Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection

ABSTRACT To obtain an insight into host-pathogen interactions in clostridial myonecrosis, we carried out comparative transcriptome analysis of both the bacterium and the host in a murine Clostridium perfringens infection model, which is the first time that such an investigation has been conducted. A...

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Autores principales: Lee-Yean Low, Paul F. Harrison, Jodee Gould, David R. Powell, Jocelyn M. Choo, Samuel C. Forster, Ross Chapman, Linden J. Gearing, Jackie K. Cheung, Paul Hertzog, Julian I. Rood
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:4ad7616006074ac0b0e8ec60d59ddcd52021-11-15T15:53:26ZConcurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection10.1128/mBio.00473-182150-7511https://doaj.org/article/4ad7616006074ac0b0e8ec60d59ddcd52018-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00473-18https://doaj.org/toc/2150-7511ABSTRACT To obtain an insight into host-pathogen interactions in clostridial myonecrosis, we carried out comparative transcriptome analysis of both the bacterium and the host in a murine Clostridium perfringens infection model, which is the first time that such an investigation has been conducted. Analysis of the host transcriptome from infected muscle tissues indicated that many genes were upregulated compared to the results seen with mock-infected mice. These genes were enriched for host defense pathways, including Toll-like receptor (TLR) and Nod-like receptor (NLR) signaling components. Real-time PCR confirmed that host TLR2 and NLRP3 inflammasome genes were induced in response to C. perfringens infection. Comparison of the transcriptome of C. perfringens cells from the infected tissues with that from broth cultures showed that host selective pressure induced a global change in C. perfringens gene expression. A total of 33% (923) of C. perfringens genes were differentially regulated, including 10 potential virulence genes that were upregulated relative to their expression in vitro. These genes encoded putative proteins that may be involved in the synthesis of cell wall-associated macromolecules, in adhesion to host cells, or in protection from host cationic antimicrobial peptides. This report presents the first successful expression profiling of coregulated transcriptomes of bacterial and host genes during a clostridial myonecrosis infection and provides new insights into disease pathogenesis and host-pathogen interactions. IMPORTANCE Clostridium perfringens is the causative agent of traumatic clostridial myonecrosis, or gas gangrene. In this study, we carried out transcriptional analysis of both the host and the bacterial pathogen in a mouse myonecrosis infection. The results showed that in comparison to mock-infected control tissues, muscle tissues from C. perfringens-infected mice had a significantly altered gene expression profile. In particular, the expression of many genes involved in the innate immune system was upregulated. Comparison of the expression profiles of C. perfringens cells isolated from the infected tissues with those from equivalent broth cultures identified many potential virulence genes that were significantly upregulated in vivo. These studies have provided a new understanding of the range of factors involved in host-pathogen interactions in a myonecrosis infection.Lee-Yean LowPaul F. HarrisonJodee GouldDavid R. PowellJocelyn M. ChooSamuel C. ForsterRoss ChapmanLinden J. GearingJackie K. CheungPaul HertzogJulian I. RoodAmerican Society for Microbiologyarticleclostridial myonecrosisClostridium perfringensRNA-seqgas gangrenehost-pathogen interactionsinflammasomeMicrobiologyQR1-502ENmBio, Vol 9, Iss 2 (2018)
institution DOAJ
collection DOAJ
language EN
topic clostridial myonecrosis
Clostridium perfringens
RNA-seq
gas gangrene
host-pathogen interactions
inflammasome
Microbiology
QR1-502
spellingShingle clostridial myonecrosis
Clostridium perfringens
RNA-seq
gas gangrene
host-pathogen interactions
inflammasome
Microbiology
QR1-502
Lee-Yean Low
Paul F. Harrison
Jodee Gould
David R. Powell
Jocelyn M. Choo
Samuel C. Forster
Ross Chapman
Linden J. Gearing
Jackie K. Cheung
Paul Hertzog
Julian I. Rood
Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection
description ABSTRACT To obtain an insight into host-pathogen interactions in clostridial myonecrosis, we carried out comparative transcriptome analysis of both the bacterium and the host in a murine Clostridium perfringens infection model, which is the first time that such an investigation has been conducted. Analysis of the host transcriptome from infected muscle tissues indicated that many genes were upregulated compared to the results seen with mock-infected mice. These genes were enriched for host defense pathways, including Toll-like receptor (TLR) and Nod-like receptor (NLR) signaling components. Real-time PCR confirmed that host TLR2 and NLRP3 inflammasome genes were induced in response to C. perfringens infection. Comparison of the transcriptome of C. perfringens cells from the infected tissues with that from broth cultures showed that host selective pressure induced a global change in C. perfringens gene expression. A total of 33% (923) of C. perfringens genes were differentially regulated, including 10 potential virulence genes that were upregulated relative to their expression in vitro. These genes encoded putative proteins that may be involved in the synthesis of cell wall-associated macromolecules, in adhesion to host cells, or in protection from host cationic antimicrobial peptides. This report presents the first successful expression profiling of coregulated transcriptomes of bacterial and host genes during a clostridial myonecrosis infection and provides new insights into disease pathogenesis and host-pathogen interactions. IMPORTANCE Clostridium perfringens is the causative agent of traumatic clostridial myonecrosis, or gas gangrene. In this study, we carried out transcriptional analysis of both the host and the bacterial pathogen in a mouse myonecrosis infection. The results showed that in comparison to mock-infected control tissues, muscle tissues from C. perfringens-infected mice had a significantly altered gene expression profile. In particular, the expression of many genes involved in the innate immune system was upregulated. Comparison of the expression profiles of C. perfringens cells isolated from the infected tissues with those from equivalent broth cultures identified many potential virulence genes that were significantly upregulated in vivo. These studies have provided a new understanding of the range of factors involved in host-pathogen interactions in a myonecrosis infection.
format article
author Lee-Yean Low
Paul F. Harrison
Jodee Gould
David R. Powell
Jocelyn M. Choo
Samuel C. Forster
Ross Chapman
Linden J. Gearing
Jackie K. Cheung
Paul Hertzog
Julian I. Rood
author_facet Lee-Yean Low
Paul F. Harrison
Jodee Gould
David R. Powell
Jocelyn M. Choo
Samuel C. Forster
Ross Chapman
Linden J. Gearing
Jackie K. Cheung
Paul Hertzog
Julian I. Rood
author_sort Lee-Yean Low
title Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection
title_short Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection
title_full Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection
title_fullStr Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection
title_full_unstemmed Concurrent Host-Pathogen Transcriptional Responses in a <italic toggle="yes">Clostridium perfringens</italic> Murine Myonecrosis Infection
title_sort concurrent host-pathogen transcriptional responses in a <italic toggle="yes">clostridium perfringens</italic> murine myonecrosis infection
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/4ad7616006074ac0b0e8ec60d59ddcd5
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