PIAS1 interacts with FLASH and enhances its co-activation of c-Myb

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Alm Kristiansen, Anne Hege ^a,b   Lorenzo, Petra I ^a,c   Molværsmyr, Ann Kristin ^a   Matre, Vilborg ^a   Ledsaak, Marit ^a   Sæther, Thomas ^a   Gabrielsen, Odd S ^a  

^a UNIVERSITY OF OSLO   (Norway)

^b BioKapital AS   (Norway)

^c CABIMER Andalusian Center for Molecular Biology and Regenerative Medicine CSIC University of Seville UPO   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; GLUTATHIONE TRANSFERASE; NUCLEAR PROTEIN; PROTEIN C MYB; PROTEIN FLASH; PROTEIN PIAS1; RNA POLYMERASE; RNA POLYMERASE II; UNCLASSIFIED DRUG; APOPTOSIS REGULATORY PROTEIN; CALCIUM BINDING PROTEIN; CASP8AP2 PROTEIN, HUMAN; PIAS1 PROTEIN, HUMAN; PROTEIN INHIBITOR OF ACTIVATED STAT; SUMO PROTEIN;

ARTICLE; CONTROLLED STUDY; GENE ACTIVATION; HUMAN; HUMAN CELL; MOLECULAR INTERACTION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; TWO HYBRID SYSTEM; YEAST; ANIMAL; CELL NUCLEUS; CELL STRAIN COS1; CERCOPITHECUS; CHROMATIN; GENE EXPRESSION REGULATION; METABOLISM; PROTEIN BINDING; PROTEIN TRANSPORT;

ANIMALS; APOPTOSIS REGULATORY PROTEINS; CALCIUM-BINDING PROTEINS; CELL NUCLEUS; CERCOPITHECUS AETHIOPS; CHROMATIN; COS CELLS; GENE EXPRESSION REGULATION; HUMANS; PROTEIN BINDING; PROTEIN INHIBITORS OF ACTIVATED STAT; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-MYB; RNA POLYMERASE II; SMALL UBIQUITIN-RELATED MODIFIER PROTEINS;

EID: 79951696298     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-21     Document Type: Article

References (63)

