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STRUCTURAL AND FUNCTIONAL ORGANIZATION
OF THE SYNAPSE
STRUCTURAL AND FUNCTIONAL ORGANIZATION
OF THE SYNAPSE
Johannes W. Hell University of Iowa Iowa City, IA, USA
and
Michael D. Ehlers
Duke University Medical Center Durham, NC, USA
1 3
Edited by
Editors Johannes W. Hell Michael D. Ehlers Department of Pharmacology 2-512 BSB Department of NeurobiologyUniversity of Iowa Iowa City, IA 52242
ISBN: 978-0-387-77231-8 e-ISBN: 978-0-387-77232-5 DOI: 10.1007/978-0-387-77232-5 Library of Congress Control Number: 2007941249 © 2008 Springer Science+Business Media, LLC All rights reserved. This work may not be translated or copied in whole or in part without the written permission of the publisher (Springer Science+Business Media, LLC, 233 Spring Street, New York, NY 10013, USA), except for brief excerpts in connection with reviews or scholarly analysis. Use in connec-tion with any form of information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed is forbidden. The use in this publication of trade names, trademarks, service marks, and similar terms, even if they are not identified as such, is not to be taken as an expression of opinion as to whether or not they are subject to proprietary rights. While the advice and information in this book are believed to be true and accurate at the date of going to press, neither the authors nor the editors nor the publisher can accept any legal responsibility for any errors or omissions that may be made. The publisher makes no warranty, express or implied, with respect to the material contained herein.
Printed on acid-free paper 9 8 7 6 5 4 3 2 1 springer.com
Cover illustration: The cover illustration shows an immunofluorsecence micrograph of a hippocampal pyramidal neuron at two weeks in culture. The neuron was stained for the abundant calcium and calmodulin-dependent protein kinase CaMKII (green) and the presynaptic protein synapsin (red). The pictures was provided by Y. Chen and J. W. Hell, University of Iowa.
Duke University Medical Center Box 3209 Durham, NC 27710
With special dedication to our late friend and colleague Alaa El-Husseini
Preface
The synapse is a fascinating structure for many reasons. Biologically, it is an exquisitely organized subcellular compartment that has a remarkable capacity for fidelity and endurance. Computationally, synapses play a central role in signal transmission and processing that represent evolution’s solution to learning and memory. Nervous systems, including our own brains, possess an extraordinary capacity for adaptation and memory because the synapse, not the neuron, constitutes the basic unit for information storage.
Because the molecular complexities underlying signal processing and information storage must occur within the tiny space of the synapse, the precise molecular organization of proteins, lipids, and membranes at the synapse is paramount. Given the central role of the synapse in neuronal communication, it comes as no surprise that dysregulation of the synapse accounts for many, if not most, neurological and psychiatric disorders. Clinically, the synapse thus constitutes a prime target for treatments of these diseases.
It is for these reasons that we have chosen to focus our work on deciphering the structural and functional organization of the synapse. We have assembled leaders in the field of synapse biology to describe and distill the wonders and mysteries of the synapse. This book provides a fundamental description of the synapse developed over many decades by numerous investigators, paired with recent insight into new aspects of synapse structure and function that is still in flux and at the cutting edge of research.
This book grew out of a symposium and a research seminar at the University of Iowa that were sponsored, in large part, by the generous support of the Obermann Center for Advanced Studies. Obermann Seminars are specifically designed to gather international scholars and produce interdisciplinary research publications.
We are grateful for the exceptional efforts of our contributing authors, without whom this book would not have been possible. Their willingness to take time from their busy research schedules to share their insight and ideas with the breadth and depth that allow us to compile a collective work that is illuminating and useful, for both the general biologist and specialized neuroscientist, is very much appreciated. We express our gratitude to our assistants Ms. Susan Harward and Ms. Sue Birely for their professionalism and help with the book layout and proof reading. Lastly, we would like to thank our families (Laura and Henrik, Mary, Solon, Anselm, and Hans), who provided the support, encouragement, inspiration and comic relief, that in many ways helped to make this book possible.
