Role of Retinoic Acid in the Differentiation of Embryonal Carcinoma and Embryonic Stem Cells

Vitamins and Hormones

Volumn 75, Issue , 2007, Pages 69-95

  Soprano, Dianne Robert ^a   Teets, Bryan W ^a   Soprano, Kenneth J ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOIC ACID;

ANIMAL; CELL DIFFERENTIATION; DRUG EFFECT; EMBRYONAL CARCINOMA; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; MOUSE; REVIEW; STEM CELL;

ANIMALS; CARCINOMA, EMBRYONAL; CELL DIFFERENTIATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MICE; STEM CELLS; TRANSCRIPTION, GENETIC; TRETINOIN;

EID: 33947100875     PISSN: 00836729     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0083-6729(06)75003-8     Document Type: Review

References (149)

1. An J., Yuan Q., Wang C., Liu L., Tang K., Tian H.Y., Jing N.H., and Zhao F.K. Differential display of proteins involved in the neural differentiation of mouse embryonic carcinoma P19 cells by comparative proteomic analysis. Proteomics 5 (2005) 1656-1668
2. Ansari H., Greco G., and Luban J. Cyclophilin A peptidyl-prolyl isomerase activity promotes ZPR1 nuclear export. Mol. Cell. Biol. 22 (2002) 6993-7003
3. Bain G., Ray W.J., Yao M., and Gottlieb D.I. From embryonal carcinoma cells to neurons: The P19 pathway. BioEssays 16 (1994) 343-348
4. Bain G., Mansergh F.C., Wride M.A., Hance J.E., Isogawa A., Rancourt S.L., Ray W.J., Yoshimura Y., Tsuzuki T., Gottlieb D.I., and Rancourt D.E. ES cell neural differentiation reveals a substantial number of novel ESTs. Funct. Integr. Genomics 1 (2000) 127-139
5. Ben-Shushan E., Thompson J.R., Gudas L.J., and Bergman Y. Rex-1, a gene encoding a transcription factor expressed in the early embryo, is regulated via Oct-3/4 and Oct-6 binding to an octamer site and a novel protein, Rox-1, binding to an adjacent site. Mol. Cell. Biol. 18 (1998) 1866-1878
6. Bixby J.L., and Zhang R. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J. Cell Biol. 110 (1990) 1253-1260
7. Bouillet P., Oulad-Abdelghani M., Vicaire S., Garnier J.-M., Schuhbaur B., Dolle P., and Chambon P. Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel muse gene, stra1 (Mouse LERK-2/Eplg2). Dev. Biol. 170 (1995) 420-433
8. Boylan J.F., Lohnes D., Taneja R., Chambon P., and Gudas L.J. Loss of retinoic acid receptor γ function in F9 cells by gene disruption results in aberrant Hoxa-I expression and differentiation upon retinoic acid treatment. Proc. Natl. Acad. Sci. USA 90 (1993) 9601-9605
9. Boylan J.F., Lufkin D., Achkar C.C., Taneja R., Chambon P., and Gudas L.J. Targeted disruption of retinoic acid receptor α (RARα) and RARγ results in receptor-specific alterations in retinoic acid-mediated differentiation and retinoic acid metabolism. Mol. Cell. Biol. 15 (1995) 843-851
10. Chambon P. A decade of molecular biology of retinoic acid receptors. FASEB J. 10 (1996) 940-954
11. Chiba H., Clifford J., Metzger D., and Chambon P. Distinct retinoid X receptors-retinoic acid receptor heterodimers are differentially involved in the control of expression of retinoid target genes in F9 embryonal carcinoma cells. Mol. Cell. Biol. 17 (1997) 3013-3020
12. Chiba H., Clifford J., Metzger D., and Chambon P. Specific and redundant function of retinoid X receptor/retinoic acid receptor heterodimers in differentiation, proliferation, and apoptosis of F9 embryonal carcinoma cells. J. Cell Biol. 139 (1997) 735-747
13. Chiu R., Rey O., Zheng J.Q., Twiss J.L., Song J., Pang S., and Yokoyama K.K. Effects of altered expression and localization of cyclophilin A on differentiation of p19 embryonic carcinoma cells. Cell. Mol. Neurobiol. 23 (2003) 929-943
