Skip to main content

The Remarkable Mitochondrion of Trypanosomes and Related Flagellates

  • Chapter
  • First Online:
Structures and Organelles in Pathogenic Protists

Part of the book series: Microbiology Monographs ((MICROMONO,volume 17))

Abstract

While the single mitochondrion of trypanosomatid flagellates contains many of the hallmarks that are known from mitochondria in other conventional model organisms, it also possesses several unique features, making it a subject of intense research. Here, we summarize current knowledge of the (1) structure, maintenance and replication of the extensive kinetoplastid DNA network, (2) byzantine organellar RNA metabolism, including insertion/deletion RNA editing, (3) translation of mitochondrial-encoded proteins, and, finally, (4) distinctive aspects of energy metabolism of the organelle. While we focus on the mitochondrion of Trypanosoma brucei, particularly in the context of its radical physiological and biochemical changes during the life cycle of the parasite, in order to get a more complete picture of the workings of this fascinating organelle, we also discuss significant findings obtained from other trypanosomatids.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
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

  • Abu-Elneel K, Robinson DR, Drew ME, Englund PT, Shlomai J (2001) Intramitochondrial localization of universal minicircle sequence-binding protein, a trypanosomatid protein that binds kinetoplast minicircle replication origin. J Cell Biol 153:725–733

    Article  CAS  PubMed  Google Scholar 

  • Adler BK, Harris ME, Bertrand KI, Hajduk SL (1991) Modification of Trypanosoma brucei mitochondrial rRNA by posttranscriptional 3′ polyuridine tail formation. Mol Cell Biol 11:5878–5884

    CAS  PubMed  Google Scholar 

  • Alfonzo JD, Blanc V, Estévez AM, Rubio MA, Simpson L (1999) C to U editing of the anticodon of imported mitochondrial tRNATrp allows decoding of the UGA stop codon in Leishmania tarentolae. EMBO J 24:7056–7062

    Article  Google Scholar 

  • Amaro RE, Schnaufer A, Interthal H, Hol W, Stuart KD, McCammon JA (2008) Discovery of drug-like inhibitors of an essential RNA-editing ligase in Trypanosoma brucei. Proc Natl Acad Sci USA 105:17278–17283

    Article  CAS  PubMed  Google Scholar 

  • Ammerman ML, Fisk JC, Read LK (2008) gRNA/pre-mRNA annealing and RNA chaperone activities of RBP16. RNA 14:1069–1080

    Article  CAS  PubMed  Google Scholar 

  • Aphasizhev R, Aphasizheva I, Simpson L (2003a) A tale of two TUTases. Proc Natl Acad Sci USA 100:10617–10622

    Article  CAS  PubMed  Google Scholar 

  • Aphasizhev R, Aphasizheva I, Nelson RE, Simpson L (2003b) A 100-kD complex of two RNA-binding proteins from mitochondria of Leishmania tarentolae catalyzes RNA annealing and interacts with several RNA editing components. RNA 9:62–76

    Article  CAS  PubMed  Google Scholar 

  • Attardi GM, Chomyn A (1995) Mitochondrial biogenesis and genetics. Academic, San Diego

    Google Scholar 

  • Avliyakulov NK, Lukeš J, Ray DS (2004) Mitochondrial histone-like DNA-binding proteins are essential for normal cell growth and mitochondrial function in Crithidia fasciculata. Eukaryot Cell 3:518–526

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Besteiro S, Barrett MP, Riviere L, Bringaud F (2005) Energy generation in insect stages of Trypanosoma brucei: metabolism in flux. Trends Parasitol 21:185–191

    Article  CAS  PubMed  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

    Google Scholar 

  • Bouzaidi-Tiali N, Aeby E, Charriere F, Pusnik M, Schneider A (2007) Elongation factor 1a mediates the specificity of mitochondrial tRNA import in T. brucei. EMBO J 26:4302–4312

    Article  CAS  PubMed  Google Scholar 

  • Bringaud F, Riviére L, Coustou V (2006) Energy metabolism of trypanosomatids: adaptation to available carbon sources. Mol Biochem Parasitol 149:1–9

    Article  CAS  PubMed  Google Scholar 

  • Brown SV, Hosking P, Li J, Williams N (2006) ATP synthase is responsible for maintaining mitochondrial membrane potential in bloodstream form Trypanosoma brucei. Eukaryot Cell 5:45–53

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Cazzulo JJ (1992) Aerobic fermentation of glucose by trypanosomatids. FASEB J 6:3153–3161

    CAS  PubMed  Google Scholar 

  • Chaudhuri M, Ott RD, Hill GC (2006) Trypanosome alternative oxidase: from molecule to function. Trends Parasitol 22:484–491

    Article  CAS  PubMed  Google Scholar 

  • Chen JH, Rauch CA, White JH, Englund PT, Cozzarelli NR (1995) The topology of the kinetoplast DNA network. Cell 80:61–69

    Article  CAS  PubMed  Google Scholar 

  • Coustou V, Biran M, Breton M, Guegan FR, Plazolles N, Nolan D, Barrett MP, Franconi JM, Bringaud F (2008) Glucose-induced remodeling of intermediary and energy metabolism in procyclic Trypanosoma brucei. J Biol Chem 283:16342–16354

    Article  CAS  PubMed  Google Scholar 

  • Deng J, Schnaufer A, Salavati R, Stuart KD, Hol WG (2004) High resolution crystal structure of a key editosome enzyme from Trypanosoma brucei: RNA editing ligase 1. J Mol Biol 343:601–613

    Article  CAS  PubMed  Google Scholar 

  • Downey N, Hines JC, Sinha KM, Ray DS (2005) Mitochondrial DNA ligases of Trypanosoma brucei. Eukaryot Cell 4:765–774

    Article  CAS  PubMed  Google Scholar 

  • Drew ME, Englund PT (2001) Intramitochondrial location and dynamics of Crithidia fasciculata kinetoplast minicircle replication intermediates. J Cell Biol 153:735–744

    Article  CAS  PubMed  Google Scholar 

  • Dyková I, Fiala I, Lom J, Lukeš J (2003) Perkinsiella amoebae-like endosymbionts of Neoparamoeba spp., relatives of the kinetoplastid Ichthyobodo. Eur J Protistol 39:37–52

    Article  Google Scholar 

  • Englund PT (1979) Free minicircles of kinetoplast DNA in Crihidia fasciculata. J Biol Chem 254:4895–4900

    CAS  PubMed  Google Scholar 

  • Estevez AM, Simpson L (1999) Uridine insertion/deletion RNA editing in trypanosome mitochondria – a review. Gene 240:247–260

    Article  CAS  PubMed  Google Scholar 

  • Etheridge RD, Aphasizheva I, Gershon PD, Aphasizhev R (2008) 3′ adenylation determines mRNA abundance and monitors completion of RNA editing in T. brucei mitochondria. EMBO J 27:1596–1608

    Article  CAS  PubMed  Google Scholar 

  • Fang J, Beattie DS (2003a) Alternative oxidase present in procyclic Trypanosoma brucei may act to lower the mitochondrial production of superoxide. Arch Biochem Biophys 414:294–302

    Article  CAS  PubMed  Google Scholar 

  • Fang J, Beattie DS (2003b) Identification of a gene encoding a 54 kDa alternative NADH dehydrogenase in Trypanosoma brucei. Mol Biochem Parasitol 127:73–77

    Article  CAS  PubMed  Google Scholar 

  • Fisk JC, Ammerman ML, Presnyak V, Read LK (2008) TbRGG2, an essential RNA editing accessory factor in two Trypanosoma brucei life cycle stages. J Biol Chem 283:23016–23025

    Article  CAS  PubMed  Google Scholar 

  • Flegontov PN, Zhirenkina EN, Gerasimov ES, Ponirovsky EN, Strelkova MV, Kolesnikov AA (2009) Selective amplification of maxicircle classes during the life cycle of Leishmania major. Mol Biochem Parasitol 165:142–152

    Article  CAS  PubMed  Google Scholar 

  • Fontanesi F, Soto IC, Barrientos A (2008) Cytochrome c oxidase biogenesis: new levels of regulation. IUBMB Life 60:557–568

    Article  CAS  PubMed  Google Scholar 

  • Gabaldón T, Rainey D, Huynen MA (2005) Tracing the evolution of a large protein complex in the eukaryotes, NADH:ubiquinone oxidoreductase (complex I). J Mol Biol 348:857–870

