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Activation of Immediate Early Genes by Drugs of Abuse National Institute on Drug Abuse RESEARCH MONOGRAPH SERIES Activation of Immediate Early Genes by Drugs of Abuse 125 U.S. Department of Health and Human Services • Public Health Service • National Institutes of Health Activation of Immediate Early Genes By Drugs of Abuse Editors: Reinhard Grzanna, Ph.D. Roger M. Brown, Ph.D. NIDA Research Monograph 125 1993 U.S. DEPARTMENT OF HEALTH AND HUMAN SERVICES Public Health Service National Institutes of Health National Institute on Drug Abuse 5600 Fishers Lane Rockville, MD 20857 ACKNOWLEDGMENT This monograph is based on the papers and discussions from a technical review on “Activation of Immediate Early Genes by Drugs of Abuse” held on June 3-4, 1991, in Rockville, MD. The technical review was sponsored by the National Institute on Drug Abuse (NIDA). COPYRIGHT STATUS The National Institute on Drug Abuse has obtained permission from the copyright holders to reproduce certain previously published material as noted in the text. Further reproduction of this copyrighted material is permitted only as part of a reprinting of the entire publication or chapter. For any other use, the copyright holder’s permission is required. All other material in this volume except quoted passages from copyrighted sources is in the public domain and may be used or reproduced without permission from the Institute or the authors, Citation of the source is appreciated. Opinions expressed in this volume are those of the authors and do not necessarily reflect the opinions or official policy of the National Institute on Drug Abuse or any other part of the U.S. Department of Health and Human Services. The U.S. Government does not endorse or favor any specific commercial product or company. Trade, proprietary, or company names appearing in this publication are used only because they are considered essential in the context of the studies reported herein. NIDA Research Monographs are indexed in the “Index Medicus.” They are selectively included in the coverage of “American Statistics Index,” “BioSciences Information Service,” “Chemical Abstracts,” “Current Contents,” “Psychological Abstracts,” and “Psychopharmacology Abstracts.” National Institute on Drug Abuse NIH Publication No. 93-3504 Printed 1993 ii Contents Page Introduction 1 Reinhard Grzanna and Roger M. Brown Regulation of Immediate Early Gene Expression 3 Brent H. Cochran Everything Activates C-fos- How Can It Matter? 25 Steven E. Hyman, Barry E. Kosofsky, Tuong V. Nguyen, Bruce M. Cohen, and Michael J. Comb Immediate Early Genes: Their Involvement in Physiological and Pathological Responses in the Nervous System 39 Michael O. Hayward, Tom Curran, and James I. Morgan Immediate Early Gene Activation and Long-Term Changes in Neural Function: A Possible Role in Addiction? 54 Harold A. Robertson Acute Effects of Psychomotor Stimulant Drugs on Gene Expression in the Striatum 72 Ann M. Graybiel Functional Organization of the Striatum: Relevance to Actions of Psychostimulant Drugs of Abuse 82 Charles R. Gerfen iii Regulation of Neural Gene Expression in Opiate and Cocaine Addiction 92 Eric J. Nestler, Clare M. Bergson. Xavier Guitart, and Bruce T. Hope C-Fos and Fos-Related Antigens as Markers for Neuronal Activity: Perspectives From Neuroendocrine Systems 117 Gloria E. Hoffman, Wen-Sen Lee, M. Susan Smith, Rula Abbud, Michelle M. Roberts, Alan G. Robinson, and Joseph G. Verbalis Mechanisms of Opioid-Mediated Antinociception: Correlation of Fos Expression and Behavior 134 Kathleen R. Gogas, Jon D. Levine, and Allan I. Basbaum The Ontogeny of Immediate Early Gene Response to Cocaine: A Molecular Analysis of the Effects of Cocaine on Developing Rat Brain 181 Barry E. Kosofsky and Steven E. Hyman NMDA Receptor Blockade Prevents Translation, but Not Transcription, of the C-fos Gene Following Stimulation With Multiple Extracellular Signals in Cultured Cortical Neurons: Implications for Plasticity and Molecular Memory 172 Frank R. Sharp, Kinya Hisanaga, and Stephen M. Sagar Induction and Suppression of Proto-Oncogenes in Rat Striatum After Single or Multiple Treatments With Cocaine or GBR-12909 181 Michael J. ladaroia, Eric J. Chuang, Choh-Lun Yeung, Yin Hoo, Mayme Silverthorn, Jun Gu, and Gaetano Draisci List of NIDA Research Monographs 212 iv Introduction Reinhard Grzanna and Roger M. Brown A major goal in drug abuse research is to determine the neurobiological mechanisms by which drugs of abuse produce tolerance, dependence, and addiction. These behavioral manifestations of drug abuse have been attributed to longlasting neuroadaptations in central nervous system (CNS) neurons. The nature and extent of these neuroadaptations remain to be characterized, but investigators agree that they are the result of drug-induced alterations