The DOI matches its Crossref record; 68 of the 68 references it cites were found in a registry or an index.
Dimerization with Retinoid X Receptors and Phosphorylation Modulate the Retinoic Acid-induced Degradation of Retinoic Acid Receptors α and γ through the Ubiquitin-Proteasome Pathway
Open accessAbstract
In eukaryotic cells, the ubiquitin-proteasome pathway is the major mechanism for targeted degradation of proteins. We show that, in F9 cells and in transfected COS-1 cells, the nuclear retinoid receptors, retinoic acid receptor gamma2 (RARgamma2), RARalpha1, and retinoid X receptor alpha1 (RXRalpha1) are degraded in a retinoic acid-dependent manner through the ubiquitin-proteasome pathway. The degradation of RARgamma2 is entirely dependent on its phosphorylation and on its heterodimerization with liganded RXRalpha1. In contrast, RARalpha1 degradation can occur in the absence of heterodimerization, whereas it is inhibited by phosphorylation, and heterodimerization reverses that inhibition. RXRalpha1 degradation is also modulated by heterodimerization. Thus, each partner of RARgamma/RXRalpha and RARalpha/RXRalpha heterodimers modulates the degradation of the other. We conclude that the ligand-dependent degradation of RARs and RXRs by the ubiquitin-proteasome pathway, which is regulated by heterodimerization and by phosphorylation, could be important for the regulation of the magnitude and duration of the effects of retinoid signals.
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“RARs are also degraded by the ubiquitin-proteasome system, through the recruitment of TRIP1/SUG-1, which is a subunit of the 19S regulatory subcomplex of the proteasome with an ATPase activity ( 110-112 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [110]
In the citing paper
“At the end of the RA signal, the proteasomal degradation of RAR ␥ has been shown to depend on the phosphorylation by p38MAPK of an additional serine residue located in the NTD ( 110, 111 ).”
From Vitamin A and retinoid signaling: genomic and nongenomic effects (2013) · cites this paper as [110]
Citations
Cites
Hershko, A., & Ciechanover, A. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.425 · Cited by 8,840
Site-directed mutagenesis by overlap extension using the polymerase chain reaction
Ho, S. N., Hunt, H. D., Horton, R. M., Pullen, J. K., & Pease, L. R. (1989) · Gene · doi:10.1016/0378-1119(89)90358-2 · Cited by 7,414
The nuclear receptor superfamily: the second decade
Mangelsdorf, D. J., Thummel, C., Beato, M., Herrlich, P., Schütz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., et al. (1995) · Cell · doi:10.1016/0092-8674(95)90199-x · Cited by 6,964
Self-citationA decade of molecular biology of retinoic acid receptors
Chambon, P. (1996) · The FASEB Journal · doi:10.1096/fasebj.10.9.8801176 · Cited by 2,889
Self-citationThe induction of differentiation in teratocarcinoma stem cells by retinoic acid
Strickland, S., & Mahdavi, V. (1978) · Cell · doi:10.1016/0092-8674(78)90008-9 · Cited by 1,420
Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-α
Bourguet, W., Ruff, M., Chambon, P., Gronemeyer, H., & Moras, D. (1995) · Nature · doi:10.1038/375377a0 · Cited by 1,192
Self-citationNonsteroid nuclear receptors: What Are genetic studies telling us about their role in real life?
