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In vitro and in vivo behaviour of sympatric Leishmania (V.) braziliensis, L. (V.) peruviana and their hybrids

Published online by Cambridge University Press:  07 November 2011

SOFIA CORTES*
Affiliation:
Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal Centro de Malária e Outras Doenças Tropicais (CMDT)/IHMT, Lisboa, Portugal
CARINA ESTEVES
Affiliation:
Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal Centro de Malária e Outras Doenças Tropicais (CMDT)/IHMT, Lisboa, Portugal
ISABEL MAURÍCIO
Affiliation:
Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal Department of Pathogen Molecular Biology, London School of Hygiene and Tropical Medicine (LSHTM), Keppel Street, London WCIE 7HT, UK
CARLA MAIA
Affiliation:
Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal Centro de Malária e Outras Doenças Tropicais (CMDT)/IHMT, Lisboa, Portugal
JOSÉ MANUEL CRISTOVÃO
Affiliation:
Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal
MICHAEL MILES
Affiliation:
Department of Pathogen Molecular Biology, London School of Hygiene and Tropical Medicine (LSHTM), Keppel Street, London WCIE 7HT, UK
LENEA CAMPINO
Affiliation:
Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical (IHMT), Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal
*
*Corresponding author: Unidade de Parasitologia Médica, Instituto de Higiene e Medicina Tropical, Universidade Nova de Lisboa, Rua da Junqueira, 100, 1346-008 Lisboa, Portugal. Tel: +351 213652600. Fax: +351 213632105. E-mail: [email protected]

Summary

Leishmania (Viannia) braziliensis is the main cause of highly disfiguring mucocutaneous leishmaniasis (MCL) in South America. The related species L. (V.) peruviana has only been identified in simple cutaneous lesions (CL). Hybrids between L. braziliensis and L. peruviana have been reported although genetic exchange in Leishmania is considered to be rare. Here we compared growth in vitro, adaptive capacity under thermal and oxidative stress and behaviour in a hamster model, of L. braziliensis, L. peruviana, and their putative hybrids. At 24°C, the optimal temperature for in vitro growth, L. braziliensis had the highest growth rate. In in vitro studies hybrid clones presented heterogeneous phenotypes, from slower growth rates, similar to L. peruviana, to higher growth rates, as observed in L. braziliensis. Hamsters infected with hybrid strains, presented the highest parasite densities and aggressive relapses at a later stage of infection. Hybrids generally presented higher plasticity and phenotypic diversity than the putative parental species, with potential eco-epidemiological implications, including an impact on the success of disease control.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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References

