National Academies Press: OpenBook
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page R4
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page R6
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page viii Cite
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page R8
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page R9
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page R10
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Page R11
Suggested Citation:"Front Matter." National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models: Proceedings of a Workshop. Washington, DC: The National Academies Press. doi: 10.17226/25362.
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Transgenic Neuroscience Research: Exploring the Scientific Opportunities Afforded by New Nonhuman Primate Models PROCEEDINGS OF A WORKSHOP Lisa Bain, Sheena M. Posey Norris, and Clare Stroud, Rapporteurs Forum on Neuroscience and Nervous System Disorders Board on Health Sciences Policy Health and Medicine Division PREPUBLICATION COPY: UNCORRECTED PROOFS

THE NATIONAL ACADEMIES PRESS 500 Fifth Street, NW Washington, DC 20001 This activity was supported by contracts between the National Academy of Sciences and the Alzheimer’s Association; Cohen Veterans Bioscience; Department of Health and Human Services’ Food and Drug Administration (5R13FD005362-02) and National Institutes of Health (NIH) (HHSN26300089 [Under Master Base #DHHS-10002880]) through the National Center for Complementary and Integrative Health, National Eye Institute, National Institute of Mental Health, National Institute of Neurological Disorders and Stroke, National Institute on Aging, National Institute on Alcohol Abuse and Alcoholism, National Institute on Drug Abuse, and NIH Blueprint for Neuroscience Research; Department of Veterans Affairs (VA240-14-C-0057); Eli Lilly and Company; Foundation for the National Institutes of Health; Gatsby Charitable Foundation; George and Anne Ryan Institute for Neuroscience at The University of Rhode Island; Janssen Research & Development, LLC; The Kavli Foundation; Lundbeck Research USA; Merck Research Laboratories; The Michael J. Fox Foundation for Parkinson’s Research; National Multiple Sclerosis Society; National Science Foundation (BCS-1064270); One Mind; Sanofi; Society for Neuroscience; Takeda Pharmaceuticals International, Inc.; and Wellcome Trust. Any opinions, findings, conclusions, or recommendations expressed in this publication do not necessarily reflect the views of any organization or agency that provided support for the project. International Standard Book Number-13: International Standard Book Number-10: Digital Object Identifier: https://doi.org/10.17266/25362 Additional copies of this publication are available from the National Academies Press, 500 Fifth Street, NW, Keck 360, Washington, DC 20001; (800) 624-6242 or (202) 334-3313; http://www.nap.edu. Copyright 2019 by the National Academy of Sciences. All rights reserved. Printed in the United States of America Suggested citation: National Academies of Sciences, Engineering, and Medicine. 2019. Transgenic neuroscience research: Exploring the scientific opportunities afforded by new nonhuman primate models: Proceedings of a workshop. Washington, DC: The National Academies Press. doi:https://doi.org/10.17266/25362. PREPUBLICATION COPY: UNCORRECTED PROOFS

The National Academy of Sciences was established in 1863 by an Act of Congress, signed by President Lincoln, as a private, nongovernmental institution to advise the nation on issues related to science and technology. Members are elected by their peers for outstanding contributions to research. Dr. Marcia McNutt is president. The National Academy of Engineering was established in 1964 under the charter of the National Academy of Sciences to bring the practices of engineering to advising the nation. Members are elected by their peers for extraordinary contributions to engineering. Dr. C. D. Mote, Jr., is president. The National Academy of Medicine (formerly the Institute of Medicine) was established in 1970 under the charter of the National Academy of Sciences to advise the nation on medical and health issues. Members are elected by their peers for distinguished contributions to medicine and health. Dr. Victor J. Dzau is president. The three Academies work together as the National Academies of Sciences, Engineering, and Medicine to provide independent, objective analysis and advice to the nation and conduct other activities to solve complex problems and inform public policy decisions. The National Academies also encourage education and research, recognize outstanding contributions to knowledge, and increase public understanding in matters of science, engineering, and medicine. Learn more about the National Academies of Sciences, Engineering, and Medicine at www.nationalacademies.org. PREPUBLICATION COPY: UNCORRECTED PROOFS

Consensus Study Reports published by the National Academies of Sciences, Engineering, and Medicine document the evidence- based consensus on the study’s statement of task by an authoring committee of experts. Reports typically include findings, conclusions, and recommendations based on information gathered by the committee and the committee’s deliberations. Each report has been subjected to a rigorous and independent peer-review process and it represents the position of the National Academies on the statement of task. Proceedings published by the National Academies of Sciences, Engineering, and Medicine chronicle the presentations and discussions at a workshop, symposium, or other event convened by the National Academies. The statements and opinions contained in proceedings are those of the participants and are not endorsed by other participants, the planning committee, or the National Academies. For information about other products and activities of the National Academies, please visit www.nationalacademies.org/ about/whatwedo. PREPUBLICATION COPY: UNCORRECTED PROOFS

