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 Journal

Volumn 16, Issue 21, 1997, Pages 6452-6465

  Taneja, Reshma ^b   Rochette Egly, Cécile ^a   Plassat, Jean Luc ^a   Penna, Lucia ^a   Gaub, Marie Pierre ^c   Chambon, Pierre ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c HÔPITAL DE HAUTEPIERRE   (France)

Author keywords

Parietal endoderm; Primitive endoderm; Proline directed kinases; Protein kinase A; Signal transduction

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; PROLINE; PROTEIN KINASE; RETINOIC ACID; RETINOIC ACID RECEPTOR;

ANIMAL CELL; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN; CONTROLLED STUDY; ENDODERM; GENE INDUCTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSACTIVATION;

ANIMALS; BINDING SITES; CARCINOMA, EMBRYONAL; CELL DIFFERENTIATION; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENDODERM; LIGANDS; MICE; PHOSPHORYLATION; RECEPTORS, RETINOIC ACID; TRETINOIN; TUMOR CELLS, CULTURED;

ANIMALIA;

EID: 0030775347     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.21.6452     Document Type: Article

References (49)

1. Adra,C.N., Boer,P.H and McBurney,M.W. (1987) Cloning and expression of the mouse pgk-1 gene and the nucleotide sequence of its promoter. Gene, 60, 65-74.
2. Ali,S., Metzger,D., Bomert,J.M. and Chambon,P. (1993) Modulation of transcriptionaf activation by ligand-dependent phosphorylation of the human oestrogen receptor A/B region. EMBO J., 12, 1153-1160.
3. Blomhoff,R.B. (1994) Vitamin A in Health and Disease. Marcel Dekker, New York.
4. Bouillet,P., Oulad-Ahdelghani,M., Vicaite,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 Stra1 (mouse Lerk-2). Dev. Biol., 170, 420-433.
5. Boylan,J.F. Lohnes,D., Taneja,R., Chambon,P. and Gudas,L.J. (1993) Loss of retinoic acid receptor gamma function in F9 cells by gene disruption results in aberrant Hoxa-1 expression and differentiation upon retinoic acid treatment. Proc. Natl Acad. Sci. USA, 90, 9601-9605.
6. Boylan,J.F., Lufkin,T., Achkar,C.C., Taneja,R., Chambon,P. and Gudas, L.J. (1995) Targeted disruption of retinoic acid receplor alpha (RAR alpha) and RAR gamma results in receptor-specific alterations in retinoic acid-mediated differentiation and retinoic acid metabolism. Mol. Cell. Biol. 15, 843-851.
7. Brocard,J., Kastner,P. and Chambon,P. (1996) Two novel RXRα isoforms from mouse testis. Biochem. Biophys. Res. Commun., 229, 211-218.
8. Bunone,G., Briand,P.A., Miksicek,R.J. and Picard,D. (1996) Activation of the unliganded estrogen receptor by EGF involves the MAP kinase pathway and direct phosphorylation. EMBO J., 15, 2174-2183.
9. Chambon,P. (1994) The retinoid signaling pathway: molecular and genetic analyses. Semin. Cell Biol., 5, 115-125.
10. Chambon,P. (1996) A decade of molecular biology of retinoic acid receptors. FASEB. J., 10, 940-954.
11. Chen,J-Y., Clifford,J., Zusi,C., Starrett,J., Tortolani,D., Ostrowski,J., Reczek,P., Chambon,P. and Gronemeyer,H. (1996) Two distinct actions of retinoid-receptor ligands. Nature, 382, 819-822.
12. Chiba,H., Clifford,J., Metzger,D. and Chambon,P. (1997) Distinct Retinoid X receptor-retinoic acid receptor heterodimers are differentially involved in the control of expression of retinoid target genes. Mol. Cell. Biol., 17, 3013-3020.
13. Clifford,J., Chiba,H., Sobieszczuk,D., Metzger,D. and Chambon,P. (1996) RXRα-null F9 embryonal carcinoma cells are resistant to the differentiation, anti-proliferative and apoptotic effects of retinoids. EMBO J., 15, 4142-4155.
14. Davis,R.J. (1994) MAPKs: new JNK expands the group. Trends Biochem. Sci., 19, 470-473.
15. 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 activating domain and influence of the nature of the response element on AF-2 activity. EMBO J., 13, 5370-5382.
16. Folkers,G.E., van der Leede,B.M. and van der Saag,P.T. (1993) The retinoic acid reccptor-β2 contains two separate cell-specific transactivation domains, at the N-terminus and in the ligand-binding domain. Mol. Endocrinol., 7, 616-627.
17. Gaub,M.P., Rochette-Egly,C., Lutz,Y., Ali,S., Matthes,H., Scheuer,I. and Chambon,P. (1992) Immunodetection of multiple species of retinoic acid receptor alpha: evidence for phosphorylation. Exp. Cell Res., 201, 335-346.
18. Ghyselinek,N.B., Dupé,V., Dierich,A., Messaddeq,N., Garnier,J-M., Rochette-Egly,C., Chambon,P. and Mark,M. (1997) Role of the retinoic acid receptor beta (RARβ) during mouse development. Int. J Dev. Biol., 41, 425-447.
