Origin of pluripotent germ cell tumours: The role of microenvironment during embryonic development

Molecular and Cellular Endocrinology

Volumn 288, Issue 1-2, 2008, Pages 111-118

  Kristensen, David Møbjerg ^a   Sonne, Si Brask ^a   Ottesen, Anne Marie ^a   Perrett, Rebecca M ^b   Nielsen, John E ^a   Almstrup, Kristian ^a   Skakkebaek, Niels E ^a   Leffers, Henrik ^a   Meyts, Ewa Rajpert De ^a  

^a Rigshospitalet   (Denmark)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

Cancer stem cells; Carcinoma in situ testis; Germ cell differentiation; Germ cell neoplasm; Pluripotency; Stem cells

Indexed keywords

OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN TFAP2C; REGULATOR PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2;

ARTICLE; CANCER GROWTH; CANCER INVASION; CANCER STEM CELL; CARCINOMA IN SITU; CELL DIFFERENTIATION; CELL MATURATION; CELL PROLIFERATION; CELL STRUCTURE; CELL TRANSFORMATION; DOWN REGULATION; EMBRYO DEVELOPMENT; EMBRYONIC STEM CELL; FETUS CELL; GERM CELL TUMOR; GONAD DEVELOPMENT; HUMAN; INNER CELL MASS; MEIOSIS; MICROENVIRONMENT; NONHUMAN; PATHOGENESIS; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEMINOMA; SPERMATOGENESIS; TERATOMA; TISSUE TYPES; UPREGULATION;

ANIMALS; BIOLOGICAL MARKERS; CARCINOMA IN SITU; EMBRYONIC DEVELOPMENT; ENDOCRINE DISRUPTORS; HUMANS; NEOPLASMS, GERM CELL AND EMBRYONAL; NEOPLASTIC STEM CELLS;

EID: 44649170845     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.02.018     Document Type: Article

References (84)

1. Albrechtsen R., Nielsen M.H., Skakkebaek N.E., and Wewer U. Carcinoma in situ of the testis. Some ultrastructural characteristics of germ cells. Acta Pathol. Microbiol. Immunol. Scand. 90 (1982) 301-303
2. Almstrup K., Hoei-Hansen C.E., Wirkner U., Blake J., Schwager C., Ansorge W., Nielsen J.E., Skakkebaek N.E., Rajpert-De Meyts E., and Leffers H. Embryonic stem cell-like features of testicular carcinoma in situ revealed by genome-wide gene expression profiling. Cancer Res. 64 (2004) 4736-4743
3. Almstrup K., Hoei-Hansen C.E., Nielsen J.E., Wirkner U., Ansorge W., Skakkebaek N.E., Rajpert-De Meyts E., and Leffers H. Genome-wide gene expression profiling of testicular carcinoma in situ progression into overt tumours. Brit. J. Cancer 92 (2005) 1934-1941
4. Andrews P.W. Teratocarcinomas and human embryology: pluripotent human EC cell lines. Review article. APMIS 106 (1998) 158-167
5. Andrews P.W., Matin M.M., Bahrami A.R., Damjanov I., Gokhale P., and Draper J.S. Embryonic stem (ES) cells and embryonal carcinoma (EC) cells: opposite sides of the same coin. Biochem. Soc. Trans. 33 (2005) 1526-1530
6. Atkin N.B., and Baker M.C. Specific chromosome change, i(12p), in testicular tumours?. Lancet 8311 (1982) 1349
7. Avilion A.A., Nicolis S.K., Pevny L.H., Perez L., Vivian N., and Lovell-Badge R. Multipotent cell lineages in early mouse development depend on SOX2 function. Genes Dev. 17 (2003) 126-140
8. Baker D.E., Harrison N.J., Maltby E., Smith K., Moore H.D., Shaw P.J., Heath P.R., Holden H., and Andrews P.W. Adaptation to culture of human embryonic stem cells and oncogenesis in vivo. Nat. Biotechnol. 25 (2007) 207-215
9. Birnbaum L.S., and Fenton S.E. Cancer and developmental exposure to endocrine disruptors. Environ. Health Perspect. 111 (2003) 389-394
10. Cavaleri F., and Scholer H.R. Nanog: a new recruit to the embryonic stem cell orchestra. Cell 113 (2003) 551-552
11. Chambers I., Colby D., Robertson M., Nichols J., Lee S., Tweedie S., and Smith A. Functional expression cloning of Nanog, a pluripotency sustaining factor in embryonic stem cells. Cell 113 (2003) 643-655
12. Clark A.T., Rodriguez R.T., Bodnar M.S., Abeyta M.J., Cedars M.I., Turek P.J., Firpo M.T., and Reijo-Pera R.A. Human STELLAR, NANOG, and GDF3 genes are expressed in pluripotent cells and map to chromosome 12p13, a hotspot for teratocarcinoma. Stem Cells 22 (2004) 169-179
13. Cools M., Stoop H., Kersemaekers A.M., Drop S.L., Wolffenbuttel K.P., Bourguignon J.P., Slowikowska-Hilczer J., Kula K., Faradz S.M., Oosterhuis J.W., and Looijenga L.H. Gonadoblastoma arising in undifferentiated gonadal tissue within dysgenetic gonads. J. Clin. Endocrinol. Metab. 91 (2006) 2404-2413
14. Dieckmann K.P. Residual carcinoma-in-situ of contralateral testis after chemotherapy. Lancet 1 (1988) 765
15. Dieckmann K.P., and Loy V. Persistent testicular intraepithelial neoplasia after chemotherapy. Eur. Urol. 20 (1991) 258-260
16. Draper J.S., Smith K., Gokhale P., Moore H.D., Maltby E., Johnson J., Meisner L., Zwaka T.P., Thomson J.A., and Andrews P.W. Recurrent gain of chromosomes 17q and 12 in cultured human embryonic stem cells. Nat. Biotechnol. 22 (2004) 53-54
17. Fisher J.S., Macpherson S., Marchetti N., and Sharpe R.M. Human 'testicular dysgenesis syndrome': a possible model using in-utero exposure of the rat to dibutyl phthalate. Hum. Reprod. 18 (2003) 1383-1394
18. Forest M.G., Cathiard A.M., and Bertrand J.A. Evidence of testicular activity in early infancy. J. Clin. Endocrinol. Metab. 37 (1973) 148-151
