Deregulation of internal ribosome entry site-mediated p53 translation in cancer cells with defective p53 response to DNA damage

Molecular and Cellular Biology

Volumn 35, Issue 23, 2015, Pages 4006-4017

  Halaby, Marie Jo ^a,d   Harris, Benjamin R E ^a   Miskimins, W Keith ^c   Cleary, Margot P ^a,b   Yang, Da Qing ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF SOUTH DAKOTA   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; RNA HELICASE; RNA HELICASE A; SHORT HAIRPIN RNA; TRANS ACTING FACTOR; TRANSLATIONAL CONTROL PROTEIN 80; UNCLASSIFIED DRUG; 5' UNTRANSLATED REGION; DEAD BOX PROTEIN; DHX9 PROTEIN, HUMAN; ILF3 PROTEIN, HUMAN; INTERLEUKIN ENHANCER BINDING FACTOR 3; INTERNAL RIBOSOME ENTRY SITE; PROTEIN BINDING; TP53 PROTEIN, HUMAN; TUMOR PROTEIN;

ARTICLE; BREAST CANCER CELL LINE; CARCINOGENESIS; CELL AGING; CELL LEVEL; CONTROLLED STUDY; DNA DAMAGE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; INTERNAL RIBOSOME ENTRY SITE; MALIGNANT TRANSFORMATION; MCF 7 CELL LINE; MDA MB 175 CELL LINE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INACTIVATION; PROTEIN INDUCTION; PROTEIN SYNTHESIS; REGULATORY MECHANISM; TRANSLATION REGULATION; WILD TYPE; ZR75 1 CELL LINE; 5' UNTRANSLATED REGION; BREAST; BREAST TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MCF-7 CELL LINE; METABOLISM; PATHOLOGY; PROTEIN DEGRADATION; TUMOR CELL LINE;

5' UNTRANSLATED REGIONS; BREAST; BREAST NEOPLASMS; CELL LINE, TUMOR; DEAD-BOX RNA HELICASES; DNA DAMAGE; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTERNAL RIBOSOME ENTRY SITES; MCF-7 CELLS; NEOPLASM PROTEINS; NUCLEAR FACTOR 90 PROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEOLYSIS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84946237679     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00365-15     Document Type: Article

References (51)

