Erratum: Single-Cell Profiling of an In Vitro Model of Human Interneuron Development Reveals Temporal Dynamics of Cell Type Production and Maturation (Neuron (2017) (93) (5)(1035–1048.e5) (S0896627317300983) (10.1016/j.neuron.2017.02.014));Single-Cell Profiling of an In Vitro Model of Human Interneuron Development Reveals Temporal Dynamics of Cell Type Production and Maturation

Neuron

Volumn 93, Issue 5, 2017, Pages 1035-1048.e5

  Close, Jennie L ^a   Yao, Zizhen ^a   Levi, Boaz P ^a   Miller, Jeremy A ^a   Bakken, Trygve E ^a   Menon, Vilas ^a   Ting, Jonathan T ^a   Wall, Abigail ^a   Krostag, Anne Rachel ^c   Thomsen, Elliot R ^a   Nelson, Angel M ^b   Mich, John K ^a   Hodge, Rebecca D ^a   Shehata, Soraya I ^a   Glass, Ian A ^d   Bort, Susan ^a   Shapovalova, Nadiya V ^a   Ngo, N Kiet ^a   Grimley, Joshua S ^e   Phillips, John W ^a   Thompson, Carol L ^a   Ramanathan, Sharad ^f   Lein, Ed ^a   more..

^a ALLEN INSTITUTE FOR BRAIN SCIENCE   (United States)

^b Allen Institute for Cell Science   (United States)

^c BLUEBIRD BIO   (United States)

^d UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^e Universal Cells   (United States)

^f HARVARD UNIVERSITY   (United States)

Author keywords

human cortex; interneurons; MGE; single cell RNA seq

Indexed keywords

TRANSCRIPTOME; 4 AMINOBUTYRIC ACID RECEPTOR; NERVE PROTEIN; TRANSCRIPTION FACTOR;

ARTICLE; CELL MATURATION; CONTROLLED STUDY; EMBRYONIC STEM CELL; FETUS; GENE IDENTIFICATION; GLIA CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VITRO STUDY; INTERNEURON; LIMIT OF QUANTITATION; MALE; MENTAL DISEASE; NERVE CELL; RNA SEQUENCE; CELL CULTURE; CELL DIFFERENTIATION; CELL MOTION; CYTOLOGY; GLIA; METABOLISM; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY; SINGLE CELL ANALYSIS;

CELL DIFFERENTIATION; CELL MOVEMENT; CELLS, CULTURED; GABAERGIC NEURONS; HUMANS; INTERNEURONS; NERVE TISSUE PROTEINS; NEUROGENESIS; NEUROGLIA; SINGLE-CELL ANALYSIS; TRANSCRIPTION FACTORS;

EID: 85014804284     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2017.10.024     Document Type: Erratum

References (82)

