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Suggested Citation:"Appendix A: References." 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:"Appendix A: References." 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:"Appendix A: References." 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:"Appendix A: References." 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.
×
Page 56
Suggested Citation:"Appendix A: References." 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.
×
Page 57
Suggested Citation:"Appendix A: References." 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.
×
Page 58
Suggested Citation:"Appendix A: References." 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.
×
Page 59
Suggested Citation:"Appendix A: References." 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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A References Acland, G. M., G. D. Aguirre, J. Ray, Q. Zhang, T. S. Aleman, A. V. Cideciyan, S. E. Pearce-Kelling, V. Anand, Y. Zeng, A. M. Maguire, S. G. Jacobson, W. W. Hauswirth, and J. Bennett. 2001. Gene therapy restores vision in a canine model of childhood blindness. Nature Genetics 28(1):92–95. Agustin-Pavon, C., K. Braesicke, Y. Shiba, A. M. Santangelo, Y. Mikheenko, G. Cockroft, F. Asma, H. Clarke, M. S. Man, and A. C. Roberts. 2012. Lesions of ventrolateral prefrontal or anterior orbitofrontal cortex in primates heighten negative emotion. Biological Psychiatry 72(4):266–272. Akerboom, J., T. W. Chen, T. J. Wardill, L. Tian, J. S. Marvin, S. Mutlu, N. C. Calderon, F. Esposti, B. G. Borghuis, X. R. Sun, A. Gordus, M. B. Orger, R. Portugues, F. Engert, J. J. Macklin, A. Filosa, A. Aggarwal, R. A. Kerr, R. Takagi, S. Kracun, E. Shigetomi, B. S. Khakh, H. Baier, L. Lagnado, S. S. Wang, C. I. Bargmann, B. E. Kimmel, V. Jayaraman, K. Svoboda, D. S. Kim, E. R. Schreiter, and L. L. Looger. 2012. Optimization of a GCaMP calcium indicator for neural activity imaging. Journal of Neuroscience 32(40):13819– 13840. Alexander, L., P. L. Gaskin, S. J. Sawiak, T. D. Fryer, Y. T. Hong, G. J. Cockcroft, H. F. Clarke, and A. C. Roberts, 2018. Fractionating blunted reward processing characteristic of anhedonia by over-activating primate subgenual anterior cingulate cortex. Neuron 101:1–14. Amado, D., F. Mingozzi, D. Hui, J. L. Bennicelli, Z. Wei, Y. Chen, E. Bote, R. L. Grant, J. A. Golden, K. Narfstrom, N. A. Syed, S. E. Orlin, K. A. High, A. M. Maguire, and J. Bennett. 2010. Safety and efficacy of subretinal readministration of a viral vector in large animals to treat congenital blindness. Science Translational Medicine 2(21):21ra16. Amaral, D. G., D. Li, L. Libero, M. Solomon, J. Van de Water, A. Mastergeorge, L. Naigles, S. Rogers, and C. Wu Nordahl. 2017. In pursuit of neurophenotypes: The consequences of having autism and a big brain. Autism Research 10(5):711–722. 53 PREPUBLICATION COPY: UNCORRECTED PROOFS

54 TRANSGENIC NEUROSCIENCE RESEARCH APA (American Psychiatric Association). 2013. Diagnostic and statistical manual of mental disorders (DSM-5®). Arlington, VA: American Psychiatric Association. Bass, J., and J. S. Takahashi. 2010. Circadian integration of metabolism and energetics. Science 330(6009):1349–1354. Belmonte, J. C. I., E. M. Callaway, P. Churchland, S. J. Caddick, G. Feng, G. E. Homanics, K.-F. Lee, D. A. Leopold, C. T. Miller, J. F. Mitchell, S. Mitalipov, A. R. Moutri, J. A. Movshon, H. Okano, J. H. Reynolds, D. Ringach, T. J. Sejnowski, A. C. Silva, P. L. Strick, J. Wu, and F. Zhang. 