Analysis of TET Expression/Activity and 5mC oxidation during normal and malignant germ cell development

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Nettersheim, Daniel ^a   Heukamp, Lukas C ^a,c   Fronhoffs, Florian ^a,d   Grewe, Marc J ^a   Haas, Natalie ^a   Waha, Anke ^a   Honecker, Friedemann ^b,d   Waha, Andreas ^a   Kristiansen, Glen ^a   Schorle, Hubert ^a  

^a UNIVERSITY HOSPITAL BONN   (Germany)

^b UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^c UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^d Tumor und Brustzentrum ZeTuP Silberturm ^*  (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXYGLUTARIC ACID; 5 CARBOXYLCYTOSINE; 5 FORMYLCYTOSINE; 5 HYDROXYMETHYLCYTOSINE; 5 METHYLCYTOSINE; CYTOSINE DERIVATIVE; DNA METHYLTRANSFERASE 3B; ISOCITRATE DEHYDROGENASE 1; ISOCITRATE DEHYDROGENASE 2; OXYGENASE; PROTEIN TET1; PROTEIN TET2; PROTEIN TET3; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOMA IN SITU; DEMETHYLATION; DNA METHYLATION; DNMT3B GENE; DNMT3L GENE; DOWN REGULATION; ENZYME ACTIVITY; GENE; GENE EXPRESSION; GENE MUTATION; GERM CELL; GERM CELL TUMOR; HUMAN; HUMAN CELL; HUMAN TISSUE; IDH1 GENE; IDH2 GENE; MALE; MOUSE; NONHUMAN; OXIDATION; PROTEIN EXPRESSION; SEMINOMA; SPERMATOGENESIS; TDG GENE; TESTIS; TET1 GENE; UPREGULATION;

5-METHYLCYTOSINE; CARCINOMA; CELL LINE, TUMOR; CYTOSINE; DNA METHYLATION; DNA-BINDING PROTEINS; DOWN-REGULATION; GERM CELLS; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEOPLASMS, GERM CELL AND EMBRYONAL; OXIDATION-REDUCTION; PROTO-ONCOGENE PROTEINS; SPERMATOGENESIS; TESTIS;

EID: 84891301484     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082881     Document Type: Article

References (59)

1. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, et al. (2010) Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329: 78-82.
2. Hajkova P, Erhardt S, Lane N, Haaf T, El-Maarri O, et al. (2002) Epigenetic reprogramming in mouse primordial germ cells. Mech Dev 117: 15-23. (Pubitemid 36158711)
3. Mochizuki K, Matsui Y (2010) Epigenetic profiles in primordial germ cells: global modulation and fine tuning of the epigenome for acquisition of totipotency. Dev Growth Differ 52: 517-525.
4. Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127: 643-651. (Pubitemid 38878420)
5. Morgan HD, Santos F, Green K, Dean W, Reik W (2005) Epigenetic reprogramming in mammals. Hum Mol Genet 14 Spec No 1: R47-58. (Pubitemid 40542620)
6. Gong Z, Zhu JK (2011) Active DNA demethylation by oxidation and repair. Cell Res 21: 1649-1651.
7. Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43: 143-166.
8. Branco MR, Ficz G, Reik W (2012) Uncovering the role of 5-hydroxymethylcytosine in the epigenome. Nat Rev Genet 13: 7-13.
9. Maiti A, Drohat AC (2011) Thymine DNA glycosylase can rapidly excise 5- formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem 286: 35334-35338.
10. He YF, Li BZ, Li Z, Liu P, Wang Y, et al. (2011) Tet-mediated formation of 5- carboxylcytosine and its excision by TDG in mammalian DNA. Science 333: 1303-1307.
11. Wu H, Zhang Y (2011) Tet1 and 5-hydroxymethylation: a genome-wide view in mouse embryonic stem cells. Cell Cycle 10: 2428-2436.
12. Ito S, D'Alessio AC, Taranova OV, Hong K, Sowers LC, et al. (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466: 1129-1133.
13. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, et al. (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2: 241.
14. Skakkebaek NE (1972) Possible carcinoma-in-situ of the testis. Lancet 2: 516-517.
15. Oosterhuis JW, Looijenga LH (2005) Testicular germ-cell tumours in a broader perspective. Nat Rev Cancer 5: 210-222. (Pubitemid 40314952)
16. de Jong J, Stoop H, Gillis AJ, van Gurp RJ, van de Geijn GJ, et al. (2008) Differential expression of SOX17 and SOX2 in germ cells and stem cells has biological and clinical implications. J Pathol 215: 21-30. (Pubitemid 351619872)
17. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, et al. (2009) IDH1 and IDH2 mutations in gliomas. N Engl J Med 360: 765-773.
18. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, et al. (2010) Cancerassociated IDH1 mutations produce 2-hydroxyglutarate. Nature 465: 966.
19. Muller T, Gessi M, Waha A, Isselstein LJ, Luxen D, et al. (2012) Nuclear Exclusion of TET1 Is Associated with Loss of 5-Hydroxymethylcytosine in IDH1 Wild-Type Gliomas. Am J Pathol.
20. Muller T, Gessi M, Waha A, Isselstein LJ, Luxen D, et al. (2012) Nuclear exclusion of TET1 is associated with loss of 5-hydroxymethylcytosine in IDH1 wild-type gliomas. Am J Pathol 181: 675-683.
21. Noushmehr H, Weisenberger DJ, Diefes K, Phillips HS, Pujara K, et al. (2010) Identification of a CpG island methylator phenotype that defines a distinct subgroup of glioma. Cancer Cell 17: 510-522.
22. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-935.
23. Mizuno Y, Gotoh A, Kamidono S, Kitazawa S (1993) [Establishment and characterization of a new human testicular germ cell tumor cell line (TCam-2)]. Nihon Hinyokika Gakkai Zasshi 84: 1211-1218. (Pubitemid 23275551)
24. Andrews PW, Goodfellow PN, Shevinsky LH, Bronson DL, Knowles BB (1982) Cell-surface antigens of a clonal human embryonal carcinoma cell line: morphological and antigenic differentiation in culture. Int J Cancer 29: 523-531. (Pubitemid 12114626)
25. Andrews PW, Damjanov I, Simon D, Banting GS, Carlin C, et al. (1984) Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Differentiation in vivo and in vitro. Lab Invest 50: 147-162. (Pubitemid 14199076)
26. Bronson DL, Andrews PW, Solter D, Cervenka J, Lange PH, et al. (1980) Cell line derived from a metastasis of a human testicular germ cell tumor. Cancer Res 40: 2500-2506. (Pubitemid 10082273)
27. Hiraoka A, Vogelzang NJ, Rosner MC, Golomb HM (1988) Ultrastructure of four human germ cell tumor-derived cell lines: effect of 12-O-tetradecanoyl phorbol-13-acetate. Cancer Invest 6: 393-402. (Pubitemid 18259788)
28. Mueller T, Mueller LP, Luetzkendorf J, Voigt W, Simon H, et al. (2006) Loss of Oct-3/4 expression in embryonal carcinoma cells is associated with induction of cisplatin resistance. Tumour Biol 27: 71-83.
29. Schlappack OK, Bush C, Delic JI, Steel GG (1988) Growth and chemotherapy of a human germ-cell tumour line (GCT 27). Eur J Cancer Clin Oncol 24: 777-781. (Pubitemid 18095586)
30. Vogelzang NJ, Bronson D, Savino D, Vessella RL, Fraley EF (1985) A human embryonal-yolk sac carcinoma model system in athymic mice. Cancer 55: 2584-2593. (Pubitemid 15092143)
31. Pattillo RA, Hussa RO, Huang WY, Delfs E, Mattingly RF (1972) Estrogen production by trophoblastic tumors in tissue culture. J Clin Endocrinol 34: 59-61.
32. Kohler PO, Bridson WE (1971) Isolation of hormone-producing clonal lines of human choriocarcinoma. J Clin Endocrinol Metab 32: 683-687.
33. Biermann K, Heukamp LC, Steger K, Zhou H, Franke FE, et al. (2007) Genome-wide expression profiling reveals new insights into pathogenesis and progression of testicular germ cell tumors. Cancer Genomics Proteomics 4: 359-367. (Pubitemid 350067366)
34. Nettersheim D, Biermann K, Gillis AJ, Steger K, Looijenga LH, et al. (2011) NANOG promoter methylation and expression correlation during normal and malignant human germ cell development. Epigenetics 6: 114-122.
35. Nettersheim D, Gillis AJ, Looijenga LH, Schorle H (2011) TGF-beta1, EGF and FGF4 synergistically induce differentiation of the seminoma cell line TCam-2 into a cell type resembling mixed non-seminoma. Int J Androl 34: e189-203.
36. Eckert D, Nettersheim D, Heukamp LC, Kitazawa S, Biermann K, et al. (2008) TCam-2 but not JKT-1 cells resemble seminoma in cell culture. Cell Tissue Res 331: 529-538.
37. Nettersheim D, Westernstroer B, Haas N, Leinhaas A, Brustle O, et al. (2012) Establishment of a versatile seminoma model indicates cellular plasticity of germ cell tumor cells. Genes Chromosomes Cancer 51: 717-726.
38. Sasaki H, Matsui Y (2008) Epigenetic events in mammalian germ-cell development: reprogramming and beyond. Nat Rev Genet 9: 129-140.
39. Inoue A, Shen L, Dai Q, He C, Zhang Y (2011) Generation and replicationdependent dilution of 5fC and 5caC during mouse preimplantation development. Cell Res 21: 1670-1676.
40. Inoue A, Zhang Y (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334: 194.
41. Netto GJ, Nakai Y, Nakayama M, Jadallah S, Toubaji A, et al. (2008) Global DNA hypomethylation in intratubular germ cell neoplasia and seminoma, but not in nonseminomatous male germ cell tumors. Mod Pathol 21: 1337-1344.
42. Wermann H, Stoop H, Gillis AJ, Honecker F, van Gurp RJ, et al. (2011) Global DNA methylation in fetal human germ cells and germ cell tumours: association with differentiation and cisplatin resistance. J Pathol 221: 433-442.
43. Li W, Liu M (2011) Distribution of 5-hydroxymethylcytosine in different human tissues. J Nucleic Acids 2011: 870726.
44. Jin SG, Jiang Y, Qiu R, Rauch TA, Wang Y, et al. (2011) 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlate with IDH1 mutations. Cancer Res 71: 7360-7365.
45. Yang H, Liu Y, Bai F, Zhang JY, Ma SH, et al. (2012) Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene.
46. Biermann K, Heukamp LC, Steger K, Zhou H, Franke FE, et al. (2007) Gene expression profiling identifies new biological markers of neoplastic germ cells. Anticancer Res 27: 3091-3100. (Pubitemid 47607531)
47. Chen CC, Wang KY, Shen CK (2012) The mammalian de novo DNA methyltransferases DNMT3A and DNMT3B are also DNA 5-hydroxymethylcytosine dehydroxymethylases. J Biol Chem 287: 33116-33121.
48. Barreto G, Schafer A, Marhold J, Stach D, Swaminathan SK, et al. (2007) Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445: 671-675. (Pubitemid 46232889)
49. Jin SG, Guo C, Pfeifer GP (2008) GADD45A does not promote DNA demethylation. PLoS Genet 4: e1000013.
50. Almstrup K, Hoei-Hansen CE, Nielsen JE, Wirkner U, Ansorge W, et al. (2005) Genome-wide gene expression profiling of testicular carcinoma in situ progression into overt tumours. Br J Cancer 92: 1934-1941. (Pubitemid 40826144)
51. Manning M, Lissens W, Weidner W, Liebaers I (2001) DNA methylation analysis in immature testicular sperm cells at different developmental stages. Urol Int 67: 151-155. (Pubitemid 32722329)
52. Benchaib M, Braun V, Ressnikof D, Lornage J, Durand P, et al. (2005) Influence of global sperm DNA methylation on IVF results. Hum Reprod 20: 768-773. (Pubitemid 40425507)
53. Tunc O, Tremellen K (2009) Oxidative DNA damage impairs global sperm DNA methylation in infertile men. J Assist Reprod Genet 26: 537-544.
54. Skotheim RI, Lind GE, Monni O, Nesland JM, Abeler VM, et al. (2005) Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res 65: 5588-5598. (Pubitemid 40911159)
55. Okano M, Xie S, Li E (1998) Cloning and characterization of a family of novel mammalian DNA (cytosine-5) methyltransferases. Nat Genet 19: 219-220. (Pubitemid 28309328)
56. Deng J, Shoemaker R, Xie B, Gore A, LeProust EM, et al. (2009) Targeted bisulfite sequencing reveals changes in DNA methylation associated with nuclear reprogramming. Nat Biotechnol 27: 353-360.
57. Ueda Y, Okano M, Williams C, Chen T, Georgopoulos K, et al. (2006) Roles for Dnmt3b in mammalian development: a mouse model for the ICF syndrome. Development 133: 1183-1192.
58. Saitou M, Kagiwada S, Kurimoto K (2012) Epigenetic reprogramming in mouse pre-implantation development and primordial germ cells. Development 139: 15-31.
59. Lian CG, Xu Y, Ceol C, Wu F, Larson A, et al. (2012) Loss of 5- hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell 150: 1135-1146.