Modeling developmental neuropsychiatric disorders with iPSC technology: Challenges and opportunities

Current Opinion in Neurobiology

Volumn 36, Issue , 2016, Pages 66-73

  Young Pearse, Tracy L ^a   Morrow, Eric M ^b,c  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b BROWN UNIVERSITY   (United States)

^c BROWN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTISM; BIPOLAR DISORDER; CELL FATE; CELL SPECIFICITY; COPY NUMBER VARIATION; GENE EXPRESSION; GENE MUTATION; GENETIC HETEROGENEITY; HUMAN; IDIOPATHIC DISEASE; MENTAL DISEASE; NERVE CELL DIFFERENTIATION; NEUROLOGIC DISEASE; NEUROPSYCHIATRIC DISORDER; NONHUMAN; NUCLEAR REPROGRAMMING; PHELAN MCDERMID SYNDROME; PHENOTYPIC VARIATION; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; REVIEW; SYNAPTIC TRANSMISSION; THEORETICAL STUDY; ANIMAL; BIOLOGICAL MODEL; CELL REPROGRAMMING TECHNIQUE; DENDRITE; GLIA; IN VITRO STUDY; INDUCED PLURIPOTENT STEM CELL; LONG QT SYNDROME; METABOLISM; NERVE CELL; PATHOPHYSIOLOGY; PHENOTYPE; PHYSIOLOGY; REPRODUCIBILITY; SCHIZOPHRENIA; SYNAPSE; SYNDACTYLY;

ANIMALS; AUTISM SPECTRUM DISORDER; AUTISTIC DISORDER; CELLULAR REPROGRAMMING TECHNIQUES; DENDRITES; HUMANS; IN VITRO TECHNIQUES; INDUCED PLURIPOTENT STEM CELLS; LONG QT SYNDROME; MODELS, NEUROLOGICAL; NEUROGLIA; NEURONS; PHENOTYPE; REPRODUCIBILITY OF RESULTS; SCHIZOPHRENIA; SYNAPSES; SYNDACTYLY;

EID: 84945152039     PISSN: 09594388     EISSN: 18736882     Source Type: Journal    
DOI: 10.1016/j.conb.2015.10.006     Document Type: Review

References (35)

1. Pasca S.P., Portmann T., Voineagu I., Yazawa M., Shcheglovitov A., Pasca A.M., Cord B., Palmer T.D., Chikahisa S., Nishino S., et al. Using iPSC-derived neurons to uncover cellular phenotypes associated with Timothy syndrome. Nat Med 2011, 17:1657-1662.
2. Krey J.F., Pasca S.P., Shcheglovitov A., Yazawa M., Schwemberger R., Rasmusson R., Dolmetsch R.E. Timothy syndrome is associated with activity-dependent dendritic retraction in rodent and human neurons. Nat Neurosci 2013, 16:201-209.
3. Johnson M.B., Wang P.P., Atabay K.D., Murphy E.A., Doan R.N., Hecht J.L., Walsh C.A. Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex. Nat Neurosci 2015, 18:637-646.
4. Macosko E.Z., Basu A., Satija R., Nemesh J., Shekhar K., Goldman M., Tirosh I., Bialas A.R., Kamitaki N., Martersteck E.M., et al. Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 2015, 161:1202-1214.
5. Zhang Y., Pak C., Han Y., Ahlenius H., Zhang Z., Chanda S., Marro S., Patzke C., Acuna C., Covy J., et al. Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 2013, 78:785-798.
6. Srikanth P., Han K., Callahan D.G., Makovkina E., Muratore C.R., Lalli M.A., Zhou H., Boyd J.D., Kosik K.S., Selkoe D.J., Young-Pearse T.L. Genomic DISC1 disruption in hiPSCs alters wnt signaling and neural cell fate. Cell Rep 2015, 15:851-857.
7. Porteous D.J., Millar J.K., Brandon N.J., Sawa A. DISC1 at 10: connecting psychiatric genetics and neuroscience. Trends Mol Med 2011, 17:699-706.
8. Millar J.K., Wilson-Annan J.C., Anderson S., Christie S., Taylor M.S., Semple C.A., Devon R.S., St Clair D.M., Muir W.J., Blackwood D.H., Porteous D.J. Disruption of two novel genes by a translocation co-segregating with schizophrenia. Hum Mol Genet 2000, 22:1415-1423. (9).
9. Brennand K.J., Simone A., Jou J., Gelboin-Burkhart C., Tran N., Sangar S., Li Y., Mu Y., Chen G., Yu D., et al. Modelling schizophrenia using human induced pluripotent stem cells. Nature 2011, 473:221-225.
10. Lancaster M.A., Knoblich J.A. Generation of cerebral organoids from human pluripotent stem cells. Nat Protoc 2014, 9:2329-2340.
11. Lancaster M.A., Renner M., Martin C.A., Wenzel D., Bicknell L.S., Hurles M.E., Homfray T., Penninger J.M., Jackson A.P., Knoblich J.A. Cerebral organoids model human brain development and microcephaly. Nature 2013, 501:373-379.
12. Brennand K., Savas J.N., Kim Y., Tran N., Simone A., Hashimoto-Torii K., Beaumont K.G., Kim H.J., Topol A., Ladran I., Abdelrahim M., Matikainen-Ankney B., Chao S.H., Mrksich M., Rakic P., Fang G., Zhang B., Yates J.R., Gage F.H. Phenotypic differences in hiPSC NPCs derived from patients with schizophrenia. Mol Psychiatry 2015, 20:361-368.
13. Shcheglovitov A., Shcheglovitova O., Yazawa M., Portmann T., Shu R., Sebastiano V., Krawisz A., Froehlich W., Bernstein J.A., Hallmayer J.F., et al. SHANK3 and IGF1 restore synaptic deficits in neurons from 22q13 deletion syndrome patients. Nature 2013, 503:267-271.
14. Smith C., Gore A., Yan W., Abalde-Atristain L., Li Z., He C., Wang Y., Brodsky R.A., Zhang K., Cheng L., et al. Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 2014, 15:12-13.
15. Veres A., Gosis B.S., Ding Q., Collins R., Ragavendran A., Brand H., Erdin S., Cowan C.A., Talkowski M.E., Musunuru K. Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 2014, 15:27-30.
16. Suzuki K., Yu C., Qu J., Li M., Yao X., Yuan T., Goebl A., Tang S., Ren R., Aizawa E., et al. Targeted gene correction minimally impacts whole-genome mutational load in human-disease-specific induced pluripotent stem cell clones. Cell Stem Cell 2014, 15:31-36.
17. Tchieu J., Kuoy E., Chin M.H., Trinh H., Patterson M., Sherman S.P., Aimiuwu O., Lindgren A., Hakimian S., Zack J.A., et al. Female human iPSCs retain an inactive X chromosome. Cell Stem Cell 2010, 7:329-342.
18. Bruck T., Benvenisty N. Meta-analysis of the heterogeneity of X chromosome inactivation in human pluripotent stem cells. Stem Cell Res 2011, 6:187-193.
19. Kim D.H., Jeon Y., Anguera M.C., Lee J.T. X-chromosome epigenetic reprogramming in pluripotent stem cells via noncoding genes. Semin Cell Dev Biol 2011, 22:336-342.
