Insulin-like peptides (ILPs) play important roles in growth and metabolic homeostasis, but have also emerged as key regulators of stress responses and immunity in a variety of vertebrates and invertebrates. Furthermore, a growing literature suggests that insulin signaling-dependent metabolic provisioning can influence host responses to infection and affect infection outcomes. In line with these studies, we previously showed that knockdown of either of two closely related, infection-induced ILPs, ILP3 and ILP4, in the mosquito Anopheles stephensi decreased infection with the human malaria parasite Plasmodium falciparum through kinetically distinct effects on parasite death. However, the precise mechanisms by which ILP3 and ILP4 control the response to infection remained unknown. To address this knowledge gap, we used a complementary approach of direct ILP supplementation into the blood meal to further define ILP-specific effects on mosquito biology and parasite infection. Notably, we observed that feeding resulted in differential effects of ILP3 and ILP4 on blood-feeding behavior and P. falciparum development. These effects depended on ILP-specific regulation of intermediary metabolism in the mosquito midgut, suggesting a major contribution of ILP-dependent metabolic shifts to the regulation of infection resistance and parasite transmission. Accordingly, our data implicate endogenous ILP signaling in balancing intermediary metabolism for the host response to infection, affirming this emerging tenet in host–pathogen interactions with novel insights from a system of significant public health importance.
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October 2016
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A representation of a mitochondrion. In this issue, Kowaltowski et al. review aspects of mitochondrial biology that have an impact on aging in model organisms and selected mammalian cells and tissues. See pp. 3421–3449 for further details.
Research Article|
October 11 2016
Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism
Jose E. Pietri;
Jose E. Pietri
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Nazzy Pakpour;
Nazzy Pakpour
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Eleonora Napoli;
Eleonora Napoli
2Department of Molecular Biosciences, University of California Davis, Davis, CA, U.S.A.
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Gyu Song;
Gyu Song
2Department of Molecular Biosciences, University of California Davis, Davis, CA, U.S.A.
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Eduardo Pietri;
Eduardo Pietri
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Rashaun Potts;
Rashaun Potts
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Kong W. Cheung;
Kong W. Cheung
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Gregory Walker;
Gregory Walker
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Michael A. Riehle;
Michael A. Riehle
3Department of Entomology, University of Arizona, Tucson, AZ, U.S.A.
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Hannah Starcevich;
Hannah Starcevich
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Cecilia Giulivi;
Cecilia Giulivi
2Department of Molecular Biosciences, University of California Davis, Davis, CA, U.S.A.
4Medical Investigations of Neurodevelopmental Disorders (M.I.N.D.) Institute, University of California Davis, Sacramento, CA, U.S.A.
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Edwin E. Lewis;
Edwin E. Lewis
5Department of Entomology and Nematology, University of California, Davis, CA, U.S.A.
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Shirley Luckhart
Shirley Luckhart
1Department of Medical Microbiology and Immunology, University of California Davis, Davis, CA, U.S.A.
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Publisher: Portland Press Ltd
Received:
March 30 2016
Revision Received:
August 02 2016
Accepted:
August 05 2016
Accepted Manuscript online:
August 05 2016
Online ISSN: 1470-8728
Print ISSN: 0264-6021
© 2016 The Author(s); published by Portland Press Limited on behalf of the Biochemical Society
2016
Biochem J (2016) 473 (20): 3487–3503.
Article history
Received:
March 30 2016
Revision Received:
August 02 2016
Accepted:
August 05 2016
Accepted Manuscript online:
August 05 2016
Citation
Jose E. Pietri, Nazzy Pakpour, Eleonora Napoli, Gyu Song, Eduardo Pietri, Rashaun Potts, Kong W. Cheung, Gregory Walker, Michael A. Riehle, Hannah Starcevich, Cecilia Giulivi, Edwin E. Lewis, Shirley Luckhart; Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism. Biochem J 15 October 2016; 473 (20): 3487–3503. doi: https://doi.org/10.1042/BCJ20160271
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