Multilocus genotyping reveals a polyphyletic pattern among naturally antimony-resistant Leishmania braziliensis isolates from Peru

Infection, Genetics and Evolution

Volumn 11, Issue 8, 2011, Pages 1873-1880

  Adaui, Vanessa ^a,b   Maes, Ilse ^b   Huyse, Tine ^b,c   Van den Broeck, Frederik ^b,c   Talledo, Michael ^a,d   Kuhls, Katrin ^e   De Doncker, Simonne ^b   Maes, Louis ^d   Llanos Cuentas, Alejandro ^a   Schönian, Gabriele ^e   Arevalo, Jorge ^a,f   Dujardin, Jean Claude ^b,d  

^a INSTITUTO DE MEDICINA TROPICAL ALEXANDER VON HUMBOLDT   (Peru)

^b INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^c UNIVERSITY OF LEUVEN   (Belgium)

^d UNIVERSITY OF ANTWERP   (Belgium)

^e CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^f UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

Author keywords

Antimony resistance; Clinical isolates; Leishmania braziliensis; Microsatellite markers; Population genetics; Zoonotic tegumentary leishmaniasis

Indexed keywords

ANTIMONY;

ARTICLE; DRUG RESISTANCE; DRUG SENSITIVITY; GENE LOCUS; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; IN VITRO STUDY; LEISHMANIA BRAZILIENSIS; LEISHMANIA DONOVANI; MICROSATELLITE MARKER; MOLECULAR DYNAMICS; MOLECULAR EPIDEMIOLOGY; NONHUMAN; PARASITE ISOLATION; PARASITE TRANSMISSION; PERU; POLYPHYLY; POPULATION STRUCTURE; PRIORITY JOURNAL; SEXUAL BEHAVIOR; SKIN LEISHMANIASIS; STRUCTURE ANALYSIS; TREATMENT OUTCOME; ZOONOSIS;

ANIMALS; ANTIMONY; ANTIPROTOZOAL AGENTS; DRUG RESISTANCE; GENETIC VARIATION; GENOTYPE; HUMANS; LEISHMANIA BRAZILIENSIS; LEISHMANIASIS, CUTANEOUS; MICROSATELLITE REPEATS; PARASITIC SENSITIVITY TESTS; PERU; TREATMENT OUTCOME;

LEISHMANIA BRAZILIENSIS; LEISHMANIA DONOVANI;

EID: 82655172399     PISSN: 15671348     EISSN: 15677257     Source Type: Journal    
DOI: 10.1016/j.meegid.2011.08.008     Document Type: Article

References (36)