    Article  PubMed  CAS  Google Scholar 

  • Gluenz E, Shaw MK, Gull K (2007) Structural asymmetry and discrete nucleic acid subdomains in the Trypanosoma brucei kinetoplast. Mol Microbiol 64:1529–1539

    Article  CAS  PubMed  Google Scholar 

  • Golas MM, Böhm C, Sander B, Effenberger K, Brecht M, Stark H, Göringer HU (2009) Snapshots of the RNA editing machine in trypanosomes captured at different assembly stages in vivo. EMBO J 28:766–778

    Article  CAS  PubMed  Google Scholar 

  • Golden DE, Hajduk SL (2005) The 3′-untranslated region of cytochrome oxidase II mRNA functions in RNA editing of African trypanosomes exclusively as a cis guide RNA. RNA 11:29–37

    Article  CAS  PubMed  Google Scholar 

  • Grams J, McManus MT, Hajduk SL (2000) Processing of polycistronic guide RNAs is associated with RNA editing complexes in Trypanosoma brucei. EMBO J 19:5525–5532

    Article  CAS  PubMed  Google Scholar 

  • Grams J, Morris JC, Drew ME, Wang ZF, Englund PT, Hajduk SL (2002) A trypanosome mitochondrial RNA polymerase is required for transcription and replication. J Biol Chem 277:16952–16959

    Article  CAS  PubMed  Google Scholar 

  • Guerra DG, Decottignies A, Bakker BM, Michels PAM (2006) The mitochondrial FAD-dependent glycerol-3-phosphate dehydrogenase of Trypanosomatidae and the glycosomal redox balance of insect stage of Trypanosoma brucei and Leishmania spp. Mol Biochem Parasitol 149:155–169

    Article  CAS  PubMed  Google Scholar 

  • Guler JL, Kriegová E, Smith TK, Lukeš J, Englund PT (2008) Mitochondrial fatty acid synthesis is required for normal mitochondrial morphology and function in Trypanosoma brucei. Mol Microbiol 67:1125–1142

    Article  CAS  PubMed  Google Scholar 

  • Hannaert V, Bringaud F, Opperdoes FR, Michels PAM (2003) Evolution of energy metabolism and its compartmentation in Kinetoplastida. Kinetoplastid Biol Dis 2:11–40

    Article  PubMed  Google Scholar 

  • Hashimi H, Zíková A, Panigrahi AK, Stuart KD, Lukeš J (2008) TbRGG1, a component of a novel multi-protein complex involved in kinetoplastid RNA editing. RNA 14:970–980

    Article  CAS  PubMed  Google Scholar 

  • Hashimi H, Čičová Z, Novotná L, Wen YZ, Lukeš J (2009) Kinetoplastid guide RNA biogenesis is dependant on subunits of the mitochondrial RNA binding complex and mitochondrial RNA polymerase. RNA 15:588–599

    Article  CAS  PubMed  Google Scholar 

  • Hashimi H, Benkovičová V, Čermáková P, Lai D-H, Horváth A, Lukeš J (2010) The assembly of F1FO-ATP synthase is disrupted upon interference of RNA editing in Trypanosoma brucei. Int J Parasitol 40:45–54

    Article  CAS  PubMed  Google Scholar 

  • Hernandez FR, Turrens JF (1998) Rotenone at high concenrations inhibits NADH-fumarate reductase and the mitochondrial respiratory chain of Trypanosoma brucei and T. cruzi. Mol Biochem Parasitol 93:135–137

    Article  CAS  PubMed  Google Scholar 

  • Horváth A, Berry EA, Huang L, Maslov DA (2000) Leishmania tarentolae: a parallel isolation of cytochrome bc1 and cytochrome c oxidase. Exp Parasitol 96:160–167

    Article  PubMed  CAS  Google Scholar 

  • Horváth A, Horáková E, Dunajčíková P, Verner Z, Pravdová E, Šlapetová I, Cuninková L, Lukeš J (2005) Down-regulation of the nuclear-encoded subunits of the complexes III and IV disrupts their respective complexes but not complex I in procyclic Trypanosoma brucei. Mol Microbiol 58:116–130

