BMP4- and RA-induced apoptosis is mediated through the activation of retinoic acid receptor α and γ in P19 embryonal carcinoma cells

Experimental Cell Research

Volumn 242, Issue 1, 1998, Pages 165-173

  Glozak, Michele A ^a   Rogers, Melissa B ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE; PROTEIN SUBUNIT; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; EMBRYONAL CARCINOMA; GENE EXPRESSION REGULATION; NERVE CELL DIFFERENTIATION; PRIORITY JOURNAL; PROTEIN INDUCTION; RECEPTOR INTRINSIC ACTIVITY; SIGNAL TRANSDUCTION;

EID: 0031868837     PISSN: 00144827     EISSN: None     Source Type: Journal    
DOI: 10.1006/excr.1998.4075     Document Type: Article

References (51)

1. Graham, A., Francis-West, P., Brickell, P., and Lumsden, A. (1994). The signalling molecule BMP4 mediates apoptosis in the rhombencephalic neural crest. Nature 372, 684-686.
2. Gañan, Y., Macias, D., Duterque-Coquillaud, M., Ros, M. A., and Hurle, J. M. (1996). Role of TGFβs and BMPs as signals controlling the position of the digits and the areas of interdigital cell death in the developing chick limb autopod. Development 122, 2349-2357.
3. Macias, D., Gañan, Y., Sampath, T. K., Piedra, M. E., Ros, M. A., and Hurle, J. M. (1997). Role of BMP-2 and OP-1 (BMP-7) in programmed cell death and skeletogenesis during chick limb development. Development 124, 1109-1117.
4. tenDijke, P., Miyazono, K., and Heldin, C.-H. (1996). Signaling through hetero-oligomeric complexes of type I and type II serine/threonine kinase receptors. Curr. Opin. Cell Biol. 8, 139-145.
5. Baker, J. C., and Harland, R. M. (1997). From receptor to nucleus: The Smad pathway. Curr. Opin. Genet. Dev. 7, 467-473.
6. Zou, H., and Niswander, L. (1996). Requirement for BMP signaling in interdigital apoptosis and scale formation. Science 272, 738-741.
7. Hofmann, C., and Eichele, G. (1994). Retinoids in development. In "The Retinoids: Biology, Chemistry and Medicine" (M. B. Sporn, A. B. Roberts, and D. S. Goodman, Eds.), Raven Press, New York.
8. Leid, M., Kastner, P., and Chambon, P. (1992). Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sci. 17, 427-433.
9. Zhang, L.-X., Mills, K. J., Dawson, M. I., Collins, S. J., and Jetton., A. M. (1995). Evidence for the involvement of retinoic acid receptor RAR α-dependent signalling pathway in the induction of tissue transglutaminase and apoptosis by retinoids. J. Biol. Chem. 270, 6022-6029.
10. 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.
11. Martin, G. (1980). Teratocarcinomas and mammalian embryo-genesis. Science 209, 768-776.
12. Gamow, E. I., and Prescott, D. M. (1970). The cell life cycle during early embryogenesis of the mouse. Exp. Cell Res. 59, 117-123.
13. Rosenstraus, M., Sundell, C., and Liskay, R. (1982). Cell-cycle characteristics of undifferentiated and differentiating embryonal carcinoma cells. Dev. Biol. 89, 516-520.
14. Savatier, P., Lapillonne, H., van Grunsven, L. A., Rudkin, B. B., and Samarut, J. (1996). Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene 12, 309-322.
15. Rossant, J., and McBurney, M. W. (1982). The developmental potential of a euploid male teratocarcinoma cell line after blastocyst injection. J. Embryol. Exp. Morphol. 70, 99-112.
16. Jones-Villeneuve, E. M. V., McBurney, M. W., Rogers, K. A., and Kalnins, V. I. (1982). Retinoic acid induces embryonal carcinoma cells to differentiate into neurons and glial cells. J. Cell Biol. 94, 253-262.
17. Mummery, C. L., van den Brink, C. E., and de Laat, S. W. (1987). Commitment to differentiation induced by retinoic acid in P19 embryonal carcinoma cells is cell cycle dependent. Dev. Biol. 121, 10-19.
18. Glozak, M. A., and Rogers, M. B. (1996). Specific induction of apoptosis in P19 embryonal carcinoma cells by retinoic acid and BMP2 or BMP4. Dev. Biol. 179, 458-470.
