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Accepted Manuscript

Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism

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
Biochemical Journal Aug 05, 2016, BCJ20160271; DOI: 10.1042/BCJ20160271
Jose E Pietri
UC Davis, Davis, California, United States
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Nazzy Pakpour
UC Davis, Davis, United States
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Eleonora Napoli
UC Davis, Davis, United States
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Gyu Song
UC Davis, Davis, United States
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Eduardo Pietri
UC Davis, Davis, United States
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Rashaun Potts
UC Davis, Davis, United States
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Kong W Cheung
UC Davis, Davis, United States
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Gregory Walker
UC Davis, Davis, United States
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Michael A Riehle
University of Arizona, Tucson, United States
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Hannah Starcevich
UC Davis, Davis, United States
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Cecilia Giulivi
Department Molecular Biosciences, University of California, School of Veterinary Medicine, One Shields Ave, 1120 Haring Hall, DAVIS, CA, 95616, United States
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Edwin E Lewis
UC Davis, Davis, United States
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Shirley Luckhart
UC Davis, Davis, United States
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  • For correspondence: sluckhart@ucdavis.edu
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Abstract

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. Further, 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.

  • Plasmodium falciparum
  • Anopheles
  • malaria
  • insulin
  • ILP
  • mosquito
  • ©2016 The Author(s)

This is an Accepted Manuscript; not the final Version of Record. Archiving permitted only in line with the archiving policy of Portland Press Limited. All other rights reserved.

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Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism
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
Biochemical Journal Aug 2016, BCJ20160271; DOI: 10.1042/BCJ20160271
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Two insulin-like peptides differentially regulate malaria parasite infection in the mosquito through effects on intermediary metabolism
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
Biochemical Journal Aug 2016, BCJ20160271; DOI: 10.1042/BCJ20160271

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Keywords

Plasmodium falciparum
Anopheles
malaria
insulin
ILP
mosquito

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