1932

Abstract

“What makes us human?” is a central question of many research fields, notably anthropology. In this review, we focus on the development of the human neocortex, the part of the brain with a key role in cognition, to gain neurobiological insight toward answering this question. We first discuss cortical stem and progenitor cells and human-specific genes that affect their behavior. We thus aim to understand the molecular foundation of the expansion of the neocortex that occurred in the course of human evolution, as this expansion is generally thought to provide a basis for our unique cognitive abilities. We then review the emerging evidence pointing to differences in the development of the neocortex between present-day humans and Neanderthals, our closest relatives. Finally, we discuss human-specific genes that have been implicated in neuronal circuitry and offer a perspective for future studies addressing the question of what makes us human.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-112122-032521
2024-10-02
2025-06-12
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/40/1/annurev-cellbio-112122-032521.html?itemId=/content/journals/10.1146/annurev-cellbio-112122-032521&mimeType=html&fmt=ahah

Literature Cited

  1. Alcantara D, O'Driscoll M. 2014.. Congenital microcephaly. . Am. J. Med. Genet. C 166:(2):12439
    [Crossref] [Google Scholar]
  2. Andrews MG, Subramanian L, Salma J, Kriegstein AR. 2022.. How mechanisms of stem cell polarity shape the human cerebral cortex. . Nat. Rev. Neurosci. 23::71124
    [Crossref] [Google Scholar]
  3. Antonacci F, Dennis MY, Huddleston J, Sudmant PH, Steinberg KM, et al. 2014.. Palindromic GOLGA8 core duplicons promote chromosome 15q13.3 microdeletion and evolutionary instability. . Nat. Genet. 46::1293302
    [Crossref] [Google Scholar]
  4. Azevedo FAC, Carvalho LRB, Grinberg LT, Farfel JM, Ferretti REL, et al. 2009.. Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. . J. Comp. Neurol. 513::53241
    [Crossref] [Google Scholar]
  5. Benito-Kwiecinski S, Giandomenico SL, Sutcliffe M, Riis ES, Freire-Pritchett P, et al. 2021.. An early cell shape transition drives evolutionary expansion of the human forebrain. . Cell 184::2084102.e19
    [Crossref] [Google Scholar]
  6. Bilgic M, Wu Q, Suetsugu T, Shitamukai A, Tsunekawa Y, et al. 2023.. Truncated radial glia as a common precursor in the late corticogenesis of gyrencephalic mammals. . eLife 12::RP91406
    [Crossref] [Google Scholar]
  7. Charrier C, Joshi K, Coutinho-Budd J, Kim JE, Lambert N, et al. 2012.. Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. . Cell 149::92335
    [Crossref] [Google Scholar]
  8. Coy JF, Dressler D, Wilde J, Schubert P. 2005.. Mutations in the transketolase-like gene TKTL1: clinical implications for neurodegenerative diseases, diabetes and cancer. . Clin. Lab. 51::25773
    [Google Scholar]
  9. Dehay C, Kennedy H, Kosik KS. 2015.. The outer subventricular zone and primate-specific cortical complexification. . Neuron 85::68394
    [Crossref] [Google Scholar]
  10. del Alamo D, Rouault H, Schweisguth F. 2011.. Mechanism and significance of cis-inhibition in Notch signalling. . Curr. Biol. 21::R4047
    [Crossref] [Google Scholar]
  11. Dennis MY, Eichler EE. 2016.. Human adaptation and evolution by segmental duplication. . Curr. Opin. Genet. Dev. 41::4452
