EZH2 knockdown suppresses the growth and invasion of human inflammatory breast cancer cells

Journal of Experimental and Clinical Cancer Research

Volumn 32, Issue 1, 2013, Pages

  Mu, Zhaomei ^a,b   Li, Hua ^c   Fernandez, Sandra V ^a,b   Alpaugh, Katherine R ^b   Zhang, Rugang ^c   Cristofanilli, Massimo ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b FOX CHASE CANCER CENTER   (United States)

^c WISTAR INSTITUTE   (United States)

Author keywords

Cancer stem cell; EZH2; Inflammatory breast cancer; Tumor spheroid formation

Indexed keywords

SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR EZH2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CANCER GROWTH; CANCER INHIBITION; CELL ASSAY; CELL LEVEL; CELL MIGRATION; CONTROLLED STUDY; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY BREAST CANCER; MALIGNANT PLEURA EFFUSION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR INVASION; TUMOR SPHEROID; TUMOR VASCULARIZATION; TUMOR XENOGRAFT;

ANIMALS; CELL GROWTH PROCESSES; FEMALE; GENE KNOCKDOWN TECHNIQUES; HUMANS; INFLAMMATORY BREAST NEOPLASMS; LENTIVIRUS INFECTIONS; MICE; MICE, SCID; NEOPLASTIC STEM CELLS; POLYCOMB REPRESSIVE COMPLEX 2; SPHEROIDS, CELLULAR; SURVIVAL ANALYSIS;

EID: 84884623771     PISSN: None     EISSN: 17569966     Source Type: Journal    
DOI: 10.1186/1756-9966-32-70     Document Type: Article

References (43)

1. Trends in inflammatory breast carcinoma incidence and survival: the surveillance, epidemiology, and end results program at the National Cancer Institute. Hance KW, Anderson WF, Devesa SS, Young HA, Levine PH, J Natl Cancer Inst 2005 97 13 966 975 10.1093/jnci/dji172 15998949 (Pubitemid 41430562)
2. International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Dawood S, Merajver SD, Viens P, Vermeulen PB, Swain SM, Buchholz TA, Dirix LY, Levine PH, Lucci A, Krishnamurthy S, et al. Ann Oncol 2011 22 3 515 523 10.1093/annonc/mdq345 20603440
3. Inflammatory breast cancer: a review. Jaiyesimi IA, Buzdar AU, Hortobagyi G, J Clin Oncol 1992 10 6 1014 1024 1588366
4. Inflammatory breast cancer (IBC) and patterns of recurrence: understanding the biology of a unique disease. Cristofanilli M, Valero V, Buzdar AU, Kau SW, Broglio KR, Gonzalez-Angulo AM, Sneige N, Islam R, Ueno NT, Buchholz TA, et al. Cancer 2007 110 7 1436 1444 10.1002/cncr.22927 17694554 (Pubitemid 47463056)
5. Cooperative role of E-cadherin and sialyl-Lewis X/A-deficient MUC1 in the passive dissemination of tumor emboli in inflammatory breast carcinoma. Alpaugh ML, Tomlinson JS, Kasraeian S, Barsky SH, Oncogene 2002 21 22 3631 3643 10.1038/sj.onc.1205389 12032865 (Pubitemid 34587695)
6. Inflammatory breast cancer: what progress have we made? Dawood S, Cristofanilli M, Oncology 2011 25 3 264 270 21548470
7. Epidermal growth factor receptor tyrosine kinase inhibitor reverses mesenchymal to epithelial phenotype and inhibits metastasis in inflammatory breast cancer. Zhang D, LaFortune TA, Krishnamurthy S, Esteva FJ, Cristofanilli M, Liu P, Lucci A, Singh B, Hung MC, Hortobagyi GN, et al. Clin Cancer Res 2009 15 21 6639 6648 10.1158/1078-0432.CCR-09-0951 19825949
8. Expression of growth factor and chemokine receptors: new insights in the biology of inflammatory breast cancer. Cabioglu N, Gong Y, Islam R, Broglio KR, Sneige N, Sahin A, Gonzalez-Angulo AM, Morandi P, Bucana C, Hortobagyi GN, et al. Ann Oncol 2007 18 6 1021 1029 10.1093/annonc/mdm060 17351259 (Pubitemid 47050493)
9. Molecular targets for treatment of inflammatory breast cancer. Yamauchi H, Cristofanilli M, Nakamura S, Hortobagyi GN, Ueno NT, Nat Rev Clin Oncol 2009 6 7 387 394 10.1038/nrclinonc.2009.73 19468291
10. Identification of cell-of-origin breast tumor subtypes in inflammatory breast cancer by gene expression profiling. Van Laere SJ, Van den Eynden GG, Van der Auwera I, Vandenberghe M, van Dam P, Van Marck EA, van Golen KL, Vermeulen PB, Dirix LY, Breast Cancer Res Treat 2006 95 3 243 255 10.1007/s10549-005-9015- 9 16261404
11. SUZ12 is required for both the histone methyltransferase activity and the silencing function of the EED-EZH2 complex. Cao R, Zhang Y, Mol Cell 2004 15 1 57 67 10.1016/j.molcel.2004.06.020 15225548 (Pubitemid 38850219)
12. The role of EZH2 in tumour progression. Chang CJ, Hung MC, Br J Cancer 2012 106 2 243 247 10.1038/bjc.2011.551 22187039
13. Polycomb group proteins: multi-faceted regulators of somatic stem cells and cancer. Sauvageau M, Sauvageau G, Cell Stem Cell 2010 7 3 299 313 10.1016/j.stem.2010.08.002 20804967
14. Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Collett K, Eide GE, Arnes J, Stefansson IM, Eide J, Braaten A, Aas T, Otte AP, Akslen LA, Clin Cancer Res 2006 12 4 1168 1174 10.1158/1078-0432.CCR- 05-1533 16489070 (Pubitemid 43342505)
15. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Kleer CG, Cao Q, Varambally S, Shen R, Ota I, Tomlins SA, Ghosh D, Sewalt RG, Otte AP, Hayes DF, et al. Proc Natl Acad Sci U S A 2003 100 20 11606 11611 10.1073/pnas.1933744100 14500907 (Pubitemid 37205983)
16. Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. Raaphorst FM, Meijer CJ, Fieret E, Blokzijl T, Mommers E, Buerger H, Packeisen J, Sewalt RA, Otte AP, van Diest PJ, Neoplasia 2003 5 6 481 488 14965441 (Pubitemid 38045085)
17. EZH2 expression is associated with high proliferation rate and aggressive tumor subgroups in cutaneous melanoma and cancers of the endometrium, prostate, and breast. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, Haukaas SA, Salvesen HB, Otte AP, Akslen LA, J Clin Oncol 2006 24 2 268 273 16330673 (Pubitemid 46622055)
18. Enhancer of Zeste 2 as a marker of preneoplastic progression in the breast. Ding L, Kleer CG, Cancer Res 2006 66 19 9352 9355 10.1158/0008-5472.CAN- 06-2384 17018586 (Pubitemid 44623628)
19. Downregulation of EZH2 decreases growth of estrogen receptor-negative invasive breast carcinoma and requires BRCA1. Gonzalez ME, Li X, Toy K, DuPrie M, Ventura AC, Banerjee M, Ljungman M, Merajver SD, Kleer CG, Oncogene 2009 28 6 843 853 10.1038/onc.2008.433 19079346
20. EZH2 and BMI1 inversely correlate with prognosis and TP53 mutation in breast cancer. Pietersen AM, Horlings HM, Hauptmann M, Langerod A, Ajouaou A, Cornelissen-Steijger P, Wessels LF, Jonkers J, van de Vijver MJ, van Lohuizen M, Breast Cancer Res 2008 10 6 109 19099573
21. Polycomb group protein EZH2 is frequently expressed in inflammatory breast cancer and is predictive of worse clinical outcome. Gong Y, Huo L, Liu P, Sneige N, Sun X, Ueno NT, Lucci A, Buchholz TA, Valero V, Cristofanilli M, Cancer 2011 117 24 5476 5484 10.1002/cncr.26179 21713757
22. Inflammatory breast cancer (IBC): clues for targeted therapies. Fernandez SV, Robertson FM, Pei J, Aburto-Chumpitaz L, Mu Z, Chu K, Alpaugh RK, Huang Y, Cao Y, Ye Z, et al. Breast Cancer Res Treat 2013 140 1 23 33 10.1007/s10549-013-2600-4 23784380
23. Prospective identification of tumorigenic breast cancer cells. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, Proc Natl Acad Sci U S A 2003 100 7 3983 3988 10.1073/pnas.0530291100 12629218 (Pubitemid 36418143)
24. Stem cells in normal breast development and breast cancer. Dontu G, Al-Hajj M, Abdallah WM, Clarke MF, Wicha MS, Cell Prolif 2003 36 Suppl 1 59 72 14521516 (Pubitemid 37521844)
25. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. Phillips TM, McBride WH, Pajonk F, J Natl Cancer Inst 2006 98 24 1777 1785 10.1093/jnci/djj495 17179479 (Pubitemid 46017929)
26. Cancer stem cells contribute to cisplatin resistance in Brca1/p53-mediated mouse mammary tumors. Shafee N, Smith CR, Wei S, Kim Y, Mills GB, Hortobagyi GN, Stanbridge EJ, Lee EY, Cancer Res 2008 68 9 3243 3250 10.1158/0008-5472.CAN-07-5480 18451150
27. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. Korkaya H, Paulson A, Charafe-Jauffret E, Ginestier C, Brown M, Dutcher J, Clouthier SG, Wicha MS, PLoS Biol 2009 7 6 1000121 10.1371/journal.pbio.1000121 19492080
28. EZH2 promotes expansion of breast tumor initiating cells through activation of RAF1-beta-catenin signaling. Chang CJ, Yang JY, Xia W, Chen CT, Xie X, Chao CH, Woodward WA, Hsu JM, Hortobagyi GN, Hung MC, Cancer Cell 2011 19 1 86 100 10.1016/j.ccr.2010.10.035 21215703
29. Regulation of stem cell pluripotency and differentiation involves a mutual regulatory circuit of the NANOG, OCT4, and SOX2 pluripotency transcription factors with polycomb repressive complexes and stem cell microRNAs. Kashyap V, Rezende NC, Scotland KB, Shaffer SM, Persson JL, Gudas LJ, Mongan NP, Stem Cells Dev 2009 18 7 1093 1108 10.1089/scd.2009.0113 19480567