1. Adaui V., Schnorbusch K., Zimic M., Gutiérrez A., Decuypere S., Vanaerschot M., De Doncker S., Maes I., Llanos-Cuentas A., Chappuis F., Arévalo J., Dujardin J.C. Comparison of gene expression patterns among Leishmania braziliensis clinical isolates showing a different in vitro susceptibility to pentavalent antimony. Parasitology 2011, 138:183-193.
2. Adaui V., Castillo D., Zimic M., Gutierrez A., Decuypere S., Vanaerschot M., De Doncker S., Schnorbusch K., Maes I., Van der Auwera G., Maes L., Llanos-Cuentas A., Arevalo J., Dujardin J.C. Comparative gene expression analysis throughout the life cycle of Leishmania braziliensis: diversity of expression profiles among clinical isolates. PLoS Negl. Trop. Dis. 2011, 5:e1021. 10.1371/journal.pntd.0001021.
3. Ait-Oudhia K., Gazanion E., Oury B., Vergnes B., Sereno D. The fitness of antimony-resistant Leishmania parasites: lessons from the field. Trends Parasitol. 2011, 27:141-142.
4. Al-Jawabreh A., Diezmann S., Müller M., Wirth T., Schnur L.F., Strelkova M.V., Kovalenko D.A., Razakov S.A., Schwenkenbecher J., Kuhls K., Schönian G. Identification of geographically distributed sub-populations of Leishmania (Leishmania) major by microsatellite analysis. BMC Evol. Biol. 2008, 8:183. 10.1186/1471-2148-8-183.
5. Arevalo J., Ramirez L., Adaui V., Zimic M., Tulliano G., Miranda-Verástegui C., Lazo M., Loayza-Muro R., De Doncker S., Maurer A., Chappuis F., Dujardin J.C., Llanos-Cuentas A. Influence of Leishmania (Viannia) species on the response to antimonial treatment in patients with American tegumentary leishmaniasis. J. Infect. Dis. 2007, 195:1846-1851.
6. Bhattarai N.R., Van der Auwera G., Rijal S., Picado A., Speybroeck N., Khanal B., De Doncker S., Das M.L., Ostyn B., Davies C., Coosemans M., Berkvens D., Boelaert M., Dujardin J.C. Domestic animals and epidemiology of visceral leishmaniasis. Nepal. Emerg. Infect. Dis. 2010, 16:231-237.
7. Botilde Y., Laurent T., Quispe Tintaya W., Chicharro C., Cañavate C., Cruz I., Kuhls K., Schönian G., Dujardin J.C. Comparison of molecular markers for strain typing of Leishmania infantum. Infect. Genet. Evol. 2006, 6:440-446.
8. Bowcock A.M., Ruiz-Linares A., Tomfohrde J., Minch E., Kidd J.R., Cavalli-Sforza L.L. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 1994, 368:455-457.
9. Bulle B., Millon L., Bart J.M., Gállego M., Gambarelli F., Portús M., Schnur L., Jaffe C.L., Fernandez-Barredo S., Alunda J.M., Piarroux R. Practical approach for typing strains of Leishmania infantum by microsatellite analysis. J. Clin. Microbiol. 2002, 40:3391-3397.
10. Carter K.C., Hutchison S., Boitelle A., Murray H.W., Sundar S., Mullen A.B. Sodium stibogluconate resistance in Leishmania donovani correlates with greater tolerance to macrophage antileishmanial responses and trivalent antimony therapy. Parasitology 2005, 131:747-757.
11. Cavalli-Sforza L.L., Edwards A.W. Phylogenetic analysis. Models and estimation procedures. Am. J. Hum. Genet. 1967, 19:233-257.
12. Dawson K.J., Belkhir K. A Bayesian approach to the identification of panmictic populations and the assignment of individuals. Genet. Res. 2001, 78:59-77.
13. Dieringer D., Schlötterer C. Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol. Ecol. Notes 2003, 3:167-169. 10.1046/j.1471-8286.2003.00351.x.
14. Dujardin J.C., De Doncker S., Jacquet D., Bañuls A.L., Balavoine M., Van Bockstaele D., Tibayrenc M., Arevalo J., Le Ray D. Clonal propagation and the fast generation of karyotype diversity: An in vitro Leishmania model. Parasitology 2007, 134:33-39.
15. Garcia A.L., Kindt A., Quispe-Tintaya K.W., Bermudez H., Llanos A., Arevalo J., Bañuls A.L., De Doncker S., Le Ray D., Dujardin J.C. American tegumentary leishmaniasis: antigen-gene polymorphism, taxonomy and clinical pleomorphism. Infect. Genet. Evol. 2005, 5:109-116.
16. Garcia A.L., Tellez T., Parrado R., Rojas E., Bermudez H., Dujardin J.C. Epidemiological monitoring of American tegumentary leishmaniasis: molecular characterization of a peridomestic transmission cycle in the Amazonian lowlands of Bolivia. Trans. R. Soc. Trop. Med. Hyg. 2007, 101:1208-1213.
17. Holm S. A simple sequentially rejective multiple test procedure. Scand. J. Statist. 1979, 6:65-70.