1. Remke M, Pfister S, Kox C, Toedt G, Becker N, Benner A, Werft W, Breit S, Liu S, Engel F, et al. High-resolution genomic profiling of childhood T-ALL reveals frequent copy-number alterations affecting the TGF-beta and PI3K-AKT pathways and deletions at 6q15-16.1 as a genomic marker for unfavorable early treatment response. Blood 2009, 114:1053-1062. 10.1182/blood-2008-10-186536, 19406988.
2. Park TS, Lee SG, Song J, Lee KA, Kim J, Choi JR, Lee ST, Marschalek R, Meyer C. CASP8AP2 is a novel partner gene of MLL rearrangement with t(6;11)(q15;q23) in acute myeloid leukemia. Cancer Genet Cytogenet 2009, 195:94-95. 10.1016/j.cancergencyto.2009.06.023, 19837277.
3. Imai Y, Kimura T, Murakami A, Yajima N, Sakamaki K, Yonehara S. The CED-4-homologous protein FLASH is involved in Fas-mediated activation of caspase-8 during apoptosis. Nature 1999, 398:777-785. 10.1038/19709, 10235259.
4. Milovic-Holm K, Krieghoff E, Jensen K, Will H, Hofmann TG. FLASH links the CD95 signaling pathway to the cell nucleus and nuclear bodies. EMBO J 2007, 26:391-401. 10.1038/sj.emboj.7601504, 1783462, 17245429.
5. Barcaroli D, Dinsdale D, Neale MH, Bongiorno-Borbone L, Ranalli M, Munarriz E, Sayan AE, McWilliam JM, Smith TM, Fava E, et al. FLASH is an essential component of Cajal bodies. Proc Natl Acad Sci USA 2006, 103:14802-14807. 10.1073/pnas.0604225103, 1578500, 17003126.
6. Alm-Kristiansen AH, Saether T, Matre V, Gilfillan S, Dahle O, Gabrielsen OS. FLASH acts as a co-activator of the transcription factor c-Myb and localizes to active RNA polymerase II foci. Oncogene 2008, 27:4644-4656. 10.1038/onc.2008.105, 18408764.
7. Barcaroli D, Bongiorno-Borbone L, Terrinoni A, Hofmann TG, Rossi M, Knight RA, Matera AG, Melino G, De Laurenzi V. FLASH is required for histone transcription and S-phase progression. Proc Natl Acad Sci USA 2006, 103:14808-14812. 10.1073/pnas.0604227103, 1578501, 17003125.
8. Bongiorno-Borbone L, De Cola A, Vernole P, Finos L, Barcaroli D, Knight RA, Melino G, De Laurenzi V. FLASH and NPAT positive but not Coilin positive Cajal Bodies correlate with cell ploidy. Cell Cycle 2008, 7:2357-2367.
9. Yang XC, Burch BD, Yan Y, Marzluff WF, Dominski Z. FLASH, a proapoptotic protein involved in activation of caspase-8, is essential for 3' end processing of histone pre-mRNAs. Mol Cell 2009, 36:267-278. 10.1016/j.molcel.2009.08.016, 2819824, 19854135.
10. Bongiorno-Borbone L, De Cola A, Barcaroli D, Knight RA, Di Ilio C, Melino G, De Laurenzi V. FLASH degradation in response to UV-C results in histone locus bodies disruption and cell-cycle arrest. Oncogene 2010, 29:802-810. 10.1038/onc.2009.388, 19915611.
11. Kino T, Chrousos GP. Tumor necrosis factor alpha receptor- and Fas-associated FLASH inhibit transcriptional activity of the glucocorticoid receptor by binding to and interfering with its interaction with p160 type nuclear receptor coactivators. J Biol Chem 2003, 278:3023-3029. 10.1074/jbc.M209234200, 12477726.
12. Kino T, Ichijo T, Chrousos GP. FLASH interacts with p160 coactivator subtypes and differentially suppresses transcriptional activity of steroid hormone receptors. J Steroid Biochem Mol Biol 2004, 92:357-363. 10.1016/j.jsbmb.2004.09.003, 15698540.
13. Obradovic D, Tirard M, Nemethy Z, Hirsch O, Gronemeyer H, Almeida OF. DAXX, FLASH, and FAF-1 modulate mineralocorticoid and glucocorticoid receptor-mediated transcription in hippocampal cells--toward a basis for the opposite actions elicited by two nuclear receptors?. Mol Pharmacol 2004, 65:761-769. 10.1124/mol.65.3.761, 14978255.
14. Oh IH, Reddy EP. The myb gene family in cell growth, differentiation and apoptosis. Oncogene 1999, 18:3017-3033. 10.1038/sj.onc.1202839, 10378697.
