Epigenetics: A way to understand the origin and biology of testicular germ cell tumors

International Journal of Urology

Volumn 19, Issue 6, 2012, Pages 504-511

  Okamoto, Keisei ^a  

^a SHIGA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

Author keywords

Development; Epigenetics; Testicular cancer

Indexed keywords

CISPLATIN;

CANCER CHEMOTHERAPY; CLINICAL FEATURE; DNA METHYLATION; EPIGENETICS; GENE; GENE EXPRESSION; GENE FUNCTION; GERM CELL TUMOR; HISTOPATHOLOGY; HUMAN; NONHUMAN; PRIORITY JOURNAL; REVIEW; STEM CELL; TUMOR SUPPRESSOR GENE; XIST GENE;

ALU ELEMENTS; ANTINEOPLASTIC AGENTS; BIOLOGICAL MARKERS; CHROMOSOMES, HUMAN, X; CISPLATIN; CPG ISLANDS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DRUG RESISTANCE, NEOPLASM; EMBRYONIC STEM CELLS; EPIGENOMICS; GENES, TUMOR SUPPRESSOR; GENOMIC IMPRINTING; HUMANS; INTERSPERSED REPETITIVE SEQUENCES; LONG INTERSPERSED NUCLEOTIDE ELEMENTS; MALE; NEOPLASMS, GERM CELL AND EMBRYONAL; PROMOTER REGIONS, GENETIC; RNA, UNTRANSLATED; TESTICULAR NEOPLASMS; X CHROMOSOME INACTIVATION;

EID: 84861482632     PISSN: 09198172     EISSN: 14422042     Source Type: Journal    
DOI: 10.1111/j.1442-2042.2012.02986.x     Document Type: Review

References (93)

1. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J. Urol. 2003; 170: 5-11.
2. Ulbright TM. Germ cell neoplasms of the testis. Am. J. Surg. Pathol. 1993; 17: 1075-91.
3. Masters JR, Koberle B. Curing metastatic cancer: lessons from testicular germ-cell tumours. Nat. Rev. Cancer 2003; 3: 517-25.
4. Cheng L, Sung MT, Cossu-Rocca P etal. OCT4: biological functions and clinical applications as a marker of germ cell neoplasia. J. Pathol. 2007; 211: 1-9.
5. Taby R, Issa JP. Cancer epigenetics. CA Cancer J. Clin. 2010; 60: 376-92.
6. Portela A, Esteller M. Epigenetic modifications and human disease. Nat. Biotechnol. 2010; 28: 1057-68.
7. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001; 293: 1068-70.
8. Reik W, Dean W, Walter J. Epigenetic reprogramming in mammalian development. Science 2001; 293: 1089-93.
9. Baylin SB, Esteller M, Rountree MR, Bachman KE, Schuebel K, Herman JG. Aberrant patterns of DNA methylation, chromatin formation and gene expression in cancer. Hum. Mol. Genet. 2001; 10: 687-92.
10. Baylin SB, Herman JG, Graff JR, Vertino PM, Issa JP. Alterations in DNA methylation: a fundamental aspect of neoplasia. Adv. Cancer Res. 1998; 72: 141-96.
11. Esteller M. CpG island hypermethylation and tumor suppressor genes: a booming present, a brighter future. Oncogene 2002; 21: 5427-40.
12. Kawakami T, Okamoto K, Kataoka A etal. Multipoint methylation analysis indicates a distinctive epigenetic phenotype among testicular germ cell tumors and testicular malignant lymphomas. Genes Chromosomes Cancer 2003; 38: 97-101.
13. Ohm JE, McGarvey KM, Yu X etal. A stem cell-like chromatin pattern may predispose tumor suppressor genes to DNA hypermethylation and heritable silencing. Nat. Genet. 2007; 39: 237-42.
14. Costello JF, Fruhwald MC, Smiraglia DJ etal. Aberrant CpG-island methylation has non-random and tumour-type-specific patterns. Nat. Genet. 2000; 24: 132-8.
15. Smiraglia DJ, Szymanska J, Kraggerud SM, Lothe RA, Peltomaki P, Plass C. Distinct epigenetic phenotypes in seminomatous and nonseminomatous testicular germ cell tumors. Oncogene 2002; 21: 3909-16.
16. Cheung HH, Lee TL, Davis AJ, Taft DH, Rennert OM, Chan WY. Genome-wide DNA methylation profiling reveals novel epigenetically regulated genes and non-coding RNAs in human testicular cancer. Br. J. Cancer 2010; 102: 419-27.
17. Smith-Sorensen B, Lind GE, Skotheim RI etal. Frequent promoter hypermethylation of the O(6)-Methylguanine-DNA Methyltransferase (MGMT) gene in testicular cancer. Oncogene 2002; 21: 8878-84.
18. Honorio S, Agathanggelou A, Wernert N, Rothe M, Maher ER, Latif F. Frequent epigenetic inactivation of the RASSF1A tumour suppressor gene in testicular tumours and distinct methylation profiles of seminoma and nonseminoma testicular germ cell tumours. Oncogene 2003; 22: 461-6.
19. Lind GE, Skotheim RI, Fraga MF, Abeler VM, Esteller M, Lothe RA. Novel epigenetically deregulated genes in testicular cancer include homeobox genes and SCGB3A1 (HIN-1). J. Pathol. 2006; 210: 441-9.
20. Sandberg AA, Meloni AM, Suijkerbuijk RF. Reviews of chromosome studies in urological tumors. III. Cytogenetics and genes in testicular tumors. J. Urol. 1996; 155: 1531-56.
21. van Echten J, Oosterhuis JW, Looijenga LH etal. No recurrent structural abnormalities apart from i(12p) in primary germ cell tumors of the adult testis. Genes Chromosomes Cancer 1995; 14: 133-44.
22. Hasle H, Mellemgaard A, Nielsen J, Hansen J. Cancer incidence in men with Klinefelter syndrome. Br. J. Cancer 1995; 71: 416-20.
23. Brown CJ, Hendrich BD, Rupert JL etal. The human XIST gene: analysis of a 17kb inactive X-specific RNA that contains conserved repeats and is highly localized within the nucleus. Cell 1992; 71: 527-42.
24. Penny GD, Kay GF, Sheardown SA, Rastan S, Brockdorff N. Requirement for Xist in X chromosome inactivation [see comments]. Nature 1996; 379: 131-7.
