Self-organization of neural tissue architectures from pluripotent stem cells

Journal of Comparative Neurology

Volumn 522, Issue 12, 2014, Pages 2831-2844

  Karus, Michael ^a   Blaess, Sandra ^a   Brüstle, Oliver ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

3D culture; Cortical development; Neural stem cell; Rosette formation

Indexed keywords

ACTIVIN; BONE MORPHOGENETIC PROTEIN; CD133 ANTIGEN; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 2; NERVE CELL ADHESION MOLECULE; NESTIN; PROTEIN ZO1; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR SOX1; TRANSCRIPTION FACTOR SOX2; TRANSFORMING GROWTH FACTOR BETA;

BRAIN DEVELOPMENT; CELL MIGRATION; HUMAN; IN VITRO STUDY; INTRACELLULAR SIGNALING; NERVE CELL DIFFERENTIATION; NERVOUS TISSUE; NEUROECTODERM; NONHUMAN; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; ROSETTE FORMATION; TISSUE STRUCTURE; ANIMAL; BRAIN CORTEX; CELL CULTURE; CELL DIFFERENTIATION; CYTOLOGY; NERVE CELL; NEURAL STEM CELL; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; CEREBRAL CORTEX; HUMANS; IN VITRO TECHNIQUES; NEURAL STEM CELLS; NEURONS;

EID: 84911888080     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23608     Document Type: Review

References (82)

