Nuclear and extra-nuclear effects of retinoid acid receptors: How they are interconnected

Sub-Cellular Biochemistry

Volumn 70, Issue , 2014, Pages 103-127

  Piskunov, Aleksandr ^a   Tanoury, Ziad Al ^a   Rochette Egly, Cécile ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ISOPROTEIN; LIGAND; MITOGEN ACTIVATED PROTEIN KINASE; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR;

CHEMICAL STRUCTURE; CHEMISTRY; DNA RESPONSIVE ELEMENT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN MULTIMERIZATION; REVIEW; SIGNAL TRANSDUCTION;

GENE EXPRESSION REGULATION; HUMANS; LIGANDS; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, MOLECULAR; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN MULTIMERIZATION; RECEPTORS, RETINOIC ACID; RESPONSE ELEMENTS; RETINOID X RECEPTORS; SIGNAL TRANSDUCTION; TRETINOIN;

EID: 84910107395     PISSN: 03060225     EISSN: None     Source Type: Journal    
DOI: 10.1007/978-94-017-9050-5_6     Document Type: Article

References (140)

1. Adam-Stitah S, Penna L, Chambon P, Rochette-Egly C (1999) Hyperphosphorylation of the retinoid X receptor alpha (RXRa) by activated c-Jun N-terminal Kinases (JNKs). J Biol Chem 274:18932–18941
2. Al Tanoury Z, Gaouar S, Piskunov A, Ye T, Urban S, Jost B, Keime C, Davidson I, Dierich A, Rochette-Egly C (2014) Phosphorylation of the retinoic acid receptor RARγ2 is crucial for the neuronal differentiation of mouse embryonic stem cells. J Cell Sci 127:2095–2105
3. Al Tanoury Z, Piskunov A, Andriamoratsiresy D, Gaouar S, Lutzing R, Ye T, Jost B, Keime C, Rochette-Egly C (2013a) Genes involved in cell adhesion and signaling: a new repertoire of retinoic acid receptors target genes in mouse embryonic fbroblasts. J Cell Sci 127:521–533
4. Al Tanoury Z, Piskunov A, Rochette-Egly C (2013b) Vitamin A and retinoid signaling: genomic and nongenomic effects: thematic review series: fat-soluble vitamins: vitamin A. J Lipid Res 54:1761–1775
5. Alsayed Y, Uddin S, Mahmud N, Lekmine F, Kalvakolanu DV, Minucci S, Bokoch G, Platanias LC (2001) Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to all-trans-retinoic acid. J Biol Chem 276:4012–4019
6. Aoto J, Nam CI, Poon MM, Ting P, Chen L (2008) Synaptic signaling by all-trans retinoic acid in homeostatic synaptic plasticity. Neuron 60:308–320
7. Ball LJ, Kuhne R, Schneider-Mergener J, Oschkinat H (2005) Recognition of proline-rich motifs by protein-protein-interaction domains. Angew Chem Int Ed Engl 44:2852–2869
8. Balmer JE, Blomhoff R (2005) A robust characterization of retinoic acid response elements based on a comparison of sites in three species. J Steroid Biochem Mol Biol 96:347–354
9. Bastien J, Adam-Stitah S, Riedl T, Egly JM, Chambon P, Rochette-Egly C (2000) TFIIH interacts with the retinoic acid receptor gamma and phosphorylates its AF-1-activating domain through cdk7. J Biol Chem 275:21896–21904
10. Bastien J, Rochette-Egly C (2004) Nuclear retinoid receptors and the transcription of reti-noid-target genes. Gene 328:1–16
11. Berry DC, Noy N (2007) Is PPARbeta/delta a retinoid receptor? PPAR Res 2007:73256
12. Berry DC, Noy N (2009) All-trans-retinoic acid represses obesity and insulin resistance by activating both peroxisome proliferation-activated receptor beta/delta and retinoic acid receptor. Mol Cell Biol 29:3286–3296
13. Bibel M, Richter J, Lacroix E, Barde YA (2007) Generation of a defned and uniform population of CNS progenitors and neurons from mouse embryonic stem cells. Nat Protoc 2:1034–1043
14. Blume-Jensen P, Hunter T (2001) Oncogenic kinase signalling. Nature 411:355–365
