The emerging phenotype of the testicular carcinoma in situ germ cell

APMIS

Volumn 111, Issue 1, 2003, Pages 267-279

  Rajpert De Meyts, Ewa ^a   Bartkova, Jirina ^b   Samson, Michel ^c   Hoei Hansen, Christina E ^a   Frydelund Larsen, Lone ^a   Bartek, Jiri ^b   Skakkebæk, Niels E ^a   Oliver, Tim ^d   Sharpe, Richard ^d   Looijenga, Leendert ^d   Møller, Henrik ^d   Von Eyben, Finn Edler ^d  

^a Rigshospitalet   (Denmark)

^b DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^c UNIVERSITÉ DE RENNES 1   (France)

^d Section GR 5064 ^*

Author keywords

Cancer testis antigens; Carcinoma in situ (CIS); Embryonic stem cells; Germ cell differentiation; Testicular neoplasms

Indexed keywords

CANCER CELL; CANCER GROWTH; CARCINOMA IN SITU; CELL DIFFERENTIATION; CELL HETEROGENEITY; CELL LINEAGE; CELL PROLIFERATION; CELL TYPE; CHROMOSOME ANALYSIS; CONFERENCE PAPER; DISEASE COURSE; DNA REPAIR; EMBRYO CELL; EMBRYONAL CARCINOMA; GENE EXPRESSION; GENE LOCATION; GENOMICS; GERM CELL; GERM CELL TUMOR; HISTOPATHOLOGY; HUMAN; MALIGNANT TRANSFORMATION; MEIOSIS; MITOSIS; NONHUMAN; ONTOGENY; PHENOTYPE; PRIMORDIAL GERM CELL; PRIORITY JOURNAL; PUBERTY; SEMINOMA; SEX CHROMOSOME; SOMATIC CELL; SPERMATOGONIUM; STEM CELL; TERATOMA; TESTIS CANCER; X CHROMOSOME; Y CHROMOSOME;

ADOLESCENT; ADULT; ANTIGENS, NEOPLASM; CARCINOMA IN SITU; CELL CYCLE; CELL TRANSFORMATION, NEOPLASTIC; CHROMOSOMES, HUMAN, X; CHROMOSOMES, HUMAN, Y; DNA REPAIR; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; PHENOTYPE; SEMINOMA; SPERMATOZOA; STEM CELLS; TESTICULAR NEOPLASMS;

EID: 0037884916     PISSN: 09034641     EISSN: None     Source Type: Journal    
DOI: 10.1034/j.1600-0463.2003.11101301.x     Document Type: Conference Paper

References (101)

