Nucleosome positioning and histone modifications define relationships between regulatory elements and nearby gene expression in breast epithelial cells

BMC Genomics

Volumn 15, Issue 1, 2014, Pages

  Rhie, Suhn K ^a,b   Hazelett, Dennis J ^a,b   Coetzee, Simon G ^a,b,c   Yan, Chunli ^a,b   Noushmehr, Houtan ^a,b,c   Coetzee, Gerhard A ^a,b  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Breast epithelial cells; Enhancers; Epigenetics; Genes; Nucleosomes; Promoters; Transcription factors

Indexed keywords

ARTICLE; BREAST EPITHELIUM; CELL ADHESION; CELL CYCLE; CELL MATURATION; CELL SELECTION; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME POSITIONING; CONTROLLED STUDY; DNA REPLICATION; ENHANCER REGION; GENE EXPRESSION; GENE INTERACTION; GENE LOCATION; GENE SEQUENCE; GENETIC REGULATION; HISTONE MODIFICATION; HUMAN; HUMAN CELL; MITOSIS; NUCLEOSOME; NUCLEOSOME POSITIONING; NUCLEOTIDE SEQUENCE; PHENOTYPE; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN MOTIF; FEMALE; MAMMARY GLAND; METABOLISM; PATHOLOGY; REGULATORY SEQUENCE; TUMOR CELL LINE;

HISTONE; NUCLEOSOME; TRANSCRIPTION FACTOR;

CELL LINE, TUMOR; FEMALE; HISTONES; HUMANS; MAMMARY GLANDS, HUMAN; NUCLEOSOMES; REGULATORY SEQUENCES, NUCLEIC ACID; TRANSCRIPTION FACTORS;

EID: 84900391269     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-15-331     Document Type: Article

References (89)

1. Collins FS, Green ED, Guttmacher AE, Guyer MS. A vision for the future of genomics research. Nature 2003, 422:835-847. 10.1038/nature01626, 12695777.
2. Huisinga KL, Brower-Toland B, Elgin SC. The contradictory definitions of heterochromatin: transcription and silencing. Chromosoma 2006, 115:110-122. 10.1007/s00412-006-0052-x, 16506022.
3. Grewal SI, Jia S. Heterochromatin revisited. Nat Rev Genet 2007, 8:35-46. 10.1038/nrg2008, 17173056.
4. Ong CT, Corces VG. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nat Rev Genet 2011, 12:283-293. 3175006, 21358745.
5. Heintzman ND, Stuart RK, Hon G, Fu Y, Ching CW, Hawkins RD, Barrera LO, Van Calcar S, Qu C, Ching KA, Wang W, Green RD, Crawford GE, Ren B. Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet 2007, 39:311-318. 10.1038/ng1966, 17277777.
6. Wang Z, Zang C, Rosenfeld JA, Schones DE, Barski A, Cuddapah S, Cui K, Roh TY, Peng W, Zhang MQ, Zhao K. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat Genet 2008, 40:897-903. 10.1038/ng.154, 2769248, 18552846.
7. Song L, Zhang Z, Grasfeder LL, Boyle AP, Giresi PG, Lee BK, Sheffield NC, Graf S, Huss M, Keefe D, Liu Z, London D, McDaniell RM, Shibata Y, Showers KA, Simon JM, Vales T, Wang T, Winter D, Zhang Z, Clarke ND, Birney E, Iyer VR, Crawford GE, Lieb JD, Furey TS. Open chromatin defined by DNaseI and FAIRE identifies regulatory elements that shape cell-type identity. Genome Res 2011, 21:1757-1767. 10.1101/gr.121541.111, 3202292, 21750106.
8. Zhu J, Adli M, Zou JY, Verstappen G, Coyne M, Zhang X, Durham T, Miri M, Deshpande V, De Jager PL, Bennett DA, Houmard JA, Muoio DM, Onder TT, Camahort R, Cowan CA, Meissner A, Epstein CB, Shoresh N, Bernstein BE. Genome-wide Chromatin State Transitions Associated with Developmental and Environmental Cues. Cell 2013, 152:642-654. 10.1016/j.cell.2012.12.033, 3563935, 23333102.
9. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest 2011, 121:2750-2767. 10.1172/JCI45014, 3127435, 21633166.
10. Zhao X, Malhotra GK, Lele SM, Lele MS, West WW, Eudy JD, Band H, Band V. Telomerase-immortalized human mammary stem/progenitor cells with ability to self-renew and differentiate. Proc Natl Acad Sci U S A 2010, 107:14146-14151. 10.1073/pnas.1009030107, 2922525, 20660721.
11. Rochefort H, Glondu M, Sahla ME, Platet N, Garcia M. How to target estrogen receptor-negative breast cancer?. Endocr Relat Cancer 2003, 10:261-266. 10.1677/erc.0.0100261, 12790787.
12. Ostrander JH, McMahon CM, Lem S, Millon SR, Brown JQ, Seewaldt VL, Ramanujam N. Optical redox ratio differentiates breast cancer cell lines based on estrogen receptor status. Cancer Res 2010, 70:4759-4766. 10.1158/0008-5472.CAN-09-2572, 3826951, 20460512.
13. Prat A, Perou CM. Mammary development meets cancer genomics. Nat Med 2009, 15:842-844. 10.1038/nm0809-842, 19661985.
14. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, Campbell LL, Polyak K, Brisken C, Yang J, Weinberg RA. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133:704-715. 10.1016/j.cell.2008.03.027, 2728032, 18485877.
15. Morel AP, Lievre M, Thomas C, Hinkal G, Ansieau S, Puisieux A. Generation of breast cancer stem cells through epithelial-mesenchymal transition. PLoS One 2008, 3:e2888. 10.1371/journal.pone.0002888, 2492808, 18682804.
16. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9:265-273. 10.1038/nrc2620, 19262571.
17. Ye Y, Xiao Y, Wang W, Yearsley K, Gao JX, Shetuni B, Barsky SH. ERalpha signaling through slug regulates E-cadherin and EMT. Oncogene 2010, 29:1451-1462. 10.1038/onc.2009.433, 20101232.
18. He HH, Meyer CA, Chen MW, Jordan VC, Brown M, Liu XS. Differential DNase I hypersensitivity reveals factor-dependent chromatin dynamics. Genome Res 2012, 22:1015-1025. 10.1101/gr.133280.111, 3371710, 22508765.
19. Hah N, Murakami S, Nagari A, Danko CG, Kraus WL. Enhancer transcripts mark active estrogen receptor binding sites. Genome Res 2013, 23:1210-1223. 10.1101/gr.152306.112, 3730096, 23636943.
20. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 2010, 38:576-589. 10.1016/j.molcel.2010.05.004, 2898526, 20513432.
21. Ernst J, Kheradpour P, Mikkelsen TS, Shoresh N, Ward LD, Epstein CB, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein BE. Mapping and analysis of chromatin state dynamics in nine human cell types. Nature 2011, 473:43-49. 10.1038/nature09906, 3088773, 21441907.
22. Takeichi M. Cadherins in cancer: implications for invasion and metastasis. Curr Opin Cell Biol 1993, 5:806-811. 10.1016/0955-0674(93)90029-P, 8240824.
23. Tang A, Amagai M, Granger LG, Stanley JR, Udey MC. Adhesion of epidermal Langerhans cells to keratinocytes mediated by E-cadherin. Nature 1993, 361:82-85. 10.1038/361082a0, 8421498.
24. Berx G, Cleton-Jansen AM, Nollet F, de Leeuw WJ, van de Vijver M, Cornelisse C, van Roy F. E-cadherin is a tumour/invasion suppressor gene mutated in human lobular breast cancers. EMBO J 1995, 14:6107-6115. 394735, 8557030.
