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. 1991 Apr;11(4):2180–2188. doi: 10.1128/mcb.11.4.2180

A family of genes related to a new expression site-associated gene in Trypanosoma equiperdum.

I C Florent 1, A Raibaud 1, H Eisen 1
PMCID: PMC359906  PMID: 1672441

Abstract

Two genes, belonging to a new expression site-associated gene family of six to eight members in Trypanosoma equiperdum and Trypanosoma brucei, have been cloned from a T. equiperdum variant. One of them, called ESAG-9c, is contained in the 1.78-C expression site and is found just upstream of the 5' barren region. The other one, called ESAG-9u, is unique in the family, is not telomere linked, and apparently is not expression site related. A 2-kb poly(A)+ mRNA is detected with probes for this ESAG-9 family in all T. equiperdum variants examined. By using polymerase chain reaction and restriction fragment length polymorphism techniques, it has been possible to distinguish between ESAG-9c and ESAG-9u and to show that ESAG-9c is transcribed in an expression site-specific manner. However, ESAG-9u (or another gene in the family having identical characteristics) is transcribed in all variants, regardless of the expression site used by these variants. Thus, this ESAG-9 family contains at least one gene that is under expression site control but might have other genes that are not. The function of these ESAG-9 genes is unknown. Transcripts homologous to ESAG-9 were detected in T. brucei bloodstream forms but not in procyclics.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Alexandre S., Guyaux M., Murphy N. B., Coquelet H., Pays A., Steinert M., Pays E. Putative genes of a variant-specific antigen gene transcription unit in Trypanosoma brucei. Mol Cell Biol. 1988 Jun;8(6):2367–2378. doi: 10.1128/mcb.8.6.2367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alexandre S., Paindavoine P., Tebabi P., Pays A., Halleux S., Steinert M., Pays E. Differential expression of a family of putative adenylate/guanylate cyclase genes in Trypanosoma brucei. Mol Biochem Parasitol. 1990 Dec;43(2):279–288. doi: 10.1016/0166-6851(90)90152-c. [DOI] [PubMed] [Google Scholar]
  3. Aline R., Jr, MacDonald G., Brown E., Allison J., Myler P., Rothwell V., Stuart K. (TAA)n within sequences flanking several intrachromosomal variant surface glycoprotein genes in Trypanosoma brucei. Nucleic Acids Res. 1985 May 10;13(9):3161–3177. doi: 10.1093/nar/13.9.3161. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Barnes D. A., Mottram J. C., Agabian N. Bloodstream and metacyclic variant surface glycoprotein gene expression sites of Trypanosoma brucei gambiense. Mol Biochem Parasitol. 1990 Jun;41(1):101–114. doi: 10.1016/0166-6851(90)90101-q. [DOI] [PubMed] [Google Scholar]
  5. Berger J., Howard A. D., Brink L., Gerber L., Hauber J., Cullen B. R., Udenfriend S. COOH-terminal requirements for the correct processing of a phosphatidylinositol-glycan anchored membrane protein. J Biol Chem. 1988 Jul 15;263(20):10016–10021. [PubMed] [Google Scholar]
  6. Bernards A., Kooter J. M., Borst P. Structure and transcription of a telomeric surface antigen gene of Trypanosoma brucei. Mol Cell Biol. 1985 Mar;5(3):545–553. doi: 10.1128/mcb.5.3.545. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Boothroyd J. C. Antigenic variation in African trypanosomes. Annu Rev Microbiol. 1985;39:475–502. doi: 10.1146/annurev.mi.39.100185.002355. [DOI] [PubMed] [Google Scholar]
  8. Boothroyd J. C., Cross G. A., Hoeijmakers J. H., Borst P. A variant surface glycoprotein of Trypanosoma brucei synthesized with a C-terminal hydrophobic 'tail' absent from purified glycoprotein. Nature. 1980 Dec 11;288(5791):624–626. doi: 10.1038/288624a0. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Campbell D. A., van Bree M. P., Boothroyd J. C. The 5'-limit of transposition and upstream barren region of a trypanosome VSG gene: tandem 76 base-pair repeats flanking (TAA)90. Nucleic Acids Res. 1984 Mar 26;12(6):2759–2774. doi: 10.1093/nar/12.6.2759. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Capbern A., Giroud C., Baltz T., Mattern P. Trypanosoma equiperdum: etude des variations antigéniques au cours de la trypanosomose experimentale du lapin. Exp Parasitol. 1977 Jun;42(1):6–13. doi: 10.1016/0014-4894(77)90055-8. [DOI] [PubMed] [Google Scholar]
