Modeling physiological and pathological human neurogenesis in the dish

Frontiers in Neuroscience

Volumn , Issue 8 JUL, 2014, Pages

  Broccoli, Vania ^a   Giannelli, Serena G ^a   Mazzara, Pietro G ^a  

^a SAN RAFFAELE HOSPITAL   (Italy)

Author keywords

ESCs; Human neurogenesis; In vitrodisease modeling; iPSCs; Neural crest; Neural tube; Rosettes; Self aggregation

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR;

BRAIN CELL; CELL AGING; CELL MATURATION; DOPAMINERGIC NERVE CELL; HUMAN; NERVOUS SYSTEM DEVELOPMENT; NEURAL CREST CELL; NEURAL STEM CELL; NEURAL TUBE; NEURULATION; PLURIPOTENT STEM CELL; REVIEW; ROSETTE FORMATION;

EID: 84905910874     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/fnins.2014.00183     Document Type: Review

References (76)

1. Alvarez Dolado, M., and Broccoli, V. (2011). GABAergic neuronal precursor grafting: implications in brain regeneration and plasticity. Neural Plast. 2011:384216. doi: 10.1155/2011/384216
2. Barker, R. A., Barrett, J., Mason, S. L., and Björklund, A. (2013). Fetal dopaminergic transplantation trials and the future of neural grafting in Parkinson's disease. Lancet Neurol. 12, 84-91. doi: 10.1016/S1474-4422(12)70295-8
3. Baroffio, A., Dupin, E., and Le Dourin, N. M. (1991). Common precursors for neural and mesectodermal derivatives in the cephalic neural crest. Development 112, 301-305.
4. Bilican, B., Livesey, M. R., Haghi, G., Qiu, J., Burr, K., Siller, R., et al. (2014). Physiological normoxia and absence of EGF is required for the long-term propagation of anterior neural precursors from human pluripotent cells. PLoS ONE. 9:e85932. doi: 10.1371/journal.pone.0085932
5. Colleoni, S., Galli, C., Giannelli, S. G., Armentero, M. T., Blandini, F., Broccoli, V., et al. (2010). Long-term culture and differentiation of CNS precursors derived from anterior human neural rosettes following exposure to ventralizing factors. Exp. Cell Res. 316, 1148-1158. doi: 10.1016/j.yexcr.2010.02.013
6. Conti, L., Pollard, S. M., Gorba, T., Reitano, E., Toselli, M., Biella, G., et al. (2005). Niche-independent symmetrical self-renewal of a mammalian tissue stem cell. PLoS Biol. 3:e283. doi: 10.1371/journal.pbio.0030283
7. Curchoe, C. L., Maurer, J., McKeown, S. J., Cattarossi, G., Cimadamore, F., Nilbratt, M., et al. (2010). Early acquisition of neural crest competence during hESCs neuralization. PLoS ONE. 5:e13890. doi: 10.1371/journal.pone.0013890
8. Dimos, J. T., Rodolfa, K. T., Niakan, K. K., Weisenthal, L. M., Mitsumoto, H., Chung, W., et al. (2008). Induced pluripotent stem cells generated from patients with ALS can be differentiated into motor neurons. Science 321, 1218-1221. doi: 10.1126/science.1158799
9. Dunnett, S. B., Björklund, A., and Lindvall, O. (2001). Cell therapy in Parkinson's disease-stop or go? Nat. Rev. Neurosci. 2, 365-369. doi: 10.1038/35072572
10. Ebert, A. D., Yu, J., Rose, F. F. Jr., Mattis, V. B., Lorson, C. L., Thomson, J. A., et al. (2009). Induced pluripotent stem cells from a spinal muscular atrophy patient. Nature 457, 277-280. doi: 10.1038/nature07677
11. Eiraku, M., Takata, N., Ishibashi, H., Kawada, M., Sakakura, E., Okuda, S., et al. (2011). Self-organizing optic-cup morphogenesis in three-dimensional culture. Nature 472, 51-56. doi: 10.1038/nature09941
12. Eiraku, M., Watanabe, K., Matsuo-Takasaki, M., Kawada, M., Yonemura, S., Matsumura, M., et al. (2008). Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. Cell Stem Cell 3, 519-532. doi: 10.1016/j.stem.2008.09.002
