NEUROBIOLOGY OF ESSENTIAL FATTY ACIDS ADVANCES IN EXPERIMENTAL MEDICINE AND BIOLOGY Editorial Board: NATHAN BACK, State University of New York at Buffalo IRUN R. COHEN, The Weizmann Institute of Science DAVID KRITCHEVSKY, Wistar Institute ABEL LAJTHA, N.S. Kline Institute for Psychiatric Research RODOLFO PAOLETTI, University of Milan Recent Volumes in this Series Volume 310 IMMUNOLOGY OF MILK AND THE NEONATE Edited by Jiri Mestecky, Claudia Blair, and Pearay L. Ogra Volume 311 EXCITATION-CONTRACTION COUPLING IN SKELETAL, CARDIAC, AND SMOOTH MUSCLE Edited by George B. Frank, C. Paul Bianchi, and Henk E. D. J. ter Keurs Volume 312 INNOVATIONS IN ANTIVIRAL DEVELOPMENT AND THE DETECTION OF VIRUS INFECTIONS Edited by Timothy M. Block, Donald Jungkind, Richard Crowell, Mark Denison, and Lori R. Walsh Volume 313 HEPARIN AND RELATED POLYSACCHARIDES Edited by David A. Lane, Ingemar Björk, and Ulf Lindahl Volume 314 CELL-CELL INTERACTIONS IN THE RELEASE OF INFLAMMATORY MEDIATORS: Eicosanoids, Cytokines, and Adhesion Edited by Patrick Y-K Wong and Charles N. Serhan Volume 315 TAURINE: Nutritional Value and Mechanisms of Action Edited by John B. Lombardini, Stephen W. Schaffer, and Junichi Azuma Volume 316 OXYGEN TRANSPORT TO TISSUE XIII Edited by Michael McCabe, Thomas K. Goldstick, and David Maguire Volume 317 OXYGEN TRANSPORT TO TISSUE XIV Edited by Wilhelm Erdmann and Duane F. Bruley Volume 318 NEUROBIOLOGY OF ESSENTIAL FATTY ACIDS Edited by Nicolas G. Bazan, Mary G. Murphy, and Gino Toffano A Continuation Order Plan is available for this series. A continuation order will bring delivery of each new volume immediately upon publication. Volumes are billed only upon actual shipment. For further information please contact the publisher. NEUROBIOLOGY OF ESSENTIAL FATTY ACIDS Edited by Nicolas G. Bazan Louisiana State University Eye Center and . Neuroscience Center Louisiana State University School of Medicine New Orleans, Louisiana Mary G. Murphy Dalhousie University Halifax, Nova Scotia, Canada and Gino Toffano FIDIA Research Laboratories Abano Terme, Italy SPRINGER SCIENCE+BUSINESS MEDIA, LLC Library of Congress Catalog 1ng-1n-Pub11cat1on Data Neurobiology of essential fatty adds / edited by Nicolas G. Bazan, Mary G. Murphy, and G1no Toffano. p. cm. — (Advances 1n experimental medicine and biology ; v. 318) "Proceedings of a symposium on the neurobiology of essential fatty acids, held July 10-12, 1991, in Palm Cove, Far North Queensland, Australia"—T.p. verso. Includes bibliographical references and Index. ISBN 978-1-4613-6515-0 ISBN 978-1-4615-3426-6 (eBook) DOI 10.1007/978-1-4615-3426-6 1. Essential fatty acids—Physiological effect—Congresses. 2. Neurochemistry—Congresses. 3. Second messengers (Biochemistry)- -Congresses. 4. Cellular signal transduction—Congresses. 1. Bazan, Nicolas G. II. Murphy, Mary G. III. Toffano, G. IV. Series. [DNLM: 1. Fatty Acids, Essential—physiology—congresses. 