Alterations of DNA methylome in human bladder cancer

Epigenetics

Volumn 8, Issue 10, 2013, Pages 1013-1022

  Besaratinia, Ahmad ^a   Cockburn, Myles ^a   Tommasi, Stella ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Aberrant DNA methylation; Animal models; Epigenetics; Transitional cell carcinoma; Tumorigenesis

Indexed keywords

5 AZA 2' DEOXYCYTIDINE; APC PROTEIN; APOPTOTIC PROTEASE ACTIVATING FACTOR 1; ARF PROTEIN; AROMATIC AMINE; AZACITIDINE; CASPASE 8; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DEATH ASSOCIATED PROTEIN KINASE; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; FRAGILE HISTIDINE TRIAD PROTEIN; GLUTATHIONE TRANSFERASE P1; LAMININ ALPHA3; LAMININ BETA3; LAMININ GAMMA2; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; MICRORNA; PEPTIDES AND PROTEINS; PROTEIN CDH13; RAS ASSOCIATION DOMAIN FAMILY PROTEIN 1A; RETINOID RELATED ORPHAN RECEPTOR BETA; SOMATOMEDIN BINDING PROTEIN 3; TISSUE INHIBITOR OF METALLOPROTEINASE 3; TRANSCRIPTION FACTOR SOX11; UNCLASSIFIED DRUG; UNINDEXED DRUG; UVOMORULIN;

3' UNTRANSLATED REGION; BLADDER CANCER; CARCINOGENESIS; DNA METHYLATION; EPIGENETICS; FOOD AND DRUG ADMINISTRATION; GENE EXPRESSION; HUMAN; OCCUPATIONAL EXPOSURE; POLYMERASE CHAIN REACTION; PYROSEQUENCING; REVIEW; SMOKING; T CELL LYMPHOMA; TRANSITIONAL CELL CARCINOMA;

ANIMALIA;

ABERRANT DNA METHYLATION; ANIMAL MODELS; EPIGENETICS; TRANSITIONAL CELL CARCINOMA; TUMORIGENESIS;

AMINES; CARCINOGENESIS; DNA METHYLATION; EPIGENESIS, GENETIC; HUMANS; MICRORNAS; SMOKING; URINARY BLADDER NEOPLASMS;

EID: 84884948884     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.4161/epi.25927     Document Type: Review

References (169)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011; 61: 69-90; PMID: 21296855; http://dx. doi. org/10. 3322/caac. 20107
2. American Cancer Society (ACS). Cancer Facts & Figures 2013. ACS National Home Office, Atlanta, GA, 2013.
3. World Health Organization (WHO). WHO report on the global tobacco epidemic, 2008: the MPOWER package. 2008.
4. Babjuk M, Oosterlinck W, Sylvester R, Kaasinen E, Böhle A, Palou-Redorta J, et al.; European Association of Urology (EAU). EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder, the 2011 update. Eur Urol 2011; 59: 997-1008; PMID: 21458150; http://dx. doi. org/10. 1016/j. eururo. 2011. 03. 017
5. Carradori S, Cristini C, Secci D, Gulia C, Gentile V, Di Pierro GB. Current and emerging strategies in bladder cancer. Anticancer Agents Med Chem 2012; 12: 589-603; PMID: 22043990; http://dx. doi. org/10. 2174/187152012800617768
6. Prasad SM, Decastro GJ, Steinberg GD; Medscape. Urothelial carcinoma of the bladder: definition, treatment and future efforts. Nat Rev Urol 2011; 8: 631-42; PMID: 21989305; http://dx. doi. org/10. 1038/nrurol. 2011. 144
7. Kurth KH, Denis L, Bouffioux C, Sylvester R, Debruyne FM, Pavone-Macaluso M, et al. Factors affecting recurrence and progression in superficial bladder tumours. Eur J Cancer 1995; 31A: 1840-6; PMID: 8541110; http://dx. doi. org/10. 1016/0959-8049(95)00287-S
8. Allard P, Bernard P, Fradet Y, Têtu B. The early clinical course of primary Ta and T1 bladder cancer: a proposed prognostic index. Br J Urol 1998; 81: 692-8; PMID: 9634043; http://dx. doi. org/10. 1046/j. 1464-410x. 1998. 00628. x
9. Sylvester RJ, van der Meijden AP, Oosterlinck W, Witjes JA, Bouffioux C, Denis L, et al. Predicting recurrence and progression in individual patients with stage Ta T1 bladder cancer using EORTC risk tables: a combined analysis of 2596 patients from seven EORTC trials. Eur Urol 2006; 49: 466-5, discussion 475-7; PMID: 16442208; http://dx. doi. org/10. 1016/j. eururo. 2005. 12. 031
10. Cheng L, Zhang S, MacLennan GT, Williamson SR, Lopez-Beltran A, Montironi R. Bladder cancer: translating molecular genetic insights into clinical practice. Hum Pathol 2011; 42: 455-81; PMID: 21106220; http://dx. doi. org/10. 1016/j. humpath. 2010. 07. 007
11. Kriegmair M, Baumgartner R, Knüchel R, Stepp H, Hofstädter F, Hofstetter A. Detection of early bladder cancer by 5-aminolevulinic acid induced porphyrin fluorescence. J Urol 1996; 155: 105-9, discussion 109-10; PMID: 7490803; http://dx. doi. org/10. 1016/S0022-5347(01)66559-5
12. Denzinger S, Burger M, Walter B, Knuechel R, Roessler W, Wieland WF, et al. Clinically relevant reduction in risk of recurrence of superficial bladder cancer using 5-aminolevulinic acid-induced fluorescence diagnosis: 8-year results of prospective randomized study. Urology 2007; 69: 675-9; PMID: 17445650; http://dx. doi. org/10. 1016/j. urology. 2006. 12. 023
13. Zaak D, Kriegmair M, Stepp H, Stepp H, Baumgartner R, Oberneder R, et al. Endoscopic detection of transitional cell carcinoma with 5-aminolevulinic acid: results of 1012 fluorescence endoscopies. Urology 2001; 57: 690-4; PMID: 11306382; http://dx. doi. org/10. 1016/S0090-4295(00)01053-0
14. Stenzl A, Cowan NC, De Santis M, Kuczyk MA, Merseburger AS, Ribal MJ, et al.; European Association of Urology (EAU). Treatment of muscle-invasive and metastatic bladder cancer: update of the EAU guidelines. Eur Urol 2011; 59: 1009-18; PMID: 21454009; http://dx. doi. org/10. 1016/j. eururo. 2011. 03. 023
15. Morgan TM, Keegan KA, Clark PE. Bladder cancer. Curr Opin Oncol 2011; 23: 275-82; PMID: 21311329; http://dx. doi. org/10. 1097/CCO. 0b013e3283446a11
16. Papanicolaou GN, Marshall VF. Urine Sediment Smears as a Diagnostic Procedure in Cancers of the Urinary Tract. Science 1945; 101: 519-20; PMID: 17775845; http://dx. doi. org/10. 1126/science. 101. 2629. 519
17. Lotan Y, Roehrborn CG. Sensitivity and specificity of commonly available bladder tumor markers versus cytology: results of a comprehensive literature review and meta-analyses. Urology 2003; 61: 109-18, discussion 118; PMID: 12559279; http://dx. doi. org/10. 1016/S0090-4295(02)02136-2
18. van Rhijn BW, van der Poel HG, van der Kwast TH. Urine markers for bladder cancer surveillance: a systematic review. Eur Urol 2005; 47: 736-48; PMID: 15925067; http://dx. doi. org/10. 1016/j. eururo. 2005. 03. 014
19. Hajdinjak T. UroVysion FISH test for detecting urothelial cancers: meta-analysis of diagnostic accuracy and comparison with urinary cytology testing. Urol Oncol 2008; 26: 646-51; PMID: 18367109; http://dx. doi. org/10. 1016/j. urolonc. 2007. 06. 002
20. Parker J, Spiess PE. Current and emerging bladder cancer urinary biomarkers. ScientificWorldJournal 2011; 11: 1103-12; PMID: 21623456; http://dx. doi. org/10. 1100/tsw. 2011. 104
21. Bhatt J, Cowan N, Protheroe A, Crew J. Recent advances in urinary bladder cancer detection. Expert Rev Anticancer Ther 2012; 12: 929-39; PMID: 22845408; http://dx. doi. org/10. 1586/era. 12. 73
22. Gakis G, Schwentner C, Todenhöfer T, Stenzl A. Current status of molecular markers for prognostication and outcome in invasive bladder cancer. BJU Int 2012; 110: 233-7; PMID: 22233187; http://dx. doi. org/10. 1111/j. 1464-410X. 2011. 10839. x
23. Netto GJ, Cheng L. Emerging critical role of molecular testing in diagnostic genitourinary pathology. Arch Pathol Lab Med 2012; 136: 372-90; PMID: 22458900; http://dx. doi. org/10. 5858/arpa. 2011-0471-RA
24. Besaratinia A, Tommasi S. Genotoxicity of tobacco smoke-derived aromatic amines and bladder cancer: current state of knowledge and future research directions. FASEB J 2013; 27: 2090-100; PMID: 23449930; http://dx. doi. org/10. 1096/fj. 12-227074
25. Baylin SB, Jones PA. A decade of exploring the cancer epigenome-biological and translational implications. Nat Rev Cancer 2011; 11: 726-34; PMID: 21941284; http://dx. doi. org/10. 1038/nrc3130
26. Berdasco M, Esteller M. Aberrant epigenetic landscape in cancer: how cellular identity goes awry. Dev Cell 2010; 19: 698-711; PMID: 21074720; http://dx. doi. org/10. 1016/j. devcel. 2010. 10. 005
27. Shen H, Laird PW. Interplay between the cancer genome and epigenome. Cell 2013; 153: 38-55; PMID: 23540689; http://dx. doi. org/10. 1016/j. cell. 2013. 03. 008
28. Portela A, Esteller M. Epigenetic modifications and human disease. Nat Biotechnol 2010; 28: 1057-68; PMID: 20944598; http://dx. doi. org/10. 1038/nbt. 1685
29. Tsai HC, Baylin SB. Cancer epigenetics: linking basic biology to clinical medicine. Cell Res 2011; 21: 502-17; PMID: 21321605; http://dx. doi. org/10. 1038/cr. 2011. 24
30. Grønbaek K, Hother C, Jones PA. Epigenetic changes in cancer. APMIS 2007; 115: 1039-59; PMID: 18042143; http://dx. doi. org/10. 1111/j. 1600-0463. 2007. apm_636. xml. x
31. Kulis M, Esteller M. DNA methylation and cancer. Adv Genet 2010; 70: 27-56; PMID: 20920744; http://dx. doi. org/10. 1016/B978-0-12-380866-0. 60002-2
32. Laird PW. Principles and challenges of genomewide DNA methylation analysis. Nat Rev Genet 2010; 11: 191-203; PMID: 20125086; http://dx. doi. org/10. 1038/nrg2732
33. Rodríguez-Paredes M, Esteller M. Cancer epigenetics reaches mainstream oncology. Nat Med 2011; 17: 330-9; PMID: 21386836; http://dx. doi. org/10. 1038/nm. 2305
34. Rhee I, Bachman KE, Park BH, Jair KW, Yen RW, Schuebel KE, et al. DNMT1 and DNMT3b cooperate to silence genes in human cancer cells. Nature 2002; 416: 552-6; PMID: 11932749; http://dx. doi. org/10. 1038/416552a
35. Gius D, Cui H, Bradbury CM, Cook J, Smart DK, Zhao S, et al. Distinct effects on gene expression of chemical and genetic manipulation of the cancer epigenome revealed by a multimodality approach. Cancer Cell 2004; 6: 361-71; PMID: 15488759; http://dx. doi. org/10. 1016/j. ccr. 2004. 08. 029
36. Jacinto FV, Ballestar E, Esteller M. Impaired recruitment of the histone methyltransferase DOT1L contributes to the incomplete reactivation of tumor suppressor genes upon DNA demethylation. Oncogene 2009; 28: 4212-24; PMID: 19734945; http://dx. doi. org/10. 1038/onc. 2009. 267
37. Yang X, Lay F, Han H, Jones PA. Targeting DNA methylation for epigenetic therapy. Trends Pharmacol Sci 2010; 31: 536-46; PMID: 20846732; http://dx. doi. org/10. 1016/j. tips. 2010. 08. 001
