Immunotherapeutic strategies for the treatment of malignant melanoma

Giornale Italiano di Dermatologia e Venereologia

Volumn 143, Issue 2, 2008, Pages 139-149

  Alexeev, V ^a,b   Mucci, T ^a   Igoucheva, O ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

Chemokines; Dendritic cells; Melanoma; T lymphocytes, cytotoxic; Vaccines

Indexed keywords

BCG VACCINE; CHEMOKINE RECEPTOR CCR7; CORYNEBACTERIUM PARVUM VACCINE; CPG OLIGODEOXYNUCLEOTIDE; DENDRITIC CELL VACCINE; DNA VACCINE; GLYCOPROTEIN GP 100; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 12; INTERLEUKIN 2; MELANOMA ANTIGEN; MELANOMA ANTIGEN 1; MELANOMA ANTIGEN 10; MELANOMA ANTIGEN 3; MONOPHENOL MONOOXYGENASE; MONTANIDE ISA 51; NY ESO 1 ANTIGEN; PEPTIDE VACCINE; PROSTATE SPECIFIC ANTIGEN; SECONDARY LYMPHOID TISSUE CHEMOKINE;

ADJUVANT THERAPY; CLINICAL TRIAL; COMBINATION CHEMOTHERAPY; CYTOKINE RELEASE; DRUG EFFECT; HUMAN; IMMUNE RESPONSE; MELANOMA; NONHUMAN; REVIEW; T LYMPHOCYTE; VACCINIA VIRUS;

EID: 45749085810     PISSN: 03920488     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (108)

