Advertisement

Mitochondrial Translation in Trypanosomatids

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

Abstract

For a long period of time, the functional properties and the very existence of mitochondrial translation in trypanosomatids remained controversial. The unusual resistance of the system to the known inhibitors of translation, such as chloramphenicol, in conjunction with the extreme hydrophobicity of the translation products appeared to be the main factors that made detection and characterization of this system so difficult. As of today, only two mitochondrial translation products have been reliably identified in Leishmania tarentolae and Trypanosoma brucei: cytochrome c oxidase subunit I (COI) and apocytochrome b (Cyb) that are encoded by nonedited and 5′-edited mRNAs, respectively. A large body of circumstantial evidence suggests that the F1F0 ATPase subunit A6 and ribosomal protein S12 are also expressed in trypanosomatid mitochondria. The issue of existence of kinetoplast-mitochondrial ribosomes has been addressed lately by the isolation of the 50S monosome particles and reconstruction of their 3D-structure using single-particle cryo-electron microscopy. The overall architecture of these particles strikingly resembles that of eubacterial ribosomes, despite profound differences in the size of ribosomal RNAs and the protein content of these two classes of ribosomes. Evidence begins to accumulate that in order to selectively achieve translation of the fully edited mRNA templates the mitoribosomes are involved in higher-order interactions with mRNA editing and polyadenylation machineries. The pentatricopeptide repeat (PPR) proteins emerge as important participants in these interactions.

Keywords

Cryo-electron microscopy Leishmania tarentolae Mitochondrial translation Mitoribosome Pentatricopeptide repeat (PPR) proteins RNA editing Trypanosoma brucei 

Notes

Acknowledgments

The work in the authors’ laboratories has been supported by National Institutes of Health grants AI088292 (to DAM) and GM61576 (to RKA). We thank R. Aphasizhev and L. Simpson for the critical comments on the manuscript.

References

  1. Agrawal RK, Sharma MR, Yassin A, Lahiri I, Spremulli LL (2011) Structure and function of organellar ribosomes as revealed by cryo-EM. In: Rodnina M, Wintermeyer W, Green R (eds) Ribosomes: structure, function, and dynamics. Springer Wien, New York, pp 83–96Google Scholar
  2. Alfonzo JD, Soll D (2009) Mitochondrial tRNA import—the challenge to understand has just begun. Biol Chem 390:717–722PubMedCrossRefGoogle Scholar
  3. Alfonzo JD, Blanc V, Estevez AM, Rubio MA, Simpson L (1999) C to U editing of the anticodon of imported mitochondrial tRNA(Trp) allows decoding of the UGA stop codon in Leishmania tarentolae. EMBO J 18:7056–7062PubMedCrossRefGoogle Scholar
  4. Aphasizheva I, Maslov DA, Wang X, Huang L, Aphasizhev R (2011) Pentatricopeptide repeat proteins stimulate mRNA adenylation/uridylation to activate mitochondrial translation in trypanosomes. Mol Cell 42:106–117PubMedCrossRefGoogle Scholar
  5. Arts GJ, Van der Spek H, Speijer D, Van den Burg J, Van Steeg H, Sloof P, Benne R (1993) Implications of novel guide RNA features for the mechanism of RNA editing in Crithidia fasciculata. EMBO J 12:1523–1532PubMedGoogle Scholar