    Article  PubMed  CAS  Google Scholar 

  • Jensen RE, Simpson L, Englund PT (2008) What happens when Trypanosoma brucei leaves Africa. Trends Parasitol 24:428–431

    Article  PubMed  Google Scholar 

  • Kaneko T, Suzuki T, Kapushoc ST, Rubio MA, Ghazvini J, Watanabe K, Simpson L, Suzuki T (2003) Wobble modification differences and subcellular localization of tRNAs in Leishmania tarentolae: implication for tRNA sorting mechanism. EMBO J 22:657–667

    Article  CAS  PubMed  Google Scholar 

  • Kao CY, Read LK (2005) Opposing effect of polyadenylation on the stability of edited and unedited mitochondrial RNAs in Trypanosoma brucei. Mol Cell Biol 25:1634–1644

    Article  CAS  PubMed  Google Scholar 

  • Klingbeil MM, Motyka SA, Englund PT (2002) Multiple mitochondrial DNA polymerases in Trypanosoma brucei. Mol Cell 10:175–186

    Article  CAS  PubMed  Google Scholar 

  • Koslowsky DJ, Yahampath G (1997) Mitochondrial mRNA 3′ cleavage/polyadenylation and RNA editing in Trypanosoma brucei are independent events. Mol Biochem Parasitol 90:81–94

    Article  CAS  PubMed  Google Scholar 

  • Lai D-H, Hashimi H, Lun Z-R, Ayala FJ, Lukeš J (2008) Adaptation of Trypanosoma brucei to gradual loss of kinetoplast DNA: T. equiperdum and T. evansi are petite mutants of T. brucei. Proc Natl Acad Sci USA 105:1999–2004

    Article  CAS  PubMed  Google Scholar 

  • Li Z, Lindsay ME, Motyka SA, Englund PT, Wang CC (2008) Identification of a bacterial-like HsIVU protease in the mitochondria of Trypanosoma brucei and its role in mitochondrial DNA replication. PLoS Pathog 4:e1000048

    Article  PubMed  CAS  Google Scholar 

  • Li F, Ge P, Hui W, Atanasov A, Rogers K, Guo Q, Osato D, Falick AM, Zhou H, Simpson L (2009) Structure of the core editing complex (L-complex) involved in uridine insertion/deletion editing in trypanosomatid mitochondria. Proc Natl Acad Sci USA 106:12306–12310

    Article  CAS  PubMed  Google Scholar 

  • Lindsay ME, Gluenz E, Gull K, Englund PT (2008) A new function of Trypanosoma brucei mitochondrial topoisomerase II is to maintain kinetolpast DNA network topology. Mol Microbiol 70:1465–1476

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Englund PT (2007) The rotational dynamics of kinetoplast DNA replication. Mol Microbiol 64:676–690

    Article  CAS  PubMed  Google Scholar 

  • Liu B, Liu Y, Motyka SA, Agbo EEC, Englund PT (2005) Fellowship of the rings: the replication of kinetoplast DNA. Trends Parasitol 21:363–369

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Molina K, Kalume D, Pandey A, Griffith JD, Englund PT (2006) Role of p38 in replication of Trypanosoma brucei kinetoplast DNA. Mol Cell Biol 26:5382–5393

    Article  CAS  PubMed  Google Scholar 

  • Lukeš J, Votýpka J (2000) Trypanosoma avium: novel features of the kinetoplast structure. Exp Parasitol 96:178–181

    Article  PubMed  Google Scholar 

  • Lukeš J, Guilbride DL, Votýpka J, Zíková A, Benne R, Englund PT (2002) The kinetoplast DNA network: evolution of an improbable structure. Eukaryot Cell 1:495–502

    Article  PubMed  CAS  Google Scholar 

  • Lukeš J, Hashimi H, Zíková A (2005) Unexplained complexity of the mitochondrial genome and transcriptome in kinetoplastid flagellates. Curr Genet 48:277–299

    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  CAS  PubMed  Google Scholar 

  • Maslov DA, Sharma MR, Butler E, Falick AM, Gingery M, Agrawal RK, Spremulli LL, Simpson L (2006) Isolation and characterization of mitochondrial ribosomes and ribosomal subunits from Leishmania tarentolae. Mol Biochem Parasitol 148:69–78