REFERENCES

Akopyants, N., Kimblin, N., Secundino, N., Patrick, R., Peters, N., Lawyer, P., Dobson, D., Beverley, S. M. and Sacks, D. (2009). Demonstration of genetic exchange during cyclical development of Leishmania in the sand fly vector. Science 32, 265268. doi: 10.1126/science.1169464.CrossRefGoogle Scholar
Almeida, M. C., Cuba-Cuba, C. A., Moraes, M. A. P. and Miles, M. A. (1996). Dissemination of Leishmania (Viannia) braziliensis. Journal of Comparative Pathology 115, 311316.CrossRefGoogle ScholarPubMed
Almeida, M. C., Cuba Cuba, C. A., , C. M., Pharoah, M., Howard, K. 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, 325359.CrossRefGoogle ScholarPubMed
Bañuls, A. L., Hide, M. and Prugnolle, F. (2007). Leishmania and the leishmaniases: a parasite genetic update and advances in taxonomy, epidemiology and pathogenicity in humans. Advances in Parasitology 64, 1109. doi:10.1016/S0065-308X(06)64001-3.CrossRefGoogle ScholarPubMed
Belli, A. A., Miles, M. A. and Kelly, J. M. (1994). A putative Leishmania panamensis/Leishmania braziliensis hybrid is a causative agent of human cutaneous leishmaniasis in Nicaragua. Parasitology 109, 435442.Google Scholar
Callahan, H. L., Portal, I. F., Bensinger, S. J. and Grogl, M. (1996). Leishmania spp: temperature sensitivity of promastigotes in vitro as a model for tropism in vivo. Experimental Parasitology 84, 400409.CrossRefGoogle Scholar
Chargui, N., Amro, A., Haouas, N., Schönian, G., Babba, H., Schmidt, S., Ravel, C., Lefebvre, M., Bastien, P., Chaker, E., Aoun, K., Zribi, M. and Kuhls, K. (2009). Population structure of Tunisian Leishmania infantum and evidence for the existence of hybrids and gene flow between genetically different populations. International Journal for Parasitology 39, 801811. doi:10.1016/j.ijpara.2008.11.016.CrossRefGoogle ScholarPubMed
Dujardin, J. C., Bañuls, A. L., Llanos-Cuentas, A., Alvarez, E., DeDoncker, S., Jacquet, D., Le Ray, D., Arevalo, J. and Tibayrenc, M. (1995). Putative Leishmania hybrids in the Eastern Andean valley of Huanuco, Peru. Acta Tropica 59, 293307. doi:10.1016/0001-706X(95)00094-U.CrossRefGoogle ScholarPubMed
Gamboa, D., Torres, K., Doncker, S., Zimic, M., Arevalo, J. and Dujardin, J. C. (2008). Evaluation of an in vitro and in vivo model for experimental infection with Leishmania (Viannia) braziliensis and L. (V.) peruviana. Parasitology 135, 319326. doi: 10.1017/S0031182007003848.Google Scholar
Garin, Y. J., 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, 73657373. doi: 10.1128/IAI.69.12.7365-7373.2001.CrossRefGoogle ScholarPubMed
Gaunt, M. W., Yeo, M., Frame, I. A., Stothard, J. R., Carrasco, H. J., Taylor, M. C., Mena, S. S., Veazey, P., Miles, G. A., Acosta, N., de Arias, A. R. and Miles, M. A. (2003). Mechanism of genetic exchange in American trypanosomes. Nature, London 421, 936939. doi:10.1038/nature01438.CrossRefGoogle ScholarPubMed
Gibson, W. and Whittington, H. (1993). Genetic exchange in Trypanosoma brucei: selection of hybrid trypanosomes by introduction of genes conferring drug resistance. Molecular Biochemical Parasitology 60, 1926. doi:10.1016/0166-6851(93)90024-R.CrossRefGoogle ScholarPubMed
González, U., Pinart, M., Rengifo-Pardo, M., Macaya, A., Alvar, J. and Tweed, J. A. (2009). Interventions for American cutaneous and mucocutaneous leishmaniasis. Cochrane Database of Systematic Reviews 2, Art. No.: CD004834. doi: 10.1002/14651858.CD004834.pub2.Google Scholar
Kelly, J. M., Law, J. M., Chapman, C. J., Van Eys, G. J. and Evans, D. A. (1991). Evidence of genetic recombination in Leishmania. Molecular Biochemical Parasitology 46, 253263.CrossRefGoogle ScholarPubMed
Machado, C. A. and Ayala, F. J. (2001). Nucleotide sequences provide evidence of genetic exchange among distantly related lineages of Trypanosoma cruzi. Proceedings of the National Academy of Sciences, USA 98, 73967401. doi: 10.1073/pnas.121187198.Google Scholar
Miles, M. A., Yeo, M. and Mauricio, I. L. (2009). Leishmania exploit sex. Science 324, 187189. doi: 10.1126/science.1172789.Google Scholar
Nolder, D., Roncal, N., Davies, C. R., Llanos-Cuentas, A. and Miles, M. A. (2007). Multiple hybrid genotypes of Leishmania (Viannia) in a focus of mucocutaneous leishmaniasis. American Journal of Tropical Medicine and Hygiene 76, 573578.CrossRefGoogle Scholar
Ravel, C., Cortes, S., Pratlong, F., Morio, F., Dedet, J. P. and Campino, L. (2006). First report of genetic hybrids between two very divergent Leishmania species: Leishmania infantum and Leishmania major. International Journal for Parasitology 36, 13831388. doi:10.1016/j.ijpara.2006.06.019.CrossRefGoogle ScholarPubMed
Reithinger, R., Lambson, B. E., Barker, D. C., Counihan, H., Espinoza, C. J., González, J. S. and Davies, C. R. (2002). Leishmania (Viannia) spp. dissemination and tissue tropism in naturally infected dogs (Canis familiaris). Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 7678.CrossRefGoogle ScholarPubMed
Rey, J. A., Travi, B. L., Valência, A. Z. and Saravia, N. G. (1990). Infectivity of the subspecies of the Leishmania braziliensis complex in vivo and in vitro. American Journal of Tropical Medicine and Hygiene 43, 623631.Google Scholar
Rolão, N., Cortes, S., Rodrigues, O. R. and Campino, L. (2004). Quantification of Leishmania infantum parasites in tissue biopsies by real-time polymerase chain reaction and polymerase chain reaction-enzyme-linked immunosorbent assay. Journal of Parasitology 90, 11501154. doi:10.1645/GE-264R1.CrossRefGoogle ScholarPubMed
Torrico, M. C., De Doncker, S., Arevalo, J., Le Ray, D. and Dujardin, J. C. (1999) In vitro promastigote fitness of putative Leishmania (Viannia) braziliensis/Leishmania (Viannia) peruviana hybrids. Acta Tropica 72, 99110. doi: 10.1016/S0001-706X(98)00076-X.Google Scholar
Vanaerschot, M., Maes, I., Ouakad, M., Adaui, V., Maes, L., De Doncker, S., Rijal, S., Chappuis, F., Dujardin, J. C. and Decuypere, S. (2010). Linking in vitro and in vivo survival of clinical Leishmania donovani strains. PLOSone 5, e12211. doi: 10.1371/journal.pone.0012211.Google Scholar
Volf, P., Benkova, I., Myskova, J., Sadlova, J., Campino, L. and Ravel, C. (2007). Increased transmission potential of Leishmania major/Leishmania infantum hybrids. International Journal for Parasitology 37, 589–93. doi:10.1016/j.ijpara.2007.02.002.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 Diseases 42, 801809. doi: 10.1086/500326.Google Scholar