A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation

Mary O'Connell Motherway, Aileen Houston, Grace O'Callaghan, Justus Reunanen, Frances O'Brien, Tara O'Driscoll, Patrick G. Casey, Willem M. de Vos, Douwe van Sinderen, Fergus Shanahan

Research output: Contribution to journalArticleAcademicpeer-review

2 Citations (Scopus)

Abstract

Development of the human gut microbiota commences at birth, with certain bifidobacterial species representing dominant and early colonisers of the newborn gastrointestinal tract. The molecular basis of Bifidobacterium colonisation, persistence and presumed communication with the host has remained obscure. We previously identified tight adherence (Tad) pili from Bifidobacterium breve UCC2003 as an essential colonisation factor. Here, we demonstrate that bifidobacterial Tad pili also promote in vivo colonic epithelial proliferation. A significant increase in cell proliferation was detectable 5 days postadministration of B. breve UCC2003. Using advanced functional genomic approaches, bacterial strains either (a) producing the Tad2003 pili or (b) lacking the TadE or TadF pseudopilins were created. Analysis of the ability of these mutant strains to promote epithelial cell proliferation in vivo demonstrated that the pilin subunit, TadE, is the bifidobacterial molecule responsible for this proliferation response. These findings were confirmed in vitro using purified TadE protein. Our data imply that bifidobacterial Tad pili may contribute to the maturation of the naïve gut in early life through the production of a specific scaffold of extracellular protein structures, which stimulate growth of the neonatal mucosa.

LanguageEnglish
Pages287-301
JournalMolecular Microbiology
Volume111
Issue number1
Early online date23 Oct 2018
DOIs
Publication statusPublished - Jan 2019

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Cell Proliferation
Fimbriae Proteins
Aptitude
Bifidobacterium
Human Development
Gastrointestinal Tract
Mucous Membrane
Proteins
Epithelial Cells
Communication
Parturition
Growth
Bifidobacterium breve
In Vitro Techniques
Gastrointestinal Microbiome

Cite this

O'Connell Motherway, M., Houston, A., O'Callaghan, G., Reunanen, J., O'Brien, F., O'Driscoll, T., ... Shanahan, F. (2019). A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation. Molecular Microbiology, 111(1), 287-301. https://doi.org/10.1111/mmi.14155
O'Connell Motherway, Mary ; Houston, Aileen ; O'Callaghan, Grace ; Reunanen, Justus ; O'Brien, Frances ; O'Driscoll, Tara ; Casey, Patrick G. ; de Vos, Willem M. ; van Sinderen, Douwe ; Shanahan, Fergus. / A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation. In: Molecular Microbiology. 2019 ; Vol. 111, No. 1. pp. 287-301.
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abstract = "Development of the human gut microbiota commences at birth, with certain bifidobacterial species representing dominant and early colonisers of the newborn gastrointestinal tract. The molecular basis of Bifidobacterium colonisation, persistence and presumed communication with the host has remained obscure. We previously identified tight adherence (Tad) pili from Bifidobacterium breve UCC2003 as an essential colonisation factor. Here, we demonstrate that bifidobacterial Tad pili also promote in vivo colonic epithelial proliferation. A significant increase in cell proliferation was detectable 5 days postadministration of B. breve UCC2003. Using advanced functional genomic approaches, bacterial strains either (a) producing the Tad2003 pili or (b) lacking the TadE or TadF pseudopilins were created. Analysis of the ability of these mutant strains to promote epithelial cell proliferation in vivo demonstrated that the pilin subunit, TadE, is the bifidobacterial molecule responsible for this proliferation response. These findings were confirmed in vitro using purified TadE protein. Our data imply that bifidobacterial Tad pili may contribute to the maturation of the na{\"i}ve gut in early life through the production of a specific scaffold of extracellular protein structures, which stimulate growth of the neonatal mucosa.",
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O'Connell Motherway, M, Houston, A, O'Callaghan, G, Reunanen, J, O'Brien, F, O'Driscoll, T, Casey, PG, de Vos, WM, van Sinderen, D & Shanahan, F 2019, 'A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation', Molecular Microbiology, vol. 111, no. 1, pp. 287-301. https://doi.org/10.1111/mmi.14155

A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation. / O'Connell Motherway, Mary; Houston, Aileen; O'Callaghan, Grace; Reunanen, Justus; O'Brien, Frances; O'Driscoll, Tara; Casey, Patrick G.; de Vos, Willem M.; van Sinderen, Douwe; Shanahan, Fergus.

In: Molecular Microbiology, Vol. 111, No. 1, 01.2019, p. 287-301.

Research output: Contribution to journalArticleAcademicpeer-review

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AU - Houston, Aileen

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O'Connell Motherway M, Houston A, O'Callaghan G, Reunanen J, O'Brien F, O'Driscoll T et al. A Bifidobacterial pilus-associated protein promotes colonic epithelial proliferation. Molecular Microbiology. 2019 Jan;111(1):287-301. https://doi.org/10.1111/mmi.14155