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Transcriptomics and proteomics reveal two waves of translational repression during the maturation of malaria parasite sporozoites

Author

Listed:
  • Scott E. Lindner

    (Pennsylvania State University)

  • Kristian E. Swearingen

    (Institute for Systems Biology)

  • Melanie J. Shears

    (Johns Hopkins Bloomberg School of Public Health
    University of Washington)

  • Michael P. Walker

    (Pennsylvania State University)

  • Erin N. Vrana

    (Pennsylvania State University)

  • Kevin J. Hart

    (Pennsylvania State University)

  • Allen M. Minns

    (Pennsylvania State University)

  • Photini Sinnis

    (Johns Hopkins Bloomberg School of Public Health)

  • Robert L. Moritz

    (Institute for Systems Biology)

  • Stefan H. I. Kappe

    (Center for Global Infectious Disease Research, Seattle Children’s Research Institute
    University of Washington)

Abstract

Plasmodium sporozoites are transmitted from infected mosquitoes to mammals, and must navigate the host skin and vasculature to infect the liver. This journey requires distinct proteomes. Here, we report the dynamic transcriptomes and proteomes of both oocyst sporozoites and salivary gland sporozoites in both rodent-infectious Plasmodium yoelii parasites and human-infectious Plasmodium falciparum parasites. The data robustly define mRNAs and proteins that are upregulated in oocyst sporozoites (UOS) or upregulated in infectious sporozoites (UIS) within the salivary glands, including many that are essential for sporozoite functions in the vector and host. Moreover, we find that malaria parasites use two overlapping, extensive, and independent programs of translational repression across sporozoite maturation to temporally regulate protein expression. Together with gene-specific validation experiments, these data indicate that two waves of translational repression are implemented and relieved at different times during sporozoite maturation, migration and infection, thus promoting their successful development and vector-to-host transition.

Suggested Citation

  • Scott E. Lindner & Kristian E. Swearingen & Melanie J. Shears & Michael P. Walker & Erin N. Vrana & Kevin J. Hart & Allen M. Minns & Photini Sinnis & Robert L. Moritz & Stefan H. I. Kappe, 2019. "Transcriptomics and proteomics reveal two waves of translational repression during the maturation of malaria parasite sporozoites," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-12936-6
    DOI: 10.1038/s41467-019-12936-6
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    Cited by:

    1. Madeline G. Dans & Coralie Boulet & Gabrielle M. Watson & William Nguyen & Jerzy M. Dziekan & Cindy Evelyn & Kitsanapong Reaksudsan & Somya Mehra & Zahra Razook & Niall D. Geoghegan & Michael J. Mlodz, 2024. "Aryl amino acetamides prevent Plasmodium falciparum ring development via targeting the lipid-transfer protein PfSTART1," Nature Communications, Nature, vol. 15(1), pages 1-19, December.

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