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Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum

The recent emergence of the poultry bacterial pathogen Mycoplasma gallisepticum (MG) in free-living house finches (Haemorhous mexicanus), which causes mycoplasmal conjunctivitis in this passerine bird species, resulted in a rapid coevolutionary arms-race between MG and its novel avian host. Despite...

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Autores principales: Vinkler, Michal, Leon, Ariel E., Kirkpatrick, Laila, Dalloul, Rami A., Hawley, Dana M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5786573/
https://www.ncbi.nlm.nih.gov/pubmed/29403495
http://dx.doi.org/10.3389/fimmu.2018.00013
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author Vinkler, Michal
Leon, Ariel E.
Kirkpatrick, Laila
Dalloul, Rami A.
Hawley, Dana M.
author_facet Vinkler, Michal
Leon, Ariel E.
Kirkpatrick, Laila
Dalloul, Rami A.
Hawley, Dana M.
author_sort Vinkler, Michal
collection PubMed
description The recent emergence of the poultry bacterial pathogen Mycoplasma gallisepticum (MG) in free-living house finches (Haemorhous mexicanus), which causes mycoplasmal conjunctivitis in this passerine bird species, resulted in a rapid coevolutionary arms-race between MG and its novel avian host. Despite extensive research on the ecological and evolutionary dynamics of this host–pathogen system over the past two decades, the immunological responses of house finches to MG infection remain poorly understood. We developed seven new probe-based one-step quantitative reverse transcription polymerase chain reaction assays to investigate mRNA expression of house finch cytokine genes (IL1B, IL6, IL10, IL18, TGFB2, TNFSF15, and CXCLi2, syn. IL8L). These assays were then used to describe cytokine transcription profiles in a panel of 15 house finch tissues collected at three distinct time points during MG infection. Based on initial screening that indicated strong pro-inflammatory cytokine expression during MG infection at the periorbital sites in particular, we selected two key house finch tissues for further characterization: the nictitating membrane, i.e., the internal eyelid in direct contact with MG, and the Harderian gland, the secondary lymphoid tissue responsible for regulation of periorbital immunity. We characterized cytokine responses in these two tissues for 60 house finches experimentally inoculated either with media alone (sham) or one of two MG isolates: the earliest known pathogen isolate from house finches (VA1994) or an evolutionarily more derived isolate collected in 2006 (NC2006), which is known to be more virulent. We show that the more derived and virulent isolate NC2006, relative to VA1994, triggers stronger local inflammatory cytokine signaling, with peak cytokine expression generally occurring 3–6 days following MG inoculation. We also found that the extent of pro-inflammatory interleukin 1 beta signaling was correlated with conjunctival MG loads and the extent of clinical signs of conjunctivitis, the main pathological effect of MG in house finches. These results suggest that the pathogenicity caused by MG infection in house finches is largely mediated by host pro-inflammatory immune responses, with important implications for the dynamics of host–pathogen coevolution.
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spelling pubmed-57865732018-02-05 Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum Vinkler, Michal Leon, Ariel E. Kirkpatrick, Laila Dalloul, Rami A. Hawley, Dana M. Front Immunol Immunology The recent emergence of the poultry bacterial pathogen Mycoplasma gallisepticum (MG) in free-living house finches (Haemorhous mexicanus), which causes mycoplasmal conjunctivitis in this passerine bird species, resulted in a rapid coevolutionary arms-race between MG and its novel avian host. Despite extensive research on the ecological and evolutionary dynamics of this host–pathogen system over the past two decades, the immunological responses of house finches to MG infection remain poorly understood. We developed seven new probe-based one-step quantitative reverse transcription polymerase chain reaction assays to investigate mRNA expression of house finch cytokine genes (IL1B, IL6, IL10, IL18, TGFB2, TNFSF15, and CXCLi2, syn. IL8L). These assays were then used to describe cytokine transcription profiles in a panel of 15 house finch tissues collected at three distinct time points during MG infection. Based on initial screening that indicated strong pro-inflammatory cytokine expression during MG infection at the periorbital sites in particular, we selected two key house finch tissues for further characterization: the nictitating membrane, i.e., the internal eyelid in direct contact with MG, and the Harderian gland, the secondary lymphoid tissue responsible for regulation of periorbital immunity. We characterized cytokine responses in these two tissues for 60 house finches experimentally inoculated either with media alone (sham) or one of two MG isolates: the earliest known pathogen isolate from house finches (VA1994) or an evolutionarily more derived isolate collected in 2006 (NC2006), which is known to be more virulent. We show that the more derived and virulent isolate NC2006, relative to VA1994, triggers stronger local inflammatory cytokine signaling, with peak cytokine expression generally occurring 3–6 days following MG inoculation. We also found that the extent of pro-inflammatory interleukin 1 beta signaling was correlated with conjunctival MG loads and the extent of clinical signs of conjunctivitis, the main pathological effect of MG in house finches. These results suggest that the pathogenicity caused by MG infection in house finches is largely mediated by host pro-inflammatory immune responses, with important implications for the dynamics of host–pathogen coevolution. Frontiers Media S.A. 2018-01-22 /pmc/articles/PMC5786573/ /pubmed/29403495 http://dx.doi.org/10.3389/fimmu.2018.00013 Text en Copyright © 2018 Vinkler, Leon, Kirkpatrick, Dalloul and Hawley. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Vinkler, Michal
Leon, Ariel E.
Kirkpatrick, Laila
Dalloul, Rami A.
Hawley, Dana M.
Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum
title Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum
title_full Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum
title_fullStr Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum
title_full_unstemmed Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum
title_short Differing House Finch Cytokine Expression Responses to Original and Evolved Isolates of Mycoplasma gallisepticum
title_sort differing house finch cytokine expression responses to original and evolved isolates of mycoplasma gallisepticum
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5786573/
https://www.ncbi.nlm.nih.gov/pubmed/29403495
http://dx.doi.org/10.3389/fimmu.2018.00013
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