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RNA Editing Accessory Factors — the Example of mHel61p

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RNA Editing

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 20))

Abstract

The majority of mitochondrial pre-messenger RNAs in kinetoplastid protozoa are substrates of a U nucleotide-specific, insertion/deletion-type RNA editing reaction. The process converts nonfunctional pre-mRNAs into translatable molecules, and can generate protein diversity by alternative editing. A high molecular mass enzyme complex, the editosome, catalyzes the reaction. Editosomes provide a molecular platform for the individual catalytic steps of the reaction cycle. While the molecular composition of the editosome has been studied in detail, dynamic aspects of the reaction have by and large been ignored. Here, we focus on accessory proteins that bind to the editosome only at defined steps of the reaction cycle, thereby modulating the structure and function of the catalytic machinery. As an example, we concentrate on the mitochondrial DExH/D protein mHel61p, a putative RNA helicase and/or RNPase. We summarize the current structural, genetic and biochemical knowledge on mHel61p, and provide an outlook onto dynamic processes of the editing reaction.

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References

  • Allen TE, Heidmann S, Reed R, Myler PJ, Göringer HU, Stuart KD (1998) Association of guide RNA binding protein gBP21 with active RNA editing complexes in Trypanosoma brucei. Mol Cell Biol 18:6014–6022

    PubMed  CAS  Google Scholar 

  • Aphasizhev R, Simpson L (2001) Isolation and characterization of a U-specific 3ʹ–5ʹ–exonuclease from mitochondria of Leishmania tarentolae. J Biol Chem 276:21280–21284

    Article  PubMed  CAS  Google Scholar 

  • Aphasizhev R, Sbicego S, Peris M, Jang SH, Aphasizheva I, Simpson AM, Rivlin A, Simpson L (2002) Trypanosome mitochondrial 3ʹ terminal uridylyl transferase (TUTase): the key enzyme in U-insertion/deletion RNA editing. Cell 108:637–648

    Article  PubMed  CAS  Google Scholar 

  • Aphasizhev R, Aphasizheva I, Nelson RE, Gao G, Simpson AM, Kang X, Falick AM, Sbicego S, Simpson L (2003) Isolation of a U-insertion/deletion editing complex from Leishmania tarentolae mitochondria. EMBO J 22:913–924

    Article  PubMed  CAS  Google Scholar 

  • Babbarwal VK, Fleck M, Ernst NL, Schnaufer A, Stuart K (2007) An essential role of KREPB4 in RNA editing and structural integrity of the editosome in Trypanosoma brucei. RNA 13:737–744

    Article  PubMed  CAS  Google Scholar 

  • Benne R, Van Den Burg J, Brakenhoff JP, Sloof P, Van Boom JH, Tromp MC (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819–826

    Article  PubMed  CAS  Google Scholar 

  • Benz J, Trachsel H, Baumann U (1999) Crystal structure of the ATPase domain of translation initiation factor 4A from Saccharomyces cerevisiae–the prototype of the DEAD box protein family. Structure 15:671–679

    Article  Google Scholar 

  • Blom D, Burg Jv, Breek CK, Speijer D, Muijsers AO, Benne R (2001) Cloning and characterization of two guide RNA-binding proteins from mitochondria of Crithidia fasciculata: gBP27, a novel protein, and gBP29, the orthologue of Trypanosoma brucei gBP21. Nucleic Acids Res 29:2950–2962

    Article  PubMed  CAS  Google Scholar 

  • Blum B, Bakalara N, Simpson L (1990) A model for RNA editing in kinetoplastid mitochondria: “guide” RNA molecules transcribed from maxicircle DNA provide the edited information. Cell 60:189–198

    Article  PubMed  CAS  Google Scholar 

  • Brecht M, Niemann M, Schlüter E, Müller UF, Stuart K, Göringer HU (2005) TbMP42, a protein component of the RNA editing complex in African trypanosomes has endo-exoribonuclease activity. Mol Cell 17:621–630

