On becoming neural: What the embryo can tell us about differentiating neural stem cells

American Journal of Stem Cells

Volumn 2, Issue 2, 2013, Pages 74-94

  Moody, Sally A ^a,b   Klein, Steven L ^a   Karpinski, Beverley A ^a   Maynard, Thomas M ^a,b   Lamantia, Anthony Samuel ^a,b  

^a Department of Anatomy and Regenerative Biology ^*  (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Embryoid bodies; FoxD4; FoxD4l1.1; FoxD5; Neural ectodermal precursors; Neural fate stabilization; Neural gene regulatory network; Neural induction; Neural plate stem cells; Neural progenitors; Retinoic acid induction

Indexed keywords

BETA TUBULIN; BONE MORPHOGENETIC PROTEIN; CYTOKERATIN; FORKHEAD TRANSCRIPTION FACTOR; GEMININ; LEUKEMIA INHIBITORY FACTOR RECEPTOR; NERVE CELL ADHESION MOLECULE; NESTIN; NEUROFILAMENT PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR; NEUROGENIN 1; NUCLEAR PROTEIN; SMAD PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR MSX1; TRANSCRIPTION FACTOR OTX2; TRANSCRIPTION FACTOR SOX; XENOPUS PROTEIN; ZINC FINGER PROTEIN;

DOWN REGULATION; GENE EXPRESSION; GENE REGULATORY NETWORK; HUMAN; IMMUNOFLUORESCENCE TEST; NERVE CELL DIFFERENTIATION; NERVE ELONGATION; NEURAL STEM CELL; NEUROECTODERM; PLURIPOTENT STEM CELL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVIEW; STEM CELL TRANSPLANTATION; TRANSCRIPTION INITIATION; UPREGULATION; WNT SIGNALING PATHWAY;

EID: 84891738270     PISSN: None     EISSN: 21604150     Source Type: Journal    
DOI: None     Document Type: Review

References (102)

1. Spemann H, Mangold H. Induction of embryonic primordial by implantation of organizers from a different species. Reprinted in Inter J Dev Biol 2001; 45: 13-38.
2. Tropepe V, Hitoshi S, Sirard C, Mak TW, Rossant J, van der Kooy D. Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 2000; 30: 65-78.
3. Devine MJ, Ryten M, Vodicka P, Thomson AJ, Burdon T, Houlden H, Cavaleri F, Nagano M, Drummond NJ, Taanman JW, Schapira AH, Gwinn K, Hardy J, Lewis PA, Kunath T. Parkinson's disease induced pluripotent stem cells with triplication of the a-synuclein locus. Nat Commun 2011; 2: 440.
4. Wichterle H, Lieberam I, Poter JA, Jessell TM. Directed differentiation of embryonic stem cells into motor neurons. Cell 2002; 110: 385-397.
5. De Robertis EM, Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 2004; 20: 285-308.
6. Stern CD. Neural induction: old problem, new findings, yet more questions. Development 2005; 132: 2007-2021.
7. Itoh K, Sokol SY. Early Development of Epidermis and Neural Tissue. In: Moody SA, editor. Principles of Developmental Genetics. New York: Elsevier 2007; pp: 241-257.
8. Levine AJ, Brivanlou AH. Proposal of a model of mammalian neural induction. Dev Biol 2007; 308: 247-256.
9. Rogers CD, Moody SA, Casey ES. Neural induction and factors that stabilize a neural fate. Birth Defects Res C Embryo Today 2009; 87: 249-262.
10. Sasai Y. Identifying the missing links: genes that connect neural induction and primary neurogenesis in vertebrate embryos. Neuron 1998; 21: 455-458.
11. Kuo JS, Patel M, Gamse J, Merzdorf C, Liu X, Apekin V, Sive H. Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus. Development 1998; 125: 2867-2882.
12. Streit A, Lee KJ, Woo I, Roberts C, Jessell TM, Stren CD. Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 1998; 125: 507-519.
