Induction of cellular differentiation by retinoic acid in vitro

Cells Tissues Organs

Volumn 165, Issue 3-4, 1999, Pages 190-202

  Rohwedel, Jürgen ^a   Guan, Kaomei ^b   Wobus, Anna M ^b  

^a UNIVERSITY OF LÜBECK   (Germany)

^b NONE

Author keywords

Cardiogenesis; Differentiation; Embryonic stem cells; Retinoic acid

Indexed keywords

RETINOIC ACID; RETINOIC ACID BINDING PROTEIN; RETINOIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CONCENTRATION RESPONSE; DOSE TIME EFFECT RELATION; DRUG MECHANISM; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; HEART DEVELOPMENT; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL; TERATOGENICITY;

ANIMALIA;

EID: 0032703833     PISSN: 14226405     EISSN: None     Source Type: Journal    
DOI: 10.1159/000016699     Document Type: Article

References (90)

1. Alles, A.J., K.K. Sulik (1989) Retinoic-acid-induced limb-reduction defects: Perturbation of zones of programmed cell death as a pathogenetic mechanism. Teratology 40: 163-171.
2. 1 integrin-deficient cells. Dev Biol 179: 184-196.
3. Bain, G., D. Kitchens, M. Yao, J.E. Huettner, D.I. Gottlieb (1995) Embryonic stem cells express neuronal properties in vitro. Dev Biol 168: 342-357.
4. Blank, R.S., E.A. Swartz, M.M. Thompson, E.N. Olson, G.K. Owens (1995) A retinoic acid-induced clonal cell line derived from multipotential P19 embryonal carcinoma cells express smooth muscle characteristics. Circ Res 76: 742-749.
5. Blumberg, B., J. Bolado Jr, T.A. Moreno, C. Kintner, R.M. Evans, N. Papalopulu (1997) An essential role for retinoid signaling in anteroposterior neural patterning. Development 124: 373-379.
6. 3, and analogs. J Cell Biochem 56: 427-435.
7. Boncinelli E, A. Simeone, D. Acampora, F. Mavilio (1991) HOX gene activation by retinoic acid. Trends Genet 7: 329-334.
8. Boudjelal, M., R. Taneja, S. Matsubara, P. Bouillet, P. Dolle, P. Chambon (1997) Overexpression of Stral 3, a novel retinoic acid-inducible gene of the basic helix-loop-helix family, inhibits mesodermal and promotes neuronal differentiation of P19 cells. Genes Dev 11: 2052-2065.
9. Bouillet, P., M. Oulad Abdelghani, S. Vicaire, J.M. Garnier, B. Schuhbaur, P. Dolle, P. Chambon (1995) Efficient cloning of cDNAs of retinoic acid-responsive genes in P19 embryonal carcinoma cells and characterization of a novel mouse gene, Stral (mouse LERK-2/Eplg2). Dev Biol 170: 420-433.
10. Braun, T., H.-H. Arnold (1994) ES-cells carrying two inactivated myf-5 alleles form skeletal muscle cells: Activation of an alternative myf-5-independent differentiation pathway. Dev Biol 164: 24-36.
11. Breier, G., M. Bucan, U. Francke, A.M. Colberg-Poley, P. Gruss (1986) Sequential expression of murine homeo box genes during F9 EC cell differentiation. EMBO J 5: 2209-2215.
12. Chamhon, P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB J 10: 940-954.
13. Chen, Y., L. Huang, A.F. Russo, M. Solursh (1992) Retinoic acid is enriched in Hensen's node and is developmentally regulated in the early chicken embryo. Proc Natl Acad Sci USA 89: 10056-10059.
14. Chen, Y., M. Solursh (1992) Comparison of Hensen's node and retinoic acid in seconary axis induction in the early chick embryo. Dev Dyn 195: 142-151.
15. Dani, C., A.G. Smith, S. Dessolin, P. Leroy, L. Staccini, P. Villageois, C. Darimont, G. Ailhaud (1997) Differentiation of embryonic stem cells into adipocytes in vitro. J Cell Sci 110: 1279-1285.
16. Degos, L., C. Chomienne, M.T. Daniel, R. Berger, H. Dombret, P. Fenaux, S. Castaigne (1990) Treatment of first relapse in acute promyelocytic leukaemia with all-trans retinoic acid. Lancet 336: 1440-1441.
17. Doetschman, T.C., H. Eistetter, M. Katz, W. Schmidt, R. Kemler (1985) The in vitro development of blastocyst-derived embryonic stem cell lines: Formation of visceral yolk sac, blood islands and myocardium. J Embryol Exp Morphol 87: 27-45.
18. Drab, M., H. Haller, R. Bychkov, B. Erdmann, C. Lindschau, H. Haase, I. Morano, F.C. Luft, A.M. Wobus (1997) From totipotent embryonic stem cells to spontaneously contracting smooth muscle cells: A retinoic acid and db-cAMP in vitro differentiation model. FASEB J 11: 905-915.
19. Drysdale, T.A., K.D. Patterson, M. Saha, P.A. Krieg (1997) Retinoic acid can block differentiation of the myocardium after heart specification. Dev Biol 188: 205-215.
20. Durston, A.J., J.P. Timmermans, W.J. Hage, H.F. Hendriks, N.J. de Vries, M. Heideveld, P.D. Nieuwkoop (1989) Retinoic acid causes an anteroposterior transformation in the developing central nervous system. Nature 340: 140-144.
21. Edwards, M.K., J.F. Harris, M.W. McBurney (1983) Induced muscle differentiation in an embryonal carcinoma cell line. Mol Cell Biol 3: 2280-2286.
22. Edwards, M.K., M.W. McBurney (1983) The concentration of retinoic acid determines the differentiated cell types formed by a teratocarcinoma cell line. Dev Biol 98: 187-191.
23. Eichele, G. (1989) Retinoids and vertebrate limb pattern formation. Trends Genet 5: 246-251.
24. 1 integrin. J Cell Sci 109: 2989-2999.
25. Fraichard, A., O. Chassande, G. Bilbaut, C. Dehay, P. Savatier, J. Samarut (1995) In vitro differentiation of embryonic stem cells into glial cells and functional neurons. J Cell Sci 108: 3181-3188.
26. Gorry, P., T. Lufkin, A. Dierich, C. Rochette-Egly, D. Decimo, P. Dolle, M. Mark, B. Durand, P. Chambon (1994) The cellular retinoic acid binding protein I is dispensable. Proc Natl Acad Sci USA 91: 9032-9036.
27. Gruber, P.J., S.W. Kubalak, T. Pexieder, H.M. Sucov, R.M. Evans, K.R. Chien (1996) RXR alpha deficiency confers genetic susceptibility for aortic sac, conotruncal, atrioventricular cushion, and ventricular muscle defects in mice. J Clin Invest 98: 1332-1343.
28. Guan, K., J. Rohwedel, A.M. Wobus (1999) Embryonic stem cell differentiation models: Cardiogenesis, myogenesis, neurogenesis, epithelial and vascular smooth muscle cell differentiation in vitro. Cytotechnology 30: 211-226.
29. Hemmati-Brivanlou, A., D. Melton (1997) Vertebrate embryonic cells will become nerve cells unless told otherwise. Cell 88: 13-17.
30. Hogan, B.L., C. Thaller, G. Eichele (1992) Evidence that Hensen's node is a site of retinoic acid synthesis. Nature 359: 237-241.
31. Huang, M.E., Y.C. Ye, S.R. Chen, J.R. Chai, J.X. Lu, L. Zhoa, L.J. Gu, Z.Y. Wang (1988) Use of all-trams retinoic acid in the treatment of acute promyelocytic leukemia. Blood 72: 567-572.
32. Hunt, P., R. Krumlauf (1991) Deciphering the Hox code: Clues to patterning branchial reg ons of the head. Cell 66: 1075-1078.
33. Jeannotte, L., M. Lemieux, J. Charron, F. Poirier, E.J. Robertson (1993) Specification of axial identity in the mouse: Role of the Hoxa-5 (Hox 1.3) gene. Genes Dev 7: 2085-2090.
34. Jones-Villeneuve, E.M., M.A. Rudnicki, J.F. Harris, M.W. McBurney (1983) Retinoic acid-induced neural differentiation of embryonal carcinoma cells. Mol Cell Biol 3: 2271-2279.
35. Jonk, L.J.C., M.E.J. de Jonge, F.A. Kruyt, C.L. Mummery, P.T. van der Saag, W. Kruijer (1992) Aggregation and cell cycle dependent retinoic acid receptor mRNA expression in P19 embryonal carcinoma cells. Mech Dev 36: 165-172.
36. Kastner, P., J.M. Grondona, M. Mark, A. Gansmuller, M. LeMeur, D. Decimo, J.L. Vonesch, P. Dolle, P. Chambon (1994) Genetic analysis of RXR alpha developmental function: Convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell 78: 987-1003.
37. Kastner, P., M. Mark, P. Chambon (1995) Nonsteroid nuclear receptors: What are genetic studies telling us about their role in real life? Cell 83: 859-869.
38. Kastner, P., M. Mark, N. Ghyselinck, W. Krezel, V. Dupe, J.M. Grondona, P. Chambon (1997) Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development 124: 313-326.
39. Kessel, M. (1992) Respecification of vertebral identities by retinoic acid. Development 115: 487-501.
40. Kessel, M., P. Gruss (1991) Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell 67: 89-104.
41. Kochhar, D.M. (1973) Limb development in mouse embryos. I. Analysis of teratogenic effects of retinoic acid. Teratology 7: 289-298.
42. Kolm, P.J., H.L. Sive (1997) Retinoids and posterior neural induction: A reevaluation of Nieuwkoop's two-step hypothesis. Cold Spring Harb Symp Quant Biol 62: 511-521.
43. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell 78: 191-201.
44. Kruyt, F.A.E., C.E. van den Brink, L.H.K. Defize, M.-J. Donath, P. Kastner, W. Kruijer, P. Chambon, P.T. van der Saag (1991) Transcriptional regulation of retinoic acid receptor beta in retinoic acid-sensitive and -resistant P19 embryocarcinoma cells. Mech Dev 33: 171-178.
45. Lammer, E.J., D.T. Chen, R.M. Hoar N.D. Agnish, P.J. Benke, J.T. Braun, C.J. Curry, P.M. Fernhoff, A.W. Grix Jr., I.T. Lott, J.M. Richard, S.C. Sun (1985) Retinoic acid embryopathy. N Engl J Med 313: 837-841
46. Le Mouellic, H., Y. Lallemand, P. Brulet (1992) Homeosis in the mouse induced by a null mutation in the Hox-3.1 gene. Cell 69: 251-264.
47. Lee, R.Y., J. Luo, R.M. Evans, V. Giguere, H.M. Sucov (1997) Compartment-selective sensitivity of cardiovascular morphogenesis to combinations of retinoic acid receptor gene mutations. Circ Res 80: 757-764.
48. Lotan, R. (1980) Effects of vitmain A and its analogs (retinoids) on normal and neoplastic cells. Biochim Biophys Acta 605: 33-91.
49. Lotan, R. (1996) Retinoids in cancer chemoprevention. FASEB J 10: 1031-1039.
50. Maltsev, V.A., J. Rohwedel, J. Hescheler, A.M. Wobus (1993) Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech Dev 44: 41-50.
51. Maltsev, V.A., A.M. Wobus, J. Rohwedel, M. Bader, J. Hescheler (1994) Cardiomyocytes differentiated in vitro from embryonic stem cells developmentally express cardiac-specific genes and ionic currents. Circ Res 75: 233-244.
52. Mangelsdorf, D.J., C. Thummel, M. Beato, P. Herrlich, G. Schutz, K. Umesono, B. Blumberg, P. Kastner, M. Mark, P. Chambon, R.M. Evans (1995) The nuclear receptor superfamily: The second decade. Cell 83: 835-839.
53. Marshall, H., S. Nonchev, M.H. Sham, I. Muchamore, A. Lumsden, R. Krumlauf (1992) Retinoic acid alters hindbrain Hox code and induces transformation of rhombomeres 2/3 into a 4/5 identity. Nature 360: 737-741.
54. Marshall, H., M. Studer, H. Popperl, S. Aparicio, A. Kuroiwa, S. Brenner, R. Krumlauf (1994) A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature 370: 567-571.
55. Morriss-Kay, G.M., N. Sokolova (1996) Embryonic development and pattern formation. FASEB J 10: 961-968.
56. Okabe, S., K. Forsberg-Nilsson, A.C. Spiro, M. Segal, R.D. McKay (1996) Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech Dev 59: 89-102.
57. Papalopulu, N., C. Kintner ( 1996) A posteriorising factor, retinoic acid, reveals that anteroposterior patterning controls the timing of neuronal differentiation in Xenopus neuroectoderm. Development 122: 3409-3418.
58. Piccolo, S., Y. Sasai, B. Lu, E.M. De Robertis (1996) Dorsoventral patterning in Xenopus: Inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589-598.
59. Pöpperl, H., M.S. Featherstone (1993) Identification of a retinoic acid response element upstream of the murine Hox-4.2 gene. Mol Cell Biol 13: 257-265.
60. Ramirez-Solis, R., H. Zheng, J. Whiting, R. Krumlauf, A. Bradley (1993) Hoxb-4 (Hox-2.6) mutant mice show homeotic transformation of a cervical vertebra and defects in the closure of the sternal rudiments. Cell 73: 279-294.
61. 1 integrin function results in a retardation of myogenic, but an acceleration of neuronal, differentiation of embryonic stem cells in vitro. Dev Biol 201: 167-184.
62. Rohwedel, J., V. Horák, M. Hebrok, E.M. Füchtbauer, A.M. Wobus (1995) M-twist expression inhibits mouse embryonic stem cell-derived myogenic differentiation in vitro. Exp Cell Res 220: 92-100.
63. Rohwedel, J., T. Kleppisch, U. Pich, K. Guan, S. Jin, W. Zuschratter, C. Hopf, W. Hoch, J. Hescheler, V. Witzemann, A.M. Wobus (1998b) Formation of postsynaptic-like membranes during differentiation of embryonic stem cells in vitro. Exp Cell Res 239: 214-225.
64. Rohwedel, J., V. Maltsev, E. Bober, H.-H. Arnold, J. Hescheler, A.M. Wobus (1994) Muscle cell differentiation of embryonic stem cells reflects myogenesis in vivo: Developmentally regulated expression of myogenic determination genes and functional expression of ionic currents. Dev Biol 164: 87-101.
65. Rose, O., J. Rohwedel, S. Reinhardt, M. Bachmann, M. Cramer, M. Rotter, A. Wobus, A. Starzinski-Powitz (1994) Expression of M-cadherin protein in myogenic cells during prenatal mouse development and differentiation of embryonic stem cells in culture. Dev Dyn 201: 245-259.
66. Rudnicki, M.A., M.W. McBurney (1987) Cell culture methods and induction of differentiation of embryonal carcinoma cell lines; in Robertson, E.J. (ed): Teratocarcinomas and Embryonic Stem Cells. Oxford. IRL Press, pp 19-49.
67. Sasai, Y., E.M. De Robertis (1997) Ectodermal patterning in vertebrate embryos. Dev Biol 182: 5-20.
68. Schmitt, R.M., E. Bruyns, H.R. Snodgrass (1991) Hematopoietic development of embryonic stem cells in vitro: Cytokine and receptor gene expression. Genes Dev 5: 728-740.
69. Scott, M.P., J.W. Tamkun, G.W. Hartzell (1989) The structure and function of the homeodomain. Biochim Biophys Acta 989: 25-48.
