Retinoic acid signaling and neuronal differentiation

Cellular and Molecular Life Sciences

Volumn 72, Issue 8, 2015, Pages 1559-1576

  Janesick, Amanda ^a   Wu, Stephanie Cherie ^a   Blumberg, Bruce ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Neurogenesis; Proliferation differentiation switch; Retinoic acid receptor

Indexed keywords

BONE MORPHOGENETIC PROTEIN; CALCIUM ION; CELL PROTEIN; CRABP2 PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR; FABP5 PROTEIN; FIBROBLAST GROWTH FACTOR; ISOCITRATE DEHYDROGENASE 1; RETINAL DEHYDROGENASE; RETINOIC ACID; RETINOIC ACID RECEPTOR; TRANSCRIPTION FACTOR ETS; UNCLASSIFIED DRUG; ANTINEOPLASTIC AGENT; CELL CYCLE PROTEIN; TUMOR ANTIGEN;

AMNIOTE; ANTINEOPLASTIC ACTIVITY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARCINOGENESIS; CELL CYCLE REGULATION; CELL PROLIFERATION; CELL RENEWAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME REARRANGEMENT; DNA MODIFICATION; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENE SEQUENCE; GENOME; HUMAN; NERVE CELL DIFFERENTIATION; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NEURAL TUBE; NEUROBLASTOMA; NONHUMAN; PHENOTYPE; RECEPTOR BINDING; REVIEW; SIGNAL TRANSDUCTION; TUMOR DIFFERENTIATION; ANIMAL; CHEMISTRY; GENETICS; METABOLISM; NEOPLASMS; NERVE CELL; PATHOLOGY;

INVERTEBRATA; MOLLUSCA;

ANIMALS; ANTIGENS, NEOPLASM; ANTINEOPLASTIC AGENTS; CELL CYCLE PROTEINS; HUMANS; NEOPLASMS; NEUROGENESIS; NEURONS; RECEPTORS, RETINOIC ACID; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 84925798335     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-014-1815-9     Document Type: Review

References (264)

1. Semba RD (2012) On the 'discovery' of vitamin A. Ann Nutr Metab 61(3):192-198
2. Wolf G (1978) A historical note on the mode of administration of vitamin A for the cure of night blindness. Am J Clin Nutr 31(2):290-292
3. Wald G (1933) Vitamin A in the retina. Nature 132:316-317
4. Hale F (1933) Pigs born without eyeballs. J Hered 24(3):105-106
5. Wald G (1968) The molecular basis of visual excitation. Nature 219(5156):800-807
6. Hart EB, Miller WS, McCollum EV (1916) Further studies on the nutritive deficiencies of wheat and grain mixtures and the pathological conditions produced in swine by their use. J Biol Chem 25:239-259
7. Hughes JS, Lienhardt HF, Aubel CE (1929) Nerve degeneration resulting from avitaminosis A. J Nutr 2(2):183-186
8. Aberle SBD (1933) Neurological disturbances in rats reared on diets deficient in vitamin A. J Nutr 7(4):445-461
9. Jones-Villeneuve EM, McBurney MW, Rogers KA, Kalnins VI (1982) Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J Cell Biol 94(2):253-262
10. Kuff EL, Fewell JW (1980) Induction of neural-like cells and acetylcholinesterase activity in cultures of F9 teratocarcinoma treated with retinoic acid and dibutyryl cyclic adenosine monophosphate. Dev Biol 77(1):103-115
11. Maden M (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat Rev Neurosci 8(10):755-765
12. Petkovich M, Brand NJ, Krust A, Chambon P (1987) A human retinoic acid receptor which belongs to the family of nuclear receptors. Nature 330(6147):444-450
13. Giguere V, Ong ES, Segui P, Evans RM (1987) Identification of a receptor for the morphogen retinoic acid. Nature 330(6149):624-629
14. Kruyt FA, van der Veer LJ, Mader S, van den Brink CE, Feijen A, Jonk LJ, Kruijer W, van der Saag PT (1992) Retinoic acid resistance of the variant embryonal carcinoma cell line RAC65 is caused by expression of a truncated RAR alpha. Differentiation 49(1):27-37
15. Pratt MA, Kralova J, McBurney MW (1990) A dominant negative mutation of the alpha retinoic acid receptor gene in a retinoic acid-nonresponsive embryonal carcinoma cell. Mol Cell Biol 10(12):6445-6453
16. Matsuo T, Thiele CJ (1998) p27Kip1: a key mediator of retinoic acid induced growth arrest in the SMS-KCNR human neuroblastoma cell line. Oncogene 16(25):3337-3343
17. Sasaki K, Tamura S, Tachibana H, Sugita M, Gao Y, Furuyama J, Kakishita E, Sakai T, Tamaoki T, Hashimoto-Tamaoki T (2000) Expression and role of p27(kip1) in neuronal differentiation of embryonal carcinoma cells. Brain Res Mol Brain Res 77(2):209-221
18. Franco PG, Paganelli AR, Lopez SL, Carrasco AE (1999) Functional association of retinoic acid and hedgehog signaling in Xenopus primary neurogenesis. Development 126(19):4257-4265
19. Blumberg B, Bolado J Jr, Moreno TA, Kintner C, Evans RM, Papalopulu N (1997) An essential role for retinoid signaling in anteroposterior neural patterning. Development 124(2):373-379
20. Papalopulu N, Kintner C (1996) A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development 122(11):3409-3418
21. Sharpe CR, Goldstone K (1997) Retinoid receptors promote primary neurogenesis in Xenopus. Development 124(2):515-523
22. Janesick A, Abbey R, Chung C, Liu S, Taketani M, Blumberg B (2013) ERF and ETV3L are retinoic acid-inducible repressors required for primary neurogenesis. Development 140(15):3095-3106
23. Diez del Corral R, Olivera-Martinez I, Goriely A, Gale E, Maden M, Storey K (2003) Opposing FGF and retinoid pathways control ventral neural pattern, neuronal differentiation, and segmentation during body axis extension. Neuron 40(1):65-79
24. Maden M, Gale E, Kostetskii I, Zile M (1996) Vitamin A-deficient quail embryos have half a hindbrain and other neural defects. Curr Biol 6(4):417-426
25. Maden M (2002) Retinoid signalling in the development of the central nervous system. Nat Rev Neurosci 3(11):843-853
26. Rhinn M, Dolle P (2012) Retinoic acid signalling during development. Development 139(5):843-858
27. Niederreither K, Dolle P (2008) Retinoic acid in development: towards an integrated view. Nat Rev Genet 9(7):541-553
28. Cunningham TJ, Zhao X, Sandell LL, Evans SM, Trainor PA, Duester G (2013) Antagonism between retinoic acid and fibroblast growth factor signaling during limb development. Cell Rep 3(5):1503-1511
29. Wills AE, Choi VM, Bennett MJ, Khokha MK, Harland RM (2010) BMP antagonists and FGF signaling contribute to different domains of the neural plate in Xenopus. Dev Biol 337(2):335-350
30. Dorey K, Amaya E (2010) FGF signalling: diverse roles during early vertebrate embryogenesis. Development 137(22):3731-3742
31. Yan B, Neilson KM, Moody SA (2010) Microarray identification of novel downstream targets of FoxD4L1/D5, a critical component of the neural ectodermal transcriptional network. Dev Dyn 239(12):3467-3480
32. Lee HC, Tseng WA, Lo FY, Liu TM, Tsai HJ (2009) FoxD5 mediates anterior-posterior polarity through upstream modulator Fgf signaling during zebrafish somitogenesis. Dev Biol 336(2):232-245
