Modeling Rett Syndrome Using TALEN-Edited MECP2 Mutant Cynomolgus Monkeys
Open accessAbstract
Gene-editing technologies have made it feasible to create nonhuman primate models for human genetic disorders. Here, we report detailed genotypes and phenotypes of TALEN-edited MECP2 mutant cynomolgus monkeys serving as a model for a neurodevelopmental disorder, Rett syndrome (RTT), which is caused by loss-of-function mutations in the human MECP2 gene. Male mutant monkeys were embryonic lethal, reiterating that RTT is a disease of females. Through a battery of behavioral analyses, including primate-unique eye-tracking tests, in combination with brain imaging via MRI, we found a series of physiological, behavioral, and structural abnormalities resembling clinical manifestations of RTT. Moreover, blood transcriptome profiling revealed that mutant monkeys resembled RTT patients in immune gene dysregulation. Taken together, the stark similarity in phenotype and/or endophenotype between monkeys and patients suggested that gene-edited RTT founder monkeys would be of value for disease mechanistic studies as well as development of potential therapeutic interventions for RTT.
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Genome editing in nonhuman primates has been used to generate models of Duchenne muscular dystrophy by dystrophin disruption, microcephaly by MCPH1 disruption, and Rett syndrome by MECP2 disruption.
“used to generate models of neurological and related diseases: disruption of the dystrophin gene to model Duchenne muscular dystrophy29, disruption of the MCPH1 gene to model microcephaly30, and disruption of the MECP2 gene to model Rett syndrome31.”
From CRISPR-based functional genomics for neurological disease (2020) · cites this paper as [31]
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Cites
Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing
Benjamini, Y., & Hochberg, Y. (1995) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1995.tb02031.x · Cited by 109,482 · see citing works
WGCNA: an R package for weighted correlation network analysis
Langfelder, P., & Horvath, S. (2008) · BMC Bioinformatics · doi:10.1186/1471-2105-9-559 · Cited by 27,252 · see citing works
Observational study of behavior: sampling methods
Altmann, J. (1974) · Behaviour · doi:10.1163/156853974x00534 · Cited by 13,891 · see citing works
TopHat: discovering splice junctions with RNA-Seq
Trapnell, C., Pachter, L. S., & Salzberg, S. L. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp120 · Cited by 11,477 · see citing works
A General Framework for Weighted Gene Co-Expression Network Analysis
Zhang, B., & Horvath, S. (2005) · Statistical Applications in Genetics and Molecular Biology · doi:10.2202/1544-6115.1128 · Cited by 5,684 · see citing works
Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2
Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U., & Zoghbi, H. Y. (1999) · Nature Genetics · doi:10.1038/13810 · Cited by 4,990 · see citing works
Yang, H., Wang, H., Shivalila, C. S., Cheng, A. W., Shi, L., & Jaenisch, R. (2013) · Cell · doi:10.1016/j.cell.2013.08.022 · Cited by 1,596 · see citing works
Diffeomorphic demons: Efficient non-parametric image registration
Vercauteren, T. K., Pennec, X., Aymeric Perchant, B., & Ayache, N. (2008) · NeuroImage · doi:10.1016/j.neuroimage.2008.10.040 · Cited by 1,589 · see citing works
A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome
Guy, J., Hendrich, B., Holmes, M., Martin, J. E., & Bird, A. (2001) · Nature Genetics · doi:10.1038/85899 · Cited by 1,558 · see citing works
Hagberg, B. A., Aicardi, J. F., Dias, K., & Ramos, O. (1983) · Annals of Neurology · doi:10.1002/ana.410140412 · Cited by 1,515 · see citing works
Rett syndrome: Revised diagnostic criteria and nomenclature
Neul, J. L., Kaufmann, W. E., Glaze, D. G., Christodoulou, J., Clarke, A. J., Bahi‐Buisson, N., Leonard, H., Bailey, M. E. S., Schanen, N. C., Zappella, M., et al. (2010) · Annals of Neurology · doi:10.1002/ana.22124 · Cited by 1,398 · see citing works
Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice
Chen, R. Z., Akbarian, S., Tudor, M., & Jaenisch, R. (2001) · Nature Genetics · doi:10.1038/85906 · Cited by 1,275 · see citing works
(1966) · PubMed · Cited by 708 · see citing works
An update on clinically applicable diagnostic criteria in Rett syndrome
Hagberg, B. A., Hanefeld, F. A., Percy, A. K., & Skjeldal, O. H. (2002) · European Journal of Paediatric Neurology · doi:10.1053/ejpn.2002.0612 · Cited by 394 · see citing works
Stepwise evolution of stable sociality in primates
Shultz, S., Opie, C., & Atkinson, Q. D. (2011) · Nature · doi:10.1038/nature10601 · Cited by 373 · see citing works
Autism-like behaviours and germline transmission in transgenic monkeys overexpressing MeCP2
Liu, Z., Li, X., Zhang, J.-T., Cai, Y.-J., Cheng, T.-L., Cheng, C., Wang, Y., Zhang, C.-C., Nie, Y.-H., Chen, Z.-F., et al. (2016) · Nature · doi:10.1038/nature16533 · Cited by 322 · see citing works
Self-citationBelmonte, J. C. I., Callaway, E. M., Caddick, S. J., Churchland, P. S., Feng, G., Homanics, G. E., Lee, K., Leopold, D. A., Miller, C. T., Mitchell, J. F., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.021 · Cited by 269 · see citing works
Torsten Rohlfing, B., Kroenke, C. D., Sullivan, E. V., Dubach, M. F., Bowden, D. M., Grant, K. A., & Pfefferbaum, A. (2012) · Frontiers in Neuroinformatics · doi:10.3389/fninf.2012.00027 · Cited by 262 · see citing works
LINKS: Learning-based multi-source IntegratioN frameworK for Segmentation of infant brain images
Wang, L., Gao, Y., Shi, F., Li, G., Gilmore, J. H., Lin, W., & Shen, D. G. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2014.12.042 · Cited by 231 · see citing works
Self-citationThe significance of QT interval in drug development
Shah, R. R. (2002) · British Journal of Clinical Pharmacology · doi:10.1046/j.1365-2125.2002.01627.x · Cited by 231 · see citing works
MECP2 disorders: from the clinic to mice and back
Lombardi, L. M., Baker, S. A., & Zoghbi, H. Y. (2015) · Journal of Clinical Investigation · doi:10.1172/jci78167 · Cited by 221 · cited 1× · see citing works
“It is interesting that RTT-related neurological phenotypes mostly occur in adult male rodents, which is different from the human disease (Lombardi et al., 2015; Patterson et al., 2016; Chen et al., 2001; Glaze, 2004; Guy et al., 2001).”
