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Complexity of the major surface protease (msp) gene organization in Leishmania (Viannia) braziliensis: evolutionary and functional implications

Published online by Cambridge University Press:  24 March 2005

K. VICTOIR ,
J. AREVALO ,
S. DE DONCKER ,
D. C. BARKER ,
T. LAURENT ,
E. GODFROID ,
A. BOLLEN ,
D. LE RAY  and
J. C. DUJARDIN
K. VICTOIR
Affiliation:
Laboratory of Molecular Parasitology, Instituut voor Tropische Geneeskunde ‘Prins Leopold’, 155 Nationalestraat, B-2000 Antwerpen, Belgium
J. AREVALO
Affiliation:
Departamento de Bioquimica, Biologia Molecular y Farmacología, Facultad de Ciencias y Filosofía and Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, A.P. 5045, Lima 100, Peru
S. DE DONCKER
Affiliation:
Laboratory of Molecular Parasitology, Instituut voor Tropische Geneeskunde ‘Prins Leopold’, 155 Nationalestraat, B-2000 Antwerpen, Belgium
D. C. BARKER
Affiliation:
Cambridge University, Department of Pathology, Tennis Court Road, Cambridge CB2 1QP, UK
T. LAURENT
Affiliation:
Laboratory of Molecular Parasitology, Instituut voor Tropische Geneeskunde ‘Prins Leopold’, 155 Nationalestraat, B-2000 Antwerpen, Belgium
E. GODFROID
Affiliation:
Applied Genetics, IBMM, Université Libre de Bruxelles, Gosselies, Belgium
A. BOLLEN
Affiliation:
Applied Genetics, IBMM, Université Libre de Bruxelles, Gosselies, Belgium
D. LE RAY
Affiliation:
Laboratory of Molecular Parasitology, Instituut voor Tropische Geneeskunde ‘Prins Leopold’, 155 Nationalestraat, B-2000 Antwerpen, Belgium
J. C. DUJARDIN
Affiliation:
Laboratory of Molecular Parasitology, Instituut voor Tropische Geneeskunde ‘Prins Leopold’, 155 Nationalestraat, B-2000 Antwerpen, Belgium
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Abstract

The major surface protease (msp or gp63) of Leishmania plays a major role in the host–parasite interaction. We analysed here the structure of the msp gene locus in Leishmania (Viannia) braziliensis and compared it to results obtained in other species. Physical mapping of cosmid contigs revealed a minimum of 37 genes per haploid genome and at least 8 different msp gene families. Within the same organism, these genes showed a nucleotide sequence varying in certain stretches from 3 to 34%, and a mosaic structure. From an evolutionary point of view, major differences were observed between subgenera Viannia and Leishmania, both in terms of msp gene number and sequence. Within subgenus Viannia, phenetic analysis revealed three clusters in which sequence variants of L. (Viannia) braziliensis and L. (Viannia) guyanensis were interspersed. Functional implications of our results were explored from predicted L. (Viannia) braziliensis protein sequences: regions encoding the msp catalytic site showed a conserved sequence, while regions encoding surface domains possibly involved in the host–parasite interaction (macrophage adhesion sites and immunodominant B-cell and T-cell epitopes) were variable. We speculate that this would be an adaptive strategy of the parasite.

Keywords

gp63leishmanolysinLeishmania (Viannia) braziliensisgenome organizationtelomerecosmidepitopes
Type
Research Article
Information
Parasitology , Volume 131 , Issue 2 , August 2005 , pp. 207 - 214
Copyright
2005 Cambridge University Press