15. Bour G, Gaillard E, Bruck N, Lalevee S, Plassat JL, Busso D, Samama JP, Rochette-Egly C (2005) Cyclin H binding to the RARalpha activation function (AF)-2 domain directs phos-phorylation of the AF-1 domain by cyclin-dependent kinase 7. Proc Natl Acad Sci USA 102:16608–16613
16. Bour G, Lalevee S, Rochette-Egly C (2007) Protein kinases and the proteasome join in the combinatorial control of transcription by nuclear retinoic acid receptors. Trends Cell Biol 17:302–309
17. Bour G, Plassat JL, Bauer A, Lalevee S, Rochette-Egly C (2005) Vinexin beta Interacts with the non-phosphorylated AF-1 Domain of retinoid receptor gamma (RARg) and represses RARg-mediated transcription. J Biol Chem 280:17027–17037
18. Bour G, Taneja R, Rochette-Egly C (2006) Mouse embryocarcinoma F9 cells and reti-noic acid. A model to study the molecular mechanisms of endodermal differentiation. In: Taneja R (ed) Nuclear Receptors in development, vol 16. Elsevier Press Inc, Netherlands, pp 211–253
19. Bourguet W, Germain P, Gronemeyer H (2000) Nuclear receptor ligand-binding domains: three-dimensional structures, molecular interactions and pharmacological implications. Trends Pharmacol Sci 21:381–388
20. Bourguet W, Ruff M, Chambon P, Gronemeyer H, Moras D (1995) Crystal structure of the ligand-binding domain of the human nuclear receptor RXR-alpha. Nature 375:377–382
21. Bourguet W, Vivat V, Wurtz JM, Chambon P, Gronemeyer H, Moras D (2000) Crystal structure of a heterodimeric complex of RAR and RXR ligand-binding domains. Mol Cell 5:289–298
22. Brelivet Y, Rochel N, Moras D (2012) Structural analysis of nuclear receptors: from isolated domains to integral proteins. Mol Cell Endocrinol 348:466–473
23. Brondani V, Schefer Q, Hamy F, Klimkait T (2005) The peptidyl-prolyl isomerase Pin1 regulates phospho-Ser77 retinoic acid receptor alpha stability. Biochem Biophys Res Commun 328:6–13
24. Bruck N, Bastien J, Bour G, Tarrade A, Plassat JL, Bauer A, Adam-Stitah S, Rochette-Egly C (2005) Phosphorylation of the retinoid x receptor at the omega loop, modulates the expression of retinoic-acid-target genes with a promoter context specifcity. Cell Signal 17:1229–1239
25. Bruck N, Vitoux D, Ferry C, Duong V, Bauer A, dethe H, Rochette-Egly C (2009) A coordinated phosphorylation cascade initiated by p38MAPK/MSK1 directs RARalpha to target promoters. EMBO J 28:34–47
26. Budhu AS, Noy N (2002) Direct channeling of retinoic acid between cellular retinoic acid-binding protein II and retinoic acid receptor sensitizes mammary carcinoma cells to retinoic acid-induced growth arrest. Mol Cell Biol 22:2632–2641
27. Burns KA, Vanden Heuvel JP (2007) Modulation of PPAR activity via phosphorylation. Biochim Biophys Acta 1771:952–960
28. Chambon P (1996) A decade of molecular biology of retinoic acid receptors. FASEB J 10:940–954
29. Chebaro Y, Amal I, Rochel N, Rochette-Egly C, Stote R, Dejaegere A (2013) Phosphorylation of the retinoic acid receptor alpha induces a mechanical allosteric regulation and changes in internal dynamics. Plos Comp Biol 9:e1003012
30. Chen N, Napoli JL (2008) All-trans-retinoic acid stimulates translation and induces spine formation in hippocampal neurons through a membrane-associated RARalpha. FASEB J 22:236–245
31. Cheung YT, Lau WK, Yu MS, Lai CS, Yeung SC, So KF, Chang RC (2009) Effects of all-trans-retinoic acid on human SH-SY5Y neuroblastoma as in vitro model in neurotoxicity research. Neurotoxicology 30:127–135
32. Delva L, Bastie JN, Rochette-Egly C, Kraiba R, Balitrand N, Despouy G, Chambon P, Chomienne C (1999) Physical and functional interactions between cellular retinoic acid binding protein II and the retinoic acid-dependent nuclear complex. Mol Cell Biol 19:7158–7167
