High levels of 5-hydroxymethylcytosine (5hmC) is an adverse predictor of biochemical recurrence after prostatectomy in ERG-negative prostate cancer

Clinical Epigenetics

Volumn 7, Issue 1, 2015, Pages

  Strand, Siri H ^a   Hoyer, Soren ^a   Lynnerup, Anne Sofie ^a   Haldrup, Christa ^a   Storebjerg, Tine Maj ^a   Borre, Michael ^a   Orntoft, Torben F ^a   Sorensen, Karina D ^a  

^a AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

5 hydroxymethylation; 5hmC; Biomarker; DNA methylation; Epigenetics; ERG; Prognostic; Prostate cancer

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; BIOLOGICAL MARKER; PROSTATE SPECIFIC ANTIGEN; TRANSCRIPTION FACTOR ERG;

ADULT; AGED; ARTICLE; BIOCHEMICAL RECURRENCE; BLOOD LEVEL; CANCER PROGNOSIS; CANCER RECURRENCE; CANCER STAGING; CONTROLLED STUDY; DISEASE ASSOCIATION; EPIGENETICS; ERG GENE; FOLLOW UP; GLEASON SCORE; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MAJOR CLINICAL STUDY; MALE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATE CANCER PROGNOSTIC TEST; PROSTATECTOMY;

EID: 84956927080     PISSN: 18687075     EISSN: 18687083     Source Type: Journal    
DOI: 10.1186/s13148-015-0146-5     Document Type: Article

References (60)