Neuroanatomy of Rett syndrome: A volumetric imaging study
Reiss, A. L., Faruque, F., Naidu, S., Abrams, M. T., Beaty, T. H., Bryan, R. N., & Moser, H. W. (1993) · Annals of Neurology · doi:10.1002/ana.410340220 · Cited by 202 · see citing works
TALEN-Mediated Gene Mutagenesis in Rhesus and Cynomolgus Monkeys
Liu, H., Chen, Y., Niu, Y., Zhang, K., Kang, Y., Ge, W., Liu, X., Zhao, E., Wang, C., Lin, S., et al. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.01.018 · Cited by 200 · see citing works
Self-citationBehavioral and anatomical abnormalities in Mecp2 mutant mice: A model for Rett syndrome
Stearns, N. A., Schaevitz, L. R., Bowling, H. L., Nag, N., Berger, U. V., & Berger-Sweeney, J. E. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.009 · Cited by 199 · see citing works
Rett Syndrome: Crossing the Threshold to Clinical Translation
Katz, D. M., Bird, A., Coenraads, M., Gray, S. J., Menon, D. U., Philpot, B. D., & Tarquinio, D. C. (2016) · Trends in Neurosciences · doi:10.1016/j.tins.2015.12.008 · Cited by 150 · see citing works
Subramaniam, B., Naidu, S., & Reiss, A. L. (1997) · Neurology · doi:10.1212/wnl.48.2.399 · Cited by 143 · see citing works
Opportunities and challenges in modeling human brain disorders in transgenic primates
Jennings, C. G. B., Landman, R., Zhou, Y., Sharma, J., Hyman, J. B., Movshon, J. A., Qiu, Z., Roberts, A., Roe, A. W., Wang, X., et al. (2016) · Nature Neuroscience · doi:10.1038/nn.4362 · Cited by 140 · see citing works
Li, G., Nie, J., Wang, L., Shi, F., Gilmore, J. H., Lin, W., & Shen, D. G. (2014) · NeuroImage · doi:10.1016/j.neuroimage.2013.12.038 · Cited by 126 · see citing works
Self-citationSelective Cerebral Volume Reduction in Rett Syndrome: A Multiple-Approach MR Imaging Study
Carter, J. C., Lanham, D. C., Pham, D. L., Bibat, G., Naidu, S., & Kaufmann, W. E. (2007) · American Journal of Neuroradiology · doi:10.3174/ajnr.a0857 · Cited by 108 · see citing works
Ricceri, L., Filippis, B. D., & Giovanni Laviola, A. (2008) · Behavioural Pharmacology · doi:10.1097/fbp.0b013e32830c3645 · Cited by 103 · see citing works
TALENoffer: genome-wide TALEN off-target prediction
Grau, J., Boch, J., & Posch, S. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt501 · Cited by 98 · see citing works
Acoustic startle, prepulse inhibition, and fear-potentiated startle measured in rhesus monkeys
Winslow, J. T., Parr, L. A., & Davis, M. (2002) · Biological Psychiatry · doi:10.1016/s0006-3223(02)01345-8 · Cited by 94 · see citing works
Neonatal Encephalopathy in Two Boys in Families With Recurrent Rett Syndrome
Schanen, N. C., Kurczynski, T. W., Brunelle, D., Woodcock, M. M., Dure, L. S., & Percy, A. K. (1998) · Journal of Child Neurology · doi:10.1177/088307389801300507 · Cited by 94 · see citing works
Neuroimaging studies in Rett syndrome
Naidu, S., Kaufmann, W. E., Abrams, M. T., Pearlson, G. D., Lanham, D. C., Fredericksen, K., Barker, P. B., Horská, A., Golay, X., Mori, S., et al. (2001) · Brain and Development · doi:10.1016/s0387-7604(01)00381-3 · Cited by 87 · see citing works
Veeraragavan, S., Wan, Y.-W., Connolly, D. R., Hamilton, S. M., Ward, C. S., Soriano, S., Pitcher, M. R., McGraw, C. M., Huang, S. G., Green, J. R., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw178 · Cited by 59 · see citing works
Self-citationSocial Preferences in Rett Syndrome
Djukic, A., & McDermott, M. V. (2012) · Pediatric Neurology · doi:10.1016/j.pediatrneurol.2012.01.011 · Cited by 58 · see citing works
Circadian rhythm disruption in a mouse model of Rett syndrome circadian disruption in RTT
Li, Q., Loh, D. H., Kudo, T., Truong, D. A., Derakhshesh, M., Kaswan, Z. A. M., Ghiani, C. A., Tsoa, R. W., Cheng, Y., Sun, Y. E., et al. (2015) · Neurobiology of Disease · doi:10.1016/j.nbd.2015.03.009 · Cited by 58 · see citing works
Self-citationExperience-independent sex differences in newborn macaques: Females are more social than males
Simpson, E. A., Nicolini, Y., Shetler, M., Suomi, S. J., Ferrari, P. F., & Paukner, A. (2016) · Scientific Reports · doi:10.1038/srep19669 · Cited by 51 · see citing works
Rett syndrome: Of girls and mice—Lessons for regression in autism
Glaze, D. G. (2004) · Mental Retardation and Developmental Disabilities Research Reviews · doi:10.1002/mrdd.20030 · Cited by 50 · see citing works
