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Bacterial Infections | Spotlight

Evaluating Shigella flexneri Pathogenesis in the Human Enteroid Model

Sridevi Ranganathan, Michele Doucet, Christen L. Grassel, BreOnna Delaine-Elias, Nicholas C. Zachos, Eileen M. Barry
Vincent B. Young, Editor
Sridevi Ranganathan
aCenter for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
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Michele Doucet
bDepartment of Medicine, Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
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Christen L. Grassel
aCenter for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
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BreOnna Delaine-Elias
aCenter for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
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Nicholas C. Zachos
bDepartment of Medicine, Division of Gastroenterology and Hepatology, Johns Hopkins University School of Medicine, Baltimore, Maryland, USA
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Eileen M. Barry
aCenter for Vaccine Development and Global Health, University of Maryland School of Medicine, Baltimore, Maryland, USA
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Vincent B. Young
University of Michigan-Ann Arbor
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DOI: 10.1128/IAI.00740-18
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ABSTRACT

The enteric pathogen Shigella is one of the leading causes of moderate-to-severe diarrhea and death in young children in developing countries. Transformed cell lines and animal models have been widely used to study Shigella pathogenesis. In addition to altered physiology, transformed cell lines are composed of a single cell type that does not sufficiently represent the complex multicellular environment of the human colon. Most available animal models do not accurately mimic human disease. The human intestinal enteroid model, derived from LGR5+ stem cell-containing intestinal crypts from healthy subjects, represents a technological leap in human gastrointestinal system modeling and provides a more physiologically relevant system that includes multiple cell types and features of the human intestine. We established the utility of this model for studying basic aspects of Shigella pathogenesis and host responses. In this study, we show that Shigella flexneri is capable of infecting and replicating intracellularly in human enteroids derived from different segments of the intestine. Apical invasion by S. flexneri is very limited but increases ∼10-fold when enteroids are differentiated to include M cells. Invasion via the basolateral surface was at least 2-log10 units more efficient than apical infection. Increased secretion of interleukin-8 and higher expression levels of the mucin glycoprotein Muc2 were observed in the enteroids following S. flexneri infection. The human enteroid model promises to bridge some of the gaps between traditional cell culture, animal models, and human infection.

FOOTNOTES

    • Received 30 September 2018.
    • Returned for modification 15 November 2018.
    • Accepted 6 January 2019.
    • Accepted manuscript posted online 14 January 2019.
  • Supplemental material for this article may be found at https://doi.org/10.1128/IAI.00740-18.

  • Copyright © 2019 Ranganathan et al.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

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Evaluating Shigella flexneri Pathogenesis in the Human Enteroid Model
Sridevi Ranganathan, Michele Doucet, Christen L. Grassel, BreOnna Delaine-Elias, Nicholas C. Zachos, Eileen M. Barry
Infection and Immunity Mar 2019, 87 (4) e00740-18; DOI: 10.1128/IAI.00740-18

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Evaluating Shigella flexneri Pathogenesis in the Human Enteroid Model
Sridevi Ranganathan, Michele Doucet, Christen L. Grassel, BreOnna Delaine-Elias, Nicholas C. Zachos, Eileen M. Barry
Infection and Immunity Mar 2019, 87 (4) e00740-18; DOI: 10.1128/IAI.00740-18
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KEYWORDS

human intestinal enteroids
M cells
S. flexneri pathogenesis
colonoid

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