19. Geurts van Kessel A., van Drunen E., de Jong B., Oosterhuis J.W., Langeveld A., and Mulder M.P. Chromosome 12q heterozygosity is retained in i(12p)-positive testicular germ cell tumor cells. Cancer Genet. Cytogenet. 40 (1989) 129-134
20. Giwercman A., Cantell L., and Marks A. Placental-like alkaline phosphatase as a marker of carcinoma-in-situ of the testis. Comparison with monoclonal antibodies M2A and 43-9F. APMIS 99 (1991) 586-594
21. Guan K., Nayernia K., Maier L.S., Wagner S., Dressel R., Lee J.H., Nolte J., Wolf F., Li M., Engel W., and Hasenfuss G. Pluripotency of spermatogonial stem cells from adult mouse testis. Nature 440 (2006) 1199-1203
22. Hadziselimovic F., Thommen L., Girard J., and Herzog B. The significance of postnatal gonadotropin surge for testicular development in normal and cryptorchid testes. J. Urol. 136 (1986) 274-276
23. Hardell L., van Bavel B., Lindstrom G., Carlberg M., Dreifaldt A.C., Wijkstrom H., Starkhammar H., Eriksson M., Hallquist A., and Kolmert T. Increased concentrations of polychlorinated biphenyls, hexachlorobenzene, and chlordanes in mothers of men with testicular cancer. Environ. Health Perspect. 111 (2003) 930-934
24. Hemminki K., and Li X. Cancer risks in second-generation immigrants to Sweden. Int. J. Cancer 99 (2002) 229-237
25. Hemminki K., Li X., and Czene K. Cancer risks in first-generation immigrants to Sweden. Int. J. Cancer 99 (2002) 218-228
26. Hoei-Hansen C.E., Holm M., Rajpert-De Meyts E., and Skakkebaek N.E. Histological evidence of testicular dysgenesis in contralateral biopsies of 218 patients with testicular germ cell cancer. J. Pathol. 200 (2003) 370-374
27. Hoei-Hansen C.E., Nielsen J.E., Almstrup K., Sonne S.B., Graem N., Skakkebaek N.E., Leffers H., and Rajpert-De Meyts E. Transcription factor AP-2gamma is a developmentally regulated marker of testicular carcinoma in situ and germ cell tumors. Clin. Cancer Res. 10 (2004) 8521-8530
28. Hoei-Hansen C.E., Almstrup K., Nielsen J.E., Brask S.S., Graem N., Skakkebaek N.E., Leffers H., and Rajpert-De Meyts E. Stem cell pluripotency factor NANOG is expressed in human fetal gonocytes, testicular carcinoma in situ and germ cell tumours. Histopathology 47 (2005) 48-56
29. Hoei-Hansen C.E., Carlsen E., Jorgensen N., Leffers H., Skakkebaek N.E., and Rajpert-De Meyts E. Towards a non-invasive method for early detection of testicular neoplasia in semen samples by identification of fetal germ cell-specific markers. Hum. Reprod. 22 (2007) 167-173
30. Holm M., Rajpert-De Meyts E., Andersson A.M., and Skakkebaek N.E. Leydig cell micronodules are a common finding in testicular biopsies from men with impaired spermatogenesis and are associated with decreased testosterone/LH ratio. J. Pathol. 199 (2003) 378-386
31. Honecker F., Stoop H., de Krijger R.R., Lau Y.-F.C., Bokemeyer C., and Looijenga L.H. Pathobiological implications of the expression of markers of testicular carcinoma in situ by fetal germ cells. J. Pathol. 203 (2004) 849-857
32. Honecker F., Stoop H., Mayer F., Bokemeyer C., Castrillon D.H., Lau Y.F., Looijenga L.H., and Oosterhuis J.W. Germ cell lineage differentiation in non-seminomatous germ cell tumours. J. Pathol. 208 (2006) 395-400
33. Jorgensen N., Rajpert-De Meyts E., Graem N., Muller J., Giwercman A., and Skakkebaek N.E. Expression of immunohistochemical markers for testicular carcinoma in situ by normal human fetal germ cells. Lab. Invest. 72 (1995) 223-231
34. Korkola J.E., Houldsworth J., Chadalavada R.S., Olshen A.B., Dobrzynski D., Reuter V.E., Bosl G.J., and Chaganti R.S. Down-regulation of stem cell genes, including those in a 200-kb gene cluster at 12p13.31, is associated with in vivo differentiation of human male germ cell tumors. Cancer Res. 66 (2006) 820-827
