Mosquito salivary apyrase regulates blood meal hemostasis and facilitates malaria parasite transmission

Zarna Rajeshkumar Pala, Thiago Luiz Alves e Silva, Mahnaz Minai, Benjamin Crews, Eduardo Patino-Martinez, Carmelo Carmona-Rivera, Paola Carolina Valenzuela Leon, Ines Martin-Martin, Yevel Flores-Garcia, Raul E. Cachau, Liya Muslinkina, Apostolos G. Gittis, Naman Srivastava, David N. Garboczi, Derron A. Alves, Mariana J. Kaplan, Elizabeth Fischer, Eric Calvo and Joel Vega-Rodriguez ()
Additional contact information
Zarna Rajeshkumar Pala: National Institutes of Health
Thiago Luiz Alves e Silva: National Institutes of Health
Mahnaz Minai: National Institutes of Health
Benjamin Crews: National Institutes of Health
Eduardo Patino-Martinez: National Institutes of Health
Carmelo Carmona-Rivera: National Institutes of Health
Paola Carolina Valenzuela Leon: National Institutes of Health
Ines Martin-Martin: National Institutes of Health
Yevel Flores-Garcia: Johns Hopkins Bloomberg School of Public Health
Raul E. Cachau: National Institutes of Health
Liya Muslinkina: National Institutes of Health
Apostolos G. Gittis: National Institutes of Health
Naman Srivastava: National Institutes of Health
David N. Garboczi: National Institutes of Health
Derron A. Alves: National Institutes of Health
Mariana J. Kaplan: National Institutes of Health
Elizabeth Fischer: National Institutes of Health
Eric Calvo: National Institutes of Health
Joel Vega-Rodriguez: National Institutes of Health

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract The evolution of hematophagy involves a series of adaptations that allow blood-feeding insects to access and consume blood efficiently while managing and circumventing the host’s hemostatic and immune responses. Mosquito, and other insects, utilize salivary proteins to regulate these responses at the bite site during and after blood feeding. We investigated the function of Anopheles gambiae salivary apyrase (AgApyrase) in regulating hemostasis in the mosquito blood meal and in Plasmodium transmission. Our results demonstrate that salivary apyrase, a known inhibitor of platelet aggregation, interacts with and activates tissue plasminogen activator, facilitating the conversion of plasminogen to plasmin, a human protease that degrades fibrin and facilitates Plasmodium transmission. We show that mosquitoes ingest a substantial amount of apyrase during blood feeding, which reduces coagulation in the blood meal by enhancing fibrin degradation and inhibiting platelet aggregation. AgApyrase significantly enhanced Plasmodium infection in the mosquito midgut, whereas AgApyrase immunization inhibited Plasmodium mosquito infection and sporozoite transmission. This study highlights a pivotal role for mosquito salivary apyrase for regulation of hemostasis in the mosquito blood meal and for Plasmodium transmission to mosquitoes and to the mammalian host, underscoring the potential for strategies to prevent malaria transmission.

Date: 2024
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DOI: 10.1038/s41467-024-52502-3

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