BRCA1/BARD1 inhibition of mRNA 3′ processing involves targeted degradation of RNA polymerase II

Genes and Development

Volumn 19, Issue 10, 2005, Pages 1227-1237

  Kleiman, Frida E ^a,b   Wu Baer, Foon ^a   Fonseca, Danae ^b   Kaneko, Syuzo ^a   Baer, Richard ^a   Manley, James L ^a  

^a Columbia University ^*  (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

BARD1; BRCA1; Polyadenylation; RNA polymerase II

Indexed keywords

BRCA1 ASSOCIATED RING DOMAIN PROTEIN 1; BRCA1 PROTEIN; MESSENGER RNA; PROTEASOME; RNA POLYMERASE II; SMALL INTERFERING RNA; UBIQUITIN PROTEIN LIGASE;

ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA DAMAGE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA PROCESSING;

3' FLANKING REGION; ANIMALS; BRCA1 PROTEIN; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; MICE; PROTEIN BINDING; RNA 3' END PROCESSING; RNA POLYMERASE II; RNA PRECURSORS; TUMOR SUPPRESSOR PROTEINS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINS;

MAMMALIA;

EID: 18844407814     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1309505     Document Type: Article

References (59)

1. Abbott, D.W., Thompson, M.E., Robinson-Benion, C., Tomlinson, G., Jensen, R.A., and Holt, J.T. 1999. BRCA1 expression restores radiation resistance in BRCA1-deficient cancer cells through enhancement of transcription-coupled DNA repair. J. Biol. Chem. 274: 18808-18812.
2. Baer, R. and Ludwig, T. 2002. The BRCA1/BARD1 heterodimer, a tumor suppressor complex with ubiquitin E3 ligase activity. Curr. Opin. Genet. Dev. 12: 86-91.
3. Balajee, A.S., May, A., Dianova, I., and Bohr, V.A. 1998. Efficient PCNA complex formation is dependent upon both transcription coupled repair and genome overall repair. Mutat. Res. 409: 135-146.
4. Beaudenon, S.L., Huacani, M.R., Wang, G., McDonnell, D.P., and Huibregtse, J.M. 1999. Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol. Cell Biol. 19: 6972-6979.
5. Bregman, D.B., Du, L., van der Zee, S., and Warren, S.L. 1995. Transcription-dependent redistribution of the largest subunit of RNA polymerase II to discrete nuclear domains. J. Cell. Biol. 129: 287-298.
6. Bregman, D.B., Halaban, R., van Gool, A.J., Henning, K.A., Friedberg, E.C., and Warren, S.L. 1996. UV-induced ubiquitination of RNA polymerase II: A novel modification deficient in Cockayne syndrome cells. Proc. Natl. Acad. Sci. 93: 11586-11590.
7. Bruun, D., Folias, A., Akkari, Y., Cox, Y., Olson, S., and Moses, R. 2003. siRNA depletion of BRCA1, but not BRCA2, causes increased genome instability in Fanconi anemia cells. DNA Repair 2: 1007-1013.
8. Chen, A., Kleiman, F.E., Manley, J.L., Toru, O., and Pan, Z.Q. 2002. Auto-ubiquitination of the BRCA1/BARD1 RING ubiquitin ligase. J. Biol. Chem. 277: 22085-22092.
9. Chiba, N. and Parvin, J.D. 2001. Redistribution of BRCA1 among four different protein complexes following replication blockage. J. Biol. Chem. 276: 38549-38554.
10. -. 2002. The BRCA1 and BARD1 association with the RNA polymerase II holoenzyme. Cancer Res. 62: 4222-4228.
11. Choudhury, A.D., Xu, H., and Baer, R. 2004. Ubiquitination and proteasomal degradation of the BRCA1 tumor suppressor is regulated during cell cycle progression. J. Biol. Chem. 279: 33909-33918.
12. Chuvpilo, S., Zimmer, M., Kerstan, A., Glockner, J., Avots, A., Escher, C., Fischer, C., Inashkina, I., Jankevics, E., Berberich-Siebelt, F., et al. 1999. Alternative polyadenylation events contribute to the induction of NF-Atc in effector T cells. Immunity 10: 261-269.
13. Dong, Y., Hakimi, M.A., Chen, X., Kumaraswamy, E., Cooch, N.S., Godwin, A.K., and Shiekhattar, R. 2003. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol. Cell 12: 1087-1099.
14. Dornan, D., Wertz, I., Shimizu, H., Arnott, D., Frantz, G.D., Dowd, P., O'Rourke, K., Koeppen, H., and Dixit, V.M. 2004. The ubiquitin ligase COP1 is a critical negative regulator of p53. Nature 429: 86-92.
15. Hashizume, R., Fukuda, M., Maeda, I., Nishikawa, H., Oyake, D., Yabuki, Y., Ogata, H., and Ohta, T. 2001. The RING heterodimer BRCA1-BARD1 is an ubiquitin ligase inactivated by a cancer-derived mutation. J. Biol. Chem. 276: 14537-14540.