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References

REFERENCES

ALVAREZ-VALIN, F., TORT, J. F. & BERNARDI, G. ( 2000). Nonrandom spatial distribution of synonymous substitutions in the GP63 gene from Leishmania. Genetics 155, 1683–1692.Google Scholar
BAÑULS, A. L., GUERRINI, F., LE PONT, F., BARRERA, C., ESPINEL, I., GUDERIAN, R., ECHEVERRIA, R. & TIBAYRENC, M. ( 1997). Evidence for hybridization by multilocus enzyme electrophoresis and random amplified polymorphic DNA between Leishmania braziliensis and Leishmania panamensis/guyanensis in Ecuador. Journal of Eukaryotic Microbiology 44, 408–411.CrossRefGoogle Scholar
BRITTINGHAM, A., CHEN, G., McGWIRE, B. S., CHANG, K. P. & MOSSER, D. M. ( 1999). Interaction of Leishmania gp63 with cellular receptors for fibronectin. Infection and Immunity 67, 4477–4484.Google Scholar
CONWAY, D. J., ROPER, C., ODUOLA, A. M., ARNOT, D. E., KREMSNER, P. G., GROBUSCH, M. P., CURTIS, C. F. & GREENWOOD, B. M. ( 1999). High recombination rate in natural populations of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 96, 4506–4511.CrossRefGoogle Scholar
DUJARDIN, J. C., LLANOS-CUENTAS, A., CACERES, A., ARANA, M., DUJARDIN, J. P., GUERRINI, F., GOMEZ, J., ARROYO, J., DE DONCKER, S. & JACQUET, D. ( 1993). Molecular karyotype variation in Leishmania (Viannia) peruviana: indication of geographical populations in Peru distributed along a north-south cline. Annals of Tropical Medicine and Parasitology 87, 335–347.CrossRefGoogle Scholar
EL-SAYED, N. M. & DONELSON, J. E. ( 1997). African trypanosomes have differentially expressed genes encoding homologues of the LeishmaniaGP63 surface protease. Journal of Biological Chemistry 272, 26742–26748.CrossRefGoogle Scholar
ETGES, R. ( 1992). Identification of a surface metalloproteinase on 13 species of Leishmania isolated from humans, Crithidia fasciculata, and Herpetomonas samuelpessoai. Acta Tropica 50, 205–217.CrossRefGoogle Scholar
FU, G. & BARKER, D. C. ( 1998). Characterisation of Leishmania telomeres reveals unusual telomeric repeats and conserved telomere-associated sequence. Nucleic Acids Research 26, 2161–2167.CrossRefGoogle Scholar
GALTIER, N., GOUY, M. & GAUTIER, C. ( 1996). SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Computer Application in Biosciences 12, 543–554.CrossRefGoogle Scholar
GRANDGENETT, P. M., COUGHLIN, B. C., KIRCHHOFF, L. V. & DONELSON, J. E. ( 2000). Differential expression of GP63 genes in Trypanosoma cruzi. Molecular and Biochemical Parasitology 110, 409–415.CrossRefGoogle Scholar
GUBBELS, M. J., KATZER, F., HIDE, G., JONGEJAN, F. & SHIELS, B. R. ( 2000). Generation of a mosaic pattern of diversity in the major merozoite-piroplasm surface antigen of Theileria annulata. Molecular and Biochemical Parasitology 110, 23–32.CrossRefGoogle Scholar
GUERBOUJ, S., VICTOIR, K., GUIZANI, I., SERIDI, N., NUWAYRI-SALTI, N., BELKAID, M., ISMAIL, R. B., LE RAY, D. & DUJARDIN, J. C. ( 2001). Gp63 gene polymorphism and population structure of Leishmaniadonovani complex: influence of the host selection pressure? Parasitology 122, 25–35.Google Scholar
INGA, R., DE DONCKER, S., GOMEZ, J., LOPEZ, M., GARCIA, R., LE RAY, D., AREVALO, J. & DUJARDIN, J. C. ( 1998). Relation between variation in copy number of ribosomal RNA encoding genes and size of harbouring chromosomes in Leishmania of subgenus Viannia. Molecular and Biochemical Parasitology 92, 219–228.CrossRefGoogle Scholar
INVERSO, J. A., MEDINA-ACOSTA, E., O'CONNOR, J., RUSSELL, D. G. & CROSS, G. A. ( 1993). Crithidia fasciculata contains a transcribed leishmanial surface proteinase (gp63) gene homologue. Molecular and Biochemical Parasitology 57, 47–54.CrossRefGoogle Scholar
IOVANNISCI, D. M. & BEVERLEY, S. M. ( 1989). Structural alterations of chromosome 2 in Leishmania major as evidence for diploidy, including spontaneous amplification of the mini-exon array. Molecular and Biochemical Parasitology 34, 177–188.CrossRefGoogle Scholar
JANEWAY, C. A. & TRAVERS, P. ( 1996). Immunobiology. The Immune System in Health and Disease. Current Biology Ltd, London, San Francisco and Philadelphia.
JOSHI, P. B., KELLY, B. L., KAMHAWI, S., SACKS, D. L. & McMASTER, W. R. ( 2002). Targeted gene deletion in Leishmania major identifies leishmanolysin (gp63) as a virulence factor. Molecular and Biochemical Parasitology 120, 33–40.CrossRefGoogle Scholar
