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A 69 kDa immunodominant antigen of Trypanosoma (Nannomonas) congolense is homologous to immunoglobulin heavy chain binding protein (BiP)*

Published online by Cambridge University Press:  06 April 2009

A. Boulangé  and
E. Authié
A. Boulangé
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
E. Authié
Affiliation:
International Laboratory for Research on Animal Diseases, P.O. Box 30709, Nairobi, Kenya
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Summary

An immunodominant antigen in Trypanosoma congolense-infected cattle is a 69 kDa protein which is conserved among species and developmental stages of African trypanosomes. Immunoscreening of a cDNA expression library identified a 2·35 kbp clone which contains a complete open reading frame encoding a protein of 653 amino acids with a predicted molecular mass of 71 kDa. Protein sequence analyses revealed 45–65% identity with hsp70s from a broad range of organisms, the highest homology being with the mammalian BiP (immunoglobulin heavy chain binding protein). The 69 kDa trypanosome protein shares with other BiP-related molecules two characteristics that are associated with their localization in the endoplasmic reticulum and their function as chaperonins, i.e. a hydrophobic N-terminal signal sequence and a conserved C-terminal tetrapeptide (X)DEL. Divergence between the 69 kDa antigen and other BiP-homologues occurs in the C-terminal region. This may be responsible for the high immunogenicity of the trypanosome protein. The gene for the 69 kDa antigen appears to be present as a cluster of several copies which are not organized in tandem repeats. It is expressed in all developmental stages of T. congolense, but the specific mRNA levels are higher in metacyclics than in other stages.

Keywords

Trypanosoma (Nannomonas) congolenseinvariant antigenheat-shock proteinBiP/GRP78endoplasmic reticulum
Type
Research Article
Information
Parasitology , Volume 109 , Issue 2 , August 1994 , pp. 163 - 173
Copyright
Copyright © Cambridge University Press 1994

