A novel cis-acting element from the 3′UTR of DNA damage-binding protein 2 mRNA links transcriptional and post-transcriptional regulation of gene expression

Nucleic Acids Research

Volumn 41, Issue 11, 2013, Pages 5692-5703

  Melanson, Brian D ^a,b   Cabrita, Miguel A ^a,b   Bose, Reetesh ^a,b   Hamill, Jeffrey D ^a   Pan, Elysia ^a   Brochu, Christian ^a   Marcellus, Kristen A ^a   Zhao, Tong T ^c   Holcik, Martin ^b,c   McKay, Bruce C ^a,b,d  

^a OTTAWA HOSPITAL RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c CHILDREN S HOSPITAL OF EASTERN ONTARIO   (Canada)

^d CARLETON UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; CIS ACTING ELEMENT; DNA DAMAGE BINDING PROTEIN 2; MESSENGER RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; POSTTRANSCRIPTIONAL CONTROL; PRIORITY JOURNAL; RNA PROCESSING; RNA STABILITY; RNA TRANSCRIPTION; TRANSCRIPTION REGULATION;

3' UNTRANSLATED REGIONS; CELL LINE; DNA-BINDING PROTEINS; GREEN FLUORESCENT PROTEINS; HUMANS; INVERTED REPEAT SEQUENCES; RECOMBINANT FUSION PROTEINS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; TRANSCRIPTION, GENETIC;

EID: 84878883385     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt279     Document Type: Article

References (64)

