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A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva.

ABSTRACT: To development a reliable murine model of Leishmania braziliensis braziliensis infection, parasites were injected into BALB/c mice in the presence of phlebotomine sand fly salivary gland lysates, which have previously been shown to greatly increase the infectivity of L. major in mice. When injected with salivary gland lysates, L. braziliensis braziliensis produced progressively enlarging cutaneous nodules, containing many macrophages filled with Leishmania amastigotes. In contrast, L. braziliensis injected without gland extracts produced small and rapidly regressing lesions. Isoenzyme analysis, monoclonal antibodies, and the polymerase chain reaction with L. braziliensis-specific oligonucleotide primers and probes confirmed that parasites causing the lesions were L. braziliensis.

SUBMITTER: Samuelson J

PROVIDER: S-EPMC2118755 | biostudies-other | 1991 Jan

REPOSITORIES: biostudies-other

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A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva.

Samuelson J J Lerner E E Tesh R R Titus R R

The Journal of experimental medicine 19910101 1

To development a reliable murine model of Leishmania braziliensis braziliensis infection, parasites were injected into BALB/c mice in the presence of phlebotomine sand fly salivary gland lysates, which have previously been shown to greatly increase the infectivity of L. major in mice. When injected with salivary gland lysates, L. braziliensis braziliensis produced progressively enlarging cutaneous nodules, containing many macrophages filled with Leishmania amastigotes. In contrast, L. braziliens ...[more]

PMID: 1985126

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Project description:BACKGROUND:Sand flies are the vectors of Leishmania parasites. To develop in the sand fly midgut, Leishmania multiplies and undergoes various stage differentiations giving rise to the infective form, the metacyclic promastigotes. To determine the changes in sand fly midgut gene expression caused by the presence of Leishmania, we performed RNA-Seq of uninfected and Leishmania infantum-infected Lutzomyia longipalpis midguts from seven different libraries corresponding to time points which cover the various Leishmania developmental stages. RESULTS:The combined transcriptomes resulted in the de novo assembly of 13,841 sand fly midgut transcripts. Importantly, only 113 sand fly transcripts, about 1%, were differentially expressed in the presence of Leishmania parasites. Further, we observed distinct differentially expressed sand fly midgut transcripts corresponding to the presence of each of the various Leishmania stages suggesting that each parasite stage influences midgut gene expression in a specific manner. Two main patterns of sand fly gene expression modulation were noted. At early time points (days 1-4), more transcripts were down-regulated by Leishmania infection at large fold changes (>?32 fold). Among the down-regulated genes, the transcription factor Forkhead/HNF-3 and hormone degradation enzymes were differentially regulated on day 2 and appear to be the upstream regulators of nutrient transport, digestive enzymes, and peritrophic matrix proteins. Conversely, at later time points (days 6 onwards), most of the differentially expressed transcripts were up-regulated by Leishmania infection with small fold changes (<?32 fold). The molecular functions of these genes have been associated with the metabolism of lipids and detoxification of xenobiotics. CONCLUSION:Overall, our data suggest that the presence of Leishmania produces a limited change in the midgut transcript expression profile in sand flies. Further, Leishmania modulates sand fly gene expression early on in the developmental cycle in order to overcome the barriers imposed by the midgut, yet it behaves like a commensal at later time points where a massive number of parasites in the anterior midgut results only in modest changes in midgut gene expression.

Project description:BackgroundPhlebotomine sand flies transmit the haemoflagellate Leishmania, the causative agent of human leishmaniasis. The Leishmania promastigotes are confined to the gut lumen and are exposed to the gut microbiota within female sand flies. Here we study the colonisation resistance of yeast and bacteria in preventing the establishment of a Leishmania population in sand flies and the ability of Leishmania to provide colonisation resistance towards the insect bacterial pathogen Serratia marcescens that is also pathogenic towards Leishmania.MethodsWe isolated microorganisms from wild-caught and laboratory-reared female Lutzomyia longipalpis, identified as Pseudozyma sp. Asaia sp. and Ochrobactrum intermedium. We fed the females with a sugar meal containing the microorganisms and then subsequently fed them with a bloodmeal containing Leishmania mexicana and recorded the development of the Leishmania population. Further experiments examined the effect of first colonising the sand fly gut with L. mexicana followed by feeding with, Serratia marcescens, an insect bacterial pathogen. The mortality of the flies due to S. marcescens was recorded in the presence and absence of Leishmania.ResultsThere was a reduction in the number of flies harbouring a Leishmania population that had been pre-fed with Pseudozyma sp. and Asaia sp. or O. intermedium. Experiments in which L. mexicana colonised the sand fly gut prior to being fed an insect bacterial pathogen, Serratia marcescens, showed that the survival of flies with a Leishmania infection was significantly higher compared to flies without Leishmania infection.ConclusionsThe yeast and bacterial colonisation experiments show that the presence of sand fly gut microorganisms reduce the potential for Leishmania to establish within the sand fly vector. Sand flies infected with Leishmania were able to survive an attack by the bacterial pathogen that would have killed the insect and we concluded that Leishmania may benefit its insect host whilst increasing the potential to establish itself in the sand fly vector. We suggest that the increased ability of the sand fly to withstand a bacterial entomopathogen, due to the presence of the Leishmania, may provide an evolutionary pressure for the maintenance of the Leishmania-vector association.

Dataset Information

A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva.

Publications

A mouse model of Leishmania braziliensis braziliensis infection produced by coinjection with sand fly saliva.

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