20. Germain N.D., Chen P.F., Plocik A.M., Glatt-Deeley H., Brown J., Fink J.J., Bolduc K.A., Robinson T.M., Levine E.S., Reiter L.T., et al. Gene expression analysis of human induced pluripotent stem cell-derived neurons carrying copy number variants of chromosome 15q11-q13.1. Mol Autism 2014, 5:44.
21. Chamberlain S.J., Chen P.F., Ng K.Y., Bourgois-Rocha F., Lemtiri-Chlieh F., Levine E.S., Lalande M. Induced pluripotent stem cell models of the genomic imprinting disorders Angelman and Prader-Willi syndromes. Proc Natl Acad Sci U S A 2010, 107:17668-17673.
22. Radford E.J., Ferron S.R., Ferguson-Smith A.C. Genomic imprinting as an adaptative model of developmental plasticity. FEBS Lett 2011, 585:2059-2066.
23. Lin M., Hrabovsky A., Pedrosa E., Wang T., Zheng D., Lachman H.M. Allele-biased expression in differentiating human neurons: implications for neuropsychiatric disorders. PLoS ONE 2012, 7:e44017.
24. Madison J.M., Zhou F., Nigam A., Hussain A., Barker D.D., Nehme R., van der Ven K., Hsu J., Wolf P., Fleishman M., et al. Characterization of bipolar disorder patient-specific induced pluripotent stem cells from a family reveals neurodevelopmental and mRNA expression abnormalities. Mol Psychiatry 2015, 20:703-717.
25. Mariani J., Coppola G., Zhang P., Abyzov A., Provini L., Tomasini L., Amenduni M., Szekely A., Palejev D., Wilson M., Gerstein M., Grigorenko E.L., Chawarska K., Pelphrey K.A., Howe J.R., Vaccarino F.M. FOXG1-dependent dysregulation of GABA/glutamate neuron differentiation in autism spectrum disorders. Cell 2015, 162:375-390.
26. Lewis D.A., Curley A.A., Glausier J.R., Volk D.W. Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends Neurosci 2011, 35:57-67.
27. Tang G., Gudsnuk K., Kuo S.H., Cotrina M.L., Rosoklija G., Sosunov A., Sonders M.S., Kanter E., Castagna C., Yamamoto A., et al. Loss of mTOR-dependent macroautophagy causes autistic-like synaptic pruning deficits. Neuron 2014, 83:1131-1143.
28. Wen Z., Nguyen H.N., Guo Z., Lalli M.A., Wang X., Su Y., Kim N.S., Yoon K.J., Shin J., Zhang C., et al. Synaptic dysregulation in a human iPS cell model of mental disorders. Nature 2014, 515:414-418.
29. Stoner R., Chow M.L., Boyle M.P., Sunkin S.M., Mouton P.R., Roy S., Wynshaw-Boris A., Colamarino S.A., Lein E.S., Courchesne E. Patches of disorganization in the neocortex of children with autism. N Engl J Med 2014, 370:1209-1219.
30. Muratore C.R., Srikanth P., Callahan D.G., Young-Pearse T.L. Comparison and optimization of hiPSC forebrain cortical differentiation protocols. PLoS ONE 2014, 9:e105807.
31. Yuan S.H., Martin J., Elia J., Flippin J., Paramban R.I., Hefferan M.P., Vidal J.G., Mu Y., Killian R.L., Israel M.A., et al. Cell-surface marker signatures for the isolation of neural stem cells, glia and neurons derived from human pluripotent stem cells. PLoS ONE 2011, 6:e17540.
32. Zeng H., Guo M., Martins-Taylor K., Wang X., Zhang Z., Park J.W., Zhan S., Kronenberg M.S., Lichtler A., Liu H.X., et al. Specification of region-specific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS ONE 2010, 5:e11853.
33. Sloan S.A., Barres B.A. Mechanisms of astrocyte development and their contributions to neurodevelopmental disorders. Curr Opin Neurobiol 2014, 27:75-81.
34. Krencik R., Hokanson K.C., Narayan A.R., Dvornik J., Rooney G.E., Rauen K.A., Weiss L.A., Rowitch D.H., Ullian E.M. Dysregulation of astrocyte extracellular signaling in Costello syndrome. Sci Transl Med 2015, 7:286ra266.
35. Yoon K.J., Nguyen H.N., Ursini G., Zhang F., Kim N.S., Wen Z., Makri G., Nauen D., Shin J.H., Park Y., Chung R., Pekle E., Zhang C., Towe M., Hussaini S.M., Lee Y., Rujescu D., St Clair D., Kleinman J.E., Hyde T.M., Krauss G., Christian K.M., Rapoport J.L., Weinberger D.R., Song H., Ming G.L. Modeling a genetic risk for schizophrenia in iPSCs and mice reveals neural stem cell deficits associated with adherens junctions and polarity. Cell Stem Cell 2014, 15:79-91.