Adherent-invasive Escherichia coli production of cellulose influences iron-induced bacterial aggregation, phagocytosis, and induction of colitis

Melissa Ellermann, Eun Young Huh, Bo Liu, Ian M Carroll, Rita Tamayo, Ryan Balfour Sartor

Research output: Contribution to journalArticle

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Abstract

Adherent-invasive Escherichia coli (AIEC), a functionally distinct subset of resident intestinal E. coli associated with Crohn's disease, is characterized by enhanced epithelial adhesion and invasion, survival within macrophages, and biofilm formation. Environmental factors, such as iron, modulate E. coli production of extracellular structures, which in turn influence the formation of multicellular communities, such as biofilms, and bacterial interactions with host cells. However, the physiological and functional responses of AIEC to variable iron availability have not been thoroughly investigated. We therefore characterized the impact of iron on the physiology of AIEC strain NC101 and subsequent interactions with macrophages. Iron promoted the cellulose- dependent aggregation of NC101. Bacterial cells recovered from the aggregates were more susceptible to phagocytosis than planktonic cells, which corresponded with the decreased macrophage production of the proinflammatory cytokine interleukin- 12 (IL-12) p40. Prevention of aggregate formation through the disruption of cellulose production reduced the phagocytosis of iron-exposed NC101. In contrast, under iron-limiting conditions, where NC101 aggregation is not induced, the disruption of cellulose production enhanced NC101 phagocytosis and decreased macrophage secretion of IL-12 p40. Finally, abrogation of cellulose production reduced NC101 induction of colitis when NC101 was monoassociated in inflammation-prone Il10-/- mice. Taken together, our results introduce cellulose as a novel physiological factor that impacts host-microbe-environment interactions and alters the proinflammatory potential of AIEC.

LanguageEnglish (US)
Pages4068-4080
Number of pages13
JournalInfection and immunity
Volume83
Issue number10
DOIs
StatePublished - Jan 1 2015

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Colitis
Phagocytosis
Cellulose
Iron
Escherichia coli
Macrophages
Interleukin-12
Biofilms
Cytophagocytosis
Crohn Disease
Interleukin-10
Cytokines
Inflammation

ASJC Scopus subject areas

  • Parasitology
  • Microbiology
  • Immunology
  • Infectious Diseases

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Adherent-invasive Escherichia coli production of cellulose influences iron-induced bacterial aggregation, phagocytosis, and induction of colitis. / Ellermann, Melissa; Huh, Eun Young; Liu, Bo; Carroll, Ian M; Tamayo, Rita; Sartor, Ryan Balfour.

In: Infection and immunity, Vol. 83, No. 10, 01.01.2015, p. 4068-4080.

Research output: Contribution to journalArticle

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