MeCP2 deficiency results in robust Rett-like behavioural and motor deficits in male and female rats
Patterson, K. C., Hawkins, V. E., Arps, K. M., Mulkey, D. K., & Olsen, M. L. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw179 · Cited by 40 · see citing works
Sleep and social status in captive gelada baboons (Theropithecus gelada)
Noser, R., Gygax, L., & Tobler, I. (2003) · Behavioural Brain Research · doi:10.1016/s0166-4328(03)00111-6 · Cited by 29 · see citing works
Identifying patterns of communicative behaviors in girls with Rett syndrome
Hetzroni, O. E., & Rubin, C. (2006) · Augmentative and Alternative Communication · doi:10.1080/17461390500387320 · Cited by 28 · see citing works
Qin, D., Rizak, J. D., Feng, X., Yang, S., Yang, L., Fan, X.-N., Lü, L., Chen, L., & Hu, X. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.10.001 · Cited by 16 · see citing works
Self-citationRegional cerebral blood flow abnormalities in Rett syndrome.
BJURE, J., Uvebrant, P., Vestergren, E., & Hagberg, B. A. (1997) · PubMed · Cited by 10 · see citing works
Rapid Determination of the Thermal Nociceptive Threshold in Diabetic Rats
Alshahrani, S., Fernandez-Conti, F., de Araújo, A. A., & DiFulvio, M. (2012) · Journal of Visualized Experiments · doi:10.3791/3785 · Cited by 9 · see citing works
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- Subramaniam B Naidu S Reiss AL 1997 Neuroanatomyin Rett syndrome: Cerebral cortex and posterior fossa Neurology 48 399 407 9040729
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Li, H., Yang, Y., Hong, W., Huang, M., Wu, M., & Zhao, X. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-019-0089-y · Cited by 1,771 · see citing works
Atypical behaviour and connectivity in SHANK3-mutant macaques
Zhou, Y., Sharma, J., Ke, Q., Landman, R., Yuan, J., Chen, H., Hayden, D. S., Fisher, J. S., Jiang, M., Menegas, W., et al. (2019) · Nature · doi:10.1038/s41586-019-1278-0 · Cited by 244 · see citing works
Self-citationRett syndrome: insights into genetic, molecular and circuit mechanisms
Ip, J. P. K., Mellios, N., & Sur, M. (2018) · Nature reviews. Neuroscience · doi:10.1038/s41583-018-0006-3 · Cited by 247 · see citing works
Rett syndrome: a neurological disorder with metabolic components
Kyle, S. M., Vashi, N., & Justice, M. J. (2018) · Open Biology · doi:10.1098/rsob.170216 · Cited by 213 · see citing works
Targeting Homeostatic Synaptic Plasticity for Treatment of Mood Disorders
Kavalali, E. T., & Monteggia, L. M. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.015 · Cited by 179 · see citing works
CRISPR-based functional genomics for neurological disease
Kampmann, M. (2020) · Nature Reviews Neurology · doi:10.1038/s41582-020-0373-z · Cited by 163 · see citing works
The Emerging Clinical Neuroscience of Autism Spectrum Disorder
Muhle, R., Reed, H. E., Stratigos, K. A., & Veenstra-VanderWeele, J. M. (2018) · JAMA Psychiatry · doi:10.1001/jamapsychiatry.2017.4685 · Cited by 166 · see citing works
BMAL1 knockout macaque monkeys display reduced sleep and psychiatric disorders
Qiu, P., Jiang, J., Liu, Z., Cai, Y., Huang, T., Wang, Y., Liu, Q., Nie, Y., Liu, F., Cheng, J., et al. (2019) · National Science Review · doi:10.1093/nsr/nwz002 · Cited by 157 · see citing works
Genome editing in large animals: current status and future prospects
Zhao, J., Lai, L., Ji, W., & Zhou, Q. (2019) · National Science Review · doi:10.1093/nsr/nwz013 · Cited by 126 · see citing works
Self-citationA framework for the investigation of rare genetic disorders in neuropsychiatry
Sanders, S., Şahin, M., Hostyk, J. A., Thurm, A. E., Jacquemont, S., Avillach, P., Douard, E. A., Martin, C. L., Modi, M. E., Moreno-De-Luca, A., et al. (2019) · Nature Medicine · doi:10.1038/s41591-019-0581-5 · Cited by 119 · see citing works
Feng, G., Jensen, F. E., Greely, H. T., Okano, H., Treue, S., Roberts, A., Fox, J. G., Caddick, S. J., Poo, M.-M., Newsome, W. T., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2006515117 · Cited by 118 · see citing works
Single-nucleus transcriptomic landscape of primate hippocampal aging
Zhang, H., Li, J., Ren, J., Sun, S., Ma, S., Zhang, W., Yu, Y., Cai, Y., Yan, K., Li, W., et al. (2021) · Protein & Cell · doi:10.1007/s13238-021-00852-9 · Cited by 119 · see citing works
Self-citationTreating Rett syndrome: from mouse models to human therapies
Vashi, N., & Justice, M. J. (2019) · Mammalian Genome · doi:10.1007/s00335-019-09793-5 · Cited by 111 · see citing works
The array of clinical phenotypes of males with mutations in Methyl‐CpG binding protein 2
Neul, J. L., Benke, T. A., Marsh, E. D., Skinner, S. A., Merritt, J. K., Lieberman, D. N., Standridge, S. M., Feyma, T. J., Heydemann, P. T., Peters, S. U., et al. (2018) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32707 · Cited by 106 · see citing works
Zhao, H., Tu, Z., Xu, H., Yan, S., Yan, H., Zheng, Y., Yang, W., Zheng, J., Li, Z., Tian, R., et al. (2017) · Cell Research · doi:10.1038/cr.2017.95 · Cited by 94 · see citing works
Self-citationLeo Kanner and autism: a 75-year perspective
Harris, J. C. (2018) · International Review of Psychiatry · doi:10.1080/09540261.2018.1455646 · Cited by 91 · see citing works
Hippocampal deficits in neurodevelopmental disorders
Li, Y., Shen, M., Stockton, M. E., & Zhao, X. (2018) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2018.10.001 · Cited by 84 · see citing works
Rett Syndrome and MECP2 Duplication Syndrome: Disorders of MeCP2 Dosage
Collins, B. E., & Neul, J. L. (2022) · Neuropsychiatric Disease and Treatment · doi:10.2147/ndt.s371483 · Cited by 83 · see citing works
Understanding autism spectrum disorders with animal models: applications, insights, and perspectives
Zhu, L., 昆明650500，中国, 云., Zhu, Y., Gu, L., & Cheng, Y. (2021) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.251 · Cited by 84 · see citing works
Gold, W. A., Percy, A. K., Neul, J. L., Cobb, S., Pozzo‐Miller, L. D., Issar, J. K., Ben‐Zeev, B., Vignoli, A., & Kaufmann, W. E. (2024) · Nature Reviews Disease Primers · doi:10.1038/s41572-024-00568-0 · Cited by 80 · see citing works
CRISPR/Cas9-mediated disruption of SHANK3 in monkey leads to drug-treatable autism-like symptoms
Tu, Z., Zhao, H., Li, B., Yan, S., Wang, L., Tang, Y., Li, Z., Bai, D., Li, C., Lin, Y., et al. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy367 · Cited by 73 · see citing works
Self-citationShi, L., Luo, X., Jiang, J., Chen, Y., Liu, C., Hu, T., Li, M., Lin, Q., Li, Y., Huang, J. T., et al. (2019) · National Science Review · doi:10.1093/nsr/nwz043 · Cited by 71 · see citing works
Self-citationGene editing and its applications in biomedicine
Li, G., Li, X., Zhuang, S., Wang, L., Zhu, Y., Chen, Y., Sun, W. C., Wu, Z., Zhou, Z. L., Chen, J., et al. (2022) · Science China Life Sciences · doi:10.1007/s11427-021-2057-0 · Cited by 65 · see citing works
Self-citationPalmieri, M., Pozzer, D., & Landsberger, N. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1172805 · Cited by 65 · see citing works
Nakamura, T., & Takata, A. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02005-2 · Cited by 69 · see citing works
Li, H., Wu, S., Ma, X., Li, X., Cheng, T., Chen, Z., Wu, J., Lv, L., Li, L., Xu, L., et al. (2021) · Neuroscience Bulletin · doi:10.1007/s12264-021-00732-6 · Cited by 51 · see citing works
Self-citationModeling autism in non‐human primates: Opportunities and challenges
Zhao, H., Jiang, Y., & Zhang, Y. (2018) · Autism Research · doi:10.1002/aur.1945 · Cited by 50 · see citing works
Self-citationNakashima, H., Tsujimura, K., Irie, K., Imamura, T., Trujillo, C. A., Ishizu, M., Uesaka, M., Pan, M., Noguchi, H., Okada, K., et al. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109124 · Cited by 50 · see citing works
Applications of Genome Editing Technology in Animal Disease Modeling and Gene Therapy
Li, Q., Qin, Z., Wang, Q., Xu, T., Yang, Y., & He, Z. (2019) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2019.05.006 · Cited by 51 · see citing works
Park, J. E., & Silva, A. C. (2018) · American Journal of Primatology · doi:10.1002/ajp.22931 · Cited by 49 · see citing works
Zhan, Y., Wei, J., Liang, J., Xu, X., He, R., Robbins, T. W., & Wang, Z. (2020) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2020.19101091 · Cited by 49 · see citing works
Self-citationLiu, Y., Shan, L., Liu, T., Li, J., Chen, Y., Sun, C., Yang, C., Bian, X., Niu, Y., Zhang, C., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.02.010 · Cited by 45 · see citing works
Self-citationSaby, J. N., Peters, S. U., Roberts, T. P. L., Nelson, C. A., & Marsh, E. D. (2020) · Frontiers in Integrative Neuroscience · doi:10.3389/fnint.2020.00030 · Cited by 45 · see citing works
Spatially resolved gene regulatory and disease-related vulnerability map of the adult Macaque cortex
Lei, Y., Cheng, M., Li, Z., Zhuang, Z., Wu, L. L., Sun, Y., Han, L., Huang, Z., Wang, Y., Wang, Z., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34413-3 · Cited by 47 · see citing works
Self-citationSleep Disorders in Rett Syndrome and Rett-Related Disorders: A Narrative Review
Tascini, G., Dell’Isola, G. B., Mencaroni, E., Cara, G. D., Striano, P., & Verrotti, A. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.817195 · Cited by 44 · see citing works
Sleep as a translationally-relevant endpoint in studies of autism spectrum disorder (ASD)
Missig, G., McDougle, C. J., & Carlezon, W. A. (2019) · Neuropsychopharmacology · doi:10.1038/s41386-019-0409-5 · Cited by 45 · see citing works
Current advances in primate genomics: novel approaches for understanding evolution and disease
Juan, D., Santpere, G., Kelley, J. L., Cornejo, O. E., & Marquès‐Bonet, T. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-022-00554-w · Cited by 43 · see citing works
de Korte, T., Katili, P. A., Yusof, N. A. N. M., van Meer, B. J., Saleem, U., Burton, F. L., Smith, G. L., Clements, P., Mummery, C. L., Thomas Eschenhagen, A., et al. (2019) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010919-023309 · Cited by 41 · see citing works
Neurogenesis in primates versus rodents and the value of non-human primate models
Zhang, R., Quan, H., Wang, Y., & Luo, F. (2023) · National Science Review · doi:10.1093/nsr/nwad248 · Cited by 42 · see citing works
Deciphering MECP2-associated disorders: disrupted circuits and the hope for repair
Qiu, Z. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.09.004 · Cited by 39 · see citing works
Okano, H., & Kishi, N. (2017) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2017.10.016 · Cited by 40 · see citing works
Multiplex precise base editing in cynomolgus monkeys
Zhang, W., Aida, T., del Rosario, R. C. H., Wilde, J. J., Ding, C., Zhang, X., Baloch, Z., Huang, Y., Tang, Y., Li, D., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-16173-0 · Cited by 39 · see citing works
Mapping hemispheric asymmetries of the macaque cerebral cortex during early brain development
Xia, J., Wang, F., Wu, Z.-W., Wang, L., Zhang, C.-M., Shen, D., & Li, G. (2019) · Human Brain Mapping · doi:10.1002/hbm.24789 · Cited by 35 · see citing works
Self-citationApplication of CRISPR/Cas9 System in Establishing Large Animal Models
Lin, Y., Li, J., Li, C., Tu, Z., Li, S., Li, X., & Yan, S. (2022) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2022.919155 · Cited by 37 · see citing works
Self-citationResearch models of neurodevelopmental disorders: The right model in the right place
Damianidou, E., Mouratidou, L., & Kyrousi, C. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.1031075 · Cited by 36 · see citing works
Genetic approaches to access cell types in mammalian nervous systems
He, M., & Huang, Z. J. (2018) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2018.02.003 · Cited by 33 · see citing works
Genetic Analyses of Alzheimer’s Disease in China: Achievements and Perspectives
Zhang, D., Xu, M., Bi, R., & Yao, Y. (2019) · ACS Chemical Neuroscience · doi:10.1021/acschemneuro.8b00435 · Cited by 32 · see citing works
Ornoy, A., Echefu, B. E., & Becker, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms251910469 · Cited by 33 · see citing works
Genetic engineering in nonhuman primates for human disease modeling
Sato, K., & Sasaki, E. (2017) · Journal of Human Genetics · doi:10.1038/s10038-017-0351-5 · Cited by 32 · see citing works
Modeling SHANK3-associated autism spectrum disorder in Beagle dogs via CRISPR/Cas9 gene editing
Tian, R., Li, Y., Zhao, H., Lyu, W., Zhao, J., Wang, X., Lu, H., Xu, H., Ren, W., Tan, Q.-Q., et al. (2023) · Molecular Psychiatry · doi:10.1038/s41380-023-02276-9 · Cited by 30 · see citing works
The dawn of non-human primate models for neurodevelopmental disorders
Aida, T., & Feng, G. (2020) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2020.05.040 · Cited by 33 · see citing works
Modelling behaviors relevant to brain disorders in the nonhuman primate: Are we there yet?