25. McCarrey JR, Dilworth DD. Expression of Xist in mouse germ cells correlates with X-chromosome inactivation. Nat. Genet. 1992; 2: 200-3.
26. Salido EC, Yen PH, Mohandas TK, Shapiro LJ. Expression of the X-inactivation-associated gene XIST during spermatogenesis. Nat. Genet. 1992; 2: 196-9.
27. Looijenga LH, Gillis AJ, van Gurp RJ, Verkerk AJ, Oosterhuis JW. X inactivation in human testicular tumors. XIST expression and androgen receptor methylation status. Am. J. Pathol. 1997; 151: 581-90.
28. Kawakami T, Okamoto K, Sugihara H etal. The roles of supernumerical X chromosomes and XIST expression in testicular germ cell tumors. J. Urol. 2003; 169: 1546-52.
29. Allen RC, Zoghbi HY, Moseley AB, Rosenblatt HM, Belmont JW. Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation. Am. J. Hum. Genet. 1992; 51: 1229-39.
30. Kirchgessner CU, Warren ST, Willard HF. X inactivation of the FMR1 fragile X mental retardation gene. J. Med. Genet. 1995; 32: 925-9.
31. Huber R, Hansen RS, Strazzullo M etal. DNA methylation in transcriptional repression of two differentially expressed X-linked genes, GPC3 and SYBL1. Proc. Natl. Acad. Sci. U.S.A. 1999; 96: 616-21.
32. Kawakami T, Okamoto K, Ogawa O, Okada Y. XIST unmethylated DNA fragments in male-derived plasma as a tumour marker for testicular cancer. Lancet 2004; 363: 40-2.
33. Okamoto K, Kawakami T. Epigenetic profile of testicular germ cell tumours. Int. J. Androl. 2007; 30: 385-92, discussion 392.
34. Barlow DP. Methylation and imprinting: from host defense to gene regulation? Science 1993; 260: 309-10.
35. Szabo PE, Mann JR. Biallelic expression of imprinted genes in the mouse germ line: implications for erasure, establishment, and mechanisms of genomic imprinting. Genes Dev. 1995; 9: 1857-68.
36. Villar AJ, Eddy EM, Pedersen RA. Developmental regulation of genomic imprinting during gametogenesis. Dev. Biol. 1995; 172: 264-71.
37. van Gurp RJ, Oosterhuis JW, Kalscheuer V, Mariman EC, Looijenga LH. Biallelic expression of the H19 and IGF2 genes in human testicular germ cell tumors. J. Natl. Cancer Inst. 1994; 86: 1070-5.
38. Verkerk AJ, Ariel I, Dekker MC etal. Unique expression patterns of H19 in human testicular cancers of different etiology. Oncogene 1997; 14: 95-107.
39. Nonomura N, Miki T, Nishimura K, Kanno N, Kojima Y, Okuyama A. Altered imprinting of the H19 and insulin-like growth factor II genes in testicular tumors. J. Urol. 1997; 157: 1977-9.
40. Kawakami T, Chano T, Minami K, Okabe H, Okada Y, Okamoto K. Imprinted DLK1 is a putative tumor suppressor gene and inactivated by epimutation at the region upstream of GTL2 in human renal cell carcinoma. Hum. Mol. Genet. 2006; 15: 821-30.
41. Bartolomei MS, Webber AL, Brunkow ME, Tilghman SM. Epigenetic mechanisms underlying the imprinting of the mouse H19 gene. Genes Dev. 1993; 7: 1663-73.
42. Ferguson-Smith AC, Sasaki H, Cattanach BM, Surani MA. Parental-origin-specific epigenetic modification of the mouse H19 gene. Nature 1993; 362: 751-5.
43. Jinno Y, Sengoku K, Nakao M etal. Mouse/human sequence divergence in a region with a paternal-specific methylation imprint at the human H19 locus. Hum. Mol. Genet. 1996; 5: 1155-61.
44. Kerjean A, Dupont JM, Vasseur C etal. Establishment of the paternal methylation imprint of the human H19 and MEST/PEG1 genes during spermatogenesis. Hum. Mol. Genet. 2000; 9: 2183-7.
45. Lee J, Inoue K, Ono R etal. Erasing genomic imprinting memory in mouse clone embryos produced from day 11.5 primordial germ cells. Development 2002; 129: 1807-17.
46. Hajkova P, Erhardt S, Lane N etal. Epigenetic reprogramming in mouse primordial germ cells. Mech. Dev. 2002; 117: 15-23.
47. Tada T, Tada M, Hilton K etal. Epigenotype switching of imprintable loci in embryonic germ cells. Dev. Genes Evol. 1998; 207: 551-61.