2. Second Messenger Systems—congresses. W1 AD559 v.318 / QU 90 N494 1991] QP752.E84N48 1992 612.8'042--dc20 DNLM/DLC for Library of Congress 92-16989 CIP Proceedings of a symposium on the Neurobiology of Essential Fatty Acids, held July 10-12, 1991, in Palm Cove, Far North Queensland, Australia ISBN 978-1-4613-6515-0 © 1992 Springer Science+Business Media New York Originally published by Plenum Press, New York in 1992 Softcover reprint of the hardcover 1st edition 1992 All rights reserved No part of this book may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording, or otherwise, without written permission from the Publisher PREFACE It is increasingly evident that polyunsaturated fatty acids (PUFA), which in the past were often believed to be mere components of cellular membranes of neural tissue, are actually major determinants of the functional properties of neural cells and are intimately involved in brain disease processes. The two families of PUFA , which are derived from the essential polyenes, linoleic (18:2<0>6) and a-linolenic (18:3<0>3) acids, constitute a major proportion (-30%) of the total fatty acids esterified to brain phospholipids. Each family is distributed in membranes in a highly specific manner with respect to brain region, cell type, and position within each of the phosphoglycerides. Unlike their behavior in other organs, the PUFA components of brain turn over slowly and are relatively resistant to dietary modification. Their unique distribution and stability suggest that they play an important role in determining the functional properties of neural cells. However, until recently very little was known regarding the precise nature of their involvement. A great deal of excitement has been generated by the increasing realization that PUFA and phospholipids play integral roles in transmission of signals across neural membranes. PUFA, and particularly arachidonic acid (AA), can act as second messen gers per se, or as substrates for synthesis of eicosanoids (e.g., prostaglandins, 12-lipoxy genase products) that fulfill this function. Release of PUFA from parent phospholipids, such as phosphatidyIcholine and phosphatidylinositol, involves the concerted actions of various lipases, including phospholipase A2 and C, and diacylglycerol lipase. Each of these appears to be distinct with respect to its substrate requirements and sensitivity to inhibitors. A variety of cell-surface receptors are now known to use PUFA or their derivatives as second messengers. In response to inhibitory transmitters such as FRMFa or dopa mine, AA is released from Aplysia sensory neurons and 12-HPETE, and related bioactive products are produced. This triggers increased opening ofK+ channels, hyper polarization of sensory neurons, and a consequent reduction in activity in the post synaptic motor cell. By comparison, stimulation of NMDA-type glutamate receptors results in release of free AA (and perhaps other PUFA), which appears to be associated directly with inhibition of glutamate uptake into neurons and astrocytes. Depolarization of hippocampal mossy fibers also involves release of AA which is related to stimulation of the glutamate receptors that play a central role in the development of long-term potentiation. It is reasonable to assume that PUFA are intimately involved in this phenomenon. Independent of their roles as specific messengers for signal transduction, fatty acids and phospholipids modulate cell functions through interactions with functional proteins. Considerable excitement has been generated from observations that unsaturated fatty acids act synergistically with diacylglycerol (DAG) to activate species of protein kinase C (PKC), even at basal levels of Ca2+, and may thereby provide a mechanism for y