Literature DB >> 31916938

Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori.

Jennifer A Taylor1,2, Benjamin P Bratton3,4, Sophie R Sichel2,5, Kris M Blair2,6, Holly M Jacobs2,6, Kristen E DeMeester7, Erkin Kuru8, Joe Gray9, Jacob Biboy10, Michael S VanNieuwenhze11, Waldemar Vollmer10, Catherine L Grimes7,12, Joshua W Shaevitz3,13, Nina R Salama1,2,5,6.   

Abstract

Helical cell shape is necessary for efficient stomach colonization by Helicobacter pylori, but the molecular mechanisms for generating helical shape remain unclear. The helical centerline pitch and radius of wild-type H. pylori cells dictate surface curvatures of considerably higher positive and negative Gaussian curvatures than those present in straight- or curved-rod H. pylori. Quantitative 3D microscopy analysis of short pulses with either N-acetylmuramic acid or D-alanine metabolic probes showed that cell wall growth is enhanced at both sidewall curvature extremes. Immunofluorescence revealed MreB is most abundant at negative Gaussian curvature, while the bactofilin CcmA is most abundant at positive Gaussian curvature. Strains expressing CcmA variants with altered polymerization properties lose helical shape and associated positive Gaussian curvatures. We thus propose a model where CcmA and MreB promote PG synthesis at positive and negative Gaussian curvatures, respectively, and that this patterning is one mechanism necessary for maintaining helical shape.
© 2020, Taylor et al.

Entities:  

Keywords:  Helicobacter pylori; MreB; bactofilin; cell shape; infectious disease; microbiology; peptidoglycan

Mesh:

Substances:

Year:  2020        PMID: 31916938      PMCID: PMC7012605          DOI: 10.7554/eLife.52482

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.140


  53 in total

1.  Peptidoglycan crosslinking relaxation promotes Helicobacter pylori's helical shape and stomach colonization.

Authors:  Laura K Sycuro; Zachary Pincus; Kimberley D Gutierrez; Jacob Biboy; Chelsea A Stern; Waldemar Vollmer; Nina R Salama
Journal:  Cell       Date:  2010-05-28       Impact factor: 41.582

2.  A Periplasmic Polymer Curves Vibrio cholerae and Promotes Pathogenesis.

Authors:  Thomas M Bartlett; Benjamin P Bratton; Amit Duvshani; Amanda Miguel; Ying Sheng; Nicholas R Martin; Jeffrey P Nguyen; Alexandre Persat; Samantha M Desmarais; Michael S VanNieuwenhze; Kerwyn Casey Huang; Jun Zhu; Joshua W Shaevitz; Zemer Gitai
Journal:  Cell       Date:  2017-01-12       Impact factor: 41.582

3.  Cag3 is a novel essential component of the Helicobacter pylori Cag type IV secretion system outer membrane subcomplex.

Authors:  Delia M Pinto-Santini; Nina R Salama
Journal:  J Bacteriol       Date:  2009-10-02       Impact factor: 3.490

4.  The morphological transition of Helicobacter pylori cells from spiral to coccoid is preceded by a substantial modification of the cell wall.

Authors:  K Costa; G Bacher; G Allmaier; M G Dominguez-Bello; L Engstrand; P Falk; M A de Pedro; F García-del Portillo
Journal:  J Bacteriol       Date:  1999-06       Impact factor: 3.490

5.  Effects of S-(3,4-dichlorobenzyl) isothiourea on different cellular events in the cyanobacterium Anabaena sp. strain PCC 7120.

Authors:  Xuan Wu; Noritaka Iwai; Wen-Li Chen
Journal:  Res Microbiol       Date:  2011-02-12       Impact factor: 3.992

6.  comH, a novel gene essential for natural transformation of Helicobacter pylori.

Authors:  L C Smeets; J J Bijlsma; S Y Boomkens; C M Vandenbroucke-Grauls; J G Kusters
Journal:  J Bacteriol       Date:  2000-07       Impact factor: 3.490

7.  Helicobacter pylori strains vary cell shape and flagellum number to maintain robust motility in viscous environments.

Authors:  Laura E Martínez; Joseph M Hardcastle; Jeffrey Wang; Zachary Pincus; Jennifer Tsang; Timothy R Hoover; Rama Bansil; Nina R Salama
Journal:  Mol Microbiol       Date:  2015-10-14       Impact factor: 3.501

8.  Multiple peptidoglycan modification networks modulate Helicobacter pylori's cell shape, motility, and colonization potential.