33. Branney PA, Faas L, Steane SE, Pownall ME, Isaacs HV (2009) Characterisation of the fibroblast growth factor dependent transcriptome in early development. PLoS One 4(3):e4951
34. Marchal L, Luxardi G, Thome V, Kodjabachian L (2009) BMP inhibition initiates neural induction via FGF signaling and Zic genes. Proc Natl Acad Sci USA 106(41):17437-17442
35. Tropepe V, Li S, Dickinson A, Gamse JT, Sive HL (2006) Identification of a BMP inhibitor-responsive promoter module required for expression of the early neural gene zic1. Dev Biol 289(2):517-529
36. Rogers CD, Ferzli GS, Casey ES (2011) The response of early neural genes to FGF signaling or inhibition of BMP indicate the absence of a conserved neural induction module. BMC Dev Biol 11:74
37. Aruga J, Mikoshiba K (2011) Role of BMP, FGF, calcium signaling, and Zic proteins in vertebrate neuroectodermal differentiation. Neurochem Res 36(7):1286-1292
38. Merzdorf CS (2007) Emerging roles for zic genes in early development. Dev Dyn 236(4):922-940
39. Rogers CD, Harafuji N, Archer T, Cunningham DD, Casey ES (2009) 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 126(1-2):42-55
40. Aruga J, Tohmonda T, Homma S, Mikoshiba K (2002) Zic1 promotes the expansion of dorsal neural progenitors in spinal cord by inhibiting neuronal differentiation. Dev Biol 244(2):329-341
41. Ebert PJ, Timmer JR, Nakada Y, Helms AW, Parab PB, Liu Y, Hunsaker TL, Johnson JE (2003) Zic1 represses Math1 expression via interactions with the Math1 enhancer and modulation of Math1 autoregulation. Development 130(9):1949-1959
42. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122(6):947-956
43. Lim LS, Loh YH, Zhang W, Li Y, Chen X, Wang Y, Bakre M, Ng HH, Stanton LW (2007) Zic3 is required for maintenance of pluripotency in embryonic stem cells. Mol Biol Cell 18(4):1348-1358
44. Loh YH, Wu Q, Chew JL, Vega VB, Zhang W, Chen X, Bourque G, George J, Leong B, Liu J, Wong KY, Sung KW, Lee CW, Zhao XD, Chiu KP, Lipovich L, Kuznetsov VA, Robson P, Stanton LW, Wei CL, Ruan Y, Lim B, Ng HH (2006) The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet 38(4):431-440
45. Papanayotou C, De Almeida I, Liao P, Oliveira NM, Lu SQ, Kougioumtzidou E, Zhu L, Shaw A, Sheng G, Streit A, Yu D, Wah Soong T, Stern CD (2013) Calfacilitin is a calcium channel modulator essential for initiation of neural plate development. Nat Commun 4:1837
46. 2+ mediates neural induction in the amphibian embryo. Proc Natl Acad Sci USA 91(26):12639-12643
47. Leclerc C, Daguzan C, Nicolas MT, Chabret C, Duprat AM, Moreau M (1997) L-type calcium channel activation controls the in vivo transduction of the neuralizing signal in the amphibian embryos. Mech Dev 64(1-2):105-110
48. Leclerc C, Lee M, Webb SE, Moreau M, Miller AL (2003) Calcium transients triggered by planar signals induce the expression of ZIC3 gene during neural induction in Xenopus. Dev Biol 261(2):381-390
49. 2+-induced methyltransferase xPRMT1b controls neural fate in amphibian embryo. Proc Natl Acad Sci USA 102(42):15128-15133
50. Lim JW, Hummert P, Mills JC, Kroll KL (2011) Geminin cooperates with Polycomb to restrain multi-lineage commitment in the early embryo. Development 138(1):33-44
51. Spella M, Britz O, Kotantaki P, Lygerou Z, Nishitani H, Ramsay RG, Flordellis C, Guillemot F, Mantamadiotis T, Taraviras S (2007) Licensing regulators Geminin and Cdt1 identify progenitor cells of the mouse CNS in a specific phase of the cell cycle. Neuroscience 147(2):373-387
52. Seo S, Herr A, Lim JW, Richardson GA, Richardson H, Kroll KL (2005) Geminin regulates neuronal differentiation by antagonizing Brg1 activity. Genes Dev 19(14):1723-1734
53. Brewster R, Lee J, i Altaba AR (1998) Gli/Zic factors pattern the neural plate by defining domains of cell differentiation. Nature 393(6685):579-583
54. Yan B, Neilson KM, Moody SA (2009) Notch signaling downstream of foxD5 promotes neural ectodermal transcription factors that inhibit neural differentiation. Dev Dyn 238(6):1358-1365
55. Moody SA, Klein SL, Karpinski BA, Maynard TM, Lamantia AS (2013) On becoming neural: what the embryo can tell us about differentiating neural stem cells. Am J Stem Cells 2(2):74-94
56. Papanayotou C, Mey A, Birot AM, Saka Y, Boast S, Smith JC, Samarut J, Stern CD (2008) A mechanism regulating the onset of Sox2 expression in the embryonic neural plate. PLoS Biol 6(1):e2
57. Rogers CD, Moody SA, Casey ES (2009) Neural induction and factors that stabilize a neural fate. Birth Defects Res C Embryo Today 87(3):249-262
58. Chalmers AD, Welchman D, Papalopulu N (2002) Intrinsic differences between the superficial and deep layers of the Xenopus ectoderm control primary neuronal differentiation. Dev Cell 2(2):171-182
59. Sharpe C, Goldstone K (2000) The control of Xenopus embryonic primary neurogenesis is mediated by retinoid signalling in the neurectoderm. Mech Dev 91(1-2):69-80
60. Hartenstein V (1989) Early neurogenesis in Xenopus: the spatio-temporal pattern of proliferation and cell lineages in the embryonic spinal cord. Neuron 3(4):399-411
61. Carrasco AE, Blumberg B (2004) A Critical Role for Retinoid Receptors in Axial Patterning and Neuronal Differentiation. In: Grunz H (ed) The Vertebrate Organizer. Springer Science & Business Media, New York, pp 279-298
62. Wullimann MF, Rink E, Vernier P, Schlosser G (2005) Secondary neurogenesis in the brain of the African clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1, and NeuroD expression. J Comp Neurol 489(3):387-402
63. Hevner RF, Zecevic N (2006) Pioneer Neurons and Interneurons in the Developing Subplate: Molecular Markers, Cell Birthdays, and Neurotransmitters. In: Erzurumlu R, Guido W, Molnár Z (eds) Development and Plasticity in Sensory Thalamus and Cortex. Springer US, New York, pp 1-18
64. Raper J, Mason C (2010) Cellular strategies of axonal pathfinding. Cold Spring Harb Perspect Biol 2(9):a001933
65. Bystron I, Rakic P, Molnar Z, Blakemore C (2006) The first neurons of the human cerebral cortex. Nat Neurosci 9(7):880-886
66. Hyatt GA, Schmitt EA, Marsh-Armstrong N, McCaffery P, Drager UC, Dowling JE (1996) Retinoic acid establishes ventral retinal characteristics. Development 122(1):195-204
67. Diez del Corral R, Morales A (2014) Retinoic Acid Signaling during Early Spinal Cord Development. J Dev Biol 2(3):174-197
68. Kudoh T, Wilson SW, Dawid IB (2002) Distinct roles for Fgf, Wnt and retinoic acid in posteriorizing the neural ectoderm. Development 129(18):4335-4346
