Skip to main content
Top
Published in: Cancer Immunology, Immunotherapy 10/2009

01-10-2009 | Original Article

Cancer/testis antigens can be immunological targets in clonogenic CD133+ melanoma cells

Authors: Craig Gedye, Juliet Quirk, Judy Browning, Suzanne Svobodová, Thomas John, Pavel Sluka, P. Rod Dunbar, Denis Corbeil, Jonathan Cebon, Ian D. Davis

Published in: Cancer Immunology, Immunotherapy | Issue 10/2009

Login to get access

Abstract

“Cancer stem cells” that resist conventional treatments may be a cause of therapeutic failure in melanoma. We report a subpopulation of clonogenic melanoma cells that are characterized by high prominin-1/CD133 expression in melanoma and melanoma cell lines. These cells have enhanced clonogenicity and self-renewal in vitro, and serve as a limited in vitro model for melanoma stem cells. In some cases clonogenic CD133+ melanoma cells show increased expression of some cancer/testis (CT) antigens. The expression of NY-ESO-1 in an HLA-A2 expressing cell line allowed CD133+ clonogenic melanoma cells to be targeted for killing in vitro by NY-ESO-1-specific CD8+ T-lymphocytes. Our in vitro findings raise the hypothesis that if melanoma stem cells express CT antigens in vivo that immune targeting of these antigens may be a viable clinical strategy for the adjuvant treatment of melanoma.
Appendix
Available only for authorised users
Literature
1.
go back to reference Thompson JF, Scolyer RA, Kefford RF (2005) Cutaneous melanoma. Lancet 365:687–701PubMed Thompson JF, Scolyer RA, Kefford RF (2005) Cutaneous melanoma. Lancet 365:687–701PubMed
2.
go back to reference Phan GQ, Yang JC, Sherry RM et al (2003) Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci USA 100:8372–8377PubMedCrossRef Phan GQ, Yang JC, Sherry RM et al (2003) Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci USA 100:8372–8377PubMedCrossRef
3.
go back to reference Morgan RA, Dudley ME, Wunderlich JR et al (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314:126–129PubMedCrossRef Morgan RA, Dudley ME, Wunderlich JR et al (2006) Cancer regression in patients after transfer of genetically engineered lymphocytes. Science 314:126–129PubMedCrossRef
4.
go back to reference Cebon J, Gedye C, John T et al (2007) Immunotherapy of advanced or metastatic melanoma. Clin Adv Hematol Oncol 5:994–1006PubMed Cebon J, Gedye C, John T et al (2007) Immunotherapy of advanced or metastatic melanoma. Clin Adv Hematol Oncol 5:994–1006PubMed
5.
go back to reference Reya T, Morrison SJ, Clarke MF et al (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111PubMedCrossRef Reya T, Morrison SJ, Clarke MF et al (2001) Stem cells, cancer, and cancer stem cells. Nature 414:105–111PubMedCrossRef
6.
go back to reference Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284PubMedCrossRef Dalerba P, Cho RW, Clarke MF (2007) Cancer stem cells: models and concepts. Annu Rev Med 58:267–284PubMedCrossRef
8.
go back to reference Brabletz T, Jung A, Spaderna S et al (2005) Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer 5:744–749PubMedCrossRef Brabletz T, Jung A, Spaderna S et al (2005) Opinion: migrating cancer stem cells—an integrated concept of malignant tumour progression. Nat Rev Cancer 5:744–749PubMedCrossRef
9.
go back to reference Kim JJ, Tannock IF (2005) Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 5:516–525PubMedCrossRef Kim JJ, Tannock IF (2005) Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 5:516–525PubMedCrossRef
10.
go back to reference Frank NY, Margaryan A, Huang Y et al (2005) ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320–4333PubMedCrossRef Frank NY, Margaryan A, Huang Y et al (2005) ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320–4333PubMedCrossRef
