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. 1994 Dec 1;13(23):5689–5700. doi: 10.1002/j.1460-2075.1994.tb06907.x

Disruption of RNA editing in Leishmania tarentolae by the loss of minicircle-encoded guide RNA genes.

O H Thiemann 1, D A Maslov 1, L Simpson 1
PMCID: PMC395534  PMID: 7988566

Abstract

RNA editing in kinetoplastids appears to be a labile genetic trait that is affected by prolonged cell culture. The transcripts of the G1-G5 cryptogenes are pan-edited in the recently isolated LEM125 strain of Leishmania tarentolae, but not in the UC strain which has been in culture for 55 years. At least 32 minicircle-encoded guide RNAs (gRNAs) for the editing of G1-G5 transcripts are present in LEM125 and absent in UC. We hypothesize that specific minicircle sequence classes encoding gRNAs for the editing of these transcripts were lost during the long culture history of the UC strain. The protein products, which include components of complex I of the respiratory chain, are probably not required during the culture stage of the Leishmania life cycle.

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Selected References

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  1. Abraham J. M., Feagin J. E., Stuart K. Characterization of cytochrome c oxidase III transcripts that are edited only in the 3' region. Cell. 1988 Oct 21;55(2):267–272. doi: 10.1016/0092-8674(88)90049-9. [DOI] [PubMed] [Google Scholar]
  2. Benne R. RNA editing in trypanosomes. Eur J Biochem. 1994 Apr 1;221(1):9–23. doi: 10.1111/j.1432-1033.1994.tb18710.x. [DOI] [PubMed] [Google Scholar]
  3. Blum B., Bakalara N., Simpson L. A model for RNA editing in kinetoplastid mitochondria: "guide" RNA molecules transcribed from maxicircle DNA provide the edited information. Cell. 1990 Jan 26;60(2):189–198. doi: 10.1016/0092-8674(90)90735-w. [DOI] [PubMed] [Google Scholar]
  4. Braly P., Simpson L., Kretzer F. Isolation of kinetoplast-mitochondrial complexes from Leishmania tarentolae. J Protozool. 1974 Nov;21(5):782–790. doi: 10.1111/j.1550-7408.1974.tb03752.x. [DOI] [PubMed] [Google Scholar]
  5. Corell R. A., Feagin J. E., Riley G. R., Strickland T., Guderian J. A., Myler P. J., Stuart K. Trypanosoma brucei minicircles encode multiple guide RNAs which can direct editing of extensively overlapping sequences. Nucleic Acids Res. 1993 Sep 11;21(18):4313–4320. doi: 10.1093/nar/21.18.4313. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Corell R. A., Myler P., Stuart K. Trypanosoma brucei mitochondrial CR4 gene encodes an extensively edited mRNA with completely edited sequence only in bloodstream forms. Mol Biochem Parasitol. 1994 Mar;64(1):65–74. doi: 10.1016/0166-6851(94)90135-x. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. 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]
  9. Gomez-Eichelmann M. C., Holz G., Jr, Beach D., Simpson A. M., Simpson L. Comparison of several lizard Leishmania species and strains in terms of kinetoplast minicircle and maxicircle DNA sequences, nuclear chromosomes, and membrane lipids. Mol Biochem Parasitol. 1988 Jan 15;27(2-3):143–158. doi: 10.1016/0166-6851(88)90034-5. [DOI] [PubMed] [Google Scholar]
  10. Hill G. C., Cross G. A. Cyanide-resistant respiration and a branched cytochrome system in Kinetoplastidae. Biochim Biophys Acta. 1973 Jun 28;305(3):590–596. doi: 10.1016/0005-2728(73)90078-9. [DOI] [PubMed] [Google Scholar]
  11. Kanehisa M. I. Los Alamos sequence analysis package for nucleic acids and proteins. Nucleic Acids Res. 1982 Jan 11;10(1):183–196. doi: 10.1093/nar/10.1.183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kidane G. Z., Hughes D., Simpson L. Sequence heterogeneity and anomalous electrophoretic mobility of kinetoplast minicircle DNA from Leishmania tarentolae. Gene. 1984 Mar;27(3):265–277. doi: 10.1016/0378-1119(84)90071-4. [DOI] [PubMed] [Google Scholar]
  13. Landweber L. F. The evolution of RNA editing in kinetoplastid protozoa. Biosystems. 1992;28(1-3):41–45. doi: 10.1016/0303-2647(92)90006-k. [DOI] [PubMed] [Google Scholar]
  14. Lee S. T., Liu H. Y., Lee S. P., Tarn C. Selection for arsenite resistance causes reversible changes in minicircle composition and kinetoplast organization in Leishmania mexicana. Mol Cell Biol. 1994 Jan;14(1):587–596. doi: 10.1128/mcb.14.1.587. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Lee S. Y., Lee S. T., Chang K. P. Transkinetoplastidy--a novel phenomenon involving bulk alterations of mitochondrion-kinetoplast DNA of a trypanosomatid protozoan. J Protozool. 1992 Jan-Feb;39(1):190–196. doi: 10.1111/j.1550-7408.1992.tb01300.x. [DOI] [PubMed] [Google Scholar]
  16. Maslov D. A., Avila H. A., Lake J. A., Simpson L. Evolution of RNA editing in kinetoplastid protozoa. Nature. 1994 Mar 24;368(6469):345–348. doi: 10.1038/368345a0. [DOI] [PubMed] [Google Scholar]