    Article  PubMed  CAS  Google Scholar 

  • Carmel AB, Matthews BW (2004) Crystal structure of the BstDEAD N-terminal domain: a novel DEAD protein from Bacillus stearothermophilus. RNA 10:66–74

    Article  PubMed  CAS  Google Scholar 

  • Carnes J, Trotter JR, Ernst NL, Steinberg A, Stuart K (2005) An essential RNase III insertion editing endonuclease in Trypanosoma brucei. Proc Natl Acad Sci USA 102:16614–16619

    Article  PubMed  CAS  Google Scholar 

  • Caruthers JM, Johnson ER, McKay DB (2000) Crystal structure of yeast initiation factor 4A, a DEAD-box RNA helicase. Proc Natl Acad Sci USA 97:13080–13085

    Article  PubMed  CAS  Google Scholar 

  • Cheng Z, Coller J, Parker R, Song H (2005) Crystal structure and functional analysis of DEAD-box protein Dhh1p. RNA 11:1258–1270

    Article  PubMed  CAS  Google Scholar 

  • Combet C, Jambon M, Deleage G, Geourjon C (2002) Geno3D: automatic comparative molecular modelling of protein. Bioinformatics 18:213–214

    Article  PubMed  CAS  Google Scholar 

  • Company M, Arenas J, Abelson J (1991) Requirement of the RNA helicase-like protein PRP22 for release of messenger RNA from spliceosomes. Nature 349:487–493

    Article  PubMed  CAS  Google Scholar 

  • Corell RA, Read LK, Riley GR, Nellissery JK, Allen TE, Kable ML, Wachal MD, Seiwert SD, Myler PJ, Stuart KD (1996) Complexes from Trypanosoma brucei that exhibit deletion editing and other editing-associated properties. Mol Cell Biol 16:1410–1418

    PubMed  CAS  Google Scholar 

  • Erickson HP (1993) Gene knockouts of c-src, transforming growth factor , β1, and tenascin suggest superfluous, nonfunctional expression of proteins. J Cell Biol 120:1079–1081

    Article  PubMed  CAS  Google Scholar 

  • Foreman PK, Davis RW, Sachs AB (1991) The Saccharomyces cerevisiae RPB4 gene is tightly linked to the TIF2 gene. Nucleic Acids Res 19:2781

    Article  PubMed  CAS  Google Scholar 

  • Frech GC, Simpson L (1996) Uridine insertion into preedited mRNA by a mitochondrial extract from Leishmania tarentolae: stereochemical evidence for the enzyme cascade model. Mol Cell Biol 16:4584–4589

    PubMed  CAS  Google Scholar 

  • Fuller-Pace FV (1994) RNA helicases: modulators of RNA structure. Trends Cell Biol 4:271–274

    Article  PubMed  CAS  Google Scholar 

  • Gao G, Simpson L (2003) Is the Trypanosoma brucei REL1 RNA ligase specific for U-deletion RNA editing and is the REL2 RNA ligase specific for U-insertion editing? J Biol Chem 278:27570–27574

    Article  PubMed  CAS  Google Scholar 

  • Guex N, Peitsch MC (1997) SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723

    Article  PubMed  CAS  Google Scholar 

  • Hans J, Hajduk Sl, Madison-Antenucci S (2007) RNA-editing-associated protein 1 null mutant reveals link to mitochondrial RNA stability. RNA (in press) DOI 10.1261/rna.486107

    Google Scholar 

  • Hayman ML, Read LK (1999) Trypanosoma brucei RBP16 is a mitochondrial Y-box family protein with guide RNA binding activity. J Biol Chem 274:12067–12074

    Article  PubMed  CAS  Google Scholar 

  • Jankowsky E, Bowers E (2006) Remodeling of ribonucleoprotein complexes with DExD/H-box helicases. Nucleic Acids Res 34:4181–4188

    Article  PubMed  CAS  Google Scholar 

  • Johnson ER, McKay DB (1999) Crystallographic structure of the amino terminal domain of yeast initiation factor 4A, a representative DEAD-box RNA helicase. RNA 5:1526–1534

