The emerging role of histone lysine demethylases in prostate cancer

Molecular Cancer

Volumn 11, Issue , 2012, Pages

  Crea, Francesco ^a   Sun, Lei ^c   Mai, Antonello ^d   Chiang, Yan T ^a   Farrar, William L ^c   Danesi, Romano ^b   Helgason, Cheryl D ^a,e  

^a BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^b UNIVERSITY OF PISA   (Italy)

^c FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^d SAPIENZA UNIVERSITY OF ROME   (Italy)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Androgen receptor; Epigenetics; Histone demethylase; Prostate cancer; Tumor initiating cells

Indexed keywords

ANDROGEN RECEPTOR; HISTONE DEMETHYLASE; HISTONE LYSINE DEMETHYLASE; PROSTATE SPECIFIC ANTIGEN; TUMOR MARKER; UNCLASSIFIED DRUG;

CANCER PROGNOSIS; CANCER SURVIVAL; CARCINOGENESIS; CHEMICAL STRUCTURE; DRUG TARGETING; EPIGENETICS; GENE OVEREXPRESSION; GENE SILENCING; GLEASON SCORE; HISTONE METHYLATION; HUMAN; LYMPH NODE METASTASIS; METASTASIS POTENTIAL; OVERALL SURVIVAL; PROSTATE CANCER; PROTEIN EXPRESSION; RECURRENCE FREE SURVIVAL; REVIEW; TUMOR SUPPRESSOR GENE;

ENZYME INHIBITORS; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HISTONE DEMETHYLASES; HUMANS; MALE; PROGNOSIS; PROSTATIC NEOPLASMS; TUMOR MARKERS, BIOLOGICAL;

EID: 84864510460     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-11-52     Document Type: Review

References (71)

