Display options
Cite
Prodromidou K, Matsas R. Evolving features of human cortical development and the emerging roles of non-coding RNAs in neural progenitor cell diversity and function. Cell Mol Life Sci. 2021;79(1):56doi: 10.1007/s00018-021-04063-7.
Prodromidou, K., & Matsas, R. (2021). Evolving features of human cortical development and the emerging roles of non-coding RNAs in neural progenitor cell diversity and function. Cellular and molecular life sciences : CMLS, 79(1), 56. https://doi.org/10.1007/s00018-021-04063-7
Prodromidou, Kanella, and Matsas, Rebecca. "Evolving features of human cortical development and the emerging roles of non-coding RNAs in neural progenitor cell diversity and function." Cellular and molecular life sciences : CMLS vol. 79,1 (2021): 56. doi: https://doi.org/10.1007/s00018-021-04063-7
Prodromidou K, Matsas R. Evolving features of human cortical development and the emerging roles of non-coding RNAs in neural progenitor cell diversity and function. Cell Mol Life Sci. 2021 Dec 18;79(1):56. doi: 10.1007/s00018-021-04063-7. PMID: 34921638.
Copy Download .nbib Format: NLM
Share it on

Cell Mol Life Sci. 2021 Dec 18;79(1):56. doi: 10.1007/s00018-021-04063-7.

Evolving features of human cortical development and the emerging roles of non-coding RNAs in neural progenitor cell diversity and function.

Cellular and molecular life sciences : CMLS

Kanella Prodromidou, Rebecca Matsas

Affiliations

  1. Laboratory of Cellular and Molecular Neurobiology-Stem Cells, Department of Neurobiology, Hellenic Pasteur Institute, 127 Vasilissis Sofias Avenue, 11521, Athens, Greece. [email protected].
  2. Laboratory of Cellular and Molecular Neurobiology-Stem Cells, Department of Neurobiology, Hellenic Pasteur Institute, 127 Vasilissis Sofias Avenue, 11521, Athens, Greece.

PMID: 34921638 DOI: 10.1007/s00018-021-04063-7

Abstract

The human cerebral cortex is a uniquely complex structure encompassing an unparalleled diversity of neuronal types and subtypes. These arise during development through a series of evolutionary conserved processes, such as progenitor cell proliferation, migration and differentiation, incorporating human-associated adaptations including a protracted neurogenesis and the emergence of novel highly heterogeneous progenitor populations. Disentangling the unique features of human cortical development involves elucidation of the intricate developmental cell transitions orchestrated by progressive molecular events. Crucially, developmental timing controls the fine balance between cell cycle progression/exit and the neurogenic competence of precursor cells, which undergo morphological transitions coupled to transcriptome-defined temporal states. Recent advances in bulk and single-cell transcriptomic technologies suggest that alongside protein-coding genes, non-coding RNAs exert important regulatory roles in these processes. Interestingly, a considerable number of novel long non-coding RNAs (lncRNAs) and microRNAs (miRNAs) have appeared in human and non-human primates suggesting an evolutionary role in shaping cortical development. Here, we present an overview of human cortical development and highlight the marked diversification and complexity of human neuronal progenitors. We further discuss how lncRNAs and miRNAs constitute critical components of the extended epigenetic regulatory network defining intermediate states of progenitors and controlling cell cycle dynamics and fate choices with spatiotemporal precision, during human neurodevelopment.

© 2021. The Author(s), under exclusive licence to Springer Nature Switzerland AG.

Keywords: Epitranscriptomics; Evolution; Long non-coding RNAs; Neurogenesis; Single-cell RNA sequencing; miRNAs