1. Ajioka I, Nakajima K. 2005. Birth-date-dependent segregation of the mouse cerebral cortical neurons in reaggregation cultures. Eur J Neurosci 22:331-342.
2. Bielle F, Griveau A, Narboux-Neme N, Vigneau S, Sigrist M, Arber S, Wassef M, Pierani A. 2005. Multiple origins of Cajal-Retzius cells at the borders of the developing pallium. Nat Neurosci 8:1002-1012.
3. Brüstle O, Ohgaki H, Schmitt HP, Walter GF, Ostertag H, Kleihues P. 1992. Primitive neuroectodermal tumors after prophylactic central nervous system irradiation in children. Association with an activated K-ras gene. Cancer 69:2385-2392.
4. Brüstle O, Spiro AC, Karram K, Choudhary K, Okabe S, McKay RD. 1997. In vitro-generated neural precursors participate in mammalian brain development. Proc Natl Acad Sci U S A 94:14809-14814.
5. Budrene EO, Berg HC. 1995. Dynamics of formation of symmetrical patterns by chemotactic bacteria. Nature 376:49-53.
6. Campos LS, Leone DP, Relvas JB, Brakebusch C, Fassler R, Suter U, ffrench-Constant C. 2004. Beta1 integrins activate a MAPK signalling pathway in neural stem cells that contributes to their maintenance. Development 131:3433-3444.
7. 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.
8. Chizhikov VV, Millen KJ. 2005. Roof plate-dependent patterning of the vertebrate dorsal central nervous system. Dev Biol 277:287-295.
9. Conti L, Cattaneo E. 2010. Neural stem cell systems: physiological players or in vitro entities? Nat Rev Neurosci 11:176-187.
10. Conti L, Pollard SM, Gorba T, Reitano E, Toselli M, Biella G, Sun Y, Sanzone S, Ying QL, Cattaneo E, Smith A. 2005. Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol 3:e283.
11. Cruz-Sanchez FF, Rossi ML, Hughes JT, Moss TH. 1991. Differentiation in embryonal neuroepithelial tumors of the central nervous system. Cancer 67:965-976.
12. DeLong GR. 1970. Histogenesis of fetal mouse isocortex and hippocampus in reaggregating cell cultures. Dev Biol 22:563-583.
13. Desai AR, McConnell SK. 2000. Progressive restriction in fate potential by neural progenitors during cerebral cortical development. Development 127:2863-2872.
14. Eberhart CG, Brat DJ, Cohen KJ, Burger PC. 2000. Pediatric neuroblastic brain tumors containing abundant neuropil and true rosettes. Pediatr Dev Pathol 3:346-352.
15. Eiraku M, Sasai Y. 2011. Mouse embryonic stem cell culture for generation of three-dimensional retinal and cortical tissues. Nat Protoc 7:69-79.
16. 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.
17. Eiraku M, Takata N, Ishibashi H, Kawada M, Sakakura E, Okuda S, Sekiguchi K, Adachi T, Sasai Y. 2011. Selforganizing optic-cup morphogenesis in three-dimensional culture. Nature 472:51-56.
18. Eiraku M, Adachi T, Sasai Y. 2012. Relaxation-expansion model for self-driven retinal morphogenesis: a hypothesis from the perspective of biosystems dynamics at the multi-cellular level. Bioessays 34:17-25.
19. Elkabetz Y, Panagiotakos G, Al Shamy G, Socci ND, Tabar V, Studer L. 2008. Human ES cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev 22:152-165.
20. Falk A, Koch P, Kesavan J, Takashima Y, Ladewig J, Alexander M, Wiskow O, Tailor J, Trotter M, Pollard S, Smith A, Brüstle O. 2012. Capture of neuroepithelial-like stem cells from pluripotent stem cells provides a versatile system for in vitro production of human neurons. PLoS One 7:e29597.
21. 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.
22. Gaspard N, Bouschet T, Herpoel A, Naeije G, van den Ameele J, Vanderhaeghen P. 2009. Generation of cortical neurons from mouse embryonic stem cells. Nat Protoc 4:1454-1463.
23. Götz M, Huttner WB. 2005. The cell biology of neurogenesis. Nat Rev Mol Cell Biol 6:777-788.
24. Graw J. 2010. Eye development. Curr Top Dev Biol 90:343-386.
25. Hansen DV, Lui JH, Parker PR, Kriegstein AR. 2010. Neurogenic radial glia in the outer subventricular zone of human neocortex. Nature 464:554-561.
26. 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.
27. Hsu C, Kwan G, Lau Q, Bhuta S. 2012. Rosette-forming glioneuronal tumour: imaging features, histopathological correlation and a comprehensive review of literature. Br J Neurosurg 26:668-673.
28. Ideguchi M, Palmer TD, Recht LD, Weimann JM. 2010. Murine embryonic stem cell-derived pyramidal neurons integrate into the cerebral cortex and appropriately project axons to subcortical targets. J Neurosci 30:894-904.
29. Jensen JB, Parmar M. 2006. Strengths and limitations of the neurosphere culture system. Mol Neurobiol 34:153-161.
30. 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 U S A 110:20284-20289.
31. Karus M, Denecke B, ffrench-Constant C, Wiese S, Faissner A. 2011. The extracellular matrix molecule tenascin C modulates expression levels and territories of key patterning genes during spinal cord astrocyte specification. Development 138:5321-5331.