33. Dey N, De PK, Wang M, Zhang H, Dobrota EA, Robertson KA, Durden DL (2007) CSK controls retinoic acid receptor (RAR) signaling: a RAR-c-SRC signaling axis is required for neuritogenic differentiation. Mol Cell Biol 27:4179–4197
34. Dilworth FJ, Chambon P (2001) Nuclear receptors coordinate the activities of chromatin remodeling complexes and coactivators to facilitate initiation of transcription. Oncogene 20:3047–3054
35. Ding Y, Qiao A, Wang Z, Goodwin JS, Lee ES, Block ML, Allsbrook M, McDonald MP, Fan GH (2008) Retinoic acid attenuates beta-amyloid deposition and rescues memory def-cits in an Alzheimer’s disease transgenic mouse model. J Neurosci 28:11622–11634
36. Dong D, Ruuska SE, Levinthal DJ, Noy N (1999) Distinct roles for cellular retinoic acid-binding proteins I and II in regulating signaling by retinoic acid. J Biol Chem 274:23695–23698
37. Duong V, Rochette-Egly C (2011) The molecular physiology of nuclear retinoic acid receptors. From health to disease. Biochim Biophys Acta 1812:1023–1031
38. Epping MT, Wang L, Edel MJ, Carlee L, Hernandez M, Bernards R (2005) The human tumor antigen PRAME is a dominant repressor of retinoic acid receptor signaling. Cell 122:835–847
39. Farboud B, Hauksdottir H, Wu Y, Privalsky ML (2003) Isotype-restricted corepressor recruitment: a constitutively closed helix 12 conformation in retinoic acid receptors beta and gamma interferes with corepressor recruitment and prevents transcriptional repression. Mol Cell Biol 23:2844–2858
40. Ferry C, Gaouar S, Fischer B, Boeglin M, Paul N, Samarut E, Piskunov A, Pankotai-Bodo G, Brino L, Rochette-Egly C (2011) Cullin 3 mediates SRC-3 ubiquitination and degradation to control the retinoic acid response. Proc Natl Acad Sci USA 108:20603–20608
41. Ferry C, Gianni M, Lalevee S, Bruck N, Plassat JL, Raska I Jr, Garattini E, Rochette-Egly C (2009) SUG-1 plays proteolytic and non-proteolytic roles in the control of retinoic acid target genes via its interaction with SRC-3. J Biol Chem 284:8127–8135
42. Fujiki R, Chikanishi T, Hashiba W, Ito H, Takada I, Roeder RG, Kitagawa H, Kato S (2009) GlcNAcylation of a histone methyltransferase in retinoic-acid-induced granulopoiesis. Nature 459:455–459
43. Gaillard E, Bruck N, Brelivet Y, Bour G, Lalevee S, Bauer A, Poch O, Moras D, Rochette-Egly C (2006) Phosphorylation by PKA potentiates retinoic acid receptor alpha activity by means of increasing interaction with and phosphorylation by cyclin H/cdk7. Proc Natl Acad Sci USA 103:9548–9553
44. Gaj T, Gersbach CA, Barbas CF 3rd (2013) ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 31:397–405
45. Gaub MP, Rochette-Egly C, Lutz Y, Ali S, Matthes H, Scheuer I, Chambon P (1992) Immunodetection of multiple species of retinoic acid receptor alpha: evidence for phospho-rylation. Exp Cell Res 201:335–346
46. Gay F, Barath P, Desbois-Le Peron C, Metivier R, Le Guevel R, Birse D, Salbert G (2002) Multiple phosphorylation events control chicken ovalbumin upstream promoter transcription factor I orphan nuclear receptor activity. Mol Endocrinol 16:1332–1351
47. Gehani SS, Agrawal-Singh S, Dietrich N, Christophersen NS, Helin K, Hansen K (2010) Polycomb group protein displacement and gene activation through MSK-dependent H3K27me3S28 phosphorylation. Mol Cell 39:886–900
48. Germain P, Altucci L, Bourguet W, Rochette-Egly C, Gronemeyer H (2003) Nuclear receptor superfamily: principles of signaling. Pure Appl Chem IUPAC 75:1619–1664
49. Germain P, Chambon P, Eichele G, Evans RM, Lazar MA, Leid M, De Lera AR, Lotan R, Mangelsdorf DJ, Gronemeyer H (2006a) International union of pharmacology. LX. Retinoic acid receptors. Pharmacol Rev 58:712–725
