1932

Abstract

The noncoding portion of the genome, including microRNAs, has been fertile evolutionary soil for cortical development in primates. A major contribution to cortical expansion in primates is the generation of novel precursor cell populations. Because miRNA expression profiles track closely with cell identity, it is likely that numerous novel microRNAs have contributed to cellular diversity in the brain. The tools to determine the genomic context within which novel microRNAs emerge and how they become integrated into molecular circuitry are now in hand.

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2018-07-08
2024-06-21
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Literature Cited

  1. Alberti C, Manzenreither RA, Sowemimo I, Burkard TR, Wang J et al. 2018. Cell-type specific sequencing of microRNAs from complex animal tissues. Nat. Methods 15:283–89
    [Google Scholar]
  2. Ameres SL, Horwich MD, Hung JH, Xu J, Ghildiyal M et al. 2010. Target RNA-directed trimming and tailing of small silencing RNAs. Science 328:1534–39
    [Google Scholar]
  3. Ameres SL, Zamore PD 2013. Diversifying microRNA sequence and function. Nat. Rev. Mol. Cell Biol. 14:475–88
    [Google Scholar]
  4. Arcila ML, Betizeau M, Cambronne XA, Guzman E, Doerflinger N et al. 2014. Novel primate miRNAs coevolved with ancient target genes in germinal zone-specific expression patterns. Neuron 81:1255–62
    [Google Scholar]
  5. Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C et al. 2016. The origin and evolution of cell types. Nat. Rev. Genet. 17:744–57
    [Google Scholar]
  6. Banerjee S, Neveu P, Kosik KS 2009. A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation. Neuron 64:871–84
    [Google Scholar]
  7. Barrett LF, Simmons WK 2015. Interoceptive predictions in the brain. Nat. Rev. Neurosci. 16:419–29
    [Google Scholar]
  8. Becker KA, Ghule PN, Therrien JA, Lian JB, Stein JL et al. 2006. Self-renewal of human embryonic stem cells is supported by a shortened G1 cell cycle phase. J. Cell. Physiol. 209:883–93
    [Google Scholar]
  9. Berezikov E 2011. Evolution of microRNA diversity and regulation in animals. Nat. Rev. Genet. 12:846–60
    [Google Scholar]
  10. Berezikov E, Thuemmler F, Van Laake LW, Kondova I, Bontrop R et al. 2006. Diversity of microRNAs in human and chimpanzee brain. Nat. Genet. 38:1375–77
    [Google Scholar]
  11. Bernstein E, Caudy AA, Hammond SM, Hannon GJ 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363–66
    [Google Scholar]
  12. Betizeau M, Cortay V, Patti D, Pfister S, Gautier E et al. 2013. Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80:442–57
    [Google Scholar]
  13. Bian S, Hong J, Li Q, Schebelle L, Pollock A et al. 2013. MicroRNA cluster miR-17-92 regulates neural stem cell expansion and transition to intermediate progenitors in the developing mouse neocortex. Cell Rep 3:1398–406
    [Google Scholar]
  14. Bianchi S, Stimpson CD, Bauernfeind AL, Schapiro SJ, Baze WB et al. 2013. Dendritic morphology of pyramidal neurons in the chimpanzee neocortex: regional specializations and comparison to humans. Cereb. Cortex 23:2429–36
    [Google Scholar]
  15. Boward B, Wu T, Dalton S 2016. Concise review: control of cell fate through cell cycle and pluripotency networks. Stem Cells 34:1427–36
    [Google Scholar]
  16. Braun JE, Huntzinger E, Izaurralde E 2013. The role of GW182 proteins in miRNA-mediated gene silencing. Adv. Exp. Med. Biol. 768:147
    [Google Scholar]
  17. Camp JG, Badsha F, Florio M, Kanton S, Gerber T et al. 2015. Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. PNAS 112:15672–77
    [Google Scholar]
  18. Chai H, Diaz-Castro B, Shigetomi E, Monte E, Octeau JC et al. 2017. Neural circuit-specialized astrocytes: transcriptomic, proteomic, morphological, and functional evidence. Neuron 95:531–49