38. Ibragimova I, Ibáñez de Cáceres I, Hoffman AM, Potapova A, Dulaimi E, Al-Saleem T, et al. Global reactivation of epigenetically silenced genes in prostate cancer. Cancer Prev Res (Phila) 2010; 3: 1084-92; PMID: 20699414; http://dx. doi. org/10. 1158/1940-6207. CAPR-10-0039
39. Chung W, Bondaruk J, Jelinek J, Lotan Y, Liang S, Czerniak B, et al. Detection of bladder cancer using novel DNA methylation biomarkers in urine sediments. Cancer Epidemiol Biomarkers Prev 2011; 20: 1483-91; PMID: 21586619; http://dx. doi. org/10. 1158/1055-9965. EPI-11-0067
40. Wolff EM, Chihara Y, Pan F, Weisenberger DJ, Siegmund KD, Sugano K, et al. Unique DNA methylation patterns distinguish noninvasive and invasive urothelial cancers and establish an epigenetic field defect in premalignant tissue. Cancer Res 2010; 70: 8169-78; PMID: 20841482; http://dx. doi. org/10. 1158/0008-5472. CAN-10-1335
41. Sánchez-Carbayo M. Hypermethylation in bladder cancer: biological pathways and translational applications. Tumour Biol 2012; 33: 347-61; PMID: 22274923; http://dx. doi. org/10. 1007/s13277-011-0310-2
42. Momparler RL. Epigenetic therapy of cancer with 5-aza-2'-deoxycytidine (decitabine). Semin Oncol 2005; 32: 443-51; PMID: 16210084; http://dx. doi. org/10. 1053/j. seminoncol. 2005. 07. 008
43. O'Rourke CJ, Knabben V, Bolton E, Moran D, Lynch T, Hollywood D, et al. Manipulating the epigenome for the treatment of urological malignancies. Pharmacol Ther 2013; 138: 185-96; PMID: 23353098; http://dx. doi. org/10. 1016/j. pharmthera. 2013. 01. 007
44. Kandimalla R, van Tilborg AA, Zwarthoff EC. DNA methylation-based biomarkers in bladder cancer. Nat Rev Urol 2013; 10: 327-35; PMID: 23628807; http://dx. doi. org/10. 1038/nrurol. 2013. 89
45. Markl ID, Cheng J, Liang G, Shibata D, Laird PW, Jones PA. Global and gene-specific epigenetic patterns in human bladder cancer genomes are relatively stable in vivo and in vitro over time. Cancer Res 2001; 61: 5875-84; PMID: 11479229
46. Maruyama R, Toyooka S, Toyooka KO, Harada K, Virmani AK, Zöchbauer-Müller S, et al. Aberrant promoter methylation profile of bladder cancer and its relationship to clinicopathological features. Cancer Res 2001; 61: 8659-63; PMID: 11751381
47. Sathyanarayana UG, Maruyama R, Padar A, Suzuki M, Bondaruk J, Sagalowsky A, et al. Molecular detection of noninvasive and invasive bladder tumor tissues and exfoliated cells by aberrant promoter methylation of laminin-5 encoding genes. Cancer Res 2004; 64: 1425-30; PMID: 14973053; http://dx. doi. org/10. 1158/0008-5472. CAN-03-0701
48. Christoph F, Weikert S, Kempkensteffen C, Krause H, Schostak M, Miller K, et al. Regularly methylated novel pro-apoptotic genes associated with recurrence in transitional cell carcinoma of the bladder. Int J Cancer 2006; 119: 1396-402; PMID: 16642478; http://dx. doi. org/10. 1002/ijc. 21971
49. Hoque MO, Begum S, Topaloglu O, Chatterjee A, Rosenbaum E, Van Criekinge W, et al. Quantitation of promoter methylation of multiple genes in urine DNA and bladder cancer detection. J Natl Cancer Inst 2006; 98: 996-1004; PMID: 16849682; http://dx. doi. org/10. 1093/jnci/djj265
50. Wolff EM, Liang G, Cortez CC, Tsai YC, Castelao JE, Cortessis VK, et al. RUNX3 methylation reveals that bladder tumors are older in patients with a history of smoking. Cancer Res 2008; 68: 6208-14; PMID: 18676844; http://dx. doi. org/10. 1158/0008-5472. CAN-07-6616
51. Nishiyama N, Arai E, Chihara Y, Fujimoto H, Hosoda F, Shibata T, et al. Genome-wide DNA methylation profiles in urothelial carcinomas and urothelia at the precancerous stage. Cancer Sci 2010; 101: 231-40; PMID: 19775289; http://dx. doi. org/10. 1111/j. 1349-7006. 2009. 01330. x
52. Jones PA, Baylin SB. The epigenomics of cancer. Cell 2007; 128: 683-92; PMID: 17320506; http://dx. doi. org/10. 1016/j. cell. 2007. 01. 029
53. Bird A, Macleod D. Reading the DNA methylation signal. Cold Spring Harb Symp Quant Biol 2004; 69: 113-8; PMID: 16117639; http://dx. doi. org/10. 1101/sqb. 2004. 69. 113
54. Esteller M. Epigenetics in cancer. N Engl J Med 2008; 358: 1148-59; PMID: 18337604; http://dx. doi. org/10. 1056/NEJMra072067
55. Feinberg AP, Tycko B. The history of cancer epigenetics. Nat Rev Cancer 2004; 4: 143-53; PMID: 14732866; http://dx. doi. org/10. 1038/nrc1279
56. Suzuki MM, Bird A. DNA methylation landscapes: provocative insights from epigenomics. Nat Rev Genet 2008; 9: 465-76; PMID: 18463664; http://dx. doi. org/10. 1038/nrg2341
57. Takai D, Jones PA. Comprehensive analysis of CpG islands in human chromosomes 21 and 22. Proc Natl Acad Sci U S A 2002; 99: 3740-5; PMID: 11891299; http://dx. doi. org/10. 1073/pnas. 052410099
58. Fernandez AF, Assenov Y, Martin-Subero JI, Balint B, Siebert R, Taniguchi H, et al. A DNA methylation fingerprint of 1628 human samples. Genome Res 2012; 22: 407-19; PMID: 21613409; http://dx. doi. org/10. 1101/gr. 119867. 110
59. Hansen KD, Timp W, Bravo HC, Sabunciyan S, Langmead B, McDonald OG, et al. Increased methylation variation in epigenetic domains across cancer types. Nat Genet 2011; 43: 768-75; PMID: 21706001; http://dx. doi. org/10. 1038/ng. 865
60. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev 2011; 25: 1010-22; PMID: 21576262; http://dx. doi. org/10. 1101/gad. 2037511
61. Varley KE, Gertz J, Bowling KM, Parker SL, Reddy TE, Pauli-Behn F, et al. Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 2013; 23: 555-67; PMID: 23325432; http://dx. doi. org/10. 1101/gr. 147942. 112
62. Feinberg AP, Vogelstein B. Hypomethylation distinguishes genes of some human cancers from their normal counterparts. Nature 1983; 301: 89-92; PMID: 6185846; http://dx. doi. org/10. 1038/301089a0
63. Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim Biophys Acta 2007; 1775: 138-62; PMID: 17045745
64. Jones PA, Liang G. Rethinking how DNA methylation patterns are maintained. Nat Rev Genet 2009; 10: 805-11; PMID: 19789556; http://dx. doi. org/10. 1038/nrg2651
65. Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 2012; 13: 484-92; PMID: 22641018; http://dx. doi. org/10. 1038/nrg3230
66. Maunakea AK, Nagarajan RP, Bilenky M, Ballinger TJ, D'Souza C, Fouse SD, et al. Conserved role of intragenic DNA methylation in regulating alternative promoters. Nature 2010; 466: 253-7; PMID: 20613842; http://dx. doi. org/10. 1038/nature09165
67. Ehrlich M. DNA hypomethylation in cancer cells. Epigenomics 2009; 1: 239-59; PMID: 20495664; http://dx. doi. org/10. 2217/epi. 09. 33
68. Nagarajan RP, Costello JF. Epigenetic mechanisms in glioblastoma multiforme. Semin Cancer Biol 2009; 19: 188-97; PMID: 19429483; http://dx. doi. org/10. 1016/j. semcancer. 2009. 02. 005
69. Nagarajan RP, Fouse SD, Bell RJ, Costello JF. Methods for cancer epigenome analysis. Adv Exp Med Biol 2013; 754: 313-38; PMID: 22956508; http://dx. doi. org/10. 1007/978-1-4419-9967-2_15
70. Estécio MR, Issa JP. Tackling the methylome: recent methodological advances in genome-wide methylation profiling. Genome Med 2009; 1: 106; PMID: 19930617; http://dx. doi. org/10. 1186/gm106
71. Estécio MR, Yan PS, Ibrahim AE, Tellez CS, Shen L, Huang TH, et al. High-throughput methylation profiling by MCA coupled to CpG island microarray. Genome Res 2007; 17: 1529-36; PMID: 17785535; http://dx. doi. org/10. 1101/gr. 6417007
72. Shen L, Kondo Y, Guo Y, Zhang J, Zhang L, Ahmed S, et al. Genome-wide profiling of DNA methylation reveals a class of normally methylated CpG island promoters. PLoS Genet 2007; 3: 2023-36; PMID: 17967063; http://dx. doi. org/10. 1371/journal. pgen. 0030181
73. Dudziec E, Goepel JR, Catto JW. Global epigenetic profiling in bladder cancer. Epigenomics 2011; 3: 35-45; PMID: 22126151; http://dx. doi. org/10. 2217/epi. 10. 71
74. Kim WJ, Kim YJ. Epigenetics of bladder cancer. Methods Mol Biol 2012; 863: 111-8; PMID: 22359289; http://dx. doi. org/10. 1007/978-1-61779-612-8_6
75. Huepper WC, Wiely FH, Wolfe HD, Ranta KE, Leming MF, Blood FR. Experimental production of bladder tumors in dogs by administration of β-naphthylamine. J Ind Hyg Toxicol 1938; 3: 46-84
76. Spitz S, Maguigan WH, Dobriner K. The carcinogenic action of benzidine. Cancer 1950; 3: 789-804; PMID: 14772711; http://dx. doi. org/10. 1002/1097-0142(1950)3: 5<789: AIDCNCR2820030505> 3. 0. CO; 2-U
77. Walpole AL, Williams MHC, Roberts DC. Tumours of the urinary bladder in dogs after ingestion of 4-aminodiphenyl. Br J Ind Med 1954; 11: 105-9; PMID: 13149742
78. Wanibuchi H, Salim EI, Kinoshita A, Shen J, Wei M, Morimura K, et al. Understanding arsenic carcinogenicity by the use of animal models. Toxicol Appl Pharmacol 2004; 198: 366-76; PMID: 15276416; http://dx. doi. org/10. 1016/j. taap. 2003. 10. 032
79. Kitchin KT. Recent advances in arsenic carcinogenesis: modes of action, animal model systems, and methylated arsenic metabolites. Toxicol Appl Pharmacol 2001; 172: 249-61; PMID: 11312654; http://dx. doi. org/10. 1006/taap. 2001. 9157
80. Besaratinia A, Pfeifer GP. Investigating human cancer etiology by DNA lesion footprinting and mutagenicity analysis. Carcinogenesis 2006; 27: 1526-37; PMID: 16344267; http://dx. doi. org/10. 1093/carcin/bgi311
81. Ahmad I, Sansom OJ, Leung HY. Exploring molecular genetics of bladder cancer: lessons learned from mouse models. Dis Model Mech 2012; 5: 323-32; PMID: 22422829; http://dx. doi. org/10. 1242/dmm. 008888
82. Washington MK, Powell AE, Sullivan R, Sundberg JP, Wright N, Coffey RJ, et al. Pathology of rodent models of intestinal cancer: progress report and recommendations. Gastroenterology 2013; 144: 705-17; PMID: 23415801; http://dx. doi. org/10. 1053/j. gastro. 2013. 01. 067
83. Langdon SP. Animal modeling of cancer pathology and studying tumor response to therapy. Curr Drug Targets 2012; 13: 1535-47; PMID: 22974396; http://dx. doi. org/10. 2174/138945012803530152
84. U. S. Department of Health and Human Services. The health consequences of smoking: a report of the Surgeon General. U. S. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health, Atlanta, GA, 2004.