1. Dualan, R., Brody, T., Keeney, S., Nichols, A.F., Admon, A. and Linn, S. (1995) Chromosomal localization and cDNA cloning of the genes (DDB1 and DDB2) for the p127 and p48 subunits of a human damage-specific DNA binding protein. Genomics, 29, 62-69.
2. Scrima, A., Fischer, E.S., Lingaraju, G.M., Bohm, K., Cavadini, S. and Thoma, N.H. (2011) Detecting UV-lesions in the genome: the modular CRL4 ubiquitin ligase does it best! FEBS Lett., 585, 2818-2825.
3. Fujiwara, Y., Masutani, C., Mizukoshi, T., Kondo, J., Hanaoka, F. and Iwai, S. (1999) Characterization of DNA recognition by the human UV-damaged DNA-binding protein. J. Biol. Chem., 274, 20027-20033.
4. Tang, J. and Chu, G. (2002) Xeroderma pigmentosum complementation group E and UV-damaged DNA-binding protein. DNA Repair, 1, 601-616.
5. Nichols, A.F., Itoh, T., Graham, J.A., Liu, W., Yamaizumi, M. and Linn, S. (2000) Human damage-specific DNA-binding protein p48. Characterization of XPE mutations and regulation following UV irradiation. J. Biol. Chem., 275, 21422-21428.
6. Fitch, M.E., Cross, I.V. and Ford, J.M. (2003) p53 responsive nucleotide excision repair gene products p48 and XPC, but not p53, localize to sites of UV-irradiation-induced DNA damage, in vivo. Carcinogenesis, 24, 843-850.
7. Fitch, M.E., Cross, I.V., Turner, S.J., Adimoolam, S., Lin, C.X., Williams, K.G. and Ford, J.M. (2003) The DDB2 nucleotide excision repair gene product p48 enhances global genomic repair in p53 deficient human fibroblasts. DNA Repair, 2, 819-826.
8. Wang, Q.E., Zhu, Q., Wani, G., Chen, J. and Wani, A.A. (2004) UV radiation-induced XPC translocation within chromatin is mediated by damaged-DNA binding protein, DDB2. Carcinogenesis, 25, 1033-1043.
9. Moser, J., Volker, M., Kool, H., Alekseev, S., Vrieling, H., Yasui, A., van Zeeland, A.A. and Mullenders, L.H. (2005) The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair, 4, 571-582.
10. Jackson, S. and Xiong, Y. (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem. Sci., 34, 562-570.
11. Fischer, E.S., Scrima, A., Bohm, K., Matsumoto, S., Lingaraju, G.M., Faty, M., Yasuda, T., Cavadini, S., Wakasugi, M., Hanaoka, F. et al. (2011) The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell, 147, 1024-1039.
12. Rapic-Otrin, V., McLenigan, M.P., Bisi, D.C., Gonzalez, M. and Levine, A.S. (2002) Sequential binding of UV DNA damage binding factor and degradation of the p48 subunit as early events after UV irradiation. Nucleic Acids Res., 30, 2588-2598.
13. Kapetanaki, M.G., Guerrero-Santoro, J., Bisi, D.C., Hsieh, C.L., Rapic-Otrin, V. and Levine, A.S. (2006) The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc. Natl Acad. Sci. USA, 103, 2588-2593.
14. Lan, L., Nakajima, S., Kapetanaki, M.G., Hsieh, C.L., Fagerburg, M., Thickman, K., Rodriguez-Collazo, P., Leuba, S.H., Levine, A.S. and Rapic-Otrin, V. (2012) Monoubiquitinated H2A destabilizes photolesion-containing nucleosomes with the concomitant release of the UV-damaged DNA-binding protein E3 ligase. J. Biol. Chem., 287, 12039-12049.
15. Luijsterburg, M.S., Lindh, M., Acs, K., Vrouwe, M.G., Pines, A., van Attikum, H., Mullenders, L.H. and Dantuma, N.P. (2012) DDB2 promotes chromatin decondensation at UV-induced DNA damage. J. Cell Biol., 197, 267-281.
16. Sugasawa, K. (2009) UV-DDB: a molecular machine linking DNA repair with ubiquitination. DNA Repair, 8, 969-972.
17. Stoyanova, T., Roy, N., Kopanja, D., Raychaudhuri, P. and Bagchi, S. (2009) DDB2 (damaged-DNA binding protein 2) in nucleotide excision repair and DNA damage response. Cell Cycle, 8, 4067-4071.
18. Stoyanova, T., Roy, N., Kopanja, D., Bagchi, S. and Raychaudhuri, P. (2009) DDB2 decides cell fate following DNA damage. Proc. Natl Acad. Sci. USA, 106, 10690-10695.
19. Stoyanova, T., Roy, N., Bhattacharjee, S., Kopanja, D., Valli, T., Bagchi, S. and Raychaudhuri, P. (2012) p21 cooperates with DDB2 protein in suppression of ultraviolet ray-induced skin malignancies. J. Biol. Chem., 287, 3019-3028.
20. Roy, N., Stoyanova, T., Dominguez-Brauer, C., Park, H.J., Bagchi, S. and Raychaudhuri, P. (2010) DDB2, an essential mediator of premature senescence. Mol. Cell. Biol., 30, 2681-2692.
21. Bagchi, S. and Raychaudhuri, P. (2010) Damaged-DNA binding protein-2 drives apoptosis following DNA damage. Cell Div., 5, 3.
