Glycolipids of germ cell tumors: Extended globo-series glycolipids are a hallmark of human embryonal carcinoma cells
Jonathan Wenk
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA
Search for more papers by this authorPeter W. Andrews
Department of Biomedical Science, The University of Sheffield, Western Bank, Sheffield, S10 2TN, UK
Search for more papers by this authorJochen Casper
Department of Hematology and Oncology, Medizinische Hochschule Hannover, Postfach 61 01 80, D-3000 Hannover 61, Germany
Search for more papers by this authorJun-Ichi Hata
Department of Pathology, Keio University School of Medicine, 35 Shinanomachi, Shtnjuku-ku Tokyo 160, Japan
Search for more papers by this authorMartin F. Pera
CRC Growth Factors, Department of Zoology, University of Oxford, South Parks Road, Oxford OX13PS, UK
Search for more papers by this authorAlexander von Keitz
Department of Urology, University of Marburg, Baldinger St., 35043 Marburg, Germany
Search for more papers by this authorIvan Damjanov
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA
Search for more papers by this authorCorresponding Author
Bruce A. Fenderson
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Rm. 233 Jefferson Hall, Philadelphia, PA 19107 USA. Fax: (215) 955-8703Search for more papers by this authorJonathan Wenk
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA
Search for more papers by this authorPeter W. Andrews
Department of Biomedical Science, The University of Sheffield, Western Bank, Sheffield, S10 2TN, UK
Search for more papers by this authorJochen Casper
Department of Hematology and Oncology, Medizinische Hochschule Hannover, Postfach 61 01 80, D-3000 Hannover 61, Germany
Search for more papers by this authorJun-Ichi Hata
Department of Pathology, Keio University School of Medicine, 35 Shinanomachi, Shtnjuku-ku Tokyo 160, Japan
Search for more papers by this authorMartin F. Pera
CRC Growth Factors, Department of Zoology, University of Oxford, South Parks Road, Oxford OX13PS, UK
Search for more papers by this authorAlexander von Keitz
Department of Urology, University of Marburg, Baldinger St., 35043 Marburg, Germany
Search for more papers by this authorIvan Damjanov
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA
Search for more papers by this authorCorresponding Author
Bruce A. Fenderson
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Philadelphia, PA 19107, USA
Department of Pathology and Cell Biology, Thomas Jefferson University, 1020 Locust Street, Rm. 233 Jefferson Hall, Philadelphia, PA 19107 USA. Fax: (215) 955-8703Search for more papers by this authorAbstract
Glycolipids of human germ cell tumor lines were analyzed co define the most common immunohistochemical profiles of embryonal carcinoma (EC), differentiated derivatives of EC, yolk sac carcinoma (YC) and choriocarcinoma (CC). Glycolipid composition was examined by high-performance thin-layer chromatography (HPTLC) combined with Immunostaining with a panel of anti-carbohydrate monoclonal antibodies (MAbs). All EC cell lines were found to contain high levels of globo-series glycolipids, including globotriosylceramide (Gb3), globoside (Gb4), Gb5 (Ga1β1 ± 1Gb4) and GL7 (sialyl Ga1β1 ± 3Gb4). Somatic differentiated derivatives (e.g., EC cells treated with retinoic acid) contained decreased levels of globo-series glycolipids and increased levels of lacto- and ganglio-series glycolipids, including GD3, GT3 and GD2. CC cell lines contained relatively large amounts of Gb3 but did not contain extended globo-series glycolipids GbS and GL7. CC cell lines also contained a macroglycolipid reactive with the antibody to SSEA-1 (Lex). Glycolipids were not detected in two YC cell lines, while other YC cell lines contained globo-series core glycolipids (Gb3 and Gb4) and gangliosides. We conclude that EC, YC and CC have distinct patterns of membrane glycolipid expression that can be identified by HPTLC and immunostaining. Our results indicate that globo-series glycolipids GbS and GL7, which carry stage-specific embryonic antigens 3 and 4 (SSEA-3 and SSEA-4), are a hallmark of human EC cells. Cell lines derived from human germ cell tumors that do not express Gb5 and GL7 deserve to be re-evaluated, since they may represent different stem cells, most likely equivalent to somatic cells and their developmentally committed precursors (e.g., neuroblasts). © 1994 Wiley-Liss, Inc.
