Skip to main content
SpringerLink
Log in

RNA Polymerases and Transcription Factors of Trypanosomes

  • Chapter
  • First Online:
Book cover RNA Metabolism in Trypanosomes

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 28))

Abstract

RNA synthesis in trypanosomatid organisms deviates substantially from what we see in model organisms. In these parasites, protein-coding genes are arranged in long tandem arrays that are polycistronically transcribed by an unresolved mode of transcription initiation. Moreover, the African Trypanosoma brucei has evolved a multifunctional RNA polymerase I system which it employs for pre-rRNA synthesis as well as for transcription of specific gene units encoding its major cell surface antigens. Additionally, the trypanosomatid RNA polymerase III system, by relying mostly on bidirectional tRNA gene promoters, exhibits clear differences to other eukaryotic systems. Interestingly, annotation of completed trypanosomatid genomes revealed only a small subset of basal transcription factors (BTFs), which suggested that trypanosomes have a simplified transcription machinery. Recent research, however, has demonstrated that trypanosomes possess extremely divergent orthologs of most BTFs and that these factors deviate in many aspects from their human counterparts; they are the focus of this chapter.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aeby E, Ullu E, Yepiskoposyan H, Schimanski B, Roditi I, Mühlemann O, Schneider A (2010) tRNASec is transcribed by RNA polymerase II in Trypanosoma brucei but not in humans. Nucleic Acids Res 38:5833–5843

    PubMed  CAS  Google Scholar 

  • Aksoy S, Lalor TM, Martin J, Van der Ploeg LH, Richards FF (1987) Multiple copies of a retroposon interrupt spliced leader RNA genes in the African trypanosome, Trypanosoma gambiense. EMBO J 6:3819–3826

    PubMed  CAS  Google Scholar 

  • Alsford S, Kawahara T, Isamah C, Horn D (2007) A sirtuin in the African trypanosome is involved in both DNA repair and telomeric gene silencing but is not required for antigenic variation. Mol Microbiol 63:724–736

    PubMed  CAS  Google Scholar 

  • Baek HJ, Kang YK, Roeder RG (2006) Human mediator enhances basal transcription by facilitating recruitment of transcription factor IIB during preinitiation complex assembly. J Biol Chem 281:15172–15181

    PubMed  CAS  Google Scholar 

  • Belotserkovskaya R, Reinberg D (2004) Facts about FACT and transcript elongation through chromatin. Curr Opin Genet Dev 14:139–146

    PubMed  CAS  Google Scholar 

  • Belotserkovskaya R, Oh S, Bondarenko VA, Orphanides G, Studitsky VM, Reinberg D (2003) FACT facilitates transcription-dependent nucleosome alteration. Science 301:1090–1093

    PubMed  CAS  Google Scholar 

  • Ben Amar MF, Jefferies D, Pays A, Bakalara N, Kendall G, Pays E (1991) The actin gene promoter of Trypanosoma brucei. Nucleic Acids Res 19:5857–5862

    PubMed  CAS  Google Scholar 

  • Bentley DL (2005) Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol 17:251–256

    PubMed  CAS  Google Scholar 

  • Berriman M, Ghedin E, Hertz-Fowler C, Blandin G, Renauld H, Bartholomeu DC, Lennard NJ, Caler E, Hamlin NE, Haas B, Böhme U, Hannick L, Aslett MA, Shallom J, Marcello L, Hou L, Wickstead B, Alsmark UC, Arrowsmith C, Atkin RJ, Barron AJ, Bringaud F, Brooks K, Carrington M, Cherevach I, Chillingworth TJ, Churcher C, Clark LN, Corton CH, Cronin A, Davies RM, Doggett J, Djikeng A, Feldblyum T, Field MC, Fraser A, Goodhead I, Hance Z, Harper D, Harris BR, Hauser H, Hostetler J, Ivens A, Jagels K, Johnson D, Johnson J, Jones K, Kerhornou AX, Koo H, Larke N, Landfear S, Larkin C, Leech V, Line A, Lord A, MacLeod A, Mooney PJ, Moule S, Martin DM, Morgan GW, Mungall K, Norbertczak H, Ormond D, Pai G, Peacock CS, Peterson J, Quail MA, Rabbinowitsch E, Rajandream MA, Reitter C, Salzberg SL, Sanders M, Schobel S, Sharp S, Simmonds M, Simpson AJ, Tallon L, Turner CM, Tait A, Tivey AR, Van Aken S, Walker D, Wanless D, Wang S, White B, White O, Whitehead S, Woodward J, Wortman J, Adams MD, Embley TM, Gull K, Ullu E, Barry JD, Fairlamb AH, Opperdoes F, Barrell BG, Donelson JE, Hall N, Fraser CM, Melville SE, El Sayed NM (2005) The genome of the African Trypanosome Trypanosoma brucei. Science 309:416–422

    PubMed  CAS  Google Scholar 

  • Biebinger S, Rettenmaier S, Flaspohler J, Hartmann C, Pena Diaz J, Wirtz LE, Hotz HR, Barry JD, Clayton C (1996) The PARP promoter of Trypanosoma brucei is developmentally regulated in a chromosomal context. Nucleic Acids Res 24:1202–1211

    PubMed  CAS  Google Scholar 

  • Brandenburg J, Schimanski B, Nogoceke E, Nguyen TN, Padovan JC, Chait BT, Cross GA, Günzl A (2007) Multifunctional class I transcription in Trypanosoma brucei depends on a novel protein complex. EMBO J 26:4856–4866

    PubMed  CAS  Google Scholar 

  • Brown SD, Huang J, Van der Ploeg LH (1992) The promoter for the procyclic acidic repetitive protein (PARP) genes of Trypanosoma brucei shares features with RNA polymerase I promoters. Mol Cell Biol 12:2644–2652