Michael D. Ehlers and Johannes W. Hell
Editors
Contents
List of Contributors Diversity in Synapse Structure and Composition ...................................................1 Kristen M. Harris The Role of Glutamate Transporters in Synaptic Transmission .........................23 Dwight E. Bergles and Robert H. Edwards Structure and Function of Vertebrate and Invertebrate Active Zones ...............63 Craig C. Garner and Kang Shen Neurotransmitter Release Machinery: Components of the Neuronal SNARE Complex and Their Function .................91 Deniz Atasoy and Ege T. Kavalali The Molecular Machinery for Synaptic Vesicle Endocytosis.............................111 Peter S. McPherson, Brigitte Ritter, and George J. Augustine Initiation and Regulation of Synaptic Transmission by Presynaptic Calcium Channel Signaling Complexes ..............................................................147 Zu-Hang Sheng, Amy Lee, and William A. Catterall Adhesion Molecules at the Synapse ......................................................................173 Alaa El-Husseini Dendritic Organelles for Postsynaptic Trafficking .............................................205 Cyril Hanus and Michael D. Ehlers Structure and Mechanism of Action of AMPA and Kainate Receptors............251 Mark L. Mayer Cellular Biology of AMPA Receptor Trafficking and Synaptic Plasticity ........271 Jose A. Esteban
................................................................................................xiii
Structure and Function of the NMDA Receptor .................................................289 Hongjie Yuan, Matthew T. Geballe, Kasper B. Hansen, and Stephen F. Traynelis Molecular Properties and Cell Biology of the NMDA Receptor ........................317 Robert J. Wenthold, Rana A. Al-Hallaq, Catherine Croft Swanwick, and Ronald S. Petralia Surface Trafficking of Membrane Proteins at Excitatory and Inhibitory Synapses ........................................................................................369 Daniel Choquet and Antoine Triller Scaffold Proteins in the Postsynaptic Density......................................................407 Mary B. Kennedy, Edoardo Marcora, and Holly J. Carlisle Ca2+ Signaling in Dendritic Spines .......................................................................441 Bernardo L. Sabatini and Karel Svoboda Postsynaptic Targeting of Protein Kinases and Phosphatases ...........................459 Stefan Strack and Johannes W. Hell Long-Term Potentiation........................................................................................501 John E. Lisman and Johannes W. Hell Homeostatic Synaptic Plasticity............................................................................535 Gina G. Turrigiano Ubiquitin and Protein Degradation in Synapse Function...................................553 Thomas D. Helton and Michael D. Ehlers Signaling from Synapse to Nucleus ......................................................................601 Carrie L. Heusner and Kelsey C. Martin Molecular Organization of the Postsynaptic Membrane at Inhibitory Synapses ...........................................................................................621 I. Lorena Arancibia-Carcamo, Antoine Triller, and Josef T. Kittler Acid-Sensing Ion Channels (ASICs) and pH in Synapse Physiology .................661 John A. Wemmie, Xiang-ming Zha, and Michael J. Welsh Glia as Active Participants in the Development and Function of Synapses ......683 Cagla Eroglu, Ben A. Barres and Beth Stevens Plasticity of Dentate Granule Cell Mossy Fiber Synapses: A Putative Mechanism of Limbic Epileptogenesis ..............................................715 James O. McNamara, Yang Z. Huang, and Enhui Pan
x Contents
Stroke – A Synaptic Perspective ...........................................................................731 Robert Meller and Roger P. Simon Neuroplasticity and Pathological Pain .................................................................759 Michael W. Salter Index .......................................................................................................................781