25. Shimoyama Y, Hirohashi S. Expression of E- and P-cadherin in gastric carcinomas. Cancer Res 1991, 51:2185-2192.
26. Palacios J, Benito N, Pizarro A, Suarez A, Espada J, Cano A, Gamallo C. Anomalous expression of P-cadherin in breast carcinoma. Correlation with E-cadherin expression and pathological features. Am J Pathol 1995, 146:605-612. 1869170, 7534041.
27. Rasbridge SA, Gillett CE, Sampson SA, Walsh FS, Millis RR. Epithelial (E-) and placental (P-) cadherin cell adhesion molecule expression in breast carcinoma. J Pathol 1993, 169:245-250. 10.1002/path.1711690211, 8383197.
28. Paredes J, Correia AL, Ribeiro AS, Albergaria A, Milanezi F, Schmitt FC. P-cadherin expression in breast cancer: a review. Breast Cancer Res 2007, 9:214. 10.1186/bcr1774, 2242663, 18001487.
29. Bragdon B, Moseychuk O, Saldanha S, King D, Julian J, Nohe A. Bone morphogenetic proteins: a critical review. Cell Signal 2011, 23:609-620. 10.1016/j.cellsig.2010.10.003, 20959140.
30. Guo D, Huang J, Gong J. Bone morphogenetic protein 4 (BMP4) is required for migration and invasion of breast cancer. Mol Cell Biochem 2012, 363:179-190. 10.1007/s11010-011-1170-1, 22167620.
31. Cho KW, Kim JY, Song SJ, Farrell E, Eblaghie MC, Kim HJ, Tickle C, Jung HS. Molecular interactions between Tbx3 and Bmp4 and a model for dorsoventral positioning of mammary gland development. Proc Natl Acad Sci U S A 2006, 103:16788-16793. 10.1073/pnas.0604645103, 1636533, 17071745.
32. Malin J, Aniba MR, Hannenhalli S. Enhancer networks revealed by correlated DNAse hypersensitivity states of enhancers. Nucleic Acids Res 2013, 41(14):6828-6838. 10.1093/nar/gkt374, 3737527, 23700312.
33. D'Amato NC, Ostrander JH, Bowie ML, Sistrunk C, Borowsky A, Cardiff RD, Bell K, Young LJ, Simin K, Bachelder RE, Delrow J, Dawson A, Yee LD, Mrózek K, Clay TM, Osada T, Seewaldt VL. Evidence for phenotypic plasticity in aggressive triple-negative breast cancer: human biology is recapitulated by a novel model system. PLoS One 2012, 7:e45684. 10.1371/journal.pone.0045684, 3458110, 23049838.
34. Chepelev I, Wei G, Wangsa D, Tang Q, Zhao K. Characterization of genome-wide enhancer-promoter interactions reveals co-expression of interacting genes and modes of higher order chromatin organization. Cell Res 2012, 22:490-503. 10.1038/cr.2012.15, 3292289, 22270183.
35. Sheffield NC, Thurman RE, Song L, Safi A, Stamatoyannopoulos JA, Lenhard B, Crawford GE, Furey TS. Patterns of regulatory activity across diverse human cell types predict tissue identity, transcription factor binding, and long-range interactions. Genome Res 2013, 23:777-788. 10.1101/gr.152140.112, 3638134, 23482648.
36. Zentner GE, Scacheri PC. The chromatin fingerprint of gene enhancer elements. J Biol Chem 2012, 287:30888-30896. 10.1074/jbc.R111.296491, 3438921, 22952241.
37. Creyghton MP, Cheng AW, Welstead GG, Kooistra T, Carey BW, Steine EJ, Hanna J, Lodato MA, Frampton GM, Sharp PA, Boyer LA, Young RA, Jaenisch R. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc Natl Acad Sci U S A 2010, 107:21931-21936. 10.1073/pnas.1016071107, 3003124, 21106759.
38. Taberlay PC, Kelly TK, Liu CC, You JS, De Carvalho DD, Miranda TB, Zhou XJ, Liang G, Jones PA. Polycomb-repressed genes have permissive enhancers that initiate reprogramming. Cell 2011, 147:1283-1294. 10.1016/j.cell.2011.10.040, 3240866, 22153073.