1. Skakkebæk NE. Possible carcinoma-in-situ of the testis. Lancet 1972;ii:516-7.
2. Skakkebæk NE, Berthelsen JG, Giwercman A, Müller 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 1987;10:19-28.
3. Ulbright TM, Amin MB, Young RH. Atlas of tumor pathology. Tumors of the testis, adnexa, spermatic cord, and scrotum. Armed Forces Institute of Pathology, Washington DC, USA, 1999, pp. 1-385.
4. Loy V, Dieckmann K-P. Carcinoma in situ of the testis: Intratubular germ cell neoplasia or testicular intraepithelial neoplasia? Hum Pathol 1990;21:457.
5. Grigor KM. A new classification of germ cell tumours of the testis. Eur Urol 1993;23:93-103.
6. Nielsen H, Nielsen M, Skakkebæk NE. The fine structure of a possible carcinoma-in-situ in the seminiferous tubules in the testis of four infertile men. APMIS 1974;82:235-48.
7. Holstein AE Körner F. Light and electron microscopical analysis of cell types in human seminoma. Virch Arch A 1974;363:97-112.
8. Albrechtsen R, Nielsen MH, Skakkebæk NE, Wewer U. Carcinoma in situ of the testis. Some ultrastructural characteristics of germ cells. APMIS 1982;90:301-3.
9. Gondos B. Ultrastructure of developing and malignant germ cells. Eur Urol 1993;23:68-75.
10. Müller J, Skakkebæk NE, Ritzén EM, Plöen L, Petersen KE. Carcinoma in situ of the testis in children with 45,X/46,XY gonadal dysgenesis. J Pediatr 1985;106:431-6.
11. MacMahon RA, Cussen LJ. Detection of gonadal carcinoma in situ in childhood and implications for management. Aust N Z J Surg 1991;61:667-9.
12. Müller J, Visfeldt J, Philip J, Skakkebæk NE. Carcinoma in situ, gonadoblastoma, and early invasive neoplasia in a nine-year-old girl with 46,XY gonadal dysgenesis. APMIS 1992;100:170-4.
13. Jacobsen GK, Henriques UV. A fetal testis with intratubular germ cell neoplasia (ITGCN). Mod Pathol 1992;5:547-9.
14. Ramani P, Yeung CK, Habeebu SSM. Testicular intratubular germ cell neoplasia in children and adolescents with intersex. Am J Surg Pathol 1993;17:1124-33.
15. Slowikowska-Hilczer J, Szarras-Czapnik M, Kula K. Testicular pathology in 46,XY dysgenetic male pseudohermaphroditism: an approach to pathogenesis of testis cancer. J Androl 2001;22:781-92.
16. Beckstead JH. Alkaline phosphatase histochemistry in human germ cell neoplasms. Am J Surg Pathol 1983;7:341-9.
17. Jacobsen GK, Nørgaard-Pedersen B. Placental alkaline phosphatase in testicular germ cell tumours and in carcinoma-in-situ of the testis. Acta Pathol Microbiol Scand A 1984;92:323-9.
18. Manivel JC, Jessurun J, Wick MR, Dehner LP. Placental alkaline phosphatase immunoreactivity in testicular germ-cell neoplasms. Am J Surg Pathol 1987;11:21-9.
19. Hustin J, Collette J, Franchimont P. Immunohistochemical demonstration of placental alkaline phosphatase in various states of testicular development and in germ cell turnouts. Int J Androl 1987;10:29-35.
20. Koide O, Iwai S, Baba K, Iri H. Identification of testicular atypical germ cells by an immunohistochemical technique for placental alkaline phosphatase. Cancer 1987;60:1325-30.
21. Burke AR Mostofi FK. Intratubular malignant germ cells in testicular biopsies: Clinical course and identification by staining for placental alkaline phosphatase. Mod Pathol 1988;1:475-9.
22. Giwercman A, Cantell L, 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 1991;99:586-94.
23. Hofmann MC, Millán JL. Developmental expression of alkaline phosphatase genes; reexpression in germ cell tumours and in vitro immortalized germ cells. Eur Urol 1993;23:38-45.
24. Jørgensen N, Rajpert-De Meyts E, Graem N, Müller J, Giwercman A, Skakkebæk NE. Expression of immunohistochemical markers for testicular carcinoma in situ by normal human fetal germ cells. Lab Invest 1995;72:223-31.
