5′-3′-UTR interactions regulate p53 mRNA translation and provide a target for modulating p53 induction after DNA damage

Genes and Development

Volumn 24, Issue 19, 2010, Pages 2146-2156

  Chen, Jing ^a   Kastan, Michael B ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Cytoprotection; DNA damage; p53; Translational control

Indexed keywords

COMPLEMENTARY RNA; DOUBLE STRANDED RNA; MESSENGER RNA; OLIGONUCLEOTIDE; PROTEIN P53; RIBOSOME PROTEIN; RPL26 PROTEIN, HUMAN;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BASE PAIRING; CELL DEATH; CELL STRESS; CONTROLLED STUDY; DNA DAMAGE; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PROCESSING; RNA TRANSLATION; SEQUENCE ALIGNMENT; TRANSCRIPTION REGULATION; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY;

3' UNTRANSLATED REGIONS; 5' UNTRANSLATED REGIONS; DNA DAMAGE; GENE EXPRESSION REGULATION; HUMANS; OLIGONUCLEOTIDES; PROTEIN BINDING; RIBOSOMAL PROTEINS; RNA, DOUBLE-STRANDED; RNA, MESSENGER; STRESS, PHYSIOLOGICAL; TUMOR SUPPRESSOR PROTEIN P53;

EID: 77957679426     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1968910     Document Type: Article

References (46)