  6. Attardi G, Ojala D (1971) Mitochondrial ribosomes in HeLa cells. Nature 229:133–135CrossRefGoogle Scholar
  7. Benne R, Van den Burg J, Brakenhoff J, Sloof P, Van Boom J, Tromp M (1986) Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell 46:819–826PubMedCrossRefGoogle Scholar
  8. Berry EA, Guergova-Kuras M, Huang LS, Crofts AR (2000) Structure and function of cytochrome bc complexes. Annu Rev Biochem 69:1005–1075PubMedCrossRefGoogle Scholar
  9. Bhat GJ, Koslowsky DJ, Feagin JE, Smiley BL, Stuart K (1990) An extensively edited mitochondrial transcript in kinetoplastids encodes a protein homologous to ATPase subunit 6. Cell 61:885–894PubMedCrossRefGoogle Scholar
  10. Bhat GJ, Myler PJ, Stuart K (1991) The two ATPase 6 mRNAs of Leishmania tarentolae differ at their 3′ ends. Mol Biochem Parasitol 48:139–150PubMedCrossRefGoogle Scholar
  11. Bhat GJ, Souza AE, Feagin JE, Stuart K (1992) Transcript-specific developmental regulation of polyadenylation in Trypanosoma brucei mitochondria. Mol Biochem Parasitol 52:231–240PubMedCrossRefGoogle Scholar
  12. 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 60:189–198PubMedCrossRefGoogle Scholar
  13. Borst P, Grivell LA (1971) Mitochondrial ribosomes. FEBS Lett 13:73–88PubMedCrossRefGoogle Scholar
  14. Breek CK, Speijer D, Dekker H, Muijsers AO, Benne R (1997) Further evidence for the presence of mitochondrially encoded subunits in cytochrome c oxidase of the trypanosomatid Crithidia fasciculata. Biol Chem 378:837–841PubMedCrossRefGoogle Scholar
  15. Brega A, Vesco C (1971) Ribonucleoprotein particles involved in HeLa mitochondrial protein synthesis. Nature 229:136–139CrossRefGoogle Scholar
  16. Campbell DA, Thomas S, Sturm NR (2003) Transcription in kinetoplastid protozoa: why be normal? Microbes Infect 5:1231–1240PubMedCrossRefGoogle Scholar
  17. Čermáková P, Verner Z, Man P, Lukeš J, Horváth A (2007) Characterization of the NADH:ubiquinone oxidoreductase (complex I) in the trypanosomatid Phytomonas serpens (Kinetoplastida). FEBS J 274:3150–3158PubMedCrossRefGoogle Scholar
  18. Chang KP (1974) Ultrastructure of symbiotic bacteria in normal and antibiotic-treated Blastocrithidia culicis and Crithidia oncopelti. J Protozool 21:699–707PubMedGoogle Scholar
  19. Corell RA, Myler P, Stuart K (1994) Trypanosoma brucei mitochondrial CR4 gene encodes an extensively edited mRNA with completely edited sequence only in bloodstream forms. Mol Biochem Parasitol 64:65–74PubMedCrossRefGoogle Scholar
  20. Cristodero M, Seebeck T, Schneider A (2010) Mitochondrial translation is essential in bloodstream forms of Trypanosoma brucei. Mol Microbiol 78:757–769PubMedCrossRefGoogle Scholar
  21. Curgy J-J (1985) The mitoribosomes. Biol Cell 54:1–38PubMedCrossRefGoogle Scholar
  22. de la Cruz V, Lake JA, Simpson AM, Simpson L (1985a) A minimal ribosomal RNA: sequence and secondary structure of the 9S kinetoplast ribosomal RNA from Leishmania tarentolae. Proc Natl Acad Sci USA 82:1401–1405PubMedCrossRefGoogle Scholar
  23. de la Cruz V, Simpson A, Lake J, Simpson L (1985b) Primary sequence and partial secondary structure of the 12S kinetoplast (mitochondrial) ribosomal RNA from Leishmania tarentolae: conservation of peptidyl-transferase structural elements. Nucleic Acids Res 13:2337–2356PubMedCrossRefGoogle Scholar
