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. 1989 Sep;8(9):2633–2638. doi: 10.1002/j.1460-2075.1989.tb08403.x

Transcription of telomere repeats in protozoa.

G Rudenko 1, L H Van der Ploeg 1
PMCID: PMC401269  PMID: 2511008

Abstract

The telomerically located variant cell surface glycoprotein (VSG) gene expression sites of the protozoan parasite Trypanosoma brucei are transcribed by an unusual alpha-amanitin resistant RNA polymerase. We show that the telomere GGGTTA repeats located at the chromosome ends of T. brucei and the related protozoan T. equiperdum are also transcribed by alpha-amanitin resistant RNA polymerases. This transcription predominantly proceeds unidirectionally towards the end of the chromosome, in both bloodstream and insect form trypanosomes and results in the generation of heterogeneously sized steady state RNA. We postulate that telomere repeat transcription results from readthrough downstream of telomeric genes. Telomere repeat transcription was found in all seven protozoan species tested, but was alpha-amanitin resistant only in trypanosome species which exhibited antigenic variation. The data indicate that in some trypanosome species a subset of telomeres is transcribed by a different type of RNA polymerase.

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Selected References

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  1. BONE G. J., STEINERT M. Isotopes incorporated in the nucleic acids of Trypanosoma mega. Nature. 1956 Aug 11;178(4528):308–309. doi: 10.1038/178308a0. [DOI] [PubMed] [Google Scholar]
  2. Berger S. L. Isolation of cytoplasmic RNA: ribonucleoside-vanadyl complexes. Methods Enzymol. 1987;152:227–234. doi: 10.1016/0076-6879(87)52024-9. [DOI] [PubMed] [Google Scholar]
  3. Bernards A., Van der Ploeg L. H., Frasch A. C., Borst P., Boothroyd J. C., Coleman S., Cross G. A. Activation of trypanosome surface glycoprotein genes involves a duplication-transposition leading to an altered 3' end. Cell. 1981 Dec;27(3 Pt 2):497–505. doi: 10.1016/0092-8674(81)90391-3. [DOI] [PubMed] [Google Scholar]
  4. Blackburn E. H., Challoner P. B. Identification of a telomeric DNA sequence in Trypanosoma brucei. Cell. 1984 Feb;36(2):447–457. doi: 10.1016/0092-8674(84)90238-1. [DOI] [PubMed] [Google Scholar]
  5. Borst P. Discontinuous transcription and antigenic variation in trypanosomes. Annu Rev Biochem. 1986;55:701–732. doi: 10.1146/annurev.bi.55.070186.003413. [DOI] [PubMed] [Google Scholar]
  6. Borst P., Greaves D. R. Programmed gene rearrangements altering gene expression. Science. 1987 Feb 6;235(4789):658–667. doi: 10.1126/science.3544215. [DOI] [PubMed] [Google Scholar]
  7. Brun R., Schönenberger Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Short communication. Acta Trop. 1979 Sep;36(3):289–292. [PubMed] [Google Scholar]
  8. Cross G. A. Identification, purification and properties of clone-specific glycoprotein antigens constituting the surface coat of Trypanosoma brucei. Parasitology. 1975 Dec;71(3):393–417. doi: 10.1017/s003118200004717x. [DOI] [PubMed] [Google Scholar]
  9. De Lange T., Kooter J. M., Michels P. A., Borst P. Telomere conversion in trypanosomes. Nucleic Acids Res. 1983 Dec 10;11(23):8149–8165. doi: 10.1093/nar/11.23.8149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Evers R., Hammer A., Köck J., Jess W., Borst P., Mémet S., Cornelissen A. W. Trypanosoma brucei contains two RNA polymerase II largest subunit genes with an altered C-terminal domain. Cell. 1989 Feb 24;56(4):585–597. doi: 10.1016/0092-8674(89)90581-3. [DOI] [PubMed] [Google Scholar]