22. Yan, Y., Zhang, X. and Legerski, R.J. (2011) Artemis interacts with the Cul4A-DDB1DDB2 ubiquitin E3 ligase and regulates degradation of the CDK inhibitor p27. Cell Cycle, 10, 4098-4109.
23. Castells, E., Molinier, J., Benvenuto, G., Bourbousse, C., Zabulon, G., Zalc, A., Cazzaniga, S., Genschik, P., Barneche, F. and Bowler, C. (2011) The conserved factor DE-ETIOLATED 1 cooperates with CUL4-DDB1DDB2 to maintain genome integrity upon UV stress. EMBO J., 30, 1162-1172.
24. Oh, K.S., Emmert, S., Tamura, D., DiGiovanna, J.J. and Kraemer, K.H. (2011) Multiple skin cancers in adults with mutations in the XP-E (DDB2) DNA repair gene. J. Invest. Dermatol., 131, 785-788.
25. Itoh, T., O'Shea, C. and Linn, S. (2003) Impaired regulation of tumor suppressor p53 caused by mutations in the xeroderma pigmentosum DDB2 gene: mutual regulatory interactions between p48(DDB2) and p53. Mol. Cell. Biol., 23, 7540-7553.
26. Liu, W., Nichols, A.F., Graham, J.A., Dualan, R., Abbas, A. and Linn, S. (2000) Nuclear transport of human DDB protein induced by ultraviolet light. J. Biol. Chem., 275, 21429-21434.
27. Hwang, B.J., Ford, J.M., Hanawalt, P.C. and Chu, G. (1999) Expression of the p48 xeroderma pigmentosum gene is p53-dependent and is involved in global genomic repair. Proc. Natl Acad. Sci. USA, 96, 424-428.
28. Shiyanov, P., Hayes, S.A., Donepudi, M., Nichols, A.F., Linn, S., Slagle, B.L. and Raychaudhuri, P. (1999) The naturally occurring mutants of DDB are impaired in stimulating nuclear import of the p125 subunit and E2F1-activated transcription. Mol. Cell. Biol., 19, 4935-4943.
29. Melanson, B.D., Bose, R., Hamill, J.D., Marcellus, K.A., Pan, E.F. and McKay, B.C. (2011) The role of mRNA decay in p53-induced gene expression. RNA, 17, 2222-2234.
30. Brady, C.A. and Attardi, L.D. (2010) p53 at a glance. J. Cell Sci., 123, 2527-2532.
31. McKay, B.C., Chen, F., Perumalswami, C.R., Zhang, F. and Ljungman, M. (2000) The tumor suppressor p53 can both stimulate and inhibit ultraviolet light-induced apoptosis. Mol. Biol. Cell, 11, 2543-2551.
32. Li, X., Zhao, X., Fang, Y., Jiang, X., Duong, T., Fan, C., Huang, C.C. and Kain, S.R. (1998) Generation of destabilized green fluorescent protein as a transcription reporter. J. Biol. Chem., 273, 34970-34975.
33. Liwak, U., Thakor, N., Jordan, L.E., Roy, R., Lewis, S.M., Pardo, O.E., Seckl, M. and Holcik, M. (2012) Tumor suppressor PDCD4 represses internal ribosome entry site-mediated translation of antiapoptotic proteins and is regulated by S6 kinase 2. Mol. Cell. Biol., 32, 1818-1829.
34. Mackinnon-Roy, C., Stubbert, L.J. and McKay, B.C. (2011) RNA interference against transcription elongation factor SII does not support its role in transcription-coupled nucleotide excision repair. Mut. Res., 706, 53-58.
35. Fan, J., Yang, X., Wang, W., Wood, W.H. III, Becker, K.G. and Gorospe, M. (2002) Global analysis of stress-regulated mRNA turnover by using cDNA arrays. Proc. Natl Acad. Sci. USA, 99, 10611-10616.
36. Friedel, C.C., Dolken, L., Ruzsics, Z., Koszinowski, U.H. and Zimmer, R. (2009) Conserved principles of mammalian transcriptional regulation revealed by RNA half-life. Nucleic Acids Res., 37, e115.
37. Munchel, S.E., Shultzaberger, R.K., Takizawa, N. and Weis, K. (2011) Dynamic profiling of mRNA turnover reveals gene-specific and system-wide regulation of mRNA decay. Mol. Biol. Cell, 22, 2787-2795.
38. Keene, J.D. (2010) The global dynamics of RNA stability orchestrates responses to cellular activation. BMC Biol., 8, 95.
39. Yang, E., van Nimwegen, E., Zavolan, M., Rajewsky, N., Schroeder, M., Magnasco, M. and Darnell, J.E. Jr (2003) Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res., 13, 1863-1872.
40. Raghavan, A. and Bohjanen, P.R. (2004) Microarray-based analyses of mRNA decay in the regulation of mammalian gene expression. Brief. Funct. Genomics Proteomics, 3, 112-124.
41. Mata, J., Marguerat, S. and Bahler, J. (2005) Post-transcriptional control of gene expression: a genome-wide perspective. Trends Biochem. Sci., 30, 506-514.
42. Sharova, L.V., Sharov, A.A., Nedorezov, T., Piao, Y., Shaik, N. and Ko, M.S. (2009) Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res., 16, 45-58.