    [Google Scholar]
  19. Christodoulou F, Raible F, Tomer R, Simakov O, Trachana K et al. 2010. Ancient animal microRNAs and the evolution of tissue identity. Nature 463:1084–88
    [Google Scholar]
  20. Clovis YM, Enard W, Marinaro F, Huttner WB, De Pietri Tonelli D 2012. Convergent repression of Foxp2 3′UTR by miR-9 and miR-132 in embryonic mouse neocortex: implications for radial migration of neurons. Development 139:3332–42
    [Google Scholar]
  21. Dajas-Bailador F, Bonev B, Garcez P, Stanley P, Guillemot F, Papalopulu N 2012. microRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nat. Neurosci. 15:697–99
    [Google Scholar]
  22. Darmanis S, Sloan SA, Zhang Y, Enge M, Caneda C et al. 2015. A survey of human brain transcriptome diversity at the single cell level. PNAS 112:7285–90
    [Google Scholar]
  23. Davis TH, Cuellar TL, Koch SM, Barker AJ, Harfe BD et al. 2008. Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28:4322–30
    [Google Scholar]
  24. de la Torre-Ubieta L, Stein JL, Won H, Opland CK, Liang D et al. 2018. The dynamic landscape of open chromatin during human cortical neurogenesis. Cell 172:289–304.e18
    [Google Scholar]
  25. De Pietri Tonelli D, Pulvers JN, Haffner C, Murchison EP, Hannon GJ, Huttner WB 2008. miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development 135:3911–21
    [Google Scholar]
  26. Dehay C, Kennedy H 2007. Cell-cycle control and cortical development. Nat. Rev. Neurosci. 8:438–50
    [Google Scholar]
  27. Dehay C, Kennedy H, Kosik KS 2015. The outer subventricular zone and primate-specific cortical complexification. Neuron 85:683–94
    [Google Scholar]
  28. Delalle I, Takahashi T, Nowakowski RS, Tsai LH, Caviness VS Jr 1999. Cyclin E-p27 opposition and regulation of the G1 phase of the cell cycle in the murine neocortical PVE: a quantitative analysis of mRNA in situ hybridization. Cereb. Cortex 9:824–32
    [Google Scholar]
  29. Elkayam E, Kuhn CD, Tocilj A, Haase AD, Greene EM et al. 2012. The structure of human argonaute-2 in complex with miR-20a. Cell 150:100–10
    [Google Scholar]
  30. Elston GN 2003. Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb. Cortex 13:1124–38
    [Google Scholar]
  31. Fabian MR, Sonenberg N 2012. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 19:586–93
    [Google Scholar]
  32. Fededa JP, Esk C, Mierzwa B, Stanyte R, Yuan S et al. 2016. MicroRNA-34/449 controls mitotic spindle orientation during mammalian cortex development. EMBO J 35:2386–98
    [Google Scholar]
  33. Fietz SA, Huttner WB 2011. Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective. Curr. Opin. Neurobiol. 21:23–35
    [Google Scholar]
  34. Fietz SA, Kelava I, Vogt J, Wilsch-Bräuninger M, Stenzel D et al. 2010. OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat. Neurosci. 13:690–99
    [Google Scholar]
  35. Fineberg SK, Datta P, Stein CS, Davidson BL 2012. MiR-34a represses Numbl in murine neural progenitor cells and antagonizes neuronal differentiation. PLOS ONE 7:e38562
    [Google Scholar]
  36. Fish JL, Dehay C, Kennedy H, Huttner WB 2008. Making bigger brains—the evolution of neural-progenitor-cell division. J. Cell Sci. 121:2783–93
    [Google Scholar]
  37. Franzoni E, Booker SA, Parthasarathy S, Rehfeld F, Grosser S et al. 2015. miR-128 regulates neuronal migration, outgrowth and intrinsic excitability via the intellectual disability gene Phf6. eLife 4:e04263
    [Google Scholar]
  38. Friedlander MR, Chen W, Adamidi C, Maaskola J, Einspanier R et al. 2008. Discovering microRNAs from deep sequencing data using miRDeep. Nat. Biotechnol. 26:407–15
    [Google Scholar]
  39. Friedman RC, Farh KK, Burge CB, Bartel DP 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 19:92–105
    [Google Scholar]
  40. García-Moreno F, Vasistha NA, Trevia N, Bourne JA, Molnár Z 2012. Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. Cereb. Cortex 22:482–92