13. Elkabetz, Y., Panagiotakos, G., Al Shamy, G., Socci, N. D., Tabar, V., and Studer, L. (2008). Human, E. S. cell-derived neural rosettes reveal a functionally distinct early neural stem cell stage. Genes Dev. 22, 152-165. doi: 10.1101/gad.1616208
14. Espuny-Camacho, I., Michelsen, K. A., Gall, D., Linaro, D., Hasche, A., Bonnefont, J., et al. (2013). Pyramidal neurons derived from human pluripotent stem cells integrate efficiently into mouse brain circuits in vivo. Neuron 77, 440-456. doi: 10.1016/j.neuron.2012.12.011
15. Gossrau, G., Thiele, J., Konang, R., Schmandt, T., and Brüstle, O. (2007). Bone morphogenetic protein-mediated modulation of lineage diversification during neural differentiation of embryonic stem cells. Stem Cells 25, 939-949. doi: 10.1634/stemcells.2006-0299
16. Grealish, S., Jönsson, M. E., Li, M., Kirik, D., Björklund, A., and Thompson, L. H. (2010). The A9 dopamine neuron component in grafts of ventral mesencephalon is an important determinant for recovery of motor function in a rat model of Parkinson's disease. Brain. 133(pt 2), 482-495. doi: 10.1093/brain/awp328
17. Greig, L. C., Woodworth, M. B., Galazo, M. J., Padmanabhan, H., and Macklis, J. D. (2013). Molecular logic of neocortical projection neuron specification, development and diversity. Nat. Rev. Neurosci. 14, 755-769. doi: 10.1038/nrn3586
18. Hu, B. Y., Weick, J. P., Yu, J., Ma, L. X., Zhang, X. Q., Thomson, J. A., et al. (2010). Neural differentiation of human induced pluripotent stem cells follows developmental principles but with variable potency. Proc. Natl. Acad. Sci. U.S.A. 107, 4335-4340. doi: 10.1073/pnas.0910012107
19. Israel, M. A., Yuan, S. H., Bardy, C., Reyna, S. M., Mu, Y., Herrera, C., et al. (2012). Probing sporadic and familial Alzheimer's disease using induced pluripotent stem cells. Nature 482, 216-220. doi: 10.1038/nature10821
20. Kadoshima, T., Sakaguchi, H., Nakano, T., Soen, M., Ando, S., Eiraku, M., et al. (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. doi: 10.1073/pnas.1315710110
21. Kepecs, A., and Fishell, G. (2014). Interneuron cell types are fit to function. Nature 505, 318-326. doi: 10.1038/nature12983
22. Kim, D. S., Lee, D. R., Kim, H. S., Yoo, J. E., Jung, S. J., Lim, B. Y., et al. (2012). Highly pure and expandable PSA-NCAM-positive neural precursors from human ESC and iPSC-derived neural rosettes. PLoS ONE. 7:e39715. doi: 10.1371/journal.pone.0039715
23. Kim, J. H., Auerbach, J. M., Rodriguez-Gomez, J. A., Velasco, I., Gavin, D., Lumelsky, N., et al. (2002). Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418, 50-56. doi: 10.1038/nature00900
24. Kirkeby, A., Grealish, S., Wolf, D. A., Nelander, J., Wood, J., Lundblad, M., et al. (2012). Generation of regionally specified neural progenitors and functional neurons from human embryonic stem cells under defined conditions. Cell Rep. 1, 703-714. doi: 10.1016/j.celrep.2012.04.009
25. Koch, P., Opitz, T., Steinbeck, J. A., and Brustle, O. (2009). A rosette-type, self-renewing human ES cell-derived neural stem cell with potential for in vitroinstruction and synaptic integration. Proc. Natl. Acad. Sci. U.S.A. 106, 3225-3230. doi: 10.1073/pnas.0808387106
26. Kriks, S., Shim, J. W., Piao, J., Ganat, Y. M., Wakeman, D. R., Xie, Z., et al. (2011). Dopamine neurons derived from human ES cells efficiently engraft in animal models of Parkinson's disease. Nature 480, 547-551. doi: 10.1038/nature10648
27. Lancaster, M. A., Renner, M., Martin, C. A., Wenzel, D., Bicknell, L. S., Hurles, M. E., et al. (2013). Cerebral organoids model human brain development and microcephaly. Nature 501, 373-379. doi: 10.1038/nature12517
