26
Views
10
CrossRef citations to date
0
Altmetric
Article

Identification by Random Mutagenesis of Functional Domains in KREPB5 That Differentially Affect RNA Editing between Life Cycle Stages of Trypanosoma brucei

, &
Pages 3945-3961 | Received 11 Aug 2015, Accepted 08 Sep 2015, Published online: 20 Mar 2023

REFERENCES

  • Sutton RE, Boothroyd JC. 1986. Evidence for trans splicing in trypanosomes. Cell 47:527–535. http://dx.doi.org/10.1016/0092-8674(86)90617-3.
  • Borst P, Cross GA. 1982. Molecular basis for trypanosome antigenic variation. Cell 29:291–303. http://dx.doi.org/10.1016/0092-8674(82)90146-5.
  • Ferguson MA, Cross GA. 1984. Myristylation of the membrane form of a Trypanosoma brucei variant surface glycoprotein. J Biol Chem 259:3011–3015.
  • de Almeida ML, Turner MJ, Stambuk BB, Schenkman S. 1988. Identification of an acid-lipase in human serum which is capable of solubilizing glycophosphatidylinositol-anchored proteins. Biochem Biophys Res Commun 150:476–482. http://dx.doi.org/10.1016/0006-291X(88)90545-1.
  • Agabian N. 1990. Trans splicing of nuclear pre-mRNAs. Cell 61:1157–1160. http://dx.doi.org/10.1016/0092-8674(90)90674-4.
  • Bridgen PJ, Cross GA, Bridgen J. 1976. N-terminal amino acid sequences of variant-specific surface antigens from Trypanosoma brucei. Nature 263:613–614. http://dx.doi.org/10.1038/263613a0.
  • Johnson PJ, Kooter JM, Borst P. 1987. Inactivation of transcription by UV irradiation of T. brucei provides evidence for a multicistronic transcription unit including a VSG gene. Cell 51:273–281. http://dx.doi.org/10.1016/0092-8674(87)90154-1.
  • Holder AA, Cross GA. 1981. Glycopeptides from variant surface glycoproteins of Trypanosoma brucei. C-terminal location of antigenically cross-reacting carbohydrate moieties. Mol Biochem Parasitol 2:135–150.
  • 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. http://dx.doi.org/10.1016/0092-8674(86)90063-2.
  • Shaw JM, Feagin JE, Stuart K, Simpson L. 1988. Editing of kinetoplastid mitochondrial mRNAs by uridine addition and deletion generates conserved amino acid sequences and AUG initiation codons. Cell 53:401–411. http://dx.doi.org/10.1016/0092-8674(88)90160-2.
  • Feagin JE, Jasmer DP, Stuart K. 1987. Developmentally regulated addition of nucleotides within apocytochrome b transcripts in Trypanosoma brucei. Cell 49:337–345. http://dx.doi.org/10.1016/0092-8674(87)90286-8.
  • Shapiro TA, Englund PT. 1995. The structure and replication of kinetoplast DNA. Annu Rev Microbiol 49:117–143. http://dx.doi.org/10.1146/annurev.mi.49.100195.001001.
  • Stuart K, Feagin JE. 1992. Mitochondrial DNA of kinetoplastids. Int Rev Cytol 141:65–88. http://dx.doi.org/10.1016/S0074-7696(08)62063-X.
  • Stuart KD, Schnaufer A, Ernst NL, Panigrahi AK. 2005. Complex management: RNA editing in trypanosomes. Trends Biochem Sci 30:97–105. http://dx.doi.org/10.1016/j.tibs.2004.12.006.
  • Goringer HU. 2012. ‘Gestalt,’ composition and function of the Trypanosoma brucei editosome. Annu Rev Microbiol 66:65–82. http://dx.doi.org/10.1146/annurev-micro-092611-150150.
  • Aphasizhev R, Aphasizheva I. 2011. Uridine insertion/deletion editing in trypanosomes: a playground for RNA-guided information transfer. Wiley Interdiscip Rev RNA 2:669–685. http://dx.doi.org/10.1002/wrna.82.
  • Priest JW, Hajduk SL. 1994. Developmental regulation of mitochondrial biogenesis in Trypanosoma brucei. J Bioenerg Biomembr 26:179–191. http://dx.doi.org/10.1007/BF00763067.
  • Schneider A. 2001. Unique aspects of mitochondrial biogenesis in trypanosomatids. Int J Parasitol 31:1403–1415. http://dx.doi.org/10.1016/S0020-7519(01)00296-X.
  • Koslowsky DJ, Riley GR, Feagin JE, Stuart K. 1992. Guide RNAs for transcripts with developmentally regulated RNA editing are present in both life cycle stages of Trypanosoma brucei. Mol Cell Biol 12:2043–2049.
  • Riley GR, Myler PJ, Stuart K. 1995. Quantitation of RNA editing substrates, products and potential intermediates: implications for developmental regulation. Nucleic Acids Res 23:708–712. http://dx.doi.org/10.1093/nar/23.4.708.