13. Streit A, Berliner AJ, Papanayotou C, Sirulnik A, Stern CD. Initiation of neural induction by FGF signaling before gastrulation. Nature 2000; 406: 74-78.
14. Wilson SI, Graziano E, Harland R, Jessell TM, Edlund T. An early requirement for FGF signalling in the acquisition of neural cell fate in the chick embryo. Curr Biol 2000; 10: 421-429.
15. Sheng G, dos Reis M, Stern CD. Churchill, a zinc finger transcriptional activator regulates the transition between gastrulation and neurulation. Cell 2003; 115: 603-613.
16. Verschueren K, Remacle JE, Collart C, Kraft H, Baker BS, Tylzanowski P, Nelles L, Wuytens G, Su MT, Bodmer R, Smith JC, Huylebroeck D. SIP1, a novel zinc finger/homeodomain repressor, interacts with Smad proteins and binds to 5'-CACCT sequences in candidate target genes. J Biol Chem1999; 274: 20489-20498.
17. Eisaki A, Kuroda H, Fukui A, Asashima M. XSIP1, a member of two-handed zinc finger proteins, induced anterior neural markers in Xenopus laevis animal cap. BBRC 2000; 271: 151-157.
18. Nitta KR, Tanegashima K, Takahashi S, Asashima M. XSIP1 is essential for early neural gene expression and neural differentiation by suppression of BMP signaling. Dev Biol 2004; 274: 258-267.
19. Nitta KR, Takahashi S, Haramoto Y, Fukuda M, Tanegashima K, Onuma Y, Asashima M. The Nterminus zinc finger domain of Xenopus SIP1 is important for neural induction, but not for suppression of Xbra expression. Int J Dev Biol 2007; 51: 321-325.
20. Snir M, Ofir R, Elias S, Frank D. Xenopus laevis POU91 protein, an Oct3/4 homologue, regulates competence transitions from mesoderm to neural cell fates. EMBO J 2006; 25: 3664-3674.
21. Greber B, Coulon P, Zhang M, Moritz S, Frank S, Muller-Molina AJ, Arauzo-Bravo MJ, Han DW, Pape HC, Scholer HR. FGF signaling inhibits neural induction in human embryonic stem cells. EMBO J 2012; 30: 4874-4884.
22. Chng Z, Teo A, Pedersen RA, Vallier L. SIP1 mediates cell-fate decisions between neuroectoderm and mesendoderm in human pluripotent stem cells. Cell Stem Cell 2010; 6: 59-70.
23. Taylor JJ, Wang T, Kroll KL. Tcfand Vent-binding sites regulate neural-specific geminin expression in the gastrula embryo. Dev Biol 2006; 289: 494-506.
24. Rogers C, Archer TC, Cunningham DD, Grammer TC, Silva Casey EM. Sox3 expression is maintained by FGF signaling and restricted to the neural plate by Vent proteins in the Xenopus embryo. Dev Biol 2008; 313: 307-319.
25. Kroll KL, Salic AN, Evans LM, Kirschner MW. Geminin, a neuralizing molecule that demarcates the future neural plate at the onset of gastrulation. Development 1998; 125: 3247-3258.
26. Glavic A, Gomez-Skarmeta JL, Mayor R. Xiro-1 controls mesoderm patterning by repressing bmp-4 expression in the Spemann organizer. Dev Dyn 2001; 222: 368-376.
27. Gomez-Skarmeta J, de La Calle-Mustienes E, Modolell J. The Wnt-activated Xiro1 gene encodes a repressor that is essential for neural development and downregulates Bmp4. Development 2001; 128: 551-560.
28. Rogers CD, Harafuji N, Archer T, Cunningham DD, Casey ES. Xenopus Sox3 activates sox2 and geminin and indirectly represses Xvent2 expression to induce neural progenitor formation at the expense of non-neural ectodermal derivatives. Mech Dev 2009; 126: 42-55.
29. Yan B, Neilson KM, Moody SA. FoxD5 plays a critical upstream role in regulating neural fate and onset of differentiation. Dev Biol 2009; 329: 80-95.