References

  1. Li Z, Tyler WA, Zeldich E, Santpere Baro G, Okamoto M, Gao T et al (2020) Transcriptional priming as a conserved mechanism of lineage diversification in the developing mouse and human neocortex. Sci Adv 6:45 - PubMed
  2. Le Bail R, Bonafina A, Espuny-Camacho I, Nguyen L (2020) Learning about cell lineage, cellular diversity and evolution of the human brain through stem cell models. Curr Opin Neurobiol 66:166–177 - PubMed
  3. Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146(1):18–36 - PubMed
  4. Carninci P, Kasukawa T, Katayama S, Gough J, Frith MC, Maeda N et al (2005) The transcriptional landscape of the mammalian genome. Science 309(5740):1559–1563 - PubMed
  5. Consortium EP, Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR et al (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447(7146):799–816 - PubMed
  6. Aprea J, Prenninger S, Dori M, Ghosh T, Monasor LS, Wessendorf E et al (2013) Transcriptome sequencing during mouse brain development identifies long non-coding RNAs functionally involved in neurogenic commitment. EMBO J 32(24):3145–3160 - PubMed
  7. Prodromidou K, Matsas R (2019) Species-specific miRNAs in human brain development and disease. Front Cell Neurosci 13:559 - PubMed
  8. Qureshi IA, Mattick JS, Mehler MF (2010) Long non-coding RNAs in nervous system function and disease. Brain Res 1338:20–35 - PubMed
  9. Mercer TR, Dinger ME, Sunkin SM, Mehler MF, Mattick JS (2008) Specific expression of long noncoding RNAs in the mouse brain. Proc Natl Acad Sci USA 105(2):716–721 - PubMed
  10. Lake BB, Ai R, Kaeser GE, Salathia NS, Yung YC, Liu R et al (2016) Neuronal subtypes and diversity revealed by single-nucleus RNA sequencing of the human brain. Science 352(6293):1586–1590 - PubMed
  11. Hardwick LJ, Ali FR, Azzarelli R, Philpott A (2015) Cell cycle regulation of proliferation versus differentiation in the central nervous system. Cell Tissue Res 359(1):187–200 - PubMed
  12. Lodato S, Arlotta P (2015) Generating neuronal diversity in the mammalian cerebral cortex. Annu Rev Cell Dev Biol 31:699–720 - PubMed
  13. Hill RS, Walsh CA (2005) Molecular insights into human brain evolution. Nature 437(7055):64–67 - PubMed
  14. 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(1):37–53 - PubMed
  15. Rosenberg AB, Roco CM, Muscat RA, Kuchina A, Sample P, Yao Z et al (2018) Single-cell profiling of the developing mouse brain and spinal cord with split-pool barcoding. Science 360(6385):176–182 - PubMed
  16. Paul A, Crow M, Raudales R, He M, Gillis J, Huang ZJ (2017) Transcriptional architecture of synaptic communication delineates GABAergic neuron identity. Cell 171(3):522-39e20 - PubMed
  17. Farnsworth DR, Saunders LM, Miller AC (2020) A single-cell transcriptome atlas for zebrafish development. Dev Biol 459(2):100–108 - PubMed
  18. Nowakowski TJ, Bhaduri A, Pollen AA, Alvarado B, Mostajo-Radji MA, Di Lullo E et al (2017) Spatiotemporal gene expression trajectories reveal developmental hierarchies of the human cortex. Science 358(6368):1318–1323 - PubMed
  19. Zhong S, Zhang S, Fan X, Wu Q, Yan L, Dong J et al (2018) A single-cell RNA-seq survey of the developmental landscape of the human prefrontal cortex. Nature 555(7697):524–528 - PubMed
  20. Tasic B, Yao Z, Graybuck LT, Smith KA, Nguyen TN, Bertagnolli D et al (2018) Shared and distinct transcriptomic cell types across neocortical areas. Nature 563(7729):72–78 - PubMed
  21. Hodge RD, Bakken TE, Miller JA, Smith KA, Barkan ER, Graybuck LT et al (2019) Conserved cell types with divergent features in human versus mouse cortex. Nature 573(7772):61–68 - PubMed
  22. Khrameeva E, Kurochkin I, Han D, Guijarro P, Kanton S, Santel M et al (2020) Single-cell-resolution transcriptome map of human, chimpanzee, bonobo, and macaque brains. Genome Res 30(5):776–789 - PubMed
  23. Bayraktar OA, Bartels T, Holmqvist S, Kleshchevnikov V, Martirosyan A, Polioudakis D et al (2020) Astrocyte layers in the mammalian cerebral cortex revealed by a single-cell in situ transcriptomic map. Nat Neurosci 23(4):500–509 - PubMed
  24. Marques S, Zeisel A, Codeluppi S, van Bruggen D, Mendanha Falcao A, Xiao L et al (2016) Oligodendrocyte heterogeneity in the mouse juvenile and adult central nervous system. Science 352(6291):1326–1329 - PubMed
  25. Lake BB, Chen S, Sos BC, Fan J, Kaeser GE, Yung YC et al (2018) Integrative single-cell analysis of transcriptional and epigenetic states in the human adult brain. Nat Biotechnol 36(1):70–80 - PubMed
  26. Zeisel A, Munoz-Manchado AB, Codeluppi S, Lonnerberg P, La Manno G, Jureus A et al (2015) Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347(6226):1138–1142 - PubMed
  27. Tasic B, Menon V, Nguyen TN, Kim TK, Jarsky T, Yao Z et al (2016) Adult mouse cortical cell taxonomy revealed by single cell transcriptomics. Nat Neurosci 19(2):335–346 - PubMed