  24. Delannoy E, Stanley WA, Bond CS, Small ID (2007) Pentatricopeptide repeat (PPR) proteins as sequence-specificity factors in post-transcriptional processes in organelles. Biochem Soc Trans 35:1643–1647PubMedCrossRefGoogle Scholar
  25. Dunstan HM, Green-Willms NS, Fox TD (1997) In vivo analysis of Saccharomyces cerevisiae COX2 mRNA 5′-untranslated leader functions in mitochondrial translation initiation and translational activation. Genetics 147:87–100PubMedGoogle Scholar
  26. Eperon I, Janssen J, Hoeijmakers J, Borst P (1983) The major transcripts of the kinetoplast DNA of T. brucei are very small ribosomal RNAs. Nucleic Acids Res 11:105–125PubMedCrossRefGoogle Scholar
  27. 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 27:1596–1608PubMedCrossRefGoogle Scholar
  28. Fang J, Wang YD, Beattie DS (2001) Isolation and characterization of complex I, rotenone-sensitive NADH:ubiquinone oxidoreductase, from the procyclic forms of Trypanosoma brucei. Eur J Biochem 268:3075–3082PubMedCrossRefGoogle Scholar
  29. Feagin JE (2000) Mitochondrial genome diversity in parasites. Int J Parasitol 30:371–390PubMedCrossRefGoogle Scholar
  30. Feagin JE, Shaw JM, Simpson L, Stuart K (1988) Creation of AUG initiation codons by addition of uridines within cytochrome b transcripts of kinetoplastids. Proc Natl Acad Sci USA 85:539–543PubMedCrossRefGoogle Scholar
  31. Fox TD (1996) Genetics of mitochondrial translation. In: Hershey JWB, Matthews MB, Sonnenberg N (eds) Translational control. Cold Spring Harbor, New York, pp 733–758Google Scholar
  32. Gabashvili IS, Agrawal RK, Spahn CM, Grassucci RA, Svergun DI, Frank J, Penczek P (2000) Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100:537–549PubMedCrossRefGoogle Scholar
  33. Gao GG, Kapushoc ST, Simpson AM, Thiemann OH, Simpson L (2001) Guide RNAs of the recently isolated LEM125 strain of Leishmania tarentolae: an unexpected complexity. RNA Publ RNA Soc 7:1335–1347Google Scholar
  34. Gaston KW, Rubio MA, Spears JL, Pastar I, Papavasiliou FN, Alfonzo JD (2007) C to U editing at position 32 of the anticodon loop precedes tRNA 5′ leader removal in trypanosomatids. Nucleic Acids Res 35:6740–6749PubMedCrossRefGoogle Scholar
  35. Goswami S, Dhar G, Mukherjee S, Mahata B, Chatterjee S, Home P, Adhya S (2006) A bifunctional tRNA import receptor from Leishmania mitochondria. Proc Natl Acad Sci USA 103:8354–8359PubMedCrossRefGoogle Scholar
  36. Greco M, Cantatore P, Pepe G, Saccone C (1973) Isolation and characterization of rat-liver mitochondrial ribosomes highly active in poly(U)-directed polyphenylalanine synthesis. Eur J Biochem 37:171–177PubMedCrossRefGoogle Scholar
  37. Green-Willms NS, Fox TD, Costanzo MC (1998) Functional interactions between yeast mitochondrial ribosomes and mRNA 5′ untranslated leaders. Mol Cell Biol 18:1826–1834PubMedGoogle Scholar
  38. Green-Willms NS, Butler CA, Dunstan HM, Fox TD (2001) Pet111p, an inner membrane-bound translational activator that limits expression of the Saccharomyces cerevisiae mitochondrial gene COX2. J Biol Chem 276:6392–6397PubMedCrossRefGoogle Scholar
  39. Gruschke S, Ott M (2010) The polypeptide tunnel exit of the mitochondrial ribosome is tailored to meet the specific requirements of the organelle. Bioessays 32:1050–1057PubMedCrossRefGoogle Scholar