1. International Agency for Research on Cancer, W.H.O. Globocan 2012. http://globocan.iarc.fr/Pages/fact_sheets_cancer.aspx. Accessed on May 14, 2015.
2. Albertsen PC, Hanley JA, Fine J. 20-year outcomes following conservative management of clinically localized prostate cancer. JAMA. 2005;293: 2095-101.
3. Telesca D, Etzioni R, Gulati R. Estimating lead time and overdiagnosis associated with PSA screening from prostate cancer incidence trends. Biometrics. 2008;64:10-9.
4. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science. 2005;310:644-8.
5. Bostrom, P.J.; Bjartell, A.S.; Catto, J.W.; Eggener, S.E.; Lilja, H.; Loeb, S.; Schalken, J.; Schlomm, T.; Cooperberg, M.R. Genomic predictors of outcome in prostate cancer. European urology 2015: doi: 10.1016/ j.eururo.2015.04.008
6. Barbieri CE, Baca SC, Lawrence MS, Demichelis F, Blattner M, Theurillat JP, et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat Genet. 2012;44:685-9.
7. Brase JC, Johannes M, Mannsperger H, Falth M, Metzger J, Kacprzyk LA, et al. TMPRSS2-ERG-specific transcriptional modulation is associated with prostate cancer biomarkers and TGF-beta signaling. BMC Cancer. 2011;11:507.
8. Gasi Tandefelt D, Boormans JL, van der Korput HA, Jenster GW, Trapman J. A 36-gene signature predicts clinical progression in a subgroup of ERG-positive prostate cancers. Eur Urol. 2013;64:941-50.
9. Karnes RJ, Cheville JC, Ida CM, Sebo TJ, Nair AA, Tang H, et al. The ability of biomarkers to predict systemic progression in men with high-risk prostate cancer treated surgically is dependent on ERG status. Cancer Res. 2010;70:8994-9002.
10. Kron K, Liu L, Trudel D, Pethe V, Trachtenberg J, Fleshner N, et al. Correlation of ERG expression and DNA methylation biomarkers with adverse clinicopathologic features of prostate cancer. Clin Cancer Res. 2012;18:2896-904.
11. Tomlins SA, Rhodes DR, Yu J, Varambally S, Mehra R, Perner S, et al. The role of SPINK1 in ETS rearrangement-negative prostate cancers. Cancer Cell. 2008;13:519-28.
12. Vinarskaja A, Schulz WA, Ingenwerth M, Hader C, Arsov C. Association of PITX2 mRNA down-regulation in prostate cancer with promoter hypermethylation and poor prognosis. Urol Oncol. 2013;31:622-7.
13. Kron K, Trudel D, Pethe V, Briollais L, Fleshner N, van der Kwast T, et al. Altered DNA methylation landscapes of polycomb-repressed loci are associated with prostate cancer progression and ERG oncogene expression in prostate cancer. Clin Cancer Res. 2013;19:3450-61.
14. Tomlins SA, Alshalalfa M, Davicioni E, Erho N, Yousefi K, Zhao S, et al. Characterization of 1577 primary prostate cancers reveals novel biological and clinicopathologic insights into molecular subtypes. Eur Urol. 2015;68(4):555-67.
15. Dobosy JR, Roberts JL, Fu VX, Jarrard DF. The expanding role of epigenetics in the development, diagnosis and treatment of prostate cancer and benign prostatic hyperplasia. J Urol. 2007;177:822-31.
16. Chiam K, Ricciardelli C, Bianco-Miotto T. Epigenetic biomarkers in prostate cancer: current and future uses. Cancer Lett. 2014;342:248-56.
17. Haldrup C, Mundbjerg K, Vestergaard EM, Lamy P, Wild P, Schulz WA, et al. DNA methylation signatures for prediction of biochemical recurrence after radical prostatectomy of clinically localized prostate cancer. J Clin Oncol. 2013;31:3250-8.
18. Kristensen H, Haldrup C, Strand S, Mundbjerg K, Mortensen MM, Thorsen K, et al. Hypermethylation of the GABRE~mir-452~mir-224 promoter in prostate cancer predicts biochemical recurrence after radical prostatectomy. Clin Cancer Res. 2014;20:2169-81.
19. Strand SH, Orntoft TF, Sorensen KD. Prognostic DNA methylation markers for prostate cancer. Int J Mol Sci. 2014;15:16544-76.
20. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324:930-5.
21. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, Zhang Y. Role of Tet proteins in 5mc to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature. 2010;466:1129-33.
22. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, et al. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011;333:1300-3.
23. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science. 2011;333:1303-7.
24. Ye C, Li L. 5-hydroxymethylcytosine: a new insight into epigenetics in cancer. Cancer Biol Ther. 2014;15:10-5.
25. Iurlaro M, Ficz G, Oxley D, Raiber EA, Bachman M, Booth MJ, et al. A screen for hydroxymethylcytosine and formylcytosine binding proteins suggests functions in transcription and chromatin regulation. Genome Biol. 2013;14:R119.
26. Huang Y, Pastor WA, Shen Y, Tahiliani M, Liu DR, Rao A. The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS One. 2010;5:e8888.
27. Haffner MC, Chaux A, Meeker AK, Esopi DM, Gerber J, Pellakuru LG, et al. Global 5-hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget. 2011;2:627-37.
28. Haffner MC, Pellakuru LG, Ghosh S, Lotan TL, Nelson WG, De Marzo AM, et al. Tight correlation of 5-hydroxymethylcytosine and polycomb marks in health and disease. Cell Cycle. 2013;12:1835-41.
29. Orr BA, Haffner MC, Nelson WG, Yegnasubramanian S, Eberhart CG. Decreased 5-hydroxymethylcytosine is associated with neural progenitor phenotype in normal brain and shorter survival in malignant glioma. PLoS One. 2012;7:e41036.
30. Ko M, Huang Y, Jankowska AM, Pape UJ, Tahiliani M, Bandukwala HS, et al. Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature. 2010;468:839-43.