1. -/- mutants due to a defective anterior neuroectoderm specification during gastrulation. Development 121 (1995), 3279–3290.
2. Akgül, G., McBain, C.J., Diverse roles for ionotropic glutamate receptors on inhibitory interneurons in developing and adult brain. J. Physiol. 594 (2016), 5471–5490.
3. Anderson, S.A., Eisenstat, D.D., Shi, L., Rubenstein, J.L., Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278 (1997), 474–476.
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 19 (1997), 27–37.
5. Anton, E.S., Ghashghaei, H.T., Weber, J.L., McCann, C., Fischer, T.M., Cheung, I.D., Gassmann, M., Messing, A., Klein, R., Schwab, M.H., et al. Receptor tyrosine kinase ErbB4 modulates neuroblast migration and placement in the adult forebrain. Nat. Neurosci. 7 (2004), 1319–1328.
6. Bakken, T.E., Miller, J.A., Ding, S.L., Sunkin, S.M., Smith, K.A., Ng, L., Szafer, A., Dalley, R.A., Royall, J.J., Lemon, T., et al. A comprehensive transcriptional map of primate brain development. Nature 535 (2016), 367–375.
7. Bandler, R.C., Mayer, C., Fishell, G., Cortical interneuron specification: the juncture of genes, time and geometry. Curr. Opin. Neurobiol. 42 (2016), 17–24.
8. Batista-Brito, R., Rossignol, E., Hjerling-Leffler, J., Denaxa, M., Wegner, M., Lefebvre, V., Pachnis, V., Fishell, G., The cell-intrinsic requirement of Sox6 for cortical interneuron development. Neuron 63 (2009), 466–481.
9. Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T.M., Rubenstein, J.L., Ericson, J., Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398 (1999), 622–627.
10. Brown, J.P., Couillard-Després, S., Cooper-Kuhn, C.M., Winkler, J., Aigner, L., Kuhn, H.G., Transient expression of doublecortin during adult neurogenesis. J. Comp. Neurol. 467 (2003), 1–10.
11. Butt, S.J., Fuccillo, M., Nery, S., Noctor, S., Kriegstein, A., Corbin, J.G., Fishell, G., The temporal and spatial origins of cortical interneurons predict their physiological subtype. Neuron 48 (2005), 591–604.
12. Casarosa, S., Fode, C., Guillemot, F., Mash1 regulates neurogenesis in the ventral telencephalon. Development 126 (1999), 525–534.
13. Cellerino, A., Siciliano, R., Domenici, L., Maffei, L., Parvalbumin immunoreactivity: a reliable marker for the effects of monocular deprivation in the rat visual cortex. Neuroscience 51 (1992), 749–753.
14. Chambers, S.M., Fasano, C.A., Papapetrou, E.P., Tomishima, M., Sadelain, M., Studer, L., Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat. Biotechnol. 27 (2009), 275–280.
15. Chow, A., Erisir, A., Farb, C., Nadal, M.S., Ozaita, A., Lau, D., Welker, E., Rudy, B., K(+) channel expression distinguishes subpopulations of parvalbumin- and somatostatin-containing neocortical interneurons. J. Neurosci. 19 (1999), 9332–9345.
16. Close, J., Xu, H., De Marco García, N., Batista-Brito, R., Rossignol, E., Rudy, B., Fishell, G., Satb1 is an activity-modulated transcription factor required for the terminal differentiation and connectivity of medial ganglionic eminence-derived cortical interneurons. J. Neurosci. 32 (2012), 17690–17705.
17. Cobos, I., Long, J.E., Thwin, M.T., Rubenstein, J.L., Cellular patterns of transcription factor expression in developing cortical interneurons. Cereb. Cortex 16:Suppl 1 (2006), i82–i88.
18. Colantuoni, C., Lipska, B.K., Ye, T., Hyde, T.M., Tao, R., Leek, J.T., Colantuoni, E.A., Elkahloun, A.G., Herman, M.M., Weinberger, D.R., Kleinman, J.E., Temporal dynamics and genetic control of transcription in the human prefrontal cortex. Nature 478 (2011), 519–523.
19. Colombo, E., Collombat, P., Colasante, G., Bianchi, M., Long, J., Mansouri, A., Rubenstein, J.L., Broccoli, V., Inactivation of Arx, the murine ortholog of the X-linked lissencephaly with ambiguous genitalia gene, leads to severe disorganization of the ventral telencephalon with impaired neuronal migration and differentiation. J. Neurosci. 27 (2007), 4786–4798.
20. Couillard-Despres, S., Winner, B., Schaubeck, S., Aigner, R., Vroemen, M., Weidner, N., Bogdahn, U., Winkler, J., Kuhn, H.G., Aigner, L., Doublecortin expression levels in adult brain reflect neurogenesis. Eur. J. Neurosci. 21 (2005), 1–14.
21. de Lecea, L., del Rio, J.A., Criado, J.R., Alcántara, S., Morales, M., Danielson, P.E., Henriksen, S.J., Soriano, E., Sutcliffe, J.G., Cortistatin is expressed in a distinct subset of cortical interneurons. J. Neurosci. 17 (1997), 5868–5880.
22. De Marco García, N.V., Karayannis, T., Fishell, G., Neuronal activity is required for the development of specific cortical interneuron subtypes. Nature 472 (2011), 351–355.
23. DeFelipe, J., López-Cruz, P.L., Benavides-Piccione, R., Bielza, C., Larrañaga, P., Anderson, S., Burkhalter, A., Cauli, B., Fairén, A., Feldmeyer, D., et al. New insights into the classification and nomenclature of cortical GABAergic interneurons. Nat. Rev. Neurosci. 14 (2013), 202–216.
24. Deneen, B., Ho, R., Lukaszewicz, A., Hochstim, C.J., Gronostajski, R.M., Anderson, D.J., The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52 (2006), 953–968.
25. Donato, R., Cannon, B.R., Sorci, G., Riuzzi, F., Hsu, K., Weber, D.J., Geczy, C.L., Functions of S100 proteins. Curr. Mol. Med. 13 (2013), 24–57.
26. Dou, C.L., Li, S., Lai, E., Dual role of brain factor-1 in regulating growth and patterning of the cerebral hemispheres. Cereb. Cortex 9 (1999), 543–550.
27. Eberhard, D.A., Brown, M.D., VandenBerg, S.R., Alterations of annexin expression in pathological neuronal and glial reactions. Immunohistochemical localization of annexins I, II (p36 and p11 subunits), IV, and VI in the human hippocampus. Am. J. Pathol. 145 (1994), 640–649.
28. Eisenstat, D.D., Liu, J.K., Mione, M., Zhong, W., Yu, G., Anderson, S.A., Ghattas, I., Puelles, L., Rubenstein, J.L., DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J. Comp. Neurol. 414 (1999), 217–237.
29. Ferri, A., Favaro, R., Beccari, L., Bertolini, J., Mercurio, S., Nieto-Lopez, F., Verzeroli, C., La Regina, F., De Pietri Tonelli, D., Ottolenghi, S., et al. Sox2 is required for embryonic development of the ventral telencephalon through the activation of the ventral determinants Nkx2.1 and Shh. Development 140 (2013), 1250–1261.
30. Filmus, J., Glypicans in growth control and cancer. Glycobiology 11 (2001), 19R–23R.
31. Flames, N., Pla, R., Gelman, D.M., Rubenstein, J.L., Puelles, L., Marín, O., Delineation of multiple subpallial progenitor domains by the combinatorial expression of transcriptional codes. J. Neurosci. 27 (2007), 9682–9695.
32. Flandin, P., Zhao, Y., Vogt, D., Jeong, J., Long, J., Potter, G., Westphal, H., Rubenstein, J.L., Lhx6 and Lhx8 coordinately induce neuronal expression of Shh that controls the generation of interneuron progenitors. Neuron 70 (2011), 939–950.
