SALL4 is a novel diagnostic marker for testicular germ cell tumors

American Journal of Surgical Pathology

Volumn 33, Issue 7, 2009, Pages 1065-1077

  Cao, Dengfeng ^a   Li, Jianping ^a   Guo, Charles C ^b   Allan, Robert W ^c   Humphrey, Peter A ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c UNIVERSITY OF FLORIDA   (United States)

Author keywords

Diagnostic marker; Germ cell tumor; SALL4; Testis; Yolk sac tumor

Indexed keywords

ALPHA FETOPROTEIN; GLYPICAN 3; OCTAMER TRANSCRIPTION FACTOR 4; SALL4 PROTEIN; TUMOR MARKER; UNCLASSIFIED DRUG;

ARTICLE; CHORIOCARCINOMA; EMBRYONAL CARCINOMA; GERM CELL TUMOR; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; SEMINOMA; SPERMATOCYTE; SPERMATOGONIUM; STATISTICAL ANALYSIS; TERATOMA; TROPHOBLAST; YOLK SAC TUMOR;

ADOLESCENT; CHILD; CHILD, PRESCHOOL; HUMANS; IMMUNOHISTOCHEMISTRY; INFANT; MALE; NEOPLASMS, GERM CELL AND EMBRYONAL; SENSITIVITY AND SPECIFICITY; TESTICULAR NEOPLASMS; TRANSCRIPTION FACTORS; TUMOR MARKERS, BIOLOGICAL; YOUNG ADULT;

EID: 67649562737     PISSN: 01475185     EISSN: 15320979     Source Type: Journal    
DOI: 10.1097/PAS.0b013e3181a13eef     Document Type: Article

References (57)