  11. Feinberg A. P., Vogelstein B. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal Biochem. 1984 Feb;137(1):266–267. doi: 10.1016/0003-2697(84)90381-6. [DOI] [PubMed] [Google Scholar]
  12. Giannini S. H., D'Alesandro P. A. Isolation of protective antigens from Trypanosoma lewisi by using trypanostatic (ablastic) immunoglobulin G from the surface coat. Infect Immun. 1984 Feb;43(2):617–621. doi: 10.1128/iai.43.2.617-621.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Giannini S. H., Schittini M., Keithly J. S., Warburton P. W., Cantor C. R., Van der Ploeg L. H. Karyotype analysis of Leishmania species and its use in classification and clinical diagnosis. Science. 1986 May 9;232(4751):762–765. doi: 10.1126/science.3961502. [DOI] [PubMed] [Google Scholar]
  14. Kafatos F. C., Jones C. W., Efstratiadis A. Determination of nucleic acid sequence homologies and relative concentrations by a dot hybridization procedure. Nucleic Acids Res. 1979 Nov 24;7(6):1541–1552. doi: 10.1093/nar/7.6.1541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kooter J. M., Borst P. Alpha-amanitin-insensitive transcription of variant surface glycoprotein genes provides further evidence for discontinuous transcription in trypanosomes. Nucleic Acids Res. 1984 Dec 21;12(24):9457–9472. doi: 10.1093/nar/12.24.9457. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kooter J. M., De Lange T., Borst P. Discontinuous synthesis of mRNA in trypanosomes. EMBO J. 1984 Oct;3(10):2387–2392. doi: 10.1002/j.1460-2075.1984.tb02144.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kooter J. M., van der Spek H. J., Wagter R., d'Oliveira C. E., van der Hoeven F., Johnson P. J., Borst P. The anatomy and transcription of a telomeric expression site for variant-specific surface antigens in T. brucei. Cell. 1987 Oct 23;51(2):261–272. doi: 10.1016/0092-8674(87)90153-x. [DOI] [PubMed] [Google Scholar]
  18. Laird P. W., Kooter J. M., Loosbroek N., Borst P. Mature mRNAs of Trypanosoma brucei possess a 5' cap acquired by discontinuous RNA synthesis. Nucleic Acids Res. 1985 Jun 25;13(12):4253–4266. doi: 10.1093/nar/13.12.4253. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Langsley G., Hyde J. E., Goman M., Scaife J. G. Cloning and characterisation of the rRNA genes from the human malaria parasite Plasmodium falciparum. Nucleic Acids Res. 1983 Dec 20;11(24):8703–8717. doi: 10.1093/nar/11.24.8703. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Le Trant N., Meshnick S. R., Kitchener K., Eaton J. W., Cerami A. Iron-containing superoxide dismutase from Crithidia fasciculata. Purification, characterization, and similarity to Leishmanial and trypanosomal enzymes. J Biol Chem. 1983 Jan 10;258(1):125–130. [PubMed] [Google Scholar]
  21. Lenardo M. J., Dorfman D. M., Reddy L. V., Donelson J. E. Characterization of the Trypanosoma brucei 5S ribosomal RNA gene and transcript: the 5S rRNA is a spliced-leader-independent species. Gene. 1985;35(1-2):131–141. doi: 10.1016/0378-1119(85)90165-9. [DOI] [PubMed] [Google Scholar]
  22. Longacre S., Hibner U., Raibaud A., Eisen H., Baltz T., Giroud C., Baltz D. DNA rearrangements and antigenic variation in Trypanosoma equiperdum: multiple expression-linked sites in independent isolates of trypanosomes expressing the same antigen. Mol Cell Biol. 1983 Mar;3(3):399–409. doi: 10.1128/mcb.3.3.399. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. MacDonald R. J., Swift G. H., Przybyla A. E., Chirgwin J. M. Isolation of RNA using guanidinium salts. Methods Enzymol. 1987;152:219–227. doi: 10.1016/0076-6879(87)52023-7. [DOI] [PubMed] [Google Scholar]
