Natural killer cells kill human melanoma cells with characteristics of cancer stem cells

International Immunology

Volumn 21, Issue 7, 2009, Pages 793-801

  Pietra, Gabriella ^a   Manzini, Claudia ^a   Vitale, Massimo ^b   Balsamo, Mirna ^a   Ognio, Emanuela ^b   Boitano, Monica ^b   Queirolo, Paola ^b   Moretta, Lorenzo ^a,c   Mingari, Maria Cristina ^a,b  

^a UNIVERSITY OF GENOA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c G GASLINI INSTITUTE   (Italy)

Author keywords

Cancer stem cells; CD133; Melanoma; Melanospheres; NK cells

Indexed keywords

CD133 ANTIGEN; INTERLEUKIN 2; NEUROTROPHIN RECEPTOR P75; STEM CELL FACTOR RECEPTOR;

APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CANCER RESISTANCE; CANCER STEM CELL; CELL ACTIVITY; CELL INTERACTION; CELL SELECTION; CONTROLLED STUDY; CULTURE MEDIUM; CYTOLYSIS; ENRICHMENT CULTURE; HUMAN; HUMAN CELL; HUMAN TISSUE; LYMPHOCYTE ACTIVATION; MELANOMA CELL; MOLECULAR RECOGNITION; NATURAL KILLER CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOSENSITIVITY;

ANTIGENS, CD; CASPASE 3; CELL LINE, TUMOR; CYTOTOXICITY, IMMUNOLOGIC; GLYCOPROTEINS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; INTERLEUKIN-2; KILLER CELLS, NATURAL; MELANOMA; NEOPLASTIC STEM CELLS; NERVE TISSUE PROTEINS; PEPTIDES; PROTO-ONCOGENE PROTEINS C-KIT; RECEPTORS, NERVE GROWTH FACTOR; SKIN NEOPLASMS; TUMOR CELLS, CULTURED;

EID: 67649864077     PISSN: 09538178     EISSN: 14602377     Source Type: Journal    
DOI: 10.1093/intimm/dxp047     Document Type: Article

References (42)

