Self-capping of nucleoprotein filaments protects Newcastle Disease Virus genome

  1. Xiyong Song
  2. Hong Shan
  3. Yanping Zhu
  4. Shunlin Hu
  5. Ling Xue
  6. Yong Chen
  7. Wei Ding
  8. Tongxin Niu
  9. Jian Gu
  10. Songying Ouyang  Is a corresponding author
  11. Qing-Tao Shen  Is a corresponding author
  12. Zhi-Jie Liu  Is a corresponding author
  1. Kunming Medical University, China
  2. ShanghaiTech University, China
  3. Chinese Academy of Sciences, China
  4. Yangzhou University, China
  5. Fujian Normal University, China

Abstract

Non-segmented negative-strand RNA viruses, such as Measles, Ebola and Newcastle disease viruses (NDV), encapsidate viral genomic RNAs into helical nucleocapsids which serve as the template for viral replication and transcription. Here, the clam-shaped nucleocapsid structure, where the NDV viral genome is sequestered, was determined at 4.8 Å resolution by cryo-electron microscopy. The clam-shaped structure is composed of two single-turn spirals packed in a back-to-back mode, and the tightly packed structure functions as a seed for nucleocapsid to assemble from both directions and grows into double-headed filaments with two separate RNA strings inside. Disruption of this structure by mutations on its loop interface yielded a single-headed unfunctional filament.

Data availability

The cryo-EM density map has been deposited in EMDB with the accession number EMD-9793. The atom coordinates of the structure have been deposited in PDB with the PDB ID 6JC3.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Xiyong Song

    Institute of Molecular and Clinical Medicine, Kunming Medical University, Kunming, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Hong Shan

    iHuman Institute, ShanghaiTech University, Shanghai, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Yanping Zhu

    National Laboratory of Biomacromolecules, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Shunlin Hu

    College of Veterinary Medicine, Yangzhou University, Yangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ling Xue

    College of Veterinary Medicine, Yangzhou University, Yangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Yong Chen

    National Laboratory of Biomacromolecules, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Wei Ding

    Center for Biological Imaging, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  8. Tongxin Niu

    Center for Biological Imaging, Chinese Academy of Sciences, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  9. Jian Gu

    College of Veterinary Medicine, Yangzhou University, Yangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  10. Songying Ouyang

    College of Life Sciences, Fujian Normal University, Fuzhou, China
    For correspondence
    ouyangsy@fjnu.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  11. Qing-Tao Shen

    iHuman Institute, ShanghaiTech University, Shanghai, China
    For correspondence
    shenqt@shanghaitech.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  12. Zhi-Jie Liu

    Institute of Molecular and Clinical Medicine, Kunming Medical University, Kunming, China
    For correspondence
    liuzhj@shanghaiTech.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7279-2893

Funding

National Nature Science Foundation of China grant (31330019)

  • Zhi-Jie Liu

National Nature Science Foundation of China grant (31770948)

  • Songying Ouyang

National Nature Science Foundation of China grant (31570875)

  • Songying Ouyang

National Natural Science Foundation of China grant (81590761)

  • Songying Ouyang

the National Key R&D program of China (2017YFA0504800)

  • Qing-Tao Shen

Yunnan Provincial Science and Technology Department Project (2016FC007)

  • Zhi-Jie Liu

The Pujiang Talent program (17PJ1406700)

  • Qing-Tao Shen

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

Copyright

© 2019, Song 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.

