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Helicobacter pylori Adapts to Chronic Infection and Gastric Disease via pH-Responsive BabA-Mediated Adherence

Authors :
Verena Königer
D. Scott Merrell
Roman Andriiovych Moskalenko
Rainer Haas
Thomas Borén
Sara Henriksson
Jafar Mahdavi
Abhijit Chowdhury
Johan Ögren
Anders Hofer
Jay V. Solnick
Dan Danielsson
Sara K. Lindén
Dag Ilver
Konstantinos S. Papadakos
Susanne Vikström
Jörgen Ådén
Jan Holgersson
Gerhard Gröbner
Alexej Schmidt
Jeanna Bugaytsova
Oscar Björnham
Göran O. Bylund
Rolf Sjöström
Stefan Oscarson
Dionyssios N. Sgouras
Lori M. Hansen
Yevgen A Chernov
Anders Esberg
Kristof Moonens
Christopher Aisenbrey
Charles Kelly
Ludmilla A. Morozova-Roche
Jeannette M. Whitmire
Beatriz Martinez-Gonzalez
Asish K. Mukhopadhyay
Angela Eldridge
Nicklas Strömberg
Robert H. Gilman
Andre Dubois
Lars Engstrand
Staffan Schedin
Brett A. Chromy
Justine Younson
Matthew Goldman
Anna Shevtsova
Macarena P. Quintana-Hayashi
Hui Liu
Magnus Unemo
Lena Rakhimova
Anna Åberg
Sebastian Suerbaum
Anna Arnqvist
Pär Gideonsson
Maréne Landström
Douglas E. Berg
Kristoffer Brännström
Anders Olofsson
Melissa Mendez
G. Balakrish Nair
Han Remaut
Umeå University
School of Life Sciences
University of Nottingham, UK (UON)
Sahlgrenska Academy at University of Gothenburg [Göteborg]
Université libre de Bruxelles (ULB)
VIB-VUB Center for Structural Biology [Bruxelles]
VIB [Belgium]
Sumy State University
Max Von Pettenkofer Institute (MVP)
Ludwig-Maximilians-Universität München (LMU)
Uniformed Services University of the Health Sciences (USUHS)
King‘s College London
Johns Hopkins Bloomberg School of Public Health [Baltimore]
Johns Hopkins University (JHU)
School of Digestive and Liver Diseases [Kolkata] (SDLD)
National Institute of Cholera and Enteric Diseases
Translational Health Science and Technology Institute [Faridabad] (THSTI)
Institut Pasteur Hellénique
Réseau International des Instituts Pasteur (RIIP)
Department of Microbiology, Tumor and Cell Biology, Karolinska Institutet
Karolinska Institutet [Stockholm]
Örebro University Hospital [Örebro, Sweden]
Hannover Medical School [Hannover] (MHH)
German Center for Infection Research - partner site Hannover-Braunschweig (DZIF)
School of Chemistry and Chemical Biology (UCD)
University College Dublin [Dublin] (UCD)
University of California [Davis] (UC Davis)
University of California
German Center for Infection Research, Partnersite Munich (DZIF)
Département d'Informatique [Bruxelles] (ULB)
Faculté des Sciences [Bruxelles] (ULB)
Université libre de Bruxelles (ULB)-Université libre de Bruxelles (ULB)
University of California [San Diego] (UC San Diego)
This work was supported by grants from Vetenskapsrådet (VR/M) to T.B. and S.K.L., Cancerfonden to T.B. and A.A., VR/NT to A.A. and S. Schedin, Formas to S.K.L., the J.C. Kempe and Seth M. Kempe Memorial Foundation, the Knut and Alice Wallenberg Foundation (2012.0090) to T.B. and M.L., European Union Seventh Framework Program GastricGlycoExplorer ITN grant number 316929 to T.B. and Y.A.C., Magn. Bergvall’s Foundation to S. Schedin, DFG (SFB 900/A1) to S. Suerbaum, DFG (HA2697/16-1) to R.H., FP6 ANR-06-PATHO-00701 ERA-NET and Actions Concertées Inter-Pasteuriennes (ACIP) (2006) to D.N.S., NIH R01DK063041 to D.E.B., NIH CA082312 to D.S.M., NIH AI070803 and AI081037 to J.V.S., CSIR project, India (No. 37(1640)/14/EMR –II) to A.K.M., and VIB and FWO (grants: G033717N and 12H8416N) to K.M. and H.R.
This paper is dedicated to the memory of our friend, collaborator, and co-author Dr. Andre Dubois, a great scientist who contributed importantly both intellectually and materially to this project. We thank S. Michopoulos and G. Mantzaris for H. pylori clinical isolates and Ö. Furberg (NoPolo.se), N. Ulander (softplanbangkok.com), S. Lindström, and M. Borén for the digital movie, tech, art, and figure work, respectively.
Vrije Universiteit Brussel
Basic (bio-) Medical Sciences
Structural Biology Brussels
Department of Bio-engineering Sciences
Source :
Cell Host and Microbe, Cell Host and Microbe, Elsevier, 2017, 21 (3), pp.376-389. ⟨10.1016/j.chom.2017.02.013⟩, Cell host & microbe, vol 21, iss 3, Bugaytsova, J A, Björnham, O, Chernov, Y A, Gideonsson, P, Henriksson, S, Mendez, M, Sjöström, R, Mahdavi, J, Shevtsova, A, Ilver, D, Moonens, K, Quintana-Hayashi, M P, Moskalenko, R, Aisenbrey, C, Bylund, G, Schmidt, A, Åberg, A, Brännström, K, Königer, V, Vikström, S, Rakhimova, L, Hofer, A, Ögren, J, Liu, H, Goldman, M D, Whitmire, J M, Ådén, J, Younson, J, Kelly, C G, Gilman, R H, Chowdhury, A, Mukhopadhyay, A K, Nair, G B, Papadakos, K S, Martinez-Gonzalez, B, Sgouras, D N, Engstrand, L, Unemo, M, Danielsson, D, Suerbaum, S, Oscarson, S, Morozova-Roche, L A, Olofsson, A, Gröbner, G, Holgersson, J, Esberg, A, Strömberg, N, Landström, M, Eldridge, A M, Chromy, B A, Hansen, L M, Solnick, J V, Lindén, S K, Haas, R, Dubois, A, Merrell, D S, Schedin, S, Remaut, H, Arnqvist, A, Berg, D E & Borén, T 2017, ' Helicobacter pylori Adapts to Chronic Infection and Gastric Disease via pH-Responsive BabA-Mediated Adherence ', Cell Host & Microbe, vol. 21, no. 3, pp. 376-389 . https://doi.org/10.1016/j.chom.2017.02.013
Publication Year :
2017
Publisher :
HAL CCSD, 2017.

