A probabilistic approach to learn chromatin architecture and accurate inference of the NF-κB/RelA regulatory network using ChIP-Seq

Nucleic Acids Research

Volumn 41, Issue 15, 2013, Pages 7240-7259

  Yang, Jun ^a   Mitra, Abhishek ^a   Dojer, Norbert ^b,c   Fu, Shuhua ^b   Rowicka, Maga ^a,b   Brasier, Allan R ^a,b  

^a University of Texas Medical Branch School of Medicine   (United States)

^b UNIVERSITY OF TEXAS MEDICAL BRANCH   (United States)

^c UNIVERSITY OF WARSAW   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; TRANSCRIPTION FACTOR RELA;

ACCURACY; ARTICLE; BINDING SITE; CELL ACTIVATION; CHROMATIN IMMUNOPRECIPITATION; CHROMATIN STRUCTURE; CONTROLLED STUDY; CPG ISLAND; GENE CONTROL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENE TARGETING; GENETIC ANALYSIS; HUMAN; HUMAN CELL; INTRON; LUNG ALVEOLUS EPITHELIUM; NEGATIVE FEEDBACK; NF KAPPA B GENE; PRIORITY JOURNAL; PROMOTER REGION; RELA GENE; SIGNAL TRANSDUCTION;

ALU ELEMENTS; BINDING SITES; CELL LINE, TUMOR; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMATIN IMMUNOPRECIPITATION; GENE REGULATORY NETWORKS; GENOME, HUMAN; HUMANS; MODELS, STATISTICAL; MOLECULAR SEQUENCE ANNOTATION; NF-KAPPA B; NUCLEOTIDE MOTIFS; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; SEQUENCE ANALYSIS, RNA; TRANSCRIPTION FACTOR RELA;

EID: 84883483703     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt493     Document Type: Article

References (52)