33. Fragkouli, A., Hearn, C., Errington, M., Cooke, S., Grigoriou, M., Bliss, T., Stylianopoulou, F., Pachnis, V., Loss of forebrain cholinergic neurons and impairment in spatial learning and memory in LHX7-deficient mice. Eur. J. Neurosci. 21 (2005), 2923–2938.
34. Fragkouli, A., van Wijk, N.V., Lopes, R., Kessaris, N., Pachnis, V., LIM homeodomain transcription factor-dependent specification of bipotential MGE progenitors into cholinergic and GABAergic striatal interneurons. Development 136 (2009), 3841–3851.
35. Friocourt, G., Parnavelas, J.G., Identification of Arx targets unveils new candidates for controlling cortical interneuron migration and differentiation. Front. Cell. Neurosci., 5, 2011, 28.
36. Friocourt, G., Liu, J.S., Antypa, M., Rakic, S., Walsh, C.A., Parnavelas, J.G., Both doublecortin and doublecortin-like kinase play a role in cortical interneuron migration. J. Neurosci. 27 (2007), 3875–3883.
37. Gestri, G., Carl, M., Appolloni, I., Wilson, S.W., Barsacchi, G., Andreazzoli, M., Six3 functions in anterior neural plate specification by promoting cell proliferation and inhibiting Bmp4 expression. Development 132 (2005), 2401–2413.
38. Glickstein, S.B., Moore, H., Slowinska, B., Racchumi, J., Suh, M., Chuhma, N., Ross, M.E., Selective cortical interneuron and GABA deficits in cyclin D2-null mice. Development 134 (2007), 4083–4093.
39. Halevi, S., Yassin, L., Eshel, M., Sala, F., Sala, S., Criado, M., Treinin, M., Conservation within the RIC-3 gene family. Effectors of mammalian nicotinic acetylcholine receptor expression. J. Biol. Chem. 278 (2003), 34411–34417.
40. Hammond, V., So, E., Gunnersen, J., Valcanis, H., Kalloniatis, M., Tan, S.S., Layer positioning of late-born cortical interneurons is dependent on Reelin but not p35 signaling. J. Neurosci. 26 (2006), 1646–1655.
41. Hansen, D.V., Lui, J.H., Flandin, P., Yoshikawa, K., Rubenstein, J.L., Alvarez-Buylla, A., Kriegstein, A.R., Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat. Neurosci. 16 (2013), 1576–1587.
42. Hashimoto, T., Maekawa, S., Miyata, S., IgLON cell adhesion molecules regulate synaptogenesis in hippocampal neurons. Cell Biochem. Funct. 27 (2009), 496–498.
43. Kelly, G.M., Moon, R.T., Involvement of wnt1 and pax2 in the formation of the midbrain-hindbrain boundary in the zebrafish gastrula. Dev. Genet. 17 (1995), 129–140.
44. Kessaris, N., Fogarty, M., Iannarelli, P., Grist, M., Wegner, M., Richardson, W.D., Competing waves of oligodendrocytes in the forebrain and postnatal elimination of an embryonic lineage. Nat. Neurosci. 9 (2006), 173–179.
45. Lin, L.C., Sibille, E., Reduced brain somatostatin in mood disorders: a common pathophysiological substrate and drug target?. Front. Pharmacol., 4, 2013, 110.
46. Ma, Y., Hu, H., Berrebi, A.S., Mathers, P.H., Agmon, A., Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26 (2006), 5069–5082.
47. Marín, O., Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13 (2012), 107–120.
48. Marin, O., Anderson, S.A., Rubenstein, J.L., Origin and molecular specification of striatal interneurons. J. Neurosci. 20 (2000), 6063–6076.
49. Maroof, A.M., Keros, S., Tyson, J.A., Ying, S.W., Ganat, Y.M., Merkle, F.T., Liu, B., Goulburn, A., Stanley, E.G., Elefanty, A.G., et al. Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12 (2013), 559–572.
50. Matsuo, I., Kuratani, S., Kimura, C., Takeda, N., Aizawa, S., Mouse Otx2 functions in the formation and patterning of rostral head. Genes Dev. 9 (1995), 2646–2658.
