Abstract

Rotavirus genome replication and assembly take place in cytoplasmic electron dense inclusions termed viroplasms (VPs). Previous conventional optical microscopy studies observing the intracellular distribution of rotavirus proteins and their organization in VPs have lacked molecular-scale spatial resolution, due to inherent spatial resolution constraints. In this work we employed super-resolution microscopy to reveal the nanometric-scale organization of VPs formed during rotavirus infection, and quantitatively describes the structural organization of seven viral proteins within and around the VPs. The observed viral components are spatially organized as 5 concentric layers, in which NSP5 localizes at the center of the VPs, surrounded by a layer of NSP2 and NSP4 proteins, followed by an intermediate zone comprised of the VP1, VP2, VP6. In the outermost zone, we observed a ring of VP4 and finally a layer of VP7. These findings show that rotavirus VPs are highly organized organelles.

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All data generated or analysed during this study are included in the manuscript and supporting files.

Article and author information

Author details

  1. Yasel Garcés Suárez

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  2. Jose L Martínez

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  3. David Torres Hernández

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  4. Haydee Olinca Hernández

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  5. Arianna Pérez-Delgado

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  6. Mayra Méndez

    Centro de Investigación en Ciencias, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  7. Christopher D Wood

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  8. Juan Manuel Rendon-Mancha

    Centro de Investigación en Ciencias, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9629-7050
  9. Daniela Silva-Ayala

    Center for Virology and Vaccine Research, Harvard Medical School, Boston, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Susana López

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  11. Adán Guerrero

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    For correspondence
    adanog@ibt.unam.mx
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4389-5516
  12. Carlos F Arias

    Departamento de Genética del Desarrollo y Fisiología Molecular, Universidad Nacional Autónoma de México, Cuernavaca, Mexico
    For correspondence
    arias@ibt.unam.mx
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-3130-4501

Funding

DGAPA-PAPIIT-UNAM (IG200317)

  • Susana López
  • Carlos F Arias

DGAPA-PAPIIT-UNAM (IA202417)

  • Adán Guerrero

DGTIC-UNAM (SC15-1-IR-89)

  • Adán Guerrero

Conacyt-Mexico (252213)

  • Adán Guerrero

DGAPA-PAPIIT-UNAM (IN202312)

  • Haydee Olinca Hernández

DGTIC-UNAM (SC16-1-IR-102)

  • Adán Guerrero

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

Reviewing Editor

  1. Arup K Chakraborty, Massachusetts Institute of Technology, United States

Version history

  1. Received: October 17, 2018
  2. Accepted: July 22, 2019
  3. Accepted Manuscript published: July 25, 2019 (version 1)
  4. Version of Record published: August 13, 2019 (version 2)
  5. Version of Record updated: August 22, 2019 (version 3)
  6. Version of Record updated: September 17, 2019 (version 4)

Copyright

© 2019, Garcés Suárez 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. Yasel Garcés Suárez
  2. Jose L Martínez
  3. David Torres Hernández
  4. Haydee Olinca Hernández
  5. Arianna Pérez-Delgado
  6. Mayra Méndez
  7. Christopher D Wood
  8. Juan Manuel Rendon-Mancha
  9. Daniela Silva-Ayala
  10. Susana López
  11. Adán Guerrero
  12. Carlos F Arias
(2019)
Nanoscale organization of rotavirus replication machineries
eLife 8:e42906.
https://doi.org/10.7554/eLife.42906

Share this article

https://doi.org/10.7554/eLife.42906

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