Porcisia transmission by prediuresis of sand flies

. 2022 ; 12 () : 981071. [epub] 20220810

Jazyk angličtina Země Švýcarsko Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid36034718

Parasites of the genus Porcisia, together with the genus Endotrypanum, form a sister clade to the species-rich and medically important genus Leishmania. Both Porcisia species, P. hertigi and P. deanei, are dixenous parasites of Neotropical porcupines. Almost 50 years after their first discovery, knowledge of their life cycle remains poor and their insect vectors are unknown. Because competent vectors of their closest phylogenetic relatives, genera Endotrypanum and Leishmania, are phlebotomine sand flies (Diptera: Psychodidae) and/or biting midges (Diptera: Ceratopogonidae), we examined here the potential of both sand flies and biting midges to transmit Porcisia parasites. The insects (Lutzomyia longipalpis, L. migonei and Culicoides sonorensis) were exposed to parasites through the chicken skin membrane and dissected at various time intervals post bloodmeal. Potentially infected females were also allowed to feed on the ears of anaesthetized BALB/c mice and the presence of parasite DNA was subsequently confirmed in the mice by PCR. Porcisia hertigi did not survive defecation in L. longipalpis or L. migonei, suggesting that these sand fly species are unlikely to serve as natural vectors of this parasite. Similarly, P. hertigi infections were lost in Culicoides midges. In contrast, mature P. deanei infections developed in 51-61% of L. longipalpis females, 7.3% of L. migonei females and 7.7% of Culicoides sonorensis females. In all three vector species, P. deanei colonized predominantly Malpighian tubules and produced metacyclic infective forms. Transmission of P. daenei to BALB/c mice was demonstrated via the prediuresis of L. longipalpis females. This mode of transmission, as well the colonization of Malpighian tubules as the dominant tissue of the vector, is unique among trypanosomatids. In conclusion, we demonstrated the vector competence of L. longipalpis for P. deanei but not for P. hertigi, and further studies are needed to evaluate competence of other Neotropical vectors for these neglected parasites.

Zobrazit více v PubMed

Alexandre J., Sadlova J., Lestinova T., Vojtkova B., Jancarova M., Podesvova L., et al. . (2020). Experimental infections and co-infections with leishmania braziliensis and Leishmania infantum in two sand fly species, Lutzomyia migonei and Lutzomyia longipalpis . Sci. Rep. 10, 1–8. doi: 10.1038/s41598-020-60600-7 PubMed DOI PMC

Anez N., Nieves E., Cazorla D. (1989). The validity of the developmental pattern in the sandfly gut for classification of Leishmania . Trans. R. Soc Trop. Med. Hyg. 83, 634–635. doi: 10.1016/0035-9203(89)90378-7 PubMed DOI

Becvar T., Vojtkova B., Siriyasatien P., Votypka J., Modry D., Jahn P., et al. . (2021). Experimental transmission of Leishmania (Mundinia) parasites by biting midges (Diptera: Ceratopogonidae). PloS Pathog. 17, 1–18. doi: 10.1371/journal.ppat.1009654 PubMed DOI PMC

Brotánková A., Fialová M., Čepička I., Brzoňová J., Svobodová M. (2022). Trypanosomes of the Trypanosoma theileri group: Phylogeny and new potential vectors. Microorganisms 10 (2), 294. doi: 10.3390/microorganisms10020294 PubMed DOI PMC

Chanmol W., Jariyapan N., Somboon P., Bates M. D., Bates P. A. (2019). Development of Leishmania orientalis in the sand fly Lutzomyia longipalpis (Diptera: Psychodidae) and the biting midge Culicoides soronensis (Diptera: Ceratopogonidae). Acta Trop. 199, 105157. doi: 10.1016/j.actatropica.2019.105157 PubMed DOI

Croft S. L., Molyneux D. H. (1979). Studies on the ultrastructure, virus-like particles and infectivity of Leishmania hertigi. Ann. Trop. Med. Parasitol. 73, 213–226. doi: 10.1080/00034983.1979.11687251 PubMed DOI

da Silva D. A., de Madeira F., Filho C. J. L. B., Schubach E. Y. P., da S J. H., Figueiredo F. B. (2013). Leishmania (Leishmania) hertigi in a porcupine (Coendou sp.) found in brasília, federal district, Brazil. Rev. Bras. Parasitol. Vet. 22, 297–299. doi: 10.1590/s1984-29612013005000014 PubMed DOI

Deane L. M., da Silva J. E., de Figueiredo P. Z. (1974). Leishmaniae in the viscera of porcupines from the state of piaui, Brazil. Rev. Inst. Med. Trop. Sao Paulo 16, 68–69. PubMed