KEBEDE, A., DE DONCKER, S., AREVALO, J., LE RAY, D. & DUJARDIN, J. C. ( 1999). Size-polymorphism of mini-exon gene-bearing chromosomes among natural populations of Leishmania, subgenus Viannia. International Journal for Parasitology 29, 549–557.CrossRefGoogle Scholar
KERR, S. F., MERKELZ, R. & MacKINNON, C. ( 2000). Further support for a Palaeartic origin of Leishmania. Memorias Instituto Oswaldo Cruz 95, 579–581.CrossRefGoogle Scholar
LEWIS, J., BALFE, P., ARNOLD, C., KAYE, S., TEDDER, R. S. & McKEATING, J. A. ( 1998). Development of a neutralizing antibody response during acute primary human immunodeficiency virus type 1 infection and the emergence of antigenic variants. Journal of Virology 72, 8943–8951.Google Scholar
MEDINA-ACOSTA, E., BEVERLEY, S. M. & RUSSELL, D. G. ( 1993). Evolution and expression of the Leishmania surface proteinase (gp63) gene locus. Infectious Agents and Diseases 2, 25–34.Google Scholar
MORALES, G., CARRILLO, G., REQUENA, J. M., GUZMAN, F., GOMEZ, L. C., PATARROYO, M. E. & ALONSO, C. ( 1997). Mapping of the antigenic determinants of the Leishmania infantum gp63 protein recognized by antibodies elicited during canine visceral Leishmaniasis. Parasitology 114, 507–516.Google Scholar
PAYS, E. & NOLAN, D. P. ( 1998). Expression and function of surface proteins in Trypanosoma brucei. Molecular and Biochemical Parasitology 91, 3–36.CrossRefGoogle Scholar
PUENTES, F., GUZMAN, F., MARIN, V., ALONSO, C., PATARROYO, M. E. & MORENO, A. ( 1999). Leishmania: fine mapping of the Leishmanolysin molecule's conserved core domains involved in binding and internalization. Experimental Parasitology 93, 7–22.CrossRefGoogle Scholar
RUSSO, D. M., JARDIM, A., CARVALHO, E. M., SLEATH, P. R., ARMITAGE, R. J., OLAFSON, R. W. & REED, S. G. ( 1993). Mapping human T cell epitopes in Leishmania gp63. Identification of cross-reactive and species-specific epitopes. Journal of Immunology 150, 932–939.Google Scholar
SAITOU, N. & NEI, M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular and Biological Evolution 4, 406–425.Google Scholar
SAMBROOK, J., FRITSCH, E. F. & MANIATIS, T. ( 1989). Molecular Cloning. A Laboratory Manual, 2nd Edn. Cold Spring Harbor Laboratory Press, New York.
SCHLAGENHAUF, E., ETGES, R. & METCALF, P. ( 1998). The crystal structure of the Leishmania major surface proteinase leishmanolysin (gp63). Structure 6, 1035–1046.CrossRefGoogle Scholar
STEINKRAUS, H. B., GREER, J. M., STEPHENSON, D. C. & LANGER, P. J. ( 1993). Sequence heterogeneity and polymorphic gene arrangements of the Leishmania guyanensis gp63 genes. Molecular and Biochemical Parasitology 62, 173–185.CrossRefGoogle Scholar
STILES, J. K., HICOCK, P. I., SHAH, P. H. & MEADE, J. C. ( 1999). Genomic organization, transcription, splicing and gene regulation in Leishmania. Annals of Tropical Medicine and Parasitology 93, 781–807.CrossRefGoogle Scholar
THOMPSON, J. D., HIGGINS, D. G. & GIBSON, T. J. ( 1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, positions-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle Scholar
VICTOIR, K., BANULS, A. L., AREVALO, J., LLANOS-CUENTAS, A., HAMERS, R., NOEL, S., DE DONCKER, S., LE RAY, D., TIBAYRENC, M. & DUJARDIN, J. C. ( 1998). The gp63 gene locus, a target for genetic characterization of Leishmania belonging to subgenus Viannia. Parasitology 117, 1–13.Google Scholar
VICTOIR, K. ( 2001). Genomic organisation and dynamics of the gp63 genes in Leishmania (Viannia) braziliensis and Leishmania (Viannia) peruviana: functional and diagnostic implications. Ph.D. thesis, VUB, Brussels, Belgium.
VICTOIR, K. & DUJARDIN, J. C. ( 2002). How to succeed in parasitic life without sex? Asking Leishmania. Trends in Parasitology 18, 81–85.CrossRefGoogle Scholar
VOTH, B. R., KELLY, B. L., JOSHI, P. B., IVENS, A. C. & McMASTER, W. R. ( 1998). Differentially expressed Leishmania major gp63 genes encode cell surface leishmanolysin with distinct signals for glycosylphosphatidylinositol attachment. Molecular and Biochemical Parasitology 93, 31–41.CrossRefGoogle Scholar
WICKSTEAD, B., ERSFELD, K. & GULL, K. ( 2003). Repetitive elements in genomes of parasitic protozoa. Microbiology and Molecular Biology Reviews 67, 360–375.CrossRefGoogle Scholar
YAO, C., DONELSON, J. & WILSON, M. ( 2003). The major surface protease (MSP or gp63) of Leishmania sp. Biosynthesis, regulation of expression, and function. Molecular and Biochemical Parasitology 132, 1–16.Google Scholar