Modeling psychiatric disorders for developing effective treatments

Nature Medicine

Volumn 21, Issue 9, 2015, Pages 979-988

  Kaiser, Tobias ^a,b   Feng, Guoping ^a,b,c  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; ANTINEOPLASTIC AGENT; CYTOTOXIC AGENT; TRANSCRIPTOME;

AUTISM; BRAIN DEPTH STIMULATION; BRAIN FUNCTION; CIRCADIAN RHYTHM; CLINICAL RESEARCH; CONCEPTUAL FRAMEWORK; CONNECTOME; CONSTRUCT VALIDITY; GENETIC ASSOCIATION; HUMAN; MENTAL DISEASE; MENTAL PATIENT; NEUROBIOLOGY; NEUROPHYSIOLOGY; NEUROSCIENCE; NONHUMAN; PATHOPHYSIOLOGY; PLURIPOTENT STEM CELL; PRIMATE MODEL; PRIORITY JOURNAL; REVIEW; RISK FACTOR; SCHIZOPHRENIA; SCIENCE; STRATEGIC PLANNING; TRANSLATIONAL RESEARCH; TREATMENT INDICATION; TREATMENT RESPONSE; ZEBRA FISH; ANIMAL; AUTISM SPECTRUM DISORDER; CYTOLOGY; DISEASE MODEL; GENETICS; MENTAL DISORDERS;

ANIMALS; AUTISM SPECTRUM DISORDER; DISEASE MODELS, ANIMAL; GENOME-WIDE ASSOCIATION STUDY; HUMANS; INDUCED PLURIPOTENT STEM CELLS; MENTAL DISORDERS;

EID: 84940983037     PISSN: 10788956     EISSN: 1546170X     Source Type: Journal    
DOI: 10.1038/nm.3935     Document Type: Review

References (108)

1. Purcell, S.M. et al. A polygenic burden of rare disruptive mutations in schizophrenia. Nature 506, 185-190 (2014).
2. Fromer, M. et al. De novo mutations in schizophrenia implicate synaptic networks. Nature 506, 179-184 (2014).
3. Weiss, L.A., Arking, D.E., Daly, M.J. & Chakravarti, A. A genome-wide linkage and association scan reveals novel loci for autism. Nature 461, 802-808 (2009).
4. Schizophrenia Working Group of the Psychiatric Genomics Consortium. Biological insights from 108 schizophrenia-associated genetic loci. Nature 511, 421-427 (2014).
5. Wang, K. et al. Common genetic variants on 5p14.1 associate with autism spectrum disorders. Nature 459, 528-533 (2009).
6. Maloney, S.E., Rieger, M.A. & Dougherty, J.D. Identifying essential cell types and circuits in autism spectrum disorders. Int. Rev. Neurobiol. 113, 61 (2013).
7. Monteiro, P. & Feng, G. Learning from animal models of obsessive-compulsive disorder. Biol. Psychiatry (2015).
8. Willner, P. Validation criteria for animal models of human mental disorders: learned helplessness as a paradigm case. Prog. Neuropsychopharmacol. Biol. Psychiatry 10, 677-690 (1986).
9. McKinney, W.T. & Bunney, W.E. Animal model of depression: I. Review of evidence: implications for research. Arch. Gen. Psychiatry 21, 240-248 (1969).
10. McFarlane, H.G. et al. Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 7, 152-163 (2008).
11. Silverman, J.L., Oliver, C., Karras, M., Gastrell, P. & Crawley, J. AMPAKINE enhancement of social interaction in the BTBR mouse model of autism. Neuropharmacology 64, 268-282 (2013).
12. Silverman, J.L., Tolu, S.S., Barkan, C.L. & Crawley, J.N. Repetitive self-grooming behavior in the BTBR mouse model of autism is blocked by the mGluR5 antagonist MPEP. Neuropsychopharmacology 35, 976-989 (2010).
13. Lourenço Da Silva, A. et al. Effect of riluzole on MK-801 and amphetamine-induced hyperlocomotion. Neuropsychobiology 48, 27-30 (2003).
14. Breier, A. et al. Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomographymethod. Proc. Natl. Acad. Sci. USA 94, 2569-2574 (1997).
15. Nestler, E.J. & Hyman, S.E. Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169 (2010).
16. Cardno, A.G. et al. Heritability estimates for psychotic disorders: the Maudsley twin psychosis series. Arch. Gen. Psychiatry 56, 162-168 (1999).
17. Caspi, A. & Moffitt, T.E. Gene-environment interactions in psychiatry: joining forces with neuroscience. Nat. Rev. Neurosci. 7, 583-590 (2006).
18. Kannan, G., Sawa, A. & Pletnikov, M.V. Mouse models of gene-environment interactions in schizophrenia. Neurobiol. Dis. 57, 5-11 (2013).
19. Klengel, T. & Binder, E.B. Epigenetics of stress-related psychiatric disorders and gene × environment interactions. Neuron 86, 1343-1357 (2015).
20. McCarroll, S.A., Feng, G. & Hyman, S.E. Genome-scale neurogenetics: methodology and meaning. Nat. Neurosci. 17, 756-763 (2014).
21. Haesemeyer, M. & Schier, A.F. The study of psychiatric disease genes and drugs in zebrafish. Curr. Opin. Neurobiol. 30, 122-130 (2015).
22. Zweier, C. et al. CNTNAP2 and NRXN1 are mutated in autosomal-recessive Pitt-Hopkins-like mental retardation and determine the level of a common synaptic protein in Drosophila. Am. J. Hum. Genet. 85, 655-666 (2009).
23. Gottesman, I.I. & Gould, T.D. The endophenotype concept in psychiatry: etymology and strategic intentions. Am. J. Psychiatry 160, 636-645 (2003).
24. Gould, T.D. & Gottesman, I.I. Psychiatric endophenotypes and the development of valid animal models. Genes Brain Behav. 5, 113-119 (2006).
25. Dincheva, I. et al. FAAH genetic variation enhances fronto-amygdala function in mouse and human. Nat. Commun. 6, 6395 (2015).
26. Mague, S.D. et al. Mouse model of OPRM1 (A118G) polymorphism has sex-specific effects on drug-mediated behavior. Proc. Natl. Acad. Sci. USA 106, 10847-10852 (2009).
27. Chen, Z.-Y. et al. Genetic variant BDNF (Val66Met) polymorphism alters anxiety-related behavior. Science 314, 140-143 (2006).
28. Böckers, T.M. et al. Synaptic scaffolding proteins in rat brain. Ankyrin repeats of the multidomain Shank protein family interact with the cytoskeletal protein a-fodrin. J. Biol. Chem. 276, 40104-40112 (2001).
29. Peça, J. et al. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 472, 437-442 (2011).
30. Etherton, M.R., Blaiss, C.A., Powell, C.M. & Sudhof, T.C. Mouse neurexin-1a deletion causes correlated electrophysiological and behavioral changes consistent with cognitive impairments. Proc. Natl. Acad. Sci. USA 106, 17998-18003 (2009).
31. Peñagarikano, O. et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities and core autism-related deficits. Cell 147, 235-246 (2011).
32. Clement, J.P. et al. Pathogenic SYNGAP1 mutations impair cognitive development by disrupting maturation of dendritic spine synapses. Cell 151, 709-723 (2012).
33. Tabuchi, K. et al. A Neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318, 71-76 (2007).
34. Derecki, N.C. et al. Wild-type microglia arrest pathology in a mouse model of Rett syndrome. Nature 484, 105-109 (2012).
35. Lioy, D.T. et al. A role for glia in the progression of Rett's syndrome. Nature 475, 497-500 (2011).
36. Wang, J. et al. Wild-type microglia do not reverse pathology in mouse models of Rett syndrome. Nature 521, E1-E4 (2015).
