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Journal of Oncology
Volume 2010, Article ID 689893, 8 pages
http://dx.doi.org/10.1155/2010/689893
Review Article

Advanced Malignant Melanoma: Immunologic and Multimodal Therapeutic Strategies

National Center for Tumor Diseases, Department of Medical Oncology, University of Heidelberg, 69120 Heidelberg, Germany

Received 9 November 2009; Accepted 7 January 2010

Academic Editor: Douglas S. Tyler

Copyright © 2010 Niels Halama et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. E. Mold, J. Michaelsson, T. D. Burt et al., “Maternal alloantigens promote the development of tolerogenic fetal regulatory T cells in utero,” Science, vol. 322, no. 5907, pp. 1562–1565, 2008. View at Publisher · View at Google Scholar · View at Scopus
  2. A. M. Sharkey, L. Gardner, S. Hiby, L. Farrell et al., “Killer Ig-like receptor expression in uterine NK cells is biased toward recognition of HLA-C and alters with gestational age,” Journal of Immunology, vol. 181, no. 1, pp. 39–46, 2008. View at Google Scholar · View at Scopus
  3. C. Ohnmacht, A. Pullner, S. B. S. King et al., “Constitutive ablation of dendritic cells breaks self-tolerance of CD4 T cells and results in spontaneous fatal autoimmunity,” Journal of Experimental Medicine, vol. 206, no. 3, pp. 549–559, 2009. View at Publisher · View at Google Scholar · View at Scopus
  4. J. Shimizu, S. Yamazaki, and S. Sakaguchi, “Induction of tumor immunity by removing CD25+CD4+ T cells: a common basis between tumor immunity and autoimmunity,” Journal of Immunology, vol. 163, no. 10, pp. 5211–5218, 1999. View at Google Scholar · View at Scopus
  5. J. D. Bui and R. D. Schreiber, “Cancer immunosurveillance, immunoediting and inflammation: independent or interdependent processes?” Current Opinion in Immunology, vol. 19, no. 2, pp. 203–208, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. G. P. Dunn, A. T. Bruce, H. Ikeda, L. J. Old, and R. D. Schreiber, “Cancer immunoediting: from immunosurveillance to tumor escape,” Nature Immunology, vol. 3, no. 11, pp. 991–998, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. C. M. Koebel, W. Vermi, J. B. Swann et al., “Adaptive immunity maintains occult cancer in an equilibrium state,” Nature, vol. 450, no. 7171, pp. 903–907, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. E. Jager, Y.-T. Chen, J. W. Drijfhout et al., “Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes,” Journal of Experimental Medicine, vol. 187, no. 2, pp. 265–270, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. E. Jager, S. Gnjatic, Y. Nagata et al., “Induction of primary NY-ESO-1 immunity: CD8+ T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 22, pp. 12198–12203, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. E. Jager, D. Jager, and A. Knuth, “Antigen-specific immunotherapy and cancer vaccines,” International Journal of Cancer, vol. 106, no. 6, pp. 817–820, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. D. Jager, J. Karbach, C. Pauligk et al., “Humoral and cellular immune responses against the breast cancer antigen NY-BR-1: definition of two HLA-A2 restricted peptide epitopes,” Cancer Immunity, vol. 5, p. 11, 2005. View at Google Scholar · View at Scopus
  12. D. Jager, E. Stockert, A. O. Gure et al., “Identification of a tissue-specific putative transcription factor in breast tissue by serological screening of a breast cancer library,” Cancer Research, vol. 61, no. 5, pp. 2055–2061, 2001. View at Google Scholar · View at Scopus
  13. D. Jager, V. Filonenko, I. Gout et al., “NY-BR-1 is a differentiation antigen of the mammary gland,” Applied Immunohistochemistry and Molecular Morphology, vol. 15, no. 1, pp. 77–83, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. M. J. Scanlan, S. Welt, C. M. Gordon et al., “Cancer-related serological recognition of human colon cancer: identification of potential diagnostic and immunotherapeutic targets,” Cancer Research, vol. 62, no. 14, pp. 4041–4047, 2002. View at Google Scholar · View at Scopus
  15. H. Gogas, J. Ioannovich, U. Dafni et al., “Prognostic significance of autoimmunity during treatment of melanoma with interferon,” The New England Journal of Medicine, vol. 354, no. 7, pp. 709–718, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. M. G. Bouwhuis, S. Suciu, S. Collette et al., “Autoimmune antibodies and recurrence-free interval in melanoma patients treated with adjuvant interferon,” Journal of the National Cancer Institute, vol. 101, no. 12, pp. 869–877, 2009. View at Publisher · View at Google Scholar · View at Scopus