1. Parkin DM, Bray F, Ferlay J, Pisani P. Global cancer statistics, 2002. CA Cancer J Clin 2005;55:74-108.
2. Knuth A, Wolfel T, Klehmann E, Boon T, Meyer zum Buschenfelde KH. Cytolytic T-cell clones against an autologous human melanoma: specificity study and definition of three antigens by immunoselection. Proceedings of the National Academy of Sciences of the United States of America 1989;86:2804-8.
3. Boon T. Toward a genetic analysis of tumor rejection antigens. Adv Cancer Res 1992;58:177-210.
4. Brichard V, Van Pel A, Wolfel T, Wolfel C, De Plaen E, Lethe B et al. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J Exp Med 1993;178:489-95.
5. Coulie PG, Brichard V, Van Pel A, Wolfel T, Schneider J, Traversari C et al. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas J Exp Med 1994;180:35-42.
6. Kawakami Y, Eliyahu S, Delgado CH, Robbins PF, Rivoltini L, Topalian SL et al. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proceedings of the National Academy of Sciences of the United States of America 1994; 91:3515-9.
7. Wolfel T, Hauer M, Schneider J, Serrano M, Wolfel C, Klehmann-Hieb E, et al. A p16INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science New York, NY 1995;269:1281-4.
8. van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B et al. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science New York, NY 1991;254:1643-7.
9. Spagnoli GC, Adamina M, Bolli M, Weber WP, Zajac P, Marti W et al. Active antigen-specific immunotherapy of melanoma: from basic science to clinical investigation. World J Surg 2005;29:692-9.
10. Blanchet JS, Valmori D, Dufau I, Ayyoub M, Nguyen C, Guillaume P et al. A new generation of Melan-A/MART-1 peptides that fulfill both increased immunogenicity and high resistance to biodegradation: implication for molecular anti-melanoma immunotherapy. J Immunol 2001;167:5852-61.
11. Talebi T, Weber JS. Peptide vaccine trials for melanoma: preclinical background and clinical results. Semin Cancer Biol 2003;13:431-8.
12. Slingluff CL, Jr., Petroni GR, Chianese-Bullock KA, Smolkin ME, Hibbitts S, Murphy C et al. Immunologic and clinical outcomes of a randomized phase II trial of two multipeptide vaccines for melanoma in the adjuvant setting. Clin Cancer Res 2007;13:6386-95.
13. Testori A, Richards J, Whitman E, Mann GB, Lutzky J, Camacho L 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. J Clin Oncol 2008;26:955-62.
14. Hamid O, Solomon JC, Scotland R, Garcia M, Sian S, Ye W et al. Alum with interleukin-12 augments immunity to a melanoma peptide vaccine: correlation with time to relapse in patients with resected high-risk disease. Clin Cancer Res 2007;13:215-22.
15. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-52.
16. Bell D, Young JW, Banchereau J. Dendritic cells. Adv Immunol 1999;72:255-324.
17. Hsu FJ, Benike C, Fagnoni F, Liles TM, Czerwinski D, B Taidi et al. Vaccination of patients with B-cell lymphoma using autologous antigen-pulsed dendritic cells. Nat Med 1996;2:52-8.
18. Porgador A, Snyder D and Gilboa E. Induction of antitumor immunity using bone marrow-generated dendritic cells. J Immunol 1996;156:2918-26.
19. Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, Dummer R et al. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med 1998;4:328-32.
20. Thurner B, Haendle I, Roder C, Dieckmann D, Keikavoussi P, Jonuleit H et al. Vaccination with mage-3A1 peptide-pulsed mature, monocyte-derived dendritic cells expands specific cytotoxic T cells and induces regression of some metastases in advanced stage IV melanoma. J Exp Med 1999;190:1669-78.
21. Jonuleit H, Giesecke-Tuettenberg A, Tuting T, Thumer-Schuler B, Stuge TB, Paragnik L et al. A comparison of two types of dendritic cell as adjuvants for the induction of melanoma-specific T-cell responses in humans following intranodal injection. Int J Cancer 2001;93:243-51.
22. Jaksits S, Kriehuber E, Charbonnier AS, Rappersberger K, Stingl G, Maurer D. CD34+ cell-derived CD14+ precursor cells develop into Langerhans cells in a TGF-beta 1-dependent manner. J Immunol 1999;163:4869-77.
23. Larregina AT, Morelli AE, Spencer LA, Logar AJ, Watkins SC, Thomson AW et al. Dermal-resident CD14+ cells differentiate into Langerhans cells. Nat Immunol 2001;2:1151-8.
24. Valladeau J, Saeland S. Cutaneous dendritic cells. Semin Immunol 2005;17:273-83.
25. Wollenberg A, Wagner M, Gunther S, Towarowski A, Tuma E, Moderer M et al. Plasmacytoid dendritic cells: a new cutaneous dendritic cell subset with distinct role in inflammatory skin diseases. J Invest Dermatol 2002;119:1096-102.
26. Jonuleit H, Kuhn U, Muller G, Steinbrink K, Paragnik L, Schmitt E et al. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997;27:3135-42.
