RXRα-null F9 embryonal carcinoma cells are resistant to the differentiation, anti-proliferative and apoptotic effects of retinoids

EMBO Journal

Volumn 15, Issue 16, 1996, Pages 4142-4155

  Clifford, John ^a   Chiba, Hideki ^a   Sobieszczuk, Dorothy ^a   Metzger, Daniel ^a   Chambon, Pierre ^a  

^a PSL Research University   (France)

Author keywords

Apoptosis; Cellular proliferation; Heterodimers; RXR RAR; RXR ; Synthetic retinoids

Indexed keywords

RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR; RETINOID; TRANSCRIPTION FACTOR; TUMOR PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; EMBRYO; EMBRYONAL CARCINOMA; ENDODERM; GENETIC RECOMBINATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; ANIMAL; CELL CULTURE; CELL DIVISION; COMPARATIVE STUDY; CYTOLOGY; DRUG EFFECT; DRUG RESISTANCE; GENE TARGETING; GENETICS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; CARCINOMA, EMBRYONAL; CELL DIFFERENTIATION; CELL DIVISION; DRUG RESISTANCE; ENDODERM; GENE TARGETING; MICE; NEOPLASM PROTEINS; RECEPTORS, RETINOIC ACID; RETINOID X RECEPTORS; RETINOIDS; TRANSCRIPTION FACTORS; TUMOR CELLS, CULTURED;

EID: 0029736862     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1460-2075.1996.tb00789.x     Document Type: Article

References (72)

