LYSOPHOSPHOLIPID RECEPTORS LYSOPHOSPHOLIPID RECEPTORS Signaling and Biochemistry Edited by JEROLD CHUN TIMOTHY HLA SARA SPIEGEL WOUTER MOOLENAAR Copyright © 2013 by John Wiley & Sons, Inc. All rights reserved Published by John Wiley & Sons, Inc., Hoboken, New Jersey Published simultaneously in Canada No part of this publication may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, scanning, or otherwise, except as permitted under Section 107 or 108 of the 1976 United States Copyright Act, without either the prior written permission of the Publisher, or authorization through payment of the appropriate per-copy fee to the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, (978) 750-8400, fax (978) 750-4470, or on the web at www.copyright.com. 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Receptors, Lysophospholipid– metabolism. 3. Signal Transduction–physiology. QU 55.7] 571.7'4–dc23 2012045178 Printed in the United States of America 10 9 8 7 6 5 4 3 2 1 CONTENTS PREFACE ix CONTRIBUTORS xi 1 LYSOPHOSPHATIDIC ACID (LPA) RECEPTOR SIGNALING 1 Hope Mirendil, Mu-En Lin, and Jerold Chun 2 SPHINGOSINE 1-PHOSPHATE (S1P) RECEPTORS 41 Bongnam Jung and Timothy Hla 3 GLOBAL GENE EXPRESSION PROGRAM OF LYSOPHOSPHATIDIC ACID (LPA)-STIMULATED FIBROBLASTS 61 Catelijne Stortelers and Wouter H. Moolenaar 4 IDENTIFICATION OF DIRECT INTRACELLULAR TARGETS OF SPHINGOSINE 1-PHOSPHATE (S1P) 71 Nitai C. Hait, Sheldon Milstien, and Sarah Spiegel 5 LYSOPHOSPHOLIPID RECEPTOR SIGNALING PLATFORMS: THE RECEPTOR TYROSINE KINASE–G PROTEIN-COUPLED RECEPTOR SIGNALING COMPLEX 85 Nigel J. Pyne and Susan Pyne 6 AUTOTAXIN: A UNIQUE ECTO-TYPE PYROPHOSPHODIESTERASE WITH DIVERSE FUNCTIONS 103 Hiroshi Yukiura and Junken Aoki v vi CONTENTS 7 STUDIES ON AUTOTAXIN SIGNALING IN ENDOCYTIC VESICLE BIOGENESIS AND EMBRYONIC DEVELOPMENT USING WHOLE EMBRYO CULTURE AND ELECTROPORATION 121 Masayuki Masu, Seiichi Koike, Takuya Okada, and Kazuko Keino-Masu 8 STANDARDIZATION AND QUANTIFICATION OF LYSOPHOSPHATIDIC ACID COMPOUNDS BY NORMAL-PHASE AND REVERSED-PHASE CHROMATOGRAPHY–TANDEM MASS SPECTROMETRY 137 Jeff D. Moore, Shengrong Li, David S. Myers, Stephen B. Milne, H. Alex Brown, and Walter A. Shaw 9 SPHINGOSINE KINASES: BIOCHEMISTRY, REGULATION, AND ROLES 153 Melissa R. Pitman, Kate E. Jarman, Tamara M. Leclercq, Duyen H. Pham, and Stuart M. Pitson 10 FUNCTIONAL AND PHYSIOLOGICAL ROLES OF SPHINGOSINE 1-PHOSPHATE TRANSPORTERS 185 Atsuo Kawahara and Tsuyoshi Nishi 11 LIPID PHOSPHATE PHOSPHATASES AND SIGNALING BY LYSOPHOSPHOLIPID RECEPTORS 201 Ganesh Venkatraman and David N. Brindley 12 LIPID PHOSPHATE PHOSPHATASES: RECENT PROGRESS AND ASSAY METHODS 229 Andrew J. Morris, Susan S. Smyth, Abdel K. Salous, and Andrew D. Renault 13 LYSOPHOSPHATIDIC ACID (LPA) SIGNALING AND CARDIOVASCULAR PATHOLOGY 265 Susan S. Smyth, Anping Dong, Jessica Wheeler, Manikandan Panchatcharam, and Andrew J. Morris 14 SPHINGOSINE 1-PHOSPHATE (S1P) SIGNALING IN CARDIOVASCULAR PHYSIOLOGY AND DISEASE 283 Bodo Levkau 15 SPHINGOSINE 1-PHOSPHATE (S1P) SIGNALING AND THE VASCULATURE 313 Christian Waeber 16 REGULATION OF THE NUCLEAR HORMONE RECEPTOR PPARγ BY ENDOGENOUS LYSOPHOSPHATIDIC ACIDS (LPAS) 349 Ryoko Tsukahara, Tamotsu Tsukahara, and Gabor Tigyi CONTENTS vii 17 MECHANISMS AND MODELS FOR ELUCIDATING THE CARDIAC EFFECTS OF SPHINGOSINE 1-PHOSPHATE (S1P) 373 Shigeki Miyamoto, Sunny Yang Xiang, Nicole H. Purcell, and Joan Heller Brown 18 NEURAL EFFECTS OF LYSOPHOSPHATIDIC ACID (LPA) SIGNALING 399 Nobuyuki Fukushima 19 WIDESPREAD EXPRESSION OF SPHINGOSINE KINASES AND SPHINGOSINE 1-PHOSPHATE (S1P) LYASE SUGGESTS DIVERSE FUNCTIONS IN THE VERTEBRATE NERVOUS SYSTEM 419 H. Meng and V.M. Lee 20 LYSOPHOSPHATIDIC ACID AND NEUROPATHIC PAIN: DEMYELINATION AND LPA BIOSYNTHESIS 433 Hiroshi Ueda 21 ROLE OF LYSOPHOSPHATIDIC ACID (LPA) IN BEHAVIORAL PROCESSES: IMPLICATIONS FOR PSYCHIATRIC DISORDERS 451 Guillermo Estivill-Torrús, Luis Javier Santín, Carmen Pedraza, Estela Castilla-Ortega, and Fernando Rodríguez de Fonseca 22 SPHINGOSINE 1-PHOSPHATE (S1P) SIGNALING AND LYMPHOCYTE EGRESS 475 Alejandra Mendoza, Lauren A. Pitt, and Susan