1. Siegel R, Ward E, Brawley O, Jemal A. Cancer statistics, 2011: the impact of eliminating socioeconomic and racial disparities on premature cancer deaths. CA Cancer J Clin 2011, 61(4):212-236. 10.3322/caac.20121, 21685461.
2. Dal Pra A, Cury FL, Souhami L. Radiation therapy and androgen deprivation in the management of high risk prostate cancer. Int Braz J Urol 2011, 37(2):161-175. discussion 176-169.
3. Pezaro C, Attard G. Prostate cancer in 2011: redefining the therapeutic landscape for CRPC. Nat Rev Urol 2012, 9(2):63-64. 10.1038/nrurol.2011.235, 22249187.
4. Saad F, Hotte SJ. Guidelines for the management of castrate-resistant prostate cancer. Can Urol Assoc J 2010, 4(6):380-384. 10.5489/cuaj.10167, 2997826, 21191494.
5. Attard G, de Bono JS. Translating scientific advancement into clinical benefit for castration-resistant prostate cancer patients. Clin Cancer Res 2011, 17(12):3867-3875. 10.1158/1078-0432.CCR-11-0943, 21680542.
6. Rodriguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med 2011, 17(3):330-339.
7. Jeronimo C, Bastian PJ, Bjartell A, Carbone GM, Catto JW, Clark SJ, Henrique R, Nelson WG, Shariat SF. Epigenetics in prostate cancer: biologic and clinical relevance. Eur Urol 2011, 60(4):753-766. 10.1016/j.eururo.2011.06.035, 21719191.
8. Sawan C, Herceg Z. Histone modifications and cancer. Adv Genet 2010, 70:57-85.
9. Mathews LA, Crea F, Farrar WL. Epigenetic gene regulation in stem cells and correlation to cancer. Differentiation 2009, 78(1):1-17. 10.1016/j.diff.2009.04.002, 2706282, 19443100.
10. Abbas A, Gupta S. The role of histone deacetylases in prostate cancer. Epigenetics : official journal of the DNA Methylation Society 2008, 3(6):300-309.
11. Marrocco DL, Tilley WD, Bianco-Miotto T, Evdokiou A, Scher HI, Rifkind RA, Marks PA, Richon VM, Butler LM. Suberoylanilide hydroxamic acid (vorinostat) represses androgen receptor expression and acts synergistically with an androgen receptor antagonist to inhibit prostate cancer cell proliferation. Mol Cancer Ther 2007, 6(1):51-60. 10.1158/1535-7163.MCT-06-0144, 17218635.
12. Rathkopf D, Wong BY, Ross RW, Anand A, Tanaka E, Woo MM, Hu J, Dzik-Jurasz A, Yang W, Scher HI. A phase I study of oral panobinostat alone and in combination with docetaxel in patients with castration-resistant prostate cancer. Cancer Chemother Pharmacol 2010, 66(1):181-189. 10.1007/s00280-010-1289-x, 20217089.
13. Berezovska OP, Glinskii AB, Yang Z, Li XM, Hoffman RM, Glinsky GV. Essential role for activation of the Polycomb group (PcG) protein chromatin silencing pathway in metastatic prostate cancer. Cell Cycle 2006, 5(16):1886-1901. 10.4161/cc.5.16.3222, 16963837.
14. Yu J, Yu J, Rhodes DR, Tomlins SA, Cao X, Chen G, Mehra R, Wang X, Ghosh D, Shah RB, et al. A polycomb repression signature in metastatic prostate cancer predicts cancer outcome. Cancer Res 2007, 67(22):10657-10663. 10.1158/0008-5472.CAN-07-2498, 18006806.
15. Robbins CM, Tembe WA, Baker A, Sinari S, Moses TY, Beckstrom-Sternberg S, Beckstrom-Sternberg J, Barrett M, Long J, Chinnaiyan A, et al. Copy number and targeted mutational analysis reveals novel somatic events in metastatic prostate tumors. Genome Res 2011, 21(1):47-55. 10.1101/gr.107961.110, 3012925, 21147910.
16. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA, Shi Y. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119(7):941-953. 10.1016/j.cell.2004.12.012, 15620353.
17. Rotili D, Mai A. Targeting histone demethylases: a new avenue for the fight against cancer. Genes Cancer 2011, 2(6):663-679. 10.1177/1947601911417976, 3174264, 21941621.
18. Chen MW, Hua KT, Kao HJ, Chi CC, Wei LH, Johansson G, Shiah SG, Chen PS, Jeng YM, Cheng TY, et al. H3K9 histone methyltransferase G9a promotes lung cancer invasion and metastasis by silencing the cell adhesion molecule Ep-CAM. Cancer Res 2010, 70(20):7830-7840. 10.1158/0008-5472.CAN-10-0833, 20940408.
19. Futreal PA, Coin L, Marshall M, Down T, Hubbard T, Wooster R, Rahman N, Stratton MR. A census of human cancer genes. Nat Rev Cancer 2004, 4(3):177-183. 10.1038/nrc1299, 2665285, 14993899.