15. Ramsay RG, Gonda TJ. MYB function in normal and cancer cells. Nat Rev Cancer 2008, 8:523-534. 10.1038/nrc2439, 18574464.
16. Lahortiga I, De Keersmaecker K, Van Vlierberghe P, Graux C, Cauwelier B, Lambert F, Mentens N, Beverloo HB, Pieters R, Speleman F, et al. Duplication of the MYB oncogene in T cell acute lymphoblastic leukemia. Nat Genet 2007, 39:593-595. 10.1038/ng2025, 17435759.
17. Clappier E, Cuccuini W, Kalota A, Crinquette A, Cayuela JM, Dik WA, Langerak AW, Montpellier B, Nadel B, Walrafen P, et al. The C-MYB locus is involved in chromosomal translocation and genomic duplications in human T-cell acute leukemia (T-ALL), the translocation defining a new T-ALL subtype in very young children. Blood 2007, 110:1251-1261. 10.1182/blood-2006-12-064683, 17452517.
18. Persson M, Andren Y, Mark J, Horlings HM, Persson F, Stenman G. Recurrent fusion of MYB and NFIB transcription factor genes in carcinomas of the breast and head and neck. Proc Natl Acad Sci USA 2009, 106:18740-18744. 10.1073/pnas.0909114106, 2773970, 19841262.
19. Zhao H, Kalota A, Jin S, Gewirtz AM. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood 2009, 113:505-516. 10.1182/blood-2008-01-136218, 2628359, 18818396.
20. Andersson KB, Kowenz-Leutz E, Brendeford EM, Tygsett AH, Leutz A, Gabrielsen OS. Phosphorylation-dependent Down-regulation of c-Myb DNA Binding Is Abrogated by a Point Mutation in the v-myb Oncogene. J Biol Chem 2003, 278:3816-3824. 10.1074/jbc.M209404200, 12456674.
21. Ganter B, Lipsick JS. Myb and oncogenesis. Adv Cancer Res 1999, 76:21-60. full_text, 10218098.
22. Winn LM, Lei W, Ness SA. Pim-1 phosphorylates the DNA binding domain of c-Myb. Cell Cycle 2003, 2:258-262. 10.4161/cc.2.3.383, 12734436.
23. Matre V, Nordgard O, Alm-Kristiansen AH, Ledsaak M, Gabrielsen OS. HIPK1 interacts with c-Myb and modulates its activity through phosphorylation. Biochem Biophys Res Commun 2009, 388:150-154. 10.1016/j.bbrc.2009.07.139, 19646965.
24. Bies J, Markus J, Wolff L. Covalent attachment of the SUMO-1 protein to the negative regulatory domain of the c-Myb transcription factor modifies its stability and transactivation capacity. J Biol Chem 2002, 277:8999-9009. 10.1074/jbc.M110453200, 11779867.
25. Dahle O, Andersen TO, Nordgard O, Matre V, Del Sal G, Gabrielsen OS. Transactivation properties of c-Myb are critically dependent on two SUMO-1 acceptor sites that are conjugated in a PIASy enhanced manner. Eur J Biochem 2003, 270:1338-1348. 10.1046/j.1432-1033.2003.03504.x, 12631292.
26. Molvaersmyr AK, Saether T, Gilfillan S, Lorenzo PI, Kvaloy H, Matre V, Gabrielsen OS. A SUMO-regulated activation function controls synergy of c-Myb through a repressor-activator switch leading to differential p300 recruitment. Nucleic Acids Res 2010, 38:4970-4984. 10.1093/nar/gkq245, 2926607, 20385574.
27. Sano Y, Ishii S. Increased affinity of c-Myb for CREB-binding protein (CBP) after CBP-induced acetylation. J Biol Chem 2001, 276:3674-3682. 10.1074/jbc.M006896200, 11073948.
28. Tomita A, Towatari M, Tsuzuki S, Hayakawa F, Kosugi H, Tamai K, Miyazaki T, Kinoshita T, Saito H. c-Myb acetylation at the carboxyl-terminal conserved domain by transcriptional co-activator p300. Oncogene 2000, 19:444-451. 10.1038/sj.onc.1203329, 10656693.
29. Saether T, Berge T, Ledsaak M, Matre V, Alm-Kristiansen AH, Dahle O, Aubry F, Gabrielsen OS. The chromatin remodeling factor Mi-2alpha acts as a novel co-activator for human c-Myb. J Biol Chem 2007, 282:13994-14005. 10.1074/jbc.M700755200, 17344210.
