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. 1994 Aug 1;126(3):631–639. doi: 10.1083/jcb.126.3.631

Kinetoplast DNA replication: mechanistic differences between Trypanosoma brucei and Crithidia fasciculata

PMCID: PMC2120141  PMID: 8045928

Abstract

Kinetoplast DNA, the mitochondrial DNA of trypanosomatid parasites, is a network containing several thousand minicircles and a few dozen maxicircles. We compared kinetoplast DNA replication in Trypanosoma brucei and Crithidia fasciculata using fluorescence in situ hybridization and electron microscopy of isolated networks. One difference is in the location of maxicircles in situ. In C. fasciculata, maxicircles are concentrated in discrete foci embedded in the kinetoplast disk; during replication the foci increase in number but remain scattered throughout the disk. In contrast, T. brucei maxicircles generally fill the entire disk. Unlike those in C. fasciculata, T. brucei maxicircles become highly concentrated in the central region of the kinetoplast after replication; then during segregation they redistribute throughout the daughter kinetoplasts. T. brucei and C. fasciculata also differ in the pattern of attachment of newly synthesized minicircles to the network. In C. fasciculata it was known that minicircles are attached at two antipodal sites but subsequently are found uniformly distributed around the network periphery, possibly due to a relative movement of the kinetoplast disk and two protein complexes responsible for minicircle synthesis and attachment. In T. brucei, minicircles appear to be attached at two antipodal sites but then remain concentrated in these two regions. Therefore, the relative movement of the kinetoplast and the two protein complexes may not occur in T. brucei.