References
- Andrews, P. W., Retinoic acid induces neuronal differentiation of a cloned human embryonal carcinoma cell line in vitro. Dev. Biol., 103, 285–293 (1984).
-
Andrews, P. W., and
Damjanov, I.,
Cell lines from human germ cell tumors.
In: R. J. Hay,
J.-G. Park and
A. Gazdar (eds.),
Atlas of Human Tumor Cell Lines,
pp. 443–476,
Academic Press, San Diego
(1994).
10.1016/B978-0-12-333530-2.50021-6 Google Scholar
- Andrews, P. W., Bronson, D. L., Benham, F., Strickland, S. and Knowles, B. B., A comparative study of eight cell lines derived from human teslicular teratocarcinoma. Int. J. Cancer, 26, 269–280 (1980).
- Andrews, P. W., Damjanov, I., Simon, D., Banting, G., Carun, C., Dracopoli, N. C. and Fogh, J., Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2: differentiation in vivo and in vitro. Lab. Invest., 50, 147–162 (1984).
- Andrews, P. W., Goodfellow, P. N. and Damjanov, I., Human teratocarcinoma cells in culture. Cancer Surv., 2, 41–73 (1983).
- Andrews, P. W., Nudelman, E., Hakomori, S. and Fenderson, B. A., Different patterns of glycolipid antigens are expressed following differentiation of TERA-2 human embryonal carcinoma cells induced by retinoic acid, hexamcthylene bisacetamide (HMBA) or bromodeoxyuridine (BUdR). Differentiation, 43, 131–138 (1990).
- Blaineau, C., Le Pendu, J., Arnaud, D., Connan, F. and Avner, P., The glycosidic antigen recognised by a novel monoclonal antibody, 75.12, is developmentally regulated on mouse embryonal carcinoma cells. EMBO J., 2, 2217–2222 (1983).
- Bronson, D. L., Andrews, P. W., Solter, D., Cervenka, J., Lange, P. H. and Fraley, E. E., A cell line derived from a metastasis of a human testicular germ-cell tumor. Cancer Res., 40, 2500–2506 (1980).
- Bronson, D. L., Andrews, P. W., Vessella, R. L. and Fraley, E. E., In vitro differentiation of human embryonal carcinoma cells. In: L. M. Silver, G. R. Martin and S. Strickland (eds.), Teratocarcinoma Stem Cells, Cold Spring Harbor Conferences on Cell Proliferation, 10, pp. 597–605, Cold Spring Harbor Press, New York (1983).
- Casper, J., Schmoll, H.-J., Schnaidt, U. and Fonatsch, C., Cell lines of human germinal cancer. Int. J. Androl., 10, 105–113 (1987).
- Chen, C., Fenderson, B. A., Andrews, P. W. and Hakomori, S., Glycolipid glycosyltransferases in human embryonal carcinoma cells during retinoic acid induced differentiation. Biochemistry, 28, 2229–2238 (1989).
- Damjanov, I., Pathobiology of human germ cell neoplasia. Recent Results Cancer Res., 123, 1–19 (1991).
- Damjanov, I., Fox, N., Knowles, B. B., Solter, D., Lange, P. H. and Fraley, E. E., Immunohistochemical localization of murine stage-specific embryonic antigen in human testicular germ cell tumors. Amer. J. Pathol., 108, 225–230 (1982).
- Damjanov, I., Horvat, B. and Gibas, Z., Retinoic acid-induced differentiation of the developmentally pluripotent human germ cell tumor-derived cell line, NCCIT. Lab. Invest., 68, 220–232 (1993).
- Fenderson, B. A. and Andrews, P. W., Carbohydrate antigens of embryonal carcinoma cells: changes upon differentiation. In: H. Clausen and E. Dabelsteen (eds.), Carbohydrate Pathology, Acta pathol. microbiol. immunol. Scand. 100, 109–118 (1992).
