Construction of the gene regulatory network identifies MYC as a transcriptional regulator of SWI/SNF complex.
Animals
Chromatin
/ genetics
Chromosomal Proteins, Non-Histone
/ genetics
Gene Expression Regulation
Gene Regulatory Networks
Humans
Mice
Multiprotein Complexes
/ genetics
Nuclear Proteins
/ genetics
Promoter Regions, Genetic
Proto-Oncogene Proteins c-myc
/ genetics
Transcription Factors
/ genetics
Transcription, Genetic
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
13 01 2020
13 01 2020
Historique:
received:
21
08
2019
accepted:
17
12
2019
entrez:
15
1
2020
pubmed:
15
1
2020
medline:
13
11
2020
Statut:
epublish
Résumé
Precise positioning of nucleosomes at the gene regulatory elements mediated by the SWI/SNF family of remodelling complex is important for the transcriptional regulation of genes. A wide set of genes are either positively or negatively regulated by SWI/SNF. In higher eukaryotes, around thirty genes were found to code for SWI/SNF subunits. The construction of a gene regulatory network of SWI/SNF subunits identifies MYC as a common regulator for many of the SWI/SNF subunit genes. A meta-analysis study was conducted to investigate the MYC dependent regulation of SWI/SNF remodelling complex. Subunit information and the promoter sequences of the subunit genes were used to find the canonical E-box motif and its variants. Detailed analysis of mouse and human ChIP-Seq at the SWI/SNF subunit loci indicates the presence of MYC binding peaks overlapping with E-boxes. The co-expression correlation and the differential expression analysis of wt vs. MYC perturbed MEFs indicate the MYC dependent regulation of some of the SWI/SNF subunits. The extension of the analysis was done on MYC proficient and MYC deficient embryonic fibroblast cell lines, TGR1 and HO15, and in one of the MYC amplified cancer types, Medulloblastoma. A transcriptional regulatory feedback loop between MYC and SWI/SNF could be a major factor contributing to the aggressiveness of MYC dependent cancers.
Identifiants
pubmed: 31932624
doi: 10.1038/s41598-019-56844-7
pii: 10.1038/s41598-019-56844-7
pmc: PMC6957478
doi:
Substances chimiques
Chromatin
0
Chromosomal Proteins, Non-Histone
0
Multiprotein Complexes
0
Nuclear Proteins
0
Proto-Oncogene Proteins c-myc
0
SWI-SNF-B chromatin-remodeling complex
0
Transcription Factors
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
158Références
Lee, T. I. & Young, R. A. Non-Coding RNAs in Transcriptional Regulation. Cell. 152, 1237–51 (2014).
doi: 10.1016/j.cell.2013.02.014
Chen, Y. A. & Aravin, A. A. Non-Coding RNAs in Transcriptional Regulation. Curr. Mol. Biol. Rep. 1, 10–18 (2015).
pubmed: 26120554
pmcid: 4479201
doi: 10.1007/s40610-015-0002-6
Hirschhorn, J. N., Brown, S. A., Clark, C. D. & Winston, F. Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev. 6, 2288–2298 (1992).
pubmed: 1459453
doi: 10.1101/gad.6.12a.2288
Villagra, A. et al. Chromatin remodelling and transcriptional activity of the bone specific osteocalcigene require CCAAT/enhancer-binding protein beta dependent recruitment of SWI/SNF activity. J. Biol. Chem. 281, 22695–706 (2006).
pubmed: 16772287
doi: 10.1074/jbc.M511640200
Cheng, S. W. et al. c-MYC interacts with INI1/hSNF5 and requires the SWI/SNF complex for transactivation function. Nat Genet. 22, 102–5 (1999).
pubmed: 10319872
doi: 10.1038/8811
Debril, M. B. et al. Transcription Factors and Nuclear Receptors Interact with the SWI/SNF Complex through the BAF60c Subunit. J. Biol. Chem. 279, 16677–16686 (2004).
pubmed: 14701856
doi: 10.1074/jbc.M312288200
Quinn, J., Fyrberg, A. M., Ganster, R. W., Schmidt, M. C. & Peterson, C. L. DNA-binding properties of the yeast SWI/SNF complex. Nature. 379, 844–7 (1996).
pubmed: 8587611
doi: 10.1038/379844a0
Mani, U., S., A. S., Goutham, R. N. A. & Mohan, S. S. SWI/SNF Infobase—An exclusive information portal for SWI/SNF remodeling complex subunits. PLoS One. 12, e0184445 (2017).
pubmed: 28961249
pmcid: 5621669
doi: 10.1371/journal.pone.0184445
Wang, W. et al. Diversity and specialization of mammalian SWI/SNF complexes. Genes Dev. 10, 2117–2130 (1996).
pubmed: 8804307
doi: 10.1101/gad.10.17.2117
Romero, O. A. & Sanchez-Cespedes, M. The SWI/SNF genetic blockade: effects in cell differentiation, cancer and developmental diseases. Oncogene. 33, 2681–2689 (2014).