20. Tsukada Y, Fang J, Erdjument-Bromage H, Warren ME, Borchers CH, Tempst P, Zhang Y. Histone demethylation by a family of JmjC domain-containing proteins. Nature 2006, 439(7078):811-816. 10.1038/nature04433, 16362057.
21. Fodor BD, Kubicek S, Yonezawa M, O'Sullivan RJ, Sengupta R, Perez-Burgos L, Opravil S, Mechtler K, Schotta G, Jenuwein T. Jmjd2b antagonizes H3K9 trimethylation at pericentric heterochromatin in mammalian cells. Genes Dev 2006, 20(12):1557-1562. 10.1101/gad.388206, 1482475, 16738407.
22. Hubner MR, Spector DL. Role of H3K27 demethylases Jmjd3 and UTX in transcriptional regulation. Cold Spring Harb Symp Quant Biol 2011, 75:43-49. PMID: 21289048.
23. Amente S, Bertoni A, Morano A, Lania L, Avvedimento EV, Majello B. LSD1-mediated demethylation of histone H3 lysine 4 triggers Myc-induced transcription. Oncogene 2010, 29(25):3691-3702. 10.1038/onc.2010.120, 20418916.
24. Huang J, Sengupta R, Espejo AB, Lee MG, Dorsey JA, Richter M, Opravil S, Shiekhattar R, Bedford MT, Jenuwein T, et al. p53 is regulated by the lysine demethylase LSD1. Nature 2007, 449(7158):105-108. 10.1038/nature06092, 17805299.
25. Metzger E, Wissmann M, Yin N, Muller JM, Schneider R, Peters AH, Gunther T, Buettner R, Schule R. LSD1 demethylates repressive histone marks to promote androgen-receptor-dependent transcription. Nature 2005, 437(7057):436-439.
26. Metzger E, Imhof A, Patel D, Kahl P, Hoffmeyer K, Friedrichs N, Muller JM, Greschik H, Kirfel J, Ji S, et al. Phosphorylation of histone H3T6 by PKCbeta(I) controls demethylation at histone H3K4. Nature 2010, 464(7289):792-796. 10.1038/nature08839, 20228790.
27. Stratmann A, Haendler B. Histone demethylation and steroid receptor function in cancer. Mol Cell Endocrinol 2012, 348(1):12-20. 10.1016/j.mce.2011.09.028, 21958694.
28. Frescas D, Guardavaccaro D, Kuchay SM, Kato H, Poleshko A, Basrur V, Elenitoba-Johnson KS, Katz RA, Pagano M. KDM2A represses transcription of centromeric satellite repeats and maintains the heterochromatic state. Cell Cycle 2008, 7(22):3539-3547. 10.4161/cc.7.22.7062, 2636745, 19001877.
29. Cai C, He HH, Chen S, Coleman I, Wang H, Fang Z, Chen S, Nelson PS, Liu XS, Brown M, et al. Androgen receptor gene expression in prostate cancer is directly suppressed by the androgen receptor through recruitment of lysine-specific demethylase 1. Cancer Cell 2011, 20(4):457-471. 10.1016/j.ccr.2011.09.001, 22014572.
30. Kahl P, Gullotti L, Heukamp LC, Wolf S, Friedrichs N, Vorreuther R, Solleder G, Bastian PJ, Ellinger J, Metzger E, et al. Androgen receptor coactivators lysine-specific histone demethylase 1 and four and a half LIM domain protein 2 predict risk of prostate cancer recurrence. Cancer Res 2006, 66(23):11341-11347. 10.1158/0008-5472.CAN-06-1570, 17145880.
31. Suikki HE, Kujala PM, Tammela TL, van Weerden WM, Vessella RL, Visakorpi T. Genetic alterations and changes in expression of histone demethylases in prostate cancer. Prostate 2010, 70(8):889-898.
32. Wissmann M, Yin N, Muller JM, Greschik H, Fodor BD, Jenuwein T, Vogler C, Schneider R, Gunther T, Buettner R, et al. Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression. Nat Cell Biol 2007, 9(3):347-353. 10.1038/ncb1546, 17277772.
33. Cloos PA, Christensen J, Agger K, Maiolica A, Rappsilber J, Antal T, Hansen KH, Helin K. The putative oncogene GASC1 demethylates tri- and dimethylated lysine 9 on histone H3. Nature 2006, 442(7100):307-311. 10.1038/nature04837, 16732293.
34. Bjorkman M, Ostling P, Harma V, Virtanen J, Mpindi JP, Rantala J, Mirtti T, Vesterinen T, Lundin M, Sankila A, et al. Systematic knockdown of epigenetic enzymes identifies a novel histone demethylase PHF8 overexpressed in prostate cancer with an impact on cell proliferation, migration and invasion. Oncogene 2011, 31(29):3444-3456. PMID: 22120715.
35. van der Horst G, van den Hoogen C, Buijs JT, Cheung H, Bloys H, Pelger RC, Lorenzon G, Heckmann B, Feyen J, Pujuguet P, et al. Targeting of alpha(v)-integrins in stem/progenitor cells and supportive microenvironment impairs bone metastasis in human prostate cancer. Neoplasia 2011, 13(6):516-525. 3114245, 21677875.
