Caspar-like Gene Depletion Reduces Leishmania Infection in Sand Fly Host Lutzomyia longipalpis

Telleria, Erich Loza; Sant’Anna, Maurício Roberto Viana; Ortigão-Farias, João Ramalho; Pitaluga, André Nóbrega; Dillon, Vivian M.; Bates, Paul A.; Traub-Csekö, Yara M.; Dillon, Rod J.

doi:10.1074/jbc.m111.331561

Cited by 59 publications

(66 citation statements)

References 42 publications

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“…We hypothesize that local bacterial genera in the vector provide the signals that trigger parasite differentiation either directly, by altering the concentration of key nutrients that trigger parasite differentiation, or indirectly, through effects on sand fly epithelial cell biology. Sand fly epithelial cells are immunoregulatory, responding to stimuli with Imd or Toll immune response pathways (38–39). Similar to other insect vectors of disease, the sand fly epithelial environment could support or disallow parasite survival (40–43).…”

Section: Discussionmentioning

confidence: 99%

The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

Kelly

Bahr

Serafim

et al. 2017

mBio

119

144

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The vector-borne disease leishmaniasis, caused by Leishmania species protozoa, is transmitted to humans by phlebotomine sand flies. Development of Leishmania to infective metacyclic promastigotes in the insect gut, a process termed metacyclogenesis, is an essential prerequisite for transmission. Based on the hypothesis that vector gut microbiota influence the development of virulent parasites, we sequenced midgut microbiomes in the sand fly Lutzomyia longipalpis with or without Leishmania infantum infection. Sucrose-fed sand flies contained a highly diverse, stable midgut microbiome. Blood feeding caused a decrease in microbial richness that eventually recovered. However, bacterial richness progressively decreased in L. infantum-infected sand flies. Acetobacteraceae spp. became dominant and numbers of Pseudomonadaceae spp. diminished coordinately as the parasite underwent metacyclogenesis and parasite numbers increased. Importantly, antibiotic-mediated perturbation of the midgut microbiome rendered sand flies unable to support parasite growth and metacyclogenesis. Together, these data suggest that the sand fly midgut microbiome is a critical factor for Leishmania growth and differentiation to its infective state prior to disease transmission.

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Section: Discussionmentioning

confidence: 99%

The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

Kelly

Bahr

Serafim

et al. 2017

mBio

119

144

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“…AMP expression is a key determinant of infection success for C. bombi (55) and other trypanosomes, such as Trypanosoma brucei (56), in their insect hosts. Leishmania, another genus of trypanosome more closely related to C. bombi, infection reduces host immune expression in both the vertebrate (57) and its insect vector hosts (58,59). In mammals, this is achieved by manipulation of signaling through MAP kinases (57), and in the sandfly vector, it appears to result in reduced expression of caspar (58), a gene controlling the immune deficiency (IMD) pathway, and suppressed expression of the AMP defensin (59).…”

Section: Discussionmentioning

confidence: 99%

Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system

Barribeau

Sadd

Plessis

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

115

151

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In many systems, host-parasite evolutionary dynamics have led to the emergence and maintenance of diverse parasite and host genotypes within the same population. Genotypes vary in key attributes: Parasite genotypes vary in ability to infect, host genotypes vary in susceptibility, and infection outcome is frequently the result of both parties' genotypic identities. These host-parasite genotype-by-genotype (G H × G P ) interactions influence evolutionary and ecological dynamics in important ways. Interactions can be produced through genetic variation; however, here, we assess the role of variable gene expression as an additional source of G H × G P interactions. The bumblebee Bombus terrestris and its trypanosome gut parasite Crithidia bombi are a model system for host-parasite matching. Full-transcriptome sequencing of the bumblebee host revealed that different parasite genotypes indeed induce fundamentally different host expression responses and host genotypes vary in their responses to the infecting parasite genotype. It appears that broadly and successfully infecting parasite genotypes lead to reduced host immune gene expression relative to unexposed bees but induce the expression of genes responsible for controlling gene expression. Contrastingly, a poorly infecting parasite genotype induced the expression of immunologically important genes, including antimicrobial peptides. A targeted expression assay confirmed the transcriptome results and also revealed strong host genotype effects. In all, the expression of a number of genes depends on the host genotype and the parasite genotype and the interaction between both host and parasite genotypes. These results suggest that alongside sequence variation in coding immunological genes, variation that controls immune gene expression can also produce patterns of host-parasite specificity.coevolution | manipulation | Red Queen

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“…mexicana promastigotes within the midgut of L . longipalpis , possibly by nonspecific activation of the IMD pathway [59]. In A .…”

Section: Discussionmentioning

confidence: 99%

Bacterial feeding, Leishmania infection and distinct infection routes induce differential defensin expression in Lutzomyia longipalpis

et al. 2013

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BackgroundPhlebotomine insects harbor bacterial, viral and parasitic pathogens that can cause diseases of public health importance. Lutzomyia longipalpis is the main vector of visceral leishmaniasis in the New World. Insects can mount a powerful innate immune response to pathogens. Defensin peptides take part in this response and are known to be active against Gram-positive and Gram-negative bacteria, and some parasites. We studied the expression of a defensin gene from Lutzomyia longipalpis to understand its role in sand fly immune response.MethodsWe identified, sequenced and evaluated the expression of a L. longipalpis defensin gene by semi-quantitative RT-PCR. The gene sequence was compared to other vectors defensins and expression was determined along developmental stages and after exposure of adult female L. longipalpis to bacteria and Leishmania.ResultsPhylogenetic analysis showed that the L. longipalpis defensin is closely related to a defensin from the Old World sand fly Phlebotomus duboscqi. Expression was high in late L4 larvae and pupae in comparison to early larval stages and newly emerged flies. Defensin expression was modulated by oral infection with bacteria. The Gram-positive Micrococcus luteus induced early high defensin expression, whilst the Gram-negative entomopathogenic Serratia marcescens induced a later response. Bacterial injection also induced defensin expression in adult insects. Female sand flies infected orally with Leishmania mexicana showed no significant difference in defensin expression compared to blood fed insects apart from a lower defensin expression 5 days post Leishmania infection. When Leishmania was introduced into the hemolymph by injection there was no induction of defensin expression until 72 h later.ConclusionsOur results suggest that L. longipalpis modulates defensin expression upon bacterial and Leishmania infection, with patterns of expression that are distinct among bacterial species and routes of infection.

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Caspar-like Gene Depletion Reduces Leishmania Infection in Sand Fly Host Lutzomyia longipalpis

Cited by 59 publications

References 42 publications

The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

The Gut Microbiome of the Vector Lutzomyia longipalpis Is Essential for Survival of Leishmania infantum

Gene expression differences underlying genotype-by-genotype specificity in a host–parasite system

Bacterial feeding, Leishmania infection and distinct infection routes induce differential defensin expression in Lutzomyia longipalpis

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