1. Giaccia AJ, Kastan MB. 1998. The complexity of p53 modulation: emerging patterns from divergent signals. Genes Dev 12:2973-2983. http://dx.doi.org/10.1101/gad.12.19.2973.
2. Vogelstein B, Lane D, Levine AJ. 2000. Surfing the p53 network. Nature 408:307-310. http://dx.doi.org/10.1038/35042675.
3. Horn HF, Vousden KH. 2007. Coping with stress: multiple ways to activate p53. Oncogene 26:1306-1316. http://dx.doi.org/10.1038/sj.onc.1210263.
4. Halaby MJ, Yang DQ. 2007. p53 translational control: a new facet of p53 regulation and its implication for tumorigenesis and cancer therapeutics. Gene 395:1-7. http://dx.doi.org/10.1016/j.gene.2007.01.029.
5. 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.
6. 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. http://dx.doi.org/10.1016/j.cell.2005.07.034.
7. Gingras AC, Raught B, Sonenberg N. 1999. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem 68:913-963. http://dx.doi.org/10.1146/annurev.biochem.68.1.913.
8. Stoneley M, Willis AE. 2004. Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene 23:3200-3207. http://dx.doi.org/10.1038/sj.onc.1207551.
9. Holcik M, Sonenberg N. 2005. Translational control in stress and apoptosis. Nat Rev Mol Cell Biol 6:318-327. http://dx.doi.org/10.1038/nrm1618.
10. Yang DQ, Halaby MJ, Zhang Y. 2006. The identification of an internal ribosomal entry site in the 5'-untranslated region of p53 mRNA provides a novel mechanism for the regulation of its translation following DNA damage. Oncogene 25:4613-4619. http://dx.doi.org/10.1038/sj.onc.1209483.
11. Ray PS, Grover R, Das S. 2006. Two internal ribosome entry sites mediate the translation of p53 isoforms. EMBO Rep 7:404-410.
12. Candeias MM, Powell DJ, Roubalova E, Apcher S, Bourougaa K, Vojtesek B, Bruzzoni-Giovanelli H, Fahraeus R. 2006. Expression of p53 and p53/47 are controlled by alternative mechanisms of messenger RNA translation initiation. Oncogene 25:6936-6947. http://dx.doi.org/10.1038/sj.onc.1209996.
13. Sayan AE, Roperch JP, Sayan BS, Rossi M, Pinkoski MJ, Knight RA, Willis AE, Melino G. 2007. Generation of DeltaTAp73 proteins by translation from a putative internal ribosome entry site. Ann N Y Acad Sci 1095:315-324. http://dx.doi.org/10.1196/annals.1397.035.
14. Kim DY, Kim W, Lee KH, Kim SH, Lee HR, Kim HJ, Jung Y, Choi JH, Kim KT. 2013. hnRNP Q regulates translation of p53 in normal and stress conditions. Cell Death Differ 20:226-234. http://dx.doi.org/10.1038/cdd.2012.109.
15. Grover R, Ray PS, Das S. 2008. Polypyrimidine tract binding protein regulates IRES-mediated translation of p53 isoforms. Cell Cycle 7:2189-2198. http://dx.doi.org/10.4161/cc.7.14.6271.
16. Montanaro L, Calienni M, Bertoni S, Rocchi L, Sansone P, Storci G, Santini D, Ceccarelli C, Taffurelli M, Carnicelli D, Brigotti M, Bonafe M, Trere D, Derenzini M. 2010. Novel dyskerin-mediated mechanism of p53 inactivation through defective mRNA translation. Cancer Res 70:4767-4777. http://dx.doi.org/10.1158/1538-7445.AM10-4767.
17. Bellodi C, Kopmar N, Ruggero D. 2010. Deregulation of oncogene-induced senescence and p53 translational control in X-linked dyskeratosis congenita. EMBO J 29:1865-1876. http://dx.doi.org/10.1038/emboj.2010.83.
18. Sharathchandra A, Lal R, Khan D, Das S. 2012. Annexin A2 and PSF proteins interact with p53 IRES and regulate translation of p53 mRNA. RNA Biol 9:1429-1439. http://dx.doi.org/10.4161/rna.22707.
19. Weingarten-Gabbay S, Khan D, Liberman N, Yoffe Y, Bialik S, Das S, Oren M, Kimchi A. 2013. The translation initiation factor DAP5 promotes IRES-driven translation of p53 mRNA. Oncogene 33:611-618.