- Fenderson, B. A., Andrews, P. W., Nudelman, E., Clausen, H. and Hakomori, S., Giycolipid core structure switching from globo- to lacto- and ganglio-series during retinoic acid-induced differentiation of TERA-2-derived human embryonal carcinoma cells. Dev. Biol., 122, 21–34 (1987).
- Fenderson, B. A., Radin, N. and Andrews, P. W., Differentiation antigens of human germ cell tumors: distribution of carbohydrate epitopes on glycolipids and glycoproteins analyzed using PDMP, an inhibitor of glycolipid synthesis. Europ. Urol., 23, 30–37 (1993).
-
Fogh, J. and
Trempe, G.,
New human tumor cell lines.
In: J. Fogh (ed.),
Human Tumor Cells in Vitro,
pp. 115–159,
Plenum, New York
(1975).
10.1007/978-1-4757-1647-4_5 Google Scholar
- Fox, N. W., Damjanov, I., Knowles, B. B. and Solter, D., Stage-specific embryonic antigen 3 as a marker of visceral extraembryonic endoderm. Dev. Biol., 103, 263–266 (1984).
- Fukuda, N. M., Bothner, B., Lloyd, K. O., Rettig, W. J., Tiller, P. R. and Dell, A., Structures of glycosphingolipids isolated from human embryonal carcinoma cells. The presence of mono- and disialosyl glycolipids with blood group type 1 sequence. J. boil. Chem., 261, 5145–5153 (1986).
- Giovanella, B. C., Stehlin, J. S. and Williams, L. J., Heterotransplantation of human malignant tumors in “nude” thymusless mice. II. Malignant tumors induced by injection of cell cultures derived from human solid tumors. J. nat. Cancer Inst., 52, 921–930 (1974).
- Grossman, H. B. and Wedemeyer, G., Um-TC-1, a new human testicular carcinoma cell line. Cancer J., 1, 22–24 (1986).
- Hata, J., Fujumoto, J., Ishii, E., Kokai, Y., Matsubayashi, Y., Abe, H., Kusakari, S., Yamada, T., Umezawa, A., Kikuchi, H. and Maruyama, T., Differentiation of human germ cell tumor cells in vivo and vitro. Acta Histochem. Cytochem., 25, 563–576 (1992).
- Hiraoka, A., Vogelzang, N. J., Rosner, M. C. and Golomb, H. M., Ultrastructure of four human germ cell tumor-derived cell lines: effect of 12-O-tetradccanoylphorbol-13-acctatc. Cancer Invest., 6, 393–402 (1988).
- Hogan, B., Fellous, M., Avner, P. and Jacob, F., Isolation of a human teratoma cell line which expresses F9 antigen. Nature (Lond.), 270, 515–518 (1977).
- IUPAC-IUB, Commission on Biochemical Nomenclature. Biochem. J., 171, 21–35 (1978).
- Kannagi, R., Cochran, N. A., Ishigami, F., Hakomori, S., Andrews, P. W., Knowles, B. B. and Solter, D., Stage-specific embryonic antigens (SSEA-3 and -4) are epitopes of a unique globo-series ganglioside isolated from human teratocarcinoma cells. EMBO J., 2, 2355–2361 (1983a).
- Kannagi, R., Levery, S. B., Ishigami, F., Hakomori, S., Shevinski, L. H., Knowles, B. B. and Solter, D., New globoseries glycosphingolipids in human teratocarcinoma reactive with the monoclonal antibody directed to a developmentally regulated antigen, stage-specific embryonic antigen 3. J. biol. Chem., 258, 8934–8942 (1983b).
- Ohyama, C., Fukushi, Y., Satoh, M., Saitoh, S., Orikasa, S., Nudelman, E., Stroud, M. and Hakomori, S., Changes in glycolipid expression in human testicular tumor. Int. J. Cancer, 45, 1040–1044 (1990).
