Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1983 Dec 10;11(23):8343–8357. doi: 10.1093/nar/11.23.8343

An African trypanosome variant surface glycoprotein gene whose expression is not activated by duplication.

N A Penncavage, M A Julius, K B Marcu
PMCID: PMC326586  PMID: 6324082

Abstract

A variant surface glycoprotein (VSG) of Trypanosoma brucei is encoded by a gene whose expression is not governed by duplication-transposition. There are two copies of this gene. The 5' flanking regions of the two genes are indistinguishable by restriction mapping, although each possesses approximately 5-10 Kbp of DNA which is devoid of restriction sites. All restriction enzymes tested appeared to cut genomic DNA at a uniform distance 3' of the gene. This, coupled with the observed sensitivity of both genes to BAL 31, indicates that they lie near chromosomal termini. Length variation occurs 3' of these genes in bloodstream clones and their procyclic derivatives, although the number of length variants is conserved. This suggests that length variation alone does not control VSG switching or gene expression and that constraints exist on the extent to which 3' flanking regions can vary in length.

Full text

PDF
8343

Images in this article

Selected References

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

  1. Bernards A., Michels P. A., Lincke C. R., Borst P. Growth of chromosome ends in multiplying trypanosomes. Nature. 1983 Jun 16;303(5918):592–597. doi: 10.1038/303592a0. [DOI] [PubMed] [Google Scholar]
  2. 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]
  3. Blin N., von Gabain A., Bujard H. Isolation of large molecular weight DNA from agarose gels for further digestion by restriction enzymes. FEBS Lett. 1975 Apr 15;53(1):84–86. doi: 10.1016/0014-5793(75)80688-0. [DOI] [PubMed] [Google Scholar]
  4. Borst P., Cross G. A. Molecular basis for trypanosome antigenic variation. Cell. 1982 Jun;29(2):291–303. doi: 10.1016/0092-8674(82)90146-5. [DOI] [PubMed] [Google Scholar]
  5. 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]
  6. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  7. 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]
  8. Cunningham I. New culture medium for maintenance of tsetse tissues and growth of trypanosomatids. J Protozool. 1977 May;24(2):325–329. doi: 10.1111/j.1550-7408.1977.tb00987.x. [DOI] [PubMed] [Google Scholar]
  9. 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]
  10. Donelson J. E., Young J. R., Dorfman D., Majiwa P. A., Williams R. O. The ILtat 1.4 surface antigen gene family of Trypanosoma brucei. Nucleic Acids Res. 1982 Nov 11;10(21):6581–6595. doi: 10.1093/nar/10.21.6581. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Glisin V., Crkvenjakov R., Byus C. Ribonucleic acid isolated by cesium chloride centrifugation. Biochemistry. 1974 Jun 4;13(12):2633–2637. doi: 10.1021/bi00709a025. [DOI] [PubMed] [Google Scholar]
  12. Hoeijmakers J. H., Frasch A. C., Bernards A., Borst P., Cross G. A. Novel expression-linked copies of the genes for variant surface antigens in trypanosomes. Nature. 1980 Mar 6;284(5751):78–80. doi: 10.1038/284078a0. [DOI] [PubMed] [Google Scholar]
  13. Honigberg B. M., Cunningham I., Stanley H. A., Su-Lin K. E., Luckins A. G. Trypanosoma brucei: antigenic analysis of bloodstream, vector, and culture stages by the quantitative fluorescent antibody methods. Exp Parasitol. 1976 Jun;39(3):496–522. doi: 10.1016/0014-4894(76)90052-7. [DOI] [PubMed] [Google Scholar]
  14. Lanham S. M., Godfrey D. G. Isolation of salivarian trypanosomes from man and other mammals using DEAE-cellulose. Exp Parasitol. 1970 Dec;28(3):521–534. doi: 10.1016/0014-4894(70)90120-7. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Longacre S., Raibaud A., Hibner U., Buck G., Eisen H., Baltz T., Giroud C., Baltz D. DNA rearrangements and antigenic variation in Trypanosoma equiperdum: expression-independent DNA rearrangements in the basic copy of a variant surface glycoprotein gene. Mol Cell Biol. 1983 Mar;3(3):410–414. doi: 10.1128/mcb.3.3.410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Majiwa P. A., Young J. R., Englund P. T., Shapiro S. Z., Williams R. O. Two distinct forms of surface antigen gene rearrangement in Trypanosoma brucei. Nature. 1982 Jun 10;297(5866):514–516. doi: 10.1038/297514a0. [DOI] [PubMed] [Google Scholar]
  18. Marcu K. B., Banerji J., Penncavage N. A., Lang R., Arnheim N. 5' flanking region of immunoglobulin heavy chain constant region genes displays length heterogeneity in germlines of inbred mouse strains. Cell. 1980 Nov;22(1 Pt 1):187–196. doi: 10.1016/0092-8674(80)90167-1. [DOI] [PubMed] [Google Scholar]
  19. McNeillage G. J., Herbert W. J., Lumsden W. H. Antigenic type of first relapse variants arising from a strain of Trypanosoma (Trypanozoon) brucei. Exp Parasitol. 1969 Aug;25(1):1–7. doi: 10.1016/0014-4894(69)90046-0. [DOI] [PubMed] [Google Scholar]
