Cargando…

The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection

The salivary glands (SG) of ixodid ticks play a pivotal role in blood feeding, producing both the cement and the saliva. The cement is an adhesive substance that helps the attachment of the tick to the host skin, while the saliva contains a rich mixture of antihemostatic, anti-inflammatory, and immu...

Descripción completa

Detalles Bibliográficos
Autores principales: Martins, Larissa A., Malossi, Camila D., Galletti, Maria F. B. de M., Ribeiro, José M., Fujita, André, Esteves, Eliane, Costa, Francisco B., Labruna, Marcelo B., Daffre, Sirlei, Fogaça, Andréa C.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6509419/
https://www.ncbi.nlm.nih.gov/pubmed/31130872
http://dx.doi.org/10.3389/fphys.2019.00529
_version_ 1783417245704126464
author Martins, Larissa A.
Malossi, Camila D.
Galletti, Maria F. B. de M.
Ribeiro, José M.
Fujita, André
Esteves, Eliane
Costa, Francisco B.
Labruna, Marcelo B.
Daffre, Sirlei
Fogaça, Andréa C.
author_facet Martins, Larissa A.
Malossi, Camila D.
Galletti, Maria F. B. de M.
Ribeiro, José M.
Fujita, André
Esteves, Eliane
Costa, Francisco B.
Labruna, Marcelo B.
Daffre, Sirlei
Fogaça, Andréa C.
author_sort Martins, Larissa A.
collection PubMed
description The salivary glands (SG) of ixodid ticks play a pivotal role in blood feeding, producing both the cement and the saliva. The cement is an adhesive substance that helps the attachment of the tick to the host skin, while the saliva contains a rich mixture of antihemostatic, anti-inflammatory, and immunomodulatory substances that allow ticks to properly acquire the blood meal. The tick saliva is also a vehicle used by several pathogens to be transmitted to the vertebrate host, including various bacterial species from the genus Rickettsia. Rickettsia rickettsii is a tick-borne obligate intracellular bacterium that causes the severe Rocky Mountain spotted fever. In Brazil, the dog yellow tick Amblyomma aureolatum is a vector of R. rickettsii. In the current study, the effects of an experimental infection with R. rickettsii on the global gene expression profile of A. aureolatum SG was determined by next-generation RNA sequencing. A total of 260 coding sequences (CDSs) were modulated by infection, among which 161 were upregulated and 99 were downregulated. Regarding CDSs in the immunity category, we highlight one sequence encoding one microplusin-like antimicrobial peptide (AMP) (Ambaur-69859). AMPs are important effectors of the arthropod immune system, which lack the adaptive response of the immune system of vertebrates. The expression of microplusin was confirmed to be significantly upregulated in the SG as well as in the midgut (MG) of infected A. aureolatum by a quantitative polymerase chain reaction preceded by reverse transcription. The knockdown of the microplusin expression by RNA interference caused a significant increase in the prevalence of infected ticks in relation to the control. In addition, a higher rickettsial load of one order of magnitude was recorded in both the MG and SG of ticks that received microplusin-specific dsRNA. No effect of microplusin knockdown was observed on the R. rickettsii transmission to rabbits. Moreover, no significant differences in tick engorgement and oviposition were recorded in ticks that received dsMicroplusin, demonstrating that microplusin knockdown has no effect on tick fitness. Further studies must be performed to determine the mechanism of action of this AMP against R. rickettsii.
format Online
Article
Text
id pubmed-6509419
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-65094192019-05-24 The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection Martins, Larissa A. Malossi, Camila D. Galletti, Maria F. B. de M. Ribeiro, José M. Fujita, André Esteves, Eliane Costa, Francisco B. Labruna, Marcelo B. Daffre, Sirlei Fogaça, Andréa C. Front Physiol Physiology The salivary glands (SG) of ixodid ticks play a pivotal role in blood feeding, producing both the cement and the saliva. The cement is an adhesive substance that helps the attachment of the tick to the host skin, while the saliva contains a rich mixture of antihemostatic, anti-inflammatory, and immunomodulatory substances that allow ticks to properly acquire the blood meal. The tick saliva is also a vehicle used by several pathogens to be transmitted to the vertebrate host, including various bacterial species from the genus Rickettsia. Rickettsia rickettsii is a tick-borne obligate intracellular bacterium that causes the severe Rocky Mountain spotted fever. In Brazil, the dog yellow tick Amblyomma aureolatum is a vector of R. rickettsii. In the current study, the effects of an experimental infection with R. rickettsii on the global gene expression profile of A. aureolatum SG was determined by next-generation RNA sequencing. A total of 260 coding sequences (CDSs) were modulated by infection, among which 161 were upregulated and 99 were downregulated. Regarding CDSs in the immunity category, we highlight one sequence encoding one microplusin-like antimicrobial peptide (AMP) (Ambaur-69859). AMPs are important effectors of the arthropod immune system, which lack the adaptive response of the immune system of vertebrates. The expression of microplusin was confirmed to be significantly upregulated in the SG as well as in the midgut (MG) of infected A. aureolatum by a quantitative polymerase chain reaction preceded by reverse transcription. The knockdown of the microplusin expression by RNA interference caused a significant increase in the prevalence of infected ticks in relation to the control. In addition, a higher rickettsial load of one order of magnitude was recorded in both the MG and SG of ticks that received microplusin-specific dsRNA. No effect of microplusin knockdown was observed on the R. rickettsii transmission to rabbits. Moreover, no significant differences in tick engorgement and oviposition were recorded in ticks that received dsMicroplusin, demonstrating that microplusin knockdown has no effect on tick fitness. Further studies must be performed to determine the mechanism of action of this AMP against R. rickettsii. Frontiers Media S.A. 2019-05-03 /pmc/articles/PMC6509419/ /pubmed/31130872 http://dx.doi.org/10.3389/fphys.2019.00529 Text en Copyright © 2019 Martins, Malossi, Galletti, Ribeiro, Fujita, Esteves, Costa, Labruna, Daffre and Fogaça. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Martins, Larissa A.
Malossi, Camila D.
Galletti, Maria F. B. de M.
Ribeiro, José M.
Fujita, André
Esteves, Eliane
Costa, Francisco B.
Labruna, Marcelo B.
Daffre, Sirlei
Fogaça, Andréa C.
The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection
title The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection
title_full The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection
title_fullStr The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection
title_full_unstemmed The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection
title_short The Transcriptome of the Salivary Glands of Amblyomma aureolatum Reveals the Antimicrobial Peptide Microplusin as an Important Factor for the Tick Protection Against Rickettsia rickettsii Infection
title_sort transcriptome of the salivary glands of amblyomma aureolatum reveals the antimicrobial peptide microplusin as an important factor for the tick protection against rickettsia rickettsii infection
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6509419/
https://www.ncbi.nlm.nih.gov/pubmed/31130872
http://dx.doi.org/10.3389/fphys.2019.00529
work_keys_str_mv AT martinslarissaa thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT malossicamilad thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT gallettimariafbdem thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT ribeirojosem thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT fujitaandre thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT esteveseliane thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT costafranciscob thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT labrunamarcelob thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT daffresirlei thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT fogacaandreac thetranscriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT martinslarissaa transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT malossicamilad transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT gallettimariafbdem transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT ribeirojosem transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT fujitaandre transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT esteveseliane transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT costafranciscob transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT labrunamarcelob transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT daffresirlei transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection
AT fogacaandreac transcriptomeofthesalivaryglandsofamblyommaaureolatumrevealstheantimicrobialpeptidemicroplusinasanimportantfactorforthetickprotectionagainstrickettsiarickettsiiinfection