Trypanosomatid genomes contain several subfamilies of ingi-related retroposons

Eukaryotic Cell

Volumn 8, Issue 10, 2009, Pages 1532-1542

  Bringaud, Frédéric ^a   Berriman, Matthew ^b   Hertz Fowler, Christiane ^b  

^a CNRS University Bordeaux Segalen   (France)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

EUKARYOTA; LEISHMANIA BRAZILIENSIS; LEISHMANIA MAJOR; LEISHMANIA SP.; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CONGOLENSE; TRYPANOSOMA CRUZI; TRYPANOSOMA VIVAX; TRYPANOSOMATIDAE;

EID: 70349667789     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00183-09     Document Type: Article

References (39)

1. Berriman, M., E. Ghedin, C. Hertz-Fowler, G. Blandin, H. Renauld, D. C. Bartholomeu, N. J. Lennard, E. Caler, N. E. Hamlin, B. Haas, U. Böhme, L. Hannick, M. A. Aslett, J. Shallom, L. Marcello, L. Hou, B. Wickstead, U. C. Alsmark, C. Arrowsmith, R. J. Atkin, A. J. Barron, F. Bringaud, K. Brooks, M. Carrington, I. Cherevach, T. J. Chillingworth, C. Churcher, L. N. Clark, C. H. Corton, A. Cronin, R. M. Davies, J. Doggett, A. Djikeng, T. Feldblyum, M. C. Field, A. Fraser, I. Goodhead, Z. Hance, D. Harper, B. R. Harris, H. Hauser, J. Hostetier, A. Ivens, K. Jageis, D. Johnson, J. Johnson, K. Jones, A. X. Kerhornou, H. Koo, N. Larke, S. Landfear, C. Larkin, V. Leech, A. Line, A. Lord, A. Macleod, P. J. Mooney, S. Moule, D. M. Martin, G. W. Morgan, K. Mungall, H. Norbertczak, D. Ormond, G. Pai, C. S. Peacock, J. Peterson, M. A. Quail, E. Rabbinowitsch, M. A. Rajandream, C. Reitter, S. L. Salzberg, M. Sanders, S. Schobel, S. Sharp, M. Simmonds, A. J. Simpson, L. Talion, C. M. Turner, A. Tait, A. R. Tivey, S. Van Aken, D. Walker, D. Wanless, S. Wang, B. White, O. White, S. Whitehead, J. Woodward, J. Wortman, M. D. Adams, T. M. Embley, K. Gull, E. Ullu, J. D. Barry, A. H. Fairlamb, F. Opperdoes, B. G. Barrell, J. E. Donelson, N. Hall, C. M. Fraser, S. E. Melville, and N. M. El-Sayed. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422.
2. Bohne, A., F. Brunet, D. Galiana-Arnoux, C. Schultheis, and J. N. Volff. 2008. Transposable elements as drivers of genomic and biological diversity in vertebrates. Chromosome Res. 16:203-215.
3. Boucher, N., Y. Wu, C. Dumas, M. Dube, D. Sereno, M. Breton, and B. Papadopoulou. 2002. A common mechanism of stage-regulated gene expression in Leishmania mediated by a conserved 3′-untranslated region element. J. Biol. Chem. 277:19511-19520.
4. Bringaud, F., D. C. Bartholomeu, G. Blandin, A. Delcher, T. Baltz, N. M. El-Sayed, and E. Ghedin. 2006. The Trypanosoma cruzi L1Tc and NARTc non-LTR retrotransposons show relative site-specificity for insertion. MoI. Biol. Evol. 23:411-420.
5. Bringaud, F., N. Biteau, E. Zuiderwijk, M. Berriman, N. M. El-Sayed, E. Ghedin, S. E. Melville, N. Hall, and T. Baltz. 2004. The ingi and RIME non-LTR retrotransposons are not randomly distributed in the genome of Trypanosoma brucei. Mol. Biol. Evol. 21:520-528. (Pubitemid 38339668)