Kastner, P., Mark, M. P., & Chambon, P. (1995) · Cell · doi:10.1016/0092-8674(95)90202-3 · Cited by 989
Self-citationA canonical structure for the ligand-binding domain of nuclear receptors
Wurtz, J., Bourguet, W., Renaud, J., Vivat, V., Chambon, P., Moras, D., & Gronemeyer, H. (1996) · Nature Structural Biology · doi:10.1038/nsb0196-87 · Cited by 986
Self-citationThe nuclear receptor ligand-binding domain: structure and function
Moras, D., & Gronemeyer, H. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80015-x · Cited by 838
Multiplicity generates diversity in the retinoic acid signalling pathways
Leid, M., Kastner, P., & Chambon, P. (1992) · Trends in Biochemical Sciences · doi:10.1016/0968-0004(92)90014-z · Cited by 821
Self-citationStrickland, S., Smith, K. K., & Marotti, K. R. (1980) · Cell · doi:10.1016/0092-8674(80)90471-7 · Cited by 801
Zelent, A., Krust, A., Petkovich, M. P., Kastner, P., & Chambon, P. (1989) · Nature · doi:10.1038/339714a0 · Cited by 792
Self-citationSerine Phosphorylation-regulated Ubiquitination and Degradation of β-Catenin
Orford, K. W., Crockett, C., Jensen, J. P., Weissman, A. M., & Byers, S. W. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.40.24735 · Cited by 715
Proteasome-dependent degradation of the human estrogen receptor
Nawaz, Z., Lonard, D. M., Dennis, A. P., Smith, C. L., & O’Malley, B. W. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.5.1858 · Cited by 589
Douarin, B. L., Nielsen, A. L., Garnier, J., Ichinose, H., Jeanmougin, F., Losson, R., & Chambon, P. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb01060.x · Cited by 544
Self-citationTremblay, A., Tremblay, G. B., Labrie, F., & Giguère, V. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80479-7 · Cited by 469
Reduced Ubiquitin-Dependent Degradation of c-Jun After Phosphorylation by MAP Kinases
Musti, A. M., Treier, M., & Bohmann, D. (1997) · Science · doi:10.1126/science.275.5298.400 · Cited by 463
Lange, C. A., Shen, T., & Horwitz, K. B. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.3.1032 · Cited by 451
Substrate Targeting in the Ubiquitin System
Laney, J. D., & Hochstrasser, M. (1999) · Cell · doi:10.1016/s0092-8674(00)80752-7 · Cited by 442
Increasing the Complexity of Coactivation in Nuclear Receptor Signaling
Freedman, L. P. (1999) · Cell · doi:10.1016/s0092-8674(00)80708-4 · Cited by 437
Kastner, P., Mark, M. P., Ghyselinck, N. B., Krężel, W., Dupé, V., Grondona, J. M., & Chambon, P. (1997) · Development · doi:10.1242/dev.124.2.313 · Cited by 429
Self-citationCrystal Structure of a Heterodimeric Complex of RAR and RXR Ligand-Binding Domains
Bourguet, W., Vivat, V., Wurtz, J., Chambon, P., Gronemeyer, H., & Moras, D. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)80424-4 · Cited by 417
Self-citationBaur, E. V., Zechel, C., Heery, D. M., Heine, M. J., Garnier, J., Vivat, V., Douarin, B. L., Gronemeyer, H., Chambon, P., & Losson, R. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00339.x · Cited by 403
Self-citationPhosphorylation of the Nuclear Receptor SF-1 Modulates Cofactor Recruitment
Hammer, G. D., Krylova, I., Zhang, Y., Darimont, B. D., Simpson, K., Weigel, N. L., & Ingraham, H. A. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80480-3 · Cited by 375
Zhu, J., Gianni’, M., Kopf, E., Honoré, N., Chelbi‐Alix, M. K., Koken, M. H. M., Quignon, F., Rochette‐Egly, C., & de Thé, H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.14807 · Cited by 371
Self-citationHauser, S., Adelmant, G., Sarraf, P., Wright, H. M., Mueller, E., & Spiegelman, B. M. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001297200 · Cited by 367
Targeting of substrates to the 26S proteasome
Pickart, C. M. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.13.9367341 · Cited by 365
Durand, B., Saunders, M., Gaudon, C., Roy, B., Losson, R., & Chambon, P. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06872.x · Cited by 354
Self-citationNagpal, S., Saunders, M., Kastner, P., Durand, B., Nakshatri, H., & Chambon, P. (1992) · Cell · doi:10.1016/0092-8674(92)90250-g · Cited by 332
Self-citationMarti, A., Wirbelauer, C., Scheffner, M., & Krek, W. (1999) · Nature Cell Biology · doi:10.1038/8984 · Cited by 318
Pathways of ubiquitin conjugation
Haas, A. L., & Siepmann, T. J. (1997) · The FASEB Journal · doi:10.1096/fasebj.11.14.9409544 · Cited by 311
Rochette-Egly, C., Adam, S., Rossignol, M., Egly, J.-M., & Chambon, P. (1997) · Cell · doi:10.1016/s0092-8674(00)80317-7 · Cited by 308
Self-citationZechel, C., Shen, X.-Q., Chen, J. Y., Zp, C., Chambon, P., & Gronemeyer, H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06396.x · Cited by 254
Self-citationRole of the retinoic acid receptor beta (RARbeta) during mouse development.