39. Zhang B, Day DS, Ho JW, Song L, Cao J, Christodoulou D, Seidman JG, Crawford GE, Park PJ, Pu WT. A dynamic H3K27ac signature identifies VEGFA-stimulated endothelial enhancers and requires EP300 activity. Genome Res 2013, 23(6):917-927. 10.1101/gr.149674.112, 3668360, 23547170.
40. Ye T, Krebs AR, Choukrallah MA, Keime C, Plewniak F, Davidson I, Tora L. seqMINER: an integrated ChIP-seq data interpretation platform. Nucleic Acids Res 2011, 39:e35. 10.1093/nar/gkq1287, 3064796, 21177645.
41. Hogan GJ, Lee CK, Lieb JD. Cell cycle-specified fluctuation of nucleosome occupancy at gene promoters. PLoS Genet 2006, 2:e158. 10.1371/journal.pgen.0020158, 1570381, 17002501.
42. Giresi PG, Kim J, McDaniell RM, Iyer VR, Lieb JD. FAIRE (Formaldehyde-Assisted Isolation of Regulatory Elements) isolates active regulatory elements from human chromatin. Genome Res 2007, 17:877-885. 10.1101/gr.5533506, 1891346, 17179217.
43. Arnold CD, Gerlach D, Stelzer C, Boryn LM, Rath M, Stark A. Genome-wide quantitative enhancer activity maps identified by STARR-seq. Science 2013, 339:1074-1077. 10.1126/science.1232542, 23328393.
44. Simon JM, Hacker KE, Singh D, Brannon AR, Parker JS, Weiser M, Ho TH, Kuan PF, Jonasch E, Furey TS, Prins JF, Lieb JD, Rathmell WK, Davis IJ. Variation in chromatin accessibility in human kidney cancer links H3K36 methyltransferase loss with widespread RNA processing defects. Genome Res 2014, 24(2):241-250. 10.1101/gr.158253.113, 24158655.
45. Rhie SK, Coetzee SG, Noushmehr H, Yan C, Kim JM, Haiman CA, Coetzee GA. Comprehensive functional annotation of seventy-one breast cancer risk Loci. PLoS One 2013, 8:e63925. 10.1371/journal.pone.0063925, 3661550, 23717510.
46. Neph S, Vierstra J, Stergachis AB, Reynolds AP, Haugen E, Vernot B, Thurman RE, John S, Sandstrom R, Johnson AK, Maurano MT, Humbert R, Rynes E, Wang H, Vong S, Lee K, Bates D, Diegel M, Roach V, Dunn D, Neri J, Schafer A, Hansen RS, Kutyavin T, Giste E, Weaver M, Canfield T, Sabo P, Zhang M, Balasundaram G. An expansive human regulatory lexicon encoded in transcription factor footprints. Nature 2012, 489:83-90. 10.1038/nature11212, 3736582, 22955618.
47. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, Valen E, Yusuf D, Lenhard B, Wasserman WW, Sandelin A. JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 2010, 38:D105-D110. 10.1093/nar/gkp950, 2808906, 19906716.
48. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, Reuter I, Chekmenev D, Krull M, Hornischer K, Voss N, Stegmaier P, Lewicki-Potapov B, Saxel H, Kel AE, Wingender E. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 2006, 34:D108-D110. 10.1093/nar/gkj143, 1347505, 16381825.
49. De Rosa L, Antonini D, Ferone G, Russo MT, Yu PB, Han R, Missero C. p63 Suppresses non-epidermal lineage markers in a bone morphogenetic protein-dependent manner via repression of Smad7. J Biol Chem 2009, 284:30574-30582. 10.1074/jbc.M109.049619, 2781612, 19717565.
50. Terrinoni A, Serra V, Bruno E, Strasser A, Valente E, Flores ER, van Bokhoven H, Lu X, Knight RA, Melino G. Role of p63 and the Notch pathway in cochlea development and sensorineural deafness. Proc Natl Acad Sci U S A 2013, 110:7300-7305. 10.1073/pnas.1214498110, 3645580, 23589895.
