Global proteome changes in larvae of Callosobruchus maculatus Coleoptera: Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor

Fábio C S Nogueira, Carlos P. Silva, Daniel Alexandre, Richard I. Samuels, Emanoella L. Soares, Francisco J L Aragão, Giuseppe Palmisano, Gilberto B. Domont, Peter Roepstorff, Francisco A P Campos

Research output: Contribution to journalArticle

15 Citations (Scopus)

Abstract

The seed-feeding beetle Callosobruchus maculatus is an important cowpea pest (Vigna unguiculata) as well as an interesting model to study insect digestive physiology. The larvae of C. maculatus rely on cysteine and aspartic peptidases to digest proteins in their diet. In this work, the global proteomic changes induced in the intestinal tract of larval C. maculatus challenged by the ingestion of cystatin, a cysteine peptidase inhibitor, was investigated by a nanoLC-MS/MS approach. The ingestion of cystatin caused a delay in the development of the larvae, but the mortality was not high, indicating that C. maculatus is able to adapt to this inhibitor. This proteomic strategy resulted in the identification of 752 and 550 protein groups in the midgut epithelia and midgut contents, respectively, and quantitative analyses allowed us to establish relative differences of the identified proteins. Ingestion of cystatin led to significant changes in the proteome of both the midgut epithelia and midgut contents. We have observed that proteins related to plant cell wall degradation, particularly the key glycoside hydrolases of the families GH5 (endo-β-1,4-mannanase) and GH 28 (polygalacturonase) were overexpressed. Conversely, α-amylases were downexpressed, indicating that an increase in hemicelluloses digestion helps the larvae to cope with the challenge of cystatin ingestion. Furthermore, a number of proteins associated with transcription/translation and antistress reactions were among the cystatin-responsive proteins, implying that a substantial rearrangement in the proteome occurred in C. maculatus exposed to the inhibitor.

Original languageEnglish
Pages (from-to)2704-2715
Number of pages12
JournalProteomics
Volume12
Issue number17
DOIs
Publication statusPublished - Aug 2012

Fingerprint

Cysteine Proteinase Inhibitors
Cystatins
Beetles
Proteome
Larva
Eating
Proteins
Proteomics
Cysteine
Digestive System Physiological Phenomena
Epithelium
Polygalacturonase
Glycoside Hydrolases
Physiology
Plant Cells
Transcription
Amylases
Nutrition
Protease Inhibitors
Cell Wall

Keywords

  • Callosobruchus maculatus
  • Egg white cystatin
  • Insect digestive enzymes
  • Peptidase inhibitors
  • Plant proteomics
  • Vigna unguiculata

ASJC Scopus subject areas

  • Molecular Biology
  • Biochemistry

Cite this

Nogueira, F. C. S., Silva, C. P., Alexandre, D., Samuels, R. I., Soares, E. L., Aragão, F. J. L., ... Campos, F. A. P. (2012). Global proteome changes in larvae of Callosobruchus maculatus Coleoptera: Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor. Proteomics, 12(17), 2704-2715. https://doi.org/10.1002/pmic.201200039

Global proteome changes in larvae of Callosobruchus maculatus Coleoptera : Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor. / Nogueira, Fábio C S; Silva, Carlos P.; Alexandre, Daniel; Samuels, Richard I.; Soares, Emanoella L.; Aragão, Francisco J L; Palmisano, Giuseppe; Domont, Gilberto B.; Roepstorff, Peter; Campos, Francisco A P.

In: Proteomics, Vol. 12, No. 17, 08.2012, p. 2704-2715.

Research output: Contribution to journalArticle

Nogueira, FCS, Silva, CP, Alexandre, D, Samuels, RI, Soares, EL, Aragão, FJL, Palmisano, G, Domont, GB, Roepstorff, P & Campos, FAP 2012, 'Global proteome changes in larvae of Callosobruchus maculatus Coleoptera: Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor', Proteomics, vol. 12, no. 17, pp. 2704-2715. https://doi.org/10.1002/pmic.201200039
Nogueira, Fábio C S ; Silva, Carlos P. ; Alexandre, Daniel ; Samuels, Richard I. ; Soares, Emanoella L. ; Aragão, Francisco J L ; Palmisano, Giuseppe ; Domont, Gilberto B. ; Roepstorff, Peter ; Campos, Francisco A P. / Global proteome changes in larvae of Callosobruchus maculatus Coleoptera : Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor. In: Proteomics. 2012 ; Vol. 12, No. 17. pp. 2704-2715.
@article{f45c3791df09498a8a9f7bb15155b6d4,
title = "Global proteome changes in larvae of Callosobruchus maculatus Coleoptera: Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor",
abstract = "The seed-feeding beetle Callosobruchus maculatus is an important cowpea pest (Vigna unguiculata) as well as an interesting model to study insect digestive physiology. The larvae of C. maculatus rely on cysteine and aspartic peptidases to digest proteins in their diet. In this work, the global proteomic changes induced in the intestinal tract of larval C. maculatus challenged by the ingestion of cystatin, a cysteine peptidase inhibitor, was investigated by a nanoLC-MS/MS approach. The ingestion of cystatin caused a delay in the development of the larvae, but the mortality was not high, indicating that C. maculatus is able to adapt to this inhibitor. This proteomic strategy resulted in the identification of 752 and 550 protein groups in the midgut epithelia and midgut contents, respectively, and quantitative analyses allowed us to establish relative differences of the identified proteins. Ingestion of cystatin led to significant changes in the proteome of both the midgut epithelia and midgut contents. We have observed that proteins related to plant cell wall degradation, particularly the key glycoside hydrolases of the families GH5 (endo-β-1,4-mannanase) and GH 28 (polygalacturonase) were overexpressed. Conversely, α-amylases were downexpressed, indicating that an increase in hemicelluloses digestion helps the larvae to cope with the challenge of cystatin ingestion. Furthermore, a number of proteins associated with transcription/translation and antistress reactions were among the cystatin-responsive proteins, implying that a substantial rearrangement in the proteome occurred in C. maculatus exposed to the inhibitor.",
keywords = "Callosobruchus maculatus, Egg white cystatin, Insect digestive enzymes, Peptidase inhibitors, Plant proteomics, Vigna unguiculata",
author = "Nogueira, {F{\'a}bio C S} and Silva, {Carlos P.} and Daniel Alexandre and Samuels, {Richard I.} and Soares, {Emanoella L.} and Arag{\~a}o, {Francisco J L} and Giuseppe Palmisano and Domont, {Gilberto B.} and Peter Roepstorff and Campos, {Francisco A P}",
year = "2012",
month = "8",
doi = "10.1002/pmic.201200039",
language = "English",
volume = "12",
pages = "2704--2715",
journal = "Proteomics",
issn = "1615-9853",
publisher = "Wiley-VCH Verlag",
number = "17",

