKINASES; PROMOTER REGIONS, GENETIC; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; UP-REGULATION;

EID: 84928994228     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.017269     Document Type: Article

References (63)

1. Basseri, S., and R. C. Austin, 2012 Endoplasmic reticulum stress and lipid metabolism: mechanisms and therapeutic potential. Biochem. Res. Int. 2012: 1-13
2. Blais, J. D., V. Filipenko, M. Bi, H. P. Harding, D. Ron et al., 2004 Activating transcription factor 4 is translationally regulated by hypoxic stress. Mol. Cell. Biol. 24: 7469-7482
3. Bouman, L., A. Schlierf, A. K. Lutz, J. Shan, A. Deinlein et al., 2010 Parkin is transcriptionally regulated by ATF4: evidence for an interconnection between mitochondrial stress and ER stress. Cell Death Differ. 18: 769-782
4. Calfon, M., H. Zeng, F. Urano, J. H. Till, S. R. Hubbard et al., 2002 IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415: 92-96
5. Chiang, C.-K., M. Nangaku, T. Tanaka, T. Iwawaki, and R. Inagi, 2013 Endoplasmic reticulum stress signal impairs erythropoietin production: a role for ATF4. Am. J. Physiol. Cell Physiol. 304: C342-C353.
6. Chow, C. Y., M. F. Wolfner, and A. G. Clark, 2013 Using natural variation in Drosophila to discover previously unknown endoplasmic reticulum stress genes. Proc. Natl. Acad. Sci. USA 110: 9013-9018
7. Cox, J. S., C. E. Shamu, and P. Walter, 1993 Transcriptional induction of genes encoding endoplasmic reticulum resident proteins requires a transmembrane protein kinase. Cell 73: 1197-1206
8. Cullinan, S. B., and J. A. Diehl, 2006 Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int. J. Biochem. Cell Biol. 38: 317-332
9. Dang, C. V., 2012 Links between metabolism and cancer. Genes Dev. 26: 877-890
10. Denzel, M. S., N. J. Storm, A. Gutschmidt, R. Baddi, Y. Hinze et al., 2014 Hexosamine pathway metabolites enhance protein quality control and prolong life. Cell 156: 1167-1178
11. Epple, L. M., R. D. Dodd, A. L. Merz, A. M. Dechkovskaia, M. Herring et al., 2013 Induction of the unfolded protein response drives enhanced metabolism and chemoresistance in glioma cells. PLoS One 8: e73267.
12. Fang, M., Z. Shen, S. Huang, L. Zhao, S. Chen et al., 2010 The ER UDPase ENTPD5 promotes protein N-glycosylation, the Warburg effect, and proliferation in the PTEN pathway. Cell 143: 711-724
13. Fawcett, T. W., J. L. Martindale, K. Z. Guyton, T. Hai, and N. J. Holbrook, 1999 Complexes containing activating transcription factor (ATF)/ cAMP-responsive-element-binding protein (CREB) interact with the CCAAT/enhancer-binding protein (C/EBP)-ATF composite site to regulate Gadd153 expression during the stress response. Biochem. J. 339: 135-141
14. Fox, C. J., P. S. Hammerman, and C. B. Thompson, 2005 Fuel feeds function: energy metabolism and the T-cell response. Nat. Rev. Immunol. 5: 844-852
15. Gaddam, D., N. Stevens, and J. Hollien, 2013 Comparison of mRNA localization and regulation during endoplasmic reticulum stress in Drosophila cells. Mol. Biol. Cell 24: 14-20
16. Garg, A. D., A. Kaczmarek, O. Krysko, P. Vandenabeele, D. V. Krysko et al., 2012 ER stress-induced inflammation: does it aid or impede disease progression? Trends Mol. Med. 18: 589-598
17. Gjymishka, A., S. S. Palii, J. Shan, and M. S. Kilberg, 2008 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. 283: 27736-27747
18. Gombart, A. F., J. Grewal, and H. P. Koeffler, 2007 ATF4 differentially regulates transcriptional activation of myeloid-specific genes by C/EB-Pepsilon and C/EBPalpha. J. Leukoc. Biol. 81: 1535-1547
19. Han, J., S. H. Back, J. Hur, Y.-H. Lin, R. Gildersleeve et al., 2013 ERstress-induced transcriptional regulation increases protein synthesis leading to cell death. Nat. Cell Biol. 15: 481-490
