University of Oulu

O'Connell Motherway, M. , Houston, A. , O’Callaghan, G. , Reunanen, J. , O’Brien, F. , O’Driscoll, T. , Casey, P. G., de Vos, W. M., van Sinderen, D. and Shanahan, F. (2019), A Bifidobacterial pilus‐associated protein promotes colonic epithelial proliferation. Mol Microbiol, 111: 287-301. doi:10.1111/mmi.14155

A bifidobacterial pilus‐associated protein promotes colonic epithelial proliferation

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Author: O'Connell Motherway, Mary1,2; Houston, Aileen1,3; O’Callaghan, Grace1,3;
Organizations: 1APC Microbiome Ireland, National University of Ireland, Western Road, Cork, Ireland
2School of Microbiology, National University of Ireland, Western Road, Cork, Ireland
3Department of Medicine, National University of Ireland, Cork University Hospital, Cork, Ireland
4Research Programme Unit Immunobiology, Department of Bacteriology and Immunology, Helsinki University, Helsinki, Finland
5Cancer and Translational Medicine Research Unit and Biocenter Oulu, University of Oulu, Oulu, Finland
6Laboratory of Microbiology, Wageningen University, The Netherlands
Format: article
Version: accepted version
Access: embargoed
Persistent link: http://urn.fi/urn:nbn:fi-fe2019070822844
Language: English
Published: John Wiley & Sons, 2019
Publish Date: 2020-01-31
Description:

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.

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Series: Molecular microbiology
ISSN: 0950-382X
ISSN-E: 1365-2958
ISSN-L: 0950-382X
Volume: 111
Issue: 1
Pages: 287 - 301
DOI: 10.1111/mmi.14155
OADOI: https://oadoi.org/10.1111/mmi.14155
Type of Publication: A1 Journal article – refereed
Field of Science: 1182 Biochemistry, cell and molecular biology
3111 Biomedicine
Subjects:
Funding: This work was supported by Science Foundation Ireland (SFI) (grant no. SFI/12/RC/2273) awarded to the APC Microbiome Institute, and HRB postdoctoral fellowship (grant no. PDTM/20011/9) awarded to MOCM. WMdV is supported by a Gravitation grant (024.002.002 SIAM) and Spinoza Award of the Netherlands Organization for Scientific Research and the Finland Academy of Sciences (Grant 141130 to WMdV) and JR by the Academy of Finland (Grant number 299749). The authors acknowledge the assistance of the staff, and the facilities provided at the Electron Microscopy Unit of the Institute of Biotechnology at the University of Helsinki.
Academy of Finland Grant Number: 299749
Detailed Information: 299749 (Academy of Finland Funding decision)
Copyright information: © 2018 John Wiley & Sons Ltd. This is the peer reviewed version of the following article: O'Connell Motherway, M. , Houston, A. , O’Callaghan, G. , Reunanen, J. , O’Brien, F. , O’Driscoll, T. , Casey, P. G., de Vos, W. M., van Sinderen, D. and Shanahan, F. (2019), A Bifidobacterial pilus‐associated protein promotes colonic epithelial proliferation. Mol Microbiol, 111: 287-301. doi:10.1111/mmi.14155, which has been published in final form at https://doi.org/10.1111/mmi.14155. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.