11.
go back to reference Fang D, Nguyen TK, Leishear K et al (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65:9328–9337PubMedCrossRef Fang D, Nguyen TK, Leishear K et al (2005) A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res 65:9328–9337PubMedCrossRef
12.
go back to reference Klein WM, Wu BP, Zhao S et al (2007) Increased expression of stem cell markers in malignant melanoma. Mod Pathol 20:102–107PubMedCrossRef Klein WM, Wu BP, Zhao S et al (2007) Increased expression of stem cell markers in malignant melanoma. Mod Pathol 20:102–107PubMedCrossRef
13.
go back to reference Monzani E, Facchetti F, Galmozzi E et al (2007) Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 43:935–946PubMedCrossRef Monzani E, Facchetti F, Galmozzi E et al (2007) Melanoma contains CD133 and ABCG2 positive cells with enhanced tumourigenic potential. Eur J Cancer 43:935–946PubMedCrossRef
14.
go back to reference Schatton T, Murphy GF, Frank NY et al (2008) Identification of cells initiating human melanomas. Nature 451:345–349PubMedCrossRef Schatton T, Murphy GF, Frank NY et al (2008) Identification of cells initiating human melanomas. Nature 451:345–349PubMedCrossRef
15.
go back to reference Quintana E, Shackleton M, Sabel MS et al (2008) Efficient tumour formation by single human melanoma cells. Nature 456:593–598PubMedCrossRef Quintana E, Shackleton M, Sabel MS et al (2008) Efficient tumour formation by single human melanoma cells. Nature 456:593–598PubMedCrossRef
17.
go back to reference Nicholaou T, Ebert L, Davis ID et al (2006) Directions in the immune targeting of cancer: lessons learned from the cancer-testis Ag NY-ESO-1. Immunol Cell Biol 84:303–317PubMedCrossRef Nicholaou T, Ebert L, Davis ID et al (2006) Directions in the immune targeting of cancer: lessons learned from the cancer-testis Ag NY-ESO-1. Immunol Cell Biol 84:303–317PubMedCrossRef
18.
go back to reference Simpson AJ, Caballero OL, Jungbluth A et al (2005) Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 5:615–625PubMedCrossRef Simpson AJ, Caballero OL, Jungbluth A et al (2005) Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 5:615–625PubMedCrossRef
19.
go back to reference Jäger D, Taverna C, Zippelius A et al (2004) Identification of tumor antigens as potential target antigens for immunotherapy by serological expression cloning. Cancer Immunol Immunother 53:144–147PubMedCrossRef Jäger D, Taverna C, Zippelius A et al (2004) Identification of tumor antigens as potential target antigens for immunotherapy by serological expression cloning. Cancer Immunol Immunother 53:144–147PubMedCrossRef
20.
go back to reference Yang B, O’Herrin SM, Wu J et al (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67:9954–9962PubMedCrossRef Yang B, O’Herrin SM, Wu J et al (2007) MAGE-A, mMage-b, and MAGE-C proteins form complexes with KAP1 and suppress p53-dependent apoptosis in MAGE-positive cell lines. Cancer Res 67:9954–9962PubMedCrossRef
21.
go back to reference Laduron S, Deplus R, Zhou S et al (2004) MAGE-A1 interacts with adaptor SKIP and the deacetylase HDAC1 to repress transcription. Nucleic Acids Res 32:4340–4350PubMedCrossRef Laduron S, Deplus R, Zhou S et al (2004) MAGE-A1 interacts with adaptor SKIP and the deacetylase HDAC1 to repress transcription. Nucleic Acids Res 32:4340–4350PubMedCrossRef
23.
go back to reference Davis ID, Chen W, Jackson H et al (2004) Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc Natl Acad Sci USA 101:10697–10702PubMedCrossRef Davis ID, Chen W, Jackson H et al (2004) Recombinant NY-ESO-1 protein with ISCOMATRIX adjuvant induces broad integrated antibody and CD4(+) and CD8(+) T cell responses in humans. Proc Natl Acad Sci USA 101:10697–10702PubMedCrossRef