20. Khan D, Katoch A, Das A, Sharathchandra A, Lal R, Roy P, Das S, Chattopadhyay S, Das S. 2015. Reversible induction of translational isoforms of p53 in glucose deprivation. Cell Death Differ 33:611-618. http://dx.doi.org/10.1038/onc.2012.626.
21. Hellen CU, Sarnow P. 2001. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev 15:1593-1612. http://dx.doi.org/10.1101/gad.891101.
22. Jackson RJ. 2005. Alternative mechanisms of initiating translation of mammalian mRNAs. Biochem Soc Trans 33:1231-1241. http://dx.doi.org/10.1042/BST20051231.
23. Gasco M, Shami S, Crook T. 2002. The p53 pathway in breast cancer. Breast Cancer Res 4:70-76. http://dx.doi.org/10.1186/bcr426.
24. Fierro-Monti I, Mathews MB. 2000. Proteins binding to duplexed RNA: one motif, multiple functions. Trends Biochem Sci 25:241-246. http://dx.doi.org/10.1016/S0968-0004(00)01580-2.
25. Xu YH, Grabowski GA. 1999. Molecular cloning and characterization of a translational inhibitory protein that binds to coding sequences of the human acid beta-glucosidase and other mRNAs. Mol Genet Metab 68:441-454. http://dx.doi.org/10.1006/mgme.1999.2934.
26. Merrill MK, Gromeier M. 2006. The double-stranded RNA binding protein 76:NF45 heterodimer inhibits translation initiation at the rhinovirus type 2 internal ribosome entry site. J Virol 80:6936-6942. http://dx.doi.org/10.1128/JVI.00243-06.
27. Reichman TW, Parrott AM, Fierro-Monti I, Caron DJ, Kao PN, Lee CG, Li H, Mathews MB. 2003. Selective regulation of gene expression by nuclear factor 110, a member of the NF90 family of double-stranded RNA-binding proteins. J Mol Biol 332:85-98. http://dx.doi.org/10.1016/S0022-2836(03)00885-4.
28. Hartman TR, Qian S, Bolinger C, Fernandez S, Schoenberg DR, Boris-Lawrie K. 2006. RNA helicase A is necessary for translation of selected messenger RNAs. Nat Struct Mol Biol 13:509-516. http://dx.doi.org/10.1038/nsmb1092.
29. Tuck SP, Crawford L. 1989. Characterization of the human p53 gene promoter. Mol Cell Biol 9:2163-2172.
30. Grover R, Sharathchandra A, Ponnuswamy A, Khan D, Das S. 2011. Effect of mutations on the p53 IRES RNA structure: implications for deregulation of the synthesis of p53 isoforms. RNA Biol 8:132-142. http://dx.doi.org/10.4161/rna.8.1.14260.
31. Concin N, Zeillinger C, Tong D, StimpflM, Konig M, Printz D, Stonek F, Schneeberger C, Hefler L, Kainz C, Leodolter S, Haas OA, Zeillinger R. 2003. Comparison of p53 mutational status with mRNA and protein expression in a panel of 24 human breast carcinoma cell lines. Breast Cancer Res Treat 79:37-46. http://dx.doi.org/10.1023/A:1023351717408.
32. Wasielewski M, Elstrodt F, Klijn JG, Berns EM, Schutte M. 2006. Thirteen new p53 gene mutants identified among 41 human breast cancer cell lines. Breast Cancer Res Treat 99:97-101. http://dx.doi.org/10.1007/s10549-006-9186-z.
33. Vousden KH, Prives C. 2005. P53 and prognosis: new insights and further complexity. Cell 120:7-10. http://dx.doi.org/10.1016/S0092-8674(04)01252-8.
34. Parker LM, Fierro-Monti I, Mathews MB. 2001. Nuclear factor 90 is a substrate and regulator of the eukaryotic initiation factor 2 kinase doublestranded RNA-activated protein kinase. J Biol Chem 276:32522-32530. http://dx.doi.org/10.1074/jbc. M104408200.
35. Itahana K, Dimri G, Campisi J. 2001. Regulation of cellular senescence by p53. Eur J Biochem 268:2784-2791. http://dx.doi.org/10.1046/j.1432-1327.2001.02228.x.
36. Schmitt E, Paquet C, Beauchemin M, Bertrand R. 2007. DNA-damage response network at the crossroads of cell-cycle checkpoints, cellular senescence and apoptosis. J Zhejiang Univ Sci B 8:377-397. http://dx.doi.org/10.1631/jzus.2007.B0377.
