Candidalysin Drives Epithelial Signaling, Neutrophil Recruitment, and Immunopathology at the Vaginal Mucosa

Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen , is a disease of immunocompetent and otherwise healthy women. Despite its prevalence, the fungal factors responsible for initiating symptomatic infection remain poorly understood. One of the hallmar...

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Vydané v:Infection and immunity Ročník 86; číslo 2
Hlavní autori: Richardson, Jonathan P, Willems, Hubertine M E, Moyes, David L, Shoaie, Saeed, Barker, Katherine S, Tan, Shir Lynn, Palmer, Glen E, Hube, Bernhard, Naglik, Julian R, Peters, Brian M
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States 01.02.2018
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Abstract Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen , is a disease of immunocompetent and otherwise healthy women. Despite its prevalence, the fungal factors responsible for initiating symptomatic infection remain poorly understood. One of the hallmarks of vaginal candidiasis is the robust recruitment of neutrophils to the site of infection, which seemingly do not clear the fungus, but rather exacerbate disease symptomatology. Candidalysin, a newly discovered peptide toxin secreted by hyphae during invasion, drives epithelial damage, immune activation, and phagocyte attraction. Therefore, we hypothesized that Candidalysin is crucial for vulvovaginal candidiasis immunopathology. Anti- immune responses are anatomical-site specific, as effective gastrointestinal, oral, and vaginal immunities are uniquely compartmentalized. Thus, we aimed to identify the immunopathologic role of Candidalysin and downstream signaling events at the vaginal mucosa. Microarray analysis of -infected human vaginal epithelium revealed signaling pathways involved in epithelial damage responses, barrier repair, and leukocyte activation. Moreover, treatment of A431 vaginal epithelial cells with Candidalysin induced dose-dependent proinflammatory cytokine responses (including interleukin 1α [IL-1α], IL-1β, and IL-8), damage, and activation of c-Fos and mitogen-activated protein kinase (MAPK) signaling, consistent with fungal challenge. Mice intravaginally challenged with strains deficient in Candidalysin exhibited no differences in colonization compared to isogenic controls. However, significant decreases in neutrophil recruitment, damage, and proinflammatory cytokine expression were observed with these strains. Our findings demonstrate that Candidalysin is a key hypha-associated virulence determinant responsible for the immunopathogenesis of vaginitis.
AbstractList Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen Candida albicans, is a disease of immunocompetent and otherwise healthy women. Despite its prevalence, the fungal factors responsible for initiating symptomatic infection remain poorly understood. One of the hallmarks of vaginal candidiasis is the robust recruitment of neutrophils to the site of infection, which seemingly do not clear the fungus, but rather exacerbate disease symptomatology. Candidalysin, a newly discovered peptide toxin secreted by C. albicans hyphae during invasion, drives epithelial damage, immune activation, and phagocyte attraction. Therefore, we hypothesized that Candidalysin is crucial for vulvovaginal candidiasis immunopathology. Anti-Candida immune responses are anatomical-site specific, as effective gastrointestinal, oral, and vaginal immunities are uniquely compartmentalized. Thus, we aimed to identify the immunopathologic role of Candidalysin and downstream signaling events at the vaginal mucosa. Microarray analysis of C. albicans-infected human vaginal epithelium in vitro revealed signaling pathways involved in epithelial damage responses, barrier repair, and leukocyte activation. Moreover, treatment of A431 vaginal epithelial cells with Candidalysin induced dose-dependent proinflammatory cytokine responses (including interleukin 1α [IL-1α], IL-1β, and IL-8), damage, and activation of c-Fos and mitogen-activated protein kinase (MAPK) signaling, consistent with fungal challenge. Mice intravaginally challenged with C. albicans strains deficient in Candidalysin exhibited no differences in colonization compared to isogenic controls. However, significant decreases in neutrophil recruitment, damage, and proinflammatory cytokine expression were observed with these strains. Our findings demonstrate that Candidalysin is a key hypha-associated virulence determinant responsible for the immunopathogenesis of C. albicans vaginitis.Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen Candida albicans, is a disease of immunocompetent and otherwise healthy women. Despite its prevalence, the fungal factors responsible for initiating symptomatic infection remain poorly understood. One of the hallmarks of vaginal candidiasis is the robust recruitment of neutrophils to the site of infection, which seemingly do not clear the fungus, but rather exacerbate disease symptomatology. Candidalysin, a newly discovered peptide toxin secreted by C. albicans hyphae during invasion, drives epithelial damage, immune activation, and phagocyte attraction. Therefore, we hypothesized that Candidalysin is crucial for vulvovaginal candidiasis immunopathology. Anti-Candida immune responses are anatomical-site specific, as effective gastrointestinal, oral, and vaginal immunities are uniquely compartmentalized. Thus, we aimed to identify the immunopathologic role of Candidalysin and downstream signaling events at the vaginal mucosa. Microarray analysis of C. albicans-infected human vaginal epithelium in vitro revealed signaling pathways involved in epithelial damage responses, barrier repair, and leukocyte activation. Moreover, treatment of A431 vaginal epithelial cells with Candidalysin induced dose-dependent proinflammatory cytokine responses (including interleukin 1α [IL-1α], IL-1β, and IL-8), damage, and activation of c-Fos and mitogen-activated protein kinase (MAPK) signaling, consistent with fungal challenge. Mice intravaginally challenged with C. albicans strains deficient in Candidalysin exhibited no differences in colonization compared to isogenic controls. However, significant decreases in neutrophil recruitment, damage, and proinflammatory cytokine expression were observed with these strains. Our findings demonstrate that Candidalysin is a key hypha-associated virulence determinant responsible for the immunopathogenesis of C. albicans vaginitis.
Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen , is a disease of immunocompetent and otherwise healthy women. Despite its prevalence, the fungal factors responsible for initiating symptomatic infection remain poorly understood. One of the hallmarks of vaginal candidiasis is the robust recruitment of neutrophils to the site of infection, which seemingly do not clear the fungus, but rather exacerbate disease symptomatology. Candidalysin, a newly discovered peptide toxin secreted by hyphae during invasion, drives epithelial damage, immune activation, and phagocyte attraction. Therefore, we hypothesized that Candidalysin is crucial for vulvovaginal candidiasis immunopathology. Anti- immune responses are anatomical-site specific, as effective gastrointestinal, oral, and vaginal immunities are uniquely compartmentalized. Thus, we aimed to identify the immunopathologic role of Candidalysin and downstream signaling events at the vaginal mucosa. Microarray analysis of -infected human vaginal epithelium revealed signaling pathways involved in epithelial damage responses, barrier repair, and leukocyte activation. Moreover, treatment of A431 vaginal epithelial cells with Candidalysin induced dose-dependent proinflammatory cytokine responses (including interleukin 1α [IL-1α], IL-1β, and IL-8), damage, and activation of c-Fos and mitogen-activated protein kinase (MAPK) signaling, consistent with fungal challenge. Mice intravaginally challenged with strains deficient in Candidalysin exhibited no differences in colonization compared to isogenic controls. However, significant decreases in neutrophil recruitment, damage, and proinflammatory cytokine expression were observed with these strains. Our findings demonstrate that Candidalysin is a key hypha-associated virulence determinant responsible for the immunopathogenesis of vaginitis.
Author Willems, Hubertine M E
Richardson, Jonathan P
Peters, Brian M
Shoaie, Saeed
Palmer, Glen E
Hube, Bernhard
Barker, Katherine S
Moyes, David L
Naglik, Julian R
Tan, Shir Lynn
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  givenname: Jonathan P
  surname: Richardson
  fullname: Richardson, Jonathan P
  organization: King's College London, Division of Mucosal and Salivary Biology, London, United Kingdom
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  givenname: Hubertine M E
  surname: Willems
  fullname: Willems, Hubertine M E
  organization: University of Tennessee Health Science Center, Department of Clinical Pharmacy, Memphis, Tennessee, USA
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  givenname: David L
  surname: Moyes
  fullname: Moyes, David L
  organization: King's College London, Centre for Host-Microbiome Interactions, London, United Kingdom
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  givenname: Saeed
  surname: Shoaie
  fullname: Shoaie, Saeed
  organization: King's College London, Centre for Host-Microbiome Interactions, London, United Kingdom
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  givenname: Katherine S
  surname: Barker
  fullname: Barker, Katherine S
  organization: University of Tennessee Health Science Center, Department of Clinical Pharmacy, Memphis, Tennessee, USA
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  givenname: Shir Lynn
  surname: Tan
  fullname: Tan, Shir Lynn
  organization: King's College London, Division of Mucosal and Salivary Biology, London, United Kingdom
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  givenname: Glen E
  surname: Palmer
  fullname: Palmer, Glen E
  organization: University of Tennessee Health Science Center, Department of Clinical Pharmacy, Memphis, Tennessee, USA
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  givenname: Bernhard
  surname: Hube
  fullname: Hube, Bernhard
  organization: Friedrich-Schiller-University Jena, Jena, Germany
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  givenname: Julian R
  surname: Naglik
  fullname: Naglik, Julian R
  email: julian.naglik@kcl.ac.uk, brian.peters@uthsc.edu
  organization: King's College London, Division of Mucosal and Salivary Biology, London, United Kingdom julian.naglik@kcl.ac.uk brian.peters@uthsc.edu
– sequence: 10
  givenname: Brian M
  surname: Peters
  fullname: Peters, Brian M
  email: julian.naglik@kcl.ac.uk, brian.peters@uthsc.edu
  organization: University of Tennessee Health Science Center, Department of Clinical Pharmacy, Memphis, Tennessee, USA julian.naglik@kcl.ac.uk brian.peters@uthsc.edu
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29109176$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
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Issue 2
Keywords Candidalysin
immunopathogenesis
vulvovaginal
Candida
mucosal pathogens
epithelial cells
mycology
vaginitis
mucosal immunity
Language English
License Copyright © 2018 American Society for Microbiology.
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Snippet Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen , is a disease of immunocompetent and otherwise healthy...
Unlike other forms of candidiasis, vulvovaginal candidiasis, caused primarily by the fungal pathogen Candida albicans, is a disease of immunocompetent and...
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SubjectTerms Animals
Candida albicans - pathogenicity
Candidiasis, Vulvovaginal - immunology
Candidiasis, Vulvovaginal - metabolism
Cytokines - metabolism
Epithelial Cells - metabolism
Epithelial Cells - microbiology
Female
Fungal Proteins - metabolism
Fungal Proteins - pharmacology
Humans
Mice
Mucous Membrane - microbiology
Mucous Membrane - pathology
Neutrophil Infiltration - immunology
Signal Transduction
Vagina - immunology
Vagina - metabolism
Vagina - microbiology
Virulence Factors
Title Candidalysin Drives Epithelial Signaling, Neutrophil Recruitment, and Immunopathology at the Vaginal Mucosa
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