28. Lane, E. L., Björklund, A., Dunnett, S. B., and Winkler, C. (2010). Neural grafting in Parkinson's disease unraveling the mechanisms underlying graft-induced dyskinesia. Prog. Brain Res. 184, 295-309. doi: 10.1016/S0079-6123(10)84015-4
29. Lazzari, G., Colleoni, S., Giannelli, S. G., Brunetti, D., Colombo, E., Lagutina, I., et al. (2006). Direct derivation of neural rosettes from cloned bovine blastocysts: a model of early neurulation events and neural crest specification in vitro. Stem Cells. 24, 2514-2521. doi: 10.1634/stemcells.2006-0149
30. Le Douarin, N. M., Creuzet, S., Couly, G., and Dupin, E. (2004). Neural crest cell plasticity and its limits. Development 131, 4637-4650. doi: 10.1242/dev.01350
31. Lee, G., Chambers, S. M., Tomishima, M. J., and Studer, L. (2010). Derivation of neural crest cells from human pluripotent stem cells. Nat. Protoc. 5, 688-701. doi: 10.1038/nprot.2010.35
32. Lee, G., Kim, H., Elkabetz, Y., Al Shamy, G., Panagiotakos, G., Barberi, T., et al. (2007). Isolation and directed differentiation of neural crest stem cells derived from human embryonic stem cells. Nat. Biotechnol. 25, 1468-1475. doi: 10.1038/nbt1365
33. Lee, G., Papapetrou, E. P., Kim, H., Chambers, S. M., Tomishima, M. J., Fasano, C. A., et al. (2009). Modelling pathogenesis and treatment of familial dysautonomia using patient-specific iPSCs. Nature 461, 402-406. doi: 10.1038/nature08320
34. Li, Y., Wang, H., Muffat, J., Cheng, A. W., Orlando, D. A., Lovén, J., et al. (2013). Global transcriptional and translational repression in human-embryonic-stem-cell-derived Rett syndrome neurons. Cell Stem Cell 13, 446-458. doi: 10.1016/j.stem.2013.09.001
35. Lindvall, O., and Björklund, A. (2004). Cell therapy in Parkinson's disease. NeuroRx 1, 382-393. doi: 10.1602/neurorx.1.4.382
36. Lindvall, O., and Björklund, A. (2011). Cell therapeutics in Parkinson's disease. Neurotherapeutics 8, 539-548. doi: 10.1007/s13311-011-0069-6
37. Liu, G. H., Qu, J., Suzuki, K., Nivet, E., Li, M., Montserrat, N., et al. (2012). Progressive degeneration of human neural stem cells caused by pathogenic LRRK2. Nature 491, 603-607. doi: 10.1038/nature11557
38. Marchetto, M. C., Carromeu, C., Acab, A., Yu, D., Yeo, G. W., Mu, Y., et al. (2010). A model for neural development and treatment of Rett syndrome using human induced pluripotent stem cells. Cell 143, 527-539. doi: 10.1016/j.cell.2010.10.016
39. Marchetto, M. C., and Gage, F. H. (2012). Modeling brain disease in a dish: really? Cell Stem Cell 10, 642-645. doi: 10.1016/j.stem.2012.05.008
40. Marín, O. (2012). Interneuron dysfunction in psychiatric disorders. Nat. Rev. Neurosci. 13, 107-120. doi: 10.1038/nrn3155
41. Marín, O. (2013). Cellular and molecular mechanisms controlling the migration of neocortical interneurons. Eur. J. Neurosci. 38, 2019-2029. doi: 10.1111/ejn.12225
42. Maroof, A. M., Keros, S., Tyson, J. A., Ying, S. W., Ganat, Y. M., Merkle, F. T., et al. (2013). Directed differentiation and functional maturation of cortical interneurons from human embryonic stem cells. Cell Stem Cell 12, 559-572. doi: 10.1016/j.stem.2013.04.008
43. Meissner, W. G., Frasier, M., Gasser, T., Goetz, C. G., Lozano, A., Piccini, P., et al. (2011). Priorities in Parkinson's disease research. Nat. Rev. Drug Discov. 10, 377-393. doi: 10.1038/nrd3430
44. Mica, Y., Lee, G., Chambers, S. M., Tomishima, M. J., and Studer, L. (2013). Modeling neural crest induction, melanocyte specification, and disease-related pigmentation defects in hESCs and patient-specific iPSCs. Cell Rep. 3, 1140-1152. doi: 10.1016/j.celrep.2013.03.025