37. Saxena, S., Brody, A.L., Schwartz, J.M. & Baxter, L.R. Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br. J. Psychiatry Suppl. 35, 26-37 (1998).
38. Saxena, S. & Rauch, S.L. Functional neuroimaging and the neuroanatomy of obsessive-compulsive disorder. Psychiatr. Clin. North Am. 23, 563-586 (2000).
39. Burguière, E., Monteiro, P., Feng, G. & Graybiel, A.M. Optogenetic stimulation of lateral orbitofronto-striatal pathway suppresses compulsive behaviors. Science 340, 1243-1246 (2013).
40. Ahmari, S.E. et al. Repeated cortico-striatal stimulation generates persistent OCD-like behavior. Science 340, 1234-1239 (2013).
41. Hoischen, A., Krumm, N. & Eichler, E.E. Prioritization of neurodevelopmental disease genes by discovery of new mutations. Nat. Neurosci. 17, 764-772 (2014).
42. Rothwell, P.E. et al. Autism-associated neuroligin-3 mutations commonly impair striatal circuits to boost repetitive behaviors. Cell 158, 198-212 (2014).
43. Grabli, D. et al. Behavioural disorders induced by external globus pallidus dysfunction in primates: I. Behavioural study. Brain 127, 2039-2054 (2004).
44. Reiner, A., Medina, L. & Veenman, C.L. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res. Brain Res. Rev. 28, 235-285 (1998).
45. Shultz, S., Opie, C. & Atkinson, Q.D. Stepwise evolution of stable sociality in primates. Nature 479, 219-222 (2011).
46. Bayés, A. et al. Comparative study of human and mouse postsynaptic proteomes finds high compositional conservation and abundance differences for key synaptic proteins. PLoS ONE 7, e46683 (2012).
47. Neale, B.M. & Sklar, P. Genetic analysis of schizophrenia and bipolar disorder reveals polygenicity but also suggests new directions for molecular interrogation. Curr. Opin. Neurobiol. 30, 131-138 (2015).
48. Devlin, B. & Scherer, S.W. Genetic architecture in autism spectrum disorder. Curr. Opin. Genet. Dev. 22, 229-237 (2012).
49. Geschwind, D.H. Genetics of autism spectrum disorders. Trends Cogn. Sci. 15, 409-416 (2011).
50. Rujescu, D. et al. Disruption of the neurexin 1 gene is associated with schizophrenia. Hum. Mol. Genet. 18, 988-996 (2009).
51. Ching, M.S. et al. Deletions of NRXN1 (neurexin-1) predispose to a wide spectrum of developmental disorders. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 153B, 937-947 (2010).
52. Marchetto, M.C. et al. A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143, 527-539 (2010).
53. Paşca, S.P. et al. Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome. Nat. Med. 17, 1657-1662 (2011).
54. Shcheglovitov, A. et al. SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 503, 267-271 (2013).
55. Wen, Z. et al. Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 515, 414-418 (2014).
56. Brennand, K.J. et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature 473, 221-225 (2011).
57. Hook, V. et al. Human iPSC neurons display activity-dependent neurotransmitter secretion: Aberrant catecholamine levels in schizophrenia neurons. Stem Cell Reports 3, 531-538 (2014).
58. Eiraku, M. et al. Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56 (2011).
59. Sato, T. et al. Single Lgr5 stem cells build crypt villus structures in vitro without a mesenchymal niche. Nature 459, 262-265 (2009).
60. Lancaster, M.A. et al. Cerebral organoids model human brain development and microcephaly. Nature 501, 373-379 (2013).
61. Mariani, J. et al. FOXG1-dependent dysregulation of GABA/glutamate neuron differentiation in autism spectrum disorders. Cell 162, 375-390 (2015).
62. Kriks, S. et al. Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551 (2011).
63. Espuny-Camacho, I. et al. Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77, 440-456 (2013).
64. Hay, M., Thomas, D.W., Craighead, J.L., Economides, C. & Rosenthal, J. Clinical development success rates for investigational drugs. Nat. Biotechnol. 32, 40-51 (2014).
65. Insel, T. et al. Research domain criteria (RDoC): toward a new classification framework for research on mental disorders. Am. J. Psychiatry 167, 748-751 (2010).
66. Belzung, C. & Lemoine, M. Criteria of validity for animal models of psychiatric disorders: focus on anxiety disorders and depression. Biol. Mood Anxiety Disord. 1, 9 (2011).
67. Ferrarelli, F. et al. Thalamic dysfunction in schizophrenia suggested by whole-night deficits in slow and fast spindles. Am. J. Psychiatry 167, 1339-1348 (2010).
68. Wamsley, E.J. et al. Reduced sleep spindles and spindle coherence in schizophrenia: mechanisms of impaired memory consolidation? Biol. Psychiatry 71, 154-161 (2012).
69. Kwon, J.S. et al. Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Arch. Gen. Psychiatry 56, 1001-1005 (1999).
70. Teale, P. et al. Cortical source estimates of gamma band amplitude and phase are different in schizophrenia. Neuroimage 42, 1481-1489 (2008).
71. Chang, X. et al. Altered default mode and fronto-parietal network subsystems in patients with schizophrenia and their unaffected siblings. Brain Res. 1562, 87-99 (2014).
72. Chai, X.J. et al. Abnormal medial prefrontal cortex resting-state connectivity in bipolar disorder and schizophrenia. Neuropsychopharmacology 36, 2009-2017 (2011).