  12. Caras I. W., Weddell G. N. Signal peptide for protein secretion directing glycophospholipid membrane anchor attachment. Science. 1989 Mar 3;243(4895):1196–1198. doi: 10.1126/science.2466338. [DOI] [PubMed] [Google Scholar]
  13. Cully D. F., Gibbs C. P., Cross G. A. Identification of proteins encoded by variant surface glycoprotein expression site-associated genes in Trypanosoma brucei. Mol Biochem Parasitol. 1986 Nov;21(2):189–197. doi: 10.1016/0166-6851(86)90022-8. [DOI] [PubMed] [Google Scholar]
  14. Cully D. F., Ip H. S., Cross G. A. Coordinate transcription of variant surface glycoprotein genes and an expression site associated gene family in Trypanosoma brucei. Cell. 1985 Aug;42(1):173–182. doi: 10.1016/s0092-8674(85)80113-6. [DOI] [PubMed] [Google Scholar]
  15. De Lange T., Borst P. Genomic environment of the expression-linked extra copies of genes for surface antigens of Trypanosoma brucei resembles the end of a chromosome. Nature. 1982 Sep 30;299(5882):451–453. doi: 10.1038/299451a0. [DOI] [PubMed] [Google Scholar]
  16. De Lange T., Kooter J. M., Luirink J., Borst P. Transcription of a transposed trypanosome surface antigen gene starts upstream of the transposed segment. EMBO J. 1985 Dec 1;4(12):3299–3306. doi: 10.1002/j.1460-2075.1985.tb04080.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dever T. E., Glynias M. J., Merrick W. C. GTP-binding domain: three consensus sequence elements with distinct spacing. Proc Natl Acad Sci U S A. 1987 Apr;84(7):1814–1818. doi: 10.1073/pnas.84.7.1814. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Donelson J. E., Rice-Ficht A. C. Molecular biology of trypanosome antigenic variation. Microbiol Rev. 1985 Jun;49(2):107–125. doi: 10.1128/mr.49.2.107-125.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  20. Ferguson M. A., Williams A. F. Cell-surface anchoring of proteins via glycosyl-phosphatidylinositol structures. Annu Rev Biochem. 1988;57:285–320. doi: 10.1146/annurev.bi.57.070188.001441. [DOI] [PubMed] [Google Scholar]
  21. Florent I., Baltz T., Raibaud A., Eisen H. On the role of repeated sequences 5' to variant surface glycoprotein genes in African trypanosomes. Gene. 1987;53(1):55–62. doi: 10.1016/0378-1119(87)90092-8. [DOI] [PubMed] [Google Scholar]
  22. Gibbs C. P., Cross G. A. Cloning and transcriptional analysis of a variant surface glycoprotein gene expression site in Trypanosoma brucei. Mol Biochem Parasitol. 1988 Apr;28(3):197–206. doi: 10.1016/0166-6851(88)90004-7. [DOI] [PubMed] [Google Scholar]
  23. Gubler U., Hoffman B. J. A simple and very efficient method for generating cDNA libraries. Gene. 1983 Nov;25(2-3):263–269. doi: 10.1016/0378-1119(83)90230-5. [DOI] [PubMed] [Google Scholar]
  24. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  25. Jefferies D., Tebabi P., Pays E. Transient activity assays of the Trypanosoma brucei variant surface glycoprotein gene promoter: control of gene expression at the posttranscriptional level. Mol Cell Biol. 1991 Jan;11(1):338–343. doi: 10.1128/mcb.11.1.338. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Johnson P. J., Kooter J. M., Borst P. Inactivation of transcription by UV irradiation of T. brucei provides evidence for a multicistronic transcription unit including a VSG gene. Cell. 1987 Oct 23;51(2):273–281. doi: 10.1016/0092-8674(87)90154-1. [DOI] [PubMed] [Google Scholar]
  27. 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]
  28. Kooter J. M., Winter A. J., de Oliveira C., Wagter R., Borst P. Boundaries of telomere conversion in Trypanosoma brucei. Gene. 1988 Sep 15;69(1):1–11. doi: 10.1016/0378-1119(88)90372-1. [DOI] [PubMed] [Google Scholar]
  29. 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]
  30. Kyte J., Doolittle R. F. A simple method for displaying the hydropathic character of a protein. J Mol Biol. 1982 May 5;157(1):105–132. doi: 10.1016/0022-2836(82)90515-0. [DOI] [PubMed] [Google Scholar]