1. Chin, L., Garraway, L. A. and Fisher, D. E. 2006. Malignant melanoma: genetics and therapeutics in the genomic era. Genes Dev. 20:2149.
2. Grichnik, J. M., Burch, J. A., Schulteis, R. D. et al. 2006. Melanoma, a tumor based on a mutant stem cell? J. Invest. Dermatol. 126:142.
3. Reya, T., Morrison, S. J., Clarke, M. F. and Weissman, I. L. 2001. Stem cells, cancer, and cancer stem cells. Nature 414:105.
4. Morrison, S. J. and Kimble, J. 2006. Asymmetric and symmetric stem-cell divisions in development and cancer. Nature 441:1068.
5. Bonnet, D. and Dick, J. E. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3:730.
6. Al-Hajj, M., Wicha, M. S., Benito-Hernandez, A., Morrison, S. J. and Clarke, M. F. 2003. Prospective identification of tumorigenic breast cancer cells. Proc. Natl Acad. Sci. USA 100:3983.
7. Singh, S. K., Clarke, I. D., Terasaki, M. et al. 2003. Identification of a cancer stem cell in human brain tumors. Cancer Res. 63:5821.
8. Singh, S. K., Hawkins, C., Clarke, I. D. et al. 2004. Identification of human brain tumour initiating cells. Nature 432:396.
9. Ricci-Vitiani, L., Lombardi, D. G., Pilozzi, E. et al. 2007. Identification and expansion of human colon-cancer-initiating cells. Nature 445:111.
10. O'Brien, C. A., Pollett, A., Gallinger, S. and Dick, J. E. 2007. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 445:106.
11. Li, C., Heidt, D. G., Dalerba, P. et al. 2007. Identification of pancreatic cancer stem cells. Cancer Res. 67:1030.
12. Lee, C. J., Li, C. and Simeone, D. M. 2008. Human pancreatic cancer stem cells: Implications for how we treat pancreatic cancer. Transl. Oncol. 1:14.
13. Dean, M., Fojo, T. and Bates, S. 2005. Tumour stem cells and drug resistance. Nat. Rev. Cancer 5:275.
14. Gottesman, M. M., Fojo, T. and Bates, S. E. 2002. Multidrug resistance in cancer: Role of ATP-dependent transporters. Nat. Rev. Cancer 2:48.
15. Bao, S., Wu, Q., McLendon, R. E. et al. 2006. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:756.
16. Fang, D., Nguyen, T. K., Leishear, K. et al. 2005. A tumorigenic subpopulation with stem cell properties in melanomas. Cancer Res. 65:9328.
17. 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.
18. Balint, K., Xiao, M., Pinnix, C. C. et al. 2005. Activation of Notch1 signaling is required for beta-catenin-mediated human primary melanoma progression. J. Clin. Invest. 115:3166.
19. Weeraratna, A. T., Jiang, Y., Hostetter, G. et al. 2002. Wnt5a signaling directly affects cell motility and invasion of metastatic melanoma. Cancer Cell 1:279.
20. Frank, N. Y., Margaryan, A., Huang, Y. et al. 2005. ABCB5-mediated doxorubicin transport and chemoresistance in human malignant melanoma. Cancer Res 65:4320.
21. Klein, W. M., Wu, B. P., Zhao, S., Wu, H., Klein-Szanto, A. J. and Tahan, S. R. 2007. Increased expression of stem cell markers in malignant melanoma. Mod. Pathol. 20:102.
22. Flørenes, V. A., Holm, R., Myklebost, O., Lendahl, U. and Fodstad, O. 1994. Expression of the neuroectodermal intermediate filament nestin in human melanomas. Cancer Res. 54:354.
23. Schatton, T., Murphy, G. F., Frank, N. Y. et al. 2008. Identification of cells initiating human melanomas. Nature 451:345.
24. Keshet, G. I., Goldstein, I., Itzhaki, O. et al. 2008. MDR1 expression identifies human melanoma stem cells. Biochem. Biophys. Res. Commun. 368:930.
25. Ljunggren, H. G. and Malmberg, K. J. 2007. Prospects for the use of NK cells in immunotherapy of human cancer. Nat. Rev. Immunol. 7:329.
26. Malmberg, K. J., Bryceson, Y. T., Carlsten, M. et al. 2008. NK cell-mediated targeting of human cancer and possibilities for new means of immunotherapy. Cancer Immunol. Immunother. 57:1541.
27. Moretta, A., Bottino, C., Vitale, M. et al. 1996. Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 14:619.
28. Moretta, A., Bottino, C., Vitale, M. et al. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19:197.
29. Moretta, L. and Moretta, A. 2004. Unravelling natural killer cell function: Triggering and inhibitory human NK receptors. EMBO J. 23:255.
30. Bauer, S., Groh, V., Wu, J. et al. 1999. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285:727.
31. Cosman, D., Mullberg, J., Sutherland, C. L. et al. 2001. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14:123.
32. Bottino, C., Castriconi, R., Pende, D. et al. 2003. Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 198:557.
33. Wu, A., Wiesner, S., Xiao, J. et al. 2007. Expression of MHC I and NK ligands on human CD133+ glioma cells: Possible targets of immunotherapy. J. Neurooncol. 83:121.
34. Pende, D., Spaggiari, G. M., Marcenaro, S. et al. 2005. Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoblastic leukemias: Evidence for the involvement of the Poliovirus receptor (CD155) and Nectin-2 (CD112). Blood 105:2066.
35. Lapidot, T., Sirard, C., Vormoor, J. et al. 1994. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367:645.
36. Pende, D., Rivera, P., Marcenaro, S. et al. 2002. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: Analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res. 62:6178.
37. Huang, S., Luca, M., Gutman, M. et al. 1996. Enforced c-KIT expression renders highly metastatic human melanoma cells susceptible to stem cell factor-induced apoptosis and inhibits their tumorigenic and metastatic potential. Oncogene 13: 2339.
38. Welker, P., Schadendorf, D., Artuc, M., Grabbe, J. and Henz, B. M. 2000. Expression of SCF splice variants in human melanocytes and melanoma cell lines: Potential prognostic implications. Br. J. Cancer 82:1453.
39. Shih, I. M. 1999. The role of CD146 (Mel-CAM) in biology and pathology. J. Pathol. 189:4.
40. Mills, L., Tellez, C., Huang, S. et al. 2002. Fully human antibodies to MCAM/MUC18 inhibit tumor growth and metastasis of human melanoma. Cancer Res. 62:5106.
41. Ponti, D., Costa, A., Zaffaroni, N. et al. 2005. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/ progenitor cell properties. Cancer Res. 65:5506.
42. Pellegatta, S., Poliani, P. L., Corno, D. et al. 2006. Neurospheres enriched in cancer stem-like cells are highly effective in eliciting a dendritic cell-mediated immune response against malignant gliomas. Cancer Res. 66:10247.