pubmed: 23752187
doi: 10.1038/onc.2013.227
Bishop, J. M. Retroviruses and cancer genes. Adv. Cancer Res. 37, 1–3 (1982).
pubmed: 6763842
doi: 10.1016/S0065-230X(08)60880-5
pmcid: 6763842
Tansey, W. P. Mammalian MYC Proteins and Cancer. New J. Sci. 2103, 1–27 (2014).
doi: 10.1155/2014/757534
Dang, C. V. et al. Function of the c-Myc Oncogenic Transcription Factor. Exp. Cell Res. 253, 63–77 (1999).
pubmed: 10579912
doi: 10.1006/excr.1999.4686
pmcid: 10579912
Gabay, M., Li, Y. & Felsher, D. W. MYC activation is a hallmark of cancer initation and maintenance. Cold Spring Harb Perspect Med. 4, a014241 (2014).
pubmed: 24890832
pmcid: 4031954
doi: 10.1101/cshperspect.a014241
Xie, Y. et al. Meta-Analysis of Arabidopsis KANADI1 Direct Target Genes Identifies a Basic Growth-Promoting Module Acting Upstream of Hormonal Signaling Pathways. Plant Physiol. 169, 1240–53 (2015).
pubmed: 26246448
pmcid: 4587460
doi: 10.1104/pp.15.00764
Jha, P. K., Vijay, A., Sahu, A. & Ashraf, M. Z. Comprehensive Gene expression meta-analysis and integrated bioinformatic approaches reveal shared signatures between thrombosis and myelo proliferative disorders. Sci. Rep. 6, 37099 (2016).
pubmed: 27892526
pmcid: 5125005
doi: 10.1038/srep37099
Guerrero-Martínez, J. A. & Reyes, J. C. High expression of SMARCA4 or SMARCA2 is frequently associated with an opposite prognosis in cancer. Sci. Rep. 8, 2043 (2018).
pubmed: 29391527
pmcid: 5794756
doi: 10.1038/s41598-018-20217-3
Shu, W., Chen, H., Bo, X. & Wang, S. Genome-wide analysis of the relationships between DNaseI HS, histone modifications and gene expression reveals distinct modes of chromatin domains. Nucleic Acids Res. 39, 7428–7443 (2011).
pubmed: 21685456
pmcid: 3177195
doi: 10.1093/nar/gkr443
Nagl, N. G. Jr, Zweitzig, D. R., Thimmapaya, B., Beck, G. R. Jr & Moran, E. The c-myc gene is a direct target of mammalian SWI/SNF-related complexes during differentiation associated cell cycle arrest. Cancer Res. 66, 1289–93 (2006).
pubmed: 16452181
doi: 10.1158/0008-5472.CAN-05-3427
pmcid: 16452181
Shi, J. et al. Role of SWI/SNF in acute leukemia maintenance and enhancer mediated Myc regulation. Genes Dev. 27, 2648–62 (2013).
pubmed: 24285714
pmcid: 3877755
doi: 10.1101/gad.232710.113
Stojanova, A. et al. MYC interaction with the tumor suppressive SWI/SNF complex member INI1 regulates transcription and cellular transformation. Cell Cycle. 15, 1693–705 (2016).
pubmed: 27267444
pmcid: 4957596
doi: 10.1080/15384101.2016.1146836
Romero, O. A. et al. MAX inactivation in small cell lung cancer disrupts MYC-SWI/SNF programs and is synthetic lethal with BRG1. Cancer Discov. 4, 292–303 (2014).
pubmed: 24362264
doi: 10.1158/2159-8290.CD-13-0799
pmcid: 24362264
Allevato, M. et al. Sequence-specificDNAbinding by MYC/MAX to low-affinity non-E-box motifs. PLoS One. 12, e0180147 (2017).
pubmed: 28719624
pmcid: 5515408
doi: 10.1371/journal.pone.0180147
Hirsch, C. L. et al. Myc and SAGA rewire an alternative splicing network during early somatic cell reprogramming. Genes Dev. 29, 803–16 (2015).
pubmed: 25877919
pmcid: 4403257
doi: 10.1101/gad.255109.114
Jimenez, R. H. et al. Regulation of gene expression in hepatic cells by the mammalian Target of Rapamycin (mTOR). PLoS One. 5, e9084 (2010).
pubmed: 20140209
pmcid: 2816708
doi: 10.1371/journal.pone.0009084
Seitz, V. et al. Deep sequencing of MYC DNA-binding sites in Burkitt lymphoma. PLoS One. 6, e26837 (2011).
pubmed: 22102868
pmcid: 3213110
doi: 10.1371/journal.pone.0026837
Reymann, S. & Borlak, J. Transcription profiling of lung adenocarcinomas of c-myc-transgenic mice: identification of the c-myc regulatory gene network. BMC Syst. Biol. 22, 46 (2008).
doi: 10.1186/1752-0509-2-46
Hota, S. K. & Bruneau, B. G. ATP-dependent chromatin remodeling during mammalian development. Development. 143, 2882–2897 (2016).
pubmed: 27531948
pmcid: 5004879
doi: 10.1242/dev.128892
Casey, S.C., Baylot, V. & Felsher, D.W. The MYC oncogene is a global regulator of the immune response. Blood. 131 (2018).
