Essential role for activation of the polycomb group (PcG) protein chromatin silencing pathway in metastatic prostate cancer

Cell Cycle

Volumn 5, Issue 16, 2006, Pages 1886-1901

  Berezovska, Olga P ^a   Glinskii, Anna B ^a   Yang, Zhijian ^c   Li, Xiao Ming ^c   Hoffman, Robert M ^c   Glinsky, Gennadi V ^a,b,d  

^a ORDWAY RESEARCH INSTITUTE   (United States)

^b ALBANY MEDICAL COLLEGE   (United States)

^c ANTICANCER INC   (United States)

^d SIDNEY KIMMEL CANCER CENTER   (United States)

Author keywords

BMI1; Ezh2; Metastasis; Microarray analysis; Polycomb proteins; Prostate cancer; Self renewal; Stem cells; Survival predictor; Xenograft models

Indexed keywords

HISTONE; MESSENGER RNA; ONCOPROTEIN; POLYCOMB GROUP PROTEIN; PROTEIN H2AUBIK119 HISTONE; PROTEIN H3METK27 HISTONE; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ARTICLE; BMI1 GENE; CANCER GROWTH; CANCER RELAPSE; CELL RENEWAL; CHROMATIN; CONTROLLED STUDY; EZH2 GENE; GENE AMPLIFICATION; GENE EXPRESSION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; HUMAN TISSUE; IMAGING SYSTEM; IMMUNOFLUORESCENCE TEST; IN VIVO STUDY; LEUKEMIA; MAJOR CLINICAL STUDY; MALE; METASTASIS; ONCOGENE; PATHOGENESIS; PROSTATE CANCER; PROSTATECTOMY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; QUANTITATIVE ANALYSIS; STEM CELL; TISSUE MICROARRAY; TREATMENT FAILURE;

ANIMALIA;

EID: 33748951908     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.5.16.3222     Document Type: Article

References (50)