30. Yan B, Neilson KM, Moody SA. Microarray identification of novel downstream targets of FoxD5, a critical component of the neural ectodermal transcriptional network. Dev Dyn 2010; 239: 3467-3480.
31. Hyodo-Miura J, Urushiyama S, Nagai S, Nishita M, Ueno N, Shibuya H. Involvement of NLK and Sox11 in neural induction in Xenopus development. Genes Cells 2002; 7: 487-96.
32. Chaddah R, Arntfield M, Runciman S, Clarke L, van der Kooy D. Clonal neural stem cells from human embryonic stem cell colonies. J Neurosci 2012; 32: 7771-7781.
33. Neely MD, Litt MJ, Tidball AM, Li GG, Aboud AA, Hopkins CR, Chamberlin R, Hong CC, Ess KC, Bowman AB. DMH1, a highly selective small molecule BMP inhibitor promotes neurogenesis of hiPSCs: comparison of PAX6 and Sox1 expression during neural induction. ACS Chem Neurosci 2012; 3: 482-491.
34. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, Kroll KL. Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 2005; 19: 1723-1734.
35. Seo S, Kroll KL. Geminin's double life: chromatin connections that regulate transcription at the transition from proliferation to differentiation. Cell Cycle 2006; 5: 374-379.
36. Sullivan SA, Akers L, Moody SA. foxD5a, a Xenopus winged helix gene, maintains an immature neural ectoderm via transcriptional repression that is dependent on the C-terminal domain. Dev Biol 2001; 232: 439-457.
37. Brewster R, Lee J, Ruiz I Altaba A. Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 1998; 393: 579-583.
38. Penzel R, Oschwald R, Chen Y, Tacke L, Grunz H. Characterization and early embryonic expression of a neural specific transcription factor xSOX3 in Xenopus laevis. Int J Dev Biol 1997; 41: 667-677.
39. Mizuseki K, Kishi M, Matsui M, Nakanishi S, Sasai Y. Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development 1998; 125: 579-587.
40. Kishi M, Mizuseki K, Sasai N, Yamazaki H, Shiota K, Nakanishi S, Sasai Y. Requirement of Sox2-mediated signaling for differentiation of early Xenopus neuroectoderm. Development 2000; 127: 791-800.
41. Bylund M, Andersson E, Novitch BG, Muhr J. Vertebrate neurogenesis is counteracted by Sox1-3 activity. Nat Neurosci 2003; 6: 1162-1168.
42. Graham V, Khudyakov J, Ellis P, Pevny L. SOX2 functions to maintain neural progenitor identity. Neuron 2003; 39: 749-765.
43. Wegner M, Stolt CC. From stem cells to neurons and glia: a Soxist's view of neural development. Trends Neurosci 2005; 28: 583-588.
44. Wang TW, Sromberg GP, Whitney JT, Brower NW, Klymkowsky MW, Parent JM. Sox3 expression identifies neural progenitors in persistent neonatal and adult mouse forebrain germinative zones. J Comp Neurol 2006; 497: 88-100.
45. Li M, Pevny L, Lovell-Badge R, Smith A. Generation of purified neural precursors from embryonic stem cells by lineage selection. Curr Biol 1998; 8: 971-974.
46. Zappone MV, Galli R, Catena R, Meani N, De Biasi S, Mattei E, Tiveron C, Vescovi AL, LovellBadge R, Ottolenghi S, Nicolis SK. Sox2 regulatory sequences direct expression of a (beta) geo transgene to telencephalic neural stem cells and precursors of the mouse embryo, revealing regionalization of gene expression in CNS stem cells. Development 2000; 127: 2367-2382.
47. Ellis P, Fagan BM, Magness ST, Hutton S, Taranova O, Hayashi S, McMahon A, Rao M, Pevny L. SOX2, a persistent marker for multipotential neural stem cells derived from embryonic stem cells, the embryo or the adult. Dev Neurosci 2004; 26: 148-165.