51. McKinsey, G.L., Lindtner, S., Trzcinski, B., Visel, A., Pennacchio, L.A., Huylebroeck, D., Higashi, Y., Rubenstein, J.L., Dlx1&2-dependent expression of Zfhx1b (Sip1, Zeb2) regulates the fate switch between cortical and striatal interneurons. Neuron 77 (2013), 83–98.
52. Minhas, H.M., Pescosolido, M.F., Schwede, M., Piasecka, J., Gaitanis, J., Tantravahi, U., Morrow, E.M., An unbalanced translocation involving loss of 10q26.2 and gain of 11q25 in a pedigree with autism spectrum disorder and cerebellar juvenile pilocytic astrocytoma. Am. J. Med. Genet. A. 161A (2013), 787–791.
53. Monuki, E.S., Porter, F.D., Walsh, C.A., Patterning of the dorsal telencephalon and cerebral cortex by a roof plate-Lhx2 pathway. Neuron 32 (2001), 591–604.
54. Nicholas, C.R., Chen, J., Tang, Y., Southwell, D.G., Chalmers, N., Vogt, D., Arnold, C.M., Chen, Y.J., Stanley, E.G., Elefanty, A.G., et al. Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 12 (2013), 573–586.
55. Nielsen, S., Nagelhus, E.A., Amiry-Moghaddam, M., Bourque, C., Agre, P., Ottersen, O.P., Specialized membrane domains for water transport in glial cells: high-resolution immunogold cytochemistry of aquaporin-4 in rat brain. J. Neurosci. 17 (1997), 171–180.
56. Olincy, A., Stevens, K.E., Treating schizophrenia symptoms with an alpha7 nicotinic agonist, from mice to men. Biochem. Pharmacol. 74 (2007), 1192–1201.
57. Olincy, A., Harris, J.G., Johnson, L.L., Pender, V., Kongs, S., Allensworth, D., Ellis, J., Zerbe, G.O., Leonard, S., Stevens, K.E., et al. Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia. Arch. Gen. Psychiatry 63 (2006), 630–638.
58. Peñagarikano, O., Abrahams, B.S., Herman, E.I., Winden, K.D., Gdalyahu, A., Dong, H., Sonnenblick, L.I., Gruver, R., Almajano, J., Bragin, A., et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell 147 (2011), 235–246.
59. Petros, T.J., Bultje, R.S., Ross, M.E., Fishell, G., Anderson, S.A., Apical versus basal neurogenesis directs cortical interneuron subclass fate. Cell Rep. 13 (2015), 1090–1095.
60. Picelli, S., Faridani, O.R., Björklund, A.K., Winberg, G., Sagasser, S., Sandberg, R., Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc. 9 (2014), 171–181.
61. Pla, R., Borrell, V., Flames, N., Marín, O., Layer acquisition by cortical GABAergic interneurons is independent of Reelin signaling. J. Neurosci. 26 (2006), 6924–6934.
62. Pollen, A.A., Nowakowski, T.J., Chen, J., Retallack, H., Sandoval-Espinosa, C., Nicholas, C.R., Shuga, J., Liu, S.J., Oldham, M.C., Diaz, A., et al. Molecular identity of human outer radial glia during cortical development. Cell 163 (2015), 55–67.
63. Ritchie, M.E., Phipson, B., Wu, D., Hu, Y., Law, C.W., Shi, W., Smyth, G.K., limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res., 43, 2015, e47.
64. Sadegh, C., Macklis, J.D., Established monolayer differentiation of mouse embryonic stem cells generates heterogeneous neocortical-like neurons stalled at a stage equivalent to midcorticogenesis. J. Comp. Neurol. 522 (2014), 2691–2706.
65. Sanz, R., Ferraro, G.B., Fournier, A.E., IgLON cell adhesion molecules are shed from the cell surface of cortical neurons to promote neuronal growth. J. Biol. Chem. 290 (2015), 4330–4342.
66. Schlüter, O.M., Basu, J., Südhof, T.C., Rosenmund, C., Rab3 superprimes synaptic vesicles for release: implications for short-term synaptic plasticity. J. Neurosci. 26 (2006), 1239–1246.
