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Article

Structures and Functions of the Multiple KOW Domains of Transcription Elongation Factor Spt5

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Pages 3354-3369 | Received 21 May 2015, Accepted 15 Jul 2015, Published online: 20 Mar 2023

REFERENCES

  • Thomas MC, Chiang CM. 2006. The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41:105–178. http://dx.doi.org/10.1080/10409230600648736.
  • Perales R, Bentley D. 2009. “Cotranscriptionality”: the transcription elongation complex as a nexus for nuclear transactions. Mol Cell 36:178–191. http://dx.doi.org/10.1016/j.molcel.2009.09.018.
  • Hsin JP, Manley JL. 2012. The RNA polymerase II CTD coordinates transcription and RNA processing. Genes Dev 26:2119–2137. http://dx.doi.org/10.1101/gad.200303.112.
  • Rondon AG, Jimeno S, Aguilera A. 2010. The interface between transcription and mRNP export: from THO to THSC/TREX-2. Biochim Biophys Acta 1799:533–538. http://dx.doi.org/10.1016/j.bbagrm.2010.06.002.
  • Hartzog GA, Fu J. 2013. The Spt4-Spt5 complex: a multi-faceted regulator of transcription elongation. Biochim Biophys Acta 1829:105–115. http://dx.doi.org/10.1016/j.bbagrm.2012.08.007.
  • Zhou Q, Li T, Price DH. 2012. RNA polymerase II elongation control. Annu Rev Biochem 81:119–143. http://dx.doi.org/10.1146/annurev-biochem-052610-095910.
  • Yamaguchi Y, Shibata H, Handa H. 2013. Transcription elongation factors DSIF and NELF: promoter-proximal pausing and beyond. Biochim Biophys Acta 1829:98–104. http://dx.doi.org/10.1016/j.bbagrm.2012.11.007.
  • Conaway RC, Conaway JW. 2013. The Mediator complex and transcription elongation. Biochim Biophys Acta 1829:69–75. http://dx.doi.org/10.1016/j.bbagrm.2012.08.017.
  • Jansen LE, den Dulk H, Brouns RM, de Ruijter M, Brandsma JA, Brouwer J. 2000. Spt4 modulates Rad26 requirement in transcription-coupled nucleotide excision repair. EMBO J 19:6498–6507. http://dx.doi.org/10.1093/emboj/19.23.6498.
  • Ding B, LeJeune D, Li S. 2010. The C-terminal repeat domain of Spt5 plays an important role in suppression of Rad26-independent transcription coupled repair. J Biol Chem 285:5317–5326. http://dx.doi.org/10.1074/jbc.M109.082818.
  • Li W, Giles C, Li S. 2014. Insights into how Spt5 functions in transcription elongation and repressing transcription coupled DNA repair. Nucleic Acids Res 42:7069–7083. http://dx.doi.org/10.1093/nar/gku333.
  • Pavri R, Gazumyan A, Jankovic M, Di Virgilio M, Klein I, Ansarah-Sobrinho C, Resch W, Yamane A, Reina San-Martin B, Barreto V, Nieland TJ, Root DE, Casellas R, Nussenzweig MC. 2010. Activation-induced cytidine deaminase targets DNA at sites of RNA polymerase II stalling by interaction with Spt5. Cell 143:122–133. http://dx.doi.org/10.1016/j.cell.2010.09.017.
  • Lindstrom DL, Squazzo SL, Muster N, Burckin TA, Wachter KC, Emigh CA, McCleery JA, Yates JR, III, Hartzog GA. 2003. Dual roles for Spt5 in pre-mRNA processing and transcription elongation revealed by identification of Spt5-associated proteins. Mol Cell Biol 23:1368–1378. http://dx.doi.org/10.1128/MCB.23.4.1368-1378.2003.
  • Tardiff DF, Abruzzi KC, Rosbash M. 2007. Protein characterization of Saccharomyces cerevisiae RNA polymerase II after in vivo cross-linking. Proc Natl Acad Sci U S A 104:19948–19953. http://dx.doi.org/10.1073/pnas.0710179104.
  • Yamaguchi Y, Wada T, Watanabe D, Takagi T, Hasegawa J, Handa H. 1999. Structure and function of the human transcription elongation factor DSIF. J Biol Chem 274:8085–8092. http://dx.doi.org/10.1074/jbc.274.12.8085.