45. Miller, J. D., Ganat, Y. M., Kishinevsky, S., Bowman, R. L., Liu, B., Tu, E. Y., et al. (2013). Human iPSC-based modeling of late-onset disease via progerin-induced aging. Cell Stem Cell 13, 691-705. doi: 10.1016/j.stem.2013.11.006
46. Molyneaux, B. J., Arlotta, P., Menezes, J. R., and Macklis, J. D. (2007). Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 8, 427-437. doi: 10.1038/nrn2151
47. Muñoz-Sanjuán, I., and Brivanlou, A. H. (2002). Neural induction, the default model and embryonic stem cells. Nat. Rev. Neurosci. 3, 271-280. doi: 10.1038/nrn786
48. Nakano, T., Ando, S., Takata, N., Kawada, M., Muguruma, K., Sekiguchi, K., et al. (2012). Self-formation of optic cups and storable stratified neural retina from human ESCs. Cell Stem Cell 10, 771-785. doi: 10.1016/j.stem.2012.05.009
49. Newgard, C. B., and Sharpless, N. E. (2013). Coming of age: molecular drivers of aging and therapeutic opportunities. J. Clin. Invest. 123, 946-950. doi: 10.1172/JCI68833
50. Nicholas, C. R., Chen, J., Tang, Y., Southwell, D. G., Chalmers, N., Vogt, D., et al. (2013). Functional maturation of hPSC-derived forebrain interneurons requires an extended timeline and mimics human neural development. Cell Stem Cell 12, 573-586. doi: 10.1016/j.stem.2013.04.005
51. Perrier, A. L., Tabar, V., Barberi, T., Rubio, M. E., Bruses, J., Topf, N., et al. (2004). Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. U.S.A. 101, 12543-12548. doi: 10.1073/pnas.0404700101
52. Reubinoff, B. E., Itsykson, P., Turetsky, T., Pera, M. F., Reinhartz, E., Itzik, A., et al. (2001). Neural progenitors from human embryonic stem cells. Nat. Biotechnol. 19, 1134-1140. doi: 10.1038/nbt1201-1134
53. Ricciardi, S., Boggio, E. M., Grosso, S., Lonetti, G., Forlani, G., Stefanelli, G., et al. (2011). Reduced AKT/mTOR signaling and protein synthesis dysregulation in a Rett syndrome animal model. Hum. Mol. Genet. 20, 1182-1196. doi: 10.1093/hmg/ddq563
54. Ricciardi, S., Ungaro, F., Hambrock, M., Rademacher, N., Stefanelli, G., Brambilla, D., et al. (2012). CDKL5 ensures excitatory synapse stability by reinforcing NGL-1-PSD95 interaction in the postsynaptic compartment and is impaired in patient iPSC-derived neurons. Nat. Cell Biol. 14, 911-923. doi: 10.1038/ncb2566
55. Robson, E. J., Khaled, W. T., Abell, K., and Watson, C. J. (2006). Epithelial-to-mesenchymal transition confers resistance to apoptosis in three murine mammary epithelial cell lines. Differentiation 74, 254-264. doi: 10.1111/j.1432-0436.2006.00075.x
56. Saha, K., and Jaenisch, R. (2009). Technical challenges in using human induced pluripotent stem cells to model disease. Cell Stem Cell 5, 584-595. doi: 10.1016/j.stem.2009.11.009
57. Sandoe, J., and Eggan, K. (2013). Opportunities and challenges of pluripotent stem cell neurodegenerative disease models. Nat. Neurosci. 16, 780-789. doi: 10.1038/nn.3425
58. Sato, T., Vries, R. G., Snippert, H. J., van de Wetering, M., Barker, N., Stange, D. E., et al. (2009). Single Lgr 5 stem cells build crypt-villus structures in vitrowithout a mesenchymal niche. Nature 459, 262-265. doi: 10.1038/nature07935
59. Shi, Y., Kirwan, P., Smith, J., Robinson, H. P., and Livesey, F. J. (2012). Human cerebral cortex development from pluripotent stem cells to functional excitatory synapses. Nat. Neurosci. 15, 477-846, S1. doi: 10.1038/nn.3041
60. Soldner, F., Hockemeyer, D., Beard, C., Gao, Q., Bell, G. W., Cook, E. G., et al. (2009). Parkinson's disease patient-derived induced pluripotent stem cells free of viral reprogramming factors. Cell 136, 964-977. doi: 10.1016/j.cell.2009.02.013