1. Amrani N, Ghosh S, Mangus DA, Jacobson A. 2008. Translation factors promote the formation of two states of the closedloop mRNP. Nature 453: 1276-1280. (Pubitemid 351913593)
2. Ashcroft M, Vousden KH. 1999. Regulation of p53 stability. Oncogene 18: 7637-7643.
3. Edgil D, Harris E. 2006. End-to-end communication in the modulation of translation by mammalian RNA viruses. Virus Res 119: 43-51. (Pubitemid 43765978)
4. Franch T, Gultyaev AP, Gerdes K. 1997. Programmed cell death by hok/sok of plasmid R1: Processing at the hok mRNA 3′-end triggers structural rearrangements that allow translation and antisense RNA binding. J Mol Biol 273: 38-51. (Pubitemid 27460212)
5. Fu L, Benchimol S. 1997. Participation of the human p53 3′UTR in translational repression and activation following γ-irradiation. EMBO J 16: 4117-4125. (Pubitemid 27281026)
6. Giaccia AJ, Kastan MB. 1998. The complexity of p53 modulation: Emerging patterns from divergent signals. Genes Dev 12: 2973-2983.
7. Gray NK, Hentze MW. 1994. Regulation of protein synthesis by mRNA structure. Mol Biol Rep 19: 195-200.
8. Grivna ST, Pyhtila B, Lin H. 2006a. MIWI associates with translational machinery and PIWI-interacting RNAs (piRNAs) in regulating spermatogenesis. Proc Natl Acad Sci 103: 13415-13420. (Pubitemid 44380122)
9. Grivna ST, Beyret E, Wang Z, Lin H. 2006b. A novel class of small RNAs in mouse spermatogenic cells. Genes Dev 20: 1709-1714. (Pubitemid 43992878)
10. Gruber AR, Lorenz R, Bernhart SH, Neubock R, Hofacker IL. 2008. The Vienna RNA websuite. Nucleic Acids Res 36: W70-W74. doi: 10.1093/nar/gkn188.
11. Gudkov AV, Komarova EA. 2003. The role of p53 in determining sensitivity to radiotherapy. Nat Rev Cancer 3: 117-129.
12. Guo L, Allen EM, Miller WA. 2001. Base-pairing between untranslated regions facilitates translation of uncapped, nonpolyadenylated viral RNA. Mol Cell 7: 1103-1109. (Pubitemid 32525756)
13. Haupt Y, Maya R, Kazaz A, Oren M. 1997. Mdm2 promotes the rapid degradation of p53. Nature 387: 296-299. (Pubitemid 27220766)
14. Hofacker IL. 2004. RNA secondary structure analysis using the Vienna RNA package. Curr Protoc Bioinformatics 4: 12.2.1-12.2.12.
15. Honda R, Tanaka H, Yasuda H. 1997. Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53. FEBS Lett 420: 25-27.
16. Kastan MB. 2007. Wild-type p53: Tumors can't stand it. Cell 128: 837-840.
17. Kastan MB, Bartek J. 2004. Cell-cycle checkpoints and cancer. Nature 432: 316-323.
18. Komarov PG, Komarova EA, Kondratov RV, Christov-Tselkov K, Coon JS, Chernov MV, Gudkov AV. 1999. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285: 1733-1737.
19. Kubbutat MH, Jones SN, Vousden KH. 1997. Regulation of p53 stability by Mdm2. Nature 387: 299-303.
20. Kuersten S, Goodwin EB. 2003. The power of the 3′ UTR: Translational control and development. Nat Rev Genet 4: 626-637.
21. Levine AJ. 1997. p53, the cellular gatekeeper for growth and division. Cell 88: 323-331.
22. Levine AJ, Oren M. 2009. The first 30 years of p53: Growing ever more complex. Nat Rev Cancer 9: 749-758.
23. Malkin D, Li FP, Strong LC, Fraumeni JF Jr, Nelson CE, Kim DH, Kassel J, Gryka MA, Bischoff FZ, Tainsky MA. 1990. Germ line p53 mutations in a familial syndrome of breast cancer, sarcomas, and other neoplasms. Science 250: 1233-1238.
24. Martins CP, Brown-Swigart L, Evan GI. 2006. Modeling the therapeutic efficacy of p53 restoration in tumors. Cell 127: 1323-1334.
25. Mazan-Mamczarz K, Galban S, Lopez de Silanes I, Martindale JL, Atasoy U, Keene JD, Gorospe M. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc Natl Acad Sci 100:8354-8359.
26. Melefors O, Hentze MW. 1993. Translational regulation by mRNA/protein interactions in eukaryotic cells: Ferritin and beyond. Bioessays 15: 85-90.
27. Michael D, Oren M. 2003. The p53-Mdm2 module and the ubiquitin system. Semin Cancer Biol 13: 49-58.
28. Mosner J, Mummenbrauer T, Bauer C, Sczakiel G, Grosse F, Deppert W. 1995. Negative feedback regulation of wild-type p53 biosynthesis. EMBO J 14: 4442-4449.
29. Ofir-Rosenfeld Y, Boggs K, Michael D, Kastan MB, Oren M. 2008. Mdm2 regulates p53 mRNA translation through inhibitory interactions with ribosomal protein L26. Mol Cell 32: 180-189.
30. Olivier M, Hollstein M, Hainaut P. 2010. TP53 mutations in human cancers: Origins, consequences, and clinical use. Cold Spring Harb Perspect Biol 2: a001008. doi: 10.1101/cshperspect.a001008.
31. Pickering BM, Willis AE. 2005. The implications of structured 5′ untranslated regions on translation and disease. Semin Cell Dev Biol 16: 39-47.
32. Prives C. 1998. Signaling to p53: Breaking the MDM2-p53 circuit. Cell 95: 5-8.
33. Sachs AB. 1993. Messenger RNA degradation in eukaryotes. Cell 74: 413-421.
34. Schumacher B, Hanazawa M, Lee MH, Nayak S, Volkmann K, Hofmann ER, Hengartner M, Schedl T, Gartner A. 2005. Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 120: 357-368.
35. Sherr CJ, DePinho RA. 2000. Cellular senescence: Mitotic clock or culture shock. Cell 102: 407-410.
36. Sohn D, Graupner V, Neise D, Essmann F, Schulze-Osthoff K, Janicke RU. 2009. Pifithrin-a protects against DNA damage-induced apoptosis downstream of mitochondria independent of p53. Cell Death Differ 16: 869-878.
37. Sonenberg N, Hinnebusch AG. 2007. New modes of translational control in development, behavior, and disease. Mol Cell 28: 721-729.
38. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745.
39. Standart N, Jackson RJ. 1994. Regulation of translation by specific protein/mRNA interactions. Biochimie 76: 867-879.
40. Takagi M, Absalon MJ, McLure KG, Kastan MB. 2005. Regulation of p53 translation and induction after DNA damage by ribosomal protein L26 and nucleolin. Cell 123: 49-63.
41. Vasudevan S, Tong Y, Steitz JA. 2007. Switching from repression to activation: MicroRNAs can up-regulate translation. Science 318: 1931-1934.
42. Ventura A, Kirsch DG, McLaughlin ME, Tuveson DA, Grimm J, Lintault L, Newman J, Reczek EE, Weissleder R, Jacks T. 2007. Restoration of p53 function leads to tumour regression in vivo. Nature 445: 661-665.
43. Wade M, Wang YV, Wahl GM. 2010. The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol 20: 299-309.
44. Westphal CH, Hoyes KP, Canman CE, Hua X, Kastan MB, Hendry JH, Leder P. 1998. Loss of atm radiosensitizes multiple p53 null tissues. Cancer Res 58: 5637-5639.
45. Xue W, Zender L, Miething C, Dickins RA, Hernando E, Krizhanovsky V, Cordon-Cardo C, Lowe SW. 2007. Senescence and tumour clearance is triggered by p53 restoration in murine liver carcinomas. Nature 445: 656-660.
46. Yu Y, Little JB. 1998. p53 is involved in but not required for ionizing radiation-induced caspase-3 activation and apoptosis in human lymphoblast cell lines. Cancer Res 58: 4277-4281.