2015. Brains, genes and primates. Neuron 86(3):617–631. Bernier, R., C. Golzio, B. Xiong, H. A. Stessman, B. P. Coe, O. Penn, K. Witherspoon, J. Gerdts, C. Baker, A. T. Vulto-van Silfhout, J. H. Schuurs- Hoeijmakers, M. Fichera, P. Bosco, S. Buono, A. Alberti, P. Failla, H. Peeters, J. Steyaert, L. Vissers, L. Francescatto, H. C. Mefford, J. A. Rosenfeld, T. Bakken, B. J. O’Roak, M. Pawlus, R. Moon, J. Shendure, D. G. Amaral, E. Lein, J. Rankin, C. Romano, B. B. A. de Vries, N. Katsanis, and E. E. Eichler. 2014. Disruptive CHD8 mutations define a subtype of autism early in development. Cell 158(2):263–276. Broussard, G. J., R. Liang, and L. Tian. 2014. Monitoring activity in neural circuits with genetically encoded indicators. Frontiers in Molecular Neuroscience 7:97. Chamberlain, S. R., N. A. Fineberg, A. D. Blackwell, T. W. Robbins, and B. J. Sahakian. 2006. Motor inhibition and cognitive flexibility in obsessive- compulsive disorder and trichotillomania. American Journal of Psychiatry 163(7):1282–1284. Chan, A. W., J. Jiang, Y. Chen, C. Li, M. S. Prucha, Y. Hu, T. Chi, S. Moran, T. Rahim, S. Li, X. Li, S. M. Zola, C. M. Testa, H. Mao, R. Villalba, Y. Smith, X. Zhang, and J. Bachevalier. 2015. Progressive cognitive deficit, motor impairment and striatal pathology in a transgenic Huntington disease monkey model from infancy to adulthood. PLoS ONE 10(5):e0122335. Chan, K. Y., M. J. Jang, B. B. Yoo, A. Greenbaum, N. Ravi, W. L. Wu, L. Sanchez-Guardado, C. Lois, S. K. Mazmanian, B. E. Deverman, and V. Gradinaru. 2017. Engineered AAVs for efficient noninvasive gene delivery to the central and peripheral nervous systems. Nature Neuroscience 20(8):1172–1179. Chang, L., Q. Fang, S. Zhang, M. M. Poo, and N. Gong. 2015. Mirror-induced self-directed behaviors in rhesus monkeys after visual-somatosensory training. Current Biology 25(2):212–217. Chang, L., S. Zhang, M. M. Poo, and N. Gong. 2017. Spontaneous expression of mirror self-recognition in monkeys after learning precise visual- PREPUBLICATION COPY: UNCORRECTED PROOFS

APPENDIX A 55 proprioceptive association for mirror images. Proceedings of the National Academy of Sciences of the United States of America 114(12):3258–3263. Constantino, J. N., and R. D. Todd. 2003. Autistic traits in the general population: A twin study. Archives of General Psychiatry 60(5):524–530. Deverman, B. E., P. L. Pravdo, B. P. Simpson, S. R. Kumar, K. Y. Chan, A. Banerjee, W. L. Wu, B. Yang, N. Huber, S. P. Pasca, and V. Gradinaru. 2016. Cre-dependent selection yields AAV variants for widespread gene transfer to the adult brain. Nature Biotechnology 34(2):204–209. Dias, R., T. W. Robbins, and A. C. Roberts. 1996. Dissociation in prefrontal cortex of affective and attentional shifts. Nature 380(6569):69–72. Durand, C. M., C. Betancur, T. M. Boeckers, J. Bockmann, P. Chaste, F. Fauchereau, G. Nygren, M. Rastam, I. C. Gillberg, H. Anckarsater, E. Sponheim, H. Goubran-Botros, R. Delorme, N. Chabane, M. C. Mouren- Simeoni, P. de Mas, E. Bieth, B. Roge, D. Heron, L. Burglen, C. Gillberg, M. Leboyer, and T. Bourgeron. 2007. Mutations in the gene encoding the synaptic scaffolding protein SHANK3 are associated with autism spectrum disorders. Nature Genetics 39(1):25–27. Emborg, M. E. 2007. Nonhuman primate models of Parkinson’s disease. ILAR Journal 48(4):339–355. Feigin, V. L., A. A. Abajobir, K. H. Abate, F. Abd-Allah, A. M. Abdulle, S. F. Abera, G. Y. Abyu, M. B. Ahmed, A. N. Aichour, I. Aichour, and M. T. E. Aichour. 