Role of cytoneme structures and extracellular vesicles in Trichomonas vaginalis parasite: parasite communication

  1. Nehuén Salas
  2. Manuela Blasco Pedreros
  3. Tuanne dos Santos Melo
  4. Vanina G Maguire
  5. Jihui Sha
  6. James A Wohlschlegel
  7. Antonio Pereira-Neves
  8. Natalia de Miguel  Is a corresponding author
  1. Instituto Tecnológico de Chascomús, Argentina
  2. Instituto Aggeu Magalhães, Brazil
  3. Estación Experimental Agropecuaria, Argentina
  4. University of California, Los Angeles, United States

Abstract

Trichomonas vaginalis, the etiologic agent of the most common non-viral sexually transmitted infection worldwide, colonizes the human urogenital tract where it remains extracellular and adheres to epithelial cells. With an estimated annual prevalence of 276 million new cases, mixed infections with different parasite strains are expected. Although it is considered as obvious that parasites interact with their host to enhance their own survival and transmission, evidence of mixed infections call into question the extent to which unicellular parasites communicate with each other. Here, we demonstrated that different T. vaginalis strains can communicate through the formation of cytoneme-like membranous cell connections. We showed that T. vaginalis adherent strains form abundant membrane protrusions and cytonemes formation of an adherent parasite strain (CDC1132) is affected in the presence of a different strain (G3 or B7RC2). Using cell culture inserts assays, we demonstrated that the effect in cytoneme formation is contact-independent and that extracellular vesicles (EVs) are responsible, at least in part, of the communication among strains. We found that EVs isolated from G3, B7RC2, and CDC1132 strains contain a highly distinct repertoire of proteins, some of them involved in signaling and communication, among other functions. Finally, we showed that parasite adherence to host cells is affected by this communication between strains as binding of adherent T. vaginalis CDC1132 strain to prostate cells is significantly higher in the presence of G3 or B7RC2 strains. Demonstrating that interaction of isolates with distinct phenotypic characteristics may have significant clinical repercussions, we also observed that a poorly adherent parasite strain (G3) adheres more strongly to prostate cells in the presence of an adherent strain. The study of signaling, sensing, and cell communication in parasitic organisms will surely enhance our understanding of the basic biological characteristics of parasites, which may have important consequences in pathogenesis.

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Article and author information

Author details

  1. Nehuén Salas

    Laboratorio de Parásitos Anaerobios, Instituto Tecnológico de Chascomús, Buenos Aires, Argentina
    Competing interests
    No competing interests declared.
  2. Manuela Blasco Pedreros

    Laboratorio de Parásitos Anaerobios, Instituto Tecnológico de Chascomús, Buenos Aires, Argentina
    Competing interests
    No competing interests declared.
  3. Tuanne dos Santos Melo

    Departamento de Microbiologia, Instituto Aggeu Magalhães, Recife, Brazil
    Competing interests
    No competing interests declared.
  4. Vanina G Maguire

    Área de mejoramiento genético vegetal, Estación Experimental Agropecuaria, Cordoba, Argentina
    Competing interests
    No competing interests declared.
  5. Jihui Sha

    Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  6. James A Wohlschlegel

    Department of Biological Chemistry, University of California, Los Angeles, Los Angeles, United States
    Competing interests
    No competing interests declared.
  7. Antonio Pereira-Neves

    Departamento de Microbiologia, Instituto Aggeu Magalhães, Recife, Brazil
    Competing interests
    No competing interests declared.
  8. Natalia de Miguel

    Laboratorio de Parásitos Anaerobios, Instituto Tecnológico de Chascomús, Buenos Aires, Argentina
    For correspondence
    ndemiguel@intech.gov.ar
    Competing interests
    Natalia de Miguel, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3864-0703

Funding

Fondo para la Investigación Científica y Tecnológica (PICT-2019-01671)

  • Natalia de Miguel

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Marcio L Rodrigues, Instituto Carlos Chagas - Fiocruz PR, Brazil

Version history

  1. Received: January 10, 2023
  2. Preprint posted: January 19, 2023 (view preprint)
  3. Accepted: May 1, 2023
  4. Accepted Manuscript published: May 2, 2023 (version 1)
  5. Version of Record published: June 15, 2023 (version 2)

Copyright

© 2023, Salas 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. Nehuén Salas
  2. Manuela Blasco Pedreros
  3. Tuanne dos Santos Melo
  4. Vanina G Maguire
  5. Jihui Sha
  6. James A Wohlschlegel
  7. Antonio Pereira-Neves
  8. Natalia de Miguel
(2023)
Role of cytoneme structures and extracellular vesicles in Trichomonas vaginalis parasite: parasite communication
eLife 12:e86067.
https://doi.org/10.7554/eLife.86067

Share this article

https://doi.org/10.7554/eLife.86067

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