Molecular detection of tumor-associated antigens shared by human cutaneous melanomas and gliomas (original) (raw)

. 1997 Jun;150(6):2143–2152.

Abstract

Both melanocytes and glial cells are derived embryologically from the neural ectoderm. Their malignant transformed counterparts, melanoma and glioma cells, respectively, may share common antigens. Numerous tumor-associated antigens have been identified in melanomas but only a few a gliomas. Using an established reverse transcriptase polymerase chain reaction plus Southern blot assay, we compared the mRNA expression of melanoma-associated antigens (MAAs) of melanomas to brain tumors primarily derived from glial cells. The MAAs studied included tyrosinase (Tyr), tyrosinase-related protein-1 and -2 (TRP-1 and TRP-2), gp100, human melanoma antigen-encoding genes 1 and 3 (MAGE-1 and MAGE-3), and melanotransferrin (p97). Glioblastoma multiforme (n = 21), anaplastic astrocytoma (n = 3), ependymoma (n = 2), meningioma (n = 3), oligodendroglioma (n = 1), and melanoma (n = 12) tumor specimens were assayed for MAA mRNA expression. Glioblastoma multiforme, astrocytoma, and melanoma cell lines were also assayed. We observed that individual MAA mRNAs were expressed in these brain tumors and cell lines at varying frequencies. The melanogenesis-pathway-related MAAs Tyr, TRP-1, TRP-2, and gp100 mRNAs were also expressed at different levels in normal brain tissues but at a much lower frequency than in glioblastoma multiforme and melanoma. MAGE-1 and MAGE-3 mRNA were expressed in different types of tumor specimens and cell lines but never in normal brain tissue. Tumor antigen p97 was expressed in all types of tumors and also in normal brain tissues. These studies demonstrate that melanomas and primary brain tumors express common MAAs and could be exploited in patients with malignant glioma by active specific immunotherapy against these common MAAs.

2143

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anker L., Ohgaki H., Ludeke B. I., Herrmann H. D., Kleihues P., Westphal M. p53 protein accumulation and gene mutations in human glioma cell lines. Int J Cancer. 1993 Dec 2;55(6):982–987. doi: 10.1002/ijc.2910550618. [DOI] [PubMed] [Google Scholar]
  2. Azizi E., Friedman J., Pavlotsky F., Iscovich J., Bornstein A., Shafir R., Trau H., Brenner H., Nass D. Familial cutaneous malignant melanoma and tumors of the nervous system. A hereditary cancer syndrome. Cancer. 1995 Nov 1;76(9):1571–1578. doi: 10.1002/1097-0142(19951101)76:9<1571::aid-cncr2820760912>3.0.co;2-6. [DOI] [PubMed] [Google Scholar]
  3. Barth A., Hoon D. S., Foshag L. J., Nizze J. A., Famatiga E., Okun E., Morton D. L. Polyvalent melanoma cell vaccine induces delayed-type hypersensitivity and in vitro cellular immune response. Cancer Res. 1994 Jul 1;54(13):3342–3345. [PubMed] [Google Scholar]
  4. Brown J. P., Woodbury R. G., Hart C. E., Hellström I., Hellström K. E. Quantitative analysis of melanoma-associated antigen p97 in normal and neoplastic tissues. Proc Natl Acad Sci U S A. 1981 Jan;78(1):539–543. doi: 10.1073/pnas.78.1.539. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cowen D. The melanoneurons of the human cerebellum (nucleus pigmentosus cerebellaris) and homologues in the monkey. J Neuropathol Exp Neurol. 1986 May;45(3):205–221. [PubMed] [Google Scholar]