  28. Noctor SC, Flint AC, Weissman TA, Dammerman RS, Kriegstein AR (2001) Neurons derived from radial glial cells establish radial units in neocortex. Nature 409(6821):714–720 - PubMed
  29. Frantz GD, Weimann JM, Levin ME, McConnell SK (1994) Otx1 and Otx2 define layers and regions in developing cerebral cortex and cerebellum. J Neurosci 14(10):5725–5740 - PubMed
  30. Anderson SA, Kaznowski CE, Horn C, Rubenstein JL, McConnell SK (2002) Distinct origins of neocortical projection neurons and interneurons in vivo. Cereb Cortex 12(7):702–709 - PubMed
  31. Angevine JB Jr, Sidman RL (1961) Autoradiographic study of cell migration during histogenesis of cerebral cortex in the mouse. Nature 192:766–768 - PubMed
  32. Arimatsu Y, Ishida M (2002) Distinct neuronal populations specified to form corticocortical and corticothalamic projections from layer VI of developing cerebral cortex. Neuroscience 114(4):1033–1045 - PubMed
  33. Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183(4123):425–427 - PubMed
  34. Takahashi T, Goto T, Miyama S, Nowakowski RS, Caviness VS Jr (1999) Sequence of neuron origin and neocortical laminar fate: relation to cell cycle of origin in the developing murine cerebral wall. J Neurosci 19(23):10357–10371 - PubMed
  35. Uzquiano A, Gladwyn-Ng I, Nguyen L, Reiner O, Gotz M, Matsuzaki F et al (2018) Cortical progenitor biology: key features mediating proliferation versus differentiation. J Neurochem 146(5):500–525 - PubMed
  36. Guo C, Eckler MJ, McKenna WL, McKinsey GL, Rubenstein JL, Chen B (2013) Fezf2 expression identifies a multipotent progenitor for neocortical projection neurons, astrocytes, and oligodendrocytes. Neuron 80(5):1167–1174 - PubMed
  37. Han W, Sestan N (2013) Cortical projection neurons: sprung from the same root. Neuron 80(5):1103–1105 - PubMed
  38. Franco SJ, Gil-Sanz C, Martinez-Garay I, Espinosa A, Harkins-Perry SR, Ramos C et al (2012) Fate-restricted neural progenitors in the mammalian cerebral cortex. Science 337(6095):746–749 - PubMed
  39. Silbereis JC, Pochareddy S, Zhu Y, Li M, Sestan N (2016) The cellular and molecular landscapes of the developing human central nervous system. Neuron 89(2):248–268 - PubMed
  40. Subramanian L, Bershteyn M, Paredes MF, Kriegstein AR (2017) Dynamic behaviour of human neuroepithelial cells in the developing forebrain. Nat Commun 8:14167 - PubMed
  41. Mora-Bermudez F, Badsha F, Kanton S, Camp JG, Vernot B, Kohler K et al (2016) Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development. Elife 2016:5 - PubMed
  42. Zhu Y, Sousa AMM, Gao T, Skarica M, Li M, Santpere G et al (2018) Spatiotemporal transcriptomic divergence across human and macaque brain development. Science 362:6420 - PubMed
  43. 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(6):1219–1227 - PubMed
  44. Vaid S, Camp JG, Hersemann L, Eugster Oegema C, Heninger AK, Winkler S et al (2018) A novel population of Hopx-dependent basal radial glial cells in the developing mouse neocortex. Development 145:20 - PubMed
  45. Fietz SA, Kelava I, Vogt J, Wilsch-Brauninger M, Stenzel D, Fish JL et al (2010) OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling. Nat Neurosci 13(6):690–699 - PubMed
  46. Hansen DV, Lui JH, Parker PR, Kriegstein AR (2010) Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464(7288):554–561 - PubMed
  47. Shitamukai A, Konno D, Matsuzaki F (2011) Oblique radial glial divisions in the developing mouse neocortex induce self-renewing progenitors outside the germinal zone that resemble primate outer subventricular zone progenitors. J Neurosci 31(10):3683–3695 - PubMed
  48. Martinez-Cerdeno V, Cunningham CL, Camacho J, Antczak JL, Prakash AN, Cziep ME et al (2012) Comparative analysis of the subventricular zone in rat, ferret and macaque: evidence for an outer subventricular zone in rodents. PLoS ONE 7(1):E30178 - PubMed
  49. Lukaszewicz A, Savatier P, Cortay V, Giroud P, Huissoud C, Berland M et al (2005) G1 phase regulation, area-specific cell cycle control, and cytoarchitectonics in the primate cortex. Neuron 47(3):353–364 - PubMed
  50. Telley L, Agirman G, Prados J, Amberg N, Fievre S, Oberst P et al (2019) Temporal patterning of apical progenitors and their daughter neurons in the developing neocortex. Science 364:6440 - PubMed
  51. Schuurmans C, Armant O, Nieto M, Stenman JM, Britz O, Klenin N et al (2004) Sequential phases of cortical specification involve Neurogenin-dependent and -independent pathways. EMBO J 23(14):2892–2902 - PubMed
  52. Leingartner A, Richards LJ, Dyck RH, Akazawa C, O’Leary DD (2003) Cloning and cortical expression of rat Emx2 and adenovirus-mediated overexpression to assess its regulation of area-specific targeting of thalamocortical axons. Cereb Cortex 13(6):648–660 - PubMed
