The U4/U6 recycling factor SART3 has histone chaperone activity and associates with USP15 to regulate H2B deubiquitination

Journal of Biological Chemistry

Volumn 289, Issue 13, 2014, Pages 8916-8930

  Long, Lindsey ^a   Thelen, Joseph P ^a   Furgason, Melonnie ^a,d   Haj Yahya, Mahmood ^b   Brik, Ashraf ^b   Cheng, Dongmei ^c   Peng, Junmin ^c   Yao, Tingting ^a  

^a Department of Environmental and Radiological Health Sciences   (United States)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

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

^d Kettering College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MACHINERY; NUCLEIC ACIDS; TRANSCRIPTION;

AFFINITY PURIFICATION; DEUBIQUITINATING ENZYMES; DNA REPAIR PROCESS; HISTONE CHAPERONE NAP1; PHYSICAL INTERACTIONS; POST-TRANSLATIONAL MODIFICATIONS; REGULATION OF TRANSCRIPTION; SPLICING MACHINERY;

PROTEINS;

CHAPERONE; HISTONE H2B; MESSENGER RNA; SART3 PROTEIN; UNCLASSIFIED DRUG; DEUBIQUITINASE; HISTONE; NUCLEOSOME; RNA BINDING PROTEIN; RNF20 PROTEIN, HUMAN; RNF40 PROTEIN, HUMAN; SART3 PROTEIN, HUMAN; SMALL NUCLEAR RIBONUCLEOPROTEIN; TUMOR ANTIGEN; UBIQUITIN PROTEIN LIGASE; USP15 PROTEIN, HUMAN;

ARTICLE; CHROMATIN STRUCTURE; CONJUGATION; DNA REPAIR; DNA REPLICATION; DNA TRANSCRIPTION; HISTONE UBIQUITINATION; NUCLEOSOME; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; RNA SPLICING; ANIMAL; CELL LINE; CHEMISTRY; ENZYME SPECIFICITY; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; UBIQUITINATION;

ANIMALS; ANTIGENS, NEOPLASM; CELL LINE; HISTONES; HUMANS; NUCLEOSOMES; RIBONUCLEOPROTEIN, U4-U6 SMALL NUCLEAR; RNA SPLICING; RNA-BINDING PROTEINS; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC; UBIQUITIN-PROTEIN LIGASES; UBIQUITIN-SPECIFIC PROTEASES; UBIQUITINATION;

EID: 84897373749     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.551754     Document Type: Article

References (66)

1. Kouzarides, T. (2007) Chromatin modifications and their function. Cell 128, 693-705
2. Patel, D. J., and Wang, Z. (2013) Readout of epigenetic modifications. Annu. Rev. Biochem. 82, 81-118
3. Pickart, C. M., and Eddins, M. J. (2004) Ubiquitin: structures, functions, mechanisms. Biochim. Biophys. Acta 1695, 55-72 (Pubitemid 39585154)
4. Osley, M. A. (2006) Regulation of histone H2A and H2B ubiquitylation. Brief Funct. Genomic Proteomic 5, 179-189
5. Weake, V. M., and Workman, J. L. (2008) Histone ubiquitination: triggering gene activity. Mol. Cell 29, 653-663 (Pubitemid 351400924)
6. Kim, J., and Roeder, R. G. (2009) Direct Bre1-Paf1 complex interactions and RING finger-independent Bre1-Rad6 interactions mediate histone H2B ubiquitylation in yeast. J. Biol. Chem. 284, 20582-20592
7. Kim, J., Hake, S. B., and Roeder, R. G. (2005) The human homolog of yeast BRE1 functions as a transcriptional coactivator through direct activator interactions. Mol. Cell 20, 759-770 (Pubitemid 41740697)
8. Xiao, T., Kao, C. F., Krogan, N. J., Sun, Z. W., Greenblatt, J. F., Osley, M. A., and Strahl, B. D. (2005) Histone H2B ubiquitylation is associated with elongating RNA polymerase II. Mol. Cell. Biol. 25, 637-651 (Pubitemid 40096585)
9. Minsky, N., Shema, E., Field, Y., Schuster, M., Segal, E., and Oren, M. (2008) Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat. Cell Biol. 10, 483-488
10. Jung, I., Kim, S. K., Kim, M., Han, Y. M., Kim, Y. S., Kim, D., and Lee, D. (2012) H2B monoubiquitylation is a 5′-enriched active transcription mark and correlates with exon-intron structure in human cells. Genome Res. 22, 1026-1035
11. Shieh, G. S., Pan, C. H., Wu, J. H., Sun, Y. J., Wang, C. C., Hsiao, W. C., Lin, C. Y., Tung, L., Chang, T. H., Fleming, A. B., Hillyer, C., Lo, Y. C., Berger, S. L., Osley, M. A., and Kao, C. F. (2011) H2B ubiquitylation is part of chromatin architecture that marks exon-intron structure in budding yeast. BMC Genomics 12, 627
12. Sun, Z. W., and Allis, C. D. (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418, 104-108
13. Lee, J. S., Shukla, A., Schneider, J., Swanson, S. K., Washburn, M. P., Florens, L., Bhaumik, S. R., and Shilatifard, A. (2007) Histone crosstalk between H2B monoubiquitination and H3 methylation mediated by COMPASS. Cell 131, 1084-1096 (Pubitemid 350235018)
14. Fierz, B., Chatterjee, C., McGinty, R. K., Bar-Dagan, M., Raleigh, D. P., and Muir, T. W. (2011) Histone H2B ubiquitylation disrupts local and higherorder chromatin compaction. Nat. Chem. Biol. 7, 113-119
15. Lee, J. S., Garrett, A. S., Yen, K., Takahashi, Y. H., Hu, D., Jackson, J., Seidel, C., Pugh, B. F., and Shilatifard, A. (2012) Codependency of H2B monoubiquitination and nucleosome reassembly on Chd1. Genes Dev. 26, 914-919
16. Fleming, A. B., Kao, C. F., Hillyer, C., Pikaart, M., and Osley, M. A. (2008) H2B ubiquitylation plays a role in nucleosome dynamics during transcription elongation. Mol. Cell 31, 57-66 (Pubitemid 351905918)
17. Pavri, R., Zhu, B., Li, G., Trojer, P., Mandal, S., Shilatifard, A., and Reinberg, D. (2006) Histone H2B monoubiquitination functions cooperatively with FACT to regulate elongation by RNA polymerase II. Cell 125, 703-717 (Pubitemid 43732350)
18. Wyce, A., Xiao, T., Whelan, K. A., Kosman, C., Walter, W., Eick, D., Hughes, T. R., Krogan, N. J., Strahl, B. D., and Berger, S. L. (2007) H2B ubiquitylation acts as a barrier to Ctk1 nucleosomal recruitment prior to removal by Ubp8 within a SAGA-related complex. Mol. Cell 27, 275-288 (Pubitemid 47058302)
19. Shema, E., Kim, J., Roeder, R. G., and Oren, M. (2011) RNF20 inhibits TFIIS-facilitated transcriptional elongation to suppress pro-oncogenic gene expression. Mol. Cell 42, 477-488
20. Batta, K., Zhang, Z., Yen, K., Goffman, D. B., and Pugh, B. F. (2011) Genome-wide function of H2B ubiquitylation in promoter and genic regions. Genes Dev. 25, 2254-2265
21. Turner, S. D., Ricci, A. R., Petropoulos, H., Genereaux, J., Skerjanc, I. S., and Brandl, C. J. (2002) The E2 ubiquitin conjugase Rad6 is required for the ArgR/Mcm1 repression of ARG1 transcription. Mol. Cell. Biol. 22, 4011-4019 (Pubitemid 34556572)
22. Henry, K. W., Wyce, A., Lo, W. S., Duggan, L. J., Emre, N. C., Kao, C. F., Pillus, L., Shilatifard, A., Osley, M. A., and Berger, S. L. (2003) Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev. 17, 2648-2663 (Pubitemid 37363070)
23. Rodríguez-Navarro, S. (2009) Insights into SAGA function during gene expression. EMBO Rep. 10, 843-850
24. Moehle, E. A., Ryan, C. J., Krogan, N. J., Kress, T. L., and Guthrie, C. (2012) The yeast SR-like protein Npl3 links chromatin modification to mRNA processing. PLoS Genet. 8, e1003101
25. Yao, T., Song, L., Xu, W., DeMartino, G. N., Florens, L., Swanson, S. K., Washburn, M. P., Conaway, R. C., Conaway, J. W., and Cohen, R. E. (2006) Proteasome recruitment and activation of the Uch37 deubiquitinating enzyme by Adrm1. Nat. Cell Biol. 8, 994-1002 (Pubitemid 44314731)
26. Dyer, P. N., Edayathumangalam, R. S., White, C. L., Bao, Y., Chakravarthy, S., Muthurajan, U. M., and Luger, K. (2004) Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23-44 (Pubitemid 38124858)
27. Baker, R. T., Catanzariti, A. M., Karunasekara, Y., Soboleva, T. A., Sharwood, R., Whitney, S., and Board, P. G. (2005) Using deubiquitylating enzymes as research tools. Methods Enzymol. 398, 540-554 (Pubitemid 41578912)
28. McBryant, S. J., Park, Y. J., Abernathy, S. M., Laybourn, P. J., Nyborg, J. K., and Luger, K. (2003) Preferential binding of the histone (H3-H4)2 tetramer by NAP1 is mediated by the amino-terminal histone tails. J. Biol. Chem. 278, 44574-44583 (Pubitemid 37377211)
29. McGinty, R. K., Kim, J., Chatterjee, C., Roeder, R. G., and Muir, T. W. (2008) Chemically ubiquitylated histone H2B stimulates hDot1L-mediated intranucleosomal methylation. Nature 453, 812-816 (Pubitemid 351793779)
30. Rogakou, E. P., Redon, C., Boon, C., Johnson, K., and Bonner, W. M. (2000) Rapid histone extraction for electrophoretic analysis. BioTechniques 28, 38-40
31. Haj-Yahya, M., Eltarteer, N., Ohayon, S., Shema, E., Kotler, E., Oren, M., and Brik, A. (2012) N-methylation of isopeptide bond as a strategy to resist deubiquitinases. Angew Chem. Int. Ed Engl. 51, 11535-11539
32. Dechassa, M. L., Wyns, K., Li, M., Hall, M. A., Wang, M. D., and Luger, K. (2011) Structure and Scm3-mediated assembly of budding yeast centromeric nucleosomes. Nature Commun. 2, 313
33. Yin, L., Krantz, B., Russell, N. S., Deshpande, S., and Wilkinson, K. D. (2000) Nonhydrolyzable diubiquitin analogues are inhibitors of ubiquitin conjugation and deconjugation. Biochemistry 39, 10001-10010 (Pubitemid 30626851)
34. Carlile, C. M., Pickart, C. M., Matunis, M. J., and Cohen, R. E. (2009) Synthesis of free and proliferating cell nuclear antigen-bound polyubiquitin chains by the RING E3 ubiquitin ligase Rad5. J. Biol. Chem. 284, 29326-29334
35. Fierz, B., Kilic, S., Hieb, A. R., Luger, K., and Muir, T. W. (2012) Stability of nucleosomes containing homogenously ubiquitylated H2A and H2B prepared using semisynthesis. J. Am. Chem. Soc. 134, 19548-19551
