Longitudinal analysis of Plasmodium sporozoite motility in the dermis reveals component of blood vessel recognition

  1. Christine S Hopp
  2. Kevin Chiou
  3. Daniel RT Ragheb
  4. Ahmed Salman
  5. Shahid M Khan
  6. Andrea J Liu
  7. Photini Sinnis  Is a corresponding author
  1. Johns Hopkins Bloomberg School of Public Health, United States
  2. University of Pennsylvania, United States
  3. Leiden University Medical Center, Netherlands

Abstract

Malaria infection starts with injection of Plasmodium sporozoites by an Anopheles mosquito into the skin of the mammalian host. How sporozoites locate and enter a blood vessel is a critical, but poorly understood process. Here, we examine sporozoite motility and their interaction with dermal blood vessels, using intravital microscopy in mice. Our data suggest that sporozoites exhibit two types of motility: In regions far from blood vessels, they exhibit ′avascular motility′, defined by high speed and less confinement, while in the vicinity of blood vessels their motility is more constrained. We find that curvature of sporozoite tracks engaging with vasculature optimizes contact with dermal capillaries. Imaging of sporozoites with mutations in key adhesive proteins highlight the importance of the sporozoite's gliding speed and its ability to modulate adhesive properties for successful exit from the inoculation site.

Article and author information

Author details

  1. Christine S Hopp

    Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Kevin Chiou

    Department of Physics and Astronomy, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Daniel RT Ragheb

    Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ahmed Salman

    Department of Parasitology, Leiden Malaria Research Group, Leiden University Medical Center, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  5. Shahid M Khan

    Department of Parasitology, Leiden Malaria Research Group, Leiden University Medical Center, Leiden, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  6. Andrea J Liu

    Department of Physics and Astronomy, University of Pennsylvania, Philadelphia, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Photini Sinnis

    Department of Molecular Microbiology & Immunology, Johns Hopkins Bloomberg School of Public Health, Baltimore, United States
    For correspondence
    psinnis@jhsph.edu
    Competing interests
    The authors declare that no competing interests exist.

Ethics

Animal experimentation: All animal work was conducted in accordance with the recommendations by the Johns Hopkins University Animal Care and Use Committee (IACUC), under the IACUC-approved protocol #M011H467.

Reviewing Editor

  1. Urszula Krzych, Walter Reed Army Institute of Research, United States

Publication history

  1. Received: March 29, 2015
  2. Accepted: August 12, 2015
  3. Accepted Manuscript published: August 13, 2015 (version 1)
  4. Version of Record published: October 6, 2015 (version 2)

Copyright

© 2015, Hopp et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Christine S Hopp
  2. Kevin Chiou
  3. Daniel RT Ragheb
  4. Ahmed Salman
  5. Shahid M Khan
  6. Andrea J Liu
  7. Photini Sinnis
(2015)
Longitudinal analysis of Plasmodium sporozoite motility in the dermis reveals component of blood vessel recognition
eLife 4:e07789.
https://doi.org/10.7554/eLife.07789
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