Regulation of autophagy by ATF4 in response to severe hypoxia

Oncogene

Volumn 29, Issue 31, 2010, Pages 4424-4435

  Rzymski, T ^a   Milani, M ^a   Pike, L ^a   Buffa, F ^a   Mellor, H R ^a   Winchester, L ^b   Pires, I ^c   Hammond, E ^c   Ragoussis, I ^b   Harris, A L ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

anoxia; autophagy; cancer; hypoxia; tumour; UPR

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; BORTEZOMIB; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; SMALL INTERFERING RNA;

ARTICLE; AUTOPHAGY; BINDING SITE; CANCER CELL; CELL DEATH; CELL SURVIVAL; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; FEMALE; GENE CONTROL; GENOME ANALYSIS; HUMAN; HUMAN CELL; HYPOXIA; MICROARRAY ANALYSIS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN STABILITY; REGULATORY MECHANISM; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ANTINEOPLASTIC AGENTS; AUTOPHAGY; BASE SEQUENCE; BORONIC ACIDS; CELL HYPOXIA; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOPLASMIC RETICULUM; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HCT116 CELLS; HELA CELLS; HUMANS; NEOPLASMS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN; PYRAZINES; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; UNFOLDED PROTEIN RESPONSE; VALIDATION STUDIES AS TOPIC;

EID: 77955467319     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2010.191     Document Type: Article

References (41)

1. Ameri K, Lewis CE, Raida M, Sowter H, Hai T, Harris AL. (2004). Anoxic induction of ATF-4 through HIF-1-independent pathways of protein stabilization in human cancer cells. Blood 103: 1876-1882.
2. Averous J, Bruhat A, Jousse C, Carraro V, Thiel G, Fafournoux P. (2004). Induction of CHOP expression by amino acid limitation requires both ATF4 expression and ATF2 phosphorylation. J Biol Chem 279: 5288-5297.
3. Azad MB, Chen Y, Henson ES, Cizeau J, McMillan-Ward E, Israels SJ et al. (2008). Hypoxia induces autophagic cell death in apoptosiscompetent cells through a mechanism involving BNIP3. Autophagy 4: 195-204.
4. Bernales S, McDonald KL, Walter P. (2006). Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4: e423.
5. Bi M, Naczki C, Koritzinsky M, Fels D, Blais J, Hu N et al. (2005). ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth. EMBO J 24: 3470-3481.
6. Blais JD, Addison CL, Edge R, Falls T, Zhao H, Wary K et al. (2006). Perk-dependent translational regulation promotes tumor cell adaptation and angiogenesis in response to hypoxic stress. Mol Cell Biol 26: 9517-9532.
7. Graeber TG, Osmanian C, Jacks T, Housman DE, Koch CJ, Lowe SW et al. (1996). Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379: 88-91.
8. Harding HP, Zhang Y, Ron D. (1999). Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397: 271-274.
9. Harding HP, Zhang Y, Bertolotti A, Zeng H, Ron D. (2000). Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol Cell 5: 897-904.
10. 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.
11. Harris AL. (2002). Hypoxia\a key regulatory factor in tumour growth. Nat Rev Cancer 2: 38-47.
12. He H, Dang Y, Dai F, Guo Z, Wu J, She X et al. (2003). Posttranslational modifications of three members of the human MAP1LC3 family and detection of a novel type of modification for MAP1LC3B. J Biol Chem 278: 29278-29287.
13. Karpinski BA, Morle GD, Huggenvik J, Uhler MD, Leiden JM. (1992). Molecular cloning of human CREB-2: an ATF/CREB transcription factor that can negatively regulate transcription from the cAMP response element. Proc Natl Acad Sci USA 89: 4820-4824.
14. Koumenis C, Naczki C, Koritzinsky M, Rastani S, Diehl A, Sonenberg N et al. (2002). Regulation of protein synthesis by hypoxia via activation of the endoplasmic reticulum kinase PERK and phosphorylation of the translation initiation factor eIF2alpha. Mol Cell Biol 22: 7405-7416.
15. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H et al. (2007). ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14: 230-239.
16. Kroemer G, Jaattela M. (2005). Lysosomes and autophagy in cell death control. Nat Rev Cancer 5: 886-897.
17. Kuma A, Hatano M, Matsui M, Yamamoto A, Nakaya H, Yoshimori T et al. (2004). The role of autophagy during the early neonatal starvation period. Nature 432: 1032-1036.
18. Lu PD, Jousse C, Marciniak SJ, Zhang Y, Novoa I, Scheuner D et al. (2004). Cytoprotection by pre-emptive conditional phosphorylation of translation initiation factor 2. EMBO J 23: 169-179.
19. Lum JJ, Bauer DE, Kong M, Harris MH, Li C, Lindsten T et al. (2005). Growth factor regulation of autophagy and cell survival in the absence of apoptosis. Cell 120: 237-248.
20. Milani M, Rzymski T, Mellor HR, Pike L, Bottini A, Generali D et al. (2009). The role of ATF4 stabilization and autophagy in resistance of breast cancer cells treated with Bortezomib. Cancer Res 69: 4415-4423.
21. Mizushima N, Yamamoto A, Matsui M, Yoshimori T, Ohsumi Y. (2004). in vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell 15: 1101-1111.
22. Mujcic H, Rzymski T, Rouschop KM, Koritzinsky M, Milani M, Harris AL et al. (2009). Hypoxic activation of the unfolded protein response (UPR) induces expression of the metastasis-associated gene LAMP3. Radiother Oncol 92: 450-459.
23. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S et al. (2006). Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26: 9220-9231.
24. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. (2005). TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24: 1243-1255.
25. Olive PL, Banath JP, Durand RE. (2002). The range of oxygenation in SiHa tumor xenografts. Radiat Res 158: 159-166.
26. Papandreou I, Krishna C, Kaper F, Cai D, Giaccia AJ, Denko NC. (2005). Anoxia is necessary for tumor cell toxicity caused by a low-oxygen environment. Cancer Res 65: 3171-3178.
27. Rouschop KM, van den Beucken T, Dubois L, Niessen H, Bussink J, Savelkouls K et al. (2009). The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J Clin Invest 120: 127-141.
28. Rzymski T, Paantjens A, Bod J, Harris AL. (2008). Multiple pathways are involved in the anoxia response of SKIP3 including HuRregulated RNA stability, NF-kappaB and ATF4. Oncogene 27: 4532-4543.
29. Rzymski T, Milani M, Singleton DC, Harris AL. (2009). Role of ATF4 in regulation of autophagy and resistance to drugs and hypoxia. Cell Cycle 8: 3838-3847.
30. Sarkar S, Perlstein EO, Imarisio S, Pineau S, Cordenier A, Maglathlin RL et al. (2007). Small molecules enhance autophagy and reduce toxicity in Huntington's disease models. Nat Chem Biol 3: 331-338.
31. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P et al. (2001). Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7: 1165-1176.
32. Semenza GL. (2003). Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3: 721-732.
33. Semenza GL. (2008). Mitochondrial autophagy: life and breath of the cell. Autophagy 4: 534-536.
34. Shimizu S, Kanaseki T, Mizushima N, Mizuta T, Arakawa-Kobayashi S, Thompson CB et al. (2004). Role of Bcl-2 family proteins in a non-apoptotic programmed cell death dependent on autophagy genes. Nat Cell Biol 6: 1221-1228.
35. Shintani T, Klionsky DJ. (2004). Autophagy in health and disease: a double-edged sword. Science 306: 990-995.
36. Tu BP, Weissman JS. (2004). Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164: 341-346.
37. Wenger RH, Gassmann M. (1996). Little difference. Nature 380: 100.
38. Wouters BG, Brown JM. (1997). Cells at intermediate oxygen levels can be more important than the 'hypoxic fraction' in determining tumor response to fractionated radiotherapy. Radiat Res 147: 541-550.
39. Wu J, Dang Y, Su W, Liu C,Ma H, Shan Y et al. (2006).Molecular cloning and characterization of rat LC3A and LC3B\two novel markers of autophagosome. Biochem Biophys Res Commun 339: 437-442.
40. Yamamoto A, Tagawa Y, Yoshimori T, Moriyama Y, Masaki R, Tashiro Y. (1998). Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct 23: 33-42.
41. Yorimitsu T, Nair U, Yang Z, Klionsky DJ. (2006). Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281: 30299-30304.