51. Westfall MD, Pietenpol JA. p63: Molecular complexity in development and cancer. Carcinogenesis 2004, 25:857-864. 10.1093/carcin/bgh148, 15033906.
52. Flores ER. The roles of p63 in cancer. Cell Cycle 2007, 6:300-304. 10.4161/cc.6.3.3793, 17264676.
53. Wang X, Mori I, Tang W, Nakamura M, Nakamura Y, Sato M, Sakurai T, Kakudo K. p63 expression in normal, hyperplastic and malignant breast tissues. Breast Cancer 2002, 9:216-219. 10.1007/BF02967592, 12185332.
54. Peter AK, Ko CY, Kim MH, Hsu N, Ouchi N, Rhie S, Izumiya Y, Zeng L, Walsh K, Crosbie RH. Myogenic Akt signaling upregulates the utrophin-glycoprotein complex and promotes sarcolemma stability in muscular dystrophy. Hum Mol Genet 2009, 18:318-327. 2638781, 18986978.
55. Yang A, Kaghad M, Wang Y, Gillett E, Fleming MD, Dotsch V, Andrews NC, Caput D, McKeon F. p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities. Mol Cell 1998, 2:305-316. 10.1016/S1097-2765(00)80275-0, 9774969.
56. Zaret KS, Carroll JS. Pioneer transcription factors: establishing competence for gene expression. Genes Dev 2011, 25:2227-2241. 10.1101/gad.176826.111, 3219227, 22056668.
57. Yang A, Zhu Z, Kapranov P, McKeon F, Church GM, Gingeras TR, Struhl K. Relationships between p63 binding, DNA sequence, transcription activity, and biological function in human cells. Mol Cell 2006, 24:593-602. 10.1016/j.molcel.2006.10.018, 17188034.
58. Huntley RP, Binns D, Dimmer E, Barrell D, O'Donovan C, Apweiler R. QuickGO: a user tutorial for the web-based Gene Ontology browser. Database (Oxford) 2009, 2009:bap010. 2794795, 20157483.
59. Sathyanarayana UG, Padar A, Huang CX, Suzuki M, Shigematsu H, Bekele BN, Gazdar AF. Aberrant promoter methylation and silencing of laminin-5-encoding genes in breast carcinoma. Clin Cancer Res 2003, 9:6389-6394.
60. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JE, Liu ET, Bergh J, Kuznetsov VA, Miller LD. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 2006, 66:10292-10301. 10.1158/0008-5472.CAN-05-4414, 17079448.
61. Hutchins JR, Toyoda Y, Hegemann B, Poser I, Heriche JK, Sykora MM, Augsburg M, Hudecz O, Buschhorn BA, Bulkescher J, Conrad C, Comartin D, Schleiffer A, Sarov M, Pozniakovsky A, Slabicki MM, Schloissnig S, Steinmacher I, Leuschner M, Ssykor A, Lawo S, Pelletier L, Stark H, Nasmyth K, Ellenberg J, Durbin R, Buchholz F, Mechtler K, Hyman AA, Peters JM. Systematic analysis of human protein complexes identifies chromosome segregation proteins. Science 2010, 328:593-599. 10.1126/science.1181348, 2989461, 20360068.
62. Chan GK, Jablonski SA, Sudakin V, Hittle JC, Yen TJ. Human BUBR1 is a mitotic checkpoint kinase that monitors CENP-E functions at kinetochores and binds the cyclosome/APC. J Cell Biol 1999, 146:941-954. 10.1083/jcb.146.5.941, 2169490, 10477750.
63. Cahill DP, Lengauer C, Yu J, Riggins GJ, Willson JK, Markowitz SD, Kinzler KW, Vogelstein B. Mutations of mitotic checkpoint genes in human cancers. Nature 1998, 392:300-303. 10.1038/32688, 9521327.