27. de Vries IJ, Lesterhuis WJ, Scharenborg NM, Engelen LP, Ruiter DJ, Gerritsen MJ et al. Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients. Clin Cancer Res 2003;9:5091-100.
28. Dhodapkar MV, Krasovsky J, Steinman RM, Bhardwaj N. Mature dendritic cells boost functionally superior CD8(+) T-cell in humans without foreign helper epitopes. J Clin Invest 2000;105:R9-R14.
29. Mackensen A, Herbst B, Chen JL, Kohler G, Noppen C, Herr W et al. Phase I study in melanoma patients of a vaccine with peptide-pulsed dendritic cells generated in vitro from CD34(+) hematopoietic progenitor cells. Int J Cancer 2000;86:385-92.
30. Schuler-Thurner B, Schultz ES, Berger TG, Weinlich G, Ebner S, Woerl P et al. Rapid induction of tumor-specific type 1T helper cells in metastatic melanoma patients by vaccination with mature, cryopreserved, peptide-loaded monocyte-derived dendritic cells. J Exp Med 2002;195:1279-88.
31. Banchereau J, Palucka AK, Dhodapkar M, Burkeholder S, Taquet N Rolland A et al. Immune and clinical responses in patients with metastatic melanoma to CD34(+) progenitor-derived dendritic cell vaccine. Cancer Res 2001;61:6451-8.
32. Rosenberg SA, Sherry RM, Morton KE, Scharfman WJ, Yang JC, Topalian SL et al. Tumor progression can occur despite the induction of very high levels of self/tumor antigen-specific CD8+ T cells in patients with melanoma. J Immunol 2005;175:6169-76.
33. Tuettenberg A, Becker C, Huter E, Knop J, Enk AH and Jonuleit H. Induction of strong and persistent MelanA/MART-1-specific immune responses by adjuvant dendritic cell-based vaccination of stage II melanoma patients. Int J Cancer 2006;118:2617-27.
34. Engelhard VH, Bullock TN, Colella TA, Sheasley SL, Mullins DW. Antigens derived from melanocyte differentiation proteins: self-tolerance, autoimmunity, and use for cancer immunotherapy. Immunol Rev 2002;188:136-46.
35. Gallimore A, Sakaguchi S. Regulation of tumour immunity by CD25+ T cells. Immunology 2002;107:5-9.
36. Antony PA, Piccirillo CA, Akpinarli A, Finkelstein SE, Speiss PJ, Surman DR et al. CD8+ T cell immunity against a tumor/self-antigen is augmented by CD4+ T helper cells and hindered by naturally occurring T regulatory cells. J Immunol 2005;174:2591-601.
37. Jager E, Ringhoffer M, Altmannsberger M, Arand M, Karbach J, Jager D et al. Immunoselection in vivo: independent loss of MHC class I and melanocyte differentiation antigen expression in metastatic melanoma. Int J Cancer 1997;71:142-7.
38. Propper DJ, Chao D, Braybrooke JP, Bahl P, Thavasu P, Balkwill F et al. Low-dose IFN-gamma induces tumor MHC expression in metastatic malignant melanoma. Clin Cancer Res 2003;9:84-92.
39. Kim R, Emi M, Tanabe K, Arihiro K. Tumor-driven evolution of immunosuppressive networks during malignant progression. Cancer Res 2006;66:5527-36.
40. Gorelik L, Prokhorova A, Mokyr MB. Low-dose melphalan-induced shift in the production of a Th2-type cytokine to a Th1-type cytokine in mice bearing a large MOPC-315 tumor. Cancer Immunol Immunother 1994;39:117-26.
41. Weiskirch LM, Bar-Dagan Y, Mokyr MB. Transforming growth factor-beta-mediated down-regulation of antitumor cytotoxicity of spleen cells from MOPC-315 tumor-bearing mice engaged in tumor eradication following low-dose melphalan therapy. Cancer Immunol Immunother 1994;38:215-24.
42. Howard M, O'Garra A, Ishida H, de Waal Malefyt R, de Vries J. Biological properties of interleukin 10. J Clin Immunol 1992;12:239-47.
43. Enk AH, Saloga J, Becker D, Mohamadzadeh M, Knop J. Induction of hapten-specific tolerance by interleukin 10 in vivo. J Exp Med 1994;179:1397-402.
44. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/TL-12 synthesis in accessory cells. J Exp Med 1993;178:1041-8.
45. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10(IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991;174:1209-20.
46. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J Immunol 1991; 147:3815-22.
47. Fiorentino DF, Zlotnik A, Vieira P, Mosmann TR, Howard M, Moore KW et al. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 1991;146:3444-51.
48. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997;389:737-42.
49. Cong Y, Weaver CT, Lazenby A, Elson CO. Bacterial-reactive T regulatory cells inhibit pathogenic immune responses to the enteric flora. J Immunol 2002;169:6112-9.
50. Cottrez F, Hurst SD, Coffman RL, Groux H. T regulatory cells 1 inhibit a Th2-specific response in vivo. J Immunol 2000;165:4848-53.
51. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001;2:725-31.
52. Curiel TJ, Wei S, Dong H, Alvarez X, Cheng P, Mottram P et al. