Abstract
Several genes of the Trypanosoma brucei mitochondrial genome (the maxicircle) encode mRNAs that are so extensively altered by RNA editing that the gene cannot be identified by analysis of the DNA sequence. The 322-nucleotide preedited RNA of one of these genes, CR2, is converted into a 647-nucleotide transcript by the addition of 345 uridines and the deletion of 20 genomically encoded uridines. The fully edited transcript has an open reading frame that predicts a 194-amino-acid protein. This protein, which we name ND9 (NADH dehydrogenase subunit 9), has homology to a subunit of NADH dehydrogenase (respiratory complex I). Seven guide RNAs that can specify edited CR2 sequence have been identified. Steady-state levels of unedited ND9 transcripts are greater in bloodstream than in procyclic forms, but edited ND9 mRNA is present in similar abundance in both life cycle stages.
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- Bairoch A. PROSITE: a dictionary of sites and patterns in proteins. Nucleic Acids Res. 1991 Apr 25;19 (Suppl):2241–2245. doi: 10.1093/nar/19.suppl.2241. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barrois M., Riou G., Galibert F. Complete nucleotide sequence of minicircle kinetoplast DNA from Trypanosoma equiperdum. Proc Natl Acad Sci U S A. 1981 Jun;78(6):3323–3327. doi: 10.1073/pnas.78.6.3323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bass K. E., Wang C. C. The in vitro differentiation of pleomorphic Trypanosoma brucei from bloodstream into procyclic form requires neither intermediary nor short-stumpy stage. Mol Biochem Parasitol. 1991 Feb;44(2):261–270. doi: 10.1016/0166-6851(91)90012-u. [DOI] [PubMed] [Google Scholar]
- Bennoun P. Evidence for a respiratory chain in the chloroplast. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4352–4356. doi: 10.1073/pnas.79.14.4352. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bhat G. J., Koslowsky D. J., Feagin J. E., Smiley B. L., Stuart K. An extensively edited mitochondrial transcript in kinetoplastids encodes a protein homologous to ATPase subunit 6. Cell. 1990 Jun 1;61(5):885–894. doi: 10.1016/0092-8674(90)90199-o. [DOI] [PubMed] [Google Scholar]
- Bhat G. J., Myler P. J., Stuart K. The two ATPase 6 mRNAs of Leishmania tarentolae differ at their 3' ends. Mol Biochem Parasitol. 1991 Oct;48(2):139–149. doi: 10.1016/0166-6851(91)90110-r. [DOI] [PubMed] [Google Scholar]
- Bhat G. J., Souza A. E., Feagin J. E., Stuart K. Transcript-specific developmental regulation of polyadenylation in Trypanosoma brucei mitochondria. Mol Biochem Parasitol. 1992 Jun;52(2):231–240. doi: 10.1016/0166-6851(92)90055-o. [DOI] [PubMed] [Google Scholar]
- Bienen E. J., Saric M., Pollakis G., Grady R. W., Clarkson A. B., Jr Mitochondrial development in Trypanosoma brucei brucei transitional bloodstream forms. Mol Biochem Parasitol. 1991 Apr;45(2):185–192. doi: 10.1016/0166-6851(91)90085-k. [DOI] [PubMed] [Google Scholar]
- Böhm R., Sauter M., Böck A. Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol. 1990 Feb;4(2):231–243. doi: 10.1111/j.1365-2958.1990.tb00590.x. [DOI] [PubMed] [Google Scholar]
- Chen K. K., Donelson J. E. Sequences of two kinetoplast DNA minicircles of Tryptanosoma brucei. Proc Natl Acad Sci U S A. 1980 May;77(5):2445–2449. doi: 10.1073/pnas.77.5.2445. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Clarkson A. B., Jr, Bienen E. J., Pollakis G., Grady R. W. Respiration of bloodstream forms of the parasite Trypanosoma brucei brucei is dependent on a plant-like alternative oxidase. J Biol Chem. 1989 Oct 25;264(30):17770–17776. [PubMed] [Google Scholar]
