Progress in molecular biology and translational science, volume 128

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Academic Press is an imprint of Elsevier 225 Wyman Street, Waltham, MA 02451, USA 525 B Street, Suite 1800, San Diego, CA 92101-4495, USA 32 Jamestown Road, London NW1 7BY, UK The Boulevard, Langford Lane, Kidlington, Oxford OX5 1GB, UK First edition 2014 Copyright © 2014, Elsevier Inc All rights reserved No part of this publication may be reproduced or transmitted in any form or by any means, electronic or mechanical, including photocopying, recording, or any information storage and retrieval system, without permission in writing from the publisher Details on how to seek permission, further information about the Publisher’s permissions policies and our arrangements with organizations such as the Copyright Clearance Center and the Copyright Licensing Agency, can be found at our website: www.elsevier.com/permissions This book and the individual contributions contained in it are protected under copyright by the Publisher (other than as may be noted herein) Notices Knowledge and best practice in this field are constantly changing As new research and experience broaden our understanding, changes in research methods, professional practices, or medical treatment may become necessary 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 products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions, or ideas contained in the material herein ISBN: 978-0-12-800977-2 ISSN: 1877-1173 For information on all Academic Press publications visit our website at store.elsevier.com CONTRIBUTORS Schahram Akbarian Department of Psychiatry, and Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, USA Angel Barco Instituto de Neurociencias, Universidad Miguel Herna´ndez-Consejo Superior de Investigaciones Cientı´ficas, Alicante, Spain Elisabeth B Binder Department of Translational Research in Psychiatry, Max Planck Institute of Psychiatry, Munich, Germany, and Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, Georgia, USA Erbo Dong The Psychiatric Institute, Department of Psychiatry, College of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA Janina Galler Judge Baker Children’s Center, Harvard Medical School, Boston, Massachusetts, USA Dennis R Grayson The Psychiatric Institute, Department of Psychiatry, College of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA Alessandro Guidotti The Psychiatric Institute, Department of Psychiatry, College of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA Leah N Hitchcock Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, Oregon, USA Timothy J Jarome Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL, USA K Matthew Lattal Department of Behavioral Neuroscience, Oregon Health & Science University, Portland, Oregon, USA Robert H Lipsky Inova Neurosciences Institute, Inova Health System, Falls Church, and Department of Molecular Neuroscience, The Krasnow Institute for Advanced Study, George Mason University, Fairfax, Virginia, USA Sermsak Lolak Department of Psychiatry, The George Washington University School of Medicine and Health Sciences, Washington, District of Columbia, USA ix x Contributors Jose P Lopez-Atalaya Instituto de Neurociencias, Universidad Miguel Herna´ndez-Consejo Superior de Investigaciones Cientı´ficas, Alicante, Spain Farah D Lubin Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL, USA Amanda Mitchell Department of Psychiatry, and Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, USA Cyril Peter Department of Psychiatry, and Department of Neuroscience, Icahn School of Medicine at Mount Sinai, New York, USA Nadine Provenc¸al Department of Translational Research in Psychiatry, Max Planck Institute of Psychiatry, Munich, Germany Danielle Galler Rabinowitz Judge Baker Children’s Center, Harvard Medical School, Boston, Massachusetts, USA Carina Rampp Department of Translational Research in Psychiatry, Max Planck Institute of Psychiatry, Munich, Germany Panos Roussos Department of Psychiatry; Department of Neuroscience, and Department of Genetics and Genomic Sciences, Icahn School of Medicine at Mount Sinai, New York, USA Pim Suwannarat Department of Genetics, Mid-Atlantic Permanente Medical Group, Rockville, Maryland, USA Jasmyne S Thomas Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL, USA Nadejda Tsankova Department of Neuroscience, and Department of Pathology, Icahn School of Medicine at Mount Sinai, New York, USA Patricia Tueting The Psychiatric Institute, Department of Psychiatry, College of Medicine, University of Illinois at Chicago, Chicago, Illinois, USA Luis M Valor Instituto de Neurociencias, Universidad Miguel Herna´ndez-Consejo Superior de Investigaciones Cientı´ficas, Alicante, Spain PREFACE This issue of Progress in Molecular Biology and Translational Science is focused on neuroepigenetics, a still relatively “young” area of research exploring the roles of