Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod

Detalhes bibliográficos
Autor(a) principal: Fuzita, Felipe J.
Data de Publicação: 2015
Outros Autores: Pinkse, Martijn W. H., Patane, Jose S. L., Juliano, Maria Aparecida [UNIFESP], Verhaert, Peter D. E. M., Lopes, Adriana R.
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Institucional da UNIFESP
dARK ID: ark:/48912/001300000788z
Texto Completo: http://dx.doi.org/10.1371/journal.pone.0123841
http://repositorio.unifesp.br/handle/11600/39004
Resumo: Scorpions are among the oldest terrestrial arthropods and they have passed through small morphological changes during their evolutionary history on land. They are efficient predators capable of capturing and consuming large preys and due to envenomation these animals can become a human health challenge. Understanding the physiology of scorpions can not only lead to evolutionary insights but also is a crucial step in the development of control strategies. However, the digestive process in scorpions has been scarcely studied. in this work, we describe the combinatory use of next generation sequencing, proteomic analysis and biochemical assays in order to investigate the digestive process in the yellow scorpion Tityus serrulatus, mainly focusing in the initial protein digestion. the transcriptome generated database allowed the quantitative identification by mass spectrometry of different enzymes and proteins involved in digestion. All the results suggested that cysteine cathepsins play an important role in protein digestion. Two digestive cysteine cathepsins were isolated and characterized presenting acidic characteristics (pH optima and stability), zymogen conversion to the mature form after acidic activation and a cross-class inhibition by pepstatin. A more elucidative picture of the molecular mechanism of digestion in a scorpion was proposed based on our results from Tityus serrulatus. the midgut and midgut glands (MMG) are composed by secretory and digestive cells. in fasting animals, the secretory granules are ready for the next predation event, containing enzymes needed for alkaline extra-oral digestion which will compose the digestive fluid, such as trypsins, astacins and chitinase. the digestive vacuoles are filled with an acidic proteolytic cocktail to the intracellular digestion composed by cathepsins L, B, F, D and legumain. Other proteins as lipases, carbohydrases, ctenitoxins and a chitolectin with a perithrophin domain were also detected. Evolutionarily, a large gene duplication of cathepsin L occurred in Arachnida with the sequences from ticks being completely divergent from other arachnids probably due to the particular selective pressures over this group.
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spelling Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient ArthropodScorpions are among the oldest terrestrial arthropods and they have passed through small morphological changes during their evolutionary history on land. They are efficient predators capable of capturing and consuming large preys and due to envenomation these animals can become a human health challenge. Understanding the physiology of scorpions can not only lead to evolutionary insights but also is a crucial step in the development of control strategies. However, the digestive process in scorpions has been scarcely studied. in this work, we describe the combinatory use of next generation sequencing, proteomic analysis and biochemical assays in order to investigate the digestive process in the yellow scorpion Tityus serrulatus, mainly focusing in the initial protein digestion. the transcriptome generated database allowed the quantitative identification by mass spectrometry of different enzymes and proteins involved in digestion. All the results suggested that cysteine cathepsins play an important role in protein digestion. Two digestive cysteine cathepsins were isolated and characterized presenting acidic characteristics (pH optima and stability), zymogen conversion to the mature form after acidic activation and a cross-class inhibition by pepstatin. A more elucidative picture of the molecular mechanism of digestion in a scorpion was proposed based on our results from Tityus serrulatus. the midgut and midgut glands (MMG) are composed by secretory and digestive cells. in fasting animals, the secretory granules are ready for the next predation event, containing enzymes needed for alkaline extra-oral digestion which will compose the digestive fluid, such as trypsins, astacins and chitinase. the digestive vacuoles are filled with an acidic proteolytic cocktail to the intracellular digestion composed by cathepsins L, B, F, D and legumain. Other proteins as lipases, carbohydrases, ctenitoxins and a chitolectin with a perithrophin domain were also detected. Evolutionarily, a large gene duplication of cathepsin L occurred in Arachnida with the sequences from ticks being completely divergent from other arachnids probably due to the particular selective pressures over this group.Inst Butantan, Biochem & Biophys Lab, São Paulo, BrazilUniv São Paulo, Biotechnol Program, São Paulo, BrazilDelft Univ Technol, Lab Analyt Biotechnol & Innovat Peptide Biol, Delft, NetherlandsUniv São Paulo, Inst Chem, Dept Biochem, São Paulo, BrazilUniversidade Federal de São Paulo, Dept Biophys, São Paulo, BrazilUniversidade Federal de São Paulo, Dept Biophys, São Paulo, BrazilWeb of ScienceFundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP)Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)Netherlands Proteomics CentreFAPESP: 2005/02486-1FAPESP: 2006/03474-0CNPq: 237706/2012-1Public Library ScienceInst ButantanUniversidade de São Paulo (USP)Delft Univ TechnolUniversidade Federal de São Paulo (UNIFESP)Fuzita, Felipe J.Pinkse, Martijn W. H.Patane, Jose S. L.Juliano, Maria Aparecida [UNIFESP]Verhaert, Peter D. E. M.Lopes, Adriana R.2016-01-24T14:40:24Z2016-01-24T14:40:24Z2015-04-15info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersion31application/pdfhttp://dx.doi.org/10.1371/journal.pone.0123841Plos One. San Francisco: Public Library Science, v. 10, n. 4, 31 p., 2015.10.1371/journal.pone.0123841WOS000353015800119.pdf1932-6203http://repositorio.unifesp.br/handle/11600/39004WOS:000353015800119ark:/48912/001300000788zengPlos Oneinfo:eu-repo/semantics/openAccessreponame:Repositório Institucional da UNIFESPinstname:Universidade Federal de São Paulo (UNIFESP)instacron:UNIFESP2024-08-01T08:07:10Zoai:repositorio.unifesp.br/:11600/39004Repositório InstitucionalPUBhttp://www.repositorio.unifesp.br/oai/requestbiblioteca.csp@unifesp.bropendoar:34652024-12-11T20:02:33.106972Repositório Institucional da UNIFESP - Universidade Federal de São Paulo (UNIFESP)false
dc.title.none.fl_str_mv Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
title Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
spellingShingle Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
Fuzita, Felipe J.