    Article  CAS  PubMed  Google Scholar 

  • Mattiacio JL, Read LK (2008) Roles for TbDSS-1 in RNA surveillance and decay of maturation by-products from the 12S rRNA locus. Nucleic Acids Res 36:319–329

    Article  CAS  PubMed  Google Scholar 

  • McManus MT, Adler BK, Pollard VW, Hajduk SL (2000) Trypanosoma brucei guide RNA poly(U) tail formation is stabilized by cognate mRNA. Mol Cell Biol 20:883–891

    Article  CAS  PubMed  Google Scholar 

  • Militello KT, Read LK (2000) UTP-dependent and -independent pathways of mRNA turnover in Trypanosoma brucei mitochondria. Mol Cell Biol 20:2308–2316

    Article  CAS  PubMed  Google Scholar 

  • Milman N, Motyka SA, Englund PT, Robinson D, Shlomai J (2007) Mitochondrial origin-binding protein UMSBP mediates DNA replication and segregation in trypanosomes. Proc Natl Acad Sci USA 104:19250–19255

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Morales J, Mogi T, Mineki S, Takshima E, Mineki R, Hirawake H, Sakamoto K, Omura S, Kita K (2009) Novel mitochondrial complex II isolated from Trypanosoma cruzi is composed of twelve peptides including a heterodimeric Ip subunit. J Biol Chem 284:7255–7263

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee S, Basu S, Home P, Dhar G, Adhya S (2007) Necessary and sufficient factors for the import of transfer RNA into the kinetoplast mitochondrion. EMBO Rep 8:589–595

    Article  CAS  PubMed  Google Scholar 

  • Neboháčová M, Kim CE, Simpson L, Maslov DA (2009) RNA editing and mitochondrial activity in promastigotes and amastigotes of Leishmania donovani. Int J Parasitol 39:635–644

    Article  PubMed  CAS  Google Scholar 

  • Ochsenreiter T, Anderson S, Wood ZA, Hajduk SL (2008a) Alternative RNA editing produces a novel protein involved in mitochondrial DNA maintenance in trypanosomes. Mol Cell Biol 28:5595–5604

    Article  CAS  PubMed  Google Scholar 

  • Ochsenreiter T, Cipriano M, Hajduk SL (2008b) Alternative mRNA editing in trypanosomes is extensive and may contribute to mitochondrial protein diversity. PLoS One 3:e1566

    Article  PubMed  CAS  Google Scholar 

  • Ogbadoyi EO, Robinson DR, Gull K (2003) A high-order transmembrane structural linkage is responsible for mitochondrial genome positioning and segregation by flagellar basal bodies in trypanosomes. Mol Biol Cell 14:1769–1779

    Article  CAS  PubMed  Google Scholar 

  • Opperdoes FR, Michels PAM (2008) Complex I of Trypanosomatidae: does it exist? Trends Parasitol 24:310–317

    Article  CAS  PubMed  Google Scholar 

  • Pagliarini DJ, Calvo SE, Chang B, Sheth SA, Vafai SB, Ong S-E, Walford GA, Sugiana C, Boneh A, Chen WK, Hill DE, Vidal M, Evans JG, Thornburn DR, Carr SA, Mootha VK (2008) A mitochondrial protein compendium elucidates complex I disease biology. Cell 134:112–123

    Article  CAS  PubMed  Google Scholar 

  • Panigrahi AK, Zíková A, Halley RA, Acestor N, Ogata Y, Myler PJ, Stuart K (2008) Mitochondrial complexes in Trypanosoma brucei: a novel complex and a unique oxidoreductase complex. Mol Cell Proteomics 7:534–545

    CAS  PubMed  Google Scholar 

  • Panigrahi AK, Ogata Y, Zíková A, Anupama A, Dalley RA, Acestor N, Myler PJ, Stuart KD (2009) A comprehensive analysis of Trypanosoma brucei mitochondrial proteome. Proteomics 9:434–450

    Article  CAS  PubMed  Google Scholar 

  • Paris Z, Rubio MAT, Lukeš J, Alfonzo JD (2009) Mitochondrial tRNA import in Trypanosoma brucei is independent of thiolation and the Rieske protein. RNA 15:1398–1406