19. Horn, V., Minucci, S., Ogryzko, V. V., Adamson, E. D., Howard, B. H., Levin, A. A., and Ozato, K. (1996). RAR and RXR selective ligands cooperatively induce apoptosis and neuronal differentiation in P19 embryonal carcinoma cells. FASEB J. 10, 1071-1077.
20. Jonk, L. J. C., deJonge, M. E. J., Kruyt, F. A. E., Mummery, C. L., van der Saag, P. T., and Kruijer, W. (1992). Aggregation and cell cycle dependent retinoic acid receptor mRNA expression in P19 embryonal carcinoma cells. Mech. Dev. 36, 165-172.
21. Bain, G., and Gottlieb, D. I. (1994). Expression of retinoid X receptors in P19 embryonal carcinoma cells and embryonic stem cells. Biochem. Biophys. Res. Commun. 200, 1252-1256.
22. Bernard, B. A., Bernardon, J.-M., Delescluse, C., Martin, B., Lenoir, M.-C., Maignan, J., Charpentier, B., Pilgrim, W. R., Reichert, U., and Shroot, B. (1992). Identification of synthetic retinoids with selectivity for human nuclear retinoic acid receptor g. Biochem. Biophys. Res. Commun. 186, 977-983.
23. Apfel, C., Bauer, F., Crettaz, M., Forni, L., Kamber, M., Kaufmann, F., LeMotte, P., Pirson, W., and Klaus, M. (1992). A retinoic acid receptor alpha antagonist selectively counteracts retinoic acid effects. Proc. Natl. Acad. Sci. USA 89, 7129-7133.
24. Szondy, Z., Reichert, U., Bernardon, J. M., Michel, S., Toth, R., Ancian, P., Ajzner, E., and Fesus, L. (1997). Induction of apoptosis by retinoids and retinoic acid receptor gamma-selective compounds in mouse thymocytes through a novel apoptosis pathway. Mol. Pharmacol. 51, 972-982.
25. Boehm, M. F., Zhang, L., Badea, B. A., White, S. K., Mais, D. E., Berger, E., Suto, C. M., Goldman, M. E., and Heyman, R. A. (1994). Synthesis and structure-activity relationships of novel retinoid X receptor-selective retinoids. J. Med. Chem. 37, 2930-2941.
26. Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. (Eds.) (1995). "Current Protocols in Molecular Biology," Wiley, New York.
27. Rio, M. C., Bellocq, J. P., Gairard, B., Rasmussen, U. B., Krust, A., Koehl, C., Calderoli, H., Schiff, V., Renaud, R., and Chambon, P. (1987). Specific expression of the pS2 gene in subclasses of breast cancers in comparison with expression of the estrogen and progesterone receptors and the oncogene ERBB2. Proc. Natl. Acad. Sci. USA 84, 9243-9247.
28. Gubler, M. L., and Sherman, M. I. (1985). Metabolism of retinoids by embryonal carcinoma cells. J. Biol. Chem. 260, 9552-9558.
29. Thaller, C., Hofmann, C., and Eichele, G. (1993). 9-cis-Retinoic acid, a potent inducer of digit pattern duplications in the chick wing bud. Development 118, 957-965.
30. Heyman, R. A., Mangelsdorf, D. J., Dyck, J. A., Stein, R. B., Eichele, G., Evans, R. M., and Thaller, C. (1992). 9-cis-Retinoic acid is a high affinity ligand for the retinoid X receptor. Cell 68, 397-406.
31. Levin, A. A., Sturzenbecker, L. J., Kazmer, S., Bosakowski, T., Huselton, C., Allenby, G., Speck, J., Kratzeisen, C., Rosenberger, M., Lovey, A., and Grippo, J. F. (1992). 9-cis-Retinoic acid stereoisomer binds and activates the nuclear receptor RXRa. Nature 355, 359-361.
32. Ormerod, M. (Ed.) (1994). "Flow Cytometry: A Practical Approach," Oxford Univ. Press, Oxford.
33. Berg, R. W., and McBurney, M. W. (1990). Cell density and cell cycle effects on retinoic acid-induced embryonal carcinoma cell differentiation. Dev. Biol. 138, 123-135.
34. Allegretto, E. A., McClurg, M. R., Lazarchik, S. B., Clemm, D. L., Kerner, S. A., Elgort, M. G., Boehm, M. F., White, S. K., Pike, J. W., and Heyman, R. A. (1993). Transactivation properties of retinoic acid and retinoid X receptors in mammalian cells and yeast: Correlation with hormone binding and effects of metabolism. J. Biol. Chem. 268, 26625-26633.
35. Pratt, M. A. C., Kralova, J., and McBurney, M. W. (1990). Dominant negative mutation of the alpha retinoic acid receptor gene in a retinoic acid-nonresponsive embryonal carcinoma cell. Mol. Cell. Biol. 10, 6445-6453.
36. Kruyt, F. A. E., van der Veer, L. J., Mader, S., van den Brink, C. E., Feijen, A., Jonk, L. J. C., Kruijer, W., and van der Saag, P. T. (1992). Retinoic acid resistance of the variant embryonal carcinoma cell line RAC65 is caused by expression of a truncated RARα. Differentiation 49, 27-37.
37. Graupner, G., Malle, G., Maignan, J., Lang, G., Prunieras, M., and Pfahl, M. (1991). 6′-Substituted naphthalene-2-carboxylic acid analogs, a new class of retinoic acid receptor subtype-specific ligands. Biochem. Biophys. Res. Commun. 179, 1554-1561.
38. Piacentini, M., Davies, P. J. A., and Fesus, L. (1994). Tissue transglutaminase in cells undergoing apoptosis. In "Apoptosis II: The Molecular Basis of Apoptosis in Disease" (L. D. Tomei, and F. O. Cope, Eds.), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
39. Dawson, M. I., Chao, W., Pine, P., Jong, L., Hobbs, P. D., Rudd, C. K., Quick, T. C., Niles, R. M., Zhang, X., Lombardo, A., Ely, K. R., Shroot, B., and Fontana, J. A. (1995). Correlation of retinoid binding affinity to retinoic acid receptor a with retinoid inhibition of growth of estrogen receptor-positive MCF-7 mammary carcinoma cells. Cancer Res. 55, 4446-4451.
40. Spanjaard, R. A., Ikeda, M., Lee, P. J., Charpentier, B., Chin, W. W., and Eberlein, T. J. (1997). Specific activation of retinoic acid receptors (RARs) and retinoid X receptors reveals a unique role for RARy in induction of differentiation and apoptosis of S91 melanoma cells. J. Biol. Chem. 272, 18990-18999.
41. Roy, B., Taneja, R., and Chambon, P. (1995). Synergistic activation 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.
42. Boylan, J. F., 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.
43. Hsu, C. A., Rishi, A. K., Su-Li, X., Gerald, T. M., Dawson, M. I., Schiffer, C., Reichert, U., Shroot, B., Poirer, G. C., and Fontana, J. A. (1997). Retinoid induced apoptosis in leukemia cells through a retinoic acid nuclear receptor-independent pathway. Blood 89, 4470-4479.
44. Seewaldt, V. L., Johnson, B. S., Parker, M. B., Collins, S. J., and Swisshelm, K. (1995). Expression of retinoic acid receptor β mediates retinoic acid-induced growth arrest and apoptosis in breast cancer cells. Cell Growth Differ. 6, 1077-1088.
45. Lu, X.-P., Fanjul, A., Picard, N., Pfahl, M., Rungta, D., Nared-Hood, K., Carter, B., Piedrafita, J., Tang, S., Fabbrizio, E., and Pfahl, M. (1997). Novel retinoid-related molecules as apoptosis inducers and effective inhibitors of human lung cancer cells in vivo. Nature 3, 686-690.
46. Cowan, W. M., Fawcett, J. W., O'Leary, D. D., and Stanfield, B. B. (1984). Regressive events in neurogenesis. Science 225, 1258-1265.
47. Okazawa, H., Shimizu, J., Kamei, M., Imafuku, I., Hamada, H., and Kanazawa, I. (1996). Bcl-2 inhibits retinoic acid-induced apoptosis during the neural differentiation of embryonal stem cells. J. Cell Biol. 132, 955-968.
48. Ninomiya, Y., Adams, R., Morriss-Kay, G. M., and Eto, K. (1997). Apoptotic cell death in neuronal differentiation of P19 EC cells: Cell death follows reentry into S phase. J. Cell. Phys. 172, 25-35.
49. Lufkin, T., Lohnes, D., Mark, M., Dierich, A., Gorry, P., Gaub, M.-P., LeMeur, M., and Chambon, P. (1993). High postnatal lethality and testis degeneration in retinoic acid receptor α mutant mice. Proc. Natl. Acad. Sci. USA 90, 7225-7229.
50. Lohnes, D., Kastner, P., Dierich, A., Mark, M., LeMeur, M., and Chambon, P. (1993). Function of retinoic acid receptor γ in the mouse. Cell 73, 643-658.
51. Ahuja, H. S., James, W., and Zakeri, Z. (1997). Rescue of the limb deformity in hammertoe mutant mice by retinoic acid-induced cell death. Dev. Dyn. 208, 466-481.