The role of bacterial size, shape and surface in macrophage engulfment of uropathogenic E. coli cells.

Peterson, E; Söderström, B; Prins, N; Le, GHB; Hartley-Tassell, LE; Evenhuis, C; Grønnemose, RB; Andersen, TE; Møller-Jensen, J; Iosifidis, G; Duggin, IG; Saunders, B; Harry, EJ; Bottomley, AL

The role of bacterial size, shape and surface in macrophage engulfment of uropathogenic E. coli cells.

Peterson, E Söderström, B Prins, N Le, GHB Hartley-Tassell, LE Evenhuis, C Grønnemose, RB Andersen, TE Møller-Jensen, J Iosifidis, G Duggin, IG Saunders, B

Harry, EJ Bottomley, AL

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Publisher:: PUBLIC LIBRARY SCIENCE
Publication Type:: Journal Article
Citation:: PLoS Pathog, 2024, 20, (9), pp. e1012458
Issue Date:: 2024-09

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Field	Value	Language
dc.contributor.author	Peterson, E
dc.contributor.author	Söderström, B
dc.contributor.author	Prins, N
dc.contributor.author	Le, GHB
dc.contributor.author	Hartley-Tassell, LE
dc.contributor.author	Evenhuis, C
dc.contributor.author	Grønnemose, RB
dc.contributor.author	Andersen, TE
dc.contributor.author	Møller-Jensen, J
dc.contributor.author	Iosifidis, G
dc.contributor.author	Duggin, IG
dc.contributor.author	Saunders, B https://orcid.org/0000-0003-0540-4445
dc.contributor.author	Harry, EJ
dc.contributor.author	Bottomley, AL
dc.contributor.editor	Mulvey, MA
dc.date.accessioned	2024-12-02T00:51:13Z
dc.date.available	2024-07-26
dc.date.available	2024-12-02T00:51:13Z
dc.date.issued	2024-09
dc.identifier.citation	PLoS Pathog, 2024, 20, (9), pp. e1012458
dc.identifier.issn	1553-7366
dc.identifier.issn	1553-7374
dc.identifier.uri	http://hdl.handle.net/10453/182177
dc.description.abstract	Uropathogenic Escherichia coli (UPEC) can undergo extensive filamentation in the host during acute urinary tract infections (UTIs). It has been hypothesised that this morphological plasticity allows bacteria to avoid host immune responses such as macrophage engulfment. However, it is still unclear what properties of filaments are important in macrophage-bacteria interactions. The aim of this work was to investigate the contribution of bacterial biophysical parameters, such as cell size and shape, and physiological parameters, such as cell surface and the environment, to macrophage engulfment efficiency. Viable, reversible filaments of known lengths and volumes were produced in the UPEC strain UTI89 using a variety of methods, including exposure to cell-wall targeting antibiotics, genetic manipulation and isolation from an in vitro human bladder cell model. Quantification of the engulfment ability of macrophages using gentamicin-protection assays and fluorescence microscopy demonstrated that the ability of filaments to avoid macrophage engulfment is dependent on a combination of size (length and volume), shape, cell surface and external environmental factors. UTI89 filamentation and macrophage engulfment efficiency were also found to occur independently of the SOS-inducible filamentation genes, sulA and ymfM in both in vivo and in vitro models of infection. Compared to filaments formed via antibiotic inhibition of division, the infection-derived filaments were preferentially targeted by macrophages. With several strains of UPEC now resistant to current antibiotics, our work identifies the importance of bacterial physiological and morphological states during infection.
dc.format	Electronic-eCollection
dc.language	eng
dc.publisher	PUBLIC LIBRARY SCIENCE
dc.relation	http://purl.org/au-research/grants/arc/DP220101143
dc.relation.ispartof	PLoS Pathog
dc.relation.isbasedon	10.1371/journal.ppat.1012458
dc.rights	info:eu-repo/semantics/openAccess
dc.subject	0605 Microbiology, 1107 Immunology, 1108 Medical Microbiology
dc.subject.classification	Virology
dc.subject.classification	3107 Microbiology
dc.subject.classification	3204 Immunology
dc.subject.classification	3207 Medical microbiology
dc.subject.mesh	Uropathogenic Escherichia coli
dc.subject.mesh	Macrophages
dc.subject.mesh	Humans
dc.subject.mesh	Urinary Tract Infections
dc.subject.mesh	Escherichia coli Infections
dc.subject.mesh	Phagocytosis
dc.subject.mesh	Mice
dc.subject.mesh	Animals
dc.subject.mesh	Macrophages
dc.subject.mesh	Animals
dc.subject.mesh	Humans
dc.subject.mesh	Mice
dc.subject.mesh	Escherichia coli Infections
dc.subject.mesh	Urinary Tract Infections
dc.subject.mesh	Phagocytosis
dc.subject.mesh	Uropathogenic Escherichia coli
dc.title	The role of bacterial size, shape and surface in macrophage engulfment of uropathogenic E. coli cells.
dc.type	Journal Article
utslib.citation.volume	20
utslib.location.activity	United States
utslib.for	0605 Microbiology
utslib.for	1107 Immunology
utslib.for	1108 Medical Microbiology
pubs.organisational-group	University of Technology Sydney
pubs.organisational-group	University of Technology Sydney/Faculty of Science
pubs.organisational-group	University of Technology Sydney/Faculty of Science/School of Life Sciences
pubs.organisational-group	University of Technology Sydney/UTS Groups
pubs.organisational-group	University of Technology Sydney/UTS Groups/Australian Institute for Microbiology & Infection (AIMI)
pubs.organisational-group	University of Technology Sydney/UTS Groups/Centre for Inflammation (CFI)
pubs.organisational-group	University of Technology Sydney/UTS Groups/Australian Institute for Microbiology & Infection (AIMI)/Australian Institute for Microbiology & Infection (AIMI) Associate Members
utslib.copyright.status	open_access	*
dc.rights.license	This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0). To view a copy of this license, visit https://creativecommons.org/licenses/by/4.0/
dc.date.updated	2024-12-02T00:51:06Z
pubs.issue	9
pubs.publication-status	Published online
pubs.volume	20
utslib.citation.issue	9

Abstract:

Uropathogenic Escherichia coli (UPEC) can undergo extensive filamentation in the host during acute urinary tract infections (UTIs). It has been hypothesised that this morphological plasticity allows bacteria to avoid host immune responses such as macrophage engulfment. However, it is still unclear what properties of filaments are important in macrophage-bacteria interactions. The aim of this work was to investigate the contribution of bacterial biophysical parameters, such as cell size and shape, and physiological parameters, such as cell surface and the environment, to macrophage engulfment efficiency. Viable, reversible filaments of known lengths and volumes were produced in the UPEC strain UTI89 using a variety of methods, including exposure to cell-wall targeting antibiotics, genetic manipulation and isolation from an in vitro human bladder cell model. Quantification of the engulfment ability of macrophages using gentamicin-protection assays and fluorescence microscopy demonstrated that the ability of filaments to avoid macrophage engulfment is dependent on a combination of size (length and volume), shape, cell surface and external environmental factors. UTI89 filamentation and macrophage engulfment efficiency were also found to occur independently of the SOS-inducible filamentation genes, sulA and ymfM in both in vivo and in vitro models of infection. Compared to filaments formed via antibiotic inhibition of division, the infection-derived filaments were preferentially targeted by macrophages. With several strains of UPEC now resistant to current antibiotics, our work identifies the importance of bacterial physiological and morphological states during infection.

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http://hdl.handle.net/10453/182177