  53. Chen B, Schaevitz LR, McConnell SK (2005) Fezl regulates the differentiation and axon targeting of layer 5 subcortical projection neurons in cerebral cortex. Proc Natl Acad Sci USA 102(47):17184–17189 - PubMed
  54. 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(32):11382–11387 - PubMed
  55. Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, Sandhu JK et al (2006) Role of Sox2 in the development of the mouse neocortex. Dev Biol 295(1):52–66 - PubMed
  56. Britanova O, Akopov S, Lukyanov S, Gruss P, Tarabykin V (2005) Novel transcription factor Satb2 interacts with matrix attachment region DNA elements in a tissue-specific manner and demonstrates cell-type-dependent expression in the developing mouse CNS. Eur J Neurosci 21(3):658–668 - PubMed
  57. Oberst P, Fievre S, Baumann N, Concetti C, Bartolini G, Jabaudon D (2019) Temporal plasticity of apical progenitors in the developing mouse neocortex. Nature 573(7774):370–374 - PubMed
  58. Okamoto M, Miyata T, Konno D, Ueda HR, Kasukawa T, Hashimoto M et al (2016) Cell-cycle-independent transitions in temporal identity of mammalian neural progenitor cells. Nat Commun 7:11349 - PubMed
  59. Gaspard N, Bouschet T, Hourez R, Dimidschstein J, Naeije G, van den Ameele J et al (2008) An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455(7211):351–357 - PubMed
  60. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR et al (2006) The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9(6):743–751 - PubMed
  61. Morris SA (2019) The evolving concept of cell identity in the single cell era. Development 146:12 - PubMed
  62. Estivill-Torrus G, Pearson H, van Heyningen V, Price DJ, Rashbass P (2002) Pax6 is required to regulate the cell cycle and the rate of progression from symmetrical to asymmetrical division in mammalian cortical progenitors. Development 129(2):455–466 - PubMed
  63. Pollen AA, Nowakowski TJ, Chen J, Retallack H, Sandoval-Espinosa C, Nicholas CR et al (2015) Molecular identity of human outer radial glia during cortical development. Cell 163(1):55–67 - PubMed
  64. Thomsen ER, Mich JK, Yao Z, Hodge RD, Doyle AM, Jang S et al (2016) Fixed single-cell transcriptomic characterization of human radial glial diversity. Nat Methods 13(1):87–93 - PubMed
  65. Johnson MB, Wang PP, Atabay KD, Murphy EA, Doan RN, Hecht JL et al (2015) Single-cell analysis reveals transcriptional heterogeneity of neural progenitors in human cortex. Nat Neurosci 18(5):637–646 - PubMed
  66. Kawaguchi A, Ikawa T, Kasukawa T, Ueda HR, Kurimoto K, Saitou M et al (2008) Single-cell gene profiling defines differential progenitor subclasses in mammalian neurogenesis. Development 135(18):3113–3124 - PubMed
  67. Kageyama J, Wollny D, Treutlein B, Camp JG (2018) ShinyCortex: exploring single-cell transcriptome data from the developing human cortex. Front Neurosci 12:315 - PubMed
  68. Benito-Kwiecinski S, Giandomenico SL, Sutcliffe M, Riis ES, Freire-Pritchett P, Kelava I et al (2021) An early cell shape transition drives evolutionary expansion of the human forebrain. Cell - PubMed
  69. Noctor SC, Martinez-Cerdeno V, Ivic L, Kriegstein AR (2004) Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat Neurosci 7(2):136–144 - PubMed
  70. Nelson BR, Hodge RD, Bedogni F, Hevner RF (2013) Dynamic interactions between intermediate neurogenic progenitors and radial glia in embryonic mouse neocortex: potential role in Dll1-Notch signaling. J Neurosci 33(21):9122–9139 - PubMed
  71. Betizeau M, Cortay V, Patti D, Pfister S, Gautier E, Bellemin-Menard A et al (2013) Precursor diversity and complexity of lineage relationships in the outer subventricular zone of the primate. Neuron 80(2):442–457 - PubMed
  72. Takahashi T, Nowakowski RS, Caviness VS Jr (1996) The leaving or Q fraction of the murine cerebral proliferative epithelium: a general model of neocortical neuronogenesis. J Neurosci 16(19):6183–6196 - PubMed
  73. De Juan RC, Borrell V (2015) Coevolution of radial glial cells and the cerebral cortex. Glia 63(8):1303–1319 - PubMed
  74. Cai L, Hayes NL, Takahashi T, Caviness VS Jr, Nowakowski RS (2002) Size distribution of retrovirally marked lineages matches prediction from population measurements of cell cycle behavior. J Neurosci Res 69(6):731–744 - PubMed
  75. Nonaka-Kinoshita M, Reillo I, Artegiani B, Martinez-Martinez MA, Nelson M, Borrell V et al (2013) Regulation of cerebral cortex size and folding by expansion of basal progenitors. EMBO J 32(13):1817–1828 - PubMed
  76. Lui JH, Nowakowski TJ, Pollen AA, Javaherian A, Kriegstein AR, Oldham MC (2014) Radial glia require PDGFD-PDGFRbeta signalling in human but not mouse neocortex. Nature 515(7526):264–268 - PubMed
  77. Florio M, Albert M, Taverna E, Namba T, Brandl H, Lewitus E et al (2015) Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347(6229):1465–1470 - PubMed