32. Kim DS, Lee JS, Leem JW, Huh YJ, Kim JY, Kim HS, Park IH, Daley GQ, Hwang DY, Kim DW. 2010. Robust enhancement of neural differentiation from human ES and iPS cells regardless of their innate difference in differentiation propensity. Stem Cell Rev 6:270-281.
33. Koch P, Opitz T, Steinbeck JA, Ladewig J, Brüstle O. 2009. A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitro instruction and synaptic integration. Proc Natl Acad Sci U S A 106:3225-3230.
34. Krispin S, Nitzan E, Kalcheim C. 2010. The dorsal neural tube: a dynamic setting for cell fate decisions. Dev Neurobiol 70:796-812.
35. Krushel LA, van der Kooy D. 1993. Pattern formation in the developing mammalian forebrain: selective adhesion of early but not late postmitotic cortical and striatal neurons within forebrain reaggregate cultures. Dev Biol 158:145-162.
36. 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.
37. Lancaster MA, Renner M, Martin CA, 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.
38. Lee G, Kim H, Elkabetz Y, Al Shamy G, Panagiotakos G, Barberi T, Tabar V, Studer L. 2007. Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat Biotechnol 25:1468-1475.
39. Li W, Sun W, Zhang Y, Wei W, Ambasudhan R, Xia P, Talantova M, Lin T, Kim J, Wang X, Kim WR, Lipton SA, Zhang K, Ding S. 2011. Rapid induction and long-term self-renewal of primitive neural precursors from human embryonic stem cells by small molecule inhibitors. Proc Natl Acad Sci U S A 108:8299-8304.
40. Li XJ, Zhang X, Johnson MA, Wang ZB, Lavaute T, Zhang SC. 2009. Coordination of sonic hedgehog and Wnt signaling determines ventral and dorsal telencephalic neuron types from human embryonic stem cells. Development 136:4055-4063.
41. Lui JH, Hansen DV, Kriegstein AR. 2011. Development and evolution of the human neocortex. Cell 146:18-36.
42. 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 U S A 109:12770-12775.
43. McConnell SK. 1988. Fates of visual cortical neurons in the ferret after isochronic and heterochronic transplantation. J Neurosci 8:945-974.
44. McLoon LK, Lund RD, McLoon SC. 1982. Transplantation of reaggregates of embryonic neural retinae to neonatal rat brain: differentiation and formation of connections. J Comp Neurol 205:179-189.
45. Metin C, Baudoin JP, Rakic S, Parnavelas JG. 2006. Cell and molecular mechanisms involved in the migration of cortical interneurons. Eur J Neurosci 23:894-900.
46. Mica Y, Lee G, Chambers SM, Tomishima MJ, Studer L. 2013. Modeling neural crest induction, melanocyte specification, and disease-related pigmentation defects in hESCs and patient-specific iPSCs. Cell Rep (in press).
47. Molyneaux BJ, Arlotta P, Menezes JR, Macklis JD. 2007. Neuronal subtype specification in the cerebral cortex. Nat Rev Neurosci 8:427-437.
48. Nakano T, Ando S, Takata N, Kawada M, Muguruma K, Sekiguchi K, Saito K, Yonemura S, Eiraku M, Sasai Y. 2012. Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10:771-785.
49. Nasu M, Takata N, Danjo T, Sakaguchi H, Kadoshima T, Futaki S, Sekiguchi K, Eiraku M, Sasai Y. 2012. Robust formation and maintenance of continuous stratified cortical neuroepithelium by laminin-containing matrix in mouse ES cell culture. PLoS One 7:e53024.
50. Nose A, Nagafuchi A, Takeichi M. 1988. Expressed recombinant cadherins mediate cell sorting in model systems. Cell 54:993-1001.
51. Okabe S, Forsberg-Nilsson K, Spiro AC, Segal M, McKay RD. 1996. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 59:89-102.
52. Pankratz MT, Li XJ, Lavaute TM, Lyons EA, Chen X, Zhang SC. 2007. Directed neural differentiation of human embryonic stem cells via an obligated primitive anterior stage. Stem Cells 25:1511-1520.
53. Pastrana E, Silva-Vargas V, Doetsch F. 2011. Eyes wide open: a critical review of sphere-formation as an assay for stem cells. Cell Stem Cell 8:486-498.
54. Rathjen J, Lake JA, Bettess MD, Washington JM, Chapman G, Rathjen PD. 1999. Formation of a primitive ectoderm like cell population, EPL cells, from ES cells in response to biologically derived factors. J Cell Sci 112:601-612.
55. Rathjen J, Haines BP, Hudson KM, Nesci A, Dunn S, Rathjen PD. 2002. Directed differentiation of pluripotent cells to neural lineages: homogeneous formation and differentiation of a neurectoderm population. Development 129:2649-2661.
56. Reinhardt P, Glatza M, Hemmer K, Tsytsyura Y, Thiel CS, Hoing S, Moritz S, Parga JA, Wagner L, Bruder JM, Wu G, Schmid B, Ropke A, Klingauf J, Schwamborn JC, Gasser T, Scholer HR, Sterneckert J. 2013. Derivation and expansion using only small molecules of human neural progenitors for neurodegenerative disease modeling. PLoS One 8:e59252.
57. Reynolds BA, Rietze RL. 2005. Neural stem cells and neurospheres-re-evaluating the relationship. Nat Methods 2:333-336.
