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. 1987 Jan 12;15(1):51–65. doi: 10.1093/nar/15.1.51

The nucleotide sequence of a 3.2 kb segment of mitochondrial maxicircle DNA from Crithidia fasciculata containing the gene for cytochrome oxidase subunit III, the N-terminal part of the apocytochrome b gene and a possible frameshift gene; further evidence for the use of unusual initiator triplets in trypanosome mitochondria.

P Sloof, J van den Burg, A Voogd, R Benne
PMCID: PMC340397  PMID: 3029678

Abstract

A 3.2 kb segment of the maxicircle of Crithidia fasciculata mitochondrial (mt) DNA contains the gene for cytochrome oxidase subunit III (coxIII), the N-terminal portion of the gene for apocytochrome b (cytb) and two partially overlapping Unassigned Reading Frames (C.URF2/1). Transcript analysis of the segment reveals that both the coxIII gene and the C.URF2/1 area are transcribed into a pair of RNA products. With the C. fasciculata gene version as a probe, a coxIII gene could not be detected in nuclear and mtDNA of Trypanosoma brucei, indicating that the cytochrome oxidases of these two closely related trypanosome species may differ. The nucleotide homology in the N-terminal region of the coxIII and cytb genes in T. brucei, Leishmania tarentolae and C. fasciculata starts at a UUA leucine codon, which adds further support to the hypothesis that apart from AUG, other initiator triplets are used in trypanosomal mitochondria: UUG, CUG and UUA, all triplets coding for leucine in the universal code. Finally, the possibility is discussed that the two overlapping URFs (C.URF2/1) in fact represent a single, frameshift containing, gene.