  20. Pays E., Lheureux M., Steinert M. Analysis of the DNA and RNA changes associated with the expression of isotypic variant-specific antigens of trypanosomes. Nucleic Acids Res. 1981 Sep 11;9(17):4225–4238. doi: 10.1093/nar/9.17.4225. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Pays E., Lheureux M., Steinert M. Structure and expression of a Trypanosoma brucei gambiense variant specific antigen gene. Nucleic Acids Res. 1982 May 25;10(10):3149–3163. doi: 10.1093/nar/10.10.3149. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Pays E., Lheureux M., Steinert M. The expression-linked copy of a surface antigen gene in Trypanosoma is probably the one transcribed. Nature. 1981 Jul 16;292(5820):265–267. doi: 10.1038/292265a0. [DOI] [PubMed] [Google Scholar]
  23. Pays E., Van Meirvenne N., Le Ray D., Steinert M. Gene duplication and transposition linked to antigenic variation in Trypanosoma brucei. Proc Natl Acad Sci U S A. 1981 May;78(5):2673–2677. doi: 10.1073/pnas.78.5.2673. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Raibaud A., Gaillard C., Longacre S., Hibner U., Buck G., Bernardi G., Eisen H. Genomic environment of variant surface antigen genes of Trypanosoma equiperdum. Proc Natl Acad Sci U S A. 1983 Jul;80(14):4306–4310. doi: 10.1073/pnas.80.14.4306. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. SEED J. R. ANTIGENIC SIMILARITY AMONG CULTURE FORMS OF THE 'BRUCEI' GROUP OF TRYPANOSOMES. Parasitology. 1964 Aug;54:593–596. doi: 10.1017/s0031182000082639. [DOI] [PubMed] [Google Scholar]
  26. 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]
  27. Stalder J., Groudine M., Dodgson J. B., Engel J. D., Weintraub H. Hb switching in chickens. Cell. 1980 Apr;19(4):973–980. doi: 10.1016/0092-8674(80)90088-4. [DOI] [PubMed] [Google Scholar]
  28. Steiger R. F. On the ultrastructure of Trypanosoma (Trypanozoon) brucei in the course of its life cycle and some related aspects. Acta Trop. 1973;30(1):64–168. [PubMed] [Google Scholar]
  29. Van Meirvenne N., Janssens P. G., Magnus E. Antigenic variation in syringe passaged populations of Trypanosoma (Trypanozoon) brucei. 1. Rationalization of the experimental approach. Ann Soc Belg Med Trop. 1975;55(1):1–23. [PubMed] [Google Scholar]
  30. Van der Ploeg L. H., Bernards A., Rijsewijk F. A., Borst P. Characterization of the DNA duplication-transposition that controls the expression of two genes for variant surface glycoproteins in Trypanosoma brucei. Nucleic Acids Res. 1982 Jan 22;10(2):593–609. doi: 10.1093/nar/10.2.593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Van der Ploeg L. H., Liu A. Y., Michels P. A., De Lange T., Borst P., Majumder H. K., Weber H., Veeneman G. H., Van Boom J. RNA splicing is required to make the messenger RNA for a variant surface antigen in trypanosomes. Nucleic Acids Res. 1982 Jun 25;10(12):3591–3604. doi: 10.1093/nar/10.12.3591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Van der Ploeg L. H., Valerio D., De Lange T., Bernards A., Borst P., Grosveld F. G. An analysis of cosmid clones of nuclear DNA from Trypanosoma brucei shows that the genes for variant surface glycoproteins are clustered in the genome. Nucleic Acids Res. 1982 Oct 11;10(19):5905–5923. doi: 10.1093/nar/10.19.5905. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vickerman K., Luckins A. G. Localization of variable antigens in the surface coat of Trypanosoma brucei using ferritin conjugated antibody. Nature. 1969 Dec 13;224(5224):1125–1126. doi: 10.1038/2241125a0. [DOI] [PubMed] [Google Scholar]
  34. Wahl G. M., Stern M., Stark G. R. Efficient transfer of large DNA fragments from agarose gels to diazobenzyloxymethyl-paper and rapid hybridization by using dextran sulfate. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3683–3687. doi: 10.1073/pnas.76.8.3683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Weintraub H., Groudine M. Chromosomal subunits in active genes have an altered conformation. Science. 1976 Sep 3;193(4256):848–856. doi: 10.1126/science.948749. [DOI] [PubMed] [Google Scholar]
  36. Weisbrod S. Active chromatin. Nature. 1982 May 27;297(5864):289–295. doi: 10.1038/297289a0. [DOI] [PubMed] [Google Scholar]
  37. Williams R. O., Young J. R., Majiwa P. A., Doyle J. J., Shapiro S. Z. Contextural genomic rearrangements of variable-antigen genes in Trypanosoma brucei. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):945–949. doi: 10.1101/sqb.1981.045.01.111. [DOI] [PubMed] [Google Scholar]
  38. Williams R. O., Young J. R., Majiwa P. A. Genomic environment of T. brucei VSG genes: presence of a minichromosome. Nature. 1982 Sep 30;299(5882):417–421. doi: 10.1038/299417a0. [DOI] [PubMed] [Google Scholar]
  39. Williams R. O., Young J. R., Majiwa P. A. Genomic rearrangements correlated with antigenic variation in Trypanosoma brucei. Nature. 1979 Dec 20;282(5741):847–849. doi: 10.1038/282847a0. [DOI] [PubMed] [Google Scholar]
  40. Young J. R., Donelson J. E., Majiwa P. A., Shapiro S. Z., Williams R. O. analysis of genomic rearrangements associated with two variable antigen genes of Trypanosoma brucei. Nucleic Acids Res. 1982 Feb 11;10(3):803–819. doi: 10.1093/nar/10.3.803. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Young J. R., Shah J. S., Matthyssens G., Williams R. O. Relationship between multiple copies of a T. brucei variable surface glycoprotein gene whose expression is not controlled by duplication. Cell. 1983 Apr;32(4):1149–1159. doi: 10.1016/0092-8674(83)90298-2. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES