Expression of polycomb targets predicts breast cancer prognosis

Molecular and Cellular Biology

Volumn 33, Issue 19, 2013, Pages 3951-3961

  Jene Sanz, Alba ^a,b   Váraljai, Renáta ^b   Vilkov, Alexandra V ^a,b   Khramtsov, Galina F ^a,c   Khramtsov, Andrey I ^c   Olopade, Olufunmilayo I ^c   Lopez Bigas, Nuria ^a,d   Benevolenskaya, Elizaveta V ^b  

^a UNIVERSITAT POMPEU FABRA   (Spain)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c UNIVERSITY OF CHICAGO   (United States)

^d INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE 3 LYSINE 27 METHYLTRANSFERASE; METHYLTRANSFERASE; POLYCOMB GROUP PROTEIN; TRANSCRIPTION FACTOR EZH2; UNCLASSIFIED DRUG;

ARTICLE; BREAST CANCER; CANCER GROWTH; CANCER PATIENT; CANCER PROGNOSIS; CELL ADHESION; CELL CYCLE; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; EPIGENETICS; FEMALE; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; METHYLATION; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

BREAST NEOPLASMS; CELL ADHESION; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; EPITHELIAL-MESENCHYMAL TRANSITION; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HISTONES; HUMANS; IMMUNOBLOTTING; KAPLAN-MEIER ESTIMATE; MCF-7 CELLS; METHYLATION; MODELS, GENETIC; POLYCOMB REPRESSIVE COMPLEX 2; PROGNOSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA INTERFERENCE;

EID: 84886771344     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00426-13     Document Type: Article

References (56)

1. Valk-Lingbeek ME, Bruggeman SWM, van Lohuizen M. 2004. Stem cells and cancer; the Polycomb connection. Cell 118:409-418.
2. Feinberg AP, Ohlsson R, Henikoff S. 2006. The epigenetic progenitor origin of human cancer. Nat. Rev. Genet. 7:21-33.
3. Sauvageau M, Sauvageau G. 2010. Polycomb group proteins: multifaceted regulators of somatic stem cells and cancer. Cell Stem Cell 7:299-313.
4. Sparmann A, van Lohuizen M. 2006. Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer 6:846-856.
5. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, Sabel MS, Livant D, Weiss SJ, Rubin MA, Chinnaiyan AM. 2003. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc. Natl. Acad. Sci. U. S. A. 100:11606-11611.
6. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RG, Otte AP, Rubin MA, Chinnaiyan AM. 2002. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 419:624-629.
7. Bachmann IM. 2006. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. J. Clin. Oncol. 24:268-273.
8. Niida A, Smith AD, Imoto S, Aburatani H, Zhang MQ, Akiyama T. 2009. Gene set-based module discovery in the breast cancer transcriptome. BMC Bioinformatics 10:71. doi:10.1186/1471-2105-10-71.
9. Chang C-J, Yang J-Y, Xia W, Chen C-T, Xie X, Chao C-H, Woodward WA, Hsu J-M, Hortobagyi GN, Hung M-C. 2011. EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-β- catenin signaling. Cancer Cell 19:86-100.
10. Alford SH, Toy K, Merajver SD, Kleer CG. 2012. Increased risk for distant metastasis in patients with familial early-stage breast cancer and high EZH2 expression. Breast Cancer Res. Treat. 132:429-437.
11. Min J, Zaslavsky A, Fedele G, McLaughlin SK, Reczek EE, De Raedt T, Guney I, Strochlic DE, MacConaill LE, Beroukhim R, Bronson RT, Ryeom S, Hahn WC, Loda M, Cichowski K. 2010. An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factor-B. Nat. Med. 16:286-294.
12. Ding L, Erdmann C, Chinnaiyan AM, Merajver SD, Kleer CG. 2006. Identification of EZH2 as a molecular marker for a precancerous state in morphologically normal breast tissues. Cancer Res. 66:4095-4099.
13. Boyer LA, Plath K, Zeitlinger J, Brambrink T, Medeiros LA, Lee TI, Levine SS, Wernig M, Tajonar A, Ray MK, Bell GW, Otte AP, Vidal M, Gifford DK, Young RA, Jaenisch R. 2006. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 441: 349-353.
14. Bracken AP. 2006. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 20:1123-1136.
15. Boyer LA, Lee TI, Cole MF, Johnstone SE, Levine SS, Zucker JP, Guenther MG, Kumar RM, Murray HL, Jenner RG, Gifford DK, Melton DA, Jaenisch R, Young RA. 2005. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 122:947-956.
16. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K-I, Koseki H, Fuchikami T, Abe K, Murray HL, Zucker JP, Yuan B, Bell GW, Herbolsheimer E, Hannett NM, Sun K, Odom DT, Otte AP, Volkert TL, Bartel DP, Melton DA, Gifford DK, Jaenisch R, Young RA. 2006. Control of developmental regulators by Polycomb in human embryonic stem cells. Cell 125:301-313.
17. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Pietra Della A, III, Diaz E, LaFrance LV, Mellinger M, Duquenne C, Tian X, Kruger RG, McHugh CF, Brandt M, Miller WH, Dhanak D, Verma SK, Tummino PJ, Creasy CL. 2012. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2- activating mutations. Nature 492:108-112.
18. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, Deming SL, Geradts J, Cheang MCU, Nielsen TO, Moorman PG, Earp HS, Millikan RC. 2006. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA 295:2492-2502.
19. Carr JR, Kiefer MM, Park HJ, Li J, Wang Z, Fontanarosa J, Dewaal D, Kopanja D, Benevolenskaya EV, Guzman G, Raychaudhuri P. 2012. FoxM1 regulates mammary luminal cell fate. Cell Rep. 1:715-729.
20. Debnath J, Muthuswamy SK, Brugge JS. 2003. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in threedimensional basement membrane cultures. Methods 30:256-268.
21. Ku M, Koche RP, Rheinbay E, Mendenhall EM, Endoh M, Mikkelsen TS, Presser A, Nusbaum C, Xie X, Chi AS, Adli M, Kasif S, Ptaszek LM, Cowan CA, Lander ES, Koseki H, Bernstein BE. 2008. Genomewide analysis of PRC1 and PRC2 occupancy identifies two classes of bivalent domains. PLoS Genet. 4:e1000242. doi:10.1371/journal.pgen.1000242.
22. Birney E, Stamatoyannopoulos JA, Dutta A, Guigo R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Stamatoyannopoulos JA, Thurman RE, Kuehn MS, Taylor CM, Neph S, Koch CM, Asthana S, Malhotra A, Adzhubei I, Greenbaum JA, Andrews RM, Flicek P, Boyle PJ, Cao H, Carter NP, Clelland GK, Davis S, Day N, Dhami P, Dillon SC, Dorschner MO, Fiegler H, Giresi PG, Goldy J, Hawrylycz M, Haydock A, Humbert R, James KD, Johnson BE, Johnson EM, Frum TT, Rosenzweig ER, Karnani N, Lee K, Lefebvre GC, Navas PA, Neri F, Parker SCJ, Sabo PJ, Sandstrom R, Shafer A, et al. 2007. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799-816.
23. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10:R25. doi:10.1186/gb-2009-10-3-r25.
24. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nussbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 9:R137. doi:10.1186/gb-2008 -9-9-r137.
25. Althammer S, González-Vallinas J, Ballarž C, Beato M, Eyras E. 2011. Pyicos: a versatile toolkit for the analysis of high-throughput sequencing data. Bioinformatics 27:3333-3340.
26. Zang C, Schones DE, Zeng C, Cui K, Zhao K, Peng W. 2009. A clustering approach for identification of enriched domains from histone modification ChIP-Seq data. Bioinformatics 25:1952-1958.
27. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26:841-842.
28. Shin H, Liu T, Manrai AK, Liu XS. 2009. CEAS: cis-regulatory element annotation system. Bioinformatics 25:2605-2606.
29. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES, Mesirov JP. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U. S. A. 102:15545-15550.
30. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JEL, Liu ET, Bergh J, Kuznetsov VA, Miller LD. 2006. Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 66:10292-10301.
31. Sabatier R, Finetti P, Cervera N, Lambaudie E, Esterni B, Mamessier E, Tallet A, Chabannon C, Extra J-M, Jacquemier J, Viens P, Birnbaum D, Bertucci F. 2010. A gene expression signature identifies two prognostic subgroups of basal breast cancer. Breast Cancer Res. Treat. 126:407-420.
32. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 40:D109-D114.
33. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. 2000. Gene Ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet. 25: 25-29.
34. Su AI, Wiltshire T, Batalov S, Lapp H, Ching KA, Block D, Zhang J, Soden R, Hayakawa M, Kreiman G, Cooke MP, Walker JR, Hogenesch JB. 2004. A gene atlas of the mouse and human protein-encoding transcriptomes. Proc. Natl. Acad. Sci. U. S. A. 101:6062-6067.
35. Roth RB, Hevezi P, Lee J, Willhite D, Lechner SM, Foster AC, Zlotnik A. 2006. Gene expression analyses reveal molecular relationships among 20 regions of the human CNS. Neurogenetics 7:67-80.
36. Schmidt M, Bohm D, von Torne C, Steiner E, Puhl A, Pilch H, Lehr HA, Hengstler JG, Kolbl H, Gehrmann M. 2008. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res. 68:5405-5413.
37. Pawitan Y, Bjöhle J, Amler L, Borg A-L, Egyhazi S, Hall P, Han X, Holmberg L, Huang F, Klaar S, Liu ET, Miller L, Nordgren H, Ploner A, Sandelin K, Shaw PM, Smeds J, Skoog L, Wedrén S, Bergh J. 2005. Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res. 7:R953. doi:10.1186/bcr1325.
38. Koboldt DC, Fulton RS, McLellan MD, Schmidt H, Kalicki-Veizer J, McMichael JF, Fulton LL, Dooling DJ, Ding L, Mardis ER, Wilson RK, Ally A, Balasundaram M, Butterfield YSN, Carlsen R, Carter C, Chu A, Chuah E, Chun H-JE, Coope RJN, Dhalla N, Guin R, Hirst C, Hirst M, Holt RA, Lee D, Li HI, Mayo M, Moore RA, Mungall AJ, Pleasance E, Gordon Robertson A, Schein JE, Shafiei A, Sipahimalani P, Slobodan JR, Stoll D, Tam A, Thiessen N, Varhol RJ, Wye N, Zeng T, Zhao Y, Birol I, Jones SJM, Marra MA, Cherniack AD, Saksena G, Onofrio RC, Pho NH, et al. 2012. Comprehensive molecular portraits of human breast tumours. Nature 490:61-70.
39. Gundem G, Lopez-Bigas N. 2012. Sample-level enrichment analysis unravels shared stress phenotypes among multiple cancer types. Genome Med. 4:28. doi:10.1186/gm327.
40. 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. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. doi:10.1186/gb-2004-5-10-r80.
41. Perez-Llamas C, Lopez-Bigas N. 2011. Gitools: analysis and visualisation of genomic data using interactive heat-maps. PLoS One 6:e19541. doi:10 .1371/journal.pone.0019541.
42. Lopez-Bigas N, De S, Teichmann SA. 2008. Functional protein divergence in the evolution of Homo sapiens. Genome Biol. 9:R33. doi:10.1186 /gb-2008-9-2-r33.
43. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Statist. Soc. Ser. B 57:289-300.
44. Nijhawan D, Zack TI, Ren Y, Strickland MR, Lamothe R, Schumacher SE, Tsherniak A, Besche HC, Rosenbluh J, Shehata S, Cowley GS, Weir BA, Goldberg AL, Mesirov JP, Root DE, Bhatia SN, Beroukhim R, Hahn WC. 2012. Cancer vulnerabilities unveiled by genomic loss. Cell 150:842-854.
45. van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AAM, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH. 2002. Gene expression profiling predicts clinical outcome of breast cancer. Nature 415:530-536.
46. Gonzalez ME, DuPrie ML, Krueger H, Merajver SD, Ventura AC, Toy KA, Kleer CG. 2011. Histone methyltransferase EZH2 induces Aktdependent genomic instability and BRCA1 inhibition in breast cancer. Cancer Res. 71:2360-2370.
47. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai M-C, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY. 2010. Long noncoding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071-1076.
48. Lee ST, Li Z, Wu Z, Aau M, Guan P, Karuturi RKM, Liou YC, Yu Q. 2011. Context-specific regulation of NF-B target gene expression by EZH2 in breast cancers. Mol. Cell 43:798-810.
49. Whitfield ML, Sherlock G, Saldanha AJ, Murray JI, Ball CA, Alexander KE, Matese JC, Perou CM, Hurt MM, Brown PO, Botstein D. 2002. Identification of genes periodically expressed in the human cell cycle and their expression in tumors. Mol. Biol. Cell 13:1977-2000.
50. Sørlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, Demeter J, Perou CM, Lønning PE, Brown PO, Børresen-Dale A-L, Botstein D. 2003. Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc. Natl. Acad. Sci. U. S. A. 100:8418-8423.
51. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA. 2008. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat. Genet. 40: 499-507.
52. Kim J, Woo AJ, Chu J, Snow JW, Fujiwara Y, Kim CG, Cantor AB, Orkin SH. 2010. A Myc network accounts for similarities between embryonic stem and cancer cell transcription programs. Cell 143:313-324.
53. Yap DB, Chu J, Berg T, Schapira M, Cheng S-WG, Moradian A, Morin RD, Mungall AJ, Meissner B, Boyle M, Marquez VE, Marra MA, Gascoyne RD, Humphries RK, Arrowsmith CH, Morin GB, Aparicio SA. 2011. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood 117:2451-2459.
54. Xu K, Wu ZJ, Groner AC, He HH, Cai C, Lis RT, Wu X, Stack EC, Loda M, Liu T, Xu H, Cato L, Thornton JE, Gregory RI, Morrissey C, Vessella RL, Montironi R, Magi-Galluzzi C, Kantoff PW, Balk SP, Liu XS, Brown M. 2012. EZH2 oncogenic activity in castration-resistant prostate cancer cells is Polycomb-independent. Science 338:1465-1469.
55. Kim H, Watkinson J, Varadan V, Anastassiou D. 2010. Multi-cancer computational analysis reveals invasion-associated variant of desmoplastic reaction involving INHBA, THBS2 and COL11A1. BMC Med. Genomics 3:51. doi:10.1186/1755-8794-3-51.
56. Schmidt M, Bohm D, von Torne C, Steiner E, Puhl A, Pilch H, Lehr HA, Hengstler JG, Kolbl H, Gehrmann M. 2008. The humoral immune system has a key prognostic impact in node-negative breast cancer. Cancer Res 68:5405-5413.