Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq

Johne’s disease, caused by infection with Mycobacterium avium subsp. paratuberculosis, (MAP), is a chronic intestinal disease of ruminants with serious economic consequences for cattle production in the United States and elsewhere. During infection, MAP bacilli are phagocytosed and subvert host macr...

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Main Authors: Maura E Casey, Kieran G. Meade, Nicolas C Nalpas, Maria eTaraktsoglou, John A Browne, Kate E Killick, Stephen David Edward Park, Eamonn eGormley, Karsten eHokamp, David A Magee, David E Machugh
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-02-01
Series:Frontiers in Immunology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fimmu.2015.00023/full
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author Maura E Casey
Maura E Casey
Kieran G. Meade
Nicolas C Nalpas
Maria eTaraktsoglou
John A Browne
Kate E Killick
Kate E Killick
Stephen David Edward Park
Stephen David Edward Park
Eamonn eGormley
Karsten eHokamp
David A Magee
David A Magee
David E Machugh
David E Machugh
author_facet Maura E Casey
Maura E Casey
Kieran G. Meade
Nicolas C Nalpas
Maria eTaraktsoglou
John A Browne
Kate E Killick
Kate E Killick
Stephen David Edward Park
Stephen David Edward Park
Eamonn eGormley
Karsten eHokamp
David A Magee
David A Magee
David E Machugh
David E Machugh
author_sort Maura E Casey
collection DOAJ
description Johne’s disease, caused by infection with Mycobacterium avium subsp. paratuberculosis, (MAP), is a chronic intestinal disease of ruminants with serious economic consequences for cattle production in the United States and elsewhere. During infection, MAP bacilli are phagocytosed and subvert host macrophage processes, resulting in subclinical infections that can lead to immunopathology and dissemination of disease. Analysis of the host macrophage transcriptome during infection can therefore shed light on the molecular mechanisms and host-pathogen interplay associated with Johne’s disease. Here we describe results of an in vitro study of the bovine monocyte-derived macrophage (MDM) transcriptome response during MAP infection using RNA-seq. MDM were obtained from seven age- and sex-matched Holstein-Friesian cattle and were infected with MAP across a six-hour infection time course with non-infected controls. We observed 245 and 574 differentially expressed genes in MAP-infected versus non-infected control samples (adjusted P value ≤ 0.05) at 2 and 6 hours post-infection, respectively. Functional analyses of these differentially expressed genes, including biological pathway enrichment, highlighted potential functional roles for genes that have not been previously described in the host response to infection with MAP bacilli. In addition, differential expression of pro- and anti-inflammatory cytokine genes, such as those associated with the IL-10 signaling pathway, and other immune-related genes that encode proteins involved in the bovine macrophage response to MAP infection emphasize the balance between protective host immunity and bacilli survival and proliferation. Systematic comparisons of RNA-seq gene expression results with Affymetrix® microarray data generated from the same experimental samples also demonstrated that RNA-seq represents a superior technology for studying host transcriptional responses to intracellular infection.
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spelling doaj.art-62c531bc224b41648374f052273879552022-12-21T19:15:12ZengFrontiers Media S.A.Frontiers in Immunology1664-32242015-02-01610.3389/fimmu.2015.00023118960Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seqMaura E Casey0Maura E Casey1Kieran G. Meade2Nicolas C Nalpas3Maria eTaraktsoglou4John A Browne5Kate E Killick6Kate E Killick7Stephen David Edward Park8Stephen David Edward Park9Eamonn eGormley10Karsten eHokamp11David A Magee12David A Magee13David E Machugh14David E Machugh15University College DublinTeagascTeagascUniversity College DublinHealth and Safety ExecutiveUniversity College DublinUniversity College DublinUniversity College DublinUniversity College DublinIdentiGEN Ltd.University College DublinTrinity College DublinUniversity College DublinUniversity of ConnecticutUniversity College DublinUniversity College DublinJohne’s disease, caused by infection with Mycobacterium avium subsp. paratuberculosis, (MAP), is a chronic intestinal disease of ruminants with serious economic consequences for cattle production in the United States and elsewhere. During infection, MAP bacilli are phagocytosed and subvert host macrophage processes, resulting in subclinical infections that can lead to immunopathology and dissemination of disease. Analysis of the host macrophage transcriptome during infection can therefore shed light on the molecular mechanisms and host-pathogen interplay associated with Johne’s disease. Here we describe results of an in vitro study of the bovine monocyte-derived macrophage (MDM) transcriptome response during MAP infection using RNA-seq. MDM were obtained from seven age- and sex-matched Holstein-Friesian cattle and were infected with MAP across a six-hour infection time course with non-infected controls. We observed 245 and 574 differentially expressed genes in MAP-infected versus non-infected control samples (adjusted P value ≤ 0.05) at 2 and 6 hours post-infection, respectively. Functional analyses of these differentially expressed genes, including biological pathway enrichment, highlighted potential functional roles for genes that have not been previously described in the host response to infection with MAP bacilli. In addition, differential expression of pro- and anti-inflammatory cytokine genes, such as those associated with the IL-10 signaling pathway, and other immune-related genes that encode proteins involved in the bovine macrophage response to MAP infection emphasize the balance between protective host immunity and bacilli survival and proliferation. Systematic comparisons of RNA-seq gene expression results with Affymetrix® microarray data generated from the same experimental samples also demonstrated that RNA-seq represents a superior technology for studying host transcriptional responses to intracellular infection.http://journal.frontiersin.org/Journal/10.3389/fimmu.2015.00023/fullCattleTranscriptomeMicroarrayimmune responsemacrophageJohne’s disease
spellingShingle Maura E Casey
Maura E Casey
Kieran G. Meade
Nicolas C Nalpas
Maria eTaraktsoglou
John A Browne
Kate E Killick
Kate E Killick
Stephen David Edward Park
Stephen David Edward Park
Eamonn eGormley
Karsten eHokamp
David A Magee
David A Magee
David E Machugh
David E Machugh
Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq
Frontiers in Immunology
Cattle
Transcriptome
Microarray
immune response
macrophage
Johne’s disease
title Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq
title_full Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq
title_fullStr Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq
title_full_unstemmed Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq
title_short Analysis of the bovine monocyte-derived macrophage response to Mycobacterium avium subspecies paratuberculosis infection using RNA-seq
title_sort analysis of the bovine monocyte derived macrophage response to mycobacterium avium subspecies paratuberculosis infection using rna seq
topic Cattle
Transcriptome
Microarray
immune response
macrophage
Johne’s disease
url http://journal.frontiersin.org/Journal/10.3389/fimmu.2015.00023/full
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