}

TY - JOUR

T1 - Global proteome changes in larvae of Callosobruchus maculatus Coleoptera

T2 - Chrysomelidae:Bruchinae) following ingestion of a cysteine proteinase inhibitor

AU - Nogueira, Fábio C S

AU - Silva, Carlos P.

AU - Alexandre, Daniel

AU - Samuels, Richard I.

AU - Soares, Emanoella L.

AU - Aragão, Francisco J L

AU - Palmisano, Giuseppe

AU - Domont, Gilberto B.

AU - Roepstorff, Peter

AU - Campos, Francisco A P

PY - 2012/8

Y1 - 2012/8

N2 - The seed-feeding beetle Callosobruchus maculatus is an important cowpea pest (Vigna unguiculata) as well as an interesting model to study insect digestive physiology. The larvae of C. maculatus rely on cysteine and aspartic peptidases to digest proteins in their diet. In this work, the global proteomic changes induced in the intestinal tract of larval C. maculatus challenged by the ingestion of cystatin, a cysteine peptidase inhibitor, was investigated by a nanoLC-MS/MS approach. The ingestion of cystatin caused a delay in the development of the larvae, but the mortality was not high, indicating that C. maculatus is able to adapt to this inhibitor. This proteomic strategy resulted in the identification of 752 and 550 protein groups in the midgut epithelia and midgut contents, respectively, and quantitative analyses allowed us to establish relative differences of the identified proteins. Ingestion of cystatin led to significant changes in the proteome of both the midgut epithelia and midgut contents. We have observed that proteins related to plant cell wall degradation, particularly the key glycoside hydrolases of the families GH5 (endo-β-1,4-mannanase) and GH 28 (polygalacturonase) were overexpressed. Conversely, α-amylases were downexpressed, indicating that an increase in hemicelluloses digestion helps the larvae to cope with the challenge of cystatin ingestion. Furthermore, a number of proteins associated with transcription/translation and antistress reactions were among the cystatin-responsive proteins, implying that a substantial rearrangement in the proteome occurred in C. maculatus exposed to the inhibitor.

AB - The seed-feeding beetle Callosobruchus maculatus is an important cowpea pest (Vigna unguiculata) as well as an interesting model to study insect digestive physiology. The larvae of C. maculatus rely on cysteine and aspartic peptidases to digest proteins in their diet. In this work, the global proteomic changes induced in the intestinal tract of larval C. maculatus challenged by the ingestion of cystatin, a cysteine peptidase inhibitor, was investigated by a nanoLC-MS/MS approach. The ingestion of cystatin caused a delay in the development of the larvae, but the mortality was not high, indicating that C. maculatus is able to adapt to this inhibitor. This proteomic strategy resulted in the identification of 752 and 550 protein groups in the midgut epithelia and midgut contents, respectively, and quantitative analyses allowed us to establish relative differences of the identified proteins. Ingestion of cystatin led to significant changes in the proteome of both the midgut epithelia and midgut contents. We have observed that proteins related to plant cell wall degradation, particularly the key glycoside hydrolases of the families GH5 (endo-β-1,4-mannanase) and GH 28 (polygalacturonase) were overexpressed. Conversely, α-amylases were downexpressed, indicating that an increase in hemicelluloses digestion helps the larvae to cope with the challenge of cystatin ingestion. Furthermore, a number of proteins associated with transcription/translation and antistress reactions were among the cystatin-responsive proteins, implying that a substantial rearrangement in the proteome occurred in C. maculatus exposed to the inhibitor.

KW - Callosobruchus maculatus

KW - Egg white cystatin

KW - Insect digestive enzymes

KW - Peptidase inhibitors

KW - Plant proteomics

KW - Vigna unguiculata

UR - http://www.scopus.com/inward/record.url?scp=84865547286&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84865547286&partnerID=8YFLogxK

U2 - 10.1002/pmic.201200039

DO - 10.1002/pmic.201200039

M3 - Article

C2 - 22833537

AN - SCOPUS:84865547286

VL - 12

SP - 2704

EP - 2715

JO - Proteomics

JF - Proteomics

SN - 1615-9853

IS - 17

ER -