37. Li Y, Yang DQ. 2010. The ATM inhibitor KU-55933 suppresses cell proliferation and induces apoptosis by blocking Akt in cancer cells with overactivated Akt. Mol Cancer Ther 9:113-125. http://dx.doi.org/10.1158/1535-7163.MCT-08-1189.
38. Meng Z, Jackson NL, Choi H, King PH, Emanuel PD, Blume SW. 2008. Alterations in RNA-binding activities of IRES-regulatory proteins as a mechanism for physiological variability and pathological dysregulation of IGF-IR translational control in human breast tumor cells. J Cell Physiol 217:172-183. http://dx.doi.org/10.1002/jcp.21486.
39. Lee CG, Eki T, Okumura K, Nogami M, Soares Vda C, Murakami Y, Hanaoka F, Hurwitz J. 1999. The human RNA helicase A (DDX9) gene maps to the prostate cancer susceptibility locus at chromosome band 1q25 and its pseudogene (DDX9P) to 13q22, respectively. Somat Cell Mol Genet 25:33-39. http://dx.doi.org/10.1023/B:SCAM.0000007138.44216.3a.
40. MacGrogan D, Bookstein R. 1997. Tumour suppressor genes in prostate cancer. Semin Cancer Biol 8:11-19. http://dx.doi.org/10.1006/scbi.1997.0048.
41. Zhang S, Hemmerich P, Grosse F. 2007. Werner syndrome helicase (WRN), nuclear DNA helicase II (NDH II) and histone gammaH2AX are localized to the centrosome. Cell Biol Int 31:1109-1121. http://dx.doi.org/10.1016/j.cellbi.2007.03.027.
42. Zhang S, Schlott B, Gorlach M, Grosse F. 2004. DNA-dependent protein kinase (DNA-PK) phosphorylates nuclear DNA helicase II/RNA helicase A and hnRNP proteins in an RNA-dependent manner. Nucleic Acids Res 32:1-10. http://dx.doi.org/10.1093/nar/gkg933.
43. Neplioueva V, Dobrikova EY, Mukherjee N, Keene JD, Gromeier M. 2010. Tissue type-specific expression of the dsRNA-binding protein 76 and genome-wide elucidation of its target mRNAs. PLoS One 5:e11710. http://dx.doi.org/10.1371/journal.pone.0011710.
44. Jeffers JR, Parganas E, Lee Y, Yang C, Wang J, Brennan J, MacLean KH, Han J, Chittenden T, Ihle JN, McKinnon PJ, Cleveland JL, Zambetti GP. 2003. Puma is an essential mediator of p53-dependent and -independent apoptotic pathways. Cancer Cell 4:321-328. http://dx.doi.org/10.1016/S1535-6108(03)00244-7.
45. Garrison SP, Phillips DC, Jeffers JR, Chipuk JE, Parsons MJ, Rehg JE, Opferman JT, Green DR, Zambetti GP. 2012. Genetically defining the mechanism of Puma- and Bim-induced apoptosis. Cell Death Differ 19:642-649. http://dx.doi.org/10.1038/cdd.2011.136.
46. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. 2010. The essence of senescence. Genes Dev 24:2463-2479. http://dx.doi.org/10.1101/gad.1971610.
47. MacInnes AW, Amsterdam A, Whittaker CA, Hopkins N, Lees JA. 2008. Loss of p53 synthesis in zebrafish tumors with ribosomal protein gene mutations. Proc Natl Acad SciUS A 105:10408-10413. http://dx.doi.org/10.1073/pnas.0805036105.
48. Fu L, Ma W, Benchimol S. 1999. A translation repressor element resides in the 3' untranslated region of human p53 mRNA. Oncogene 18:6419-6424. http://dx.doi.org/10.1038/sj.onc.1203064.
49. Chen J, Kastan MB. 2010. 5'-3'-UTR interactions regulate p53 mRNA translation and provide a target for modulating p53 induction after DNA damage. Genes Dev 24:2146-2156. http://dx.doi.org/10.1101/gad.1968910.
50. 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 U S A 100:8354-8359. http://dx.doi.org/10.1073/pnas.1432104100.
51. Abdelmohsen K, Panda AC, Kang MJ, Guo R, Kim J, Grammatikakis I, Yoon JH, Dudekula DB, Noh JH, Yang X, Martindale JL, Gorospe M. 2014. 7SL RNA represses p53 translation by competing with HuR. Nucleic Acids Res 42:10099-10111. http://dx.doi.org/10.1093/nar/gku686.