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Penschow JL, Sleve DA, Ryan CM, Read LK (2004) TbDSS-1, an essential Trypanosoma brucei exoribonuclease homolog that has pleiotropic effects on mitochondrial RNA metabolism. Eukaryot Cell 3:1206–1216

    Article  CAS  PubMed  Google Scholar 

  • Pusnik M, Small I, Read LK, Fabbro T, Schneider A (2007) Pentatricopeptide repeat proteins in Trypanosoma brucei function in mitochondrial ribosomes. Mol Cell Biol 27:6876–6888

    Article  CAS  PubMed  Google Scholar 

  • Rubio MAT, Alfonzo J (2005) Editing and modification in trypanosomatids: the reshaping of non-coding RNAs. Top Curr Genet 12:71–86

    Google Scholar 

  • Ryan CM, Read LK (2005) UTP-dependent turnover of Trypanosoma brucei mitochondrial mRNA requires UTP polymerization and involves the RET1 TUTase. RNA 11:1–11

    Article  CAS  Google Scholar 

  • Saxowsky TT, Choudhary G, Klingbeil MM, Englund PT (2003) Trypanosoma brucei has two distinct mitochondrial DNA polymerase beta enzymes. J Biol Chem 278:49095–49101

    Article  CAS  PubMed  Google Scholar 

  • Schnaufer A, Panigrahi AK, Panicucci B, Igo RP Jr, Wirtz E, Salavati R, Stuart K (2001) An RNA ligase essential for RNA editing and survival of the bloodstream form of Trypanosoma brucei. Science 291:2159–2162

    Article  CAS  PubMed  Google Scholar 

  • Schnaufer A, Domingo GJ, Stuart K (2002) Natural and induced dyskinetoplastic trypanosomatids: how to live without mitochondrial DNA. Int J Parasitol 32:1071–1084

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Schnaufer A, Clark-Walker GD, Steinberg AG, Stuart K (2005) The F1-ATP synthase complex in bloodstram stage of trypanosomes has an unusual and essential function. EMBO J 24:4029–4040

    Article  CAS  PubMed  Google Scholar 

  • Schneider A (2001) Unique aspects of mitochondrial biogenesi in trypanosomatids. Int J Parasitol 31:1403–1415

    Article  CAS  PubMed  Google Scholar 

  • Schumacher MA, Karamooz E, Zíková A, Trantírek L, Lukeš J (2006) Crystal structures of Trypanosoma brucei MRP1/MRP2 guide-RNA-binding complex reveals RNA matchmaking mechanism. Cell 126:701–711

    Article  CAS  PubMed  Google Scholar 

  • Sela D, Shlomai J (2009) Regulation of UMSBP activities through redox-sensitive protein domains. Nucleic Acids Res 37:279–288

    Article  CAS  PubMed  Google Scholar 

  • Shapiro TA, Englund PT (1995) The structure and replication of kinetoplast DNA. Annu Rev Microbiol 49:117–143

    Article  CAS  PubMed  Google Scholar 

  • Shlomai J (2004) The structure and replication of kinetoplast DNA. Curr Mol Med 4:623–647

    Article  CAS  PubMed  Google Scholar 

  • Simpson L, Aphasizhev R, Gao G, Kang X (2004) Mitochondrial proteins and complexes in Leishmania and Trypanosoma involved in U-insertion/deletion RNA editing. RNA 10:159–170

    Article  CAS  PubMed  Google Scholar 

  • Simpson AGB, Stevens JR, Lukeš J (2006) The evolution and diversity of kinetoplastid flagellates. Trends Parasitol 22:168–174

    Article  CAS  PubMed  Google Scholar 

  • Simpson L, Aphasizhev R, Lukeš J, Cruz-Reyes J (2010) Guide to the nomenclature of kinetoplastid RNA editing: a proposal. Protist 161:2–6

    Article  CAS  PubMed  Google Scholar 

  • Sinha KM, Hines JC, Ray DS (2006) Cell cycle-dependent localization and properties of a second mitochondrial DNA ligase in Crithidia fasciculata. Eukaryot Cell 5:54–61

    Article  CAS  PubMed  Google Scholar 

  • Speijer D (2008) Evolutionary aspects of RNA editing. In: Goringer HU (ed) RNA editing. Springer, Berlin, pp 199–229