chromatin structure and function in the context of development, adulthood, and disease In the broadest sense, epigenetics could be viewed as the mechanisms and molecular bridges by which countless internal and external factors (re)organize the genomic material that is packaged inside the nuclei of brain cells, thereby potentially affecting synaptic plasticity and behavior Epigenetic mechanisms, which among many others include proper regulation of DNA cytosine methylation, histone modifications, and nucleosomal organization (a nucleosome is the elementary unit of chromatin, with 147 bp of genomic DNA wrapped around a core of eight histone proteins), are thought to play an important role in various neurodevelopmental and neurological disorders Some of these key concepts linking epigenetic mechanisms to neuronal plasticity and (mal)adaptive mechanisms in the immature and also adult brain are highlighted in the eight chapters published in this issue The first chapter, written by Jarome, Thomas, and Lubin, provides a general overview and detailed discussion on regulatory mechanisms governing covalent DNA and nucleosomal histone modifications during memory formation and storage in the mammalian brain Next in Chapter 2, Rampp, Binder, and Provenc¸al discuss gene  environment interactions in the context of traumatic memory and posttraumatic stress disorder, with particular focus on steroid hormone and other stress-responsive pathways In Chapter 3, Hitchcock and Lattal describe the increasingly recognized importance of histone methylation and acetylation and other modifications for plasticitydependent phenomena in the brain’s reward circuit, and the potential implications for the treatment of addiction and substance abuse and dependence Chapters 4, written by Guidotti, Dong, Tueting, and Grayson, and 5, written by Lolak, Suwannarat, and Lipsky, discuss epigenetic risk factors in the context of mood and psychosis spectrum disorders, including schizophrenia and depression Next, Lopez-Atalaya, Valor, and Barco in Chapter provide a highly informative discussion of Rubinstein–Taybi syndrome (RSTS), a neurodevelopmental syndrome caused by mutations in the genes encoding the lysine acetyltransferases CBP and p300 RSTS serves as a prototype example of monogenic neurological disease associated xi xii Preface with epigenetic dysregulation (histone acetylation in this case), affecting both the developing brain and mature circuitry via multiple mechanisms While aforementioned reviews focus on environmental or genetic mechanisms directly impacting the epigenome of brain cells, Chapter by Galler and Galler Rabinowitz explores intergenerational effects of early adversity, including the potential role of epigenetics in intergenerational transmission The final chapter of this issue, written by Mitchell, Roussos, Peter, Tsankova, and Akbarian, embarks on future developments in the field of neuroepigenetics (which will include the exploration of the nonrandomness in three-dimensional chromosomal organization and other principles often referred to as “higher order chromatin”) and how such type of molecular approaches could provide further insights into genetic and epigenetic risk architecture of cognitive disorders unique to the human brain We, as volume editors, have asked the authors of these various chapters not only to summarize the evidence collected so far in their field but also to highlight some of the important topics that are subject to ongoing debate or hitherto underexplored It is our hope and expectation that such type of discussion will further stimulate interest in epigenetic approaches and excite the younger generation of neuroscientists about these lines of research Just to mention a few examples of debate mentioned in this issue: Chapter highlights the bulk of the epigenetics literature pertaining to the learning and memory field and is preoccupied with mechanisms that are primarily relevant for initial acquisition of memory, while much less attention has been given to the equally important stages of consolidation, retrieval, and extinction This chapter also highlights the potential epigenetic targets that may serve to improve or enhance memory function, while Chapter cautions on the effects of neurological therapies on these epigenetic mechanisms Several chapters include some remarks on tissue specificity of epigenetic signals, which is particularly relevant in the context of approaches aimed at exploring epigenetic signals in blood and the periphery as biomarkers for brain-related disease (Chapter 2) or chromatin state mappings in brain tissue with its extremely complex and highly heterogenous mixture of neuronal and glial subpopulations (Chapter 8) Furthermore, Chapter points to two other important problems in neuroepigenetics including the often unresolved question of correlational association versus causal mechanism, and the difficulties and challenges in linking the molecular