- Decker C. J., Sollner-Webb B. RNA editing involves indiscriminate U changes throughout precisely defined editing domains. Cell. 1990 Jun 15;61(6):1001–1011. doi: 10.1016/0092-8674(90)90065-m. [DOI] [PubMed] [Google Scholar]
- Denicola-Seoane A., Rubbo H., Prodanov E., Turrens J. F. Succinate-dependent metabolism in Trypanosoma cruzi epimastigotes. Mol Biochem Parasitol. 1992 Aug;54(1):43–50. doi: 10.1016/0166-6851(92)90093-y. [DOI] [PubMed] [Google Scholar]
- Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Feagin J. E., Abraham J. M., Stuart K. Extensive editing of the cytochrome c oxidase III transcript in Trypanosoma brucei. Cell. 1988 May 6;53(3):413–422. doi: 10.1016/0092-8674(88)90161-4. [DOI] [PubMed] [Google Scholar]
- Feagin J. E., Jasmer D. P., Stuart K. Apocytochrome b and other mitochondrial DNA sequences are differentially expressed during the life cycle of Trypanosoma brucei. Nucleic Acids Res. 1985 Jun 25;13(12):4577–4596. doi: 10.1093/nar/13.12.4577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fearnley I. M., Runswick M. J., Walker J. E. A homologue of the nuclear coded 49 kd subunit of bovine mitochondrial NADH-ubiquinone reductase is coded in chloroplast DNA. EMBO J. 1989 Mar;8(3):665–672. doi: 10.1002/j.1460-2075.1989.tb03424.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Frohman M. A., Dush M. K., Martin G. R. Rapid production of full-length cDNAs from rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8998–9002. doi: 10.1073/pnas.85.23.8998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gajendran N., Vanhecke D., Songa E. B., Hamers R. Kinetoplast minicircle DNA of Trypanosoma evansi encode guide RNA genes. Nucleic Acids Res. 1992 Feb 11;20(3):614–614. doi: 10.1093/nar/20.3.614. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gribskov M., McLachlan A. D., Eisenberg D. Profile analysis: detection of distantly related proteins. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4355–4358. doi: 10.1073/pnas.84.13.4355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Higgins D. G., Bleasby A. J., Fuchs R. CLUSTAL V: improved software for multiple sequence alignment. Comput Appl Biosci. 1992 Apr;8(2):189–191. doi: 10.1093/bioinformatics/8.2.189. [DOI] [PubMed] [Google Scholar]
- Hiratsuka J., Shimada H., Whittier R., Ishibashi T., Sakamoto M., Mori M., Kondo C., Honji Y., Sun C. R., Meng B. Y. The complete sequence of the rice (Oryza sativa) chloroplast genome: intermolecular recombination between distinct tRNA genes accounts for a major plastid DNA inversion during the evolution of the cereals. Mol Gen Genet. 1989 Jun;217(2-3):185–194. doi: 10.1007/BF02464880. [DOI] [PubMed] [Google Scholar]
- Jasmer D. P., Feagin J. E., Payne M., Stuart K. Variation of G-rich mitochondrial transcripts among stocks of Trypanosoma brucei. Mol Biochem Parasitol. 1987 Jan 15;22(2-3):259–272. doi: 10.1016/0166-6851(87)90057-0. [DOI] [PubMed] [Google Scholar]
- Jasmer D. P., Stuart K. Conservation of kinetoplastid minicircle characteristics without nucleotide sequence conservation. Mol Biochem Parasitol. 1986 Mar;18(3):257–269. doi: 10.1016/0166-6851(86)90084-8. [DOI] [PubMed] [Google Scholar]
- Koslowsky D. J., Bhat G. J., Perrollaz A. L., Feagin J. E., Stuart K. The MURF3 gene of T. brucei contains multiple domains of extensive editing and is homologous to a subunit of NADH dehydrogenase. Cell. 1990 Sep 7;62(5):901–911. doi: 10.1016/0092-8674(90)90265-g. [DOI] [PubMed] [Google Scholar]
