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Evaluation of an in vitro and in vivo model for experimental infection with Leishmania (Viannia) braziliensis and L. (V.) peruviana

Published online by Cambridge University Press:  26 October 2007

D. GAMBOA ,
K. TORRES ,
S. DE DONCKER ,
M. ZIMIC ,
J. AREVALO  and
J.-C. DUJARDIN
D. GAMBOA
Affiliation:
Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, A.P. 4314, Lima 100, Peru Unit of Molecular Parasitology, Intituut voor Tropische Geneeskunde, 155 Nationalestraat, B-2000 Antwerpen, Belgium
K. TORRES
Affiliation:
Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, A.P. 4314, Lima 100, Peru
S. DE DONCKER
Affiliation:
Unit of Molecular Parasitology, Intituut voor Tropische Geneeskunde, 155 Nationalestraat, B-2000 Antwerpen, Belgium
M. ZIMIC
Affiliation:
Departamento de Bioquimica, Biologia Molecular y Farmacologia, Facultad de Ciencias y Filosofia, Universidad Peruana Cayetano Heredia, A.P. 4314, Lima 100, Peru
J. AREVALO
Affiliation:
Instituto de Medicina Tropical “Alexander von Humboldt”, Universidad Peruana Cayetano Heredia, A.P. 4314, Lima 100, Peru Departamento de Bioquimica, Biologia Molecular y Farmacologia, Facultad de Ciencias y Filosofia, Universidad Peruana Cayetano Heredia, A.P. 4314, Lima 100, Peru
J.-C. DUJARDIN*
Affiliation:
Unit of Molecular Parasitology, Intituut voor Tropische Geneeskunde, 155 Nationalestraat, B-2000 Antwerpen, Belgium
*
*Corresponding author: Unit of Molecular Parasitology, Intituut voor Tropische Geneeskunde, 155 Nationalestraat, B-2000 Antwerpen, Belgium. Tel: +32 3 2476358. Fax: +32 3 2476359. E-mail: jcdujardin@itg.be
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Summary

Leishmania (Viannia) braziliensis and L. (V.) peruviana are two parasite species characterized by a very different pathogenicity in humans despite a high genetic similarity. We hypothesized previously that L. (V.) peruviana would descend from L. (V.) braziliensis and would have acquired its ‘peruviana’ character during the southward colonization and adaptation of the transmission cycle in the Peruvian Andes. In order to have a first appreciation of the differences in virulence between both species, we evaluated an in vitro and in vivo model for experimental infection. A procedure was adapted to enrich culture forms in infective stages and the purified metacyclics were used to infect macrophage cell lines and golden hamsters. The models were tested with 2 representative strains of L. (V.) braziliensis from cutaneous and mucosal origin respectively and 2 representative strains of L. (V.) peruviana from Northern and Southern Peru respectively. Our models were reproducible and sensitive enough to detect phenotypic differences among strains. We showed in vitro as well as in vivo that the L. (V.) braziliensis was more infective than L. (V.) peruviana. Furthermore, we found that in vitro infectivity patterns of the 4 strains analysed, were in agreement with the geographical structuring of parasite populations demonstrated in our previous studies. Further work is needed to confirm our results with more strains of different geographical origin and their specific clinical outcome. However, our data open new perspectives for understanding the process of speciation in Leishmania and its implications in terms of pathogenicity.

Keywords

Leishmania (V.) braziliensisLeishmania (V.) peruvianainfectivityvirulencemacrophagehamster
Type
Original Articles
Information
Parasitology , Volume 135 , Issue 3 , March 2008 , pp. 319 - 326
Copyright
Copyright © Cambridge University Press 2007