1. Lessard J, Sauvageau G. BMI1 determines the proliferative capacity of normal and leukaemic stem cells. Nature 2003; 423:255-60.
2. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL, Morrison SJ, Clarke MF. Bmi1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 2003; 423:302-5.
3. Molofsky AV, Pardal R, Iwashita T, Park IK, Clarke MF, Morrison SJ. Bmi1 dependence distinguishes neural stem cell self-renewal from progenitor proliferation. Nature 2003; 425:962-7.
4. Dick JE. Self-renewal writ in blood. Nature 2003; 423:231-3.
5. Lessard J, Baban S, Sauvageau G. Stage-specific expression of polycomb group genes in human bone marrow cells. Blood 1998; 91:1216-24.
6. Haupt Y, Bath MI, Harris AW, Adams JM. BMI1 transgene induces lymphomas and collaborates with Myc in tumorigenesis. Oncogene 1993; 8:3161-4.
7. Alkema MJ, Jacobs H, van Lohuizen M, Berns A. Perturbation of B and T cell development and predisposition to lymphomagenesis in Eμ-Bmi1 transgenic mice require the Bmi1 RING finger. Oncogene 1997; 15:899-910.
8. Vonlanthen S, Heighway J, Altermatt HJ, Gugger M, Kappeler A, Borner MM, van Lohuizen M, Betticher DC. The Bmi1 oncoprotein is differentially expressed in nonsmall-cell lung cancer and correlates with INK4A-ARF locus expression. Br J Cancer 2001; 84:1372-6.
9. Dimri GP, Martinez JL, Jacobs JJL, Keblusek P, Itahana K, van Lohuizen M, Campisi J, Wazer DE, Band V. The Bmi1 oncogene induces telomerase activity and immortalizes human mammary epithelial cells. Cancer Res 2002; 62:4736-45.
10. Raaphorst FM, Vermeer M, Fieret E, Blokzijl T, Mommers E, Buerger H, Packeisen J, Sewalt RA, Otte AP, van Diset PJ. Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. Neoplasia 2003; 5:481-8.
11. Leung C, Lingbeek M, Shakhova O, Liu J, Tanger E, Saremaslani P, van Lohuizen M, Marino S. BMI1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 2004; 428:337-41.
12. Glinsky GV, Berezovska O, Glinskii AB. Microarray analysis identifies a death from cancer signature predicting therapy failure in patients with multiple types of cancer. J Clin Invest 2005; 115:1503-21.
13. Kim JH, Yoon SY, Kim CN, Joo JH, Moon SK, Choe JS, Choe YK, Kim JW. The Bmi-1 oncoprotein is overexpressed in human colorectal cancer and correlates with the reduced p16INK4a/p14ARF proteins. Cancer Lett 2004; 203:217-24.
14. Raaphorst FM, van Kemenade FJ, Blokzijl T, Fieret JH, Hamer K, Otte AP, Meijer CJLM. Coexpression of BMI-1 and EZH2 Polycomb-group genes in Reed-Sternberg cells of Hodgkin's disease. Am J Pathol 2000; 157:709-15.
15. van Kemenade FJ, Raaphorst FM, Blokzijl T, Fieret JH, Hamer KM, Satijn DP, Otte E, AP, Meijer CJLM. Coexpression of the BMI-1 and EZH2 Polycomb-group genes is associated with cycling cells and degree of malignancy in B-NHL. Blood 2001; 97:3896-901.
16. Visser HPJ, Gunster MJ, Kluin-Nelemans HC, Manders EMM, Raaphorst FM, Meijer CJLM, Otte AP. The Polycomb-group protein EZH2 is upregulated in proliferating, cultured human mantle cell lymphoma. Br J Haematol 2001; 112:950-8.
17. Bea S, Tort F, Pinyol M, Puig X, Hernández L, Hernández S, Fernandez PL, van Lohuizen M, Colomer D, Campo E. BMI-1 gene amplification and overexpression in hematological malignancies occur mainly in mantle cell lymphoma. Cancer Res 2001; 61:2409-12.
18. Dukers DF, van Galen JC, Giroth C, Jansen P, Sewalt RG, Otte AP, Kluin-Nelemans HC, Meijer CJ, Raaphorst FM. Unique polycomb gene expression pattern in Hodgkin's lymphoma and Hodgkin's lymphoma-derived cell lines. Am J Pathol 2004; 164:873-81.
19. Varambally S, Dhanasekaran SM, Zhou M, Barrette TR, Kumar-Sinha C, Sanda MG, Ghosh D, Pienta KJ, Sewalt RGAB, Otte AP, Rubin MA, Chinnaiyan AM. The polycomb group protein EZH2 is involved in progression of prostate cancer. Nature 2002; 419:624-9.
20. Rhodes DR, Sanda MG, Otte AP, Chinnaiyan AM, Rubin MA. Multiplex biomarker approach for determining risk of prostate-specific antigen-defined recurrence of prostate cancer. J Natl Cancer Inst 2003; 95:661-8.
21. Bachmann IM, Halvorsen OJ, Collett K, Stefansson IM, Straume O, Haukaas SA, Salvesen HB, Otte AP, Akslen LA. 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 2006; 24:268-73.
22. Saramaki OR, Tammela TL, Martikainen PM, Vessella RL, Visakorpi T. The gene for polycomb group protein enhancer of zeste homolog 2 (EZH2) is amplified in late-stage prostate cancer. Genes Chromosomes Cancer 2006; 45:639-45.
23. 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. EZH2 is a marker of aggressive breast cancer and promotes neoplastic transformation of breast epithelial cells. Proc Natl Acad Sci USA 2003; 100:11606-11.
24. Raaphorst FM, Meijer CJ, Fieret E, Blokzijl T, Mommers E, Buerger H, Packeisen J, Sewalt RA, Otte AP, van Diest PJ. Poorly differentiated breast carcinoma is associated with increased expression of the human polycomb group EZH2 gene. Neoplasia 2003; 5:481-8.
25. Zeidler M, Varambally S, Cao Q, Chinnaiyan AM, Ferguson DO, Merajver SD, Kleer CG. The Polycomb group protein EZH2 impairs DNA repair in breast epithelial cells. Neoplasia 2005; 7:1011-9.
