A new, expressed multigene family containing a hot spot for insertion of retroelements is associated with polymorphic subtelomeric regions of Trypanosoma brucei

Eukaryotic Cell

Volumn 1, Issue 1, 2002, Pages 137-151

  Bringaud, Frédéric ^a   Biteau, Nicolas ^a   Melville, Sara E ^b   Hez, Stéphanie ^a   El Sayed, Najib M ^d,e   Leech, Vanessa ^b   Berriman, Matthew ^c   Hall, Neil ^c   Donelson, John E ^f   Baltz, Théo ^a  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d J CRAIG VENTER INSTITUTE   (United States)

^e GEORGE WASHINGTON UNIVERSITY   (United States)

^f UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INSERTION SEQUENCES; PROTOZOA; TRANSPOSONS; TRYPANOSOMA; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

PRIMER DNA; PROTOZOAL DNA; PROTOZOAL PROTEIN; RHS1A PROTEIN, TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CHEMISTRY; CLASSIFICATION; ESCHERICHIA COLI; GENE; GENE EXPRESSION REGULATION; GENETIC POLYMORPHISM; GENETICS; MOLECULAR CLONING; MOLECULAR GENETICS; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE; PHYLOGENY; PSEUDOGENE; RETROPOSON; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY; TELOMERE; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; DNA PRIMERS; DNA, PROTOZOAN; ESCHERICHIA COLI; GENES, PROTOZOAN; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; MUTAGENESIS, INSERTIONAL; PHYLOGENY; POLYMORPHISM, GENETIC; PROTOZOAN PROTEINS; PSEUDOGENES; RETROELEMENTS; SEQUENCE ALIGNMENT; SEQUENCE HOMOLOGY, AMINO ACID; TELOMERE; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA CRUZI;

EID: 0036464010     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.1.1.137-151.2002     Document Type: Article

References (69)