  24. Michels P. A., Liu A. Y., Bernards A., Sloof P., Van der Bijl M. M., Schinkel A. H., Menke H. H., Borst P., Veeneman G. H., Tromp M. C. Activation of the genes for variant surface glycoproteins 117 and 118 in Trypanosoma brucei. J Mol Biol. 1983 Jun 5;166(4):537–556. doi: 10.1016/s0022-2836(83)80283-6. [DOI] [PubMed] [Google Scholar]
  25. Mowatt M. R., Clayton C. E. Developmental regulation of a novel repetitive protein of Trypanosoma brucei. Mol Cell Biol. 1987 Aug;7(8):2838–2844. doi: 10.1128/mcb.7.8.2838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Peterson D. S., Wrightsman R. A., Manning J. E. Cloning of a major surface-antigen gene of Trypanosoma cruzi and identification of a nonapeptide repeat. Nature. 1986 Aug 7;322(6079):566–568. doi: 10.1038/322566a0. [DOI] [PubMed] [Google Scholar]
  27. Ponnudurai T., Lensen A. H., Leeuwenberg A. D., Meuwissen J. H. Cultivation of fertile Plasmodium falciparum gametocytes in semi-automated systems. 1. Static cultures. Trans R Soc Trop Med Hyg. 1982;76(6):812–818. doi: 10.1016/0035-9203(82)90116-x. [DOI] [PubMed] [Google Scholar]
  28. Ponzi M., Pace T., Dore E., Frontali C. Identification of a telomeric DNA sequence in Plasmodium berghei. EMBO J. 1985 Nov;4(11):2991–2995. doi: 10.1002/j.1460-2075.1985.tb04034.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Roditi I., Carrington M., Turner M. Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei. Nature. 1987 Jan 15;325(6101):272–274. doi: 10.1038/325272a0. [DOI] [PubMed] [Google Scholar]
  30. Smith J. L., Levin J. R., Ingles C. J., Agabian N. In trypanosomes the homolog of the largest subunit of RNA polymerase II is encoded by two genes and has a highly unusual C-terminal domain structure. Cell. 1989 Mar 10;56(5):815–827. doi: 10.1016/0092-8674(89)90686-7. [DOI] [PubMed] [Google Scholar]
  31. Thomashow L. S., Milhausen M., Rutter W. J., Agabian N. Tubulin genes are tandemly linked and clustered in the genome of trypanosoma brucei. Cell. 1983 Jan;32(1):35–43. doi: 10.1016/0092-8674(83)90494-4. [DOI] [PubMed] [Google Scholar]
  32. Van der Ploeg L. H., Cornelissen A. W., Michels P. A., Borst P. Chromosome rearrangements in Trypanosoma brucei. Cell. 1984 Nov;39(1):213–221. doi: 10.1016/0092-8674(84)90207-1. [DOI] [PubMed] [Google Scholar]
  33. Van der Ploeg L. H. Discontinuous transcription and splicing in trypanosomes. Cell. 1986 Nov 21;47(4):479–480. doi: 10.1016/0092-8674(86)90608-2. [DOI] [PubMed] [Google Scholar]
  34. Van der Ploeg L. H., Liu A. Y., Borst P. Structure of the growing telomeres of Trypanosomes. Cell. 1984 Feb;36(2):459–468. doi: 10.1016/0092-8674(84)90239-3. [DOI] [PubMed] [Google Scholar]
  35. Van der Ploeg L. H., Smith C. L., Polvere R. I., Gottesdiener K. M. Improved separation of chromosome-sized DNA from Trypanosoma brucei, stock 427-60. Nucleic Acids Res. 1989 Apr 25;17(8):3217–3227. doi: 10.1093/nar/17.8.3217. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vickerman K. On the surface coat and flagellar adhesion in trypanosomes. J Cell Sci. 1969 Jul;5(1):163–193. doi: 10.1242/jcs.5.1.163. [DOI] [PubMed] [Google Scholar]
  37. White T. C., Rudenko G., Borst P. Three small RNAs within the 10 kb trypanosome rRNA transcription unit are analogous to domain VII of other eukaryotic 28S rRNAs. Nucleic Acids Res. 1986 Dec 9;14(23):9471–9489. doi: 10.1093/nar/14.23.9471. [DOI] [PMC free article] [PubMed] [Google Scholar]

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