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Circulating and Tissue-Resident CD4+ T Cells with Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function Is Altered During Inflammation

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Circulating and Tissue-Resident CD4+ T Cells with Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function Is Altered During Inflammation Accepted Manuscript Circulating and Tissue-resident CD4+ T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function is Altered During Inflammation Ahmed N. Hegazy, Nathaniel R. West, Michael J.T. Stubbington, Emily Wendt, Kim I.M. Suijker, Angeliki Datsi, Sebastien This, Camille Danne, Suzanne Campion, Sylvia H. Duncan, Benjamin M.J. Owens, Holm H. Uhlig, Andrew McMichael, Andreas Bergthaler, Sarah A. Teichmann, Satish Keshav, Fiona Powrie PII: S0016-5085(17)35979-6 DOI: 10.1053/j.gastro.2017.07.047 Reference: YGAST 61339 To appear in: Gastroenterology Accepted Date: 25 July 2017 Please cite this article as: Hegazy AN, West NR, Stubbington MJT, Wendt E, Suijker KIM, Datsi A, This S, Danne C, Campion S, Duncan SH, Owens BMJ, Uhlig HH, McMichael A, Oxford IBD Cohort Investigators, Bergthaler A, Teichmann SA, Keshav S, Powrie F, Circulating and Tissue-resident CD4+ T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function is Altered During Inflammation, Gastroenterology (2017), doi: 10.1053/j.gastro.2017.07.047. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. ACCEPTED MANUSCRIPT CFSE Memory CD4+ T cells labelling (CD3+ CD4+ MACS/FACS CFSE A CD45RA- ) dilution Expansion 3-7 days Co-culture C MACS Incubation with 100 **** Monocytes bacterial lysates CD14+ **** 80 S. typhimurium F. prausnitzii C. difficile S. aureus cells (%) 5 5 5 B 5 10 10 10 + 10 0.26 0.2 0.25 0.431 60 4 4 4 104 10 10 10 0.84 0.21 0.34 1.07 3 3 3 103 10 10 10 40 Day 3 of CD4 low 0 0 0 0 20 0.01 0.07 0.05 0.03 2 3 4 5 2 3 4 5 2 3 4 5 CFSE 0 102 103 104 105 0 10 10 10 10 0 10 10 10 10 0 10 10 10 10 1.69 5 5 5 ICOS 105 15.1 10 16.2 1 10 17.1 1 10 40.4 1.9 0 4 4 4 104 10 10 10 3 3 3 103 10 10 10 Day 6 S. aureus 2 2 2 no microbe 102 10 10 10 0 0 0 0 M. tuberculosis 0.77 4.39 1.72 0.9 3 4 5 0 103 104 105 0 103 104 105 0 103 104 105 0 10 10 10 CFSE D E. coli S. typhimurium B. animalis L. acidophilus F. prausnitzii C. difficile S. aureus 15 **** 20 **** 10 **** 40 **** 15 **** 15 *** 25 **** **** **** **** **** **** *** **** 8 20 15 30 cells (%) + 10 10 10 6 15 10 20 4 10 of CD4 5 5 5 10 low ns 5 ns ns ns ns ns ns 2 5 0 0 0 0 0 0 0 CFSE + + + + + + + microbe microbe microbe microbe microbe microbe -MHC II -MHC II -MHC II -MHC II -MHC II -MHC II microbe-MHC no II microbe microbeα no microbe microbeα no microbe microbeα no microbe microbeα no microbeMANUSCRIPT microbeα no microbe microbeα no microbe α E E. coli B. animalis L. acidophilus F 5 80 5 10 100 10 17 0.7 13.2 0.6 9.8 0.5 *** *** **** **** **** **** **** **** **** **** **** **** **** **** **** **** **** **** 104 cells 103 + 80 cells (%) cells (%) + + 60 CD25 4 0 10 CD4 60 CD4 3.6 78.7 2.22 83.9 4.4 85.4 CD4 low 3 4 5 3 4 5 0 103 104 105 0 10 10 10 0 10 10 10 low low 40 105 8.58 0.632 8.4 0.5 7.4 1.2 40 104 3 (Geo mean) 10 103 20 of CFSE of CFSE 20 + + OX40 0 12 78.8 6.9 84.2 6.5 85 ICOS of CFSE 2 3 4 5 3 4 5 3 4 5 0 0 10 10 10 0 10 10 10 0 10 10 10 10 CD25 0 OX40 high high high CFSE E. coli E. coli E. coli CFSE CFSE CFSE C. difficile C. difficile C. difficile B. animalis B. animalis B. animalis F. prausnitzii F. prausnitzii F. prausnitzii S. typhimuriumL. acidophilus S. typhimuriumL. acidophilus S. typhimuriumL. acidophilus Shared clonotypes, TCRVβ Donor 1 Donor 2 Donor 3 (%) G H 10 105 E. coli s e S. typhimurium 8 p 104 y t ACCEPTEDB. animalis lono 3 6 c 10 f L. acidophilus o r e F. prausnitzii 4 b 102 m u C. difficile N 1 2 10 SEB rium u PHA SEB E. coli PHA 0 phim C. difficile B. animalis F. prausnitzii S. ty L. acidophilus rium rium rium u SEB PHA u SEB PHA u SEB PHA E. coli E. coli E. coli C. difficile C. difficile C. difficile phim B. animalis phim B. animalis phim B. animalis F. prausnitzii F. prausnitzii F. prausnitzii S. ty L. acidophilus S. ty L. acidophilus S. ty L. acidophilus Supplementary Figure S4 ACCEPTED MANUSCRIPT Manuscript Number : GASTRO-D-16-01275R1 Title: Circulating and Tissue-resident CD4+ T Cells With Reactivity to Intestinal Microbiota Are Abundant in Healthy Individuals and Function is Altered During Inflammation Authors: Ahmed N. Hegazy 1,2,10 , Nathaniel R. West 1,2,10 , Michael J. T. Stubbington 3,4 , Emily Wendt 1, Kim I. M. Suijker 2, Angeliki Datsi 1, Sebastien This 1, Camille Danne 2, Suzanne Campion 5, Sylvia H. Duncan 6, Benjamin M. J. Owens 1, Holm