1. Harrow,J., Frankish,A., Gonzalez,J.M., Tapanari,E., Diekhans,M., Kokocinski,F., Aken,B.L., Barrell,D., Zadissa,A., Searle,S. et al. (2012) GENCODE: the reference human genome annotation for The ENCODE Project. Genome Res., 22, 1760-1774
2. Gerstein,M.B., Kundaje,A., Hariharan,M., Landt,S.G., Yan,K.K., Cheng,C., Mu,X.J., Khurana,E., Rozowsky,J., Alexander,R. et al. (2012) Architecture of the human regulatory network derived from ENCODE data. Nature, 489, 91-100
3. Zhang,Y., Liu,T., Eeckhoute,J., Johnson,D.S., Bernstein,D.E., Nusbaum,C., Myers,D.E., Brown,M., Li,W. and Liu,X.S. (2008) Model-based analysis of ChIP-Seq (MACS). Genome Biol., 9, R137
4. Boyer,L.A., Lee,T.I., Cole,M.F., Johnstone,S.E., Levine,S.S., Zucker,J.P., Guenther,M.G., Kumar,R.M., Murray,H.L., Jenner,R.G. et al. (2005) Core transcriptional regulatory circuitry in human embryonic stem cells. Cell, 122, 947-956
5. Hartman,S.E., Bertone,P., Nath,A.K., Royce,T.E., Gerstein,M., Weissman,S. and Snyder,M. (2005) Global changes in STAT target selection and transcription regulation upon interferon treatments. Genes Dev., 19, 2953-2968
6. Cheng,C., Min,R. and Gerstein,M. (2011) TIP: a probabilistic method for identifying transcription factor target genes from ChIP-seq binding profiles. Bioinformatics, 27, 3221-3227
7. Mercurio,F., DiDonato,J.A., Rosette,C. and Karin,M. (1993) p105 and p98 precursor proteins play an active role in NF-kBmediated signal transduction. Genes Dev., 7, 705-718
8. Beg,A.A. and Baldwin,A.S. Jr (1993) The I kappa B proteins: multifunctional regulators of Rel/NF-kappa B transcription factors. Genes Dev., 7, 2064-2070
9. Tian,B., Zhang,Y., Luxon,B.A., Garofalo,R.P., Casola,A., Sinha,M. and Brasier,A.R. (2002) Identification of NF-kappaBdependent gene networks in respiratory syncytial virus-infected cells. J. Virol., 76, 6800-6814
10. Tian,B., Nowak,D.E., Jamaluddin,M., Wang,S. and Brasier,A.R. (2005) Identification of direct genomic targets downstream of the nuclear factor-{kappa}b transcription factor mediating tumor necrosis factor signaling. J. Biol. Chem., 280, 17435-17448
11. Tian,B., Nowak,D.E. and Brasier,A.R. (2005) A TNF-induced gene expression program under oscillatory NF-kappaB control. BMC Genomics, 6, 137-154
12. Tian,B. and Brasier,A.R. (2005) Microarrays and Transcription Factor Networks. Landes Bioscience, Austin, TX, USA
13. Brasier,A.R. (2006) The NF-k B regulatory network. Cardiovasc. Toxicol., 6, 111-130
14. Nowak,D.E., Tian,B., Jamaluddin,M., Boldogh,I., Vergara,L.A., Choudhary,S. and Brasier,A.R. (2008) RelA Ser276 phosphorylation is required for activation of a subset of NF-{kappa}B-dependent genes by recruiting cyclin-dependent kinase 9/cyclin T1 complexes. Mol. Cell. Biol., 28, 3623-3638
15. Maniatis,T. (1997) Catalysis by a multiprotein IkB kinase complex. Science, 278, 818-819
16. Han,Y., Weinman,S., Boldogh,I., Walker,R.K. and Brasier,A.R. (1999) Tumor necrosis factor-alpha-inducible IkappaBalpha proteolysis mediated by cytosolic m-calpain. A mechanism parallel to the ubiquitin-proteasome pathway for nuclear factor-kappab activation. J. Biol. Chem., 274, 787-794
17. Jamaluddin,M., Wang,S., Boldogh,I., Tian,B. and Brasier,A.R. (2007) TNF-a-induced NF-kB/Rel A Ser 276 phosphorylation and enhanceosome formation on the IL-8 promoter is mediated by a reactive oxygen species (ROS)-dependent pathway. Cell. Signal., 9, 1419-1433
18. Zhong,H., Voll,R.E. and Ghosh,S. (1998) Phosphorylation of NFkB p65 by PKA stimulates transcriptional activity by promoting a novel bivalent interaction with the coactivator CBP/p300. Mol. Cell, 1, 661-671
19. Kunsch,C., Ruben,S.M. and Rosen,C.A. (1992) Selection of optimal kB/Rel DNA-binding motifs: interaction of both subunits of NF-kB with DNA is required for transcriptional activation. Mol. Cell. Biol., 12, 4412-4421
20. Shikama,N., Lyon,J. and LaThangue,N.B. (1997) The p300/CBP family: integrating signals with transcription factors and chromatin. Trends Cell Biol., 7, 230-236
21. Sheppard,K.A., Phelps,K.M., Williams,A.M., Thanos,D., Glass,C.K., Rosenfeld,M.G., Gerritsen,M.E. and Collins,T. (1998) Nuclear integration of glucocorticoid receptor and nuclear factorkB singlaing by CREB binding protein and steroid receptor coactivator-1. J. Biol. Chem., 273, 29291-29294
22. Huang,B., Yang,X.D., Zhou,M.M., Ozato,K. and Chen,L.F. (2009) Brd4 Coactivates Transcriptional activation of NF-{kappa}B via specific binding to acetylated RelA. Mol. Cell. Biol., 29, 1375-1387
23. Casola,A., Garofalo,R., Jamaluddin,M., Vlahopoulos,S. and Brasier,A.R. (2000) Requirement of a novel upstream response element in respiratory syncytial virus-induced IL-8 gene expression. J. Immunol., 164, 5944-5951
24. Vlahopoulos,S., Boldogh,I. and Brasier,A.R. (1999) NF-k B dependent induction of interleukin-8 gene expression by tumor necrosis factor a : evidence for an antioxidant sensitive activating pathway distinct from nuclear translocation. Blood, 94, 1878-1889
25. Robertson,G., Hirst,M., Bainbridge,M., Bilenky,M., Zhao,Y., Zeng,T., Euskirchen,G., Bernier,B., Varhol,R., Delaney,A. et al. (2007) Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing. Nat. Methods, 4, 651-657
26. Johnson,D.S., Mortazavi,A., Myers,R.M. and Wold,B. (2007) Genome-wide mapping of in vivo protein-DNA interactions. Science, 316, 1497-1502