50. Germain P, Chambon P, Eichele G, Evans RM, Lazar MA, Leid M, De Lera AR, Lotan R, Mangelsdorf DJ, Gronemeyer H (2006b) International union of pharmacology. LXIII. Retinoid X receptors. Pharmacol Rev 58:760–772
51. Germain P, Staels B, Dacquet C, Spedding M, Laudet V (2006) Overview of nomenclature of nuclear receptors. Pharmacol Rev 58:685–704
52. Gianni M, Bauer A, Garattini E, Chambon P, Rochette-Egly C (2002) Phosphorylation by p38MAPK and recruitment of SUG-1 are required for RA-induced RARγ degradation and transactivation. EMBO J 21:3760–3769
53. Gianni M, Boldetti A, Guarnaccia V, Rambaldi A, Parrella E, Raska I Jr, Rochette-Egly C, Del Sal G, Rustighi A, Terao M, Garattini E (2009) Inhibition of the peptidyl-prolyl-isomer-ase Pin1 enhances the responses of acute myeloid leukemia cells to retinoic acid via stabilization of RARalpha and PML-RARalpha. Cancer Res 69:1016–1026
54. Gianni M, Parrella E, Raska I, Gaillard E, Nigro EA, Gaudon C, Garattini E, Rochette-Egly C (2006) P38MAPK-dependent phosphorylation and degradation of SRC-3/AIB1 and RARalpha-mediated transcription. EMBO J 25:739–751
55. Gillespie RF, Gudas LJ (2007) Retinoic acid receptor isotype specifcity in F9 teratocarci-noma stem cells results from the differential recruitment of coregulators to retinoic response elements. J Biol Chem 282:33421–33434
56. Gillespie RF, Gudas LJ (2007) Retinoid regulated association of transcriptional co-regulators and the polycomb group protein SUZ12 with the retinoic acid response elements of Hoxa1, RARbeta(2), and Cyp26A1 in F9 embryonal carcinoma cells. J Mol Biol 372:298–316
57. Glass CK, Rosenfeld MG (2000) The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev 14:121–141
58. Gudas LJ, Wagner JA (2011) Retinoids regulate stem cell differentiation. J Cell Physiol 226:322–330
59. Gupta P, Ho PC, Huq MM, Ha SG, Park SW, Khan AA, Tsai NP, Wei LN (2008) Retinoic acid-stimulated sequential phosphorylation, PML recruitment, and SUMOylation of nuclear receptor TR2 to suppress Oct4 expression. Proc Natl Acad Sci USA 105:11424–11429
60. Hauksdottir H, Farboud B, Privalsky ML (2003) Retinoic acid receptors beta and gamma do not repress, but instead activate target gene transcription in both the absence and presence of hormone ligand. Mol Endocrinol 17:373–385
61. Hilgeroth A, Tell V, Kramer S, Totzke F, Schachtele C (2013) Approaches to a multitarget-ing drug development: frst profled 3-Ethoxycarbonyl-1-aza-9-oxafuorenes representing a perspective compound class targeting alzheimer disease relevant kinases CDK1, CDK5 and GSK-3beta. Med Chem
62. Hu X, Chen Y, Farooqui M, Thomas MC, Chiang CM, Wei LN (2004) Suppressive effect of receptor-interacting protein 140 on coregulator binding to retinoic acid receptor complexes, histone-modifying enzyme activity, and gene activation. J Biol Chem 279:319–325
63. Jetten AM, Kurebayashi S, Ueda E (2001) The ROR nuclear orphan receptor subfamily: critical regulators of multiple biological processes. Prog Nucleic Acid Res Mol Biol 69:205–247
64. Jonas BA, Varlakhanova N, Hayakawa F, Goodson M, Privalsky ML (2007) Response of SMRT (silencing mediator of retinoic acid and thyroid hormone receptor) and N-CoR (nuclear receptor corepressor) corepressors to mitogen-activated protein kinase kinase kinase cascades is determined by alternative mRNA splicing. Mol Endocrinol 21:1924–1939
65. Kay BK, Williamson MP, Sudol M (2000) The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains. FASEB J 14:231–241
66. Keriel A, Stary A, Sarasin A, Rochette-Egly C, Egly JM (2002) XPD mutations prevent TFIIH-dependent transactivation by nuclear receptors and phosphorylation of RARalpha. Cell 109:125–135