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References

REFERENCES

Almeida, M. C., Cuba, C. A., de Sa, C. M., Pharoah, M. M., Howard, K. M. and Miles, M. A. (1993). Metacyclogenesis of Leishmania (Viannia) braziliensis in vitro: evidence that lentil lectin is a marker of complement resistance and enhanced infectivity. Transactions of the Royal Society of Tropical Medicine and Hygiene 87, 325–329.CrossRefGoogle ScholarPubMed
Achour, Y. B., Chenik, M., Louzir, H. and Dellagi, K. (2002). Identification of a disulfide isomerase protein of Leishmania major as a putative virulence factor. Infection and Immunity 70, 3576–3585.CrossRefGoogle ScholarPubMed
Baldwin, T. M., Elso, C., Curtis, J., Buckingham, L. and Handman, E. (2003). The site of Leishmania major infection determines disease severity and immune responses. Infection and Immunity 71, 6830–6834.CrossRefGoogle ScholarPubMed
Bañuls, A. L. (1998). Apport de la génétique évolutive á la taxonomie et á l'epidémiologie du genre Leishmania. Ph.D. dissertation, University of Montpellier, France.Google Scholar
Bañuls, A. L., Dujardin, J. C., Guerrini, F., De Doncker, S., Jaquet, D., Arevalo, J., Noël, S., Le Ray, D. and Tibayrenc, M. (2000). Is Leishmania (Viannia) peruviana a distinct species? A MLEE/RAPD evolutionary genetics answer. Journal of Eukaryotic Microbiology 47, 197–207.CrossRefGoogle ScholarPubMed
Bates, P. and Tetley, L. (1993). Leishmania mexicana: induction of metacyclogenesis by cultivation of promastigotes at acidic pH. Experimental Parasitology 76, 412–423.CrossRefGoogle ScholarPubMed
Chang, K. P., Reed, S. G., McGwire, B. S. and Soong, L. (2003). Leishmania model for microbial virulence: the relevance of parasite multiplication and pathoantigenicity. Acta Tropica 85, 375–390.CrossRefGoogle ScholarPubMed
de Almeida, M. C., Vilhena, V., Barral, A. and Barral-Netto, M. (2003). Leishmanial infection: analysis of its first steps. A review. Mémorias do Insituto Oswaldo Cruz 98, 861–870.CrossRefGoogle ScholarPubMed
Dujardin, J. C., Gajendran, N., Hamers, R., Mathijsen, G., Urjel, R., Recacoechea, M., Villaroel, G., Bermudez, H., Desjeux, P., De Doncker, S. and Le Ray, D. (1987). Leishmaniasis in the lowlands of Bolivia. VII. Characterization and identification of Bolivian isolates by PFG karyotyping. In Leishmaniasis: the First Centenary (1885–1985). New Strategies for Control (ed. Hart, D.), pp. 137–148. NATO ASI Series A, Plenum Press, New York.Google Scholar
Dujardin, J. C., Llanos-Cuentas, A., Cáceres, A., Arana, M., Dujardin, J. P., Guerrini, F., Gomez, J., Arroyo, J., De Doncker, S., Jacquet, D., Hamers, R., Guerra, H., Le Ray, D. and Arevalo, J. (1993). Molecular karyotype variation in Leishmania (Viannia) peruviana: indication of geographical populations in Peru distributed along north-south cline. Annals of Tropical Medicine and Parasitology 87, 335–347.CrossRefGoogle ScholarPubMed
Dujardin, J. C., Bañuls, A. L., Victoir, K., De Doncker, S., Arevalo, J., Llanos-Cuentas, A., Tibayrenc, M. and Le Ray, D. (1995 a). From population to genome: ecogenetics of Leishmania (Viannia) braziliensis and L. (V.) peruviana. Annals of Tropical Medicine and Parasitology 89, 45–53.CrossRefGoogle ScholarPubMed
Dujardin, J. C., Dujardin, J. P., Tibayrenc, M., Timperman, G., De Doncker, S., Jacquet, D., Arevalo, J., Llanos-Cuentas, A., Guerra, H., Bermudez, H., Hamers, R. and Le Ray, D. (1995 b). Karyotype plasticity in Neotropical Leishmania: an index for measuring genomic distance among L. (V.) peruviana and L. (V.) braziliensis populations. Parasitology 110, 21–30.CrossRefGoogle ScholarPubMed
Dujardin, J. C., Bañuls, A. L., Arevalo, J., Tibayrenc, M. and Le Ray, D. (1998). Comparison of chromosomal and isoenzymatic variation in eco-geographical populations of Leishmania (Viannia) peruviana. Parasitology 117, 547–554.CrossRefGoogle Scholar
Dujardin, J. C., Henriksson, J., Victoir, K., Brisse, S., Gamboa, D., Arevalo, J. and Le Ray, D. (2000). Genomic rearrangements in Trypanosomatids: an alternative to the ‘one gene’ evolutionary hypotheses? Memorias do Instituto Oswaldo Cruz 95, 527–534.CrossRefGoogle Scholar
