Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype

Abstract Background Mastitis is an economically important disease of dairy cows with Staphylococcus aureus a major cause worldwide. Challenge of Holstein-Friesian cows demonstrated that S. aureus strain MOK124, which belongs to Clonal Complex (CC)151, caused clinical mastitis, while strain MOK023, b...

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Autores principales:	Dagmara A. Niedziela, Paul Cormican, Gilles Foucras, Finola C. Leonard, Orla M. Keane
Formato:	article
Lenguaje:	EN
Publicado:	BMC 2021
Materias:	Mastitis Transcriptomics Staphylococcus aureus Bovine immune response RNA sequencing Host-pathogen interaction Biotechnology TP248.13-248.65 Genetics QH426-470
Acceso en línea:	https://doaj.org/article/f85878dc818e4bd491d6656e62eba73b
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spelling	oai:doaj.org-article:f85878dc818e4bd491d6656e62eba73b2021-11-08T10:57:34ZBovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype10.1186/s12864-021-08135-71471-2164https://doaj.org/article/f85878dc818e4bd491d6656e62eba73b2021-11-01T00:00:00Zhttps://doi.org/10.1186/s12864-021-08135-7https://doaj.org/toc/1471-2164Abstract Background Mastitis is an economically important disease of dairy cows with Staphylococcus aureus a major cause worldwide. Challenge of Holstein-Friesian cows demonstrated that S. aureus strain MOK124, which belongs to Clonal Complex (CC)151, caused clinical mastitis, while strain MOK023, belonging to CC97, caused mild or subclinical mastitis. The aim of this study was to elucidate the molecular mechanisms of the host immune response utilising a transcriptomic approach. Milk somatic cells were collected from cows infected with either S. aureus MOK023 or MOK124 at 0, 24, 48, 72 and 168 h post-infection (hpi) and analysed for differentially expressed (DE) genes in response to each strain. Results In response to MOK023, 1278, 2278, 1986 and 1750 DE genes were found at 24, 48, 72 and 168 hpi, respectively, while 2293, 1979, 1428 and 1544 DE genes were found in response to MOK124 at those time points. Genes involved in milk production (CSN1, CSN10, CSN1S2, CSN2, a-LACTA and PRLR) were downregulated in response to both strains, with a more pronounced decrease in the MOK124 group. Immune response pathways such as NF-κB and TNF signalling were overrepresented in response to both strains at 24 hpi. These immune pathways continued to be overrepresented in the MOK023 group at 48 and 72 hpi, while the Hippo signalling, extracellular matrix interaction (ECM) and tight junction pathways were overrepresented in the MOK124 group between 48 and 168 hpi. Cellular composition analysis demonstrated that a neutrophil response was predominant in response to MOK124, while M1 macrophages were the main milk cell type post-infection in the MOK023 group. Conclusions A switch from immune response pathways to pathways involved in maintaining the integrity of the epithelial cell layer was observed in the MOK124 group from 48 hpi, which coincided with the occurrence of clinical signs in the infected animals. The higher proportion of M1 macrophages in the MOK023 group and lack of substantial neutrophil recruitment in response to MOK023 may indicate immune evasion by this strain. The results of this study highlight that the somatic cell transcriptomic response to S. aureus is dependent on the genotype of the infecting strain.Dagmara A. NiedzielaPaul CormicanGilles FoucrasFinola C. LeonardOrla M. KeaneBMCarticleMastitisTranscriptomicsStaphylococcus aureusBovine immune responseRNA sequencingHost-pathogen interactionBiotechnologyTP248.13-248.65GeneticsQH426-470ENBMC Genomics, Vol 22, Iss 1, Pp 1-20 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Mastitis Transcriptomics Staphylococcus aureus Bovine immune response RNA sequencing Host-pathogen interaction Biotechnology TP248.13-248.65 Genetics QH426-470
spellingShingle	Mastitis Transcriptomics Staphylococcus aureus Bovine immune response RNA sequencing Host-pathogen interaction Biotechnology TP248.13-248.65 Genetics QH426-470 Dagmara A. Niedziela Paul Cormican Gilles Foucras Finola C. Leonard Orla M. Keane Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype
description	Abstract Background Mastitis is an economically important disease of dairy cows with Staphylococcus aureus a major cause worldwide. Challenge of Holstein-Friesian cows demonstrated that S. aureus strain MOK124, which belongs to Clonal Complex (CC)151, caused clinical mastitis, while strain MOK023, belonging to CC97, caused mild or subclinical mastitis. The aim of this study was to elucidate the molecular mechanisms of the host immune response utilising a transcriptomic approach. Milk somatic cells were collected from cows infected with either S. aureus MOK023 or MOK124 at 0, 24, 48, 72 and 168 h post-infection (hpi) and analysed for differentially expressed (DE) genes in response to each strain. Results In response to MOK023, 1278, 2278, 1986 and 1750 DE genes were found at 24, 48, 72 and 168 hpi, respectively, while 2293, 1979, 1428 and 1544 DE genes were found in response to MOK124 at those time points. Genes involved in milk production (CSN1, CSN10, CSN1S2, CSN2, a-LACTA and PRLR) were downregulated in response to both strains, with a more pronounced decrease in the MOK124 group. Immune response pathways such as NF-κB and TNF signalling were overrepresented in response to both strains at 24 hpi. These immune pathways continued to be overrepresented in the MOK023 group at 48 and 72 hpi, while the Hippo signalling, extracellular matrix interaction (ECM) and tight junction pathways were overrepresented in the MOK124 group between 48 and 168 hpi. Cellular composition analysis demonstrated that a neutrophil response was predominant in response to MOK124, while M1 macrophages were the main milk cell type post-infection in the MOK023 group. Conclusions A switch from immune response pathways to pathways involved in maintaining the integrity of the epithelial cell layer was observed in the MOK124 group from 48 hpi, which coincided with the occurrence of clinical signs in the infected animals. The higher proportion of M1 macrophages in the MOK023 group and lack of substantial neutrophil recruitment in response to MOK023 may indicate immune evasion by this strain. The results of this study highlight that the somatic cell transcriptomic response to S. aureus is dependent on the genotype of the infecting strain.
format	article
author	Dagmara A. Niedziela Paul Cormican Gilles Foucras Finola C. Leonard Orla M. Keane
author_facet	Dagmara A. Niedziela Paul Cormican Gilles Foucras Finola C. Leonard Orla M. Keane
author_sort	Dagmara A. Niedziela
title	Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype
title_short	Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype
title_full	Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype
title_fullStr	Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype
title_full_unstemmed	Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype
title_sort	bovine milk somatic cell transcriptomic response to staphylococcus aureus is dependent on strain genotype
publisher	BMC
publishDate	2021
url	https://doaj.org/article/f85878dc818e4bd491d6656e62eba73b
work_keys_str_mv	AT dagmaraaniedziela bovinemilksomaticcelltranscriptomicresponsetostaphylococcusaureusisdependentonstraingenotype AT paulcormican bovinemilksomaticcelltranscriptomicresponsetostaphylococcusaureusisdependentonstraingenotype AT gillesfoucras bovinemilksomaticcelltranscriptomicresponsetostaphylococcusaureusisdependentonstraingenotype AT finolacleonard bovinemilksomaticcelltranscriptomicresponsetostaphylococcusaureusisdependentonstraingenotype AT orlamkeane bovinemilksomaticcelltranscriptomicresponsetostaphylococcusaureusisdependentonstraingenotype
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Bovine milk somatic cell transcriptomic response to Staphylococcus aureus is dependent on strain genotype

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