Neural induction, the default model and embryonic stem cells

Nature Reviews Neuroscience

Volumn 3, Issue 4, 2002, Pages 271-280

  Muñoz Sanjuán, Ignacio ^a   Brivanlou, Ali H ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; FIBROBLAST GROWTH FACTOR; ONCOPROTEIN; SOMATOMEDIN C; WNT PROTEIN; ZEBRAFISH PROTEIN;

ANIMAL; ANIMAL EMBRYO; BIOLOGICAL MODEL; CELL LINEAGE; EMBRYO INDUCTION; EMBRYONIC STRUCTURES; HISTOLOGY; HUMAN; METABOLISM; NERVE CELL; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION; STEM CELL;

ANIMALS; BONE MORPHOGENETIC PROTEINS; CELL LINEAGE; EMBRYO, NONMAMMALIAN; EMBRYONIC INDUCTION; FIBROBLAST GROWTH FACTORS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; MODELS, NEUROLOGICAL; NEURONS; ORGANIZERS, EMBRYONIC; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; WNT PROTEINS; ZEBRAFISH PROTEINS;

VERTEBRATA; XENOPUS LAEVIS;

EID: 0036546980     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn786     Document Type: Article

References (111)

1. Spemann, H. & Mangold, H. Über Induktion von Embryonanlagen durch Implantation artfremder Organisatoren. Wilhelm Roux Arch. Entw. Mech. Organ. 100, 599-638 (1924).
2. Hamburger V. Ontogeny of neuroembryology. J. Neurosci. 8, 3535-3540 (1988).
3. Hemmati-Brivanlou, A. & Melton, D. A. A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature 359, 609-614 (1992).
4. Hemmati-Brivanlou, A. & Melton, D. A. Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 77, 273-281 (1994).
5. Hemmati-Brivanlou, A., Kelly, O. G. & Melton, D. A. Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77, 283-295 (1994).
6. Smith, W. C. & Harland, R. M. Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell 70, 829-840 (1992).
7. Lamb, T. M. et al. Neural induction by the secreted polypeptide noggin. Science 262, 713-718 (1993).
8. Sasai, Y., Lu, B., Steinbeisser, H. & De Robertis, E. M. Regulation of neural induction by the Chd and Bmp-4 antagonistic patterning signals in Xenopus. Nature 376, 333-336 (1995).
9. Piccolo, S., Sasai, Y., Lu, B. & De Robertis, E. M. Dorsoventral patterning in Xenopus. inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86, 589-598 (1996).
10. Ferguson, E. L. & Anderson, K. V. Decapentaplegic acts as a morphogen to organize dorsal-ventral pattern in the Drosophiia embryo. Cell 71, 451-461 (1992).
11. Wharton, K. A., Ray, R. P & Gelbart, W. M. An activity gradient of decapentaplegic is necessary for the specification of dorsal pattern elements in the Drosophila embryo. Development 117, 807-822 (1993).
12. Godsave, S. F. & Slack, J. M. Clonal analysis of mesoderm induction in Xenopus laevis. Dev. Biol. 134, 486-490 (1989).
13. Grunz, H. & Tacke, L. Neural differentiation of Xenopus iaevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Differ. Dev. 28, 211-217 (1989).
14. Sato, S. M. & Sargent, T. D. Development of neural inducing capacity in dissociated Xenopus embryos. Dev. Biol. 134, 263-266 (1989).
15. Wilson, P A. & Hemmati-Brivanlou, A. Induction of epidermis and inhibition of neural fate by Bmp-4. Nature 376, 331-333 (1995).
16. Yamashita, H. et al. Osteogenic protein-1 binds to activin type II receptors and induces certain activin-like effects. J. Cell Biol. 130, 217-226 (1995).
17. Piccolo, S. et al. The head inducer Cerberus is a multifunctional antagonist of Nodal, BMP and Wnt signals. Nature 397, 707-710 (1999).
18. Zimmerman, L. B., De Jesus-Escobar, J. M. & Harland, R. M. The Spemann organizer signal noggin binds and i nactivates bone morphogenetic protein 4. Cell 86, 599-606 (1996).