58. Reynolds BA, Weiss S. 1992. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255:1707-1710.
59. Reynolds BA, Weiss S. 1996. Clonal and population analyses demonstrate that an EGF-responsive mammalian embryonic CNS precursor is a stem cell. Dev Biol 175:1-13.
60. Reynolds BA, Tetzlaff W, Weiss S. 1992. A multipotent EGFresponsive striatal embryonic progenitor cell produces neurons and astrocytes. J Neurosci 12:4565-4574.
61. Sansom SN, Livesey FJ. 2009. Gradients in the brain: the control of the development of form and function in the cerebral cortex. Cold Spring Harbor Perspect Biol 1: a002519.
62. Sasai Y. 2013a. Cytosystems dynamics in self-organization of tissue architecture. Nature 493:318-326.
63. Sasai Y. 2013b. Next-generation regenerative medicine: organogenesis from stem cells in 3D culture. Cell Stem Cell 12:520-530.
64. Sasaki R, Aoki S, Yamato M, Uchiyama H, Wada K, Okano T, Ogiuchi H. 2008. Neurosphere generation from dental pulp of adult rat incisor. Eur J Neurosci 27:538-548.
65. Satomi K, Morishita Y, Sakashita S, Kondou Y, Furuya S, Minami Y, Noguchi M. 2011. Specific expression of ZO-1 and N-cadherin in rosette structures of various tumors: possible recapitulation of neural tube formation in embryogenesis and utility as a potentially novel immunohistochemical marker of rosette formation in pulmonary neuroendocrine tumors. Virchows Arch 459:399-407.
66. Shen Q, Wang Y, Dimos JT, Fasano CA, Phoenix TN, Lemischka IR, Ivanova NB, Stifani S, Morrisey EE, Temple S. 2006. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nat Neurosci 9:743-751.
67. Shi Y, Kirwan P, Livesey FJ. 2012a. Directed differentiation of human pluripotent stem cells to cerebral cortex neurons and neural networks. Nat Protoc 7:1836-1846.
68. Shi Y, Kirwan P, Smith J, Robinson HP, Livesey FJ. 2012b. Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat Neurosci 15:477-486, S471.
69. Sirko S, von Holst A, Wizenmann A, Gotz M, Faissner A. 2007. Chondroitin sulfate glycosaminoglycans control proliferation, radial glia cell differentiation and neurogenesis in neural stem/progenitor cells. Development 134:2727-2738.
70. Steinberg MS, Gilbert SF. 2004. Townes and Holtfreter (1955): directed movements and selective adhesion of embryonic amphibian cells. J Exp Zool A Comp Exp Biol 301:701-706.
71. Stern CD. 2001. Initial patterning of the central nervous system: how many organizers? Nat Rev Neurosci 2:92-98.
72. Tailor J, Kittappa R, Leto K, Gates M, Borel M, Paulsen O, Spitzer S, Karadottir RT, Rossi F, Falk A, Smith A. 2013. Stem cells expanded from the human embryonic hindbrain stably retain regional specification and high neurogenic potency. J Neurosci 33:12407-12422.
73. Tomooka Y, Kitani H, Jing N, Matsushima M, Sakakura T. 1993. Reconstruction of neural tube-like structures in vitro from primary neural precursor cells. Proc Natl Acad Sci U S A 90:9683-9687.
74. von Holst A, Sirko S, Faissner A. 2006. The unique 473HDchondroitinsulfate epitope is expressed by radial glia and involved in neural precursor cell proliferation. J Neurosci 26:4082-4094.
75. Watanabe K, Kamiya D, Nishiyama A, Katayama T, Nozaki S, Kawasaki H, Watanabe Y, Mizuseki K, Sasai Y. 2005. Directed differentiation of telencephalic precursors from embryonic stem cells. Nat Neurosci 8:288-296.
76. Weible MW 2nd, Chan-Ling T. 2007. Phenotypic characterization of neural stem cells from human fetal spinal cord: synergistic effect of LIF and BMP4 to generate astrocytes. Glia 55:1156-1168.
77. Whitesides JG 3rd, LaMantia AS. 1995. Distinct adhesive behaviors of neurons and neural precursor cells during regional differentiation in the mammalian forebrain. Dev Biol 169:229-241.
78. Wonders CP, Anderson SA. 2006. The origin and specification of cortical interneurons. Nat Rev Neurosci 7:687-696.
79. Young KM, Mitsumori T, Pringle N, Grist M, Kessaris N, Richardson WD. 2010. An Fgfr3-iCreER(T2) transgenic mouse line for studies of neural stem cells and astrocytes. Glia 58:943-953.
80. Zeng H, Guo M, Martins-Taylor K, Wang X, Zhang Z, Park JW, Zhan S, Kronenberg MS, Lichtler A, Liu HX, Chen FP, Yue L, Li XJ, Xu RH. 2010. Specification of regionspecific neurons including forebrain glutamatergic neurons from human induced pluripotent stem cells. PLoS One 5:e11853.
81. Zhang SC, Wernig M, Duncan ID, Brüstle O, Thomson JA. 2001. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat Biotechnol 19:1129-1133.
82. Zhou J, Su P, Li D, Tsang S, Duan E, Wang F. 2010. Highefficiency induction of neural conversion in human ESCs and human induced pluripotent stem cells with a single chemical inhibitor of transforming growth factor beta superfamily receptors. Stem Cells 28:1741-1750.