Progress in Inflammation Research

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4 Progress in Inflammation Research Series Editor Prof. Michael J. Parnham PhD Senior Scientific Advisor PLIVA Research Institute Ltd. Prilaz baruna Filipovića 29 HR Zagreb Croatia Advisory Board G. Z. Feuerstein (Merck Research Laboratories, West Point, PA, USA) M. Pairet (Boehringer Ingelheim Pharma KG, Biberach a. d. Riss, Germany) W. van Eden (Universiteit Utrecht, Utrecht, The Netherlands) Forthcoming titles: NPY Family of Peptides in Immune Disorders, Inflammation, Angiogenesis and Cancer, G.Z. Feuerstein, Z. Zukowska (Editors), 2005 Turning up the Heat on Pain: Vanilloid Receptors in Pain and Inflammation, A.B Malmberg, K.R. Bley (Editors), 2005 Sodium Channels, Pain, and Analgesia, K. Coward, M. Baker (Editors), 2005 Complement and Kidney Disease, P.F. Zipfel (Editor), 2005 (Already published titles see last page.)

5 Regulatory T Cells in Inflammation Leonie S. Taams Arne N. Akbar Marca H. M. Wauben Editors Birkhäuser Verlag Basel Boston Berlin

6 Editors Leonie S. Taams Infection & Immunity Research Group Franklin-Wilkins Building King's College London 150 Stamford Street London SE1 9NN UK Arne N. Akbar Department of Immunology and Molecular Pathology Division of Infection and Immunity University College London 46 Cleveland Street London W1T 4JF UK Marca H. M. Wauben Department of Immunohematology and Blood Transfusion E3-Q, Leiden University Medical Center Albinusdreef 2, P.O. Box RC Leiden The Netherlands Library of Congress Cataloging-in-Publication Data Regulatory T cells in inflammation / Leonie Taams, Arne N. Akbar, Marca H.M. Wauben, editors. p. ; cm. -- (Progress in inflammation research) Includes bibliographical references and index. ISBN (alk. paper) 1. Inflammation. 2. T cells. I. Taams, Leonie. II. Akbar, Arne N. III. Wauben, Marca H. M. IV. PIR (Series) [DNLM: 1. T-Lymphocytes--immunology. 2. Immunity, Cellular. 3. Immunotherapy--methods. QW 568 R ] RB131.R dc Bibliographic information published by Die Deutsche Bibliothek Die Deutsche Bibliothek lists this publication in the Deutsche Nationalbibliografie; detailed bibliographic data is available in the internet at The publisher and editor can give no guarantee for the information on drug dosage and administration contained in this publication. The respective user must check its accuracy by consulting other sources of reference in each individual case. The use of registered names, trademarks etc. in this publication, even if not identified as such, does not imply that they are exempt from the relevant protective laws and regulations or free for general use. ISBN-10: Birkhäuser Verlag, Basel Boston Berlin ISBN-13: Birkhäuser Verlag, Basel Boston Berlin This work is subject to copyright. All rights are reserved, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, re-use of illustrations, recitation, broadcasting, reproduction on microfilms or in other ways, and storage in data banks. For any kind of use, permission of the copyright owner must be obtained Birkhäuser Verlag, P.O. Box 133, CH-4010 Basel, Switzerland Part of Springer Science+Business Media Printed on acid-free paper produced from chlorine-free pulp. TCF Cover design: Markus Etterich, Basel Cover illustration: Cross-talk between antigen presenting cell and regulatory T cell. (By: E.N.M. Nolte -t Hoen and M.H.M. Wauben) Printed in Germany ISBN-10: ISBN-13:

7 Contents List of contributors Preface vii xi Part I: Origin, function and distribution of regulatory T cells Shimon Sakaguchi and Noriko Sakaguchi History of CD25 + CD4 + regulatory T cells Dirk Homann and Matthias G. von Herrath Natural and induced regulatory T cells purpose and problems associated with an emerging distinction Robert N. Barker and Frank J. Ward The role of interleukin-10 in regulatory-t-cell suppression: reconciling the discrepancies Esther N. M. Nolte- t Hoen and Marca H. M. Wauben Activation and distribution of regulatory T cells in naïve and antigen-stimulated immune systems Kevin J. Maloy and Fiona Powrie Regulatory T cells and the innate immune system Part II: The potential use of regulatory T cells in immunotherapy Nadia Giarratana, Giuseppe Penna, Silvia Gregori, Kenn C. Daniel and Luciano Adorini Exploiting the potential of regulatory T cells in the control of type 1 diabetes Sophie Candon and Lucienne Chatenoud Regulatory T cells in type 1 autoimmune diabetes

8 Clare Baecher-Allan, Vissia Viglietta and David A. Hafler The potential for targeting CD4 + CD25 + regulatory T cells in the treatment of multiple sclerosis in humans Jocea M. van Amelsfort, Johannes W. J. Bijlsma and Leonie S. Taams Immunotherapy of rheumatoid arthritis using CD4 + CD25 + regulatory T cells Douglas S. Robinson and Eleanor M. Ling Potential for manipulation of regulatory T cells in treatment or prevention of allergic disease Katie E. Birch, Milica Vukmanovic-Stejic, John R. Reed, Malcolm H. A. Rustin and Arne N. Akbar The role of regulatory T cells in cutaneous disorders Kathryn J. Wood and Ahmed Akl The potential role of CD25 + CD4 + regulatory T cells in the induction and maintenance of transplantation tolerance in humans Index

9 List of contributors Luciano Adorini, BioXell, Via Olgettina 58, Milano, Italy; Arne N. Akbar, Department of Immunology and Molecular Pathology, Division of Infection and Immunity, University College London, 46 Cleveland Street, London W1T 4JF, UK; Ahmed Akl, Nuffield Department of Surgery, John Radcliffe Hospital, University of Oxford, Oxford OX3 9DU, United Kingdom; Clare Baecher-Allan, Laboratory of Molecular Immunology, Center for Neurologic Diseases, Brigham and Women s Hospital and Harvard Medical School, 77 Avenue Louis Pasteur, Boston, MA 02115, USA; callan@rics.bwh.harvard.edu Robert N. Barker, Department of Medicine and Therapeutics, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, UK; r.n.barker@abdn.ac.uk Johannes W. J. Bijlsma, Dept Rheumatology & Clinical Immunology, University Medical Center Utrecht, 3508 GA Utrecht, the Netherlands; j.w.j.bijlsma@azu.nl Katie E. Birch, Department of Immunology and Molecular Pathology, Division of Infection and Immunity, University College London, 46 Cleveland Street, London W1T 4JF, UK; and Department of Dermatology, Royal Free Hospital, Pond Street, London NW3 2QG, UK; Kebirch@aol.com Sophie Candon, INSERM U580, Hôpital Necker, 161 Rue de Sèvres, Paris Cedex 15, France; candon@necker.fr vii

10 List of contributors Lucienne Chatenoud, INSERM U580, Hôpital Necker, 161 Rue de Sèvres, Paris Cedex 15, France; Kenn C. Daniel, BioXell, Via Olgettina 58, Milano, Italy; Nadia Giarratana, BioXell, Via Olgettina 58, Milano, Italy; Silvia Gregori, San Raffaele Telethon Institute for Gene Therapy (HSR-TIGET), Via Olgettina 58, Milano, Italy; David A. Hafler, Laboratory of Molecular Immunology, Center for Neurologic Diseases, Brigham and Women s Hospital and Harvard Medical School, 77 Avenue Louis Pasteur, Boston, MA 02115, USA; dhafler@rics.bwh.harvard.edu Dirk Homann, University of Colorado Health Sciences Center, Barbara Davis Center for Childhood Diabetes, 4200 East 9th Avenue, Box 140, Denver, CO 80262, USA; dhomann@scripps.edu Eleanor M. Ling, Leukocyte Biology Section, Division of Biomedical Sciences and Allergy and Clinical Immunology, National Heart and Lung Institute, Sir Alexander Fleming Building, Imperial College London, Exhibition Road, London SW7 2AZ, UK Kevin J. Maloy, Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford, OX1 3RE, UK; kevin.maloy@path.ox.ac.uk Esther N. M. Nolte- t Hoen, Faculty of Biological Sciences, Imperial College London, South Kensington Campus, London SW7 2AZ, UK; e.nolte@imperial.ac.uk Giuseppe Penna, BioXell, Via Olgettina 58, Milano, Italy; giuseppe.penna@bioxell.com Fiona Powrie, Sir William Dunn School of Pathology, University of Oxford, South Parks Road, Oxford, OX1 3RE, UK; fiona.powrie@path.ox.ac.uk John R. Reed, Department of Immunology and Molecular Pathology, Division of Infection and Immunity, University College London, 46 Cleveland Street, London W1T 4JF, UK; j.reed@rfc.ucl.ac.uk viii

11 List of contributors Douglas S. Robinson, Leukocyte Biology Section, Division of Biomedical Sciences and Allergy and Clinical Immunology, National Heart and Lung Institute, Sir Alexander Fleming Building, Imperial College London, Exhibition Road, London SW7 2AZ, UK; Malcolm H.A. Rustin, Department of Dermatology, Royal Free Hospital, Pond Street, London NW3 2QG, UK Noriko Sakaguchi, Department of Experimental Pathology, Institute for Frontier Medical Sciences, Kyoto University, Kyoto , Japan; and Laboratory of Immunopathology, Research Center for Allergy and Immunology, The Institute for Physical and Chemical Research (RIKEN), Yokohama , Japan; Shimon Sakaguchi, Department of Experimental Pathology, Institute for Frontier Medical Sciences, Kyoto University, 53 Shogoin Kawahara-cho, Sakyo-ku, Kyoto , Japan; and Laboratory of Immunopathology, Research Center for Allergy and Immunology, The Institute for Physical and Chemical Research (RIKEN), Yokohama , Japan; and Core Research for Evolutional Science and Technology (CREST), Science and Technology Agency of Japan, Kawaguchi , Japan; Leonie S. Taams, Infection & Immunity Research Group, Franklin-Wilkins Building, King s College London, 150 Stamford Street, London SE1 9NN, UK; leonie.taams@kcl.ac.uk Jocea M. van Amelsfort, Dept Rheumatology & Clinical Immunology, University Medical Center Utrecht, 3508 GA Utrecht, the Netherlands; j.m.r.vanamelsfort@azu.nl Vissia Viglietta, Laboratory of Molecular Immunology, Center for Neurologic Diseases, Brigham and Women s Hospital and Harvard Medical School, 77 Avenue Louis Pasteur, Boston, MA 02115, USA; vviglietta@rics.bwh.harvard.edu Matthias G. von Herrath, La Jolla Institute for Allergy and Immunology, Division of Immune Regulation, Science Center Drive, La Jolla, San Diego, CA 92121, USA; matthias@liai.org Milica Vukmanovic-Stejic, Department of Immunology and Molecular Pathology, Division of Infection and Immunity, University College London, 46 Cleveland Street, London W1T 4JF, UK; m.vukmanovic-stejic@ucl.ac.uk ix