19. Bouwmeester, T., Kim, S., Sasai, Y., Lu, B. & De Robertis, E. M. Cerberus is a head-inducing secreted factor expressed in the anterior endoderm of Spemann's organizer. Nature 382, 595-601 (1996).
20. Hansen, C. S., Marion, C. D., Steele, K., George, S. & Smith, W. C. Direct neural induction and selective inhibition of mesoderm and epidermis inducers by Xnr3. Development 124, 483-492 (1997).
21. Harland, R. & Gerhart, J. Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol. 13, 611-667 (1997).
22. Gritsman, K. et al. The EGF-CFC protein one-eyed pinhead is essential for nodal signaling. Cell 97, 121-132 (1999).
23. Shimizu, T. et al. Cooperative roles of Bozozok/Dharma and Nodal-related proteins in the formation of the dorsal organizer in zebrafish. Mech. Dev. 91, 293-303 (2000).
24. Klingensmith, J., Ang, S. L., Bachiller, D. & Rossant, J. Neural induction and patterning in the mouse in the absence of the node and its derivatives. Dev. Biol. 15, 535-549 (1999).
25. Weinstein, D. C. et al. The winged-helix transcription factor HNF-3β is required for notochord development in the mouse embryo. Cell 78, 575-588 (1994).
26. Ang, S. L. & Rossant, J. HNF-3β is essential for node and notochord formation in mouse development. Cell 78, 561-574 (1994).
27. Streit, A. et al. Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125, 507-519 (1998).
28. Streit, A., Berliner, A. J., Papnayotou, C., Sirulnik, A. & Stern, C. Initiation of neural induction by FGF signaling before gastrulation. Nature 406, 74-78 (2000).
29. Wessely, O., Agius, E., Oelgeschlager, M., Pera, E. M. & DeRobertis, E. M. Neural induction in the absence of mesoderm: β-catenin dependent expression of secreted BMP antagonists at the blastula stage in Xenopus. Dev. Biol. 234, 161-173 (2001).
30. Nakao, A. et al. Identification of Smad7, a TGF-β-inducible antagonist of TGF-β signalling. Nature 389, 631-635 (1997).
31. Casellas, R. & Brivanlou, A. H. Xenopus Smad7 inhibits both the activin and BMP pathways and acts as a neural inducer. Dev. Biol. 198, 1-12 (1998).
32. Nakayama, T., Gardner, H., Berg, L. K. & Christian, J. L. Smad6 functions as an intracellular antagonist of some TGF-β family members during Xenopusembryogenesis. Genes Cells 3, 387-934 (1998).
33. Hata, A., Lagna, G., Massague, J. & Hemmati-Brivanlou, A. Smad6 inhibits BMP/Smad1 signaling by specifically competing with the Smad4 tumor suppressor. Genes Dev. 12, 186-197 (1998).
34. Kavsak, P. et al. Smad7 binds to Smurf2 to form an E3 ubiquitin ligase that targets the TGF-β receptor for degradation. Moi. Cell 6, 1365-1375 (2000).
35. Ebisawa, T. et al. Smurf1 interacts with transforming growth factor-β type I receptor through Smad7 and induces receptor degradation. J. Biol. Chem. 276, 12477-12480 (2001).
36. Massague, J. & Chen, Y. Controling TGF-β signaling. Genes Dev. 14, 627-644 (2000).
37. Gamse, J. T. & Sive, H. Early anterior-posterior division of the presumptive neuroectoderm in Xenopus. Mech. Dev. 104, 21-36 (2001).
38. Harland, R. M. Neural induction. Curr. Opin. Genet. Dev. 10, 357-362 (2000).
39. Wilson, S. I. & Edlund, T. Neural induction: toward a unifying mechanism. Nature Neurosci. 4, 1161-1168 (2001).
40. Wilson, P. A. & Hemmati-Brivanlou, A. Vertebrate neural induction: inducers, inhibitors, and a new synthesis. Neuron 18, 699-710 (1997).
41. Wilson, S. I., Graziano, E., Harland, R., Jessell, T. M. & Edlund, T. An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo. Curr. Biol. 10, 421-429 (2000).
42. Wilson, S. I. et al. The status of Wnt signalling regulates neural and epidermal fates in the chick embryo. Nature 411, 325-330 (2001).
43. Weinstein, D. C. & Hemmati-Brivanlou, A. Neural induction. Annu. Rev. Cell Dev. Biol. 15, 411-433 (1999).
44. Wilson, P. A., Lagna, G., Suzuki, A. & Hemmati-Brivanlou, A. Concentration-dependent patterning of the Xenopus ectoderm by BMP4 and its signal transducer Smad1. Development 124, 3177-3184 (1997).
45. Malacinski, G. M., Brothers, A. J. & Chung, H. M. Disruption of components of the neural induction system of the amphibian egg with ultraviolet irradiation. Dev. Biol. 56, 24-39 (1975).
46. Kengaku, M. & Okamoto, H. Basic fibroblast growth factor induces differentiation of neural tube and neural crest lineages of cultured ectoderm cells from Xenopus gastrula. Development 119, 1067-1078 (1993).
47. Lamb, T. M. & Harland, R. M. Fibroblast growth factor is a direct neural inducer, which combined with noggin generates anterior-posterior pattern. Development 121, 3627-3636 (1995).
48. Launay, C., Fromentoux, V., Shi, D. & Boucaut, J.-C. A truncated FGF receptor blocks neural induction by endogenous Xenopus inducers. Development 122, 869-880 (1996).
49. Gammill, L. S. & Sive, H. Coincidence of otx2 and BMP4 signaling correlates with Xenopus cement gland formation. Mech. Dev. 92, 217-226 (2000).
50. Cox, W. G. & Hemmati-Brivanlou, A. Caudalization of neural fate by tissue recombination and bFGF. Development 121, 4349-4358 (1995).
51. Baker, J. C., Beddington, R. S. P. & Harland, R. M. Wnt signaling in Xenopus embryos inhibits Bmp4 expression and activates neural development. Genes Dev. 13, 3149-3159 (1999).
52. Gomez-Skarmeta, J. L., De La Calle-Mustienes & Modolell, J. The Wnt-activated Xirol gene encodes a repressor that is essential for neural development and downregulates Bmp4. Development 128, 551-560 (2001).
53. Pera, E. M., Wessely, O., Li, S.-Y. & DeRobertis, E. M. Neural and head induction by insulin-like growth factor signals. Dev. Cell 1, 655-665 (2001).
54. Bohni, R. et al. Autonomous control of cell and organ size by CHICO, a Drosophila homolog of vertebrate IRS1-4. Cell 97, 865-875 (1999).
55. Verdu, J., Buratovich, M. A., Wilder, E. L. & Birnbaum, M. J. Cell autonomous regulation of cell and organ growth in Drosophila by Akt/PKB. Nature Cell Biol. 1, 500-506 (1999).
56. Dudley A. T. & Robertson E. J. Overlapping expression domains of bone morphogenetic protein family members potentially account for limited tissue defects in BMP7 deficient embryos. Dev. Dyn. 208, 349-362 (1997).
57. Matzuk, M. M. et al. Multiple defects and perinatal death in mice deficient in follistatin. Nature 374, 360-363 (1995).
58. McMahon, J. A. et al. Noggin-mediated antagonism of BMP signaling is required for growth and patterning of neural tube and somite. Genes Dev. 12, 1438-1452 (1998).
59. Simpson, E. H. et al. The mouse Cer1 (Cerberus related or homologue) gene is not required for anterior pattern formation. Dev. Biol. 213, 202-206 (1999).
60. Bachiller, D. et al. The organizer factors chordin and noggin are required for mouse forebrain development. Nature 403, 658-661 (2000).
61. Thomas, P & Beddington, R. Anterior primitive endoderm may be responsible for patterning the anterior neural plate in the mouse embryo. Curr. Biol. 6, 1487-1496 (1996).
62. Schulte-Merker, S., Lee, K. J., McMahon, A. P. & Hammerschmidt, M. The zebrafish organizer requires chordino. Nature 387, 862-863 (1997).
63. Nguyen, V. H. et al. Ventral and lateral regions of the zebrafish gastrula, including the neural crest progenitors, are established by a bmp2/swiri pathway of genes. Dev. Biol. 199, 93-110 (1998).