R. Schwab 23 BIOLOGY REVEALED BY SPHINGOSINE 1-PHOSPHATE (S1P) RECEPTOR GENE-ALTERED MICE 489 Maria L. Allende, Mari Kono, Aikaterini Alexaki, Christina Giannouli, Jiman Kang, Catherine C. Theisen, Eleanor L. Koerner, and Richard L. Proia 24 ROLE OF LYSOPHOSPHATIDIC ACID (LPA) IN THE INTESTINE 507 C. Chris Yun and Peijian He 25 LYSOPHOSPHOLIPID SIGNALING IN FEMALE AND MALE REPRODUCTIVE SYSTEMS 529 Xiaoqin Ye 26 THE GONADS AND THEIR MAGIC BULLET, LYSOPHOSPHATIDIC ACID: PHYSIOLOGICAL AND TOXICOLOGICAL FUNCTIONS OF LYSOPHOSPHATIDIC ACID (LPA) IN FEMALE AND MALE REPRODUCTIVE SYSTEMS 569 Lygia Therese Budnik, Bärbel Brunswig-Spickenheier, and Dieter Müller viii CONTENTS 27 LYSOPHOSPHOLIPID REGULATION OF LUNG FIBROSIS 587 Barry S. Shea and Andrew M. Tager 28 LYSOPHOSPHATIDIC ACID (LPA) SIGNALING AND BONE 609 Jean Pierre Salles, Sara Laurencin-Dalicieux, Françoise Conte-Auriol, Fabienne Briand-Mésange, and Isabelle Gennero 29 LYSOPHOSPHATIDIC ACID (LPA) SIGNALING AND BONE CANCER 627 Olivier Peyruchaud, Marion David, Timothy L. Macdonald, and Kevin R. Lynch 30 UNDERSTANDING THE FUNCTIONS OF LYSOPHOSPHATIDIC ACID RECEPTORS IN CANCER 641 Nattapon Panupinthu and Gordon B. Mills 31 LYSOPHOSPHATIDIC ACID RECEPTORS IN CANCER 661 Abir Mukherjee, Jinhua Wu, Yongling Gong, and Xianjun Fang 32 LPA RECEPTOR SUBTYPES LPA AND LPA 1 2 AS POTENTIAL DRUG TARGETS 681 Gretchen Bain and T. Jon Seiders 33 CLINICAL INTRODUCTION OF LYSOPHOSPHATIDIC ACID (LPA) AND AUTOTAXIN ASSAYS 709 Yutaka Yatomi, Koji Igarashi, Kazuhiro Nakamura, Ryunosuke Ohkawa, Akiko Masuda, Akiko Suzuki, Tatsuya Kishimoto, Hitoshi Ikeda, and Junken Aoki 34 ANTIBODIES TO BIOACTIVE LYSOPHOSPHOLIPIDS 737 Roger A. Sabbadini, Jonathan M. Wojciak, Kelli Moreno, James S. Swaney, and Barbara Visentin INDEX 753 PREFACE Lysophospholipids are simple phospholipids that arise from cell membranes and related compartments. They are epitomized by two well-known species, lysophosphatidic acid (LPA) and sphingosine 1-phosphate (S1P). Studies on these lipids have shown a dramatic increase in number, from comparatively rare reports before the 1990s to what is now a vibrant and expansive scientific literature encompassing thousands of publications that range from fundamen- tal lipid biochemistry and cell signaling to physiologies and pathophysiologies of virtually every organ system. A galvanizing event for this field’s expansion was the discovery of related cell surface G protein-coupled receptors (GPCRs) for LPA and S1P, which served to bring together scientists from many different areas. This book grew out of a desire to capture the dynamism of this field, representing both a snapshot of current knowledge as well as a single source of information for backgrounds, techniques, and literature references that encompass the current field of lysophospholipid signaling. The book can be considered to have two parts, the first covering receptors and enzymes (Chapters 1–12), and the second covering physiology and patho- physiology (Chapters 13–34). Efforts have been made, where feasible, to pair themes common to LPA and S1P signaling, such as the receptors themselves or cardiovascular effects, in an effort to provide readers new to the field with a sampling of themes from both lipids. Complementing elements common to both lipids, such as degradative pathways mediated by lipid phosphate phos- phatases, are noted, as well as distinguishing features that could provide a basis for molecular selectivity. The comprehensive index will aid access to specific topics, including methodologies. The depth and breadth of the lysophospholipid signaling field precludes an all-encompassing treatment, and the reader is encouraged to use the pro- vided chapters as a starting point to explore the primary literature for more ix x    PREFACE thorough and timely reports. All scientific fields contain controversies and inconsistencies that are also represented within this book; rather than enforce a single viewpoint, the decision was made to provide balance with alternative views, the validity of which awaits independent study, as seen in some