24.
go back to reference Fargeas CA, Fonseca A-V, Huttner WB et al (2006) Prominin–1 (CD133): from progenitor cells to human diseases. Future Lipidol 1:213–225CrossRef Fargeas CA, Fonseca A-V, Huttner WB et al (2006) Prominin–1 (CD133): from progenitor cells to human diseases. Future Lipidol 1:213–225CrossRef
25.
go back to reference Singh SK, Hawkins C, Clarke ID et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRef Singh SK, Hawkins C, Clarke ID et al (2004) Identification of human brain tumour initiating cells. Nature 432:396–401PubMedCrossRef
26.
go back to reference Belicchi M, Pisati F, Lopa R et al (2004) Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J Neurosci Res 77:475–486PubMedCrossRef Belicchi M, Pisati F, Lopa R et al (2004) Human skin-derived stem cells migrate throughout forebrain and differentiate into astrocytes after injection into adult mouse brain. J Neurosci Res 77:475–486PubMedCrossRef
27.
go back to reference Gibbs P, Hutchins AM, Dorian KT et al (2000) MAGE-12 and MAGE-6 are frequently expressed in malignant melanoma. Melanoma Res 10:259–264PubMedCrossRef Gibbs P, Hutchins AM, Dorian KT et al (2000) MAGE-12 and MAGE-6 are frequently expressed in malignant melanoma. Melanoma Res 10:259–264PubMedCrossRef
28.
go back to reference Carey TE, Takahashi T, Resnick LA et al (1976) Cell surface antigens of human malignant melanoma: mixed hemadsorption assays for humoral immunity to cultured autologous melanoma cells. Proc Natl Acad Sci USA 73:3278–3282PubMedCrossRef Carey TE, Takahashi T, Resnick LA et al (1976) Cell surface antigens of human malignant melanoma: mixed hemadsorption assays for humoral immunity to cultured autologous melanoma cells. Proc Natl Acad Sci USA 73:3278–3282PubMedCrossRef
29.
go back to reference Karbanova J, Missol-Kolka E, Fonseca AV et al (2008) The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J Histochem Cytochem 56:977–993PubMedCrossRef Karbanova J, Missol-Kolka E, Fonseca AV et al (2008) The stem cell marker CD133 (Prominin-1) is expressed in various human glandular epithelia. J Histochem Cytochem 56:977–993PubMedCrossRef
30.
go back to reference Barrow C, Browning J, MacGregor D et al (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771PubMedCrossRef Barrow C, Browning J, MacGregor D et al (2006) Tumor antigen expression in melanoma varies according to antigen and stage. Clin Cancer Res 12:764–771PubMedCrossRef
31.
go back to reference Jungbluth AA, Chen YT, Busam KJ et al (2002) CT7 (MAGE-C1) antigen expression in normal and neoplastic tissues. Int J Cancer 99:839–845PubMedCrossRef Jungbluth AA, Chen YT, Busam KJ et al (2002) CT7 (MAGE-C1) antigen expression in normal and neoplastic tissues. Int J Cancer 99:839–845PubMedCrossRef
32.
go back to reference Vaughan HA, Svobodova S, MacGregor D et al (2004) Immunohistochemical and molecular analysis of human melanomas for expression of the human cancer-testis antigens NY-ESO-1 and LAGE-1. Clin Cancer Res 10:8396–8404PubMedCrossRef Vaughan HA, Svobodova S, MacGregor D et al (2004) Immunohistochemical and molecular analysis of human melanomas for expression of the human cancer-testis antigens NY-ESO-1 and LAGE-1. Clin Cancer Res 10:8396–8404PubMedCrossRef
33.
go back to reference Chen JL, Dunbar PR, Gileadi U et al (2000) Identification of NY-ESO-1 peptide analogues capable of improved stimulation of tumor-reactive CTL. J Immunol 165:948–955PubMed Chen JL, Dunbar PR, Gileadi U et al (2000) Identification of NY-ESO-1 peptide analogues capable of improved stimulation of tumor-reactive CTL. J Immunol 165:948–955PubMed
34.
