An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus

Detalhes bibliográficos
Autor(a) principal: Ribeiro, Jose M. C.
Data de Publicação: 2014
Outros Autores: Genta, Fernando A., Sorgine, Marcos H. F., Logullo, Raquel, Mesquita, Rafael D., Paiva-Silva, Gabriela O., Majerowicz, David, Medeiros, Marcelo, Koerich, Leonardo, Terra, Walter R., Ferreira, Clelia, Pimentel, Andre C., Bisch, Paulo M., Leite, Daniel C., Diniz, Michelle M. P., Junior, Joao Lidio da S. G. V., Da Silva, Manuela L., Araujo, Ricardo N., Gandara, Ana Caroline P., Brosson, Sebastien, Salmon, Didier, Bousbata, Sabrina, Gonzalez-Caballero, Natalia, Silber, Ariel Mariano, Alves-Bezerra, Michele, Gondim, Katia C., Silva-Neto, Mario Alberto C., Atella, Georgia C., Araujo, Helena, Dias, Felipe A., Polycarpo, Carla, Vionette-Amaral, Raquel J., Fampa, Patricia, Melo, Ana Claudia A., Tanaka, Aparecida S. [UNIFESP], Balczun, Carsten, Oliveira, Jose Henrique M., Goncalves, Renata L. S., Lazoski, Cristiano, Rivera-Pomar, Rolando, Diambra, Luis, Schaub, Guenter A., Garcia, Eloi S., Azambuja, Patricia, Braz, Gloria R. C., Oliveira, Pedro L.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNIFESP
Texto Completo: http://dx.doi.org/10.1371/journal.pntd.0002594
http://repositorio.unifesp.br/handle/11600/37171
Resumo: The bloodsucking hemipteran Rhodnius prolixus is a vector of Chagas' disease, which affects 7-8 million people today in Latin America. in contrast to other hematophagous insects, the triatomine gut is compartmentalized into three segments that perform different functions during blood digestion. Here we report analysis of transcriptomes for each of the segments using pyrosequencing technology. Comparison of transcript frequency in digestive libraries with a whole-body library was used to evaluate expression levels. All classes of digestive enzymes were highly expressed, with a predominance of cysteine and aspartic proteinases, the latter showing a significant expansion through gene duplication. Although no protein digestion is known to occur in the anterior midgut (AM), protease transcripts were found, suggesting secretion as proenzymes, being possibly activated in the posterior midgut (PM). As expected, genes related to cytoskeleton, protein synthesis apparatus, protein traffic, and secretion were abundantly transcribed. Despite the absence of a chitinous peritrophic membrane in hemipterans - which have instead a lipidic perimicrovillar membrane lining over midgut epithelia several gut-specific peritrophin transcripts were found, suggesting that these proteins perform functions other than being a structural component of the peritrophic membrane. Among immunity-related transcripts, while lysozymes and lectins were the most highly expressed, several genes belonging to the Toll pathway - found at low levels in the gut of most insects were identified, contrasting with a low abundance of transcripts from IMD and STAT pathways. Analysis of transcripts related to lipid metabolism indicates that lipids play multiple roles, being a major energy source, a substrate for perimicrovillar membrane formation, and a source for hydrocarbons possibly to produce the wax layer of the hindgut. Transcripts related to amino acid metabolism showed an unanticipated priority for degradation of tyrosine, phenylalanine, and tryptophan. Analysis of transcripts related to signaling pathways suggested a role for MAP kinases, GTPases, and LKBP1/AMP kinases related to control of cell shape and polarity, possibly in connection with regulation of cell survival, response of pathogens and nutrients. Together, our findings present a new view of the triatomine digestive apparatus and will help us understand trypanosome interaction and allow insights into hemipteran metabolic adaptations to a blood-based diet.