61. Soldner, F., Laganière, J., Cheng, A. W., Hockemeyer, D., Gao, Q., Alagappan, R., et al. (2011). Generation of isogenic pluripotent stem cells differing exclusively at two early onset Parkinson point mutations. Cell 146, 318-331. doi: 10.1016/j.cell.2011.06.019
62. Southwell, D. G., Nicholas, C. R., Basbaum, A. I., Stryker, M. P., Kriegstein, A. R., Rubenstein, J. L., et al. (2014). Interneurons from embryonic development to cell-based therapy. Science344:1240622. doi: 10.1126/science.1240622
63. Suga, H., Kadoshima, T., Minaguchi, M., Ohgushi, M., Soen, M., Nakano, T., et al. (2011). Self-formation of functional adenohypophysis in three-dimensional culture. Nature 480, 57-62. doi: 10.1038/nature10637
64. Tang, X., Zhou, L., Wagner, A. M., Marchetto, M. C., Muotri, A. R., Gage, F. H., et al. (2013). Astroglial cells regulate the developmental timeline of human neurons differentiated from induced pluripotent stem cells. Stem Cell Res. 11, 743-757. doi: 10.1016/j.scr.2013.05.002
65. Taverna, E., and Huttner, W. B. (2010). Neural progenitor nuclei IN motion. Neuron 67, 906-914. doi: 10.1016/j.neuron.2010.08.027
66. Theka, I., Caiazzo, M., Dvoretskova, E., Leo, D., Ungaro, F., Curreli, S., et al. (2013). Rapid generation of functional dopaminergic neurons from human induced pluripotent stem cells through a single-step procedure using cell lineage transcription factors. Stem Cells Transl. Med. 2, 473-479. doi: 10.5966/sctm.2012-0133
67. Thompson, L. H., Grealish, S., Kirik, D., and Björklund, A. (2009). Reconstruction of the nigrostriatal dopamine pathway in the adult mouse brain. Eur. J. Neurosci. 30, 625-638. doi: 10.1111/j.1460-9568.2009.06878.x
68. Tiscornia, G., Vivas, E. L., and Izpisúa Belmonte, J. C. (2011). Diseases in a dish: modeling human genetic disorders using induced pluripotent cells. Nat. Med. 17, 1570-1576. doi: 10.1038/nm.2504
69. Tyson, J. A., and Anderson, S. A. (2014). GABAergic interneuron transplants to study development and treat disease. Trends Neurosci. 37, 169-177. doi: 10.1016/j.tins.2014.01.003
70. Valiente, M., and Marín, O. (2010). Neuronal migration mechanisms in development and disease. Curr. Opin. Neurobiol. 20, 68-78. doi: 10.1016/j.conb.2009.12.003
71. Vega, S., Morales, A. V., Ocaña, O. H., Valdés, F., Fabregat, I., and Nieto, M. A. (2004). Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131-1143. doi: 10.1101/gad.294104
72. Verpelli, C., Carlessi, L., Bechi, G., Fusar Poli, E., Orellana, D., Heise, C., et al. (2013). Comparative neuronal differentiation of self-renewing neural progenitor cell lines obtained from human induced pluripotent stem cells. Front. Cell. Neurosci. 7:175. doi: 10.3389/fncel.2013.00175
73. Watanabe, K., Ueno, M., Kamiya, D., Nisgiyama, A., Matsumura, M., Wataya, T., et al. (2007). A ROCK inhibitor permits survival of dissociated human embryonic stem cells. Nat. Biotechnol. 25, 681-686. doi: 10.1038/nbt1310
74. Zhang, S. C., Wernig, M., Duncan, I. D., Brüstle, O., and Thomson, J. A. (2001). In vitrodifferentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133. doi: 10.1038/nbt1201-1129
75. Zhang, Y., Pak, C., Han, Y., Ahlenius, H., Zhang, Z., Chanda, S., et al. (2013). Rapid single-step induction of functional neurons from human pluripotent stem cells. Neuron 78, 785-798. doi: 10.1016/j.neuron.2013.05.029
76. Zhu, H., Lensch, M. W., Cahan, P., and Daley, G. Q. (2011). Investigating monogenic and complex diseases with pluripotent stem cells. Nat. Rev. Genet. 12, 266-275. doi: 10.1038/nrg2951