Programming and reprogramming neuronal subtypes in the central nervous system

Developmental Neurobiology

Volumn 72, Issue 7, 2012, Pages 1085-1098

  Rouaux, Caroline ^a   Bhai, Salman ^a   Arlotta, Paola ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

Cellular replacement; Corticospinal motor neurons; Directed differentiation; Reprogramming

Indexed keywords

KRUPPEL LIKE FACTOR 4; MYC PROTEIN; NEUROGENIN 3; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR MAFA; TRANSCRIPTION FACTOR PDX 1; TRANSCRIPTION FACTOR SOX2;

ADULT STEM CELL; ADULTHOOD; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL FATE; CELL FUNCTION; CELL NUCLEUS; CELL TRANSFORMATION; CENTRAL NERVOUS SYSTEM; DENTATE GYRUS; EMBRYO DEVELOPMENT; EPIGENETICS; HUMAN; MITOSIS; NERVE CELL DIFFERENTIATION; NERVOUS TISSUE; NEURAL STEM CELL; NONHUMAN; NUCLEAR REPROGRAMMING; OLIGODENDROGLIA; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; SUBGRANULAR ZONE; SUBVENTRICULAR ZONE;

ADULT STEM CELLS; ANIMALS; CELL DIFFERENTIATION; NEURAL STEM CELLS; NEURONS; NUCLEAR REPROGRAMMING;

EID: 84862123720     PISSN: 19328451     EISSN: 10974695     Source Type: Journal    
DOI: 10.1002/dneu.22018     Document Type: Article

References (105)