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spelling An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixusThe bloodsucking hemipteran Rhodnius prolixus is a vector of Chagas' disease, which affects 7-8 million people today in Latin America. in contrast to other hematophagous insects, the triatomine gut is compartmentalized into three segments that perform different functions during blood digestion. Here we report analysis of transcriptomes for each of the segments using pyrosequencing technology. Comparison of transcript frequency in digestive libraries with a whole-body library was used to evaluate expression levels. All classes of digestive enzymes were highly expressed, with a predominance of cysteine and aspartic proteinases, the latter showing a significant expansion through gene duplication. Although no protein digestion is known to occur in the anterior midgut (AM), protease transcripts were found, suggesting secretion as proenzymes, being possibly activated in the posterior midgut (PM). As expected, genes related to cytoskeleton, protein synthesis apparatus, protein traffic, and secretion were abundantly transcribed. Despite the absence of a chitinous peritrophic membrane in hemipterans - which have instead a lipidic perimicrovillar membrane lining over midgut epithelia several gut-specific peritrophin transcripts were found, suggesting that these proteins perform functions other than being a structural component of the peritrophic membrane. Among immunity-related transcripts, while lysozymes and lectins were the most highly expressed, several genes belonging to the Toll pathway - found at low levels in the gut of most insects were identified, contrasting with a low abundance of transcripts from IMD and STAT pathways. Analysis of transcripts related to lipid metabolism indicates that lipids play multiple roles, being a major energy source, a substrate for perimicrovillar membrane formation, and a source for hydrocarbons possibly to produce the wax layer of the hindgut. Transcripts related to amino acid metabolism showed an unanticipated priority for degradation of tyrosine, phenylalanine, and tryptophan. Analysis of transcripts related to signaling pathways suggested a role for MAP kinases, GTPases, and LKBP1/AMP kinases related to control of cell shape and polarity, possibly in connection with regulation of cell survival, response of pathogens and nutrients. Together, our findings present a new view of the triatomine digestive apparatus and will help us understand trypanosome interaction and allow insights into hemipteran metabolic adaptations to a blood-based diet.NIAID, Sect Vector Biol, Lab Malaria & Vector Res, NIH, Rockville, MD 20892 USAUniv Fed Rio de Janeiro, Inst Nacl Ciencia & Tecnol Entomol Mol, Rio de Janeiro, BrazilFundacao Oswaldo Cruz, Inst Oswaldo Cruz, Rio de Janeiro, BrazilUniv Fed Rio de Janeiro, Inst Bioquim Med, Programa Biotecnol & Biol Mol, Rio de Janeiro, BrazilUniv Fed Rio de Janeiro, Inst Chem, Dept Biochem, Rio de Janeiro, BrazilPrograma Biotecnol, Diretoria Metrol Aplicada Ciencias Vida, Inst Nacl Metrol Qualidade & Tecnol, BR-25250020 Rio de Janeiro, BrazilUniv Fed Rio de Janeiro, Inst Biol, Dept Genet, BR-21944970 Rio de Janeiro, BrazilUniv São Paulo, Inst Quim, Dept Bioquim, BR-01498 São Paulo, BrazilUniv Fed Rio de Janeiro, Inst Biofis Carlos Chagas Filho, BR-21941 Rio de Janeiro, BrazilEvandro Chagas Inst, Ctr Technol Innovat, Ananindeua, Para, BrazilUniv Fed Minas Gerais, Inst Ciencias Biol, Dept Parasitol, Belo Horizonte, MG, BrazilUniv Libre Bruxelles, IBMM, Gosselies, BelgiumUniv São Paulo, Inst Ciencias Biomed, Dept Parasitol, BR-05508 São Paulo, BrazilUniv Fed Rio de Janeiro, Inst Biomed Sci, Rio de Janeiro, BrazilUniv Fed Rural Rio de Janeiro, DBA, Inst Biol, Rio de