Modeling neuropsychiatric disorders using human induced pluripotent stem cells
Meiyan Wang, Lei Zhang, Fred H. Gage
Modeling neuropsychiatric disorders using human induced pluripotent stem cells
Neuropsychiatric disorders are complex disorders characterized by heterogeneous genetic variations, variable symptoms, and widespread changes in anatomical pathology. In the context of neuropsychiatric disorders, limited access to relevant tissue types presents challenges for understanding disease etiology and developing effective treatments. Induced pluripotent stem cells (iPSCs) reprogrammed from patient somatic cells offer an opportunity to recapitulate disease development in relevant cell types, and they provide novel approaches for understanding disease mechanisms and for development of effective treatments. Here we review recent progress and challenges in differentiation paradigms for generating disease-relevant cells and recent studies of neuropsychiatric disorders using human pluripotent stem cell (hPSC) models where cellular phenotypes linked to disease have been reported. The use of iPSC-based disease models holds great promise for understanding disease mechanisms and supporting discovery of effective treatments.
neuropsychiatric disorders / iPSCs / brain organoid / schizophrenia / autism spectrum disorder / bipolar disorder
[1] |
Abud EM, Ramirez RN, Martinez ES, Healy LM, Nguyen CHH, Newman SA, Yeromin AV, Scarfone VM, Marsh SE, Fimbres C
CrossRef
Google scholar
|
[2] |
Amiri A, Coppola G, Scuderi S, Wu F, Roychowdhury T, Liu F, Pochareddy S, Shin Y, Safi A, Song L
CrossRef
Google scholar
|
[3] |
Bagley JA, Reumann D, Bian S, Levi-Strauss J, Knoblich JA (2017) Fused cerebral organoids model interactions between brain regions. Nat Methods 14:743–751
CrossRef
Google scholar
|
[4] |
Bavamian S, Mellios N, Lalonde J, Fass DM, Wang J, Sheridan SD, Madison JM, Zhou F, Rueckert EH, Barker D
CrossRef
Google scholar
|
[5] |
Bershteyn M, Nowakowski TJ, Pollen AA, Di Lullo E, Nene A, Wynshaw-Boris A, Kriegstein AR (2017) Human iPSC-derived cerebral organoids model cellular features of lissencephaly and reveal prolonged mitosis of outer radial glia. Cell Stem Cell 20 (435–449):e434
CrossRef
Google scholar
|
[6] |
Bipolar D, Schizophrenia Working Group of the Psychiatric Genomics Consortium. Electronic address, d.r.v.e., Bipolar, D., and Schizophrenia Working Group of the PsychiatricGenomics, C (2018) Genomic dissection of bipolar disorder and schizophrenia, including 28 SUBPHENOTYPES. Cell 173:1705e1716–1715e1716
|
[7] |
Birey F, Andersen J, Makinson CD, Islam S, Wei W, Huber N, Fan HC, Metzler KRC, Panagiotakos G, Thom N
CrossRef
Google scholar
|
[8] |
Brennand K, Savas JN, Kim Y, Tran N, Simone A, Hashimoto-Torii K, Beaumont KG, Kim HJ, Topol A, Ladran I
CrossRef
Google scholar
|
[9] |
Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S, Li Y, Mu Y, Chen G, Yu D
CrossRef
Google scholar
|
[10] |
Bundo M, Toyoshima M, Okada Y, Akamatsu W, Ueda J, Nemoto-Miyauchi T, Sunaga F, Toritsuka M, Ikawa D, Kakita A
CrossRef
Google scholar
|
[11] |
Butovsky O, Jedrychowski MP, Moore CS, Cialic R, Lanser AJ, Gabriely G, Koeglsperger T, Dake B, Wu PM, Doykan CE
CrossRef
Google scholar
|
[12] |
Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27:275–280
CrossRef
Google scholar
|
[13] |
Ciani L, Salinas PC (2005) WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci 6:351–362
CrossRef
Google scholar
|
[14] |
Cirillo MA, Seidman LJ (2003) Verbal declarative memory dysfunction in schizophrenia: from clinical assessment to genetics and brain mechanisms. Neuropsychol Rev 13:43–77
CrossRef
Google scholar
|
[15] |
Darmanis S, Sloan SA, Zhang Y, Enge M, Caneda C, Shuer LM, Hayden Gephart MG, Barres BA, Quake SR (2015) A survey of human brain transcriptome diversity at the single cell level. Proc Natl Acad Sci U S A 112:7285–7290
CrossRef
Google scholar
|
[16] |
Dehay C, Kennedy H, Kosik KS (2015) The outer subventricular zone and primate-specific cortical complexification. Neuron 85:683–694
CrossRef
Google scholar
|
[17] |
Deshpande A, Yadav S, Dao DQ, Wu ZY, Hokanson KC, Cahill MK, Wiita AP, Jan YN, Ullian EM, Weiss LA (2017) Cellular phenotypes in human iPSC-derived neurons from a genetic model of autism spectrum disorder. Cell Rep 21:2678–2687
CrossRef
Google scholar
|
[18] |
Di Lullo E, Kriegstein AR (2017) The use of brain organoids to investigate neural development and disease. Nat Rev Neurosci 18:573–584
CrossRef
Google scholar
|
[19] |
Edlund T, Jessell TM (1999) Progression from extrinsic to intrinsic signalling in cell fate specification: a view from the nervous system. Cell 96:211–224
CrossRef
Google scholar
|
[20] |
Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S, Matsumura M, Wataya T, Nishiyama A, Muguruma K, Sasai Y (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3:519–532
CrossRef
Google scholar
|
[21] |
Emery B (2010) Regulation of oligodendrocyte differentiation and myelination. Science 330:779–782
CrossRef
Google scholar
|
[22] |
Espuny-Camacho I, Michelsen KA, Gall D, Linaro D, Hasche A, Bonnefont J, Bali C, Orduz D, Bilheu A, Herpoel A
CrossRef
Google scholar
|
[23] |
Feinberg I (1982) Schizophrenia: caused by a fault in programmed synaptic elimination during adolescence? J Psychiatr Res 17:319–334
CrossRef
Google scholar
|
[24] |
Freedman R, Goldowitz D (2010) Studies on the hippocampal formation: From basic development to clinical applications: Studies on schizophrenia. Prog Neurobiol 90:263–275
CrossRef
Google scholar
|
[25] |
Fuccillo M, Joyner AL, Fishell G (2006) Morphogen to mitogen: the multiple roles of hedgehog signalling in vertebrate neural development. Nat Rev Neurosci 7:772–783
CrossRef
Google scholar
|
[26] |
Galceran J, Miyashita-Lin EM, Devaney E, Rubenstein JL, Grosschedl R (2000) Hippocampus development and generation of dentate gyrus granule cells is regulated by LEF1. Development 127:469–482
|
[27] |
Gaspard N, Bouschet T, Hourez R, Dimidschstein J, Naeije G, van den Ameele J, Espuny-Camacho I, Herpoel A, Passante L, Schiffmann SN
CrossRef
Google scholar
|
[28] |
Ginhoux F, Greter M, Leboeuf M, Nandi S, See P, Gokhan S, Mehler MF, Conway SJ, Ng LG, Stanley ER
CrossRef
Google scholar
|
[29] |
Gore A, Li Z, Fung HL, Young JE, Agarwal S, Antosiewicz-Bourget J, Canto I, Giorgetti A, Israel MA, Kiskinis E
CrossRef
Google scholar
|
[30] |
Greter M, Lelios I, Pelczar P, Hoeffel G, Price J, Leboeuf M, Kundig TM, Frei K, Ginhoux F, Merad M
CrossRef
Google scholar
|
[31] |
Griesi-Oliveira K, Acab A, Gupta AR, Sunaga DY, Chailangkarn T, Nicol X, Nunez Y, Walker MF, Murdoch JD, Sanders SJ
CrossRef
Google scholar
|
[32] |
Grove J, Ripke S, Als TD, Mattheisen M, Walters RK, Won H, Pallesen J, Agerbo E, Andreassen OA, Anney R
CrossRef
Google scholar
|
[33] |
Guillemot F, Zimmer C (2011) From cradle to grave: the multiple roles of fibroblast growth factors in neural development. Neuron 71:574–588
CrossRef
Google scholar
|
[34] |
Hakak Y, Walker JR, Li C, Wong WH, Davis KL, Buxbaum JD, Haroutunian V, Fienberg AA (2001) Genome-wide expression analysis reveals dysregulation of myelination-related genes in chronic schizophrenia. Proc Natl Acad Sci U S A 98:4746–4751
CrossRef
Google scholar
|
[35] |
Hashimoto-Torii K, Torii M, Fujimoto M, Nakai A, El Fatimy R, Mezger V, Ju MJ, Ishii S, Chao SH, Brennand KJ
CrossRef
Google scholar
|
[36] |
Hook V, Brennand KJ, Kim Y, Toneff T, Funkelstein L, Lee KC, Ziegler M, Gage FH (2014) Human iPSC neurons display activitydependent neurotransmitter secretion: aberrant catecholamine levels in schizophrenia neurons. Stem Cell Rep 3:531–538
CrossRef
Google scholar
|
[37] |
Hu BY, Du ZW, Zhang SC (2009) Differentiation of human oligodendrocytes from pluripotent stem cells. Nat Protoc 4:1614–1622
CrossRef
Google scholar
|
[38] |
Iefremova V, Manikakis G, Krefft O, Jabali A, Weynans K, Wilkens R, Marsoner F, Brandl B, Muller FJ, Koch P
CrossRef
Google scholar
|
[39] |
Ji J, Ng SH, Sharma V, Neculai D, Hussein S, Sam M, Trinh Q, Church GM, McPherson JD, Nagy A
CrossRef
Google scholar
|
[40] |
Jo J, Xiao Y, Sun AX, Cukuroglu E, Tran HD, Goke J, Tan ZY, Saw TY, Tan CP, Lokman H
CrossRef
Google scholar
|
[41] |
Jones JR, Kong L, Hanna MGT, Hoffman B, Krencik R, Bradley R, Hagemann T, Choi J, Doers M, Dubovis M
CrossRef
Google scholar
|
[42] |
Kadoshima T, Sakaguchi H, Nakano T, Soen M, Ando S, Eiraku M, Sasai Y (2013) Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc Natl Acad Sci U S A 110:20284–20289
CrossRef
Google scholar
|
[43] |
Kang E, Wang X, Tippner-Hedges R, Ma H, Folmes CD, Gutierrez NM, Lee Y, Van Dyken C, Ahmed R, Li Y
CrossRef
Google scholar
|
[44] |
Keirstead HS, Nistor G, Bernal G, Totoiu M, Cloutier F, Sharp K, Steward O (2005) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants remyelinate and restore locomotion after spinal cord injury. J Neurosci 25:4694–4705
CrossRef
Google scholar
|
[45] |
Kelsom C, Lu W (2013) Development and specification of GABAergic cortical interneurons. Cell Biosci 3:19
CrossRef
Google scholar
|
[46] |
Kepecs A, Fishell G (2014) Interneuron cell types are fit to function. Nature 505:318–326
CrossRef
Google scholar
|
[47] |
Kerr CL, Letzen BS, Hill CM, Agrawal G, Thakor NV, Sterneckert JL, Gearhart JD, All AH (2010) Efficient differentiation of human embryonic stem cells into oligodendrocyte progenitors for application in a rat contusion model of spinal cord injury. Int J Neurosci 120:305–313
CrossRef
Google scholar
|
[48] |
Khakh BS, Sofroniew MV (2015) Diversity of astrocyte functions and phenotypes in neural circuits. Nat Neurosci 18:942–952
CrossRef
Google scholar
|
[49] |
Kierdorf K, Erny D, Goldmann T, Sander V, Schulz C, Perdiguero EG, Wieghofer P, Heinrich A, Riemke P, Holscher C
CrossRef
Google scholar
|
[50] |
Kolomeets NS, Orlovskaya DD, Uranova NA (2007) Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse 61:615–621
CrossRef
Google scholar
|
[51] |
Krencik R, Weick JP, Liu Y, Zhang ZJ, Zhang SC (2011) Specification of transplantable astroglial subtypes from human pluripotent stem cells. Nat Biotechnol 29:528–534
CrossRef
Google scholar
|
[52] |
Krencik R, Zhang SC (2011) Directed differentiation of functional astroglial subtypes from human pluripotent stem cells. Nat Protoc 6:1710–1717
CrossRef
Google scholar
|
[53] |
Lake BB, Ai R, Kaeser GE, Salathia NS, Yung YC, Liu R, Wildberg A, Gao D, Fung HL, Chen S
CrossRef
Google scholar
|
[54] |
Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA (2013) Cerebral organoids model human brain development and microcephaly. Nature 501:373–379
CrossRef
Google scholar
|
[55] |
Lee S, Hjerling-Leffler J, Zagha E, Fishell G, Rudy B (2010) The largest group of superficial neocortical GABAergic interneurons expresses ionotropic serotonin receptors. J Neurosci 30:16796–16808
CrossRef
Google scholar
|
[56] |
Lee SM, Tole S, Grove E, McMahon AP (2000) A local Wnt-3a signal is required for development of the mammalian hippocampus. Development 127:457–467
|
[57] |
Li L, Tian E, Chen X, Chao J, Klein J, Qu Q, Sun G, Sun G, Huang Y, Warden CD
CrossRef
Google scholar
|
[58] |
Li W, Ghose S, Gleason K, Begovic A, Perez J, Bartko J, Russo S, Wagner AD, Selemon L, Tamminga CA (2015) Synaptic proteins in the hippocampus indicative of increased neuronal activity in CA3 in schizophrenia. Am J Psychiatry 172:373–382
CrossRef
Google scholar
|
[59] |
Li Y, Muffat J, Omer A, Bosch I, Lancaster MA, Sur M, Gehrke L, Knoblich JA, Jaenisch R (2017) Induction of expansion and folding in human cerebral organoids. Cell Stem Cell 20(385–396): e383
CrossRef
Google scholar
|
[60] |
Liu A, Niswander LA (2005) Bone morphogenetic protein signalling and vertebrate nervous system development. Nat Rev Neurosci 6:945–954
CrossRef
Google scholar
|
[61] |
Liu Y, Liu H, Sauvey C, Yao L, Zarnowska ED, Zhang SC (2013) Directed differentiation of forebrain GABA interneurons from human pluripotent stem cells. Nat Protoc 8:1670–1679
CrossRef
Google scholar
|
[62] |
Maden M (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 8:755–765
CrossRef
Google scholar
|
[63] |
Madhavan M, Nevin ZS, Shick HE, Garrison E, Clarkson-Paredes C, Karl M, Clayton BLL, Factor DC, Allan KC, Barbar L
CrossRef
Google scholar
|
[64] |
Madison JM, Zhou F, Nigam A, Hussain A, Barker DD, Nehme R, van der Ven K, Hsu J, Wolf P, Fleishman M
CrossRef
Google scholar
|
[65] |
Mansour AA, Goncalves JT, Bloyd CW, Li H, Fernandes S, Quang D, Johnston S, Parylak SL, Jin X, Gage FH (2018) An in vivo model of functional and vascularized human brain organoids. Nat Biotechnol 36:432–441
CrossRef
Google scholar
|
[66] |
Marchetto MC, Belinson H, Tian Y, Freitas BC, Fu C, Vadodaria K, Beltrao-Braga P, Trujillo CA, Mendes APD, Padmanabhan K
CrossRef
Google scholar
|
[67] |
Marchetto MC, Carromeu C, Acab A, Yu D, Yeo GW, Mu Y, Chen G, Gage FH, Muotri AR (2010) A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143:527–539
CrossRef
Google scholar
|
[68] |
Mariani J, Coppola G, Zhang P, Abyzov A, Provini L, Tomasini L, Amenduni M, Szekely A, Palejev D, Wilson M
CrossRef
Google scholar
|
[69] |
Maroof AM, Keros S, Tyson JA, Ying SW, Ganat YM, Merkle FT, Liu B, Goulburn A, Stanley EG, Elefanty AG
CrossRef
Google scholar
|
[70] |
Mayer C, Hafemeister C, Bandler RC, Machold R, Batista Brito R, Jaglin X, Allaway K, Butler A, Fishell G, Satija R (2018) Developmental diversification of cortical inhibitory interneurons. Nature 555:457–462
CrossRef
Google scholar
|
[71] |
Mertens J, Marchetto MC, Bardy C, Gage FH (2016) Evaluating cell reprogramming, differentiation and conversion technologies in neuroscience. Nat Rev Neurosci 17:424–437
CrossRef
Google scholar
|
[72] |
Mertens J, Wang QW, Kim Y, Yu DX, Pham S, Yang B, Zheng Y, Diffenderfer KE, Zhang J, Soltani S
CrossRef
Google scholar
|
[73] |
Miller FD, Gauthier AS (2007) Timing is everything: making neurons versus glia in the developing cortex. Neuron 54:357–369
CrossRef
Google scholar
|
[74] |
Miyoshi G, Hjerling-Leffler J, Karayannis T, Sousa VH, Butt SJ, Battiste J, Johnson JE, Machold RP, Fishell G (2010) Genetic fate mapping reveals that the caudal ganglionic eminence produces a large and diverse population of superficial cortical interneurons. J Neurosci 30:1582–1594
CrossRef
Google scholar
|
[75] |
Morrison SJ, Perez SE, Qiao Z, Verdi JM, Hicks C, Weinmaster G, Anderson DJ (2000) Transient Notch activation initiates an irreversible switch from neurogenesis to gliogenesis by neural crest stem cells. Cell 101:499–510
CrossRef
Google scholar
|
[76] |
Muffat J, Li Y, Yuan B, Mitalipova M, Omer A, Corcoran S, Bakiasi G, Tsai LH, Aubourg P, Ransohoff RM
CrossRef
Google scholar
|
[77] |
Muguruma K, Nishiyama A, Kawakami H, Hashimoto K, Sasai Y (2015) Self-organization of polarized cerebellar tissue in 3D culture of human pluripotent stem cells. Cell Rep 10:537–550
CrossRef
Google scholar
|
[78] |
Munoz-Sanjuan I, Brivanlou AH (2002) Neural induction, the default model and embryonic stem cells. Nat Rev Neurosci 3:271–280
CrossRef
Google scholar
|
[79] |
Murai K, Sun G, Ye P, Tian E, Yang S, Cui Q, Sun G, Trinh D, Sun O, Hong T
CrossRef
Google scholar
|
[80] |
Nave KA, Ehrenreich H (2014) Myelination and oligodendrocyte functions in psychiatric diseases. JAMA Psychiatry 71:582–584
CrossRef
Google scholar
|
[81] |
Nestler EJ, Hyman SE (2010) Animal models of neuropsychiatric disorders. Nat Neurosci 13:1161–1169
CrossRef
Google scholar
|
[82] |
Nicholas CR, Chen J, Tang Y, Southwell DG, Chalmers N, Vogt D, Arnold CM, Chen YJ, Stanley EG, Elefanty AG
CrossRef
Google scholar
|
[83] |
Nistor GI, Totoiu MO, Haque N, Carpenter MK, Keirstead HS (2005) Human embryonic stem cells differentiate into oligodendrocytes in high purity and myelinate after spinal cord transplantation. Glia 49:385–396
CrossRef
Google scholar
|
[84] |
Pandya H, Shen MJ, Ichikawa DM, Sedlock AB, Choi Y, Johnson KR, Kim G, Brown MA, Elkahloun AG, Maric D
CrossRef
Google scholar
|
[85] |
Pasca AM, Sloan SA, Clarke LE, Tian Y, Makinson CD, Huber N, Kim CH, Park JY, O’Rourke NA, Nguyen KD
CrossRef
Google scholar
|
[86] |
Pasca SP (2018) The rise of three-dimensional human brain cultures. Nature 553:437–445
CrossRef
Google scholar
|
[87] |
Pasca SP (2019) Assembling human brain organoids. Science 363:126–127
CrossRef
Google scholar
|
[88] |
Pasca SP, Portmann T, Voineagu I, Yazawa M, Shcheglovitov A, Pasca AM, Cord B, Palmer TD, Chikahisa S, Nishino S
CrossRef
Google scholar
|
[89] |
Piao J, Major T, Auyeung G, Policarpio E, Menon J, Droms L, Gutin P, Uryu K, Tchieu J, Soulet D
CrossRef
Google scholar
|
[90] |
Qian X, Nguyen HN, Song MM, Hadiono C, Ogden SC, Hammack C, Yao B, Hamersky GR, Jacob F, Zhong C
CrossRef
Google scholar
|
[91] |
Quadrato G, Nguyen T, Macosko EZ, Sherwood JL, Min Yang S, Berger DR, Maria N, Scholvin J, Goldman M, Kinney JP
CrossRef
Google scholar
|
[92] |
Rasetti R, Mattay VS, White MG, Sambataro F, Podell JE, Zoltick B, Chen Q, Berman KF, Callicott JH, Weinberger DR (2014) Altered hippocampal-parahippocampal function during stimulus encoding: a potential indicator of genetic liability for schizophrenia. JAMA Psychiatry 71:236–247
CrossRef
Google scholar
|
[93] |
Ricciardi S, Ungaro F, Hambrock M, Rademacher N, Stefanelli G, Brambilla D, Sessa A, Magagnotti C, Bachi A, Giarda E
CrossRef
Google scholar
|
[94] |
Rodrigues GMC, Gaj T, Adil MM, Wahba J, Rao AT, Lorbeer FK, Kulkarni RU, Diogo MM, Cabral JMS, Miller EW
CrossRef
Google scholar
|
[95] |
Sakaguchi H, Kadoshima T, Soen M, Narii N, Ishida Y, Ohgushi M, Takahashi J, Eiraku M, Sasai Y (2015) Generation of functional hippocampal neurons from self-organizing human embryonic stem cell-derived dorsomedial telencephalic tissue. Nat Commun 6:8896
CrossRef
Google scholar
|
[96] |
Santos R, Vadodaria KC, Jaeger BN, Mei A, Lefcochilos-Fogelquist S, Mendes APD, Erikson G, Shokhirev M, Randolph-Moore L, Fredlender C
CrossRef
Google scholar
|
[97] |
Sarkar A, Mei A, Paquola ACM, Stern S, Bardy C, Klug JR, Kim S, Neshat N, Kim HJ, Ku M
CrossRef
Google scholar
|
[98] |
Schafer ST, Paquola ACM, Stern S, Gosselin D, Ku M, Pena M, Kuret TJM, Liyanage M, Mansour AA, Jaeger BN
CrossRef
Google scholar
|
[99] |
Schizophrenia Working Group of the PsychiatricGenomics, C (2014) Biological insights from 108 schizophrenia-associated genetic loci. Nature 511:421–427
CrossRef
Google scholar
|
[100] |
Schulz C, Gomez Perdiguero E, Chorro L, Szabo-Rogers H, Cagnard N, Kierdorf K, Prinz M, Wu B, Jacobsen SE, Pollard JW
CrossRef
Google scholar
|
[101] |
Sellgren CM, Gracias J, Watmuff B, Biag JD, Thanos JM, Whittredge PB, Fu T, Worringer K, Brown HE, Wang J
CrossRef
Google scholar
|
[102] |
Shao Z, Noh H, Bin Kim W, Ni P, Nguyen C, Cote SE, Noyes E, Zhao J, Parsons T, Park JM
CrossRef
Google scholar
|
[103] |
Sharp J, Frame J, Siegenthaler M, Nistor G, Keirstead HS (2010) Human embryonic stem cell-derived oligodendrocyte progenitor cell transplants improve recovery after cervical spinal cord injury. Stem Cells 28:152–163
CrossRef
Google scholar
|
[104] |
Shcheglovitov A, Shcheglovitova O, Yazawa M, Portmann T, Shu R, Sebastiano V, Krawisz A, Froehlich W, Bernstein JA, Hallmayer JF
CrossRef
Google scholar
|
[105] |
Shi Y, Inoue H, Wu JC, Yamanaka S (2017) Induced pluripotent stem cell technology: a decade of progress. Nat Rev Drug Discov 16:115–130
CrossRef
Google scholar
|
[106] |
Shi Y, Kirwan P, Smith J, Robinson HP, Livesey FJ (2012) Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat Neurosci 15(477–486):S471
CrossRef
Google scholar
|
[107] |
Sloan SA, Darmanis S, Huber N, Khan TA, Birey F, Caneda C, Reimer R, Quake SR, Barres BA, Pasca SP (2017) Human astrocyte maturation captured in 3D cerebral cortical spheroids derived from pluripotent stem cells. Neuron 95(779–790):e776
CrossRef
Google scholar
|
[108] |
Stern S, Santos R, Marchetto MC, Mendes APD, Rouleau GA, Biesmans S, Wang QW, Yao J, Charnay P, Bang AG
CrossRef
Google scholar
|
[109] |
Sur M, Rubenstein JL (2005) Patterning and plasticity of the cerebral cortex. Science 310:805–810
CrossRef
Google scholar
|
[110] |
Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131:861–872
CrossRef
Google scholar
|
[111] |
Tamminga CA, Stan AD, Wagner AD (2010) The hippocampal formation in schizophrenia. Am J Psychiatry 167:1178–1193
CrossRef
Google scholar
|
[112] |
Tao Y, Zhang SC (2016) Neural subtype specification from human pluripotent stem cells. Cell Stem Cell 19:573–586
CrossRef
Google scholar
|
[113] |
Tekin S, Cummings JL (2002) Frontal-subcortical neuronal circuits and clinical neuropsychiatry: an update. J Psychosom Res 53:647–654
CrossRef
Google scholar
|
[114] |
Tkachev D, Mimmack ML, Ryan MM, Wayland M, Freeman T, Jones PB, Starkey M, Webster MJ, Yolken RH, Bahn S (2003) Oligodendrocyte dysfunction in schizophrenia and bipolar disorder. Lancet 362:798–805
CrossRef
Google scholar
|
[115] |
Vadodaria KC, Ji Y, Skime M, Paquola A, Nelson T, Hall-Flavin D, Fredlender C, Heard KJ, Deng Y, Le AT
CrossRef
Google scholar
|
[116] |
Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, Mill J, Cantor RM, Blencowe BJ, Geschwind DH (2011) Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature 474:380–384
CrossRef
Google scholar
|
[117] |
Wang L, Xia J, Li J, Hagemann TL, Jones JR, Fraenkel E, Weitz DA, Zhang SC, Messing A, Feany MB (2018) Tissue and cellular rigidity and mechanosensitive signaling activation in Alexander disease. Nat Commun 9:1899
CrossRef
Google scholar
|
[118] |
Wang S, Bates J, Li X, Schanz S, Chandler-Militello D, Levine C, Maherali N, Studer L, Hochedlinger K, Windrem M
CrossRef
Google scholar
|
[119] |