Dougall A. M., Alexander B., Holt D. C., Harris T., Sultan A. H., Bates P. A., et al. . (2011). Evidence incriminating midges (Diptera : Ceratopogonidae ) as potential vectors of Leishmania in Australia q. Int. J. Parasitol. 41, 571–579. doi: 10.1016/j.ijpara.2010.12.008 PubMed DOI

Dvořák V., Shaw J. J., Volf P. (2018). “Parasite biology: The vectors,” in The leishmaniases: Old neglected tropical diseases. Eds. Bruschi F., Gradoni L.. Cham, Switzerland:Springer, 31–78. doi: 10.1007/978-3-319-72386-0 DOI

Espinosa O. A., Serrano M. G., Camargo E. P., Teixeira M. M. G., Shaw J. J. (2016). An appraisal of the taxonomy and nomenclature of trypanosomatids presently classified as Leishmania and Endotrypanum . Parasitology 145, 430–442. doi: 10.1017/S0031182016002092 PubMed DOI

Franco A. M. R., Tesh R. B., Guzman H., Deane M. P., Grimaldi G. J. (1997). Development od Endotrypanum (Kinetoplastida: Trypanosomatidae) in experimentally infected phlebotomine sand flies (Ditera: Psychodidae). J. Med. Entomol. 34, 189–192. doi: 10.1093/jmedent/34.2.189 PubMed DOI

Guimarães V. C. F. V., Pruzinova K., Sadlova J., Volfova V., Myskova J., Filho S. P. B., et al. . (2016). Lutzomyia migonei is a permissive vector competent for Leishmania infantum . Parasites Vectors 9, 1–6. doi: 10.1186/s13071-016-1444-2 PubMed DOI PMC

Herrer A. (1971). Leishmania hertigi sp. n., from the tropical porcupine, Coendou rothschildi Thomas. J. Parasitol. 57, 626–629. doi: 10.2307/3277928 PubMed DOI

Herrer A., Thatcher V. E., Johnson C. M. (1966). Natural infections of Leishmania and trypanosomes demonstrated by skin culture. J. Parasitol. 52, 954–957. doi: 10.2307/3276542 PubMed DOI

Hertig M., Mcconnell P. (1963). Experimental infection of Panamanian phlebotomus sandflies with Leishmania . Exp. Parasitol 14, 92–106. doi: 10.1016/0014-4894(63)90014-6 PubMed DOI

Killick-Kendrick R. (1979). “Biology of leishmania in phlebotomine sandflies,” in Biology of kinetoplastida. Eds. Lumsden W. H., Evans D. A. (London: Academic Press; ), 396–460.

Lainson R., Shaw J. J. (1968). Leishmaniasis in Brazil: I. observations on enzootic rodent leishmaniasis. incrimination of Lutzomyia flaviscutellata (Mangabeira) as the vector in the lower Amazon basin. Trans. R. Soc. Trop. Med. Hyg. 62, 385–395. doi: 10.1016/0035-9203(68)90090-4 PubMed DOI

Lainson R., Shaw J. J. (1977). Leishmanias of Neotropical porcupines: Leishmania hertigi deanei nov. Subsp. Acta Amaz. 7, 51–57. doi: 10.1590/1809-43921977071051 DOI

Lainson R., Shaw J. J. (1987). “Evolution, classification and geographical distribution,” in The leishmaniases in biology and medicine: Volume I biology and epidemiology. Eds. Peters W., Killick-Kendrick R. (London: Academic Press Inc; ), 1–120.

Lainson R., Ward R. D., Shaw J. J. (1977). Leishmania in phlebotomid sandflies: VI. importance of hindgut development in distinguishing between parasites of the Leishmania mexicana and L. braziliensis complexes. Proc. R. Soc. Lond. B 199, 309–320. doi: 10.1098/rspb.1977.0141 PubMed DOI

Lukeš J., Butenko A., Hashimi H., Maslov D. A., Votýpka J., Yurchenko V. (2018). Trypanosomatids are much more than just trypanosomes: Clues from the expanded family tree. Trends Parasitol. 34, 466–480. doi: 10.1016/j.pt.2018.03.002 PubMed DOI

Maroli M., Feliciangeli M. D., Bichaud L., Charrel R. N., Gradoni L. (2013). Phlebotomine sandflies and the spreading of leishmaniases and other diseases of public health concern. Med. Vet. Entomol. 27, 123–147. doi: 10.1111/j.1365-2915.2012.01034.x PubMed DOI

Mutero C. M., Mutinga M. J. (1993). Defecation by Anopheles arabiensis mosquitoes of host blood infected with live Trypanosoma congolense . Trop. Med. Parasitol. 44, 23–26. PubMed