67. Khetchoumian K, Teletin M, Tisserand J, Mark M, Herquel B, Ignat M, Zucman-Rossi J, Cammas F, Lerouge T, Thibault C, Metzger D, Chambon P, Losson R (2007) Loss of Trim24 (Tif1alpha) gene function confers oncogenic activity to retinoic acid receptor alpha. Nat Genet 39:1500–1506
68. Kopf E, Plassat JL, Vivat V, deThe H, Chambon P, Rochette-Egly C (2000) Dimerization with retinoid X receptors and phosphorylation modulate the retinoic acid-induced degradation of retinoic acid receptors alpha and gamma through the ubiquitin-proteasome pathway. J Biol Chem 275:33280–33288
69. Kruse SW, Suino-Powell K, Zhou XE, Kretschman JE, Reynolds R, Vonrhein C, Xu Y, Wang L, Tsai SY, Tsai MJ, Xu HE (2008) Identifcation of COUP-TFII orphan nuclear receptor as a retinoic acid-activated receptor. PLoS Biol 6:e227
70. Lalevee S, Bour G, Quinternet M, Samarut E, Kessler P, Vitorino M, Bruck N, Delsuc MA, Vonesch JL, Kieffer B, Rochette-Egly C (2010) Vinexinss, an atypical “sensor” of retinoic acid receptor gamma signaling: union and sequestration, separation, and phosphorylation. FASEB J 24:4523–4534
71. Lalevee S, Ferry C, Rochette-Egly C (2010) Phosphorylation control of nuclear receptors. Methods Mol Biol 647:251–266
72. Lane MA, Bailey SJ (2005) Role of retinoid signalling in the adult brain. Prog Neurobiol 75:275–293
73. Laudet V, Gronemeyer H (2001) Nuclear receptor factsbook. Academic Press, London
74. Lavery DN, McEwan IJ (2005) Structure and function of steroid receptor AF1 transactiva-tion domains: induction of active conformations. Biochem J 391:449–464
75. Le Douarin B, Zechel C, Garnier JM, Lutz Y, Tora L, Pierrat P, Heery D, Gronemeyer H, Chambon P, Losson R (1995) The N-terminal part of TIF1, a putative mediator of the ligand-dependent activation function (AF-2) of nuclear receptors, is fused to B-raf in the oncogenic protein T18. EMBO J 14:2020–2033
76. le Maire A, Teyssier C, Erb C, Grimaldi M, Alvarez S, de Lera AR, Balaguer P, Gronemeyer H, Royer CA, Germain P, Bourguet W (2010) A unique secondary-structure switch controls constitutive gene repression by retinoic acid receptor. Nat Struct Mol Biol 17:801–807
77. Le May N, Mota-Fernandes D, Velez-Cruz R, Iltis I, Biard D, Egly JM (2010) NER factors are recruited to active promoters and facilitate chromatin modifcation for transcription in the absence of exogenous genotoxic attack. Mol Cell 38:54–66
78. Le May N, Iltis I, Amé J, Zhovner A, Biard D, Egly JM, Schreiber V, Coin F (2012) Poly (ADP-ribose) glycohydrolase regulates retinoic acid receptor-mediated gene expression. Mol Cell 48:785–798
79. Lee HY, Suh YA, Robinson MJ, Clifford JL, Hong WK, Woodgett JR, Cobb MH, Mangelsdorf DJ, Kurie JM (2000) Stress pathway activation induces phosphorylation of retinoid X receptor. J Biol Chem 275:32193–32199
80. Lee MG, Villa R, Trojer P, Norman J, Yan KP, Reinberg D, Di Croce L, Shiekhattar R (2007) Demethylation of H3K27 regulates polycomb recruitment and H2A ubiquitination. Science 318:447–450
81. Lefebvre P, Martin PJ, Flajollet S, Dedieu S, Billaut X, Lefebvre B (2005) Transcriptional activities of retinoic acid receptors. Vitam Horm 70:199–264
82. Losel R, Wehling M (2003) Nongenomic actions of steroid hormones. Nat Rev Mol Cell Biol 4:46–56
83. Luconi M, Cantini G, Serio M (2010) Peroxisome proliferator-activated receptor gamma (PPARgamma): is the genomic activity the only answer? Steroids 75:585–594
84. Macias MJ, Wiesner S, Sudol M (2002) WW and SH3 domains, two different scaffolds to recognize proline-rich ligands. FEBS Lett 513:30–37
