Generation of Human Striatal Neurons by MicroRNA-Dependent Direct Conversion of Fibroblasts

Neuron

Volumn 84, Issue 2, 2014, Pages 311-323

  Victor, Matheus B ^a   Richner, Michelle ^a   Hermanstyne, Tracey O ^a   Ransdell, Joseph L ^a   Sobieski, Courtney ^a   Deng, Pan Yue ^b   Klyachko, Vitaly A ^b   Nerbonne, Jeanne M ^a   Yoo, Andrew S ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MICRORNA 124; MICRORNA 9; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCL11B; TRANSCRIPTION FACTOR DLX1; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR MYT1L; UNCLASSIFIED DRUG; MICRORNA;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL FATE; CELL FUNCTION; CELL POPULATION; CONTROLLED STUDY; CORPUS STRIATUM; FIBROBLAST; GAPDH GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; HOUSEKEEPING GENE; HPRT1 GENE; HUMAN; HUMAN CELL; HUMAN TISSUE; MOUSE; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NONHUMAN; NUCLEAR REPROGRAMMING; PROTEIN ANALYSIS; PROTEIN EXPRESSION; RSP18 GENE; ANIMAL; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; METABOLISM; NEOSTRIATUM; NERVE CELL; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CORPUS STRIATUM; FIBROBLASTS; HUMANS; MICE; MICRORNAS; NEOSTRIATUM; NEURONS; TRANSCRIPTION FACTORS;

EID: 84908231578     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2014.10.016     Document Type: Article

References (62)

1. Alavian K.N., Li H., Collis L., Bonanni L., Zeng L., Sacchetti S., Lazrove E., Nabili P., Flaherty B., Graham M., et al. Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase. Nat. Cell Biol. 2011, 13:1224-1233.
2. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
3. Albu D.I., Feng D., Bhattacharya D., Jenkins N.A., Copeland N.G., Liu P., Avram D. BCL11B is required for positive selection and survival of double-positive thymocytes. J.Exp. Med. 2007, 204:3003-3015.
4. Anderson S.A., Qiu M., Bulfone A., Eisenstat D.D., Meneses J., Pedersen R., Rubenstein J.L. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 1997, 19:27-37.
5. Arlotta P., Molyneaux B.J., Jabaudon D., Yoshida Y., Macklis J.D. Ctip2 controls the differentiation of medium spiny neurons and the establishment of the cellular architecture of the striatum. J.Neurosci. 2008, 28:622-632.
6. Ballas N., Mandel G. The many faces of REST oversee epigenetic programming of neuronal genes. Curr. Opin. Neurobiol. 2005, 15:500-506.
7. Banito A., Rashid S.T., Acosta J.C., Li S., Pereira C.F., Geti I., Pinho S., Silva J.C., Azuara V., Walsh M., et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev. 2009, 23:2134-2139.
8. Battaglioli E., Andrés M.E., Rose D.W., Chenoweth J.G., Rosenfeld M.G., Anderson M.E., Mandel G. REST repression of neuronal genes requires components of the hSWI.SNF complex. J.Biol. Chem. 2002, 277:41038-41045.
9. Blömer U., Kafri T., Randolph-Moore L., Verma I.M., Gage F.H. Bcl-xL protects adult septal cholinergic neurons from axotomized cell death. Proc. Natl. Acad. Sci. USA 1998, 95:2603-2608.
10. Boutz P.L., Stoilov P., Li Q., Lin C.H., Chawla G., Ostrow K., Shiue L., Ares M., Black D.L. A post-transcriptional regulatory switch in polypyrimidine tract-binding proteins reprograms alternative splicing in developing neurons. Genes Dev. 2007, 21:1636-1652.
11. Caiazzo M., Dell'Anno M.T., Dvoretskova E., Lazarevic D., Taverna S., Leo D., Sotnikova T.D., Menegon A., Roncaglia P., Colciago G., et al. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 2011, 476:224-227.
12. Conaco C., Otto S., Han J.J., Mandel G. Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. USA 2006, 103:2422-2427.
13. Induced pluripotent stem cells from patients with Huntington's disease show CAG-repeat-expansion-associated phenotypes. Cell Stem Cell 2012, 11:264-278. HD iPSC Consortium.
14. Desplats P.A., Kass K.E., Gilmartin T., Stanwood G.D., Woodward E.L., Head S.R., Sutcliffe J.G., Thomas E.A. Selective deficits in the expression of striatal-enriched mRNAs in Huntington's disease. J.Neurochem. 2006, 96:743-757.
15. Do J., Kim J.I., Bakes J., Lee K., Kaang B.K. Functional roles of neurotransmitters and neuromodulators in the dorsal striatum. Learn. Mem. 2012, 20:21-28.
16. Dougherty J.D., Schmidt E.F., Nakajima M., Heintz N. Analytical approaches to RNA profiling data for the identification of genes enriched in specific cells. Nucleic Acids Res. 2010, 38:4218-4230.
17. Ferland R.J., Cherry T.J., Preware P.O., Morrisey E.E., Walsh C.A. Characterization of Foxp2 and Foxp1 mRNA and protein in the developing and mature brain. J.Comp. Neurol. 2003, 460:266-279.
18. Fishell G., Heintz N. The neuron identity problem: form meets function. Neuron 2013, 80:602-612.
19. Gerfen C.R. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu. Rev. Neurosci. 1992, 15:285-320.
20. Gertler T.S., Chan C.S., Surmeier D.J. Dichotomous anatomical properties of adult striatal medium spiny neurons. J.Neurosci. 2008, 28:10814-10824.
21. Gong S., Zheng C., Doughty M.L., Losos K., Didkovsky N., Schambra U.B., Nowak N.J., Joyner A., Leblanc G., Hatten M.E., Heintz N. A gene expression atlas of the central nervous system based on bacterial artificial chromosomes. Nature 2003, 425:917-925.
22. Graybiel A.M., Aosaki T., Flaherty A.W., Kimura M. The basal ganglia and adaptive motor control. Science 1994, 265:1826-1831.
23. Hobert O. Regulation of terminal differentiation programs in the nervous system. Annu. Rev. Cell Dev. Biol. 2011, 27:681-696.
24. Hu B.Y., Weick J.P., Yu J., Ma L.X., Zhang X.Q., Thomson J.A., Zhang S.C. Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. USA 2010, 107:4335-4340.
25. Johnston J.G., Gerfen C.R., Haber S.N., van der Kooy D. Mechanisms of striatal pattern formation: conservation of mammalian compartmentalization. Brain Res. Dev. Brain Res. 1990, 57:93-102.
26. Kadoch C., Hargreaves D.C., Hodges C., Elias L., Ho L., Ranish J., Crabtree G.R. Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 2013, 45:592-601.
27. Karl C., Couillard-Despres S., Prang P., Munding M., Kilb W., Brigadski T., Plötz S., Mages W., Luhmann H., Winkler J., et al. Neuronal precursor-specific activity of a human doublecortin regulatory sequence. J.Neurochem. 2005, 92:264-282.
28. Koós T., Tepper J.M. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 1999, 2:467-472.
29. Kreitzer A.C. Physiology and pharmacology of striatal neurons. Annu. Rev. Neurosci. 2009, 32:127-147.
30. Lalchandani R.R., Vicini S. Inhibitory collaterals in genetically identified medium spiny neurons in mouse primary corticostriatal cultures. Physiol. Rep. 2013, Published online November 24, 2013. 10.1002/phy2.164.
31. Lapasset L., Milhavet O., Prieur A., Besnard E., Babled A., Aït-Hamou N., Leschik J., Pellestor F., Ramirez J.M., De Vos J., et al. Rejuvenating senescent and centenarian human cells by reprogramming through the pluripotent state. Genes Dev. 2011, 25:2248-2253.