  • Zhang Z, Wu CH, Gilmour DS. 2004. Analysis of polymerase II elongation complexes by native gel electrophoresis: evidence for a novel carboxyl-terminal domain-mediated termination mechanism. J Biol Chem 279:23223–23228. http://dx.doi.org/10.1074/jbc.M402956200.
  • Viktorovskaya OV, Appling FD, Schneider DA. 2011. Yeast transcription elongation factor Spt5 associates with RNA polymerase I and RNA polymerase II directly. J Biol Chem 286:18825–18833. http://dx.doi.org/10.1074/jbc.M110.202119.
  • Ping YH, Rana TM. 2001. DSIF and NELF interact with RNA polymerase II elongation complex and HIV-1 Tat stimulates P-TEFb-mediated phosphorylation of RNA polymerase II and DSIF during transcription elongation. J Biol Chem 276:12951–12958. http://dx.doi.org/10.1074/jbc.M006130200.
  • Bourgeois CF, Kim YK, Churcher MJ, West MJ, Karn J. 2002. Spt5 cooperates with human immunodeficiency virus type 1 Tat by preventing premature RNA release at terminator sequences. Mol Cell Biol 22:1079–1093. http://dx.doi.org/10.1128/MCB.22.4.1079-1093.2002.
  • Liu Y, Warfield L, Zhang C, Luo J, Allen J, Lang WH, Ranish J, Shokat KM, Hahn S. 2009. Phosphorylation of the transcription elongation factor Spt5 by yeast Bur1 kinase stimulates recruitment of the PAF complex. Mol Cell Biol 29:4852–4863. http://dx.doi.org/10.1128/MCB.00609-09.
  • Swanson MS, Malone EA, Winston F. 1991. SPT5, an essential gene important for normal transcription in Saccharomyces cerevisiae, encodes an acidic nuclear protein with a carboxy-terminal repeat. Mol Cell Biol 11:3009–3019.
  • Pei Y, Shuman S. 2003. Characterization of the Schizosaccharomyces pombe Cdk9/Pch1 protein kinase: Spt5 phosphorylation, autophosphorylation, and mutational analysis. J Biol Chem 278:43346–43356. http://dx.doi.org/10.1074/jbc.M307319200.
  • Yamada T, Yamaguchi Y, Inukai N, Okamoto S, Mura T, Handa H. 2006. P-TEFb-mediated phosphorylation of hSpt5 C-terminal repeats is critical for processive transcription elongation. Mol Cell 21:227–237. http://dx.doi.org/10.1016/j.molcel.2005.11.024.
  • Werner F. 2012. A nexus for gene expression-molecular mechanisms of Spt5 and NusG in the three domains of life. J Mol Biol 417:13–27. http://dx.doi.org/10.1016/j.jmb.2012.01.031.
  • Hirtreiter A, Damsma GE, Cheung AC, Klose D, Grohmann D, Vojnic E, Martin AC, Cramer P, Werner F. 2010. Spt4/5 stimulates transcription elongation through the RNA polymerase clamp coiled-coil motif. Nucleic Acids Res 38:4040–4051. http://dx.doi.org/10.1093/nar/gkq135.
  • Martinez-Rucobo FW, Sainsbury S, Cheung AC, Cramer P. 2011. Architecture of the RNA polymerase-Spt4/5 complex and basis of universal transcription processivity. EMBO J 30:1302–1310. http://dx.doi.org/10.1038/emboj.2011.64.
  • Hartzog GA, Kaplan CD. 2011. Competing for the clamp: promoting RNA polymerase processivity and managing the transition from initiation to elongation. Mol Cell 43:161–163. http://dx.doi.org/10.1016/j.molcel.2011.07.002.
  • Belogurov GA, Vassylyeva MN, Svetlov V, Klyuyev S, Grishin NV, Vassylyev DG, Artsimovitch I. 2007. Structural basis for converting a general transcription factor into an operon-specific virulence regulator. Mol Cell 26:117–129. http://dx.doi.org/10.1016/j.molcel.2007.02.021.
  • Burns CM, Richardson LV, Richardson JP. 1998. Combinatorial effects of NusA and NusG on transcription elongation and Rho-dependent termination in Escherichia coli. J Mol Biol 278:307–316. http://dx.doi.org/10.1006/jmbi.1998.1691.