    Chapter  Google Scholar 

  • Stuart K, Allen TE, Heidmann S, Seiwert SD (1997) RNA editing in kinetoplastid protozoa. Microbiol Mol Biol Rev 61:105–120

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sturm NR, Simpson L (1990) Kinetoplast DNA minicircles encode guide RNAs for editing of cytochrome oxidase subunit III mRNA. Cell 61:879–884

    Article  CAS  PubMed  Google Scholar 

  • Thiemann OH, Maslov DA, Simpson L (1994) Disruption of RNA editing in Leishmania tarentolae by the loss of minicircle-encoded guide RNA genes. EMBO J 13:5689–5700

    CAS  PubMed  Google Scholar 

  • Torri AF, Englund PT (1995) A DNA polymerace β in the mitochondrion of the trypanosomatid Crithidia fasciculata. J Biol Chem 270:3495–3497

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • van Weelden SW, van Hellemond JJ, Opperdoes FR, Tielens AG (2005) New functions for parts of the Krebs cycle in procyclic Trypanosoma brucei, a cycle not operating as a cycle. J Biol Chem 280:12451–12460

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vondrušková E, van den Burg J, Zíková A, Ernst NL, Stuart K, Benne R, Lukeš J (2005) RNA interference analyses suggest a transcript-specific regulatory role for MRP1 and MRP2 in RNA editing and other RNA processing in Trypanosoma brucei. J Biol Chem 280:2429–2438

    Article  PubMed  CAS  Google Scholar 

  • Wang Z, Englund PT (2001) RNA interference of a trypanosome topoisomerase II causes progressive loss of mitochondrial DNA. EMBO J 20:4674–4683

    Article  CAS  PubMed  Google Scholar 

  • Weng J, Aphasizheva I, Etheridge RD, Huang L, Wang X, Falick AM, Aphasizhev R (2008) Guide RNA-binding complex from mitochondria of trypanosomatids. Mol Cell 32:1–12

    Article  CAS  Google Scholar 

  • Wohlgamuth-Benedum JM, Rubio MAT, Paris Z, Long S, Poliak P, Lukeš J, Alfonzo JD (2009) Thiolation controls cytoplasmic tRNA stability and acts as a negative determinant for tRNA editing in mitochondria. J Biol Chem 284:23947–23953

    Article  CAS  PubMed  Google Scholar 

  • Woodward R, Gull K (1990) Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J Cell Sci 95:49–57

    PubMed  Google Scholar 

  • Zhao Z, Lindsay ME, Roy Chowdhury A, Robinson DR, Englund PT (2008) p166, a link between the trypanosome mitochondrial DNA and flagellum, mediates genome segregation. EMBO J 27:143–154

    Article  CAS  PubMed  Google Scholar 

  • Ziemann H (1898) Eine Methode der Doppelfarbung bei Flagellaten, Pilzen, Spirillen und Bakterien, sowie bei einigen Amoben. Zentralbl Bakt Parasitenkd Infekt 24:945–955

    Google Scholar 

  • Zíková A, Panigrahi AK, Dalley RA, Acestor N, Anupama A, Ogata Y, Myler PJ, Stuart K (2008a) Trypanosoma brucei mitochondrial ribosomes: affinity purification and component identification by mass spectrometry. Mol Cell Proteomics 7:1286–1296

    Article  PubMed  CAS  Google Scholar 

  • Zíková A, Kopečná J, Schumacher MA, Stuart KD, Trantírek L, Lukeš J (2008b) Structure and function of the native and recombinant mitochondrial MRP1/MRP2 complex from Trypanosoma brucei. Int J Parasitol 38:901–912

    Article  PubMed  CAS  Google Scholar 

  • Zíková A, Schnaufer A, Dalley RA, Panigrahi AK, Stuart KD (2009) The F0F1-ATP synthase complex contains novel subunits and is essential for procyclic Trypanosoma brucei. PLoS Pathog 5:e1000436

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Julius Lukeš .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Lukeš, J., Hashimi, H., Verner, Z., Čičová, Z. (2010). The Remarkable Mitochondrion of Trypanosomes and Related Flagellates. In: de Souza, W. (eds) Structures and Organelles in Pathogenic Protists. Microbiology Monographs, vol 17. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-12863-9_10

Download citation

Publish with us

Policies and ethics