1. Alcamo EA, Chirivella L, Dautzenberg M, Dobreva G, Farinas I, Grosschedl R, McConnell SK. 2008. Satb2 regulates callosal projection neuron identity in the developing cerebral cortex. Neuron 57: 364-377.
2. Alvarez-Buylla A, Lim DA. 2004. For the long run: Maintaining germinal niches in the adult brain. Neuron 41: 683-686.
3. Andersson E, Tryggvason U, Deng Q, Friling S, Alekseenko Z, Robert B, Perlmann T, et al. 2006. Identification of intrinsic determinants of midbrain dopamine neurons. Cell 124: 393-405.
4. Ang SL. 2009. Foxa1 and Foxa2 transcription factors regulate differentiation of midbrain dopaminergic neurons. Adv Exp Med Biol 651: 58-65.
5. Arlotta P, Molyneaux BJ, Chen J, Inoue J, Kominami R, Macklis JD. 2005. Neuronal subtype-specific genes that control corticospinal motor neuron development in vivo. Neuron 45: 207-221.
6. Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. 2002. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8: 963-970.
7. Bayer SA, Altman J, Russo RJ, Dai XF, Simmons JA. 1991. Cell migration in the rat embryonic neocortex. J Comp Neurol 307: 499-516.
8. Belgard TG, Marques AC, Oliver PL, Abaan HO, Sirey TM, Hoerder-Suabedissen A, Garcia-Moreno F, et al. 2011. A transcriptomic atlas of mouse neocortical layers. Neuron 71: 605-616.
9. Berninger B, Costa MR, Koch U, Schroeder T, Sutor B, Grothe B, Gotz M. 2007. Functional properties of neurons derived from in vitro reprogrammed postnatal astroglia. J Neurosci 27: 8654-8664.
10. Bernstein BE, Meissner A, Lander ES. 2007. The mammalian epigenome. Cell 128: 669-681.
11. Bogdanove AJ, Voytas DF. 2011. TAL effectors: Customizable proteins for DNA targeting. Science 333: 1843-1846.
12. Brennand KJ, Simone A, Jou J, Gelboin-Burkhart C, Tran N, Sangar S, Li Y, et al. 2011. Modelling schizophrenia using human induced pluripotent stem cells. Nature 473: 221-225.
13. Briggs R, King TJ. 1952. Transplantation of living nuclei from blastula cells into enucleated frogs' eggs. Proc Natl Acad Sci USA 38: 455-463.
14. Britanova O, de Juan Romero C, Cheung A, Kwan KY, Schwark M, Gyorgy A, Vogel T, et al. 2008. Satb2 is a postmitotic determinant for upper-layer neuron specification in the neocortex. Neuron 57: 378-392.
15. Buffo A, Vosko MR, Erturk D, Hamann GF, Jucker M, Rowitch D, Gotz M. 2005. Expression pattern of the transcription factor Olig2 in response to brain injuries: Implications for neuronal repair. Proc Natl Acad Sci USA 102: 18183-18188.
16. Caiazzo M, Dell'Anno MT, Dvoretskova E, Lazarevic D, Taverna S, Leo D, Sotnikova TD, et al. 2011. Direct generation of functional dopaminergic neurons from mouse and human fibroblasts. Nature 476: 224-227.
17. Canty AJ, Murphy M. 2008. Molecular mechanisms of axon guidance in the developing corticospinal tract. Prog Neurobiol 85: 214-235.
18. Chen B, Schaevitz LR, McConnell SK. 2005a. Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci USA 102: 17184-17189.
19. Chen B, Wang SS, Hattox AM, Rayburn H, Nelson SB, McConnell SK. 2008. The Fezf2-Ctip2 genetic pathway regulates the fate choice of subcortical projection neurons in the developing cerebral cortex. Proc Natl Acad Sci USA 105: 11382-11387.
20. Chen J, Magavi SS, Macklis JD. 2004. Neurogenesis of corticospinal motor neurons extending spinal projections in adult mice. Proc Natl Acad Sci USA 101: 16357-16362.
21. Chen JG, Rasin MR, Kwan KY, Sestan N. 2005b. Zfp312 is required for subcortical axonal projections and dendritic morphology of deep-layer pyramidal neurons of the cerebral cortex. Proc Natl Acad Sci USA 102: 17792-17797.
22. Chiang CH, Su Y, Wen Z, Yoritomo N, Ross CA, Margolis RL, Song H, et al. 2011. Integration-free induced pluripotent stem cells derived from schizophrenia patients with a DISC1 mutation. Mol Psychiatry 16: 358-360.
23. Choi J, Costa ML, Mermelstein CS, Chagas C, Holtzer S, Holtzer H. 1990. MyoD converts primary dermal fibroblasts, chondroblasts, smooth muscle, and retinal pigmented epithelial cells into striated mononucleated myoblasts and multinucleated myotubes. Proc Natl Acad Sci USA 87: 7988-7992.
24. Cowan CA, Atienza J, Melton DA, Eggan K. 2005. Nuclear reprogramming of somatic cells after fusion with human embryonic stem cells. Science 309: 1369-1373.
25. Dasen JS, Jessell TM. 2009. Hox networks and the origins of motor neuron diversity. Curr Top Dev Biol 88: 169-200.
26. Davis RL, Weintraub H, Lassar AB. 1987. Expression of a single transfected cDNA converts fibroblasts to myoblasts. Cell 51: 987-1000.