16. Hirose, Y., and Manley, J.L. 1997. Creatine phosphate, not ATP, is required for 3′ end cleavage of mammalian pre-mRNA in vitro. J. Biol. Chem. 272: 29636-29642.
17. -. 1998. RNA polymerase II is an essential mRNA polyadenylation factor. Nature 395: 93-96.
18. -. 2000. RNA polymerase II and the integration of nuclear events. Genes & Dev. 14: 1415-1429.
19. Huibregtse, J.M., Yang, J.C., and Beaudenon, S.L. 1997. The large subunit of RNA polymerase II is a substrate of the Rsp5 ubiquitin-protein ligase. Proc. Natl. Acad. Sci. 94:3656-3661.
20. Jasin, M. 2002. Homologous repair of DNA damage and tumorigenesis: The BRCA connection. Oncogene 21: 8981-8993.
21. Jin, Y., Xu, X.L., Yang, M.C., Wei, F., Ayi, T.C., Bowcock, A.M., and Baer, R. 1997. Cell cycle-dependent colocalization of BARD1 and BRCA1 proteins in discrete nuclear domains. Proc. Natl. Acad. Sci. 94: 12075-12080.
22. Kleiman, F.E., and Manley, J.L. 1999. Functional interaction of BRCA1-associated BARD1 with polyadenylation factor CstF-50. Science 285: 1576-1579.
23. -. 2001. The BARD1-CstF-50 interaction links mRNA 3′ end formation to DNA damage and tumor suppression. Cell 104: 743-753.
24. Krum, S.A., Miranda, G.A., Lin, C., and Lane, T.F. 2003. BRCA1 associates with processive RNA polymerase II. J. Biol. Chem. 278: 52012-52020.
25. Lamond, A.I., and Spector, D.L. 2003. Nuclear speckles: A model for nuclear organelles. Nat. Rev. Mol. Cell Biol. 4: 605-612.
26. Le Page, F., Randrianarison, V., Marot, D., Cabannes, J., Perricaudet, M., Feunteun, J., and Sarasin, A. 2000. BRCA1 and BRCA2 are necessary for the transcription-coupled repair of the oxidative 8-oxoguanine lesions in human cells. Cancer Res. 60: 5548-5552.
27. Lee, K.B., Wang, D., Lippard, S.J., and Sharp, P.A. 2002. Transcription-coupled and DNA damage-dependent ubiquitination of RNA polymerase II in vitro. Proc. Natl. Acad. Sci. 99: 4239-4244.
28. Lommel, L., Gregory, S.M., Becker, K.I., and Sweder, K.S. 2000. Transcription-coupled DNA repair in yeast transcription factor IIE (TFIIE) mutants. Nucleic Acids Res. 28: 835-842.
29. Luo, Z., Zheng, J., Lu, Y., and Bregman, D.B. 2001. Ultraviolet radiation alters the phosphorylation of RNA polymerase II large subunit and accelerates its proteasome-dependent degradation. Mutat. Res. 486: 259-274.
30. Mallery, D.L., Vandenberg, C.J., and Hiom, K. 2002. Activation of the E3 ligase function of the BRCA1/BARD1 complex by polyubiquitin chains. EMBO J. 21: 6755-6762.
31. Mayne, L.V. and Lehmann, A.R. 1982. Failure of RNA synthesis to recover after UV irradiation: An early defect in cells from individuals with Cockayne's syndrome and Xxeroderma Pigmentosum. Cancer Res. 42: 1473-1478.
32. McCracken, S., Fong, N., Yankulov, K., Ballantyne, S., Pan, G., Greenblatt, J., Patterson, S.D., Wickens, M., and Bentley, D.L. 1997. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357-361.
33. McKay, B.C., Chen, F., Clarke, S.T., Wiggin, H.E., Harley, L.M., and Ljungman, M. 2001. UV light-induced degradation of RNA polymerase II is dependent of Cockayne's syndrome A and B proteins but not p53 or MLH1. Mutat. Res. 485:93-105.
34. Mitsui, A. and Sharp, P.A. 1999. Ubiquitination of RNA polymerase II large subunit signaled by phosphorylation of carboxyl-terminal domain. Proc. Natl. Acad. Sci. 96:6054-6059.
35. Muratani, M. and Tansey, W. 2003. How the ubiquitin-proteasome system controls transcription. Nat. Rev. Mol. Cell Biol. 4: 192-201.
36. Mullenders, L.H.F. 1998. Transcription response and nucleotide excision repair. Mutat. Res. 409: 59-64.
37. Neumann, S., Petfalski, E., Brugger, B., Grobhans, H., Wieland, F., Tollervey, D., and Hurt, E. 2003. Formation and nuclear export of tRNA, rRNA and mRNA is regulated by the ubiquitin ligase Rsp5p. EMBO J. 4: 1156-1162.
38. Nishikawa, H., Ooka, S., Sato, K., Arima, K., Okamoto, J., Klevit, R.E., Fukuda, M., and Ohta, T. 2004. Mass spectrometric and mutational analyses reveal Lys-6-linked polyubiquitin chains catalyzed by BRCA1-BARD1 ubiquitin ligase. J. Biol. Chem. 279: 3916-3924.