25. Roelofs H, Manes T, Millan JL, Oosterhuis JW, Looijenga LHJ. Heterogeneity in alkaline phosphatase isozyme expression in human testicular germ cell turnouts. An enzyme-/immunohistochemical and molecular analysis. J Pathol 1999;189:236-44.
26. Jørgensen N, Giwercman A, Müller J, Skakkebæk NE. Immunohistochemical markers of carcinoma in situ of the testis also expressed in normal infantile germ cells. Histopathology 1993;22:373-8.
27. Rørth M, Rajpert-De Meyts E, Andersson L, Dieckmann K-P, Fosså SD, Grigor KM, et al. Carcinoma in situ in the testis. Scand J Urol Nephrol 2000;34(Suppl. 205):166-86.
28. Parkinson MC, Harland SJ, Harnden P, Sandison A. The role of the histopathologist in the management of testicular germ cell tumour in adults. Histopathology 2001;38:183-94.
29. Slowikowska-Hilczer J, Walczak-Jedrzejowska R, Kula K. Immunohistochemical diagnosis of preinvasive germ cell cancer of the testis. Folia Histochem Cytobiol 2001;39:67-72.
30. Giwercman A, Marks A, Bailey D, Baumal R, Skakkebæk NE. A monoclonal antibody as a marker for carcinoma in situ germ cells of the human adult testis. APMIS 1988;96:667-70.
31. Bailey A, Marks A, Stratis M, Baumal R. Immunohistochemical staining of germ cell tumors and intratubular malignant germ cells of the testis using antibody to placental alkaline phosphatase and a monoclonal anti-seminoma antibody. Mod Pathol 1991;4:167-71.
32. Marks A, Sutherland DR, Bailey D, Iglesias J, Law J, Lei M, et al. Characterization and distribution of an onco-fetal antigen (M2A antigen) expressed on testicular germ cell tumours. Brit J Cancer 1999;80:569-78.
33. Giwercman A, Lindenberg S, Kimber SJ, Andersson T, Müller J, Skakkebæk NE. Monoclonal antibody 43-9F as a sensitive immunohistochemical marker of carcinoma in situ of human testis. Cancer 1990;65:1135-42.
34. Heidenreich A, Sesterhenn IA, Mostofi FK, Moul JW. Immunohistochemical expression of monoclonal antibody 43-9F in testicular germ cell tumours. Int J Androl 1998;21:283-8.
35. Giwercman A, Andrews PW, Jørgensen N, Müller J, Græm N, Skakkebæk NE. Immunohistochemical expression of embryonal marker TRA-1-60 in carcinoma in situ and germ cell tumors of the testis. Cancer 1993;72:1308-14.
36. Rajpert-De Meyts E, Skakkebæk NE. Expression of the c-kit protein product in carcinoma in situ and invasive germ cell tumours. Int J Androl 1994;17:85-92.
37. Strohmeyer T, Reese D, Press M, Ackerman R, Hartmann M, Slamon D. Expression of the c-kit proto-oncogene and its ligand stem cell factor (SCF) in normal and malignant human testicular tissue. J Urol 1995;153:511-5.
38. Robinson LL, Gaskell TL, Saunders PT, Anderson RA. Germ cell specific expression of c-kit in the human fetal gonads. Mol Hum Reprod 2001;7:845-52.
39. Rajpert-De Meyts E, Jørgensen N, Müller J, Skakkebæk NE. Prolonged expression of the c-kit receptor in germ cells of intersex fetal testes. J Pathol 1996;178:166-9.
40. Izquierdo MA, Van der Valk P, Van Ark-Otte J, Rubio G, Germa-Lluch JR, Ueda R, et al. Differential expression of the c-kit proto-oncogene in germ cell tumours. J Pathol 1995;177:253-8.
41. Bokemeyer C, Kuczyk MA, Dunn T, Serth J, Hartmann K, Jonasson J, et al. Expression of stem-cell factor and its receptor c-kit protein in normal testicular tissue and malignant germ-cell tumours. J Cancer Res Clin Oncol 1996;122:301-6.
42. Rajpert-De Meyts E, Jørgensen N, Brøndum-Nielsen K, Müller J, Skakkebæk NE. Developmental arrest of germ cells in the pathogenesis of germ cell neoplasia. APMIS 1998;106:198-206.
43. Kang J-L, Rajpert-De Meyts E, Wiels J, and Skakkebæk NE. Expression of the glycolipid globotriaosylceramide (Gb3) in testicular carcinoma in situ. Virchows Arch 1995;426:369-74.