  17. Maslov D. A., Simpson L. The polarity of editing within a multiple gRNA-mediated domain is due to formation of anchors for upstream gRNAs by downstream editing. Cell. 1992 Aug 7;70(3):459–467. doi: 10.1016/0092-8674(92)90170-h. [DOI] [PubMed] [Google Scholar]
  18. Maslov D. A., Sturm N. R., Niner B. M., Gruszynski E. S., Peris M., Simpson L. An intergenic G-rich region in Leishmania tarentolae kinetoplast maxicircle DNA is a pan-edited cryptogene encoding ribosomal protein S12. Mol Cell Biol. 1992 Jan;12(1):56–67. doi: 10.1128/mcb.12.1.56. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Muhich M. L., Neckelmann N., Simpson L. The divergent region of the Leishmania tarentolae kinetoplast maxicircle DNA contains a diverse set of repetitive sequences. Nucleic Acids Res. 1985 May 10;13(9):3241–3260. doi: 10.1093/nar/13.9.3241. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Read L. K., Wilson K. D., Myler P. J., Stuart K. Editing of Trypanosoma brucei maxicircle CR5 mRNA generates variable carboxy terminal predicted protein sequences. Nucleic Acids Res. 1994 Apr 25;22(8):1489–1495. doi: 10.1093/nar/22.8.1489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Riley G. R., Corell R. A., Stuart K. Multiple guide RNAs for identical editing of Trypanosoma brucei apocytochrome b mRNA have an unusual minicircle location and are developmentally regulated. J Biol Chem. 1994 Feb 25;269(8):6101–6108. [PubMed] [Google Scholar]
  23. Rovai L., Tripp C., Stuart K., Simpson L. Recurrent polymorphisms in small chromosomes of Leishmania tarentolae after nutrient stress or subcloning. Mol Biochem Parasitol. 1992 Jan;50(1):115–125. doi: 10.1016/0166-6851(92)90249-j. [DOI] [PubMed] [Google Scholar]
  24. Shaw J. M., Feagin J. E., Stuart K., Simpson L. Editing of kinetoplastid mitochondrial mRNAs by uridine addition and deletion generates conserved amino acid sequences and AUG initiation codons. Cell. 1988 May 6;53(3):401–411. doi: 10.1016/0092-8674(88)90160-2. [DOI] [PubMed] [Google Scholar]
  25. Simpson L. Isolation of maxicircle component of kinetoplast DNA from hemoflagellate protozoa. Proc Natl Acad Sci U S A. 1979 Apr;76(4):1585–1588. doi: 10.1073/pnas.76.4.1585. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Simpson L., Maslov D. A. RNA editing and the evolution of parasites. Science. 1994 Jun 24;264(5167):1870–1871. doi: 10.1126/science.8009214. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Simpson L., Simpson A. G. Kinetoplast RNA of Leishmania tarentolae. Cell. 1978 May;14(1):169–178. doi: 10.1016/0092-8674(78)90311-2. [DOI] [PubMed] [Google Scholar]
  29. Simpson L. The mitochondrial genome of kinetoplastid protozoa: genomic organization, transcription, replication, and evolution. Annu Rev Microbiol. 1987;41:363–382. doi: 10.1146/annurev.mi.41.100187.002051. [DOI] [PubMed] [Google Scholar]
  30. Sloof P., Arts G. J., van den Burg J., van der Spek H., Benne R. RNA editing in mitochondria of cultured trypanosomatids: translatable mRNAs for NADH-dehydrogenase subunits are missing. J Bioenerg Biomembr. 1994 Apr;26(2):193–203. doi: 10.1007/BF00763068. [DOI] [PubMed] [Google Scholar]
  31. 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]
  32. Souza A. E., Shu H. H., Read L. K., Myler P. J., Stuart K. D. Extensive editing of CR2 maxicircle transcripts of Trypanosoma brucei predicts a protein with homology to a subunit of NADH dehydrogenase. Mol Cell Biol. 1993 Nov;13(11):6832–6840. doi: 10.1128/mcb.13.11.6832. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stuart K., Feagin J. E., Abraham J. M. RNA editing: the creation of nucleotide sequences in mRNA--a minireview. Gene. 1989 Oct 15;82(1):155–160. doi: 10.1016/0378-1119(89)90040-1. [DOI] [PubMed] [Google Scholar]
  34. Sturm N. R., Maslov D. A., Blum B., Simpson L. Generation of unexpected editing patterns in Leishmania tarentolae mitochondrial mRNAs: misediting produced by misguiding. Cell. 1992 Aug 7;70(3):469–476. doi: 10.1016/0092-8674(92)90171-8. [DOI] [PubMed] [Google Scholar]
  35. Sturm N. R., Simpson L. Kinetoplast DNA minicircles encode guide RNAs for editing of cytochrome oxidase subunit III mRNA. Cell. 1990 Jun 1;61(5):879–884. doi: 10.1016/0092-8674(90)90198-n. [DOI] [PubMed] [Google Scholar]
  36. Sturm N. R., Simpson L. Leishmania tarentolae minicircles of different sequence classes encode single guide RNAs located in the variable region approximately 150 bp from the conserved region. Nucleic Acids Res. 1991 Nov 25;19(22):6277–6281. doi: 10.1093/nar/19.22.6277. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wallbanks K. R., Maazoun R., Canning E. U., Rioux J. A. The identity of Leishmania tarentolae Wenyon 1921. Parasitology. 1985 Feb;90(Pt 1):67–78. doi: 10.1017/s0031182000049027. [DOI] [PubMed] [Google Scholar]

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