The Evolution of the Immune System: Conservation and Diversification
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Title The Evolution of the Immune System Conservation and Diversification Page left intentionally blank The Evolution of the Immune System Conservation and Diversification Davide Malagoli Department of Life Sciences Biology Building, University of Modena and Reggio Emilia, Modena, Italy AMSTERDAM • BOSTON • HEIDELBERG • LONDON NEW YORK • OXFORD • PARIS • SAN DIEGO SAN FRANCISCO • SINGAPORE • SYDNEY • TOKYO Academic Press is an imprint of Elsevier Academic Press is an imprint of Elsevier 125 London Wall, London EC2Y 5AS, United Kingdom 525 B Street, Suite 1800, San Diego, CA 92101-4495, United States 50 Hampshire Street, 5th Floor, Cambridge, MA 02139, United States The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK Copyright © 2016 Elsevier Inc. All rights reserved. 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Practitioners and researchers must always rely on their own experience and knowledge in evaluating and using any information, methods, compounds, or experiments described herein. In using such information or methods they should be mindful of their own safety and the safety of others, including parties for whom they have a professional responsibility. To the fullest extent of the law, neither the Publisher nor the authors, contributors, or editors, assume any liability for any injury and/or damage to persons or property as a matter of prod- ucts liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein. British Library Cataloguing-in-Publication Data A catalogue record for this book is available from the British Library Library of Congress Cataloging-in-Publication Data A catalog record for this book is available from the Library of Congress ISBN: 978-0-12-801975-7 For information on all Academic Press publications visit our website at https://www.elsevier.com/ Typeset by Thomson Digital Dedication To my teachers, my students, and all the people who taught me something. Page left intentionally blank Table of Content Contents Contributors xv Preface xvii 1. Hematopoiesis and Hemocytes in Pancrustacean and Molluscan Models Valerie J. Smith, Alice Accorsi, Davide Malagoli 1 Introduction 1 2 Hematopoiesis in Pancrustacean Models 2 2.1 Insect Hematopoiesis 2 2.2 Crustacean Hematopoiesis 5 3 Molluscan Hematopoiesis 6 3.1 Bivalves 6 3.2 Gastropods 7 3.3 Cephalopods 8 4 Hematopoiesis in Pancrustacean and Molluscan Models: Final Considerations 9 5 Hemocytes in Pancrustacean and Molluscan Models 9 5.1 Hemocytes and Their Lineages in Insects 10 5.2 Hemocytes and Their Lineages in Crustaceans 15 5.3 Hemocytes and Their Lineages in Mollusks 17 6 Concluding Remarks 20 Acknowledgments 21 References 21 2. Origin and Functions of Tunicate Hemocytes Francesca Cima, Nicola Franchi, Loriano Ballarin 1 Introduction 29 2 Ascidian Circulation 30 3 Ascidian Hemocytes 31 3.1 Hematopoietic Tissues 31 3.2 Hemocyte Morphology 31 4 Immune Role of Tunicate Hemocytes 33 4.1 Phagocytosis 33 4.2 Encapsulation 34 4.3 Cytotoxicity 35 4.4 Inflammation 35 vii viii Contents 5 Humoral Factors Produced by Hemocytes 37 5.1 Phenoloxidase 37 5.2 Lectins 37 5.3 Cytokines 37 5.4 Complement 38 5.5 Antibacterial Activity 39 6 Ascidian Hemocytes and Oxidative Stress Response 40 7 Hemocytes of Pelagic Tunicates 40 8 Concluding Remarks 40 References 41 3. Lymphocyte Populations in Jawless Vertebrates: Insights Into the Origin and Evolution of Adaptive Immunity Yoichi Sutoh, Masanori Kasahara 1 Introduction 51 2 Overview of VLRS 52 2.1 Structure of VLR Proteins and Gene Assembly 52 2.2 Both Lampreys and Hagfish Have Three VLR Genes 54 2.3 Crystal Structure of VLR Proteins and Antigen Recognition 55 2.4 VLRA and VLRC Genes are Tightly Linked in the Lamprey Genome 56 3 Three Populations of Agnathan Lymphocytes 56 3.1 VLRA+ Cells and VLRC+ Cells Resemble Gnathostome T Cells, Whereas VLRB+ Cells Resemble Gnathostome B Cells 56 3.2 Antigen Recognition by Agnathan T-Like Cells is Still Full of Mystery 57 4 Lymphocyte Development in Jawless Vertebrates 59 4.1 Development of VLRB+ Cells 59 4.2 Development of VLRA+ Cells and VLRC+ Cells 59 4.3 Cell Fate Determination of VLRA+ Cells and VLRC+ Cells 61 4.4 Evidence for Selection in “Thymoids” 61 4.5 Evolution of Lymphocytes in Vertebrates 61 5 Conclusions 64 Acknowledgments 64 References 