18. Holzmuller P., Sereno D., Lemesre J.L. Lower nitric oxide susceptibility of trivalent antimony-resistant amastigotes of Leishmania infantum. Antimicrob. Agents Chemother. 2005, 49:4406-4409.
19. Jamjoom M.B., Ashford R.W., Bates P.A., Kemp S.J., Noyes H.A. Towards a standard battery of microsatellite markers for the analysis of the Leishmania donovani complex. Ann. Trop. Med. Parasitol. 2002, 96:265-270.
20. Kumar S., Tamura K., Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform. 2004, 5:150-163.
21. Laurent T., Rijal S., Yardley V., Croft S., De Doncker S., Decuypere S., Khanal B., Singh R., Schönian G., Kuhls K., Chappuis F., Dujardin J.C. Epidemiological dynamics of antimonial resistance in Leishmania donovani: genotyping reveals a polyclonal population structure among naturally-resistant clinical isolates from Nepal. Infect. Genet. Evol. 2007, 7:206-212.
22. Llanos-Cuentas A., Tulliano G., Araujo-Castillo R., Miranda-Verastegui C., Santamaria-Castrellon G., Ramirez L., Lazo M., De Doncker S., Boelaert M., Robays J., Dujardin J.C., Arevalo J., Chappuis F. Clinical and parasite species risk factors for pentavalent antimonial treatment failure in cutaneous leishmaniasis in Peru. Clin. Infect. Dis. 2008, 46:223-231.
23. Matschiner M., Salzburger W. TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinformatics 2009, 25:1982-1983.
24. Murray H.W., Berman J.D., Davies C.R., Saravia N.G. Advances in leishmaniasis. Lancet 2005, 366:1561-1577.
25. Ochsenreither S., Kuhls K., Schaar M., Presber W., Schönian G. Multilocus microsatellite typing as a new tool for discrimination of Leishmania infantum MON-1 strains. J. Clin. Microbiol. 2006, 44:495-503.
26. Oddone R., Schweynoch C., Schönian G., de Sousa Cdos S., Cupolillo E., Espinosa D., Arevalo J., Noyes H., Mauricio I., Kuhls K. Development of a multilocus microsatellite typing approach for discriminating strains of Leishmania (Viannia) species. J. Clin. Microbiol. 2009, 47:2818-2825.
27. Perry, M.R., Wyllie, S., Kumar Prajapati, V., Feldmann, J., Sundar, S., Boelaert, M., Fairlamb, A.H., in press. Visceral leishmaniasis and arsenic: an ancient poison contributing to antimonial treatment failure in the Indian Subcontinent? PLoS Negl. Trop. Dis.
28. Pompanon F., Bonin A., Bellemain E., Taberlet P. Genotyping errors: causes, consequences and solutions. Nat. Rev. Genet. 2005, 6:847-859.
29. Rougeron V., Waleckx E., Hide M., De Meeûs T., Arevalo J., Llanos-Cuentas A., Bañuls A.L. A set of 12 microsatellite loci for genetic studies of Leishmania braziliensis. Mol. Ecol. Res. 2008, 8:351-353. 10.1111/j.1471-8286.2007.01953.x.
30. Rougeron V., De Meeûs T., Hide M., Waleckx E., Bermudez H., Arevalo J., Llanos-Cuentas A., Dujardin J.C., De Doncker S., Le Ray D., Ayala F.J., Bañuls A.L. Extreme inbreeding in Leishmania braziliensis. Proc. Natl. Acad. Sci. USA 2009, 106:10224-10229.
31. Russell R., Iribar M.P., Lambson B., Brewster S., Blackwell J.M., Dye C., Ajioka J.W. Intra and inter-specific microsatellite variation in the Leishmania subgenus Viannia. Mol. Biochem. Parasitol. 1999, 103:71-77.
32. Schönian G., Kuhls K., Mauricio I.L. Molecular approaches for a better understanding of the epidemiology and population genetics of Leishmania. Parasitology 2011, 138:405-425.
33. Schwenkenbecher J.M., Wirth T., Schnur L.F., Jaffe C.L., Schallig H., Al-Jawabreh A., Hamarsheh O., Azmi K., Pratlong F., Schönian G. Microsatellite analysis reveals genetic structure of Leishmania tropica. Int. J. Parasitol. 2006, 36:237-246.
34. Sterkers Y., Lachaud L., Crobu L., Bastien P., Pagès M. FISH analysis reveals aneuploidy and continual generation of chromosomal mosaicism in Leishmania major. Cell Microbiol. 2011, 13:274-283. 10.1111/j.1462-5822.2010.01534.x.
35. Vergel C., Palacios R., Cadena H., Posso C.J., Valderrama L., Perez M., Walker J., Travi B.L., Saravia N.G. Evidence for Leishmania (Viannia) parasites in the skin and blood of patients before and after treatment. J. Infect. Dis. 2006, 194:503-511.
36. Yardley V., Ortuño N., Llanos-Cuentas A., Chappuis F., De Doncker S., Ramirez L., Croft S., Arevalo J., Adaui V., Bermudez H., Decuypere S., Dujardin J.C. American tegumentary leishmaniasis: is antimonial treatment outcome related to parasite drug susceptibility?. J. Infect. Dis. 2006, 194:1168-1175.