  78. Namba T, Dóczi J, Pinson A, Xing L, Kalebic N, Wilsch-Bräuninger M et al (2020) Human-specific ARHGAP11B acts in mitochondria to expand neocortical progenitors by glutainolysis. Neuron 105(5):867–81.e9 - PubMed
  79. Florio M, Heide M, Pinson A, Brandl H, Albert M, Winkler S et al (2018) Evolution and cell-type specificity of human-specific genes preferentially expressed in progenitors of fetal neocortex. Elife 2018:7 - PubMed
  80. Visel A, Minovitsky S, Dubchak I, Pennacchio LA (2007) VISTA enhancer browser–a database of tissue-specific human enhancers. Nucleic Acids Res 35:D88-92 - PubMed
  81. Gregorio I, Braghetta P, Bonaldo P, Cescon M (2018) Collagen VI in healthy and diseased nervous system. Dis Models Mech. 11:6 - PubMed
  82. Schep AN, Wu B, Buenrostro JD, Greenleaf WJ (2017) chromVAR: inferring transcription-factor-associated accessibility from single-cell epigenomic data. Nat Methods 14(10):975–978 - PubMed
  83. LaMonica BE, Lui JH, Hansen DV, Kriegstein AR (2013) Mitotic spindle orientation predicts outer radial glial cell generation in human neocortex. Nat Commun 4:1665 - PubMed
  84. Chenn A, McConnell SK (1995) Cleavage orientation and the asymmetric inheritance of Notch1 immunoreactivity in mammalian neurogenesis. Cell 82(4):631–641 - PubMed
  85. Dehay C, Kennedy H (2007) Cell-cycle control and cortical development. Nat Rev Neurosci 8(6):438–450 - PubMed
  86. Caviness VS Jr, Takahashi T, Nowakowski RS (1999) The G1 restriction point as critical regulator of neocortical neuronogenesis. Neurochem Res 24(4):497–506 - PubMed
  87. Salomoni P, Calegari F (2010) Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 20(5):233–243 - PubMed
  88. Lange C, Huttner WB, Calegari F (2009) Cdk4/cyclinD1 overexpression in neural stem cells shortens G1, delays neurogenesis, and promotes the generation and expansion of basal progenitors. Cell Stem Cell 5(3):320–331 - PubMed
  89. Kanton S, Boyle MJ, He Z, Santel M, Weigert A, Sanchis-Calleja F et al (2019) Organoid single-cell genomic atlas uncovers human-specific features of brain development. Nature 574(7778):418–422 - PubMed
  90. Matsuda M, Hayashi H, Garcia-Ojalvo J, Yoshioka-Kobayashi K, Kageyama R, Yamanaka Y et al (2020) Species-specific segmentation clock periods are due to differential biochemical reaction speeds. Science 369(6510):1450–1455 - PubMed
  91. Fietz SA, Lachmann R, Brandl H, Kircher M, Samusik N, Schroder R et al (2012) Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. Proc Natl Acad Sci USA 109(29):11836–11841 - PubMed
  92. Fan X, Fu Y, Zhou X, Sun L, Yang M, Wang M et al (2020) Single-cell transcriptome analysis reveals cell lineage specification in temporal-spatial patterns in human cortical development. Sci Adv 6(34):eaaz2978 - PubMed
  93. Eze UC, Bhaduri A, Haeussler M, Nowakowski TJ, Kriegstein AR (2021) Single-cell atlas of early human brain development highlights heterogeneity of human neuroepithelial cells and early radial glia. Nat Neurosci 24(4):584–594 - PubMed
  94. Taft RJ, Pheasant M, Mattick JS (2007) The relationship between non-protein-coding DNA and eukaryotic complexity. BioEssays 29(3):288–299 - PubMed
  95. Yoon KJ, Vissers C, Ming GL, Song H (2018) Epigenetics and epitranscriptomics in temporal patterning of cortical neural progenitor competence. J Cell Biol 217(6):1901–1914 - PubMed
  96. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A et al (2012) Landscape of transcription in human cells. Nature 489(7414):101–108 - PubMed
  97. Fatica A, Bozzoni I (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15(1):7–21 - PubMed
  98. Mercer TR, Qureshi IA, Gokhan S, Dinger ME, Li G, Mattick JS et al (2010) Long noncoding RNAs in neuronal-glial fate specification and oligodendrocyte lineage maturation. BMC Neurosci 11:14 - PubMed
  99. Hung T, Wang Y, Lin MF, Koegel AK, Kotake Y, Grant GD et al (2011) Extensive and coordinated transcription of noncoding RNAs within cell-cycle promoters. Nat Genet 43(7):621–629 - PubMed
  100. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G et al (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143(1):46–58 - PubMed
  101. Yoon JH, Abdelmohsen K, Gorospe M (2013) Posttranscriptional gene regulation by long noncoding RNA. J Mol Biol 425(19):3723–3730 - PubMed
  102. Zhang X, Wang W, Zhu W, Dong J, Cheng Y, Yin Z et al (2019) Mechanisms and functions of long non-coding RNAs at multiple regulatory levels. Int J Mol Sci 20:22 - PubMed
  103. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43(6):904–914 - PubMed
  104. Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H et al (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22(9):1775–1789 - PubMed
  105. Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154(1):26–46 - PubMed
  106. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A et al (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25(18):1915–1927 - PubMed