1. Alstrump K, Hoei-Hansen CE, Wieknrt U, et al. Embryonic stem cell-like features of testicular carcinoma in situ revealed by genomewide gene expression profiling. Cancer Res. 2004;64:4736-4743.
2. Alstrump K, Sonne SB, Hoei-Hansen CE, et al. From embryonic stem cells to testicular germ cell cancer-should we be concerned? Int J Androl. 2006;29:211-218.
3. Bahrami A, Ro JY, Ayala AG. An overview of testicular GCTs. Arch Pathol Lab Med. 2007;131:1267-1280.
4. Berney DM, Shamash J, Pieroni K, et al. Loss of CD30 expression in metastatic embryonal carcinoma: the effects of chemotherapy? Histopathology. 2001;39:382-385.
5. Burke AP, Mostofi FK. Placental alkaline phosphatase immunohistochemistry of intratubular malignant germ cells and associated testicular GCTs. Hum Pathol. 1988;19:663-670.
6. Cao D, Humphrey PA, Allan RW. SALL4 is a novel sensitive and specific marker of metastatic germ cell tumors, with particular utility in detection of metastatic yolk sac tumor. Cancer. In press.
7. Cui W, Kong NR, Ma Y, et al. Differential expression of the novel oncogene, SALL4, in lymphoma, plasma cell myeloma, and acute lymphoblastic leukemia. Mod Pathol. 2006;19:1585-1592.
8. de Jong J, Stoop H, Gills AJ, et al. Differential expression of SOX17 and SOX2 in germ cells and stem cells has biological and clinical implications. J Pathol. 2008;215:21-30.
9. Eble JN, Sauter G, Epstein JI, et al, World Health Organization Classification of Tumors. Pathology and Genetics of Tumors of the Urinary Tract and Male Genital Organs. Lyon, France: IARC Press; 2004;218-278.
10. Eglen DE, Ulbright TM. The differential diagnosis of yolk sac tumor and seminoma. Usefulness of cytokeratin, alpha-fetoprotein, and alpha-1-antitrypsin immunoperoxidase reactions. Am J Clin Pathol. 1987;88:328-332.
11. Einhorn L. Chemotherapeutic and surgical strategies for GCTs. Chest Surg Clin N Am. 2002;12:695-706.
12. Hamilton-Dutoit SJ, Lou H, Pallesen G. The expression of placental alkaline phosphatase (PLAP) and PLAP-like enzymes in normal and neoplastic human tissues. An immunohistological survey using monoclonal antibodies. APMIS. 1990;98:797-811.
13. Hart AH, Hartley L, Parker K, et al. The pluripotency homeobox gene NANOG is expressed in human GCTs. Cancer. 2005; 104:2092-2098.
14. Iczkowski KA, Butler SL, Shanks JH, et al. Trials of new germ cell immunohistochemical stains in 93 extragonadal and metastatic GCTs. Hum Pathol. 2008;39:275-281.
15. Jacobsen GK, Nørgaard-Pedersen B. Placental alkaline phosphatase in testicular germ cell tumours and in carcinoma-in-situ of the testis. An immunohistochemical study. Acta Pathol Microbiol Immunol Scand (A). 1984;92:323-329.
16. Jones TD, Ulbright TM, Eble JN, et al. OCT4 staining in testicular tumors: a sensitive and specific marker for seminoma and embryonal carcinoma. Am J Surg Pathol. 2004;28:935-940.
17. Jü rgens G. Head and tail development of the Drosophila embryo involves spalt, a novel homeotic gene. EMBO J. 1988;7:189-196.
18. Kohlhase J, Heinrich M, Schubert L, et al. Okihiro syndrome is caused by SALL4 mutations. Hum Mol Genet. 2002;11:2979-2987.
19. Koide O, Iwai S, Baba K, et al. Identification of testicular atypical germ cells by an immunohistochemical technique for placental alkaline phosphatase. Cancer. 1987;60:1325-1330.
20. Leroy X, Augusto D, Leteurtre E, et al. CD30 and CD117 (c-kit) used in combination are useful for distinguishing embryonal carcinoma from seminoma. J Histochem Cytochem. 2002; 50:283-285.
21. Li SS, Liu YH, Tseng CN, et al. Characterization and gene expression profiling of five new human embryonic stem cell lines derived in Taiwan. Stem Cells Dev. 2006;15:532-555.
22. Lim CY, Tam WL, Zhang J, et al. Sall4 regulates distinct transcription circuitries in different blastocyst-derived stem cell lineages. Cell Stem Cell. 2008;3:543-554.
23. Loh YH, Wu Q, Chew JL et al. The Oct4 and Nanog transcription network regulates pluripotency in mouse embryonic stem cells. Nat Genet. 2006;38:431-440.
24. Looijenga LH, Oosterhuis JW. Pathogenesis of testicular germ cell tumours. Rev Reprod. 1999;4:90-100.
25. Looijenga LH, Hersmus R, Gillis AJ, et al. Genomic and expression profiling of human spermatocytic seminomas: primary spermatocyte as tumorigenic precursor and DMRT1 as candidate chromosome 9 gene. Cancer Res. 2006;66:290-302.
26. Morinaga S, Ojima M, Sasano N. Human chorionic gonadotropin and alpha-fetoprotein in testicular GCTs. An immunohistochemical study in comparison with tissue concentrations. Cancer. 1983; 52:1281-1289.
27. Mostofi FK. Histological change ostensibly induced by therapy in the metastasis of GCTs of testis. Prog Clin Biol Res. 1985;203:47-60.
28. Mostofi FK, Sesterhenn IA, Davis CJ Jr. Immunopathology of GCTs of the testis. Semin Diagn Pathol. 1987;4:320-341.
29. Niehans GA, Manivel JC, Copland GT, et al. Immunohistochemistry of germ cell and trophoblastic neoplasms. Cancer. 1988;62: 1113-1123.