27. Di Giorgio FP, Boulting GL, Bobrowicz S, Eggan KC. 2008. Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying an ALS-causing mutation. Cell Stem Cell 3: 637-648.
28. Di Giorgio FP, Carrasco MA, Siao MC, Maniatis T, Eggan K. 2007. Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat Neurosci 10: 608-614.
29. Dimos JT, Rodolfa KT, Niakan KK, Weisenthal LM, Mitsumoto H, Chung W, Croft GF, et al. 2008. Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321: 1218-1221.
30. Ebert AD, Yu J, Rose FFJr, Mattis VB, Lorson CL, Thomson JA, Svendsen CN. 2009. Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457: 277-280.
31. Efe JA, Hilcove S, Kim J, Zhou H, Ouyang K, Wang G, Chen J, et al. 2011. Conversion of mouse fibroblasts into cardiomyocytes using a direct reprogramming strategy. Nat Cell Biol 13: 215-222.
32. Eggan K, Baldwin K, Tackett M, Osborne J, Gogos J, Chess A, Axel R, et al. 2004. Mice cloned from olfactory sensory neurons. Nature 428: 44-49.
33. Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S, Matsumura M, Wataya T, et al. 2008. Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3: 519-532.
34. Fame RM, MacDonald JL, Macklis JD. 2011. Development, specification, and diversity of callosal projection neurons. Trends Neurosci 34: 41-50.
35. Feng R, Desbordes SC, Xie H, Tillo ES, Pixley F, Stanley ER, Graf T. 2008. PU.1 and C/EBPalpha/beta convert fibroblasts into macrophage-like cells. Proc Natl Acad Sci USA 105: 6057-6062.
36. Gage FH. 2000. Mammalian neural stem cells. Science 287: 1433-1438.
37. Gaspard N, Bouschet T, Hourez R, Dimidschstein J, Naeije G, van den Ameele J, Espuny-Camacho I, et al. 2008. An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455: 351-357.
38. Gurdon JB. 1962. The developmental capacity of nuclei taken from intestinal epithelium cells of feeding tadpoles. J Embryol Exp Morphol 10: 622-640.
39. Gurdon JB, Laskey RA, Reeves OR. 1975. The developmental capacity of nuclei transplanted from keratinized skin cells of adult frogs. J Embryol Exp Morphol 34: 93-112.
40. Han W, Kwan KY, Shim S, Lam MM, Shin Y, Xu X, Zhu Y, et al. 2011. TBR1 directly represses Fezf2 to control the laminar origin and development of the corticospinal tract. Proc Natl Acad Sci USA 108: 3041-3046.
41. Heinrich C, Blum R, Gascon S, Masserdotti G, Tripathi P, Sanchez R, Tiedt S, et al. 2010. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol 8: e1000373.
42. Heins N, Malatesta P, Cecconi F, Nakafuku M, Tucker KL, Hack MA, Chapouton P, et al. 2002. Glial cells generate neurons: The role of the transcription factor Pax6. Nat Neurosci 5: 308-315.
43. Hevner RF, Shi L, Justice N, Hsueh Y, Sheng M, Smiga S, Bulfone A, et al. 2001. Tbr1 regulates differentiation of the preplate and layer 6. Neuron 29: 353-366.
44. Hochedlinger K, Jaenisch R. 2002. Monoclonal mice generated by nuclear transfer from mature B and T donor cells. Nature 415: 1035-1038.
45. Huang P, He Z, Ji S, Sun H, Xiang D, Liu C, Hu Y, et al. 2011. Induction of functional hepatocyte-like cells from mouse fibroblasts by defined factors. Nature 475: 386-389.
46. Ieda M, Fu JD, Delgado-Olguin P, Vedantham V, Hayashi Y, Bruneau BG, Srivastava D. 2010. Direct reprogramming of fibroblasts into functional cardiomyocytes by defined factors. Cell 142: 375-386.
47. Izumikawa M, Minoda R, Kawamoto K, Abrashkin KA, Swiderski DL, Dolan DF, Brough DE, et al. 2005. Auditory hair cell replacement and hearing improvement by Atoh1 gene therapy in deaf mammals. Nat Med 11: 271-276.
48. Jackson EL, Garcia-Verdugo JM, Gil-Perotin S, Roy M, Quinones-Hinojosa A, VandenBerg S, Alvarez-Buylla A. 2006. PDGFR alpha-positive B cells are neural stem cells in the adult SVZ that form glioma-like growths in response to increased PDGF signaling. Neuron 51: 187-199.
49. Jessberger S, Toni N, Clemenson GDJr, Ray J, Gage FH. 2008. Directed differentiation of hippocampal stem/progenitor cells in the adult brain. Nat Neurosci 11: 888-893.
50. Joshi PS, Molyneaux BJ, Feng L, Xie X, Macklis JD, Gan L. 2008. Bhlhb5 regulates the postmitotic acquisition of area identities in layers II-V of the developing neocortex. Neuron 60: 258-272.
51. Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y. 2003. Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 23: 4395-4400.
52. Kim J, Lengner CJ, Kirak O, Hanna J, Cassady JP, Lodato MA, Wu S, et al. 2011a. Reprogramming of postnatal neurons into induced pluripotent stem cells by defined factors. Stem Cells 29: 992-1000.