85. Mahony S, Mazzoni EO, McCuine S, Young RA, Wichterle H, Gifford DK (2011) Ligand-dependent dynamics of retinoic acid receptor binding during early neurogenesis. Genome Biol 12:R2
86. Mark M, Ghyselinck NB, Chambon P (2009) Function of retinoic acid receptors during embryonic development. Nucl Recept Signal 7:e002
87. Masia S, Alvarez S, de Lera AR, Barettino D (2007) Rapid, nongenomic actions of reti-noic acid on phosphatidylinositol-3-kinase signaling pathway mediated by the retinoic acid receptor. Mol Endocrinol 21:2391–2402
88. Matsushima-Nishiwaki R, Okuno M, Adachi S, Sano T, Akita K, Moriwaki H, Friedman SL, Kojima S (2001) Phosphorylation of retinoid X receptor alpha at serine 260 impairs its metabolism and function in human hepatocellular carcinoma. Cancer Res 61:7675–7682
89. Mendoza-Parra MA, Walia M, Sankar M, Gronemeyer H (2011) Dissecting the retinoid-induced differentiation of F9 embryonal stem cells by integrative genomics. Mol Syst Biol 7:538
90. Mengeling BJ, Goodson ML, Bourguet W, Privalsky ML (2012) SMRTepsilon, a corepres-sor variant, interacts with a restricted subset of nuclear receptors, including the retinoic acid receptors alpha and beta. Mol Cell Endocrinol 351:306–316
91. Moutier E, Ye T, Choukrallah MA, Urban S, Osz J, Chatagnon A, Delacroix L, Langer D, Rochel N, Moras D, Benoit G, Davidson I (2012) Retinoic acid receptors recognise the mouse genome through binding elements with diverse spacing and topology. J Biol Chem 287:26328–26341
92. Osz J, Brelivet Y, Peluso-Iltis C, Cura V, Eiler S, Ruff M, Bourguet W, Rochel N, Moras D (2012) Structural basis for a molecular allosteric control mechanism of cofactor binding to nuclear receptors. Proc Natl Acad Sci USA 109:E588–E594
93. Pan J, Kao YL, Joshi S, Jeetendran S, Dipette D, Singh US (2005) Activation of Rac1 by phosphatidylinositol 3-kinase in vivo: role in activation of mitogen-activated protein kinase (MAPK) pathways and retinoic acid-induced neuronal differentiation of SH-SY5Y cells. J Neurochem 93:571–583
94. Perissi V, Aggarwal A, Glass CK, Rose DW, Rosenfeld MG (2004) A corepressor/coactiva-tor exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116:511–526
95. Perissi V, Jepsen K, Glass CK, Rosenfeld MG (2010) Deconstructing repression: evolving models of co-repressor action. Nat Rev Genet 11:109–123
96. Perissi V, Rosenfeld MG (2005) Controlling nuclear receptors: the circular logic of cofactor cycles. Nat Rev Mol Cell Biol 6:542–554
97. Perissi V, Scafoglio C, Zhang J, Ohgi KA, Rose DW, Glass CK, Rosenfeld MG (2008) TBL1 and TBLR1 phosphorylation on regulated gene promoters overcomes dual CtBP and NCoR/SMRT transcriptional repression checkpoints. Mol Cell 29:755–766
98. Perissi V, Staszewski LM, McInerney EM, Kurokawa R, Krones A, Rose DW, Lambert MH, Milburn M V, Glass CK, Rosenfeld MG (1999) Molecular determinants of nuclear receptor-corepressor interaction. Genes Dev 13:3198–3208
99. Piskunov A, Rochette-Egly C (2011) MSK1 and nuclear receptor signaling. In: MSKs, Arthur S, Vermeulen L (eds) Landes Biosciences, Austin
100. Piskunov A, Rochette-Egly C (2012) A retinoic acid receptor RARalpha pool present in membrane lipid rafts forms complexes with G protein alphaQ to activate p38MAPK. Oncogene 31:3333–3345
101. Poon MM, Chen L (2008) Retinoic acid-gated sequence-specifc translational control by RARalpha. Proc Natl Acad Sci USA 105:20303–20308
102. Privalsky ML (2004) The role of corepressors in transcriptional regulation by nuclear hormone receptors. Annu Rev Physiol 66:315–360
103. Renaud JP, Rochel N, Ruff M, Vivat V, Chambon P, Gronemeyer H, Moras D (1995) Crystal structure of the RAR-gamma ligand-binding domain bound to all-trans retinoic acid. Nature 378:681–689
