DNA damage and eIF4G1 in breast cancer cells reprogram translation for survival and DNA repair mRNAs

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 46, 2012, Pages 18767-18772

  Badura, Michelle ^a,b   Braunstein, Steve ^a,c   Zavadil, Jiri ^a   Schneider, Robert J ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

eIF; Translational control

Indexed keywords

ATM PROTEIN; BINDING PROTEIN; CHECKPOINT KINASE 1; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INITIATION FACTOR 4E; INITIATION FACTOR 4G; INITIATION FACTOR 4G1; INITIATION FACTOR 4G2; MEIOTIC RECOMBINATION PROTEIN 11; MESSENGER RNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; PROTEIN P53; REPLICATION FACTOR C; UNCLASSIFIED DRUG; X LINKED INHIBITOR OF APOPTOSIS;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOPHAGY; BREAST CANCER; CANCER CELL; CELL CYCLE ARREST; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; GENOTOXICITY; IONIZING RADIATION; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; PROTEIN SYNTHESIS; RNA TRANSLATION;

CELL LINE, TUMOR; CELL SURVIVAL; DNA DAMAGE; DNA REPAIR; DNA, NEOPLASM; EUKARYOTIC INITIATION FACTOR-4G; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NEOPLASM PROTEINS; PROTEIN BIOSYNTHESIS; RNA, MESSENGER; RNA, NEOPLASM;

ATAXIA TELANGIECTASIA; EUKARYOTA;

EID: 84869216705     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1203853109     Document Type: Article

References (47)