    [Crossref] [Google Scholar]
  12. Dennis MY, Nuttle X, Sudmant PH, Antonacci F, Graves TA, et al. 2012.. Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. . Cell 149::91222
    [Crossref] [Google Scholar]
  13. DeSilva JM, Traniello JFA, Claxton AG, Fannin LD. 2021.. When and why did human brains decrease in size? a new change-point analysis and insights from brain evolution in ants. . Front. Ecol. Evol. 9::742639
    [Crossref] [Google Scholar]
  14. Diaz-Moralli S, Aguilar E, Marin S, Coy JF, Dewerchin M, et al. 2016.. A key role for transketolase-like 1 in tumor metabolic reprogramming. . Oncotarget 7::5187597
    [Crossref] [Google Scholar]
  15. Fiddes IT, Lodewijk GA, Mooring M, Bosworth CM, Ewing AD, et al. 2018.. Human-specific NOTCH2NL genes affect notch signaling and cortical neurogenesis. . Cell 173::135669.e22
    [Crossref] [Google Scholar]
  16. Fiddes IT, Pollen AA, Davis JM, Sikela JM. 2019.. Paired involvement of human-specific Olduvai domains and NOTCH2NL genes in human brain evolution. . Hum. Genet. 138::71521
    [Crossref] [Google Scholar]
  17. 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::69099
    [Crossref] [Google Scholar]
  18. Fietz SA, Lachmann R, Brandl H, Kircher M, Samusik N, et al. 2012.. Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal. . PNAS 109::1183641
    [Crossref] [Google Scholar]
  19. Fischer J, Fernández Ortuño E, Marsoner F, Artioli A, Peters J, et al. 2022.. Human-specific ARHGAP11B ensures human-like basal progenitor levels in hominid cerebral organoids. . EMBO Rep. 23::e54728
    [Crossref] [Google Scholar]
  20. Florio M, Albert M, Taverna E, Namba T, Brandl H, et al. 2015.. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. . Science 347::146570
    [Crossref] [Google Scholar]
  21. Florio M, Heide M, Pinson A, Brandl H, Albert M, et al. 2018.. Evolution and cell-type specificity of human-specific genes preferentially expressed in progenitors of fetal neocortex. . eLife 7::e32332
    [Crossref] [Google Scholar]
  22. Florio M, Namba T, Pääbo S, Hiller M, Huttner WB. 2016.. A single splice site mutation in human-specific ARHGAP11B causes basal progenitor amplification. . Sci. Adv. 2::e1601941
    [Crossref] [Google Scholar]
  23. Foley EA, Kapoor TM. 2013.. Microtubule attachment and spindle assembly checkpoint signalling at the kinetochore. . Nat. Rev. Mol. Cell Biol. 14::2537
    [Crossref] [Google Scholar]
  24. Fossati M, Pizzarelli R, Schmidt ER, Kupferman JV, Stroebel D, et al. 2016.. SRGAP2 and its human-specific paralog co-regulate the development of excitatory and inhibitory synapses. . Neuron 91::35669
    [Crossref] [Google Scholar]
  25. Galakhova AA, Hunt S, Wilbers R, Heyer DB, de Kock CPJ, et al. 2022.. Evolution of cortical neurons supporting human cognition. . Trends Cogn. Sci. 26::90922
    [Crossref] [Google Scholar]
  26. Ganapathee DS, Gunz P. 2023.. Insights into brain evolution through the genotype-phenotype connection. . Prog. Brain Res. 275::7392
    [Crossref] [Google Scholar]
  27. Gilmore EC, Walsh CA. 2013.. Genetic causes of microcephaly and lessons for neuronal development. . Wiley Interdiscip. Rev. Dev. Biol. 2::46178
    [Crossref] [Google Scholar]
  28. Gkini V, Namba T. 2023.. Glutaminolysis and the control of neural progenitors in neocortical development and evolution. . Neuroscientist 29::17789
    [Crossref] [Google Scholar]
  29. Gonda Y, Namba T, Hanashima C. 2020.. Beyond axon guidance: roles of Slit-Robo signaling in neocortical formation. . Front. Cell Dev. Biol. 8::607415
    [Crossref] [Google Scholar]
  30. Grohmanova K, Schlaepfer D, Hess D, Gutierrez P, Beck M, Kroschewski R. 2004.. Phosphorylation of IQGAP1 modulates its binding to Cdc42, revealing a new type of Rho-GTPase regulator. . J. Biol. Chem. 279::48495504
    [Crossref] [Google Scholar]
  31. Guerrier S, Coutinho-Budd J, Sassa T, Gresset A, Jordan NV, et al. 2009.. The F-BAR domain of srGAP2 induces membrane protrusions required for neuronal migration and morphogenesis. . Cell 138::9901004
    [Crossref] [Google Scholar]
  32. Heide M, Haffner C, Murayama A, Kurotaki Y, Shinohara H, et al. 2020.. Human-specific ARHGAP11B increases size and folding of primate neocortex in the fetal marmoset. . Science 369::54650
    [Crossref] [Google Scholar]
  33. Herai R, Semendeferi K, Muotri AR. 2023.. Comment on “Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals. .” Science 379::eadf0602
    [Crossref] [Google Scholar]
  34. Herai RH, Szeto RA, Trujillo CA, Muotri AR. 2021.. Response to comment on “Reintroduction of the archaic variant of NOVA1 in cortical organoids alters neurodevelopment. .” Science 374::eabi9881
    [Crossref] [Google Scholar]
  35. Herculano-Houzel S. 2009.. The human brain in numbers: a linearly scaled-up primate brain. . Front. Hum. Neurosci. 3::31
    [Crossref] [Google Scholar]
  36. Herculano-Houzel S. 2012.. The remarkable, yet not extraordinary, human brain as a scaled-up primate brain and its associated cost. . PNAS 109:(Suppl. 1):1066168
    [Crossref] [Google Scholar]
  37. Hodzic D, Kong C, Wainszelbaum MJ, Charron AJ, Su X, Stahl PD. 2006.. TBC1D3, a hominoid oncoprotein, is encoded by a cluster of paralogues located on chromosome 17q12. . Genomics 88::73136
    [Crossref] [Google Scholar]
  38. Holland AJ, Cleveland DW. 2012.. Losing balance: the origin and impact of aneuploidy in cancer. . EMBO Rep. 13::50114
    [Crossref] [Google Scholar]
  39. Hou QQ, Xiao Q, Sun XY, Ju XC, Luo ZG. 2021.. TBC1D3 promotes neural progenitor proliferation by suppressing the histone methyltransferase G9a. . Sci. Adv. 7::eaba8053
    [Crossref] [Google Scholar]
  40. Huttner WB, ed. 2023.. Neocortical Neurogenesis in Development and Evolution. Hoboken, NJ:: Wiley
    [Google Scholar]
  41. Jayaraman D, Bae BI, Walsh CA. 2018.. The genetics of primary microcephaly. . Annu. Rev. Genom. Hum. Genet. 19::177200
    [Crossref] [Google Scholar]
  42. Jiang Z, Tang H, Ventura M, Cardone MF, Marques-Bonet T, et al. 2007.. Ancestral reconstruction of segmental duplications reveals punctuated cores of human genome evolution. . Nat. Genet. 39::136168
    [Crossref] [Google Scholar]
  43. Johnson M, Sharma M, Brocardo MG, Henderson BR. 2011.. IQGAP1 translocates to the nucleus in early S-phase and contributes to cell cycle progression after DNA replication arrest. . Int. J. Biochem. Cell Biol. 43::6573
    [Crossref] [Google Scholar]
  44. Ju XC, Hou QQ, Sheng AL, Wu KY, Zhou Y, et al. 2016.. The hominoid-specific gene TBC1D3 promotes generation of basal neural progenitors and induces cortical folding in mice. . eLife 5::e18197
    [Crossref] [Google Scholar]