64 4. The Evolution of Lymphocytes in Ectothermic Gnathostomata Giuseppe Scapigliati, Francesco Buonocore 1 Introduction 69 2 Fishes 71 2.1 B Cells 72 2.2 T Cells 76 3 Conclusions 79 References 79 Contents ix 5. Vertebrate Cytokines and Their Evolution Christopher J Secombes, Tiehui Wang, Steve Bird 1 Introduction 87 2 The IL-1 Cytokine Family 87 2.1 Vertebrate IL-1F2 88 2.2 Vertebrate IL-1F4 92 2.3 Bird and Reptile IL-1F3 and IL-1F5 94 2.4 Novel Fish IL-1F 96 3 The IL-2 Cytokine Family (gC Cytokines) 96 3.1 IL-2 and IL-2L 96 3.2 IL-4 and IL-4/13 97 3.3 IL-7 98 3.4 IL-9 98 3.5 IL-15 and IL-15L 99 3.6 IL-21 99 4 IL-6/IL-12 Superfamily 100 4.1 IL-6 Family 101 4.2 The IL-12 Family 104 5 IL-10 Family 109 5.1 IL-22 109 5.2 IL-26 110 5.3 IL-10 110 5.4 vIL-10 112 6 IL-17 Family 112 7 TNF Family 116 7.1 Protostomian Invertebrates 116 7.2 Primitive Chordates and Basal Vertebrates: Cephalochordates, Urochordates, and Cyclostomata 118 7.3 Fish 119 7.4 Birds, Reptiles, and Amphibians 126 References 128 6. The Evolution of Complement System Functions and Pathways in Vertebrates Miki Nakao, Tomonori Somamoto 1 Introduction 151 2 Invertebrate Complement System Representing an Ancestral Architecture of Vertebrate System 153 3 Phylogeny of Complement Pathways 154 3.1 Lectin Pathway 154 3.2 Alternative Pathway 159 3.3 Classical Pathway 160 3.4 Lytic Pathway 161 4 Phylogeny of Complement Receptors 162 5 Phylogeny of the Regulatory Mechanism of Complement Activation 163 x Contents 6 Evolutionary Significance of Multiple Isoforms in Teleost Complement Components 164 7 Concluding Remarks 166 Acknowledgments 167 References 167 7. Antiviral Immunity: Origin and Evolution in Vertebrates Jun Zou, Rosario Castro, Carolina Tafalla 1 Introduction 173 2 Virus-Sensing Pattern Recognition Receptors 174 2.1 Toll-Like Receptor Family 175 2.2 RIG-Like Receptor Family 178 2.3 NOD-Like Receptor Family 179 3 RNA Interference 180 4 Type I IFNs 181 4.1 Mammalian IFNs 181 4.2 Avian and Reptile Type I IFNs 184 4.3 Amphibian IFNs 184 4.4 Fish IFNs 185 5 IFN Receptors 187 6 Downstream Modulators of the Interferon Response 188 6.1 Mx Protein 189 6.2 Viperin 190 6.3 PKR 190 6.4 ISG15 191 6.5 TRIM 191 7 Conclusions 192 Acknowledgments 192 References 193 8. Lectins as Innate Immune Recognition Factors: Structural, Functional, and Evolutionary Aspects Gerardo R. Vasta 1 Introduction 205 2 Galectins: A Conserved Lectin Family with Multiple Roles in Development and Immunity 207 2.1 Molecular, Structural, and Evolutionary Aspects 208 2.2 Functional Aspects 210 3 F-type Lectins: A Structurally and Functionally Diversified Lectin Family 213 3.1 Molecular, Structural, and Evolutionary Aspects 213 3.2 Functional Aspects 217 4 Conclusions 218 Acknowledgments 219 References 219 Contents xi 9. Origin and Evolution of the Neuro-Immune Cross-Talk in Immunity Enzo Ottaviani 1 Introduction 225 1.1 Lymphocyte as a Neuroendocrine Cell 226 1.2 Immunocyte as an Immune–Neuroendocrine Cell 227 2 Role of Neuroendocrine Hormones, Opioid Peptides and Cytokines in the Invertebrate Immune and Neuroendocrine (Stress Response) Responses 229 2.1 Immune Responses 229 2.2 Cell-Shape Changes 230 2.3 Chemotaxis 230 2.4 Pagocytosis 231 2.5 Stress Response 231 2.6 The Immune–Mobile Brain 233 3 Concluding Remarks 234 References 234 10. The Immune-Related Roles and the Evolutionary History of Dscam in Arthropods Sophie A.O. Armitage, Daniela Brites 1 The Down Syndrome Cell Adhesion Molecule 241 1.1 From One Gene to Thousands of Protein Isoforms 242 1.2 Structural Aspects of Dscam 242 2 Immune-Related Roles of Dscam-HV in Arthropods 244 2.1 What Is the Evidence That Dscam-hv is Involved in the Immune defence of Pancrustaceans? 244 2.2 How Has Dscam-hv Been Predicted to Function in Arthropod Immunity? 257 3 The Evolutionary History of Dscam-HV in Arthropods 260 3.1 The Origin of Dscam 260 3.2 Dscam Radiation in Arthropods 262 3.3 The Evolutionary History of Dscam-hv in Pancrustaceans 264 3.4 Dscam Clusters of Duplicated Exons 265 3.5 Are the Patterns of Dscam-hv Molecular Evolution Compatible with a Role in Immunity? 266 4 Experimental Methodology and Future Perspectives 267 4.1 Experimental Methodology: Choice of Experimental Host and Parasite/Antigen, and Other Experimental Parameters 267 4.2 Future Perspectives 268 5 Concluding Remarks 269 Acknowledgments 269 References 269 xii Contents 11.