44. Kang J-L, Rajpert-De Meyts E, Skakkebæk NE. Immunoreactive neuron-specific enolase (NSE) is expressed in testicular carcinoma-in-situ. J Pathol 1996;178:161-5.
45. Drescher B, Lauke H, Hartmann M, Davidoff MS, Zumkeller W. Immunohistochemical pattern of insulin-like growth factor (IGF) I, IGF II, and IGF binding proteins 1 to 6 in carcinoma in situ of the testis. J Clin Pathol: Mol Pathol 1997;50:298-303.
46. Luo L-Y, Rajpert-De Meyts E, Jung K, Diamandis EP. Expression of the normal epithelial cell-specific 1 (NES1; KLK10) candidate tumour suppressor gene in normal testis and malignant testicular cancer. Br J Cancer 2001;85:220-4.
47. Franke FE, Pauls K, Metzger R, Danilov SM. Angiotensin 1-converting enzyme and potential substrates in human testis and testicular tumours. Review article. APMIS 2003;111:234-44.
48. Siegrist S, Féral C, Chami M, Solhonne B, Mattei MG, Rajpert-De Meyts E, et al. hHRev107, a class II tumour suppressor gene, is expressed by testicular germ cells and CIS cells but not by human testicular germ cell tumours. Oncogene 2001;20:5155-63.
49. Castrillon DH, Quade BJ, Wang TY, Quigley C, Crum CP. The human VASA gene is specifically expressed in the germ cell lineage. Proc Natl Acad Sci USA 2000;97:9585-90.
50. Zeeman AM, Stoop H, Boter M, Gillis AJM, Castrillon DH, Oosterhuis JW, Looijenga LHJ. VASA is a specific marker for both normal and malignant human germ cells. Lab Invest 2002;83;159-66.
51. Lahn BT, Page DC. Functional coherence of the Y chromosome. Science 1997;278:675-80.
52. Schnieders F, Dörk T, Arnemann J, Vogel T, Werner M, Schmidtke J. Testis-specific protein, Y-encoded (TSPY) expression in testicular tissues. Hum Mol Genet 1996;5:1801-7.
53. Lau Y-FC, Chou PM, Iezzoni JC, Alonzo JA, Kömüves LG. Expression of a candidate gene for the gonadoblastoma locus in gonadoblastoma and testicular seminoma. Cytogenet Cell Genet 2000;91:160-4.
54. Jørgensen N, Müller J, Jaubert F, Clausen OP, Skakkebæk NE. Heterogeneity of gonadoblastoma germ cells: similarities with immature germ cells, spermatogonia and testicular carcinoma in situ cells. Histopathology 1997;30:177-86.
55. Vogt P, Chandley AC, Hargreave TB, Keil R, Ma K, Sharkey A. Microdeletions in interval 6 of the Y chromosome of males with idiopathic sterility points to disruption of AZE a human spermatogenesis gene. Hum Genet 1992;89:491-6.
56. Reijo R, Lee TY, Salo P, Alagappan R, Brown LG, Rosenberg M, et al. Diverse spermatogenic defects in humans caused by Y chromosome deletions encompassing a novel RNA-binding protein gene. Nat Genet 1995;10:383-93.
57. Cooke HJ. Y chromosome and male infertility. Rev Reprod 1999;4:5-10.
58. Elliott DJ, Millar MR, Oghene K, Ross A, Kiesewetter F, Pryor J, et al. Expression of RBM in the nuclei of human germ cells is dependent on a critical region of the Y chromosome long arm. Proc Natl Acad Sci U S A 1997;94:3848-53.
59. Lifschitz-Mercer B, Elliott DJ, Leider-Trejo L, Schreiber-Bramante L, Hassner A, Eisenthal A, Maymon BB. Absence of RBM expression as a marker of intratubular (in situ) germ cell neoplasia of the testis. Hum Pathol 2000;31:1116-20.
60. Xu EY, Moore FL, Pera RA. A gene family required for human germ cell development evolved from an ancient meiotic gene conserved in metazoans. Proc Natl Acad Sci U S A 2001;98:7414-9.
61. Lifschitz-Mercer B, Elliott DJ, Issakov J, Leider-Trejo L, Schreiber L, et al. Localization of a specific germ cell marker, DAZL1, in testicular germ cell neoplasias. Virchows Arch 2002;440:387-91.
62. Reijo RA, Dorfman DM, Slee R, Renshaw AA, Loughlin KR, Cooke H, Page DC. DAZ family proteins exist throughout male germ cell development and transit from nucleus to cytoplasm at meiosis in humans and mice. Biol Reprod 2000;63:1490-6.