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Selected References

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  1. Anderson S., Bankier A. T., Barrell B. G., de Bruijn M. H., Coulson A. R., Drouin J., Eperon I. C., Nierlich D. P., Roe B. A., Sanger F. Sequence and organization of the human mitochondrial genome. Nature. 1981 Apr 9;290(5806):457–465. doi: 10.1038/290457a0. [DOI] [PubMed] [Google Scholar]
  2. Anderson S., de Bruijn M. H., Coulson A. R., Eperon I. C., Sanger F., Young I. G. Complete sequence of bovine mitochondrial DNA. Conserved features of the mammalian mitochondrial genome. J Mol Biol. 1982 Apr 25;156(4):683–717. doi: 10.1016/0022-2836(82)90137-1. [DOI] [PubMed] [Google Scholar]
  3. Auffray C., Rougeon F. Purification of mouse immunoglobulin heavy-chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem. 1980 Jun;107(2):303–314. doi: 10.1111/j.1432-1033.1980.tb06030.x. [DOI] [PubMed] [Google Scholar]
  4. Benne R., De Vries B. F., Van den Burg J., Klaver B. The nucleotide sequence of a segment of Trypanosoma brucei mitochondrial maxi-circle DNA that contains the gene for apocytochrome b and some unusual unassigned reading frames. Nucleic Acids Res. 1983 Oct 25;11(20):6925–6941. doi: 10.1093/nar/11.20.6925. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Benne R., Van den Burg J., Brakenhoff J. P., Sloof P., Van Boom J. H., Tromp M. C. Major transcript of the frameshifted coxII gene from trypanosome mitochondria contains four nucleotides that are not encoded in the DNA. Cell. 1986 Sep 12;46(6):819–826. doi: 10.1016/0092-8674(86)90063-2. [DOI] [PubMed] [Google Scholar]
  6. Borst P., Hoeijmakers J. H. Kinetoplast DNA. Plasmid. 1979 Jan;2(1):20–40. doi: 10.1016/0147-619x(79)90003-9. [DOI] [PubMed] [Google Scholar]
  7. Browning K. S., RajBhandary U. L. Cytochrome oxidase subunit III gene in Neurospora crassa mitochondria. Location and sequence. J Biol Chem. 1982 May 10;257(9):5253–5256. [PubMed] [Google Scholar]
  8. Cordingley J. S., Turner M. J. 6.5 S RNA; preliminary characterisation of unusual small RNAs in Trypanosoma brucei. Mol Biochem Parasitol. 1980 Apr;1(2):91–96. doi: 10.1016/0166-6851(80)90003-1. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Feagin J. E., Stuart K. Differential expression of mitochondrial genes between life cycle stages of Trypanosoma brucei. Proc Natl Acad Sci U S A. 1985 May;82(10):3380–3384. doi: 10.1073/pnas.82.10.3380. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Hensgens L. A., Brakenhoff J., De Vries B. F., Sloof P., Tromp M. C., Van Boom J. H., Benne R. The sequence of the gene for cytochrome c oxidase subunit I, a frameshift containing gene for cytochrome c oxidase subunit II and seven unassigned reading frames in Trypanosoma brucei mitochondrial maxi-circle DNA. Nucleic Acids Res. 1984 Oct 11;12(19):7327–7344. doi: 10.1093/nar/12.19.7327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hoeijmakers J. H., Schoutsen B., Borst P. Kinetoplast DNA in the insect trypanosomes Crithidia luciliae and Crithidia fasciculata. I. Sequence evolution and transcription of the maxicircle. Plasmid. 1982 May;7(3):199–209. doi: 10.1016/0147-619x(82)90001-4. [DOI] [PubMed] [Google Scholar]
  13. Hoeijmakers J. H., Snijders A., Janssen J. W., Borst P. Transcription of kinetoplast DNA in Trypanosoma brucei bloodstream and culture forms. Plasmid. 1981 May;5(3):329–350. doi: 10.1016/0147-619x(81)90009-3. [DOI] [PubMed] [Google Scholar]
  14. Muhich M. L., Simpson L., Simpson A. M. Comparison of maxicircle DNAs of Leishmania tarentolae and Trypanosoma brucei. Proc Natl Acad Sci U S A. 1983 Jul;80(13):4060–4064. doi: 10.1073/pnas.80.13.4060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Netzker R., Köchel H. G., Basak N., Küntzel H. Nucleotide sequence of Aspergillus nidulans mitochondrial genes coding for ATPase subunit 6, cytochrome oxidase subunit 3, seven unidentified proteins, four tRNAs and L-rRNA. Nucleic Acids Res. 1982 Aug 11;10(15):4783–4794. doi: 10.1093/nar/10.15.4783. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Payne M., Rothwell V., Jasmer D. P., Feagin J. E., Stuart K. Identification of mitochondrial genes in Trypanosoma brucei and homology to cytochrome c oxidase II in two different reading frames. Mol Biochem Parasitol. 1985 May;15(2):159–170. doi: 10.1016/0166-6851(85)90117-3. [DOI] [PubMed] [Google Scholar]
  17. Pinck L., Franck A., Fritsch C. Formation of ribosome-RNA initiation complexes with alfalfa mosaic virus RNA 4 and RNA 3. Nucleic Acids Res. 1979 Sep 11;7(1):151–166. doi: 10.1093/nar/7.1.151. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Poncz M., Solowiejczyk D., Ballantine M., Schwartz E., Surrey S. "Nonrandom" DNA sequence analysis in bacteriophage M13 by the dideoxy chain-termination method. Proc Natl Acad Sci U S A. 1982 Jul;79(14):4298–4302. doi: 10.1073/pnas.79.14.4298. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Prochaska L. J., Bisson R., Capaldi R. A., Steffens G. C., Buse G. Inhibition of cytochrome c oxidase function by dicyclohexylcarbodiimide. Biochim Biophys Acta. 1981 Sep 14;637(2):360–373. doi: 10.1016/0005-2728(81)90175-4. [DOI] [PubMed] [Google Scholar]
  20. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Simpson A. M., Neckelmann N., de la Cruz V. F., Muhich M. L., Simpson L. Mapping and 5' end determination of kinetoplast maxicircle gene transcripts from Leishmania tarentolae. Nucleic Acids Res. 1985 Aug 26;13(16):5977–5993. doi: 10.1093/nar/13.16.5977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Sloof P., Van den Burg J., Voogd A., Benne R., Agostinelli M., Borst P., Gutell R., Noller H. Further characterization of the extremely small mitochondrial ribosomal RNAs from trypanosomes: a detailed comparison of the 9S and 12S RNAs from Crithidia fasciculata and Trypanosoma brucei with rRNAs from other organisms. Nucleic Acids Res. 1985 Jun 11;13(11):4171–4190. doi: 10.1093/nar/13.11.4171. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Swinkels B. W., Gibson W. C., Osinga K. A., Kramer R., Veeneman G. H., van Boom J. H., Borst P. Characterization of the gene for the microbody (glycosomal) triosephosphate isomerase of Trypanosoma brucei. EMBO J. 1986 Jun;5(6):1291–1298. doi: 10.1002/j.1460-2075.1986.tb04358.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Thalenfeld B. E., Tzagoloff A. Assembly of the mitochondrial membrane system. Sequence of the oxi 2 gene of yeast mitochondrial DNA. J Biol Chem. 1980 Jul 10;255(13):6173–6180. [PubMed] [Google Scholar]
  25. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. de Bruijn M. H. Drosophila melanogaster mitochondrial DNA, a novel organization and genetic code. Nature. 1983 Jul 21;304(5923):234–241. doi: 10.1038/304234a0. [DOI] [PubMed] [Google Scholar]
  27. de la Cruz V. F., Neckelmann N., Simpson L. Sequences of six genes and several open reading frames in the kinetoplast maxicircle DNA of Leishmania tarentolae. J Biol Chem. 1984 Dec 25;259(24):15136–15147. [PubMed] [Google Scholar]

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