19. Gronemeyer,H. and Laudet,V. (1995) Transcription factors 3: nuclear receptors. In Sheterline,P. (ed.). Protein Profile. Vol. 2. Academic Press, Liverpool, pp. 1173-1236.
20. Gudas,L.J., Sporn,MB and Roberts,A.B. (1994) Cellular biology and biochemistry of the retinoids. In Sporn,M.B., Roberts,A.B. and Goodman,D.S. (eds), The Retinoids, Biology, Chemistry and Medicine. Raven Press Ltd, New York, pp. 443-520.
21. Ho,S.N., Hunt,H.D., Horton,R.M., Pullen,J.K. and Pease,L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene, 77, 51-59.
22. 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.
23. Hunter,T. (1995) Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell, 80, 225-236.
24. 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.
25. Kastner,P., Mark,M., Ghyselinck,N., Krezel,W., Dupé,V., Grondona,J.M. and Chambon,P. (1997) Genetic evidence that the retinoid signal is transduced by heterodimeric RXR/RAR functional units during mouse development. Development, 124, 313-326.
26. Kato,S. et al. (1995) Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science, 270, 1491-1494.
27. 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.
28. Kruyt,F.A.H., 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.
29. Kuiper,G.O.J.M. and Brinkmann,A.O. (1994) Steroid hormone receptor phosphorylation: is there a physiological role? Mol. Cell. Endocrinol., 100, 103-107.
30. 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.
31. Leid,M., Kastner,P. and Chambon,P. (1992) Multiplicity generates diversity in the retinoic acid signalling pathways. Trends Biochem. Sei., 17, 427-433.
32. Mangelsdorf,D.J. and Evans,R.M. (1995) The RXR heterodimers and orphan receptors. Cell, 83, 841-850.
33. Marshall,C.J. (1995) Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell, 80, 179-185.
34. Morgan,D.O. (1995) Principles of CDK regulation. Nature, 374, 131-134
35. Nagpal,S., Saunders,M., Kastner,P., Durand,B., Nakshatri,H. and Chambon,P. (1992) Promoter context- and response element-dependent specificity of the transcriptional activation and modulating functions of retinoic acid receptors. Cell, 70, 1007-1019.
36. Nagpal,S., Friant,S., Nakshatri,H. and Chambon,P. (1993) RARs and RXRs: evidence for two autonomous transactivation functions (AF-1 and AF-2) and heterodimerization in vivo. EMBO J., 12, 2349-2360.
37. Pratt,M.A.C., Kralova,J. and McBurney,M.W. (1990) A dominant negative mutation of the alpha retinoic acid receptor gene in a retinoic acid-nonresponsive embryonal carcinoma cell. Mol. Cell. Biol., 10, 6445-6453.
38. Rocheue-Egly,C., Lutz,Y. Saunders,M., Scheuer,I., Gaub,M.P. and Chambon,P (1991) Retinoic acid receptor gamma: specific immunodetection and phosphorylation. J. Cell Biol., 115, 535-545.
39. Rochette-Egly,C., Oulad-Abdelghani,M., Staub,A., Pfister,V. Scheuer,I., Chambon,P. and Gaub,M.P. (1995) Phosphorylation of the retinoic acid receptor-alpha by protein kinase A. Mol. Endocrinol., 9, 860-871.
40. Rochette-Egly,C., Adam,S., Rossignol,M., Egly,J.M. and Chambon,P. (1997) Stimulation of RARα activation function AF-1 through binding to the general transcription factor TFIIH and phosphorylation by cdk7 Cell, 90, 97-107.
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 alpha (RAR alpha)-, RAR beta-, or RAR gamma-selective ligand in combination with a retinoid X receptor-specific ligand. Mol. Cell. Biol., 15, 6481-6487.
42. Sporn,M.B., Robens,A.B. and Goodman,D.S. (1994) The Retinoids. Biology, Chemistry, and Medicine, Raven Press, New York.
43. Strickland,S. and Mahdavi,V. (1978) The induction of differentiation in teratocarcinoma cells by retinoic acid. Cell, 15, 393-403.
44. Strickland,S., Smith,K.K. and Marotti,K.R. (1980) Hormonal induction of differentiation in teratocarcinoma cells: generation of parietal endoderm by retinoic acid and dibutyryl cAMP. Cell, 21, 347-355.
45. 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) 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, 7854-7858.
46. Taneja,R., Roy,B., Plassat,J-L., Zusi,C.F., Ostrowski,J., Reczek,P.R. and Chambon,P. (1996) Cell-type and promoter-context dependent retinoic acid receptor (RAR) redundancies for RAR beta 2 and Hoxa-1 activation in F9 and P19 cells can be artefactually generated by gene knockouts. Proc. Natl Acad. Sci. USA, 93, 6197-6202.
47. 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.
48. Weigel,N.L. (1996) Steroid hormone receptors and their regulation by phosphorylation. Biochem. J., 319, 657-667.
49. 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.