sustained cross-talk between receptors. Other studies are using molecular biological ap proaches to identify specific regions of lipid-PKC interactions. It has been known for some time that acute pathological events, such as ischemia, epileptic seizures, hypoglycemic coma, and trauma, trigger phospholipase activation and accumulation of free PUFA (particularly arachidonic and docosahexaenoic acids) and other potential second messengers (e.g., DAG, IP3 ' eicosanoids). Possible consequences of these events include uncontrolled receptor and/or enzyme activation, loss of ionic (e.g., Ca2+) homeostasis, and lipid peroxidation. Another product of phospholipid remodeling, and a relative newcomer in lipid neuropathology, is the alkyl-acetyl phospholipid, platelet-activating factor (PA F). P AF produced in response to ischemic injury appears to exert its deleterious effects through actions at synaptic membranes, with possible involvement of excitatory amino acids. However, it is now evident that P AF also acts at intracellular receptors where it stimulates expression of immediate early genes, including c{os and c-jun. These rapid but brief genomic responses can be linked with long-term transcriptional changes and, in this manner, can provide a mechanism for the neuronal plasticity that is required for repair processes. Such a mechanism may also be involved in the phenomenon of long-term potentiation. This book summarizes the results of a Satellite Symposium, "The Neurobiology of Essential Fatty Acids," that was held in Palm Cove, Far North Queensland, Australia, in July, 1991. The conference was generously supported by the Fidia Research Founda tion. The purpose of the symposium was to discuss exciting recent developments concerning the dynamic involvement of fatty acids and phospholipids both in nervous system function and in disease processes. The topics spanned a variety of research interests including the molecular biology of enzyme and gene regulation, physiological and pharmacological aspects of lipid metabolism, mechanisms of biological signal transduction (and possible behavioral relationships), as well as the molecular mechan isms of cerebral ischemia, convulsive disorders, and inborn errors of fatty-acid catabolism. We were particularly pleased to have some newcomers in the group. It is largely through this interdisciplinary approach that we are able to gain new perspectives and to fully appreciate the many challenges that lie ahead. This is certainly one of the most exciting scientific research fields of our time. We are grateful to the Fidia Research Foundation for providing the financial support that made the symposium possible and to Ms. Oriana Casadei, the meeting's manager. Many thanks also to Ms. Paula Gebhardt for her expert and patient editorial assistance in the production of this book. And, of course, we are grateful to the speakers and other participants who contributed their efforts to make this symposium so valuable. Nicolas G. Bazan Mary G. Murphy Gino Toffano \II CONTENTS PHOSPHOLIPASES A2: PROPERTIES AND MODUlATION THE INDUCfION OF CELLULAR GROUP II PHOSPHOLIPASE A2 BY CYTOKINES AND ITS PREVENTION BY DEXAMETHASONE ............. . . . . . . . . . . . . . . . . . . . . . .. 1 H. van den Bosch, C. Schalkwijk, J. Pfeilschifter, and F. Marki BRAIN PHOSPHOLIPA SES AND THEIR ROLE IN SIGNAL TRANSDUCfION . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. 11 Akhlaq A. Farooqui, Yutaka Hirashima, and Lloyd A. Horrocks CHARACTERISTICS AND POSSIBLE FUNCfIONS OF MAST CELL PHOSPHOLIPA SES A2 . . . . . . . . . . . . . . . . . . . . . .. 27 Makoto Murakami, Ichiro Kudo, and Keizo Inoue EXTRACELLULAR PHOSPHOLIPASE A2 . . . . . . . . . . . . . . . . . . . . . . . . .. 35 Edward A. Dennis, Raymond A. Deems, and Lin Yu ISCHEMIC BRAIN DAMAGE: FOCUS ON LIPIDS AND LIPID MEDIATORS . . . . . . . . . . . . . . . . .. 41 Bo K. Siesjo and Kenichiro Katsura CELL SIGNALING AND ESSENTIAL FATlY ACIDS: CROSS-TALK BE1WEEN RECEPTORS AND MESSENGERS RECIPROCAL REGULATION OF FArry ACID RELEASE IN THE BRAIN BY GABA AND GLUTAMATE. . . . . . . . . . . . . . . .. 57 Dale L. Birkle NMDA RECEPTOR-MEDIATED ARACHIDONIC ACID RELEASE IN NEURONS: ROLE IN SIGNAL TRANSDUCfION AND PATHOLOGICAL ASPECfS ........................... 73 Jerzy W. Lazarewicz, E. Salinska, and J.T. Wroblewski NON-EICOSANOID FUNCfIONS OF ESSENTIAL FArry ACIDS: REGULATION OF ADENOSINE-RELATED FUNCfIONS IN CULTURED NEUROBLASTOMA CELLS . . . . . . . . . . . . . . . . . .. 91 Mary G. Murphy and Zenobia Byczko vii CONTRIBUTIONS TO ARACHIDONIC ACID RELEASE IN MOUSE CEREBRUM BY THE PHOSPHOINOSITIDE- PHOSPHOLIPASE C AND PHOSPHOLIPASE A2 PATHWAyS ..... 103 Grace Y. Sun MODULATION OF ARACHIDONIC ACID METABOLISM IN CULTURED RAT ASTROGLIAL CELLS BY LONG-CHAIN N-3 FATTY ACIDS ........................ 115 C. Galli, F. Marangoni, and A Petroni MODULATION OF GLUTAMATE RELEASE FROM HIPPOCAMPAL MOSSY FIBER NERVE ENDINGS BY ARACHIDONIC ACID AND EICOSANOIDS ................ 121 RV. Dorman, T.F.R Hamm, D.S. Damron, and E.J. Freeman METABOTROPIC GLUTAMATE RECEPTORS AND NEURONAL TOXICITY ............................... 137 G. Aleppo, A Pisani, A Copani, V. Bruno, E. Aronica, V. D'Agata, P.L. Canonico, and F. Nicoletti METABOLITES OF ESSENTIAL FATTY ACIDS AND OTHER MEMBRANE-DERIVED SECOND MESSENGERS IN CELL SIGNALING A ROLE FOR THE ARACHIDONIC ACID CASCADE IN FAST SYNAPTIC MODULATION: ION CHANNELS AND TRANSMITTER UPTAKE SYSTEMS AS TARGET PROTEINS ..... 147 A Volterra, D. Trotti, P. Cassutti, C. Tromba, R Galimberti, P. Lecchi, and G. Racagni APLYSIA CALIFORNlCA CONTAINS A NOVEL 12-LIPOXYGENASE WHICH GENERATES BIOLOGICALLY ACTIVE PRODUCTS FROM ARACHIDONIC ACID ............................... 159 Steven J. Feinmark, Douglas J. Steel, Anoopkumar Thekkuveettil, Mayumi Abe, Xiang-Duan Li, and James H. Schwartz ESSENTIAL FATTY ACID DEFICIENCY IN CULTURED SK-N-SH HUMAN NEUROBLASTOMA CELLS ........................ 171 E.B. Stubbs, Jr., RO. Carlson, C. Lee, S.K. Fisher, AK. Hajra, and B.W. Agranoff PHOSPHOLIPID METABOLISM AND SECOND MESSENGER SYSTEM AFTER BRAIN ISCHEMIA ......................... 183 Koji Abe, Tsutomu Araki, Jun-ichi Kawagoe, Masashi Aoki, and Kyuya Kogure DIETARY SUPPLY OF ESSENTIAL FATTY ACIDS, SYNAPTOGENESIS, AND PHOTORECEPTOR MEMBRANE BIOGENESIS IMPACT OF DIETARY FATTY ACID BALANCE ON MEMBRANE STRUCTURE AND FUNCTION OF NEURAL TISSUES .......... 197 M.T. Clandinin, M. Suh, and K. Hargreaves viii STRUCTURAL AND FUNCTIONAL IMPORTANCE OF DIETARY POLYUNSATURATED FATTY ACIDS IN THE NERVOUS SYSTEM ............................... 