  45. Kagawa Y, Matsumoto S, Kamioka Y, Mimori K, Naito Y, et al. 2013.. Cell cycle–dependent Rho GTPase activity dynamically regulates cancer cell motility and invasion in vivo. . PLOS ONE 8::e83629
    [Crossref] [Google Scholar]
  46. Kaindl AM, Passemard S, Kumar P, Kraemer N, Issa L, et al. 2010.. Many roads lead to primary autosomal recessive microcephaly. . Prog. Neurobiol. 90::36383
    [Crossref] [Google Scholar]
  47. Kalebic N, Gilardi C, Albert M, Namba T, Long KR, et al. 2018.. Human-specific ARHGAP11B induces hallmarks of neocortical expansion in developing ferret neocortex. . eLife 7::e41241
    [Crossref] [Google Scholar]
  48. Kalebic N, Gilardi C, Stepien B, Wilsch-Bräuninger M, Long KR, et al. 2019.. Neocortical expansion due to increased proliferation of basal progenitors is linked to changes in their morphology. . Cell Stem Cell 24::53550.e9
    [Crossref] [Google Scholar]
  49. Kalebic N, Namba T. 2021.. Inheritance and flexibility of cell polarity: a clue for understanding human brain development and evolution. . Development 148::dev199417
    [Crossref] [Google Scholar]
  50. Kanton S, Boyle MJ, He ZS, Santel M, Weigert A, et al. 2019.. Organoid single-cell genomic atlas uncovers human-specific features of brain development. . Nature 574::41822
    [Crossref] [Google Scholar]
  51. Karakostis FA, Haeufle D, Anastopoulou I, Moraitis K, Hotz G, et al. 2021.. Biomechanics of the human thumb and the evolution of dexterity. . Curr. Biol. 31::131725.e8
    [Crossref] [Google Scholar]
  52. 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::46981
    [Crossref] [Google Scholar]
  53. Kriegstein AR, Götz M. 2003.. Radial glia diversity: a matter of cell fate. . Glia 43::3743
    [Crossref] [Google Scholar]
  54. Kuhlwilm M, Boeckx C. 2019.. A catalog of single nucleotide changes distinguishing modern humans from archaic hominins. . Sci. Rep. 9::8463
    [Crossref] [Google Scholar]
  55. Kurella VB, Richard JM, Parke CL, Lecour LF Jr., Bellamy HD, Worthylake DK. 2009.. Crystal structure of the GTPase-activating protein–related domain from IQGAP1. . J. Biol. Chem. 284::1485765
    [Crossref] [Google Scholar]
  56. Kuroda S, Fukata M, Nakagawa M, Fujii K, Nakamura T, et al. 1998.. Role of IQGAP1, a target of the small GTPases Cdc42 and Rac1, in regulation of E-cadherin-mediated cell-cell adhesion. . Science 281::83235
    [Crossref] [Google Scholar]
  57. Liu J, Liu W, Yang L, Wu Q, Zhang H, et al. 2017.. The primate-specific gene TMEM14B marks outer radial glia cells and promotes cortical expansion and folding. . Cell Stem Cell 21::63549.e8
    [Crossref] [Google Scholar]
  58. Marchetto MC, Hrvoj-Mihic B, Kerman BE, Yu DX, Vadodaria KC, et al. 2019.. Species-specific maturation profiles of human, chimpanzee and bonobo neural cells. . eLife 8::e37527
    [Crossref] [Google Scholar]
  59. Maricic T, Helmbrecht N, Riesenberg S, Macak D, Kanis P, et al. 2021.. Comment on “Reintroduction of the archaic variant of NOVA1 in cortical organoids alters neurodevelopment. .” Science 374::eabi6060
    [Crossref] [Google Scholar]
  60. Martins PT, Marí M, Boeckx C. 2018.. SRGAP2 and the gradual evolution of the modern human language faculty. . J. Lang. Evol. 3::6778
    [Crossref] [Google Scholar]
  61. Mefford HC, Sharp AJ, Baker C, Itsara A, Jiang Z, et al. 2008.. Recurrent rearrangements of chromosome 1q21.1 and variable pediatric phenotypes. . N. Engl. J. Med. 359::168599