64. Kishimoto, Y, Lee, K. H., Zon, L., Hammerschmidt, M. & Schulte-Merker, S. The molecular nature of zebrafish swirl: BMP2 function is essential during early dorsoventral patterning. Development 124, 4457-4466 (1997).
65. Dick, A. et al. Essential role of Bmp7 (snailhouse) and its prodomain in dorsoventral patterning of the zebrafish embryo. Development 127, 343-354 (2000).
66. Schmid, B. et al. Equivalent genetic roles for bmp7/ snaiihouse and bmp2b/swiri in dorsoventral pattern formation. Development 127, 957-967 (2000).
67. Gonzalez, E. M. et al. Head and trunk in zebrafish arise via coinhibition of BMP signaling by bozozok and chordin. Genes Dev. 14, 3087-3092 (2000).
68. Fekany K. et al. The zebrafish bozozok locus encodes Dharma, a homeodomain protein essential for induction of gastrula organizer and dorsoanterior embryonic structures. Development 126, 1427-1438 (1999).
69. Koos, D. S. & Ho, R. K. The nieuwkoid/dharma homeobox gene is essential for bmp2b repression in the zebrafish pregastrula. Dev. Biol. 215, 190-207 (1999).
70. Hammerschmidt, M. et al. Mutations affecting morphogenesis during gastrulation and tail formation in the zebrafish, Danio rerio. Development 123, 143-151 (1996).
71. Miller-Bertoglio, V. et al. Maternal and zygotic activity of the zebrafish ogon locus antagonizes BMP signaling. Dev. Biol. 214, 72-86 (1999).
72. Winnier, G., Blessing, M., Labosky, P. A. & Hogan, B. L. M. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116 (1995).
73. Zhang, H. & Bradley, A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development 122, 2977-2986 (1996).
74. Dudley, A. T., Lyons, K. M. & Robertson, E. J. A requirement for bone morphogenetic protein-7 during development of the mammalian kidney and eye. Genes Dev. 9, 2795-2807 (1995).
75. Luo, G. et al. BMP-7 is an inducer of nephrogenesis, and is also required for eye development and skeletal patterning. Genes Dev. 9, 2808-2820 (1995).
76. Chang, H. et al. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 126, 1631-1642 (1999).
77. Tremblay, K. D., Dunn, N. R. & Robertson, E. J. Mouse embryos lacking Smad1 signals display defects in extra- embryonic tissues and germ cell formation. Development 128, 3609-3621 (2001).
78. Sirard, C. et al. The tumor suppressor gene Smad4/dpc4 is required for gastrulation and later for anterior development of the mouse embryo. Genes Dev. 12, 107-119 (1998).
79. Weinstein, M., Yang, X. & Deng, C.-X. Functions of mammalian Smad genes as revealed by targeted gene disruption in mice. Cytokine Growth Factor Rev. 11, 49-58 (2000).
80. Thomson, J. A. et al. Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147 (1998).
81. Schuldiner, M., Yanuka, O., Itskovitz-Eldor, J., Melton, D. A. & Benvenisty, N. From the cover: effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc. NatiAcad. Sci. USA 97, 11307-11312 (2000).
82. Hemmati-Brivanlou, A. & Melton, D. A. Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell 88, 13-17 (1997).
83. Tropepe, V. et al. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30, 65-78 (2001).
84. Tropepe, V. et al. Distinct neural stem cells proliferate in response to EGF and FGF in the developing mouse telencephalon. Dev. Biol. 208, 166-188 (1999).
85. Ciruna, B. G., Schwartz, L., Harpal, K., Yamaguchi, T. P & Rossant, J. Chimeric analysis of fibroblast growth factor receptor-1 (Fgfr1) function: a role for FGFR1 in morphogenetic movement through the primitive streak. Development 124, 2829-2841 (1997).
86. Taupin, P. et al. FGF-2-responsive neural stem cell proliferation requires CCg, a novel autocrine/paracrine cofactor. Neuron 28, 385-397 (2000).