    [Google Scholar]
  41. Ghosh T, Aprea J, Nardelli J, Engel H, Selinger C et al. 2014. MicroRNAs establish robustness and adaptability of a critical gene network to regulate progenitor fate decisions during cortical neurogenesis. Cell Rep 7:1779–88
    [Google Scholar]
  42. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP 2007. MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol. Cell 27:91–105
    [Google Scholar]
  43. Hansen DV, Lui JH, Parker PR, Kriegstein AR 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554–61
    [Google Scholar]
  44. Hébert SS, Horré K, Nicolaï L, Papadopoulou AS, Mandemakers W et al. 2008. Loss of microRNA cluster miR-29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/β-secretase expression. PNAS 105:6415–20
    [Google Scholar]
  45. Herculano-Houzel S, Catania K, Manger PR, Kaas JH 2015. Mammalian brains are made of these: a dataset of the numbers and densities of neuronal and nonneuronal cells in the brain of glires, primates, Scandentia, eulipotyphlans, afrotherians and artiodactyls, and their relationship with body mass. Brain Behav. Evol. 86:145–63
    [Google Scholar]
  46. Hill RS, Walsh CA 2005. Molecular insights into human brain evolution. Nature 437:64–67
    [Google Scholar]
  47. Hofman MA 1989. On the evolution and geometry of the brain in mammals. Prog. Neurobiol. 32:137–58
    [Google Scholar]
  48. Hornstein E, Shomron N 2006. Canalization of development by microRNAs. Nat. Genet. 38:Suppl.S20–24
    [Google Scholar]
  49. Houle D, Bolstad GH, Van Der Linde K, Hansen TF 2017. Mutation predicts 40 million years of fly wing evolution. Nature 548:447–50
    [Google Scholar]
  50. Hu HY, Guo S, Xi J, Yan Z, Fu N et al. 2011. MicroRNA expression and regulation in human, chimpanzee, and macaque brains. PLOS Genet 7:e1002327
    [Google Scholar]
  51. Hu Z, Zhao J, Hu T, Luo Y, Zhu J, Li Z 2015. miR-501-3p mediates the activity-dependent regulation of the expression of AMPA receptor subunit GluA1. J. Cell Biol. 208:949–59
    [Google Scholar]
  52. Huntzinger E, Izaurralde E 2011. Gene silencing by microRNAs: contributions of translational repression and mRNA decay. Nat. Rev. Genet. 12:99–110
    [Google Scholar]
  53. Hutsler JJ, Lee DG, Porter KK 2005. Comparative analysis of cortical layering and supragranular layer enlargement in rodent carnivore and primate species. Brain Res 1052:71–81
    [Google Scholar]
  54. Hutvagner G, Zamore PD 2002. A microRNA in a multiple-turnover RNAi enzyme complex. Science 297:2056–60
    [Google Scholar]
  55. Ipsaro JJ, Joshua-Tor L 2015. From guide to target: molecular insights into eukaryotic RNA-interference machinery. Nat. Struct. Mol. Biol. 22:20–28
    [Google Scholar]
  56. Ivey KN, Srivastava D 2010. MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7:36–41
    [Google Scholar]
  57. Jang J, Wang Y, Lalli MA, Guzman E, Godshalk SE et al. 2016. Primary cilium-autophagy-Nrf2 (PAN) axis activation commits human embryonic stem cells to a neuroectoderm fate. Cell 165:410–20
    [Google Scholar]
  58. Jiang X, Shen S, Cadwell CR, Berens P, Sinz F et al. 2015. Principles of connectivity among morphologically defined cell types in adult neocortex. Science 350:aac9462
    [Google Scholar]
  59. Jönsson ME, Nelander Wahlestedt J, Åkerblom M, Kirkeby A, Malmevik J et al. 2015. Comprehensive analysis of microRNA expression in regionalized human neural progenitor cells reveals microRNA-10 as a caudalizing factor. Development 142:3166–77
    [Google Scholar]
  60. Jovičić A, Roshan R, Moisoi N, Pradervand S, Moser R et al. 2013. Comprehensive expression analyses of neural cell-type-specific miRNAs identify new determinants of the specification and maintenance of neuronal phenotypes. J. Neurosci. 33:5127–37