    PubMed  CAS  Google Scholar 

  • Buratowski S (2009) Progression through the RNA polymerase II CTD cycle. Mol Cell 36:541–546

    PubMed  CAS  Google Scholar 

  • Bushnell DA, Westover KD, Davis RE, Kornberg RD (2004) Structural basis of transcription: an RNA polymerase II-TFIIB cocrystal at 4.5 Angstroms. Science 303:983–988

    PubMed  CAS  Google Scholar 

  • Cai G, Imasaki T, Yamada K, Cardelli F, Takagi Y, Asturias FJ (2010) Mediator head module structure and functional interactions. Nat Struct Mol Biol 17:273–279

    PubMed  CAS  Google Scholar 

  • Carninci P, Sandelin A, Lenhard B, Katayama S, Shimokawa K, Ponjavic J, Semple CA, Taylor MS, Engström PG, Frith MC, Forrest AR, Alkema WB, Tan SL, Plessy C, Kodzius R, Ravasi T, Kasukawa T, Fukuda S, Kanamori-Katayama M, Kitazume Y, Kawaji H, Kai C, Nakamura M, Konno H, Nakano K, Mottagui-Tabar S, Arner P, Chesi A, Gustincich S, Persichetti F, Suzuki H, Grimmond SM, Wells CA, Orlando V, Wahlestedt C, Liu ET, Harbers M, Kawai J, Bajic VB, Hume DA, Hayashizaki Y (2006) Genome-wide analysis of mammalian promoter architecture and evolution. Nat Genet 38:626–635

    PubMed  CAS  Google Scholar 

  • Carrington M, Roditi I, Williams RO (1987) The structure and transcription of an element interspersed between tandem arrays of mini-exon donor RNA genes in Trypanosoma brucei. Nucleic Acids Res 15:10179–10198

    PubMed  CAS  Google Scholar 

  • Chapman AB, Agabian N (1994) Trypanosoma brucei RNA polymerase II is phosphorylated in the absence of carboxyl-terminal domain heptapeptide repeats. J Biol Chem 269:4754–4760

    PubMed  CAS  Google Scholar 

  • Das A, Bellofatto V (2003) RNA polymerase II-dependent transcription in trypanosomes is associated with a SNAP complex-like transcription factor. Proc Natl Acad Sci USA 100:80–85

    PubMed  CAS  Google Scholar 

  • Das A, Bellofatto V (2009) The non-canonical CTD of RNAP-II is essential for productive RNA synthesis in Trypanosoma brucei. PLoS One 4:e6959

    PubMed  Google Scholar 

  • Das A, Zhang Q, Palenchar JB, Chatterjee B, Cross GA, Bellofatto V (2005) Trypanosomal TBP functions with the multisubunit transcription factor tSNAP to direct spliced-leader RNA gene expression. Mol Cell Biol 25:7314–7322

    PubMed  CAS  Google Scholar 

  • Das A, Li H, Liu T, Bellofatto V (2006) Biochemical characterization of Trypanosoma brucei RNA polymerase II. Mol Biochem Parasitol 150:201–210

    PubMed  CAS  Google Scholar 

  • de Lange T, Liu AY, Van der Ploeg LH, Borst P, Tromp MC, Van Boom JH (1983) Tandem repetition of the 5′ mini-exon of variant surface glycoprotein genes: a multiple promoter for VSG gene transcription? Cell 34:891–900

    PubMed  Google Scholar 

  • Denninger V, Fullbrook A, Bessat M, Ersfeld K, Rudenko G (2010) The FACT subunit TbSpt16 is involved in cell cycle specific control of VSG expression sites in Trypanosoma brucei. Mol Microbiol 78:459–474

    PubMed  CAS  Google Scholar 

  • Devaux S, Lecordier L, Uzureau P, Walgraffe D, Dierick JF, Poelvoorde P, Pays E, Vanhamme L (2006) Characterization of RNA polymerase II subunits of Trypanosoma brucei. Mol Biochem Parasitol 148:60–68

    PubMed  CAS  Google Scholar 

  • Djikeng A, Ferreira L, D'Angelo M, Dolezal P, Lamb T, Murta S, Triggs V, Ulbert S, Villarino A, Renzi S, Ullu E, Tschudi C (2001) Characterization of a candidate Trypanosoma brucei U1 small nuclear RNA gene. Mol Biochem Parasitol 113:109–115

    PubMed  CAS  Google Scholar 

  • Donelson JE (2003) Antigenic variation and the African trypanosome genome. Acta Trop 85:391–404

    PubMed  CAS  Google Scholar 

  • Dunbar DA, Chen AA, Wormsley S, Baserga SJ (2000) The genes for small nucleolar RNAs in Trypanosoma brucei are organized in clusters and are transcribed as a polycistronic RNA. Nucleic Acids Res 28:2855–2861

    PubMed  CAS  Google Scholar 

  • Ehlers B, Czichos J, Overath P (1987) RNA turnover in Trypanosoma brucei. Mol Cell Biol 7:1242–1249

    PubMed  CAS  Google Scholar 

  • El Sayed NM, Myler PJ, Bartholomeu DC, Nilsson D, Aggarwal G, Tran AN, Ghedin E, Worthey EA, Delcher AL, Blandin G, Westenberger SJ, Caler E, Cerqueira GC, Branche C, Haas B, Anupama A, Arner E, Aslund L, Attipoe P, Bontempi E, Bringaud F, Burton P, Cadag E, Campbell DA, Carrington M, Crabtree J, Darban H, da Silveira JF, de Jong P, Edwards K, Englund PT, Fazelina G, Feldblyum T, Ferella M, Frasch AC, Gull K, Horn D, Hou L, Huang Y, Kindlund E, Klingbeil M, Kluge S, Koo H, Lacerda D, Levin MJ, Lorenzi H, Louie T, Machado CR, McCulloch R, McKenna A, Mizuno Y, Mottram JC, Nelson S, Ochaya S, Osoegawa K, Pai G, Parsons M, Pentony M, Pettersson U, Pop M, Ramirez JL, Rinta J, Robertson L, Salzberg SL, Sanchez DO, Seyler A, Sharma R, Shetty J, Simpson AJ, Sisk E, Tammi MT, Tarleton R, Teixeira S, Van Aken S, Vogt C, Ward PN, Wickstead B, Wortman J, White O, Fraser CM, Stuart KD, Andersson B (2005) The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409–415

    PubMed  CAS  Google Scholar 

  • Esnault C, Ghavi-Helm Y, Brun S, Soutourina J, Van Berkum N, Boschiero C, Holstege F, Werner M (2008) Mediator-dependent recruitment of TFIIH modules in preinitiation complex. Mol Cell 31:337–346

    PubMed  CAS  Google Scholar 

  • Evers R, Hammer A, Köck J, Jess W, Borst P, Memet S, Cornelissen AW (1989) Trypanosoma brucei contains two RNA polymerase II largest subunit genes with an altered C-terminal domain [published erratum appears in Cell 58:419]. Cell 56:585–597

    PubMed  CAS  Google Scholar 

  • Fantoni A, Dare AO, Tschudi C (1994) RNA polymerase III-mediated transcription of the trypanosome U2 small nuclear RNA gene is controlled by both intragenic and extragenic regulatory elements. Mol Cell Biol 14:2021–2028

    PubMed  CAS  Google Scholar 

  • Figueiredo LM, Cross GA (2010) Nucleosomes are depleted at the VSG expression site transcribed by RNA polymerase I in African trypanosomes. Eukaryot Cell 9:148–154

    PubMed  CAS  Google Scholar 

  • Figueiredo LM, Janzen CJ, Cross GA (2008) A histone methyltransferase modulates antigenic variation in African trypanosomes. PLoS Biol 6:e161

    PubMed  Google Scholar 

  • Gilinger G, Bellofatto V (2001) Trypanosome spliced leader RNA genes contain the first identified RNA polymerase II gene promoter in these organisms. Nucleic Acids Res 29:1556–1564

    PubMed  CAS  Google Scholar 

  • Gilinger G, Luo H, Bellofatto V (2004) In vivo transcription analysis utilizing chromatin immunoprecipitation reveals a role for trypanosome transcription factor PBP-1 in RNA polymerase III-dependent transcription. Mol Biochem Parasitol 134:169–173

    PubMed  CAS  Google Scholar 

  • Ginger ML, Blundell PA, Lewis AM, Browitt A, Günzl A, Barry JD (2002) Ex vivo and in vitro identification of a consensus promoter for VSG genes expressed by metacyclic-stage trypanosomes in the tsetse fly. Eukaryot Cell 1:1000–1009

    PubMed  CAS  Google Scholar 

  • Goldshmidt H, Matas D, Kabi A, Carmi S, Hope R, Michaeli S (2010) Persistent ER stress induces the spliced leader RNA silencing pathway (SLS), leading to programmed cell death in Trypanosoma brucei. PLoS Pathog 6:e1000731

    PubMed  Google Scholar 

  • Grummt I, Skinner JA (1985) Efficient transcription of a protein-coding gene from the RNA polymerase I promoter in transfected cells. Proc Natl Acad Sci USA 82:722–726

    PubMed  CAS  Google Scholar 

  • Günzl A (2003) Transcription. In: Marr JJ, Nielsen TW, Komuniecki RW (eds) Molecular medical parasitology. Academic Press, London, pp 47–65

    Google Scholar 

  • Günzl A (2010) The pre-mRNA splicing machinery of trypanosomes: complex or simplified? Eukaryot Cell 9:1159–1170

    PubMed  Google Scholar 

  • Günzl A, Schimanski B (2009) Tandem affinity purification of proteins. Curr Protoc Protein Sci Chapter 19:Unit 19.19

    Google Scholar 

  • Günzl A, Ullu E, Dörner M, Fragoso SP, Hoffmann KF, Milner JD, Morita Y, Nguu EK, Vanacova S, Wünsch S, Dare AO, Kwon H, Tschudi C (1997) Transcription of the Trypanosoma brucei spliced leader RNA gene is dependent only on the presence of upstream regulatory elements. Mol Biochem Parasitol 85:67–76

    PubMed  Google Scholar 

  • Günzl A, Bruderer T, Laufer G, Schimanski B, Tu LC, Chung HM, Lee PT, Lee MG (2003) RNA polymerase I transcribes procyclin genes and variant surface glycoprotein gene expression sites in Trypanosoma brucei. Eukaryot Cell 2:542–551

    PubMed  Google Scholar 

  • Günzl A, Vanhamme L, Myler PJ (2007) Transcription in trypanosomes: a different means to the end. In: Barry JD, Mottram JC, McCulloch R, Acosta-Serrano A (eds) Trypanosomes—after the genome. Horizon Press, Pittsburgh, pp 177–208

    Google Scholar 

  • Guo Z, Stiller JW (2004) Comparative genomics of cyclin-dependent kinases suggest co-evolution of the RNAP II C-terminal domain and CTD-directed CDKs. BMC Genomics 5:69

    PubMed  Google Scholar 

  • Hartree D, Bellofatto V (1995) Essential components of the mini-exon gene promoter in the trypanosomatid Leptomonas seymouri. Mol Biochem Parasitol 71:27–39