go back to reference Lev DC, Onn A, Melinkova VO et al (2004) Exposure of melanoma cells to dacarbazine results in enhanced tumor growth and metastasis in vivo. J Clin Oncol 22:2092–2100PubMedCrossRef Lev DC, Onn A, Melinkova VO et al (2004) Exposure of melanoma cells to dacarbazine results in enhanced tumor growth and metastasis in vivo. J Clin Oncol 22:2092–2100PubMedCrossRef
35.
go back to reference Grichnik JM, Burch JA, Schulteis RD et al (2006) Melanoma, a tumor based on a mutant stem cell? J Invest Dermatol 126:142–153PubMedCrossRef Grichnik JM, Burch JA, Schulteis RD et al (2006) Melanoma, a tumor based on a mutant stem cell? J Invest Dermatol 126:142–153PubMedCrossRef
36.
go back to reference Clarke MF (2005) A self-renewal assay for cancer stem cells. Cancer Chemother Pharmacol 56(Suppl 7):64–68PubMedCrossRef Clarke MF (2005) A self-renewal assay for cancer stem cells. Cancer Chemother Pharmacol 56(Suppl 7):64–68PubMedCrossRef
37.
go back to reference Jaksch M, Munera J, Bajpai R et al (2008) Cell cycle-dependent variation of a CD133 epitope in human embryonic stem cell, colon cancer, and melanoma cell lines. Cancer Res 68:7882–7886PubMedCrossRef Jaksch M, Munera J, Bajpai R et al (2008) Cell cycle-dependent variation of a CD133 epitope in human embryonic stem cell, colon cancer, and melanoma cell lines. Cancer Res 68:7882–7886PubMedCrossRef
38.
go back to reference Herlyn M, Balaban G, Bennicelli J et al (1985) Primary melanoma cells of the vertical growth phase: similarities to metastatic cells. J Natl Cancer Inst 74:283–289PubMed Herlyn M, Balaban G, Bennicelli J et al (1985) Primary melanoma cells of the vertical growth phase: similarities to metastatic cells. J Natl Cancer Inst 74:283–289PubMed
39.
go back to reference Lee J, Kotliarova S, Kotliarov Y et al (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9:391–403PubMedCrossRef Lee J, Kotliarova S, Kotliarov Y et al (2006) Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 9:391–403PubMedCrossRef
40.
go back to reference Li A, Walling J, Kotliarov Y et al (2008) Genomic changes and gene expression profiles reveal that established glioma cell lines are poorly representative of primary human gliomas. Mol Cancer Res 6:21–30PubMedCrossRef Li A, Walling J, Kotliarov Y et al (2008) Genomic changes and gene expression profiles reveal that established glioma cell lines are poorly representative of primary human gliomas. Mol Cancer Res 6:21–30PubMedCrossRef
41.
go back to reference De Witt Hamer PC, Van Tilborg AA, Eijk PP et al (2008) The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene 27:2091–2096PubMedCrossRef De Witt Hamer PC, Van Tilborg AA, Eijk PP et al (2008) The genomic profile of human malignant glioma is altered early in primary cell culture and preserved in spheroids. Oncogene 27:2091–2096PubMedCrossRef
42.
go back to reference Vogl A, Sartorius U, Vogt T et al (2005) Gene expression profile changes between melanoma metastases and their daughter cell lines: implication for vaccination protocols. J Investig Dermatol 124:401–404PubMedCrossRef Vogl A, Sartorius U, Vogt T et al (2005) Gene expression profile changes between melanoma metastases and their daughter cell lines: implication for vaccination protocols. J Investig Dermatol 124:401–404PubMedCrossRef
43.
go back to reference Sigalotti L, Covre A, Zabierowski S et al (2008) Cancer testis antigens in human melanoma stem cells: expression, distribution, and methylation status. J Cell Physiol 215:287–291PubMedCrossRef Sigalotti L, Covre A, Zabierowski S et al (2008) Cancer testis antigens in human melanoma stem cells: expression, distribution, and methylation status. J Cell Physiol 215:287–291PubMedCrossRef
44.