H. Uhlig 1,7, Andrew McMichael 5, Oxford IBD Cohort Investigators 8, Andreas Bergthaler 9, Sarah A. Teichmann 3,4 , Satish Keshav 1, Fiona Powrie 1,2 Affiliations: 1Translational Gastroenterology Unit, Nuffield Department of Clinical Medicine, Experimental Medicine Division, John Radcliffe Hospital, UniversMANUSCRIPTity of Oxford, UK 2Kennedy Institute of Rheumatology, Nuffield Department of Orthopaedics, Rheumatology and Musculoskeletal Sciences, University of Oxford, UK 3European Molecular Biology Laboratory-European Bioinformatics Institute, Hinxton, UK 4Wellcome Trust Sanger Institute, Wellcome Trust Genome Campus, Hinxton, Cambridge, UK 5Nuffield Department of Medicine Research Building, University of Oxford, Oxford, UK 6Microbial Ecology Group, Rowett Institute of Nutrition and Health, University of Aberdeen, UK 7Department of Paediatrics, University of Oxford, Oxford, UK 8Individual investigatorsACCEPTED are listed in the acknowledgement section 9CeMM Research Center for Molecular Medicine of the Austrian Academy of Sciences, Vienna, Austria 10 Co-first authors Grant support: ANH was supported by an EMBO long-term fellowship and a Marie Curie 1 ACCEPTED MANUSCRIPT fellowship. NRW was supported by a CRI Irvington Post-doctoral Fellowship. BMJO was supported by an Oxford-UCB Pharma Postdoctoral Fellowship. MJTS and SAT were supported by ERC grant ThSWITCH and ThDEFINE (260507). SC and AM were supported by the Center for HIV/AIDS Vaccine Immunology and Immunogen Discovery (grant UM1-AI100645). The Rowett Institute of Nutrition and Health receives financial support from the Scottish Government Rural and Environmental Sciences and Analytical Services (SG-RESAS). Foundation Louis Jeantet, Wellcome Trust (Investigator award 095688/Z/11/Z), and ERC (ERC/HN/2013/21) supported FP and this project. HHU is supported by the Crohn’s & Colitis Foundation of America (CCFA), The Leona M. and Harry B. Helmsley Charitable Trust. SD receive financial support from the Scottish Government Rural and Environmental Sciences and Analytical Services (RESAS). Abbreviations: Antigen presenting cells (APCs), Brefeldin A (BFA), Carboxyfluorescein succinimidyl ester (CFSE), Central memory (CM), Chemokine ligand (CCL), Chemokine receptor (CCR), Crohn’s disease (CD), Effector memoryMANUSCRIPT (EM), Fluorescence minus one (FMO), Gastrointestinal tract (GIT), GATA-binding factor-3 (GATA-3), Inflammatory bowel disease (IBD), Interferon-gamma (IFN-γ), Interleukin (IL-), Lamina propria mononuclear cells (LPMCs), Lipopolysaccharide (LPS), Magnetic cell separation (MACS), Major histocompatibility complex (MHC), Peripheral blood mononuclear cell (PBMC), Phytohaemagglutinin (PHA), RAR-related orphan receptor gamma t (ROR γt), Regulatory T cells (Treg), Staphylococcus enterotoxin B (SEB), T cell receptor (TCR), T helper (Th), T-box-expressed-in-T-cells (T-bet), Tumour necrosis factor alpha (TNF-α), Ulcerative colitis (UC), Violet proliferation dye (VPD). Corresponding ACCEPTEDauthor: Prof. Fiona Powrie, FRS, Kennedy Institute of Rheumatology, University of Oxford, Roosevelt Drive, Headington, Oxford, OX3 7FY, UK Email: [email protected]; Tel: +44 (0)1865 612 659 Disclosures: These authors disclose the following: F.P. has received research support or 2 ACCEPTED MANUSCRIPT consultancy fees from Eli Lilly, Merck, GSK, Janssen, Compugen, UCB, and MedImmune. S.K. has received consulting fees and research support from ChemoCentryx Inc. and GSK in the past. The remaining authors declare no conflict of interest. HHU has project collaboration with Eli Lilly and UCB Pharma related to this project. Dr Keshav has provided consultancy services for a number of pharmaceutical and healthcare companies including Abbvie, Actavis Allergan, Astra-Zeneca, Boehringer Ingelheim, ChemoCentryx, Dr Falk Pharma, Ferring, Gilead, GSK, Merck, Mitsubishi Tanabe Pharma, Pharmacosmos, Pfizer, Takeda, and Vifor Pharma, and received research support from Abbvie, ChemoCentryx, GSK, and Merck. Transcript Profiling: None Writing Assistance: None Author Contributions: ANH, NRW designed, performed, and analysed experiments. ANH, NRW, and FP conceived and designed the project, interpreted data, and wrote the manuscript. MJTS analysed TCR sequencing data. EW, KS, AD, ST,MANUSCRIPT SC, BMJO, CD, SHD, AB were involved in acquisition of data, data analysis and interpretation of data. SAT, SK, HHU, AM provided essential materials and were involved in data interpretation and discussions. Oxford IBD Cohort Investigators provided IBD patient samples and ethical approval for the project. The Oxford IBD Cohort Investigators are: Dr.
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