1. Affolter, M., L. Rindisbacher, and R. Braun. 1989. The tubulin gene cluster of Trypanosoma brucei starts with an intact beta-gene and ends with a truncated beta-gene interrupted by a retrotransposon-like sequence. Gene 80:177-183.
2. Aguero, F., R. E. Verdun, A. C. Frasch, and D. O. Sanchez. 2000. A random sequencing approach for the analysis of the Trypanosoma cruzi genome: general structure, large gene and repetitive DNA families, and gene discovery. Genome Res. 10:1996-2005.
3. Aksoy, S., T. M. Lalor, J. Martin, L. H. Van der Ploeg, and F. F. Richards. 1987. Multiple copies of a retroposon interrupt spliced leader RNA genes in the African trypanosome Trypanosoma gambiense. EMBO J. 6:3819-3826.
4. Barry, J. D., S. V. Graham, M. Fotheringham, V. S. Graham, K. Kobryn, and B. Wymer. 1998. VSG gene control and infectivity strategy of metacyclic stage Trypanosoma brucei. Mol. Biochem. Parasitol. 91:93-105.
5. Barry, J. D., and R. McCulloch. 2001. Antigenic variation in trypanosomes: enhanced phenotypic variation in a eukaryotic parasite. Adv. Parasitol. 49:1-70.
6. Baruch, D. I., B. L. Pasloske, H. B. Singh, X. Bi, X. C. Ma, M. Feldman, T. F. Taraschi, and R. J. Howard. 1995. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell 82:77-87.
7. Beals, T. P., and J. C. Boothroyd. 1992. Genomic organization and context of a trypanosome variant surface glycoprotein gene family. J. Mol. Biol. 225:961-971.
8. Bernards, A., L. H. Van der Ploeg, A. C. Frasch, P. Borst, J. C. Boothroyd, S. Coleman, and G. A. Cross. 1981. Activation of trypanosome surface giycoprotein genes involves a duplication-transposition leading to an altered 3′ end. Cell 27:497-505.
9. Besansky, N. J., S. M. Paskewitz, D. M. Hamm, and F. H. Collins. 1992. Distinct families of site-specific retrotransposons occupy identical positions in the rRNA genes of Anopheles gambiae. Mol. Cell. Biol. 12:5102-5110.
10. Borst, P., W. Bitter, P. A. Blundell, I. Chaves, M. Cross, H. Gerrits, F. van Leeuwen, R. McCulloch, M. Taylor, and G. Rudenko. 1998. Control of VSG gene expression sites in Trypanosoma brucei. Mol. Biochem. Parasitol. 91:67-76.
11. Bringaud, F., D. Baltz, and T. Baltz. 1998. Functional and molecular characterization of a glycosomal PPi-dependent enzyme in trypanosomatids: pyruvate, phosphate dikinase. Proc. Natl. Acad. Sci. USA 95:7963-7968.
12. Bringaud, F., and T. Baltz. 1992. A potential hexose transporter gene expressed predominantly in the bloodstream form of Trypanosoma brucei. Mol. Biochem. Parasitol. 52:111-121.
13. Bringaud, F., N. Biteau, J. E. Donelson, and T. Baltz. 2001. Conservation of metacyclic variant surface glycoprotein expression sites among different trypanosome isolates. Mol. Biochem. Parasitol. 113:67-78.
14. Bringaud, F., C. Vedrenne, A. Cuvillier, D. Parzy, D. Baltz, E. Tetaud, E. Pays, J. Venegas, G. Merlin, and T. Baltz. 1998. Conserved organization of genes in trypanosomatids. Mol. Biochem. Parasitol. 94:249-264.
15. Brun, R., and M. Schonenberger. 1979. Cultivation and in vitro cloning or procyclic culture forms of Trypanosoma brucei in a semi-defined medium. Acta Trop. 36:289-292.
16. Burke, W. D., F. Muller, and T. H. Eickbush. 1995. R4, a non-LTR retrotransposon specific to the large subunit rRNA genes of nematodes. Nucleic Acids Res. 23:4628-4634.
17. Campbell, D. A. 1989. c2X75, a derivative of the cosmid vector c2XB. Nucleic Acids Res. 17:458.
18. Cheng, Q., N. Cloonan, K. Fischer, J. Thompson, G. Waine, M. Lanzer, and A. Saul. 1998. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol. 97:161-176.
19. Cross, G. A., L. E. Wirtz, and M. Navarro. 1998. Regulation of vsg expression site transcription and switching in Trypanosoma brucei. Mol. Biochem. Parasitol. 91:77-91.
20. del Portillo, H. A., C. Fernandez-Becerra, S. Bowman, K. Oliver, M. Preuss, C. P. Sanchez, N. K. Schneider, J. M. Villalobos, M. A. Rajandream, D. Harris, L. H. Pereira da Silva, B. Barrell, and M. Lanzer. 2001. A super-family of variant genes encoded in the subtelomeric region of Plasmodium vivax. Nature 410:839-842.
21. Djlkeng, A., C. Agufa, J. E. Donelson, and P. A. Majiwa. 1998. Generation of expressed sequence tags as physical landmarks in the genome of Trypanosoma brucei. Gene 221:93-106.