48. Bani-Yaghoub M, Tremblay RG, Lei JX, Zhang D, Zurakowski B, Sandhu JK, Smith B, RibeccoLutkiewicz M, Kennedy J, Walker PR, Sikorska M. Role of Sox2 in the development of the mouse neocortex. Dev Biol 2006; 295: 52-66.
49. Bergsland M, Werme M, Malewicz M, Perlmann T, Muhr J. The establishment of neuronal properties is controlled by Sox4 and Sox11. Genes Dev 2006; 20: 3475-3486.
50. Uwanogho D, Rex M, Cartwright EJ, Pearl G, Healy C, Scotting PJ, Sharpe PT. Embryonic expression of the chicken Sox2, Sox3 and Sox11 genes suggests an interactive role in neuronal development. Mech Dev 1995; 49: 23-36.
51. Wegner M. From head to toes: the multiple facets of Sox proteins. Nucleic Acids Res 1999; 27: 1409-1420.
52. Mizuseki K, Kishi M, Shiota K, Nakanishi S, Sasai Y. SoxD: an essential mediator of induction of anterior neural tissues in Xenopus embryos. Neuron 1998; 21: 77-85.
53. Nakata K, Nagai T, Aruga J, Mikoshiba K. Xenopus Zic3, a primary regulator both in neural and neural crest development. Proc Natl Acad Sci USA 1997; 94: 11980-11985.
54. Nakata K, Nagai T, Aruga J, Mikoshiba K. Xenopus Zic family and its role in neural and neural crest development. Mech Dev 1998; 75: 43-51.
55. Aruga J, Tohmonda T, Homma S, Mikoshiba K. Zic1 promotes expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev Biol 2002; 244: 329-341.
56. Inoue T, Ota M, Ogawa M, Mikoshiba J, Aruga J. Zic1 and Zic3 regulate medial forebrain development through expansion of neuronal progenitors. J Neurosci 2007; 27: 5461-5473.
57. Gomez-Skarmeta JL, Diez del Corral R, de la Calle-Mustienes E, Ferré-Marcó D, Modolell J. Araucan and caupolican, two members of the novel iroquois complex, encode homeoproteins that control proneural and vein-forming genes. Cell 1996; 85: 95-105.
58. Bellefroid EJ, Kobbe A, Gruss P, Pieler T, Gurdon JB, Papalopulu N. Xiro3 encodes a Xenopus homolog of the Drosophila Iroquois genes and functions in neural specification. EMBO J 1998; 17: 191-203.
59. Gómez-Skarmeta JL, Glavic A, de la Calle-Mustienes E, Modolell J, Mayor R. Xiro, a Xenopus homolog of the Drosophila Iroquois complex genes, controls development at the neural plate. EMBO J 1998; 17: 181-190.
60. de la Calle-Mustienes E, Glavic A, Modolell J, Gomez-Skarmeta JL. Xiro homeoproteins coordinate cell cycle exit and primary neuron formation by upregulating neuronal-fate repressors and downregulating the cell-cycle inhibitor XGadd45-γ. Mech Dev 2002; 119: 69-80.
61. Levine M, Davidson EH. Gene regulatory networks for development. Proc Natl Acad Sci USA 2005; 102: 4936-4942.
62. Sölter M, Köster M, Hollemann T, Brey A, Pieler T, Knöchel W. Characterization of a subfamily of related winged helix genes, XFD-12/12'/12" (XFLIP), during Xenopus embryogenesis. Mech Dev 1999; 89: 161-165.
63. Fetka I, Doederlein G, Bouwmeester T. Neuroectodermal specification and regionalization of the Spemann organizer in Xenopus. Mech Dev 2000; 93: 49-58.
64. Shapira E, Marom K, Levy V, Yelin R, Fainsod A. The xvex-1 antimorph reveals the temporal competence for organizer formation and an early role for ventral homeobox genes. Mech Dev 2000; 90: 77-87.
65. Papanayotou C, Mey A, Birot AM, Saka Y, Boast S, Smith JC, Samarut J, Stern CD. A mechanism regulating the onset of sox2 expression in the embryonic neural plate. PLoS 2008; 6: 109-123.