20. Harding, H. P., Y. Zhang, and D. Ron, 1999 Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274
21. Harding, H. P., I. Novoa, Y. Zhang, H. Zeng, R. Wek et al., 2000 Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6: 1099-1108
22. Harding, H. P., Y. Zhang, H. Zeng, I. Novoa, P. D. Lu et al., 2003 An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. MOLCEL 11: 619-633
23. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori, 1999 Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell 10: 3787-3799
24. Hewes, R. S., A. M. Schaefer, and P. H. Taghert, 2000 The cryptocephal gene (ATF4) encodes multiple basic-leucine zipper proteins controlling molting and metamorphosis in Drosophila. Genetics 155: 1711-1723
25. Higa, A., and E. Chevet, 2012 Redox signaling loops in the unfolded protein response. Cell. Signal. 24: 1548-1555
26. Hollien, J., 2013 Evolution of the unfolded protein response. Biochim. Biophys. Acta. 1833: 2458-2463
27. Hollien, J., and J. S. Weissman, 2006 Decay of endoplasmic reticulumlocalized mRNAs during the unfolded protein response. Science 313: 104-107
28. Hollien, J., J. H. Lin, H. Li, N. Stevens, P. Walter et al., 2009 Regulated Ire1dependent decay of messenger RNAs in mammalian cells. J. Cell Biol. 186: 323-331
29. Kode, A., I. Mosialou, B. C. Silva, S. Joshi, M. Ferron et al., 2012 FoxO1 protein cooperates with ATF4 protein in osteoblasts to control glucose homeostasis. J. Biol. Chem. 287: 8757-8768
30. Lee, A.-H., E. F. Scapa, D. E. Cohen, and L. H. Glimcher, 2008 Regulation of hepatic lipogenesis by the transcription factor XBP1. Science 320: 1492-1496
31. Li, Y., D. Padmanabha, L. B. Gentile, C. I. Dumur, R. B. Beckstead et al., 2013 HIF- and non-HIF-regulated hypoxic responses require the estrogen-related receptor in Drosophila melanogaster. PLoS Genet. 9: e1003230.
32. Lin, Y. S., and M. R. Green, 1988 Interaction of a common cellular transcription factor, ATF, with regulatory elements in both E1a- and cyclic AMP-inducible promoters. Proc. Natl. Acad. Sci. USA 85: 3396-3400
33. Liu, H., C. C. Jiang, C. J. Lavis, A. Croft, L. Dong et al., 2009 2-Deoxy-Dglucose enhances TRAIL-induced apoptosis in human melanoma cells through XBP-1-mediated up-regulation of TRAIL-R2. Mol. Cancer 8: 122
34. Logue, S., P. Cleary, S. Saveljeva, and A. Samali, 2013 New directions in ER stress-induced cell death. Apoptosis 18: 537-546
35. Marciniak, S. J., C. Y. Yun, S. Oyadomari, I. Novoa, Y. Zhang et al., 2004 CHOP induces death by promoting protein synthesis and oxidation in the stressed endoplasmic reticulum. Genes Dev. 18: 3066-3077
36. Moore, K. A., and J. Hollien, 2012 The unfolded protein response in secretory cell function. Annu. Rev. Genet. 46: 165-183
37. Moore, K. A., J. J. Plant, D. Gaddam, J. Craft, and J. Hollien, 2013 Regulation of sumo mRNA during endoplasmic reticulum stress. PLoS ONE 8: e75723.
38. Mori, K., W. Ma, M. J. Gething, and J. Sambrook, 1993 A transmembrane protein with a cdc2+/CDC28-related kinase activity is required for signaling from the ER to the nucleus. Cell 74: 743-756.
39. Muñoz, J. P., S. Ivanova, J. Sánchez-Wandelmer, P. Martínez-Cristóbal, E. Noguera et al., 2013 Mfn2 modulates the UPR and mitochondrial function via repression of PERK. EMBO J. 32: 2348-2361
40. Palorini, R., F. P. Cammarata, F. Cammarata, C. Balestrieri, A. Monestiroli et al., 2013 Glucose starvation induces cell death in K-rastransformed cells by interfering with the hexosamine biosynthesis pathway and activating the unfolded protein response. Cell Death Dis. 4: e732.
