Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika

José Henrique M. Oliveira, Octávio A.C. Talyuli, Renata L.S. Goncalves, Gabriela Oliveira Paiva-Silva, Marcos Henrique F. Sorgine, Patricia H. Alvarenga, Pedro L. Oliveira

Research output: Contribution to journalArticle

Abstract

Background: Digestion of blood in the midgut of Aedes aegypti results in the release of pro-oxidant molecules that can be toxic to the mosquito. We hypothesized that after a blood meal, the antioxidant capacity of the midgut is increased to protect cells against oxidative stress. Concomitantly, pathogens present in the blood ingested by mosquitoes, such as the arboviruses Dengue and Zika, also have to overcome the same oxidative challenge, and the antioxidant program induced by the insect is likely to influence infection status of the mosquito and its vectorial competence. Methodology/Principal findings: We found that blood-induced catalase mRNA and activity in the midgut peaked 24 h after feeding and returned to basal levels after the completion of digestion. RNAi-mediated silencing of catalase (AAEL013407-RB) reduced enzyme activity in the midgut epithelia, increased H2O2leakage and decreased fecundity and lifespan when mosquitoes were fed H2O2. When infected with Dengue 4 and Zika virus, catalase-silenced mosquitoes showed no alteration in infection intensity (number of plaque forming units/midgut) 7 days after the infectious meal. However, catalase knockdown reduced Dengue 4, but not Zika, infection prevalence (percent of infected midguts). Conclusion/Significance: Here, we showed that blood ingestion triggers an antioxidant response in the midgut through the induction of catalase. This protection facilitates the establishment of Dengue virus in the midgut. Importantly, this mechanism appears to be specific for Dengue because catalase silencing did not change Zika virus prevalence. In summary, our data suggest that redox balance in the midgut modulates mosquito vectorial competence to arboviral infections.

Original languageEnglish (US)
Article numbere0005525
JournalPLoS Neglected Tropical Diseases
Volume11
Issue number4
DOIs
StatePublished - Apr 5 2017
Externally publishedYes

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Dengue
Aedes
Culicidae
Catalase
Oxidative Stress
Infection
Dengue Virus
Antioxidants
Mental Competency
Meals
Digestion
Arboviruses
Poisons
RNA Interference
Oxidation-Reduction
Fertility
Insects
Reactive Oxygen Species
Epithelium
Eating

ASJC Scopus subject areas

  • Pharmacology, Toxicology and Pharmaceutics(all)
  • Public Health, Environmental and Occupational Health
  • Infectious Diseases

Cite this

Oliveira, J. H. M., Talyuli, O. A. C., Goncalves, R. L. S., Paiva-Silva, G. O., Sorgine, M. H. F., Alvarenga, P. H., & Oliveira, P. L. (2017). Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika. PLoS Neglected Tropical Diseases, 11(4), [e0005525]. https://doi.org/10.1371/journal.pntd.0005525

Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika. / Oliveira, José Henrique M.; Talyuli, Octávio A.C.; Goncalves, Renata L.S.; Paiva-Silva, Gabriela Oliveira; Sorgine, Marcos Henrique F.; Alvarenga, Patricia H.; Oliveira, Pedro L.

In: PLoS Neglected Tropical Diseases, Vol. 11, No. 4, e0005525, 05.04.2017.

Research output: Contribution to journalArticle

Oliveira, JHM, Talyuli, OAC, Goncalves, RLS, Paiva-Silva, GO, Sorgine, MHF, Alvarenga, PH & Oliveira, PL 2017, 'Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika', PLoS Neglected Tropical Diseases, vol. 11, no. 4, e0005525. https://doi.org/10.1371/journal.pntd.0005525
Oliveira, José Henrique M. ; Talyuli, Octávio A.C. ; Goncalves, Renata L.S. ; Paiva-Silva, Gabriela Oliveira ; Sorgine, Marcos Henrique F. ; Alvarenga, Patricia H. ; Oliveira, Pedro L. / Catalase protects Aedes aegypti from oxidative stress and increases midgut infection prevalence of Dengue but not Zika. In: PLoS Neglected Tropical Diseases. 2017 ; Vol. 11, No. 4.
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abstract = "Background: Digestion of blood in the midgut of Aedes aegypti results in the release of pro-oxidant molecules that can be toxic to the mosquito. We hypothesized that after a blood meal, the antioxidant capacity of the midgut is increased to protect cells against oxidative stress. Concomitantly, pathogens present in the blood ingested by mosquitoes, such as the arboviruses Dengue and Zika, also have to overcome the same oxidative challenge, and the antioxidant program induced by the insect is likely to influence infection status of the mosquito and its vectorial competence. Methodology/Principal findings: We found that blood-induced catalase mRNA and activity in the midgut peaked 24 h after feeding and returned to basal levels after the completion of digestion. RNAi-mediated silencing of catalase (AAEL013407-RB) reduced enzyme activity in the midgut epithelia, increased H2O2leakage and decreased fecundity and lifespan when mosquitoes were fed H2O2. When infected with Dengue 4 and Zika virus, catalase-silenced mosquitoes showed no alteration in infection intensity (number of plaque forming units/midgut) 7 days after the infectious meal. However, catalase knockdown reduced Dengue 4, but not Zika, infection prevalence (percent of infected midguts). Conclusion/Significance: Here, we showed that blood ingestion triggers an antioxidant response in the midgut through the induction of catalase. This protection facilitates the establishment of Dengue virus in the midgut. Importantly, this mechanism appears to be specific for Dengue because catalase silencing did not change Zika virus prevalence. In summary, our data suggest that redox balance in the midgut modulates mosquito vectorial competence to arboviral infections.",
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AU - Goncalves, Renata L.S.

AU - Paiva-Silva, Gabriela Oliveira

AU - Sorgine, Marcos Henrique F.

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