43. Lee, J.E., Lee, J.Y., Wilusz, J., Tian, B. and Wilusz, C.J. (2010) Systematic analysis of cis-elements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells. PloS One, 5, e11201.
44. Vlasova, I.A., Tahoe, N.M., Fan, D., Larsson, O., Rattenbacher, B., Sternjohn, J.R., Vasdewani, J., Karypis, G., Reilly, C.S., Bitterman, P.B. et al. (2008) Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol. Cell, 29, 263-270.
45. Hau, H.H., Walsh, R.J., Ogilvie, R.L., Williams, D.A., Reilly, C.S. and Bohjanen, P.R. (2007) Tristetraprolin recruits functional mRNA decay complexes to ARE sequences. J. Cell. Biochem., 100, 1477-1492.
46. Chen, C.Y., Gherzi, R., Ong, S.E., Chan, E.L., Raijmakers, R., Pruijn, G.J., Stoecklin, G., Moroni, C., Mann, M. and Karin, M. (2001) AU binding proteins recruit the exosome to degrade AREcontaining mRNAs. Cell, 107, 451-464.
47. Chen, C.Y., Xu, N. and Shyu, A.B. (1995) mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocytemacrophage colony-stimulating factor transcripts: different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol., 15, 5777-5788.
48. Kuwano, Y., Kim, H.H., Abdelmohsen, K., Pullmann, R. Jr, Martindale, J.L., Yang, X. and Gorospe, M. (2008) MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Mol. Cell. Biol., 28, 4562-4575.
49. Wang, W., Martindale, J.L., Yang, X., Chrest, F.J. and Gorospe, M. (2005) Increased stability of the p16 mRNA with replicative senescence. EMBO Rep., 6, 158-164.
50. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. and Lipman, D.J. (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res., 25, 3389-3402.
51. Zhao, T.T., Graber, T.E., Jordan, L.E., Cloutier, M., Lewis, S.M., Goulet, I., Cote, J. and Holcik, M. (2009) hnRNP A1 regulates UV-induced NF-kappaB signalling through destabilization of cIAP1 mRNA. Cell Death Diff., 16, 244-252.
52. Kastelic, T., Schnyder, J., Leutwiler, A., Traber, R., Streit, B., Niggli, H., MacKenzie, A. and Cheneval, D. (1996) Induction of rapid IL-1 beta mRNA degradation in THP-1 cells mediated through the AU-rich region in the 30UTR by a radicicol analogue. Cytokine, 8, 751-761.
53. Garcia-Martinez, J., Aranda, A. and Perez-Ortin, J.E. (2004) Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol. Cell, 15, 303-313.
54. Cheadle, C., Fan, J., Cho-Chung, Y.S., Werner, T., Ray, J., Do, L., Gorospe, M. and Becker, K.G. (2005) Control of gene expression during T cell activation: alternate regulation of mRNA transcription and mRNA stability. BMC Genomics, 6, 75.
55. Rabani, M., Levin, J.Z., Fan, L., Adiconis, X., Raychowdhury, R., Garber, M., Gnirke, A., Nusbaum, C., Hacohen, N., Friedman, N. et al. (2011) Metabolic labeling of RNA uncovers principles of RNA production and degradation dynamics in mammalian cells. Nat. Biotechnol., 29, 436-442.
56. Elkon, R., Zlotorynski, E., Zeller, K.I. and Agami, R. (2010) Major role for mRNA stability in shaping the kinetics of gene induction. BMC Genomics, 11, 259.
57. Bregman, A., Avraham-Kelbert, M., Barkai, O., Duek, L., Guterman, A. and Choder, M. (2011) Promoter elements regulate cytoplasmic mRNA decay. Cell, 147, 1473-1483.
58. Trcek, T., Larson, D.R., Moldon, A., Query, C.C. and Singer, R.H. (2011) Single-molecule mRNA decay measurements reveal promoter-regulated mRNA stability in yeast. Cell, 147, 1484-1497.
59. Dori-Bachash, M., Shema, E. and Tirosh, I. (2011) Coupled evolution of transcription and mRNA degradation. PLoS Biol., 9, e1001106.
60. Choder, M. (2011) mRNA imprinting: additional level in the regulation of gene expression. Cell. Logist., 1, 37-40.
61. Goler-Baron, V., Selitrennik, M., Barkai, O., Haimovich, G., Lotan, R. and Choder, M. (2008) Transcription in the nucleus and mRNA decay in the cytoplasm are coupled processes. Genes Dev., 22, 2022-2027.
62. Harel-Sharvit, L., Eldad, N., Haimovich, G., Barkai, O., Duek, L. and Choder, M. (2010) RNA polymerase II subunits link transcription and mRNA decay to translation. Cell, 143, 552-563.
63. Shalem, O., Groisman, B., Choder, M., Dahan, O. and Pilpel, Y. (2011) Transcriptome kinetics is governed by a genome-wide coupling of mRNA production and degradation: a role for RNA Pol II. PLoS Genet., 7, e1002273.
64. Dahan, N. and Choder, M. (2013) The eukaryotic transcriptional machinery regulates mRNA translation and decay in the cytoplasm. Biochim. Biophys. Acta, 1829, 169-173.