63. Wang PJ, McCarrey JR, Yang F, Page DC. An abundance of X-linked genes expressed in spermatogonia. Nat Genet 2001;27:422-6.
64. Atkin NB, Baker MC. X-chromatin, sex chromosomes, and ploidy in 37 germ cell tumors of the testis. Cancer Genet Cytogenet 1992;59:54-6.
65. Looijenga LHJ, Gillis AJM, van Gurp RJHM, Verkerk AJMH, Oosterhuis JW. X inactivation in human testicular tumours. XIST expression and androgen receptor methylation status. Am J Pathol 1997;151:581-90.
66. Aubry F, Satie A-P, Rioux-Leclercq N, Rajpert-De Meyts E, Spagnoli GC, Chomez P, et al. MAGE-A4, a germ-cell specific marker is differentially expressed in testicular tumours. Cancer 2001;902:2778-85.
67. Satie A-P, Rajpert-De Meyts E, Spagnoli GC, Henno S, Olivo L, Jacobsen GK, et al. The cancer-testis gene, NY-ESO-1 is expressed in normal foetal and adult testes, in spermatocytic seminoma and testicular carcinoma in situ. Lab Invest 2002;82:775-80.
68. Van den Eynde B, van der Bruggen P. T cell-defined tumor antigens. Curr Opin Immunol 1997;9:684-93.
69. Rajpert-De Meyts E, Jacobsen GK, Bartkova J, Aubry F, Samson M, Bartek J, Skakkebæk NE. The imunohistochemical expression pattern of Chk2, p19-INK4d, p53, MAGE-A4 and other selected antigens provides new evidence for the pre-meiotic origin of spermatocytic seminoma. Histopathology 2003;42:217-26.
70. Rudolph P, Kellner U, Schmidt D, Kirchner V, Talerman A, Harms D, Parwaresch R. Ki-A10, a germ cell nuclear antigen retained in a subset of germ cell-derived tumors. Am J Pathol 1999;154:795-803.
71. Stoop H, van Gurp R, de Krijger R, Geurts van Kessel A, Köberle B, Oosterhuis W, Looijenga L. Reactivity of germ cell maturation stage-specific markers in spermatocytic seminoma: diagnostic and etiological implications. Lab Invest 2001;81:919-28.
72. Einhorn LH. Testicular cancer: an oncological success story. Clin Cancer Res 1997;3:2630-2.
73. Rajpert-De Meyts E, Lauke H, Skakkebæk NE. In vitro survival of human neoplastic germ cells. Adv Exp Med Biol 1998;444:59-66.
74. Andrews PW. Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev Biol 1984;103:285-93.
75. Andrews PW. Teratocarcinomas and human embryology: Pluripotent human EC lines. APMIS 1998;106:158-68.
76. Bartkova J, Bartek J, Lukas J, Vojtesek B, Staskova Z, Rejthar A et al. p53 protein alterations in human testicular cancer including preinvasive intratubular germ cell neoplasia. Int J Cancer 1991;49:196-202.
77. Peng HQ, Hogg D, Malkin D, Bailey D, Gallie BL, Bulbui M, et al. Mutations of the p53 gene do not occur in testis cancer. Cancer Res 1993;53:3574-8.
78. Lutzker SG. P53 tumour suppressor gene and germ cell neoplasia. APMIS 1998;106:85-9.
79. Kuczyk M, Serth J, Bokemeyer C, Jonassen J, Machtens S, Wermer M, Jonas U. Alterations of the p53 tumour suppressor gene in carcinoma in situ of the testis. Cancer 1996;78:1958-66.
80. Quenby SM, Gazvani MR, Brazeau C, Neilson J, Lewis-Jones DI, Vince G. Oncogenes and tumour suppressor genes in first trimester human fetal gonadal development. Mol Hum Reprod 1999;5:737-41.
81. Nowak R, Grzybowska EA, Wilczynska A, Pykalo R, Siedlecki JA. Low expression of DNA polymerase β in human testicular germ cell tumours. Impact on foetal gonocytic origin theory. Acta Oncol 2002;41:188-91.
82. Datta MW, Macri E, Signoretti S, Renshaw A, Loda M. Transition from in situ to invasive testicular germ cell neoplasia is associated with the loss of p21 and gain of mdm-2 expression. Mod Pathol 2002;14:437-42.
83. Bartkova J, Falck J, Rajpert-De Meyts E, Skakkebæk NE, Lukas J, Bartek J. Chk2 tumour suppressor protein in human spermatogenesis and testicular germ-cell tumours. Oncogene 2001;20:5897-902.