85. Boffetta P. Tobacco smoking and risk of bladder cancer. Scand J Urol Nephrol Suppl 2008; 218: 45-54; PMID: 18815916; http://dx. doi. org/10. 1080/03008880802283664
86. Kiriluk KJ, Prasad SM, Patel AR, Steinberg GD, Smith ND. Bladder cancer risk from occupational and environmental exposures. Urol Oncol 2012; 30: 199-211; PMID: 22385990; http://dx. doi. org/10. 1016/j. urolonc. 2011. 10. 010
87. Vineis P, Pirastu R. Aromatic amines and cancer. Cancer Causes Control 1997; 8: 346-55; PMID: 9498898; http://dx. doi. org/10. 1023/A: 1018453104303
88. Patrianakos C, Hoffman D. Chemical studies on tobacco smoke LXIV. On the analysis of aromatic amines in cigarette smoke. J Anal Chem 1979; 3: 150-4
89. D'Avanzo B, Negri E, La Vecchia C, Gramenzi A, Bianchi C, Franceschi S, et al. Cigarette smoking and bladder cancer. Eur J Cancer 1990; 26: 714-8; PMID: 2144159; http://dx. doi. org/10. 1016/0277-5379(90)90124-C
90. Vineis P, Esteve J, Hartge P, Hoover R, Silverman DT, Terracini B. Effects of timing and type of tobacco in cigarette-induced bladder cancer. Cancer Res 1988; 48: 3849-52; PMID: 3378220
91. Bartsch H, Malaveille C, Friesen M, Kadlubar FF, Vineis P. Black (air-cured) and blond (flue-cured) tobacco cancer risk. IV: Molecular dosimetry studies implicate aromatic amines as bladder carcinogens. Eur J Cancer 1993; 29A: 1199-207; PMID: 8518034; http://dx. doi. org/10. 1016/S0959-8049(05)80315-6
92. Besaratinia A, Bates SE, Pfeifer GP. Mutational signature of the proximate bladder carcinogen N-hydroxy-4-acetylaminobiphenyl: inconsistency with the p53 mutational spectrum in bladder cancer. Cancer Res 2002; 62: 4331-8; PMID: 12154037
93. Kadlubar FF, Beland FA, Beranek DT, Dooley KL, Heflich RH, Evans FE. Arylamine-DNA adduct formation in relation to urinary bladder carcinogenesis and Salmonella typhimurium mutagenesis. In: Sugimura T, Kondo S, Takebe H, eds. Environmental mutagens and carcinogens. New York, NY: Alan R. Liss, 1982: 385-96.
94. Talaska G, al-Juburi AZ, Kadlubar FF. Smoking related carcinogen-DNA adducts in biopsy samples of human urinary bladder: identification of N-(deoxyguanosin-8-yl)-4-aminobiphenyl as a major adduct. Proc Natl Acad Sci U S A 1991; 88: 5350-4; PMID: 2052611; http://dx. doi. org/10. 1073/pnas. 88. 12. 5350
95. Yoon JI, Kim SI, Tommasi S, Besaratinia A. Organ specificity of the bladder carcinogen 4-aminobiphenyl in inducing DNA damage and mutation in mice. Cancer Prev Res (Phila) 2012; 5: 299-308; PMID: 22086680; http://dx. doi. org/10. 1158/1940-6207. CAPR-11-0309
96. Thompson PA, DeMarini DM, Kadlubar FF, McClure GY, Brooks LR, Green BL, et al. Evidence for the presence of mutagenic arylamines in human breast milk and DNA adducts in exfoliated breast ductal epithelial cells. Environ Mol Mutagen 2002; 39: 134-42; PMID: 11921181; http://dx. doi. org/10. 1002/em. 10067
97. Zayas B, Stillwell SW, Wishnok JS, Trudel LJ, Skipper P, Yu MC, et al. Detection and quantification of 4-ABP adducts in DNA from bladder cancer patients. Carcinogenesis 2007; 28: 342-9; PMID: 16926175; http://dx. doi. org/10. 1093/carcin/bgl142
98. Faraglia B, Chen SY, Gammon MD, Zhang Y, Teitelbaum SL, Neugut AI, et al. Evaluation of 4-aminobiphenyl-DNA adducts in human breast cancer: the influence of tobacco smoke. Carcinogenesis 2003; 24: 719-25; PMID: 12727801; http://dx. doi. org/10. 1093/carcin/bgg013
99. Besaratinia A, Pfeifer GP. DNA damage and mutagenesis induced by polycyclic aromatic hydrocarbons. In: Luch A, ed. The carcinogenic effects of polycyclic aromatic hydrocarbons. London, UK: Imperial College Press, 2005: 171-210.
100. Luch A. Nature and nurture-lessons from chemical carcinogenesis. Nat Rev Cancer 2005; 5: 113-25; PMID: 15660110; http://dx. doi. org/10. 1038/nrc1546
101. Poirier MC. Chemical-induced DNA damage and human cancer risk. Nat Rev Cancer 2004; 4: 630-7; PMID: 15286742; http://dx. doi. org/10. 1038/nrc1410
102. International Agency for Research on Cancer (IARC). Some aromatic amines, hydrazine and related substances, N-nitroso compounds and miscellaneous alkylating agents. 2-Naphthylamine. Lyon (France), 1974: 97-111.