36. Xiang Y, Zhu Z, Han G, Ye X, Xu B, Peng Z, Ma Y, Yu Y, Lin H, Chen AP, et al. JARID1B is a histone H3 lysine 4 demethylase up-regulated in prostate cancer. Proc Natl Acad Sci U S A 2007, 104(49):19226-19231. 10.1073/pnas.0700735104, 2148272, 18048344.
37. Kim TD, Shin S, Janknecht R. Repression of Smad3 activity by histone demethylase SMCX/JARID1C. Biochem Biophys Res Commun 2008, 366(2):563-567. 10.1016/j.bbrc.2007.12.013, 18078810.
38. Buijs JT, Henriquez NV, van Overveld PG, van der Horst G, ten Dijke P, van der Pluijm G. TGF-beta and BMP7 interactions in tumour progression and bone metastasis. Clin Exp Metastasis 2007, 24(8):609-617. 10.1007/s10585-007-9118-2, 18008174.
39. Xiang Y, Zhu Z, Han G, Lin H, Xu L, Chen CD. JMJD3 is a histone H3K27 demethylase. Cell Res 2007, 17(10):850-857. 10.1038/cr.2007.83, 17923864.
40. Crea F, Hurt EM, Mathews LA, Cabarcas SM, Sun L, Marquez VE, Danesi R, Farrar WL. Pharmacologic disruption of Polycomb Repressive Complex 2 inhibits tumorigenicity and tumor progression in prostate cancer. Mol Cancer 2011, 10:40. 10.1186/1476-4598-10-40, 3100246, 21501485.
41. Lotem J, Sachs L. Epigenetics and the plasticity of differentiation in normal and cancer stem cells. Oncogene 2006, 25(59):7663-7672. 10.1038/sj.onc.1209816, 16847453.
42. Donzella V, Crea F. Optical biosensors to analyze novel biomarkers in oncology. J Biophotonics 2011, 4(6):442-452. 10.1002/jbio.201000123, 21567973.
43. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010, 18(1):11-22. 10.1016/j.ccr.2010.05.026, 3198787, 20579941.
44. Rhodes DR, Yu J, Shanker K, Deshpande N, Varambally R, Ghosh D, Barrette T, Pandey A, Chinnaiyan AM. ONCOMINE: a cancer microarray database and integrated data-mining platform. Neoplasia 2004, 6(1):1-6. 1635162, 15068665.
45. Forneris F, Binda C, Vanoni MA, Battaglioli E, Mattevi A. Human histone demethylase LSD1 reads the histone code. J Biol Chem 2005, 280(50):41360-41365. 10.1074/jbc.M509549200, 16223729.
46. Lee MG, Wynder C, Schmidt DM, McCafferty DG, Shiekhattar R. Histone H3 lysine 4 demethylation is a target of nonselective antidepressive medications. Chem Biol 2006, 13(6):563-567. 10.1016/j.chembiol.2006.05.004, 16793513.
47. Ueda R, Suzuki T, Mino K, Tsumoto H, Nakagawa H, Hasegawa M, Sasaki R, Mizukami T, Miyata N. Identification of cell-active lysine specific demethylase 1-selective inhibitors. J Am Chem Soc 2009, 131(48):17536-17537. 10.1021/ja907055q, 19950987.
48. Adli M, Pilhatsch M, Bauer M, Koberle U, Ricken R, Janssen G, Ulrich S, Bschor T. Safety of high-intensity treatment with the irreversible monoamine oxidase inhibitor tranylcypromine in patients with treatment-resistant depression. Pharmacopsychiatry 2008, 41(6):252-257. 10.1055/s-0028-1083819, 19067263.
49. Zhao H, Flamand V, Peehl DM. Anti-oncogenic and pro-differentiation effects of clorgyline, a monoamine oxidase A inhibitor, on high grade prostate cancer cells. BMC Med Genomics 2009, 2:55. 10.1186/1755-8794-2-55, 2736984, 19691856.
50. Willmann D, Lim S, Wetzel S, Metzger E, Jandausch A, Wilk W, Jung M, Forne I, Imhof A, Janzer A, Willmann D, Lim S, Wetzel S, Metzger E, Jandausch A, Wilk W, Jung M, Forne I, Imhof A, Janzer A, et al. Impairment of prostate cancer cell growth by a selective and reversible LSD1 inhibitor. Int J Cancer 2012, [Epub ahead of print].
51. Singh MM, Manton CA, Bhat KP, Tsai WW, Aldape K, Barton MC, Chandra J. Inhibition of LSD1 sensitizes glioblastoma cells to histone deacetylase inhibitors. Neuro Oncol 2011, 13(8):894-903. 10.1093/neuonc/nor049, 3145466, 21653597.
52. Huang PH, Chen CH, Chou CC, Sargeant AM, Kulp SK, Teng CM, Byrd JC, Chen CS. Histone deacetylase inhibitors stimulate histone H3 lysine 4 methylation in part via transcriptional repression of histone H3 lysine 4 demethylases. Mol Pharmacol 2011, 79(1):197-206. 10.1124/mol.110.067702, 3014276, 20959362.