    [Google Scholar]
  61. Kaas JH 2012. The evolution of neocortex in primates. Prog. Brain Res. 195:91–102
    [Google Scholar]
  62. Kawase-Koga Y, Otaegi G, Sun T 2009. Different timings of Dicer deletion affect neurogenesis and gliogenesis in the developing mouse central nervous system. Dev. Dyn. 238:2800–12
    [Google Scholar]
  63. Kelava I, Reillo I, Murayama AY, Kalinka AT, Stenzel D et al. 2012. Abundant occurrence of basal radial glia in the subventricular zone of embryonic neocortex of a lissencephalic primate, the common marmoset Callithrix jacchus. Cereb. Cortex 22:469–81
    [Google Scholar]
  64. Kennedy H, Dehay C 2012. Self-organization and interareal networks in the primate cortex. Prog. Brain Res. 195:341–60
    [Google Scholar]
  65. Kennell JA, Cadigan KM, Shakhmantsir I, Waldron EJ 2012. The microRNA miR-8 is a positive regulator of pigmentation and eclosion in Drosophila. Dev. Dyn. 241:161–68
    [Google Scholar]
  66. Kosik KS 2009. MicroRNAs tell an evo-devo story. Nat. Rev. Neurosci. 10:754–59
    [Google Scholar]
  67. Kriegstein A, Noctor S, Martínez-Cerdeño V 2006. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat. Rev. Neurosci. 7:883–90
    [Google Scholar]
  68. Lake BB, Ai R, Kaeser GE, Salathia NS, Yung YC et al. 2016. Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain. Science 352:1586–90
    [Google Scholar]
  69. Lamonica BE, Lui JH, Wang X, Kriegstein AR 2012. OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr. Opin. Neurobiol. 22:747–53
    [Google Scholar]
  70. Lee CT, Risom T, Strauss WM 2007. Evolutionary conservation of microRNA regulatory circuits: an examination of microRNA gene complexity and conserved microRNA-target interactions through metazoan phylogeny. DNA Cell Biol 26:209–18
    [Google Scholar]
  71. Lee Y, Ahn C, Han J, Choi H, Kim J et al. 2003. The nuclear RNase III Drosha initiates microRNA processing. Nature 425:415–19
    [Google Scholar]
  72. Lein ES, Belgard TG, Hawrylycz M, Molnár Z 2017. Transcriptomic perspectives on neocortical structure, development, evolution, and disease. Annu. Rev. Neurosci. 40:629–52
    [Google Scholar]
  73. Levitt P, Cooper ML, Rakic P 1981. Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci. 1:27–39
    [Google Scholar]
  74. Lewis BP, Shih IH, Jones-Rhoades MW, Bartel DP, Burge CB 2003. Prediction of mammalian microRNA targets. Cell 115:787–98
    [Google Scholar]
  75. Li X, Cassidy JJ, Reinke CA, Fischboeck S, Carthew RW 2009. A microRNA imparts robustness against environmental fluctuation during development. Cell 137:273–82
    [Google Scholar]
  76. Lin Y, Sohn CH, Dalal CK, Cai L, Elowitz MB 2015. Combinatorial gene regulation by modulation of relative pulse timing. Nature 527:54–58
    [Google Scholar]
  77. Londin E, Loher P, Telonis AG, Quann K, Clark P et al. 2015. Analysis of 13 cell types reveals evidence for the expression of numerous novel primate- and tissue-specific microRNAs. PNAS 112:E1106–15
    [Google Scholar]
  78. Lui JH, Hansen DV, Kriegstein AR 2011. Development and evolution of the human neocortex. Cell 146:18–36
    [Google Scholar]
  79. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C et al. 2005. G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47:353–64
    [Google Scholar]
  80. Luo C, Keown CL, Kurihara L, Zhou J, He Y et al. 2017. Single-cell methylomes identify neuronal subtypes and regulatory elements in mammalian cortex. Science 357:600–4
    [Google Scholar]
  81. Lv X, Jiang H, Liu Y, Lei X, Jiao J 2014. MicroRNA-15b promotes neurogenesis and inhibits neural progenitor proliferation by directly repressing TET3 during early neocortical development. EMBO Rep 15:1305–14
    [Google Scholar]
  82. Makeyev EV, Zhang J, Carrasco MA, Maniatis T 2007. The microRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27:435–48
