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Bacterial Infections

Aggregative Adherence Fimbriae II of Enteroaggregative Escherichia coli Are Required for Adherence and Barrier Disruption during Infection of Human Colonoids

Laura A. Gonyar, Rachel M. Smith, Jorge A. Giron, Nicholas C. Zachos, Fernando Ruiz-Perez, James P. Nataro
Igor E. Brodsky, Editor
Laura A. Gonyar
aDepartment of Pediatrics, University of Virginia, Charlottesville, Virginia, USA
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Rachel M. Smith
aDepartment of Pediatrics, University of Virginia, Charlottesville, Virginia, USA
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Jorge A. Giron
aDepartment of Pediatrics, University of Virginia, Charlottesville, Virginia, USA
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Nicholas C. Zachos
bDepartment of Medicine, Division of Gastroenterology and Hepatology, Johns Hopkins University, Baltimore, Maryland, USA
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Fernando Ruiz-Perez
aDepartment of Pediatrics, University of Virginia, Charlottesville, Virginia, USA
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James P. Nataro
aDepartment of Pediatrics, University of Virginia, Charlottesville, Virginia, USA
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Igor E. Brodsky
University of Pennsylvania
Roles: Editor
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DOI: 10.1128/IAI.00176-20
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ABSTRACT

Symptomatic and asymptomatic infection with the diarrheal pathogen enteroaggregative Escherichia coli (EAEC) is associated with growth faltering in children in developing settings. The mechanism of this association is unknown, emphasizing a need for better understanding of the interactions between EAEC and the human gastrointestinal mucosa. In this study, we investigated the role of the aggregative adherence fimbriae II (AAF/II) in EAEC adherence and pathogenesis using human colonoids and duodenal enteroids. We found that a null mutant in aafA, the major subunit of AAF/II, adhered significantly less than wild-type (WT) EAEC strain 042, and adherence was restored in a complemented strain. Immunofluorescence confocal microscopy of differentiated colonoids, which produce an intact mucus layer comprised of the secreted mucin MUC2, revealed bacteria at the epithelial surface and within the MUC2 layer. The WT strain adhered to the epithelial surface, whereas the aafA deletion strain remained within the MUC2 layer, suggesting that the presence or absence of AAF/II determines both the abundance and location of EAEC adherence. In order to determine the consequences of EAEC adherence on epithelial barrier integrity, colonoid monolayers were exposed to EAEC constructs expressing or lacking aafA. Colonoids infected with WT EAEC had significantly decreased epithelial resistance, an effect that required AAF/II, suggesting that binding of EAEC to the epithelium is necessary to impair barrier function. In summary, we show that production of AAF/II is critical for adherence and barrier disruption in human colonoids, suggesting a role for this virulence factor in EAEC colonization of the gastrointestinal mucosa.

FOOTNOTES

    • Received 25 March 2020.
    • Returned for modification 9 June 2020.
    • Accepted 30 June 2020.
    • Accepted manuscript posted online 6 July 2020.
  • Supplemental material is available online only.

  • Copyright © 2020 American Society for Microbiology.

All Rights Reserved.

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Aggregative Adherence Fimbriae II of Enteroaggregative Escherichia coli Are Required for Adherence and Barrier Disruption during Infection of Human Colonoids
Laura A. Gonyar, Rachel M. Smith, Jorge A. Giron, Nicholas C. Zachos, Fernando Ruiz-Perez, James P. Nataro
Infection and Immunity Aug 2020, 88 (9) e00176-20; DOI: 10.1128/IAI.00176-20

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Aggregative Adherence Fimbriae II of Enteroaggregative Escherichia coli Are Required for Adherence and Barrier Disruption during Infection of Human Colonoids
Laura A. Gonyar, Rachel M. Smith, Jorge A. Giron, Nicholas C. Zachos, Fernando Ruiz-Perez, James P. Nataro
Infection and Immunity Aug 2020, 88 (9) e00176-20; DOI: 10.1128/IAI.00176-20
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KEYWORDS

Escherichia coli
adherence
aggregative
barrier disruption
colonoid
fimbriae
organoid

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