  40. Hanas J, Linden G, Stuart K (1975) Mitochondrial and cytoplasmic ribosomes and their activity in blood and culture form Trypanosoma brucei. J Cell Biol 65:103–111PubMedCrossRefGoogle Scholar
  41. Hancock K, Hajduk SL (1990) The mitochondrial tRNAs of Trypanosoma brucei are nuclear encoded. J Biol Chem 265:19208–19215PubMedGoogle Scholar
  42. Hashimi H, Benkovičová V, Čermáková P, Lai DH, Horváth A, Lukeš J (2010) The assembly of F1F0-ATP synthase is disrupted upon interference of RNA editing in Trypanosoma brucei. Int J Parasitol 40:45–54PubMedCrossRefGoogle Scholar
  43. Herrmann JM, Neupert W (2003) Protein insertion into the inner membrane of mitochondria. IUBMB Life 55:219–225PubMedCrossRefGoogle Scholar
  44. Hill RC, Morris CA, Weber MM (1975) Chloramphenicol resistant mitochondrial protein synthesis in Crithidia fasciculata. Arch Biochem Biophys 170:392–399PubMedCrossRefGoogle Scholar
  45. Horváth A, Berry EA, Maslov DA (2000a) Translation of the edited mRNA for cytochrome b in trypanosome mitochondria. Science 287:1639–1640PubMedCrossRefGoogle Scholar
  46. Horváth A, Kingan TG, Maslov DA (2000b) Detection of the mitochondrially encoded cytochrome c oxidase subunit I in the trypanosomatid protozoan Leishmania tarentolae. J Biol Chem 275:17160–17165PubMedCrossRefGoogle Scholar
  47. Horváth A, Neboháčová M, Lukeš J, Maslov DA (2002) Unusual polypeptide synthesis in the kinetoplast-mitochondria from Leishmania tarentolae. Identification of individual de novo translation products. J Biol Chem 277:7222–7230PubMedCrossRefGoogle Scholar
  48. Kleisen CM, Borst P (1975) Are 50% of all cellular proteins synthesized on mitochondrial ribosomes in Crithidia luciliae? Biochim Biophys Acta 390:78–81PubMedCrossRefGoogle Scholar
  49. Krause K, de Lopes SR, Roberts DG, Dieckmann CL (2004) The mitochondrial message-specific mRNA protectors Cbp1 and Pet309 are associated in a high-molecular weight complex. Mol Biol Cell 15:2674–2683PubMedCrossRefGoogle Scholar
  50. Lamb AJ, Clark-Walker GD, Linnane AW (1968) The biogenesis of mitochondria. 4. The differentiation of mitochondrial and cytoplasmic protein synthesizing systems in vitro by antibiotics. Biochim Biophys Acta 161:415–427PubMedCrossRefGoogle Scholar
  51. Laub-Kuperszteijn R, Thirion J (1974) Existence of two distinct protein synthesis systems in the trypanosomatid Crithidia luciliae. Biochim Biophys Acta 340:314–322CrossRefGoogle Scholar
  52. Lightowlers RN, Chrzanowska-Lightowlers ZM (2008) PPR (pentatricopeptide repeat) proteins in mammals: important aids to mitochondrial gene expression. Biochem J 416:e5–e6PubMedCrossRefGoogle Scholar
  53. Ludwig B, Bender E, Arnold S, Hüttemann M, Lee I, Kadenbach B (2001) Cytochrome c oxidase and the regulation of oxidative phosphorylation. Chembiochem 2:403CrossRefGoogle Scholar
  54. Maarouf M, Lawrence F, Croft SL, Robert-Gero M (1995) Ribosomes of Leishmania are a target for the aminoglycosides. Parasitol Res 81:421–425PubMedCrossRefGoogle Scholar
  55. Marres CAM, Slater EC (1977) Polypeptide composition of purified QH2:cytochrome c oxidoreductase from beef-heart mitochondria. Biochim Biophys Acta 462:531–548PubMedCrossRefGoogle Scholar
  56. Maslov DA (2010) Complete set of mitochondrial pan-edited mRNAs in Leishmania mexicana amazonensis LV78. Mol Biochem Parasitol 173:107–114PubMedCrossRefGoogle Scholar
  57. 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 70:459–467PubMedCrossRefGoogle Scholar