41. Pfeiffer, T., S. Schuster, and S. Bonhoeffer, 2001 Cooperation and competition in the evolution of ATP-producing pathways. Science 292: 504-507
42. Rafalski, V. A., E. Mancini, and A. Brunet, 2012 Energy metabolism and energy-sensing pathways in mammalian embryonic and adult stem cell fate. J. Cell Sci. 125: 5597-5608
43. Ryoo, H. D., and H. Steller, 2007 Unfolded protein response in Drosophila: why another model can make it fly. Cell Cycle 6: 830-835
44. Seo, J., E. S. Fortuno, J. M. Suh, D. Stenesen, W. Tang et al., 2009 Atf4 regulates obesity, glucose homeostasis, and energy expenditure. Diabetes 58: 2565-2573
45. Shen, Z., S. Huang, M. Fang, and X. Wang, 2011 ENTPD5, an endoplasmic reticulum UDPase, alleviates ER stress induced by protein overloading in AKT-activated cancer cells. Cold Spring Harb. Symp. Quant. Biol. 76: 217-223
46. Shi, Y., K. M. Vattem, R. Sood, J. An, J. Liang et al., 1998 Identification and characterization of pancreatic eukaryotic initiation factor 2 alpha-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18: 7499-7509
47. Solaini, G., A. Baracca, G. Lenaz, and G. Sgarbi, 2010 Hypoxia and mitochondrial oxidative metabolism. Biochim. Biophys. Acta 1797: 1171-1177
48. Sriburi, R., 2004 XBP1: a link between the unfolded protein response, lipid biosynthesis, and biogenesis of the endoplasmic reticulum. J. Cell Biol. 167: 35-41
49. Sriburi, R., H. Bommiasamy, G. L. Buldak, G. R. Robbins, M. Frank et al., 2006 Coordinate regulation of phospholipid biosynthesis and secretory pathway gene expression in XBP-1(S)-induced endoplasmic reticulum biogenesis. J. Biol. Chem. 282: 7024-7034
50. Swiech, K., C. S. D. Silva, M. K. Arantes, A. S. dos Santos, R. M. Astray et al., 2008 Characterization of growth and metabolism of Drosophila melanogaster cells transfected with the rabies-virus glycoprotein gene. Biotechnol. Appl. Biochem. 49: 41
51. Tavender, T. J., and N. J. Bulleid, 2010 Peroxiredoxin IV protects cells from oxidative stress by removing H2O2 produced during disulphide formation. J. Cell Sci. 123: 2672-2679.
52. Tennessen, J. M., K. D. Baker, G. Lam, J. Evans, and C. S. Thummel, 2011 The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth. Cell Metab. 13: 139-148
53. Travers, K. J., C. K. Patil, L. Wodicka, D. J. Lockhart, J. S. Weissman et al., 2000 Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101: 249-258
54. Walter, P., and D. Ron, 2011 The unfolded protein response: from stress pathway to homeostatic regulation. Science 334: 1081-1086
55. Wang, M., and R. J. Kaufman, 2014 The impact of the endoplasmic reticulum protein-folding environment on cancer development. Nat. Rev. Cancer 14: 581-597
56. Wang, S., and R. J. Kaufman, 2012 The impact of the unfolded protein response on human disease. J. Cell Biol. 197: 857-867
57. Wang, Y., J. Shen, N. Arenzana, W. Tirasophon, R. J. Kaufman et al., 2000 Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J. Biol. Chem. 275: 27013-27020
58. Wang, Z. V., Y. Deng, N. Gao, Z. Pedrozo, D. L. Li et al., 2014 Spliced Xbox binding protein 1 couples the unfolded protein response to hexosamine biosynthetic pathway. Cell 156: 1179-1192
59. Win, S., T. A. Than, J. C. Fernandez-Checa, and N. Kaplowitz, 2013 JNK interaction with Sab mediates ER stress induced inhibition of mitochondrial respiration and cell death. Cell Death Dis. 5: e989.
60. Wu, M., A. Neilson, A. L. Swift, R. Moran, J. Tamagnine et al., 2007 Multiparameter metabolic analysis reveals a close link between attenuated mitochondrial bioenergetic function and enhanced glycolysis dependency in human tumor cells. Am. J. Physiol. Cell Physiol. 292: C125-C136.
61. Xi, H., M. Kurtoglu, H. Liu, M. Wangpaichitr, M. You et al., 2011 2-Deoxy-D-glucose activates autophagy via endoplasmic reticulum stress rather than ATP depletion. Cancer Chemother. Pharmacol. 67: 899-910
62. Yoshida, H., T. Matsui, A. Yamamoto, T. Okada, and K. Mori, 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
63. Zheng, J., 2012 Energy metabolism of cancer: Glycolysis vs. oxidative phosphorylation (Review). Oncol. Lett. 4: 1151-1157