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
Autor(a) principal: | |
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Data de Publicação: | 2019 |
Outros Autores: | , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UNESP |
Texto Completo: | http://dx.doi.org/10.3389/fphys.2019.00529 http://hdl.handle.net/11449/184484 |
Resumo: | 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. |
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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 Infectionspotted fevertick-rickettsiae interactionimmunemicroplusinantimicrobial peptidesalivary glandstranscriptomeRNAiThe 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.Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)National Council for Scientific and Technological Development [The National Institutes of Science and Technology Program in Molecular Entomology (INCT-EM)]Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)University of Sao Paulo [Research Support Center on Bioactive Molecules from Arthropod Vectors]National Institute of Allergy and Infectious DiseasesUniv Sao Paulo, Dept Parasitol, Inst Ciencias Biomed, Sao Paulo, BrazilNIAID, Lab Malaria & Vector Res, 9000 Rockville Pike, Bethesda, MD 20892 USAUniv Sao Paulo, Inst Matemat & Estat, Dept Ciencia Comp, Sao Paulo, BrazilUniv Sao Paulo, Inst Ciencias Biomed, Dept Imunol, Sao Paulo, BrazilUniv Sao Paulo, Dept Med Vet Prevent & Saude Anim, Fac Med Vet & Zootecnia, Sao Paulo, BrazilUniv Estadual Paulista, Inst Biotecnol, Botucatu, SP, BrazilUniv Estadual Paulista, Inst Biotecnol, Botucatu, SP, BrazilFAPESP: 2008/053570-0FAPESP: 2013/26450-2CNPq: CNPq 573959/2008-0University of Sao Paulo [Research Support Center on Bioactive Molecules from Arthropod Vectors]: NAP-MOBIARVE 12.1.17661.1.7CNPq: 304382/2017-5Frontiers Media SaUniversidade de São Paulo (USP)NIAIDUniversidade Estadual Paulista (Unesp)Martins, Larissa A.Malossi, Camila D. [UNESP]Galletti, Maria F. B. de M. [UNESP]Ribeiro, Jose M.Fujita, AndreEsteves, ElianeCosta, Francisco B.Labruna, Marcelo B.Daffre, SirleiFogaca, Andrea C.2019-10-04T12:14:03Z2019-10-04T12:14:03Z2019-05-03info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/article13http://dx.doi.org/10.3389/fphys.2019.00529Frontiers In Physiology. Lausanne: Frontiers Media Sa, v. 10, 13 p., 2019.1664-042Xhttp://hdl.handle.net/11449/18448410.3389/fphys.2019.00529WOS:000467355100001Web of Sciencereponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengFrontiers In Physiologyinfo:eu-repo/semantics/openAccess2021-10-23T16:36:46Zoai:repositorio.unesp.br:11449/184484Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T23:51:53.293206Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
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 |
spellingShingle |
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. spotted fever tick-rickettsiae interaction immune microplusin antimicrobial peptide salivary glands transcriptome RNAi |
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_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_sort |
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 |
author |
Martins, Larissa A. |
author_facet |
Martins, Larissa A. Malossi, Camila D. [UNESP] Galletti, Maria F. B. de M. [UNESP] Ribeiro, Jose M. Fujita, Andre Esteves, Eliane Costa, Francisco B. Labruna, Marcelo B. Daffre, Sirlei Fogaca, Andrea C. |
author_role |
author |
author2 |
Malossi, Camila D. [UNESP] Galletti, Maria F. B. de M. [UNESP] Ribeiro, Jose M. Fujita, Andre Esteves, Eliane Costa, Francisco B. Labruna, Marcelo B. Daffre, Sirlei Fogaca, Andrea C. |
author2_role |
author author author author author author author author author |
dc.contributor.none.fl_str_mv |
Universidade de São Paulo (USP) NIAID Universidade Estadual Paulista (Unesp) |
dc.contributor.author.fl_str_mv |
Martins, Larissa A. Malossi, Camila D. [UNESP] Galletti, Maria F. B. de M. [UNESP] Ribeiro, Jose M. Fujita, Andre Esteves, Eliane Costa, Francisco B. Labruna, Marcelo B. Daffre, Sirlei Fogaca, Andrea C. |
dc.subject.por.fl_str_mv |
spotted fever tick-rickettsiae interaction immune microplusin antimicrobial peptide salivary glands transcriptome RNAi |
topic |
spotted fever tick-rickettsiae interaction immune microplusin antimicrobial peptide salivary glands transcriptome RNAi |
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. |
publishDate |
2019 |
dc.date.none.fl_str_mv |
2019-10-04T12:14:03Z 2019-10-04T12:14:03Z 2019-05-03 |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://dx.doi.org/10.3389/fphys.2019.00529 Frontiers In Physiology. Lausanne: Frontiers Media Sa, v. 10, 13 p., 2019. 1664-042X http://hdl.handle.net/11449/184484 10.3389/fphys.2019.00529 WOS:000467355100001 |
url |
http://dx.doi.org/10.3389/fphys.2019.00529 http://hdl.handle.net/11449/184484 |
identifier_str_mv |
Frontiers In Physiology. Lausanne: Frontiers Media Sa, v. 10, 13 p., 2019. 1664-042X 10.3389/fphys.2019.00529 WOS:000467355100001 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Frontiers In Physiology |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.format.none.fl_str_mv |
13 |
dc.publisher.none.fl_str_mv |
Frontiers Media Sa |
publisher.none.fl_str_mv |
Frontiers Media Sa |
dc.source.none.fl_str_mv |
Web of Science reponame:Repositório Institucional da UNESP instname:Universidade Estadual Paulista (UNESP) instacron:UNESP |
instname_str |
Universidade Estadual Paulista (UNESP) |
instacron_str |
UNESP |
institution |
UNESP |
reponame_str |
Repositório Institucional da UNESP |
collection |
Repositório Institucional da UNESP |
repository.name.fl_str_mv |
Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP) |
repository.mail.fl_str_mv |
|
_version_ |
1808129559487315968 |