<p><i>Plasmodium</i> sporozoites, the infective stage of malaria, must invade the mosquito salivary glands (SGs) before being transmitted to a vertebrate host. However, the physiological and biochemical effects of this invasion remain largely unexplored. We examined the impact of <i>Plasmodium</i> infection on <i>Anopheles gambiae</i> salivary glands using high-resolution proteomics, gene expression, and morphological analysis. The data reveal differential expression of various proteins, including the enrichment of hemolymph-derived humoral proteins in infected salivary glands. These proteins diffuse into the SGs due to structural damage caused by the sporozoites during invasion, while saliva proteins diffuse out into the circulation. Moreover, proteomic analysis of saliva from <i>P. berghei</i>– or <i>P. falciparum</i>–infected mosquitoes revealed changes in composition, with a pronounced reduction of immune proteins relative to uninfected mosquitoes. This reduction is likely due to the association of these proteins with the surface of sporozoites and/or changes in the saliva’s physical properties within the invaded salivary secretory cavities. The saliva protein profiles from mosquitoes infected with both <i>Plasmodium</i> species are remarkably similar, suggesting a conserved interaction between sporozoites and salivary glands. Our results provide a foundation for understanding the molecular interactions between <i>Plasmodium</i> sporozoites and mosquito salivary glands.</p>

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High-resolution proteomics unveils salivary gland disruption and saliva-hemolymph protein exchange in Plasmodium-infected mosquitoes

  • Thiago Luiz Alves e Silva,
  • Sachi Kanatani,
  • Ana Beatriz Barletta Ferreira,
  • Cindi L. Schwartz,
  • Benjamin Liffner,
  • Octavio A. C. Talyuli,
  • Janet Olivas,
  • Bianca M. Nagata,
  • Zarna Rajeshkumar Pala,
  • Tales Pascini,
  • Derron A. Alves,
  • Ming Zhao,
  • Motoshi Suzuki,
  • Lilian P. Dorner,
  • Friedrich Frischknecht,
  • Isabelle Coppens,
  • Carolina Barillas-Mury,
  • Sabrina Absalon,
  • Jose M. C. Ribeiro,
  • Photini Sinnis,
  • Joel Vega-Rodriguez

摘要

Plasmodium sporozoites, the infective stage of malaria, must invade the mosquito salivary glands (SGs) before being transmitted to a vertebrate host. However, the physiological and biochemical effects of this invasion remain largely unexplored. We examined the impact of Plasmodium infection on Anopheles gambiae salivary glands using high-resolution proteomics, gene expression, and morphological analysis. The data reveal differential expression of various proteins, including the enrichment of hemolymph-derived humoral proteins in infected salivary glands. These proteins diffuse into the SGs due to structural damage caused by the sporozoites during invasion, while saliva proteins diffuse out into the circulation. Moreover, proteomic analysis of saliva from P. berghei– or P. falciparum–infected mosquitoes revealed changes in composition, with a pronounced reduction of immune proteins relative to uninfected mosquitoes. This reduction is likely due to the association of these proteins with the surface of sporozoites and/or changes in the saliva’s physical properties within the invaded salivary secretory cavities. The saliva protein profiles from mosquitoes infected with both Plasmodium species are remarkably similar, suggesting a conserved interaction between sporozoites and salivary glands. Our results provide a foundation for understanding the molecular interactions between Plasmodium sporozoites and mosquito salivary glands.