69. Glover JC, Renaud JS, Rijli FM (2006) Retinoic acid and hindbrain patterning. J Neurobiol 66(7):705-725
70. Wilson L, Gale E, Chambers D, Maden M (2004) Retinoic acid and the control of dorsoventral patterning in the avian spinal cord. Dev Biol 269(2):433-446
71. Kelley MW, Turner JK, Reh TA (1994) Retinoic acid promotes differentiation of photoreceptors in vitro. Development 120(8):2091-2102
72. Osakada F, Ikeda H, Mandai M, Wataya T, Watanabe K, Yoshimura N, Akaike A, Sasai Y, Takahashi M (2008) Toward the generation of rod and cone photoreceptors from mouse, monkey and human embryonic stem cells. Nat Biotechnol 26(2):215-224
73. Jacobs S, Lie DC, DeCicco KL, Shi Y, DeLuca LM, Gage FH, Evans RM (2006) Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc Natl Acad Sci USA 103(10):3902-3907
74. Siegenthaler JA, Ashique AM, Zarbalis K, Patterson KP, Hecht JH, Kane MA, Folias AE, Choe Y, May SR, Kume T, Napoli JL, Peterson AS, Pleasure SJ (2009) Retinoic acid from the meninges regulates cortical neuron generation. Cell 139(3):597-609
75. McCaffery PJ, Adams J, Maden M, Rosa-Molinar E (2003) Too much of a good thing: retinoic acid as an endogenous regulator of neural differentiation and exogenous teratogen. Eur J Neurosci 18(3):457-472
76. Semmler H, Chiodin M, Bailly X, Martinez P, Wanninger A (2010) Steps towards a centralized nervous system in basal bilaterians: insights from neurogenesis of the acoel Symsagittifera roscoffensis. Dev Growth Differ 52(8):701-713
77. Burnett AL, Diehl NA (1964) The nervous system of Hydra. I. Types, distribution and origin of nerve elements. J Exp Zool 157:217-226
78. Galliot B, Quiquand M, Ghila L, de Rosa R, Miljkovic-Licina M, Chera S (2009) Origins of neurogenesis, a cnidarian view. Dev Biol 332(1):2-24
79. Simmons DK, Pang K, Martindale MQ (2012) Lim homeobox genes in the Ctenophore Mnemiopsis leidyi: the evolution of neural cell type specification. Evodevo 3(1):2
80. Jager M, Chiori R, Alie A, Dayraud C, Queinnec E, Manuel M (2011) New insights on ctenophore neural anatomy: immunofluorescence study in Pleurobrachia pileus (Muller, 1776). J Exp Zool B Mol Dev Evol 316B(3):171-187
81. Burkhardt P, Stegmann CM, Cooper B, Kloepper TH, Imig C, Varoqueaux F, Wahl MC, Fasshauer D (2011) Primordial neurosecretory apparatus identified in the choanoflagellate Monosiga brevicollis. Proc Natl Acad Sci USA 108(37):15264-15269
82. Canestro C, Bassham S, Postlethwait J (2005) Development of the central nervous system in the larvacean Oikopleura dioica and the evolution of the chordate brain. Dev Biol 285(2):298-315
83. Canestro C, Albalat R, Postlethwait JH (2010) Oikopleura dioica alcohol dehydrogenase class 3 provides new insights into the evolution of retinoic acid synthesis in chordates. Zoolog Sci 27(2):128-133
84. Marletaz F, Holland LZ, Laudet V, Schubert M (2006) Retinoic acid signaling and the evolution of chordates. Int J Biol Sci 2(2):38-47
85. Canestro C, Postlethwait JH, Gonzalez-Duarte R, Albalat R (2006) Is retinoic acid genetic machinery a chordate innovation? Evol Dev 8(5):394-406
86. Albalat R, Canestro C (2009) Identification of Aldh1a, Cyp26 and RAR orthologs in protostomes pushes back the retinoic acid genetic machinery in evolutionary time to the bilaterian ancestor. Chem Biol Interact 178(1-3):188-196
87. Castro LF, Lima D, Machado A, Melo C, Hiromori Y, Nishikawa J, Nakanishi T, Reis-Henriques MA, Santos MM (2007) Imposex induction is mediated through the Retinoid × Receptor signalling pathway in the neogastropod Nucella lapillus. Aquat Toxicol 85(1):57-66
88. Horiguchi T (2006) Masculinization of female gastropod mollusks induced by organotin compounds, focusing on mechanism of actions of tributyltin and triphenyltin for development of imposex. Environ Sci 13(2):77-87
89. Horiguchi T, Ohta Y, Nishikawa T, Shiraishi F, Shiraishi H, Morita M (2008) Exposure to 9-cis retinoic acid induces penis and vas deferens development in the female rock shell, Thais clavigera. Cell Biol Toxicol 24(6):553-562
90. Nishikawa J, Mamiya S, Kanayama T, Nishikawa T, Shiraishi F, Horiguchi T (2004) Involvement of the retinoid × receptor in the development of imposex caused by organotins in gastropods. Environ Sci Technol 38(23):6271-6276
91. Campo-Paysaa F, Marletaz F, Laudet V, Schubert M (2008) Retinoic acid signaling in development: tissue-specific functions and evolutionary origins. Genesis 46(11):640-656
92. Dmetrichuk JM, Carlone RL, Jones TR, Vesprini ND, Spencer GE (2008) Detection of endogenous retinoids in the molluscan CNS and characterization of the trophic and tropic actions of 9-cis retinoic acid on isolated neurons. J Neurosci 28(48):13014-13024
93. Urushitani H, Katsu Y, Ohta Y, Shiraishi H, Iguchi T, Horiguchi T (2013) Cloning and characterization of the retinoic acid receptor-like protein in the rock shell, Thais clavigera. Aquat Toxicol 142-143:403-413
94. Gutierrez-Mazariegos J, Nadendla EK, Lima D, Pierzchalski K, Jones JW, Kane M, Nishikawa J, Hiromori Y, Nakanishi T, Santos MM, Castro LF, Bourguet W, Schubert M, Laudet V (2014) A mollusk retinoic acid receptor (RAR) ortholog sheds light on the evolution of ligand binding. Endocrinology 155(11):4275-4286
95. Urushitani H, Katsu Y, Ohta Y, Shiraishi H, Iguchi T, Horiguchi T (2011) Cloning and characterization of retinoid X receptor (RXR) isoforms in the rock shell, Thais clavigera. Aquat Toxicol 103(1-2):101-111
96. Markov GV, Laudet V (2011) Origin and evolution of the ligand-binding ability of nuclear receptors. Mol Cell Endocrinol 334(1-2):21-30
97. Bridgham JT, Carroll SM, Thornton JW (2006) Evolution of hormone-receptor complexity by molecular exploitation. Science 312(5770):97-101
98. Thornton JW, Need E, Crews D (2003) Resurrecting the ancestral steroid receptor: ancient origin of estrogen signaling. Science 301(5640):1714-1717
99. Albalat R (2009) The retinoic acid machinery in invertebrates: ancestral elements and vertebrate innovations. Mol Cell Endocrinol 313(1-2):23-35
100. Morrison SJ, Kimble J (2006) Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441(7097):1068-1074
101. Salomoni P, Calegari F (2010) Cell cycle control of mammalian neural stem cells: putting a speed limit on G1. Trends Cell Biol 20(5):233-243
102. Pardee AB (1989) G1 events and regulation of cell proliferation. Science 246(4930):603-608
103. Bertoli C, Skotheim JM, de Bruin RA (2013) Control of cell cycle transcription during G1 and S phases. Nat Rev Mol Cell Biol 14(8):518-528