30. Altered gene expression in morphologically normal epithelial cells from heterozygous carriers of BRCA1 or BRCA2 mutations. Bellacosa A, Godwin AK, Peri S, Devarajan K, Caretti E, Vanderveer L, Bove B, Slater C, Zhou Y, Daly M, et al. Cancer Prev Res 2010 3 1 48 61 10.1158/1940-6207.CAPR-09-0078
31. Enhancer of zeste homolog 2 promotes the proliferation and invasion of epithelial ovarian cancer cells. Li H, Cai Q, Godwin AK, Zhang R, Mol Cancer Res 2010 8 12 1610 1618 10.1158/1541-7786.MCR-10-0398 21115743
32. Antisense MDM2 enhances the response of androgen insensitive human prostate cancer cells to androgen deprivation in vitro and in vivo. Mu Z, Hachem P, Hensley H, Stoyanova R, Kwon HW, Hanlon AL, Agrawal S, Pollack A, Prostate 2008 68 6 599 609 10.1002/pros.20731 18196567 (Pubitemid 351614638)
33. Uncovering the molecular secrets of Inflammatory Breast Cancer biology: An integrated analysis of three distinct Affymetrix gene expression data sets. Van Laere SJ, Ueno NT, Finetti P, Vermeulen PB, Lucci A, Robertson FM, Marsan M, Iwamoto T, Krishnamurthy S, Masuda H, et al. Clin Cancer Res 2013 19 17 4685 4696 10.1158/1078-0432.CCR-12-2549 23396049
34. Global H3K27 trimethylation and EZH2 abundance in breast tumor subtypes. Holm K, Grabau D, Lovgren K, Aradottir S, Gruvberger-Saal S, Howlin J, Saal LH, Ethier SP, Bendahl PO, Stal O, et al. Mol Oncol 2012 6 5 494 506 10.1016/j.molonc.2012.06.002 22766277
35. A novel human xenograft model of inflammatory breast cancer. Alpaugh ML, Tomlinson JS, Shao ZM, Barsky SH, Cancer Res 1999 59 20 5079 5084 10537277 (Pubitemid 29503962)
36. Absence of endothelial cells, central necrosis, and fibrosis are associated with aggressive inflammatory breast cancer. Shirakawa K, Tsuda H, Heike Y, Kato K, Asada R, Inomata M, Sasaki H, Kasumi F, Yoshimoto M, Iwanaga T, et al. Cancer Res 2001 61 2 445 451 11212228 (Pubitemid 32128594)
37. Emerging role of cancer stem cells in the biology and treatment of ovarian cancer: basic knowledge and therapeutic possibilities for an innovative approach. Tomao F, Papa A, Rossi L, Strudel M, Vici P, Lo Russo G, Tomao S, J Exp Clin Cancer Res 2013 32 48 doi: 10.1186/1756-9966 10.1186/1756-9966-32-48 23902592
38. Compound Kushen Injection suppresses human breast cancer stem-like cells by down-regulating the canonical Wnt/β-catenin pathway. Xu W, Lin H, Zhang Y, Chen X, Hua B, Hou W, Qi X, Pei Y, Zhu X, Zhao Z, Yang L, J Exp Clin Cancer Res 2011 30 103 10.1186/1756-9966 10.1186/1756-9966-30-103 22032476
39. Regulation of tumor angiogenesis by EZH2. Lu C, Han HD, Mangala LS, Ali-Fehmi R, Newton CS, Ozbun L, Armaiz-Pena GN, Hu W, Stone RL, Munkarah A, et al. Cancer Cell 2010 18 2 185 197 10.1016/j.ccr.2010.06.016 20708159
40. Selective inhibition of Ezh2 by a small molecule inhibitor blocks tumor cells proliferation. Qi W, Chan H, Teng L, Li L, Chuai S, Zhang R, Zeng J, Li M, Fan H, Lin Y, et al. Proc Natl Acad Sci U S A 2012 109 52 21360 21365 10.1073/pnas.1210371110 23236167
41. A selective inhibitor of EZH2 blocks H3K27 methylation and kills mutant lymphoma cells. Knutson SK, Wigle TJ, Warholic NM, Sneeringer CJ, Allain CJ, Klaus CR, Sacks JD, Raimondi A, Majer CR, Song J, et al. Nat Chem Biol 2012 8 11 890 896 23023262
42. EZH2 inhibition as a therapeutic strategy for lymphoma with EZH2-activating mutations. McCabe MT, Ott HM, Ganji G, Korenchuk S, Thompson C, Van Aller GS, Liu Y, Graves AP, Della Pietra A 3rd, Diaz E, et al. Nature 2012 492 7427 108 112 10.1038/nature11606 23051747
43. Three-dimensional culture sensitizes epithelial ovarian cancer cells to EZH2 methyltransferase inhibition. Amatangelo MD, Garipov A, Li H, Conejo-Garcia JR, Speicher DW, Zhang R, Cell Cycle 2013 12 13 2113 2119 10.4161/cc.25163 23759589