14. Cho S.Y., Cho S.Y., Lee S.H., and Park S.S. Differential expression of mouse Disabled 2 gene in retinoic acid-treated F9 embryonal carcinoma cells and early mouse embryos. Mol. Cells 30 (1999) 179-184
15. Clifford J., Chiba H., Sobieszczuk D., Metzger D., and Chambon P. RXRα-null F9 embryonal carcinoma cells are resistant to the differentiation, anti-proliferative and apoptotic effects of retinoids. EMBO J. 15 (1996) 4142-4155
16. Clagett-Dame M., and De Luca H.F. The role of vitamin A in mammalian reproduction and embryonic development. Annu. Rev. Nutr. 22 (2002) 347-381
17. Cohlan S.Q. Excessive intakes of vitamin A as a cause of congential anomalies in the rat. Science 117 (1953) 535-536
18. Connor F., Wright E., Denny P., Koopman P., and Ashworth A. The Sry-related HMG box-containing gene Sox6 is expressed in the adult testis and developing nervous system of the mouse. Nucleic Acids Res. 17 (1995) 3365-3372
19. Dani C., Smith A.G., Dessolin S., Leroy P., Staccini L., Villageois P., Darimont C., and Ailhaud G. Differentiation of embryonic stem cells into adipocytes in vitro. J. Cell Sci. 110 (1997) 1279-1285
20. De Luca L.M., Darwiche N., Jones C.S., and Scita G. Retinoids in differentiation and neoplasia. Sci. Med. 2 (1995) 28-37
21. Di Rocco G., Gavalas A., Popperl H., Krumlauf R., Mavilio F., and Zappavigna V. The recruitment of SOX/OCT complexes and the differential activity of HOXA1 and HOXB1 modulate the hox-b1 auto-regulatory enhancer function. J. Biol. Chem. 276 (2001) 20506-20515
22. Drab M., Haller H., Bychkov R., Erdmann B., Lindschau C., Haase H., Morano I., Luft F.C., and Wobus A.M. From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: A retinoic acid and db-cAMP in vitro differentiation model. FASEB J. 11 (1997) 905-915
23. Eiges R., and Benvenisty N. A molecular view on pluripotent stem cells. FEBS Lett. 529 (2002) 135-141
24. Espeseth A.S., Murphy S.P., and Linney E. Retinoic acid receptor expression vector inhibits differentiation of F9 embryonal carcinoma cells. Genes Dev. 3 (1989) 1647-1656
25. Evans M.J., and Kaufman M. Establishment in culture of pluripotential cells from mouse embryos. Nature 292 (1981) 154-156
26. Farah M.H., Olson J.M., Sucic H.B., Hume R.I., Tapscott S.J., and Turner D.L. Generation of neurons by transient expression of neural bHLH proteins in mammalian cells. Development 127 (2000) 693-702
27. Faria T.N., LaRosa G.J., Wilen E., Liao J., and Gudas L.J. Characterization of genes which exhibit reduced expression during the retinoic acid-induced differentiation of F9 teratocarcinoma cells: Involvement of cyclin D3 in RA-mediated growth arrest. Mol. Cell. Endocrinol. 143 (1998) 155-166
28. Faria T.N., Mendelsohn C., Chambon P., and Gudas L.J. The targeted disruption of both alleles of RARβ2 in F9 cells results in the loss of retinoic acid-associated growth arrest. J. Biol. Chem. 274 (1999) 26783-26788
29. Fraichard A., Chassande O., Bilbaut G., Dehay C., Savatier P., and Samarut J. In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J. Cell. Sci. 108 (1995) 3181-3188
30. Gao X., Bian W., Yang J., Tang K., Kitani H., Atsumi T., and Jing N. A role of N-cadherin in neuronal differentiation of embryonic carcinoma P19 cells. Biochem. Biophys. Res. Commun. 284 (2001) 1098-1103
31. Geiger B., and Ayalon O. Cadherin. Annu. Rev. Cell Biol. 8 (1992) 307-320
32. Glaser T., and Brustle O. Retinoic acid induction of ES-cell-derived neurons: The radial glia connection. Trends Neurosci. 28 (2005) 397-400
33. Goliger J.A., and Gudas L.J. Mouse F9 teratocarcinoma stem cells expressing the stably transfected homeobox gene Hox 1.6 exhibit an altered morphology. Gene Expr. 2 (1992) 147-160
34. Gottlieb D.I., and Huettner J.E. An in vitro pathway from embryonic stem cells to neurons and glia. Cells Tissues Organs 165 (1999) 165-172
