Differences and similarities between human and chimpanzee neural progenitors during cerebral cortex development.
Human neocortex expansion likely contributed to the remarkable cognitive abilities of humans. This expansion is thought to primarily reflect differences in proliferationversusdifferentiation of neural progenitors during cortical development. Here, we have searched for such differences by analysing cerebral organoids from human and chimpanzees using immunohistofluorescence, live imaging, and single-cell transcriptomics. We find that the cytoarchitecture, cell type composition, and neurogenic gene expression programs of humans and chimpanzees are remarkably similar. Notably, however, live imaging of apical progenitor mitosis uncovered a lengthening of prometaphase-metaphase in humans compared to chimpanzees that is specific to proliferating progenitors and not observed in non-neural cells. Consistent with this, the small set of genes more highly expressed in human apical progenitors points to increased proliferative capacity, and the proportion of neurogenic basal progenitors is lower in humans. These subtle differences in cortical progenitors between humans and chimpanzees may have consequences for human neocortex evolution.
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Felipe
F
Mora-Bermúdez
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Farhath
F
Badsha
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Sabina
S
Kanton
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
J Gray
JG
Camp
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Benjamin
B
Vernot
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Kathrin
K
Köhler
Institute of Laboratory Animals, Graduate School of Medicine, Kyoto University, Kyoto, Japan.
Birger
B
Voigt
Department of Reprogramming Science, Center for iPS Cell Research and Application, Kyoto University, Kyoto, Japan.
Keisuke
K
Okita
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Tomislav
T
Maricic
CAS-MPG Partner Institute for Computational Biology, Shanghai, China.
Zhisong
Z
He
Universitätsklinikum Carl Gustav Carus, Klinik und Poliklinik für Frauenheilkunde und Geburtshilfe, Technische Universität Dresden, Dresden, Germany.
Robert
R
Lachmann
Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Svante
S
Pääbo
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.|Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.
Barbara
B
Treutlein
Max Planck Institute of Molecular Cell Biology and Genetics, Dresden, Germany.
Wieland B
0000-0003-4143-7201
WB
Huttner
D000818:Animals; D049109:Cell Proliferation; D002540:Cerebral Cortex / Q000196:embryology*; D020869:Gene Expression Profiling; D006801:Humans; D000069416:Intravital Microscopy; D008856:Microscopy, Fluorescence; D008938:Mitosis; D058953:Neural Stem Cells / Q000502:physiology*; D009940:Organoids / Q000254:growth & development; D002679:Pan troglodytes; D059010:Single-Cell Analysis
cell biology; cell division; cerebral organoids; chimpanzee; cortical development; developmental biology; human; mouse; neural stem and progenitor cells; single-cell RNA-seq; stem cells
Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3196-201
14963232
Nat Protoc. 2012 Mar 01;7(3):562-78
22383036
Bioinformatics. 2015 Mar 1;31(5):770-2
25359895
RNA. 2014 Jul;20(7):1103-11
24847104
Nat Biotechnol. 2014 Apr;32(4):381-386
24658644
Annu Rev Cell Dev Biol. 2014;30:465-502
25000993
Bioinformatics. 2013 May 1;29(9):1208-9
23471300
Bioinformatics. 2015 Jan 15;31(2):166-9
25260700
Nat Rev Neurosci. 2009 Oct;10(10):724-35
19763105
Proc Natl Acad Sci U S A. 2015 Dec 22;112(51):15672-7
26644564
Cell Stem Cell. 2016 Apr 7;18(4):467-80
27049876
Nature. 2013 Jul 25;499(7459):481-4
23823721
Cell. 2015 May 21;161(5):1202-1214
26000488
Stem Cells. 2013 Mar;31(3):458-66
23193063
Nature. 2014 Jul 10;511(7508):177-83
25008523
Dev Growth Differ. 2012 Apr;54(3):277-86
22524601
Curr Protoc Immunol. 2007 Feb;Chapter 7:7.22.1-7.22.4
18432996
Nat Protoc. 2009;4(1):44-57
19131956
Front Hum Neurosci. 2013 Aug 01;7:424
23914167
Nat Rev Mol Cell Biol. 2005 Oct;6(10):777-88
16314867
Dev Neurobiol. 2012 Jul;72(7):955-71
22684946
Methods. 2007 Feb;41(2):158-67
17189858
Elife. 2014 Jul 04;3:
24996848
Nat Protoc. 2014 Oct;9(10):2329-40
25188634
Nature. 2013 Nov 28;503(7477):525-529
24153179
Neuron. 2013 Oct 30;80(3):633-47
24183016
Development. 2014 Jun;141(11):2182-94
24866113
Proc Natl Acad Sci U S A. 2013 Dec 10;110(50):20284-9
24277810
PLoS Biol. 2014 Nov 18;12(11):e1002000
25405475
EMBO J. 2004 Jun 2;23(11):2314-24
15141162
Curr Opin Neurobiol. 2012 Oct;22(5):737-46
22554882
Nature. 2013 Sep 19;501(7467):373-9
23995685
Nat Methods. 2014 Jul;11(7):740-2
24836921
Nat Commun. 2011 Jan 11;2:154
21224845
Anat Rec. 1970 Feb;166(2):257-61
5414696
Cell. 2015 Jul 16;162(2):375-390
26186191
J Neurocytol. 1989 Jun;18(3):311-8
2746304
Neuron. 2015 Feb 18;85(4):683-94
25695268
Front Hum Neurosci. 2009 Nov 09;3:31
19915731
Nat Cell Biol. 2008 Jan;10(1):93-101
18084280
Cell. 2016 May 19;165(5):1238-1254
27118425
Annu Rev Neurosci. 2009;32:149-84
19555289
Mol Biol Cell. 2015 Dec 1;26(24):4302-6
26628750
Bioinformatics. 2013 Jan 1;29(1):15-21
23104886
Nature. 2014 May 15;509(7500):371-5
24739965
Methods. 2015 Sep 1;85:54-61
26142758
Nucleic Acids Res. 2014 Oct;42(18):e141
25100869
Cell. 2011 Jul 8;146(1):18-36
21729779
Neuron. 2016 Jan 6;89(1):83-99
26748089
Proc Natl Acad Sci U S A. 2012 Jul 17;109(29):11836-41
22753484
Science. 2015 Mar 27;347(6229):1465-70
25721503
Proc Natl Acad Sci U S A. 1999 Apr 13;96(8):4639-44
10200315
Cereb Cortex. 2002 Jan;12(1):37-53
11734531
Nat Rev Mol Cell Biol. 2007 May;8(5):379-93
17426725