Myskova J., Votypka J. A. N., Volf P. (2008). Leishmania in sand flies: Comparison of quantitative polymerase chain reaction with other techniques to determine the intensity of infection. J. Med. Ento Mol., 45 (1) 133–138. doi: 10.1093/jmedent/45.1.133 PubMed DOI

Nieves E., Pimenta P. F. P. (2000). Development of Leishmania (Viannia) braziliensis and Leishmania (Leishmania) amazonensis in the sand fly Lutzomyia migonei (Diptera: Psychodidae). J. Med. Entomol. 37, 134–140. doi: 10.1603/0022-2585-37.1.134 PubMed DOI

Nocelli R., Cintra-Socolowski P., Roat T., Silva-Zacarin E., Malaspina O. (2016). Comparative physiology of malpighian tubules: form and function. Open Access Insect Physiol. 6, 13–23. doi: 10.2147/oaip.s72060 DOI

Rangel E. F., Deane L. M., Grimaldi G., De Souza N. A., Wermelinger E. D., Barbosa A. F. (1985). Flagellates in the malpighian tubules of laboratory-bred Lutzomyia longipalpis fed on a hamster experimentally infected with Leishmania mexicana amazonensis . Mem. Inst. Oswaldo Cruz 80, 371–372. doi: 10.1590/s0074-02761985000300016 PubMed DOI

Sadlova J., Price H. P., Smith B. A., Votypka J., Volf P., Smith D. F. (2010). The stage-regulated HASPB and SHERP proteins are essential for differentiation of the protozoan parasite Leishmania major in its sand fly vector, Phlebotomus papatasi . Cell. Microbiol. 12, 1765–1779. doi: 10.1111/j.1462-5822.2010.01507.x PubMed DOI PMC

Sádlová J., Reishig J., Volf P. (1998). Prediuresis in female Phlebotomus sandflies (Diptera: Psychodidae). Eur. J. Entomol. 95, 643–647.

Sádlová J., Volf P. (1999). Occurrence of Leishmania major in sandfly urine. Parasitology 118, 455–460. doi: 10.1017/S0031182099004254 PubMed DOI

Shaw J. J. (1981). “The behaviour of endotrypanum schaudinni (Kinetoplastida: Trypanosomatidae) in three species of laboratory-bred Neotropical sandflies (Diptera: Psychodidae) and its influence on the classification of the genus leishmania,” in Parasitological topics. a presentation volume to p. c. c. garnham, f. r. s., on the occasion of his 80th birthday. Ed. Canning E. U. (Lawrence, KS, USA: Allen Press; ), 232–241.

Shimabukuro P. H. F., De Andrade A. J., Galati E. A. B. (2017). Checklist of American sand flies (Diptera, psychodidae, phlebotominae): Genera, species, and their distribution. Zookeys 2017, 67–106. doi: 10.3897/zookeys.660.10508 PubMed DOI PMC

Thies S. F., de Bronzoni R. V. M., Michalsky É.M., dos Santos E. S., da Silva D. J. F., Dias E. S., et al. . (2018). Aspects on the ecology of phlebotomine sand flies and natural infection by Leishmania hertigi in the southeastern Amazon basin of Brazil. Acta Trop. 177, 37–43. doi: 10.1016/j.actatropica.2017.09.023 PubMed DOI

Ticha L., Kykalova B., Sadlova J., Gramiccia M., Gradoni L., Volf P. (2021). Development of various Leishmania (Sauroleishmania) tarentolae strains in three phlebotomus species. Microorganisms 9, 1–13. doi: 10.3390/microorganisms9112256 PubMed DOI PMC

Tyler K. M., Engman D. M. (2001). The life cycle of Trypanosoma cruzi revisited. Int. J. Parasit. 31, 472–481. doi: 10.1016/s0020-7519(01)00153-9 PubMed DOI

Volf P., Volfova V. (2011). Establishment and maintenance of sand fly colonies. J. Vector Ecol. 36, 1–9. doi: 10.1111/j.1948-7134.2011.00106.x PubMed DOI

Voss R. S. (2015). “Superfamily erethizontoidea Bonaparte 1845,” in Mammals of south America, volume 2 rodents. Eds. Patton J. L., Pardiñas U. F. J., D’Elía G. (Chicago: University of Chcago Press; ), 786–805

Walters L. L., Modi G. B., Tesh R. B., Burrage T. (1987). Host-parasite relationship of Leishmania mexicana mexicana and Lutzomyia abonnenci (Diptera: Psychodidae). Am. J. Trop. Med. Hyg. 36, 294–314. doi: 10.4269/ajtmh.1987.36.294 PubMed DOI

Zeledón R., Ponce C., de Ponce E. (1977). Finding of Leishmania hertigi in the Costa Rican porcupine. J. Parasitol. 63, 924–925. doi: 10.2307/3279912 PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace