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Minireview | Spotlight

Candida albicans Pathogenesis: Fitting within the Host-Microbe Damage Response Framework

Mary Ann Jabra-Rizk, Eric F. Kong, Christina Tsui, M. Hong Nguyen, Cornelius J. Clancy, Paul L. Fidel Jr.,, Mairi Noverr
A. T. Maurelli, Editor
Mary Ann Jabra-Rizk
aDepartment of Oncology and Diagnostic Sciences, Dental School, University of Maryland, Baltimore, Maryland, USA
bDepartment of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, Maryland, USA
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Eric F. Kong
aDepartment of Oncology and Diagnostic Sciences, Dental School, University of Maryland, Baltimore, Maryland, USA
bDepartment of Microbiology and Immunology, School of Medicine, University of Maryland, Baltimore, Maryland, USA
cGraduate Program in Life Sciences, Molecular Microbiology and Immunology Program, University of Maryland, Baltimore, Maryland, USA
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Christina Tsui
aDepartment of Oncology and Diagnostic Sciences, Dental School, University of Maryland, Baltimore, Maryland, USA
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M. Hong Nguyen
dDivision of Infectious Diseases, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
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Cornelius J. Clancy
dDivision of Infectious Diseases, Department of Medicine, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania, USA
eInfectious Diseases Section, VA Pittsburgh Healthcare System, Pittsburgh, Pennsylvania, USA
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Paul L. Fidel Jr.,
fCenter of Excellence in Oral and Craniofacial Biology, Louisiana State University Health Sciences Center School of Dentistry, New Orleans, Louisiana, USA
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Mairi Noverr
fCenter of Excellence in Oral and Craniofacial Biology, Louisiana State University Health Sciences Center School of Dentistry, New Orleans, Louisiana, USA
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A. T. Maurelli
University of Florida
Roles: Editor
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DOI: 10.1128/IAI.00469-16
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    FIG 1

    Anatomical defenses and host damage associated with the various manifestations of candidiasis. The illustration shows the diverse and site-specific diseases caused by C. albicans, highlighting the disease pathogenesis in each case and site-specific host immune responses.

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    FIG 2

    Damage response framework curves. Individual graphs are included for each class, with an associated Candida infection. (A) Class 1, pathogens that cause damage only in situations of weak immune responses (e.g., oral candidiasis). (B) Class 2, pathogens that cause damage either in hosts with weak immune responses or in the setting of normal immune responses (e.g., invasive candidiasis). (C) Class 3, pathogens that cause damage in the setting of appropriate immune responses and produce damage at both ends of the continuum of immune responses (e.g., intra-abdominal candidiasis). (D) Class 4, pathogens that cause damage primarily at the extremes of both weak and strong immune responses (e.g., gastrointestinal candidiasis). (E) Class 5, pathogens that cause damage across the spectrum of immune responses, but damage can be enhanced by strong immune responses (e.g., denture stomatitis). (F) Class 6, microorganisms that can cause damage only under conditions of strong immune responses (e.g., vaginal candidiasis). (Adapted from reference 1 with permission.)

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    FIG 3

    Clinical manifestations of oral candidiasis. (A) Pseudomembranous candidiasis is characterized by white plaques formed on the tongue and the buccal mucosa. (B) Erythematous candidiasis example, showing the subtle red lesions on the tongue, which can also occur on the palate.

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    FIG 4

    Mouse model of oral candidiasis. (A) An infected mouse exhibiting clinical signs of advanced candidiasis on the surface of the tongue 4 days post-sublingual infection with C. albicans. (B) Histopathology of an infected tongue tissue section, demonstrating the extensive presence of C. albicans around the periphery of the tongue. Hyphae can be seen penetrating the subepithelial tissue, along with a marked presence of host inflammatory cells. (C) Magnified image of tongue tissue, revealing the depth of hyphal invasion into the subepithelium (arrows). Bar, 20 μm. (D) Scanning electron micrograph of excised tongue showing the thick biofilm formed on the outer epithelial surface consisting of C. albicans hyphae invading the subepithelium. (E) Higher-magnification image of the outer surface of the tongue showing the epithelium spiny layer with hyphae penetrating through the surface. (F) Significant gap in the tissue caused by hyphae invading from the sublingual area as it emerges through the tongue surface. (Reprinted from reference 166.)

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    FIG 5

    Clinical manifestations of denture stomatitis. (A) Red inflammatory lesions formed on the denture-associated palatal tissue in a patient with a partial denture. (B) Inflammation of the gingival tissue in a patient with a full denture.

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    FIG 6

    Rat model of Candida-associated denture stomatitis. Individual impressions were made for each rat, using vinyl polysiloxane impression material. Molds were made from the impressions, which were then used to construct the fixed and removable portions of the denture system. (B) Scanning electron and confocal fluorescence microscopy analysis images of a C. albicans biofilm formed in vivo on the denture and palate of rats 4 and 8 weeks postinfection with C. albicans. (Reprinted from reference 166.)

Tables

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  • TABLE 1

    Examples of C. albicans infections, host predisposing factors, and animal models for each DRF class

    DRF classCandidal infection examplePrimary predisposing factor(s)Rodent model(s)
    Class 1Oropharyngeal candidiasisImmunocompromised state (AIDS, cancer patients)Mouse oral infection model
    Class 2Hematogenously disseminated candidiasisGI tract mucosal disturbances; intravenous catheters; surgery; use of broad-spectrum antibiotics; neutropenia and other immunosuppressed conditionsRodent intravenous, subcutaneous catheter and GI tract translocation models
    Class 3Intra-abdominal candidiasisPeritoneal dialysis; bowel surgery; GI tract perforation; hepatobiliary leaksMouse peritonitis and abscess models
    Class 4Gastrointestinal candidiasisImmune deficiency; cancer; antibiotic or immunosuppressive therapyMouse mucosal GI model
    Class 5Denture stomatitisDenture usage; poor oral hygieneRat denture model
    Class 6Vulvovaginal candidiasisAntibiotic or hormone therapy; estrogen replacement; vaginal microbiome dysbiosisRodent vaginal infection models
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Candida albicans Pathogenesis: Fitting within the Host-Microbe Damage Response Framework
Mary Ann Jabra-Rizk, Eric F. Kong, Christina Tsui, M. Hong Nguyen, Cornelius J. Clancy, Paul L. Fidel Jr.,, Mairi Noverr
Infection and Immunity Sep 2016, 84 (10) 2724-2739; DOI: 10.1128/IAI.00469-16

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Candida albicans Pathogenesis: Fitting within the Host-Microbe Damage Response Framework
Mary Ann Jabra-Rizk, Eric F. Kong, Christina Tsui, M. Hong Nguyen, Cornelius J. Clancy, Paul L. Fidel Jr.,, Mairi Noverr
Infection and Immunity Sep 2016, 84 (10) 2724-2739; DOI: 10.1128/IAI.00469-16
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  • Top
  • Article
    • ABSTRACT
    • INTRODUCTION
    • DAMAGE RESPONSE FRAMEWORK
    • DRF CLASSIFICATION OF MICROBIAL SPECIES
    • CANDIDA ALBICANS: A VERSATILE FUNGAL PATHOGEN
    • FITTING C. ALBICANS WITHIN THE DAMAGE RESPONSE FRAMEWORK
    • THE HOST AND THE HOST MICROBIOTA
    • CONCLUDING REMARKS AND FUTURE PERSPECTIVES
    • ACKNOWLEDGMENTS
    • REFERENCES
  • Figures & Data
  • Info & Metrics
  • PDF

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