1. Amos, B. and Lotan, R. (1991) Retinoid-sensitive cells and cell lines. Methods Enzymol., 190, 217-225.
2. Atencia, R., Garcia-Sanz, M., Unda, F. and Arechaga, J. (1994) Apoptosis during retinoic acid-induced differentiation of F9 embryonal carcinoma cells. Exp. Cell Res., 214, 663-667.
3. Bouillet, P., Oulad-Abdelghani, M., Vicaire, S., Garnier, J.-M., Schuhbaur, B., Dollé, P. and Chambon, P. (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.
4. Boylan, J., Lohnes, D., Taneja, R., Chambon, P. and Gudas, L.J. (1993) Loss of RARγ function by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc. Natl Acad Sci. USA, 90, 9601-9605.
5. Boylan, J., Lufkin, T., Achkar, C.C., Taneja, R., Chambon, P. and Gudas, L.J. (1995) 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, 843-851.
6. Chambon, P. (1994) The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol., 5, 115-125.
7. deThé, H., Vivanco-Ruiz, M., Tiollais, P., Stunnenberg, H. and Dejean, A. (1990) Identification of a retinoic acid responsive element in the retinoic acid receptor β gene. Nature, 343, 177-180.
8. Duprey, P. Chowdhury, K., Dressler, G.R., Balling, R., Simon, D., Guenet, J.-L. and Gruss, P. (1988) A mouse gene homologous to the drosophila gene caudal is expressed in epithelial cells from the embryonic intestine. Genes Dev., 2, 1647-1654.
9. Durand, B., Saunders, M., Leroy, P., Leid, M. and Chambon, P. (1992) All-trans and 9-cis retinoic acid induction of CRABPII transcription is mediated by RAR-RXR heterodimers bound to DR1 and DR2 repeated motifs. Cell, 71, 73-85.
10. Durand, B., Saunders, M., Gaudon, C., Roy, B., Losson, R. and Chambon, P. (1994) Activation function 2 (AF-2) of retinoic acid receptor and 9-cis retinoic acid receptor: presence of a conserved autonomous constitutive activation domain and influence of the nature of the response element on AF-2 activity. EMBO J., 13, 5370-5382.
11. Fesus, L., Davies, P.J.A. and Piacentini, M. (1991) Apoptosis: molecular mechanisms in programmed cell death. Eur. J. Cell Biol., 56, 170-177.
12. Fisher, D.E. (1994) Apoptosis in cancer therapy: crossing the threshold. Cell, 78, 539-542.
13. Forman, B.M., Umesono, K., Chen, J. and Evans, R.M. (1995) Unique response pathways are established by allosteric interactions among nuclear hormone receptors. Cell, 81, 541-550.
14. Giguère, V. (1994) Retinoic acid receptors and cellular retinoid binding proteins: complex interplay in retinoid signaling. Endocrine Rev., 15, 61-79.
15. Giguère, V., Lyn, S., Yip, P., Siu, C.-H. and Amin, S. (1990) Molecular cloning of cDNA encoding a second cellular retinoic acid-binding protein. Proc. Natl Acad. Sci. USA, 87, 6233-6237.
16. Glass, C.K. (1994) Differential recognition of target genes by nuclear receptor monomers, dimers, and heterodimers. Endocrine Rev., 15, 391-407.
17. Glick, A.B., Flanders, K.C., Danielpour, D., Yuspa, S.H. and Sporn, M.B. (1989) Retinoic acid induces transforming growth factor-β2 in cultured keratinocytes and mouse epidermis. Cell Regul., 1, 87-97.
18. Gorin, M.B., Cooper, D.L., Eiferman, F., van de Rijn, P. and Tilghman, S.M. (1981) The evolution of α-fetoprotein and albumin I. A comparison of the primary amino acid sequences of mammalian α-fetoprotein and albumin. J. Biol. Chem., 256, 1954-1959.
19. Gronemeyer, H. and Laudet, V. (1995) Nuclear receptors. Protein Profile, 2, 1173-1308.
20. Gudas, L.J., Sporn, M.B. and Roberts, A.B. (1994) Cellular biology and biochemistry of the retinoids. In Sporn, M.B. and Roberts, A.B. (eds), The Retinoids: Biology, Chemistry, and Medicine. Raven Press, New York, pp. 443-520.
21. Hazel, T.G., Nathans, D. and Lau, L. (1988) A gene inducible by serum growth factors encodes a member of the steroid and thyroid hormone receptor superfamily. Proc. Natl Acad. Sci. USA, 85, 8444-8448.
22. Heath, J.K. (1987) Experimental analysis of teratocarcinoma cell multiplication and purification of embryonal carcinoma-derived growth factor. In Robertson, E.J. (ed.), Teratocarcinomas and Embryonic Stem Cells: A Practical Approach. IRL Press, Oxford, UK, pp. 183-206.
23. Hogan, B.L., Taylor, A. and Adamson, E. (1981) Cell interactions modulate embryonal carcinoma cell differentiation into parietal or visceral endoderm. Nature, 291, 235-237.
24. Hogan, B.L.M., Barlow, D. and Tilly, R. (1983) F9 teratocarcinoma cells as a model for the differentiation of parietal and visceral endoderm in the mouse embryo. Cancer Surveys, 2, 115-140.
25. Hong, W.K. and Itri, L.M. (1994) Retinoids and human cancer. In Sporn, M.B. and Roberts, A.B. (eds), The Retinoids: Biology, Chemistry, and Medicine. Raven Press, New York, pp. 597-630.
26. Kastner, P., Grondona, J.M., Mark, M., Gansmuller, A., LeMeur, M., Decimo, D., Vonesch, J., Dollé, P. and Chambon, P. (1994) Genetic analysis of RXRα developmental function: convergence of RXR and RAR signaling pathways in heart and eye morphogenesis. Cell, 78, 987-1003.
27. Kastner, P., Mark, M. and Chambon, P. (1995) Nonsteroid nuclear receptors: What are genetic studies telling us about their role in real life? Cell, 83, 859-869.
28. Kastner, P. et al. (1996) Abnormal spermatogenesis in RXRβ mutant mice. Genes Dev., 10, 80-92.
29. Kelly, D., Campbell, W.J., Tiesman, J. and Rizzino, A. (1990) Regulation and expression of transforming growth factor type-β during early mammalian development. Cytotechnology, 4, 227-242.
30. Kerr, J.F.R., Gobé, G.C., Winterford, C.M. and Harmon, B.V. (1995) Anatomical methods in cell death. Methods Cell Biol., 46, 1-27.
31. Killen, P.D., Burbelo, P., Sakurai, Y. and Yamada, Y. (1988) Structure of the amino-terminal portion of the murine α1(IV) collagen chain and the corresponding region of the gene. J. Biol. Chem., 263, 8706-8709.
32. Krowczynska, A.M., Coutts, M., Makrides, S. and Brawerman, G. (1989) The mouse homologue of the human acidic ribosomal phosphoprotein PO: a highly conserved polypeptide that is under translational control. Nucleic Acids Res., 17, 6408.
33. Kuchler, R. (1977) Developmenl of animal cell populations in vitro. In Kuchler, R. (ed.), Biochemical Methods in Cell Culture and Virology. Dowden, Hutchinson and Ross Inc., Stroudsburg, PA, pp. 90-113.
34. Langston, A.W. and Gudas, L.J. (1992) Identification of a retinoic acid responsive enhancer 3′ of the murine homeobox gene Hox-1.6. Mech. Dev., 38, 217-228.
35. LaRosa, G.L. and Gudas, L.J. (1988a) An early effect of retinoic acid: Cloning of an mRNA (Era-1) exhibiting rapid and protein synthesis-independent induction during teratocarcinoma stem cell differentiation. Proc. Natl Acad. Sci. USA, 85, 329-333.
36. LaRosa, G.L. and Gudas, L.J. (1988b) Early retinoic acid-induced F9 teratocarcinoma stem cell gene ERA-1: alternate splicing creates transcripts for a homeobox-containing protein and one lacking the homeobox. Mol. Cell. Biol., 8, 3906-3917.
37. Law, S.W., Conneely, O.M., DeMayo, F.J. and O'Malley, B.W. (1992) Identification of a new brain-specific transcription factor, NURR1. Mol. Endocrinol., 6, 2129-2135.
38. Leblanc, B.P. and Stunnenberg, H.G. (1995) 9-cis retinoic acid signaling: changing partners causes some excitement. Genes Dev., 9, 1811-1816.
39. Lehmann, J.M., Jong, L., Fanjul, A., Cameron, J.F., Lu, X.P., Haefner, P., Dawson, M.I. and Pfahl, M. (1992) Retinoids selective for retinoid X receptor response pathways. Science, 258, 1944-1946.
40. Leid, M., Kastner, P. and Chambon, P. (1992a) Multiplicity generates diversity in the retinoic acid signaling pathways. Trends Biochem. Sci., 17, 427-433.
41. Leid, M. et al. (1992b) Purification, cloning, and RXR identity of the HeLa cell factor with which RAR or TR heterodimerizes to bind target sequences efficiently. Cell, 68, 377-395.
42. Linder, S., Krondahl, U., Sennerstam, R. and Ringertz, N.R. (1981) Retinoic acid-induced differentiation of F9 embryonal carcinoma cells. Exp. Cell Res., 132, 453-460.
43. Lotan, R. (1980) Effect of vitamin A and its analogs (retinoids) on normal and neoplastic cells. Biochim. Biophys. Acta, 605, 33-91.
44. Love, J.M. and Gudas, L.J. (1994) Vitamin A. differentiation and cancer. Curr. Biol., 6, 825-831.
45. Mangelsdorf, D.J. and Evans, R.M. (1995) The RXR heterodimers and orphan receptors. Cell, 83, 841-850.
46. Mangelsdorf, D.J., Ong, E.S., Dyck, J.A. and Evans, R.M. (1990) Nuclear receptor that identifies a novel retinoic acid response pathway. Nature, 345, 224-229.
47. Marshall, H., Studer, M., Popperl, H., Aparicio, S., Kuroiwa, A., Brenner, S. and Krumlauf, R. (1994) A conserved retinoic acid response element required for early expression of the homeobox gene Hoxb-1. Nature, 370, 567-571.
48. Martin, S.J., Bradley, J.G. and Cotter, T.G. (1990) HL-60 cells induced to differentiate towards neutrophils subsequently die via apoptosis. Clin. Exp. Immunol., 79, 448-453.
49. Metzger, D., Clifford, J., Chiba, H. and Chambon, P. (1995) Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre-recombinase. Proc. Natl Acad. Sci. USA, 92, 6991-6995.
50. Meyer, B.I. and Gruss, P. (1993) Mouse Cdx1 expression during gastrulation. Development, 117, 191-203.
51. Murphy, P. and Hill, R.E. (1991) Expression of the mouse labial-like homeobox-containing genes, Hox 2.9 and Hox 1.6, during segmentation of the hindbrain. Development, 111, 61-74.
52. Nagy, L., Thomazy, V.A., Shipley, G.L., Fesus, L., Lamph, W., Heyman, R.A., Chandraratna, R.A.S. and Davies, P.J.A. (1995) Activation of retinoid X receptors induces apoptosis in HL-60 cell lines. Mol. Cell Biol., 15, 3540-3551.
53. Noma, T., Glick, A.B., Geiser, A.G., O'Reilly, M.A., Miller, J., Roberts, A.B. and Sporn, M.B. (1991) Molecular cloning and structure of the human transforming growth factor-β2 gene promoter. Growth Factors, 4, 247-255.
54. Perlmann, T. and Jansson, L. (1995) A novel pathway for vitamin A signaling mediated by RXR heterodimerization with NGFI-B and Nurr1. Genes Dev., 9, 769-782.
55. Raff, M.C., Barres, B.A., Burne, J.F., Coles, H.S., Ishizaki, Y. and Jacobson, M.D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science, 262, 695-700.
56. Rochette-Egly, C., Lutz, Y., Pfister, V., Heyberger, S., Scheuer, I., Chambon, P. and Gaub, M.-P. (1994) Detection of retinoid X receptors using specific monoclonal and polyclonal antibodies. Biochem. Biophys. Res. Commun., 204, 525-536.
57. Rogers, M.B., Watkins, S.C. and Gudas, L.J. (1990) Gene expression in visceral endoderm: A comparison of mutant and wild-type F9 embryonal carcinoma cell differentiation. J Cell Biol., 110, 1767-1777.
58. Rosenstraus, M.J., Sundell, C.L. and Liskay, R.M. (1982) Cell-cycle characteristics of undifferentiated and differentiating embryonal carcinoma cells. Dev. Biol., 89, 516-520.
59. Roy, B., Taneja, R. and Chambon, P. (1995) Synergistic activation of expression of retinoic acid (RA)-responsive genes and induction of embryonal carcinoma cell differentiation by an RA receptor α (RARα)-, RARβ-, or RARγ-selective ligand in combination with a retinoid X receptor-specific ligand. Mol. Cell. Biol., 15, 6481-6487.
60. Sasaki, M., Kato, S., Kohno, K., Martin, G.R. and Yamada, Y. (1987) Sequence of the cDNA encoding the laminin B1 chain reveals a multidomain protein containing cysteine-rich repeats. Proc. Natl Acad. Sci. USA, 84, 935-939.
61. Sauer, B. and Henderson, N. (1990) Targeted insertion of exogenous DNA into the eukaryotic genome by the Cre recombinase. New Biol., 2, 441-449.
62. Sleigh, M.J. (1992) Differentiation and proliferation in mouse embryonal carcinoma cells. BioEssays, 14, 769-775.
63. Smith, M.A., Parkinson, D.R., Cheson, B.D. and Friedman, M.A. (1992) Retinoids in cancer therapy. J. Clin. Oncol., 10, 839-864.
64. Strickland, S. and Mahdavi, V. (1978) The induction of differentiation in teratocarcinoma stem cells by retinoic acid. Cell, 15, 393-403.
65. Strickland, S., Smith, K.K. and Marotti, K.R. (1980) Hormonal induction of differentiation in teratocarcinoma stem cells: Generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell, 21, 347-355.
66. Sucov, H.M., Dyson, E., Gumeringer, C.L., Price, J., Chien, K.R. and Evans, R.M. (1994) RXRα mutant mice establish a genetic basis for vitamin A signaling in heart morphogenesis. Genes Dev., 8, 1007-1018.
67. Taneja, R., Bouillet, P., Boylan, J.F., Gaub, M.-P., Roy, B., Gudas, L.J. and Chambon, P. (1995) Reexpression of retinoic acid receptor (RAR)γ or overexpression of RARα or RARβ in RARγ-null F9 cells reveals a partial functional redundancy between the three RAR types. Proc. Natl Acad. Sci. USA, 92, 7854-7858.
68. Wan, Y.-J., Wang, L. and Wu, T.-C. (1994) The expression of retinoid X receptor genes is regulated by all-trans and 9-cis-retinoic acid in F9 teratocarcinoma cells. Exp. Cell Res., 210, 56-61.
69. Wang, S.-Y. and Gudas, L.J. (1983) Isolation of cDNA clones specific for collagen IV and laminin from mouse teratocarcinoma cells. Proc. Natl Acad. Sci. USA, 80, 5880-5884.
70. Yu, V.C. et al. (1991) RXRβ: A coregulator that enhances binding of retinoic acid, thyroid hormone, and vitamin D receptors to their cognate response elements. Cell, 67, 1251-1266.
71. Zelent, A., Krust, A., Petkovich, M., Kastner, P. and Chambon, P. (1989) Cloning of murine α and β retinoic acid receptors and a novel receptor γ predominantly expressed in skin. Nature, 339, 714-717.
72. Zelent, A., Mendelsohn, C., Kastner, P., Krust, A., Garnier, J.-M., Ruffenach, F., Leroy, P. and Chambon, P. (1991) Differentially expressed isoforms of the mouse retinoic acid receptor β are generated by usage of two promoters and alternative splicing. EMBO J., 10, 71-81.