A G-tract element in apoptotic agents-induced alternative splicing

Nucleic Acids Research

Volumn 36, Issue 10, 2008, Pages 3320-3331

  Hai, Yan ^a,b   Cao, Wenguang ^b   Liu, Guodong ^b   Hong, Say Pham ^b   Elela, Sherif Abou ^c   Klinck, Roscoe ^c   Chu, Jiayou ^a   Xie, Jiuyong ^b  

^a INSTITUTE OF MEDICAL BIOLOGY   (China)

^b UNIVERSITY OF MANITOBA   (Canada)

^c UNIVERSITÉ DE SHERBROOKE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 [1 (3 AMIDINOTHIOPROPYL) 1H INDOL 3 YL] 3 (1 METHYL 1H INDOL 3 YL)MALEIMIDE; ISOPROTEIN; MESSENGER RNA PRECURSOR; OKADAIC ACID; PHOSPHOPROTEIN PHOSPHATASE 1; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN BCL XL; PROTEIN KINASE C; RETINOIC ACID; RNA; STRESS ACTIVATED PROTEIN KINASE; ENZYME INHIBITOR; GUANINE; INDOLE DERIVATIVE; MESSENGER RNA; PHOSPHATASE; PROTEIN BCL X; RNA PRECURSOR; RO 31-8220;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL DEATH; CELL GROWTH; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; EXON; GENE FUNCTION; HUMAN; HUMAN CELL; MUTAGENESIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; CHEMISTRY; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; METABOLISM; REGULATORY RNA SEQUENCE; TUMOR CELL LINE;

ALTERNATIVE SPLICING; APOPTOSIS; BCL-X PROTEIN; CELL LINE, TUMOR; ENZYME INHIBITORS; GUANINE; HUMANS; INDOLES; OKADAIC ACID; PHOSPHORIC MONOESTER HYDROLASES; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA PRECURSORS; RNA, MESSENGER;

EID: 45549096260     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkn207     Document Type: Article

References (98)

1. Maniatis,T. and Tasic,B. (2002) Alternative pre-mRNA splicing and proteome expansion in metazoans. Nature, 418, 236-243.
2. Black,D.L. (2000) Protein diversity from alternative splicing: A challenge for bioinformatics and post-genome biology. Cell, 103 367-370.
3. Black,D.L. (2003) Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem., 27, 27.
4. Graveley,B.R. (2001) Alternative splicing: Increasing diversity in the proteomic world. Trends Genet., 17, 100-107.
5. Jiang,Z.H., Zhang,W.J., Rao,Y. and Wu,J.Y. (1998) Regulation of Ich-1 pre-mRNA alternative splicing and apoptosis by mammalian splicing factors. Proc. Natl Acad. Sci. USA, 95, 9155-9160.
6. Wu,J.Y., Tang,H. and Havlioglu,N. (2003) Alternative pre-mRNA splicing and regulation of programmed cell death. Prog. Mol. Subcell. Biol. 31, 153-185.
7. Roberts,G.C. and Smith,C.W. (2002) Alternative splicing: Combinatorial output from the genome. Curr. Opin. Chem. Biol., 6, 375-383.
8. Fu,X.D. (1995).The superfamily of arginine/serine-rich splicing factors. RNA, 1, 663-580.
9. Sanford,J.R., Longman,D. and Caceres,J.F. (2003) Multiple roles of the SR protein family in splicing regulation. Prog. Mol. Subcell. Biol. 31, 33-58.
10. Graveley,B.R. (2000) Sorting out the complexity of SR protein functions. RNA, 6, 1197-1211.
11. Chabot,B., LeBel,C., Hutchison,S., Nasim,F.H. and Simard,M.J. (2003) Heterogeneous nuclear ribonucleoprotein particle A/B proteins and the control of alternative splicing of the mammalian heterogeneous nuclear ribonucleoprotein particle A1 pre-mRNA. Prog. Mol. Subcell. Biol., 31, 59-88.
12. Wagner,E.J. and Garcia-Blanco,M.A. (2001) Polypyrimidine tract binding protein antagonizes exon definition. Mol. Cell. Biol., 21, 3281-3288.
13. Ladd,A.N., Charlet,N. and Cooper,T.A. (2001) The CELF family of RNA binding proteins is implicated in cell-specific and developmentally regulated alternative splicing. Mol. Cell. Biol., 21, 1285-1296.