87. Reubinoff, B. E. et al. Neural progenitors from human embryonic stem cells. Nature Neurosci. 19, 1134-1140 (2001).
88. Zhang, S., Wernig, M., Duncan, I. D., Brustle, O. & Thomson, J. A. In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nature Neurosci. 19, 1129-1133 (2001).
89. Elefanty, A. G., Robb, L., Bimer, R. & Begley, C. G. Hematopoietic-specific genes are not induced during the in vitro differentiation of sci-null embryonic stem cells. Blood 90, 1435-1447 (1997).
90. Mukhopadhyay, M. et al. Dickkopf1 is required for embryonic head induction and limb morphogenesis in the mouse. Dev. Cell 1, 423-434 (2001).
91. LeSueur, J. A. & Graff, J. M. Spemann organizer activity of Smad. Development 126, 137-146 (1999).
92. Howell, M. et al. Xenopus Smad4P is the co-Smad component of developmentally regulated transcription factor complexes responsible for induction of early mesodermal genes. Dev. Biol. 214, 354-369 (1999).
93. BjörkJund, L. M. et al. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl Acad. Sci. USA 10, 1073-1079 (2002).
94. Kawasaki, H. et al. Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40 (2000).
95. Servetnick, M. & Grainger, R. M. Changes in neural and lens competence in Xenopus ectoderm: evidence for an autonomous developmental timer. Development 112, 177-188 (1991).
96. Lim, D. A. et al. Noggin antagonizes BMP signaling to create a niche for adult neurogenesis. Neuron 28, 713-726 (2000).
97. Gross, R. E. et al. Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells. Neuron 17, 595-606 (1996).
98. Gage, F. H. Mammalian neural stem cells. Science 287, 1433-1438 (2000).
99. Doetsch, F., Caille, I., Lim, D. A., Garcia-Verdugo, J. M. & Alvarez-Buylla, A. Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97, 703-716 (1999).
100. Tropepe, V. et al. Retinal stem cells in the adult mammalian eye. Science 287, 2032-2036 (2000).
101. Kornblum, H. I. & Geschwind, D. H. Molecular markers in CNS stem cell research: hitting a moving target. Nature Neurosci. 2, 843-846 (2001).
102. Chen, Z-F., Paquette, A. J. & Anderson, D. J. NRSF/REST is required in vivo for repression of multiple neuronal target genes during embryogenesis. Nature Genet. 20, 136-142. (1998).
103. Huang, Y., Myers, S. J. & Dingledine, R. Transcriptional repression by REST: recruitment of Sin3A and histone deacetylase to neuronal genes. Nature Neurosci. 2, 867-872 (1999).
104. Jepsen, K. et al. Combinatorial roles of the nuclear receptor corepressor in transcription and development. Cell 102, 753-763 (2000).
105. Kinoshita, M., Hatada, S., Asashima, M. & Noda, M. HMG-X, a Xenopus gene encoding an HMG1 homolog, is abundantly expressed in the developing nervous system. FEBS Lett. 352, 191-196 (1994).
106. Schier, A. F. & Shen, M. M. Nodal signalling in vertebrate development. Nature 403, 385-389 (2000).
107. Munoz-Sanjuan, I. & Brivanlou, A. H. Early posterior/ventral fate specification in the vertebrate embryo. Dev. Biol. 237, 1-17 (2001).
108. Chang, C. et al. Twisted gastrulation can function as a BMP antagonist. Nature 410, 483-487 (2001).
109. Zhu, H., Kavsak, P., Abdollah, S., Wrana, J. L. & Thomsen, G. H. A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature 400, 687-693 (1999).
110. Wang, W., Mariani, F. V., Harland, R. M. & Luo, K. Ski represses bone morphogenetic protein signaling in Xenopus and mammalian cells. Proc. Natl Acad. Sci. USA 97, 14394-14399 (2000).
111. Nomura, T. et al. Ski is a component of the histone deacetylase complex required for transcriptional repression by Mad and thyroid hormone receptor. Genes Dev. 13, 412-423 (1999).