Janeiro, BrazilUniversidade Federal de São Paulo, Escola Paulista Med, Dept Bioquim, São Paulo, BrazilRuhr Univ Bochum, Zool Parasitol Grp, Bochum, GermanyUniv Nacl La Plata, Ctr Reg Estudios Genom, Florencio Varela, ArgentinaUniv Nacl Noroeste Buenos Aires, Ctr Bioinvest, Pergamino, ArgentinaUniversidade Federal de São Paulo, Escola Paulista Med, Dept Bioquim, São Paulo, BrazilWeb of ScienceIntramural Research Program of the NIH, National Institute of Allergy and Infectious DiseasesCoordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ)Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)PRPq/UFMGANPCyTUNNOBAMax Planck Society Partner Laboratory ProgramINBEQMeDIWHOANPCyT: PICT-2010-0135UNNOBA: PFCI-512/12Public Library ScienceNIAIDUniversidade Federal do Rio de Janeiro (UFRJ)Fundacao Oswaldo CruzPrograma BiotecnolUniversidade de São Paulo (USP)Evandro Chagas InstUniversidade Federal de Minas Gerais (UFMG)Univ Libre BruxellesUniv Fed Rural Rio de JaneiroUniversidade Federal de São Paulo (UNIFESP)Ruhr Univ BochumUniv Nacl La PlataUniv Nacl Noroeste Buenos AiresRibeiro, Jose M. C.Genta, Fernando A.Sorgine, Marcos H. F.Logullo, RaquelMesquita, Rafael D.Paiva-Silva, Gabriela O.Majerowicz, DavidMedeiros, MarceloKoerich, LeonardoTerra, Walter R.Ferreira, CleliaPimentel, Andre C.Bisch, Paulo M.Leite, Daniel C.Diniz, Michelle M. P.Junior, Joao Lidio da S. G. V.Da Silva, Manuela L.Araujo, Ricardo N.Gandara, Ana Caroline P.Brosson, SebastienSalmon, DidierBousbata, SabrinaGonzalez-Caballero, NataliaSilber, Ariel MarianoAlves-Bezerra, MicheleGondim, Katia C.Silva-Neto, Mario Alberto C.Atella, Georgia C.Araujo, HelenaDias, Felipe A.Polycarpo, CarlaVionette-Amaral, Raquel J.Fampa, PatriciaMelo, Ana Claudia A.Tanaka, Aparecida S. [UNIFESP]Balczun, CarstenOliveira, Jose Henrique M.Goncalves, Renata L. S.Lazoski, CristianoRivera-Pomar, RolandoDiambra, LuisSchaub, Guenter A.Garcia, Eloi S.Azambuja, PatriciaBraz, Gloria R. C.Oliveira, Pedro L.2016-01-24T14:34:58Z2016-01-24T14:34:58Z2014-01-01info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersion31application/pdfhttp://dx.doi.org/10.1371/journal.pntd.0002594Plos Neglected Tropical Diseases. San Francisco: Public Library Science, v. 8, n. 1, 31 p., 2014.10.1371/journal.pntd.0002594WOS000337977300008.pdf1935-2735http://repositorio.unifesp.br/handle/11600/37171WOS:000337977300008engPlos Neglected Tropical Diseasesinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UNIFESPinstname:Universidade Federal de São Paulo (UNIFESP)instacron:UNIFESP2024-10-14T10:29:39Zoai:repositorio.unifesp.br/:11600/37171Repositório InstitucionalPUBhttp://www.repositorio.unifesp.br/oai/requestbiblioteca.csp@unifesp.bropendoar:34652024-10-14T10:29:39Repositório Institucional da UNIFESP - Universidade Federal de São Paulo (UNIFESP)false
dc.title.none.fl_str_mv An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
title An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
spellingShingle An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
Ribeiro, Jose M. C.
title_short An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
title_full An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
title_fullStr An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
title_full_unstemmed An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
title_sort An Insight into the Transcriptome of the Digestive Tract of the Bloodsucking Bug, Rhodnius prolixus
author Ribeiro, Jose M. C.
author_facet Ribeiro, Jose M. C.
Genta, Fernando A.
Sorgine, Marcos H. F.
Logullo, Raquel
Mesquita, Rafael D.
Paiva-Silva, Gabriela O.
Majerowicz, David
Medeiros, Marcelo
Koerich, Leonardo
Terra, Walter R.
Ferreira, Clelia
Pimentel, Andre C.
Bisch, Paulo M.
Leite, Daniel C.
Diniz, Michelle M. P.
Junior, Joao Lidio da S. G. V.
Da Silva, Manuela L.