70. Shea, T.B., I. Fischer, V.S. Sapirstein (1985) Effect of retinoic acid on growth and morphological differentiation of mouse NB2a neuroblastoma cells in culture. Brain Res 353: 307-314.
71. Simeone, A., D. Acampora, L. Arcioni, P.W. Andrews, E. Boncinelli, F. Mavilio (1990) Sequential activation of HOX2 homeobox genes by retinoic acid in human embryonal carcinoma cells. Nature 346: 763-766.
72. Simon, M.C., L. Pevny, M.V. Wiles, G. Keller, F. Costantini, S.H. Orkin (1992) Rescue of erythroid development in gene targeted GATA-1-mouse embryonic stem cells. Nature Genet 1: 92-98.
73. Sive, H.L., B.W. Draper, R.M. Harland, H. Weintraub (1990) Identification of a retinoic acid-sensitive period during primary axis formation in Xenopus laevis. Genes Dev 4: 932-942.
74. Soudais, C., M. Bielinska, M. Heikinheimo, C.A. MacArthur, N. Narita, J.E. Saffitz, M.C. Simon, J.M. Leiden, D.B. Wilson (1955) Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121: 3877-3888.
75. Strickland, S., Mahdavi (1978) The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell 15: 393-403.
76. Strübing, C., G. Ahnert Hilger, J. Shan, B. Wiedenmann, J. Hescheler, A.M. Wobus (1995) Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech Dev 53: 275-287.
77. Sucov, H.M., E. Dyson, C.L. Gumeringer, J. Price, K.R. Chien, R.M. Evans (1994) RXR alpha mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev 8: 1007-1018.
78. Tabin, C.J. (1991) Retinoids, homeoboxes, and growth factors: Toward molecular models for limb development. Cell 66: 199-217.
79. Taylor, S.M., P.A. Jones (1979) Multiple new phenotypes induced in 10T1/2 and 3T3 cells treated with 5-azacytidine. Cell 17: 771-779.
80. Thomas, K.R., M.R. Capecchi (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51: 503-512.
81. Wiles, M.V. (1993) Embryonic stem cell differentiation in vitro. Methods Enzymol 225: 900-918.
82. Wilson, J.G., C.B. Roth, J. Warkany (1953) An analysis of the syndrome of malformations induced by maternal vitamin A deficiency. Effects of restoration of vitamin A at various times during gestation. Am J Anat 92: 189-217.
83. Wilson, J.G., J. Warkany (1949) Aortic arch and cardiac anomalies in the offspring of vitamin A deficient rats. Am J Anat 85: 113-155.
84. Wobus, A.M., K. Guan (1998) Embryonic stem cell-derived cardiac differentiation: Modulation of differentiation and 'loss-of-function' analysis in vitro. Trends Cardiovasc Med 8: 64-74.
85. Wobus, A.M., K. Guan, J. Shan, M.C. Wellner, J. Rohwedel, J. Guanju, B. Fleischmann, H.A. Katus, J. Hescheler, W.M. Franz (1997) Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J Mol Cell Cardiol 29: 1525-1539.
86. 2+ channels. In Vitro Cell Dev Biol Anim 30A: 425-434.
87. Wobus, A.M., J. Rohwedel, V. Maltsev, J. Hescheler (1994b) In vitro differentiation of embryonic stem cells into cardiomyocytes or skeletal muscle cells is specifically modulated by retinoic acid. Rouxs Arch Dev Biol 204: 36-45.
88. 2+ channel blockers. Differentiation 48: 173-182.
89. Wolf, G. (1996) A history of vitamin A and retinoids. FASEB J 10: 1102-1107.
90. Yu, V.C., C. Delsert, B. Andersen, J.M. Holloway, O.V. Devary, A.M. Naar, S.Y. Kim, J.M. Boutin, C.K. Glass, M.G. Rosenfeld (1991) RXR beta: A coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell 67: 1251-1266.