1. Cell Biology
  2. Structural Biology and Molecular Biophysics
Download icon

Lateral interactions between protofilaments of the bacterial tubulin homolog FtsZ are essential for cell division

  1. Fenghui Guan
  2. Jiayu Yu
  3. Jie Yu
  4. Yang Liu
  5. Ying Li
  6. Xin-Hua Feng
  7. Kerwyn Casey Huang
  8. Zengyi Chang  Is a corresponding author
  9. Sheng Ye  Is a corresponding author
  1. Zhejiang University, China
  2. Peking University, China
  3. Stanford University, United States
Research Article
  • Cited 18
  • Views 2,563
  • Annotations
Cite this article as: eLife 2018;7:e35578 doi: 10.7554/eLife.35578

Abstract

The prokaryotic tubulin homolog FtsZ polymerizes into protofilaments, which further assemble into higher-order structures at future division sites to form the Z-ring, a dynamic structure essential for bacterial cell division. The precise nature of interactions between FtsZ protofilaments that organize the Z-ring and their physiological significance remain enigmatic. In this study, we solved two crystallographic structures of a pair of FtsZ protofilaments,and demonstrated that they assemble in an antiparallel manner through the formation of two different inter-protofilament lateral interfaces. Our in vivo photocrosslinking studies confirmed that such lateral interactions occur in living cells, and disruption of the lateral interactions rendered cells unable to divide. The inherently weak lateral interactions enable FtsZ protofilaments to self-organize into a dynamic Z-ring. These results have fundamental implications for our understanding of bacterial cell division and for developing antibiotics that target this key process.

Data availability

Diffraction data have been deposited in PDB under the accession code 5ZUE

The following data sets were generated

Article and author information

Author details

  1. Fenghui Guan

    Life Sciences Institute, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Jiayu Yu

    School of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Jie Yu

    Life Sciences Institute, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Yang Liu

    School of Life Sciences, Peking University, Beijing, China
    Competing interests
    The authors declare that no competing interests exist.
  5. Ying Li

    Life Sciences Institute, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  6. Xin-Hua Feng

    Life Sciences Institute, Zhejiang University, Hangzhou, China
    Competing interests
    The authors declare that no competing interests exist.
  7. Kerwyn Casey Huang

    Department of Bioengineering, Stanford University, Stanford, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. Zengyi Chang

    School of Life Sciences, Peking University, Beijing, China
    For correspondence
    changzy@pku.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
  9. Sheng Ye

    Life Sciences Institute, Zhejiang University, Hangzhou, China
    For correspondence
    sye@zju.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9300-6257

Funding

Ministry of Science and Technology of the People's Republic of China (2016YFA0500404)

  • Sheng Ye

Ministry of Science and Technology of the People's Republic of China (2014CB910300)

  • Sheng Ye

Ministry of Science and Technology of the People's Republic of China (2012CB917300)

  • Zengyi Chang

National Natural Science Foundation of China (31525001)

  • Sheng Ye

National Natural Science Foundation of China (31430019)

  • Sheng Ye

National Natural Science Foundation of China (31670775)

  • Zengyi Chang

National Natural Science Foundation of China (31470766)

  • Zengyi Chang

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

Reviewing Editor

  1. Edward H Egelman, University of Virginia, United States

Publication history

  1. Received: January 31, 2018
  2. Accepted: June 10, 2018
  3. Accepted Manuscript published: June 11, 2018 (version 1)
  4. Version of Record published: July 17, 2018 (version 2)

Copyright

© 2018, Guan 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

  • 2,563
    Page views
  • 498
    Downloads
  • 18
    Citations

Article citation count generated by polling the highest count across the following sources: Crossref, Scopus, PubMed Central.

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)

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

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

Further reading

    1. Cell Biology
    2. Developmental Biology
    Sun-Hee Hwang et al.
    Research Article

    The role of compartmentalized signaling in primary cilia during tissue morphogenesis is not well understood. The cilia-localized G-protein-coupled receptor—Gpr161 represses hedgehog pathway via cAMP signaling. We engineered a knock-in at Gpr161 locus in mice to generate a variant (Gpr161mut1), which was ciliary localization defective but cAMP signaling competent. Tissue phenotypes from hedgehog signaling depend on downstream bifunctional Gli transcriptional factors functioning as activators/repressors. Compared to knockout (ko), Gpr161mut1/ko had delayed embryonic lethality, moderately increased hedgehog targets and partially down-regulated Gli3-repressor. Unlike ko, the Gpr161mut1/ko neural tube did not show Gli2-activator-dependent expansion of ventral-most progenitors. Instead, the intermediate neural tube showed progenitor expansion that depends on loss of Gli3-repressor. Increased extraciliary receptor (Gpr161mut1/mut1) prevented ventralization. Morphogenesis in limb buds and midface requires Gli-repressor; these tissues in Gpr161mut1/mut1 manifested hedgehog hyperactivation phenotypes—polydactyly and midfacial widening. Thus, ciliary and extraciliary Gpr161 pools likely establish tissue-specific Gli-repressor thresholds in determining morpho-phenotypic outcomes.

    1. Cell Biology
    2. Developmental Biology
    Evelien Eenjes et al.
    Research Article Updated

    SOX2 expression levels are crucial for the balance between maintenance and differentiation of airway progenitor cells during development and regeneration. Here, we describe patterning of the mouse proximal airway epithelium by SOX21, which coincides with high levels of SOX2 during development. Airway progenitor cells in this SOX2+/SOX21+ zone show differentiation to basal cells, specifying cells for the extrapulmonary airways. Loss of SOX21 showed an increased differentiation of SOX2+ progenitor cells to basal and ciliated cells during mouse lung development. We propose a mechanism where SOX21 inhibits differentiation of airway progenitors by antagonizing SOX2-induced expression of specific genes involved in airway differentiation. Additionally, in the adult tracheal epithelium, SOX21 inhibits basal to ciliated cell differentiation. This suppressing function of SOX21 on differentiation contrasts SOX2, which mainly drives differentiation of epithelial cells during development and regeneration after injury. Furthermore, using human fetal lung organoids and adult bronchial epithelial cells, we show that SOX2+/SOX21+ regionalization is conserved. Lastly, we show that the interplay between SOX2 and SOX21 is context and concentration dependent leading to regulation of differentiation of the airway epithelium.