35. Kraggerud S.M., Skotheim R.I., Szymanska J., Eknaes M., Fossa S.D., Stenwig A.E., Peltomaki P., and Lothe R.A. Genome profiles of familial/bilateral and sporadic testicular germ cell tumors. Genes Chromosomes Cancer 34 (2002) 168-174
36. Kristensen D.M., Kalisz M., and Nielsen J.H. Cytokine signalling in embryonic stem cells. APMIS 113 (2005) 756-772
37. Kristensen D.M., Nielsen J.E., Skakkebaek N.E., Graem N., Jacobsen G.K., Rajpert-De Meyts E., and Leffers H. Presumed pluripotency markers UTF-1 and REX-1 are expressed in human adult testes and germ cell neoplasms. Hum. Reprod. 23 (2008) 775-782
38. Looijenga L.H., Rosenberg C., van Gurp R.J., Geelen E., Echten-Arends J., de Jong B., Mostert M., and Wolter O.J. Comparative genomic hybridization of microdissected samples from different stages in the development of a seminoma and a non-seminoma. J. Pathol. 191 (2000) 187-192
39. Looijenga L.H., Stoop H., de Leeuw H.P., Gouveia Brazao C.A., Gillis A.J., van Roozendaal K.E., van Zoelen E.J., Weber R.F., Wolffenbuttel K.P., van Dekken H., Honecker F., Bokemeyer C., Perlman E.J., Schneider D.T., Kononen J., Sauter G., and Oosterhuis J.W. POU5F1 (OCT3/4) identifies cells with pluripotent potential in human germ cell tumors. Cancer Res. 63 (2003) 2244-2250
40. von der Maase H., Meinecke B., and Skakkebaek N.E. Residual carcinoma-in-situ of contralateral testis after chemotherapy. Lancet 27 (1988) 477-478
41. Main K.M., Kiviranta H., Virtanen H.E., Sundqvist E., Tuomisto J.T., Tuomisto J., Vartiainen T., Skakkebaek N.E., and Toppari J. Flame retardants in placenta and breast milk and cryptorchidism in newborn boys. Environ. Health Perspect. 115 (2007) 1519-1526
42. Mitsui K., Tokuzawa Y., Itoh H., Segawa K., Murakami M., Takahashi K., Maruyama M., Maeda M., and Yamanaka S. The homeoprotein Nanog is required for maintenance of pluripotency in mouse epiblast and ES cells. Cell 113 (2003) 631-642
43. Møller H. Decreased testicular cancer risk in men born in wartime. J. Natl. Cancer Inst. 81 (1989) 1668-1669
44. Muller J., Skakkebaek N.E., Nielsen O.H., and Graem N. Cryptorchidism and testis cancer. Atypical infantile germ cells followed by carcinoma in situ and invasive carcinoma in adulthood. Cancer 54 (1984) 629-634
45. Muller J., Visfeldt J., Philip J., and Skakkebaek N.E. Carcinoma in situ, gonadoblastoma, and early invasive neoplasia in a nine-year-old girl with 46,XY gonadal dysgenesis. APMIS 100 (1992) 170-174
46. Mylchreest E., Cattley R.C., and Foster P.M. Male reproductive tract malformations in rats following gestational and lactational exposure to di(n-butyl) phthalate: an antiandrogenic mechanism?. Toxicol. Sci. 43 (1998) 47-60
47. Nichols J., Zevnik B., Anastassiadis K., Niwa H., Klewe-Nebenius D., Chambers I., Scholer H., and Smith A. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95 (1998) 379-391
48. Nielsen H., Nielsen M., and Skakkebaek N.E. The fine structure of possible carcinoma-in-situ in the seminiferous tubules in the testis of four infertile men. Acta Pathol. Microbiol. Scand. A 82 (1974) 235-248
49. Nishimoto M., Miyagi S., Yamagishi T., Sakaguchi T., Niwa H., Muramatsu M., and Okuda A. Oct-3/4 maintains the proliferative embryonic stem cell state via specific binding to a variant octamer sequence in the regulatory region of the UTF1 locus. Mol. Cell Biol. 25 (2005) 5084-5094
50. Nistal M., Gonzalez-Peramato P., Regadera J., Serrano A., Tarin V., and De Miguel M.P. Primary testicular lesions are associated with testicular germ cell tumors of adult men. Am. J. Surg. Pathol. 30 (2006) 1260-1268