12 List of contributors Frank J. Ward, Department of Medicine and Therapeutics, Institute of Medical Sciences, University of Aberdeen, Foresterhill, Aberdeen AB25 2ZD, UK; Marca H. M. Wauben, Department of Immunohematology and Blood Transfusion, E3-Q, Leiden University Medical Center, Albinusdreef 2, P.O. Box 9600, 2300 RC Leiden, The Netherlands; Kathryn J. Wood, Nuffield Department of Surgery, John Radcliffe Hospital, University of Oxford, Oxford OX3 9DU, United Kingdom; x

13 Preface Scientific interest in regulatory T cells has revived during the last decade. Initially described in the early seventies as suppressor T cells, the concept of suppressor/regulatory T cells went through turbulent times during the eighties when molecular analysis failed to identify putative suppressor genes. The constructive and elegant cellular experiments on regulatory T cells during the nineties, initiated by Shimon Sakaguchi and co-workers, however has brought these cells back into the limelight. Nowadays, regulatory T cells are regarded as essential components of the immune system, and several different subsets of regulatory T cells have been described. An important regulatory role has been attributed to the CD4 + CD25 + T cells. They act by suppressing immune reactivity thereby maintaining or restoring the balance between immunity and tolerance. The aim of this book is to bring together recent developments and viewpoints in the field of CD4 + CD25 + regulatory T cells and to discuss the potential use of regulatory T cells as target for immunotherapy of inflammatory diseases. By linking data on regulatory T cells from experimental models with recent findings from the clinic, this topical book will be of interest to immunologists and other biomedical researchers as well as clinicians that are interested in regulation and manipulation of the immune response during (chronic) inflammatory disease. October 2004 Leonie S. Taams Arne N. Akbar Marca H. M. Wauben xi

14 Part I Origin, function and distribution of regulatory T cells

15 History of CD25 + CD4 + regulatory T cells Shimon Sakaguchi 1,2,3 and Noriko Sakaguchi 1,2 1 Department of Experimental Pathology, Institute for Frontier Medical Sciences, Kyoto University, 53 Shogoin Kawahara-cho, Sakyo-ku, Kyoto , Japan; 2 Laboratory of Immunopathology, Research Center for Allergy and Immunology, The Institute for Physical and Chemical Research (RIKEN), Yokohama , Japan; 3 Core Research for Evolutional Science and Technology (CREST), Science and Technology Agency of Japan, Kawaguchi , Japan Introduction It is still a key issue in immunology to understand how the immune system discriminates between self and non-self, inhibiting autoimmune responses while allowing effective immune responses to non-self antigens. In addition to physical elimination of self-reactive T cells (clonal deletion) and their functional inactivation (clonal anergy), there is now substantial evidence that T-cell-mediated suppression of selfreactive T cells is also a key mechanism of immunologic self-tolerance [1 3]. Although the idea of T cells that negatively control immune responses is not a new one, for a long time it was controversial whether they actually constituted a definite cellular entity in the immune system [4]. In recent years, however, we have witnessed resurgent interest in suppressor or regulatory T (T R ) cells in many fields of basic and clinical immunology [5, 6]. This change is partly due to our new understanding that the normal immune system endogenously produces as its normal cellular constituent a T-cell subpopulation which is highly specified for suppressive function; abnormality of this population in number or function can indeed be a cause of immunological diseases in particular autoimmune disease and this naturally occurring T R cell population can be exploited for induction of immunological tolerance (e.g., transplantation tolerance), negative control of pathological immune responses (e.g., allergy), and enhancement of host defense (e.g. tumor immunity and microbial immunity) [5]. In addition to these endogenous T R cells, there are other types of T R cell that can be induced by specific methods of antigenic stimulation in vivo or in vivo [7, 8]. In this chapter, we shall provide a brief historical sketch of how endogenous T R cells were recognized and characterized, and discuss their roles in immunologic tolerance and immunoregulation. Regulatory T Cells in Inflammation, edited by Leonie S. Taams, Arne N. Akbar and Marca H.M. Wauben 2005 Birkhäuser Verlag Basel/Switzerland 3