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Redundancy and recombination in the Echinococcus AgB multigene family: is there any similarity with protozoan contingency genes?

Published online by Cambridge University Press:  04 July 2006

K. L. HAAG ,
B. GOTTSTEIN ,
N. MÜLLER ,
A. SCHNORR  and
F. J. AYALA
K. L. HAAG
Affiliation:
Department of Genetics, Institute of Biological Sciences, UFRGS, Porto Alegre, 91501-970 RS, Brazil PPGBM, Institute of Biological Sciences, UFRGS, Porto Alegre, 91501-970 RS, Brazil
B. GOTTSTEIN
Affiliation:
Institute of Parasitology, Faculty of Medicine and Veterinary Medicine, University of Berne, Berne, CH-3001, Switzerland
N. MÜLLER
Affiliation:
Institute of Parasitology, Faculty of Medicine and Veterinary Medicine, University of Berne, Berne, CH-3001, Switzerland
A. SCHNORR
Affiliation:
PPGBM, Institute of Biological Sciences, UFRGS, Porto Alegre, 91501-970 RS, Brazil
F. J. AYALA
Affiliation:
Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697, USA
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Abstract

Numerous genetic variants of the Echinococcus antigen B (AgB) are encountered within a single metacestode. This could be a reflection of gene redundancy or the result of a somatic hypermutation process. We evaluate the complexity of the AgB multigene family by characterizing the upstream promoter regions of the 4 already known genes (EgAgB1-EgAgB4) and evaluating their redundancy in the genome of 3 Echinococcus species (E. granulosus, E. ortleppi and E. multilocularis) using PCR-based approaches. We have ascertained that the number of AgB gene copies is quite variable, both within and between species. The most repetitive gene seems to be AgB3, of which there are more than 110 copies in E. ortleppi. For E. granulosus, we have cloned and characterized 10 distinct upstream promoter regions of AgB3 from a single metacestode. Our sequences suggest that AgB1 and AgB3 are involved in gene conversion. These results are discussed in light of the role of gene redundancy and recombination in parasite evasion mechanisms of host immunity, which at present are known for protozoan organisms, but virtually unknown for multicellular parasites.

Keywords

hydatid diseaseantigen Bpromoterrecombinationantigen diversityreal-time PCR
Type
Research Article
Information
Parasitology , Volume 133 , Issue 4 , October 2006 , pp. 411 - 419
Copyright
© 2006 Cambridge University Press