6. Bringaud, F., J. L. Garcia-Perez, S. R. Heras, E. Ghedin, N. M. El-Sayed, B. Andersson, T. Baltz, and M. C. Lopez. 2002. Identification of non-autonomous non-LTR retrotransposons in the genome of Trypanosoma cruzi. Mol. Biochem. Parasitol. 124:73-78.
7. Bringaud, F., E. Ghedin, G. Blandin, D. C. Bartholomeu, E. Caler, M. J. Levin, T. Baltz, and N. M. El-Sayed. 2006. Evolution of non-LTR retrotransposons in the trypanosomatid genomes: Leishmania major has lost the active elements. Mol. Biochem. Parasitol. 145:158-170.
8. Bringaud, F., E. Ghedin, N. M. El-Sayed, and B. Papadopoulou. 2008. Role of transposable elements in trypanosomatids. Microbes Infect. 10:575-581.
9. Bringaud, F., M. Müller, G. C. Cerqueira, M. Smith, A. Rochette, N. M. El-Sayed, B. Papadopoulou, and E. Ghedin. 2007. Members of a large retroposon family are determinants of post-transcriptional gene expression in Leishmania. PLoS Pathog. 3:e136. (Pubitemid 47510282)
10. Capy, P., C. Bazin, D. Higuet, and T. Langin. 1998. Dynamics and evolution of transposable elements. Landes Bioscience, Austin, TX.
11. Crooks, G. E., G. Hon, J. M. Chandonia, and S. E. Brenner. 2004. WebLogo: a sequence logo generator. Genome Res. 14:1188-1190.
12. Dewannieux, M., C. Esnault, and T. Heidmann. 2003. LINE-mediated retrotransposition of marked Alu sequences. Nat. Genet. 35:41-48.
13. Eickbush, T. H., and H. S. Malik. 2002. Origins and evolution of retrotransposons, p. 1111-1144. In A. G. Craig, R. Craigie, M. Geliert, and A. M. Lambowitz (ed.), Mobile DNA II. ASM Press, Washington, DC.
14. El-Sayed, N. M., P. J. Myler, D. C. Bartholomeu, D. Nilsson, G. Aggarwal, A. N. Tran, E. Ghedin, E. A. Worthey, A. L. Deicher, G. Blandin, S. J. Westenberger, E. Caler, G. C. Cerqueira, C. Branche, B. Haas, A. Anupama, E. Arner, L. Aslund, P. Attipoe, E. Bontempi, F. Bringaud, P. Burton, E. Cadag, D. A. Campbell, M. Carrington, J. Crabtree, H. Darban, J. F. da Silveira, P. de Jong, K. Edwards, P. T. Englund, G. Fazelina, T. Feldblyum, M. Ferella, A. C. Frasch, K. Gull, D. Horn, L. Hou, Y. Huang, E. Kindlund, M. Klingbeil, S. Kluge, H. Koo, D. Lacerda, M. J. Levin, H. Lorenzi, T. Louie, C. R. Machado, R. McCulloch, A. McKenna, Y. Mizuno, J. C. Mottram, S. Nelson, S. Ochaya, K. Osoegawa, G. Pai, M. Parsons, M. Pentony, U. Pettersson, M. Pop, J. L. Ramirez, J. Rinta, L. Robertson, S. L. Salzberg, D. O. Sanchez, A. Seyler, R. Sharma, J. Shetty, A. J. Simpson, E. Sisk, M. T. Tammi, R. Tarleton, S. Teixeira, S. Van Aken, C. Vogt, P. N. Ward, B. Wickstead, J. Wortman, O. White, C. M. Fraser, K. D. Stuart, and B. Andersson. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415.