Pal, S. et al. mSin3A/histone deacetylase 2- and PRMT5-containing Brg1 complex is involved in transcriptional repression of the Myc target gene cad. Mol. Cell Biol. 23, 7475–87 (2003).
pubmed: 14559996
pmcid: 207647
doi: 10.1128/MCB.23.21.7475-7487.2003
Pham, L. V. et al. Recruitment of the SWI/SNF Chromatin Remodeling Complex by NFATc1 in the Transcriptional Regulation of the C-MYC Oncogene in Aggressive B-Cell Lymphomas. Blood. 112, 3808 (2008).
doi: 10.1182/blood.V112.11.3808.3808
Gu, W., Cechova, K., Tassi, V. & Dalla-Favera, R. Opposite regulation of gene transcription and cell proliferation by c-Myc and Max. Proc. Natl. Acad. Sci. USA 90, 2935–9 (1993).
pubmed: 8385351
doi: 10.1073/pnas.90.7.2935
Liu, Y. et al. BRD7 expression and c-Myc activation forms a double negative feedback loop that controls the cell proliferation and tumor growth of nasopharyngeal carcinoma by targeting oncogenic miR-141. J. Exp. Clin. Cancer Res. 37, 64 (2018).
doi: 10.1158/0008-5472.CAN-17-0815
Tatarskiy, E. V., Georgiev, G. P. & Soshnikova, N. V. Oncogene c-MYC Controls the Expression of PHF10 Subunit of PBAF Chromatin Remodeling Complex in SW620 Cell Line. Dokl. Biochem. Biophys. 484, 66–68 (2019).
pubmed: 31012017
doi: 10.1134/S1607672919010204
pmcid: 31012017
Malynn, B. A. et al. N-myc can functionally replace c myc in murine development, cellular growth, and differentiation. Genes Dev. 14, 1390–9 (2000).
pubmed: 10837031
pmcid: 316670
Cappellen, D., Schlange, T., Bauer, M., Maurer, F. & Hynes, N. E. Novel c MYC target genes mediate differential effects on cell proliferation and migration. EMBO Rep. 8, 70–6 (2007).
pubmed: 17159920
doi: 10.1038/sj.embor.7400849
pmcid: 17159920
Ji, H. et al. Cell type independent MYC target genes reveal a primordial signature involved in biomas saccumulation. PLoS One. 6, e26057 (2011).
pubmed: 22039435
pmcid: 3198433
doi: 10.1371/journal.pone.0026057
Shain, A. H. & Pollack, J. R. The spectrum of SWI/SNF mutations, ubiquitous in human cancers. PLoS One. 8, e55119 (2013).
pubmed: 23355908
pmcid: 3552954
doi: 10.1371/journal.pone.0055119
Roberts, C. W. & Orkin, S. H. The SWI/SNF complex-chromatin and cancer. Nat. Rev. Cancer. 4, 133–42 (2004).
pubmed: 14964309
doi: 10.1038/nrc1273
pmcid: 14964309
Bouchard, C., Staller, P. & Eilers, M. Control of cell proliferation by Myc. Trends Cell Biol. 8, 202–6 (1998).
pubmed: 9695840
doi: 10.1016/S0962-8924(98)01251-3
pmcid: 9695840
Zhou, K. R. et al. ChIPBase v2.0: decoding transcriptional regulatory networks of non-coding RNAs and protein-coding genes from ChIP-seq data. Nucleic Acids Res. 45, D43–D50 (2017).
pubmed: 27924033
doi: 10.1093/nar/gkw965
pmcid: 27924033
Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–504 (2003).
pubmed: 14597658
pmcid: 403769
doi: 10.1101/gr.1239303
Kent, W. J. et al. The human genome browser at UCSC. Genome Res. 12, 996–1006 (2002).
pubmed: 12045153
pmcid: 12045153
doi: 10.1101/gr.229102
Bailey, T. L. et al. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res. 37, W202–W208 (2009).
pubmed: 19458158
pmcid: 2703892
doi: 10.1093/nar/gkp335
Zeng, J. & Li, G. TFmapper: A Tool for Searching Putative Factors Regulating Gene Expression Using ChIP-seq Data. Int. J. Biol. Sci. 14, 1724–1731 (2018).
pubmed: 30416387
pmcid: 6216026
doi: 10.7150/ijbs.28850
Robinson, J. T. et al. Integrative Genomics Viewer. Nat. Biotechnol. 29, 24–26 (2011).
pubmed: 21221095
pmcid: 3346182
doi: 10.1038/nbt.1754
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 26, 139–140 (2010).
pubmed: 19910308
pmcid: 19910308
doi: 10.1093/bioinformatics/btp616
R Core Team. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org/ (2013).