    [Crossref] [Google Scholar]
  62. Meyer M, Kircher M, Gansauge MT, Li H, Racimo F, et al. 2012.. A high-coverage genome sequence from an archaic Denisovan individual. . Science 338::22226
    [Crossref] [Google Scholar]
  63. 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
    [Crossref] [Google Scholar]
  64. Mora-Bermúdez F, Kanis P, Macak D, Peters J, Naumann R, et al. 2022.. Longer metaphase and fewer chromosome segregation errors in modern human than Neanderthal brain development. . Sci. Adv. 8::eabn7702
    [Crossref] [Google Scholar]
  65. Musacchio A, Desai A. 2017.. A molecular view of kinetochore assembly and function. . Biology 6::5
    [Crossref] [Google Scholar]
  66. Musacchio A, Salmon ED. 2007.. The spindle-assembly checkpoint in space and time. . Nat. Rev. Mol. Cell Biol. 8::37993
    [Crossref] [Google Scholar]
  67. Namba T, Doczi J, Pinson A, Xing L, Kalebic N, et al. 2020.. Human-specific ARHGAP11B acts in mitochondria to expand neocortical progenitors by glutaminolysis. . Neuron 105::86781
    [Crossref] [Google Scholar]
  68. Namba T, Funahashi Y, Nakamuta S, Xu C, Takano T, Kaibuchi K. 2015.. Extracellular and intracellular signaling for neuronal polarity. . Physiol. Rev. 95::9951024
    [Crossref] [Google Scholar]
  69. Namba T, Huttner WB. 2017.. Neural progenitor cells and their role in the development and evolutionary expansion of the neocortex. . Wiley Interdiscip. Rev. Dev. Biol. 6::e256
    [Crossref] [Google Scholar]
  70. Namba T, Kibe Y, Funahashi Y, Nakamuta S, Takano T, et al. 2014.. Pioneering axons regulate neuronal polarization in the developing cerebral cortex. . Neuron 81::81429
    [Crossref] [Google Scholar]
  71. Namba T, Nardelli J, Gressens P, Huttner WB. 2021.. Metabolic regulation of neocortical expansion in development and evolution. . Neuron 109::40819
    [Crossref] [Google Scholar]
  72. Neubauer S, Hublin JJ, Gunz P. 2018.. The evolution of modern human brain shape. . Sci. Adv. 4::eaao5961
    [Crossref] [Google Scholar]
  73. Noritake J, Watanabe T, Sato K, Wang S, Kaibuchi K. 2005.. IQGAP1: a key regulator of adhesion and migration. . J. Cell Sci. 118::208592
    [Crossref] [Google Scholar]
  74. 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::121927
    [Crossref] [Google Scholar]
  75. Phan TP, Holland AJ. 2021.. Time is of the essence: the molecular mechanisms of primary microcephaly. . Genes Dev. 35::155178
    [Crossref] [Google Scholar]
  76. Pilaz LJ, Liu J, Joshi K, Tsunekawa Y, Musso CM, et al. 2023.. Subcellular mRNA localization and local translation of Arhgap11a in radial glial progenitors regulates cortical development. . Neuron 111::83956.e5
    [Crossref] [Google Scholar]
  77. Pinson A, Maricic T, Zeberg H, Pääbo S, Huttner WB. 2023.. Response to comment on “Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals. .” Science 379::eadf2212
    [Crossref] [Google Scholar]
  78. Pinson A, Xing L, Namba T, Kalebic N, Peters J, et al. 2022.. Human TKTL1 implies greater neurogenesis in frontal neocortex of modern humans than Neanderthals. . Science 377::eabl6422
    [Crossref] [Google Scholar]
  79. Prüfer K, de Filippo C, Grote S, Mafessoni F, Korlevic P, et al. 2017.. A high-coverage Neandertal genome from Vindija Cave in Croatia. . Science 358::65558