    [Google Scholar]
  83. Marín-Padilla M 1992. Ontogenesis of the pyramidal cell of the mammalian neocortex and developmental cytoarchitectonics: a unifying theory. J. Comp. Neurol. 321:223–40
    [Google Scholar]
  84. Markov NT, Ercsey-Ravasz M, Van Essen DC, Knoblauch K, Toroczkai Z, Kennedy H 2013. Cortical high-density counterstream architectures. Science 342:1238406
    [Google Scholar]
  85. Martí E, Pantano L, Bañez-Coronel M, Llorens F, Miñones-Moyano E et al. 2010. A myriad of miRNA variants in control and Huntington's disease brain regions detected by massively parallel sequencing. Nucleic Acids Res 38:7219–35
    [Google Scholar]
  86. Martin KC, Kosik KS 2002. Synaptic tagging – who's it?. Nat. Rev. Neurosci. 3:813–20
    [Google Scholar]
  87. Martínez-Cerdeño V, Noctor SC, Kriegstein AR 2006. The role of intermediate progenitor cells in the evolutionary expansion of the cerebral cortex. Cereb. Cortex 16:Suppl. 1i152–61
    [Google Scholar]
  88. Martínez-Martínez , De Juan Romero C, Fernández V, Cárdenas A, Götz M, Borrell V 2016. A restricted period for formation of outer subventricular zone defined by Cdh1 and Trnp1 levels. Nat. Commun. 7:11812
    [Google Scholar]
  89. Mattick JS 2004. RNA regulation: a new genetics?. Nat. Rev. Genet. 5:316–23
    [Google Scholar]
  90. McCreight JC, Schneider SE, Wilburn DB, Swanson WJ 2017. Evolution of microRNA in primates. PLOS ONE 12:e0176596
    [Google Scholar]
  91. McKenna A, Findlay GM, Gagnon JA, Horwitz MS, Schier AF, Shendure J 2016. Whole-organism lineage tracing by combinatorial and cumulative genome editing. Science 353:aaf7907
    [Google Scholar]
  92. Miller KD 2016. Canonical computations of cerebral cortex. Curr. Opin. Neurobiol. 37:75–84
    [Google Scholar]
  93. Miyama S, Takahashi T, Nowakowski RS, Caviness VS Jr 1997. A gradient in the duration of the G1 phase in the murine neocortical proliferative epithelium. Cereb. Cortex 7:678–89
    [Google Scholar]
  94. Mora-Bermúdez F, Badsha F, Kanton S, Camp JG, Vernot B et al. 2016. Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development. eLife 5:e18683
    [Google Scholar]
  95. Moreau MP, Bruse SE, Jornsten R, Liu Y, Brzustowicz LM 2013. Chronological changes in microRNA expression in the developing human brain. PLOS ONE 8:e60480
    [Google Scholar]
  96. Nielsen JA, Lau P, Maric D, Barker JL, Hudson LD 2009. Integrating microRNA and mRNA expression profiles of neuronal progenitors to identify regulatory networks underlying the onset of cortical neurogenesis. BMC Neurosci 10:98
    [Google Scholar]
  97. Nigro A, Menon R, Bergamaschi A, Clovis YM, Baldi A et al. 2012. MiR-30e and miR-181d control radial glia cell proliferation via HtrA1 modulation. Cell Death Dis 3:e360
    [Google Scholar]
  98. Noctor SC, Martínez-Cerdeño V, Ivic L, Kriegstein AR 2004. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7:136–44
    [Google Scholar]
  99. Nowakowski TJ, Fotaki V, Pollock A, Sun T, Pratt T, Price DJ 2013a. MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. PNAS 110:7056–61
    [Google Scholar]
  100. Nowakowski TJ, Mysiak KS, O'Leary T, Fotaki V, Pratt T, Price DJ 2013b. Loss of functional Dicer in mouse radial glia cell-autonomously prolongs cortical neurogenesis. Dev. Biol. 382:530–37
    [Google Scholar]
  101. Nowakowski TJ, Pollen AA, Sandoval-Espinosa C, Kriegstein AR 2016. Transformation of the radial glia scaffold demarcates two stages of human cerebral cortex development. Neuron 91:1219–27
    [Google Scholar]
  102. Olejniczak SH, La Rocca G, Gruber JJ, Thompson CB 2013. Long-lived microRNA-Argonaute complexes in quiescent cells can be activated to regulate mitogenic responses. PNAS 110:157
    [Google Scholar]
  103. Otani T, Marchetto MC, Gage FH, Simons BD, Livesey FJ 2016. 2D and 3D stem cell models of primate cortical development identify species-specific differences in progenitor behavior contributing to brain size. Cell Stem Cell 18:467–80