  107. Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U et al (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505(7485):635–640 - PubMed
  108. Chatterjee S, Fasler M, Bussing I, Grosshans H (2011) Target-mediated protection of endogenous microRNAs in C. elegans. Dev Cell 20(3):388–396 - PubMed
  109. Fuchs Wightman F, Giono LE, Fededa JP, de la Mata M (2018) Target RNAs strike back on microRNAs. Front Genet 9:435 - PubMed
  110. Marcinowski L, Tanguy M, Krmpotic A, Radle B, Lisnic VJ, Tuddenham L et al (2012) Degradation of cellular mir-27 by a novel, highly abundant viral transcript is important for efficient virus replication in vivo. PLoS Pathog 8(2):e1002510 - PubMed
  111. Saliminejad K, Khorram Khorshid HR, Soleymani Fard S, Ghaffari SH (2019) An overview of microRNAs: biology, functions, therapeutics, and analysis methods. J Cell Physiol 234(5):5451–5465 - PubMed
  112. Adlakha YK, Saini N (2014) Brain microRNAs and insights into biological functions and therapeutic potential of brain enriched miRNA-128. Mol Cancer 13:33 - PubMed
  113. Davis GM, Haas MA, Pocock R (2015) MicroRNAs: not “fine-tuners” but key regulators of neuronal development and function. Front Neurol 6:245 - PubMed
  114. Nowakowski TJ, Rani N, Golkaram M, Zhou HR, Alvarado B, Huch K et al (2018) Regulation of cell-type-specific transcriptomes by microRNA networks during human brain development. Nat Neurosci 21(12):1784–1792 - PubMed
  115. Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136(4):629–641 - PubMed
  116. Harrow J, Frankish A, Gonzalez JM, Tapanari E, Diekhans M, Kokocinski F et al (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res 22(9):1760–1774 - PubMed
  117. Belgard TG, Marques AC, Oliver PL, Abaan HO, Sirey TM, Hoerder-Suabedissen A et al (2011) A transcriptomic atlas of mouse neocortical layers. Neuron 71(4):605–616 - PubMed
  118. Molyneaux BJ, Goff LA, Brettler AC, Chen HH, Hrvatin S, Rinn JL et al (2015) DeCoN: genome-wide analysis of in vivo transcriptional dynamics during pyramidal neuron fate selection in neocortex. Neuron 85(2):275–288 - PubMed
  119. Briggs JA, Wolvetang EJ, Mattick JS, Rinn JL, Barry G (2015) Mechanisms of long non-coding RNAs in mammalian nervous system development, plasticity, disease, and evolution. Neuron 88(5):861–877 - PubMed
  120. Guttman M, Donaghey J, Carey BW, Garber M, Grenier JK, Munson G et al (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477(7364):295–300 - PubMed
  121. Ng SY, Johnson R, Stanton LW (2012) Human long non-coding RNAs promote pluripotency and neuronal differentiation by association with chromatin modifiers and transcription factors. EMBO J 31(3):522–533 - PubMed
  122. Lin N, Chang KY, Li Z, Gates K, Rana ZA, Dang J et al (2014) An evolutionarily conserved long noncoding RNA TUNA controls pluripotency and neural lineage commitment. Mol Cell 53(6):1005–1019 - PubMed
  123. Vance KW, Sansom SN, Lee S, Chalei V, Kong L, Cooper SE et al (2014) The long non-coding RNA Paupar regulates the expression of both local and distal genes. EMBO J 33(4):296–311 - PubMed
  124. Zhang L, Xue Z, Yan J, Wang J, Liu Q, Jiang H (2019) LncRNA Riken-201 and Riken-203 modulates neural development by regulating the Sox6 through sequestering miRNAs. Cell Prolif 52(3):e12573 - PubMed
  125. Sauvageau M, Goff LA, Lodato S, Bonev B, Groff AF, Gerhardinger C et al (2013) Multiple knockout mouse models reveal lincRNAs are required for life and brain development. Elife 2:e01749 - PubMed
  126. Ramos AD, Andersen RE, Liu SJ, Nowakowski TJ, Hong SJ, Gertz C et al (2015) The long noncoding RNA Pnky regulates neuronal differentiation of embryonic and postnatal neural stem cells. Cell Stem Cell 16(4):439–447 - PubMed
  127. Bocchi VD, Conforti P, Vezzoli E, Besusso D, Cappadona C, Lischetti T et al (2021) The coding and long noncoding single-cell atlas of the developing human fetal striatum. Science 372:6542 - PubMed
  128. Grassi DA, Brattas PL, Jonsson ME, Atacho D, Karlsson O, Nolbrant S et al (2020) Profiling of lincRNAs in human pluripotent stem cell derived forebrain neural progenitor cells. Heliyon. 6(1):e03067 - PubMed
  129. Prajapati B, Fatma M, Maddhesiya P, Sodhi MK, Fatima M, Dargar T et al (2019) Identification and epigenetic analysis of divergent long non-coding RNAs in multilineage differentiation of human Neural Progenitor Cells. RNA Biol 16(1):13–24 - PubMed
  130. Rani N, Nowakowski TJ, Zhou H, Godshalk SE, Lisi V, Kriegstein AR et al (2016) A primate lncRNA mediates notch signaling during neuronal development by sequestering miRNA. Neuron 90(6):1174–1188 - PubMed
  131. Peschansky VJ, Pastori C, Zeier Z, Wentzel K, Velmeshev D, Magistri M et al (2016) The long non-coding RNA FMR4 promotes proliferation of human neural precursor cells and epigenetic regulation of gene expression in trans. Mol Cell Neurosci 74:49–57 - PubMed