104. Rochel N, Ciesielski F, Godet J, Moman E, Roessle M, Peluso-Iltis C, Moulin M, Haertlein M, Callow P, Mely Y, Svergun DI, Moras D (2011) Common architecture of nuclear receptor heterodimers on DNA direct repeat elements with different spacings. Nat Struct Mol Biol 18:564–570
105. Rochette-Egly C (2003) Nuclear receptors: integration of multiple signalling pathways through phosphorylation. Cell Signal 15:355–366
106. Rochette-Egly C, Adam S, Rossignol M, Egly JM, Chambon P (1997) Stimulation of RAR alpha activation function AF-1 through binding to the general transcription factor TFIIH and phosphorylation by CDK7. Cell 90:97–107
107. Rochette-Egly C, Gaub MP, Lutz Y, Ali S, Scheuer I, Chambon P (1992) Retinoic acid receptor-beta: immunodetection and phosphorylation on tyrosine residues. Mol Endocrinol 6:2197–2209
108. Rochette-Egly C, Germain P (2009) Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors. Nucl Recept Signal 7:e005
109. Rochette-Egly C, Lutz Y, Saunders M, Scheuer I, Gaub MP, Chambon P (1991) Retinoic acid receptor gamma: specifc immunodetection and phosphorylation. J Cell Biol 115:535–545
110. Rochette-Egly C, Oulad-Abdelghani M, Staub A, Pfster V, Scheuer I, Chambon P, Gaub MP (1995) Phosphorylation of the retinoic acid receptor-alpha by protein kinase A. Mol Endocrinol 9:860–871
111. Rosenfeld MG, Lunyak V V, Glass CK (2006) Sensors and signals: a coactivator/corepres-sor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20:1405–1428
112. Samarut E, Amal I, Markov G, Stote R, Dejaegere A, Laudet V, Rochette-Egly C (2011) Evolution of nuclear retinoic acid receptors alpha (RARa) phosphorylation sites. Serine gain provides fne-tuned regulation. Mol Biol Evol 28:2125–2137
113. Samarut E, Rochette-Egly C (2012) Nuclear retinoic acid receptors: conductors of the reti-noic acid symphony during development. Mol Cell Endocrinol 348:348–360
114. Santos NC, Kim KH (2010) Activity of retinoic acid receptor-alpha is directly regulated at its protein kinase A sites in response to follicle-stimulating hormone signaling. Endocrinology 151:2361–2372
115. Schoenfelder S, Sexton T, Chakalova L, Cope NF, Horton A, Andrews S, Kurukuti S, Mitchell JA, Umlauf D, Dimitrova DS, Eskiw CH, Luo Y, Wei CL, Ruan Y, Bieker JJ, Fraser P (2010) Preferential associations between co-regulated genes reveal a transcriptional inter-actome in erythroid cells. Nat Genet 42:53–61
116. Schug TT, Berry DC, Shaw NS, Travis SN, Noy N (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129:723–733
117. Schug TT, Berry DC, Toshkov IA, Cheng L, Nikitin AY, Noy N (2008) Overcoming retinoic acid-resistance of mammary carcinomas by diverting retinoic acid from PPARbeta/delta to RAR. Proc Natl Acad Sci USA 105:7546–7551
118. Sims RJ 3rd, Reinberg D (2008) Is there a code embedded in proteins that is based on post-translational modifcations? Nat Rev Mol Cell Biol 9:815–820
119. Slamon DJ, Clark GM, Wong SG, Levin WJ, Ullrich A, McGuire WL (1987) Human breast cancer: correlation of relapse and survival with amplifcation of the HER-2/neu oncogene. Science 235:177–182
120. Sodhi RK, Singh N (2013) All-trans retinoic acid rescues memory defcits and neuropatho-logical changes in mouse model of streptozotocin-induced dementia of Alzheimer’s type. Prog Neuropsychopharmacol Biol Psychiatry 40:38–46
121. Srinivas H, Juroske DM, Kalyankrishna S, Cody DD, Price RE, Xu XC, Narayanan R, Weigel NL, Kurie JM (2005) c-Jun N-terminal kinase contributes to aberrant retinoid signaling in lung cancer cells by phosphorylating and inducing proteasomal degradation of reti-noic acid receptor alpha. Mol Cell Biol 25:1054–1069