PLANNING COMMITTEE ON TRANSGENIC AND CHIMERIC NEUROSCIENCE RESEARCH: EXPLORING THE SCIENTIFIC OPPORTUNITIES AFFORDED BY NEW NONHUMAN PRIMATE MODELS 1 FRANCES JENSEN (Chair), University of Pennsylvania SUSAN AMARA, National Institute of Mental Health SARAH CADDICK, Gatsby Charitable Foundation MARINA EMBORG, University of Wisconsin–Madison GUOPING FENG, Massachusetts Institute of Technology JOSHUA GORDON, National Institute of Mental Health HENRY T. GREELY, Stanford University JEFFREY KAHN, Johns Hopkins University WALTER KOROSHETZ, National Institute of Neurological Disorders and Stroke JOHN MORRISON, University of California, Davis WILLIAM NEWSOME, Stanford University KAREN PARKER, Stanford University MICHAEL STEINMETZ, National Eye Institute ANDREW WELCHMAN, Wellcome Trust STEVIN ZORN, MindImmune Therapeutics, Inc. Health and Medicine Division Staff CLARE STROUD, Director, Forum on Neuroscience and Nervous System Disorders SHEENA M. POSEY NORRIS, Program Officer DANIEL FLYNN, Research Associate (until November 2018) PHOENIX WILSON, Senior Program Assistant ANDREW M. POPE, Senior Director, Board on Health Sciences Policy 1The National Academies of Sciences, Engineering, and Medicine’s planning committees are solely responsible for organizing the workshop, identifying topics, and choosing speakers. The responsibility for the published Proceedings of a Workshop rests with the workshop rapporteurs and the institution. v PREPUBLICATION COPY: UNCORRECTED PROOFS

FORUM ON NEUROSCIENCE AND NERVOUS SYSTEM DISORDERS 1 STORY LANDIS (Co-Chair), Director Emeritus, National Institute of Neurological Disorders and Stroke JOHN KRYSTAL (Co-Chair), Yale University SUSAN AMARA, Society for Neuroscience RITA BALICE-GORDON, Sanofi KATJA BROSE, Chan Zuckerberg Initiative EMERY BROWN, Harvard Medical School and Massachusetts Institute of Technology DANIEL BURCH, Pharmaceutical Product Development, LLC JOSEPH BUXBAUM, Icahn School of Medicine at Mount Sinai SARAH CADDICK, Gatsby Charitable Foundation ROSA CANET-AVILES, Foundation for the National Institutes of Health MARIA CARRILLO, Alzheimer’s Association E. ANTONIO CHIOCCA, Harvard Medical School TIMOTHY COETZEE, National Multiple Sclerosis Society JONATHAN COHEN, Princeton University ROBERT CONLEY, Eli Lilly and Company (from October 2018) JAMES DESHLER, National Science Foundation BILLY DUNN, Food and Drug Administration MICHAEL EGAN, Merck Research Laboratories JOSHUA GORDON, National Institute of Mental Health HENRY T. GREELY, Stanford University RAQUEL GUR, University of Pennsylvania MAGALI HAAS, Cohen Veterans Bioscience RAMONA HICKS, One Mind RICHARD HODES, National Institute on Aging STUART HOFFMAN, Department of Veterans Affairs STEVEN HYMAN, Broad Institute of Massachusetts Institute of Technology and Harvard University MICHAEL IRIZARRY, Eli Lilly and Company (until October 2018) FRANCES JENSEN, University of Pennsylvania GEORGE KOOB, National Institute on Alcohol Abuse and Alcoholism 1The National Academies of Sciences, Engineering, and Medicine’s forums and round- tables do not issue, review, or approve individual documents. The responsibility for the published Proceedings of a Workshop rests with the workshop rapporteurs and the institution. vii PREPUBLICATION COPY: UNCORRECTED PROOFS