  • Panigrahi AK, Gygi SP, Ernst NL, Igo RP, Jr, Palazzo SS, Schnaufer A, Weston DS, Carmean N, Salavati R, Aebersold R, Stuart KD. 2001. Association of two novel proteins, TbMP52 and TbMP48, with the Trypanosoma brucei RNA editing complex. Mol Cell Biol 21:380–389. http://dx.doi.org/10.1128/MCB.21.2.380-389.2001.
  • 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. http://dx.doi.org/10.1128/MCB.21.20.6833-6840.2001.
  • Panigrahi AK, Allen TE, Stuart K, Haynes PA, Gygi SP. 2003. Mass spectrometric analysis of the editosome and other multiprotein complexes in Trypanosoma brucei. J Am Soc Mass Spectrom 14:728–735. http://dx.doi.org/10.1016/S1044-0305(03)00126-0.
  • Panigrahi AK, Schnaufer A, Ernst NL, Wang B, Carmean N, Salavati R, Stuart K. 2003. Identification of novel components of Trypanosoma brucei editosomes. RNA 9:484–492. http://dx.doi.org/10.1261/rna.2194603.
  • 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. http://dx.doi.org/10.1261/rna.45506.
  • Carnes J, Soares CZ, Wickham C, Stuart K. 2011. Endonuclease associations with three distinct editosomes in Trypanosoma brucei. J Biol Chem 286:19320–19330. http://dx.doi.org/10.1074/jbc.M111.228965.
  • 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 U S A 102:16614–16619. http://dx.doi.org/10.1073/pnas.0506133102.
  • Carnes J, Trotter JR, Peltan A, Fleck M, Stuart K. 2008. RNA editing in Trypanosoma brucei requires three different editosomes. Mol Cell Biol 28:122–130. http://dx.doi.org/10.1128/MCB.01374-07.
  • Trotter JR, Ernst NL, Carnes J, Panicucci B, Stuart K. 2005. A deletion site editing endonuclease in Trypanosoma brucei. Mol Cell 20:403–412. http://dx.doi.org/10.1016/j.molcel.2005.09.016.
  • Lerch M, Carnes J, Acestor N, Guo X, Schnaufer A, Stuart K. 2012. Editosome accessory factors KREPB9 and KREPB10 in Trypanosoma brucei. Eukaryot Cell 11:832–843. http://dx.doi.org/10.1128/EC.00046-12.
  • Ernst NL, Panicucci B, Igo RP, Jr, Panigrahi AK, Salavati R, Stuart K. 2003. TbMP57 is a 3′ terminal uridylyl transferase (TUTase) of the Trypanosoma brucei editosome. Mol Cell 11:1525–1536. http://dx.doi.org/10.1016/S1097-2765(03)00185-0.
  • Guo X, Carnes J, Ernst NL, Winkler M, Stuart K. 2012. KREPB6, KREPB7, and KREPB8 are important for editing endonuclease function in Trypanosoma brucei. RNA 18:308–320. http://dx.doi.org/10.1261/rna.029314.111.
  • Wang B, Ernst NL, Palazzo SS, Panigrahi AK, Salavati R, Stuart K. 2003. TbMP44 is essential for RNA editing and structural integrity of the editosome in Trypanosoma brucei. Eukaryot Cell 2:578–587. http://dx.doi.org/10.1128/EC.2.3.578-587.2003.
  • McDermott SM, Guo X, Carnes J, Stuart K. 24 August 2015. Differential editosome protein function between life cycle stages of Trypanosoma brucei. J Biol Chem http://dx.doi.org/10.1074/jbc.M115.669432.
  • Carnes J, Schnaufer A, McDermott SM, Domingo G, Proff R, Steinberg AG, Kurtz I, Stuart K. 2012. Mutational analysis of Trypanosoma brucei editosome proteins KREPB4 and KREPB5 reveals domains critical for function. RNA 18:1897–1909. http://dx.doi.org/10.1261/rna.035048.112.
  • Worthey EA, Schnaufer A, Mian IS, Stuart K, Salavati R. 2003. Comparative analysis of editosome proteins in trypanosomatids. Nucleic Acids Res 31:6392–6408. http://dx.doi.org/10.1093/nar/gkg870.
  • Gray PN, Busser KJ, Chappell TG. 2007. A novel approach for generating full-length, high coverage allele libraries for the analysis of protein interactions. Mol Cell Proteomics 6:514–526.
  • Merritt C, Stuart K. 2013. Identification of essential and non-essential protein kinases by a fusion PCR method for efficient production of transgenic Trypanosoma brucei. Mol Biochem Parasitol 190:44–49. http://dx.doi.org/10.1016/j.molbiopara.2013.05.002.
  • Raz B, Iten M, Grether-Buhler Y, Kaminsky R, Brun R. 1997. The Alamar Blue assay to determine drug sensitivity of African trypanosomes (T.b. rhodesiense and T.b. gambiense) in vitro. Acta Trop 68:139–147. http://dx.doi.org/10.1016/S0001-706X(97)00079-X.
