Signal transducer and activator of transcription STAT5 is recruited to c-Myc super-enhancer

BMC Molecular Biology

Volumn 17, Issue 1, 2016, Pages

  Pinz, Sophia ^a   Unser, Samy ^a   Rascle, Anne ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

BET; BRD2; c Myc; Chromatin; STAT5; Super enhancer

Indexed keywords

4 (4 CHLOROPHENYL) 2,3,9 TRIMETHYL 6H THIENO[3,2 F][1,2,4]TRIAZOLO[4,3 A][1,4]DIAZEPINE 6 ACETIC ACID TERT BUTYL ESTER; BROMODOMAIN CONTAINING PROTEIN 2; GENOMIC DNA; MESSENGER RNA; MUTANT PROTEIN; MYC PROTEIN; REGULATOR PROTEIN; STAT5 PROTEIN; TRICHOSTATIN A; UNCLASSIFIED DRUG; BRD2 PROTEIN, HUMAN; CELL SURFACE RECEPTOR; DNER PROTEIN, MOUSE; NERVE PROTEIN; PROTEIN BINDING; PROTEIN SERINE THREONINE KINASE;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BA F3 CELL LINE; BINDING AFFINITY; BINDING SITE; CELL LINE; CELL TRANSFORMATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENHANCER REGION; GENE EXPRESSION REGULATION; GENE LOCUS; MOUSE; NONHUMAN; ONCOGENE C MYC; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; STABLE EXPRESSION; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSCRIPTION TERMINATION; ANIMAL; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; ONCOGENE MYC; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TRANSFORMED CELL LINE;

ANIMALS; BASE SEQUENCE; CELL LINE; CELL LINE, TRANSFORMED; GENE EXPRESSION REGULATION; GENES, MYC; MICE; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT; STAT5 TRANSCRIPTION FACTOR;

EID: 84963500007     PISSN: None     EISSN: 14712199     Source Type: Journal    
DOI: 10.1186/s12867-016-0063-y     Document Type: Article

References (50)