51. Niwa H. Molecular mechanism to maintain stem cell renewal of ES cells. Cell Struct. Funct. 26 (2001) 137-148
52. Niwa H., Miyazaki J., and Smith A.G. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat. Genet. 24 (2000) 372-376
53. Oosterhuis J.W., and Looijenga L.H. Testicular germ-cell tumours in a broader perspective. Nat. Rev. Cancer. 5 (2005) 210-222
54. Oosterhuis J.W., Castedo S.M., de Jong B., Seruca R., Dam A., Vos A., de Koning J., Schraffordt K.H., and Sleijfer D.T. A malignant mixed gonadal stromal tumor of the testis with heterologous components and i(12p) in one of its metastases. Cancer Genet. Cytogenet. 41 (1989) 105-114
55. Ottesen A.M., Skakkebaek N.E., Lundsteen C., Leffers H., Larsen J., and Rajpert-De Meyts E. High-resolution comparative genomic hybridization detects extra chromosome arm 12p material in most cases of carcinoma in situ adjacent to overt germ cell tumors, but not before the invasive tumor development. Genes Chromosomes Cancer 38 (2003) 117-125
56. Ottesen A.M., Larsen J., Gerdes T., Larsen J.K., Lundsteen C., Skakkebaek N.E., and Rajpert-De Meyts E. Cytogenetic investigation of testicular carcinoma in situ and early seminoma by high-resolution comparative genomic hybridization analysis of subpopulations flow sorted according to DNA content. Cancer Genet. Cytogenet. 149 (2004) 89-97
57. Ottesen A.M., Rajpert-De Meyts E., Holm M., Andersen I.L., Vogt P.H., Lundsteen C., and Skakkebaek N.E. Cytogenetic and molecular analysis of a family with three brothers afflicted with germ-cell cancer. Clin. Genet. 65 (2004) 32-39
58. Perrett R.M., Turpenny L., Eckert J.J., O'Shea M., Sonne S.B., Cameron I.T., Wilson D.A., Rajpert-De Meyts E., Hanley N.A., in press. The human germ cell lineage does not express SOX2 during early development or in early in vitro culture. Biol Reprod.
59. Rajpert-De Meyts E. Developmental model for the pathogenesis of testicular carcinoma in situ: genetic and environmental aspects. Hum. Reprod. Update 12 (2006) 303-323
60. Rajpert-De Meyts E., and Skakkebaek N.E. Expression of the c-kit protein product in carcinoma-in-situ and invasive testicular germ cell tumours. Int. J. Androl. 17 (1994) 85-92
61. Rajpert-De Meyts E., Jørgensen N., Müller J., and Skakkebaek N.E. Prolonged expression of the c-kit receptor in germ cells of intersex fetal testes. J. Pathol. 178 (1996) 166-169
62. Rajpert-De Meyts E., Jorgensen N., Brøndum-Nielsen K., Müller J., and Skakkebaek N.E. Developmental arrest of germ cells in the pathogenesis of germ cell neoplasia. APMIS 106 (1998) 198-206
63. Rajpert-De Meyts E., Hanstein R., Jorgensen N., Graem N., Vogt P.H., and Skakkebaek N.E. Developmental expression of POU5F1 (OCT-3/4) in normal and dysgenetic human gonads. Hum. Reprod. 19 (2004) 1338-1344
64. Richiardi L., Bellocco R., Adami H.O., Torrang A., Barlow L., Hakulinen T., Rahu M., Stengrevics A., Storm H., Tretli S., Kurtinaitis J., Tyczynski J.E., and Akre O. Testicular cancer incidence in eight northern European countries: secular and recent trends. Cancer Epidemiol. Biomarkers Prev. 13 (2004) 2157-2166
65. Santagata S., Ligon K.L., and Hornick J.L. Embryonic stem cell transcription factor signatures in the diagnosis of primary and metastatic germ cell tumors. Am. J. Surg. Pathol. 31 (2007) 836-845
66. Scholer H.R., Ruppert S., Suzuki N., Chowdhury K., and Gruss P. New type of POU domain in germ line-specific protein Oct-4. Nature 344 (1990) 435-439