  58. Maslov DA, Sturm NR, Niner BM, Gruszynski ES, Peris M, Simpson L (1992) An intergenic G-rich region in Leishmania tarentolae kinetoplast maxicircle DNA is a pan-edited cryptogene encoding ribosomal protein S12. Mol Cell Biol 12:56–67PubMedGoogle Scholar
  59. Maslov DA, Nawathean P, Scheel J (1999) Partial kinetoplast-mitochondrial gene organization and expression in the respiratory deficient plant trypanosomatid Phytomonas serpens. Mol Biochem Parasitol 99:207–221PubMedCrossRefGoogle Scholar
  60. 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 148:69–78PubMedCrossRefGoogle Scholar
  61. Maslov DA, Spremulli LL, Sharma MR, Bhargava K, Grasso D, Falick AM, Agrawal RK, Parker CE, Simpson L (2007) Proteomics and electron microscopic characterization of the unusual mitochondrial ribosome-related 45S complex in Leishmania tarentolae. Mol Biochem Parasitol 152:203–212PubMedCrossRefGoogle Scholar
  62. McLean JR, Cohn GL, Brandt IK, Simpson MV (1958) Incorporation of labeled amino acids into the protein of muscle and liver mitochondria. J Biol Chem 233:657–663PubMedGoogle Scholar
  63. Mears JA, Cannone JJ, Stagg SM, Gutell RR, Agrawal RK, Harvey SC (2002) Modeling a minimal ribosome based on comparative sequence analysis. J Mol Biol 321:215–234PubMedCrossRefGoogle Scholar
  64. Mears JA, Sharma MR, Gutell RR, McCook AS, Richardson PE, Caulfield TR, Agrawal RK, Harvey SC (2006) A structural model for the large subunit of the mammalian mitochondrial ribosome. J Mol Biol 358:193–212PubMedCrossRefGoogle Scholar
  65. Militello KT, Read LK (1999) Coordination of kRNA editing and polyadenylation in Trypanosoma brucei mitochondria: complete editing is not required for long poly(A) tract addition. Nucleic Acids Res 27:1377–1385PubMedCrossRefGoogle Scholar
  66. Mingler MK, Hingst AM, Clement SL, Yu LE, Reifur L, Koslowsky DJ (2006) Identification of pentatricopeptide repeat proteins in Trypanosoma brucei. Mol Biochem Parasitol 150:37–45PubMedCrossRefGoogle Scholar
  67. Moazed D, Robertson JM, Noller HF (1988) Interaction of elongation factors EF-G and EF-Tu with a conserved loop in 23S RNA. Nature 334:362–364PubMedCrossRefGoogle Scholar
  68. 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 8:589–595PubMedCrossRefGoogle Scholar
  69. Mulkidjanian AY, Makarova KS, Galperin MY, Koonin EV (2007) Inventing the dynamo machine: the evolution of the F-type and V-type ATPases. Nat Rev Microbiol 5:892–899PubMedCrossRefGoogle Scholar
  70. Nabholz CE, Speijer D, Schneider A (1999) Chloramphenicol-sensitive mitochondrial translation in Trypanosoma brucei. Parasitol Res 85:779–782PubMedCrossRefGoogle Scholar
  71. Naithani S, Saracco SA, Butler CA, Fox TD (2003) Interactions among COX1, COX2, and COX3 mRNA-specific translational activator proteins on the inner surface of the mitochondrial inner membrane of Saccharomyces cerevisiae. Mol Biol Cell 14:324–333PubMedCrossRefGoogle Scholar
  72. Neboháčová M, Maslov DA, Falick AM, Simpson L (2004) The effect of RNA interference Down-regulation of RNA editing 3′-terminal uridylyl transferase (TUTase) 1 on mitochondrial de novo protein synthesis and stability of respiratory complexes in Trypanosoma brucei. J Biol Chem 279:7819–7825PubMedCrossRefGoogle Scholar
