Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies

ABSTRACT The major surface lipophosphoglycan (LPG) of Leishmania parasites is critical to vector competence in restrictive sand fly vectors in mediating Leishmania attachment to the midgut epithelium, considered essential to parasite survival and development. However, the relevance of LPG for sand f...

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Autores principales:	Iliano V. Coutinho-Abreu, James Oristian, Waldionê de Castro, Timothy R. Wilson, Claudio Meneses, Rodrigo P. Soares, Valéria M. Borges, Albert Descoteaux, Shaden Kamhawi, Jesus G. Valenzuela
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	LPG Leishmania parasite binding parasite survival sand fly sand fly midgut Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0b30551295bf45d08c38afbdd2583c42
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spelling	oai:doaj.org-article:0b30551295bf45d08c38afbdd2583c422021-11-15T15:30:58ZBinding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies10.1128/mSphere.00594-202379-5042https://doaj.org/article/0b30551295bf45d08c38afbdd2583c422020-10-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00594-20https://doaj.org/toc/2379-5042ABSTRACT The major surface lipophosphoglycan (LPG) of Leishmania parasites is critical to vector competence in restrictive sand fly vectors in mediating Leishmania attachment to the midgut epithelium, considered essential to parasite survival and development. However, the relevance of LPG for sand flies that harbor multiple species of Leishmania remains elusive. We tested binding of Leishmania infantum wild-type (WT), LPG-defective (Δlpg1 mutants), and add-back (Δlpg1 + LPG1) lines to sand fly midguts in vitro and their survival in Lutzomyia longipalpis sand flies in vivo. Le. infantum WT parasites attached to the Lu. longipalpis midgut in vitro, with late-stage parasites binding to midguts in significantly higher numbers than were seen with early-stage promastigotes. Δlpg1 mutants did not bind to Lu. longipalpis midguts, and this was rescued in the Δlpg1 + LPG1 lines, indicating that midgut binding is mediated by LPG. When Lu. longipalpis sand flies were infected with the Le. infantum WT or Le. infantum Δlpg1 or Le. infantum Δlpg1 + LPG1 line of the BH46 or BA262 strains, the BH46 Δlpg1 mutant, but not the BA262 Δlpg1 mutant, survived and grew to numbers similar to those seen with the WT and Δlpg1 + LPG1 lines. Exposure of BH46 and BA262 Δlpg1 mutants to blood-engorged midgut extracts led to mortality of the BA262 Δlpg1 but not the BH46 Δlpg1 parasites. These findings suggest that Le. infantum LPG protects parasites on a strain-specific basis early in infection, likely against toxic components of blood digestion, but that it is not necessary to prevent Le. infantum evacuation along with the feces in the permissive vector Lu. longipalpis. IMPORTANCE It is well established that the presence of LPG is sufficient to define the vector competence of restrictive sand fly vectors with respect to Leishmania parasites. However, the permissiveness of other sand flies with respect to multiple Leishmania species suggests that other factors might define vector competence for these vectors. In this study, we investigated the underpinnings of Leishmania infantum survival and development in its natural vector, Lutzomyia longipalpis. We found that LPG-mediated midgut binding persists in late-stage parasites. This observation is of relevance for the understanding of vector-parasite molecular interactions and suggests that only a subset of infective metacyclic-stage parasites (metacyclics) lose their ability to attach to the midgut, with implications for parasite transmission dynamics. However, our data also demonstrate that LPG is not a determining factor in Leishmania infantum retention in the midgut of Lutzomyia longipalpis, a permissive vector. Rather, LPG appears to be more important in protecting some parasite strains from the toxic environment generated during blood meal digestion in the insect gut. Thus, the relevance of LPG in parasite development in permissive vectors appears to be a complex issue and should be investigated on a strain-specific basis.Iliano V. Coutinho-AbreuJames OristianWaldionê de CastroTimothy R. WilsonClaudio MenesesRodrigo P. SoaresValéria M. BorgesAlbert DescoteauxShaden KamhawiJesus G. ValenzuelaAmerican Society for MicrobiologyarticleLPGLeishmaniaparasite bindingparasite survivalsand flysand fly midgutMicrobiologyQR1-502ENmSphere, Vol 5, Iss 5 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	LPG Leishmania parasite binding parasite survival sand fly sand fly midgut Microbiology QR1-502