30. Saether T, Pattabiraman DR, Alm-Kristiansen AH, Vogt-Kielland LT, Gonda TJ, Gabrielsen OS. A functional SUMO-interacting motif in the transactivation domain of c-Myb regulates its myeloid transforming ability. Oncogene 2011, 30:212-222. 10.1038/onc.2010.397, 20802522.
31. Schmidt D, Muller S. PIAS/SUMO: new partners in transcriptional regulation. Cell Mol Life Sci 2003, 60:2561-2574. 10.1007/s00018-003-3129-1, 14685683.
32. Sharrocks AD. PIAS proteins and transcriptional regulation--more than just SUMO E3 ligases?. Genes Dev 2006, 20:754-758. 10.1101/gad.1421006, 16600908.
33. Huang CY, Beliakoff J, Li X, Lee J, Sharma M, Lim B, Sun Z. hZimp7, a novel PIAS-like protein, enhances androgen receptor-mediated transcription and interacts with SWI/SNF-like BAF complexes. Mol Endocrinol 2005, 19:2915-2929. 10.1210/me.2005-0097, 16051670.
34. Sharma M, Li X, Wang Y, Zarnegar M, Huang CY, Palvimo JJ, Lim B, Sun Z. hZimp10 is an androgen receptor co-activator and forms a complex with SUMO-1 at replication foci. EMBO J 2003, 22:6101-6114. 10.1093/emboj/cdg585, 275443, 14609956.
35. Shuai K, Liu B. Regulation of gene-activation pathways by PIAS proteins in the immune system. Nat Rev Immunol 2005, 5:593-605. 10.1038/nri1667, 16056253.
36. Gill G. Something about SUMO inhibits transcription. Curr Opin Genet Dev 2005, 15:536-541. 10.1016/j.gde.2005.07.004, 16095902.
37. Hay RT. SUMO: a history of modification. Mol Cell 2005, 18:1-12. 10.1016/j.molcel.2005.03.012, 15808504.
38. Lee H, Quinn JC, Prasanth KV, Swiss VA, Economides KD, Camacho MM, Spector DL, Abate-Shen C. PIAS1 confers DNA-binding specificity on the Msx1 homeoprotein. Genes Dev 2006, 20:784-794. 10.1101/gad.1392006, 1472282, 16600910.
39. Matsuura T, Shimono Y, Kawai K, Murakami H, Urano T, Niwa Y, Goto H, Takahashi M. PIAS proteins are involved in the SUMO-1 modification, intracellular translocation and transcriptional repressive activity of RET finger protein. Exp Cell Res 2005, 308:65-77. 10.1016/j.yexcr.2005.04.022, 15907835.
40. Sachdev S, Bruhn L, Sieber H, Pichler A, Melchior F, Grosschedl R. PIASy, a nuclear matrix-associated SUMO E3 ligase, represses LEF1 activity by sequestration into nuclear bodies. Genes Dev 2001, 15:3088-3103. 10.1101/gad.944801, 312834, 11731474.
41. Stielow B, Sapetschnig A, Wink C, Kruger I, Suske G. SUMO-modified Sp3 represses transcription by provoking local heterochromatic gene silencing. EMBO Rep 2008, 9:899-906. 10.1038/embor.2008.127, 2529347, 18617891.
42. Kotaja N, Karvonen U, Janne OA, Palvimo JJ. PIAS proteins modulate transcription factors by functioning as SUMO-1 ligases. Mol Cell Biol 2002, 22:5222-5234. 10.1128/MCB.22.14.5222-5234.2002, 139781, 12077349.
43. Lee JM, Kang HJ, Lee HR, Choi CY, Jang WJ, Ahn JH. PIAS1 enhances SUMO-1 modification and the transactivation activity of the major immediate-early IE2 protein of human cytomegalovirus. FEBS Lett 2003, 555:322-328. 10.1016/S0014-5793(03)01268-7, 14644436.
44. Munarriz E, Barcaroli D, Stephanou A, Townsend PA, Maisse C, Terrinoni A, Neale MH, Martin SJ, Latchman DS, Knight RA, et al. PIAS-1 is a checkpoint regulator which affects exit from G1 and G2 by sumoylation of p73. Mol Cell Biol 2004, 24:10593-10610. 10.1128/MCB.24.24.10593-10610.2004, 533962, 15572666.
45. Alm-Kristiansen AH, Norman IL, Matre V, Gabrielsen OS. SUMO modification regulates the transcriptional activity of FLASH. Biochem Biophys Res Commun 2009, 387:494-499. 10.1016/j.bbrc.2009.07.053, 19615980.
46. Sramko M, Markus J, Kabat J, Wolff L, Bies J. Stress-induced inactivation of the c-Myb transcription factor through conjugation of SUMO-2/3 proteins. J Biol Chem 2006, 281:40065-40075. 10.1074/jbc.M609404200, 17077080.