66. Carlsson P, Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev Biol 2002; 250: 1-23.
67. Pohl BS, Knochel W. Of Fox and Frogs: Fox (fork head/winged helix) transcription factors in Xenopus development. Gene 2005; 344: 21-32.
68. Wijcher PJ, Burbach JP, Smidt MP. In control of biology: of mice, men and Foxes. Biochem J 2006; 397: 233-246.
69. Hannenhalli S, Kaestner KH. The evolution of Fox genes and their role in development and disease. Nat Rev Genet 2009; 10: 233-240.
70. Jackson BC, Carpenter C, Nebert DW, Vasiliou V. Update of human and mouse forkhead box (Fox) gene families. Hum Genomics 2010; 4: 345-352.
71. Zaret KS. Regulatory phases of early liver development: Paradigms of organogenesis. Nat Rev Genet 2002; 3: 499-512.
72. Zaret KS, Watts J, Xu J, Wandzioch E, Smale ST, Sekiya T. Pioneer factors, genetic competence, and inductive signaling: programming liver and pancreas progenitors from the endoderm. Cold Spring Harb Symp Quant Biol 2008; 73: 119-126.
73. Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 2011; 25: 2227-2241.
74. Cirillo L, Lin FR, Cuesta I, Jarnik M, Friedman D, Zaret KS. Opening of compacted chromatin by early developmental transcription factors HNF3 (FOXA) and GATA-4. Molec Cell 2002; 9: 279-289.
75. Ptashne M. How eukaryotic transcriptional activators work. Nature 1988; 335: 683-689.
76. Schuddekopf K, Schorpp M, Boehm T. The whn transcription factor encoded by the nude locus contains an evolutionarily conserved and functionally indispensable activation domain. Proc Natl Acad Sci USA 1996; 93: 9661-9664.
77. Neilson KM, Klein SL, Mhaske P, Mood K, Daar IO, Moody SA. Specific domains of FoxD4/5 activate and repress neural transcription factor genes to control the progression of immature neural ectoderm to differentiating neural plate. Dev Biol 2012; 365: 363-375.
78. Klein SL, Neilson KM, Orban J, Yaklichlin S, Hoffbauer J, Mood K, Daar IO, Moody SA. Conserved structural domains in FoxD4L1, a neural forkhead box transcription factor, are required to repress or activate target genes. PloS One 2013; submitted.
79. Yaklichkin S, Vekker A, Stayrook S, Lewis M, Kessler DS. Prevalence of the EHI Groucho interaction motif in the metazoan Fox family of transcriptional regulators. BMC Genomics 2007; 8: 201-218.
80. Sekiya T, Zaret KS. Repression by Groucho/TLE/Grg proteins: genomic site recruitment generates a compacted chromatin structure in vitro and impairs activator binding in vivo. Mol Cell 2007; 28: 291-303.
81. Yaklichkin S, Steiner AB, Lu Q, Kessler DS. FoxD3 and Grg4 physically interact to repress transcription and induce mesoderm in Xenopus. J Biol Chem 2007; 282: 2548-2557.
82. Essien K, Vigneau S, Apreleva S, Singh LN, Bartolomei MS, Hannenhalli S. CTCF binding site classes exhibit distinct evolutionary, genomic, epigenomic and transcriptomic features. Genome Biol 2009; 10: R131.
83. Fan Y, Newman T, Linardopoulou E, Trask BJ. Gene content and function of the ancestral chromosome fusion site in human chromosome 2q13-2q14.1 and paralogous regions. Genome Res 2002; 12: 1663-1672.
84. Freyaldenhoven B, Fried C, Wielckens K. FOXD4a and FOXD4b, two new winged helix transcription factors, are expressed in human leukemia cell lines. Gene 2004; 294: 131-140.
85. Kaestner KH, Monaghan AP, Kern H, Ang SL, Weitz S, Lichter P, Schütz G. The mouse fkh-2 gene. Implications for notochord, foregut, and midbrain regionalization. J Biol Chem 1995; 270: 30029-30035.