104. Galderisi U, Jori FP, Giordano A (2003) Cell cycle regulation and neural differentiation. Oncogene 22(33):5208-5219
105. Herrup K, Yang Y (2007) Cell cycle regulation in the postmitotic neuron: oxymoron or new biology? Nat Rev Neurosci 8(5):368-378
106. Trotter KW, Archer TK (2008) The BRG1 transcriptional coregulator. Nucl Recept Signal 6:e004
107. Seo S, Richardson GA, Kroll KL (2005) The SWI/SNF chromatin remodeling protein Brg1 is required for vertebrate neurogenesis and mediates transactivation of Ngn and NeuroD. Development 132(1):105-115
108. Ahmed M, Xu J, Xu PX (2012) EYA1 and SIX1 drive the neuronal developmental program in cooperation with the SWI/SNF chromatin-remodeling complex and SOX2 in the mammalian inner ear. Development 139(11):1965-1977
109. Lessard J, Wu JI, Ranish JA, Wan M, Winslow MM, Staahl BT, Wu H, Aebersold R, Graef IA, Crabtree GR (2007) An essential switch in subunit composition of a chromatin remodeling complex during neural development. Neuron 55(2):201-215
110. Ninkovic J, Steiner-Mezzadri A, Jawerka M, Akinci U, Masserdotti G, Petricca S, Fischer J, von Holst A, Beckers J, Lie CD, Petrik D, Miller E, Tang J, Wu J, Lefebvre V, Demmers J, Eisch A, Metzger D, Crabtree G, Irmler M, Poot R, Gotz M (2013) The BAF complex interacts with Pax6 in adult neural progenitors to establish a neurogenic cross-regulatory transcriptional network. Cell Stem Cell 13(4):403-418
111. Sherr CJ, Roberts JM (1999) CDK inhibitors: positive and negative regulators of G1-phase progression. Genes Dev 13(12):1501-1512
112. Harper JW, Adami GR, Wei N, Keyomarsi K, Elledge SJ (1993) The p21 Cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75(4):805-816
113. Polyak K, Lee MH, Erdjument-Bromage H, Koff A, Roberts JM, Tempst P, Massague J (1994) Cloning of p27Kip1, a cyclin-dependent kinase inhibitor and a potential mediator of extracellular antimitogenic signals. Cell 78(1):59-66
114. Dulic V, Kaufmann WK, Wilson SJ, Tlsty TD, Lees E, Harper JW, Elledge SJ, Reed SI (1994) p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76(6):1013-1023
115. Kato JY, Matsuoka M, Polyak K, Massague J, Sherr CJ (1994) Cyclic AMP-induced G1 phase arrest mediated by an inhibitor (p27Kip1) of cyclin-dependent kinase 4 activation. Cell 79(3):487-496
116. Hengst L, Gopfert U, Lashuel HA, Reed SI (1998) Complete inhibition of Cdk/cyclin by one molecule of p21(Cip1). Genes Dev 12(24):3882-3888
117. Reynisdottir I, Polyak K, Iavarone A, Massague J (1995) Kip/Cip and Ink4 Cdk inhibitors cooperate to induce cell cycle arrest in response to TGF-beta. Genes Dev 9(15):1831-1845
118. Cunningham JJ, Roussel MF (2001) Cyclin-dependent kinase inhibitors in the development of the central nervous system. Cell Growth Differ 12(8):387-396
119. Mitsuhashi T, Aoki Y, Eksioglu YZ, Takahashi T, Bhide PG, Reeves SA, Caviness VS Jr (2001) Overexpression of p27Kip1 lengthens the G1 phase in a mouse model that targets inducible gene expression to central nervous system progenitor cells. Proc Natl Acad Sci USA 98(11):6435-6440
120. Vernon AE, Devine C, Philpott A (2003) The cdk inhibitor p27Xic1 is required for differentiation of primary neurones in Xenopus. Development 130(1):85-92
121. Carruthers S, Mason J, Papalopulu N (2003) Depletion of the cell-cycle inhibitor p27(Xic1) impairs neuronal differentiation and increases the number of ElrC(+) progenitor cells in Xenopus tropicalis. Mech Dev 120(5):607-616
122. Su JY, Rempel RE, Erikson E, Maller JL (1995) Cloning and characterization of the Xenopus cyclin-dependent kinase inhibitor p27XIC1. Proc Natl Acad Sci USA 92(22):10187-10191
123. Ali F, Hindley C, McDowell G, Deibler R, Jones A, Kirschner M, Guillemot F, Philpott A (2011) Cell cycle-regulated multi-site phosphorylation of Neurogenin 2 coordinates cell cycling with differentiation during neurogenesis. Development 138(19):4267-4277
124. Sabherwal N, Thuret R, Lea R, Stanley P, Papalopulu N (2014) aPKC phosphorylates p27Xic1, providing a mechanistic link between apicobasal polarity and cell-cycle control. Dev Cell 31(5):559-571
125. Souopgui J, Solter M, Pieler T (2002) XPak3 promotes cell cycle withdrawal during primary neurogenesis in Xenopus laevis. EMBO J 21(23):6429-6439
126. Barth LG, Barth LJ (1964) Sequential Induction of the Presumptive Epidermis of the Rana pipiens gastrula. Biol Bull 127(3):413-427
127. Grunz H, Tacke L (1989) Neural differentiation of Xenopus laevis ectoderm takes place after disaggregation and delayed reaggregation without inducer. Cell Differ Dev 28(3):211-217
128. Saint-Jeannet JP, Huang S, Duprat AM (1990) Modulation of neural commitment by changes in target cell contacts in Pleurodeles waltl. Dev Biol 141(1):93-103
129. Leclerc C, Rizzo C, Daguzan C, Neant I, Batut J, Auge B, Moreau M (2001) Neural determination in Xenopus laevis embryos: control of early neural gene expression by calcium. J Soc Biol 195(3):327-337
130. Takata K, Yamamoto KY, Ishii I, Takahashi N (1984) Glycoproteins responsive to the neural-inducing effect of concanavalin A in Cynops presumptive ectoderm. Cell Differ 14(1):25-31
131. Gualandris L, Rouge P, Duprat AM (1985) Target cell surface glycoconjugates and neural induction in an amphibian. J Embryol Exp Morphol 86:39-51
132. Ozato K, Huang L, Ebert JD (1977) Accelerated calcium ion uptake in murine thymocytes induced by concanavalin A. J Cell Physiol 93(1):153-160
133. Greenberg DA, Carpenter CL, Messing RO (1987) Lectin-induced enhancement of voltage-dependent calcium flux and calcium channel antagonist binding. J Neurochem 48(3):888-894
134. Hemmati-Brivanlou A, Kelly OG, Melton DA (1994) Follistatin, an antagonist of activin, is expressed in the Spemann organizer and displays direct neuralizing activity. Cell 77(2):283-295
135. Hemmati-Brivanlou A, Melton DA (1994) Inhibition of activin receptor signaling promotes neuralization in Xenopus. Cell 77(2):273-281
136. Delaune E, Lemaire P, Kodjabachian L (2005) Neural induction in Xenopus requires early FGF signalling in addition to BMP inhibition. Development 132(2):299-310
137. Lee KW, Moreau M, Neant I, Bibonne A, Leclerc C (2009) FGF-activated calcium channels control neural gene expression in Xenopus. Biochim Biophys Acta 1793(6):1033-1040
138. (2+) signaling. Stem Cells 28(11):1950-1960
139. Moreau M, Neant I, Webb SE, Miller AL, Leclerc C (2008) Calcium signalling during neural induction in Xenopus laevis embryos. Philos Trans R Soc Lond B Biol Sci 363(1495):1371-1375
140. Rebellato P (2013) Calcium signaling in neurogenesis: regulation of proliferation, differentiation and migration of neural stem cells. Karolinska Institutet, Stockholm
141. Kahl CR, Means AR (2003) Regulation of cell cycle progression by calcium/calmodulin-dependent pathways. Endocr Rev 24(6):719-736
142. Boynton AL, Whitfield JF, Isaacs RJ (1976) The different roles of serum and calcium in the control of proliferation of BALB/c 3T3 mouse cells. In Vitro 12(2):120-123
143. Weissman TA, Riquelme PA, Ivic L, Flint AC, Kriegstein AR (2004) Calcium waves propagate through radial glial cells and modulate proliferation in the developing neocortex. Neuron 43(5):647-661
144. Leclerc C, Neant I, Moreau M (2012) The calcium: an early signal that initiates the formation of the nervous system during embryogenesis. Front Mol Neurosci 5:3
145. 2+ channel during early embryogenesis in Xenopus laevis. Int J Dev Biol 39(6):1027-1032
146. Otte AP, Kramer IM, Mannesse M, Lambrechts C, Durston AJ (1990) Characterization of protein kinase C in early Xenopus embryogenesis. Development 110(2):461-470
147. Otte AP, van Run P, Heideveld M, van Driel R, Durston AJ (1989) Neural induction is mediated by cross-talk between the protein kinase C and cyclic AMP pathways. Cell 58(4):641-648
148. Otte AP, Koster CH, Snoek GT, Durston AJ (1988) Protein kinase C mediates neural induction in Xenopus laevis. Nature 334(6183):618-620
149. Otte AP, Moon RT (1992) Protein kinase C isozymes have distinct roles in neural induction and competence in Xenopus. Cell 68(6):1021-1029
150. Stern CD (2005) Neural induction: old problem, new findings, yet more questions. Development 132(9):2007-2021
151. Ling F, Kang B, Sun XH (2014) Id proteins: small molecules, mighty regulators. Curr Top Dev Biol 110:189-216
152. Perk J, Iavarone A, Benezra R (2005) Id family of helix-loop-helix proteins in cancer. Nat Rev Cancer 5(8):603-614
153. Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O'Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401(6754):670-677
154. Kee Y, Bronner-Fraser M (2005) To proliferate or to die: role of Id3 in cell cycle progression and survival of neural crest progenitors. Genes Dev 19(6):744-755
155. Yun K, Mantani A, Garel S, Rubenstein J, Israel MA (2004) Id4 regulates neural progenitor proliferation and differentiation in vivo. Development 131(21):5441-5448
156. Rothschild G, Zhao X, Iavarone A, Lasorella A (2006) E Proteins and Id2 converge on p57Kip2 to regulate cell cycle in neural cells. Mol Cell Biol 26(11):4351-4361
157. Longo A, Guanga GP, Rose RB (2008) Crystal structure of E47-NeuroD1/beta2 bHLH domain-DNA complex: heterodimer selectivity and DNA recognition. Biochemistry 47(1):218-229
158. Cuende J, Moreno S, Bolanos JP, Almeida A (2008) Retinoic acid downregulates Rae1 leading to APC(Cdh1) activation and neuroblastoma SH-SY5Y differentiation. Oncogene 27(23):3339-3344
159. Lasorella A, Stegmuller J, Guardavaccaro D, Liu G, Carro MS, Rothschild G, de la Torre-Ubieta L, Pagano M, Bonni A, Iavarone A (2006) Degradation of Id2 by the anaphase-promoting complex couples cell cycle exit and axonal growth. Nature 442(7101):471-474
160. Eguren M, Porlan E, Manchado E, Garcia-Higuera I, Canamero M, Farinas I, Malumbres M (2013) The APC/C cofactor Cdh1 prevents replicative stress and p53-dependent cell death in neural progenitors. Nat Commun 4:2880
161. Ohtani N, Zebedee Z, Huot TJ, Stinson JA, Sugimoto M, Ohashi Y, Sharrocks AD, Peters G, Hara E (2001) Opposing effects of Ets and Id proteins on p16INK4a expression during cellular senescence. Nature 409(6823):1067-1070
162. Molofsky AV, Slutsky SG, Joseph NM, He S, Pardal R, Krishnamurthy J, Sharpless NE, Morrison SJ (2006) Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing. Nature 443(7110):448-452
163. Sharrocks AD (2001) The ETS-domain transcription factor family. Nat Rev Mol Cell Biol 2(11):827-837
164. Oikawa T, Yamada T (2003) Molecular biology of the Ets family of transcription factors. Gene 303:11-34
165. Le Gallic L, Virgilio L, Cohen P, Biteau B, Mavrothalassitis G (2004) ERF nuclear shuttling, a continuous monitor of Erk activity that links it to cell cycle progression. Mol Cell Biol 24(3):1206-1218
166. Sgouras DN, Athanasiou MA, Beal GJ Jr, Fisher RJ, Blair DG, Mavrothalassitis GJ (1995) ERF: an ETS domain protein with strong transcriptional repressor activity, can suppress ets-associated tumorigenesis and is regulated by phosphorylation during cell cycle and mitogenic stimulation. EMBO J 14(19):4781-4793
167. Verykokakis M, Papadaki C, Vorgia E, Le Gallic L, Mavrothalassitis G (2007) The RAS-dependent ERF control of cell proliferation and differentiation is mediated by c-Myc repression. J Biol Chem 282(41):30285-30294
168. Malynn BA, de Alboran IM, O'Hagan RC, Bronson R, Davidson L, DePinho RA, Alt FW (2000) N-myc can functionally replace c-myc in murine development, cellular growth, and differentiation. Genes Dev 14(11):1390-1399
169. Knoepfler PS, Cheng PF, Eisenman RN (2002) N-myc is essential during neurogenesis for the rapid expansion of progenitor cell populations and the inhibition of neuronal differentiation. Genes Dev 16(20):2699-2712
170. White JH, Fernandes I, Mader S, Yang XJ (2004) Corepressor recruitment by agonist-bound nuclear receptors. Vitam Horm 68:123-143
171. Kolm PJ, Sive HL (1995) Regulation of the Xenopus labial homeodomain genes, HoxA1 and HoxD1: activation by retinoids and peptide growth factors. Dev Biol 167(1):34-49
172. Langston AW, Thompson JR, Gudas LJ (1997) Retinoic acid-responsive enhancers located 3 of the Hox A and Hox B homeobox gene clusters. Functional analysis. J Biol Chem 272(4):2167-2175
173. Martinez-Ceballos E, Gudas LJ (2008) Hoxa1 is required for the retinoic acid-induced differentiation of embryonic stem cells into neurons. J Neurosci Res 86(13):2809-2819
174. Donato LJ, Suh JH, Noy N (2007) Suppression of mammary carcinoma cell growth by retinoic acid: the cell cycle control gene Btg2 is a direct target for retinoic acid receptor signaling. Cancer Res 67(2):609-615
175. Arima K, Shiotsugu J, Niu R, Khandpur R, Martinez M, Shin Y, Koide T, Cho KW, Kitayama A, Ueno N, Chandraratna RA, Blumberg B (2005) Global analysis of RAR-responsive genes in the Xenopus neurula using cDNA microarrays. Dev Dyn 232(2):414-431
176. Janesick A, Nguyen TT, Aisaki K, Igarashi K, Kitajima S, Chandraratna RA, Kanno J, Blumberg B (2014) Active repression by RARgamma signaling is required for vertebrate axial elongation. Development 141(11):2260-2270
177. Passeri D, Marcucci A, Rizzo G, Billi M, Panigada M, Leonardi L, Tirone F, Grignani F (2006) Btg2 enhances retinoic acid-induced differentiation by modulating histone H4 methylation and acetylation. Mol Cell Biol 26(13):5023-5032
178. Iacopetti P, Barsacchi G, Tirone F, Maffei L, Cremisi F (1994) Developmental expression of PC3 gene is correlated with neuronal cell birthday. Mech Dev 47(2):127-137
179. el-Ghissassi F, Valsesia-Wittmann S, Falette N, Duriez C, Walden PD, Puisieux A (2002) BTG2(TIS21/PC3) induces neuronal differentiation and prevents apoptosis of terminally differentiated PC12 cells. Oncogene 21(44):6772-6778
180. Sugimoto K, Okabayashi K, Sedohara A, Hayata T, Asashima M (2007) The role of XBtg2 in Xenopus neural development. Dev Neurosci 29(6):468-479
181. Canzoniere D, Farioli-Vecchioli S, Conti F, Ciotti MT, Tata AM, Augusti-Tocco G, Mattei E, Lakshmana MK, Krizhanovsky V, Reeves SA, Giovannoni R, Castano F, Servadio A, Ben-Arie N, Tirone F (2004) Dual control of neurogenesis by PC3 through cell cycle inhibition and induction of Math1. J Neurosci 24(13):3355-3369
182. Georgopoulou N, Hurel C, Politis PK, Gaitanou M, Matsas R, Thomaidou D (2006) BM88 is a dual function molecule inducing cell cycle exit and neuronal differentiation of neuroblastoma cells via cyclin D1 down-regulation and retinoblastoma protein hypophosphorylation. J Biol Chem 281(44):33606-33620
183. Kosaka C, Sasaguri T, Komiyama Y, Takahashi H (2001) All-trans retinoic acid inhibits vascular smooth muscle cell proliferation targeting multiple genes for cyclins and cyclin-dependent kinases. Hypertens Res 24(5):579-588
184. Luo P, Wang A, Payne KJ, Peng H, Wang JG, Parrish YK, Rogerio JW, Triche TJ, He Q, Wu L (2007) Intrinsic retinoic acid receptor alpha-cyclin-dependent kinase-activating kinase signaling involves coordination of the restricted proliferation and granulocytic differentiation of human hematopoietic stem cells. Stem Cells 25(10):2628-2637
185. Sueoka N, Lee HY, Walsh GL, Hong WK, Kurie JM (1999) Posttranslational mechanisms contribute to the suppression of specific cyclin:CDK complexes by all-trans retinoic acid in human bronchial epithelial cells. Cancer Res 59(15):3838-3844
186. Klappacher GW, Lunyak VV, Sykes DB, Sawka-Verhelle D, Sage J, Brard G, Ngo SD, Gangadharan D, Jacks T, Kamps MP, Rose DW, Rosenfeld MG, Glass CK (2002) An induced Ets repressor complex regulates growth arrest during terminal macrophage differentiation. Cell 109(2):169-180
187. Hester KD, Verhelle D, Escoubet-Lozach L, Luna R, Rose DW, Glass CK (2007) Differential repression of c-myc and cdc2 gene expression by ERF and PE-1/METS. Cell Cycle 6(13):1594-1604
188. Sawka-Verhelle D, Escoubet-Lozach L, Fong AL, Hester KD, Herzig S, Lebrun P, Glass CK (2004) PE-1/METS, an antiproliferative Ets repressor factor, is induced by CREB-1/CREM-1 during macrophage differentiation. J Biol Chem 279(17):17772-17784
189. Papadaki C, Alexiou M, Cecena G, Verykokakis M, Bilitou A, Cross JC, Oshima RG, Mavrothalassitis G (2007) Transcriptional repressor erf determines extraembryonic ectoderm differentiation. Mol Cell Biol 27(14):5201-5213
190. Shi Z, Lou M, Zhao Y, Zhang Q, Cui D, Wang K (2013) Effect of all-trans retinoic acid on the differentiation of U87 glioma stem/progenitor cells. Cell Mol Neurobiol 33(7):943-951
191. Arisi MF, Starker RA, Addya S, Huang Y, Fernandez SV (2014) All trans-retinoic acid (ATRA) induces re-differentiation of early transformed breast epithelial cells. Int J Oncol 44(6):1831-1842
192. Su D, Gudas LJ (2008) Gene expression profiling elucidates a specific role for RARgamma in the retinoic acid-induced differentiation of F9 teratocarcinoma stem cells. Biochem Pharmacol 75(5):1129-1160
193. Oliveira E, Casado M, Raldua D, Soares A, Barata C, Pina B (2013) Retinoic acid receptors' expression and function during zebrafish early development. J Steroid Biochem Mol Biol 138:143-151
194. Akanuma H, Qin XY, Nagano R, Win-Shwe TT, Imanishi S, Zaha H, Yoshinaga J, Fukuda T, Ohsako S, Sone H (2012) Identification of Stage-Specific Gene Expression Signatures in Response to Retinoic Acid during the Neural Differentiation of Mouse Embryonic Stem Cells. Front Genet 3:141
195. Ishibashi T, Usami T, Fujie M, Azumi K, Satoh N, Fujiwara S (2005) Oligonucleotide-based microarray analysis of retinoic acid target genes in the protochordate, Ciona intestinalis. Dev Dyn 233(4):1571-1578
196. Coyle DE, Li J, Baccei M (2011) Regional differentiation of retinoic acid-induced human pluripotent embryonic carcinoma stem cell neurons. PLoS One 6(1):e16174
197. Castro DS, Martynoga B, Parras C, Ramesh V, Pacary E, Johnston C, Drechsel D, Lebel-Potter M, Garcia LG, Hunt C, Dolle D, Bithell A, Ettwiller L, Buckley N, Guillemot F (2011) A novel function of the proneural factor Ascl1 in progenitor proliferation identified by genome-wide characterization of its targets. Genes Dev 25(9):930-945
198. Jacob J, Kong J, Moore S, Milton C, Sasai N, Gonzalez-Quevedo R, Terriente J, Imayoshi I, Kageyama R, Wilkinson DG, Novitch BG, Briscoe J (2013) Retinoid acid specifies neuronal identity through graded expression of Ascl1. Curr Biol 23(5):412-418
199. Nieber F, Hedderich M, Jahn O, Pieler T, Henningfeld KA (2013) NumbL is essential for Xenopus primary neurogenesis. BMC Dev Biol 13:36
200. Verdi JM, Bashirullah A, Goldhawk DE, Kubu CJ, Jamali M, Meakin SO, Lipshitz HD (1999) Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc Natl Acad Sci USA 96(18):10472-10476
201. Bani-Yaghoub M, Kubu CJ, Cowling R, Rochira J, Nikopoulos GN, Bellum S, Verdi JM (2007) A switch in numb isoforms is a critical step in cortical development. Dev Dyn 236(3):696-705
202. Alam AH, Suzuki H, Tsukahara T (2010) Retinoic acid treatment and cell aggregation independently regulate alternative splicing in P19 cells during neural differentiation. Cell Biol Int 34(6):631-643
203. Meseguer S, Mudduluru G, Escamilla JM, Allgayer H, Barettino D (2011) MicroRNAs-10a and -10b contribute to retinoic acid-induced differentiation of neuroblastoma cells and target the alternative splicing regulatory factor SFRS1 (SF2/ASF). J Biol Chem 286(6):4150-4164
204. Bohlken A, Cheung BB, Bell JL, Koach J, Smith S, Sekyere E, Thomas W, Norris M, Haber M, Lovejoy DB, Richardson DR, Marshall GM (2009) ATP7A is a novel target of retinoic acid receptor beta2 in neuroblastoma cells. Br J Cancer 100(1):96-105
205. Yasukawa T, Bhatt S, Takeuchi T, Kawauchi J, Takahashi H, Tsutsui A, Muraoka T, Inoue M, Tsuda M, Kitajima S, Conaway RC, Conaway JW, Trainor PA, Aso T (2012) Transcriptional elongation factor elongin A regulates retinoic acid-induced gene expression during neuronal differentiation. Cell Rep 2(5):1129-1136