  73. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA (2000) The structural basis of ribosome activity in peptide bond synthesis. Science 289:920–930PubMedCrossRefGoogle Scholar
  74. O’Brien TW (2002) Evolution of a protein-rich mitochondrial ribosome: implications for human genetic disease. Gene 286:73–79PubMedCrossRefGoogle Scholar
  75. O’Brien TW (2003) Properties of human mitochondrial ribosomes. IUBMB Life 55:505–513PubMedCrossRefGoogle Scholar
  76. O’Brien TW, Denslow ND (1996) Bovine mitochondrial ribosomes. In: Attardi GM, Chomyn A (eds) Methods in enzymology, vol 264. Academic Press, San Diego, pp 237–248Google Scholar
  77. O’Brien TW, Kalf GF (1967a) Ribosomes from rat liver mitochondria. II. Partial characterization. J Biol Chem 242:2180–2185PubMedGoogle Scholar
  78. O’Brien TW, Kalf GF (1967b) Ribosomes from rat liver mitochondria. I. Isolation procedure and contamination studies. J Biol Chem 242:2172–2179PubMedGoogle Scholar
  79. Ochsenreiter T, Hajduk SL (2006) Alternative editing of cytochrome c oxidase III mRNA in trypanosome mitochondria generates protein diversity. EMBO Rep 7:1128–1133PubMedCrossRefGoogle Scholar
  80. Ochsenreiter T, Cipriano M, Hajduk SL (2008) Alternative mRNA editing in trypanosomes is extensive and may contribute to mitochondrial protein diversity. PLoS One 3:e1566PubMedCrossRefGoogle Scholar
  81. Opperdoes FR, Michels PA (2008) Complex I of Trypanosomatidae: does it exist? Trends Parasitol 24(7):310–317PubMedCrossRefGoogle Scholar
  82. Ott M, Herrmann JM (2010) Co-translational membrane insertion of mitochondrially encoded proteins. Biochim Biophys Acta 1803:767–775PubMedCrossRefGoogle Scholar
  83. Ott M, Prestele M, Bauerschmitt H, Funes S, Bonnefoy N, Herrmann JM (2006) Mba1, a membrane-associated ribosome receptor in mitochondria. EMBO J 25:1603–1610PubMedCrossRefGoogle Scholar
  84. Pel HJ, Grivell LA (1994) Protein synthesis in mitochondria. Mol Biol Rep 19:183–194PubMedCrossRefGoogle Scholar
  85. Pietromonaco SF, Denslow ND, O’Brien TW (1991) Proteins of mammalian mitochondrial ribosomes. Biochimie 73:827–836PubMedCrossRefGoogle Scholar
  86. Priest JW, Hajduk SL (1992) Cytochrome c reductase purified from Crithidia fasciculata contains an atypical cytochrome c 1. J Biol Chem 267:20188–20195PubMedGoogle Scholar
  87. Pusnik M, Small I, Read LK, Fabbro T, Schneider A (2007) Pentatricopeptide repeat proteins in Trypanosoma brucei function in mitochondrial ribosomes. Mol Cell Biol 27:6876–6888PubMedCrossRefGoogle Scholar
  88. Read LK, Myler PJ, Stuart K (1992) Extensive editing of both processed and preprocessed maxicircle CR6 transcripts in Trypanosoma brucei. J Biol Chem 267:1123–1128PubMedGoogle Scholar
  89. Read LK, Stankey KA, Fish WR, Muthiani AM, Stuart K (1994a) Developmental regulation of RNA editing and polyadenylation in four life cycle stages of Trypanosoma congolense. Mol Biochem Parasitol 68:297–306PubMedCrossRefGoogle Scholar
  90. Read LK, Wilson KD, Myler PJ, Stuart K (1994b) Editing of Trypanosoma brucei maxicircle CR5 mRNA generates variable carboxy terminal predicted protein sequences. Nucleic Acids Res 22:1489–1495PubMedCrossRefGoogle Scholar
  91. Remacle C, Barbieri MR, Cardol P, Hamel PP (2008) Eukaryotic complex I: functional diversity and experimental systems to unravel the assembly process. Mol Genet Genomics 280:93–110PubMedCrossRefGoogle Scholar