15. El-Sayed, N. M., P. J. Myler, G. Blandin, M. Berriman, J. Crabtree, G. Aggarwal, E. Caler, H. Renauld, E. A. Worthey, C. Hertz-Fowler, E. Ghedin, C. Peacock, D. C. Bartholomeu, B. J. Haas, A. N. Tran, J. R. Wortman, U. C. Alsmark, S. Angiuoli, A. Anupama, J. Badger, F. Bringaud, E. Cadag, J. M. Carlton, G. C. Cerqueira, T. Creasy, A. L. Delcher, A. Djikeng, T. M. Embley, C. Häuser, A. C. Ivens, S. K. Kummerfeld, J. B. Pereira-Leal, D. Nilsson, J. Peterson, S. L. Salzberg, J. Shallom, J. C. Silva, J. Sundaram, S. Westenberger, O. White, S. E. Melville, J. E. Donelson, B. Andersson, K. D. Stuart, and N. Hall. 2005. Comparative genomics of trypanosomatid parasitic protozoa. Science 309:404-409.
16. Gibson, W. C., J. R. Stevens, C. M. Mwendia, J. N. Ngotho, and J. M. Ndung'u. 2001. Unravelling the phylogenetic relationships of African trypanosomes of suids. Parasitology 122:625-631.
17. Goodier, J. L., and H. H. Kazazian, Jr. 2008. Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135:23-35.
18. Haag, J., C. O'Huigin, and P. Overath. 1998. The molecular phylogeny of trypanosomes: evidence for an early divergence of the Salivaria. Mol. Biochem. Parasitol. 91:37-49.
19. Hasan, G., M. J. Turner, and J. S. Cordingley. 1984. Complete nucleotide sequence of an unusual mobile element from Trypanosoma brucei. Cell 37:333-341.
20. International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409:860-921.
21. Ivens, A. C, C. S. Peacock, E. A. Worthey, L. Murphy, G. Aggarwal, M. Berriman, E. Sisk, M. A. Rajandream, E. Adlem, R. Aert, A. Anupama, Z. Apostolou, P. Attipoe, N. Bason, C. Bauser, A. Beck, S. M. Beverley, G. Bianchettin, K. Borzym, G. Bothe, C. V. Bruschi, M. Collins, E. Cadag, L. Ciarloni, C. Clayton, R. M. Coulson, A. Cronin, A. K. Cruz, R. M. Davies, J. De Gaudenzi, D. E. Dobson, A. Duesterhoeft, G. Fazelina, N. Fosker, A. C. Frasch, A. Fraser, M. Fuchs, C. Gabel, A. Goble, A. Goffeau, D. Harris, C. Hertz-Fowler, H. Hubert, D. Horn, Y. Huang, S. Klages, A. Knights, M. Kube, N. Larke, L. Litvin, A. Lord, T. Louie, M. Marra, D. Masuy, K. Matthews, S. Michaeli, J. C. Mottram, S. MuUer-Auer, H. Munden, S. Nelson, H. Norbertczak, K. Oliver, S. O'Neil, M. Pentony, T. M. Pohl, C. Price, B. Purnelle, M. A. Quail, E. Rabbinowitsch, R. Reinhardt, M. Rieger, J. Rinta, J. Robben, L. Robertson, J. C. Ruiz, S. Rutter, D. Saunders, M. Schafer, J. Schein, D. C. Schwartz, K. Seeger, A. Seyler, S. Sharp, H. Shin, D. Sivam, R. Squares, S. Squares, V. Tosato, C. Vogt, G. Volckaert, R. Wambutt, T. Warren, H. Wedler, J. Woodward, S. Zhou, W. Zimmermann, D. F. Smith, J. M. Blackwell, K. D. Stuart, B. Barrell, and P. J. Myler. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442.
22. Jurka, J. 1997. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc. Natl. Acad. Sci. USA 94:1872-1877.
23. Kajikawa, M., and N. Okada. 2002. LINEs mobilize SINEs in the eel through a shared 3′ sequence. Cell 111:433-444. (Pubitemid 35341395)
24. Kimmel, B. E., O. K. Ole-MoiYoi, and J. R. Young. 1987. Ingi, a 5.2-kb dispersed sequence element from Trypanosoma brucei that carries half of a smaller mobile element at either end and has homology with mammalian LINEs. Mol. Cell. Biol. 7:1465-1475.
25. Luan, D. D., M. H. Korman, J. L. Jakubczak, and T. H. Eickbush. 1993. Reverse transcription of R2Bm RNA is primed by a nick at the chromosomal target site: a mechanism for non-LTR retrotransposition. Cell 72:595-605.
