Digestive peptidase evolution in holometabolous insects led to a divergent group of enzymes in Lepidoptera

Handle URI:
http://hdl.handle.net/10754/597981
Title:
Digestive peptidase evolution in holometabolous insects led to a divergent group of enzymes in Lepidoptera
Authors:
Dias, Renata O.; Via, Allegra; Brandão, Marcelo M.; Tramontano, Anna; Silva-Filho, Marcio C. ( 0000-0003-2129-0388 )
Abstract:
© 2015 Elsevier Ltd. Trypsins and chymotrypsins are well-studied serine peptidases that cleave peptide bonds at the carboxyl side of basic and hydrophobic l-amino acids, respectively. These enzymes are largely responsible for the digestion of proteins. Three primary processes regulate the activity of these peptidases: secretion, precursor (zymogen) activation and substrate-binding site recognition. Here, we present a detailed phylogenetic analysis of trypsins and chymotrypsins in three orders of holometabolous insects and reveal divergent characteristics of Lepidoptera enzymes in comparison with those of Coleoptera and Diptera. In particular, trypsin subsite S1 was more hydrophilic in Lepidoptera than in Coleoptera and Diptera, whereas subsites S2-S4 were more hydrophobic, suggesting different substrate preferences. Furthermore, Lepidoptera displayed a lineage-specific trypsin group belonging only to the Noctuidae family. Evidence for facilitated trypsin auto-activation events were also observed in all the insect orders studied, with the characteristic zymogen activation motif complementary to the trypsin active site. In contrast, insect chymotrypsins did not seem to have a peculiar evolutionary history with respect to their mammal counterparts. Overall, our findings suggest that the need for fast digestion allowed holometabolous insects to evolve divergent groups of peptidases with high auto-activation rates, and highlight that the evolution of trypsins led to a most diverse group of enzymes in Lepidoptera.
Citation:
Dias RO, Via A, Brandão MM, Tramontano A, Silva-Filho MC (2015) Digestive peptidase evolution in holometabolous insects led to a divergent group of enzymes in Lepidoptera. Insect Biochemistry and Molecular Biology 58: 1–11. Available: http://dx.doi.org/10.1016/j.ibmb.2014.12.009.
Publisher:
Elsevier BV
Journal:
Insect Biochemistry and Molecular Biology
KAUST Grant Number:
KUK-I1-012-43
Issue Date:
Mar-2015
DOI:
10.1016/j.ibmb.2014.12.009
PubMed ID:
25600115
Type:
Article
ISSN:
0965-1748
Sponsors:
This work was supported by Sao Paulo Research Foundation (FAPESP) grants 2008/52067-3, to MCSF, 2010/17110-5 and 2012/03040-0 to ROD and 2011/00417-3 to MMB. This work was also supported by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) grant 482737/2012-3 to MCSF. AV is supported by the King Abdullah University of Science and Technology (KAUST, grant KUK-I1-012-43). We thank Walter R. Terra for critical reading of this manuscript. MCSF is also a research fellow of CNPq.
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Full metadata record

DC FieldValue Language
dc.contributor.authorDias, Renata O.en
dc.contributor.authorVia, Allegraen
dc.contributor.authorBrandão, Marcelo M.en
dc.contributor.authorTramontano, Annaen
dc.contributor.authorSilva-Filho, Marcio C.en
dc.date.accessioned2016-02-25T13:10:18Zen
dc.date.available2016-02-25T13:10:18Zen
dc.date.issued2015-03en
dc.identifier.citationDias RO, Via A, Brandão MM, Tramontano A, Silva-Filho MC (2015) Digestive peptidase evolution in holometabolous insects led to a divergent group of enzymes in Lepidoptera. Insect Biochemistry and Molecular Biology 58: 1–11. Available: http://dx.doi.org/10.1016/j.ibmb.2014.12.009.en
dc.identifier.issn0965-1748en
dc.identifier.pmid25600115en
dc.identifier.doi10.1016/j.ibmb.2014.12.009en
dc.identifier.urihttp://hdl.handle.net/10754/597981en
dc.description.abstract© 2015 Elsevier Ltd. Trypsins and chymotrypsins are well-studied serine peptidases that cleave peptide bonds at the carboxyl side of basic and hydrophobic l-amino acids, respectively. These enzymes are largely responsible for the digestion of proteins. Three primary processes regulate the activity of these peptidases: secretion, precursor (zymogen) activation and substrate-binding site recognition. Here, we present a detailed phylogenetic analysis of trypsins and chymotrypsins in three orders of holometabolous insects and reveal divergent characteristics of Lepidoptera enzymes in comparison with those of Coleoptera and Diptera. In particular, trypsin subsite S1 was more hydrophilic in Lepidoptera than in Coleoptera and Diptera, whereas subsites S2-S4 were more hydrophobic, suggesting different substrate preferences. Furthermore, Lepidoptera displayed a lineage-specific trypsin group belonging only to the Noctuidae family. Evidence for facilitated trypsin auto-activation events were also observed in all the insect orders studied, with the characteristic zymogen activation motif complementary to the trypsin active site. In contrast, insect chymotrypsins did not seem to have a peculiar evolutionary history with respect to their mammal counterparts. Overall, our findings suggest that the need for fast digestion allowed holometabolous insects to evolve divergent groups of peptidases with high auto-activation rates, and highlight that the evolution of trypsins led to a most diverse group of enzymes in Lepidoptera.en
dc.description.sponsorshipThis work was supported by Sao Paulo Research Foundation (FAPESP) grants 2008/52067-3, to MCSF, 2010/17110-5 and 2012/03040-0 to ROD and 2011/00417-3 to MMB. This work was also supported by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) grant 482737/2012-3 to MCSF. AV is supported by the King Abdullah University of Science and Technology (KAUST, grant KUK-I1-012-43). We thank Walter R. Terra for critical reading of this manuscript. MCSF is also a research fellow of CNPq.en
dc.publisherElsevier BVen
dc.subjectChymotrypsinen
dc.subjectColeopteraen
dc.subjectDipteraen
dc.subjectLepidopteraen
dc.subjectSerine peptidaseen
dc.subjectTrypsinen
dc.titleDigestive peptidase evolution in holometabolous insects led to a divergent group of enzymes in Lepidopteraen
dc.typeArticleen
dc.identifier.journalInsect Biochemistry and Molecular Biologyen
dc.contributor.institutionUniversidade de Sao Paulo - USP, Sao Paulo, Brazilen
dc.contributor.institutionUniversita degli Studi di Roma La Sapienza, Rome, Italyen
dc.contributor.institutionUniversidade Estadual de Campinas, Campinas, Brazilen
kaust.grant.numberKUK-I1-012-43en

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