14. Fukumura,K., Kato,A., Jin,Y., Ideue,T., Hirose,T., Kataoka,N., Fujiwara,T., Sakamoto,H. and Inoue,K. (2007) Tissue-specific splicing regulator Fox-1 induces exon skipping by interfering E complex formation on the downstream intron of human F1gamma gene. Nucleic Acids Res. 35, 5303-5311.
15. Zhou,H.L., Baraniak,A.P. and Lou,H. (2007) Role for Fox-1/Fox-2 in mediating the neuronal pathway of calcitonin/calcitonin gene-related peptide alternative RNA processing. Mol. Cell. Biol., 27, 830-841.
16. Stamm,S. (2008) Regulation of alternative splicing by reversible protein phosphorylation. J. Biol. Chem., 283, 1223-1227.
17. Shin,C. and Manley,J.L. (2004) Cell signalling and the control of pre-mRNA splicing. Nat. Rev. Mol. Cell. Biol., 5, 727-738.
18. Stamm,S. (2002) Signals and their transduction pathways regulating alternative splicing: A new dimension of the human genome. Hum. Mol. Genet., 11, 2409-2416.
19. Konig,H., Ponta,H. and Herrlich,P. (1998) Coupling of signal transduction to alternative pre-mRNA splicing by a composite splice regulator. EMBO J., 17, 2904-2913.
20. Matter,N., Marx,M., Weg-Remers,S., Ponta,H., Herrlich,P. and Konig,H. (2000) Heterogeneous ribonucleoprotein A1 is part of an exon-specific splice-silencing complex controlled by oncogenic signaling pathways. J. Biol. Chem., 275, 35353-35360.
21. Matter,N., Herrlich,P. and Konig,H. (2002) Signal-dependent regulation of splicing via phosphorylation of Sam68. Nature, 420, 691-695.
22. Goekjian,P.G. and Jirousek,M.R. (2001) Protein kinase C inhibitors as novel anticancer drugs. Expert Opin. Invest. Drugs, 10, 2117-2140.
23. Dieter,P. and Fitzke,E. (1991) RO 31-8220 and RO 31-7549 show improved selectivity for protein kinase C over staurosporine in macrophages. Biochem. Biophys. Res. Commun., 181, 396-401.
24. Beltman,J., McCormick,F. and Cook,S.J. (1996) The selective protein kinase C inhibitor, Ro-31-8220, inhibits mitogen-activated protein kinase phosphatase-1 (MKP-1) expression, induces c-Jun expression, and activates Jun N-terminal kinase. J. Biol. Chem., 271, 27018-27024.
25. Han,Z., Pantazis,P., Lange,T.S., Wyche,J.H. and Hendrickson,E.A. (2000) The staurosporine analog, Ro-31-8220, induces apoptosis independently of its ability to inhibit protein kinase C. Cell Death Differ., 7 521-530.
26. Zhu,G.H., Wong,B.C, Eggo,M.C., Yuen,S.T., Lai,K.C. and Lam,S.K. (1999) Pharmacological inhibition of protein kinase C activity could induce apoptosis in gastric cancer cells by differential regulation of apoptosis-related genes. Dig. Dis. Sci., 44, 2020-2026.
27. Motoyama,N., Wang,F., Roth,K.A., Sawa,H., Nakayama,K., Negishi,I., Senju,S., Zhang,Q., Fujii,S. and Loh,D.Y. (1995) Massive cell death of immature hematopoietic cells and neurons in Bcl-x- deficient mice. Science, 267, 1506-1510.
28. Borner,C. (2003) The Bcl-2 protein family: Sensors and checkpoints for life-or-death decisions. Mol. Immunol., 39, 615-647.
29. Boise,L.H., Gonzalez-Garcia,M., Postema,C.E., Ding,L., Lindsten,T., Turka,L.A., Mao,X., Nunez,G. and Thompson,C.B. (1993) bcl-x, a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell, 74, 597-608.
30. Gonzalez-Garcia,M., Garcia,I., Ding,L., O'Shea,S., Boise,L.H., Thompson,C.B. and Nunez,G. (1995) bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent neuronal cell death. Proc. Natl Acad. Sci. USA, 92, 4304-4308.
31. Reed,J.C. (1999) Splicing and dicing apoptosis genes. Nat. Biotechnol., 17, 1064-1065.
32. Mercatante,D.R., Bortner,C.D., Cidlowski,J.A. and Kole,R. (2001) Modification of alternative splicing of Bcl-x pre-mRNA in prostate and breast cancer cells. Analysis of apoptosis and cell death. J. Biol. Chem., 276, 16411-16417.
33. Taylor,J.K., Zhang,Q.Q., Wyatt,J.R. and Dean,N.M. (1999) Induction of endogenous Bcl-xS through the control of Bcl-x pre-mRNA splicing by antisense oligonucleotides. Nat. Biotechnol., 17, 1097-1100.
34. Gonzalez-Garcia,M., Perez-Ballestero,R., Ding,L., Duan,L., Boise,L.H., Thompson,C.B. and Nunez,G. (1994) bcl-XL is the major bcl-x mRNA form expressed during murine development and its product localizes to mitochondria. Development, 120, 3033-3042.
35. Xerri,L., Parc,P., Brousset,P., Schlaifer,D., Hassoun,J., Reed,J.C., Krajewski,S. and Birnbaum,D. (1996) Predominant expression of the long isoform of Bcl-x (Bcl-xL) in human lymphomas. Br. J. Haematol., 92, 900-906.
36. Chalfant,C.E., Rathman,K., Pinkerman,R.L., Wood,R.E., Obeid,L.M., Ogretmen,B. and Hannun,Y.A. (2002) De navo ceramide regulates the alternative splicing of caspase 9 and Bcl-x in A549 lung adenocarcinoma cells. Dependence on protein phosphatase-1. J. Biol. Chem., 277 12587-12595.
37. Li,C.Y., Chu,J.Y., Yu,J.K., Huang,X.Q., Liu,X.J., Shi,L., Che,Y.C. and Xie,J.Y. (2004) Regulation of alternative splicing of Bcl-x by IL-6, GM-CSF and TPA. Cell Res., 14, 473-479.
38. Revil,T., Toutant,J., Shkreta,L., Garneau,D., Cloutier,P. and Chabot,B. (2007) Protein kinase C-dependent control of Bcl-x alternative splicing. Mol. Cell. Biol., 27, 8431-8441.
39. Villemaire,J., Dion,I., Elela,S.A. and Chabot,B. (2003) Reprogramming alternative pre-messenger RNA splicing through the use of protein-binding antisense oligonucleotides. J. Biol. Chem., 278 50031-50039.
40. Wilusz,J.E., Devanney,S.C. and Caputi,M. (2005) Chimeric peptide nucleic acid compounds modulate splicing of the bcl-x gene in vitro and in vivo. Nucleic Acids Res., 33, 6547-6554.
41. Garneau,D., Revil,T., Fisette,J.F. and Chabot,B. (2005) Heterogeneous nuclear ribonucleoprotein F/H proteins modulate the alternative splicing of the apoptotic mediator Bcl-x. J. Biol. Chem., 280, 22641-22650.
42. Massiello,A., Roesser,J.R. and Chalfant,C.E. (2006) SAP155 Binds to ceramide-responsive RNA cis-element 1 and regulates the alternative 5′ splice site selection of Bcl-x pre-mRNA. FASEB J., 20, 1680-1682.
43. Massiello,A., Salas,A., Pinkerman,R.L., Roddy,P., Roesser,J.R. and Chalfant,C.E. (2004) Identification of two RNA cis-elements that function to regulate the 5′ splice site selection of Bcl-x pre-mRNA in response to ceramide. J. Biol. Chem., 279, 15799-15804.
44. Paronetto,M.P., Achsel,T., Massiello,A., Chalfant,C.E. and Sette,C. (2007) The RNA-binding prdtein Sam68 modulates the alternative splicing of Bcl-x. J. Cell. Biol., 176, 929-939.
45. Modafferi,E.F. and Black,D.L. (1999) Combinatorial control of a neuron-specific exon. RNA, 5, 687-706.
46. Smith,C.W. and Valcarcel,J. (2000) Alternative pre-mRNA splicing: The logic of combinatorial control. Trends Biochem. Sci., 25, 381-388.