Authors:  Laura K Sycuro; Timna J Wyckoff; Jacob Biboy; Petra Born; Zachary Pincus; Waldemar Vollmer; Nina R Salama
Journal:  PLoS Pathog       Date:  2012-03-22       Impact factor: 6.823

9.  Flow cytometry-based enrichment for cell shape mutants identifies multiple genes that influence Helicobacter pylori morphology.

Authors:  Laura K Sycuro; Chelsea S Rule; Timothy W Petersen; Timna J Wyckoff; Tate Sessler; Dilip B Nagarkar; Fakhra Khalid; Zachary Pincus; Jacoby Biboy; Waldemar Vollmer; Nina R Salama
Journal:  Mol Microbiol       Date:  2013-10-16       Impact factor: 3.501

10.  The Helicobacter pylori HpyAXII restriction-modification system limits exogenous DNA uptake by targeting GTAC sites but shows asymmetric conservation of the DNA methyltransferase and restriction endonuclease components.

Authors:  Olivier Humbert; Nina R Salama
Journal:  Nucleic Acids Res       Date:  2008-10-31       Impact factor: 16.971

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  17 in total

1.  A bacterial cytolinker couples positioning of magnetic organelles to cell shape control.

Authors:  Daniel Pfeiffer; Mauricio Toro-Nahuelpan; Ram Prasad Awal; Frank-Dietrich Müller; Marc Bramkamp; Jürgen M Plitzko; Dirk Schüler
Journal:  Proc Natl Acad Sci U S A       Date:  2020-11-30       Impact factor: 11.205

Review 2.  Cell morphology as a virulence determinant: lessons from Helicobacter pylori.

Authors:  Nina R Salama
Journal:  Curr Opin Microbiol       Date:  2020-01-31       Impact factor: 7.934

3.  A Division of Labor in the Recruitment and Topological Organization of a Bacterial Morphogenic Complex.

Authors:  Paul D Caccamo; Maxime Jacq; Michael S VanNieuwenhze; Yves V Brun
Journal:  Curr Biol       Date:  2020-08-13       Impact factor: 10.834

Review 4.  Regulation of peptidoglycan synthesis and remodelling.

Authors:  Alexander J F Egan; Jeff Errington; Waldemar Vollmer
Journal:  Nat Rev Microbiol       Date:  2020-05-18       Impact factor: 60.633

5.  Distinct cytoskeletal proteins define zones of enhanced cell wall synthesis in Helicobacter pylori.

Authors:  Jennifer A Taylor; Benjamin P Bratton; Sophie R Sichel; Kris M Blair; Holly M Jacobs; Kristen E DeMeester; Erkin Kuru; Joe Gray; Jacob Biboy; Michael S VanNieuwenhze; Waldemar Vollmer; Catherine L Grimes; Joshua W Shaevitz; Nina R Salama
Journal:  Elife       Date:  2020-01-09       Impact factor: 8.140

Review 6.  Chemical Reporters for Bacterial Glycans: Development and Applications.

Authors:  Nicholas Banahene; Herbert W Kavunja; Benjamin M Swarts
Journal:  Chem Rev       Date:  2021-12-14       Impact factor: 60.622

7.  Investigating Peptidoglycan Recycling Pathways in Tannerella forsythia with N-Acetylmuramic Acid Bioorthogonal Probes.

Authors:  Kimberly A Wodzanowski; Stephen N Hyland; Sreedevi Chinthamani; Liam-Michael D Sandles; Kiyonobu Honma; Ashu Sharma; Catherine L Grimes
Journal:  ACS Infect Dis       Date:  2022-08-04       Impact factor: 5.578

8.  Localizing Peptidoglycan Synthesis in Helicobacter pylori using Clickable Metabolic Probes.

Authors:  Jennifer A Taylor; Cintia C Santiago; Joe Gray; Kimberly A Wodzanowski; Kristen E DeMeester; Jacob Biboy; Waldemar Vollmer; Catherine L Grimes; Nina R Salama
Journal:  Curr Protoc       Date:  2021-04

9.  A Dynamic, Ring-Forming Bactofilin Critical for Maintaining Cell Size in the Obligate Intracellular Bacterium Chlamydia trachomatis.

Authors:  Mary R Brockett; Junghoon Lee; John V Cox; George W Liechti; Scot P Ouellette
Journal:  Infect Immun       Date:  2021-07-15       Impact factor: 3.441

10.  Protected N-Acetyl Muramic Acid Probes Improve Bacterial Peptidoglycan Incorporation via Metabolic Labeling.

Authors:  Ashley R Brown; Kimberly A Wodzanowski; Cintia C Santiago; Stephen N Hyland; Julianna L Follmar; PapaNii Asare-Okai; Catherine Leimkuhler Grimes
Journal:  ACS Chem Biol       Date:  2021-09-10       Impact factor: 4.634

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