Self-organized developmental patterning and differentiation in cerebral organoids

EMBO Journal

Volumn 36, Issue 10, 2017, Pages 1316-1329

  Renner, Magdalena ^a   Lancaster, Madeline A ^a,b   Bian, Shan ^a   Choi, Heejin ^c   Ku, Taeyun ^c   Peer, Angela ^a   Chung, Kwanghun ^c,d,e   Knoblich, Juergen A ^a  

^a ERICH SCHMID INSTITUTE OF MATERIALS SCIENCE   (Austria)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c Massachusetts Institute of Technology   (United States)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

Author keywords

development; human brain development; neurogenesis; organoid; patterning; signaling

Indexed keywords

ARTICLE; ASTROCYTE; BRAIN DEVELOPMENT; CYTOPLASM; FOREBRAIN; FUNCTIONAL CONNECTIVITY; HUMAN; HUMAN CELL; NERVE CELL DIFFERENTIATION; NERVE EXCITABILITY; OLIGODENDROGLIA; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYOLOGY; GROWTH, DEVELOPMENT AND AGING; MORPHOGENESIS; SPATIOTEMPORAL ANALYSIS;

BODY PATTERNING; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; HUMANS; ORGANOIDS; SPATIO-TEMPORAL ANALYSIS;

EID: 85014923623     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201694700     Document Type: Article

References (40)