in neuronal gene expression. The recent discovery that cocaine and amphetamine rapidly and transiently induce immediate early genes (IEGs) provided the most direct indication that drugs of abuse can profoundly influence gene expression. Following their description a few years ago, IEGs and their protein products became recognized as important links by which extracellular signals can produce alterations in gene transcription. Turning on IEG expression by drugs of abuse may be the initial step by which drugs alter the expression of late genes to produce longlasting changes in neuronal functions. Thus, studies of the effects of drugs of abuse on IEGs may hold the key to providing the answer to how drugs of abuse produce long-term changes in neurons. Studies of this class of genes also should provide a powerful approach to explore correlations between drug-induced changes in behavior and the neuronal systems in which drugs permanently alter gene expression. Studies of the effects of drugs of abuse on IEGs are greatly facilitated by the availability of methods to visualize the activity states of these genes in tissue sections by immunohistochemistry and by in situ hybridization histochemistry. This has opened a new and promising approach to define drug-induced, permanent changes in the CNS and to identify the neuronal circuitries in which they occur. The chapters in this volume were presented at a conference on June 3-4, 1991, in Rockville, MD, organized by the National Institute on Drug Abuse. The main goal of this conference was to assess the potential impact of studies of IEGs in the field of drug abuse research. The contributors to this volume reviewed 1 current developments in the field and discussed to what extent studies of the effects of drugs of abuse on IEGs are likely to provide new insights into the molecular underpinning of drug-seeking behavior. Among the topics discussed were the specificity of the activation of IEGs by drugs of abuse, the nature of the long-term alterations following the induction, and the possible relationship between the observed changes in IEG activity and behavior. Many of the questions discussed remain unresolved. Yet, there was excitement about the remarkable specificity in the patterns of IEG activation induced by different drugs in the CNS. The participants expressed confidence about the prospects of linking drug-induced IEG induction to specific alterations in peptide gene expression in identified populations of CNS neurons. This volume reflects the considerable optimism among drug abuse researchers that studies of IEGs offer a new path to identify the long-term effects of drug exposure in the CNS. The chapters reveal a sense of confidence that studies of the action of drugs of abuse on IEGs will greatly facilitate efforts to identify the neuronal systems critically involved in the development of drug addiction and the nature of the changes produced within these systems. AUTHORS Reinhard Grzanna, Ph.D. Senior Staff Fellow Roger M. Brown, Ph.D. Chief Neuroscience Research Branch National Institute on Drug Abuse Parklawn Building, Room 11A-33 5600 Fishers Lane Rockville, MD 20657 2 Regulation of Immediate Early Gene Expression Brent H. Cochran INTRODUCTION Recently, much excitement has been generated by the finding that various immediate early genes (IEGs) are expressed in neurons in response to a variety of neurotropic stimuli. Part of the reason these findings have generated so much interest is that earlier work has suggested that long-term changes in nervous system behavior require changes in gene expression (Goelet et al. 1986). Thus, since changes in IEG expression are coupled to neuronal activity and neurotransmitter release, it may now be possible, using in situ techniques that provide resolution at the single-cell level, to correlate the physiological state of a neuron with behavioral and physiological outputs. This chapter reviews what is currently known about IEGs and speculates on what roles these genes might be playing in the operation of the nervous system. IEGs (sometimes called early-response genes or primary-response genes) were first identified not in the nervous system but through the study of cell growth regulation. During the 1970s it became apparent that polypeptide growth factors were key modulators of cell growth and differentiation of multicellular organisms. Early studies had suggested that the mitogenic effects of serum growth factors were mediated in part by the ability of these factors to regulate gene expression (Smith and Stiles 1981). To identify such genes, several investigators set out to clone them by differential or subtractive cDNA cloning. The first of such genes cloned were those induced by the platelet- derived growth factor (PDGF) in 3T3 fibroblasts (Cochran et
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