    [Crossref] [Google Scholar]
  80. Prüfer K, Racimo F, Patterson N, Jay F, Sankararaman S, et al. 2014.. The complete genome sequence of a Neanderthal from the Altai Mountains. . Nature 505::4349
    [Crossref] [Google Scholar]
  81. Rakic P. 1988.. Specification of cerebral cortical areas. . Science 241::17076
    [Crossref] [Google Scholar]
  82. Rakic P. 1999.. Introduction to the session. . Ann. N. Y. Acad. Sci. 882::6667
    [Crossref] [Google Scholar]
  83. Rakic P. 2000.. Radial unit hypothesis of neocortical expansion. . Novartis Found. Symp. 228::3042
    [Crossref] [Google Scholar]
  84. Rakic P. 2009.. Evolution of the neocortex: a perspective from developmental biology. . Nat. Rev. Neurosci. 10::72435
    [Crossref] [Google Scholar]
  85. Reardon S. 2022.. Did this gene give modern human brains their edge?. Nature 609::66566
    [Crossref] [Google Scholar]
  86. Rosenfeld JA, Traylor RN, Schaefer GB, McPherson EW, Ballif BC, et al. 2012.. Proximal microdeletions and microduplications of 1q21.1 contribute to variable abnormal phenotypes. . Eur. J. Hum. Genet. 20::75461
    [Crossref] [Google Scholar]
  87. Ruff CB, Trinkaus E, Holliday TW. 1997.. Body mass and encephalization in Pleistocene Homo. . Nature 387::17376
    [Crossref] [Google Scholar]
  88. Schenk G, Duggleby RG, Nixon PF. 1998.. Properties and functions of the thiamin diphosphate dependent enzyme transketolase. . Int. J. Biochem. Cell Biol. 30::1297318
    [Crossref] [Google Scholar]
  89. Schmidt ERE, Kupferman JV, Stackmann M, Polleux F. 2019.. The human-specific paralogs SRGAP2B and SRGAP2C differentially modulate SRGAP2A-dependent synaptic development. . Sci. Rep. 9::18692
    [Crossref] [Google Scholar]
  90. Schörnig M, Ju X, Fast L, Ebert S, Weigert A, et al. 2021.. Comparison of induced neurons reveals slower structural and functional maturation in humans than in apes. . eLife 10::e59323
    [Crossref] [Google Scholar]
  91. Shashidharan P, Plaitakis A. 2014.. The discovery of human of GLUD2 glutamate dehydrogenase and its implications for cell function in health and disease. . Neurochem. Res. 39::46070
    [Crossref] [Google Scholar]
  92. 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::3753
    [Crossref] [Google Scholar]
  93. Somel M, Franz H, Yan Z, Lorenc A, Guo S, et al. 2009.. Transcriptional neoteny in the human brain. . PNAS 106::574348
    [Crossref] [Google Scholar]
  94. Spanaki C, Zaganas I, Kleopa KA, Plaitakis A. 2010.. Human GLUD2 glutamate dehydrogenase is expressed in neural and testicular supporting cells. . J. Biol. Chem. 285::1674856
    [Crossref] [Google Scholar]
  95. Stephan H, Frahm H, Baron G. 1981.. New and revised data on volumes of brain structures in insectivores and primates. . Folia Primatol. 35::129
    [Crossref] [Google Scholar]
  96. Sudmant PH, Kitzman JO, Antonacci F, Alkan C, Malig M, et al. 2010.. Diversity of human copy number variation and multicopy genes. . Science 330::64146
    [Crossref] [Google Scholar]
  97. Suzuki IK, Gacquer D, Van Heurck R, Kumar D, Wojno M, et al. 2018.. Human-specific NOTCH2NL genes expand cortical neurogenesis through Delta/Notch regulation. . Cell 173::137084
    [Crossref] [Google Scholar]
  98. Tachibana M, Ueda J, Fukuda M, Takeda N, Ohta T, et al. 2005.. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. . Genes Dev. 19::81526