Contents xi
List of Contributors
Rana A. Al-Hallaq Laboratory of Neurochemistry, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD, USA, e-mail: [email protected] I. Lorena Arancibia-Carcamo Department of Pharmacology, University College London, Gower Street, London, WC1E 6BT, UK, e-mail: [email protected] Deniz Atasoy Department of Neuroscience, U.T. Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9111, USA, e-mail: [email protected] George J. Augustine Department of Neurobiology, Duke University Medical Center, Box 3209, Durham, NC 27710, USA, e-mail: [email protected] Ben A. Barres Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA, e-mail: [email protected] Dwight E. Bergles The Solomon H. Snyder Department of Neuroscience, Johns Hopkins School of Medicine, 725 N. Wolfe St., WBSB 1003, Baltimore, MD 21205, USA, e-mail: [email protected] Holly J. Carlisle Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA, e-mail: [email protected] William A. Catterall Department of Pharmacology, University of Washington, Seattle, WA 98195-7280, USA, e-mail: [email protected] Daniel Choquet UMR 5091 CNRS, Université de Bordeaux 2, Physiologie Cellulaire de la Synapse, Institut François Magendie rue Camille Saint Saëns 33077 Bordeaux Cedex, France, e-mail: [email protected]
xiv List of Contributors Robert H. Edwards The Departments of Neurology and Physiology, UCSF School of Medicine, San Francisco, CA 94158-2517, USA, e-mail: [email protected] Michael D. Ehlers Howard Hughes Medical Institute, Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA, e-mail: [email protected] Alaa El-Husseini University of British Columbia, Department of Psychiatry, Vancouver, British Columbia, Canada, e-mail: [email protected] Cagla Eroglu Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA, e-mail: [email protected] José A. Esteban University of Michigan, Department of Pharmacology, Ann Arbor, MI 48109, USA, e-mail: [email protected] Craig C. Garner Department of Psychiatry and Behavioral Science, Nancy Pritzker Laboratory, Stanford University, Palo Alto, CA 94304-5485, USA, e-mail: [email protected] Matthew T. Geballe Department of Chemistry, Emory University, Atlanta, GA 30322, USA, e-mail: [email protected] Kasper B. Hansen
Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322, USA, e-mail: [email protected] Cyril Hanus Howard Hughes Medical Institute, Department of Neurobiology, Duke University Medical Center, Durham, NC 27710, USA, e-mail: [email protected] Kristen M. Harris Neurobiology Department, Center for Learning and Memory, University of Texas at Austin, Austin, Texas 78712, USA, e-mail: [email protected] Johannes W. Hell Department of Pharmacology, University of Iowa, Iowa City, IA 52242-1109, USA, e-mail: [email protected]
List of Contributors xv Thomas D. Helton Department of Neurobiology, Duke University Medical Center, Howard Hughes Medical Institute, Durham, NC 27710, USA, e-mail: [email protected] Carrie L. Heusner Department of Biological Chemistry and Department of Psychiatry and Biobehavioral Sciences, Brain Research Institute, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA 90095, USA, e-mail: [email protected] Yang Z. Huang Duke University, Department of Neurobiology, Durham, NC 27710, USA, e-mail: [email protected] Ege T. Kavalali Department of Neuroscience, U.T. Southwestern Medical Center, 5323 Harry Hines Boulevard, Dallas, TX 75390-9111, USA, e-mail: [email protected] Mary B. Kennedy Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA, e-mail: [email protected] Josef T. Kittler Department of Physiology, University College London, Gower Street, London, WC1E 6BT, UK, e-mail: [email protected] Amy Lee Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322, USA, e-mail: [email protected] John E. Lisman