Araujo, Ricardo N.
Gandara, Ana Caroline P.
Brosson, Sebastien
Salmon, Didier
Bousbata, Sabrina
Gonzalez-Caballero, Natalia
Silber, Ariel Mariano
Alves-Bezerra, Michele
Gondim, Katia C.
Silva-Neto, Mario Alberto C.
Atella, Georgia C.
Araujo, Helena
Dias, Felipe A.
Polycarpo, Carla
Vionette-Amaral, Raquel J.
Fampa, Patricia
Melo, Ana Claudia A.
Tanaka, Aparecida S. [UNIFESP]
Balczun, Carsten
Oliveira, Jose Henrique M.
Goncalves, Renata L. S.
Lazoski, Cristiano
Rivera-Pomar, Rolando
Diambra, Luis
Schaub, Guenter A.
Garcia, Eloi S.
Azambuja, Patricia
Braz, Gloria R. C.
Oliveira, Pedro L.
author_role author
author2 Genta, Fernando A.
Sorgine, Marcos H. F.
Logullo, Raquel
Mesquita, Rafael D.
Paiva-Silva, Gabriela O.
Majerowicz, David
Medeiros, Marcelo
Koerich, Leonardo
Terra, Walter R.
Ferreira, Clelia
Pimentel, Andre C.
Bisch, Paulo M.
Leite, Daniel C.
Diniz, Michelle M. P.
Junior, Joao Lidio da S. G. V.
Da Silva, Manuela L.
Araujo, Ricardo N.
Gandara, Ana Caroline P.
Brosson, Sebastien
Salmon, Didier
Bousbata, Sabrina
Gonzalez-Caballero, Natalia
Silber, Ariel Mariano
Alves-Bezerra, Michele
Gondim, Katia C.
Silva-Neto, Mario Alberto C.
Atella, Georgia C.
Araujo, Helena
Dias, Felipe A.
Polycarpo, Carla
Vionette-Amaral, Raquel J.
Fampa, Patricia
Melo, Ana Claudia A.
Tanaka, Aparecida S. [UNIFESP]
Balczun, Carsten
Oliveira, Jose Henrique M.
Goncalves, Renata L. S.
Lazoski, Cristiano
Rivera-Pomar, Rolando
Diambra, Luis
Schaub, Guenter A.
Garcia, Eloi S.
Azambuja, Patricia
Braz, Gloria R. C.
Oliveira, Pedro L.
author2_role author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv NIAID
Universidade Federal do Rio de Janeiro (UFRJ)
Fundacao Oswaldo Cruz
Programa Biotecnol
Universidade de São Paulo (USP)
Evandro Chagas Inst
Universidade Federal de Minas Gerais (UFMG)
Univ Libre Bruxelles
Univ Fed Rural Rio de Janeiro
Universidade Federal de São Paulo (UNIFESP)
Ruhr Univ Bochum
Univ Nacl La Plata
Univ Nacl Noroeste Buenos Aires
dc.contributor.author.fl_str_mv Ribeiro, Jose M. C.
Genta, Fernando A.
Sorgine, Marcos H. F.
Logullo, Raquel
Mesquita, Rafael D.
Paiva-Silva, Gabriela O.
Majerowicz, David
Medeiros, Marcelo
Koerich, Leonardo
Terra, Walter R.
Ferreira, Clelia
Pimentel, Andre C.
Bisch, Paulo M.
Leite, Daniel C.
Diniz, Michelle M. P.
Junior, Joao Lidio da S. G. V.
Da Silva, Manuela L.
Araujo, Ricardo N.
Gandara, Ana Caroline P.
Brosson, Sebastien
Salmon, Didier
Bousbata, Sabrina
Gonzalez-Caballero, Natalia
Silber, Ariel Mariano
Alves-Bezerra, Michele
Gondim, Katia C.
Silva-Neto, Mario Alberto C.
Atella, Georgia C.
Araujo, Helena
Dias, Felipe A.
Polycarpo, Carla
Vionette-Amaral, Raquel J.
Fampa, Patricia
Melo, Ana Claudia A.