67. Seandel M., James D., Shmelkov S.V., Falciatori I., Kim J., Chavala S., Scherr D.S., Zhang F., Torres R., Gale N.W., Yancopoulos G.D., Murphy A., Valenzuela D.M., Hobbs R.M., Pandolfi P.P., and Rafii S. Generation of functional multipotent adult stem cells from GPR125+ germline progenitors. Nature 20 449 (2007) 346-350
68. Sharpe R.M. Pathways of endocrine disruption during male sexual differentiation and masculinization. Best. Pract. Res. Clin. Endocrinol. Metab. 20 (2006) 91-110
69. Skakkebaek N.E. Abnormal morphology of germ cells in two infertile men. Acta Pathol. Microbiol. Scand. A 80 (1972) 374-378
70. Skakkebaek N.E. Possible carcinoma-in-situ of the testis. Lancet 2 (1972) 516-517
71. Skakkebaek N.E. Carcinoma in situ of the testis: frequency and relationship to invasive germ cell tumours in infertile men. Histopathology 2 (1978) 157-170
72. Skakkebaek N.E., Berthelsen J.G., Giwercman A., and Muller J. Carcinoma-in-situ of the testis: possible origin from gonocytes and precursor of all types of germ cell tumours except spermatocytoma. Int. J. Androl. 10 (1987) 19-28
73. Skakkebaek N.E., Rajpert-De Meyts E., and Main K.M. Testicular dysgenesis syndrome: an increasingly common developmental disorder with environmental aspects. Hum. Reprod. 16 (2001) 972-978
74. Skotheim R.I., Monni O., Mousses S., Fossa S.D., Kallioniemi O.P., Lothe R.A., and Kallioniemi A. New insights into testicular germ cell tumorigenesis from gene expression profiling. Cancer Res. 62 (2002) 2359-2364
75. Skotheim R.I., Lind G.E., Monni O., Nesland J.M., Abeler V.M., Fossa S.D., Duale N., Brunborg G., Kallioniemi O., Andrews P.W., and Lothe R.A. Differentiation of human embryonal carcinomas in vitro and in vivo reveals expression profiles relevant to normal development. Cancer Res. 65 (2005) 5588-5598
76. Skotheim R.I., Autio R., Lind G.E., Kraggerud S.M., Andrews P.W., Monni O., Kallioniemi O., and Lothe R.A. Novel genomic aberrations in testicular germ cell tumors by array-CGH, and associated gene expression changes. Cell Oncol. 28 (2006) 315-326
77. Solter D. From teratocarcinomas to embryonic stem cells and beyond: a history of embryonic stem cell research. Nat. Rev. Genet. 7 (2006) 319-327
78. Sperger J.M., Chen X., Draper J.S., Antosiewicz J.E., Chon C.H., Jones S.B., Brooks J.D., Andrews P.W., Brown P.O., and Thomson J.A. Gene expression patterns in human embryonic stem cells and human pluripotent germ cell tumors. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 13350-13355
79. Summersgill B., Osin P., Lu Y.J., Huddart R., and Shipley J. Chromosomal imbalances associated with carcinoma in situ and associated testicular germ cell tumours of adolescents and adults. Brit. J. Cancer. 85 (2001) 213-220
80. Swan S.H., Main K.M., Liu F., Stewart S.L., Kruse R.L., Calafat A.M., Mao C.S., Redmon J.B., Ternand C.L., Sullivan S., and Teague J.L. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ. Health Perspect. 113 (2005) 1056-1061
81. Ulbright T.M., Amin M.B., and Young R.H. Atlas of Tumor Pathology. Tumors of the Testis, Adnexa, Spermatic Cord, and Scrotum (1999), Armed Forces Institute of Pathology, Washington, DC, USA 1-385
82. Visfeldt J., Jorgensen N., Muller J., Moller H., and Skakkebaek N.E. Testicular germ cell tumours of childhood in Denmark, 1943-1989: incidence and evaluation of histology using immunohistochemical techniques. J. Pathol. 174 (1994) 39-47
83. von Eyben F.E. Chromosomes, genes, and development of testicular germ cell tumors. Cancer Genet. Cytogenet. 151 (2004) 93-138
84. Wicha M.S., Liu S., and Dontu G. Cancer stem cells: an old idea-a paradigm shift. Cancer Res. 66 (2006) 1883-1890