    Article  PubMed  CAS  Google Scholar 

  • Kable ML, Seiwert SD, Heidmann S, Stuart K (1996) RNA editing: a mechanism for gRNA-specified uridylate insertion into precursor mRNA. Science 273:1189–1195

    Article  PubMed  CAS  Google Scholar 

  • Köller J, Müller UF, Schmid B, Missel A, Kruft V, Stuart K, Göringer HU (1997) Trypanosoma brucei gBP21: an arginine-rich mitochondrial protein that binds to guide RNA with high affinity. J Biol Chem 272:3749–3757

    Article  PubMed  Google Scholar 

  • Kopp J, Schwede T (2004) The SWISS-MODEL repository of annotated three-dimensional protein structure homology models. Nucleic Acids Res 32:D230–D234

    Article  PubMed  CAS  Google Scholar 

  • Langer T (2000) AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem Sci 25:247–251

    Article  PubMed  CAS  Google Scholar 

  • Leonhard K, Herrmann JM, Stuart RA, Mannhaupt G, Neupert W, Langer T (1996) AAA proteases with catalytic sites on opposite membrane surfaces comprise a proteolytic system for the ATP-dependent degradation of inner membrane proteins in mitochondria. EMBO J 15:4218–4229

    PubMed  CAS  Google Scholar 

  • Linder P (2006) DEAD-box proteins: a family affair – active and passive players in RNP-remodeling. Nucleic Acids Res 34:4168–4180

    Article  PubMed  CAS  Google Scholar 

  • Madison-Antenucci S, Hajduk SL (2001) RNA editing-associated protein 1 is an RNA binding protein with specificity for preedited mRNA. Mol Cell 7:879–886

    Article  PubMed  CAS  Google Scholar 

  • Madison-Antenucci S, Sabatini RS, Pollard VW, Hajduk SL (1998) Kinetoplastid RNA-editing-associated protein 1 (REAP-1): a novel editing complex protein with repetitive domains. EMBO J 17:6368–6376

    Article  PubMed  CAS  Google Scholar 

  • Madison-Antenucci S, Grams J, Hajduk SL (2002) Editing machines: the complexities of trypanosome RNA editing. Cell 108:435–438

    Article  PubMed  CAS  Google Scholar 

  • Maslov DA, Simpson L (1992) The polarity of editing within a multiple gRNA-mediated domain is due to formation of anchors for upstream gRNAs by downstream editing. Cell 70:459–467

    Article  PubMed  CAS  Google Scholar 

  • McManus MT, Shimamura M, Grams J, Hajduk SL (2001) Identification of candidate mitochondrial RNA editing ligases from Trypanosoma brucei. RNA 7:167–175

    Article  PubMed  CAS  Google Scholar 

  • Merrick WC (2004) Cap-dependent and cap-independent translation in eukaryotic systems. Gene 332:1–11

    Article  PubMed  CAS  Google Scholar 

  • Miller MM, Read LK (2003) Trypanosoma brucei: functions of RBP16 cold shock and RGG domains in macromolecular interactions. Exp Parasitol 105:140–148

    Article  PubMed  CAS  Google Scholar 

  • Missel A, Göringer HU (1994) Trypanosoma brucei mitochondria contain RNA helicase activity. Nucleic Acids Res 22:4050–4056

    Article  PubMed  CAS  Google Scholar 

  • Missel A, Souza AE, Nörskau G, Göringer HU (1997) Gene disruption of a mitochondrial DEAD box protein in Trypanosoma brucei affects edited mRNAs. Mol Cell Biol 17:4895–4903

    PubMed  CAS  Google Scholar 

  • Müller UF, Göringer HU (2002) Mechanism of the gBP21-mediated RNA/RNA annealing reaction: matchmaking and charge reduction. Nucleic Acids Res 30:447–455

