Quantitative genome-wide methylation analysis of high-grade non-muscle invasive bladder cancer

Epigenetics

Volumn 11, Issue 3, 2016, Pages 237-246

  Kitchen, Mark O ^a,b   Bryan, Richard T ^c   Emes, Richard D ^d   Glossop, John R ^a   Luscombe, Christopher ^b   Cheng, K K ^c   Zeegers, Maurice P ^c,e,f   James, Nicholas D ^g   Devall, Adam J ^c   Mein, Charles A ^h   Gommersall, Lyndon ^b   Fryer, Anthony A ^a   Farrell, William E ^a  

^a KEELE UNIVERSITY   (United Kingdom)

^b UNIVERSITY HOSPITALS OF NORTH MIDLANDS NHS TRUST   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^f MAASTRICHT UNIVERSITY   (Netherlands)

^g UNIVERSITY OF WARWICK   (United Kingdom)

^h QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Epigenetics; gene expression; high grade non muscle invasive bladder cancer; HumanMethylation450 BeadChip Array; methylation

Indexed keywords

RNA POLYMERASE II; ARHGEF4 PROTEIN, HUMAN; ARYLDIALKYLPHOSPHATASE; HOMEODOMAIN PROTEIN; PON3 PROTEIN, HUMAN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; STAT5 PROTEIN; STAT5A PROTEIN, HUMAN; TUMOR MARKER; TUMOR PROTEIN; TUMOR SUPPRESSOR PROTEIN; VAX2 PROTEIN, HUMAN;

ARHGEF4 GENE; ARTICLE; ATP5G2 GENE; CLINICAL ARTICLE; CLUSTER ANALYSIS; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DNA TRANSCRIPTION; GENE; GENE EXPRESSION; GENE ONTOLOGY; HIST1H4F GENE; HUMAN; INSRR GENE; IRX1 GENE; NON MUSCLE INVASIVE BLADDER CANCER; PON3 GENE; PRDM14 GENE; PROMOTER REGION; PRRX1 GENE; PYROSEQUENCING; QUANTITATIVE ANALYSIS; TFAP2B GENE; VALIDATION PROCESS; VAX2 GENE; VSX1 GENE; BLADDER TUMOR; FEMALE; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HUMAN GENOME; MALE; PATHOLOGY; TUMOR INVASION; TUMOR RECURRENCE;

ARYLDIALKYLPHOSPHATASE; BIOMARKERS, TUMOR; CPG ISLANDS; DNA METHYLATION; FEMALE; GENOME, HUMAN; GENOME-WIDE ASSOCIATION STUDY; HOMEODOMAIN PROTEINS; HUMANS; MALE; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASM RECURRENCE, LOCAL; PROMOTER REGIONS, GENETIC; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; STAT5 TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEINS; URINARY BLADDER NEOPLASMS;

EID: 84962045457     PISSN: 15592294     EISSN: 15592308     Source Type: Journal    
DOI: 10.1080/15592294.2016.1154246     Document Type: Article

References (78)

1. J.Ferlay, I.Soerjomataram, R.Dikshit, S.Eser, C.Mathers, M.Rebelo, D.M.Parkin, D.Forman, F.Bray. Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer J Int Du Cancer 2015; 136:E359-86; PMID:26712904; http://dx.doi.org/10.1002/ijc.29210
2. Z.Kirkali, T.Chan, M.Manoharan, F.Algaba, C.Busch, L.Cheng, L.Kiemeney, M.Kriegmair, R.Montironi, W.M.Murphy, et al. Bladder cancer: epidemiology, staging and grading, and diagnosis. Urology 2005; 66:4-34; PMID:16399414; http://dx.doi.org/10.1016/j.urology.2005.07.062
3. R.J.Sylvester, A.P.van der Meijden, W.Oosterlinck, J.A.Witjes, C.Bouffioux, L.Denis, D.W.Newling, K.Kurth. 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 75–7; PMID:16442208; http://dx.doi.org/10.1016/j.eururo.2005.12.031
4. G.B.Boustead, S.Fowler, R.Swamy, R.Kocklebergh, L.Hounsome. Section of Oncology B. Stage, grade and pathological characteristics of bladder cancer in the UK: British Association of Urological Surgeons (BAUS) urological tumour registry. BJU Int 2014; 113:924-30; PMID:24447825; http://dx.doi.org/10.1111/bju.12468
5. S.Cambier, R.J.Sylvester, L.Collette, P.Gontero, M.A.Brausi, G.van Andel, W.J.Kirkels, F.C.Silva, W.Oosterlinck, S.Prescott, et al. EORTC Nomograms and Risk Groups for Predicting Recurrence, Progression, and Disease-specific and Overall Survival in Non-Muscle-invasive Stage Ta-T1 Urothelial Bladder Cancer Patients Treated with 1–3 Years of Maintenance Bacillus Calmette-Guerin. Eur Urol 2016; 69(1):60-9; PMID:26210894; http://dx.doi.org/10.1016/j.eururo.2015.06.045
6. M.M.Vedder, M.Marquez, E.W.de Bekker-Grob, M.L.Calle, L.Dyrskjot, M.Kogevinas, U.Segersten, P.U.Malmstrom, F.Algaba, W.Beukers, et al. Risk prediction scores for recurrence and progression of non-muscle invasive bladder cancer: an international validation in primary tumours. PloS One 2014; 9:e96849; PMID:24905984; http://dx.doi.org/10.1371/journal.pone.0096849
7. M.A.Knowles. Molecular pathogenesis of bladder cancer. Int J Clin Oncol 2008; 13:287-97; PMID:18704628; http://dx.doi.org/10.1007/s10147-008-0812-0
8. E.Dudziec, J.R.Goepel, J.W.Catto. Global epigenetic profiling in bladder cancer. Epigenomics 2011; 3:35-45; PMID:22126151; http://dx.doi.org/10.2217/epi.10.71
9. J.Van Batavia, T.Yamany, A.Molotkov, H.Dan, M.Mansukhani, E.Batourina, K.Schneider, D.Oyon, M.Dunlop, X.R.Wu, et al. Bladder cancers arise from distinct urothelial sub-populations. Nat Cell Biol 2014; 16:982-91; PMID:25218638; http://dx.doi.org/10.1038/ncb3038
10. A.A.Bakkar, H.Wallerand, F.Radvanyi, J.B.Lahaye, S.Pissard, L.Lecerf, J.C.Kouyoumdjian, C.C.Abbou, J.C.Pairon, M.C.Jaurand, et al. FGFR3 and TP53 gene mutations define two distinct pathways in urothelial cell carcinoma of the bladder. Cancer Res 2003; 63:8108-12; PMID:14678961
11. J.Van Batavia, T.Yamany, A.Molotkov, H.Dan, M.Mansukhani, E.Batourina, K.Schneider, D.Oyon, M.Dunlop, X.R.Wu, et al. Bladder cancers arise from distinct urothelial sub-populations. Nat Cell Biol 2014; 16:982-91, 1–5; PMID:25218638; http://dx.doi.org/10.1038/ncb3038
12. R.T.Bryan, D.G.Ward. Words of wisdom. Bladder cancers arise from distinct urothelial sub-populations. Eur Urol 2015; 67:590-1; PMID:25760413; http://dx.doi.org/10.1016/j.eururo.2014.11.058
13. D.J.McConkey, S.Lee, W.Choi, M.Tran, T.Majewski, S.Lee, A.Siefker-Radtke, C.Dinney, B.Czerniak. Molecular genetics of bladder cancer: Emerging mechanisms of tumor initiation and progression. Urologic Oncol 2010; 28:429-40; PMID:20610280; http://dx.doi.org/10.1016/j.urolonc.2010.04.008
14. M.Castillo-Martin, J.Domingo-Domenech, O.Karni-Schmidt, T.Matos, C.Cordon-Cardo. Molecular pathways of urothelial development and bladder tumorigenesis. Urologic Oncol 2010; 28:401-8; PMID:20610278; http://dx.doi.org/10.1016/j.urolonc.2009.04.019
15. M.A.Knowles, C.D.Hurst. Molecular biology of bladder cancer: new insights into pathogenesis and clinical diversity. Nat Rev Cancer 2015; 15:25-41; PMID:25533674; http://dx.doi.org/10.1038/nrc3817
16. T.Majewski, S.Lee, J.Jeong, D.S.Yoon, A.Kram, M.S.Kim, T.Tuziak, J.Bondaruk, S.Lee, W.S.Park, et al. Understanding the development of human bladder cancer by using a whole-organ genomic mapping strategy. Lab Invest; J Tech Methods Pathol 2008; 88:694-721; PMID:18458673; http://dx.doi.org/10.1038/labinvest.2008.27
17. S.Sharma, T.K.Kelly, P.A.Jones. Epigenetics in cancer. Carcinogenesis 2010; 31:27-36; PMID:19752007; http://dx.doi.org/10.1093/carcin/bgp220
18. S.B.Baylin, P.A.Jones. 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
19. M.A.Dawson, T.Kouzarides. Cancer epigenetics: from mechanism to therapy. Cell 2012; 150:12-27; PMID:22770212; http://dx.doi.org/10.1016/j.cell.2012.06.013
20. R.Kanwal, S.Gupta. Epigenetic modifications in cancer. Clin Genetics 2012; 81:303-11; PMID:22082348; http://dx.doi.org/10.1111/j.1399-0004.2011.01809.x
21. E.M.Wolff, Y.Chihara, F.Pan, D.J.Weisenberger, K.D.Siegmund, K.Sugano, K.Kawashima, P.W.Laird, P.A.Jones, G.Liang. 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
22. J.W.Catto, A.R.Azzouzi, I.Rehman, K.M.Feeley, S.S.Cross, N.Amira, G.Fromont, M.Sibony, O.Cussenot, M.Meuth, et al. Promoter hypermethylation is associated with tumor location, stage, and subsequent progression in transitional cell carcinoma. J Clin Oncol 2005; 23:2903-10; PMID:15753461; http://dx.doi.org/10.1200/JCO.2005.03.163
23. M.O.Kitchen, R.T.Bryan, K.E.Haworth, R.D.Emes, C.Luscombe, L.Gommersall, K.K.Cheng, M.P.Zeegers, N.D.James, A.J.Devall, et al. Methylation of HOXA9 and ISL1 Predicts Patient Outcome in High-Grade Non-Invasive Bladder Cancer. PloS One 2015; 10:e0137003; PMID:26332997; http://dx.doi.org/10.1371/journal.pone.0137003
24. M.Alvarez-Mugica, V.Cebrian, J.M.Fernandez-Gomez, F.Fresno, S.Escaf, M.Sanchez-Carbayo. Myopodin methylation is associated with clinical outcome in patients with T1G3 bladder cancer. J Urol 2010; 184:1507-13; PMID:20723929; http://dx.doi.org/10.1016/j.juro.2010.05.085
25. J.R.Glossop, N.B.Nixon, R.D.Emes, K.E.Haworth, J.C.Packham, P.T.Dawes, A.A.Fryer, D.L.Mattey, W.E.Farrell. Epigenome-wide profiling identifies significant differences in DNA methylation between matched-pairs of T- and B-lymphocytes from healthy individuals. Epigenetics 2013; 8:1188-97; PMID:24005183; http://dx.doi.org/10.4161/epi.26265
26. E.de Araujo, F.A.Marchi, T.C.Rodrigues, H.C.Vieira, H.Kuasne, M.I.Achatz, L.F.Moredo, B.C.de Sa, J.P.Duprat, H.P.Brentani, et al. Genome-wide DNA methylation profile of leukocytes from melanoma patients with and without CDKN2A mutations. Exp Mol Pathol 2014; 97:425-32; PMID:25236571; http://dx.doi.org/10.1016/j.yexmp.2014.09.009
27. O.A.Stefansson, S.Moran, A.Gomez, S.Sayols, C.Arribas-Jorba, J.Sandoval, H.Hilmarsdottir, E.Olafsdottir, L.Tryggvadottir, J.G.Jonasson, et al. A DNA methylation-based definition of biologically distinct breast cancer subtypes. Mol Oncol 2015; 9:555-68; PMID:25468711; http://dx.doi.org/10.1016/j.molonc.2014.10.012
28. F.Sanchez-Vega, V.Gotea, H.M.Petrykowska, G.Margolin, T.C.Krivak, J.A.DeLoia, D.W.Bell, L.Elnitski. Recurrent patterns of DNA methylation in the ZNF154, CASP8, and VHL promoters across a wide spectrum of human solid epithelial tumors and cancer cell lines. Epigenetics 2013; 8:1355-72; PMID:24149212; http://dx.doi.org/10.4161/epi.26701
29. A.Besaratinia, M.Cockburn, S.Tommasi. Alterations of DNA methylome in human bladder cancer. Epigenetics 2013; 8:1013-22; PMID:23975266; http://dx.doi.org/10.4161/epi.25927
30. R.T.Bryan, R.Kirby, H.Mostafid. Does the nonurologic scientific community understand urothelial bladder cancer? Europ Urol 2014; 66:601-2; PMID:24821580; http://dx.doi.org/10.1016/j.eururo.2014.04.010
31. T.K.Kelly, D.D.De Carvalho, P.A.Jones. Epigenetic modifications as therapeutic targets. Nat Biotechnol 2010; 28:1069-78; PMID:20944599; http://dx.doi.org/10.1038/nbt.1678
32. J.P.Issa, H.M.Kantarjian. Targeting DNA methylation. Clin Cancer Res 2009; 15:3938-46; PMID:19509174; http://dx.doi.org/10.1158/1078-0432.CCR-08-2783
33. S.Dedeurwaerder, M.Defrance, E.Calonne, H.Denis, C.Sotiriou, F.Fuks. Evaluation of the Infinium Methylation 450 K technology. Epigenomics 2011; 3:771-84; PMID:22126295; http://dx.doi.org/10.2217/epi.11.105
34. J.Roessler, O.Ammerpohl, J.Gutwein, B.Hasemeier, S.L.Anwar, H.Kreipe, U.Lehmann. Quantitative cross-validation and content analysis of the 450 k DNA methylation array from Illumina, Inc. BMC Res Notes 2012; 5:210; PMID:22546179; http://dx.doi.org/10.1186/1756-0500-5-210
35. T.Reinert, C.Modin, F.M.Castano, P.Lamy, T.K.Wojdacz, L.L.Hansen, C.Wiuf, M.Borre, L.Dyrskjot, T.F.Orntoft. Comprehensive genome methylation analysis in bladder cancer: identification and validation of novel methylated genes and application of these as urinary tumor markers. Clin Cancer Res 2011; 17:5582-92; PMID:21788354; http://dx.doi.org/10.1158/1078-0432.CCR-10-2659
36. N.G.Bediaga, A.Acha-Sagredo, I.Guerra, A.Viguri, C.Albaina, I.Ruiz Diaz, R.Rezola, M.J.Alberdi, J.Dopazo, D.Montaner, et al. DNA methylation epigenotypes in breast cancer molecular subtypes. Breast Cancer Res 2010; 12:R77; PMID:20920229; http://dx.doi.org/10.1186/bcr2721
37. C.V.Duong, R.D.Emes, F.Wessely, K.Yacqub-Usman, R.N.Clayton, W.E.Farrell. Quantitative, genome-wide analysis of the DNA methylome in sporadic pituitary adenomas. Endocrine-Related Cancer 2012; 19:805-16; PMID:23045325; http://dx.doi.org/10.1530/ERC-12-0251
38. Y.J.Kim, H.Y.Yoon, J.S.Kim, H.W.Kang, B.D.Min, S.K.Kim, Y.S.Ha, I.Y.Kim, K.H.Ryu, S.C.Lee, et al. HOXA9, ISL1 and ALDH1A3 methylation patterns as prognostic markers for nonmuscle invasive bladder cancer: array-based DNA methylation and expression profiling. Int J Cancer J Int Du Cancer 2013; 133:1135-42; PMID:23436614; http://dx.doi.org/10.1002/ijc.28121
39. D.Schubeler. Function and information content of DNA methylation. Nature 2015; 517:321-6; PMID:25592537; http://dx.doi.org/10.1038/nature14192
40. M.Bibikova, B.Barnes, C.Tsan, V.Ho, B.Klotzle, J.M.Le, D.Delano, L.Zhang, G.P.Schroth, K.L.Gunderson, et al. High density DNA methylation array with single CpG site resolution. Genomics 2011; 98:288-95; PMID:21839163; http://dx.doi.org/10.1016/j.ygeno.2011.07.007
41. V.Barrera, M.A.Peinado. Evaluation of single CpG sites as proxies of CpG island methylation states at the genome scale. Nucleic Acids Res 2012; 40:11490-8; PMID:23066096; http://dx.doi.org/10.1093/nar/gks928
42. V.A.Naumov, E.V.Generozov, N.B.Zaharjevskaya, D.S.Matushkina, A.K.Larin, S.V.Chernyshov, M.V.Alekseev, Y.A.Shelygin, V.M.Govorun. Genome-scale analysis of DNA methylation in colorectal cancer using Infinium HumanMethylation450 BeadChips. Epigenetics 2013; 8:921-34; PMID:23867710; http://dx.doi.org/10.4161/epi.25577
43. A.Karlsson, M.Jonsson, M.Lauss, H.Brunnstrom, P.Jonsson, A.Borg, G.Jonsson, M.Ringner, M.Planck, J.Staaf. Genome-wide DNA methylation analysis of lung carcinoma reveals one neuroendocrine and four adenocarcinoma epitypes associated with patient outcome. Clin Cancer Res 2014; 20:6127-40; PMID:25278450; http://dx.doi.org/10.1158/1078-0432.CCR-14-1087
44. H.Nagase, S.Ghosh. Epigenetics: differential DNA methylation in mammalian somatic tissues. FEBS J 2008; 275:1617-23; PMID:18331347; http://dx.doi.org/10.1111/j.1742-4658.2008.06330.x
45. U.Cavallaro, G.Christofori. Cell adhesion and signalling by cadherins and Ig-CAMs in cancer. Nat rev Cancer 2004; 4:118-32; PMID:14964308; http://dx.doi.org/10.1038/nrc1276
46. P.A.Jones, S.B.Baylin. The epigenomics of cancer. Cell 2007; 128:683-92; PMID:17320506; http://dx.doi.org/10.1016/j.cell.2007.01.029
47. I.Ibragimova, E.Dulaimi, M.J.Slifker, D.Y.Chen, R.G.Uzzo, P.Cairns. A global profile of gene promoter methylation in treatment-naive urothelial cancer. Epigenetics 2014; 9:760-73; PMID:24521710; http://dx.doi.org/10.4161/epi.28078
48. Y.Li, S.Li, J.Chen, T.Shao, C.Jiang, Y.Wang, H.Chen, J.Xu, X.Li. Comparative epigenetic analyses reveal distinct patterns of oncogenic pathways activation in breast cancer subtypes. Hum Mol Genetics 2014; 23:5378-93; PMID:24871326; http://dx.doi.org/10.1093/hmg/ddu256
49. M.T.Gyparaki, E.K.Basdra, A.G.Papavassiliou. DNA methylation biomarkers as diagnostic and prognostic tools in colorectal cancer. J Mol Med 2013; 91:1249-56; PMID:24057814; http://dx.doi.org/10.1007/s00109-013-1088-z
50. M.Guo, J.Ren, M.G.House, Y.Qi, M.V.Brock, J.G.Herman. Accumulation of promoter methylation suggests epigenetic progression in squamous cell carcinoma of the esophagus. Clin Cancer Res 2006; 12:4515-22; PMID:16899597; http://dx.doi.org/10.1158/1078-0432.CCR-05-2858
51. A.Kaneda, K.Matsusaka, E.Sakai, S.Funata. DNA methylation accumulation and its predetermination of future cancer phenotypes. J Biochem 2014; 156:63-72; PMID:24962701; http://dx.doi.org/10.1093/jb/mvu038
52. K.Yagi, K.Akagi, H.Hayashi, G.Nagae, S.Tsuji, T.Isagawa, Y.Midorikawa, Y.Nishimura, H.Sakamoto, Y.Seto, et al. Three DNA methylation epigenotypes in human colorectal cancer. Clin Cancer Res 2010; 16:21-33; PMID:20028768; http://dx.doi.org/10.1158/1078-0432.CCR-09-2006
53. M.J.Fackler, C.B.Umbricht, D.Williams, P.Argani, L.A.Cruz, V.F.Merino, W.W.Teo, Z.Zhang, P.Huang, K.Visvananthan, et al. Genome-wide methylation analysis identifies genes specific to breast cancer hormone receptor status and risk of recurrence. Cancer Res 2011; 71:6195-207; PMID:21825015; http://dx.doi.org/10.1158/0008-5472.CAN-11-1630
54. J.Sandoval, J.Mendez-Gonzalez, E.Nadal, G.Chen, F.J.Carmona, S.Sayols, S.Moran, H.Heyn, M.Vizoso, A.Gomez, et al. A prognostic DNA methylation signature for stage I non-small-cell lung cancer. J Clin Oncol 2013; 31:4140-7; PMID:24081945; http://dx.doi.org/10.1200/JCO.2012.48.5516
55. K.L.Bennett, M.Karpenko, M.T.Lin, R.Claus, K.Arab, G.Dyckhoff, P.Plinkert, E.Herpel, D.Smiraglia, C.Plass. Frequently methylated tumor suppressor genes in head and neck squamous cell carcinoma. Cancer Res 2008; 68:4494-9; PMID:18559491; http://dx.doi.org/10.1158/0008-5472.CAN-07-6509
56. S.Snellenberg, S.A.Cillessen, W.Van Criekinge, L.Bosch, C.J.Meijer, P.J.Snijders, R.D.Steenbergen. Methylation-mediated repression of PRDM14 contributes to apoptosis evasion in HPV-positive cancers. Carcinogenesis 2014; 35:2611-8; PMID:25233927; http://dx.doi.org/10.1093/carcin/bgu197
57. M.R.Morris, C.J.Ricketts, D.Gentle, F.McRonald, N.Carli, H.Khalili, M.Brown, T.Kishida, M.Yao, R.E.Banks, et al. Genome-wide methylation analysis identifies epigenetically inactivated candidate tumour suppressor genes in renal cell carcinoma. Oncogene 2011; 30:1390-401; PMID:21132003; http://dx.doi.org/10.1038/onc.2010.525
58. S.Kalari, G.P.Pfeifer. Identification of driver and passenger DNA methylation in cancer by epigenomic analysis. Adv Genetics 2010; 70:277-308; PMID:22624715; http://dx.doi.org/10.1016/B978-0-12-380866-0.60010-1
59. D.D.De Carvalho, S.Sharma, J.S.You, S.F.Su, P.C.Taberlay, T.K.Kelly, X.Yang, G.Liang, P.A.Jones. DNA methylation screening identifies driver epigenetic events of cancer cell survival. Cancer Cell 2012; 21:655-67; PMID:22624715; http://dx.doi.org/10.1016/j.ccr.2012.03.045
60. E.M.Schweikert, A.Devarajan, I.Witte, P.Wilgenbus, J.Amort, U.Forstermann, A.Shabazian, V.Grijalva, D.M.Shih, R.Farias-Eisner, et al. PON3 is upregulated in cancer tissues and protects against mitochondrial superoxide-mediated cell death. Cell Death Differ 2012; 19:1549-60; PMID:22441669; http://dx.doi.org/10.1038/cdd.2012.35
61. A.S.Sultan, J.Xie, M.J.LeBaron, E.L.Ealley, M.T.Nevalainen, H.Rui. Stat5 promotes homotypic adhesion and inhibits invasive characteristics of human breast cancer cells. Oncogene 2005; 24:746-60; PMID:15592524; http://dx.doi.org/10.1038/sj.onc.1208203
62. M.P.Zeegers, R.T.Bryan, C.Langford, L.Billingham, P.Murray, N.S.Deshmukh, S.Hussain, N.James, D.M.Wallace, K.K.Cheng. The West Midlands Bladder Cancer Prognosis Programme: rationale and design. BJU Int 2010; 105:784-8; PMID:19751260; http://dx.doi.org/10.1111/j.1464-410X.2009.08849.x
63. M.Babjuk, M.Burger, R.Zigeuner, S.F.Shariat, B.W.van Rhijn, E.Comperat, R.J.Sylvester, E.Kaasinen, A.Bohle, J.Palou Redorta, et al. EAU guidelines on non-muscle-invasive urothelial carcinoma of the bladder: update 2013. European Urol 2013; 64:639-53; PMID:23827737; http://dx.doi.org/10.1016/j.eururo.2013.06.003
64. N.Blin, D.W.Stafford. A general method for isolation of high molecular weight DNA from eukaryotes. Nucleic Acids Res 1976; 3:2303-8; PMID:987581; http://dx.doi.org/10.1093/nar/3.9.2303
65. M.Lauss, M.Aine, G.Sjodahl, S.Veerla, O.Patschan, S.Gudjonsson, G.Chebil, K.Lovgren, M.Ferno, W.Mansson, et al. DNA methylation analyses of urothelial carcinoma reveal distinct epigenetic subtypes and an association between gene copy number and methylation status. Epigenetics 2012; 7:858-67; PMID:22705924; http://dx.doi.org/10.4161/epi.20837
66. A.A.Fryer, R.D.Emes, K.M.Ismail, K.E.Haworth, C.Mein, W.D.Carroll, W.E.Farrell. Quantitative, high-resolution epigenetic profiling of CpG loci identifies associations with cord blood plasma homocysteine and birth weight in humans. Epigenetics 2011; 6:86-94; PMID:20864804; http://dx.doi.org/10.4161/epi.6.1.13392
67. F.Wessely, R.D.Emes. Identification of DNA methylation biomarkers from Infinium arrays. Front Genetics 2012; 3:161; PMID:22936948; http://dx.doi.org/10.3389/fgene.2012.00161
68. J.R.Glossop, R.D.Emes, N.B.Nixon, K.E.Haworth, J.C.Packham, P.T.Dawes, A.A.Fryer, D.L.Mattey, W.E.Farrell. Genome-wide DNA methylation profiling in rheumatoid arthritis identifies disease-associated methylation changes that are distinct to individual T- and B-lymphocyte populations. Epigenetics 2014; 9:1228-37; PMID:25147922; http://dx.doi.org/10.4161/epi.29718
69. A.Sen, N.Heredia, M.C.Senut, M.Hess, S.Land, W.Qu, K.Hollacher, M.O.Dereski, D.M.Ruden. Early life lead exposure causes gender-specific changes in the DNA methylation profile of DNA extracted from dried blood spots. Epigenomics 2015; 7:379-93; PMID:26077427; http://dx.doi.org/10.2217/epi.15.2
70. A.Sturn, J.Quackenbush, Z.Trajanoski. Genesis: cluster analysis of microarray data. Bioinformatics 2002; 18:207-8; PMID:11836235; http://dx.doi.org/10.1093/bioinformatics/18.1.207
71. P.Khatri, S.Draghici. Ontological analysis of gene expression data: current tools, limitations, and open problems. Bioinformatics 2005; 21:3587-95; PMID:15994189; http://dx.doi.org/10.1093/bioinformatics/bti565
72. P.Chomczynski, N.Sacchi. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochem 1987; 162:156-9; PMID:2440339; http://dx.doi.org/10.1016/0003-2697(87)90021-2
73. K.J.Dudley, K.Revill, P.Whitby, R.N.Clayton, W.E.Farrell. Genome-wide analysis in a murine Dnmt1 knockdown model identifies epigenetically silenced genes in primary human pituitary tumors. Mol Cancer Res 2008; 6:1567-74; PMID:18922972; http://dx.doi.org/10.1158/1541-7786.MCR-08-0234
74. H.Al-Azzawi, K.Yacqub-Usman, A.Richardson, L.J.Hofland, R.N.Clayton, W.E.Farrell. Reversal of endogenous dopamine receptor silencing in pituitary cells augments receptor-mediated apoptosis. Endocrinol 2011; 152:364-73; PMID:21177832; http://dx.doi.org/10.1210/en.2010-0886
75. K.J.Livak, T.D.Schmittgen. Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 2001; 25:402-8; PMID:11846609; http://dx.doi.org/10.1006/meth.2001.1262
76. M.O.Kitchen, K.Yacqub-Usman, R.D.Emes, A.Richardson, R.N.Clayton, W.E.Farrell. Epidrug mediated re-expression of miRNA targeting the HMGA transcripts in pituitary cells. Pituitary 2015; 18(5):674-84; PMID:25557289; http://dx.doi.org/10.1007/s11102-014-0630-5
77. M.Raponi, Y.Zhang, J.Yu, G.Chen, G.Lee, J.M.Taylor, J.Macdonald, D.Thomas, C.Moskaluk, Y.Wang, et al. Gene expression signatures for predicting prognosis of squamous cell and adenocarcinomas of the lung. Cancer Res 2006; 66:7466-72; PMID:16885343; http://dx.doi.org/10.1158/0008-5472.CAN-06-1191
78. M.Gardiner-Garden, M.Frommer. CpG islands in vertebrate genomes. J Mol Biol 1987; 196:261-82; PMID:3656447; http://dx.doi.org/10.1016/0022-2836(87)90689-9