  • Mooney RA, Schweimer K, Rosch P, Gottesman M, Landick R. 2009. Two structurally independent domains of E. coli NusG create regulatory plasticity via distinct interactions with RNA polymerase and regulators. J Mol Biol 391:341–358. http://dx.doi.org/10.1016/j.jmb.2009.05.078.
  • Kyrpides NC, Woese CR, Ouzounis CA. 1996. KOW: a novel motif linking a bacterial transcription factor with ribosomal proteins. Trends Biochem Sci 21:425–426. http://dx.doi.org/10.1016/S0968-0004(96)30036-4.
  • Steiner T, Kaiser JT, Marinkovic S, Huber R, Wahl MC. 2002. Crystal structures of transcription factor NusG in light of its nucleic acid- and protein-binding activities. EMBO J 21:4641–4653. http://dx.doi.org/10.1093/emboj/cdf455.
  • Reay P, Yamasaki K, Terada T, Kuramitsu S, Shirouzu M, Yokoyama S. 2004. Structural and sequence comparisons arising from the solution structure of the transcription elongation factor NusG from Thermus thermophilus. Proteins 56:40–51. http://dx.doi.org/10.1002/prot.20054.
  • Klein BJ, Bose D, Baker KJ, Yusoff ZM, Zhang X, Murakami KS. 2011. RNA polymerase and transcription elongation factor Spt4/5 complex structure. Proc Natl Acad Sci U S A 108:546–550. http://dx.doi.org/10.1073/pnas.1013828108.
  • Lasko P. 2010. Tudor domain. Curr Biol 20:R666–R667. http://dx.doi.org/10.1016/j.cub.2010.05.056.
  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882. http://dx.doi.org/10.1093/nar/25.24.4876.
  • Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680. http://dx.doi.org/10.1093/nar/22.22.4673.
  • Galtier N, Gouy M, Gautier C. 1996. SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548.
  • Bond CS, Schuttelkopf AW. 2009. ALINE: a WYSIWYG protein-sequence alignment editor for publication-quality alignments. Acta Crystallogr D Biol Crystallogr 65:510–512. http://dx.doi.org/10.1107/S0907444909007835.
  • Linding R, Russell RB, Neduva V, Gibson TJ. 2003. GlobPlot: exploring protein sequences for globularity and disorder. Nucleic Acids Res 31:3701–3708. http://dx.doi.org/10.1093/nar/gkg519.
  • Linding R, Jensen LJ, Diella F, Bork P, Gibson TJ, Russell RB. 2003. Protein disorder prediction: implications for structural proteomics. Structure 11:1453–1459. http://dx.doi.org/10.1016/j.str.2003.10.002.
  • Crooks GE, Hon G, Chandonia JM, Brenner SE. 2004. WebLogo: a sequence logo generator. Genome Res 14:1188–1190. http://dx.doi.org/10.1101/gr.849004.
  • Cole C, Barber JD, Barton GJ. 2008. The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36:W197–W201. http://dx.doi.org/10.1093/nar/gkn238.
  • Leaver-Fay A, Tyka M, Lewis SM, Lange OF, Thompson J, Jacak R, Kaufman K, Renfrew PD, Smith CA, Sheffler W, Davis IW, Cooper S, Treuille A, Mandell DJ, Richter F, Ban YE, Fleishman SJ, Corn JE, Kim DE, Lyskov S, Berrondo M, Mentzer S, Popovic Z, Havranek JJ, Karanicolas J, Das R, Meiler J, Kortemme T, Gray JJ, Kuhlman B, Baker D, Bradley P. 2011. ROSETTA3: an object-oriented software suite for the simulation and design of macromolecules. Methods Enzymol 487:545–574. http://dx.doi.org/10.1016/B978-0-12-381270-4.00019-6.
  • Kabsch W. 2010. Xds. Acta Crystallogr D Biol Crystallogr 66:125–132. http://dx.doi.org/10.1107/S0907444909047337.
  • Collaborative Computational Project Number 4. 1994. The CCP4 suite: programs for protein crystallography. Acta Crystallogr D 50:760–763. http://dx.doi.org/10.1107/S0907444994003112.