206. Won SJ, Kim SH, Xie L, Wang Y, Mao XO, Jin K, Greenberg DA (2006) Reelin-deficient mice show impaired neurogenesis and increased stroke size. Exp Neurol 198(1):250-259
207. Chen Y, Kundakovic M, Agis-Balboa RC, Pinna G, Grayson DR (2007) Induction of the reelin promoter by retinoic acid is mediated by Sp1. J Neurochem 103(2):650-665
208. Chen Y, Sharma RP, Costa RH, Costa E, Grayson DR (2002) On the epigenetic regulation of the human reelin promoter. Nucleic Acids Res 30(13):2930-2939
209. Lotan R, Nicolson GL (1977) Inhibitory effects of retinoic acid or retinyl acetate on the growth of untransformed, transformed, and tumor cells in vitro. J Natl Cancer Inst 59(6):1717-1722
210. Sidell N (1982) Retinoic acid-induced growth inhibition and morphologic differentiation of human neuroblastoma cells in vitro. J Natl Cancer Inst 68(4):589-596
211. Sidell N, Altman A, Haussler MR, Seeger RC (1983) Effects of retinoic acid (RA) on the growth and phenotypic expression of several human neuroblastoma cell lines. Exp Cell Res 148(1):21-30
212. Encinas M, Iglesias M, Liu Y, Wang H, Muhaisen A, Cena V, Gallego C, Comella JX (2000) Sequential treatment of SH-SY5Y cells with retinoic acid and brain-derived neurotrophic factor gives rise to fully differentiated, neurotrophic factor-dependent, human neuron-like cells. J Neurochem 75(3):991-1003
213. Wu PY, Lin YC, Chang CL, Lu HT, Chin CH, Hsu TT, Chu D, Sun SH (2009) Functional decreases in P2X7 receptors are associated with retinoic acid-induced neuronal differentiation of Neuro-2a neuroblastoma cells. Cell Signal 21(6):881-891
214. Hammerle B, Yanez Y, Palanca S, Canete A, Burks DJ, Castel V, Font de Mora J (2013) Targeting neuroblastoma stem cells with retinoic acid and proteasome inhibitor. PLoS One 8(10):e76761
215. Sumantran VN, Brederlau A, Funa K (2003) BMP-6 and retinoic acid synergistically differentiate the IMR-32 human neuroblastoma cells. Anticancer Res 23(2B):1297-1303
216. Thiele CJ, Reynolds CP, Israel MA (1985) Decreased expression of N-myc precedes retinoic acid-induced morphological differentiation of human neuroblastoma. Nature 313(6001):404-406
217. Hallahan AR, Pritchard JI, Chandraratna RA, Ellenbogen RG, Geyer JR, Overland RP, Strand AD, Tapscott SJ, Olson JM (2003) BMP-2 mediates retinoid-induced apoptosis in medulloblastoma cells through a paracrine effect. Nat Med 9(8):1033-1038
218. Patterson DM, Shohet JM, Kim ES (2011) Preclinical models of pediatric solid tumors (neuroblastoma) and their use in drug discovery. Curr Protoc Pharmacol. Chapter 14:Unit 14.17
219. Shimada H, Umehara S, Monobe Y, Hachitanda Y, Nakagawa A, Goto S, Gerbing RB, Stram DO, Lukens JN, Matthay KK (2001) International neuroblastoma pathology classification for prognostic evaluation of patients with peripheral neuroblastic tumors: a report from the Children's Cancer Group. Cancer 92(9):2451-2461
220. Stallings RL, Foley NH, Bray IM, Das S, Buckley PG (2011) MicroRNA and DNA methylation alterations mediating retinoic acid induced neuroblastoma cell differentiation. Semin Cancer Biol 21(4):283-290
221. Stallings RL (2009) MicroRNA involvement in the pathogenesis of neuroblastoma: potential for microRNA mediated therapeutics. Curr Pharm Des 15(4):456-462
222. Das S, Foley N, Bryan K, Watters KM, Bray I, Murphy DM, Buckley PG, Stallings RL (2010) MicroRNA mediates DNA demethylation events triggered by retinoic acid during neuroblastoma cell differentiation. Cancer Res 70(20):7874-7881
223. Ramaswamy S, Tamayo P, Rifkin R, Mukherjee S, Yeang CH, Angelo M, Ladd C, Reich M, Latulippe E, Mesirov JP, Poggio T, Gerald W, Loda M, Lander ES, Golub TR (2001) Multiclass cancer diagnosis using tumor gene expression signatures. Proc Natl Acad Sci USA 98(26):15149-15154
224. Pomeroy SL, Tamayo P, Gaasenbeek M, Sturla LM, Angelo M, McLaughlin ME, Kim JY, Goumnerova LC, Black PM, Lau C, Allen JC, Zagzag D, Olson JM, Curran T, Wetmore C, Biegel JA, Poggio T, Mukherjee S, Rifkin R, Califano A, Stolovitzky G, Louis DN, Mesirov JP, Lander ES, Golub TR (2002) Prediction of central nervous system embryonal tumour outcome based on gene expression. Nature 415(6870):436-442
225. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, Barrette TR, Anstet MJ, Kincead-Beal C, Kulkarni P, Varambally S, Ghosh D, Chinnaiyan AM (2007) Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 9(2):166-180
226. Oberthuer A, Hero B, Spitz R, Berthold F, Fischer M (2004) The tumor-associated antigen PRAME is universally expressed in high-stage neuroblastoma and associated with poor outcome. Clin Cancer Res 10(13):4307-4313
227. Epping MT, Wang L, Edel MJ, Carlee L, Hernandez M, Bernards R (2005) The human tumor antigen PRAME is a dominant repressor of retinoic acid receptor signaling. Cell 122(6):835-847
228. Huang S, Laoukili J, Epping MT, Koster J, Holzel M, Westerman BA, Nijkamp W, Hata A, Asgharzadeh S, Seeger RC, Versteeg R, Beijersbergen RL, Bernards R (2009) ZNF423 is critically required for retinoic acid-induced differentiation and is a marker of neuroblastoma outcome. Cancer Cell 15(4):328-340
229. Holzel M, Huang S, Koster J, Ora I, Lakeman A, Caron H, Nijkamp W, Xie J, Callens T, Asgharzadeh S, Seeger RC, Messiaen L, Versteeg R, Bernards R (2010) NF1 is a tumor suppressor in neuroblastoma that determines retinoic acid response and disease outcome. Cell 142(2):218-229
230. Altucci L, Gronemeyer H (2001) The promise of retinoids to fight against cancer. Nat Rev Cancer 1(3):181-193
231. Ulrich T (2013) Curing neuroblastoma by making it grow up, vol 2014. Boston Children's Hospital, Boston
232. Temple S (1989) Division and differentiation of isolated CNS blast cells in microculture. Nature 340(6233):471-473
233. Reynolds BA, Weiss S (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255(5052):1707-1710
234. Snyder EY, Deitcher DL, Walsh C, Arnold-Aldea S, Hartwieg EA, Cepko CL (1992) Multipotent neural cell lines can engraft and participate in development of mouse cerebellum. Cell 68(1):33-51
235. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB (2003) Identification of a cancer stem cell in human brain tumors. Cancer Res 63(18):5821-5828
236. Hemmati HD, Nakano I, Lazareff JA, Masterman-Smith M, Geschwind DH, Bronner-Fraser M, Kornblum HI (2003) Cancerous stem cells can arise from pediatric brain tumors. Proc Natl Acad Sci USA 100(25):15178-15183
237. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ (2007) A perivascular niche for brain tumor stem cells. Cancer Cell 11(1):69-82
238. Liu C, Sage JC, Miller MR, Verhaak RG, Hippenmeyer S, Vogel H, Foreman O, Bronson RT, Nishiyama A, Luo L, Zong H (2011) Mosaic analysis with double markers reveals tumor cell of origin in glioma. Cell 146(2):209-221
239. Friedmann-Morvinski D, Bushong EA, Ke E, Soda Y, Marumoto T, Singer O, Ellisman MH, Verma IM (2012) Dedifferentiation of neurons and astrocytes by oncogenes can induce gliomas in mice. Science 338(6110):1080-1084
240. Friedmann-Morvinski D, Verma IM (2014) Dedifferentiation and reprogramming: origins of cancer stem cells. EMBO Rep 15(3):244-253
241. van Es JH, Sato T, van de Wetering M, Lyubimova A, Nee AN, Gregorieff A, Sasaki N, Zeinstra L, van den Born M, Korving J, Martens AC, Barker N, van Oudenaarden A, Clevers H (2012) Dll1 + secretory progenitor cells revert to stem cells upon crypt damage. Nat Cell Biol 14(10):1099-1104
242. Schwitalla S, Fingerle AA, Cammareri P, Nebelsiek T, Goktuna SI, Ziegler PK, Canli O, Heijmans J, Huels DJ, Moreaux G, Rupec RA, Gerhard M, Schmid R, Barker N, Clevers H, Lang R, Neumann J, Kirchner T, Taketo MM, van den Brink GR, Sansom OJ, Arkan MC, Greten FR (2013) Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties. Cell 152(1-2):25-38
243. Tata PR, Mou H, Pardo-Saganta A, Zhao R, Prabhu M, Law BM, Vinarsky V, Cho JL, Breton S, Sahay A, Medoff BD, Rajagopal J (2013) Dedifferentiation of committed epithelial cells into stem cells in vivo. Nature 503(7475):218-223
244. Chaffer CL, Brueckmann I, Scheel C, Kaestli AJ, Wiggins PA, Rodrigues LO, Brooks M, Reinhardt F, Su Y, Polyak K, Arendt LM, Kuperwasser C, Bierie B, Weinberg RA (2011) Normal and neoplastic nonstem cells can spontaneously convert to a stem-like state. Proc Natl Acad Sci USA 108(19):7950-7955
245. Southall TD, Davidson CM, Miller C, Carr A, Brand AH (2014) Dedifferentiation of neurons precedes tumor formation in Lola mutants. Dev Cell 28(6):685-696
246. Yung WK, Kyritsis AP, Gleason MJ, Levin VA (1996) Treatment of recurrent malignant gliomas with high-dose 13-cis-retinoic acid. Clin Cancer Res 2(12):1931-1935
247. See SJ, Levin VA, Yung WK, Hess KR, Groves MD (2004) 13-cis-retinoic acid in the treatment of recurrent glioblastoma multiforme. Neuro Oncol 6(3):253-258
248. Kaba SE, Kyritsis AP, Conrad C, Gleason MJ, Newman R, Levin VA, Yung WK (1997) The treatment of recurrent cerebral gliomas with all-trans-retinoic acid (tretinoin). J Neurooncol 34(2):145-151
249. Wismeth C, Hau P, Fabel K, Baumgart U, Hirschmann B, Koch H, Jauch T, Grauer O, Drechsel L, Brawanski A, Bogdahn U, Steinbrecher A (2004) Maintenance therapy with 13-cis retinoid acid in high-grade glioma at complete response after first-line multimodal therapy-a phase-II study. J Neurooncol 68(1):79-86
250. Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64(19):7011-7021
251. Ying M, Wang S, Sang Y, Sun P, Lal B, Goodwin CR, Guerrero-Cazares H, Quinones-Hinojosa A, Laterra J, Xia S (2011) Regulation of glioblastoma stem cells by retinoic acid: role for Notch pathway inhibition. Oncogene 30(31):3454-3467
252. Wolf G (2008) Retinoic acid as cause of cell proliferation or cell growth inhibition depending on activation of one of two different nuclear receptors. Nutr Rev 66(1):55-59
253. Campos B, Centner FS, Bermejo JL, Ali R, Dorsch K, Wan F, Felsberg J, Ahmadi R, Grabe N, Reifenberger G, Unterberg A, Burhenne J, Herold-Mende C (2011) Aberrant expression of retinoic acid signaling molecules influences patient survival in astrocytic gliomas. Am J Pathol 178(5):1953-1964
254. Barbus S, Tews B, Karra D, Hahn M, Radlwimmer B, Delhomme N, Hartmann C, Felsberg J, Krex D, Schackert G, Martinez R, Reifenberger G, Lichter P (2011) Differential retinoic acid signaling in tumors of long- and short-term glioblastoma survivors. J Natl Cancer Inst 103(7):598-606
255. Schug TT, Berry DC, Shaw NS, Travis SN, Noy N (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129(4):723-733
256. Schug TT, Berry DC, Toshkov IA, Cheng L, Nikitin AY, Noy N (2008) Overcoming retinoic acid-resistance of mammary carcinomas by diverting retinoic acid from PPARbeta/delta to RAR. Proc Natl Acad Sci USA 105(21):7546-7551
257. Rohle D, Popovici-Muller J, Palaskas N, Turcan S, Grommes C, Campos C, Tsoi J, Clark O, Oldrini B, Komisopoulou E, Kunii K, Pedraza A, Schalm S, Silverman L, Miller A, Wang F, Yang H, Chen Y, Kernytsky A, Rosenblum MK, Liu W, Biller SA, Su SM, Brennan CW, Chan TA, Graeber TG, Yen KE, Mellinghoff IK (2013) An inhibitor of mutant IDH1 delays growth and promotes differentiation of glioma cells. Science 340(6132):626-630
258. Garrett-Bakelman FE, Melnick AM (2013) Differentiation therapy for IDH1/2 mutant malignancies. Cell Res 23(8):975-977
259. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, Berman BP, Pan F, Pelloski CE, Sulman EP, Bhat KP, Verhaak RG, Hoadley KA, Hayes DN, Perou CM, Schmidt HK, Ding L, Wilson RK, Van Den Berg D, Shen H, Bengtsson H, Neuvial P, Cope LM, Buckley J, Herman JG, Baylin SB, Laird PW, Aldape K (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17(5):510-522
260. Turcan S, Rohle D, Goenka A, Walsh LA, Fang F, Yilmaz E, Campos C, Fabius AW, Lu C, Ward PS, Thompson CB, Kaufman A, Guryanova O, Levine R, Heguy A, Viale A, Morris LG, Huse JT, Mellinghoff IK, Chan TA (2012) IDH1 mutation is sufficient to establish the glioma hypermethylator phenotype. Nature 483(7390):479-483
261. Chou AP, Chowdhury R, Li S, Chen W, Kim AJ, Piccioni DE, Selfridge JM, Mody RR, Chang S, Lalezari S, Lin J, Sanchez DE, Wilson RW, Garrett MC, Harry B, Mottahedeh J, Nghiemphu PL, Kornblum HI, Mischel PS, Prins RM, Yong WH, Cloughesy T, Nelson SF, Liau LM, Lai A (2012) Identification of retinol binding protein 1 promoter hypermethylation in isocitrate dehydrogenase 1 and 2 mutant gliomas. J Natl Cancer Inst 104(19):1458-1469
262. Liau L, Cloughesy T, Lai A (2013) Pre-Clinical Studies Investigating the Use of Isotretinoin for the Treatment of IDH1 Mutant Glioma Patients. Accelerate Brain Cancer Cure, Inc., Neuro-Oncology & Neurosurgery, UCLA
263. Lee SY, Lee HS, Moon JS, Kim JI, Park JB, Lee JY, Park MJ, Kim J (2004) Transcriptional regulation of Zic3 by heterodimeric AP-1(c-Jun/c-Fos) during Xenopus development. Exp Mol Med 36(5):468-475
264. Yoon J, Kim JH, Lee OJ, Lee SY, Lee SH, Park JB, Lee JY, Kim SC, Kim J (2013) AP-1(c-Jun/FosB) mediates xFoxD5b expression in Xenopus early developmental neurogenesis. Int J Dev Biol 57(11-12):865-872