spellingShingle	LPG Leishmania parasite binding parasite survival sand fly sand fly midgut Microbiology QR1-502 Iliano V. Coutinho-Abreu James Oristian Waldionê de Castro Timothy R. Wilson Claudio Meneses Rodrigo P. Soares Valéria M. Borges Albert Descoteaux Shaden Kamhawi Jesus G. Valenzuela Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies
description	ABSTRACT The major surface lipophosphoglycan (LPG) of Leishmania parasites is critical to vector competence in restrictive sand fly vectors in mediating Leishmania attachment to the midgut epithelium, considered essential to parasite survival and development. However, the relevance of LPG for sand flies that harbor multiple species of Leishmania remains elusive. We tested binding of Leishmania infantum wild-type (WT), LPG-defective (Δlpg1 mutants), and add-back (Δlpg1 + LPG1) lines to sand fly midguts in vitro and their survival in Lutzomyia longipalpis sand flies in vivo. Le. infantum WT parasites attached to the Lu. longipalpis midgut in vitro, with late-stage parasites binding to midguts in significantly higher numbers than were seen with early-stage promastigotes. Δlpg1 mutants did not bind to Lu. longipalpis midguts, and this was rescued in the Δlpg1 + LPG1 lines, indicating that midgut binding is mediated by LPG. When Lu. longipalpis sand flies were infected with the Le. infantum WT or Le. infantum Δlpg1 or Le. infantum Δlpg1 + LPG1 line of the BH46 or BA262 strains, the BH46 Δlpg1 mutant, but not the BA262 Δlpg1 mutant, survived and grew to numbers similar to those seen with the WT and Δlpg1 + LPG1 lines. Exposure of BH46 and BA262 Δlpg1 mutants to blood-engorged midgut extracts led to mortality of the BA262 Δlpg1 but not the BH46 Δlpg1 parasites. These findings suggest that Le. infantum LPG protects parasites on a strain-specific basis early in infection, likely against toxic components of blood digestion, but that it is not necessary to prevent Le. infantum evacuation along with the feces in the permissive vector Lu. longipalpis. IMPORTANCE It is well established that the presence of LPG is sufficient to define the vector competence of restrictive sand fly vectors with respect to Leishmania parasites. However, the permissiveness of other sand flies with respect to multiple Leishmania species suggests that other factors might define vector competence for these vectors. In this study, we investigated the underpinnings of Leishmania infantum survival and development in its natural vector, Lutzomyia longipalpis. We found that LPG-mediated midgut binding persists in late-stage parasites. This observation is of relevance for the understanding of vector-parasite molecular interactions and suggests that only a subset of infective metacyclic-stage parasites (metacyclics) lose their ability to attach to the midgut, with implications for parasite transmission dynamics. However, our data also demonstrate that LPG is not a determining factor in Leishmania infantum retention in the midgut of Lutzomyia longipalpis, a permissive vector. Rather, LPG appears to be more important in protecting some parasite strains from the toxic environment generated during blood meal digestion in the insect gut. Thus, the relevance of LPG in parasite development in permissive vectors appears to be a complex issue and should be investigated on a strain-specific basis.
format	article
author	Iliano V. Coutinho-Abreu James Oristian Waldionê de Castro Timothy R. Wilson Claudio Meneses Rodrigo P. Soares Valéria M. Borges Albert Descoteaux Shaden Kamhawi Jesus G. Valenzuela
author_facet	Iliano V. Coutinho-Abreu James Oristian Waldionê de Castro Timothy R. Wilson Claudio Meneses Rodrigo P. Soares Valéria M. Borges Albert Descoteaux Shaden Kamhawi Jesus G. Valenzuela
author_sort	Iliano V. Coutinho-Abreu
title	Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies
title_short	Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies
title_full	Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies
title_fullStr	Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies
title_full_unstemmed	Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies
title_sort	binding of <named-content content-type="genus-species">leishmania infantum</named-content> lipophosphoglycan to the midgut is not sufficient to define vector competence in <italic toggle="yes">lutzomyia longipalpis</italic> sand flies
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/0b30551295bf45d08c38afbdd2583c42
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Binding of <named-content content-type="genus-species">Leishmania infantum</named-content> Lipophosphoglycan to the Midgut Is Not Sufficient To Define Vector Competence in <italic toggle="yes">Lutzomyia longipalpis</italic> Sand Flies

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