31. Kraus TF, Globisch D, Wagner M, Eigenbrod S, Widmann D, Munzel M, et al. Low values of 5-hydroxymethylcytosine (5hmc), the “sixth base,” are associated with anaplasia in human brain tumors. Int J Cancer. 2012;131:1577-90.
32. Kudo Y, Tateishi K, Yamamoto K, Yamamoto S, Asaoka Y, Ijichi H, et al. Loss of 5-hydroxymethylcytosine is accompanied with malignant cellular transformation. Cancer Sci. 2012;103:670-6.
33. Li W, Liu M. Distribution of 5-hydroxymethylcytosine in different human tissues. J Nucleic Acids. 2011;2011:870726.
34. Lian CG, Xu Y, Ceol C, Wu F, Larson A, Dresser K, et al. Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell. 2012;150:1135-46.
35. Liu X, Zhang G, Yi Y, Xiao L, Pei M, Liu S, et al. Decreased 5-hydroxymethylcytosine levels are associated with TET2 mutation and unfavorable overall survival in myelodysplastic syndromes. Leuk Lymphoma. 2013;54:2466-73.
36. Uribe-Lewis S, Stark R, Carroll T, Dunning MJ, Bachman M, Ito Y, et al. 5-hydroxymethylcytosine marks promoters in colon that resist DNA hypermethylation in cancer. Genome Biol. 2015;16:69.
37. Yang H, Liu Y, Bai F, Zhang JY, Ma SH, Liu J, et al. Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene. 2013;32:663-9.
38. Yang Q, Wu K, Ji M, Jin W, He N, Shi B, et al. Decreased 5-hydroxymethylcytosine (5-hmC) is an independent poor prognostic factor in gastric cancer patients. J Biomed Nanotechnol. 2013;9:1607-16.
39. Jin SG, Jiang Y, Qiu R, Rauch TA, Wang Y, Schackert G, et al. 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlate with IDH1 mutations. Cancer Res. 2011;71:7360-5.
40. Kroeze LI, Aslanyan MG, van Rooij A, Koorenhof-Scheele TN, Massop M, Carell T, et al. Characterization of acute myeloid leukemia based on levels of global hydroxymethylation. Blood. 2014;124:1110-8.
41. Globisch D, Munzel M, Muller M, Michalakis S, Wagner M, Koch S, et al. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PLoS One. 2010;5:e15367.
42. Matsuda I, Imai Y, Hirota S. Distinct global DNA methylation status in B-cell lymphomas: immunohistochemical study of 5-methylcytosine and 5-hydroxymethylcytosine. J Clin Exp Hematop. 2014;54:67-73.
43. Nestor CE, Ottaviano R, Reddington J, Sproul D, Reinhardt D, Dunican D, et al. Tissue type is a major modifier of the 5-hydroxymethylcytosine content of human genes. Genome Res. 2012;22:467-77.
44. Nettersheim D, Heukamp LC, Fronhoffs F, Grewe MJ, Haas N, Waha A, et al. Analysis of TET expression/activity and 5mc oxidation during normal and malignant germ cell development. PLoS One. 2013;8:e82881.
45. Park K, Tomlins SA, Mudaliar KM, Chiu YL, Esgueva R, Mehra R, et al. Antibody-based detection of erg rearrangement-positive prostate cancer. Neoplasia. 2010;12:590-8.
46. Braun M, Goltz D, Shaikhibrahim Z, Vogel W, Bohm D, Scheble V, et al. ERG protein expression and genomic rearrangement status in primary and metastatic prostate cancer—a comparative study of two monoclonal antibodies. Prostate Cancer Prostatic Dis. 2012;15:165-9.
47. Kang MR, Kim MS, Oh JE, Kim YR, Song SY, Seo SI, et al. Mutational analysis of IDH1 codon 132 in glioblastomas and other common cancers. Int J Cancer. 2009;125:353-5.
48. Kroeze LI, van der Reijden BA, Jansen JH. 5-hydroxymethylcytosine: an epigenetic mark frequently deregulated in cancer. Biochim Biophys Acta. 1855;2015:144-54.
49. Vergis R, Corbishley CM, Norman AR, Bartlett J, Jhavar S, Borre M, et al. Intrinsic markers of tumour hypoxia and angiogenesis in localised prostate cancer and outcome of radical treatment: a retrospective analysis of two randomised radiotherapy trials and one surgical cohort study. Lancet Oncol. 2008;9:342-51.
50. Kang KA, Piao MJ, Kim KC, Kang HK, Chang WY, Park IC, et al. Epigenetic modification of Nrf2 in 5-fluorouracil-resistant colon cancer cells: involvement of TET-dependent DNA demethylation. Cell Death Dis. 2014;5:e1183.
51. Mariani CJ, Vasanthakumar A, Madzo J, Yesilkanal A, Bhagat T, Yu Y, et al. TET1-mediated hydroxymethylation facilitates hypoxic gene induction in neuroblastoma. Cell Rep. 2014;7:1343-52.
52. Tsai YP, Chen HF, Chen SY, Cheng WC, Wang HW, Shen ZJ, et al. TET1 regulates hypoxia-induced epithelial-mesenchymal transition by acting as a co-activator. Genome Biol. 2014;15:513.
53. Zhu Y, Qiu P, Ji Y. TCGA-assembler: open-source software for retrieving and processing TCGA data. Nat Methods. 2014;11:599-600.
54. Zhu Y, Xu Y, Helseth Jr DL, Gulukota K, Yang S, Pesce LL, et al. Zodiac: a comprehensive depiction of genetic interactions in cancer by integrating TCGA data. J Natl Cancer Inst. 2015;107.
55. Long Q, Xu J, Osunkoya AO, Sannigrahi S, Johnson BA, Zhou W, et al. Global transcriptome analysis of formalin-fixed prostate cancer specimens identifies biomarkers of disease recurrence. Cancer Res. 2014;74:3228-37.
56. Adamo P, Ladomery MR. The oncogene ERG: a key factor in prostate cancer. Oncogene. 2015.
57. Burdova A, Bouchal J, Tavandzis S, Kolar Z. TMPRSS2-ERG gene fusion in prostate cancer. Biomed Pap Med Fac Univ Palacky Olomouc Czechoslovakia. 2014;158:502-10.
58. Yardimci H, Zhang Y. Charting oxidized methylcytosines at base resolution. Nat Struct Mol Biol. 2015;22:656-61.
59. Epstein JI, Allsbrook WC, Jr., Amin MB, Egevad LL, Committee IG. The 2005 International Society of Urological Pathology (ISUP) Consensus Conference on Gleason Grading of Prostatic Carcinoma. Am J Surg Pathol. 2005;29:1228-42.
60. Sorensen KD, Abildgaard MO, Haldrup C, Ulhoi BP, Kristensen H, Strand S, et al. Prognostic significance of aberrantly silenced ANPEP expression in prostate cancer. Br J Cancer. 2013;108:420-8.