  • Emsley P, Cowtan K. 2004. Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60:2126–2132. http://dx.doi.org/10.1107/S0907444904019158.
  • Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, Headd JJ, Hung LW, Kapral GJ, Grosse-Kunstleve RW, McCoy AJ, Moriarty NW, Oeffner R, Read RJ, Richardson DC, Richardson JS, Terwilliger TC, Zwart PH. 2010. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr D Biol Crystallogr 66:213–221. http://dx.doi.org/10.1107/S0907444909052925.
  • Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, III, Snoeyink J, Richardson JS, Richardson DC. 2007. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35:W375–W383. http://dx.doi.org/10.1093/nar/gkm216.
  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE. 2000. The Protein Data Bank. Nucleic Acids Res 28:235–242. http://dx.doi.org/10.1093/nar/28.1.235.
  • Dolinsky TJ, Czodrowski P, Li H, Nielsen JE, Jensen JH, Klebe G, Baker NA. 2007. PDB2PQR: expanding and upgrading automated preparation of biomolecular structures for molecular simulations. Nucleic Acids Res 35:W522–W525. http://dx.doi.org/10.1093/nar/gkm276.
  • MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, Field MJ, Fischer S, Gao J, Guo H, Ha S, Joseph-McCarthy D, Kuchnir L, Kuczera K, Lau FT, Mattos C, Michnick S, Ngo T, Nguyen DT, Prodhom B, Reiher WE, Roux B, Schlenkrich M, Smith JC, Stote R, Straub J, Watanabe M, Wiorkiewicz-Kuczera J, Yin D, Karplus M. 1998. All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102:3586–3616. http://dx.doi.org/10.1021/jp973084f.
  • Baker NA, Sept D, Joseph S, Holst MJ, McCammon JA. 2001. Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98:10037–10041. http://dx.doi.org/10.1073/pnas.181342398.
  • Honig B, Nicholls A. 1995. Classical electrostatics in biology and chemistry. Science 268:1144–1149. http://dx.doi.org/10.1126/science.7761829.
  • Bond CS. 2003. TopDraw: a sketchpad for protein structure topology cartoons. Bioinformatics 19:311–312. http://dx.doi.org/10.1093/bioinformatics/19.2.311.
  • Rose MD, Winston F, Hieter P. 1990. Methods in yeast genetics: a laboratory course manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  • Li MZ, Elledge SJ. 2007. Harnessing homologous recombination in vitro to generate recombinant DNA via SLIC. Nat Methods 4:251–256. http://dx.doi.org/10.1038/nmeth1010.
  • Funakoshi M, Hochstrasser M. 2009. Small epitope-linker modules for PCR-based C-terminal tagging in Saccharomyces cerevisiae. Yeast 26:185–192. http://dx.doi.org/10.1002/yea.1658.
  • Ivanov D, Kwak YT, Guo J, Gaynor RB. 2000. Domains in the SPT5 protein that modulate its transcriptional regulatory properties. Mol Cell Biol 20:2970–2983. http://dx.doi.org/10.1128/MCB.20.9.2970-2983.2000.
  • Iwabuchi K, Basu BP, Kysela B, Kurihara T, Shibata M, Guan D, Cao Y, Hamada T, Imamura K, Jeggo PA, Date T, Doherty AJ. 2003. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J Biol Chem 278:36487–36495. http://dx.doi.org/10.1074/jbc.M304066200.
  • Charier G, Couprie J, Alpha-Bazin B, Meyer V, Quemeneur E, Guerois R, Callebaut I, Gilquin B, Zinn-Justin S. 2004. The Tudor tandem of 53BP1: a new structural motif involved in DNA and RG-rich peptide binding. Structure 12:1551–1562. http://dx.doi.org/10.1016/j.str.2004.06.014.
  • le Maire A, Schiltz M, Stura EA, Pinon-Lataillade G, Couprie J, Moutiez M, Gondry M, Angulo JF, Zinn-Justin S. 2006. A tandem of SH3-like domains participates in RNA binding in KIN17, a human protein activated in response to genotoxics. J Mol Biol 364:764–776. http://dx.doi.org/10.1016/j.jmb.2006.09.033.
  • Gong W, Wang J, Perrett S, Feng Y. 2014. Retinoblastoma-binding protein 1 has an interdigitated double Tudor domain with DNA binding activity. J Biol Chem 289:4882–4895. http://dx.doi.org/10.1074/jbc.M113.501940.