22. Donelson, J. E., K. L. Hill, and N. M. El-Sayed. 1998. Multiple mechanisms of immune evasion by African trypanosomes. Mol. Biochem. Parasitol. 91:51-66.
23. El-Sayed, N. M., C. M. Alarcon, J. C. Beck, V. C. Sheffield, and J. E. Donelson. 1995. cDNA expressed sequence tags of Trypanosoma brucei rhodesiense provide new insights into the biology of the parasite. Mol. Biochem. Parasitol. 73:75-90.
24. Esposito, T., F. Gianfrancesco, A. Ciccodicola, L. Montanini, S. Mumm, M. D'Urso, and A. Forabosco. 1999. A novel pseudoautosomal human gene encodes a putative protein similar to Ac-like transposases. Hum. Mol. Genet. 8:61-67.
25. Freitas-Junior, L. H., E. Bottius, L. A. Pirrit, K. W. Deitsch, C. Scheidig, F. Guinet, U. Nehrbass, T. E. Wellems, and A. Scherf. 2000. Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407:1018-1022.
26. Gabriel, A., T. J. Yen, D. C. Schwartz, C. L. Smith, J. D. Boeke, B. Sollner-Webb, and D. W. Cleveland. 1990. A rapidly rearranging retrotransposon within the miniexon gene locus of Crithidia fasciculata. Mol. Cell. Biol. 10:615-624.
27. Gottesdiener, K., J. Garcia-Anoveros, M. G. Lee, and L. H. Van der Ploeg. 1990. Chromosome organization of the protozoan Trypanosoma brucei. Mol. Cell. Biol. 10:6079-6083.
28. Harlow, E., and D. Lane (ed.). 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
29. 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.
30. Hope, M., A. MacLeod, V. Leech, S. Melville, J. Sasse, A. Tait, and C. M. Turner. 1999. Analysis of ploidy (in megabase chromosomes) in Trypanosoma brucei after genetic exchange. Mol. Biochem. Parasitol. 104:1-9.
31. Jurka, J. 1997. Sequence patterns indicate an enzymatic involvement in integration of mammalian retroposons. Proc. Natl. Acad. Sci. USA 94:1872-1877.
32. Kanmogne, G. D., M. Bailey, and W. C. Gibson. 1997. Wide variation in DNA content among isolates of Trypanosoma brucei ssp. Acta Trop. 63:75-87.
33. 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.
34. Kooter, J. M., H. J. van der Spek, R. Wagter, C. E. d'Oliveira, F. van der Hoeven, P. J. Johnson, and P. Borst. 1987. The anatomy and transcription of a telomeric expression site for variant-specific surface antigens in T. brucei. Cell 51:261-272.
35. Labrador, M., and V. G. Corces. 1997. Transposable element-host interactions: regulation of insertion and excision. Annu. Rev. Genet. 31:381-404.
36. LaCount, D. J., N. M. El-Sayed, S. Kaul, D. Wanless, C. M. Turner, and J. E. Donelson. 2001. Analysis of a donor gene region for a variant surface glycoprotein and its expression site in African trypanosomes. Nucleic Acids Res. 29:2012-2019.
37. Lanham, S. M., and D. G. Godfrey. 1970. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp. Parasitol. 28:521-534.
38. Levis, R. W., R. Ganesan, K. Houtchens, L. A. Tolar, and F. M. Sheen. 1993. Transposons in place of telomeric repeats at a Drosophila telomere. Cell 75:1083-1093.
39. Lodes, M. J., B. L. Smiley, A. W. Stadnyk, J. L. Bennett, P. J. Myler, and K. Stuart. 1993. Expression of a retroposon-like sequence upstream of the putative Trypanosoma brucei variant surface glycoprotein gene expression site promoter. Mol. Cell. Biol. 13:7036-7044.
40. Louis, E. J. 1995. The chromosome ends of Saccharomyces cerevisiae. Yeast 11:1553-1573.
41. Lu, Y., T. Hall, L. S. Gay, and J. E. Donelson. 1993. Point mutations are associated with a gene duplication leading to the bloodstream reexpression of a trypanosome metacyclic VSG. Cell 72:397-406.
42. Melville, S. E. 1997. Parasite genome analysis. Genome research in Trypanosoma brucei: chromosome size polymorphism and its relevance to genome mapping and analysis. Trans. R. Soc. Trop. Med. Hyg. 91:116-120.
43. Melville, S. E., C. S. Gerrard, and J. M. Blackwell. 1999. Multiple causes of size variation in the diploid megabase chromosomes of African trypanosomes. Chromosome Res. 7:191-203.
44. Melville, S. E., V. Leech, C. S. Gerrard, A. Tait, and J. M. Blackwell. 1998. The molecular karyotype of the megabase chromosomes of Trypanosoma brucei and the assignment of chromosome markers. Mol. Biochem. Parasitol. 94:155-173.
45. Melville, S. E., V. Leech, M. Navarro, and G. A. Cross. 2000. The molecular karyotype of the megabase chromosomes of Trypanosoma brucei stock 427. Mol. Biochem. Parasitol. 111:261-273.