WALTER KOROSHETZ, National Institute of Neurological Disorders and Stroke ALAN LESHNER, American Association for the Advancement of Science (Emeritus) HUSSEINI MANJI, Janssen Research & Development, LLC CAROLINE MONTOJO, The Kavli Foundation ATUL PANDE, Tal Medical STEVEN PAUL, Voyager Therapeutics, Inc. EMILIANGELO RATTI, Takeda Pharmaceuticals International, Inc. DOUGLAS SHEELEY, National Institute of Dental and Craniofacial Research TODD SHERER, The Michael J. Fox Foundation for Parkinson’s Research DAVID SHURTLEFF, National Center for Complementary and Integrative Health PAUL SIEVING, National Eye Institute NORA VOLKOW, National Institute on Drug Abuse ANDREW WELCHMAN, Wellcome Trust DOUG WILLIAMSON, Lundbeck STEVIN ZORN, MindImmune Therapeutics, Inc. Health and Medicine Division Staff CLARE STROUD, Forum Director SHEENA M. POSEY NORRIS, Program Officer DANIEL FLYNN, Research Associate (until November 2018) PHOENIX WILSON, Senior Program Assistant BARDIA MASSOUDKHAN, Financial Associate ANDREW M. POPE, Senior Director, Board on Health Sciences Policy viii PREPUBLICATION COPY: UNCORRECTED PROOFS

Reviewers This Proceedings of a Workshop was reviewed in draft form by individuals chosen for their diverse perspectives and technical expertise. The purpose of this independent review is to provide candid and critical comments that will assist the National Academies of Sciences, Engineering, and Medicine in making each published proceedings as sound as possible and to ensure that it meets the institutional standards for quality, objectivity, evidence, and responsiveness to the charge. The review comments and draft manuscript remain confidential to protect the integrity of the process. We thank the following individuals for their review of this proceedings: ROBERT DESIMONE, Massachusetts Institute of Technology HENRY T. GREELY, Stanford University JON HENNEBOLD, Oregon National Primate Research Center KAREN PARKER, Stanford University Although the reviewers listed above provided many constructive comments and suggestions, they were not asked to endorse the content of the proceedings nor did they see the final draft before its release. The review of this proceedings was overseen by ELI ADASHI, Brown University. He was responsible for making certain that an independent examination of this proceedings was carried out in accordance with standards of the National Academies and that all review comments were carefully considered. Responsibility for the final content rests entirely with the rapporteurs and the National Academies. ix PREPUBLICATION COPY: UNCORRECTED PROOFS

Contents 1 INTRODUCTION AND BACKGROUND 1 Workshop Objectives, 3 Organization of the Proceedings, 5 2 GENETICALLY MODIFIED NONHUMAN PRIMATE MODELS FOR NEUROSCIENCE RESEARCH: RATIONALE AND OVERVIEW OF POTENTIAL OPPORTUNITIES AND CHALLENGES 7 Overcoming the Limitations of Mouse Models with Nonhuman Primates, 8 Opportunities Provided by Nonhuman Primate Models to Foster Neuroscience Research, 9 Challenges of Genetically Modified Nonhuman Primate Models, 10 3 STATE OF THE SCIENCE OF TRANSGENIC NONHUMAN PRIMATE MODELS FOR NERVOUS SYSTEM DISORDERS 15 Genetically Modified Nonhuman Primate Models of Disease, 17 Gene Modification as Therapy, 23 4 TRANSLATING RESEARCH FROM NONHUMAN PRIMATES TO HUMANS 27 A Translational Research Roadmap in Autism, 28 Assessment Tools for Nonhuman Primates, 30 Brain Mapping and Imaging in Genetically Modified Nonhuman Primates, 31 xi PREPUBLICATION COPY: UNCORRECTED PROOFS

xii CONTENTS 5 BIOETHICAL CONSIDERATIONS FOR TRANSGENIC NONHUMAN PRIMATE MODELS IN NEUROSCIENCE RESEARCH 35 3R Principles and Harm–Benefit, 36 Importance of Proactive Communi6ation with the Public, 41 6 UNDERSTANDING THE POLICY, INFRASTRUCTURE, AND FUNDING NEEDED TO ADVANCE NEUROSCIENCE RESEARCH 43 Primate Research Centers, 44 Sharing Information and Data, 47 Training and Educating the Next Generation of Researchers, 48 Organizing Efforts to Meet Infrastructure and Scientific Needs, 49 Final Remarks, 50 APPENDIXES A References 53 B Workshop Agenda 61 C Registered Attendees 69 PREPUBLICATION COPY: UNCORRECTED PROOFS

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To examine the promise, concerns, and challenges related to neuroscience research using genetically modified nonhuman primates, the National Academies of Sciences, Engineering, and Medicine hosted a public workshop on October 4, 2018, bringing together an international group of experts and stakeholders representing academia, industry, laboratory animal management, disease-focused foundations, and federal agencies. The workshop was designed to explore the current state and future promise of research using genetically modified nonhuman primate models of disease to understand the complex functions of the brain that control behavior, movement, and cognition in both health and disease states. This publication summarizes the presentations and discussions from the workshop.

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