    Article  PubMed  Google Scholar 

  • Müller UF, Lambert L, Göringer HU (2001) Annealing of RNA editing substrates facilitated by guide RNA-binding protein gBP21. EMBO J 20:1394–1404

    Article  PubMed  Google Scholar 

  • Nazar RN (2004) Ribosomal RNA processing and ribosome biogenesis in eukaryotes. IUBMB Life 56:457–465

    Article  PubMed  CAS  Google Scholar 

  • Ochsenreiter T, Hajduk SL (2006) Alternative editing of cytochrome c oxidase III mRNA in trypanosome mitochondria generates protein diversity. EMBO Rep 7:1128–1133

    Article  PubMed  CAS  Google Scholar 

  • Panigrahi AK, Schnaufer A, Carmean N, Igo RP Jr, Gygi SP, Ernst NL, Palazzo SS, Weston DS, Aebersold R, Salavati R, Stuart KD (2001) Four related proteins of the Trypanosoma brucei RNA editing complex. Mol Cell Biol 21:6833–6840

    Article  PubMed  CAS  Google Scholar 

  • Panigrahi AK, Ernst NL, Domingo GJ, Fleck M, Salavati R, Stuart KD (2006) Compositionally and functionally distinct editosomes in Trypanosoma brucei. RNA 12:1038–1049

    Article  PubMed  CAS  Google Scholar 

  • Patel S, Latterich M (1998) The AAA team: related ATPases with diverse functions. Trends Cell Biol 8:65–71

    Article  PubMed  CAS  Google Scholar 

  • Pelletier M, Read LK (2003) RBP16 is a multifunctional gene regulatory protein involved in editing and stabilization of specific mitochondrial mRNAs in Trypanosoma brucei. RNA 9:457–468

    Article  PubMed  CAS  Google Scholar 

  • Pelletier M, Miller MM, Read LK (2000) RNA-binding properties of the mitochondrial Y-box protein RBP16. Nucleic Acids Res 28:1266–1275

    Article  PubMed  CAS  Google Scholar 

  • Pollard VW, Harris ME, Hajduk S (1992) Native mRNA editing complexes from Trypanosoma brucei mitochondria. EMBO J 11:4429–4438

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rusché LN, Cruz-Reyes J, Piller KJ, Sollner-Webb B (1997) Purification of a functional enzymatic editing complex from Trypanosoma brucei mitochondria. EMBO J 16:4069–4081

    Article  PubMed  Google Scholar 

  • Rusché LN, Huang CE, Piller KJ, Hemann M, Wirtz E, Sollner-Webb B (2001) The two RNA ligases of the Trypanosoma brucei RNA editing complex: cloning the essential band IV gene and identifying the band V gene. Mol Cell Biol 21:979–989

    Article  PubMed  Google Scholar 

  • Sabatini R, Hajduk SL (1995) RNA ligase and its involvement in guide RNA/mRNA chimera formation. Evidence for a cleavage-ligation mechanism of Trypanosoma brucei mRNA editing. J Biol Chem 270:7233–7240

    Article  PubMed  CAS  Google Scholar 

  • Sbicego S, Alfonzo JD, Estevez AM, Rubio MA, Kang X, Turck CW, Peris M, Simpson L (2003) RBP38, a novel RNA-binding protein from trypanosomatid mitochondria, modulates RNA stability. Eukaryot Cell 2:560–568

    Article  PubMed  CAS  Google Scholar 

  • Schmid SR, Linder P (1992) D-E-A-D protein family of putative RNA helicases. Mol Microbiol 6:283–291

    Article  PubMed  CAS  Google Scholar 

  • Schnaufer A, Ernst NL, Palazzo SS, O’Rear J, Salavati R, Stuart K (2003) Separate insertion and deletion subcomplexes of the Trypanosoma brucei RNA editing complex. Mol Cell 12:307–319

    Article  PubMed  CAS  Google Scholar 

  • Schumacher MA, Karamooz E, Zikova A, Trantirek L, Lukes J (2006) Crystal structures of T. brucei MRP1/MRP2 guide-RNA binding complex reveal RNA matchmaking mechanism. Cell 126:701–711