  6. Datta Y. H., Adams P. T., Drobyski W. R., Ethier S. P., Terry V. H., Roth M. S. Sensitive detection of occult breast cancer by the reverse-transcriptase polymerase chain reaction. J Clin Oncol. 1994 Mar;12(3):475–482. doi: 10.1200/JCO.1994.12.3.475. [DOI] [PubMed] [Google Scholar]
  7. Doi F., Chi D. D., Charuworn B. B., Conrad A. J., Russell J., Morton D. L., Hoon D. S. Detection of beta-human chorionic gonadotropin mRNA as a marker for cutaneous malignant melanoma. Int J Cancer. 1996 Feb 8;65(4):454–459. doi: 10.1002/(SICI)1097-0215(19960208)65:4<454::AID-IJC11>3.0.CO;2-A. [DOI] [PubMed] [Google Scholar]
  8. Gaugler B., Van den Eynde B., van der Bruggen P., Romero P., Gaforio J. J., De Plaen E., Lethé B., Brasseur F., Boon T. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J Exp Med. 1994 Mar 1;179(3):921–930. doi: 10.1084/jem.179.3.921. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Haninec P., Vachtenheim J. Tyrosinase protein is expressed also in some neural crest derived cells which are not melanocytes. Pigment Cell Res. 1988;1(5):340–343. doi: 10.1111/j.1600-0749.1988.tb00129.x. [DOI] [PubMed] [Google Scholar]
  10. Hoon D. S., Ando I., Sviland G., Tsuchida T., Okun E., Morton D. L., Irie R. F. Ganglioside GM2 expression on human melanoma cells correlates with sensitivity to lymphokine-activated killer cells. Int J Cancer. 1989 May 15;43(5):857–862. doi: 10.1002/ijc.2910430520. [DOI] [PubMed] [Google Scholar]
  11. Hoon D. S., Sarantou T., Doi F., Chi D. D., Kuo C., Conrad A. J., Schmid P., Turner R., Guiliano A. Detection of metastatic breast cancer by beta-hCG polymerase chain reaction. Int J Cancer. 1996 Oct 21;69(5):369–374. doi: 10.1002/(SICI)1097-0215(19961021)69:5<369::AID-IJC3>3.0.CO;2-3. [DOI] [PubMed] [Google Scholar]
  12. Hoon D. S., Wang Y., Dale P. S., Conrad A. J., Schmid P., Garrison D., Kuo C., Foshag L. J., Nizze A. J., Morton D. L. Detection of occult melanoma cells in blood with a multiple-marker polymerase chain reaction assay. J Clin Oncol. 1995 Aug;13(8):2109–2116. doi: 10.1200/JCO.1995.13.8.2109. [DOI] [PubMed] [Google Scholar]
  13. Hoon D. S., Yuzuki D., Hayashida M., Morton D. L. Melanoma patients immunized with melanoma cell vaccine induce antibody responses to recombinant MAGE-1 antigen. J Immunol. 1995 Jan 15;154(2):730–737. [PubMed] [Google Scholar]
  14. Jackson I. J., Chambers D. M., Tsukamoto K., Copeland N. G., Gilbert D. J., Jenkins N. A., Hearing V. A second tyrosinase-related protein, TRP-2, maps to and is mutated at the mouse slaty locus. EMBO J. 1992 Feb;11(2):527–535. doi: 10.1002/j.1460-2075.1992.tb05083.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kwon B. S., Chintamaneni C., Kozak C. A., Copeland N. G., Gilbert D. J., Jenkins N., Barton D., Francke U., Kobayashi Y., Kim K. K. A melanocyte-specific gene, Pmel 17, maps near the silver coat color locus on mouse chromosome 10 and is in a syntenic region on human chromosome 12. Proc Natl Acad Sci U S A. 1991 Oct 15;88(20):9228–9232. doi: 10.1073/pnas.88.20.9228. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kwon B. S., Haq A. K., Pomerantz S. H., Halaban R. Isolation and sequence of a cDNA clone for human tyrosinase that maps at the mouse c-albino locus. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7473–7477. doi: 10.1073/pnas.84.21.7473. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kwon B. S. Pigmentation genes: the tyrosinase gene family and the pmel 17 gene family. J Invest Dermatol. 1993 Feb;100(2 Suppl):134S–140S. doi: 10.1111/1523-1747.ep12465022. [DOI] [PubMed] [Google Scholar]