26. Collett K, Eide GE, Arnes J, Stefansson IM, Eide J, Braaten A, Aas T, Otte AP, Akslen LA. Expression of enhancer of zeste homologue 2 is significantly associated with increased tumor cell proliferation and is a marker of aggressive breast cancer. Clin Cancer Res 2006; 12:1168-74.
27. Raman JD, Mongan NP, Tickoo SK, Boorjian SA, Scherr DS, Gudas LJ. Increased expression of the polycomb group gene, EZH2, in transitional cell carcinoma of the bladder. Clin Cancer Res 2005; 11:8570-6.
28. Weikert S, Christoph F, Kollermann J, Muller M, Schrader M, Miller K, Krause H. Expression levels of the EZH2 polycomb transcriptional repressor correlate with aggressiveness and invasive potential of bladder carcinomas. Int J Mol Med 2005; 16:349-53.
29. Breuer RH, Snijders PJ, Smit EF, Sutedja TG, Sewalt RG, Otte AP, van Kemenade FJ, Postmus PE, Meijer CJ, Raaphorst FM. Increased expression of the EZH2 polycomb group gene in BMI-1-positive neoplastic cells during bronchial carcinogenesis. Neoplasia 2004; 6:736-43.
30. Croonquist PA, Van Ness B. The polycomb group protein enhancer of zeste homolog 2 (EZH 2) is an oncogene that influences myeloma cell growth and the mutant ras phenotype. Oncogene 2005; 24:6269-80.
31. Bracken AP, Pasini D, Capra M, Prosperini E, Colli E, Helin K. EZH2 is downstream of the pRB-E2F pathway, essential for proliferation and amplified in cancer. EMBO J 2003; 22:5323-35.
32. Glinsky GV, Ivanova YB, Glinskii AB. Common malignancy-associated regions of transcriptional activation in human prostate, breast, ovarian, and colon cancers are targets for DNA amplification. Cancer Lett 2003; 201:67-77.
33. Glinsky GV. Death-from-cancer signatures and contribution of stem cells to metastatic cancer. Cell Cycle 2005; 4:1171-5.
34. Glinsky GV. Genomic models of metastatic cancer: Functional analysis of death-from-cancer signature genes reveals aneuploid, anoikis-resistant, metastasis-enabling phenotype with altered cell cycle control and activated Polycomb Group (PcG) protein chromatin silencing pathway. Cell Cycle 2006; 5:1208-16.
35. Valk-Lingbeek ME, Bruggeman SWM, van Lohuizen M. Stem cells and cancer: The Polycomb connection. Cell 2004; 118:409-18.
36. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004; 431:873-8.
37. Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NCT, Kao CF, Pillus L, Shilatifard A, Osley MA, Berger SL. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 2003; 17:2648-63.
38. Francis NJ, Saurin AJ, Shao Z, Kingston RE. Reconstitution of a functional core polycomb repressive complex. Mol Cell 2001; 8:545-56.
39. Poux S, Melfi R, Pirrotta V. Establishment of Polycomb silencing requires a transient interaction between PC and ESC. Genes Dev 2001; 15:2509-14.
40. Kuzmichev A, Jenuwein T, Tempst P, Reinberg D. Different EZH2-containing complexes target methylation of histone H1 or nucleosomal histone H3. Mol Cell 2004; 14:183-93.
41. Singh D, Febbo PG, Ross K, Jackson DG, Manola CL, Tamayo P, Renshaw AA, D'Amico AV, Richie JP, Lander ES, Loda M, Kantoff PW, Golub TR, Sellers WR. Gene expression correlates of clinical prostate cancer behavior. Cancer Cell 2002; 1:203-9.
42. Glinsky GV, Glinskii AB, Stephenson AJ, Hoffmann RM, Gerald WL. Expression profiling predicts clinical outcome of prostate cancer. J Clin Invest 2004; 113:913-23.
43. Glinskii AB, Smith BA, Jiang P, Li XM, Yang M, Hoffman RM, Glinsky GV. Viable circulating metastatic cells produced in orthotopic but not ectopic prostate cancer models. Cancer Res 2003; 63:4239-43.
44. Berezovskaya O, Schimmer AD, Glinskii AB, Pinilla C, Hoffman RM, Reed JC, Glinsky GV. Increased expression of apoptosis inhibitor XIAP contributes to resistance to anoikis of prostate cancer metastasis precursor cells. Cancer Res 2005; 65:2378-86.
45. Glinsky GV, Krones-Herzig A, Glinskii AB, Gebauer G. Microarray analysis of xenograft-derived cancer cell lines representing multiple experimental models of human prostate cancer. Molecular Carcinogenesis 2003; 37:209-21.
46. Saurin AJ, Shiels C, Williamson J, Satijn DPE, Otte AP, Sheer D, Freemont PS. The human Polycomb Group Complex associates with pericentromeric heterochromatin to form a novel nuclear domain. J Cell Biol 1998; 142:887-98.
47. Kuzmichev A, Margueron R, Vaquero A, Preissner TS, Scher M, Kirmizis A, Ouyang X, Brockdorff N, Abate-Shen C, Farnham P, Reinberg D. Composition and histone substrates of polycomb repressive group complexes change during cellular differentiation. Proc Natl Acad Sci 2005; 102:1859-64.
48. Su I, Dobenecker M, Dickinson E, Oser M, Basavaraj A, Marqueron R, Viale A, Reinberg D, Wülfing C, Tarakhovsky A. Polycomb group protein Ezh2 controls actin polymerization and cell signaling. Cell 2005; 121:425-36.
49. 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. Polycomb complexes repress developmental regulators in murine embryonic stem cells. Nature 2006; 441:349-53.
50. Lee TI, Jenner RG, Boyer LA, Guenther MG, Levine SS, Kumar RM, Chevalier B, Johnstone SE, Cole MF, Isono K, 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. Control of developmental regulators by polycomb in human embryonic stem cells. Cell 2006; 125:301-13.