Tanaka, Aparecida S. [UNIFESP]
Balczun, Carsten
Oliveira, Jose Henrique M.
Goncalves, Renata L. S.
Lazoski, Cristiano
Rivera-Pomar, Rolando
Diambra, Luis
Schaub, Guenter A.
Garcia, Eloi S.
Azambuja, Patricia
Braz, Gloria R. C.
Oliveira, Pedro L.
description The bloodsucking hemipteran Rhodnius prolixus is a vector of Chagas' disease, which affects 7-8 million people today in Latin America. in contrast to other hematophagous insects, the triatomine gut is compartmentalized into three segments that perform different functions during blood digestion. Here we report analysis of transcriptomes for each of the segments using pyrosequencing technology. Comparison of transcript frequency in digestive libraries with a whole-body library was used to evaluate expression levels. All classes of digestive enzymes were highly expressed, with a predominance of cysteine and aspartic proteinases, the latter showing a significant expansion through gene duplication. Although no protein digestion is known to occur in the anterior midgut (AM), protease transcripts were found, suggesting secretion as proenzymes, being possibly activated in the posterior midgut (PM). As expected, genes related to cytoskeleton, protein synthesis apparatus, protein traffic, and secretion were abundantly transcribed. Despite the absence of a chitinous peritrophic membrane in hemipterans - which have instead a lipidic perimicrovillar membrane lining over midgut epithelia several gut-specific peritrophin transcripts were found, suggesting that these proteins perform functions other than being a structural component of the peritrophic membrane. Among immunity-related transcripts, while lysozymes and lectins were the most highly expressed, several genes belonging to the Toll pathway - found at low levels in the gut of most insects were identified, contrasting with a low abundance of transcripts from IMD and STAT pathways. Analysis of transcripts related to lipid metabolism indicates that lipids play multiple roles, being a major energy source, a substrate for perimicrovillar membrane formation, and a source for hydrocarbons possibly to produce the wax layer of the hindgut. Transcripts related to amino acid metabolism showed an unanticipated priority for degradation of tyrosine, phenylalanine, and tryptophan. Analysis of transcripts related to signaling pathways suggested a role for MAP kinases, GTPases, and LKBP1/AMP kinases related to control of cell shape and polarity, possibly in connection with regulation of cell survival, response of pathogens and nutrients. Together, our findings present a new view of the triatomine digestive apparatus and will help us understand trypanosome interaction and allow insights into hemipteran metabolic adaptations to a blood-based diet.
publishDate 2014
dc.date.none.fl_str_mv 2014-01-01
2016-01-24T14:34:58Z
2016-01-24T14:34:58Z
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://dx.doi.org/10.1371/journal.pntd.0002594
Plos Neglected Tropical Diseases. San Francisco: Public Library Science, v. 8, n. 1, 31 p., 2014.
10.1371/journal.pntd.0002594
WOS000337977300008.pdf
1935-2735
http://repositorio.unifesp.br/handle/11600/37171
WOS:000337977300008
url http://dx.doi.org/10.1371/journal.pntd.0002594
http://repositorio.unifesp.br/handle/11600/37171
identifier_str_mv Plos Neglected Tropical Diseases. San Francisco: Public Library Science, v. 8, n. 1, 31 p., 2014.
10.1371/journal.pntd.0002594
WOS000337977300008.pdf
1935-2735
WOS:000337977300008
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Plos Neglected Tropical Diseases
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv 31
application/pdf
dc.publisher.none.fl_str_mv Public Library Science
publisher.none.fl_str_mv Public Library Science
dc.source.none.fl_str_mv reponame:Repositório Institucional da UNIFESP
instname:Universidade Federal de São Paulo (UNIFESP)
instacron:UNIFESP
instname_str Universidade Federal de São Paulo (UNIFESP)
instacron_str UNIFESP
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reponame_str Repositório Institucional da UNIFESP
collection Repositório Institucional da UNIFESP
repository.name.fl_str_mv Repositório Institucional da UNIFESP - Universidade Federal de São Paulo (UNIFESP)
repository.mail.fl_str_mv biblioteca.csp@unifesp.br
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