  • Guo M, Xu F, Yamada J, Egelhofer T, Gao Y, Hartzog GA, Teng M, Niu L. 2008. Core structure of the yeast spt4-spt5 complex: a conserved module for regulation of transcription elongation. Structure 16:1649–1658. http://dx.doi.org/10.1016/j.str.2008.08.013.
  • Basrai MA, Kingsbury J, Koshland D, Spencer F, Hieter P. 1996. Faithful chromosome transmission requires Spt4p, a putative regulator of chromatin structure in Saccharomyces cerevisiae. Mol Cell Biol 16:2838–2847.
  • Zheng J, Benschop JJ, Shales M, Kemmeren P, Greenblatt J, Cagney G, Holstege F, Li H, Krogan NJ. 2010. Epistatic relationships reveal the functional organization of yeast transcription factors. Mol Syst Biol 6:420. http://dx.doi.org/10.1038/msb.2010.77.
  • Westover KD, Bushnell DA, Kornberg RD. 2004. Structural basis of transcription: separation of RNA from DNA by RNA polymerase II. Science 303:1014–1016. http://dx.doi.org/10.1126/science.1090839.
  • Missra A, Gilmour DS. 2010. Interactions between DSIF (DRB sensitivity inducing factor), NELF (negative elongation factor), and the Drosophila RNA polymerase II transcription elongation complex. Proc Natl Acad Sci U S A 107:11301–11306. http://dx.doi.org/10.1073/pnas.1000681107.
  • Cheng B, Price DH. 2008. Analysis of factor interactions with RNA polymerase II elongation complexes using a new electrophoretic mobility shift assay. Nucleic Acids Res 36:e135. http://dx.doi.org/10.1093/nar/gkn630.
  • Yakhnin AV, Yakhnin H, Babitzke P. 2008. Function of the Bacillus subtilis transcription elongation factor NusG in hairpin-dependent RNA polymerase pausing in the trp leader. Proc Natl Acad Sci U S A 105:16131–16136. http://dx.doi.org/10.1073/pnas.0808842105.
  • Yakhnin AV, Babitzke P. 2014. NusG/Spt5: are there common functions of this ubiquitous transcription elongation factor? Curr Opin Microbiol 18:68–71. http://dx.doi.org/10.1016/j.mib.2014.02.005.
  • Belogurov GA, Sevostyanova A, Svetlov V, Artsimovitch I. 2010. Functional regions of the N-terminal domain of the antiterminator RfaH. Mol Microbiol 76:286–301. http://dx.doi.org/10.1111/j.1365-2958.2010.07056.x.
  • Artsimovitch I, Landick R. 2002. The transcriptional regulator RfaH stimulates RNA chain synthesis after recruitment to elongation complexes by the exposed nontemplate DNA strand. Cell 109:193–203. http://dx.doi.org/10.1016/S0092-8674(02)00724-9.
  • Cui Y, Denis CL. 2003. In vivo evidence that defects in the transcriptional elongation factors RPB2, TFIIS, and SPT5 enhance upstream poly(A) site utilization. Mol Cell Biol 23:7887–7901. http://dx.doi.org/10.1128/MCB.23.21.7887-7901.2003.
  • Kaplan CD, Holland MJ, Winston F. 2005. Interaction between transcription elongation factors and mRNA 3′-end formation at the Saccharomyces cerevisiae GAL10-GAL7 locus. J Biol Chem 280:913–922. http://dx.doi.org/10.1074/jbc.M411108200.
  • Mayer A, Schreieck A, Lidschreiber M, Leike K, Martin DE, Cramer P. 2012. The spt5 C-terminal region recruits yeast 3′ RNA cleavage factor I. Mol Cell Biol 32:1321–1331. http://dx.doi.org/10.1128/MCB.06310-11.
  • Kireeva ML, Komissarova N, Kashlev M. 2000. Overextended RNA:DNA hybrid as a negative regulator of RNA polymerase II processivity. J Mol Biol 299:325–335. http://dx.doi.org/10.1006/jmbi.2000.3755.
  • Huertas P, Aguilera A. 2003. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol Cell 12:711–721. http://dx.doi.org/10.1016/j.molcel.2003.08.010.

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