2017. Global, regional, and national burden of neurological disorders during 1990–2015: A systematic analysis for the Global Burden of Disease Study 2015. The Lancet Neurology 16(11):877–897. Friedman, H., N. Ator, N. Haigwood, W. Newsome, J. S. Allan, T. G. Golos, J. H. Kordower, R. E. Shade, M. E. Goldberg, M. R. Bailey, and P. Bianchi. 2017. The critical role of nonhuman primates in medical research. Pathogens & Immunity 2(3):352–365. Ghosh, K. K., L. D. Burns, E. D. Cocker, A. Nimmerjahn, Y. Ziv, A. E. Gamal, and M. J. Schnitzer. 2011. Miniaturized integration of a fluorescence microscope. Nature Methods 8(10):871–878. Hyman, S. E. 2012. Revolution stalled. Science Translational Medicine 4(155): 155cm11. Hyman, S. E. 2016. Back to basics: Luring industry back into neuroscience. Nature Neuroscience 19(11):1383. IOM (Institute of Medicine). 2013. Improving the utility and translation of animal models for nervous system disorders: Workshop summary. Washington, DC: The National Academies Press. IOM. 2014. Improving and accelerating therapeutic development for nervous system disorders: Workshop summary. Washington, DC: The National Academies Press. PREPUBLICATION COPY: UNCORRECTED PROOFS

56 TRANSGENIC NEUROSCIENCE RESEARCH IOM and NRC (National Research Council). 2011. Chimpanzees in biomedical and behavioral research: Assessing the necessity. Washington, DC: The National Academies Press. Jennings, C., R. Landman, Y. Zhou, J. Sharma, J. Hyman, J. A. Movshon, Z. Qiu, A. Roberts, A. W. Roe, X. Wang, and H. Zhou. 2016. Opportunities and challenges in modeling human brain disorders in transgenic primates. Nature Neuroscience 19(9):1123–1130. Kaas, H. H. 2013. The evolution of brains from early mammals to humans. Wiley Interdisciplinary Review of Cognitive Sciences 4:33–45. Kaiser, T., and Feng, G., 2015. Modeling psychiatric disorders for developing effective treatments. Nature Medicine 21(9):979–988. Kalia, L. V., and A. E. Lang. 2015. Parkinson’s disease. Lancet 386(9996):896– 912. Kirk, R. G. W. 2018. Recovering the principles of humane experimental technique: The 3Rs and the human essence of animal research. Science, Technology, & Human Values 43(4):622–648. Kola, I., and J. Landis. 2004. Can the pharmaceutical industry reduce attrition rates? Nature Reviews Drug Discovery 3(8):711–715. Kondo, T., R. Saito, M. Otaka, K. Yoshino-Saito, A. Yamanaka, T. Yamamori, A. Watakabe, H. Mizukami, M. J. Schnitzer, K. F. Tanaka, J. Ushiba, and H. Okano. 2018. Calcium transient dynamics of neural ensembles in the primary motor cortex of naturally behaving monkeys. Cell Reports 24(8):2191–2195. Kostic, C., and Y. Arsenijevic. 2016. Animal modelling for inherited central vision loss. Journal of Pathology 238(2):300–310. Kruger, R., W. Kuhn, K. L. Leenders, R. Sprengelmeyer, T. Muller, D. Woitalla, A. T. Portman, R. P. Maguire, L. Veenma, U. Schroder, L. Schols, J. T. Epplen, O. Riess, and H. Przuntek. 2001. Familial parkinsonism with synuclein pathology: Clinical and PET studies of a30p mutation carriers. Neurology 56(10):1355–1362. Lemon, R. N. 2018. Applying the 3Rs to neuroscience research involving nonhuman primates. Drug Discovery Today 23(9):1574–1577. Liu, Z., X. Li, J. T. Zhang, Y. J. Cai, T. L. Cheng, C. Cheng, Y. Wang, C. C. Zhang, Y. H. Nie, Z. F. Chen, W. J. Bian, L. Zhang, J. Xiao, B. Lu, Y. F. Zhang, X. D. Zhang, X. Sang, J. J. Wu, X. Xu, Z. Q. Xiong, F. Zhang, X. Yu, N. Gong, W. H. Zhou, Q. Sun, and Z. Qiu. 2016a. Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MECP2. Nature 530(7588):98–102. Liu, Z., Y. H. Nie, C. C. Zhang, Y. J. Cai, Y. Wang, H. P. Lu, Y. Z. Li, C. Cheng, Z. L. Qiu, and Q. Sun. 2016b. Generation of macaques with sperm derived from juvenile monkey testicular xenografts. Cell Research 26(1):139–142. PREPUBLICATION COPY: UNCORRECTED PROOFS

