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 and Joel Vega-Rodriguez ()
Additional contact information
Thiago Luiz Alves e Silva: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Sachi Kanatani: Johns Hopkins University, The W. Harry Feinstone Department of Molecular Microbiology and Immunology and Johns Hopkins Malaria Research Institute, Bloomberg School of Public Health
Ana Beatriz Barletta Ferreira: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Cindi L. Schwartz: National Institutes of Health, Microscopy Unit, Research Technologies Branch, Rocky Mountain Laboratories, National Institute of Allergy and Infectious Diseases
Benjamin Liffner: Indiana University School of Medicine, Department of Pharmacology & Toxicology
Octavio A. C. Talyuli: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Janet Olivas: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Bianca M. Nagata: National Institutes of Health, Infectious Disease Pathogenesis Section, National Institute of Allergy and Infectious Diseases
Zarna Rajeshkumar Pala: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Tales Pascini: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Derron A. Alves: National Institutes of Health, Infectious Disease Pathogenesis Section, National Institute of Allergy and Infectious Diseases
Ming Zhao: National Institutes of Health, Research Technologies Branch, National Institute of Allergy and Infectious Diseases
Motoshi Suzuki: National Institutes of Health, Research Technologies Branch, National Institute of Allergy and Infectious Diseases
Lilian P. Dorner: University of Heidelberg Medical School, Integrative Parasitology, Center for Infectious Diseases
Friedrich Frischknecht: University of Heidelberg Medical School, Integrative Parasitology, Center for Infectious Diseases
Isabelle Coppens: Johns Hopkins University, The W. Harry Feinstone Department of Molecular Microbiology and Immunology and Johns Hopkins Malaria Research Institute, Bloomberg School of Public Health
Carolina Barillas-Mury: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Sabrina Absalon: Indiana University School of Medicine, Department of Pharmacology & Toxicology
Jose M. C. Ribeiro: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases
Photini Sinnis: Johns Hopkins University, The W. Harry Feinstone Department of Molecular Microbiology and Immunology and Johns Hopkins Malaria Research Institute, Bloomberg School of Public Health
Joel Vega-Rodriguez: National Institutes of Health, Laboratory of Malaria and Vector Research, National Institute of Allergy and Infectious Diseases

Nature Communications, 2025, vol. 16, issue 1, 1-20

Abstract: Abstract 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.

Date: 2025
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DOI: 10.1038/s41467-025-64837-6

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