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References

REFERENCES

AuthiÉ, E., Muteti, D. K., Mbawa, Z., Lonsdale-Eccles, J. D., Webster, P. & Wells, C. (1992). Identification of major antigen of Trypanosoma congolense as a cysteine protease. Molecular and Biochemical Parasitology 56, 103–13.CrossRefGoogle ScholarPubMed
AuthiÉ, E., Muteti, D. K. & Williams, D. J. L. (1993). Antibody responses to invariant antigens of Trypanosoma congolense in cattle of differing susceptibility to trypanosomiasis. Parasite Immunology 15, 101–11.CrossRefGoogle ScholarPubMed
Bangs, J. D., Uyetake, L., Balber, A. E. & Boothroyd, J. C. (1993). Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei—divergent retention signals in a lower eukaryote. Journal of Cell Science, 105, 1101–14.CrossRefGoogle Scholar
Beynon, R. J. & Salvesen, G. (1989). Commercially available protease inhibitors. In Proteolytic Enzymes: A Practical Approach (ed. Beynon, R. J. & Bond, J. S.), pp. 241–246. Oxford: Oxford University Press.Google Scholar
Bhat, G. J., Souza, A. E., Feagin, J. E. & Stuart, K. (1992). Transcript-specific developmental regulation of polyadenylation in Trypanosoma brucei mitochondria. Molecular and Biochemical Parasitology 52, 231–40.CrossRefGoogle ScholarPubMed
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Annals of Biochemistry 162, 156–9.CrossRefGoogle ScholarPubMed
Coppens, I., Baudhuin, P., Opperdoes, F. R. & Courtoy, P. J. (1988). Receptors for the host low density lipoproteins on the hemoflagellate Trypanosoma brucei: purification and involvement in the growth of the parasite. Proceedings of the National Academy of Sciences, USA 85, 6753–7.CrossRefGoogle ScholarPubMed
Dragon, E. A., Sias, S. R., Kato, E. A. & Gabe, J. D. (1987). The genome of Trypanosoma cruzi contains a constitutively expressed, tandemly arranged multicopy gene homologous to a major heat shock protein. Molecular and Cellular Biology 7, 1271–5.Google ScholarPubMed
Dworniczak, B. & Mirault, M. E. (1987). Structure and expression of a human gene coding for a 71 kd heat shock ‘cognate’ protein. Nucleic Acids Research 15, 5181–7.CrossRefGoogle ScholarPubMed
Ellis, R. J. & Van De Vries, S. M. (1991). Molecular chaperones. Annual Reviews of Biochemistry 60, 321–47.CrossRefGoogle ScholarPubMed
Fish, W. R., Muriuki, C. W., Muthiani, A. M., Grab, D. J. & Lonsdale-Eccles, J. D. (1989). Disulfide bond involvement in the maintenance of the cryptic nature of the cross-reacting determinant of metacyclic forms of Trypanosoma congolense. Biochemistry 28, 5415–21.CrossRefGoogle ScholarPubMed
Gething, M.-J. & Sambrook, J. (1992). Protein folding in the cell. Nature, London 355, 33–45.CrossRefGoogle ScholarPubMed
Glass, D. J., Polvere, R. I. & Van Der Ploeg, L. H. T. (1986). Conserved sequences and transcription of the hsp70 gene family in Trypanosoma brucei. Molecular and Cellular Biology 6, 4657–66.Google ScholarPubMed
Grab, D. J., Russo, D., Naessens, J. & Verjee, Y. (1992). Transferrin binding proteins in Trypanosoma brucei. FASEB Journal 6, A1900.Google Scholar
Gray, A. R. & Luckins, A. G. (1976). Antigenic variation in salivarian trypanosomes. In Biology of the Kinetoplastida, vol. 1 (ed. Lumsden, W. H. R. & Evans, D. A.), pp. 493–530. London: Academic Press.Google Scholar
Haas, I. G. & Wabl, M. (1983). Immunoglobulin heavy chain binding protein. Nature, London 306, 387–9.CrossRefGoogle ScholarPubMed
Hall, T. & Esser, K. (1984). Topologic mapping of protective and nonprotective epitopes on the variant surface glycoprotein of the WRATat 1 clone of Trypanosoma brucei rhodesiense. Journal of Immunology 132, 2059–63.CrossRefGoogle ScholarPubMed
Higgins, D. G., Bleasby, A. J. & Fuchs, R. (1992). CLUSTAL V: improved software for multiple sequence alignment. Computer Applications to the Biosciences 8, 189–91.Google ScholarPubMed
Hunkapiller, M. W., Lujan, E., Ostrander, F. & Hood, L. E. (1983). Isolation of microgram quantities of proteins from polyacrylamide gels for amino acid sequence analysis. Methods in Enzymology 91, 227–36.CrossRefGoogle ScholarPubMed
Kumar, N. & Zheng, H. (1992). Nucleotide sequence of Plasmodium falciparum stress protein with similarity to mammalian 78 kDa glucose-regulated protein. Molecular and Biochemical Parasitology 56, 353–6.CrossRefGoogle ScholarPubMed
Kumar, N., Zhao, Y., Graves, P., Perez Folgar, J., Maloy, L. & Zheng, H. (1990). Human immune response directed against Plasmodium falciparum heat shock-related proteins. Infection and Immunity 58, 1408–14.CrossRefGoogle ScholarPubMed
Laemmli, U. K. (1970). Cleavage of the structural proteins during the assembly of the head of bacteriophage T4. Nature, London 227, 680–5.CrossRefGoogle ScholarPubMed
Lanham, S. M. & Godfrey, D. G. (1970). Isolation of salivarian trypanosomes using DEAE-cellulose. Experimental Parasitology 28, 521–34.CrossRefGoogle ScholarPubMed
Layden, R. E. & Eisen, H. (1988). Alternate trans splicing in Trypanosoma equiperdum: implications for splice site selection. Molecular and Cellular Biology 8, 1352–60.Google ScholarPubMed
Leeflang, P. J., Buys, J. & Blotkamp, C. (1976). Studies on Trypanosoma vivax: infectivity and serial maintenance of natural bovine isolates in mice. International Journal for Parasitology 6, 143–7.CrossRefGoogle ScholarPubMed
Lindquist, s. (1986). The heat shock response. Annual Reviews of Biochemistry 55, 1151–91.CrossRefGoogle ScholarPubMed
Majiwa, P. A. O., Hamers, R., Van Meirvenne, N. & Matthyssens, G. (1986). Evidence for genetic diversity in Trypanosoma (Nannomonas) congolense. Parasitology 93, 291–304.CrossRefGoogle ScholarPubMed
Matthews, R. & Burnie, J. (1992). The role of hsp90 in fungal infection. Immunology Today 13, 345–8.CrossRefGoogle ScholarPubMed
Munro, S. & Pelham, H. R. B. (1986). An hsp7O-like protein in the ER: identity with the 78 kDa glucose-regulated protein and immunoglobulin heavy chain binding protein. Cell 46, 291–300.CrossRefGoogle Scholar
Munro, S. & Pelham, H. R. B. (1987). A C-terminal signal prevents secretion of luminal ER proteins. Cell 48, 899–907.CrossRefGoogle ScholarPubMed
Nantulya, V. M., Musoke, A. J., Rurangirwa, F. R. & Moloo, S. K. (1984). Resistance of cattle to tsetse-transmitted challenge with Trypanosoma brucei or T. congolense after spontaneous recovery from syringe passaged infections. Infection and Immunity 43, 735–8.CrossRefGoogle ScholarPubMed
Neupert, W., Hartl, F. U., Craig, E. A. & Pfanner, N. (1990). How do polypeptides cross the mitochondrial membrane. Cell 63, 447–50.CrossRefGoogle Scholar
Newport, G., Culpepper, J. & Agabian, N. (1988). Parasite heat shock proteins. Parasitology Today 4, 306–12.CrossRefGoogle ScholarPubMed
Oi, V. T. & Herzenberg, L. A. (1980). Immunoglobulin-producing hybrid cell lines. In Selected Methods in Cellular Immunology (ed. Mishell, B. B. & Shiigi, S. M.), pp. 351–72. San Francisco: W. H. Freeman.Google Scholar
Pelham, H. R. B. (1986). Speculations on the functions of the major heat shock and glucose-regulated proteins. Cell 46, 959–61.CrossRefGoogle ScholarPubMed
Pelham, H. R. B. (1989). Control of protein exit from the endoplasmic reticulum. Annual Reviews of Cell Biology 5, 1–23.CrossRefGoogle ScholarPubMed
PellÉ, R. & Murphy, N. B. (1993). Northern hybridization: rapid and simple electrophoretic conditions. Nucleic Acids Research 21 2783–4.CrossRefGoogle ScholarPubMed
Perlman, D. & Halvorson, H. O. (1983). A putative signal peptidase recognition site and sequence in eukaryotic and prokaryotic signal peptides. Journal of Molecular Biology 167, 391–409.CrossRefGoogle ScholarPubMed
Requena, J. M., Jimenez-Ruiz, A., Soto, M., Assiego, R., SantarÉn, J. F., Lopez, M. C., Patarroyo, M. E. & Alonso, C. (1992). Regulation of hsp70 expression in Trypanosoma cruzi by temperature and growth phase. Molecular and Biochemical Parasitology 53, 201–12.CrossRefGoogle ScholarPubMed
Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd Edn.Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
Sanger, F., Nicklen, S. & Coulson, A. R. (1977). DNA sequencing with chain terminating inhibitors. Proceedings of the National Academy of Sciences, USA 74, 5463–75.CrossRefGoogle ScholarPubMed
Shermann, M. Y. & Goldberg, A. L. (1992). Involvement of the chaperonin dnaK in the rapid degradation of a mutant protein in Escherichia coli. EMBO Journal 11, 71–7.CrossRefGoogle Scholar
Towbin, H., Staehelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proceedings of the National Academy of Sciences, USA 76, 4350–4.CrossRefGoogle ScholarPubMed
Wellde, B., Lötzch, R., Deindl, G., Sadun, E., Williams, J. & Warui, G. (1974). Trypanosoma congolense. I. Clinical observations of experimentally infected cattle. Experimental Parasitology 36, 6–19.CrossRefGoogle ScholarPubMed
Williams, D. J. L., Newson, J. & Naessens, J. (1990). Quantification of bovine immunoglobulin isotypes and allotypes using monoclonal antibodies. Veterinary Immunology and Immunopathology 24, 267–83.CrossRefGoogle Scholar
Yanish-Perron, C., Vieira, J. & Messing, J. (1985). Improved M13 phage cloning vector and host strains:nucleotidic sequences of the M13mp18 and pUC19 vectors. Gene 33, 103–12.CrossRefGoogle Scholar
Yost, H. J. & Lindquist, S. (1991). Heat shock proteins affect RNA processing during the heat shock response of Saccharomyces cerevisiae. Molecular and Cellular Biology 11, 1062–8.Google ScholarPubMed
Young, R. A. & Davis, R. W. (1983). Efficient isolation of genes by using antibody probes. Proceedings of the National Academy of Sciences, USA 80, 1194–206.CrossRefGoogle ScholarPubMed