Ghyselinck, N., Dupé, V., Dierich, A., Messaddeq, N., Garnier, J.-M., Rochette-Egly, C., Chambon, P., & Mark, M. (1997) · International Journal of Developmental Biology · doi:10.1387/ijdb.9240560 · Cited by 240
Self-citationZechel, C., Shen, X.-Q., Chambon, P., & Gronemeyer, H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06395.x · Cited by 209
Self-citationMolinari, E., Gilman, M. Z., & Natesan, S. (1999) · The EMBO Journal · doi:10.1093/emboj/18.22.6439 · Cited by 185
Roy, B., Taneja, R., & Chambon, P. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.12.6481 · Cited by 180
Self-citationMinucci, S., Leid, M. E., Toyama, R., Saint‐Jeannet, J., Peterson, V. J., Horn, V. J., Ishmael, J. E., Bhattacharyya, N., Dey, A., Dawid, I. B., et al. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.2.644 · Cited by 172
Bouillet, P., Oulad‐Abdelghani, M., Vicaire, S., Garnier, J., Schuhbaur, B., Dollé, P., & Chambon, P. (1995) · Developmental Biology · doi:10.1006/dbio.1995.1226 · Cited by 172
Self-citationDistinct steady–state nuclear receptor coregulator complexes exist in vivo
McKenna, N. J., Nawaz, Z., Tsai, S. Y., Tsai, M., & O’Malley, B. W. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.20.11697 · Cited by 168
Imhof, M. O., & McDonnell, D. P. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.6.2594 · Cited by 159
Boylan, J. F., Lufkin, T., Achkar, C., Taneja, R., Chambon, P., & Gudas, L. J. (1995) · Molecular and Cellular Biology · doi:10.1128/mcb.15.2.843 · Cited by 145
Self-citationBoylan, J. F., Lohnes, D., Taneja, R., Chambon, P., & Gudas, L. J. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.20.9601 · Cited by 144
Self-citationVivat, V., Zechel, C., Wurtz, J., Bourguet, W., Kagechika, H., Umemiya, H., Shudo, K., Moras, D., Gronemeyer, H., & Chambon, P. (1997) · The EMBO Journal · doi:10.1093/emboj/16.18.5697 · Cited by 141
Self-citationClifford, J. L., Chiba, H., Sobieszczuk, D., METZGER, D., & Chambon, P. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00789.x · Cited by 132
Self-citationSchulman, I. G., Juguilon, H., & Evans, R. M. (1996) · Molecular and Cellular Biology · doi:10.1128/mcb.16.7.3807 · Cited by 131
The phantom ligand effect: allosteric control of transcription by the retinoid X receptor.Preprint
Schulman, I. G., Li, C., Schwabe, J. W. R., & Evans, R. M. (1997) · Genes & Development · doi:10.1101/gad.11.3.299 · Cited by 127
Phosphorylation of the retinoic acid receptor-alpha by protein kinase A
Rochette-Egly, C. (1995) · Molecular Endocrinology · doi:10.1210/me.9.7.860 · Cited by 124
Self-citationImmunodetection of multiple species of retinoic acid receptor α: Evidence for phosphorylation
Gaub, M. P., Rochette‐Egly, C., Lutz, Y., Ali, S., Matthes, H. W. D., Scheuer, I., & Chambon, P. (1992) · Experimental Cell Research · doi:10.1016/0014-4827(92)90282-d · Cited by 124
Self-citationA PEST-Like Sequence Mediates Phosphorylation and Efficient Ubiquitination of Yeast Uracil Permease
Marchal, C., Haguenauer‐Tsapis, R., & Urban‐Grimal, D. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.1.314 · Cited by 124
Masuyama, H., & MacDonald, P. N. (1998) · Journal of Cellular Biochemistry · doi:10.1002/(sici)1097-4644(19981201)71:3 · Cited by 120
Retinoic acid receptor gamma: specific immunodetection and phosphorylation.
Rochette‐Egly, C., Lutz, Y., Saunders, M., Scheuer, I., Gaub, M. P., & Chambon, P. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.115.2.535 · Cited by 116
Self-citationChiba, H., Clifford, J. L., METZGER, D., & Chambon, P. (1997) · Molecular and Cellular Biology · doi:10.1128/mcb.17.6.3013 · Cited by 116
Self-citationTaneja, R., Rochette‐Egly, C., Plassat, J., Penna, L., Gaub, M., & Chambon, P. (1997) · The EMBO Journal · doi:10.1093/emboj/16.21.6452 · Cited by 113
Self-citationRAR‐independent RXR signaling induces t(15;17) leukemia cell maturation
Benoit, G., Altucci, L., Flexor, M., Ruchaud, S., Lillehaug, J., Raffelsberger, W., Gronemeyer, H., & Lanotte, M. (1999) · The EMBO Journal · doi:10.1093/emboj/18.24.7011 · Cited by 111
Bastien, J., Adam-Stitah, S., Riedl, T., Egly, J.-M., Chambon, P., & Rochette-Egly, C. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m001985200 · Cited by 107
Self-citationTaneja, R., Bouillet, P., Boylan, J. F., Gaub, M. P., Roy, B., Gudas, L. J., & Chambon, P. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.17.7854 · Cited by 103
Self-citationMitsui, A., & Sharp, P. A. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6054 · Cited by 101
Krówczyńska, A., Coutts, M., Makrides, S. C., & Brawerman, G. (1989) · Nucleic Acids Research · doi:10.1093/nar/17.15.6408 · Cited by 90
Chiba, H., Clifford, J. L., METZGER, D., & Chambon, P. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.3.735 · Cited by 87
Self-citationWeeda, G., Rossignol, M., Fraser, R. A., Winkler, G. S., Vermeulen, W., Veer, L. J. V., Ma, L., Hoeijmakers, J. H. J., & Egly, J. (1997) · Nucleic Acids Research · doi:10.1093/nar/25.12.2274 · Cited by 81
Fraser, R., Rossignol, M., Heard, D. J., Egly, J., & Chambon, P. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.11.7122 · Cited by 77
Self-citationDetection of Retinoid X Receptors Using Specific Monoclonal and Polyclonal Antibodies
Rochette‐Egly, C., Lutz, Y., Pfister, V., Heyberger, S., Scheuer, I., Chambon, P., & Gaub, M. P. (1994) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.1994.2491 · Cited by 75
Self-citationUbiquitination and Degradation of ATF2 Are Dimerization Dependent
Fuchs, S. Y., & Ronai, Z. A. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.5.3289 · Cited by 60
Thrombomodulin gene regulation by cAMP and retinoic acid in F9 embryonal carcinoma cells.