  92. Richterová L, VávrováZ Z, Lukeš J (2011) DEAD-box RNA helicase is dispensable for mitochondrial translation in Trypanosoma brucei. Exp Parasitol 127:300–303PubMedCrossRefGoogle Scholar
  93. Sanchirico ME, Fox TD, Mason TL (1998) Accumulation of mitochondrially synthesized Saccharomyces cerevisiae Cox2p and Cox3p depends on targeting information in untranslated portions of their mRNAs. EMBO J 17:5796–5804PubMedCrossRefGoogle Scholar
  94. Scheinman A, Aguinaldo A-M, Simpson AM, Peris M, Shankweiler G, Simpson L, Lake JA (1993) Reconstitution of a minimal small ribosomal subunit. In: Nierhaus K (ed) The translation apparatus. Plenum Press, New York, pp 719–726CrossRefGoogle Scholar
  95. Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670PubMedCrossRefGoogle Scholar
  96. Schnaufer A, Sbicego S, Blum B (2000) Antimycin A resistance in a mutant Leishmania tarentolae strain is correlated to a point mutation in the mitochondrial apocytochrome b gene. Curr Genet 37:234–241PubMedCrossRefGoogle Scholar
  97. Schnaufer A, Clark-Walker GD, Steinberg AG, Stuart K (2005) The F1-ATP synthase complex in bloodstream stage trypanosomes has an unusual and essential function. EMBO J 24:4029–4040PubMedCrossRefGoogle Scholar
  98. Schneider A, Martin J, Agabian N (1994) A nuclear encoded tRNA of Trypanosoma brucei is imported into mitochondria. Mol Cell Biol 14:2317–2322PubMedCrossRefGoogle Scholar
  99. Sharma MR, Koc EC, Datta PP, Booth TM, Spremulli LL, Agrawal RK (2003) Structure of the mammalian mitochondrial ribosome reveals an expanded functional role for its component proteins. Cell 115:97–108PubMedCrossRefGoogle Scholar
  100. Sharma MR, Booth TM, Simpson L, Maslov DA, Agrawal RK (2009) Structure of a mitochondrial ribosome with minimal RNA. Proc Natl Acad Sci USA 106:9637–9642PubMedCrossRefGoogle Scholar
  101. Shaw J, Feagin JE, Stuart K, Simpson L (1988) Editing of mitochondrial mRNAs by uridine addition and deletion generates conserved amino acid sequences and AUG initiation codons. Cell 53:401–411PubMedCrossRefGoogle Scholar
  102. Shaw J, Campbell D, Simpson L (1989) Internal frameshifts within the mitochondrial genes for cytochrome oxidase subunit II and maxicircle unidentified reading frame 3 in Leishmania tarentolae are corrected by RNA editing: evidence for translation of the edited cytochrome oxidase subunit II mRNA. Proc Natl Acad Sci USA 86:6220–6224PubMedCrossRefGoogle Scholar
  103. Shi X, Chen D-HT, Suyama Y (1994) A nuclear tRNA gene cluster in the protozoan Leishmania tarentolae and differential distribution of nuclear-encoded tRNAs between the cytosol and mitochondria. Mol Biochem Parasitol 65:23–37PubMedCrossRefGoogle Scholar
  104. Shu HH, Göringer HU (1998) Trypanosoma brucei mitochondrial ribonucleoprotein complexes which contain 12S and 9S ribosomal RNAs. Parasitology 116:157–164PubMedCrossRefGoogle Scholar
  105. Siep M, van Oosterum K, Neufeglise H, Van der Spek H, Grivell LA (2000) Mss51p, a putative translational activator of cytochrome c oxidase subunit-1 (COX1) mRNA, is required for synthesis of Cox1p in Saccharomyces cerevisiae. Curr Genet 37:213–220PubMedCrossRefGoogle Scholar
  106. Simpson AM, Suyama Y, Dewes H, Campbell D, Simpson L (1989) Kinetoplastid mitochondria contain functional tRNAs which are encoded in nuclear DNA and also small minicircle and maxicircle transcripts of unknown function. Nucleic Acids Res 17:5427–5445PubMedCrossRefGoogle Scholar