go back to reference Gjerstorff MF, Johansen LE, Nielsen O et al (2006) Restriction of GAGE protein expression to subpopulations of cancer cells is independent of genotype and may limit the use of GAGE proteins as targets for cancer immunotherapy. Br J Cancer 94:1864–1873PubMedCrossRef Gjerstorff MF, Johansen LE, Nielsen O et al (2006) Restriction of GAGE protein expression to subpopulations of cancer cells is independent of genotype and may limit the use of GAGE proteins as targets for cancer immunotherapy. Br J Cancer 94:1864–1873PubMedCrossRef
45.
go back to reference Adair SJ, Hogan KT (2008) Treatment of ovarian cancer cell lines with 5-aza–2′-deoxycytidine upregulates the expression of cancer-testis antigens and class I major histocompatibility complex-encoded molecules. Cancer Immunol Immunother. doi:10.1007/s00262-008-0582-6 Adair SJ, Hogan KT (2008) Treatment of ovarian cancer cell lines with 5-aza–2′-deoxycytidine upregulates the expression of cancer-testis antigens and class I major histocompatibility complex-encoded molecules. Cancer Immunol Immunother. doi:10.​1007/​s00262-008-0582-6
46.
go back to reference Rappa G, Fodstad O, Lorico A (2008) The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells 26:3008–3017PubMedCrossRef Rappa G, Fodstad O, Lorico A (2008) The stem cell-associated antigen CD133 (Prominin-1) is a molecular therapeutic target for metastatic melanoma. Stem Cells 26:3008–3017PubMedCrossRef
48.
go back to reference Smith LM, Nesterova A, Ryan MC et al (2008) CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer 99:100–109PubMedCrossRef Smith LM, Nesterova A, Ryan MC et al (2008) CD133/prominin-1 is a potential therapeutic target for antibody-drug conjugates in hepatocellular and gastric cancers. Br J Cancer 99:100–109PubMedCrossRef
49.
go back to reference Florek M, Haase M, Marzesco AM et al (2005) Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 319:15–26PubMedCrossRef Florek M, Haase M, Marzesco AM et al (2005) Prominin-1/CD133, a neural and hematopoietic stem cell marker, is expressed in adult human differentiated cells and certain types of kidney cancer. Cell Tissue Res 319:15–26PubMedCrossRef
50.
go back to reference Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4:33–45PubMedCrossRef Ponta H, Sherman L, Herrlich PA (2003) CD44: from adhesion molecules to signalling regulators. Nat Rev Mol Cell Biol 4:33–45PubMedCrossRef
52.
go back to reference Ménard C, Martin F, Apetoh L et al (2008) Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol Immunother 57:1579–1587PubMedCrossRef Ménard C, Martin F, Apetoh L et al (2008) Cancer chemotherapy: not only a direct cytotoxic effect, but also an adjuvant for antitumor immunity. Cancer Immunol Immunother 57:1579–1587PubMedCrossRef
53.
go back to reference Mine T, Matsueda S, Li Y et al (2008) Breast cancer cells expressing stem cell markers CD44(+) CD24 (lo) are eliminated by Numb-1 peptide-activated T cells. Cancer Immunol Immunother. doi:10.1007/s00262-008-0623-1 Mine T, Matsueda S, Li Y et al (2008) Breast cancer cells expressing stem cell markers CD44(+) CD24 (lo) are eliminated by Numb-1 peptide-activated T cells. Cancer Immunol Immunother. doi:10.​1007/​s00262-008-0623-1
Metadata
Title
Cancer/testis antigens can be immunological targets in clonogenic CD133+ melanoma cells
Authors
Craig Gedye
Juliet Quirk
Judy Browning
Suzanne Svobodová
Thomas John
Pavel Sluka
P. Rod Dunbar
Denis Corbeil
Jonathan Cebon
Ian D. Davis
Publication date
01-10-2009
Publisher
Springer-Verlag
Published in
Cancer Immunology, Immunotherapy / Issue 10/2009
Print ISSN: 0340-7004
Electronic ISSN: 1432-0851
DOI
https://doi.org/10.1007/s00262-009-0672-0

Other articles of this Issue 10/2009

Cancer Immunology, Immunotherapy 10/2009 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine