Saccharomyces cerevisiae sen1 helicase domain exhibits 5′- to 3′-helicase activity with a preference for translocation on DNA rather than RNA

Journal of Biological Chemistry

Volumn 290, Issue 38, 2015, Pages 22880-22889

  Martin Tumasz, Stephen ^a   Brow, David A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINS; DNA; ESCHERICHIA COLI; PROTEINS; PURIFICATION; RECOMBINANT PROTEINS; RNA; TRANSCRIPTION; YEAST;

BIOCHEMICAL STUDIES; HELICASE ACTIVITIES; SALT CONCENTRATION; SCHIZOSACCHAROMYCES POMBE; SINGLE STRANDED RNA; TRANSCRIPTION TERMINATION; TRINUCLEOTIDE; YEAST SACCHAROMYCES CEREVISIAE;

NUCLEIC ACIDS;

FUNGAL DNA; FUNGAL ENZYME; FUNGAL RNA; SEN1 HELICASE; SINGLE STRANDED DNA; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; DNA HELICASE; RECOMBINANT PROTEIN; RNA HELICASE; SACCHAROMYCES CEREVISIAE PROTEIN; SEN1 PROTEIN, S CEREVISIAE;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA RNA HYBRIDIZATION; DNA TRANSFER; ENZYME ACTIVITY; ENZYME PURIFICATION; MICROARRAY ANALYSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA BINDING; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; TRANSCRIPTION TERMINATION; TRINUCLEOTIDE REPEAT; CHEMISTRY; ENZYME SPECIFICITY; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TERTIARY STRUCTURE;

DNA HELICASES; DNA, FUNGAL; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; RNA HELICASES; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SUBSTRATE SPECIFICITY;

EID: 84942915843     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.674002     Document Type: Article

References (31)