53. Kim J, Su SC, Wang H, Cheng AW, Cassady JP, Lodato MA, Lengner CJ, et al. 2011b. Functional integration of dopaminergic neurons directly converted from mouse fibroblasts. Cell Stem Cell 9: 413-419.
54. King TJ, Briggs R. 1955. Changes in the nuclei of differentiating gastrula cells, as demonstrated by nuclear transplantation. Proc Natl Acad Sci USA 41: 321-325.
55. Klug A. 2010. The discovery of zinc fingers and their applications in gene regulation and genome manipulation. Annu Rev Biochem 79: 213-231.
56. Kohyama J, Kojima T, Takatsuka E, Yamashita T, Namiki J, Hsieh J, Gage FH, et al. 2008. Epigenetic regulation of neural cell differentiation plasticity in the adult mammalian brain. Proc Natl Acad Sci USA 105: 18012-18017.
57. Kondo T, Raff M. 2000. Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289: 1754-1757.
58. Kwan KY, Lam MM, Krsnik Z, Kawasawa YI, Lefebvre V, Sestan N. 2008. SOX5 postmitotically regulates migration, postmigratory differentiation, and projections of subplate and deep-layer neocortical neurons. Proc Natl Acad Sci USA 105: 16021-16026.
59. Lai T, Jabaudon D, Molyneaux BJ, Azim E, Arlotta P, Menezes JR, Macklis JD. 2008. SOX5 controls the sequential generation of distinct corticofugal neuron subtypes. Neuron 57: 232-247.
60. Leone DP, Srinivasan K, Chen B, Alcamo E, McConnell SK. 2008. The determination of projection neuron identity in the developing cerebral cortex. Curr Opin Neurobiol 18: 28-35.
61. Li J, Ishii T, Feinstein P, Mombaerts P. 2004. Odorant receptor gene choice is reset by nuclear transfer from mouse olfactory sensory neurons. Nature 428: 393-399.
62. Lindwall C, Fothergill T, Richards LJ. 2007. Commissure formation in the mammalian forebrain. Curr Opin Neurobiol 17: 3-14.
63. Lodato S, Rouaux C, Quast KB, Jantrachotechatchawan C, Studer M, Hensch TK, Arlotta P. 2011. Excitatory projection neuron subtypes control the distribution of local inhibitory interneurons in the cerebral cortex. Neuron 69: 763-779.
64. Magavi SS, Leavitt BR, Macklis JD. 2000. Induction of neurogenesis in the neocortex of adult mice. Nature 405: 951-955.
65. Marchetto MC, Brennand KJ, Boyer LF, Gage FH. 2011. Induced pluripotent stem cells (iPSCs) and neurological disease modeling: Progress and promises. Hum Mol Genet 20: R109-115.
66. Maroof AM, Brown K, Shi SH, Studer L, Anderson SA. 2010. Prospective isolation of cortical interneuron precursors from mouse embryonic stem cells. J Neurosci 30: 4667-4675.
67. Mattar P, Langevin LM, Markham K, Klenin N, Shivji S, Zinyk D, Schuurmans C. 2008. Basic helix-loop-helix transcription factors cooperate to specify a cortical projection neuron identity. Mol Cell Biol 28: 1456-1469.
68. McKenna WL, Betancourt J, Larkin KA, Abrams B, Guo C, Rubenstein JL, Chen B. 2011. Tbr1 and Fezf2 regulate alternate corticofugal neuronal identities during neocortical development. J Neurosci 31: 549-564.
69. Mitchell BD, Macklis JD. 2005. Large-scale maintenance of dual projections by callosal and frontal cortical projection neurons in adult mice. J Comp Neurol 482: 17-32.
70. Mitne-Neto M, Machado-Costa M, Marchetto MC, Bengtson MH, Joazeiro CA, Tsuda H, Bellen HJ, et al. 2011. Downregulation of VAPB expression in motor neurons derived from induced pluripotent stem cells of ALS8 patients. Hum Mol Genet 20: 3642-3652.
71. Molyneaux BJ, Arlotta P, Fame RM, MacDonald JL, MacQuarrie KL, Macklis JD. 2009. Novel subtype-specific genes identify distinct subpopulations of callosal projection neurons. J Neurosci 29: 12343-12354.
72. Molyneaux BJ, Arlotta P, Hirata T, Hibi M, Macklis JD. 2005. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47: 817-831.
73. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8: 427-437.
74. Nagai M, Re DB, Nagata T, Chalazonitis A, Jessell TM, Wichterle H, Przedborski S. 2007. Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat Neurosci 10: 615-622.
75. Nefzger CM, Haynes JM, Pouton CW. 2011. Directed expression of Gata2, Mash1, and Foxa2 synergize to induce the serotonergic neuron phenotype during in vitro differentiation of embryonic stem cells. Stem Cells 29: 928-939.
76. Pang ZP, Yang N, Vierbuchen T, Ostermeier A, Fuentes DR, Yang TQ, Citri A, et al. 2011. Induction of human neuronal cells by defined transcription factors. Nature 476: 220-223.