Scott, J. T., & Bourne, J. A. (2021) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2021.102183 · Cited by 29 · see citing works
Prefrontal circuits guiding social preference: Implications in autism spectrum disorder
Fortier, A. V., Meisner, O. C., Nair, A. R., & Chang, S. W. C. (2022) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2022.104803 · Cited by 30 · see citing works
Therapeutic strategies for autism: targeting three levels of the central dogma of molecular biology
Hong, D., & Iakoucheva, L. M. (2023) · Translational Psychiatry · doi:10.1038/s41398-023-02356-y · Cited by 31 · see citing works
Rett syndrome from bench to bedside: recent advances
Ehinger, Y., Matagne, V., Villard, L., & Roux, J. (2018) · F1000Research · doi:10.12688/f1000research.14056.1 · Cited by 28 · see citing works
Lv, Q., Yan, M., Shen, X., Wu, J., Yu, W., Yan, S., Yang, F., Zeljic, K., Shi, Y., Zhou, Z., et al. (2020) · Cerebral Cortex · doi:10.1093/cercor/bhaa229 · Cited by 28 · see citing works
Self-citationThe behavioral genetics of nonhuman primates: Status and prospects
Rogers, J. (2018) · American Journal of Physical Anthropology · doi:10.1002/ajpa.23384 · Cited by 27 · see citing works
Wang, Y., Zheng, Y., Yang, S.-Y., Yang, Z.-M., Zhang, L.-N., He, Y.-Q., Gong, X.-H., Liu, D., Finnell, R. H., Qiu, Z., et al. (2018) · Cell Death and Differentiation · doi:10.1038/s41418-018-0257-6 · Cited by 27 · see citing works
Sun, L., Zhang, D., Lian, C., Wang, L., Wu, Z., Shao, W., Lin, W., Shen, D. G., & Li, G. (2019) · NeuroImage · doi:10.1016/j.neuroimage.2019.05.037 · Cited by 26 · see citing works
Self-citationWu, S., Li, X., Qin, D., Zhang, L.-H., Cheng, T., Chen, Z., Nie, B., Ren, X., Wu, J., Wang, W., et al. (2020) · 中国科学通报：英文版 · doi:10.1016/j.scib.2020.12.017 · Cited by 26 · see citing works
Self-citationSelection of Models: Evolution and the Choice of Species for Translational Research
Bolker, J. A. (2019) · Brain Behavior and Evolution · doi:10.1159/000500317 · Cited by 26 · see citing works
Recent advances in therapeutic CRISPR-Cas9 genome editing: mechanisms and applications
Zhou, L., & Yao, S. (2023) · Molecular Biomedicine · doi:10.1186/s43556-023-00115-5 · Cited by 27 · see citing works
MeCP2 and transcriptional control of eukaryotic gene expression
Akhtar, G. B., Buist, M., & Rastegar, M. (2022) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2022.151237 · Cited by 23 · see citing works
CRISPR editing in biological and biomedical investigation
Huang, J., Wang, Y., & Zhao, J. (2017) · Journal of Cellular Physiology · doi:10.1002/jcp.26141 · Cited by 25 · see citing works
Estimating contribution of rare non‐coding variants to neuropsychiatric disorders
Takata, A. (2018) · Psychiatry and Clinical Neurosciences · doi:10.1111/pcn.12774 · Cited by 24 · see citing works
Li, X., Zhao, D., & Hu, X. (2020) · Scientometrics · doi:10.1007/s11192-020-03537-y · Cited by 24 · see citing works
Self-citationTranslational Neuroscience Approaches to Understanding Autism
Veenstra-VanderWeele, J. M., O’Reilly, K. C., Dennis, M. Y., Uribe‐Salazar, J. M., & Amaral, D. G. (2023) · American Journal of Psychiatry · doi:10.1176/appi.ajp.20230153 · Cited by 24 · see citing works
Zhou, W., Yang, J., Zhang, Y., Hu, X., & Wang, W. (2022) · MedComm · doi:10.1002/mco2.155 · Cited by 22 · see citing works
Self-citationLi, X., Yao, X., Mu, C., Wang, Z., Hu, R., Chang, Y. Z., & Wu, J. (2021) · Stem Cell Reviews and Reports · doi:10.1007/s12015-021-10278-9 · Cited by 21 · see citing works
Sleep problems in Rett syndrome animal models: A systematic review
Zhang, X., Lin, J., & Spruyt, K. (2020) · Journal of Neuroscience Research · doi:10.1002/jnr.24730 · Cited by 19 · see citing works
Generation of Nonhuman Primate Model of Cone Dysfunction through In Situ AAV-Mediated CNGB3 Ablation
Lin, Q., Lv, J., Wu, K., Zhang, C.-J., Liu, Q., & Jin, Z. (2020) · Molecular Therapy — Methods & Clinical Development · doi:10.1016/j.omtm.2020.08.007 · Cited by 19 · see citing works
Self-citationFrom Organoids to Assembloids: Experimental Approaches to Study Human Neuropsychiatric Disorders
Levy, R. J., & Pașca, S. P. (2025) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-112723-023232 · Cited by 22 · see citing works
Li, H., 昆明650223，中国, 中.-香., Yao, Y., Hu, X., 650107，中国, 中. 昆., & 200031，中国, 中. (2021) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.004 · Cited by 19 · see citing works