47. Schmidt M, Nazarov V, Stevens L, Watson R, Wolff L. Regulation of the resident chromosomal copy of c-myc by c-Myb is involved in myeloid leukemogenesis. Mol Cell Biol 2000, 20:1970-1981. 10.1128/MCB.20.6.1970-1981.2000, 110814, 10688644.
48. Bianchi E, Zini R, Salati S, Tenedini E, Norfo R, Tagliafico E, Manfredini R, Ferrari S. c-myb supports erythropoiesis through the transactivation of KLF1 and LMO2 expression. Blood 2010, 116:e99-110. 10.1182/blood-2009-08-238311, 20686118.
49. Berge T, Matre V, Brendeford EM, Saether T, Luscher B, Gabrielsen OS. Revisiting a selection of target genes for the hematopoietic transcription factor c-Myb using chromatin immunoprecipitation and c-Myb knockdown. Blood Cells Mol Dis 2007, 39:278-286. 10.1016/j.bcmd.2007.05.007, 17587615.
50. Liu B, Yang Y, Chernishof V, Loo RR, Jang H, Tahk S, Yang R, Mink S, Shultz D, Bellone CJ, et al. Proinflammatory stimuli induce IKKalpha-mediated phosphorylation of PIAS1 to restrict inflammation and immunity. Cell 2007, 129:903-914. 10.1016/j.cell.2007.03.056, 17540171.
51. Weber S, Maass F, Schuemann M, Krause E, Suske G, Bauer UM. PRMT1-mediated arginine methylation of PIAS1 regulates STAT1 signaling. Genes Dev 2009, 23:118-132. 10.1101/gad.489409, 2632166, 19136629.
52. Zhao X, Zheng B, Huang Y, Yang D, Katzman S, Chang C, Fowell D, Zeng WP. Interaction between GATA-3 and the transcriptional coregulator Pias1 is important for the regulation of Th2 immune responses. J Immunol 2007, 179:8297-8304.
53. Long J, Wang G, Matsuura I, He D, Liu F. Activation of Smad transcriptional activity by protein inhibitor of activated STAT3 (PIAS3). Proc Natl Acad Sci USA 2004, 101:99-104. 10.1073/pnas.0307598100, 314145, 14691252.
54. Prigge JR, Schmidt EE. Interaction of protein inhibitor of activated STAT (PIAS) proteins with the TATA-binding protein, TBP. J Biol Chem 2006, 281:12260-12269. 10.1074/jbc.M510835200, 2030495, 16522640.
55. Du JX, Yun CC, Bialkowska A, Yang VW. Protein inhibitor of activated STAT1 interacts with and up-regulates activities of the pro-proliferative transcription factor Kruppel-like factor 5. J Biol Chem 2007, 282:4782-4793. 10.1074/jbc.M603413200, 2212600, 17178721.
56. Chang LK, Lee YH, Cheng TS, Hong YR, Lu PJ, Wang JJ, Wang WH, Kuo CW, Li SS, Liu ST. Post-translational modification of Rta of Epstein-Barr virus by SUMO-1. J Biol Chem 2004, 279:38803-38812. 10.1074/jbc.M405470200, 15229220.
57. Megidish T, Xu JH, Xu CW. Activation of p53 by protein inhibitor of activated Stat1 (PIAS1). J Biol Chem 2002, 277:8255-8259. 10.1074/jbc.C200001200, 11788578.
58. Yang SH, Sharrocks AD. PIASx acts as an Elk-1 coactivator by facilitating derepression. EMBO J 2005, 24:2161-2171. 10.1038/sj.emboj.7600690, 1150884, 15920481.
59. Lee J, Beliakoff J, Sun Z. The novel PIAS-like protein hZimp10 is a transcriptional co-activator of the p53 tumor suppressor. Nucleic Acids Res 2007, 35:4523-4534. 10.1093/nar/gkm476, 1935018, 17584785.
60. Sutherland H, Bickmore WA. Transcription factories: gene expression in unions?. Nat Rev Genet 2009, 10:457-466. 10.1038/nrg2592, 19506577.
61. Choi YH, Kim KB, Kim HH, Hong GS, Kwon YK, Chung CW, Park YM, Shen ZJ, Kim BJ, Lee SY, Jung YK. FLASH coordinates NF-kappa B activity via TRAF2. J Biol Chem 2001, 276:25073-25077. 10.1074/jbc.M102941200, 11340079.
62. Gostissa M, Hengstermann A, Fogal V, Sandy P, Schwarz SE, Scheffner M, Del Sal G. Activation of p53 by conjugation to the ubiquitin-like protein SUMO-1. EMBO J 1999, 18:6462-6471. 10.1093/emboj/18.22.6462, 1171709, 10562558.
63. Gabrielsen OS, Sentenac A, Fromageot P. Specific DNA binding by c-Myb: evidence for a double helix-turn-helix- related motif. Science 1991, 253:1140-1143. 10.1126/science.1887237, 1887237.