  132. Liu SJ, Nowakowski TJ, Pollen AA, Lui JH, Horlbeck MA, Attenello FJ et al (2016) Single-cell analysis of long non-coding RNAs in the developing human neocortex. Genome Biol 17:67 - PubMed
  133. Field AR, Jacobs FMJ, Fiddes IT, Phillips APR, Reyes-Ortiz AM, LaMontagne E et al (2019) Structurally conserved primate LncRNAs are transiently expressed during human cortical differentiation and influence cell-type-specific genes. Stem Cell Rep 12(2):245–257 - PubMed
  134. 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 - PubMed
  135. Somel M, Liu X, Tang L, Yan Z, Hu H, Guo S et al (2011) MicroRNA-driven developmental remodeling in the brain distinguishes humans from other primates. PLoS Biol 9(12):e1001214 - PubMed
  136. Kosik KS (2009) MicroRNAs tell an evo-devo story. Nat Rev Neurosci 10(10):754–759 - PubMed
  137. Volvert ML, Rogister F, Moonen G, Malgrange B, Nguyen L (2012) MicroRNAs tune cerebral cortical neurogenesis. Cell Death Differ 19(10):1573–1581 - PubMed
  138. Saurat N, Andersson T, Vasistha NA, Molnar Z, Livesey FJ (2013) Dicer is required for neural stem cell multipotency and lineage progression during cerebral cortex development. Neural Dev 8:14 - PubMed
  139. 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(11):2800–2812 - PubMed
  140. De Pietri TD, 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(23):3911–3921 - PubMed
  141. Shu P, Wu C, Ruan X, Liu W, Hou L, Fu H et al (2019) Opposing gradients of microRNA expression temporally pattern layer formation in the developing neocortex. Dev Cell 49(5):764–854 - PubMed
  142. Fairchild CLA, Cheema SK, Wong J, Hino K, Simo S, La Torre A (2019) Let-7 regulates cell cycle dynamics in the developing cerebral cortex and retina. Sci Rep 9(1):15336 - PubMed
  143. Conaco C, Otto S, Han JJ, Mandel G (2006) Reciprocal actions of REST and a microRNA promote neuronal identity. Proc Natl Acad Sci USA 103(7):2422–2427 - PubMed
  144. Visvanathan J, Lee S, Lee B, Lee JW, Lee SK (2007) The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev 21(7):744–749 - PubMed
  145. Abdullah AI, Zhang H, Nie Y, Tang W, Sun T (2016) CDK7 and miR-210 co-regulate cell-cycle progression of neural progenitors in the developing neocortex. Stem Cell Rep 7(1):69–79 - PubMed
  146. Nigro A, Menon R, Bergamaschi A, Clovis YM, Baldi A, Ehrmann M et al (2012) MiR-30e and miR-181d control radial glia cell proliferation via HtrA1 modulation. Cell Death Disease. 3:e360 - PubMed
  147. 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(4):1184–1196 - PubMed
  148. Fededa JP, Esk C, Mierzwa B, Stanyte R, Yuan S, Zheng H et al (2016) MicroRNA-34/449 controls mitotic spindle orientation during mammalian cortex development. EMBO J 35(22):2386–2398 - PubMed
  149. Fineberg SK, Kosik KS, Davidson BL (2009) MicroRNAs potentiate neural development. Neuron 64(3):303–309 - PubMed
  150. Nowakowski TJ, Fotaki V, Pollock A, Sun T, Pratt T, Price DJ (2013) MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. Proc Natl Acad Sci USA 110(17):7056–7061 - PubMed
  151. Shu P, Fu H, Zhao X, Wu C, Ruan X, Zeng Y et al (2017) MicroRNA-214 modulates neural progenitor cell differentiation by targeting Quaking during cerebral cortex development. Sci Rep 7(1):8014 - PubMed
  152. 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(12):1305–1314 - PubMed
  153. Ghosh T, Aprea J, Nardelli J, Engel H, Selinger C, Mombereau 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(6):1779–1788 - PubMed
  154. Delaloy C, Liu L, Lee JA, Su H, Shen F, Yang GY et al (2010) MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6(4):323–335 - PubMed
  155. Boissart C, Nissan X, Giraud-Triboult K, Peschanski M, Benchoua A (2012) miR-125 potentiates early neural specification of human embryonic stem cells. Development 139(7):1247–1257 - PubMed
  156. Cimadamore F, Amador-Arjona A, Chen C, Huang CT, Terskikh AV (2013) SOX2-LIN28/let-7 pathway regulates proliferation and neurogenesis in neural precursors. Proc Natl Acad Sci USA 110(32):E3017–E3026 - PubMed
  157. Berezikov E (2011) Evolution of microRNA diversity and regulation in animals. Nat Rev Genet 12(12):846–860 - PubMed
  158. Arcila ML, Betizeau M, Cambronne XA, Guzman E, Doerflinger N, Bouhallier F et al (2014) Novel primate miRNAs coevolved with ancient target genes in germinal zone-specific expression patterns. Neuron 81(6):1255–1262 - PubMed
  159. Wang YM, Zheng YF, Yang SY, Yang ZM, Zhang LN, He YQ et al (2019) MicroRNA-197 controls ADAM10 expression to mediate MeCP2’s role in the differentiation of neuronal progenitors. Cell Death Differ 26(10):1863–1879 - PubMed
  160. Farahani R, Rezaei-Lotfi S, Simonian M, Hunter N (2019) Bi-modal reprogramming of cell cycle by MiRNA-4673 amplifies human neurogenic capacity. Cell Cycle 18(8):848–868 - PubMed