84. Strohmeyer T, Reissmann P, Cordon-Cardo C, Hartmann M, Ackermann R, Slamon D. Correlation between retinoblastoma gene expression and differentiation in human testicular tumors. Proc Natl Acad Sci USA 1991;88:6662-6.
85. Bartkova J, Lukas C, Sørensen CS, Rajpert-De Meyts E, Skakkebæk NE, Lukas J, Bartek J. Deregulation of the RB pathway in human testicular germ cell tumours. J Pathol 2003; in press.
86. INK4d in human testicular germ-cell tumours contrasts with high expression during normal spermatogenesis. Oncogene 2000;19:4146-50.
87. Houldsworth J, Reuter C, Bosl GJ, Chaganti RSK. Aberrant expression of cyclin D2 is an early event in human male germ cell tumorigenesis. Cell Growth Diff 1997;8:293-9.
88. Bartkova J, Rajpert-De Meyts E, Skakkebæk NE, Bartek J. D-type cyclins in adult human testis and testicular cancer: relation to cell type, proliferation, differentiation, and malignancy. J Pathol 1999;187:573-81.
89. Bartkova J, Rajpert-De Meyts E, Skakkebæk NE, Lukas J, Bartek, J. Deregulation of the G1/S-phase control in human testicular germ cell tumours. APMIS 2003;111:252-66.
90. Pierce GB, Speers WC. Tumors as caricatures of the process of tissue renewal: prospects for therapy by directing differentiation. Cancer Res 1988;48:1996-2004.
91. Damjanov I, Horvath B, Gibas Z. Retinoic-cid induced differentiation of the developmentally pluripotent human germ cell tumor-derived cell line, NCCIT. Lab Invest 1993;68:220-32.
92. Andrews PW, Banting GS, Damjanov I, Arnaud D, Avner P. Three monoclonal antibodies defining distinct differentiation antigens associated with different high molecular weight polypeptides on the surface of human embryonal carcinoma cells. Hybridoma 1984;3:347-61.
93. Henderson JK, Draper JS, Baillie HS, Fishel S, Thomson JA, Moore H, Andrews PW. Preimplantation human embryos and embryonic stem cells show comparable expression of stage-specific embryonic antigens. Stem Cells 2002;20:329-37.
94. Sharma AK, Nelson MC, Brandt JE, Wessman M, Mahmud N, Welles KP, Hoffman R. Human CD34(+) stem cells express the hiwi gene, a human homologue of the Drosophila gene piwi. Blood 2001;97:426-34.
95. Qiao D, Zeeman A-M, Deng W, Looijenga LHJ, Lin H. Molecular characterization of hiwi, a human member of the piwi gene family whose overexpression is correlated to seminomas. Oncogene 2002;21:3988-99.
96. Schöler HR, Dressler GR, Balling R, Rohdewohld H, Gruss P. Oct-4: a germline specific transcription factor mapping to the mouse t-complex. EMBO J 1990;9:2185-95.
97. Palumbo C, van Roozendaal K, Gillis AJ, van Gurp RH, de Munnik H, Oosterhuis JW, et al. Expression of the PDGF α-receptor 1.5 kb transcript, OCT-4, and c-KIT in human normal and malignant tissues. Implications for the early diagnosis of testicular germ cell tumours and for our understanding of regulatory mechanisms. J Pathol 2002;196:467-77.
98. Looijenga LHJ, Stoop H, de Leeuw HPJC, de Gouveia Brazao CA, Gillis AJM, van Roozendaal KEP, et al. POU5F1 (OCT3/4) identifies cells with pluripotent potential in human germ cell tumors. Cancer Res 2003; in press.
99. Rajpert-De Meyts E, Kvist M, Skakkebæk NE. Heterogeneity of expression of immunohistochemical tumour markers in the testicular carcinoma-in situ: Pathogenetic relevance. Virchows Arch 1996;428:133-9.
100. Zafarana G, Gillis ADM, Ruud JHLM, van Gurp RJ, Olsson PG, Elsrodt F, et al. Coamplification of DAD-R, SOXS, and EKI1 in human testicular seminoma, with specific overexpression of DAD-R, correlates with reduced levels of apoptosis and earlier clinical manifestation. Cancer Res 2002;62:1822-31.
101. Chaganti RSK, Houldsworth J. The cytogenetic theory of the pathogenesis of human adult male germ cell tumours. APMIS 1998;106:80-4.