  18. Lallier T. E. Cell lineage and cell migration in the neural crest. Ann N Y Acad Sci. 1991;615:158–171. doi: 10.1111/j.1749-6632.1991.tb37758.x. [DOI] [PubMed] [Google Scholar]
  19. Lampson L. A., Hickey W. F. Monoclonal antibody analysis of MHC expression in human brain biopsies: tissue ranging from "histologically normal" to that showing different levels of glial tumor involvement. J Immunol. 1986 Jun 1;136(11):4054–4062. [PubMed] [Google Scholar]
  20. Madajewicz S., Karakousis C., West C. R., Caracandas J., Avellanosa A. M. Malignant melanoma brain metastases. Review of Roswell Park Memorial Institute experience. Cancer. 1984 Jun 1;53(11):2550–2552. doi: 10.1002/1097-0142(19840601)53:11<2550::aid-cncr2820531129>3.0.co;2-b. [DOI] [PubMed] [Google Scholar]
  21. Maeurer M. J., Storkus W. J., Kirkwood J. M., Lotze M. T. New treatment options for patients with melanoma: review of melanoma-derived T-cell epitope-based peptide vaccines. Melanoma Res. 1996 Feb;6(1):11–24. doi: 10.1097/00008390-199602000-00003. [DOI] [PubMed] [Google Scholar]
  22. McCloskey J. J., Parker J. C., Jr, Brooks W. H., Blacker H. M. Melanin as a component of cerebral gliomas: the melanotic cerebral ependymoma. Cancer. 1976 May;37(5):2373–2379. doi: 10.1002/1097-0142(197605)37:5<2373::aid-cncr2820370529>3.0.co;2-2. [DOI] [PubMed] [Google Scholar]
  23. Mitchell M. S., Harel W., Kan-Mitchell J., LeMay L. G., Goedegebuure P., Huang X. Q., Hofman F., Groshen S. Active specific immunotherapy of melanoma with allogeneic cell lysates. Rationale, results, and possible mechanisms of action. Ann N Y Acad Sci. 1993 Aug 12;690:153–166. doi: 10.1111/j.1749-6632.1993.tb44005.x. [DOI] [PubMed] [Google Scholar]
  24. Morton D. L., Foshag L. J., Hoon D. S., Nizze J. A., Famatiga E., Wanek L. A., Chang C., Davtyan D. G., Gupta R. K., Elashoff R. Prolongation of survival in metastatic melanoma after active specific immunotherapy with a new polyvalent melanoma vaccine. Ann Surg. 1992 Oct;216(4):463–482. doi: 10.1097/00000658-199210000-00010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Natali P. G., Bigotti A., Nicotra M. R., Viora M., Manfredi D., Ferrone S. Distribution of human Class I (HLA-A,B,C) histocompatibility antigens in normal and malignant tissues of nonlymphoid origin. Cancer Res. 1984 Oct;44(10):4679–4687. [PubMed] [Google Scholar]
  26. Nordlund J. J., Abdel-Malek Z. A., Boissy R. E., Rheins L. A. Pigment cell biology: an historical review. J Invest Dermatol. 1989 Apr;92(4 Suppl):53S–60S. doi: 10.1111/1523-1747.ep13074988. [DOI] [PubMed] [Google Scholar]
  27. Rabey J. M., Hefti F. Neuromelanin synthesis in rat and human substantia nigra. J Neural Transm Park Dis Dement Sect. 1990;2(1):1–14. doi: 10.1007/BF02251241. [DOI] [PubMed] [Google Scholar]
  28. Rimoldi D., Romero P., Carrel S. The human melanoma antigen-encoding gene, MAGE-1, is expressed by other tumour cells of neuroectodermal origin such as glioblastomas and neuroblastomas. Int J Cancer. 1993 May 28;54(3):527–528. doi: 10.1002/ijc.2910540329. [DOI] [PubMed] [Google Scholar]
  29. Ritland S. R., Ganju V., Jenkins R. B. Region-specific loss of heterozygosity on chromosome 19 is related to the morphologic type of human glioma. Genes Chromosomes Cancer. 1995 Apr;12(4):277–282. doi: 10.1002/gcc.2870120407. [DOI] [PubMed] [Google Scholar]
  30. Russo V., Traversari C., Verrecchia A., Mottolese M., Natali P. G., Bordignon C. Expression of the MAGE gene family in primary and metastatic human breast cancer: implications for tumor antigen-specific immunotherapy. Int J Cancer. 1995 Jun 22;64(3):216–221. doi: 10.1002/ijc.2910640313. [DOI] [PubMed] [Google Scholar]
  31. Sawamura Y., De Tribolet N. Immunotherapy of brain tumors. J Neurosurg Sci. 1990 Jul-Dec;34(3-4):265–278. [PubMed] [Google Scholar]
  32. Seeger R. C., Rosenblatt H. M., Imai K., Ferrone S. Common antigenic determinants on human melanoma, glioma, neuroblastoma, and sarcoma cells defined with monoclonal antibodies. Cancer Res. 1981 Jul;41(7):2714–2717. [PubMed] [Google Scholar]
  33. Soffer D., Lach B., Constantini S. Melanotic cerebral ganglioglioma: evidence for melanogenesis in neoplastic astrocytes. Acta Neuropathol. 1992;83(3):315–323. doi: 10.1007/BF00296795. [DOI] [PubMed] [Google Scholar]
  34. Song Y. H., Connor E., Li Y., Zorovich B., Balducci P., Maclaren N. The role of tyrosinase in autoimmune vitiligo. Lancet. 1994 Oct 15;344(8929):1049–1052. doi: 10.1016/s0140-6736(94)91709-4. [DOI] [PubMed] [Google Scholar]
  35. Spagnoli G. C., Schaefer C., Willimann T. E., Kocher T., Amoroso A., Juretic A., Zuber M., Luscher U., Harder F., Heberer M. Peptide-specific CTL in tumor infiltrating lymphocytes from metastatic melanomas expressing MART-1/Melan-A, gp100 and Tyrosinase genes: a study in an unselected group of HLA-A2.1-positive patients. Int J Cancer. 1995 Oct 20;64(5):309–315. doi: 10.1002/ijc.2910640505. [DOI] [PubMed] [Google Scholar]
  36. Tsuzuki T., Tsunoda S., Sakaki T., Konishi N., Hiasa Y., Nakamura M. Alterations of retinoblastoma, p53, p16(CDKN2), and p15 genes in human astrocytomas. Cancer. 1996 Jul 15;78(2):287–293. doi: 10.1002/(SICI)1097-0142(19960715)78:2<287::AID-CNCR15>3.0.CO;2-S. [DOI] [PubMed] [Google Scholar]
  37. Vijayasaradhi S., Bouchard B., Houghton A. N. The melanoma antigen gp75 is the human homologue of the mouse b (brown) locus gene product. J Exp Med. 1990 Apr 1;171(4):1375–1380. doi: 10.1084/jem.171.4.1375. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Weynants P., Lethé B., Brasseur F., Marchand M., Boon T. Expression of mage genes by non-small-cell lung carcinomas. Int J Cancer. 1994 Mar 15;56(6):826–829. doi: 10.1002/ijc.2910560612. [DOI] [PubMed] [Google Scholar]
  39. Wikstrand C. J., Bigner D. D. Expression of human fetal brain antigens by human tumors of neuroectodermal origin as defined by monoclonal antibodies. Cancer Res. 1982 Jan;42(1):267–275. [PubMed] [Google Scholar]
  40. Woodbury R. G., Brown J. P., Yeh M. Y., Hellström I., Hellström K. E. Identification of a cell surface protein, p97, in human melanomas and certain other neoplasms. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2183–2187. doi: 10.1073/pnas.77.4.2183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. del Marmol V., Beermann F. Tyrosinase and related proteins in mammalian pigmentation. FEBS Lett. 1996 Mar 4;381(3):165–168. doi: 10.1016/0014-5793(96)00109-3. [DOI] [PubMed] [Google Scholar]
  42. van der Bruggen P., Traversari C., Chomez P., Lurquin C., De Plaen E., Van den Eynde B., Knuth A., Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 1991 Dec 13;254(5038):1643–1647. doi: 10.1126/science.1840703. [DOI] [PubMed] [Google Scholar]