Self-citationWang, J., Wang, Z., Zhang, H., Feng, S., Lü, Y., Wang, S., Wang, H., Sun, Y. E., & Chen, Y. (2021) · Cerebral Cortex · doi:10.1093/cercor/bhab166 · Cited by 19 · see citing works
Self-citationMeCP2 Dysfunction in Rett Syndrome and Neuropsychiatric Disorders
Chin, E., & Goh, E. L. K. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9554-7_33 · Cited by 20 · see citing works
Potent hERG channel inhibition by sarizotan, an investigative treatment for Rett Syndrome
Cheng, H., Du, C., Zhang, Y., James, A. F., Dempsey, C. E., Abdala, A. P., & Hancox, J. C. (2019) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2019.07.012 · Cited by 19 · see citing works
Zhong, T., Zhao, F., Pei, Y., Ning, Z., Liao, L., Wu, Z., Niu, Y., Wang, L., Shen, D. G., Zhang, Y., et al. (2020) · NeuroImage · doi:10.1016/j.neuroimage.2020.117649 · Cited by 19 · see citing works
Self-citationMultimodal Neuroimaging in Rett Syndrome With MECP2 Mutation
Kong, Y., Li, Q.-B., Zhao-hong, Y., Jiang, X., Zhang, G.-Q., Cheng, N., & Dang, N. (2022) · Frontiers in Neurology · doi:10.3389/fneur.2022.838206 · Cited by 19 · see citing works
Animal models of neurodevelopmental disorders with behavioral phenotypes
Harris, J. C. (2020) · Current Opinion in Psychiatry · doi:10.1097/yco.0000000000000675 · Cited by 18 · see citing works
Miao, J., Gao, P., Li, Q., He, K., Zhang, L., Wang, J., & Huang, L. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222011227 · Cited by 18 · see citing works
Self-citationSchmidt, J. K., Jones, K. M., Vleck, T. V., & Emborg, M. E. (2022) · Science Translational Medicine · doi:10.1126/scitranslmed.abf4879 · Cited by 17 · see citing works
Endophenotype trait domains for advancing gene discovery in autism spectrum disorder
Mosconi, M. W., Stevens, C. J., Unruh, K. E., Shafer, R. L., & Elison, J. T. (2023) · Journal of Neurodevelopmental Disorders · doi:10.1186/s11689-023-09511-y · Cited by 16 · see citing works
Ethical and Welfare Implications of Genetically Altered Non-Human Primates for Biomedical Research
Prescott, M. J. (2020) · Journal of Applied Animal Ethics Research · doi:10.1163/25889567-bja10002 · Cited by 15 · see citing works
Nakagami, A., Yasue, M., Nakagaki, K., Nakamura, M., Kawai, N., & Ichinohe, N. (2022) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2022.885433 · Cited by 16 · see citing works
Feng, S., Huang, H., Wang, N., Wei, Y., Liu, Y., & Qin, D. (2021) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2021.673372 · Cited by 14 · see citing works
Self-citationXu, L., Wang, D., Zhao, L., Yang, Z., Liu, X., Li, X., Yuan, T., Wang, Y., Huang, T., Bian, N., et al. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106197 · Cited by 15 · see citing works
Self-citationHara, T., Owada, Y., & Takata, A. (2022) · Journal of Human Genetics · doi:10.1038/s10038-022-01046-9 · Cited by 14 · see citing works
Construction of spatiotemporal infant cortical surface atlas of rhesus macaque
Wang, F., Lian, C., Xia, J., Wu, Z., Duan, D., Wang, L., Shen, D. G., & Li, G. (2018) · IEEE International Symposium on Biomedical Imaging (ISBI) · doi:10.1109/isbi.2018.8363671 · Cited by 14 · see citing works
Self-citationVolobueva, A. S., Orekhov, A. N., & Deykin, A. V. (2019) · Brazilian Journal of Medical and Biological Research · doi:10.1590/1414-431x20198108 · Cited by 14 · see citing works
Liu, M.-S., 中国科学院自动化研究所脑网络中心, 北. 1., Gao, J., Hu, G., Hao, G., Jiang, T., Zhang, C., Yu, S. P., 中国科学院自动化研究所模式识别国家实验室, 北. 1., 中国科学院大学人工智能学院, 北. 1., et al. (2022) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2021.353 · Cited by 13 · see citing works
Self-citationA transgenic monkey model for the study of human brain evolution
Shi, L., & Su, B. (2019) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2019.031 · Cited by 13 · see citing works
The complexity of Rett syndrome models: Primary fibroblasts as a disease-in-a-dish reliable approach
Cordone, V., Pecorelli, A., Amicarelli, F., Hayek, J., & Valacchi, G. (2019) · Drug Discovery Today Disease Models · doi:10.1016/j.ddmod.2019.11.001 · Cited by 13 · see citing works
Ryan, A. M., Murai, T., Lau, A. R., Hogrefe, C. E., McAllister, A. K., Carter, C. S., & Bauman, M. D. (2020) · Developmental Psychobiology · doi:10.1002/dev.22003 · Cited by 13 · see citing works
Li, C., 复旦大学信息科学与工程学院微纳中心, 上. 2., Xiao, Z., Li, Y., Chen, Z., Ji, X., Liu, Y., Feng, S., Zhang, Z., Zhang, K., et al. (2023) · 动物学研究 · doi:10.24272/j.issn.2095-8137.2022.449 · Cited by 12 · see citing works