Dujardin, J. C., Victoir, K., De Doncker, S., Guerbouj, S., Arevalo, J. and Le Ray, D. (2002). Molecular epidemiology and diagnosis of Leishmania: what have we learnt from genome structure, dynamics and function? Transactions of the Royal Society of Tropical Medicine and Hygiene 96(S1), 81–86.CrossRefGoogle ScholarPubMed
Gamboa, D., Van Eys, G., Victoir, K., Torres, K., Adaui, V., Arevalo, J. and Dujardin, J. C. (2007). Putative markers of infective life stages in Leishmania (Viannia) braziliensis. Parasitology 134, 1689–1698.CrossRefGoogle ScholarPubMed
Garcia, A. L., Kindt, A., Quispe-Tintaya, K. W., Bermudez, H., Llanos-Cuentas, A., Arevalo, J., Bañuls, A. L., De Doncker, S., Le Ray, D. and Dujardin, J. C. (2005). American tegumentary leishmaniasis: antigen-gene polymorphism, taxonomy and clinical pleomorphism. Infection, Genetics and Evolution 5, 109–116.CrossRefGoogle ScholarPubMed
Garin, Y. J. F., Sulahian, A., Pratlong, F., Meneceur, P., Gangneux, J. P., Prina, E., Dedet, J. P. and Derouin, F. (2001). Virulence of Leishmania infantum is expressed as a clonal and dominant phenotype in experimental infections. Infection and Immunity 69, 7373.CrossRefGoogle ScholarPubMed
Giudice, A., Camada, I., Leopoldo, P. T., Pereira, J. M., Riley, L. W., Wilson, M. E., Ho, J. L., de Jesus, A. R., Carvalho, E. M. and Almeida, R. P. (2007). Resistance of Leishmania (Leishmania) amazonensis and Leishmania (Viannia) braziliensis to nitric oxide correlates with disease severity in tegumentary leishmaniasis. BioMed Central Infectious diseases 22, 7.Google Scholar
Guerra, H. (1988). Distribution of Leishmania in Peru. In Research on Control Strategies for the Leishmaniases, IDRC-MR 184e (ed. Walton, B. C., Wijeyaratne, P. M. and Modabber, F.), pp. 135–145. International Development Research Centre, Ottawa, Canada.Google Scholar
Lucas, C. M., Franke, E. D., Cachay, M. I., Tejada, A., Cruz, M. E., Kreutzer, R. D., Barker, D. C., McCann, S. H. and Watts, D. M. (1998). Geographic distribution and clinical description of leishmaniasis cases in Peru. American Journal of Tropical Medicine and Hygiene 59, 312–317.CrossRefGoogle ScholarPubMed
Pinto-da-Silva, L. H., Camurate, M., Costa, K. A., Oliveira, S. M., da Cunha-e-Silva, N. L. and Saraiva, E. M. (2002). Leishmania (Viannia) braziliensis metacyclic promastigotes purified using Bahuina purpurea lectins are complement resistant and highly infective for macrophages in vitro and hamsters in vivo. International Journal for Parasitology 32, 1371–1377.CrossRefGoogle ScholarPubMed
Sádlová, J., Volf, P., Victoir, K., Dujardin, J. C. and Votỳpka, J. (2006). Virulent and attenuated lines of Leishmania major: DNA karyotypes and differences in metalloproteinase GP63. Folia Parasitologica 53, 81–90.CrossRefGoogle ScholarPubMed
Späth, G. F. and Beverley, S. M. (2001). A lipophosphoglycan-independent method for isolation of infective Leishmania metacyclic promastigotes by density gradient centrifugation. Experimental Parasitology 99, 97–103.CrossRefGoogle ScholarPubMed
Van Meirvenne, N., Janssens, P. G. and Magnus, E. (1975). Antigenic variation in syringe-passaged populations of Trypanosoma (Trypanosoon) brucei. 1. Rationalization of the experimental approach. Annales de la Société Belge de Médicine Tropicale 55, 1–23.Google ScholarPubMed
Victoir, K., Dujardin, J. C., De Doncker, S., Barker, D. C., Arevalo, J., Hamers, R. and Le Ray, D. (1995). Plasticity of gp63 gene organization in Leishmania (Viannia) peruviana. Parasitology 111, 265–273.CrossRefGoogle ScholarPubMed
Vladimirov, V., Badalová, J., Svobodová, M., Havelková, H., Hart, A. A. M., Blazková, H., Demant, P. and Lipoldová, M. (2003). Different genetic control of cutaneous and visceral disease after Leishmania major infection in mice. Infection and Immunity 71, 2041–2046.CrossRefGoogle ScholarPubMed
Zakai, H. A., Chance, M. L. and Bates, P. A. (1998). In vitro stimulation of metacyclogenesis in Leishmania braziliensis, L. donovani, L. major and L. mexicana. Parasitology 116, 305–309.CrossRefGoogle ScholarPubMed
Zhang, W. W., Miranda-Verastegui, C., Arevalo, J., Ndao, M., Ward, B., Llanos-Cuentas, A. and Matlashewski, G. (2006). Development of a genetic assay to distinguish between Leishmania Viannia species on the basis of isoenzyme differences. Clinical Infectious Disease 42, 801–809.CrossRefGoogle ScholarPubMed