211 Jean-Marie Bourre, Michelle Bonneil, Jean Chaudiere, Michel Clement, Odile Dumont, Georges Durand, Huguette Lafont, Gilles Nalbone, Gerard Pascal, and Michele Piciotti LONG AND VERY LONG POLYUNSATURATED FATTY ACIDS OF RETINA AND SPERMATOZOA: THE WHOLE COMPLEMENT OF POLYENOIC FATTY ACID SERIES ......... 231 Marta 1. Aveldafto PHOSPHOLIPID METABOLISM IN RAT INTESTINAL MUCOSA AFTER ORAL ADMINISTRATION OF L YSOPHOSPHOLIPIDS ................................. 243 Alessandro Bruni, Paolo Orlando, Lucia Mietto, and Giampietro Viola CARBACHOL-STIMULATED RELEASE OF ARACHIDONIC ACID AND EICOSANOIDS FROM BRAIN CORTEX SYNAPTONEUROSOME LIPIDS OF ADULT AND AGED RATS ........................................ 251 Joanna Strosznajder and Marek Samochocki CARBACHOL-INDUCED STIMULATION OF INOSITOL PHOSPHATES, ARACHIDONIC ACID AND PROSTAGLANDIN F2a IN RABBIT RETINA ................... 259 Neville N. Osborne INDUCED AND SPONTANEOUS SEIZURES IN MAN PRODUCE INCREASES IN REGIONAL BRAIN LIPID DETECTED BY IN VIVO PROTON MAGNETIC RESONANCE SPECTROSCOPY ............................. 267 Bryan T. Woods and Tak-Ming Chiu NETWORK OF SIGNAL TRANSDUCTION PATHWAYS INVOLVING LIPIDS: PROTEIN KINASE C-DEPENDENT AND -INDEPENDENT PATHWAyS .......................... 275 R Bell, D. Burns, T. Okazaki, and Y. Hannun ESSENTIAL FATlY ACIDS, EXCITABLE MEMBRANE PHOSPHOLIPIDS, AND PATHOPHYSIOLOGY CONSERVATION OF DOCOSAHEXAENOIC ACID IN THE RETINA .... 285 RE. Anderson, P.J. O'Brien, RD. Wiegand, c.A. Kautz, and A.M. Stinson DOCOSAHEXAENOIC ACID UPTAKE AND METABOLISM IN PHOTORECEPTORS: RETINAL CONSERVATION BY AN EFFICIENT RETINAL PIGMENT EPITHELIAL CELL-MEDIATED RECYCLING PROCESS .................... 295 Nicolas G. Bazan, William C. Gordon, and Elena B. Rodriguez de Turco ix ESSENTIAL FArrY ACIDS AND NEURODEVELOPMENTAL DISORDER ................. 307 Michael A. Crawford REGULATION OF ARACHIDONIC ACID METABOLISM IN THE PERINATAL BRAIN DURING DEVELOPMENT AND UNDER ISCHEMIC STRESS ........................... 315 Ephraim Yavin, Baruch Kunievsky, Nicolas G. Bazan, and Shaul Harel INTERACTIONS OF PHOSPHOLIPIDS AND FREE FArrY ACIDS WITH ANTIDEPRESSANT RECOGNITION BINDING SITES IN RAT BRAIN .......................................... 325 Marta Stockert, Luis M. Zieher, and Jorge H. Medina VERY LONG-CHAIN FArrY ACIDS IN PEROXISOMAL DISEASE ...... 331 A. Poulos, K. Beckman, D.W. Johnson, B.C. Paton, B.S. Robinson, P. Sharp, S. Usher, and H. Singh LONG CHAIN OMEGA 3 POLY UNSATURATES IN FORMULA-FED TERM INFANTS ......................... 341 R.A. Gibson, M. Makrides, K.J. Clark, M.A. Neumann, and D.R. Lines SEVERE CHANGES IN POLYUNSATURATED FATTY ACIDS IN THE BRAIN, LIVER, KIDNEY, AND RETINA IN PATIENTS WITH PEROXISOMAL DISORDERS ............. 347 Manuela Martinez DEGRADATION OF PHOSPHOLIPIDS AND PROTEIN KINASE C ACTNA TION FOR THE CONTROL OF NEURONAL FUNCTIONS .............................. 361 Tetsutaro Shinomura, Hiroyuki Mishima, Shinji Matsushima, Yoshinori Asaoka, Kimihisa Yoshida, Masahiro Oka, and Yasutomi Nishizuka ESSENTIAL FATlY ACIDS AND EXCITABLE MEMBRANE PHOSPHOLIPIDS DISPOSITION KINETICS OF PHOSPHOLIPID LIPOSOMES ............ 375 Pietro Palatini BEHAVIORAL AND MORPHO-FUNCTIONAL CORRELATES OF BRAIN AGING: A PRECLINICAL STUDY WITH PHOSPHATIDYLSERINE .................................. 393 Maria Grazia Nunzi, Diego Guidolin, Lucia Petrelli, Patrizia Polato, and Adriano Zanotti RECEPTOR COUPLING TO PHOSPHOINOSITIDE SIGNALS .......... 399 P. Kurian, L.J. Chandler, R. Patel, and F.T. Crews