30. Nistal M, Codesal J, Paniagua R, et al. Decrease in the number of human Ap and Ad spermatogonia and in the Ap/Ad ratio with advancing age. New data on the spermatogonial stem cell. J Androl. 1987;8:64-68.
31. Ota S, Hishinuma M, Yamauchi N, et al. Oncofetal protein glypican-3 in testicular germ-cell tumor. Virchows Arch. 2006; 449:308-314.
32. Paniagua R, Nistal M, Amat P, et al. Quantitative differences between variants of a spermatogonia in man. J Reprod Fertil. 1986;77:669-673.
33. Paniagua R, Codesal J, Nistal M, et al. Quantification of cell types throughout the cycle of the human seminiferous epithelium and their DNA content. A new approach to the spermatogonial stem cell in man. Anat Embryol. 1987;176:225-230.
34. Polski JM, Janney CG. Ber-H2 (CD30) immunohistochemical staining in malignant melanoma. Mod Pathol. 1999;12:903-906.
35. Rajpert-De Meyts E. Developmental model for the pathogenesis of testicular carcinoma in situ: genetic and environmental aspects. Hum Reprod Update. 2006;12:303-323.
36. Rajpert-De Meyts E. Recent advances and future directions in research on testicular germ cell cancer. Int J Androl. 2007; 30:192-197.
37. Rajpert-De Meyts E, Hanstein R, Jørgensen N, et al. Developmental expression of POU5F1 (OCT-3/4) in normal and dysgenetic human gonads. Hum Reprod. 2004;19:1338-1344.
38. Reuter D, Schuh R, Jä ckle H. The homeotic gene spalt (sal) evolved during Drosophila speciation. Proc Natl Acad Sci USA. 1989;86: 5483-5486.
39. Sakaki-Yumoto M, Kobayashi C, Sato A, et al. The murine homolog of SALL4, a causative gene in Okihiro syndrome, is essential for embryonic stem cell proliferation, and cooperates with Sall1 in anorectal, heart, brain and kidney development. Development. 2006;133:3005-3013.
40. Santagata S, Ligon KL, Hornick JL. Embryonic stem cell transcription factor signatures in the diagnosis of primary and metastatic GCTs. Am J Surg Pathol. 2007;31:836-845.
41. Schneider DT, Schuster AE, Fritsch MK, et al. Multipoint imprinting analysis indicates a common precursor cell for gonadal and nongonadal pediatric germ cell tumors. Cancer Res. 2001; 61:7268-7276.
42. Skakkebaek NE, Berthelsen JG, Giwercman A, et al. Carcinoma-insitu 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.
43. Stoop H, van Gurp R, de Krijger R, et al. Reactivity of germ cell maturation stage-specific markers in spermatocytic seminoma: diagnostic and etiological implications. Lab Invest. 2001;81:919-928.
44. Talerman A. Germ cell tumours. Ann Pathol. 1985;5:145-157.
45. Teilum G. Endodermal sinus tumors of the ovary and testis. Comparative morphogenesis of the so-called mesoephroma ovarii (Schiller) and extraembryonic (yolk sac-allantoic) structures of the rat's placenta. Cancer. 1959;12:1092-1105.
46. Tickoo SK, Hutchinson B, Bacik J, et al. Testicular seminoma: a clinicopathologic and immunohistochemical study of 105 cases with special reference to seminomas with atypical features. Int J Surg Pathol. 2002;10:23-32.
47. Ulbright TM. GCTs of the gonads: a selective review emphasizing problems in differential diagnosis, newly appreciated, and controversial issues. Mod Pathol. 2005;18(suppl 2):S61-S79.
48. Ulbright TM, Young RH. Seminoma with tubular, microcystic, and related patterns: a study of 28 cases of unusual morphologic variants that often cause confusion with yolk sac tumor. Am J Surg Pathol. 2005;29:500-505.
49. Wang J, Rao S, Chu J et al. A protein interaction network for pluripotency of embryonic stem cells. Nature. 2006;444:364-368.
50. Warren M, Wang W, Spiden S, et al. A Sall4 mutant mouse model useful for studying the role of Sall4 in early embryonic development and organogenesis. Genesis. 2007;45:51-58.
51. Wick MR, Swanson PE, Manivel JC. Placental-like alkaline phosphatase reactivity in human tumors: an immunohistochemical study of 520 cases. Hum Pathol. 1987;18:946-954.
52. Wong CC, Gaspar-Maia A, Ramalho-Santos M, et al. Highefficiency stem cell fusion-mediated assay reveals Sall4 as an enhancer of reprogramming. PLoS ONE. 2008;3:e1955.
53. Wu Q, Chen X, Zhang J, et al. Sall4 interacts with Nanog and cooccupies Nanog genomic sites in embryonic stem cells. J Biol Chem. 2006;281:24090-24094.
54. Yang J, Chai L, Gao C, et al. SALL4 is a key regulator of survival and apoptosis in human leukemic cells. Blood. 2008;112:805-813.
55. Zhang J, Tam WL, Tong GQ, et al. Sall4 modulates embryonic stem cell pluripotency and early embryonic development by the transcriptional regulation of Pou5f1. Nat Cell Biol. 2006;8:1114-1123.
56. Zhou Q, Chipperfield H, Melton DA, et al. A gene regulatory network in mouse embryonic stem cells. Proc Natl Acad Sci USA. 2007;104:16438-16443.
57. Zynger DL, Dimov ND, Luan C, et al. Glypican 3: a novel marker in testicular germ cell tumors. Am J Surg Pathol. 2006;30:1570-1575.