  17. G. P. Adams and L. M. Weiner, “Monoclonal antibody therapy of cancer,” Nature Biotechnology, vol. 23, no. 9, pp. 1147–1157, 2005. View at Publisher · View at Google Scholar · View at Scopus
  18. I. Melero, S. Hervas-Stubbs, M. Glennie, D. M. Pardoll, and L. Chen, “Immunostimulatory monoclonal antibodies for cancer therapy,” Nature Reviews Cancer, vol. 7, no. 2, pp. 95–106, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. J. S. Weber, S. O'Day, W. Urba et al., “Phase I/II study of ipilimumab for patients with metastatic melanoma,” Journal of Clinical Oncology, vol. 26, no. 36, pp. 5950–5956, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. A. Ribas, D. C. Hanson, D. A. Noe et al., “Tremelimumab (CP-675,206), a cytotoxic T lymphocyte-associated antigen 4 blocking monoclonal antibody in clinical development for patients with cancer,” Oncologist, vol. 12, no. 7, pp. 873–883, 2007. View at Publisher · View at Google Scholar · View at Scopus
  21. A. Ribas, A. Hauschild, R. Kefford et al., “Phase III, open-label, randomized, comparative study of tremelimumab CP-675,206 and chemotherapy temozolomide [TMZ] or dacarbazine [DTIC] in patients with advanced melanoma,” Journal of Clinical Oncology, vol. 12, no. 15, supplement, 2008, abstract LBA9011. View at Google Scholar
  22. J. Weber, J. A. Thompson, O. Hamid et al., “A randomized, double-blind, placebo-controlled, phase II study comparing the tolerability and efficacy of ipilimumab administered with or without prophylactic budesonide in patients with unresectable stage III or IV melanoma,” Clinical Cancer Research, vol. 15, no. 17, pp. 5591–5598, 2009. View at Publisher · View at Google Scholar · View at Scopus
  23. Y. M. Saenger and J. D. Wolchok, “The heterogeneity of the kinetics of response to ipilimumab in metastatic melanoma: patient cases,” Cancer Immunity, vol. 8, p. 1, 2008. View at Google Scholar · View at Scopus
  24. S. O. Harbers, A. Crocker, G. Catalano et al., “Antibody-enhanced cross-presentation of self antigen breaks T cell tolerance,” Journal of Clinical Investigation, vol. 117, no. 5, pp. 1361–1369, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Taylor, D. Hershman, N. Shah et al., “Augmented HER-2-specific immunity during treatment with trastuzumab and chemotherapy,” Clinical Cancer Research, vol. 13, no. 17, pp. 5133–5143, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. E. A. Manning, J. G. M. Ullman, J. M. Leatherman et al., “A vascular endothelial growth factor receptor-2 inhibitor enhances antitumor immunity through an immune-based mechanism,” Clinical Cancer Research, vol. 13, no. 13, pp. 3951–3959, 2007. View at Publisher · View at Google Scholar · View at Scopus
  27. M. J. Scanlan, “Identification of human tumor antigens by serological analysis of recombinant cDNA expression libraries (SEREX),” Current Protocols in Immunology, chapter 20, unit 20.7, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. T. Yokoe, F. Tanaka, K. Mimori et al., “Efficient identification of a novel cancer/testis antigen for immunotherapy using three-step microarray analysis,” Cancer Research, vol. 68, no. 4, pp. 1074–1082, 2008. View at Publisher · View at Google Scholar · View at Scopus
  29. P. Srivastava, “Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses,” Annual Review of Immunology, vol. 20, pp. 395–425, 2002. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Belli, A. Testori, L. Rivoltini et al., “Vaccination of metastatic melanoma patients with autologous tumor-derived heat shock protein gp96-peptide complexes: clinical and immunologic findings,” Journal of Clinical Oncology, vol. 20, no. 20, pp. 4169–4180, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Testori, J. Richards, E. Whitman et al., “Phase III comparison of vitespen, an autologous tumor-derived heat shock protein gp96 peptide complex vaccine, with physician's choice of treatment for stage IV melanoma: the C-100-21 study group,” Journal of Clinical Oncology, vol. 26, no. 6, pp. 955–962, 2008. View at Publisher · View at Google Scholar · View at Scopus
  32. J. Banchereau and A. K. Palucka, “Dendritic cells as therapeutic vaccines against cancer,” Nature Reviews Immunology, vol. 5, no. 4, pp. 296–306, 2005. View at Publisher · View at Google Scholar · View at Scopus
  33. D. Schadendorf, S. Ugurel, B. Schuler-Thurner et al., “Dacarbazine (DTIC) versus vaccination with autologous peptide-pulsed dendritic cells (DC) in first-line treatment of patients with metastatic melanoma: a randomized phase III trial of the DC study group of the DeCOG,” Annals of Oncology, vol. 17, no. 4, pp. 563–570, 2006. View at Publisher · View at Google Scholar · View at Scopus
  34. S. A. Rosenberg, J. C. Yang, and N. P. Restifo, “Cancer immunotherapy: moving beyond current vaccines,” Nature Medicine, vol. 10, no. 9, pp. 909–915, 2004. View at Publisher · View at Google Scholar · View at Scopus
  35. J. H. Stewart IV and S. A. Rosenberg, “Long-term survival of anti-tumor lymphocytes generated by vaccination of patients with melanoma with a peptide vaccine,” Journal of Immunotherapy, vol. 23, no. 4, pp. 401–404, 2000. View at Publisher · View at Google Scholar · View at Scopus
  36. R. Kaneno, G. V. Shurin, I. L. Tourkova, and M. R. Shurin, “Chemomodulation of human dendritic cell function by antineoplastic agents in low noncytotoxic concentrations,” Journal of Translational Medicine, vol. 7, article 58, 2009. View at Publisher · View at Google Scholar · View at Scopus
  37. R. J. North, “Cyclophosphamide-facilitated adoptive immunotherapy of an established tumor depends on elimination of tumor-induced suppressor T cells,” Journal of Experimental Medicine, vol. 155, no. 4, pp. 1063–1074, 1982. View at Google Scholar · View at Scopus
  38. G. V. Shurin, I. L. Tourkova, R. Kaneno, and M. R. Shurin, “Chemotherapeutic agents in noncytotoxic concentrations increase antigen presentation by dendritic cells via an IL-12-dependent mechanism,” Journal of Immunology, vol. 183, no. 1, pp. 137–144, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. A. M. M. Eggermont, “Immunotherapy: vaccine trials in melanoma—time for reflection,” Nature Reviews Clinical Oncology, vol. 6, no. 5, pp. 256–258, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. R. Buckwalter and P. K. Srivastava, ““It is the antigen(s), stupid” and other lessons from over a decade of vaccitherapy of human cancer,” Seminars in Immunology, vol. 20, no. 5, pp. 296–300, 2008. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Atanackovic, N. K. Altorki, Y. Cao et al., “Booster vaccination of cancer patients with MAGE-A3 protein reveals long-term immunological memory or tolerance depending on priming,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 5, pp. 1650–1655, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. W. Kruit, S. Suciu, B. Dreno et al., “Immunization with recombinant MAGE-A3 protein combined with adjuvant systems AS15 or AS02B in patients with unresectable and progressive metastatic cutaneous melanoma: a randomized open-label phase II study of the EORTC Melanoma Group (16032–18031),” Journal of Clinical Oncology, vol. 26, 2008, abstract 9065b. View at Google Scholar
  43. A. Hauschild, M. Weichenthal, K. Rass et al., “Prospective randomized multicenter adjuvant dermatologic cooperative oncology group trial of low-dose interferon alfa-2b with or without a modified high-dose interferon alfa-2b induction phase in patients with lymph node—negative melanoma,” Journal of Clinical Oncology, vol. 27, no. 21, pp. 3496–3502, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. J. A. Sparano, R. I. Fisher, M. Sunderland et al., “Randomized phase III trial of treatment with high-dose interleukin-2 either alone or in combination with interferon alfa-2a in patients with advanced melanoma,” Journal of Clinical Oncology, vol. 11, no. 10, pp. 1969–1977, 1993. View at Google Scholar · View at Scopus
  45. F. M. Marincola, D. E. White, A. P. Wise, and S. A. Rosenberg, “Combination therapy with interferon alfa-2a and interleukin-2 for the treatment of metastatic cancer,” Journal of Clinical Oncology, vol. 13, no. 5, pp. 1110–1122, 1995. View at Google Scholar · View at Scopus
  46. K. S. Frederiksen, D. Lundsgaard, J. A. Freeman et al., “IL-21 induces in vivo immune activation of NK cells and CD8+ T cells in patients with metastatic melanoma and renal cell carcinoma,” Cancer Immunology, Immunotherapy, vol. 57, no. 10, pp. 1439–1449, 2008. View at Publisher · View at Google Scholar · View at Scopus