Metrics

  • 2,030
    views
  • 309
    downloads
  • 22
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Xiyong Song
  2. Hong Shan
  3. Yanping Zhu
  4. Shunlin Hu
  5. Ling Xue
  6. Yong Chen
  7. Wei Ding
  8. Tongxin Niu
  9. Jian Gu
  10. Songying Ouyang
  11. Qing-Tao Shen
  12. Zhi-Jie Liu
(2019)
Self-capping of nucleoprotein filaments protects Newcastle Disease Virus genome
eLife 8:e45057.
https://doi.org/10.7554/eLife.45057

Share this article

https://doi.org/10.7554/eLife.45057

Further reading

    1. Immunology and Inflammation
    2. Microbiology and Infectious Disease
    Benita Martin-Castaño, Patricia Diez-Echave ... Julio Galvez
    Research Article

    Coronavirus disease 2019 (COVID-19) is a respiratory illness caused by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) that displays great variability in clinical phenotype. Many factors have been described to be correlated with its severity, and microbiota could play a key role in the infection, progression, and outcome of the disease. SARS-CoV-2 infection has been associated with nasopharyngeal and gut dysbiosis and higher abundance of opportunistic pathogens. To identify new prognostic markers for the disease, a multicentre prospective observational cohort study was carried out in COVID-19 patients divided into three cohorts based on symptomatology: mild (n = 24), moderate (n = 51), and severe/critical (n = 31). Faecal and nasopharyngeal samples were taken, and the microbiota was analysed. Linear discriminant analysis identified Mycoplasma salivarium, Prevotella dentalis, and Haemophilus parainfluenzae as biomarkers of severe COVID-19 in nasopharyngeal microbiota, while Prevotella bivia and Prevotella timonensis were defined in faecal microbiota. Additionally, a connection between faecal and nasopharyngeal microbiota was identified, with a significant ratio between P. timonensis (faeces) and P. dentalis and M. salivarium (nasopharyngeal) abundances found in critically ill patients. This ratio could serve as a novel prognostic tool for identifying severe COVID-19 cases.

    1. Epidemiology and Global Health
    2. Microbiology and Infectious Disease
    Bo Zheng, Bronner P Gonçalves ... Caoyi Xue
    Research Article

    Background:

    In many settings, a large fraction of the population has both been vaccinated against and infected by severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Hence, quantifying the protection provided by post-infection vaccination has become critical for policy. We aimed to estimate the protective effect against SARS-CoV-2 reinfection of an additional vaccine dose after an initial Omicron variant infection.

    Methods:

    We report a retrospective, population-based cohort study performed in Shanghai, China, using electronic databases with information on SARS-CoV-2 infections and vaccination history. We compared reinfection incidence by post-infection vaccination status in individuals initially infected during the April–May 2022 Omicron variant surge in Shanghai and who had been vaccinated before that period. Cox models were fit to estimate adjusted hazard ratios (aHRs).

    Results:

    275,896 individuals were diagnosed with real-time polymerase chain reaction-confirmed SARS-CoV-2 infection in April–May 2022; 199,312/275,896 were included in analyses on the effect of a post-infection vaccine dose. Post-infection vaccination provided protection against reinfection (aHR 0.82; 95% confidence interval 0.79–0.85). For patients who had received one, two, or three vaccine doses before their first infection, hazard ratios for the post-infection vaccination effect were 0.84 (0.76–0.93), 0.87 (0.83–0.90), and 0.96 (0.74–1.23), respectively. Post-infection vaccination within 30 and 90 days before the second Omicron wave provided different degrees of protection (in aHR): 0.51 (0.44–0.58) and 0.67 (0.61–0.74), respectively. Moreover, for all vaccine types, but to different extents, a post-infection dose given to individuals who were fully vaccinated before first infection was protective.

    Conclusions:

    In previously vaccinated and infected individuals, an additional vaccine dose provided protection against Omicron variant reinfection. These observations will inform future policy decisions on COVID-19 vaccination in China and other countries.

    Funding:

    This study was funded the Key Discipline Program of Pudong New Area Health System (PWZxk2022-25), the Development and Application of Intelligent Epidemic Surveillance and AI Analysis System (21002411400), the Shanghai Public Health System Construction (GWVI-11.2-XD08), the Shanghai Health Commission Key Disciplines (GWVI-11.1-02), the Shanghai Health Commission Clinical Research Program (20214Y0020), the Shanghai Natural Science Foundation (22ZR1414600), and the Shanghai Young Health Talents Program (2022YQ076).