39. Paull, T.T., Cortez, D., Bowers, B., Elledge, S.J., and Gellert, M. 2001. Direct DNA binding by Brca1. Proc. Natl. Acad. Sci. 98: 6086-6091.
40. Ratner, J.N., Balasubramanian, B., Corden, J., Warren, S.L., and Bregman, D.B. 1998. Ultraviolet radiation-induced ubiquitination and proteasomal degradation of the large subunit of RNA polymerase II: Implications for transcription-coupled DNA repair. J. Biol. Chem. 273: 5184-5189.
41. Sato, K., Hayami, R., Wu, W., Nishikawa, T., Nishikawa, H., Okuda, Y., Ogata, H., Fukuda, M., and Ohta, T. 2004. Nucleophosmin/B23 is a candidate substrate for the BRCA1-BARD1 ubiquitin ligase. J. Biol. Chem. 279: 30919-30922.
42. Schul, W., Groenhout, B., Koberna, K., Takagaki, Y., Jenny, A., Manders, E.M.M., Raska, I., van Driel, R., and de Jong, L. 1996. The RNA 3′ cleavage factors CstF-64 kDa and CPSF 100 kDa are concentrated in nuclear domains closely associated with coiled bodies and newly synthesized RNA. EMBO J. 15: 2883-2892.
43. Scorilas, A. 2002. Polyadenylate polymerase (PAP) and 3′ end pre-mRNA processing: Function, assays, and association with disease. Crit. Rev. Clin. Lab. Sci. 39: 193-224.
44. Scully, R., Anderson, S.F., Chao, D.M., Wei, W., Ye, L., Young, R.A., Livingston, D.M., and Parvin, J.D. 1997a. BRCA1 is a component of the RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. 94: 5605-5610.
45. Scully, R., Chen, J., Ochs, R.L., Keegan, K., Hoekstra, M., Feunteun, J., and Livingston, D.M. 1997b. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90: 425-435.
46. Shatkin, A.J. and Manley, J.L. 2000. The ends of the affair: Capping and polyadenylation. Nat. Struct. Biol. 7: 838-842.
47. Starita, L.M. and Parvin, J.D. 2003. The multiple nuclear functions of BRCA1: Transcription, ubiquitination and DNA repair. Curr. Opin. Cell. Biol. 15: 345-350.
48. Starita, L.M., Machida, Y., Sankaran, S., Elias, J.E., Griffin, K., Schlegel, B.P., Gygi, S.P., and Parvin, J.D. 2004. BRCA1-dependent ubiquitination of γ-tubulin regulates centrosome number. Mol. Cell. Biol. 24: 8457-8466.
49. Svejstrup, J.Q. 2002. Mechanisms of transcription-coupled DNA repair. Nat. Rev. Mol. Cell Biol. 3: 21-29.
50. Takagaki, Y. and Manley, J.L. 1998. Levels of polyadenylation factor CstF-64 control IgM heavy chain mRNA accumulation and other events associated with B cell differentiation. Mol. Cell 2: 761-771.
51. Takagaki, Y., Seipelt, R.L., Peterson, M.L., and Manley, J.L. 1996. The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation. Cell 87: 941-952.
52. Tornaletti, S., Reines, D., and Hanawalt, P.C. 1999. Structural characterization of RNA polymerase II complexes arrested by a cyclobutane pyrimidine dimer in the transcribed strand of template DNA. J. Biol. Chem. 274: 24124-24130.
53. van den Boom, V., Jaspers, N.G.J., and Vermeulen, W. 2002. When machines get stuck-obstructed RNA polymerase II: Displacement, degradation or suicide. Bioessays 24: 780-784.
54. Venkitaraman, A.R. 2002. Cancer susceptibility and the functions of BRCA1 and BRCA2. Cell 108: 171-182.
55. Wang, Y., Cortez, D., Yazdi, P., Neff, N., Elledge, S.J., and Qin, J. 2000. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes & Dev. 14: 927-939.
56. Woudstra, E.C., Gilbert, C., Fellows, J., Jansen, L., Brouwer, J., Erdjument-Bromage, H., Tempst, P., and Svejstrup, J.Q. 2002. A Rad26-Def1 complex coordinates repair and RNA pol II proteolysis in response to DNA damage. Nature 415: 929-933.
57. Wu-Baer, F., Lagrazon, K., Yuan, W., and Baer, R. 2003. The BRCA1/BARD1 heterodimer assembles polyubiquitin chains through an unconventional linkage involving lysine residue K6 of ubiquitin. J. Biol. Chem. 278:34743-34746.
58. Xia, Y., Pao, G.M., Chen, H.W., Verma, I.M., and Hunter, T. 2003. Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J. Biol. Chem. 278: 5255-5263.
59. Zhao, J., Hyman, L., and Moore, C. 1999. Formation of mRNA 3′ ends in eukaryotes: Mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol. Mol. Biol. Rev. 63: 405-445.