46. Melville, S. E., N. S. Shepherd, C. S. Gerrard, and R. W. F. Le Page. 1996. Selection of chromosome-specific DNA clones from African trypanosome genomic libraries, p. 257-293. In B. Birren, and E. Lai (ed.), Analysis of non-mammalian genomes. Academic Press, New York, N.Y.
47. 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.
48. Olivares, M., C. Alonso, and M. C. Lopez. 1997. The open reading frame 1 of the L1Tc retrotransposon of Trypanosoma cruzi codes for a protein with apurinic-apyrimidinic nuclease activity. J. Biol. Chem. 272:25224-25228.
49. Olivares, M., M. del Carmen Thomas, A. Lopez-Barajas, J. M. Requena, J. L. Garcia-Perez, S. Angel, C. Alonso, and M. C. Lopez. 2000. Genomic clustering of the Trypanosoma cruzi nonlong terminal L1Tc retrotransposon with defined interspersed repeated DNA elements. Electrophoresis 21:2973-2982.
50. Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12:357-358.
51. Pays, E., S. Lips, D. Nolan, L. Vanhamme, and D. Perez-Morga. 2001. The VSG expression sites of Trypanosoma brucei: multipurpose tools for the adaptation of the parasite to mammalian hosts. Mol. Biochem. Parasitol. 114:1-16.
52. Pays, E., and N. B. Murphy. 1987. DNA-binding fingers encoded by a trypanosome retroposon. J. Mol. Biol. 197:147-148.
53. Pays, E., and D. P. Nolan. 1998. Expression and function of surface proteins in Trypanosoma brucei. Mol. Biochem. Parasitol. 91:3-36.
54. Pays, E., P. Tebabi, A. Pays, H. Coquelet, P. Revelard, D. Salmon, and M. Steinert. 1989. The genes and transcripts of an antigen gene expression site from Trypanosoma brucei. Cell. 57:835-845.
55. Pedram, M., and J. E. Donelson. 1999. The anatomy and transcription of a monocistronic expression site for a metacyclic variant surface glycoprotein gene in Trypanosoma brucei. J. Biol. Chem. 274:16876-16883.
56. Robertson, H. M., and K. L. Zumpano. 1997. Molecular evolution of an ancient mariner transposon, Hsmar1, in the human genome. Gene 205:203-217.
57. Sambrook, J., E. F. Fritsch, and T. Maniatis (ed.). 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
58. Schmidt, T. 1999. LINEs, SINEs and repetitive DNA: non-LTR retrotransposons in plant genomes. Plant Mol. Biol. 40:903-910.
59. Smiley, B. L., R. F. Aline, Jr., P. J. Myler, and K. Stuart. 1990. A retroposon in the 5′ flank of a Trypanosoma brucei VSG gene lacks insertional terminal repeats. Mol. Biochem. Parasitol. 42:143-152.
60. Smit, A. F. 1999. Interspersed repeats and other mementos of transposable elements in mammalian genomes. Curr. Opin. Genet. Dev. 9:657-663.
61. Smith, J. D., C. E. Chitnis, A. G. Craig, D. J. Roberts, D. E. Hudson-Taylor, D. S. Peterson, R. Pinches, C. I. Newbold, and L. H. Miller. 1995. Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101-110.
62. Su, X. Z., V. M. Heatwole, S. P. Wertheimer, F. Guinet, J. A. Herrfeldt, D. S. Peterson, J. A. Ravetch, and T. E. Wellems. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82:89-100.
63. Teng, S. C., S. X. Wang, and A. Gabriel. 1995. A new non-LTR retrotransposon provides evidence for multiple distinct site-specific elements in Crithidia fasciculata miniexon arrays. Nucleic Acids Res. 23:2929-2936.
64. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
65. Toth, M., J. Grimsby, G. Buzsaki, and G. P. Donovan. 1995. Epileptic seizures caused by inactivation of a novel gene, jerky, related to centromere binding protein-B in transgenic mice. Nat. Genet. 11:71-75.
66. Vanhamme, L., E. Pays, R. McCulloch, and J. D. Barry. 2001. An update on antigenic variation in African trypanosomes. Trends Parasitol. 17:338-343.
67. Villanueva, M. S., S. P. Williams, C. B. Beard, F. F. Richards, and S. Aksoy. 1991. A new member of a family of site-specific retrotransposons is present in the spliced leader RNA genes of Trypanosoma cruzi. Mol. Cell. Biol. 11:6139-6148.
68. Weiden, M., Y. N. Osheim, A. L. Beyer, and L. H. Van der Ploeg. 1991. Chromosome structure: DNA nucleotide sequence elements of a subset of the minichromosomes of the protozoan Trypanosoma brucei. Mol. Cell. Biol. 11:3823-3834.
69. Wellinger, R. J., and D. Sen. 1997. The DNA structures at the ends of eukaryotic chromosomes. Eur. J. Cancer 33:735-749.