  107. Simpson L, Wang SH, Thiemann OH, Alfonzo JD, Maslov DA, Avila HA (1998) U-insertion/deletion Edited Sequence Database. Nucleic Acids Res 26:170–176PubMedCrossRefGoogle Scholar
  108. Simpson L, Thiemann OH, Savill NJ, Alfonzo JD, Maslov DA (2000) Evolution of RNA editing in trypanosome mitochondria. Proc Natl Acad Sci USA 97:6986–6993PubMedCrossRefGoogle Scholar
  109. Smits P, Smeitink JA, Van den Heuvel LP, Huynen MA, Ettema TJ (2007) Reconstructing the evolution of the mitochondrial ribosomal proteome. Nucleic Acids Res 35:4686–4703PubMedCrossRefGoogle Scholar
  110. Speijer D, Muijsers AO, Dekker H, De Haan A, Breek CKD, Albracht SPJ, Benne R (1996) Purification and characterization of cytochrome c oxidase from the insect trypanosomatid Crithidia fasciculata. Mol Biochem Parasitol 79:47–59PubMedCrossRefGoogle Scholar
  111. Speijer D, Breek CKD, Muijsers AO, Hartog AF, Berden JA, Albracht SPJ, Samyn B, Van Beeumen J, Benne R (1997) Characterization of the respiratory chain from cultured Crithidia fasciculata. Mol Biochem Parasitol 85:171–186PubMedCrossRefGoogle Scholar
  112. Spithill T, Shimer S, Hill G (1981) Inhibitory effects of chloramphenicol isomers and other antibiotics on protein synthesis and respiration in procyclic Trypanosoma brucei brucei. Mol Biochem Parasitol 2:235–256PubMedCrossRefGoogle Scholar
  113. Spremulli LL, Coursey A, Navratil T, Hunter SE (2004) Initiation and elongation factors in mammalian mitochondrial protein biosynthesis. Prog Nucleic Acid Res Mol Biol 77:211–261PubMedCrossRefGoogle Scholar
  114. Stuart R (2002) Insertion of proteins into the inner membrane of mitochondria: the role of the Oxa1 complex. Biochim Biophys Acta 1592:79–87PubMedCrossRefGoogle Scholar
  115. Stuart K, Feagin JE (1992) Mitochondrial DNA of kinetoplastids. Int Rev Cytol 141:65–88PubMedCrossRefGoogle Scholar
  116. Tan TH, Bochud-Allemann N, Horn EK, Schneider A (2002) Eukaryotic-type elongator tRNAMet of Trypanosoma brucei becomes formylated after import into mitochondria. Proc Natl Acad Sci USA 99:1152–1157PubMedCrossRefGoogle Scholar
  117. Tittawella I (1998) Protein synthesis in mitochondria isolated from the trypanosomatid protozoan Crithidia fasciculata. FEBS Lett 423:351–356PubMedCrossRefGoogle Scholar
  118. Tittawella I, Yasmin L, Baranov V (2003) Mitochondrial ribosomes in a trypanosome. Biochem Biophys Res Commun 307:578–583PubMedCrossRefGoogle Scholar
  119. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, Noller HF (2001) Crystal structure of the ribosome at 5.5 Å resolution. Science 292:883–896PubMedCrossRefGoogle Scholar
  120. Zaitseva GN, Kolesnikov AA, Shirshov AT (1977) The genetic system of kinetoplasts in trypanosomatids. Mol Cell Biochem 14:47–54PubMedCrossRefGoogle Scholar
  121. Zíková A, Panigrahi AK, Dalley RA, Acestor N, Anupama A, Ogata Y, Myler PJ, Stuart KD (2008) Trypanosoma brucei mitochondrial ribosomes: affinity purification and component identification by mass spectrometry. Mol Cell Proteomics 7:1286–1296PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of California—RiversideRiversideUSA
  2. 2.Division of Translational MedicineWadsworth Center, New York State Department of HealthAlbanyUSA

Personalised recommendations