1. Winey, M., and Culbertson, M. R. (1988) Mutations affecting the tRNAsplicing endonuclease activity of Saccharomyces cerevisiae. Genetics 118, 609-617
2. DeMarini, D. J., Winey, M., Ursic, D., Webb, F., and Culbertson, M. R. (1992) SEN1, a positive effector of tRNA-splicing endonuclease in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 2154-2164
3. Steinmetz, E. J., and Brow, D. A. (1996) Repression of gene expression by an exogenous sequence element acting in concert with a heterogeneous nuclear ribonucleoprotein-like protein, Nrd1, and the putative helicase Sen1. Mol. Cell. Biol. 16, 6993-7003
4. Steinmetz, E. J., and Brow, D. A. (1998) Control of pre-mRNA accumulation by the essential yeast protein Nrd1 requires high-affinity transcript binding and a domain implicated in RNA polymerase II association. Proc. Natl. Acad. Sci. U.S.A. 95, 6699-6704
5. Steinmetz, E. J., Conrad, N. K., Brow, D. A., and Corden, J. L. (2001) RNA-binding protein Nrd1 directs poly(A)-independent 3-end formation of RNA polymerase II transcripts. Nature 413, 327-331
6. Steinmetz, E. J., Warren, C. L., Kuehner, J. N., Panbehi, B., Ansari, A. Z., and Brow, D. A. (2006) Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell 24, 735-746
7. Ursic, D., Himmel, K. L., Gurley, K. A., Webb, F., and Culbertson, M. R. (1997) The yeast SEN1 gene is required for the processing of diverse RNA classes. Nucleic Acids Res. 25, 4778-4785
8. Rasmussen, T. P., and Culbertson, M. R. (1998) The putative nucleic acid helicase Sen1p is required for formation and stability of termini and for maximal rates of synthesis and levels of accumulation of small nucleolar RNAs in Saccharomyces cerevisiae. Mol. Cell. Biol. 18, 6885-6896
9. Ursic, D., Chinchilla, K., Finkel, J. S., and Culbertson, M. R. (2004) Multiple protein/protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNA repair and RNA processing. Nucleic Acids Res. 32, 2441-2452
10. Mischo, H. E., Gómez-González, B., Grzechnik, P., Rondón, A. G., Wei, W., Steinmetz, L., Aguilera, A., and Proudfoot, N.J. (2011) Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell 41, 21-32
11. Alzu, A., Bermejo, R., Begnis, M., Lucca, C., Piccini, D., Carotenuto, W., Saponaro, M., Brambati, A., Cocito, A., Foiani, M., and Liberi, G. (2012) Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 151, 835-846
12. Jankowsky, E. (2011) RNA helicases at work: binding and rearranging. Trends Biochem. Sci. 36, 19-29
13. Czaplinski, K., Weng, Y., Hagan, K. W., and Peltz, S. W. (1995) Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA 1, 610-623
14. Guenther, U.-P., Handoko, L., Laggerbauer, B., Jablonka, S., Chari, A., Alzheimer, M., Ohmer, J., Plöttner, O., Gehring, N., Sickmann, A., von Au, K., Schuelke, M., and Fischer, U. (2009) IGHMBP2 is a ribosome-associated helicase inactive in the neuromuscular disorder distal SMA type 1 (DSMA1). Hum. Mol. Genet. 18, 1288-1300
15. Moreira, M. C., Klur, S., Watanabe, M., Németh, A. H., Le Ber I., Moniz, J. C., Tranchant, C., Aubourg, P., Tazir, M., Schöls, L., Pandolfo, M., Schulz, J. B., Pouget, J., Calvas, P., Shizuka-Ikeda, M., et al. (2004) Senataxin, the ortholog of a yeast RNA helicase, is mutant in ataxia-ocular apraxia 2. Nat. Genet. 36, 225-227
16. Chen, Y. Z., Bennett, C. L., Huynh, H. M., Blair, I. P., Puls, I., Irobi, J., Dierick, I., Abel, A., Kennerson, M. L., Rabin, B. A., Nicholson, G. A., Auer-Grumbach, M., Wagner, K., De Jonghe, P., Griffin, J. W., et al. (2004) DNA/RNA helicase gene mutations in a form of juvenile amyotrophic lateral sclerosis (ALS4). Am. J. Hum. Genet. 74, 1128-1135
17. Grohmann, K., Schuelke, M., Diers, A., Hoffmann, K., Lucke, B., Adams, C., Bertini, E., Leonhardt-Horti, H., Muntoni, F., Ouvrier, R., Pfeufer, A., Rossi, R., Van Maldergem, L., Wilmshurst, J. M., Wienker, T. F., et al. (2001) Mutations in the gene encoding immunoglobulin μ-binding protein 2 cause spinal muscular atrophy with respiratory distress type 1. Nat. Genet. 29, 75-77
18. Kim, H.-D., Choe, J., and Seo, Y.-S. (1999) The sen1+ gene of Schizosac-charomyces pombe, a homolog of budding yeast SEN1, encodes an RNA and DNA helicase. Biochemistry 38, 14697-14710
19. Porrua, O., and Libri, D. (2013) A bacterial-like mechanism for transcription termination by the Sen1p helicase in budding yeast. Nat. Struct. Mol. Biol. 20, 884-891
20. DeMarini, D. J., Papa, F. R., Swaminathan, S., Ursic, D., Rasmussen, T. P., Culbertson, M. R., and Hochstrasser, M. (1995) The yeast SEN3 gene encodes a regulatory subunit of the 26S proteasome complex required for ubiquitin-dependent protein degradation in vivo. Mol. Cell. Biol. 15, 6311-6321
21. Chan, Y. A., Aristizabal, M. J., Lu, P. Y., Luo, Z., Hamza, A., Kobor, M.S., Stirling, P. C., and Hieter, P. (2014) Genome-wide profiling of yeast DNA: RNA hybrid prone sites with DRIP-Chip. PLoS Genet. 10, e1004288
22. Lee, C.-D., Sun, H.-C., Hu, S.-M., Chiu, C.-F., Homhuan, A., Liang, S.-M., Leng, C.-H., and Wang, T.-F. (2008) An improved SUMO fusion protein system for effective production of native proteins. Protein Sci. 17, 1241-1248
23. Myers, K. S., Yan, H., Ong, I. M., Chung, D., Liang, K., Tran, F., Keleş, S., Landick, R., and Kiley, P.J. (2013) Genome-scale analysis of E. coli FNR reveals complex features of transcription factor binding. PLoS Genet. 9, e1003565
24. Chen, X., Müller, U., Sundling, K. E., and Brow, D. A. (2014) Saccharomyces cerevisiae Sen1 as a model for the study of mutations in human senataxin that elicit cerebellar ataxia. Genetics 198, 577-590
25. Chakrabarti, S., Jayachandran, U., Bonneau, F., Fiorini, F., Basquin, C., Domcke, S., Le Hir, H., and Conti, E. (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell 41, 693-703
26. Castelnuovo, M., Rahman, S., Guffanti, E., Infantino, V., Stutz, F., and Zenklusen, D. (2013) Bimodal expression of PHO84 is modulated by early termination of antisense transcription. Nat. Struct. Mol. Biol. 20, 851-858
27. Castelnuovo, M., Zaugg, J. B., Guffanti, E., Maffioletti, A., Camblong, J., Xu, Z., Clauder-Münster, S., Steinmetz, L. M., Luscombe, N. M., and Stutz, F. (2014) Role of histone modifications and early termination in pervasive transcription and antisense-mediated gene silencing in yeast. Nucleic Acids Res. 42, 4348-4362
28. Creamer, T. J., Darby, M. M., Jamonnak, N., Schaughency, P., Hao, H., Wheelan, S. J., and Corden, J. L. (2011) Transcriptome-wide binding sites for components of the Saccharomyces cerevisiae non-poly(A) termination pathway: Nrd1, Nab3, and Sen1. PLoS Genet. 7, e1002329
29. Cheng, Z., Muhlrad, D., Lim, M. K., Parker, R., and Song, H. (2007) Structural and functional insights into the human Upf1 helicase core. EMBO J. 26, 253-264
30. Lim, S. C., Bowler, M. W., Lai, T. F., and Song, H. (2012) The ghmbp2 helicase structure reveals the molecular basis for disease-causing mutations in DMSA1. Nucleic Acids Res. 40, 11009-110022
31. Bailey, T. L., and Elkan, C. (1994) Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology, pp. 28-36, AAAI Press, Menlo Park, CA