53. Orzan F, Pellegatta S, Poliani PL, Pisati F, Caldera V, Menghi F, Kapetis D, Marras C, Schiffer D, Finocchiaro G. Enhancer of Zeste 2 (EZH2) is up-regulated in malignant gliomas and in glioma stem-like cells. Neuropathol Appl Neurobiol 2011, 37(4):381-394. 10.1111/j.1365-2990.2010.01132.x, 20946108.
54. Suzuki T, Miyata N. Lysine demethylases inhibitors. J Med Chem 2011, 54(24):8236-8250. 10.1021/jm201048w, 21955276.
55. Hamada S, Suzuki T, Mino K, Koseki K, Oehme F, Flamme I, Ozasa H, Itoh Y, Ogasawara D, Komaarashi H, et al. Design, synthesis, enzyme-inhibitory activity, and effect on human cancer cells of a novel series of jumonji domain-containing protein 2 histone demethylase inhibitors. J Med Chem 2010, 53(15):5629-5638. 10.1021/jm1003655, 20684604.
56. Dick JE. Stem cell concepts renew cancer research. Blood 2008, 112(13):4793-4807. 10.1182/blood-2008-08-077941, 19064739.
57. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nature 2001, 414(6859):105-111. 10.1038/35102167, 11689955.
58. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006, 355(12):1253-1261. 10.1056/NEJMra061808, 16990388.
59. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5(4):275-284. 10.1038/nrc1590, 15803154.
60. Mulholland DJ, Kobayashi N, Ruscetti M, Zhi A, Tran LM, Huang J, Gleave M, Wu H. Pten loss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate cancer stem/progenitor cells. Cancer Res 2012, 72(7):1878-1889. 10.1158/0008-5472.CAN-11-3132, 22350410.
61. Kelly K, Yin JJ. Prostate cancer and metastasis initiating stem cells. Cell Res 2008, 18(5):528-537. 10.1038/cr.2008.50, 18414448.
62. Chang HH, Chen BY, Wu CY, Tsao ZJ, Chen YY, Chang CP, Yang CR, Lin DP. Hedgehog overexpression leads to the formation of prostate cancer stem cells with metastatic property irrespective of androgen receptor expression in the mouse model. J Biomed Sci 2011, 18:6. 10.1186/1423-0127-18-6, 3025942, 21241512.
63. Shi Y. Histone lysine demethylases: emerging roles in development, physiology and disease. Nat Rev Genet 2007, 8(11):829-833. 10.1038/nrg2218, 17909537.
64. Shi Y, Lan F, Matson C, Mulligan P, Whetstine JR, Cole PA, Casero RA. Histone demethylation mediated by the nuclear amine oxidase homolog LSD1. Cell 2004, 119(7):941-953. 10.1016/j.cell.2004.12.012, 15620353.
65. Wang J, Lu F, Ren Q, Sun H, Xu Z, Lan R, Liu Y, Ward D, Quan J, Ye T, et al. Novel histone demethylase LSD1 inhibitors selectively target cancer cells with pluripotent stem cell properties. Cancer Res 2011, 71(23):7238-7249. 10.1158/0008-5472.CAN-11-0896, 21975933.
66. Rasheed ZA, Kowalski J, Smith BD, Matsui W. Concise review: emerging concepts in clinical targeting of cancer stem cells. Stem Cells 2011, 29(6):883-887. 10.1002/stem.648, 3355871, 21509907.
67. Loh YH, Zhang W, Chen X, George J, Ng HH. Jmjd1a and Jmjd2c histone H3 Lys 9 demethylases regulate self-renewal in embryonic stem cells. Genes Dev 2007, 21(20):2545-2557. 10.1101/gad.1588207, 2000320, 17938240.
68. Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, Mistree T, Thomas SB, Farrar WL. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis 2009, 26(5):433-446. 10.1007/s10585-009-9242-2, 2782741, 19221883.
69. Hyland PL, McDade SS, McCloskey R, Dickson GJ, Arthur K, McCance DJ, Patel D. Evidence for alteration of EZH2, BMI1, and KDM6A and epigenetic reprogramming in human papillomavirus type 16 E6/E7-expressing keratinocytes. J Virol 2011, 85(21):10999-11006. 10.1128/JVI.00160-11, 3194988, 21865393.
70. Kottakis F, Polytarchou C, Foltopoulou P, Sanidas I, Kampranis SC, Tsichlis PN. FGF-2 regulates cell proliferation, migration, and angiogenesis through an NDY1/KDM2B-miR-101-EZH2 pathway. Mol Cell 2011, 43(2):285-298. 10.1016/j.molcel.2011.06.020, 3324394, 21777817.
71. Tzatsos A, Paskaleva P, Lymperi S, Contino G, Stoykova S, Chen Z, Wong KK, Bardeesy N. Lysine-specific demethylase 2B (KDM2B)-let-7-enhancer of zester homolog 2 (EZH2) pathway regulates cell cycle progression and senescence in primary cells. J Biol Chem 2011, 286(38):33061-33069. 10.1074/jbc.M111.257667, 21757686.