    PubMed  CAS  Google Scholar 

  • Henry RW, Sadowski CL, Kobayashi R, Hernandez N (1995) A TBP-TAF complex required for transcription of human snRNA genes by RNA polymerases II and III. Nature 374:653–656

    PubMed  CAS  Google Scholar 

  • Hernandez N (2001) Small nuclear RNA genes: a model system to study fundamental mechanisms of transcription. J Biol Chem 276:26733–26736

    PubMed  CAS  Google Scholar 

  • Hertz-Fowler C, Figueiredo LM, Quail MA, Becker M, Jackson A, Bason N, Brooks K, Churcher C, Fahkro S, Goodhead I, Heath P, Kartvelishvili M, Mungall K, Harris D, Hauser H, Sanders M, Saunders D, Seeger K, Sharp S, Taylor JE, Walker D, White B, Young R, Cross GA, Rudenko G, Barry JD, Louis EJ, Berriman M (2008) Telomeric expression sites are highly conserved in Trypanosoma brucei. PLoS One 3:e3527

    PubMed  Google Scholar 

  • Hughes K, Wand M, Foulston L, Young R, Harley K, Terry S, Ersfeld K, Rudenko G (2007) A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO J 26:2400–2410

    PubMed  CAS  Google Scholar 

  • Ibrahim BS, Kanneganti N, Rieckhof GE, Das A, Laurents DV, Palenchar JB, Bellofatto V, Wah DA (2009) Structure of the C-terminal domain of transcription factor IIB from Trypanosoma brucei. Proc Natl Acad Sci USA 106:13242–13247

    PubMed  CAS  Google Scholar 

  • Ivens AC, Peacock CS, Worthey EA, Murphy L, Aggarwal G, Berriman M, Sisk E, Rajandream MA, Adlem E, Aert R, Anupama A, Apostolou Z, Attipoe P, Bason N, Bauser C, Beck A, Beverley SM, Bianchettin G, Borzym K, Bothe G, Bruschi CV, Collins M, Cadag E, Ciarloni L, Clayton C, Coulson RM, Cronin A, Cruz AK, Davies RM, De Gaudenzi J, Dobson DE, Duesterhoeft A, Fazelina G, Fosker N, Frasch AC, Fraser A, Fuchs M, Gabel C, Goble A, Goffeau A, Harris D, Hertz-Fowler C, Hilbert H, Horn D, Huang Y, Klages S, Knights A, Kube M, Larke N, Litvin L, Lord A, Louie T, Marra M, Masuy D, Matthews K, Michaeli S, Mottram JC, Müller-Auer S, Munden H, Nelson S, Norbertczak H, Oliver K, O'neil S, Pentony M, Pohl TM, Price C, Purnelle B, Quail MA, Rabbinowitsch E, Reinhardt R, Rieger M, Rinta J, Robben J, Robertson L, Ruiz JC, Rutter S, Saunders D, Schäfer M, Schein J, Schwartz DC, Seeger K, Seyler A, Sharp S, Shin H, Sivam D, Squares R, Squares S, Tosato V, Vogt C, Volckaert G, Wambutt R, Warren T, Wedler H, Woodward J, Zhou S, Zimmermann W, Smith DF, Blackwell JM, Stuart KD, Barrell B, Myler PJ (2005) The genome of the kinetoplastid parasite, Leishmania major. Science 309:436–442

    PubMed  Google Scholar 

  • Janz L, Clayton C (1994) The PARP and rRNA promoters of Trypanosoma brucei are composed of dissimilar sequence elements that are functionally interchangeable. Mol Cell Biol 14:5804–5811

    PubMed  CAS  Google Scholar 

  • Jawhari A, Uhring M, De Carlo S, Crucifix C, Tocchini-Valentini G, Moras D, Schultz P, Poterszman A (2006) Structure and oligomeric state of human transcription factor TFIIE. EMBO Rep 7:500–505

    PubMed  CAS  Google Scholar 

  • Jess W, Hammer A, Cornelissen AW (1989) Complete sequence of the gene encoding the largest subunit of RNA polymerase I of Trypanosoma brucei. FEBS Lett 249:123–128

    PubMed  CAS  Google Scholar 

  • Kaiser FJ, Tavassoli K, Van den Bemd GJ, Chang GT, Horsthemke B, Moroy T, Lüdecke HJ (2003) Nuclear interaction of the dynein light chain LC8a with the TRPS1 transcription factor suppresses the transcriptional repression activity of TRPS1. Hum Mol Genet 12:1349–1358

    PubMed  CAS  Google Scholar 

  • Kawahara T, Siegel TN, Ingram AK, Alsford S, Cross GA, Horn D (2008) Two essential MYST-family proteins display distinct roles in histone H4K10 acetylation and telomeric silencing in trypanosomes. Mol Microbiol 69:1054–1068

    PubMed  CAS  Google Scholar 

  • Kelly S, Wickstead B, Gull K (2005) An in silico analysis of trypanosomatid RNA polymerases: insights into their unusual transcription. Biochem Soc Trans 33:1435–1437

    PubMed  CAS  Google Scholar 

  • Köck J, Evers R, Cornelissen AW (1988) Structure and sequence of the gene for the largest subunit of trypanosomal RNA polymerase III. Nucleic Acids Res 16:8753–8772

    PubMed  Google Scholar 

  • Kolev NG, Franklin JB, Carmi S, Shi H, Michaeli S, Tschudi C (2010) The transcriptome of the human pathogen Trypanosoma brucei at single-nucleotide resolution. PLoS Pathog 6:e1001090