1. Abu-Khalil A, Fu L, Grove EA, Zecevic N, Geschwind DH (2004) Wnt genes define distinct boundaries in the developing human brain: implications for human forebrain patterning. J Comp Neurol 474: 276–288
2. Borello U, Pierani A (2010) Patterning the cerebral cortex: traveling with morphogens. Curr Opin Genet Dev 20: 408–415
3. Camp JG, Badsha F, Florio M, Kanton S, Gerber T, Wilsch-Bräuninger M, Lewitus E, Sykes A, Hevers W, Lancaster M, Knoblich JA, Lachmann R, Pääbo S, Huttner WB, Treutlein B (2015) Human cerebral organoids recapitulate gene expression programs of fetal neocortex development. Proc Natl Acad Sci USA 112: 15672–15677
4. Caronia-Brown G, Yoshida M, Gulden F, Assimacopoulos S, Grove EA (2014) The cortical hem regulates the size and patterning of neocortex. Development 141: 2855–2865
5. Chambers SM, Fasano CA, Papapetrou EP, Tomishima M, Sadelain M, Studer L (2009) Highly efficient neural conversion of human ES and iPS cells by dual inhibition of SMAD signaling. Nat Biotechnol 27: 275–280
6. Chizhikov VV, Lindgren AG, Mishima Y, Roberts RW, Aldinger KA, Miesegaes GR, Currle DS, Monuki ES, Millen KJ (2010) Lmx1a regulates fates and location of cells originating from the cerebellar rhombic lip and telencephalic cortical hem. Proc Natl Acad Sci USA 107: 10725–10730
7. Eiraku M, Watanabe K, Matsuo-Takasaki M, Kawada M, Yonemura S, Matsumura M, Wataya T, Nishiyama A, Muguruma K, Sasai Y (2008) Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3: 519–532
8. Elston GN (2003) Cortex, cognition and the cell: new insights into the pyramidal neuron and prefrontal function. Cereb Cortex 13: 1124–1138
9. Englund C (2005) Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J Neurosci 25: 247–251
10. Fagerberg L, Hallstrom BM, Oksvold P, Kampf C, Djureinovic D, Odeberg J, Habuka M, Tahmasebpoor S, Danielsson A, Edlund K, Asplund A, Sjostedt E, Lundberg E, Szigyarto CAK, Skogs M, Takanen JO, Berling H, Tegel H, Mulder J, Nilsson P et al (2014) Analysis of the human tissue-specific expression by genome-wide integration of transcriptomics and antibody-based proteomics. Mol Cell Proteomics 13: 397–406
11. Gaspard N, Bouschet T, Hourez R, Dimidschstein J, Naeije G, van den Ameele J, Espuny-Camacho I, Herpoel A, Passante L, Schiffmann SN, Gaillard A, Vanderhaeghen P (2008) An intrinsic mechanism of corticogenesis from embryonic stem cells. Nature 455: 351–357
12. Geffers L, Herrmann B, Eichele G (2012) Web-based digital gene expression atlases for the mouse. Mamm Genome 23: 525–538
13. Georgala PA, Carr CB, Price DJ (2011) The role of Pax6 in forebrain development. Dev Neurobiol 71: 690–709
14. Geschwind DH, Rakic P (2013) Perspective. Neuron 80: 633–647
15. Grove EA, Tole S, Limon J, Yip L, Ragsdale CW (1998) The hem of the embryonic cerebral cortex is defined by the expression of multiple Wnt genes and is compromised in Gli3-deficient mice. Development 125: 2315–2325
16. Grove EA, Monuki ES (2013) Chapter 2 - Morphogens, patterning centers, and their mechanisms of action. In Patterning and cell type specification in the developing CNS and PNS, Rubenstein JLR, Rakic P (eds), pp 25–44. Oxford: Academic Press
17. Hansen DV, Lui JH, Flandin P, Yoshikawa K, Rubenstein JL, Alvarez-Buylla A, Kriegstein AR (2013) Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat Neurosci 16: 1576–1587
18. Hevner RF, Daza RAM, Rubenstein JLR, Stunnenberg H, Olavarria JF, Englund C (2003) Beyond laminar fate: toward a molecular classification of cortical projection/pyramidal neurons. Dev Neurosci 25: 139–151
19. Kadoshima T, Sakaguchi H, Nakano T, Soen M, Ando S, Eiraku M, Sasai Y (2013) Self-organization of axial polarity, inside-out layer pattern, and species-specific progenitor dynamics in human ES cell-derived neocortex. Proc Natl Acad Sci USA 110: 20284–20289
20. Kerwin J, Yang Y, Merchan P, Sarma S, Thompson J, Wang X, Sandoval J, Puelles L, Baldock R, Lindsay S (2010) The HUDSEN Atlas: a three-dimensional (3D) spatial framework for studying gene expression in the developing human brain. J Anat 217: 289–299
21. Lancaster MA, Renner M, Martin C-A, Wenzel D, Bicknell LS, Hurles ME, Homfray T, Penninger JM, Jackson AP, Knoblich JA (2013) Cerebral organoids model human brain development and microcephaly. Nature 501: 373–379
22. Lancaster MA, Knoblich JA (2014) Generation of cerebral organoids from human pluripotent stem cells. Nat Protoc 9: 2329–2340
23. Lancaster MA, Corsini NS, Burkard TR, Knoblich JA (2016) Guided self-organization recapitulates tissue architecture in a bioengineered brain organoid model. bioRxiv doi:10.1101/049346
24. Lui JH, Hansen DV, Kriegstein AR (2011) Development and evolution of the human neocortex. Cell 146: 18–36
25. Ma T, Wang C, Wang L, Zhou X, Tian M, Zhang Q, Zhang Y, Li J, Liu Z, Cai Y, Liu F, You Y, Chen C, Campbell K, Song H, Ma L, Rubenstein JL, Yang Z (2013) Subcortical origins of human and monkey neocortical interneurons. Nat Neurosci 16: 1588–1597
26. Mariani J, Simonini MV, Palejev D, Tomasini L, Coppola G, Szekely AM, Horvath TL, Vaccarino FM (2012) Modeling human cortical development in vitro using induced pluripotent stem cells. Proc Natl Acad Sci USA 109: 12770–12775
27. Mariani J, Coppola G, Zhang P, Abyzov A, Provini L, Tomasini L, Amenduni M, Szekely A, Palejev D, Wilson M, Gerstein M, Grigorenko EL, Chawarska K, Pelphrey KA, Howe JR, Vaccarino FM (2015) FOXG1-dependent dysregulation of GABA/glutamate neuron differentiation in autism spectrum disorders. Cell 162: 375–390
28. Medina L, Abellán A (2009) Development and evolution of the pallium. Semin Cell Dev Biol 20: 698–711
29. Miller JA, Ding S-L, Sunkin SM, Smith KA, Ng L, Szafer A, Ebbert A, Riley ZL, Royall JJ, Aiona K, Arnold JM, Bennet C, Bertagnolli D, Brouner K, Butler S, Caldejon S, Carey A, Cuhaciyan C, Dalley RA, Dee N et al (2014) Transcriptional landscape of the prenatal human brain. Nature 508: 199–206
30. Molyneaux BJ, Arlotta P, Menezes JRL, Macklis JD (2007) Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8: 427–437
31. Murray E, Cho JH, Goodwin D, Ku T, Swaney J, Kim S-Y, Choi H, Park Y-G, Park J-Y, Hubbert A, McCue M, Vassallo S, Bakh N, Frosch MP, Wedeen Van J, Seung HS, Chung K (2015) Simple, scalable proteomic imaging for high- dimensional profiling of intact systems. Cell 163: 1500–1514
32. O'Leary DDM, Chou S-J, Sahara S (2007) Area patterning of the mammalian cortex. Neuron 56: 252–269
33. Paşca AM, Sloan SA, Clarke LE, Tian Y, Makinson CD, Huber N, Kim CH, Park J-Y, O'Rourke NA, Nguyen KD, Smith SJ, Huguenard JR, Geschwind DH, Barres BA, Paşca SP (2015) Functional cortical neurons and astrocytes from human pluripotent stem cells in 3D culture. Nat Methods 12: 671–678
34. Qian X, Nguyen HN, Song MM, Hadiono C, Ogden SC, Hammack C, Yao B, Hamersky GR, Jacob F, Zhong C, Yoon K-J, Jeang W, Lin L, Li Y, Thakor J, Berg DA, Zhang C, Kang E, Chickering M, Nauen D et al (2016) Brain-region-specific organoids using mini- bioreactors for modeling ZIKV exposure. Cell 165: 1238–1254
35. Rakic P (1974) Neurons in rhesus monkey visual cortex: systematic relation between time of origin and eventual disposition. Science 183: 425–427
36. Sanes DH, Reh TA, Harris WA (2011) Development of the nervous system, 3rd edn. Waltham, MA: Academic Press.
37. Sauvageot C (2002) Molecular mechanisms controlling cortical gliogenesis. Curr Opin Neurobiol 12: 244–249
38. Shi Y, Kirwan P, Smith J, Robinson HPC, Livesey FJ (2012) Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat Neurosci 15: 477–486
39. Subramanian L, Remedios R, Shetty A, Tole S (2009) Signals from the edges: the cortical hem and antihem in telencephalic development. Semin Cell Dev Biol 20: 712–718
40. 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: 465–502