APPENDIX A 57 Liu, Z., Y. Cai, Y. Wang, Y. Nie, C. Zhang, Y. Xu, X. Zhang, Y. Lu, Z. Wang, M. Poo, and Q. Sun. 2018. Cloning of macaque monkeys by somatic cell nuclear transfer. Cell 172(4):881–887. Mancuso, K., W. W. Hauswirth, Q. Li, T. B. Connor, J. A. Kuchenbecker, M. C. Mauck, J. Neitz, and M. Neitz. 2009. Gene therapy for red-green colour blindness in adult primates. Nature 461(7265):784–787. Meng, Y., J. Jiang, J. Bachevalier, X. Zhang, and A. W. Chan. 2017. Developmental whole brain white matter alterations in transgenic Huntington’s disease monkey. Scientific Reports 7(1):379. Miller, C. T., W. A. Freiwald, D. A. Leopold, J. F. Mitchell, A. C. Silva, and X. Wang. 2016. Marmosets: A neuroscientific model of human social behavior. Neuron 90(2):219–233. Nager, A. B., and R. D. Atkinson. 2016. A trillion-dollar opportunity: How brain research can drive health and prosperity. Information Technology & Innovation Foundation 1–31. NASEM (National Academies of Sciences, Engineering, and Medicine). 2017. Therapeutic development in the absence of predictive animal models of nervous system disorders: Proceedings of a workshop. Washington, DC: The National Academies Press. Nayerossadat, N., T. Maedeh, and P. A. Ali. 2012. Viral and nonviral delivery systems for gene delivery. Advanced Biomedical Research 1:27. Okano, H., and N. Kishi. 2018. Investigation of brain science and neurological/psychiatric disorders using genetically modified non-human primates. Current Opinion in Neurobiology 50:1–6. Oztan, O., J. P. Garner, S. Partap, E. H. Sherr, A. Y. Hardan, C. Farmer, A. Thurm, S. E. Swedo, and K. J. Parker. 2018. Cerebrospinal fluid vasopressin and symptom severity in children with autism. Annals of Neurology 84(4):611– 615. Park, J. E., X. F. Zhang, S. H. Choi, J. Okahara, E. Sasaki, and A. C. Silva. 2016. Generation of transgenic marmosets expressing genetically encoded calcium indicators. Scientific Reports 6:34931. Parker, K. J., J. P. Garner, O. Oztan, E. R. Tarara, J. Li, V. Sclafani, L. A. Del Rosso, K. Chun, S. W. Berquist, M. G. Chez, S. Partap, A. Y. Hardan, E. H. Sherr, and J. P. Capitanio. 2018. Arginine vasopressin in cerebrospinal fluid is a marker of sociality in nonhuman primates. Science Translational Medicine 10(439):eaam9100. Poo, M. M., J. L. Du, N. Y. Ip, Z. Q. Xiong, B. Xu, and T. Tan. 2016. China brain project: Basic neuroscience, brain diseases, and brain-inspired computing. Neuron 92(3):591–596. Prescott, M. J., J. A. Langermans, and I. Ragan. 2017. Applying the 3Rs to non- human primate research: Barriers and solutions. Drug Discovery Today: Disease Models 23:51–56. PREPUBLICATION COPY: UNCORRECTED PROOFS

58 TRANSGENIC NEUROSCIENCE RESEARCH Raper, J., S. Bosinger, Z. Johnson, G. Tharp, S. P. Moran, and A. W. S. Chan. 2016. Increased irritability, anxiety, and immune reactivity in transgenic Huntington’s disease monkeys. Brain, Behavior, and Immunity 58:181–190. Russell, W. M. S., and R. L. Burch. 1959. The principles of humane experimental technique. London, England: Methuen & Co. Sander, J. D., and J. K. Joung. 2014. CRISPR-Cas systems for editing, regulating and targeting genomes. Nature Biotechnology 32(4):347–355. Sanders, S. J., X. He, A. J. Willsey, A. G. Ercan-Sencicek, K. E. Samocha, A. E. Cicek, M. T. Murtha, V. H. Bal, S. L. Bishop, S. Dong, and A. P. Goldberg. 