    PubMed  Google Scholar 

  • Kooter JM, Borst P (1984) Alpha-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes. Nucleic Acids Res 12:9457–9472

    PubMed  CAS  Google Scholar 

  • Kuhlman TC, Cho H, Reinberg D, Hernandez N (1999) The general transcription factors IIA, IIB, IIF, and IIE are required for RNA polymerase II transcription from the human U1 small nuclear RNA promoter. Mol Cell Biol 19:2130–2141

    PubMed  CAS  Google Scholar 

  • Laufer G, Günzl A (2001) In-vitro competition analysis of procyclin gene and variant surface glycoprotein gene expression site transcription in Trypanosoma brucei. Mol Biochem Parasitol 113:55–65

    PubMed  CAS  Google Scholar 

  • Lecordier L, Devaux S, Uzureau P, Dierick JF, Walgraffe D, Poelvoorde P, Pays E, Vanhamme L (2007) Characterization of a TFIIH homologue from Trypanosoma brucei. Mol Microbiol 64:1164–1181

    PubMed  CAS  Google Scholar 

  • Lee MG (1996) An RNA polymerase II promoter in the hsp70 locus of Trypanosoma brucei. Mol Cell Biol 16:1220–1230

    PubMed  CAS  Google Scholar 

  • Lee JH, Nguyen TN, Schimanski B, Günzl A (2007) Spliced leader RNA gene transcription in Trypanosoma brucei requires transcription factor TFIIH. Eukaryot Cell 6:641–649

    PubMed  CAS  Google Scholar 

  • Lee JH, Jung HS, Günzl A (2009) Transcriptionally active TFIIH of the early-diverged eukaryote Trypanosoma brucei harbors two novel core subunits but not a cyclin-activating kinase complex. Nucleic Acids Res 37:3811–3820

    PubMed  CAS  Google Scholar 

  • Lee JH, Cai G, Panigrahi AK, Dunham-Ems S, Nguyen TN, Radolf JD, Asturias FJ, Günzl A (2010) A TFIIH-associated mediator head is a basal factor of small nuclear spliced leader RNA gene transcription in early-diverged trypanosomes. Mol Cell Biol 30:5502–5513

    PubMed  CAS  Google Scholar 

  • Li C, Harding GA, Parise J, McNamara-Schroeder KJ, Stumph WE (2004) Architectural arrangement of cloned proximal sequence element-binding protein subunits on Drosophila U1 and U6 snRNA gene promoters. Mol Cell Biol 24:1897–1906

    PubMed  CAS  Google Scholar 

  • Liang XH, Uliel S, Hury A, Barth S, Doniger T, Unger R, Michaeli S (2005) A genome-wide analysis of C/D and H/ACA-like small nucleolar RNAs in Trypanosoma brucei reveals a trypanosome-specific pattern of rRNA modification. RNA 11:619–645

    PubMed  CAS  Google Scholar 

  • Luo H, Gilinger G, Mukherjee D, Bellofatto V (1999) Transcription initiation at the TATA-less spliced leader RNA gene promoter requires at least two DNA-binding proteins and a tripartite architecture that includes an initiator element. J Biol Chem 274:31947–31954

    PubMed  CAS  Google Scholar 

  • Lustig Y, Sheiner L, Vagima Y, Goldshmidt H, Das A, Bellofatto V, Michaeli S (2007) Spliced-leader RNA silencing: a novel stress-induced mechanism in Trypanosoma brucei. EMBO Rep 8:408–413

    PubMed  CAS  Google Scholar 

  • Malik S, Roeder RG (2010) The metazoan mediator co-activator complex as an integrative hub for transcriptional regulation. Nat Rev Genet 11:761–772

    PubMed  CAS  Google Scholar 

  • Marchetti MA, Tschudi C, Silva E, Ullu E (1998) Physical and transcriptional analysis of the Trypanosoma brucei genome reveals a typical eukaryotic arrangement with close interspersionof RNA polymerase II- and III-transcribed genes. Nucleic Acids Res 26:3591–3598

    PubMed  CAS  Google Scholar 

  • Martinez-Calvillo S, Yan S, Nguyen D, Fox M, Stuart K, Myler PJ (2003) Transcription of Leishmania major Friedlin chromosome 1 initiates in both directions within a single region. Mol Cell 11:1291–1299

    PubMed  CAS  Google Scholar 

  • Martinez-Calvillo S, Nguyen D, Stuart K, Myler PJ (2004) Transcription initiation and termination on Leishmania major chromosome 3. Eukaryot Cell 3:506–517

    PubMed  CAS  Google Scholar 

  • Martinez-Calvillo S, Saxena A, Green A, Leland A, Myler PJ (2007) Characterization of the RNA polymerase II and III complexes in Leishmania major. Int J Parasitol 37:491–502

    PubMed  CAS  Google Scholar 

  • Martinez-Calvillo S, Vizuet-de-Rueda JC, Florencio-Martinez LE, Manning-Cela RG, Figueroa-Angulo EE (2010) Gene expression in trypanosomatid parasites. J Biomed Biotechnol 2010:525241

    PubMed  Google Scholar 

  • Maxon ME, Goodrich JA, Tjian R (1994) Transcription factor IIE binds preferentially to RNA polymerase IIa and recruits TFIIH: a model for promoter clearance. Genes Dev 8:515–524

    PubMed  CAS  Google Scholar 

  • McAndrew M, Graham S, Hartmann C, Clayton C (1998) Testing promoter activity in the trypanosome genome: isolation of a metacyclic-type VSG promoter, and unexpected insights into RNA polymerase II transcription. Exp Parasitol 90:65–76