Self-citationDepletion of giant ANK2 in monkeys causes drastic brain volume loss
Qin, D., Zhou, J., He, X., Shen, X., Li, C., Chen, H.-Z., Yan, L., Hu, Z., Li, X., Lv, L., et al. (2021) · Cell Discovery · doi:10.1038/s41421-021-00336-4 · Cited by 12 · see citing works
Self-citationLongitudinal brain atlases of early developing cynomolgus macaques from birth to 48 months of age
Zhong, T., Wei, J., Wu, K., Chen, L., Zhao, F., Pei, Y., Wang, Y., Zhang, H., Wu, Z., Huang, Y., et al. (2021) · NeuroImage · doi:10.1016/j.neuroimage.2021.118799 · Cited by 13 · see citing works
Self-citationMegagiannis, P., Suresh, R., Rouleau, G. A., & Zhou, Y. (2022) · Advanced Drug Delivery Reviews · doi:10.1016/j.addr.2022.114562 · Cited by 12 · see citing works
Li, W., Qiu, X., Chen, J., Chen, K., Chen, M., Wang, Y., Sun, W., Su, J., Chen, Y., Liu, X., et al. (2025) · Advanced Science · doi:10.1002/advs.202403801 · Cited by 11 · see citing works
Self-citationGene editing in monogenic autism spectrum disorder: animal models and gene therapies
Wang, N., Lv, L., Huang, X., Shi, M., Dai, Y., Wei, Y., Xu, B., Fu, C., Huang, H., Shi, H., et al. (2022) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2022.1043018 · Cited by 11 · see citing works
Self-citationStem Cell Engineering and Differentiation for Disease Modeling and Cell-based Therapies
Randolph, L. N., Jiang, Y., Lian, X. L., & equally., §. T. A. C. (2017) · AIMS Cell and Tissue Engineering · doi:10.3934/celltissue.2017.2.140 · Cited by 13 · see citing works
Self-citation
- Authors
- Chen, Y., Yu, J., Niu, Y., Qin, D., Liu, H., Li, G., Hu, Y., Wang, J., Lu, Y., Kang, Y., Jiang, Y., Wu, K., Li, S., Wei, J., He, J., Wang, J., Liu, X., Luo, Y., Si, C., Bai, R., Zhang, K., Liu, J., Huang, S., Chen, Z., Wang, S., Chen, X., Bao, X., Zhang, Q., Li, F., Geng, R., Liang, A., Shen, D., Jiang, T., Hu, X., Ma, Y., Ji, W., & Sun, Y. E.
- Affiliations
- Kunming University of Science and Technology (CN)
- Tongji University (CN)
- Kunming Institute of Zoology (CN)
- University of North Carolina at Chapel Hill (US)
- Peking University First Hospital (CN)
- University of Electronic Science and Technology of China (CN)
- Corresponding author
- Chen, Yongchang
- Ji, Weizhi
- Sun, Yi Eve
- ORCID
- Chen, Yongchang
- Yu, Juehua
- Niu, Yuyu
- Qin, Dongdong
- Liu, Hailiang
- Li, Gang
- Hu, Yingzhou
- Wang, Jiaojian
- Kang, Yu
- Jiang, Yong
- Wu, Kunhua
- Li, Siguang
- Wei, Jingkuan
- He, Jing
- Wang, Junbang
- Luo, Yuping
- Zhang, Kunshan
- Liu, Jie
- Chen, Zhenzhen
- Wang, Shuang
- Chen, Xiaoying
- Bao, Xinhua
- Zhang, Qingping
- Li, Fuxing
- Geng, Rui
- Liang, Aibin
- Shen, Dinggang
- Jiang, Tianzi
- Hu, Xintian
- Ma, Yuanye
- Ji, Weizhi
- Sun, Yi Eve
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2017-05
- Volume
- 169
- Issue
- 5
- Pages
- 945-955.e10
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5540256
- OpenAlex
- W2615586834
- Cited by
- 204
- References
- 45
- Citations by year
- 2026: 8 · 2025: 19 · 2024: 11 · 2023: 25 · 2022: 34 · 2021: 21 · 2020: 24 · 2019: 26 · 2018: 26 · 2017: 8 · 2012: 1
- FWCI
- 15.21
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Carolina Digital Repository (University of North Carolina at Chapel Hill) (submittedVersion)
- UNC Libraries
- Funders
- National Key Research and Development Program (2016YFA0101401, 2016YFA0100800)
- National & Provincial Natural Science Foundation of China (U1602224, U1302227, 31571534, 2015FA037, 91319309, 31450110428, 31620103904, 2013HB133, 13JC1407102)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA regulation and disease
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › CRISPR and Genetic Engineering
- Keywords
- Rett syndrome, MeCP2, TALEN gene editing, Macaca fascicularis, neurodevelopmental disorders, embryonic lethality, brain MRI abnormalities, gene expression profiling, endophenotypes
- MeSH terms
- Transcription Activator-Like Effector Nucleases, Gene Editing, Animals, Brain, Circadian Rhythm, Disease Models, Animal, Electrocardiography, Female, Humans, Macaca fascicularis, Magnetic Resonance Imaging, Male, Mutation, Pain, Sleep, Rett Syndrome, Chromosomes, Human, X, Methyl-CpG-Binding Protein 2, Transcriptome
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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