    Article  PubMed  CAS  Google Scholar 

  • Schwede T, Kopp J, Guex N, Peitsch MC (2003) SWISS-MODEL: an automated protein homology-model server. Nucleic Acids Res 31:3381–3385

    Article  PubMed  CAS  Google Scholar 

  • Schwer B, Guthrie C (1991) PRP16 is an RNA-dependent ATPase that interacts transiently with the spliceosome. Nature 349:494–499

    Article  PubMed  CAS  Google Scholar 

  • Seiwert SD, Stuart K (1994) RNA editing: transfer of genetic information from gRNA to precursor mRNA in vitro. Science 266:114–117

    Article  PubMed  CAS  Google Scholar 

  • Seiwert SD, Heidmann S, Stuart K (1996) Direct visualization of uridylate deletion in vitro suggests a mechanism for kinetoplastid RNA editing. Cell 84:831–841

    Article  PubMed  CAS  Google Scholar 

  • Staley JP, Guthrie C (1998) Mechanical devices of the spliceosome: motors, clocks, springs, and things. Cell 92:315–326

    Article  PubMed  CAS  Google Scholar 

  • Story RM, Li H, Abelson JN (2001) Crystal structure of a DEAD box protein from the hyperthermophile Methanococcus jannaschii. Proc Natl Acad Sci USA 13:1465–1470

    Article  Google Scholar 

  • Stuart K, Panigrahi AK, Schnaufer A, Drozdz M, Clayton C, Salavati R (2002) Composition of the editing complex of Trypanosoma brucei. Philos Trans R Soc Lond B Biol Sci 357:71–79

    Article  PubMed  CAS  Google Scholar 

  • Stuart KD, Schnaufer A, Ernst NL, Panigrahi AK (2005) Complex management: RNA editing in trypanosomes. Trends Biochem Sci 30:97–105

    Article  PubMed  CAS  Google Scholar 

  • Tanner NK, Cordin O, Banroques J, Doere M, Linder P (2003) The Q motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol Cell 11:127–138

    Article  PubMed  CAS  Google Scholar 

  • Thomas JH (1993) Thinking about genetic redundancy. Trends Genet 9:395–399

    Article  PubMed  CAS  Google Scholar 

  • Trotter JR, Ernst NL, Carnes J, Panicucci B, Stuart K (2005) A deletion site editing endonuclease in Trypanosoma brucei. Mol Cell 20:403–412

    Article  PubMed  CAS  Google Scholar 

  • Vanhamme L, Perez-Morga D, Marchal C, Speijer D, Lambert L, Geusken M, Alexandre S, Ismaïli N, Göringer HU, Benne R, Pays E (1998) Trypanosoma brucei TBRGG1, a mitochondrial oligo(U)-binding protein that co-localizes with an in vitro RNA editing activity. J Biol Chem 273:21825–21833

    Article  PubMed  CAS  Google Scholar 

  • Ye J, Osborne AR, Groll M, Rapoport TA (2004) RecA-like motor ATPases–lessons from structures. Biochim Biophys Acta 1659:1–18

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Genetics, Darmstadt University of Technology, Schnittspahnstr. 10, 64287, Darmstadt, Germany

    H. Ulrich Göringer, Michael Brecht, Cordula Böhm & Elisabeth Kruse

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  1. H. Ulrich Göringer
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  2. Michael Brecht
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  3. Cordula Böhm
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  4. Elisabeth Kruse
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  1. Institute of Microbiology and Genetics, Technical University Darmstadt, Schnittspahnstr. 10, 64287, Darmstadt, Germany

    H. Ulrich Göringer

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Göringer, H.U., Brecht, M., Böhm, C., Kruse, E. (2008). RNA Editing Accessory Factors — the Example of mHel61p. In: Göringer, H.U. (eds) RNA Editing. Nucleic Acids and Molecular Biology, vol 20. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-73787-2_8

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