  161. Moore D, Meays BM, Madduri LSV, Shahjin F, Chand S, Niu M et al (2019) Downregulation of an evolutionary young mir-1290 in an ipsc-derived neural stem cell model of autism spectrum disorder. Stem Cells Int 2019:8710180 - PubMed
  162. Yelamanchili SV, Morsey B, Harrison EB, Rennard DA, Emanuel K, Thapa I et al (2014) The evolutionary young miR-1290 favors mitotic exit and differentiation of human neural progenitors through altering the cell cycle proteins. Cell Death Dis 5:e982 - PubMed
  163. Prodromidou K, Vlachos IS, Gaitanou M, Kouroupi G, Hatzigeorgiou AG, Matsas R (2020) MicroRNA-934 is a novel primate-specific small non-coding RNA with neurogenic function during early development. Elife 2020:9 - PubMed
  164. Greig LC, Woodworth MB, Galazo MJ, Padmanabhan H, Macklis JD (2013) Molecular logic of neocortical projection neuron specification, development and diversity. Nat Rev Neurosci 14(11):755–769 - PubMed
  165. Diaz JL, Siththanandan VB, Lu V, Gonzalez-Nava N, Pasquina L, MacDonald JL et al (2020) An evolutionarily acquired microRNA shapes development of mammalian cortical projections. Proc Natl Acad Sci USA 117(46):29113–29122 - PubMed
  166. Rodriques SG, Stickels RR, Goeva A, Martin CA, Murray E, Vanderburg CR et al (2019) Slide-seq: A scalable technology for measuring genome-wide expression at high spatial resolution. Science 363(6434):1463–1467 - PubMed
  167. Spanjaard B, Hu B, Mitic N, Olivares-Chauvet P, Janjuha S, Ninov N et al (2018) Simultaneous lineage tracing and cell-type identification using CRISPR-Cas9-induced genetic scars. Nat Biotechnol 36(5):469–473 - PubMed
  168. Alemany A, Florescu M, Baron CS, Peterson-Maduro J, van Oudenaarden A (2018) Whole-organism clone tracing using single-cell sequencing. Nature 556(7699):108–112 - PubMed
  169. Frieda KL, Linton JM, Hormoz S, Choi J, Chow KK, Singer ZS et al (2017) Synthetic recording and in situ readout of lineage information in single cells. Nature 541(7635):107–111 - PubMed
  170. Lancaster MA, Renner M, Martin CA, Wenzel D, Bicknell LS, Hurles ME et al (2013) Cerebral organoids model human brain development and microcephaly. Nature 501(7467):373–379 - PubMed
  171. Qian X, Nguyen HN, Song MM, Hadiono C, Ogden SC, Hammack C et al (2016) Brain-region-specific organoids using mini-bioreactors for modeling ZIKV exposure. Cell 165(5):1238–1254 - PubMed
  172. Amiri A, Coppola G, Scuderi S, Wu F, Roychowdhury T, Liu F et al (2018) Transcriptome and epigenome landscape of human cortical development modeled in organoids. Science 362:6420 - PubMed
  173. Luo C, Lancaster MA, Castanon R, Nery JR, Knoblich JA, Ecker JR (2016) Cerebral organoids recapitulate epigenomic signatures of the human fetal brain. Cell Rep 17(12):3369–3384 - PubMed
  174. Mariani J, Coppola G, Zhang P, Abyzov A, Provini L, Tomasini L et al (2015) FOXG1-dependent dysregulation of GABA/glutamate neuron differentiation in autism spectrum disorders. Cell 162(2):375–390 - PubMed
  175. Velasco S, Kedaigle AJ, Simmons SK, Nash A, Rocha M, Quadrato G et al (2019) Individual brain organoids reproducibly form cell diversity of the human cerebral cortex. Nature 570(7762):523–527 - PubMed
  176. Bhaduri A, Andrews MG, Kriegstein AR, Nowakowski TJ (2020) Are organoids ready for prime time? Cell Stem Cell 27(3):361–365 - PubMed
  177. Bhaduri A, Andrews MG, Mancia Leon W, Jung D, Shin D, Allen D et al (2020) Cell stress in cortical organoids impairs molecular subtype specification. Nature 578(7793):142–148 - PubMed
  178. Qian X, Su Y, Adam CD, Deutschmann AU, Pather SR, Goldberg EM et al (2020) Sliced human cortical organoids for modeling distinct cortical layer formation. Cell Stem Cell 26(5):766-81e9 - PubMed
  179. Giandomenico SL, Sutcliffe M, Lancaster MA (2021) Generation and long-term culture of advanced cerebral organoids for studying later stages of neural development. Nat Protoc 16(2):579–602 - PubMed
  180. Gordon A, Yoon SJ, Tran SS, Makinson CD, Park JY, Andersen J et al (2021) Long-term maturation of human cortical organoids matches key early postnatal transitions. Nat Neurosci - PubMed
  181. Xiang Y, Tanaka Y, Cakir B, Patterson B, Kim KY, Sun P et al (2019) hESC-derived thalamic organoids form reciprocal projections when fused with cortical organoids. Cell Stem Cell 24(3):487-97e7 - PubMed
  182. Birey F, Andersen J, Makinson CD, Islam S, Wei W, Huber N et al (2017) Assembly of functionally integrated human forebrain spheroids. Nature 545(7652):54–59 - PubMed
  183. Xiang Y, Tanaka Y, Patterson B, Kang YJ, Govindaiah G, Roselaar N et al (2017) Fusion of regionally specified hPSC-derived organoids models human brain development and interneuron migration. Cell Stem Cell 21(3):383-98e7 - PubMed
  184. Andersen J, Revah O, Miura Y, Thom N, Amin ND, Kelley KW et al (2020) Generation of functional human 3D cortico-motor assembloids. Cell 183(7):1913-29e26 - PubMed

Publication Types

Grant support