73. Kubicki, M. et al. A review of diffusion tensor imaging studies in schizophrenia. J. Psychiatr. Res. 41, 15-30 (2007).
74. Kuperberg, G.R. et al. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch. Gen. Psychiatry 60, 878-888 (2003).
75. Shenton, M.E. et al. Abnormalities of the left temporal lobe and thought disorder in schizophrenia. N. Engl. J. Med. 327, 604-612 (1992).
76. Glantz, L.A. & Lewis, D.A. Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia. Arch. Gen. Psychiatry 57, 65-73 (2000).
77. Spencer, K.M. et al. Neural synchrony indexes disordered perception and cognition in schizophrenia. Proc. Natl. Acad. Sci. USA 101, 17288-17293 (2004).
78. Sutter, E.E. The brain response interface: communication through visually-induced electrical brain responses. J. Microcomput. Appl. 15, 31-45 (1992).
79. Sigurdsson, T., Stark, K.L., Karayiorgou, M., Gogos, J.A. & Gordon, J.A. Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia. Nature 464, 763-767 (2010).
80. Fejgin, K. et al. A mouse model that recapitulates cardinal features of the 15q13.3 microdeletion syndrome including schizophrenia-and epilepsy-related alterations. Biol. Psychiatry 76, 128-137 (2014).
81. Hollander, E. et al. Striatal volume on magnetic resonance imaging and repetitive behaviors in autism. Biol. Psychiatry 58, 226-232 (2005).
82. Okano, H. & Mitra, P. Brain-mapping projects using the common marmoset. Neurosci. Res. 93, 3-7 (2015).
83. Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332-337 (2013).
84. Janak, P.H. & Tye, K.M. From circuits to behaviour in the amygdala. Nature 517, 284-292 (2015).
85. Stephenson-Jones, M., Samuelsson, E., Ericsson, J., Robertson, B. & Grillner, S. Evolutionary conservation of the basal ganglia as a common vertebrate mechanism for action selection. Curr. Biol. 21, 1081-1091 (2011).
86. Graybiel, A.M. The basal ganglia. Curr. Biol. 10, R509-R511 (2000).
87. Willsey, A.J. et al. Coexpression networks implicate human midfetal deep cortical projection neurons in the pathogenesis of autism. Cell 155, 997-1007 (2013).
88. Chen, R., Romero, G., Christiansen, M.G., Mohr, A. & Anikeeva, P. Wireless magnetothermal deep brain stimulation. Science 347, 1477-1480 (2015).
89. de Bono, J.S. & Ashworth, A. Translating cancer research into targeted therapeutics. Nature 467, 543-549 (2010).
90. Collins, F.S. & Varmus, H. A new initiative on precision medicine. N. Engl. J. Med. 372, 793-795 (2015).
91. Insel, T.R. & Cuthbert, B.N. Brain disorders? Precisely. Science 348, 499-500 (2015).
92. Tufts Center for the Study of Drug Development. CNS drugs take longer to develop, have lower success rates, than other drugs. CSDD Impact Report 16 http://csdd.tufts.edu/news/complete-story/pr-ir-nov-dec-ir (2014).
93. Wise, S.P. Forward frontal fields: phylogeny and fundamental function. Trends Neurosci. 31, 599-608 (2008).
94. Cooke, D., Goldring, A., Recanzone, G.H. & Krubitzer, L. The evolution of parietal areas associated with visuomanual behavior: from grasping to tool use. in The New Visual Neurosciences (Chalupa, L. and Werner, J., eds) 1049-1063 (MIT Press, 2014).
95. Burman, K.J. & Rosa, M.G. Architectural subdivisions of medial and orbital frontal cortices in the marmoset monkey (Callithrix jacchus). J. Comp. Neurol. 514, 11-29 (2009).
96. Schmeisser, M.J. et al. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature 486, 256-260 (2012).
97. Won, H. et al. Autistic-like social behaviour in Shank2-mutant mice improved by restoring NMDA receptor function. Nature 486, 261-265 (2012).
98. Bozdagi, O. et al. Haploinsufficiency of the autism-associated Shank3 gene leads to deficits in synaptic function, social interaction, and social communication. Mol. Autism 1, 15 (2010).
99. Wang, X. et al. Synaptic dysfunction and abnormal behaviors in mice lacking major isoforms of Shank3. Hum. Mol. Genet. 20, 3093-3108 (2011).
100. Yang, M. et al. Reduced excitatory neurotransmission and mild autism-relevant phenotypes in adolescent Shank3-null mutant mice. J. Neurosci. 32, 6525-6541 (2012).
101. Kouser, M. et al. Loss of predominant shank3 isoforms results in hippocampus-dependent impairments in behavior and synaptic transmission. J. Neurosci. 33, 18448-18468 (2013).
102. Han, K. et al. SHANK3 overexpression causes manic-like behaviour with unique pharmacogenetic properties. Nature 503, 72-77 (2013).
103. Chen, R.Z., Akbarian, S., Tudor, M. & Jaenisch, R. Deficiency of methyl-CpG binding protein-2 in CNS neurons results in a Rett-like phenotype in mice. Nat. Genet. 27, 327-331 (2001).
104. Lioy, D.T. et al. A role for glia in the progression of Rett's syndrome. Nature 475, 497-500 (2011).
105. Kumar, M. et al. High-resolution magnetic resonance imaging for characterization of the neuroligin-3 knock-in mouse model associated with autism spectrum disorder. PLoS ONE 9, e109872 (2014).
106. Hashimoto, T. et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. J. Neurosci. 23, 6315-6326 (2003).
107. Frantseva, M.V. et al. Evidence for impaired long-term potentiation in schizophrenia and its relationship to motor skill learning. Cereb. Cortex. 18, 990-996 (2008).
108. Hasan, A. et al. Impaired long-term depression in schizophrenia: a cathodal tDCS pilot study. Brain Stimul. 5, 475-483 (2012).