2015. Insights into autism spectrum disorder genomic architecture and biology from 71 risk loci. Neuron 87(6):1215–1233. Santangelo, A. M., M. Ito, Y. Shiba, H. F. Clarke, E. H. Schut, G. Cockcroft, A. C. Ferguson-Smith, and A. C. Roberts. 2016. Novel primate model of serotonin transporter genetic polymorphisms associated with gene expression, anxiety and sensitivity to antidepressants. Neuropsychopharmacology 41(9):2366– 2376. Sasaki, E., H. Suemizu, A. Shimada, K. Hanazawa, R. Oiwa, M. Kamioka, I. Tomioka, Y. Sotomaru, R. Hirakawa, T. Eto, S. Shiozawa, T. Maeda, M. Ito, R. Ito, C. Kito, C. Yagihashi, K. Kawai, H. Miyoshi, Y. Tanioka, N. Tamaoki, S. Habu, H. Okano, and T. Nomura. 2009. Generation of transgenic non- human primates with germline transmission. Nature 459(7246):523–527. Sato, K., R. Oiwa, W. Kumita, R. Henry, T. Sakuma, R. Ito, R. Nozu, T. Inoue, I. Katano, K. Sato, N. Okahara, J. Okahara, Y. Shimizu, M. Yamamoto, K. Hanazawa, T. Kawakami, Y. Kametani, R. Suzuki, T. Takahashi, E. J. Weinstein, T. Yamamoto, Y. Sakakibara, S. Habu, J. Hata, H. Okano, and E. Sasaki. 2016. Generation of a nonhuman primate model of severe combined immunodeficiency using highly efficient genome editing. Cell Stem Cell 19(1):127–138. Sawiak, S. J., Y. Shiba, L. Oikonomidis, C. P. Windle, A. M. Santangelo, H. Grydeland, G. Cockcroft, E. T. Bullmore, and A. C. Roberts. 2018. Trajectories and milestones of cortical and subcortical development of the marmoset brain from infancy to adulthood. Cerebral Cortex 28(12):4440–4453. Sclafani, V., L. A. Del Rosso, S. K. Seil, L. A. Calonder, J. E. Madrid, K. J. Bone, E. H. Sherr, J. P. Garner, J. P. Capitanio, and K. J. Parker. 2016. Early predictors of impaired social functioning in male rhesus macaques (macaca mulatta). PLoS ONE 11(10):e0165401. Shiba, Y., L. Oikonomidis, S. Sawiak, T. D. Fryer, Y. T. Hong, G. Cockcroft, A. M. Santangelo, and A. C. Roberts. 2017. Converging prefronto-insula-amygdala pathways in negative emotion regulation in marmoset monkeys. Biological Psychiatry 82(12):895–903. PREPUBLICATION COPY: UNCORRECTED PROOFS

APPENDIX A 59 The Marmoset Genome Sequencing and Analysis Consortium, K. C. Worley, W. C. Warren, J. Rogers, D. Locke, D. M. Muzny, E. R. Mardis, G. M. Weinstock, S. D. Tardif, K. M. Aagaard, and N. Archidiacono. 2014. The common marmoset genome provides insight into primate biology and evolution. Nature Genetics 46(8):850–857. Vasireddy, V., J. A. Mills, R. Gaddameedi, E. Basner-Tschakarjan, M. Kohnke, A. D. Black, K. Alexandrov, S. Zhou, A. M. Maguire, D. C. Chung, H. Mac, L. Sullivan, P. Gadue, J. L. Bennicelli, D. L. French, and J. Bennett. 2013. AAV-mediated gene therapy for choroideremia: Preclinical studies in personalized models. PLoS ONE 8(5):e61396. Veenstra-VanderWeele, J., and R. D. Blakely. 2012. Networking in autism: Leveraging genetic, biomarker and model system findings in the search for new treatments. Neuropsychopharmacology 37(1):196–212. Wen, Z., T. L. Cheng, G. Z. Li, S. B. Sun, S. Y. Yu, Y. Zhang, Y. S. Du, and Z. Qiu. 2017. Identification of autism-related MECP2 mutations by whole- exome sequencing and functional validation. Molecular Autism 8(1):43. Yang, S. H., P. H. Cheng, H. Banta, K. Piotrowska-Nitsche, J. J. Yang, E. C. Cheng, B. Snyder, K. Larkin, J. Liu, J. Orkin, Z. H. Fang, Y. Smith, J. Bachevalier, S. M. Zola, S. H. Li, X. J. Li, and A. W. Chan. 2008. Towards a transgenic model of Huntington's disease in a non-human primate. Nature 453(7197):921–924. 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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