and behavioral phenotypes to the prevailing theories on reward and memory Chapter touches upon the still very novel and provocative concept of transgenerational inheritance Preface xiii We, as volume editors, are extremely grateful for the privilege to have worked with an outstanding group of colleagues We would like to thank Ms Helene Kabes for outstanding editorial assistance and the editors of the PMBTS series, Dr Michael Conn and Ms Mary Ann Zimmermann, for their support SCHAHRAM AKBARIAN FARAH LUBIN CHAPTER ONE The Epigenetic Basis of Memory Formation and Storage Timothy J Jarome, Jasmyne S Thomas, Farah D Lubin Department of Neurobiology, University of Alabama at Birmingham, Birmingham, AL, USA Contents Introduction to the Neurobiology of Learning and Memory Epigenetic Mechanisms of Memory Consolidation 2.1 Histone acetylation 2.2 Histone methylation 2.3 Histone phosphorylation 2.4 Histone ubiquitination and sumoylation 2.5 DNA methylation 2.6 Summary of epigenetic regulation of memory consolidation Epigenetic Mechanisms of Memory Reconsolidation 3.1 Histone modifications during memory reconsolidation 3.2 DNA methylation during memory reconsolidation 3.3 Epigenetic regulation of reconsolidation-dependent memory updating 3.4 Summary of epigenetic regulation of memory reconsolidation Epigenetic Mechanisms of Memory Extinction Future Directions and Conclusions Acknowledgments References 5 10 12 14 14 16 16 17 19 20 24 24 Abstract The formation of long-term memory requires a series of cellular and molecular changes that involve transcriptional regulation of gene expression While these changes in gene transcription were initially thought to be largely regulated by the activation of transcription factors by intracellular signaling molecules, epigenetic mechanisms have emerged as an important regulator of transcriptional processes across multiple brain regions to form a memory circuit for a learned event or experience Due to their self-perpetuating nature and ability to bidirectionally control gene expression, these epigenetic mechanisms have the potential to not only regulate initial memory formation but also modify and update memory over time This chapter focuses on the established, but poorly understood, role for epigenetic mechanisms such as posttranslational modifications of histone proteins and DNA methylation at the different stages of memory storage Additionally, this chapter emphasizes how these mechanisms interact to control the Progress in Molecular Biology and Translational Science, Volume 128 ISSN 1877-1173 http://dx.doi.org/10.1016/B978-0-12-800977-2.00001-2 # 2014 Elsevier Inc All rights reserved Timothy J Jarome et al ideal epigenetic environment for memory formation and modification in neurons The reader will gain insights into the limitations in our current understanding of epigenetic regulation of memory storage, especially in terms of their cell-type specificity and the lack of understanding in the interactions of various epigenetic modifiers to one another to impact gene expression changes during memory formation INTRODUCTION TO THE NEUROBIOLOGY OF LEARNING AND MEMORY The process of encoding long-term memories in the brain for later recall is complex, requiring simultaneous engagement of neurons across multiple brain regions The neuronal circuits recruited for this process can vary based on the type of behavioral task but include neurons in the hippocampus for processing of contextual and spatial information,1 the amygdala for processing of emotional content,2 and the insular cortex for processing of gustatory information.3 For example, one of the most utilized behavioral paradigms for elucidating the molecular and cellular mechanisms of memory formation and storage is Pavlovian fear conditioning.4 In this paradigm, a neutral conditioned stimulus (CS) is paired with a noxious unconditioned stimulus (UCS) Once paired, presentation of the CS by itself can elicit emotional and physiological responses similar to those produced by the aversive UCS Due to the emotional component of the task, associations acquired using Pavlovian fear conditioning requires the amygdala for longterm memory formation and storage However, some fear memories, such as those that are contextually based, also require the hippocampus, anterior cingulate cortex (ACC), and retrosplenial cortex, whereas other fear memories, such as those that are auditory-based, not rely on these regions (reviewed in Ref 5) Thus, memory storage is a dynamic process that requires synaptic plasticity in many different brain regions, though the memory-related brain regions required can vary greatly depending on the behavioral paradigm used Once acquired, memories can go through several different stages of modification and storage (Fig 1.1) For example, following the acquisition of a fear conditioning task, there is a time-dependent process (
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