    PubMed  CAS  Google Scholar 

  • McConville MJ, Ferguson MA (1993) The structure, biosynthesis and function of glycosylated phosphatidylinositols in the parasitic protozoa and higher eukaryotes. Biochem J 294:305–324

    PubMed  CAS  Google Scholar 

  • Mottram JC, Bell SD, Nelson RG, Barry JD (1991) tRNAs of Trypanosoma brucei. Unusual gene organization and mitochondrial importation. J Biol Chem 266:18313–18317

    PubMed  CAS  Google Scholar 

  • Nakaar V, Dare AO, Hong D, Ullu E, Tschudi C (1994) Upstream tRNA genes are essential for expression of small nuclear and cytoplasmic RNA genes in trypanosomes. Mol Cell Biol 14:6736–6742

    PubMed  CAS  Google Scholar 

  • Nakaar V, Tschudi C, Ullu E (1995) An unusual liaison: small nuclear and cytoplasmic RNA genes team up with tRNA genes in trypanosomatid protozoa. Parasitol Today 11:225–228

    CAS  Google Scholar 

  • Nakaar V, Günzl A, Ullu E, Tschudi C (1997) Structure of the Trypanosoma brucei U6 snRNA gene promoter. Mol Biochem Parasitol 88:13–23

    PubMed  CAS  Google Scholar 

  • Navarro M, Gull K (2001) A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414:759–763

    PubMed  CAS  Google Scholar 

  • Nelson RG, Parsons M, Barr PJ, Stuart K, Selkirk M, Agabian N (1983) Sequences homologous to the variant antigen mRNA spliced leader are located in tandem repeats and variable orphons in Trypanosoma brucei. Cell 34:901–909

    PubMed  CAS  Google Scholar 

  • Nett IR, Martin DM, Miranda-Saavedra D, Lamont D, Barber JD, Mehlert A, Ferguson MA (2009) The phosphoproteome of bloodstream form Trypanosoma brucei, causative agent of African sleeping sickness. Mol Cell Proteomics 8:1527–1538

    PubMed  CAS  Google Scholar 

  • Nguyen TN, Schimanski B, Zahn A, Klumpp B, Günzl A (2006) Purification of an eight subunit RNA polymerase I complex in Trypanosoma brucei. Mol Biochem Parasitol 149:27–37

    PubMed  CAS  Google Scholar 

  • Nguyen TN, Schimanski B, Günzl A (2007) Active RNA polymerase I of Trypanosoma brucei harbors a novel subunit essential for transcription. Mol Cell Biol 27:6254–6263

    PubMed  CAS  Google Scholar 

  • Nikolov DB, Chen H, Halay ED, Usheva AA, Hisatake K, Lee DK, Roeder RG, Burley SK (1995) Crystal structure of a TFIIB-TBP-TATA-element ternary complex. Nature 377:119–128

    PubMed  CAS  Google Scholar 

  • Nunes LR, Carvalho MR, Shakarian AM, Buck GA (1997) The transcription promoter of the spliced leader gene from Trypanosoma cruzi. Gene 188:157–168

    PubMed  CAS  Google Scholar 

  • Orphanides G, Wu WH, Lane WS, Hampsey M, Reinberg D (1999) The chromatin-specific transcription elongation factor FACT comprises human SPT16 and SSRP1 proteins. Nature 400:284–288

    PubMed  CAS  Google Scholar 

  • Palenchar JB, Bellofatto V (2006) Gene transcription in trypanosomes. Mol Biochem Parasitol 146:135–141

    PubMed  CAS  Google Scholar 

  • Palenchar JB, Liu W, Palenchar PM, Bellofatto V (2006) A divergent transcription factor TFIIB in trypanosomes is required for RNA polymerase II-dependent spliced leader RNA transcription and cell viability. Eukaryot Cell 5:293–300

    PubMed  CAS  Google Scholar 

  • Park S, Nguyen TN, Kirkham JK, Lee J, Günzl A (2011) Transcription by the multifunctional RNA polymerase I in Trypanosoma brucei functions independently of RPB7. Mol Biochem Parasitol 180:35–42

    PubMed  CAS  Google Scholar 

  • Park S, Nguyen TN, Günzl A (2012) Development of an efficient in vitro transcription system for bloodstream form Trypanosoma brucei reveals life cycle-independent functionality of class I transcription factor A. Mol Biochem Parasitol 181:29–36

    PubMed  CAS  Google Scholar 

  • Parsons M, Worthey EA, Ward PN, Mottram JC (2005) Comparative analysis of the kinomes of three pathogenic trypanosomatids: Leishmania major, Trypanosoma brucei and Trypanosoma cruzi. BMC Genomics 6:127

    PubMed  Google Scholar 

  • Patrick KL, Luz PM, Ruan JP, Shi H, Ullu E, Tschudi C (2008) Genomic rearrangements and transcriptional analysis of the spliced leader-associated retrotransposon in RNA interference-deficient Trypanosoma brucei. Mol Microbiol 67:435–447

    PubMed  CAS  Google Scholar 

  • Penate X, Lopez-Farfan D, Landeira D, Wentland A, Vidal I, Navarro M (2009) RNA pol II subunit RPB7 is required for RNA pol I-mediated transcription in Trypanosoma brucei. EMBO Rep 10:252–257

    PubMed  CAS  Google Scholar 

  • Pham VP, Qi CC, Gottesdiener KM (1996) A detailed mutational analysis of the VSG gene expression site promoter. Mol Biochem Parasitol 75:241–254

    PubMed  CAS  Google Scholar 

  • Respuela P, Ferella M, Rada-Iglesias A, Aslund L (2008) Histone acetylation and methylation at sites initiating divergent polycistronic transcription in Trypanosoma cruzi. J Biol Chem 283:15884–15892