  47. J. A. Thompson, B. D. Curti, B. G. Redman et al., “Phase I study of recombinant interleukin-21 in patients with metastatic melanoma and renal cell carcinoma,” Journal of Clinical Oncology, vol. 26, no. 12, pp. 2034–2039, 2008. View at Publisher · View at Google Scholar · View at Scopus
  48. H. Harlin, Y. Meng, A. C. Peterson et al., “Chemokine expression in melanoma metastases associated with CD8+ T-cell recruitment,” Cancer Research, vol. 69, no. 7, pp. 3077–3085, 2009. View at Publisher · View at Google Scholar · View at Scopus
  49. M. E. Dudley, J. R. Wunderlich, J. C. Yang et al., “Adoptive cell transfer therapy following non-myeloablative but lymphodepleting chemotherapy for the treatment of patients with refractory metastatic melanoma,” Journal of Clinical Oncology, vol. 23, no. 10, pp. 2346–2357, 2005. View at Publisher · View at Google Scholar · View at Scopus
  50. M. E. Dudley, J. C. Yang, R. Sherry et al., “Adoptive cell therapy for patients with metastatic melanoma: evaluation of intensive myeloablative chemoradiation preparative regimens,” Journal of Clinical Oncology, vol. 26, no. 32, pp. 5233–5239, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. W. Zou, “Regulatory T cells, tumour immunity and immunotherapy,” Nature Reviews Immunology, vol. 6, no. 4, pp. 295–307, 2006. View at Publisher · View at Google Scholar · View at Scopus
  52. H. J. Pegram, J. T. Jackson, M. J. Smyth, M. H. Kershaw, and P. K. Darcy, “Adoptive transfer of gene-modified primary NK cells can specifically inhibit tumor progression in vivo,” Journal of Immunology, vol. 181, no. 5, pp. 3449–3455, 2008. View at Google Scholar · View at Scopus
  53. H. J. Stauss, M. Cesco-Gaspere, S. Thomas et al., “Monoclonal t-cell receptors: new reagents for cancer therapy,” Molecular Therapy, vol. 15, no. 10, pp. 1744–1750, 2007. View at Publisher · View at Google Scholar · View at Scopus
  54. R. Voss, R. A. Willemsen, J. Kuball et al., “Molecular design of the Caß interface favors specific pairing of introduced TCRaß in human T cells,” Journal of Immunology, vol. 180, no. 1, pp. 391–401, 2008. View at Google Scholar · View at Scopus
  55. G. K. Abou-Alfa, L. Schwartz, S. Ricci et al., “Phase II study of sorafenib in patients with advanced hepatocellular carcinoma,” Journal of Clinical Oncology, vol. 24, no. 26, pp. 4293–4300, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Seront and J.-P. Machiels, “Targeted therapies in the treatment of advanced renal cell carcinoma,” Recent Patents on Anti-Cancer Drug Discovery, vol. 4, no. 2, pp. 146–156, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. C. Sers, R. Kuner, C. S. Falk et al., “Down-regulation of HLA class I and NKG2D ligands through a concerted action of MAPK and DNA methyltransferases in colorectal cancer cells,” International Journal of Cancer, vol. 125, no. 7, pp. 1626–1639, 2009. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Preta, D. Marescotti, C. Fortini et al., “Inhibition of serine-peptidase activity enhances the generation of a survivin-derived HLA-A2-presented CTL epitope in colon-carcinoma cells,” Scandinavian Journal of Immunology, vol. 68, no. 6, pp. 579–588, 2008. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Meier, B. Schittek, S. Busch et al., “The Ras/Raf/MEK/ERK and PI3K/AKT signaling pathways present molecular targets for the effective treatment of advanced melanoma,” Frontiers in Bioscience, vol. 10, supplement 3, pp. 2986–3001, 2005. View at Google Scholar · View at Scopus
  60. J. A. Curtin, J. Fridlyand, T. Kageshita et al., “Distinct sets of genetic alterations in melanoma,” The New England Journal of Medicine, vol. 353, no. 20, pp. 2135–2147, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. J. LoPiccolo, G. M. Blumenthal, W. B. Bernstein, and P. A. Dennis, “Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations,” Drug Resistance Updates, vol. 11, no. 1-2, pp. 32–50, 2008. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Hersey and X. D. Zhang, “Treatment combinations targeting apoptosis to improve immunotherapy of melanoma,” Cancer Immunology, Immunotherapy, vol. 58, no. 11, pp. 1751–1761, 2009. View at Publisher · View at Google Scholar · View at Scopus