  • Guo X, Ernst NL, Stuart KD. 2008. The KREPA3 zinc finger motifs and OB-fold domain are essential for RNA editing and survival of Trypanosoma brucei. Mol Cell Biol 28:6939–6953. http://dx.doi.org/10.1128/MCB.01115-08.
  • Stuart K, Panigrahi AK, Schnaufer A. 2004. Identification and characterization of trypanosome RNA-editing complex components. Methods Mol Biol 265:273–291.
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method. Methods 25:402–408. http://dx.doi.org/10.1006/meth.2001.1262.
  • Soding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33:W244–W248. http://dx.doi.org/10.1093/nar/gki408.
  • Sali A, Blundell TL. 1993. Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815. http://dx.doi.org/10.1006/jmbi.1993.1626.
  • Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Cassarino TG, Bertoni M, Bordoli L, Schwede T. 2014. SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42:W252–W258. http://dx.doi.org/10.1093/nar/gku340.
  • Stone EA, Sidow A. 2005. Physicochemical constraint violation by missense substitutions mediates impairment of protein function and disease severity. Genome Res 15:978–986. http://dx.doi.org/10.1101/gr.3804205.
  • Capra JA, Singh M. 2007. Predicting functionally important residues from sequence conservation. Bioinformatics 23:1875–1882. http://dx.doi.org/10.1093/bioinformatics/btm270.
  • Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. http://dx.doi.org/10.1093/nar/gkh340.
  • MacRae IJ, Doudna JA. 2007. Ribonuclease revisited: structural insights into ribonuclease III family enzymes. Curr Opin Struct Biol 17:138–145. http://dx.doi.org/10.1016/j.sbi.2006.12.002.
  • Nicholson AW. 2014. Ribonuclease III mechanisms of double-stranded RNA cleavage. Wiley Interdiscip Rev RNA 5:31–48. http://dx.doi.org/10.1002/wrna.1195.
  • Conrad C, Schmitt JG, Evguenieva-Hackenberg E, Klug G. 2002. One functional subunit is sufficient for catalytic activity and substrate specificity of Escherichia coli endoribonuclease III artificial heterodimers. FEBS Lett 518:93–96. http://dx.doi.org/10.1016/S0014-5793(02)02653-4.
  • Meng W, Nicholson AW. 2008. Heterodimer-based analysis of subunit and domain contributions to double-stranded RNA processing by Escherichia coli RNase III in vitro. Biochem J 410:39–48. http://dx.doi.org/10.1042/BJ20071047.
  • Melamed D, Young DL, Gamble CE, Miller CR, Fields S. 2013. Deep mutational scanning of an RRM domain of the Saccharomyces cerevisiae poly(A)-binding protein. RNA 19:1537–1551. http://dx.doi.org/10.1261/rna.040709.113.
  • Glover L, Horn D. 2009. Site-specific DNA double-strand breaks greatly increase stable transformation efficiency in Trypanosoma brucei. Mol Biochem Parasitol 166:194–197. http://dx.doi.org/10.1016/j.molbiopara.2009.03.010.
  • Alsford S, Turner DJ, Obado SO, Sanchez-Flores A, Glover L, Berriman M, Hertz-Fowler C, Horn D. 2011. High-throughput phenotyping using parallel sequencing of RNA interference targets in the African trypanosome. Genome Res 21:915–924. http://dx.doi.org/10.1101/gr.115089.110.
  • Glover L, Alsford S, Baker N, Turner DJ, Sanchez-Flores A, Hutchinson S, Hertz-Fowler C, Berriman M, Horn D. 2015. Genome-scale RNAi screens for high-throughput phenotyping in bloodstream-form African trypanosomes. Nat Protoc 10:106–133. http://dx.doi.org/10.1038/nprot.2015.005.
  • Alsford S, Eckert S, Baker N, Glover L, Sanchez-Flores A, Leung KF, Turner DJ, Field MC, Berriman M, Horn D. 2012. High-throughput decoding of antitrypanosomal drug efficacy and resistance. Nature 482:232–236. http://dx.doi.org/10.1038/nature10771.
  • Dreze M, Charloteaux B, Milstein S, Vidalain PO, Yildirim MA, Zhong Q, Svrzikapa N, Romero V, Laloux G, Brasseur R, Vandenhaute J, Boxem M, Cusick ME, Hill DE, Vidal M. 2009. ‘Edgetic’ perturbation of a C. elegans BCL2 ortholog. Nat Methods 6:843–849. http://dx.doi.org/10.1038/nmeth.1394.
  • Hirumi H, Hirumi K. 1989. Continuous cultivation of Trypanosoma brucei bloodstream forms in a medium containing a low concentration of serum protein without feeder cell layers. J Parasitol 75:985–989.
  • Brun R, Schoenenberger M. 1979. Cultivation and in vitro cloning of procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop 36:289–292.
  • Hanahan D. 1983. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.