Weiler-Guettler, H., Yu, K., Soff, G. A., Gudas, L. J., & ROSENBERG, R. D. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.6.2155 · Cited by 52
Wan, Y. Y., Wang, L., & Wu, T.-C. J. (1994) · Experimental Cell Research · doi:10.1006/excr.1994.1009 · Cited by 42
Retinoic Acid Down-regulation of Fibronectin and Retinoic Acid Receptor α Proteins in NIH-3T3 Cells
Scita, G., Darwiche, N., Greenwald, E., Rosenberg, M. I., Politi, K. A., & Luca, L. M. D. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.11.6502 · Cited by 35
ATPase and ubiquitin-binding proteins of the yeast proteasome
Rubin, D. M., van Nocker, S., Glickman, M. H., Coux, O., Wefes, I., Sadis, S., Fu, H., Goldberg, A. L., Vierstra, R. D., & Finley, D. J. (1997) · Molecular Biology Reports · doi:10.1023/a:1006844305067 · Cited by 27
Flagged first, then by citations
Research works printed but not linked: 2
- Rochette-Egly, 1995, Mol. Endocrinol., 9, 860
- Ghyselinck, 1997, Int. J. Dev. Biol., 41, 425
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Nuclear retinoid receptors and the transcription of retinoid-target genes
Bastien, J., & Rochette-Egly, C. (2004) · Gene · doi:10.1016/j.gene.2003.12.005 · Cited by 773
Self-citationControlling nuclear receptors: the circular logic of cofactor cycles
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Vitamin A and retinoid signaling: genomic and nongenomic effects
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Metadata
- Authors
- Kopf, E., Plassat, J.-L., Vivat, V., de Thé, H., Chambon, P., & Rochette-Egly, C.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Venue
- Journal of Biological Chemistry
- Publisher
- Elsevier BV
- Published
- 2000-10
- Volume
- 275
- Issue
- 43
- Pages
- 33280-33288
- ISSN
- 0021-9258 (ISSN-L)
- OpenAlex
- W2154503677
- Cited by
- 155
- References
- 68
- Citations by year
- 2026: 5 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 4 · 2020: 2 · 2019: 1 · 2018: 4 · 2017: 4 · 2016: 1 · 2015: 2 · 2014: 6 · 2013: 4 · 2012: 3
- FWCI
- 4.71
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Biological Chemistry (publishedVersion, cc-by)
- PubMed (publishedVersion)
- HAL (submittedVersion, other-oa)
- Funders
- Bristol-Myers Squibb
- Association pour la Recherche sur le Cancer
- Institut National de la Santé et de la Recherche Médicale
- Centre National de la Recherche Scientifique
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Retinoids in leukemia and cellular processes
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ubiquitin and proteasome pathways
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
- Keywords
- retinoic acid receptor alpha, retinoic acid receptor gamma, retinoid X receptor alpha, protein degradation, ubiquitin-proteasome system, receptor phosphorylation, heterodimerization, retinoic acid signaling, nuclear receptors
- MeSH terms
- Retinoic Acid Receptor alpha, Retinoic Acid Receptor gamma, Amino Acid Sequence, Animals, Cysteine Endopeptidases, Molecular Sequence Data, Multienzyme Complexes, Phosphorylation, Transcription Factors, Transfection, Tretinoin, Ubiquitins, Receptors, Retinoic Acid, Dimerization, COS Cells, Proteasome Endopeptidase Complex, Retinoid X Receptors
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