67. Scholzen, T., Gerdes, J., The Ki-67 protein: from the known and the unknown. J. Cell. Physiol. 182 (2000), 311–322.
68. Shu, T., Butz, K.G., Plachez, C., Gronostajski, R.M., Richards, L.J., Abnormal development of forebrain midline glia and commissural projections in Nfia knock-out mice. J. Neurosci. 23 (2003), 203–212.
69. Southwell, D.G., Paredes, M.F., Galvao, R.P., Jones, D.L., Froemke, R.C., Sebe, J.Y., Alfaro-Cervello, C., Tang, Y., Garcia-Verdugo, J.M., Rubenstein, J.L., et al. Intrinsically determined cell death of developing cortical interneurons. Nature 491 (2012), 109–113.
70. Southwell, D.G., Nicholas, C.R., Basbaum, A.I., Stryker, M.P., Kriegstein, A.R., Rubenstein, J.L., Alvarez-Buylla, A., Interneurons from embryonic development to cell-based therapy. Science, 344, 2014, 1240622.
71. Tasic, B., Menon, V., Nguyen, T.N., Kim, T.K., Jarsky, T., Yao, Z., Levi, B., Gray, L.T., Sorensen, S.A., Dolbeare, T., et al. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19 (2016), 335–346.
72. Thomsen, E.R., Mich, J.K., Yao, Z., Hodge, R.D., Doyle, A.M., Jang, S., Shehata, S.I., Nelson, A.M., Shapovalova, N.V., Levi, B.P., Ramanathan, S., Fixed single-cell transcriptomic characterization of human radial glial diversity. Nat. Methods 13 (2016), 87–93.
73. Tremblay, R., Lee, S., Rudy, B., GABAergic interneurons in the neocortex: from cellular properties to circuits. Neuron 91 (2016), 260–292.
74. Vogt, D., Hunt, R.F., Mandal, S., Sandberg, M., Silberberg, S.N., Nagasawa, T., Yang, Z., Baraban, S.C., Rubenstein, J.L., Lhx6 directly regulates Arx and CXCR7 to determine cortical interneuron fate and laminar position. Neuron 82 (2014), 350–364.
75. Wang, Y., Li, G., Stanco, A., Long, J.E., Crawford, D., Potter, G.B., Pleasure, S.J., Behrens, T., Rubenstein, J.L., CXCR4 and CXCR7 have distinct functions in regulating interneuron migration. Neuron 69 (2011), 61–76.
76. Williams, M.E., Burton, B., Urrutia, A., Shcherbatko, A., Chavez-Noriega, L.E., Cohen, C.J., Aiyar, J., Ric-3 promotes functional expression of the nicotinic acetylcholine receptor alpha7 subunit in mammalian cells. J. Biol. Chem. 280 (2005), 1257–1263.
77. Xu, Q., Cobos, I., De La Cruz, E., Rubenstein, J.L., Anderson, S.A., Origins of cortical interneuron subtypes. J. Neurosci. 24 (2004), 2612–2622.
78. Xu, Q., Guo, L., Moore, H., Waclaw, R.R., Campbell, K., Anderson, S.A., Sonic hedgehog signaling confers ventral telencephalic progenitors with distinct cortical interneuron fates. Neuron 65 (2010), 328–340.
79. Yamada, M., Hashimoto, T., Hayashi, N., Higuchi, M., Murakami, A., Nakashima, T., Maekawa, S., Miyata, S., Synaptic adhesion molecule OBCAM; synaptogenesis and dynamic internalization. Brain Res. 1165 (2007), 5–14.
80. Yao, Z., Mich, J.K., Ku, S., Menon, V., Krostag, A.-R., Martinez, R.A., Furchtgott, L., Mulholland, H., Bort, S., Fuqua, M.A., et al. A single-cell roadmap of lineage bifurcation in human ESC models of embryonic brain development. Cell Stem Cell 20 (2017), 120–134.
81. Zeisel, A., Muñoz-Manchado, A.B., Codeluppi, S., Lönnerberg, P., La Manno, G., Juréus, A., Marques, S., Munguba, H., He, L., Betsholtz, C., et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347 (2015), 1138–1142.
82. Zhang, W., Zhang, L., Liang, B., Schroeder, D., Zhang, Z.W., Cox, G.A., Li, Y., Lin, D.T., Hyperactive somatostatin interneurons contribute to excitotoxicity in neurodegenerative disorders. Nat. Neurosci. 19 (2016), 557–559.