47. McCullough,A.J. and Berget,S.M. (1997) G triplets located throughout a class of small vertebrate introns enforce intron borders and regulate splice site selection. Mol. Cell. Biol., 17, 4562-4571.
48. Dominguez,C. and Allain,F.H. (2006) NMR structure of the three quasi RNA recognition motifs (qRRMs) of human hnRNP F and interaction studies with Bcl-x G-tract RNA: A novel mode of RNA recognition. Nucleic Acids Res., 34, 3634-3645.
49. Schaub,M.C., Lopez,S.R. and Caputi,M. (2007) Members of the heterogeneous nuclear ribonucleoprotein H family activate splicing of an HIV-1 splicing substrate by promoting formation of ATP-dependent spliceosomal complexes. J. Biol. Chem., 282, 13617-13626.
50. Martinez-Contreras,R., Fisette,J.F., Nasim,F.U., Madden,R., Cordeau,M. and Chabot,B. (2006) Intronic binding sites for hnRNP A/B and hnRNP F/H proteins stimulate pre-mRNA splicing. PLoS Biol., 4, e21.
51. McCullough,A.J. and Berget,S.M. (2000) An intronic splicing enhancer binds U1 snRNPs to enhance splicing and select 5′ splice sites. Mol. Cell. Biol., 20, 9225-9235.
52. Mahe,D., Mahl,P., Gattoni,R., Fischer,N., Mattei,M.G., Stevenin,J. and Fuchs,J.P. (1997) Cloning of human 2H9 heterogeneous nuclear ribonucleoproteins. Relation with splicing and early beat shock-induced splicing arrest. J. Biol. Chem., 272, 1827-1836.
53. Honore,B., Rasmussen,H.H., Vorum,H., Dejgaard,K., Liu,X., Gromov,P., Madsen,P., Gesser,B., Tommerup,N. and Celis,J.E. (1995) Heterogeneous nuclear ribonucleoproteins H, H', and F are members of a ubiquitously expressed subfamily of related but distinct proteins encoded by genes mapping to different chromosomes. J. Biol. Chem., 270, 28780-28789.
54. Caputi,M. and Zahler,A.M. (2001) Determination of the RNA binding specificity of the heterogeneous nuclear ribonucleoprotein (hnRNP) H/H'/ F/2H9 family. J. Biol. Chem., 276, 43850-43859.
55. Wang,E., Dimova,N. and Cambi,F. (2007) PLP/DM20 ratio is regulated by hnRNPH and F and a novel G-rich enhancer in oligodendrocytes. Nucleic Acids Res., 35, 4164-4178.
56. Chou,M.Y., Rooke,N., Turck,C.W. and Black,D.L. (1999) hnRNP H is a component of a splicing enhancer complex that activates a c-src alternative exon in neuronal cells. Mol. Cell. Biol., 19, 69-77.
57. Han,K., Yeo,G., An,P., Burge,C.B. and Grabowski,P.J. (2005) A combinatorial code for splicing silencing: UAGG and GGGG motifs. PLoS Biol., 3, e158.
58. Caputi,M. and Zahler,A.M. (2002) SR proteins and hnRNP H regulate the splicing of the HIV-1 tev-specific exon 6D. EMBO J., 21, 845-855.
59. Chen,C.D., Kobayashi,R. and Helfman,D.M. (1999) Binding of hnRNP H to an exonic splicing silencer is involved in the regulation of alternative splicing of the rat beta-tropomyosin gene. Genes Dev., 13, 593-606.
60. Sironi,M., Menozzi,G., Riva,L., Cagliani,R., Comi,G.P., Bresolin,N., Giorda,R. and Pozzoli,U. (2004) Silencer elements as possible inhibitors of pseudoexon splicing. Nucleic Acids Res., 32, 1783-1791.
61. Xie,J. and Black,D.L. (2001) A CaMK IV responsive RNA element mediates depolarization-induced alternative splicing of ion channels. Nature 410, 936-939.
62. Dominski,Z. and Kole,R. (1991) Selection of splice sites in pre-mRNAs with short internal exons. Mol. Cell. Biol., 11, 6075-6083.
63. Klinck,R., Bramard,A., Inkel,L., Dufresne-Martin,G., Gervais-Bird,J., Madden,R., Paquet,E.R., Koh,C., Venables,J.P., Prinos,P. et al. (2008) Multiple alternative splicing markers for ovarian cancer. Cancer Res., 68, 657-663.
64. Treisman,R., Orkin,S.H. and Maniatis,T. (1983) Specific transcription and RNA splicing defects in five cloned beta- thalassaemia genes. Nature, 302, 591-596.
65. Krainer,A.R., Conway,G.C. and Kozak,D. (1990) The essential pre-mRNA splicing factor SF2 influences 5′ splice site selection by activating proximal sites. Cell, 62, 35-42.
66. Castagna,M., Takai,Y., Kaibuchi,K., Sano,K., Kikkawa,U. and Nishizuka,Y. (1982) Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J. Biol. Chem., 257, 7847-7851.
67. Bialojan,C. and Takai,A. (1988) Inhibitory effect of a marine-sponge toxin, okadaic acid, on protein phosphatases. Specificity and kinetics. Biochem. J., 256, 283-290.
68. Ule,J., Stefani,G., Mele,A., Ruggiu,M., Wang,X., Taneri,B., Gaasterland,T., Blencowe,B.J. and Damell,R.B. (2006) An RNA map predicting Nova-dependent splicing regulation. Nature, 444, 580-586.
69. Hui,J., Hung,L.H., Heiner,M., Schreiner,S., Neumuller,N., Reither,G., Haas,S.A. and Bindereif,A. (2005) Intronic CA-repeat and CA-rich elements: A new class of regulators of mammalian alternative splicing. EMBO J., 24, 1988-1998.
70. Wang,Z., Xiao,X., Van Nostrand,E. and Burge,C.B. (2006) General and specific functions of exonic splicing silencers in splicing control. Mol. Cell, 23, 61-70.
71. Jacquenet,S., Mereau,A., Bilodeau,P.S., Damier,L., Stoltzfus,C.M. and Branlant,C. (2001) A second exon splicing silencer within human immunodeficiency virus type 1 tat exon 2 represses splicing of Tat mRNA and binds protein hnRNP H. J. Biol. Chem., 276, 40464-40475.
72. Underwood,J.G., Boutz,P.L., Dougherty,J.D., Stoilov,P. and Black,D.L. (2005) Homologues of the Caenorhabditis elegans Fox-1 protein are neuronal splicing regulators in mammals. Mol. Cell. Biol., 25 10005-10016.
73. Jin,Y., Suzuki,H., Maegawa,S., Endo,H., Sugano,S., Hashimoto,K., Yasuda,K. and Inoue,K. (2003) A vertebrate RNA-binding protein Fox-1 regulates tissue-specific splicing via the pentanucleotide GCAUG. EMBO J., 22, 905-912.
74. Goren,A., Ram,O., Amit,M., Keren,H., Lev-Maor,G., Vig,I., Pupko,T. and Ast,G. (2006) Comparative analysis identifies exonic splicing regulatory sequences-The complex definition of enhancers and silencers. Mol. Cell, 22, 769-781.
75. Xie,J.Y. (2008) Control of alternative pre-mRNA splicing by Ca++ signals. Biochim. Biophys. Acta-Gene Regul. Mech., [Epub ahead of print, doi:10.1016/j.bbagrm.2008.01.0031, January 17, 2008.
76. Lee,J.A., Xing,Y., Nguyen,D., Xie,J., Lee,C.J. and Black,D.L. (2007) Depolarization and CaM kinase IV modulate NMDA receptor splicing through two essential RNA elements. PLoS Biol., 5, e40.
77. An,P. and Grabowski,P.J. (2007) Exon silencing by UAGG motifs in response to neuronal excitation. PLoS Biol., 5, e36.
78. Murray,M.V., Kobayashi,R. and Krainer,A.R. (1999) The type 2C Ser/Thr phosphatase PP2Cgamma is a pre-mRNA splicing factor. Genes Dev., 13, 87-97.
79. Shi,Y., Reddy,B. and Manley,J.L. (2006) PP1/PP2A phosphatases are required for the second step of Pre-mRNA splicing and target specific snRNP proteins. Mol. Cell, 23, 819-829.
80. Novoyatleva,T., Heinrich,B., Tang,Y., Benderska,N., Butchbach,M.E., Lorson,C.L., Lorson,M.A., Ben-Dov,C., Fehlbaum,P., Bracco,L. et al. (2008) Protein phosphatase 1 binds to the RNA recognition motif of several splicing factors and regulates alternative pre-mRNA processing. Hum. Mol. Genet., 17, 52-70.