35. Gubbay J., Collignon J., Koopman P., Capel B., Economou A., and Munsterberg A. A gene mapping to the sex-determining region of the mouse Y chromosome is a member of a novel family of embryonically expressed genes. Nature 346 (1990) 245-250
36. Gudas L.J. Retinoic acid and teratocarcinoma stem cells. Sem. Dev. Biol. 2 (1991) 171-179
37. Gudas L.J., Sporn M.B., and Roberts A.B. Cellular biology and biochemistry of retinoids. In: Sporn M.B., Roberts A.B., and Goodman D.S. (Eds). "The Retinoids: Biology, Chemistry and Medicine". 2nd ed. (1994), New York, Raven Press 443-520
38. Hale F. Relation of maternal vitamin A deficiency to microphthalmia in pigs. Texas State J. Med. 33 (1937) 228-232
39. Hamada-Kanazawa M., Ishikawa K., Nomoto K., Uozumi T., Kawai Y., Narahara M., and Miyake M. Sox6 expression causes cellular aggregation and the neuronal differentiation of P19 embryonic carcinoma cells in the absence of retinoic acid. FEBS Lett. 560 (2004) 192-198
40. Hamada-Kanazawa M., Ishikawa K., Ogawa D., Kanai M., Kawai Y., Narahara M., and Miyake M. Suppression of Sox6 in P19 cells leads to failure of neuronal differentiation by retinoic acid and induces retinoic acid-dependent apoptosis. FEBS Lett. 577 (2004) 60-66
41. Handschumacher R.E., Harding M.W., Rice J., Drugge R.J., and Speicher D.W. Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science 226 (1984) 44-47
42. Harris T.M., and Childs G. Global gene expression patterns during differentiation of F9 embryonal carcinoma cells into parietal endoderm. Funct. Integr. Genomics 2 (2002) 105-119
43. Hart S.M. Modulation of nuclear receptor dependent transcription. Biol. Res. 35 (2002) 295-303
44. Hong Y., Winkler C., and Schartl M. Pluripotentency and differentiation of embryonic stem cell lines from the medakafish (Oryzias latipes). Mech. Dev. 60 (1996) 33-44
45. Hosler B.A., LaRosa G.J., Grippo J.F., and Gudas L.J. Expression of REX-1, a gene containing zinc finger motifs, is rapidly reduced by retinoic acid in F9 teratocarcinoma cells. Mol. Cell. Biol. 9 (1989) 5623-5629
46. Hosler B.A., Rogers M.B., Kozak C.A., and Gudas L.J. An octamer motif contributes to the expression of the retinoic acid-regulated zinc finger gene Rex-1 (Zfp-42) in F9 teratocarcinoma cells. Mol. Cell. Biol. 13 (1993) 2919-2928
47. Hu L., and Gudas L.J. Cyclic AMP analogs and retinoic acid influence the expression of retinoic acid receptor αβ and γmRNAs in F9 teratocarcinoma cells. Mol. Cell. Biol. 10 (1990) 391-396
48. Jacobs S., Lie D.C., DeCicco K.L., Shi Y., DeLuca L.M., Gage F.H., and Evans R.M. Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc. Natl. Acad. Sci. USA 103 (2006) 3902-3907
49. Jan Y.N., and Jan L.Y. HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell 75 (1993) 827-830
50. Jepsen K., and Rosenfeld M.G. Biological roles and mechanistic actions of corepressor complexes. J. Cell Sci. 115 (2002) 689-698
51. Johnson J.E., Zimmerman K., Saito T., and Anderson D.J. Induction and repression of mammalian achaete-scute homologue (MASH) gene expression during neuronal differentiation of P19 embryonal carcinoma cells. Development 114 (1992) 75-87
52. Jones-Villeneuve E.M.V., McBurney M.W., Rogers K.A., and Kalnins V.I. Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell Biol. 94 (1982) 253-262
53. Jones-Villeneuve E.M.V., Rudnicki M.A., Harris J.F., and McBurney M.W. Retinoic acid-induced neural differentiation of embryonal carcinoma cells. Mol. Cell. Biol. 3 (1983) 2271-2279
54. Kawaguchi J., Mee P.J., and Smith A.G. Osteogenic and chondrogenic differentiation of embryonic stem cells in response to specific growth factors. Bone 36 (2005) 758-769
55. Kim S., Yoon Y.S., Kim J.W., Jung M., Kim S.U., Lee Y.D., and Suh-Kim H. Neurogenin1 is sufficient to induce neuronal differentiation of embryonal carcinoma P19 cells in the absence of retinoic acid. Cell. Mol. Neurobiol. 24 (2004) 343-356
56. Knoepfler P.S., and Kamps M.P. The Pbx family of proteins is strongly upregulated by a posttranscriptional mechanism during retinoic acid-induced differentiation of P19 embryonal carcinoma cells. Mech. Dev. 63 (1997) 5-14
57. Kruyt F.A., van den Brink C.E., Defize L.H., Donath M.J., Kastner P., Kruijer W., Chambon P., and van der Saag P.T. Transcriptional regulation of retinoic acid receptor beta in retinoic acid-sensitive and -resistant P19 embryonalcarcinoma cells. Mech. Dev. 33 (1991) 171-178
58. Kruyt F.A., van der Veer L.J., Mader S., van den Brink C.E., Feijen A., Jonk L.J., Kruijer W., and van der Saag P.T. Retinoic acid resistance of the variant embryonal carcinoma cell line RAC65 is caused by expression of a truncated RAR alpha. Differentiation 49 (1992) 27-37
59. Langston A.W., and Gudas L.J. Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox1-6. Mech. Dev. 38 (1992) 217-228
60. Langston A.W., Thompson J.R., and Gudas L.J. Retinoic acid-responsive enahncers located 3′ of the HoxA and HoxB homeobox gene clusters. Functional analysis. J. Biol. Chem. 272 (1997) 2167-2175
61. LaRosa G.J., and Gudas L.J. An early effect of retinoic acid: Cloning of an mRNA (Ear-1) exhibiting rapid and protein synthesis-independent induction during teratocarcinoma stem cell differentiation. Proc. Natl. Acad. Sci. USA 85 (1988) 329-333
62. 2 knockout cells. Exp. Cell Res. 294 (2004) 290-300
63. Loudig O., Babichuk C., White J., Abu-Abed S., Mueller C., and Petkovich M. Cytochrome P450RAI(CYP26) promoter, a distinct composite retinoic acid response element underlies the complex regulation of retinoic acid metabolism. Mol. Endocrinol. 14 (2000) 1483-1497
64. Ma Q., Kintner C., and Anderson D.J. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87 (1996) 43-52
65. Ma Q., Sommer L., Cserjesi P., and Anderson D.J. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing notch ligands. J. Neurosci. 17 (1997) 3644-3652
66. Mark M., Ghyselinck N.B., and Chambon P. Function of retinoid nuclear receptors: Lessons from genetic and pharamacological dissections of the retinoic acid signaling pathway during mouse embryogenesis. Ann. Rev. Pharmacol. Toxicol. 46 (2006) 451-480
67. Martin G.R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 78 (1981) 7634-7638
68. Martinez-Ceballos E., Chambon P., and Gudas L.J. Differences in gene expression between wild type and hoax-1 knockout embryonic stem cells after retinoic acid treatment or leukemia inhibitory factor (LIF) removal. J. Biol. Chem. 280 (2005) 16484-16498
69. Mason K.E. Foetal death, prolonged gestation, and difficult parturition in the rat as a result of vitamin A deficiency. Am. J. Anat. 57 (1935) 303-349
70. McBurney M.W., and Rogers B.J. Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev. Biol. 89 (1982) 503-508
71. McBurney M.W., Jones-Villeneuve E.M.V., Edwards M.K.S., and Anderson P.J. Control of muscle and neuronal differentiation in a cultured embryonal carcinoma cell line. Nature 299 (1982) 165-167
72. McCaffery P.M., and Drager U.C. Regulation of retinoic acid signaling in the embryonic nervous system: A master differentiation factor. Cytokine Growth Factor Rev. 11 (2000) 233-249
73. - mice results from stepwise deletion of engrailed-expressing cells by 9.5 days postcoitum. Cell 69 (1992) 581-595
74. Miller J.R., and Randell T.M. Signal transduction through β-catenin and specification of cell fate during embryogenesis. Genes Dev. 10 (1996) 2527-2539
75. Mummery C.L., Feijen A., Molenaar W.H., van den Brink C.E., and De Laat S.W. Establishment of a differentiated mesodermal line form P19 EC cells expressing functional PDGF and EGF receptors. Exp. Cell Res. 165 (1986) 229-242
76. Nishiguchi S., Joh T., Horie K., Zou Z., Yasunaga T., and Shimada K. A survey of genes expressed in undifferentiated mouse embryonal carcinoma F9 cells: Characterization of low-abundance mRNAs. J. Biochem. 116 (1994) 128-139
77. Nusse R., and Varmus H.E. Many tumors induced by the mouse mammary tumor virus contain a provirus integrated in the same region of the host genome. Cell 31 (1982) 99-109
78. Oda H., Iwata I., Yasunami M., and Ohkubo H. Structure of the mouse NDRF gene and its regulation during neuronal differentiation of P19 cells. Brain Res. Mol. Brain Res. 77 (2000) 37-46
79. Ogura T., and Evans R.M. Evidence for two distinct retinoic acid response pathways for HOXB1 gene regulation. Proc. Natl. Acad. Sci. USA 92 (1995) 392-396
80. Oren T., Sher J.A., and Evans T. Hematopoiesis and retinoids: Development and disease. Leuk. Lymphoma 44 (2003) 1881-1891
81. Pain B., Clark M.E., Shen M., Nakazawa M., Sakurai M., Samarut J., and Etches R.J. Long-term in vitro cultures and characterization of avian embryonic stem cells with multiple morphogenetic potentialities. Development 122 (1996) 2339-2348
82. Papkoff J. Identification and biochemical characterization of secreted Wnt-1 protein from P19 embryonal carcinoma cells induced to differentiate along the neuroectodermal lineage. Oncogene 9 (1994) 313-317
83. Pevny L.H., and Lovell-Badge R. Sox genes find their feet. Curr. Opin. Genet. Dev. 7 (1997) 338-344
84. Phillips B.W., Vernochet C., and Dani C. Differentiation of embryonic stem cells for pharmacological studies on adipose cells. Pharm. Res. 47 (2003) 264-268
85. Pozzi S., Rossetti S., Bistulfi G., and Sacchi N. RAR-mediated epigenetic control of the cytochrome P450 Cyp26a1 in embryocarcinoma cells. Oncogene 25 (2006) 1400-1407
86. Pratt M.A., Kralova J., and McBurney M.W. A dominant negative mutation of the alpha retinoic acid receptor gene in a retinoic acid-nonresponsive embryonal carcinoma cell. Mol. Cell. Biol. 10 (1990) 6445-6553
87. Pratt M.A., Langston A.W., Gudas L.J., and McBurney M.W. Retinoic acid fails to induce expression of Hox genes in differentiation-defective murine embryonal carcinoma cells carrying a mutant gene for alpha retinoic acid receptor. Differentiation 53 (1993) 105-113
88. Prior H.M., and Walter M.A. SOX genes: Architects of development. Mol. Med. 2 (1996) 405-412
89. Qin P., Haberbusch J.M., Soprano K.J., and Soprano D.R. Retinoic acid regulates the expression of PBX1, PBX2 and PBX3 in P19 cell both transcriptionally and post-transcriptionally. J. Cell. Biochem. 92 (2004) 147-163
90. Qin P., Haberbusch J.M., Zhang Z., Soprano K.J., and Soprano D.R. Pre-B cell leukemia transcription factor (PBX) proteins are important mediators for retinoic acid-dependent endodermal and neuronal differentiation of mouse embryonal carcinoma P19 cells. J. Biol. Chem. 279 (2004) 16263-16271
91. Ray W.J., Bain G., Yao M., and Gottlieb D.I. CYP26, a novel mammalian cytochrome P450, is induced by retinoic acid and defines a new family. J. Biol. Chem. 272 (1997) 18702-18708
92. Rijsewijk F., Schuermann M., Wagenaar E., Parren P., Weigel D., and Nusse R. The Drosophila homolog of the mouse mammary oncogene int-1 is identical to the segment polarity gene wingless. Cell 50 (1987) 649-657
93. Rochette-Egly C., Plassat J.L., Taneja R., and Chambon P. The AF-1 and AF-2 activating domains of retinoic acid receptor (RARalpha) and their phosphorylation are differently involved in parietal endodermal differentiation of F9 cells and retinoid-induced expression of target genes. Mol. Endo. 14 (2000) 1398-1410
94. Rogers M.B., Hosler B.A., and Gudas L.J. Specific expression of a retinoic acid-regulated, zinc-finger gene, Rex-1, in preimplantation embryos, trophoblast and spermatocytes. Development 113 (1991) 815-824
95. Rohwedel J., Guan K., and Wobus A.M. Induction of cellular differentiation by retinoic acid in vitro. Cells Tissues Organs 165 (1999) 190-202
96. Rosfjord E., and Rizzino A. The octamer motif present in the Rex-1 promoter binds Oct-1 and Oct-3 expressed by EC and ES cells. Biochem. Biophys. Res. Commun. 203 (1994) 1795-1802
97. Ross S.A., McCaffrey P.J., Drager U.C., and De Luca L.M. Retinoids in embryonal development. Physiol. Rev. 80 (2000) 1021-1054
98. Sangster-Guity N., Yu L.M., and McCormick P. Molecular profiling of embryonal carcinoma cells following retinoic acid or histone deacetylase inhibitor treatment. Cancer Biol. Ther. 3 (2004) 1109-1120
99. Schoorlemmer J., Jonk L., Sanbing S., van Puijenbroek A., Feijen A., and Kruijer W. Regulation of Oct-4 gene expression during differentiation of EC cells. Mol. Biol. Rep. 21 (1995) 129-140
100. Schuldiner M., Yanuka O., Itskovitz-Eldor J., Melton D.A., and Benvenisty N. Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 97 (2000) 11307-11312
101. Schuuring E., Deemter L., van Roelink H., and Nusse R. Transient expression of the proto-oncogene int-1 during differentiation of P19 embryonal carcinoma cells. Mol. Cell. Biol. 9 (1989) 1357-1361
102. Shamblott M., Axelman J., Wang S., Buggs E., Littlefield J., Donovan P., Blumenthal P., Huggins G., and Gearhart J. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc. Natl. Acad. Sci. USA 95 (1998) 13726-13731
103. Shen J., Wu H., and Gudas L.J. Molecular cloning and analysis of a group of genes differentially expressed in cells which overexpress the Hoxa-1 homeobox gene. Exp. Cell Res. 259 (2000) 274-283
104. Shen S., and Gudas L.J. Molecular cloning of a novel retinoic acid-responsive gene, HAIR-62, which is also up-regulated in Hoxa-1-overexpressing cells. Cell Growth Differ. 11 (2000) 11-17
105. Shen S., Kruyt F.A., den Hertoz J., van der Saag P.T., and Kruijer W. Mouse and human retinoic acid receptor beta 2 promoters: Sequence comparison and localization of retinoic acid responsiveness. DNA Seq. 2 (1991) 111-119
106. Simeone A., Acampora D., Nigro V., Faiella A., D'Esposito M., Stornauiolo A., Mavilio F., and Boncinelli E. Differential regulation by retinoic acid of the homeobox genes of the four Hox loci in human embryonal carcinoma cells. Mech. Dev. 33 (1991) 215-228
107. Sinclair A., Berta P., Palmer M., Hawkins J., Griffiths B., and Smith M. A gene from the human sex-determining region encodes a protein with homology to a conserved DNA-binding motif. Nature 346 (1990) 240-244
108. Smith A.G. Embryo-derived stem cells: Of mice and men. Annu. Rev. Cell Dev. Biol. 17 (2001) 435-462
109. Smith E.R., Capo-chichi C.D., He J., Smedberg J.L., Yang D.H., Prowse A.H., Goodwin A.K., Hamilton T.C., and Xu X.X. Disabled-2 mediates c-Fos suppression and the cell growth regulatory activity of retinoic acid in embryonic carcinoma cells. J. Biol. Chem. 276 (2001) 47303-47310
110. Smolich B.D., and Papkoff J. Regulated expression of Wnt family members during neuroectodermal differentiation of P19 embryonal carcinoma cell: Overexpression of Wnt-1 perturbs normal differentiation-specific properties. Dev. Biol. 166 (1994) 300-310
111. Sonneveld E., van den Brink C.E., Tertoolen L.G., van der Burg B., and van der Saag P.T. Retinoic acid hydroxylase (CYP26) is a key enzyme in neuronal differentiation of embryonal carcinoma cells. Dev. Biol. 21 (1999) 390-404
112. Song J., Lu Y.C., Yokoyama K., Rossi J., and Chiu R. Cyclophilin A is required for retinoic acid-induced neuronal differentiation in p19 cells. J. Biol. Chem. 279 (2004) 24414-24419
113. Soprano D.R., and Soprano K.J. Retinoids as teratogens. Annu. Rev. Nutr. 15 (1995) 111-132
114. Soprano D.R., and Soprano K.J. Role of RARs and RXRs in mediating the molecular mechanism of action of Vitamin A. In: Zempleni J., and Daniel H. (Eds). "Molecular Nutrition" (2003), CABI, Cambridge, MA 135-149
115. Soprano D.R., Soprano K.J., Wyatt M.L., and Goodman D.S. Induction of the expression of retinol-binding protein and transthyretin in F9 embryonal carcinoma cells differentiated to embryoid bodies. J. Biol. Chem. 263 (1988) 17897-17900
116. St.-Arnaud R., Craig J., McBurney M.W., and Papkoff J. The int-1 proto-oncogene is transcriptionally activated during neuroectodermal differentiation of P19 mouse embryonal carcinoma cells. Oncogene 4 (1989) 1077-1080
117. Steele B.K., Meyers C., and Ozbun M.A. Variable expression of some "housekeeping" genes during human keratinocyte differentiation. Anal. Biochem. 307 (2002) 341-347
118. Strickland S., and Mahdavi V. The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell 15 (1978) 393-403
119. Strickland S., Smith K.K., and Marotti K.R. Hormonal induction of differentiation in teratocarcinoma stem cells: Generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell 21 (1980) 347-355
120. Strubing C., Ahnert-Hilger G., Shan J., Wiedenmann B., Hescheler J., and Wobus A.M. Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev. 53 (1995) 275-287
121. Sun L., Bradford C.S., Ghosh C., Collodi P., and Barnes D.W. ES-like cell cultures derived from early zebrafish embryos. Mol. Mar. Biol. Biotechnol. 4 (1995) 193-199
122. Sun Y., Nadal-Vicens M., Misono S., Lin M.Z., Zubiaga A., Hua X., Fan G., and Greenberg M.E. Neurogenin promotes neurogenesis and inhibits glial differentiation by independent mechanisms. Cell 104 (2001) 365-376
123. Takamatsu N., Kanda H., Tsuchiya I., Yamada S., Ito M., Kabeno S., Shiba T., and Yamashita S. A gene that is related to SRY and is expressed in the testes encodes a leucine zipper-containing protein. Mol. Cell. Biol. 15 (1995) 3759-3766
124. Takeichi M. Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7 (1995) 619-627
125. Taneja R., Bouillet P., Boylan J.F., Gaub M.P., Roy B., Gudas L.J., and Chambon P. Reexpression of retinoic acid receptor (RAR) gamma or overexpression of RAR alpha or RAR beta in RAR gamma-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc. Natl. Acad. Sci. USA 92 (1995) 7854-7858
126. Taneja R., Roy B., Plassat J.-L., Zusi C.F., Ostrowski J., Reczek P.R., and Chambon P. Cell-type and promoter-context dependent retinoic acid receptor (RAR) redundancies for RARβ2 and Hoxa-1 activation in F9 and P19 cells can be artefactually generated by gene knockouts. Proc. Natl. Acad. Sci. USA 93 (1996) 6197-6202
127. Taneja R., Rochette-Egly C., Plassat J.L., Penna L., Gaub M.P., and Chambon P. Phosphorylation of activation functions AF-1 and AF-2 of RARα and RARγ is indispensable for differentiation of F9 cells upon retinoic acid and cAMP treatment. EMBO J. 16 (1997) 6452-6465
128. Tang K., Yang J., Gao X., Wang C., Liu L., Kitani H., Atsumi T., and Jing N. Wnt-1 promotes neuronal differentiation and inhibits gliogenesis in P19 cells. Biochem. Biophys. Res. Commun. 293 (2002) 167-173
129. Teramoto S., Kihara-Negishi F., Sakurai T., Yamada T., Hashimoto-Tamaoki T., Tamura S., Kohno S., and Oikawa T. Classification of neural differentiation-associated genes in P19 embryonal carcinoma cells by their expression patterns induced after cell aggregation and/or retinoic acid treatment. Oncol. Rep. 14 (2005) 1231-1238
