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Plasmodium sporozoite search strategy to locate hotspots of blood vessel invasion

Author

Listed:
  • Pauline Formaglio

    (Université Paris Cité, Malaria Infection and Immunity Unit)

  • Marina E. Wosniack

    (Max Planck Institute for Brain Research)

  • Raphael M. Tromer

    (Universidade Federal do Rio Grande do Norte)

  • Jaderson G. Polli

    (Universidade Federal do Paraná)

  • Yuri B. Matos

    (Universidade Federal do Paraná)

  • Hang Zhong

    (Université Paris Cité, Malaria Infection and Immunity Unit)

  • Ernesto P. Raposo

    (Universidade Federal de Pernambuco)

  • Marcos G. E. Luz

    (Universidade Federal do Paraná)

  • Rogerio Amino

    (Université Paris Cité, Malaria Infection and Immunity Unit)

Abstract

Plasmodium sporozoites actively migrate in the dermis and enter blood vessels to infect the liver. Despite their importance for malaria infection, little is known about these cutaneous processes. We combine intravital imaging in a rodent malaria model and statistical methods to unveil the parasite strategy to reach the bloodstream. We determine that sporozoites display a high-motility mode with a superdiffusive Lévy-like pattern known to optimize the location of scarce targets. When encountering blood vessels, sporozoites frequently switch to a subdiffusive low-motility behavior associated with probing for intravasation hotspots, marked by the presence of pericytes. Hence, sporozoites present anomalous diffusive motility, alternating between superdiffusive tissue exploration and subdiffusive local vessel exploitation, thus optimizing the sequential tasks of seeking blood vessels and pericyte-associated sites of privileged intravasation.

Suggested Citation

  • Pauline Formaglio & Marina E. Wosniack & Raphael M. Tromer & Jaderson G. Polli & Yuri B. Matos & Hang Zhong & Ernesto P. Raposo & Marcos G. E. Luz & Rogerio Amino, 2023. "Plasmodium sporozoite search strategy to locate hotspots of blood vessel invasion," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38706-z
    DOI: 10.1038/s41467-023-38706-z
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    References listed on IDEAS

    as
    1. Marina E Wosniack & Marcos C Santos & Ernesto P Raposo & Gandhi M Viswanathan & Marcos G E da Luz, 2017. "The evolutionary origins of Lévy walk foraging," PLOS Computational Biology, Public Library of Science, vol. 13(10), pages 1-31, October.
    2. G. M. Viswanathan & Sergey V. Buldyrev & Shlomo Havlin & M. G. E. da Luz & E. P. Raposo & H. Eugene Stanley, 1999. "Optimizing the success of random searches," Nature, Nature, vol. 401(6756), pages 911-914, October.
    3. David W. Sims & Emily J. Southall & Nicolas E. Humphries & Graeme C. Hays & Corey J. A. Bradshaw & Jonathan W. Pitchford & Alex James & Mohammed Z. Ahmed & Andrew S. Brierley & Mark A. Hindell & David, 2008. "Scaling laws of marine predator search behaviour," Nature, Nature, vol. 451(7182), pages 1098-1102, February.
    4. Gillespie, Colin S., 2015. "Fitting Heavy Tailed Distributions: The poweRlaw Package," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 64(i02).
    5. Minho S. Song & Hyungseok C. Moon & Jae-Hyung Jeon & Hye Yoon Park, 2018. "Neuronal messenger ribonucleoprotein transport follows an aging Lévy walk," Nature Communications, Nature, vol. 9(1), pages 1-8, December.
    6. Henrik Seckler & Ralf Metzler, 2022. "Bayesian deep learning for error estimation in the analysis of anomalous diffusion," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
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