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Selected References

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  1. 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]
  2. Borst P. Why kinetoplast DNA networks? Trends Genet. 1991 May;7(5):139–141. doi: 10.1016/0168-9525(91)90374-y. [DOI] [PubMed] [Google Scholar]
  3. Brown R. C., Evans D. A., Vickerman K. Changes in oxidative metabolism and ultrastructure accompanying differentiation of the mitochondrion in Trypanosoma brucei. Int J Parasitol. 1973 Sep;3(5):691–704. doi: 10.1016/0020-7519(73)90095-7. [DOI] [PubMed] [Google Scholar]
  4. Cosgrove W. B., Skeen M. J. The cell cycle in Crithidia fasciculata. Temporal relationships between synthesis of deoxyribonucleic acid in the nucleus and in the kinetoplast. J Protozool. 1970 May;17(2):172–177. doi: 10.1111/j.1550-7408.1970.tb02350.x. [DOI] [PubMed] [Google Scholar]
  5. Englund P. T. The replication of kinetoplast DNA networks in Crithidia fasciculata. Cell. 1978 May;14(1):157–168. doi: 10.1016/0092-8674(78)90310-0. [DOI] [PubMed] [Google Scholar]
  6. Fairlamb A. H., Weislogel P. O., Hoeijmakers J. H., Borst P. Isolation and characterization of kinetoplast DNA from bloodstream form of Trypanosoma brucei. J Cell Biol. 1978 Feb;76(2):293–309. doi: 10.1083/jcb.76.2.293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Ferguson M., Torri A. F., Ward D. C., Englund P. T. In situ hybridization to the Crithidia fasciculata kinetoplast reveals two antipodal sites involved in kinetoplast DNA replication. Cell. 1992 Aug 21;70(4):621–629. doi: 10.1016/0092-8674(92)90431-b. [DOI] [PubMed] [Google Scholar]
  8. Fernandes A. P., Nelson K., Beverley S. M. Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: perspectives on the age and origins of parasitism. Proc Natl Acad Sci U S A. 1993 Dec 15;90(24):11608–11612. doi: 10.1073/pnas.90.24.11608. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Hajduk S. L., Klein V. A., Englund P. T. Replication of kinetoplast DNA maxicircles. Cell. 1984 Feb;36(2):483–492. doi: 10.1016/0092-8674(84)90241-1. [DOI] [PubMed] [Google Scholar]
  10. 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]
  11. Hoeijmakers J. H., Weijers P. J. The segregation of kinetoplast DNA networks in Trypanosoma brucei. Plasmid. 1980 Jul;4(1):97–116. doi: 10.1016/0147-619x(80)90086-4. [DOI] [PubMed] [Google Scholar]
  12. Landweber L. F., Gilbert W. Phylogenetic analysis of RNA editing: a primitive genetic phenomenon. Proc Natl Acad Sci U S A. 1994 Feb 1;91(3):918–921. doi: 10.1073/pnas.91.3.918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Marini J. C., Levene S. D., Crothers D. M., Englund P. T. A bent helix in kinetoplast DNA. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 1):279–283. doi: 10.1101/sqb.1983.047.01.033. [DOI] [PubMed] [Google Scholar]
  14. Marini J. C., Miller K. G., Englund P. T. Decatenation of kinetoplast DNA by topoisomerases. J Biol Chem. 1980 Jun 10;255(11):4976–4979. [PubMed] [Google Scholar]
  15. 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]
  16. Melendy T., Sheline C., Ray D. S. Localization of a type II DNA topoisomerase to two sites at the periphery of the kinetoplast DNA of Crithidia fasciculata. Cell. 1988 Dec 23;55(6):1083–1088. doi: 10.1016/0092-8674(88)90252-8. [DOI] [PubMed] [Google Scholar]
  17. Pérez-Morga D. L., Englund P. T. Microtechnique for electron microscopy of DNA. Nucleic Acids Res. 1993 Mar 11;21(5):1327–1328. doi: 10.1093/nar/21.5.1327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Pérez-Morga D. L., Englund P. T. The attachment of minicircles to kinetoplast DNA networks during replication. Cell. 1993 Aug 27;74(4):703–711. doi: 10.1016/0092-8674(93)90517-t. [DOI] [PubMed] [Google Scholar]
  19. Pérez-Morga D., Englund P. T. The structure of replicating kinetoplast DNA networks. J Cell Biol. 1993 Dec;123(5):1069–1079. doi: 10.1083/jcb.123.5.1069. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Ray D. S. Kinetoplast DNA minicircles: high-copy-number mitochondrial plasmids. Plasmid. 1987 May;17(3):177–190. doi: 10.1016/0147-619x(87)90026-6. [DOI] [PubMed] [Google Scholar]
  21. Robinson D. R., Gull K. The configuration of DNA replication sites within the Trypanosoma brucei kinetoplast. J Cell Biol. 1994 Aug;126(3):641–648. doi: 10.1083/jcb.126.3.641. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ryan K. A., Englund P. T. Synthesis and processing of kinetoplast DNA minicircles in Trypanosoma equiperdum. Mol Cell Biol. 1989 Aug;9(8):3212–3217. doi: 10.1128/mcb.9.8.3212. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ryan K. A., Shapiro T. A., Rauch C. A., Englund P. T. Replication of kinetoplast DNA in trypanosomes. Annu Rev Microbiol. 1988;42:339–358. doi: 10.1146/annurev.mi.42.100188.002011. [DOI] [PubMed] [Google Scholar]
  24. Shapiro T. A. Kinetoplast DNA maxicircles: networks within networks. Proc Natl Acad Sci U S A. 1993 Aug 15;90(16):7809–7813. doi: 10.1073/pnas.90.16.7809. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Simpson A. M., Simpson L. Pulse-labeling of kinetoplast DNA: localization of 2 sites of synthesis within the networks and kinetics of labeling of closed minicircles. J Protozool. 1976 Nov;23(4):583–587. doi: 10.1111/j.1550-7408.1976.tb03846.x. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Steinert M., Van Assel S. Sequence heterogeneity in kinetoplast DNA: reassociation kinetics. Plasmid. 1980 Jan;3(1):7–17. doi: 10.1016/s0147-619x(80)90030-x. [DOI] [PubMed] [Google Scholar]
  28. Stuart K. D., Gelvin S. B. Localization of kinetoplast DNA maxicircle transcripts in bloodstream and procyclic form Trypanosoma brucei. Mol Cell Biol. 1982 Jul;2(7):845–852. doi: 10.1128/mcb.2.7.845. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Stuart K., Feagin J. E. Mitochondrial DNA of kinetoplastids. Int Rev Cytol. 1992;141:65–88. doi: 10.1016/s0074-7696(08)62063-x. [DOI] [PubMed] [Google Scholar]
  30. Sugisaki H., Ray D. S. DNA sequence of Crithidia fasciculata kinetoplast minicircles. Mol Biochem Parasitol. 1987 Apr;23(3):253–263. doi: 10.1016/0166-6851(87)90032-6. [DOI] [PubMed] [Google Scholar]
  31. Ullu E., Tschudi C. Permeable trypanosome cells as a model system for transcription and trans-splicing. Nucleic Acids Res. 1990 Jun 11;18(11):3319–3326. doi: 10.1093/nar/18.11.3319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Woodward R., Gull K. Timing of nuclear and kinetoplast DNA replication and early morphological events in the cell cycle of Trypanosoma brucei. J Cell Sci. 1990 Jan;95(Pt 1):49–57. doi: 10.1242/jcs.95.1.49. [DOI] [PubMed] [Google Scholar]

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