Brandeis University, Biology Department and Volen Center for Complex Systems, Waltham, MA 02454, USA, e-mail: [email protected] Edoardo Marcora Division of Biology, California Institute of Technology, Pasadena, CA 91125, USA, e-mail: [email protected] Kelsey C. Martin Department of Biological Chemistry and Department of Psychiatry and Biobehavioral Sciences, Brain Research Institute, Semel Institute for Neuroscience and Human Behavior, UCLA, Los Angeles, CA 90095, USA, e-mail: [email protected]
xvi List of Contributors Mark L. Mayer Porter Neuroscience Research Center, Laboratory of Cellular & Molecular Neurophysiology, NICHD, NIH, Bethesda, MD 20892, USA, e-mail: [email protected] James O. McNamara Duke University, Department of Neurobiology, Durham, NC 27710, USA, e-mail: [email protected] Peter S. McPherson Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, 3801 Rue University, Montreal, Quebec, Canada, H3A 2B4, e-mail: [email protected] Robert Meller RS Dow Neurobiology Laboratory, Legacy Clinical Research and Technology Center, 1225 NE 2nd Ave, Portland, OR, 97232, USA, e-mail: [email protected] Enhui Pan Duke University, Department of Neurobiology, Durham, NC 27710, USA, e-mail: [email protected] Ronald S. Petralia Laboratory of Neurochemistry, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD, USA,
Brigitte Ritter Department of Neurology and Neurosurgery, Montreal Neurological Institute, McGill University, 3801 Rue University, Montreal, Quebec, Canada, H3A 2B4, e-mail: [email protected] Bernardo L. Sabatini Department of Neurobiology, Harvard Medical School, 220 Longwood Avenue, Boston, MA 02115, USA, e-mail: [email protected] Michael W. Salter Program in Neurosciences & Mental Health, The Hospital for Sick Children, and The University of Toronto Centre for the Study of Pain, Toronto, ON, Canada M5G 1X8, e-mail: [email protected] Kang Shen
Department of Biological Sciences, Stanford University, Palo Alto, CA 94305-5020, USA, e-mail: [email protected]
e-mail: [email protected]
List of Contributors xvii Zu-Hang Sheng Synaptic Functions Unit, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892-3701, USA, e-mail: [email protected] Roger P. Simon RS Dow Neurobiology Laboratory, Legacy Clinical Research and Technology Center, 1225 NE 2nd Ave, Portland, OR, 97232, USA, e-mail: [email protected] Beth Stevens Department of Neurobiology, Stanford University School of Medicine, Stanford, CA 94305, USA, e-mail: [email protected] Stefan Strack Department of Pharmacology, University of Iowa, Iowa City, IA 52242-1109, USA, e-mail: [email protected] Karel Svoboda Janelia Farm Research Campus, HHMI, 19700 Helix Drive, Ashburn, VA 20147, USA, e-mail: [email protected] Catherine Croft Swanwick Laboratory of Neurochemistry, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD, USA, e-mail: [email protected] Stephen F. Traynelis Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322, USA, e-mail: [email protected] Antoine Triller Inserm UR497, Ecole Normale Supérieure, Biologie Cellulaire de la Synapse N&P, 46, rue d’Ulm 75005 Paris, France, e-mail: [email protected] Gina Turrigiano Brandeis University, Department of Biology and Center for Behavioral Genomics, Waltham, MA 02454, USA, e-mail: [email protected] Michael J. Welsh
Departments of Internal Medicine and Molecular Physiology, and Howard Hughes Medical Institute, University of Iowa, Roy J. and Lucille A. Carver College of Medicine, Iowa City, IA 52242, USA, e-mail: [email protected]
xviii List of Contributors John A. Wemmie
Department of Psychiatry, Neuroscience Program, and Department of Veterans Affairs Medical Center, University of Iowa, Roy J. and Lucille A. Carver College of Medicine, Iowa City, IA,USA, e-mail: [email protected] Robert J. Wenthold Laboratory of Neurochemistry, National Institute on Deafness and Other Communication Disorders, National Institutes of Health, Bethesda, MD, USA, e-mail: [email protected] Hongjie Yuan Department of Pharmacology, Emory University School of Medicine, Atlanta, GA 30322, USA, e-mail: [email protected] Xiang-ming Zha
Department of Internal Medicine and Howard Hughes Medical Institute, University of Iowa, Roy J. and Lucille A. Carver College of Medicine, Iowa City, IA 52242, USA, e-mail: [email protected]