48. Kawakami T, Zhang C, Okada Y, Okamoto K. Erasure of methylation imprint at the promoter and CTCF-binding site upstream of H19 in human testicular germ cell tumors of adolescents indicate their fetal germ cell origin. Oncogene 2006; 25: 3225-36.
49. Sievers S, Alemazkour K, Zahn S etal. IGF2/H19 imprinting analysis of human germ cell tumors (GCTs) using the methylation-sensitive single-nucleotide primer extension method reflects the origin of GCTs in different stages of primordial germ cell development. Genes Chromosomes Cancer 2005; 44: 256-64.
50. Takai D, Gonzales FA, Tsai YC, Thayer MJ, Jones PA. Large scale mapping of methylcytosines in CTCF-binding sites in the human H19 promoter and aberrant hypomethylation in human bladder cancer. Hum. Mol. Genet. 2001; 10: 2619-26.
51. Ulaner GA, Yang Y, Hu JF, Li T, Vu TH, Hoffman AR. CTCF binding at the insulin-like growth factor-II (IGF2)/H19 imprinting control region is insufficient to regulate IGF2/H19 expression in human tissues. Endocrinology 2003; 144: 4420-6.
52. Ulaner GA, Vu TH, Li T etal. Loss of imprinting of IGF2 and H19 in osteosarcoma is accompanied by reciprocal methylation changes of a CTCF-binding site. Hum. Mol. Genet. 2003; 12: 535-49.
53. Wermann H, Stoop H, Gillis AJ etal. Global DNA methylation in fetal human germ cells and germ cell tumours: association with differentiation and cisplatin resistance. J. Pathol. 2010; 221: 433-42.
54. Zhang C, Kawakami T, Okada Y, Okamoto K. Distinctive epigenetic phenotype of cancer testis antigen genes among seminomatous and nonseminomatous testicular germ-cell tumors. Genes Chromosomes Cancer 2005; 43: 104-12.
55. Lander ES, Linton LM, Birren B etal. Initial sequencing and analysis of the human genome. Nature 2001; 409: 860-921.
56. Jordan IK, Rogozin IB, Glazko GV, Koonin EV. Origin of a substantial fraction of human regulatory sequences from transposable elements. Trends Genet. 2003; 19: 68-72.
57. Kazazian HH Jr. Mobile elements: drivers of genome evolution. Science 2004; 303: 1626-32.
58. Wilson AS, Power BE, Molloy PL. DNA hypomethylation and human diseases. Biochim. Biophys. Acta 2007; 1775: 138-62.
59. Ushida H, Kawakami T, Minami K etal. Methylation profile of DNA repetitive elements in human testicular germ cell tumor. Mol. Carcinog. 2011; DOI: 10.1002/mc.20831.
60. Choi IS, Estecio MR, Nagano Y etal. Hypomethylation of LINE-1 and Alu in well-differentiated neuroendocrine tumors (pancreatic endocrine tumors and carcinoid tumors). Mod. Pathol. 2007; 20: 802-10.
61. Rodriguez J, Vives L, Jorda M etal. Genome-wide tracking of unmethylated DNA Alu repeats in normal and cancer cells. Nucleic Acids Res. 2008; 36: 770-84.
62. Xiang S, Liu Z, Zhang B etal. Methylation status of individual CpG sites within Alu elements in the human genome and Alu hypomethylation in gastric carcinomas. BMC Cancer 2010; 10: 44.
63. Xie H, Wang M, Bonaldo Mde F etal. Epigenomic analysis of Alu repeats in human ependymomas. Proc. Natl. Acad. Sci. U.S.A. 2010; 107: 6952-7.
64. Boyer LA, Lee TI, Cole MF etal. Core transcriptional regulatory circuitry in human embryonic stem cells. Cell 2005; 122: 947-56.
65. Loh YH, Wu Q, Chew JL etal. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat. Genet. 2006; 38: 431-40.
66. Sonne SB, Perrett RM, Nielsen JE etal. Analysis of SOX2 expression in developing human testis and germ cell neoplasia. Int. J. Dev. Biol. 2010; 54: 755-60.
67. Looijenga LH, Stoop H, de Leeuw HP etal. POU5F1 (OCT3/4) identifies cells with pluripotent potential in human germ cell tumors. Cancer Res. 2003; 63: 2244-50.
68. Cheng L. Establishing a germ cell origin for metastatic tumors using OCT4 immunohistochemistry. Cancer 2004; 101: 2006-10.
69. Jones TD, Ulbright TM, Eble JN, Baldridge LA, Cheng L. OCT4 staining in testicular tumors: a sensitive and specific marker for seminoma and embryonal carcinoma. Am. J. Surg. Pathol. 2004; 28: 935-40.
70. Hart AH, Hartley L, Parker K etal. The pluripotency homeobox gene NANOG is expressed in human germ cell tumors. Cancer 2005; 104: 2092-8.