64. Myrie KA, Percy MJ, Azim JN, Neeley CK, Petty EM. Mutation and expression analysis of human BUB1 and BUB1B in aneuploid breast cancer cell lines. Cancer Lett 2000, 152:193-199. 10.1016/S0304-3835(00)00340-2, 10773412.
65. Ha GH, Baek KH, Kim HS, Jeong SJ, Kim CM, McKeon F, Lee CW. p53 activation in response to mitotic spindle damage requires signaling via BubR1-mediated phosphorylation. Cancer Res 2007, 67:7155-7164. 10.1158/0008-5472.CAN-06-3392, 17671183.
66. Ecker JR, Bickmore WA, Barroso I, Pritchard JK, Gilad Y, Segal E. Genomics: ENCODE explained. Nature 2012, 489:52-55. 10.1038/489052a, 22955614.
67. Eskiw CH, Cope NF, Clay I, Schoenfelder S, Nagano T, Fraser P. Transcription factories and nuclear organization of the genome. Cold Spring Harb Symp Quant Biol 2010, 75:501-506. 10.1101/sqb.2010.75.046, 21467135.
68. Bantignies F, Cavalli G. Polycomb group proteins: repression in 3D. Trends Genet 2011, 27:454-464. 10.1016/j.tig.2011.06.008, 21794944.
69. Peric-Hupkes D, van Steensel B. Role of the nuclear lamina in genome organization and gene expression. Cold Spring Harb Symp Quant Biol 2010, 75:517-524. 10.1101/sqb.2010.75.014, 21209388.
70. Lieberman-Aiden E, van Berkum NL, Williams L, Imakaev M, Ragoczy T, Telling A, Amit I, Lajoie BR, Sabo PJ, Dorschner MO, Sandstrom R, Bernstein B, Bender MA, Groudine M, Gnirke A, Stamatoyannopoulos J, Mirny LA, Lander ES, Dekker J. Comprehensive mapping of long-range interactions reveals folding principles of the human genome. Science 2009, 326:289-293. 10.1126/science.1181369, 2858594, 19815776.
71. van Berkum NL, Lieberman-Aiden E, Williams L, Imakaev M, Gnirke A, Mirny LA, Dekker J, Lander ES. Hi-C: a method to study the three-dimensional architecture of genomes. JoVE 2010, 39. http://www.jove.com/details.php?id=1869, doi: 10.3791/1869.
72. Li G, Ruan X, Auerbach RK, Sandhu KS, Zheng M, Wang P, Poh HM, Goh Y, Lim J, Zhang J, Sim HS, Peh SQ, Mulawadi FH, Ong CT, Orlov YL, Hong S, Zhang Z, Landt S, Raha D, Euskirchen G, Wei CL, Ge W, Wang H, Davis C, Fisher-Aylor KI, Mortazavi A, Gerstein M, Gingeras T, Wold B, Sun Y. Extensive promoter-centered chromatin interactions provide a topological basis for transcription regulation. Cell 2012, 148:84-98. 10.1016/j.cell.2011.12.014, 3339270, 22265404.
73. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug Ii RG, Tan W, Penheiter SG, Ma AC, Leung AY, Fahrenkrug SC, Carlson DF, Voytas DF, Clark KJ, Essner JJ, Ekker SC. In vivo genome editing using a high-efficiency TALEN system. Nature 2012, 491(7422):114-118. 10.1038/nature11537, 3491146, 23000899.
74. Ting MC, Liao CP, Yan C, Jia L, Groshen S, Frenkel B, Roy-Burman P, Coetzee GA, Maxson R. An enhancer from the 8q24 prostate cancer risk region is sufficient to direct reporter gene expression to a subset of prostate stem-like epithelial cells in transgenic mice. Dis Model Mech 2012, 5:366-374. 10.1242/dmm.008458, 3339830, 22279083.
75. Kalhor R, Tjong H, Jayathilaka N, Alber F, Chen L. Genome architectures revealed by tethered chromosome conformation capture and population-based modeling. Nat Biotechnol 2012, 30:90-98.