- Koslowsky D. J., Bhat G. J., Read L. K., Stuart K. Cycles of progressive realignment of gRNA with mRNA in RNA editing. Cell. 1991 Nov 1;67(3):537–546. doi: 10.1016/0092-8674(91)90528-7. [DOI] [PubMed] [Google Scholar]
- Koslowsky D. J., Riley G. R., Feagin J. E., Stuart K. Guide RNAs for transcripts with developmentally regulated RNA editing are present in both life cycle stages of Trypanosoma brucei. Mol Cell Biol. 1992 May;12(5):2043–2049. doi: 10.1128/mcb.12.5.2043. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Oda K., Yamato K., Ohta E., Nakamura Y., Takemura M., Nozato N., Akashi K., Kanegae T., Ogura Y., Kohchi T. Gene organization deduced from the complete sequence of liverwort Marchantia polymorpha mitochondrial DNA. A primitive form of plant mitochondrial genome. J Mol Biol. 1992 Jan 5;223(1):1–7. doi: 10.1016/0022-2836(92)90708-r. [DOI] [PubMed] [Google Scholar]
- Opperdoes F. R. Biochemical peculiarities of trypanosomes, African and South American. Br Med Bull. 1985 Apr;41(2):130–136. doi: 10.1093/oxfordjournals.bmb.a072039. [DOI] [PubMed] [Google Scholar]
- Ou Y. C., Giroud C., Baltz T. Kinetoplast DNA analysis of four Trypanosoma evansi strains. Mol Biochem Parasitol. 1991 May;46(1):97–102. doi: 10.1016/0166-6851(91)90203-i. [DOI] [PubMed] [Google Scholar]
- Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peterson G. C., Souza A. E., Parsons M. Characterization of a Trypanosoma brucei nuclear gene encoding a protein homologous to a subunit of bovine NADH:ubiquinone oxidoreductase (complex I). Mol Biochem Parasitol. 1993 Mar;58(1):63–70. doi: 10.1016/0166-6851(93)90091-b. [DOI] [PubMed] [Google Scholar]
- Pilkington S. J., Skehel J. M., Walker J. E. The 30-kilodalton subunit of bovine mitochondrial complex I is homologous to a protein coded in chloroplast DNA. Biochemistry. 1991 Feb 19;30(7):1901–1908. doi: 10.1021/bi00221a024. [DOI] [PubMed] [Google Scholar]
- Pollard V. W., Rohrer S. P., Michelotti E. F., Hancock K., Hajduk S. L. Organization of minicircle genes for guide RNAs in Trypanosoma brucei. Cell. 1990 Nov 16;63(4):783–790. doi: 10.1016/0092-8674(90)90144-4. [DOI] [PubMed] [Google Scholar]
- Pritchard A. E., Seilhamer J. J., Cummings D. J. Paramecium mitochondrial DNA sequences and RNA transcripts for cytochrome oxidase subunit I, URF1, and three ORFs adjacent to the replication origin. Gene. 1986;44(2-3):243–253. doi: 10.1016/0378-1119(86)90188-5. [DOI] [PubMed] [Google Scholar]
- Pritchard A. E., Seilhamer J. J., Mahalingam R., Sable C. L., Venuti S. E., Cummings D. J. Nucleotide sequence of the mitochondrial genome of Paramecium. Nucleic Acids Res. 1990 Jan 11;18(1):173–180. doi: 10.1093/nar/18.1.173. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pritchard A. E., Venuti S. E., Ghalambor M. A., Sable C. L., Cummings D. J. An unusual region of Paramecium mitochondrial DNA containing chloroplast-like genes. Gene. 1989 May 15;78(1):121–134. doi: 10.1016/0378-1119(89)90320-x. [DOI] [PubMed] [Google Scholar]
- Read L. K., Corell R. A., Stuart K. Chimeric and truncated RNAs in Trypanosoma brucei suggest transesterifications at non-consecutive sites during RNA editing. Nucleic Acids Res. 1992 May 11;20(9):2341–2347. doi: 10.1093/nar/20.9.2341. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Read L. K., Myler P. J., Stuart K. Extensive editing of both processed and preprocessed maxicircle CR6 transcripts in Trypanosoma brucei. J Biol Chem. 1992 Jan 15;267(2):1123–1128. [PubMed] [Google Scholar]
- Saiki R. K., Gelfand D. H., Stoffel S., Scharf S. J., Higuchi R., Horn G. T., Mullis K. B., Erlich H. A. Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science. 1988 Jan 29;239(4839):487–491. doi: 10.1126/science.2448875. [DOI] [PubMed] [Google Scholar]