130. Thellin O., Zorzi W., Lakaye B., De Borman B., Coumans B., Hennen G., Grisar T., Igout A., and Heinen E. Housekeeping genes as internal standards: Use and limits. J. Biotechnol. 75 (1999) 291-295
131. Thomson J.A., and Marshall V.S. Primate embryonic stem cells. Curr. Top. Dev. Biol. 38 (1998) 133-165
132. Thomson J.A., Kalishman J., Golos T.G., Durning M., Harris C.P., Becker R.A., and Hearn J.P. Isolation of a primate embryonic stem cell line. Proc. Natl. Acad. Sci. USA 92 (1995) 7844-7848
133. Thomson J.A., Kalishman J., Golos T.G., Durning M., Harris C.P., and Hearn J.P. Pluripotent cell lines derived from common marmoset (Callithix jacchus) blastocysts. Biol. Reprod. 55 (1996) 254-259
134. Thomson J.A., Itskovitz-Eldor J., Shapiro S., Waknitz M., Swiergiel J., Marshall V., and Jones J. Embryonic stem cell lines derived from human blastocytes. Science 282 (1998) 1145-1147
135. Thompson J.R., and Gudas L.J. Retinoic acid induces parietal endoderm but not primitive endoderm and visceral endoderm differentiation in F9 teratocarcinoma stem cells with a targeted deletion of the Rex-1 (Zfp-42) gene. Mol. Cell. Endocrinol. 195 (2002) 119-133
136. Thompson J.R., Huang D.Y., and Gudas L.J. The murine Hoxb1 3′RAIDR enhancer contains multiple regulatory elements. Cell Growth Differ. 9 (1998) 969-981
137. Umbhauer M., Penzo-Mendez A., Clavilier L., Boucaut J., and Riou J. Signaling specificities of fibroblast growth factor receptors in early Xenopus embryo. J. Cell Sci. 113 (2000) 2865-2875
138. Wang Z., Ge J., Huang B., Gao Q., Liu B., Wang L., Yu L., Fan Z., Lu Z., and Liu J. Differentiation of embryonic stem cells into corneal epithelium. Sci. China Life Sci. 48 (2005) 471-480
139. Wegner M. From head to toes: The multiple facets of Sox proteins. Nucleic Acids Res. 27 (1999) 1409-1420
140. Wei L.-N. Retinoid receptors and their coregulators. Ann. Rev. Pharmacol. Toxicol. 43 (2003) 47-72
141. Wei Y., Harris T., and Childs G. Global gene expression patterns during neural differentiation of P19 embryonic carcinoma cells. Differentiation 70 (2002) 204-219
142. Westin S., Rosenfeld M.G., and Glass C.K. Nuclear receptor coactivators. Adv. Pharmacol. 47 (2000) 89-112
143. Wobus A.M., Rohwedel J., Maltsev V., and Hescheler J. In vitro differentiation of embryonic stem cells into cardiomyocytes or skeletal muscles cells is specifically modulated by retinoic acid. Rouxs Arch. Dev. Biol. 204 (1994) 36-45
144. Wobus A.M., Kaomei G., Shan J., Wellner M.C., Rohwedel J., Ji. G., Fleischmann B., Katus H.A., Hescheler J., and Franz W.J. Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 29 (1997) 1525-1539
145. Young P.R., and Tilghman S.M. Induction of alpha-fetoprotein synthesis in differentiating F9 teratocarcinoma cells is accompanied by a genome-wide loss of DNA methylation. Mol. Cell. Biol. 4 (1984) 898-907
146. Zhong H., and Simons J.W. Direct comparison of GAPDH, beta-actin, cyclophilin, and 28S rRNA as internal standards for quantifying RNA levels under hypoxia. Biochem. Biophys. Res. Commun. 259 (1999) 523-526
147. Zhuang Y., Faria T.N., Chambon P., and Gudas L.J. Identification and characterization of retinoic acid receptors beta2 target genes in F9 teratocarcinoma cells. Mol. Cancer Res. 1 (2003) 619-630
148. Zile M. Function of vitamin A in vertebrate embryonic development. J. Nutr. 131 (2001) 705-708
149. Zwartkruis F., Kruyt F., van der Saag P.T., and Meijlink F. Induction of HOX-2 genes in P19 embryocarcinoma cells is dependent on retinoic acid receptor alpha. Exp. Cell Res. 205 (1993) 422-425