    PubMed  CAS  Google Scholar 

  • Rigaut G, Shevchenko A, Rutz B, Wilm M, Mann M, Seraphin B (1999) A generic protein purification method for protein complex characterization and proteome exploration. Nat Biotechnol 17:1030–1032

    PubMed  CAS  Google Scholar 

  • Roditi I, Clayton C (1999) An unambiguous nomenclature for the major surface glycoproteins of the procyclic form of Trypanosoma brucei. Mol Biochem Parasitol 103:99–100

    PubMed  CAS  Google Scholar 

  • Ruan JP, Arhin GK, Ullu E, Tschudi C (2004) Functional characterization of a Trypanosoma brucei TATA-binding protein-related factor points to a universal regulator of transcription in trypanosomes. Mol Cell Biol 24:9610–9618

    PubMed  CAS  Google Scholar 

  • Rudenko G, Chung HM, Pham VP, Van der Ploeg LH (1991) RNA polymerase I can mediate expression of CAT and neo protein- coding genes in Trypanosoma brucei. EMBO J 10:3387–3397

    PubMed  CAS  Google Scholar 

  • Ruepp S, Furger A, Kurath U, Renggli CK, Hemphill A, Brun R, Roditi I (1997) Survival of Trypanosoma brucei in the tsetse fly is enhanced by the expression of specific forms of procyclin. J Cell Biol 137:1369–1379

    PubMed  CAS  Google Scholar 

  • Schimanski B, Klumpp B, Laufer G, Marhöfer RJ, Selzer PM, Günzl A (2003) The second largest subunit of Trypanosoma brucei’s multifunctional RNA polymerase I has a unique N-terminal extension domain. Mol Biochem Parasitol 126:193–200

    PubMed  CAS  Google Scholar 

  • Schimanski B, Laufer G, Gontcharova L, Günzl A (2004a) The Trypanosoma brucei spliced leader RNA and rRNA gene promoters have interchangeable TbSNAP50-binding elements. Nucleic Acids Res 32:700–709

    PubMed  CAS  Google Scholar 

  • Schimanski B, Ma L, Günzl A (2004b) Failure to detect binding of Trypanosoma brucei SNAPc to U2 and U6 snRNA gene sequences by in vitro transcription competition and pull-down assays. Mol Biochem Parasitol 137:293–296

    PubMed  CAS  Google Scholar 

  • Schimanski B, Nguyen TN, Günzl A (2005a) Characterization of a multisubunit transcription factor complex essential for spliced-leader RNA gene transcription in Trypanosoma brucei. Mol Cell Biol 25:7303–7313

    PubMed  CAS  Google Scholar 

  • Schimanski B, Nguyen TN, Günzl A (2005b) Highly efficient tandem affinity purification of trypanosome protein complexes based on a novel epitope combination. Eukaryot Cell 4:1942–1950

    PubMed  CAS  Google Scholar 

  • Schimanski B, Brandenburg J, Nguyen TN, Caimano MJ, Günzl A (2006) A TFIIB-like protein is indispensable for spliced leader RNA gene transcription in Trypanosoma brucei. Nucleic Acids Res 34:1676–1684

    PubMed  CAS  Google Scholar 

  • Schramm L, Hernandez N (2002) Recruitment of RNA polymerase III to its target promoters. Genes Dev 16:2593–2620

    PubMed  CAS  Google Scholar 

  • Schultz P, Fribourg S, Poterszman A, Mallouh V, Moras D, Egly JM (2000) Molecular structure of human TFIIH. Cell 102:599–607

    PubMed  CAS  Google Scholar 

  • Schwede A, Jones N, Engstler M, Carrington M (2010) The VSG C-terminal domain is inaccessible to antibodies on live trypanosomes. Mol Biochem Parasitol 175:201–204

    PubMed  Google Scholar 

  • Sherman DR, Janz L, Hug M, Clayton C (1991) Anatomy of the PARP gene promoter of Trypanosoma brucei. EMBO J 10:3379–3386

    PubMed  CAS  Google Scholar 

  • Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, Fenyo D, Wang X, Dewell S, Cross GA (2009) Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 23:1063–1076

    PubMed  CAS  Google Scholar 

  • Sikorski TW, Buratowski S (2009) The basal initiation machinery: beyond the general transcription factors. Curr Opin Cell Biol 21:344–351

    PubMed  CAS  Google Scholar 

  • Smith JL, Levin JR, Agabian N (1989a) Molecular characterization of the Trypanosoma brucei RNA polymerase I and III largest subunit genes. J Biol Chem 264:18091–18099

    PubMed  CAS  Google Scholar 

  • Smith JL, Levin JR, Ingles CJ, Agabian N (1989b) In trypanosomes the homolog of the largest subunit of RNA polymerase II is encoded by two genes and has a highly unusual C-terminal domain structure. Cell 56:815–827

    PubMed  CAS  Google Scholar 

  • Stanne TM, Rudenko G (2010) Active VSG expression sites in Trypanosoma brucei are depleted of nucleosomes. Eukaryot Cell 9:136–147

    PubMed  CAS  Google Scholar 

  • Stewart M, Haile S, Jha BA, Cristodero M, Li CH, Clayton C (2010) Processing of a phosphoglycerate kinase reporter mRNA in Trypanosoma brucei is not coupled to transcription by RNA polymerase II. Mol Biochem Parasitol 172:99–106

    PubMed  CAS  Google Scholar 

  • Sturm NR, Yu MC, Campbell DA (1999) Transcription termination and 3′-End processing of the spliced leader RNA in kinetoplastids. Mol Cell Biol 19:1595–1604