122. Srinivas H, Xia D, Moore NL, Uray IP, Kim H, Ma L, Weigel NL, Brown PH, Kurie JM (2006) Akt phosphorylates and suppresses the transactivation of retinoic acid receptor alpha. Biochem J 395:653–662
123. Stavridis MP, Collins BJ, Storey KG (2010) Retinoic acid orchestrates fbroblast growth factor signalling to drive embryonic stem cell differentiation. Development 137:881–890
124. Stehlin-Gaon C, Willmann D, Zeyer D, Sanglier S, Van Dorsselaer A, Renaud JP, Moras D, Schule R (2003) All-trans retinoic acid is a ligand for the orphan nuclear receptor ROR beta. Nat Struct Biol 10:820–825
125. Taneja R, Rochette-Egly C, Plassat JL, Penna L, Gaub MP, Chambon P (1997) Phosphorylation of activation functions AF-1 and AF-2 of RAR alpha and RAR gamma is indispensable for differentiation of F9 cells upon retinoic acid and cAMP treatment. EMBO J 16:6452–6465
126. Tansey WP (2001) Transcriptional activation: risky business. Genes Dev 15:1045–1050
127. Tari AM, Lim SJ, Hung MC, Esteva FJ, Lopez-Berestein G (2002) Her2/neu induces all-trans retinoic acid (ATRA) resistance in breast cancer cells. Oncogene 21:5224–5232
128. Tarrade A, Bastien J, Bruck N, Bauer A, Gianni M, Rochette-Egly C (2005) Retinoic acid and arsenic trioxide cooperate for apoptosis through phosphorylated RXR alpha. Oncogene 24:2277–2288
129. Varlakhanova N, Hahm JB, Privalsky ML (2011) Regulation of SMRT corepressor dimeri-zation and composition by MAP kinase phosphorylation. Mol Cell Endocrinol 332:180–188
130. Wang A, Alimova IN, Luo P, Jong A, Triche TJ, Wu L (2010) Loss of CAK phosphorylation of RAR{alpha} mediates transcriptional control of retinoid-induced cancer cell differentiation. FASEB J: Offcial Publ Fed Am Soc Exp Biol 24:833–843
131. Warnmark A, Treuter E, Wright AP, Gustafsson JA (2003) Activation functions 1 and 2 of nuclear receptors: molecular strategies for transcriptional activation. Mol Endocrinol 17:1901–1909
132. Wei LN, Hu X, Chandra D, Seto E, Farooqui M (2000) Receptor-interacting protein 140 directly recruits histone deacetylases for gene silencing. J Biol Chem 275:40782–40787
133. Westin S, Rosenfeld MG, Glass CK (2000) Nuclear receptor coactivators. Adv Pharmacol 47:89–112
134. Wilson V, Olivera-Martinez I, Storey KG (2009) Stem cells, signals and vertebrate body axis extension. Development 136:1591–1604
135. Wulf G, Finn G, Suizu F, Lu KP (2005) Phosphorylation-specifc prolyl isomerization: is there an underlying theme? Nat Cell Biol 7:435–441
136. Zarrinpar A, Lim WA (2000) Converging on proline: the mechanism of WW domain peptide recognition. Nat Struct Biol 7:611–613
137. Zechel C, Shen XQ, Chambon P, Gronemeyer H (1994) Dimerization interfaces formed between the DNA binding domains determine the cooperative binding of RXR/RAR and RXR/TR heterodimers to DR5 and DR4 elements. EMBO J 13:1414–1424
138. Zechel C, Shen XQ, Chen JY, Chen ZP, Chambon P, Gronemeyer H (1994) The dimeriza-tion interfaces formed between the DNA binding domains of RXR, RAR and TR determine the binding specifcity and polarity of the full-length receptors to direct repeats. EMBO J 13:1425–1433
139. Zhao Y, Lang G, Ito S, Bonnet J, Metzger E, Sawatsubashi S, Suzuki E, Le Guezennec X, Stunnenberg HG, Krasnov A, Georgieva SG, Schule R, Takeyama K, Kato S, Tora L, Devys D (2008) A TFTC/STAGA module mediates histone H2A and H2B deubiquitination, coacti-vates nuclear receptors, and counteracts heterochromatin silencing. Mol Cell 29:92–101
140. Zhou XE, Suino-Powell KM, Xu Y, Chan CW, Tanabe O, Kruse SW, Reynolds R, Engel JD, Xu HE (2011) The orphan nuclear receptor TR4 is a vitamin A-activated nuclear receptor. J Biol Chem 286:2877–2885