Wang Y, Szretter KJ, Vermi W, Gilfillan S, Rossini C, Cella M, Barrow AD, Diamond MS, Colonna M (2012) IL-34 is a tissue-restricted ligand of CSF1R required for the development of Langerhans cells and microglia. Nat Immunol 13:753–760
CrossRef
Google scholar
|
[120] |
Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, Kawasaki H, Watanabe Y, Mizuseki K, Sasai Y (2005) Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8:288–296
CrossRef
Google scholar
|
[121] |
Wen Z, Nguyen HN, Guo Z, Lalli MA, Wang X, Su Y, Kim NS, Yoon KJ, Shin J, Zhang C
CrossRef
Google scholar
|
[122] |
Wilson SW, Houart C (2004) Early steps in the development of the forebrain. Dev Cell 6:167–181
CrossRef
Google scholar
|
[123] |
Wimmer RA, Leopoldi A, Aichinger M, Wick N, Hantusch B, Novatchkova M, Taubenschmid J, Hammerle M, Esk C, Bagley JA
CrossRef
Google scholar
|
[124] |
Windrem MS, Osipovitch M, Liu Z, Bates J, Chandler-Militello D, Zou L, Munir J, Schanz S, McCoy K, Miller RH
CrossRef
Google scholar
|
[125] |
Wonders CP, Anderson SA (2006) The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687–696
CrossRef
Google scholar
|
[126] |
Wray NR, Ripke S, Mattheisen M, Trzaskowski M, Byrne EM, Abdellaoui A, Adams MJ, Agerbo E, Air TM, Andlauer TMF
CrossRef
Google scholar
|
[127] |
Xiang Y, Tanaka Y, Patterson B, Kang YJ, Govindaiah G, Roselaar N, Cakir B, Kim KY, Lombroso AP, Hwang SM
CrossRef
Google scholar
|
[128] |
Yamasaki R, Lu H, Butovsky O, Ohno N, Rietsch AM, Cialic R, Wu PM, Doykan CE, Lin J, Cotleur AC
CrossRef
Google scholar
|
[129] |
Yang N, Zuchero JB, Ahlenius H, Marro S, Ng YH, Vierbuchen T, Hawkins JS, Geissler R, Barres BA, Wernig M (2013) Generation of oligodendroglial cells by direct lineage conversion. Nat Biotechnol 31:434–439
CrossRef
Google scholar
|
[130] |
Yoon KJ, Nguyen HN, Ursini G, Zhang F, Kim NS, Wen Z, Makri G, Nauen D, Shin JH, Park Y
CrossRef
Google scholar
|
[131] |
Yu DX, Di Giorgio FP, Yao J, Marchetto MC, Brennand K, Wright R, Mei A, McHenry L, Lisuk D, Grasmick JM
CrossRef
Google scholar
|
[132] |
Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R
CrossRef
Google scholar
|
[133] |
Zeisel A, Munoz-Manchado AB, Codeluppi S, Lonnerberg P, La Manno G, Jureus A, Marques S, Munguba H, He L, Betsholtz C
CrossRef
Google scholar
|
[134] |
Zhang Z, Marro SG, Zhang Y, Arendt KL, Patzke C, Zhou B, Fair T, Yang N, Sudhof TC, Wernig M
CrossRef
Google scholar
|
[135] |
Zhang ZN, Freitas BC, Qian H, Lux J, Acab A, Trujillo CA, Herai RH, Nguyen Huu VAWen JH, Joshi-Barr S
CrossRef
Google scholar
|
[136] |
Zhao D, Lin M, Chen J, Pedrosa E, Hrabovsky A, Fourcade HM, Zheng D, Lachman HM (2015a) MicroRNA profiling of neurons generated using induced pluripotent stem cells derived from patients with schizophrenia and schizoaffective disorder, and 22q11.2 Del. PLoS ONE 10:e0132387
CrossRef
Google scholar
|
[137] |
Zhao T, Zhang ZN, Rong Z, Xu Y (2011) Immunogenicity of induced pluripotent stem cells. Nature 474:212–215
CrossRef
Google scholar
|
[138] |
Zhao T, Zhang ZN, Westenskow PD, Todorova D, Hu Z, Lin T, Rong Z, Kim J, He J, Wang M
CrossRef
Google scholar
|
/
〈 | 〉 |