title_short Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
title_full Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
title_fullStr Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
title_full_unstemmed Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
title_sort Biochemical, Transcriptomic and Proteomic Analyses of Digestion in the Scorpion Tityus serrulatus: Insights into Function and Evolution of Digestion in an Ancient Arthropod
author Fuzita, Felipe J.
author_facet Fuzita, Felipe J.
Pinkse, Martijn W. H.
Patane, Jose S. L.
Juliano, Maria Aparecida [UNIFESP]
Verhaert, Peter D. E. M.
Lopes, Adriana R.
author_role author
author2 Pinkse, Martijn W. H.
Patane, Jose S. L.
Juliano, Maria Aparecida [UNIFESP]
Verhaert, Peter D. E. M.
Lopes, Adriana R.
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Inst Butantan
Universidade de São Paulo (USP)
Delft Univ Technol
Universidade Federal de São Paulo (UNIFESP)
dc.contributor.author.fl_str_mv Fuzita, Felipe J.
Pinkse, Martijn W. H.
Patane, Jose S. L.
Juliano, Maria Aparecida [UNIFESP]
Verhaert, Peter D. E. M.
Lopes, Adriana R.
description Scorpions are among the oldest terrestrial arthropods and they have passed through small morphological changes during their evolutionary history on land. They are efficient predators capable of capturing and consuming large preys and due to envenomation these animals can become a human health challenge. Understanding the physiology of scorpions can not only lead to evolutionary insights but also is a crucial step in the development of control strategies. However, the digestive process in scorpions has been scarcely studied. in this work, we describe the combinatory use of next generation sequencing, proteomic analysis and biochemical assays in order to investigate the digestive process in the yellow scorpion Tityus serrulatus, mainly focusing in the initial protein digestion. the transcriptome generated database allowed the quantitative identification by mass spectrometry of different enzymes and proteins involved in digestion. All the results suggested that cysteine cathepsins play an important role in protein digestion. Two digestive cysteine cathepsins were isolated and characterized presenting acidic characteristics (pH optima and stability), zymogen conversion to the mature form after acidic activation and a cross-class inhibition by pepstatin. A more elucidative picture of the molecular mechanism of digestion in a scorpion was proposed based on our results from Tityus serrulatus. the midgut and midgut glands (MMG) are composed by secretory and digestive cells. in fasting animals, the secretory granules are ready for the next predation event, containing enzymes needed for alkaline extra-oral digestion which will compose the digestive fluid, such as trypsins, astacins and chitinase. the digestive vacuoles are filled with an acidic proteolytic cocktail to the intracellular digestion composed by cathepsins L, B, F, D and legumain. Other proteins as lipases, carbohydrases, ctenitoxins and a chitolectin with a perithrophin domain were also detected. Evolutionarily, a large gene duplication of cathepsin L occurred in Arachnida with the sequences from ticks being completely divergent from other arachnids probably due to the particular selective pressures over this group.
publishDate 2015
dc.date.none.fl_str_mv 2015-04-15
2016-01-24T14:40:24Z
2016-01-24T14:40:24Z
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.pone.0123841
Plos One. San Francisco: Public Library Science, v. 10, n. 4, 31 p., 2015.
10.1371/journal.pone.0123841
WOS000353015800119.pdf
1932-6203
http://repositorio.unifesp.br/handle/11600/39004
WOS:000353015800119
dc.identifier.dark.fl_str_mv ark:/48912/001300000788z
url http://dx.doi.org/10.1371/journal.pone.0123841
http://repositorio.unifesp.br/handle/11600/39004
identifier_str_mv Plos One. San Francisco: Public Library Science, v. 10, n. 4, 31 p., 2015.
10.1371/journal.pone.0123841
WOS000353015800119.pdf
1932-6203
WOS:000353015800119
ark:/48912/001300000788z
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Plos One
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
institution UNIFESP
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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