27. Rao,N.A., McCalman,M.T., Moulos,P., Francoijs,K.J., Chatziioannou,A., Kolisis,F.N., Alexis,M.N., Mitsiou,D.J. and Stunnenberg,H.G. (2011) Coactivation of GR and NFKB alters the repertoire of their binding sites and target genes. Genome Res., 21, 1404-1416
28. Nowak,D.E., Tian,B. and Brasier,A.R. (2005) Two-step crosslinking method for Identification of NF-k B gene network by chromatin immunoprecipitation. Biotechniques, 39, 715-725
29. Tian,B., Yang,J. and Brasier,A.R. (2012) Two-step cross-linking for analysis of protein-chromatin interactions. Methods Mol. Biol., 809, 105-120
30. Waldminhaus,T. and Skarstad,K. (2010) ChIP on Chip: surprising results are often artifacts. BMC Genomics, 11, 414
31. Langmead,B., Trapnell,C., Pop,M. and Salzberg,S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25
32. Fujita,P.A., Rhead,B., Zweig,A.S., Hinrichs,A.S., Karolchik,D., Cline,M.S., Goldman,M., Barber,G.P., Clawson,H., Coelho,A. et al. (2011) The UCSC genome browser database: update 2011. Nucleic Acids Res., 39, D876-D882
33. Smit, A., Hubley, R. and Green, P. RepeatMaster Open-3.0 (1996-2010), http://www.repeatmasker.org
34. Trapnell,C., Pachter,L. and Salzberg,S.L. (2009) TopHat: discovering splice junctions with RNA-Seq. Bioinformatics, 25, 1105-1111
35. Bosisio,D., Marazzi,I., Agresti,A., Shimizu,N., Bianchi,M.E. and Natoli,G. (2006) A hyper-dynamic equilibrium between promoterbound and nucleoplasmic dimers controls NF-kappaB-dependent gene activity. EMBO J., 25, 798-810
36. Reid,J.E., Evans,K.J., Dyer,N., Wernisch,L. and Ott,S. (2010) Variable structure motifs for transcription factor binding sites. BMC Genomics, 11, 30
37. Vlahovicek,K., Kaja,L. and Pongor,S. (2011) In: Moss,D.S., Jelaska,S. and Pongor,S. (eds), Essays in Bioinformatics, Vol 368 NATO Science Series: Life and Behavioural Sciences
38. Antonaki,A., Demetriades,C., Polyzos,A., Banos,A., Vatsellas,G., Lavigne,M.D., Apostolou,E., Mantouvalou,E., Papadopoulou,D., Mosialos,G. et al. (2011) Genomic analysis reveals a novel nuclear factor-kB (NF-kB)-binding site in alu-repetitive elements. J. Biol. Chem., 286, 38768-38782
39. Norris,J.L. and Baldwin,A.S. (1999) Oncogenic Ras enhances NF-kB transcriptional activity through raf-dependent and raf-independent mitogen-activated protein kinase signaling pathways. J. Biol. Chem., 274, 13841-13846
40. Schubbert,S., Shannon,K. and Bollag,G. (2007) Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer, 7, 295-308
41. Kalita,M.K., Sargsyan,K., Tian,B., Paulucci-Holthauzen,A., Najm,H.N., Debusschere,B.J. and Brasier,A.R. (2011) Sources of cell-to-cell variability in canonical nuclear factor-kappaB (NFkappaB) signaling pathway inferred from single cell dynamic images. J. Biol. Chem., 286, 37741-37757
42. Mengshol,J.A., Vincenti,M.P., Coon,C.I., Barchowsky,A. and Brinckerhoff,C.E. (2000) Interleukin-1 induction of collagenase 3 (matrix metalloproteinase 13) gene expression in chondrocytes requires p38, c-jun N-terminal kinase, and nuclear factor kB: differential regulation of collagenase 1 and collagenase 3. Arthritis Rheum., 43, 801-811
43. Brasier,A.R., Jamaluddin,M., Casola,A., Duan,W., Shen,Q. and Garofalo,R.P. (1998) A promoter recruitment mechanism for tumor necrosis factor-alpha-induced interleukin-8 transcription in type II pulmonary epithelial cells. Dependence on nuclear abundance of Rel A, NF-kappaB1, and c-Rel transcription factors. J. Biol. Chem., 273, 3551-3561
44. Casola,A., Garofalo,R.P., Jamaluddin,M., Vlahopoulos,S. and Brasier,A.R. (2000) Requirement of a novel upstream response element in respiratory syncytial virus-induced IL-8 gene expression. J. Immunol., 164, 5944-5951
45. Shyu,Y.J., Suarez,C.D. and Hu,C.D. (2008) Visualization of AP-1-NF-kB ternary complexes in living cells by using a BiFC-based FRET. Proc. Natl Acad. Sci. USA, 105, 151-156
46. Perkins,N.D., Edwards,N.L., Duckett,C.S., Agranoff,A.B., Schmid,R.M. and Nabel,G.J. (1993) A cooperative interaction between NF-kappa B and Sp1 is required for HIV-1 enhancer activation. EMBO J., 12, 3551-3558
47. Brasier,A.R., Tian,B., Jamaluddin,M., Kalita,M.K., Garofalo,R.P. and Lu,M. (2011) RelA Ser276 phosphorylation-coupled Lys310 acetylation controls transcriptional elongation of inflammatory cytokines in respiratory syncytial virus infection. J. Virol., 85, 11752-11769
48. Brasier,A.R. (2008) Expanding role of cyclin dependent kinases in cytokine inducible gene expression. Cell Cycle, 7, 1-6
49. Ainbinder,E., Amir-Zilberstein,L., Yamaguchi,Y., Handa,H. and Dikstein,R. (2004) Elongation inhibition by DRB sensitivity-inducing factor is regulated by the A20 promoter via a novel negative element and NF-kappaB. Mol. Cell. Biol., 24, 2444-2454
50. Brasier,A.R., Tian,B., Jamaluddin,M. and Lu,M. (2011) RelA Ser 276 phosphorylation-coupled lys 310 acetylation controls transcriptional elongation of inflammatory cytokines in RSV infection. J. Virol., 85, 11752-11769
51. Natoli,G., Saccani,S., Bosisio,D. and Marazzi,I. (2005) Interactions of NF-[kappa]B with chromatin: the art of being at the right place at the right time. Nat. Immunol., 6, 439-445
52. Zhang,W., Wang,J., Zhang,Y., Yuan,Y., Guan,W., Jin,C., Chen,H., Wang,X., Yang,X. and He,F. (2010) The sscaffold protein TANK/I-TRAF inhibits NF-kB activation by recruiting polo-like kinase 1. Mol. Biol. Cell, 21, 2500-2513.