  31. Laurent M., Pays E., Magnus E., Van Meirvenne N., Matthyssens G., Williams R. O., Steinert M. DNA rearrangements linked to expression of a predominant surface antigen gene of trypanosomes. Nature. 1983 Mar 17;302(5905):263–266. doi: 10.1038/302263a0. [DOI] [PubMed] [Google Scholar]
  32. Liu A. Y., Van der Ploeg L. H., Rijsewijk F. A., Borst P. The transposition unit of variant surface glycoprotein gene 118 of Trypanosoma brucei. Presence of repeated elements at its border and absence of promoter-associated sequences. J Mol Biol. 1983 Jun 15;167(1):57–75. doi: 10.1016/s0022-2836(83)80034-5. [DOI] [PubMed] [Google Scholar]
  33. 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]
  34. Pays E., Guyaux M., Aerts D., Van Meirvenne N., Steinert M. Telomeric reciprocal recombination as a possible mechanism for antigenic variation in trypanosomes. Nature. 1985 Aug 8;316(6028):562–564. doi: 10.1038/316562a0. [DOI] [PubMed] [Google Scholar]
  35. Pays E., Steinert M. Control of antigen gene expression in African trypanosomes. Annu Rev Genet. 1988;22:107–126. doi: 10.1146/annurev.ge.22.120188.000543. [DOI] [PubMed] [Google Scholar]
  36. Pays E., Tebabi P., Pays A., Coquelet H., Revelard P., Salmon D., Steinert M. The genes and transcripts of an antigen gene expression site from T. brucei. Cell. 1989 Jun 2;57(5):835–845. doi: 10.1016/0092-8674(89)90798-8. [DOI] [PubMed] [Google Scholar]
  37. Raibaud A., Buck G., Baltz T., Eisen H. Cloning and characterization of a variant surface glycoprotein expression site from Trypanosoma equiperdum. Mol Cell Biol. 1986 Aug;6(8):2950–2956. doi: 10.1128/mcb.6.8.2950. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Schowalter D. B., Sommer S. S. The generation of radiolabeled DNA and RNA probes with polymerase chain reaction. Anal Biochem. 1989 Feb 15;177(1):90–94. doi: 10.1016/0003-2697(89)90019-5. [DOI] [PubMed] [Google Scholar]
  40. Shah J. S., Young J. R., Kimmel B. E., Iams K. P., Williams R. O. The 5' flanking sequence of a Trypanosoma brucei variable surface glycoprotein gene. Mol Biochem Parasitol. 1987 Jun;24(2):163–174. doi: 10.1016/0166-6851(87)90103-4. [DOI] [PubMed] [Google Scholar]
  41. Shea C., Lee M. G., Van der Ploeg L. H. VSG gene 118 is transcribed from a cotransposed pol I-like promoter. Cell. 1987 Aug 14;50(4):603–612. doi: 10.1016/0092-8674(87)90033-x. [DOI] [PubMed] [Google Scholar]
  42. Shea C., Van der Ploeg L. H. Stable variant-specific transcripts of the variant cell surface glycoprotein gene 1.8 expression site in Trypanosoma brucei. Mol Cell Biol. 1988 Feb;8(2):854–859. doi: 10.1128/mcb.8.2.854. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Smiley B. L., Stadnyk A. W., Myler P. J., Stuart K. The trypanosome leucine repeat gene in the variant surface glycoprotein expression site encodes a putative metal-binding domain and a region resembling protein-binding domains of yeast, Drosophila, and mammalian proteins. Mol Cell Biol. 1990 Dec;10(12):6436–6444. doi: 10.1128/mcb.10.12.6436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Son H. J., Cook G. A., Hall T., Donelson J. E. Expression site associated genes of Trypanosoma brucei rhodesiense. Mol Biochem Parasitol. 1989 Feb;33(1):59–66. doi: 10.1016/0166-6851(89)90042-x. [DOI] [PubMed] [Google Scholar]
  45. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  46. 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]
  47. Vickerman K. Developmental cycles and biology of pathogenic trypanosomes. Br Med Bull. 1985 Apr;41(2):105–114. doi: 10.1093/oxfordjournals.bmb.a072036. [DOI] [PubMed] [Google Scholar]
  48. Vieira J., Messing J. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene. 1982 Oct;19(3):259–268. doi: 10.1016/0378-1119(82)90015-4. [DOI] [PubMed] [Google Scholar]
  49. von Heijne G. Patterns of amino acids near signal-sequence cleavage sites. Eur J Biochem. 1983 Jun 1;133(1):17–21. doi: 10.1111/j.1432-1033.1983.tb07424.x. [DOI] [PubMed] [Google Scholar]

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