81. Shi,Y. and Manley,J.L. (2007) A complex signaling pathway regulates SRp38 phosphorylation and pre-mRNA splicing in response to heat shock. Mol. Cell, 28, 79-90.
82. Boudreau,R.T., Garduno,R. and Lin,T.J. (2002) Protein phosphatase 2A and protein kinase Calpha are physically associated and are involved in Pseudomonas aeruginosa-induced interleukin 6 production by mast cells. J. Biol. Chem., 277, 5322-5329.
83. Bour,G., Lalevee,S. and 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.
84. Germain,P., Chambon,P., Eichele,G., Evans,R.M., Lazar,M.A., Leid,M., De Lera,A.R., Lotan,R., Mangelsdorf,D.J. and Gronemeyer,H. (2006) International Union of Pharmacology. LXIII. Retinoid X receptors. Pharmacol. Rev., 158, 760-772.
85. Loyer,P., Trembley,J.H., Katona,R., Kidd,V.J. and Lahti,J.M. (2005) Role,of CDK/cyclin complexes in transcription and RNA splicing. Cell Signal, 17, 1033-1051.
86. Auboeuf,D., Dowhan,D.H., Kang,Y.K., Larkin,K., Lee,J.W., Berget,S.M. and O'Malley,B.W. (2004), Differential recruitment of nuclear receptor coactivators may determine alternative RNA splice site choice in target genes. Proc. Natl Acad. Sci. USA, 101, 2270-2274.
87. Auboeuf,D., Dowhan,D,H., Li,X., Larkin,K., Ko,L., Berget,S.M. and O'Malley,B.W. (2004) CoAA, a nuclear receptor coactivator protein at the interface of transcriptional coactivation and RNA splicing. Mol. Cell. Biol., 24, 442-453.
88. Dowhan,D.H., Hong,E.P., Auboeuf,D., Dennis,A.P., Wilson,M.M., Berget,S.M. and O'Malley,B.W. (2005) Steroid hormone receptor coactivation and alternative RNA splicing by U2AF65-related proteins CAPERalpha and CAPERbeta. Mol. Cell, 17, 429-439.
89. Auboeuf,D., Honig,A., Berget,S.M. and O'Malley,B.W. (2002) Coordinate regulation of transcription and splicing by steroid receptor coregulators. Science, 298, 416-419.
90. Honore,B., Vorum,H. and Baandrup,U. (1999) hnRNPs H, H′ and F behave differently with respect to posttranslational cleavage and subcellular localization. FEBS Lett., 456, 274-280.
91. Honore,B., Baandrup,U. and Vorum,H. (2004) Heterogeneous nuclear ribonucleoproteins F and H/H′ show differential expression in normal and selected cancer tissues. Exp. Cell Res., 294, 199-209.
92. Navakauskiene,R., Treigyte,G., Gineitis,A. and Magnusson,K.E. (2004) Identification of apoptotic tyrosine-phosphorylated proteins after etoposide or retinoic acid treatment. Proteomics, 4, 1029-1041.
93. Adam-Stitah,S., Penna,L., Chambon,P. and Rochette-Egly,C. (1999) Hyperphosphorylation of the retinoid X receptor alpha by activated c-Jun NH2-terminal kinases. J. Biol. Chem., 274, 18932-18941.
94. Rochette-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.
95. Rochette-Egly,C., Adam,S., Rossignol,M., Egly,J.M. and 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.
96. Bour,G., Gaillard,E., Bruck,N., Lalevee,S., Plassat,J.L., Busso,D., Samama,J.P. and Rochette-Egly,C. (2005) Cyclin H binding to the RARalpha activation function (AF)-2 domain directs phosphorylation of the AF-1 domain by cyclin-dependent kinase 7. Proc. Natl Acad. Sci. USA, 102, 16608-16613.
97. Bastien,J., Adam-Stitah,S., Riedl,T., Egly,J.M., Chambon,P. and 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.
98. Rohaly,G., Chemnitz,J., Dehde,S., Nunez,A.M., Heukeshoven,J., Deppert,W. and Dornreiter,I. (2005) A novel human p53 isoform is an essential element of the ATR-intra-S phase checkpoint. Cell, 122, 21-32.