86. Katoh M, Katoh M. Human FOX gene family. Int J Oncology 2004; 25: 1495-1500.
87. Odenthal J, Nusslein-Volhard C. fork head domain genes in zebrafish. Dev Genes Evol 1998; 208: 245-258.
88. Suda Y, Nakabayashi J, Matsuo I, Aizawa S. Functional equivalency between Otx2 and Otx1 in development of rostral head. Development 1999; 126: 743-757.
89. Tuteja G, Kaestner KH. SnapShot: forkhead transcription factors I. Cell 2007; 130: 1160.
90. Lee HC, Tseng WA, Lo FY, Liu TM, Tsai HJ. FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis. Dev Biol 2009; 336: 232-245.
91. Jackson BC, Carpenter C, Nebert DW, Vasiliou V. Update of human and mouse forkhead box (FOX) gene families. Human Genomics 2010; 4: 345-352.
92. Minoretti P, Arra M, Emanuele E, Olivieri V, Aldeghi A, Politi P, Martinelli V, Pesenti S, Falcone C. A W148R mutation in the human FOXD4 gene segregating with dilated cardiomyopathy, obsessive-compulsive disorder, and suicidality. Int J Mol Med 2007; 19: 369-372.
93. Chen CP, Lin SP, Su YN, Su JW, Chern SR, Town DD, Wang W. Pure distal 9p deletion in a female infant with cerebral palsy. Genet Couns 2012; 23: 215-221.
94. Freitas El, Gribble SM, Simoni M, Vieira TP, Silva-Grecco RL, Balarin MA, Prigmore E, Krepisschi-Santos AC, Rosenberg C, Szuhai K, van Haeringen A, Carter NP, Gil-da-Silva-Lopes VL. Maternally inherited partial monosomy 9p (pter ® p24.1) and partial trisomy 20p (pter ® p12.1) characterized by microarray comparative genomic hybridization. Am J Med Genet A 2011; 155A: 2754-2761.
95. Avilon AA, Nicolis SK, Pevny LH, Perez L, Vivian N, Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev 2003; 17: 126-140.
96. Bhattaram P, Penzo-Mendez A, Sock E, Colmenares C, Kaneko KJ, Vassilev A, DePamphilis ML, Wegner M, Lefebvre V. Organogenesis relies on SoxC transcription factors for the survival of neural and mesenchymal progenitors. Nature Comm 2010; 1: 9.
97. Bergsland M, Ramskold D, Zaouter C, Klum S, Sandberg R, Muhr J. Sequentially acting Sox transcription factors in neural lineage development. Genes Dev 2011; 25: 2453-2464.
98. Lim JW, Hummert P, Mills JC, Kroll KL. Geminin cooperates with Polycomb to restrain multi-lineage commitment in the early embryo. Development 2011; 138: 33-44.
99. Yellajoshyula D, Patterson ES, Elitt MS, Kroll KL. Geminin promotes neural fate acquisition of embryonic stem cells by maintaining chromatin in an accessible and hyperacetylated state. Proc Natl Acad Sci USA 2011; 108: 3294-3299.
100. Yellajoshyula D, Lim JW, Thompson DM Jr, Witt JS, Patterson ES, Kroll KL. Geminin regulates the transcriptional and epigenetic status of neuronal fate-promoting genes during mammalian neurogenesis. Mol Cell Biol 2012; 32: 4549-4560.
101. Spella M, Kyrousi C, Kritikou E, Stathopoulou A, Guillemont F, Kioussis D, Pachnis V, Lygerou Z, Taraviras S. Geminin regulates cortical progenitor proliferation and differentiation. Stem Cells 2011; 8: 1269-1282.
102. Schultz KM, Banisadr G, Lastra RO, McGuire T, Kessler JA, Miller RJ, McGarry TJ. Geminin-deficient neural stem cells exhibit normal cell division and normal neurogenesis. PLoS One 2011; 6: e17736.