- Oosterhuis, J. W., Dejong, B., van Dalen, I., van der Meer, I., Visser, M., de Leu, L., Mesander, G., Collard, J. G., Schrafford Koops, H. and Sleijfer, D. M., Identical chromosome translocations involving the region of the c-myb oncogene in four metastases of a mediastinal teratocarcinoma. Cancer Genet. Cylogenet., 15, 99–107 (1985).
- Pattillo, R. A. and Gey, C. O., The establishment of a cell line of human hormone-synthesizing trophoblastic cells in vitro. Cancer Res., 28, 1231–1236 (1968).
- Pattillo, R. A., Ruckert, A., Hussa, R., Bernstein, R. and Delis, E., The Jar cell line, Continuous human multihormone production and controls. In Vitro, 6, 398–399 (1971).
- Pera, M. F., Blasco-Lafita, M. J. and Mills, J., Cultured stem-cells from human testicular teratomas: the nature of human embryonal carcinoma, and its comparison with two types of yolk-sac carcinoma. Int. J. Cancer, 40, 334–343 (1987).
- Pera, M. F., Cooper, S., Mills, J. and Parrington, J. M., Isolation and characterization of a multipotent clone of human embryonal carcinoma cells. Differentiation, 42, 10–23 (1989).
- Shevinsky, L. H., Knowles, B. B., Damjanov, I. and Solter, D., Monoclonal antibody to murine embryos defines a stage-specific embryonic antigen on mouse embryos and human teratocarcinoma cells. Cell, 30, 697–705 (1982).
- Tainsky, M. A., Cooper, C. S., Giovanella, B. C. and van de Woude, G. F., An activated rasN gene: detected in late but not early passage human PA-1 teratocarcinoma cells. Science, 225, 643–645 (1984).
- Tainsky, M. A., Krizman, D. B., Chiao, P. J., Yin, S. O. and Giovanella, B. C., PA-1, a human cell model for multistage carcinogenesis: oncogenes and other factors. Anticancer Res., 8, 899–914 (1988).
- Teshima, S., Shimosato, Y., Hirohashi, S., Tome, Y., Hayashi, I., Kanazawa, H. and Kakizoe, T., Four new human germ cell tumor cell lines. Lab. Invest., 59, 328–336 (1988).
- Tippett, P., Andrews, P. W., Knowles, B. B., Solter, D. and Good-fellow, P. N., Red cell antigens P (globoside) and Luke: identification by monoclonal antibodies defining the murine stage-specific embryonic antigens -3 and -4 (SSEA-3 and -A). Vox Sang., 51, 53–56 (1986).
- Vogelzang, N., Andrews, P. W. and Bronson, D., An extragonadal human embryonal carcinoma cell line 1618K. Proc. Amer. Assoc. Cancer Res., 24, 3 (1983).
-
Vogelzang, N. J.,
Bronson, D. L.,
Savino, D.,
Vessella, R. L. and
Fraley, E. E.,
A human embryonal-yolk sac carcinoma model system in athymic mice.
Cancer,
55,
2584–2593
(1985).
10.1002/1097-0142(19850601)55:11<2584::AID-CNCR2820551110>3.0.CO;2-B CAS PubMed Web of Science® Google Scholar
- von Keitz, A. T., Riedmiller, H., Neumann, K., Gutschank, W. and Fonatsch, C., Establishment and characterization of a seminoma cell-line (S2). Invest. Urol., (1994) (In press).
- Wang, R., Perkins, K. L., Bronson, D. L. and Fraley, E. E., Cytogenetic evidence for pre-meiotic transformation of human testicular cancers. Cancer Res., 41, 2135–2140 (1981).
- Wang, N., Trend, B., Bronson, D. L. and Fraley, E. E., Nonrandom abnormalities in chromosome 1 in human testicular cancers. Cancer Res., 40, 796–802 (1980).
- Zeuthen, J., Norgaard, J. O. R., Avner, P., Fellous, M., Wartiovaara, J., Vaheri, A., Rosen, A. and Giovanella, B. C., Characterization of a human ovarian teratocarcinoma-derived cell Inn. Int. J. Cancer, 25, 19–32 (1980).
Citing Literature