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References

REFERENCES

Arend, A. C., Zaha, A., Ayala, F. J. and Haag, K. L. ( 2004). The Echinococcus granulosus antigen B shows a high degree of genetic variability. Experimental Parasitology 108, 76–80.CrossRefGoogle Scholar
Berriman, M., Ghedin, E., Hertz-Fowler, C., Blandin, G., Renauld, H., Bartholomeu, D. C., Lennard, N. J., Caler, E., Hamlin, N. E., Haas, B., Bohme, U., Hannick, L., Aslett, M. A., Shallom, J., Marcello, L., Hou, L., Wickstead, B., Alsmark, U. C., Arrowsmith, C., Atkin, R. J., Barron, A. J., Bringaud, F., Brooks, K., Carrington, M., Cherevach, I., Chillingworth, T. J., Churcher, C., Clark, L. N., Corton, C. H., Cronin, A., Davies, R. M., Doggett, J., Djikeng, A., Feldblyum, T., Field, M. C., Fraser, A., Goodhead, I., Hance, Z., Harper, D., Harris, B. R., Hauser, H., Hostetler, J., Ivens, A., Jagels, K., Johnson, D., Johnson, J., Jones, K., Kerhornou, A. X., Koo, H., Larke, N., Landfear, S., Larkin, C., Leech, V., Line, A., Lord, A., Macleod, A., Mooney, P. J., Moule, S., Martin, D. M., Morgan, G. W., Mungall, K., Norbertczak, H., Ormond, D., Pai, G., Peacock, C. S., Peterson, J., Quail, M. A., Rabbinowitsch, E., Rajandream, M. A., Reitter, C., Salzberg, S. L., Sanders, M., Schobel, S., Sharp, S., Simmonds, M., Simpson, A. J., Tallon, L., Turner, C. M., Tait, A., Tivey, A. R., Van Aken, S., Walker, D., Wanless, D., Wang, S., White, B., White, O., Whitehead, S., Woodward, J., Wortman, J., Adams, M. D., Embley, T. M., Gull, K., Ullu, E., Barry, J. D., Fairlamb, A. H., Opperdoes, F., Barrell, B. G., Donelson, J. E., Hall, N., Fraser, C. M., Melville, S. E. and El-Sayed, N. M. ( 2005). The genome of the African trypanosome Trypanosoma brucei. Science 309, 416–422.CrossRefGoogle Scholar
Borst, P. and Ulbert, S. ( 2001). Control of VSG expression sites. Molecular and Biochemical Parasitology 114, 17–27.CrossRefGoogle Scholar
Bowles, J., Blair, D. and McManus, D. P. ( 1992). Genetic variants within the genus Echinococcus identified by mitochondrial DNA sequencing. Molecular and Biochemical Parasitology 54, 165–174.CrossRefGoogle Scholar
Chemale, G., Ferreira, H. B., Barrett, J., Brophy, P. M. and Zaha, A. ( 2005). Echinococcus granulosus antigen B hydrophobic ligand binding properties. Biochimica et Biophysica Acta 1747, 189–194.CrossRefGoogle Scholar
Chemale, G., Haag, K. L., Ferreira, H. and Zaha, A. ( 2001). Echinococcus granulosus antigen B is encoded by a gene family. Molecular and Biochemical Parasitology 116, 233–237.CrossRefGoogle Scholar
Fernández, V., Ferreira, H. B., Fernandez, C. and Zaha, A. ( 1996). Molecular characterization of a novel 8-kDa subunit of Echinococcus granulosus antigen B. Molecular and Biochemical Parasitology 77, 247–250.CrossRefGoogle Scholar
Haag, K. L., Alves-Junior, L., Zaha, A. and Ayala, F. J. ( 2004). Contingent, non-neutral evolution in a multicellular parasite: natural selection and gene conversion in the Echinococcus granulosus antigen B gene family. Gene 333, 157–167.CrossRefGoogle Scholar
Haag, K. L., Zanotto, P. M., Alves-Junior, L., Gasser, R., Zaha, A. and Ayala, F. J. ( 2006). Searching for AgB genes and their adaptive sites in distinct strains and species of the helminth Echinococcus. Infection, Genetics and Evolution 6, 251–261.CrossRefGoogle Scholar
Hall, T. A. ( 1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Machado, C. R., Augusto-Pinto, L., McCulloch, R. and Teixeira, S. M. ( 2006). DNA metabolism and genetic diversity in trypanosomes. Mutation Research 612, 40–57.CrossRefGoogle Scholar
Mamuti, W., Sako, Y., Xiao, N., Nakaya, K., Nakao, M., Yamasaki, H., Lightowlers, M. W. and Ito, A. ( 2006). Echinococcus multilocularis: Developmental stage-specific expression of Antigen B 8-kDa-subunits. Experimental Parasitology, Epub ahead of print, Feb. 1.CrossRef
Mukai, H. and Nakagawa, T. ( 1996). Long and accurate PCR (LA PCR). Nippon Rinsho 54, 917–922.Google Scholar
Pays, E. ( 2005). Regulation of antigen gene expression in Trypanosoma brucei. Trends in Parasitology 21, 517–520.CrossRefGoogle Scholar
Riganò, R., Buttari, B., de Falco, E., Profumo, E., Ortona, E., Marguti, P., Scottà, C., Teggi, A. and Siracusano, A. ( 2004). Echinococcus granulosus-specific T-cell lines derived from patients at various clinical stages of cystic echinococcosis. Parasite Immunology 26, 45–52.CrossRefGoogle Scholar
Riganò, R., Profumo, E., Bruschi, F., Carulli, G., Azarrà, A., Ioppolo, S., Buttari, B., Ortona, E., Margutti, P., Teggi, A. and Siracusano, A. ( 2001). Modulation of human immune response by Echinococcus granulosus antigen B and its possible role in evading host defenses. Infection and Immunity 69, 288–296.CrossRefGoogle Scholar
Roese, M. G. ( 2001). Application of a time-delay neural network to promoter annotation in the Drosophila melanogaster genome. Computational Chemistry 26, 51–56.CrossRefGoogle Scholar
Sawyer, S. ( 1989). Statistical tests for detecting gene conversion. Molecular Biology and Evolution 6, 526–538.Google Scholar
Shepherd, J., Aitken, A. and McManus, D. P. ( 1991). A protein secreted in vivo by Echinococcus granulosus inhibits elastase activity and neutrophil chemotaxis. Molecular and Biochemical Parasitology 44, 81–90.CrossRefGoogle Scholar
Voss, T. S., Kaestli, M., Vogel, D., Bopp, S. and Beck, H.-P. ( 2003). Identification of nuclear proteins that interact differentially with Plasmodium falciparum var gene promoters. Molecular Microbiology 48, 1593–1607.CrossRefGoogle Scholar
Zhang, W., You, H., Li, J., Zhang, Z., Turson, G., Aili, H., Wang, J. and McManus, D. P. ( 2003). Immunoglobulin profiles in a murine intermediate host model of resistance for Echinococcus granulosus infection. Parasite Immunology 25, 161–168.CrossRefGoogle Scholar