36. Ryu, K. Y., Baker, R. T., and Kopito, R. R. (2006) Ubiquitin-specific protease 2 as a tool for quantification of total ubiquitin levels in biological specimens. Anal. Biochem. 353, 153-155 (Pubitemid 43668941)
37. Samara, N. L., Datta, A. B., Berndsen, C. E., Zhang, X., Yao, T., Cohen, R. E., and Wolberger, C. (2010) Structural insights into the assembly and function of the SAGA deubiquitinating module. Science 328, 1025-1029
38. Köhler, A., Zimmerman, E., Schneider, M., Hurt, E., and Zheng, N. (2010) Structural basis for assembly and activation of the heterotetrameric SAGA histone H2B deubiquitinase module. Cell 141, 606-617
39. Kumar, K. S., Spasser, L., Ohayon, S., Erlich, L. A., and Brik, A. (2011) Expeditious chemical synthesis of ubiquitinated peptides employing orthogonal protection and native chemical ligation. Bioconjugate Chem. 22, 137-143
40. Sowa, M. E., Bennett, E. J., Gygi, S. P., and Harper, J. W. (2009) Defining the human deubiquitinating enzyme interaction landscape. Cell 138, 389-403
41. Song, E. J., Werner, S. L., Neubauer, J., Stegmeier, F., Aspden, J., Rio, D., Harper, J. W., Elledge, S. J., Kirschner, M. W., and Rape, M. (2010) The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev. 24, 1434-1447
42. Bell, M., Schreiner, S., Damianov, A., Reddy, R., and Bindereif, A. (2002) p110, a novel human U6 snRNP protein and U4/U6 snRNP recycling factor. EMBO J. 21, 2724-2735 (Pubitemid 34619388)
43. Rader, S. D., and Guthrie, C. (2002) A conserved Lsm-interaction motif in Prp24 required for efficient U4/U6 di-snRNP formation. Rna 8, 1378-1392 (Pubitemid 35332962)
44. Staněk, D., Rader, S. D., Klingauf, M., and Neugebauer, K. M. (2003) Targeting of U4/U6 small nuclear RNP assembly factor SART3/p110 to Cajal bodies. J. Cell Biol. 160, 505-516 (Pubitemid 36254389)
45. Elsasser, S. J., and D'Arcy, S. (2012) Towards a mechanism for histone chaperones. Biochim. Biophys. Acta 1819, 211-221
46. Lusser, A., and Kadonaga, J. T. (2004) Strategies for the reconstitution of chromatin. Nature Methods 1, 19-26
47. Ng, H. H., Xu, R. M., Zhang, Y., and Struhl, K. (2002) Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem. 277, 34655-34657
48. Pirngruber, J., Shchebet, A., Schreiber, L., Shema, E., Minsky, N., Chapman, R. D., Eick, D., Aylon, Y., Oren, M., and Johnsen, S. A. (2009) CDK9 directs H2B monoubiquitination and controls replication-dependent histone mRNA 3′-end processing. EMBO Rep. 10, 894-900
49. Chen, J. J., Tsu, C. A., Gavin, J. M., Milhollen, M. A., Bruzzese, F. J., Mallender, W. D., Sintchak, M. D., Bump, N. J., Yang, X., Ma, J., Loke, H. K., Xu, Q., Li, P., Bence, N. F., Brownell, J. E., and Dick, L. R. (2011) Mechanistic studies of substrate-assisted inhibition of ubiquitin-activating enzyme by adenosine sulfamate analogues. J. Biol. Chem. 286, 40867-40877
50. Shema-Yaacoby, E., Nikolov, M., Haj-Yahya, M., Siman, P., Allemand, E., Yamaguchi, Y., Muchardt, C., Urlaub, H., Brik, A., Oren, M., and Fischle, W. (2013) Systematic identification of proteins binding to chromatin-embedded ubiquitylated H2B reveals recruitment of SWI/SNF to regulate transcription. Cell Reports 4, 601-608
51. Fuchs, G., Shema, E., Vesterman, R., Kotler, E., Wolchinsky, Z., Wilder, S., Golomb, L., Pribluda, A., Zhang, F., Haj-Yahya, M., Feldmesser, E., Brik, A., Yu, X., Hanna, J., Aberdam, D., Domany, E., and Oren, M. (2012) RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol. Cell 46, 662-673
52. Mosbech, A., Lukas, C., Bekker-Jensen, S., and Mailand, N. (2013) The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J. Biol. Chem. 288, 16579-16587
53. Lang, G., Bonnet, J., Umlauf, D., Karmodiya, K., Koffler, J., Stierle, M., Devys, D., and Tora, L. (2011) The tightly controlled deubiquitination activity of the human SAGA complex differentially modifies distinct gene regulatory elements. Mol. Cell. Biol. 31, 3734-3744
54. Nicassio, F., Corrado, N., Vissers, J. H., Areces, L. B., Bergink, S., Marteijn, J. A., Geverts, B., Houtsmuller, A. B., Vermeulen, W., Di Fiore, P. P., and Citterio, E. (2007) Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr. Biol. 17, 1972-1977 (Pubitemid 350088491)
55. Zhang, Z., Jones, A., Joo, H. Y., Zhou, D., Cao, Y., Chen, S., Erdjument-Bromage, H., Renfrow, M., He, H., Tempst, P., Townes, T. M., Giles, K. E., Ma, L., and Wang, H. (2013) USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing. Genes Dev. 27, 1581-1595
56. Joo, H. Y., Zhai, L., Yang, C., Nie, S., Erdjument-Bromage, H., Tempst, P., Chang, C., and Wang, H. (2007) Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449, 1068-1072 (Pubitemid 350014605)
57. Villeneuve, N. F., Tian, W., Wu, T., Sun, Z., Lau, A., Chapman, E., Fang, D., and Zhang, D. D. (2013) USP15 negatively regulates Nrf2 through deubiquitination of Keap1. Mol. Cell 51, 68-79
58. Faronato, M., Patel, V., Darling, S., Dearden, L., Clague, M. J., Urbé, S., and Coulson, J. M. (2013) The deubiquitylase USP15 stabilizes newly synthesized REST and rescues its expression at mitotic exit. Cell Cycle 12, 1964-1977
59. Hayes, S. D., Liu, H., MacDonald, E., Sanderson, C. M., Coulson, J. M., Clague, M. J., and Urbé, S. (2012) Direct and indirect control of mitogen-activated protein kinase pathway-associated components, BRAP/IMP E3 ubiquitin ligase and CRAF/RAF1 kinase, by the deubiquitylating enzyme USP15. J. Biol. Chem. 287, 43007-43018
60. Eichhorn, P. J., Rodón, L., Gonzàlez-Junca, A., Dirac, A., Gili, M., Martínez-Sáez, E., Aura, C., Barba, I., Peg, V., Prat, A., Cuartas, I., Jimenez, J., García-Dorado, D., Sahuquillo, J., Bernards, R., Baselga, J., and Seoane, J. (2012) USP15 stabilizes TGF-beta receptor I and promotes oncogenesis through the activation of TGF-β signaling in glioblastoma. Nat. Med. 18, 429-435
61. Inui, M., Manfrin, A., Mamidi, A., Martello, G., Morsut, L., Soligo, S., Enzo, E., Moro, S., Polo, S., Dupont, S., Cordenonsi, M., and Piccolo, S. (2011) USP15 is a deubiquitylating enzyme for receptor-activated SMADs. Nat. Cell Biol. 13, 1368-1375
62. Hetfeld, B. K., Helfrich, A., Kapelari, B., Scheel, H., Hofmann, K., Guterman, A., Glickman, M., Schade, R., Kloetzel, P. M., and Dubiel, W. (2005) The zinc finger of the CSN-associated deubiquitinating enzyme USP15 is essential to rescue the E3 ligase Rbx1. Curr. Biol. 15, 1217-1221 (Pubitemid 40950520)
63. Raghunathan, P. L., and Guthrie, C. (1998)Aspliceosomal recycling factor that reanneals U4 and U6 small nuclear ribonucleoprotein particles. Science 279, 857-860 (Pubitemid 28106278)
64. Lin, S., Coutinho-Mansfield, G., Wang, D., Pandit, S., and Fu, X. D. (2008) The splicing factor SC35 has an active role in transcriptional elongation. Nature Struct. Mol. Biol. 15, 819-826
65. Sims, R. J., 3rd, Millhouse, S., Chen, C. F., Lewis, B. A., Erdjument-Bromage, H., Tempst, P., Manley, J. L., and Reinberg, D. (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol. Cell 28, 665-676 (Pubitemid 350137805)
66. Kress, T. L., Krogan, N. J., and Guthrie, C. (2008) A single SR-like protein, Npl3, promotes pre-mRNA splicing in budding yeast. Mol. Cell 32, 727-734