    [Google Scholar]
  104. Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI et al. 2000. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Nature 408:86–89
    [Google Scholar]
  105. Pauklin S, Vallier L 2013. The cell-cycle state of stem cells determines cell fate propensity. Cell 155:135–47
    [Google Scholar]
  106. Perelman P, Johnson WE, Roos C, Seuánez HN, Horvath JE et al. 2011. A molecular phylogeny of living primates. PLOS Genet 7:e1001342
    [Google Scholar]
  107. Peterson KJ, Dietrich MR, McPeek MA 2009. MicroRNAs and metazoan macroevolution: insights into canalization, complexity, and the Cambrian explosion. Bioessays 31:736–47
    [Google Scholar]
  108. Piriyapongsa J, Mariño-Ramírez L, Jordan IK 2007. Origin and evolution of human microRNAs from transposable elements. Genetics 176:1323–37
    [Google Scholar]
  109. Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C et al. 2015. Molecular identity of human outer radial glia during cortical development. Cell 163:55–67
    [Google Scholar]
  110. Pollen AA, Nowakowski TJ, Shuga J, Wang X, Leyrat AA et al. 2014. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat. Biotechnol. 32:1053–58
    [Google Scholar]
  111. Pollock A, Bian S, Zhang C, Chen Z, Sun T 2014. Growth of the developing cerebral cortex is controlled by microRNA-7 through the p53 pathway. Cell Rep 7:1184–96
    [Google Scholar]
  112. Pontious A, Kowalczyk T, Englund C, Hevner RF 2008. Role of intermediate progenitor cells in cerebral cortex development. Dev. Neurosci. 30:24–32
    [Google Scholar]
  113. Quadrato G, Nguyen T, Macosko EZ, Sherwood JL, Min Yang S et al. 2017. Cell diversity and network dynamics in photosensitive human brain organoids. Nature 545:48–53
    [Google Scholar]
  114. Rakic P 1988. Specification of cerebral cortical areas. Science 241:170–76
    [Google Scholar]
  115. Rakic P 2008. Confusing cortical columns. PNAS 105:12099–100
    [Google Scholar]
  116. Rakic P, Sidman RL 1968. Supravital DNA synthesis in the developing human and mouse brain. J. Neuropathol. Exp. Neurol. 27:246–76
    [Google Scholar]
  117. Rani N, Nowakowski TJ, Zhou H, Godshalk SE, Lisi V et al. 2016. A primate lncRNA mediates Notch signaling during neuronal development by sequestering miRNA. Neuron 90:1174–88
    [Google Scholar]
  118. Reillo I, De Juan Romero C, García-Cabezas , Borrell V 2011. A role for intermediate radial glia in the tangential expansion of the mammalian cerebral cortex. Cereb. Cortex 21:1674–94
    [Google Scholar]
  119. Sakaue-Sawano A, Kurokawa H, Morimura T, Hanyu A, Hama H et al. 2008. Visualizing spatiotemporal dynamics of multicellular cell-cycle progression. Cell 132:487–98
    [Google Scholar]
  120. Schirle NT, MacRae IJ 2012. The crystal structure of human Argonaute2. Science 336:1037–40
    [Google Scholar]
  121. Sela Y, Molotski N, Golan S, Itskovitz-Eldor J, Soen Y 2012. Human embryonic stem cells exhibit increased propensity to differentiate during the G1 phase prior to phosphorylation of retinoblastoma protein. Stem Cells 30:1097–108
    [Google Scholar]
  122. Shibata M, Nakao H, Kiyonari H, Abe T, Aizawa S 2011. MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 31:3407–22
    [Google Scholar]
  123. Shu P, Fu H, Zhao X, Wu C, Ruan X et al. 2017. MicroRNA-214 modulates neural progenitor cell differentiation by targeting Quaking during cerebral cortex development. Sci. Rep. 7:8014
    [Google Scholar]
  124. Smart IH, Dehay C, Giroud P, Berland M, Kennedy H 2002. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 12:37–53
    [Google Scholar]
  125. Smirnova L, Gräfe A, Seiler A, Schumacher S, Nitsch R, Wulczyn FG 2005. Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 21:1469–77