77. Park IH, Arora N, Huo H, Maherali N, Ahfeldt T, Shimamura A, Lensch MW, et al. 2008. Disease-specific induced pluripotent stem cells. Cell 134: 877-886.
78. Peljto M, Dasen JS, Mazzoni EO, Jessell TM, Wichterle H. 2010. Functional diversity of ESC-derived motor neuron subtypes revealed through intraspinal transplantation. Cell Stem Cell 7: 355-366.
79. Pfisterer U, Kirkeby A, Torper O, Wood J, Nelander J, Dufour A, Bjorklund A, et al. 2011. Direct conversion of human fibroblasts to dopaminergic neurons. Proc Natl Acad Sci USA 108: 10343-10348.
80. Richards LJ, Plachez C, Ren T. 2004. Mechanisms regulating the development of the corpus callosum and its agenesis in mouse and human. Clin Genet 66: 276-289.
81. Rouaux C, Arlotta P. 2010. Fezf2 directs the differentiation of corticofugal neurons from striatal progenitors in vivo. Nat Neurosci 13: 1345-1347.
82. Salero E, Hatten ME. 2007. Differentiation of ES cells into cerebellar neurons. Proc Natl Acad Sci USA 104: 2997-3002.
83. Sekiya S, Suzuki A. 2011. Direct conversion of mouse fibroblasts to hepatocyte-like cells by defined factors. Nature 475: 390-393.
84. Selvaraj V, Plane JM, Williams AJ, Deng W. 2010. Switching cell fate: The remarkable rise of induced pluripotent stem cells and lineage reprogramming technologies. Trends Biotechnol 28: 214-223.
85. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, et al. 2006. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9: 743-751.
86. Shou J, Zheng JL, Gao WQ. 2003. Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol Cell Neurosci 23: 169-179.
87. Soldner F, Hockemeyer D, Beard C, Gao Q, Bell GW, Cook EG, Hargus G, et al. 2009. Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136: 964-977.
88. Son EY, Ichida JK, Wainger BJ, Toma JS, Rafuse VF, Woolf CJ, Eggan K. 2011. Conversion of mouse and human fibroblasts into functional spinal motor neurons. Cell Stem Cell 9: 205-218.
89. Szabo E, Rampalli S, Risueno RM, Schnerch A, Mitchell R, Fiebig-Comyn A, Levadoux-Martin M, et al. 2010. Direct conversion of human fibroblasts to multilineage blood progenitors. Nature 468: 521-526.
90. Tada M, Takahama Y, Abe K, Nakatsuji N, Tada T. 2001. Nuclear reprogramming of somatic cells by in vitro hybridization with ES cells. Curr Biol 11: 1553-1558.
91. Takahashi K, Yamanaka S. 2006. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663-676.
92. Thored P, Arvidsson A, Cacci E, Ahlenius H, Kallur T, Darsalia V, Ekdahl CT, et al. 2006. Persistent production of neurons from adult brain stem cells during recovery after stroke. Stem Cells 24: 739-747.
93. Tursun B, Patel T, Kratsios P, Hobert O. 2011. Direct conversion of C. elegans germ cells into specific neuron types. Science 21;331: 304-308.
94. Vierbuchen T, Ostermeier A, Pang ZP, Kokubu Y, Sudhof TC, Wernig M. 2010. Direct conversion of fibroblasts to functional neurons by defined factors. Nature 463: 1035-1041.
95. Vierbuchen T, Wernig M. 2011. Direct lineage conversions: Unnatural but useful? Nat Biotechnol 29: 892-907.
96. Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, Kawasaki H, Watanabe Y, et al. 2005. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8: 288-296.
97. Weintraub H, Tapscott SJ, Davis RL, Thayer MJ, Adam MA, Lassar AB, Miller AD. 1989. Activation of muscle-specific genes in pigment, nerve, fat, liver, and fibroblast cell lines by forced expression of MyoD. Proc Natl Acad Sci USA 86: 5434-5438.
98. Wichterle H, Lieberam I, Porter JA, Jessell TM. 2002. Directed differentiation of embryonic stem cells into motor neurons. Cell 110: 385-397.
99. Wichterle H, Turnbull DH, Nery S, Fishell G, Alvarez-Buylla A. 2001. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128: 3759-3771.
100. Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH. 1997. Viable offspring derived from fetal and adult mammalian cells. Nature 385: 810-813.
101. Xie H, Ye M, Feng R, Graf T. 2004. Stepwise reprogramming of B cells into macrophages. Cell 117: 663-676.
102. Yoo AS, Sun AX, Li L, Shcheglovitov A, Portmann T, Li Y, Lee-Messer C, et al. 2011. MicroRNA-mediated conversion of human fibroblasts to neurons. Nature 476: 228-231.
103. Zheng JL, Gao WQ. 2000. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3: 580-586.
104. Zhou Q, Brown J, Kanarek A, Rajagopal J, Melton DA. 2008. In vivo reprogramming of adult pancreatic exocrine cells to beta-cells. Nature 455: 627-632.
105. Zhou Q, Melton DA. 2008. Extreme makeover: Converting one cell into another. Cell Stem Cell 3: 382-388.