32. Letinic K., Zoncu R., Rakic P. Origin of GABAergic neurons in the human neocortex. Nature 2002, 417:645-649.
33. Liu M.L., Zang T., Zou Y., Chang J.C., Gibson J.R., Huber K.M., Zhang C.L. Small molecules enable neurogenin 2 to efficiently convert human fibroblasts into cholinergic neurons. Nat. Commun. 2013, 4. 10.1038/ncomms3183.
34. Lobo M.K., Karsten S.L., Gray M., Geschwind D.H., Yang X.W. FACS-array profiling of striatal projection neuron subtypes in juvenile and adult mouse brains. Nat. Neurosci. 2006, 9:443-452.
35. Makeyev E.V., Zhang J., Carrasco M.A., Maniatis T. The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 2007, 27:435-448.
36. Marin O., Anderson S.A., Rubenstein J.L. Origin and molecular specification of striatal interneurons. J.Neurosci. 2000, 20:6063-6076.
37. Miller J.D., Ganat Y.M., Kishinevsky S., Bowman R.L., Liu B., Tu E.Y., Mandal P.K., Vera E., Shim J.W., Kriks S., et al. Human iPSC-based modeling of late-onset disease via progerin-induced aging. Cell Stem Cell 2013, 13:691-705.
38. Ouimet C.C., Greengard P. Distribution of DARPP-32 in the basal ganglia: an electron microscopic study. J.Neurocytol. 1990, 19:39-52.
39. * regulates REST and CoREST and is downregulated in Huntington's disease. J.Neurosci. 2008, 28:14341-14346.
40. Pang Z.P., Yang N., Vierbuchen T., Ostermeier A., Fuentes D.R., Yang T.Q., Citri A., Sebastiano V., Marro S., Südhof T.C., Wernig M. Induction of human neuronal cells by defined transcription factors. Nature 2011, 476:220-223.
41. Peça J., Feliciano C., Ting J.T., Wang W., Wells M.F., Venkatraman T.N., Lascola C.D., Fu Z., Feng G. Shank3 mutant mice display autistic-like behaviours and striatal dysfunction. Nature 2011, 472:437-442.
42. Pert C.B., Kuhar M.J., Snyder S.H. Opiate receptor: autoradiographic localization in rat brain. Proc. Natl. Acad. Sci. USA 1976, 73:3729-3733.
43. Ring K.L., Tong L.M., Balestra M.E., Javier R., Andrews-Zwilling Y., Li G., Walker D., Zhang W.R., Kreitzer A.C., Huang Y. Direct reprogramming of mouse and human fibroblasts into multipotent neural stem cells with a single factor. Cell Stem Cell 2012, 11:100-109.
44. Sahay A., Scobie K.N., Hill A.S., O'Carroll C.M., Kheirbek M.A., Burghardt N.S., Fenton A.A., Dranovsky A., Hen R. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011, 472:466-470.
45. Soldner F., Jaenisch R. Medicine. iPSC disease modeling. Science 2012, 338:1155-1156.
46. Son E.Y., Ichida J.K., Wainger B.J., Toma J.S., Rafuse V.F., Woolf C.J., Eggan K. Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 2011, 9:205-218.
47. Staahl B.T., Tang J., Wu W., Sun A., Gitler A.D., Yoo A.S., Crabtree G.R. Kinetic analysis of npBAF to nBAF switching reveals exchange of SS18 with CREST and integration with neural developmental pathways. J.Neurosci. 2013, 33:10348-10361.
48. Stenman J., Toresson H., Campbell K. Identification of two distinct progenitor populations in the lateral ganglionic eminence: implications for striatal and olfactory bulb neurogenesis. J.Neurosci. 2003, 23:167-174.
49. Takahashi K., Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126:663-676.
50. Tamura S., Morikawa Y., Iwanishi H., Hisaoka T., Senba E. Foxp1 gene expression in projection neurons of the mouse striatum. Neuroscience 2004, 124:261-267.
51. Tepper J.M., Tecuapetla F., Koos T., Ibanez-Sandoval O. Heterogeneity and diversity of striatal GABAergic interneurons. Front. Neuroanat. 2010, 4. 10.3389/fnana.2010.00150.
52. Venance L., Glowinski J. Heterogeneity of spike frequency adaptation among medium spiny neurones from the rat striatum. Neuroscience 2003, 122:77-92.
53. Vierbuchen T., Ostermeier A., Pang Z.P., Kokubu Y., Südhof T.C., Wernig M. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 2010, 463:1035-1041.
54. Visvanathan J., Lee S., Lee B., Lee J.W., Lee S.K. The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 2007, 21:744-749.
55. Wapinski O.L., Vierbuchen T., Qu K., Lee Q.Y., Chanda S., Fuentes D.R., Giresi P.G., Ng Y.H., Marro S., Neff N.F., et al. Hierarchical mechanisms for direct reprogramming of fibroblasts to neurons. Cell 2013, 155:621-635.
56. Xue Y., Ouyang K., Huang J., Zhou Y., Ouyang H., Li H., Wang G., Wu Q., Wei C., Bi Y., et al. Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated microRNA circuits. Cell 2013, 152:82-96.
57. Yoo A.S., Staahl B.T., Chen L., Crabtree G.R. MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 2009, 460:642-646.
58. Yoo A.S., Sun A.X., Li L., Shcheglovitov A., Portmann T., Li Y., Lee-Messer C., Dolmetsch R.E., Tsien R.W., Crabtree G.R. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 2011, 476:228-231.
59. Yu J., Vodyanik M.A., Smuga-Otto K., Antosiewicz-Bourget J., Frane J.L., Tian S., Nie J., Jonsdottir G.A., Ruotti V., Stewart R., et al. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007, 318:1917-1920.
60. Zhang R., Xue Y.Y., Lu S.D., Wang Y., Zhang L.M., Huang Y.L., Signore A.P., Chen J., Sun F.Y. Bcl-2 enhances neurogenesis and inhibits apoptosis of newborn neurons in adult rat brain following a transient middle cerebral artery occlusion. Neurobiol. Dis. 2006, 24:345-356.
61. Zhang N., An M.C., Montoro D., Ellerby L.M. Characterization of Human Huntington's Disease Cell Model from Induced Pluripotent Stem Cells. PLoS Curr. 2010, 2:RRN1193.
62. 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.