    PubMed  CAS  Google Scholar 

  • Takagi Y, Kornberg RD (2006) Mediator as a general transcription factor. J Biol Chem 281:80–89

    PubMed  CAS  Google Scholar 

  • Takagi Y, Calero G, Komori H, Brown JA, Ehrensberger AH, Hudmon A, Asturias F, Kornberg RD (2006) Head module control of mediator interactions. Mol Cell 23:355–364

    PubMed  CAS  Google Scholar 

  • Thomas MC, Chiang CM (2006) The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41:105–178

    PubMed  CAS  Google Scholar 

  • Thomas S, Green A, Sturm NR, Campbell DA, Myler PJ (2009) Histone acetylations mark origins of polycistronic transcription in Leishmania major. BMC Genomics 10:e152

    Google Scholar 

  • Tsai FT, Sigler PB (2000) Structural basis of preinitiation complex assembly on human pol II promoters. EMBO J 19:25–36

    PubMed  CAS  Google Scholar 

  • Uzureau P, Daniels JP, Walgraffe D, Wickstead B, Pays E, Gull K, Vanhamme L (2008) Identification and characterization of two trypanosome TFIIS proteins exhibiting particular domain architectures and differential nuclear localizations. Mol Microbiol 69:1121–1136

    PubMed  CAS  Google Scholar 

  • Vanhamme L, Pays A, Tebabi P, Alexandre S, Pays E (1995) Specific binding of proteins to the noncoding strand of a crucial element of the variant surface glycoprotein, procyclin, and ribosomal promoters of Trypanosoma brucei. Mol Cell Biol 15:5598–5606

    PubMed  CAS  Google Scholar 

  • Vanhamme L, Poelvoorde P, Pays A, Tebabi P, Xong HV, Pays E (2000) Differential RNA elongation controls the variant surface glycoprotein gene expression sites of Trypanosoma brucei. Mol Microbiol 36:328–340

    PubMed  CAS  Google Scholar 

  • Walgraffe D, Devaux S, Lecordier L, Dierick JF, Dieu M, Van Den AJ, Pays E, Vanhamme L (2005) Characterization of subunits of the RNA polymerase I complex in Trypanosoma brucei. Mol Biochem Parasitol 139:249–260

    PubMed  CAS  Google Scholar 

  • Wang QP, Kawahara T, Horn D (2010) Histone deacetylases play distinct roles in telomeric VSG expression site silencing in African trypanosomes. Mol Microbiol 77:1237–1245

    PubMed  CAS  Google Scholar 

  • Werner F (2007) Structure and function of archaeal RNA polymerases. Mol Microbiol 65:1395–1404

    PubMed  CAS  Google Scholar 

  • Wright JR, Siegel TN, Cross GA (2010) Histone H3 trimethylated at lysine 4 is enriched at probable transcription start sites in Trypanosoma brucei. Mol Biochem Parasitol 172:141–144

    PubMed  CAS  Google Scholar 

  • Yang X, Figueiredo LM, Espinal A, Okubo E, Li B (2009) RAP1 is essential for silencing telomeric variant surface glycoprotein genes in Trypanosoma brucei. Cell 137:99–109

    PubMed  CAS  Google Scholar 

  • Yeh TY, Chuang JZ, Sung CH (2005) Dynein light chain rp3 acts as a nuclear matrix-associated transcriptional modulator in a dynein-independent pathway. J Cell Sci 118:3431–3443

    PubMed  CAS  Google Scholar 

  • Yoon JB, Murphy S, Bai L, Wang Z, Roeder RG (1995) Proximal sequence element-binding transcription factor (PTF) is a multisubunit complex required for transcription of both RNA polymerase II- and RNA polymerase III-dependent small nuclear RNA genes. Mol Cell Biol 15:2019–2027

    PubMed  CAS  Google Scholar 

  • Yu MC, Sturm NR, Saito RM, Roberts TG, Campbell DA (1998) Single nucleotide resolution of promoter activity and protein binding for the Leishmania tarentolae spliced leader RNA gene. Mol Biochem Parasitol 94:265–281

    PubMed  CAS  Google Scholar 

  • Ziegelbauer K, Overath P (1993) Organization of two invariant surface glycoproteins in the surface coat of Trypanosoma brucei. Infect Immun 61:4540–4545

    PubMed  CAS  Google Scholar 

  • Zomerdijk JC, Kieft R, Borst P (1991) Efficient production of functional mRNA mediated by RNA polymerase I in Trypanosoma brucei. Nature 353:772–775

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I thank Tu N. Nguyen and Justin K. Kirkham for critical reading of the manuscript. This work was supported by National Institutes of Health grants AI059377 and AI073300 to A.G.

Author information

Authors and Affiliations

  1. Department of Genetics and Developmental Biology, University of Connecticut Health Center, 400 Farmington Avenue, Farmington, CT, 06030, USA

    Arthur Günzl

  2. Department of Molecular, Microbial and Structural Biology, University of Connecticut Health Center, 263 Farmington Avenue, Farmington, CT, 06030, USA

    Arthur Günzl

Authors
  1. Arthur Günzl
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Arthur Günzl .

Editor information

Editors and Affiliations

  1. , Department of Biology and Chemistry, Justus Liebig University of Giessen, Heinrich-Buff-Ring 58, Giessen, 35392, Germany

    Albrecht Bindereif

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag GmbH Berlin Heidelberg

About this chapter

Cite this chapter

Günzl, A. (2012). RNA Polymerases and Transcription Factors of Trypanosomes. In: Bindereif, A. (eds) RNA Metabolism in Trypanosomes. Nucleic Acids and Molecular Biology, vol 28. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-28687-2_1

Download citation

Publish with us

Policies and ethics

Search

Navigation