1. Hoffman B, Amanullah A, Shafarenko M, Liebermann DA. The proto-oncogene c-myc in hematopoietic development and leukemogenesis. Oncogene. 2002;21:3414-21.
2. Chappell J, Dalton S. Roles for MYC in the establishment and maintenance of pluripotency. Cold Spring Harb Perspect Med. 2013;3:a014381.
3. McKeown MR, Bradner JE. Therapeutic strategies to inhibit MYC. Cold Spring Harb Perspect Med. 2014;4:a014266.
4. Gabay M, Li Y, Felsher DW. MYC activation is a hallmark of cancer initiation and maintenance. Cold Spring Harb Perspect Med. 2014;4:a014241.
5. Shi J, Whyte WA, Zepeda-Mendoza CJ, Milazzo JP, Shen C, Roe J-S, et al. Role of SWI/SNF in acute leukemia maintenance and enhancer-mediated Myc regulation. Genes Dev. 2013;27:2648-62.
6. Roe J-S, Mercan F, Rivera K, Pappin DJ, Vakoc CR. BET bromodomain inhibition suppresses the function of hematopoietic transcription factors in acute myeloid leukemia. Mol Cell. 2015;58:1028-39.
7. Sotelo J, Esposito D, Duhagon MA, Banfield K, Mehalko J, Liao H, et al. Long-range enhancers on 8q24 regulate c-Myc. Proc Natl Acad Sci USA. 2010;107:3001-5.
8. Yashiro-Ohtani Y, Wang H, Zang C, Arnett KL, Bailis W, Ho Y, et al. Long-range enhancer activity determines Myc sensitivity to Notch inhibitors in T cell leukemia. Proc Natl Acad Sci USA. 2014;111:E4946-53.
9. Sengupta D, Kannan A, Kern M, Moreno MA, Vural E, Stack B, et al. Disruption of BRD4 at H3K27Ac-enriched enhancer region correlates with decreased c-Myc expression in Merkel cell carcinoma. Epigenetics. 2015;10:460-6.
10. Lord JD, McIntosh BC, Greenberg PD, Nelson BH. The IL-2 receptor promotes lymphocyte proliferation and induction of the c-myc, bcl-2, and bcl-x genes through the trans-activation domain of Stat5. J Immunol Baltim Md. 1950;2000(164):2533-41.
11. Nosaka T, Kawashima T, Misawa K, Ikuta K, Mui AL, Kitamura T. STAT5 as a molecular regulator of proliferation, differentiation and apoptosis in hematopoietic cells. EMBO J. 1999;18:4754-65.
12. Rascle A, Johnston JA, Amati B. Deacetylase activity is required for recruitment of the basal transcription machinery and transactivation by STAT5. Mol Cell Biol. 2003;23:4162-73.
13. Basham B, Sathe M, Grein J, McClanahan T, D'Andrea A, Lees E, et al. In vivo identification of novel STAT5 target genes. Nucleic Acids Res. 2008;36:3802-18.
14. Wakao H, Gouilleux F, Groner B. Mammary gland factor (MGF) is a novel member of the cytokine regulated transcription factor gene family and confers the prolactin response. EMBO J. 1994;13:2182-91.
15. Grimley PM, Dong F, Rui H. Stat5a and Stat5b: fraternal twins of signal transduction and transcriptional activation. Cytokine Growth Factor Rev. 1999;10:131-57.
16. Nosaka T, Kitamura T. Pim-1 expression is sufficient to induce cytokine independence in murine hematopoietic cells, but is dispensable for BCR-ABL-mediated transformation. Exp Hematol. 2002;30:697-702.
17. Liu CB, Itoh T, Arai K, Watanabe S. Constitutive activation of JAK2 confers murine interleukin-3-independent survival and proliferation of BA/F3 cells. J Biol Chem. 1999;274:6342-9.
18. Gesbert F, Griffin JD. Bcr/Abl activates transcription of the Bcl-X gene through STAT5. Blood. 2000;96:2269-76.
19. Valentino L, Pierre J. JAK/STAT signal transduction: regulators and implication in hematological malignancies. Biochem Pharmacol. 2006;71:713-21.
20. Ren S, Cai HR, Li M, Furth PA. Loss of Stat5a delays mammary cancer progression in a mouse model. Oncogene. 2002;21:4335-9.
21. Romanski A, Schwarz K, Keller M, Wietbrauk S, Vogel A, Roos J, et al. Deacetylase inhibitors modulate proliferation and self-renewal properties of leukemic stem and progenitor cells. Cell Cycle Georget Tex. 2012;11:3219-26.
22. Kosan C, Ginter T, Heinzel T, Krämer OH. STAT5 acetylation: mechanisms and consequences for immunological control and leukemogenesis. JAK-STAT. 2013;2:e26102.
23. Pietschmann K, Bolck HA, Buchwald M, Spielberg S, Polzer H, Spiekermann K, et al. Breakdown of the FLT3-ITD/STAT5 axis and synergistic apoptosis induction by the histone deacetylase inhibitor panobinostat and FLT3-specific inhibitors. Mol Cancer Ther. 2012;11:2373-83.
24. Evrot E, Ebel N, Romanet V, Roelli C, Andraos R, Qian Z, et al. JAK1/2 and Pan-deacetylase inhibitor combination therapy yields improved efficacy in preclinical mouse models of JAK2V617F-driven disease. Clin Cancer Res. 2013;19:6230-41.
25. Wang Y, Fiskus W, Chong DG, Buckley KM, Natarajan K, Rao R, et al. Cotreatment with panobinostat and JAK2 inhibitor TG101209 attenuates JAK2V617F levels and signaling and exerts synergistic cytotoxic effects against human myeloproliferative neoplastic cells. Blood. 2009;114:5024-33.
26. Nguyen T, Dai Y, Attkisson E, Kramer L, Jordan N, Nguyen N, et al. HDAC inhibitors potentiate the activity of the BCR/ABL kinase inhibitor KW-2449 in imatinib-sensitive or -resistant BCR/ABL+ leukemia cells in vitro and in vivo. Clin Cancer Res. 2011;17:3219-32.
