Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones

Abstract Background The sand fly Lutzomyia longipalpis is the main vector of American visceral leishmaniasis, a disease caused by parasites of the genus Leishmania. Adults of this insect feed on blood (females only) or sugar from plant sources, but their digestion of carbohydrates is poorly studied....

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Main Authors: Tainá Neves Ferreira, Daniela Pita-Pereira, Samara Graciane Costa, Reginaldo Peçanha Brazil, Caroline Silva Moraes, Hector Manuel Díaz-Albiter, Fernando Ariel Genta
Format: Article
Language:English
Published: BMC 2018-11-01
Series:Parasites & Vectors
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13071-018-3122-z
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spelling doaj-c5eba2f97a514de28f16948b8ae18d432020-11-25T01:44:35ZengBMCParasites & Vectors1756-33052018-11-0111112010.1186/s13071-018-3122-zTransmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglyconesTainá Neves Ferreira0Daniela Pita-Pereira1Samara Graciane Costa2Reginaldo Peçanha Brazil3Caroline Silva Moraes4Hector Manuel Díaz-Albiter5Fernando Ariel Genta6Laboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, FIOCRUZLaboratório de Biologia Molecular de Doenças Endêmicas, Instituto Oswaldo Cruz, FIOCRUZLaboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, FIOCRUZLaboratório de Doenças Parasitárias, Instituto Oswaldo Cruz, FIOCRUZLaboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, FIOCRUZWellcome Centre for Molecular Parasitology, University of GlasgowLaboratório de Bioquímica e Fisiologia de Insetos, Instituto Oswaldo Cruz, FIOCRUZAbstract Background The sand fly Lutzomyia longipalpis is the main vector of American visceral leishmaniasis, a disease caused by parasites of the genus Leishmania. Adults of this insect feed on blood (females only) or sugar from plant sources, but their digestion of carbohydrates is poorly studied. Beta-glycosides as esculin and amygdalin are plant compounds and release toxic compounds as esculetin and mandelonitrile when hydrolyzed. Beta-glucosidase and trehalase are essential enzymes in sand fly metabolism and participate in sugar digestion. It is therefore possible that the toxic portions of these glycosides, released during digestion, affect sand fly physiology and the development of Leishmania. Results We tested the oral administration to sand flies of amygdalin, esculin, mandelonitrile, and esculetin in the sugar meal. These compounds significantly decreased the longevity of Lutzomyia longipalpis females and males. Lutzomyia longipalpis adults have significant hydrolytic activities against esculin and feeding on this compound cause changes in trehalase and β-glucosidase activities. Female trehalase activity is inhibited in vitro by esculin. Esculin is naturally fluorescent, so its ingestion may be detected and quantified in whole insects or tissue samples stored in methanol. Mandelonitrile neither affected the amount of sugar ingested by sand flies nor showed repellent activity. Our results show that mandelonitrile significantly reduces the viability of L. amazonensis, L. braziliensis, L. infantum and L. mexicana, in a concentration-dependent manner. Esculetin caused a similar effect, reducing the number of L. infantum and L. mexicana. Female L. longipalpis fed on mandelonitrile had a reduction in the number of parasites and prevalence of infection after seven days of infection with L. mexicana, either by counting in a Neubauer chamber or by qPCR assays. Conclusions Glycosides have significant effects on L. longipalpis longevity and metabolism and also affect the development of parasites in culture and inside the insect. These observations might help to conceptualize new vector control strategies using transmission blocking sugar baits.http://link.springer.com/article/10.1186/s13071-018-3122-zLutzomyia longipalpisLeishmaniaLongevityBeta-glycosidesTrehalaseBeta-glucosidase
collection DOAJ
language English
format Article
sources DOAJ
author Tainá Neves Ferreira
Daniela Pita-Pereira
Samara Graciane Costa
Reginaldo Peçanha Brazil
Caroline Silva Moraes
Hector Manuel Díaz-Albiter
Fernando Ariel Genta
spellingShingle Tainá Neves Ferreira
Daniela Pita-Pereira
Samara Graciane Costa
Reginaldo Peçanha Brazil
Caroline Silva Moraes
Hector Manuel Díaz-Albiter
Fernando Ariel Genta
Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
Parasites & Vectors
Lutzomyia longipalpis
Leishmania
Longevity
Beta-glycosides
Trehalase
Beta-glucosidase
author_facet Tainá Neves Ferreira
Daniela Pita-Pereira
Samara Graciane Costa
Reginaldo Peçanha Brazil
Caroline Silva Moraes
Hector Manuel Díaz-Albiter
Fernando Ariel Genta
author_sort Tainá Neves Ferreira
title Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
title_short Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
title_full Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
title_fullStr Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
title_full_unstemmed Transmission blocking sugar baits for the control of Leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
title_sort transmission blocking sugar baits for the control of leishmania development inside sand flies using environmentally friendly beta-glycosides and their aglycones
publisher BMC
series Parasites & Vectors
issn 1756-3305
publishDate 2018-11-01
description Abstract Background The sand fly Lutzomyia longipalpis is the main vector of American visceral leishmaniasis, a disease caused by parasites of the genus Leishmania. Adults of this insect feed on blood (females only) or sugar from plant sources, but their digestion of carbohydrates is poorly studied. Beta-glycosides as esculin and amygdalin are plant compounds and release toxic compounds as esculetin and mandelonitrile when hydrolyzed. Beta-glucosidase and trehalase are essential enzymes in sand fly metabolism and participate in sugar digestion. It is therefore possible that the toxic portions of these glycosides, released during digestion, affect sand fly physiology and the development of Leishmania. Results We tested the oral administration to sand flies of amygdalin, esculin, mandelonitrile, and esculetin in the sugar meal. These compounds significantly decreased the longevity of Lutzomyia longipalpis females and males. Lutzomyia longipalpis adults have significant hydrolytic activities against esculin and feeding on this compound cause changes in trehalase and β-glucosidase activities. Female trehalase activity is inhibited in vitro by esculin. Esculin is naturally fluorescent, so its ingestion may be detected and quantified in whole insects or tissue samples stored in methanol. Mandelonitrile neither affected the amount of sugar ingested by sand flies nor showed repellent activity. Our results show that mandelonitrile significantly reduces the viability of L. amazonensis, L. braziliensis, L. infantum and L. mexicana, in a concentration-dependent manner. Esculetin caused a similar effect, reducing the number of L. infantum and L. mexicana. Female L. longipalpis fed on mandelonitrile had a reduction in the number of parasites and prevalence of infection after seven days of infection with L. mexicana, either by counting in a Neubauer chamber or by qPCR assays. Conclusions Glycosides have significant effects on L. longipalpis longevity and metabolism and also affect the development of parasites in culture and inside the insect. These observations might help to conceptualize new vector control strategies using transmission blocking sugar baits.
topic Lutzomyia longipalpis
Leishmania
Longevity
Beta-glycosides
Trehalase
Beta-glucosidase
url http://link.springer.com/article/10.1186/s13071-018-3122-z
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