71. de Jong J, Looijenga LH. Stem cell marker OCT3/4 in tumor biology and germ cell tumor diagnostics: history and future. Crit. Rev. Oncog. 2006; 12: 171-203.
72. Santagata S, Ligon KL, Hornick JL. Embryonic stem cell transcription factor signatures in the diagnosis of primary and metastatic germ cell tumors. Am. J. Surg. Pathol. 2007; 31: 836-45.
73. Looijenga LH, Gillis AJ, Stoop HJ, Hersmus R, Oosterhuis JW. Chromosomes and expression in human testicular germ-cell tumors: insight into their cell of origin and pathogenesis. Ann. N. Y. Acad. Sci. 2007; 1120: 187-214.
74. Perrett RM, Turnpenny L, Eckert JJ etal. The early human germ cell lineage does not express SOX2 during in vivo development or upon in vitro culture. Biol. Reprod. 2008; 78: 852-8.
75. de Jong J, Stoop H, Gillis AJ etal. Differential expression of SOX17 and SOX2 in germ cells and stem cells has biological and clinical implications. J. Pathol. 2008; 215: 21-30.
76. Minami K, Chano T, Kawakami T etal. DNMT3L is a novel marker and is essential for the growth of human embryonal carcinoma. Clin. Cancer Res. 2010; 16: 2751-9.
77. Ushida H, Kawakami T, Minami K etal. Therapeutic Potential of SOX2 Inhibition in Embryonal Carcinoma. J. Urol. 2012; (in press).
78. De Jong J, Weeda S, Gillis AJ, Oosterhuis JW, Looijenga LH. Differential methylation of the OCT3/4 upstream region in primary human testicular germ cell tumors. Oncol. Rep. 2007; 18: 127-32.
79. van de Geijn GJ, Hersmus R, Looijenga LH. Recent developments in testicular germ cell tumor research. Birth Defects Res. C Embryo Today 2009; 87: 96-113.
80. Nettersheim D, Biermann K, Gillis AJ, Steger K, Looijenga LH, Schorle H. NANOG promoter methylation and expression correlation during normal and malignant human germ cell development. Epigenetics 2011; 6: 114-22.
81. Almstrup K, Hoei-Hansen CE, Nielsen JE etal. Genome-wide gene expression profiling of testicular carcinoma in situ progression into overt tumours. Br. J. Cancer 2005; 92: 1934-41.
82. Bourc'his D, Bestor TH. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 2004; 431: 96-9.
83. Bourc'his D, Xu GL, Lin CS, Bollman B, Bestor TH. Dnmt3L and the establishment of maternal genomic imprints. Science 2001; 294: 2536-9.
84. Durcova-Hills G, Tang F, Doody G, Tooze R, Surani MA. Reprogramming primordial germ cells into pluripotent stem cells. PLoS ONE 2008; 3: e3531.
85. Jacobsen R, Bostofte E, Engholm G etal. Risk of testicular cancer in men with abnormal semen characteristics: cohort study. BMJ 2000; 321: 789-92.
86. Skakkebaek NE, Holm M, Hoei-Hansen C, Jorgensen N, Rajpert-De Meyts E. Association between testicular dysgenesis syndrome (TDS) and testicular neoplasia: evidence from 20 adult patients with signs of maldevelopment of the testis. Apmis. 2003; 111: 1-9, discussion 9-11.
87. Almstrup K, Mlynarska O, Rajpert-De Meyts E. Germ Cell Cancer, Testicular Dysgenesis Syndrome and Epigenetics. Springer, Berlin, Heidelberg, 2011.
88. Einhorn LH. Curing metastatic testicular cancer. Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 4592-5.
89. Koul S, McKiernan JM, Narayan G etal. Role of promoter hypermethylation in Cisplatin treatment response of male germ cell tumors. Mol. Cancer 2004; 3: 16.
90. Hajkova P, Ancelin K, Waldmann T etal. Chromatin dynamics during epigenetic reprogramming in the mouse germ line. Nature 2008; 452: 877-81.
91. Gaspar-Maia A, Alajem A, Meshorer E, Ramalho-Santos M. Open chromatin in pluripotency and reprogramming. Nat. Rev. Mol. Cell Biol. 2011; 12: 36-47.
92. Almstrup K, Nielsen JE, Mlynarska O etal. Carcinoma in situ testis displays permissive chromatin modifications similar to immature foetal germ cells. Br. J. Cancer 2010; 103: 1269-76.
93. Creyghton MP, Cheng AW, Welstead GG etal. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl. Acad. Sci. U.S.A. 2010; 107: 21931-6.