1. Hakem R (2008) DNA-damage repair; the good, the bad, and the ugly. EMBO J 27(4):589-605.
2. Braunstein S, Badura ML, Xi Q, Formenti SC, Schneider RJ (2009) Regulation of protein synthesis by ionizing radiation. Mol Cell Biol 29(21):5645-5656.
3. Powley IR, et al. (2009) Translational reprogramming following UVB irradiation is mediated by DNA-PKcs and allows selective recruitment to the polysomes of mRNAs encoding DNA repair enzymes. Genes Dev 23(10):1207-1220.
4. Budanov AV, Karin M (2008) p53 target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134(3):451-460.
5. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18(16):1926-1945.
6. Holcik M, Sonenberg N, Korneluk RG (2000) Internal ribosome initiation of translation and the control of cell death. Trends Genet 16(10):469-473.
7. de Breyne S, Yu Y, Unbehaun A, Pestova TV, Hellen CU (2009) Direct functional interaction of initiation factor eIF4G with type 1 internal ribosomal entry sites. Proc Natl Acad Sci USA 106(23):9197-9202.
8. Hundsdoerfer P, Thoma C, Hentze MW (2005) Eukaryotic translation initiation factor 4GI and p97 promote cellular internal ribosome entry sequence-driven translation. Proc Natl Acad Sci USA 102(38):13421-13426.
9. Ramírez-Valle F, Braunstein S, Zavadil J, Formenti SC, Schneider RJ (2008) eIF4GI links nutrient sensing by mTOR to cell proliferation and inhibition of autophagy. J Cell Biol 181(2):293-307.
10. Braunstein S, et al. (2007) A hypoxia-controlled cap-dependent to cap-independent translation switch in breast cancer. Mol Cell 28(3):501-512.
11. Shatsky IN, Dmitriev SE, Terenin IM, Andreev DE (2010) Cap- and IRES-independent scanning mechanism of translation initiation as an alternative to the concept of cellular IRESs. Mol Cells 30(4):285-293.
12. Clarkson BK, Gilbert WV, Doudna JA (2010) Functional overlap between eIF4G isoforms in Saccharomyces cerevisiae. PLoS ONE 5(2):e9114.
13. Park EH, Zhang F, Warringer J, Sunnerhagen P, Hinnebusch AG (2011) Depletion of eIF4G from yeast cells narrows the range of translational efficiencies genome-wide. BMC Genomics 12:68.
14. Franklin-Dumont TM, Chatterjee C, Wasserman SA, Dinardo S (2007) A novel eIF4G homolog, Off-schedule, couples translational control to meiosis and differentiation in Drosophila spermatocytes. Development 134(15):2851-2861.
15. Baker CC, Fuller MT (2007) Translational control of meiotic cell cycle progression and spermatid differentiation in male germ cells by a novel eIF4G homolog. Development 134(15):2863-2869.
16. Imataka H, Olsen HS, Sonenberg N (1997) A new translational regulator with homology to eukaryotic translation initiation factor 4G. EMBO J 16(4):817-825.
17. Marash L, et al. (2008) DAP5 promotes cap-independent translation of Bcl-2 and CDK1 to facilitate cell survival during mitosis. Mol Cell 30(4):447-459.
18. Silvera D, et al. (2009) Inflammatory breast cancer pathogenesis mediated by translation initiation factor eIF4G overexpression and unorthodox protein synthesis. Nat Cell Biol 11(7):903-910.
19. Silvera D, Formenti SC, Schneider RJ (2010) Translational control in cancer. Nat Rev Cancer 10(4):254-266.
20. Comtesse N, et al. (2007) Frequent overexpression of the genes FXR1, CLAPM1 and EIF4G located on amplicon 3q26-27 in squamous cell carcinoma of the lung. Int J Cancer 120(12):2538-2544.
21. Albert JM, Kim KW, Cao C, Lu B (2006) Targeting the Akt/mammalian target of rapamycin pathway for radiosensitization of breast cancer. Mol Cancer Ther 5(5):1183-1189.
22. Eisenberg-Lerner A, Kimchi A (2009) The paradox of autophagy and its implication in cancer etiology and therapy. Apoptosis 14(4):376-391.
23. Chen JH, Hales CN, Ozanne SE (2007) DNA damage, cellular senescence and organismal ageing: Causal or correlative? Nucleic Acids Res 35(22):7417-7428.
24. Lavin MF, et al. (2005) ATM signaling and genomic stability in response to DNA damage. Mutat Res 569(1-2):123-132.
25. Fillingham J, Keogh MC, Krogan NJ (2006) GammaH2AX and its role in DNA double-strand break repair. Biochem Cell Biol 84(4):568-577.
26. Moeller BJ, Dewhirst MW (2006) HIF-1 and tumour radiosensitivity. Br J Cancer 95(1):1-5.
27. Zhan Q (2005) Gadd45a, a p53- and BRCA1-regulated stress protein, in cellular response to DNA damage. Mutat Res 569(1-2):133-143.
28. Chang Q, et al. (2007) Incorporation of an internal ribosome entry site-dependent mechanism in arsenic-induced GADD45 alpha expression. Cancer Res 67(13):6146-6154.
29. Kolupaeva VG, Pestova TV, Hellen CU, Shatsky IN (1998) Translation eukaryotic initiation factor 4G recognizes a specific structural element within the internal ribosome entry site of encephalomyocarditis virus RNA. J Biol Chem 273(29):18599-18604.
30. Svitkin YV, et al. (2005) Eukaryotic translation initiation factor 4E availability controls the switch between cap-dependent and internal ribosomal entry site-mediated translation. Mol Cell Biol 25(23):10556-10565.
31. Ali IK, McKendrick L, Morley SJ, Jackson RJ (2001) Truncated initiation factor eIF4G lacking an eIF4E binding site can support capped mRNA translation. EMBO J 20(15):4233-4242.
32. De Gregorio E, Preiss T, Hentze MW (1999) Translation driven by an eIF4G core domain in vivo. EMBO J 18(17):4865-4874.
33. Graff JR, et al. (2007) Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest 117(9):2638-2648.
34. Pesole G, et al. (2001) Structural and functional features of eukaryotic mRNA untranslated regions. Gene 276(1-2):73-81.
35. Babendure JR, Babendure JL, Ding JH, Tsien RY (2006) Control of mammalian translation by mRNA structure near caps. RNA 12(5):851-861.
36. Hu SI, et al. (2012) MNK2 inhibits eIF4G activation through a pathway involving serine-arginine-rich protein kinase in skeletal muscle. Sci Signal 5(211):ra14.
37. Klionsky DJ, Emr SD (2000) Autophagy as a regulated pathway of cellular degradation. Science 290(5497):1717-1721.
38. Lee SB, Tong SY, Kim JJ, Um SJ, Park JS (2007) Caspase-independent autophagic cytotoxicity in etoposide-treated CaSki cervical carcinoma cells. DNA Cell Biol 26(10):713-720.
39. Cao C, et al. (2006) Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res 66(20):10040-10047.
40. Holcik M, Yeh C, Korneluk RG, Chow T (2000) Translational upregulation of X-linked inhibitor of apoptosis (XIAP) increases resistance to radiation induced cell death. Oncogene 19(36):4174-4177.
41. Hollander MC, Fornace AJ, Jr. (2002) Genomic instability, centrosome amplification, cell cycle checkpoints and Gadd45a. Oncogene 21(40):6228-6233.
42. Wang B, Matsuoka S, Carpenter PB, Elledge SJ (2002) 53BP1, a mediator of the DNA damage checkpoint. Science 298(5597):1435-1438.
43. Shuck SC, Short EA, Turchi JJ (2008) Eukaryotic nucleotide excision repair: From understanding mechanisms to influencing biology. Cell Res 18(1):64-72.
44. Cann KL, Hicks GG (2007) Regulation of the cellular DNA double-strand break response. Biochem Cell Biol 85(6):663-674.
45. Gilbert WV, Zhou K, Butler TK, Doudna JA (2007) Cap-independent translation is required for starvation-induced differentiation in yeast. Science 317(5842):1224-1227.
46. Connolly E, Braunstein S, Formenti S, Schneider RJ (2006) Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells. Mol Cell Biol 26(10):3955-3965.
47. Holcik M, Lefebvre C, Yeh C, Chow T, Korneluk RG (1999) A new internal-ribosome-entry-site motif potentiates XIAP-mediated cytoprotection. Nat Cell Biol 1(3):190-192.