Abstract

The BabA adhesin mediates high-affinity binding of Helicobacter pylori to the ABO blood group antigen-glycosylated gastric mucosa. Here we show that BabA is acid responsive-binding is reduced at low pH and restored by acid neutralization. Acid responsiveness differs among strains; often correlates with different intragastric regions and evolves during chronic infection and disease progression; and depends on pH sensor sequences in BabA and on pH reversible formation of high-affinity binding BabA multimers. We propose that BabA's extraordinary reversible acid responsiveness enables tight mucosal bacterial adherence while also allowing an effective escape from epithelial cells and mucus that are shed into the acidic bactericidal lumen andthat bio-selection and changes in BabA bindingproperties through mutation and recombination with babA-related genes are selected by differencesamong individuals and by changes in gastric acidity over time. These processes generate diverse H.pylori subpopulations, in which BabA's adaptive evolution contributes to H.pylori persistence and overt gastric disease.

Details

Language :
English
ISSN :
19313128
Database :
OpenAIRE
Journal :
Cell Host and Microbe, Cell Host and Microbe, Elsevier, 2017, 21 (3), pp.376-389. ⟨10.1016/j.chom.2017.02.013⟩, Cell host & microbe, vol 21, iss 3, Bugaytsova, J A, Björnham, O, Chernov, Y A, Gideonsson, P, Henriksson, S, Mendez, M, Sjöström, R, Mahdavi, J, Shevtsova, A, Ilver, D, Moonens, K, Quintana-Hayashi, M P, Moskalenko, R, Aisenbrey, C, Bylund, G, Schmidt, A, Åberg, A, Brännström, K, Königer, V, Vikström, S, Rakhimova, L, Hofer, A, Ögren, J, Liu, H, Goldman, M D, Whitmire, J M, Ådén, J, Younson, J, Kelly, C G, Gilman, R H, Chowdhury, A, Mukhopadhyay, A K, Nair, G B, Papadakos, K S, Martinez-Gonzalez, B, Sgouras, D N, Engstrand, L, Unemo, M, Danielsson, D, Suerbaum, S, Oscarson, S, Morozova-Roche, L A, Olofsson, A, Gröbner, G, Holgersson, J, Esberg, A, Strömberg, N, Landström, M, Eldridge, A M, Chromy, B A, Hansen, L M, Solnick, J V, Lindén, S K, Haas, R, Dubois, A, Merrell, D S, Schedin, S, Remaut, H, Arnqvist, A, Berg, D E & Borén, T 2017, ' Helicobacter pylori Adapts to Chronic Infection and Gastric Disease via pH-Responsive BabA-Mediated Adherence ', Cell Host & Microbe, vol. 21, no. 3, pp. 376-389 . https://doi.org/10.1016/j.chom.2017.02.013
Accession number :
edsair.doi.dedup.....6a43b410aab75acc08a9fa79a43ec0bb