76. Dekker J. The three 'C' s of chromosome conformation capture: controls, controls, controls. Nat Methods 2006, 3:17-21. 10.1038/nmeth823, 16369547.
77. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Varambally R, Yu J, Briggs BB, Barrette TR, Anstet MJ, Kincead-Beal C, Kulkarni P, Varambally S, Ghosh D, Chinnaiyan AM. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles. Neoplasia 2007, 9:166-180. 10.1593/neo.07112, 1813932, 17356713.
78. Cancer Genome Atlas Network Comprehensive molecular portraits of human breast tumours. Nature 2012, 490:61-70. 10.1038/nature11412, 3465532, 23000897, Cancer Genome Atlas Network.
79. Curtis C, Shah SP, Chin SF, Turashvili G, Rueda OM, Dunning MJ, Speed D, Lynch AG, Samarajiwa S, Yuan Y, Gräf S, Ha G, Haffari G, Bashashati A, Russell R, McKinney S, Langerød A, Green A, Provenzano E, Wishart G, Pinder S, Watson P, Markowetz F, Murphy L, Ellis I, Purushotham A, Børresen-Dale AL, Brenton JD, Tavaré S, . METABRIC Group The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012, 486:346-352. 3440846, 22522925, METABRIC Group.
80. Christopher SA, Diegelman P, Porter CW, Kruger WD. Methylthioadenosine phosphorylase, a gene frequently codeleted with p16(cdkN2a/ARF), acts as a tumor suppressor in a breast cancer cell line. Cancer Res 2002, 62:6639-6644.
81. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079. 10.1093/bioinformatics/btp352, 2723002, 19505943.
82. Fejes AP, Robertson G, Bilenky M, Varhol R, Bainbridge M, Jones SJ. FindPeaks 3.1: a tool for identifying areas of enrichment from massively parallel short-read sequencing technology. Bioinformatics 2008, 24:1729-1730. 10.1093/bioinformatics/btn305, 2638869, 18599518.
83. Jia L, Landan G, Pomerantz M, Jaschek R, Herman P, Reich D, Yan C, Khalid O, Kantoff P, Oh W, Manak JR, Berman BP, Henderson BE, Frenkel B, Haiman CA, Freedman M, Tanay A, Coetzee GA. Functional enhancers at the gene-poor 8q24 cancer-linked locus. PLoS Genet 2009, 5:e1000597. 10.1371/journal.pgen.1000597, 2717370, 19680443.
84. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008, 9:R137. 10.1186/gb-2008-9-9-r137, 2592715, 18798982.
85. Guttman M, Garber M, Levin JZ, Donaghey J, Robinson J, Adiconis X, Fan L, Koziol MJ, Gnirke A, Nusbaum C, Rinn JL, Lander ES, Regev A. Ab initio reconstruction of cell type-specific transcriptomes in mouse reveals the conserved multi-exonic structure of lincRNAs. Nat Biotechnol 2010, 28:503-510. 10.1038/nbt.1633, 2868100, 20436462.
86. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. Circos: an information aesthetic for comparative genomics. Genome Res 2009, 19:1639-1645. 10.1101/gr.092759.109, 2752132, 19541911.
87. Grant CE, Bailey TL, Noble WS. FIMO: scanning for occurrences of a given motif. Bioinformatics 2011, 27:1017-1018. 10.1093/bioinformatics/btr064, 3065696, 21330290.
88. Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, Yefanov A, Lee H, Zhang N, Robertson CL, Serova N, Davis S, Soboleva A. NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res 2013, 41:D991-D995. 10.1093/nar/gks1193, 3531084, 23193258.
89. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y, Gentry J, Hornik K, Hothorn T, Huber W, Iacus S, Irizarry R, Leisch F, Li C, Maechler M, Rossini AJ, Sawitzki G, Smith C, Smyth G, Tierney L, Yang JY, Zhang J. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004, 5:R80. 10.1186/gb-2004-5-10-r80, 545600, 15461798.