27. Fiskus W, Sharma S, Qi J, Shah B, Devaraj SGT, Leveque C, et al. BET protein antagonist JQ1 is synergistically lethal with FLT3 tyrosine kinase inhibitor (TKI) and overcomes resistance to FLT3-TKI in AML cells expressing FLT-ITD. Mol Cancer Ther. 2014;13:2315-27.
28. Fiskus W, Sharma S, Qi J, Valenta JA, Schaub LJ, Shah B, et al. Highly active combination of BRD4 antagonist and histone deacetylase inhibitor against human acute myelogenous leukemia cells. Mol Cancer Ther. 2014;13:1142-54.
29. Rascle A, Lees E. Chromatin acetylation and remodeling at the Cis promoter during STAT5-induced transcription. Nucleic Acids Res. 2003;31:6882-90.
30. Liu S, Walker SR, Nelson EA, Cerulli R, Xiang M, Toniolo PA, et al. Targeting STAT5 in hematological malignancies through inhibition of the bromodomain and extra-terminal (BET) bromodomain protein BRD2. Mol Cancer Ther. 2014;13:1194-205.
31. Pinz S, Unser S, Buob D, Fischer P, Jobst B, Rascle A. Deacetylase inhibitors repress STAT5-mediated transcription by interfering with bromodomain and extra-terminal (BET) protein function. Nucleic Acids Res. 2015;43:3524-45.
32. Pinz S, Unser S, Brueggemann S, Besl E, Al-Rifai N, Petkes H, et al. The synthetic α-bromo-2′,3,4,4′-tetramethoxychalcone (α-Br-TMC) inhibits the JAK/STAT signaling pathway. PLoS One. 2014;9:e90275.
33. de Groot RP, Raaijmakers JA, Lammers JW, Jove R, Koenderman L. STAT5 activation by BCR-Abl contributes to transformation of K562 leukemia cells. Blood. 1999;94:1108-12.
34. Nieborowska-Skorska M, Wasik MA, Slupianek A, Salomoni P, Kitamura T, Calabretta B, et al. Signal transducer and activator of transcription (STAT)5 activation by BCR/ABL is dependent on intact Src homology (SH)3 and SH2 domains of BCR/ABL and is required for leukemogenesis. J Exp Med. 1999;189:1229-42.
35. Onishi M, Nosaka T, Misawa K, Mui AL, Gorman D, McMahon M, et al. Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol Cell Biol. 1998;18:3871-9.
36. Silva M, Benito A, Sanz C, Prosper F, Ekhterae D, Nuñez G, et al. Erythropoietin can induce the expression of bcl-x(L) through Stat5 in erythropoietin-dependent progenitor cell lines. J Biol Chem. 1999;274:22165-9.
37. Xu M, Nie L, Kim S-H, Sun X-H. STAT5-induced Id-1 transcription involves recruitment of HDAC1 and deacetylation of C/EBPbeta. EMBO J. 2003;22:893-904.
38. Nelson EA, Walker SR, Alvarez JV, Frank DA. Isolation of unique STAT5 targets by chromatin immunoprecipitation-based gene identification. J Biol Chem. 2004;279:54724-30.
39. Kiuchi N, Nakajima K, Ichiba M, Fukada T, Narimatsu M, Mizuno K, et al. STAT3 is required for the gp130-mediated full activation of the c-myc gene. J Exp Med. 1999;189:63-73.
40. Ramana CV, Grammatikakis N, Chernov M, Nguyen H, Goh KC, Williams BR, et al. Regulation of c-myc expression by IFN-gamma through Stat1-dependent and -independent pathways. EMBO J. 2000;19:263-72.
41. Grigorieva I, Grigoriev VG, Rowney MK, Hoover RG. Regulation of c-myc transcription by interleukin-2 (IL-2). Identification of a novel IL-2 response element interacting with STAT-4. J Biol Chem. 2000;275:7343-50.
42. Uslu VV, Petretich M, Ruf S, Langenfeld K, Fonseca NA, Marioni JC, et al. Long-range enhancers regulating Myc expression are required for normal facial morphogenesis. Nat Genet. 2014;46:753-8.
43. Filippakopoulos P, Qi J, Picaud S, Shen Y, Smith WB, Fedorov O, et al. Selective inhibition of BET bromodomains. Nature. 2010;468:1067-73.
44. Mertz JA, Conery AR, Bryant BM, Sandy P, Balasubramanian S, Mele DA, et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc Natl Acad Sci USA. 2011;108:16669-74.
45. Palacios R, Steinmetz M. Il-3-dependent mouse clones that express B-220 surface antigen, contain Ig genes in germ-line configuration, and generate B lymphocytes in vivo. Cell. 1985;41:727-34.
46. Soldaini E, John S, Moro S, Bollenbacher J, Schindler U, Leonard WJ. DNA binding site selection of dimeric and tetrameric Stat5 proteins reveals a large repertoire of divergent tetrameric Stat5a binding sites. Mol Cell Biol. 2000;20:389-401.
47. Quentmeier H, MacLeod RA, Zaborski M, Drexler HG. JAK2 V617F tyrosine kinase mutation in cell lines derived from myeloproliferative disorders. Leukemia. 2006;20:471-6.
48. Bar-Natan M, Nelson EA, Walker SR, Kuang Y, Distel RJ, Frank DA. Dual inhibition of Jak2 and STAT5 enhances killing of myeloproliferative neoplasia cells. Leukemia. 2012;26:1407-10.
49. Dawson MA, Foster SD, Bannister AJ, Robson SC, Hannah R, Wang X, et al. Three distinct patterns of histone H3Y41 phosphorylation mark active genes. Cell Rep. 2012;2:470-7.
50. Pinz S, Rascle A. Assessing HDAC function in the regulation of signal transducer and activator of transcription 5 (STAT5) activity using chromatin immunoprecipitation (ChIP). Methods Mol Biol. 2016 (in press).