- Shinozaki K., Ohme M., Tanaka M., Wakasugi T., Hayashida N., Matsubayashi T., Zaita N., Chunwongse J., Obokata J., Yamaguchi-Shinozaki K. The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression. EMBO J. 1986 Sep;5(9):2043–2049. doi: 10.1002/j.1460-2075.1986.tb04464.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silver L. E., Torri A. F., Hajduk S. L. Organized packaging of kinetoplast DNA networks. Cell. 1986 Nov 21;47(4):537–543. doi: 10.1016/0092-8674(86)90618-5. [DOI] [PubMed] [Google Scholar]
- Simpson L., Neckelmann N., de la Cruz V. F., Simpson A. M., Feagin J. E., Jasmer D. P., Stuart K. Comparison of the maxicircle (mitochondrial) genomes of Leishmania tarentolae and Trypanosoma brucei at the level of nucleotide sequence. J Biol Chem. 1987 May 5;262(13):6182–6196. [PubMed] [Google Scholar]
- Souza A. E., Myler P. J., Stuart K. Maxicircle CR1 transcripts of Trypanosoma brucei are edited and developmentally regulated and encode a putative iron-sulfur protein homologous to an NADH dehydrogenase subunit. Mol Cell Biol. 1992 May;12(5):2100–2107. doi: 10.1128/mcb.12.5.2100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Steinmüller K., Ley A. C., Steinmetz A. A., Sayre R. T., Bogorad L. Characterization of the ndhC-psbG-ORF157/159 operon of maize plastid DNA and of the cyanobacterium Synechocystis sp. PCC6803. Mol Gen Genet. 1989 Mar;216(1):60–69. doi: 10.1007/BF00332231. [DOI] [PubMed] [Google Scholar]
- Stuart K., Gelvin S. R. Kinetoplast DNA of normal and mutant Trypanosoma brucei. Am J Trop Med Hyg. 1980 Sep;29(5 Suppl):1075–1081. doi: 10.4269/ajtmh.1980.29.1075. [DOI] [PubMed] [Google Scholar]
- Stuart K. RNA editing in trypanosomatid mitochondria. Annu Rev Microbiol. 1991;45:327–344. doi: 10.1146/annurev.mi.45.100191.001551. [DOI] [PubMed] [Google Scholar]
- Tanaka Y., Kuroe K., Angata K., Yanagisawa K. ORF209 of Dictyostelium discoideum mitochondrial DNA has a homologue in chloroplast DNA. Plant Mol Biol. 1990 Oct;15(4):659–660. doi: 10.1007/BF00017840. [DOI] [PubMed] [Google Scholar]
- Torri A. F., Hajduk S. L. Posttranscriptional regulation of cytochrome c expression during the developmental cycle of Trypanosoma brucei. Mol Cell Biol. 1988 Nov;8(11):4625–4633. doi: 10.1128/mcb.8.11.4625. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Turner C. M., Barry J. D., Vickerman K. Loss of variable antigen during transformation of Trypanosoma brucei rhodesiense from bloodstream to procyclic forms in the tsetse fly. Parasitol Res. 1988;74(6):507–511. doi: 10.1007/BF00531626. [DOI] [PubMed] [Google Scholar]
- Vickerman K. Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull. 1985 Apr;41(2):105–114. doi: 10.1093/oxfordjournals.bmb.a072036. [DOI] [PubMed] [Google Scholar]
- Videira A., Tropschug M., Werner S. Primary structure and expression of a nuclear-coded subunit of complex I homologous to proteins specified by the chloroplast genome. Biochem Biophys Res Commun. 1990 Sep 28;171(3):1168–1174. doi: 10.1016/0006-291x(90)90807-y. [DOI] [PubMed] [Google Scholar]
- Weiss H., Friedrich T., Hofhaus G., Preis D. The respiratory-chain NADH dehydrogenase (complex I) of mitochondria. Eur J Biochem. 1991 May 8;197(3):563–576. doi: 10.1111/j.1432-1033.1991.tb15945.x. [DOI] [PubMed] [Google Scholar]
- Xu X., Matsuno-Yagi A., Yagi T. Gene cluster of the energy-transducing NADH-quinone oxidoreductase of Paracoccus denitrificans: characterization of four structural gene products. Biochemistry. 1992 Aug 4;31(30):6925–6932. doi: 10.1021/bi00145a009. [DOI] [PubMed] [Google Scholar]