26. Lukes, J., M. Jirku, D. Dolezel, I. Kral'ova, L. Hollar, and D. A. Maslov. 1997. Analysis of ribosomal RNA genes suggests that trypanosomes are monophyletic. J. Mol. Evol. 44:521-527.
27. Malik, H. S., W. D. Burke, and T. H. Eickbush. 1999. The age and evolution of non-LTR retrotransposable elements. Mol. Biol. Evol. 16:793-805.
28. Martin, F., C. Maranon, M. Olivares, C. Alonso, and M. C. Lopez. 1995. Characterization of a non-long terminal repeat retrotransposon cDNA (LlTc) from Trypanosoma cruzi: homology of the first ORF with the ape family of DNA repair enzymes. J. Mol. Biol. 247:49-59.
29. McNicoll, F., M. Müller, S. Cloutier, N. Boilard, A. Rochette, M. Dube, and B. Papadopoulou. 2005. Distinct 3'-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J. Biol. Chem. 280:35238-35246.
30. Murphy, N. B., A. Pays, P. Tebabi, H. Coquelet, M. Guyaux, M. Steinert, and E. Pays. 1987. Trypanosoma brucei repeated element with unusual structural and transcriptional properties. J. Mol. Biol. 195:855-871.
31. Peacock, C. S., K. Seeger, D. Harris, L. Murphy, J. C. Ruiz, M. A. Quail, N. Peters, E. Adlem, A. Tivey, M. Aslett, A. Kerhornou, A. Ivens, A. Fraser, M. A. Rajandream, T. Carver, H. Norbertczak, T. Chillingworth, Z. Hance, K. Jagels, S. Moule, D. Ormond, S. Rutter, R. Squares, S. Whitehead, E. Rabbinowitsch, C. Arrowsmith, B. White, S. Thurston, F. Bringaud, S. L. Baldauf, A. Faulconbridge, D. Jeffares, D. P. Depledge, S. O. Oyóla, J. D. Hilley, L. O. Brito, L. R. Tosi, B. Barrell, A. K. Cruz, J. C. Mottram, D. F. Smith, and M. Berriman. 2007. Comparative genomic analysis of three Leishmania species that cause diverse human disease. Nat. Genet. 39:839-847.
32. Schneider T.D. Stephens R.M. Sequence logos: A new way to display consensus sequences Nucleic Acids Research 1990 18 20 6097-6100 32. Schneider, T. D., and R. M. Stephens. 1990. Sequence logos: a new way to display consensus sequences. Nucleic Acids Res. 18:6097-6100. (Pubitemid 20364672)
33. Smit, A. F. 1999. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 9:657-663.
34. Smith, M., F. Bringaud, and B. Papadopoulou. 2009. Organization and evolution of two SIDER retroposon subfamilies and their impact on the Leishmania genome. BMC Genomics 10:240.
35. Stevens, J., and A. Rambaut. 2001. Evolutionary rate differences in trypanosomes. Infect. Genet. Evol. 1:143-150.
36. Stevens, J. R., H. A. Noyes, C. J. Schofleld, and W. Gibson. 2001. The molecular evolution of Trypanosomatidae. Adv. Parasitol. 48:1-56.
37. Tatout, C., L. Lavie, and J. M. Deragon. 1998. Similar target site selection occurs in integration of plant and mammalian retroposons. J. Mol. Evol. 47:463-470.
38. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
39. Volff, J. N. 2006. Turning junk into gold: domestication of transposable elements and the creation of new genes in eukaryotes. Bioessays 28:913-922.