non- GPCR lysophospholipid mechanisms, or physiological mechanisms of lipid- targeted antisera. That said, the richness of possibilities as well as emerging data from the primary literature represent a prime example of the field’s activ- ity and dynamism. As important, the decision was made to leave out areas that have been superbly and extensively treated in recent reviews. A key example is the FDA approval of fingolimod—known in the scientific literature as FTY720 and com- mercially as Gilenya™ (Novartis AG, Basel) as the first oral treatment for relaps- ing forms of multiple sclerosis. Now approved worldwide, fingolimod is phosphorylated to become a non-selective S1P receptor modulator and repre- sents the first compound targeting lysophospholipid receptors that has become a human medicine. Basic mechanisms relevant to fingolimod’s activity are, however, discussed in receptor and immunology chapters, and examples can be found in the index. Other recent areas without representation include the struc- tural biology of lysophospholipid GPCRs, particularly the S1P receptor S1P, as 1 well as emerging data on newly identified lysophospholipid GPCRs for other lysophospholipid species, particularly lysophosphatidyl serine and lysophospha- tidyl inositol. These topics represent areas for any future iteration of this book. The myriad details and logistical challenges of creating this book required the efforts of many, who deserve both credit and thanks. First, this project required the efforts and vision of all of the contributors, who are integral members of the larger community of scientists whose work involves lysophos- pholipid signaling. Many of us were brought together through the biennial FASEB Summer Research Conferences as well as other venues such as Key- stone Symposia or the ASBMB meetings; we were the organizers and sponsors of these important gatherings. Second, easily an equal number of other poten- tial authors could have written chapters, and we thank them for both their willingness to contribute and apologize for not being able include so many worthy authors because of time and space constraints. Third, the tireless and painstaking efforts of Danielle Letourneau deserve special kudos, as she juggled every phase of this project while still handling the many demands of an active laboratory. This book would not exist without her. Fourth, we thank Anita Lekhwani, Kris Parrish, Cecilia Tsai, and all of their staff at John Wiley for their interest and infinite patience in the many—at times very slow—steps toward completing this project, particularly during Hurricane Sandy with its flooding and power outages in Hoboken and New York. Finally, we thank you, the reader, for your interest and future contributions to this growing field, and hope that this book provides you with useful and stimulating information that will lead to new scientific and medical advances through the field of lysophos- pholipid signaling. Jerold Chun La Jolla, California CONTRIBUTORS Aikaterini Alexaki, Genetics of Development and Disease Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Insti- tutes of Health, Bethesda, MD Maria L. Allende, Genetics of Development and Disease Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Insti- tutes of Health, Bethesda, MD Junken Aoki, Department of Molecular and Cellular Biochemistry, Graduate School of Pharmaceutical Sciences, Tohoku University, Miyagi, Japan Gretchen Bain, Amira Pharmaceuticals, Bristol-Myers Squibb, San Diego, CA Fabienne Briand-Mésange, Molecular Signaling in Diseases of Growth, Osteogenesis and Osteolysis, Biotherapy, INSERM UMR 1043, CNRS U5282, Université Toulouse III – Paul Sabatier, Centre de Physiopathologie de Toulouse Purpan (CPTP), Toulouse, France David N. Brindley, Signal Transduction Research Group, Department of Bio- chemistry, School of Translational Medicine, University of Alberta, Edmon- ton, Alberta, Canada H. Alex Brown, Department of Pharmacology, Vanderbilt University Medical Center, Nashville, TN Joan Heller Brown, Department of Pharmacology, University of California, San Diego, CA xi