    [Google Scholar]
  126. Sokol NS, Ambros V 2005. Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev 19:2343–54
    [Google Scholar]
  127. Somel M, Liu X, Tang L, Yan Z, Hu H et al. 2011. MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLOS Biol 9:e1001214
    [Google Scholar]
  128. Song JJ, Smith SK, Hannon GJ, Joshua-Tor L 2004. Crystal structure of Argonaute and its implications for RISC slicer activity. Science 305:1434–37
    [Google Scholar]
  129. Sousa AMM, Meyer KA, Santpere G, Gulden FO, Sestan N 2017a. Evolution of the human nervous system function, structure, and development. Cell 170:226–47
    [Google Scholar]
  130. Sousa AMM, Zhu Y, Raghanti MA, Kitchen RR, Onorati M et al. 2017b. Molecular and cellular reorganization of neural circuits in the human lineage. Science 358:1027–32
    [Google Scholar]
  131. Sudmant PH, Huddleston J, Catacchio CR, Malig M, Hillier LW et al. 2013. Evolution and diversity of copy number variation in the great ape lineage. Genome Res 23:1373–82
    [Google Scholar]
  132. Takahashi T, Nowakowski RS, Caviness VS Jr 1993. Cell cycle parameters and patterns of nuclear movement in the neocortical proliferative zone of the fetal mouse. J. Neurosci. 13:820–33
    [Google Scholar]
  133. Tarui T, Takahashi T, Nowakowski RS, Hayes NL, Bhide PG, Caviness VS 2005. Overexpression of p27Kip1, probability of cell cycle exit, and laminar destination of neocortical neurons. Cereb. Cortex 15:1343–55
    [Google Scholar]
  134. Tasic B, Menon V, Nguyen TN, Kim TK, Jarsky T et al. 2016. Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat. Neurosci. 19:335–46
    [Google Scholar]
  135. Thomsen ER, Mich JK, Yao Z, Hodge RD, Doyle AM et al. 2016. Fixed single-cell transcriptomic characterization of human radial glial diversity. Nat. Methods 13:87–93
    [Google Scholar]
  136. Tsai HH, Li H, Fuentealba LC, Molofsky AV, Taveira-Marques R et al. 2012. Regional astrocyte allocation regulates CNS synaptogenesis and repair. Science 337:358–62
    [Google Scholar]
  137. Tsuyama J, Bunt J, Richards LJ, Iwanari H, Mochizuki Y et al. 2015. MicroRNA-153 regulates the acquisition of gliogenic competence by neural stem cells. Stem Cell Rep 5:365–77
    [Google Scholar]
  138. Volvert ML, Prevot PP, Close P, Laguesse S, Pirotte S et al. 2014. MicroRNA targeting of CoREST controls polarization of migrating cortical neurons. Cell Rep 7:1168–83
    [Google Scholar]
  139. Waddington CH 1942. Canalization of development and the inheritance of acquired characters. Nature 150:563–65
    [Google Scholar]
  140. Woodworth MB, Girskis KM, Walsh CA 2017. Building a lineage from single cells: genetic techniques for cell lineage tracking. Nat. Rev. Genet. 18:230–44
    [Google Scholar]
  141. Xu J, Zhang R, Shen Y, Liu G, Lu X, Wu CI 2013. The evolution of evolvability in microRNA target sites in vertebrates. Genome Res 23:1810–16
    [Google Scholar]
  142. Yekta S, Shih IH, Bartel DP 2004. MicroRNA-directed cleavage of HOXB8 mRNA. Science 304:594–96
    [Google Scholar]
  143. Yu YC, Bultje RS, Wang X, Shi SH 2009. Specific synapses develop preferentially among sister excitatory neurons in the neocortex. Nature 458:501–4
    [Google Scholar]
  144. Zamore PD, Tuschl T, Sharp PA, Bartel DP 2000. RNAi: double-stranded RNA directs the ATP-dependent cleavage of mRNA at 21 to 23 nucleotide intervals. Cell 101:25
    [Google Scholar]
  145. Zhang W, Kim PJ, Chen Z, Lokman H, Qiu L et al. 2016. MiRNA-128 regulates the proliferation and neurogenesis of neural precursors by targeting PCM1 in the developing cortex. eLife 5:e11324
    [Google Scholar]
  146. Zhou H, Arcila ML, Li Z, Lee EJ, Henzler C et al. 2012. Deep annotation of mouse iso-miR and iso-moR variation. Nucleic Acids Res 40:5864–75
    [Google Scholar]
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