103. Parkes HG, Evans AEJ. Epidemiology of aromatic amine cancers. In: Searle CE, ed. Chemical carcinogens. Washington D. C.: American Chemical Society, 1984: 277-301.
104. Steineck G, Plato N, Norell SE, Hogstedt C. Urothelial cancer and some industry-related chemicals: an evaluation of the epidemiologic literature. Am J Ind Med 1990; 17: 371-91; PMID: 2407118; http://dx. doi. org/10. 1002/ajim. 4700170310
105. Carthew RW, Sontheimer EJ. Origins and Mechanisms of miRNAs and siRNAs. Cell 2009; 136: 642-55; PMID: 19239886; http://dx. doi. org/10. 1016/j. cell. 2009. 01. 035
106. Garzon R, Calin GA, Croce CM. MicroRNAs in Cancer. Annu Rev Med 2009; 60: 167-79; PMID: 19630570; http://dx. doi. org/10. 1146/annurev. med. 59. 053006. 104707
107. Winter J, Diederichs S. MicroRNA biogenesis and cancer. Methods Mol Biol 2011; 676: 3-22; PMID: 20931386; http://dx. doi. org/10. 1007/978-1-60761-863-8_1
108. Lee Y, Jeon K, Lee JT, Kim S, Kim VN. MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 2002; 21: 4663-70; PMID: 12198168; http://dx. doi. org/10. 1093/emboj/cdf476
109. Davis-Dusenbery BN, Hata A. Mechanisms of control of microRNA biogenesis. J Biochem 2010; 148: 381-92; PMID: 20833630
110. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116: 281-97; PMID: 14744438; http://dx. doi. org/10. 1016/S0092-8674(04)00045-5
111. Kozomara A, Griffiths-Jones S. miRBase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011; 39(Database issue): D152-7; PMID: 21037258; http://dx. doi. org/10. 1093/nar/gkq1027
112. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005; 120: 15-20; PMID: 15652477; http://dx. doi. org/10. 1016/j. cell. 2004. 12. 035
113. Lu J, Getz G, Miska EA, Alvarez-Saavedra E, Lamb J, Peck D, et al. MicroRNA expression profiles classify human cancers. Nature 2005; 435: 834-8; PMID: 15944708; http://dx. doi. org/10. 1038/nature03702
114. Friedman RC, Farh KK, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res 2009; 19: 92-105; PMID: 18955434; http://dx. doi. org/10. 1101/gr. 082701. 108
115. Lim LP, Lau NC, Garrett-Engele P, Grimson A, Schelter JM, Castle J, et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 2005; 433: 769-73; PMID: 15685193; http://dx. doi. org/10. 1038/nature03315
116. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-69; PMID: 16557279; http://dx. doi. org/10. 1038/nrc1840
117. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10: 704-14; PMID: 19763153; http://dx. doi. org/10. 1038/nrg2634
118. Esteller M. Non-coding RNAs in human disease. Nat Rev Genet 2011; 12: 861-74; PMID: 22094949; http://dx. doi. org/10. 1038/nrg3074
119. Ventura A, Jacks T. MicroRNAs and cancer: short RNAs go a long way. Cell 2009; 136: 586-91; PMID: 19239879; http://dx. doi. org/10. 1016/j. cell. 2009. 02. 005
120. Fabbri M, Calin GA. Epigenetics and miRNAs in human cancer. Adv Genet 2010; 70: 87-99; PMID: 20920746; http://dx. doi. org/10. 1016/B978-0-12-380866-0. 60004-6
121. Davalos V, Esteller M. MicroRNAs and cancer epigenetics: a macrorevolution. Curr Opin Oncol 2010; 22: 35-45; PMID: 19907325; http://dx. doi. org/10. 1097/CCO. 0b013e328333dcbb
122. Ayala de la Peña F, Kanasaki K, Kanasaki M, Tangirala N, Maeda G, Kalluri R. Loss of p53 and acquisition of angiogenic microRNA profile are insufficient to facilitate progression of bladder urothelial carcinoma in situ to invasive carcinoma. J Biol Chem 2011; 286: 20778-87; PMID: 21388952; http://dx. doi. org/10. 1074/jbc. M110. 198069
123. Dyrskjøt L, Ostenfeld MS, Bramsen JB, Silahtaroglu AN, Lamy P, Ramanathan R, et al. Genomic profiling of microRNAs in bladder cancer: miR-129 is associated with poor outcome and promotes cell death in vitro. Cancer Res 2009; 69: 4851-60; PMID: 19487295; http://dx. doi. org/10. 1158/0008-5472. CAN-08-4043
124. Han Y, Chen J, Zhao X, Liang C, Wang Y, Sun L, et al. MicroRNA expression signatures of bladder cancer revealed by deep sequencing. PLoS One 2011; 6: e18286; PMID: 21464941; http://dx. doi. org/10. 1371/journal. pone. 0018286
125. Ichimi T, Enokida H, Okuno Y, Kunimoto R, Chiyomaru T, Kawamoto K, et al. Identification of novel microRNA targets based on microRNA signatures in bladder cancer. Int J Cancer 2009; 125: 345-52; PMID: 19378336; http://dx. doi. org/10. 1002/ijc. 24390
126. Catto JW, Miah S, Owen HC, Bryant H, Myers K, Dudziec E, et al. Distinct microRNA alterations characterize high-and low-grade bladder cancer. Cancer Res 2009; 69: 8472-81; PMID: 19843843; http://dx. doi. org/10. 1158/0008-5472. CAN-09-0744
127. Neely LA, Rieger-Christ KM, Neto BS, Eroshkin A, Garver J, Patel S, et al. A microRNA expression ratio defining the invasive phenotype in bladder tumors. Urol Oncol 2010; 28: 39-48; PMID: 18799331; http://dx. doi. org/10. 1016/j. urolonc. 2008. 06. 006
128. Adam L, Zhong M, Choi W, Qi W, Nicoloso M, Arora A, et al. miR-200 expression regulates epithelialto-mesenchymal transition in bladder cancer cells and reverses resistance to epidermal growth factor receptor therapy. Clin Cancer Res 2009; 15: 5060-72; PMID: 19671845; http://dx. doi. org/10. 1158/1078-0432. CCR-08-2245
129. Yamada Y, Enokida H, Kojima S, Kawakami K, Chiyomaru T, Tatarano S, et al. MiR-96 and miR-183 detection in urine serve as potential tumor markers of urothelial carcinoma: correlation with stage and grade, and comparison with urinary cytology. Cancer Sci 2011; 102: 522-9; PMID: 21166959; http://dx. doi. org/10. 1111/j. 1349-7006. 2010. 01816. x
130. Miah S, Dudziec E, Drayton RM, Zlotta AR, Morgan SL, Rosario DJ, et al. An evaluation of urinary microRNA reveals a high sensitivity for bladder cancer. Br J Cancer 2012; 107: 123-8; PMID: 22644299; http://dx. doi. org/10. 1038/bjc. 2012. 221
131. Saito Y, Jones PA. Epigenetic activation of tumor suppressor microRNAs in human cancer cells. Cell Cycle 2006; 5: 2220-2; PMID: 17012846; http://dx. doi. org/10. 4161/cc. 5. 19. 3340
132. Vogt M, Munding J, Grüner M, Liffers ST, Verdoodt B, Hauk J, et al. Frequent concomitant inactivation of miR-34a and miR-34b/c by CpG methylation in colorectal, pancreatic, mammary, ovarian, urothelial, and renal cell carcinomas and soft tissue sarcomas. Virchows Arch 2011; 458: 313-22; PMID: 21225432; http://dx. doi. org/10. 1007/s00428-010-1030-5
133. Zhu J, Jiang Z, Gao F, Hu X, Zhou L, Chen J, et al. A systematic analysis on DNA methylation and the expression of both mRNA and microRNA in bladder cancer. PLoS One 2011; 6: e28223; PMID: 22140553; http://dx. doi. org/10. 1371/journal. pone. 0028223
134. Saito Y, Liang G, Egger G, Friedman JM, Chuang JC, Coetzee GA, et al. Specific activation of microRNA-127 with downregulation of the proto-oncogene BCL6 by chromatin-modifying drugs in human cancer cells. Cancer Cell 2006; 9: 435-43; PMID: 16766263; http://dx. doi. org/10. 1016/j. ccr. 2006. 04. 020
135. Dudziec E, Miah S, Choudhry HM, Owen HC, Blizard S, Glover M, et al. Hypermethylation of CpG islands and shores around specific microRNAs and mirtrons is associated with the phenotype and presence of bladder cancer. Clin Cancer Res 2011; 17: 1287-96; PMID: 21138856; http://dx. doi. org/10. 1158/1078-0432. CCR-10-2017
136. Wiklund ED, Bramsen JB, Hulf T, Dyrskjøt L, Ramanathan R, Hansen TB, et al. Coordinated epigenetic repression of the miR-200 family and miR-205 in invasive bladder cancer. Int J Cancer 2011; 128: 1327-34; PMID: 20473948; http://dx. doi. org/10. 1002/ijc. 25461
137. Shimizu T, Suzuki H, Nojima M, Kitamura H, Yamamoto E, Maruyama R, et al. Methylation of a panel of microRNA genes is a novel biomarker for detection of bladder cancer. Eur Urol 2013; 63: 1091-100; PMID: 23200812; http://dx. doi. org/10. 1016/j. eururo. 2012. 11. 030
138. Yoshitomi T, Kawakami K, Enokida H, Chiyomaru T, Kagara I, Tatarano S, et al. Restoration of miR-517a expression induces cell apoptosis in bladder cancer cell lines. Oncol Rep 2011; 25: 1661-8; PMID: 21479368
139. Yoshino H, Chiyomaru T, Enokida H, Kawakami K, Tatarano S, Nishiyama K, et al. The tumoursuppressive function of miR-1 and miR-133a targeting TAGLN2 in bladder cancer. Br J Cancer 2011; 104: 808-18; PMID: 21304530; http://dx. doi. org/10. 1038/bjc. 2011. 23
140. Liep J, Rabien A, Jung K. Feedback networks between microRNAs and epigenetic modifications in urological tumors. Epigenetics 2012; 7: 315-25; PMID: 22414795; http://dx. doi. org/10. 4161/epi. 19464
141. Schaefer A, Stephan C, Busch J, Yousef GM, Jung K. Diagnostic, prognostic and therapeutic implications of microRNAs in urologic tumors. Nat Rev Urol 2010; 7: 286-97; PMID: 20368743; http://dx. doi. org/10. 1038/nrurol. 2010. 45
142. Egger G, Liang G, Aparicio A, Jones PA. Epigenetics in human disease and prospects for epigenetic therapy. Nature 2004; 429: 457-63; PMID: 15164071; http://dx. doi. org/10. 1038/nature02625
143. Kelly TK, De Carvalho DD, Jones PA. Epigenetic modifications as therapeutic targets. Nat Biotechnol 2010; 28: 1069-78; PMID: 20944599; http://dx. doi. org/10. 1038/nbt. 1678
144. Mund C, Lyko F. Epigenetic cancer therapy: Proof of concept and remaining challenges. Bioessays 2010; 32: 949-57; PMID: 21154865; http://dx. doi. org/10. 1002/bies. 201000061
145. Hashimoto H, Vertino PM, Cheng X. Molecular coupling of DNA methylation and histone methylation. Epigenomics 2010; 2: 657-69; PMID: 21339843; http://dx. doi. org/10. 2217/epi. 10. 44
146. Stresemann C, Lyko F. Modes of action of the DNA methyltransferase inhibitors azacytidine and decitabine. Int J Cancer 2008; 123: 8-13; PMID: 18425818; http://dx. doi. org/10. 1002/ijc. 23607
147. Gray SG, Ekström TJ. The human histone deacetylase family. Exp Cell Res 2001; 262: 75-83; PMID: 11139331; http://dx. doi. org/10. 1006/excr. 2000. 5080
148. Zhou VW, Goren A, Bernstein BE. Charting histone modifications and the functional organization of mammalian genomes. Nat Rev Genet 2011; 12: 7-18; PMID: 21116306; http://dx. doi. org/10. 1038/nrg2905
149. Yang XJ, Seto E. HATs and HDACs: from structure, function and regulation to novel strategies for therapy and prevention. Oncogene 2007; 26: 5310-8; PMID: 17694074; http://dx. doi. org/10. 1038/sj. onc. 1210599
150. Lane AA, Chabner BA. Histone deacetylase inhibitors in cancer therapy. J Clin Oncol 2009; 27: 5459-68; PMID: 19826124; http://dx. doi. org/10. 1200/JCO. 2009. 22. 1291
151. Mercurio C, Minucci S, Pelicci PG. Histone deacetylases and epigenetic therapies of hematological malignancies. Pharmacol Res 2010; 62: 18-34; PMID: 20219679; http://dx. doi. org/10. 1016/j. phrs. 2010. 02. 010
152. Sachs MD, Ramamurthy M, Poel Hv, Wickham TJ, Lamfers M, Gerritsen W, et al. Histone deacetylase inhibitors upregulate expression of the coxsackie adenovirus receptor (CAR) preferentially in bladder cancer cells. Cancer Gene Ther 2004; 11: 477-86; PMID: 15118762; http://dx. doi. org/10. 1038/sj. cgt. 7700726
153. Pong RC, Roark R, Ou JY, Fan J, Stanfield J, Frenkel E, et al. Mechanism of increased coxsackie and adenovirus receptor gene expression and adenovirus uptake by phytoestrogen and histone deacetylase inhibitor in human bladder cancer cells and the potential clinical application. Cancer Res 2006; 66: 8822-8; PMID: 16951199; http://dx. doi. org/10. 1158/0008-5472. CAN-05-4672
154. Xu WS, Parmigiani RB, Marks PA. Histone deacetylase inhibitors: molecular mechanisms of action. Oncogene 2007; 26: 5541-52; PMID: 17694093; http://dx. doi. org/10. 1038/sj. onc. 1210620
155. Quintás-Cardama A, Santos FP, Garcia-Manero G. Histone deacetylase inhibitors for the treatment of myelodysplastic syndrome and acute myeloid leukemia. Leukemia 2011; 25: 226-35; PMID: 21116282; http://dx. doi. org/10. 1038/leu. 2010. 276
156. Brown BD, Naldini L. Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat Rev Genet 2009; 10: 578-85; PMID: 19609263; http://dx. doi. org/10. 1038/nrg2628
157. Kota J, Chivukula RR, O'Donnell KA, Wentzel EA, Montgomery CL, Hwang HW, et al. Therapeutic microRNA delivery suppresses tumorigenesis in a murine liver cancer model. Cell 2009; 137: 1005-17; PMID: 19524505; http://dx. doi. org/10. 1016/j. cell. 2009. 04. 021
158. Esau CC. Inhibition of microRNA with antisense oligonucleotides. Methods 2008; 44: 55-60; PMID: 18158133; http://dx. doi. org/10. 1016/j. ymeth. 2007. 11. 001
159. Krützfeldt J, Rajewsky N, Braich R, Rajeev KG, Tuschl T, Manoharan M, et al. Silencing of microRNAs in vivo with 'antagomirs'. Nature 2005; 438: 685-9; PMID: 16258535; http://dx. doi. org/10. 1038/nature04303
160. Robert C, Rassool FV. HDAC inhibitors: roles of DNA damage and repair. Adv Cancer Res 2012; 116: 87-129; PMID: 23088869
161. Elmén J, Lindow M, Schütz S, Lawrence M, Petri A, Obad S, et al. LNA-mediated microRNA silencing in non-human primates. Nature 2008; 452: 896-9; PMID: 18368051; http://dx. doi. org/10. 1038/nature06783
162. Guil S, Esteller M. DNA methylomes, histone codes and miRNAs: tying it all together. Int J Biochem Cell Biol 2009; 41: 87-95; PMID: 18834952; http://dx. doi. org/10. 1016/j. biocel. 2008. 09. 005
163. Gal-Yam EN, Saito Y, Egger G, Jones PA. Cancer epigenetics: modifications, screening, and therapy. Annu Rev Med 2008; 59: 267-80; PMID: 17937590; http://dx. doi. org/10. 1146/annurev. med. 59. 061606. 095816
164. Cherblanc F, Chapman-Rothe N, Brown R, Fuchter MJ. Current limitations and future opportunities for epigenetic therapies. Future Med Chem 2012; 4: 425-46; PMID: 22416773; http://dx. doi. org/10. 4155/fmc. 12. 7
165. Popovic R, Licht JD. Emerging epigenetic targets and therapies in cancer medicine. Cancer Discov 2012; 2: 405-13; PMID: 22588878; http://dx. doi. org/10. 1158/2159-8290. CD-12-0076
166. Azad N, Zahnow CA, Rudin CM, Baylin SB. The future of epigenetic therapy in solid tumours-lessons from the past. Nature reviews. Clin Oncol 2013; 10: 256-66
167. Dawson MA, Kouzarides T. Cancer epigenetics: from mechanism to therapy. Cell 2012; 150: 12-27; PMID: 22770212; http://dx. doi. org/10. 1016/j. cell. 2012. 06. 013
168. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144: 646-74; PMID: 21376230; http://dx. doi. org/10. 1016/j. cell. 2011. 02. 013
169. Han H, Wolff EM, Liang G. Epigenetic alterations in bladder cancer and their potential clinical implications. Adv Urol 2012; 2012: 546917; PMID: 22829811; http://dx. doi. org/10. 1155/2012/546917