    [Crossref] [Google Scholar]
  99. Tahirovic S, Hellal F, Neukirchen D, Hindges R, Garvalov BK, et al. 2010.. Rac1 regulates neuronal polarization through the WAVE complex. . J. Neurosci. 30::693043
    [Crossref] [Google Scholar]
  100. Taverna E, Götz M, Huttner WB. 2014.. The cell biology of neurogenesis: toward an understanding of the development and evolution of the neocortex. . Annu. Rev. Cell Dev. Biol. 30::465502
    [Crossref] [Google Scholar]
  101. Trujillo CA, Rice ES, Schaefer NK, Chaim IA, Wheeler EC, et al. 2021.. Reintroduction of the archaic variant of NOVA1 in cortical organoids alters neurodevelopment. . Science 371::eaax2537
    [Crossref] [Google Scholar]
  102. Vaid S, Camp JG, Hersemann L, Oegema CE, Heninger AK, et al. 2018.. A novel population of Hopx-dependent basal radial glial cells in the developing mouse neocortex. . Development 145::dev169276
    [Crossref] [Google Scholar]
  103. Vanderhaeghen P, Polleux F. 2023.. Developmental mechanisms underlying the evolution of human cortical circuits. . Nat. Rev. Neurosci. 24::21332
    [Crossref] [Google Scholar]
  104. Wang L, Pang K, Zhou L, Cebrian-Silla A, Gonzalez-Granero S, et al. 2023.. A cross-species proteomic map reveals neoteny of human synapse development. . Nature 622::11219
    [Crossref] [Google Scholar]
  105. Wang X, Tsai JW, LaMonica B, Kriegstein AR. 2011.. A new subtype of progenitor cell in the mouse embryonic neocortex. . Nat. Neurosci. 14::55561
    [Crossref] [Google Scholar]
  106. Watanabe T, Wang S, Kaibuchi K. 2015.. IQGAPs as key regulators of actin-cytoskeleton dynamics. . Cell Struct. Funct. 40::6977
    [Crossref] [Google Scholar]
  107. Wilsch-Bräuninger M, Peters J, Paridaen JTML, Huttner WB. 2012.. Basolateral rather than apical primary cilia on neuroepithelial cells committed to delamination. . Development 139::95105
    [Crossref] [Google Scholar]
  108. Xing L, Gkini V, Nieminen AI, Zhou H-C, Aquilino M, . 2024.. Functional synergy of a human-specific and an ape-specific metabolic regulator in human neocortex development. . Nat. Commun. 15::3468
    [Crossref] [Google Scholar]
  109. Xing L, Kubik-Zahorodna A, Namba T, Pinson A, Florio M, et al. 2021.. Expression of human-specific ARHGAP11B in mice leads to neocortex expansion and increased memory flexibility. . EMBO J. 40::e107093
    [Crossref] [Google Scholar]
  110. Xu J, Zhou X, Wang J, Li Z, Kong X, et al. 2013.. RhoGAPs attenuate cell proliferation by direct interaction with p53 tetramerization domain. . Cell Rep. 3::152638
    [Crossref] [Google Scholar]
  111. Yang L, Venneti S, Nagrath D. 2017.. Glutaminolysis: a hallmark of cancer metabolism. . Annu. Rev. Biomed. Eng. 19::16394
    [Crossref] [Google Scholar]
  112. Zanin E, Desai A, Poser I, Toyoda Y, Andree C, et al. 2013.. A conserved RhoGAP limits M phase contractility and coordinates with microtubule asters to confine RhoA during cytokinesis. . Dev. Cell 26::496510
    [Crossref] [Google Scholar]
  113. Zaqout S, Kaindl AM. 2022.. Autosomal recessive primary microcephaly: not just a small brain. . Front. Cell Dev. Biol. 9::784700
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-cellbio-112122-032521
Loading
/content/journals/10.1146/annurev-cellbio-112122-032521
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error