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Immunobiology of the SHARK Frontispiece A shark bleed. 1. Netting a captive shark from the sea water channel. 2. Shark in anesthe­ tizing tank. 3. Bleeding the anesthetized shark. 4. Blood withdrawn from the caudal sinus. 5. Recovered shark ready to return to the water. 6. Shark back in the channel. (Photographs courtesy of the Smith Collection.) Immunobiology of the SHARK EDITED BY Sylvia L. Smith Department of Biological Sciences Florida International University Robert B. Sim Department of Pharmacology University of Oxford Martin F. Flajnik Department of Microbiology and Immunology University of Maryland at Baltimore Boca Raton London New York CRC Press is an imprint of the Taylor & Francis Group, an informa business Front cover: Image of nurse shark. Photo copyright Max Telford. Used with permission. All rights reserved. CRC Press Taylor & Francis Group 6000 Broken Sound Parkway NW, Suite 300 Boca Raton, FL 33487-2742 © 2015 by Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, an Informa business No claim to original U.S. Government works Printed on acid-free paper Version Date: 20141015 International Standard Book Number-13: 978-1-4665-9574-3 (Hardback) This book contains information obtained from authentic and highly regarded sources. Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the valid- ity of all materials or the consequences of their use. The authors and publishers have attempted to trace the copyright holders of all material reproduced in this publication and apologize to copyright holders if permission to publish in this form has not been obtained. If any copyright material has not been acknowledged please write and let us know so we may rectify in any future reprint. ExceptThe Open as permitted Access version under U.S.of this Copyright book, available Law, no atpart www.taylorfrancis.com, of this book may be reprinted, has been reproduced,made available transmitted, under a Creativeor uti- Commons Attribution-Non Commercial-No Derivatives 4.0 license. publishers.Trademark Notice: Product or corporate names may be trademarks or registered trademarks, and are used only for identification and explanation without intent to infringe. 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Syfuia .f!u&m (!iltpleJt) Smitii 2()14 (!iltpleJt) Smitii Contents Foreword ...........................................................................................................................................ix Preface...............................................................................................................................................xi Acknowledgments .......................................................................................................................... xiii Editors ..............................................................................................................................................xv Contributors ...................................................................................................................................xvii Chapter 1 The Diversity and Natural History of Chondrichthyan Fishes ..........................................................1 Gregor M. Cailliet and David A. Ebert Chapter 2 Athena and the Evolution of Adaptive Immunity ............................................................................29 Helen Dooley Chapter 3 Shark Reproduction, Immune System Development and Maturation: A Review ........................... 51 Lynn L. Rumfelt Chapter 4 Sites of Immune Cell Production in Elasmobranch Fishes: Lymphomyeloid Tissues and Organs .... 79 Carl A. Luer, Catherine J. Walsh, and A.B. Bodine Chapter 5 Elasmobranch Blood Cells ...............................................................................................................89 Ashley N. Haines and Jill E. Arnold Chapter 6 Leukocyte Function in Elasmobranch Species: Phagocytosis, Chemotaxis, and Cytotoxicity ..... 105 Catherine J. Walsh and Carl A. Luer Chapter 7 Cytokines of Cartilaginous Fish .................................................................................................... 123 C.J. Secombes, J. Zou, and S. Bird Chapter 8 Shark Complement: Genes, Proteins and Function ....................................................................... 143 Sylvia L. Smith and Masaru Nonaka vii viii CONTENTS Chapter 9 MHC Molecules of Cartilaginous Fishes ...................................................................................... 173 Simona Bartl and Masaru Nonaka Chapter 10 Considering V(D)J Recombination in the Shark ........................................................................... 199 Ellen Hsu Chapter 11 Shark Immunoglobulin Light Chains ............................................................................................ 221 Michael F. Criscitiello Chapter 12 Shark T-Cell Receptors ..................................................................................................................237 Michael F. Criscitiello Chapter 13 The Shark-Family (Cartilaginous Fish) Immunogenome ..............................................................249 Byrappa Venkatesh and Yuko Ohta Chapter 14 In Vitro Culture of Elasmobranch Cells ........................................................................................ 255 Catherine J. Walsh and Carl A. Luer Chapter 15 Antimicrobial Molecules of Sharks and Other Elasmobranchs: A Review................................... 267 Nichole Hinds Vaughan and Sylvia L. Smith Chapter 16 Shark-Derived Immunomodulators ...............................................................................................287 Liza Merly and Sylvia L. Smith Index ..............................................................................................................................................303 Foreword With the possible exception of the giant panda, perhaps no other animal has captured the interest of the general public as the shark. As general biologists, we recognize the cartilaginous fishes, such as sharks, skates, rays, and the Chimera, of which ratfish represent an extant form, to be the living representatives of a distant major radiation in the phylogenetic development of the vertebrate form. As such, this fascinating group potentially holds clues to understanding basic biological processes whose underlying genetic bases have been obscured during the passage of evolutionary time. As immunologists, we recognize the cartilaginous fishes to be the most phylogenetically distant group of species from man that possess an adaptive immune system in which immunoglobulin and T-cell antigen receptors function as mediators of humoral and cellular immunity. Intensive studies of immunity in the cartilaginous fish over the past three decades have resulted in remarkable discover­ ies that have contributed much to our understanding of how the highly complex immune system of the vertebrates has evolved. Immunobiology of the Shark is a comprehensive resource for immunologists, evolutionary biologists, and other scientists interested in understanding how the integration of cellular and humoral processes has created a highly effective survival mechanism. This volume incorporates a rich, diverse literature into a well-reasoned, comprehensive package that will permit the reader to understand topics as diverse as the placement of the shark in phylogeny, the uniqueness of its physiology, and the mechanisms regulating how the rearranging immune genes make the somatic immune cell a selectable unit. An exceptional number of findings are described that are of immedi­ ate relevance to understanding immune regulation in the far more widely studied immune systems of man and mouse. The fundamental differences that exist between lymphoid architecture in car­ tilaginous fish and “higher” vertebrates, which create distinct microenvironments for immune cell differentiation and maturation, are the primary topics of several chapters. In addition to the unique adaptations characteristic of some components of immunity in the shark, other aspects of immunity closely resemble those seen in the higher vertebrates, presenting a remarkable story of evolutionary variation and stability. This volume is particularly notable in the diversity of approaches that were employed to study the immunobiology of the shark, ranging from basic microscopic observations to detailed genome annotation. A series of fascinating questions are raised throughout this volume that can be addressed experimentally with today’s technology. If one message rings true, it is that alternative animal model systems, such as sharks and their relatives, are critical to our understand­ ing of the scope of evolutionary change and the mechanisms underlying variation. Immunobiology of the Shark will prove to be an invaluable resource as well as guide for future investigations of how

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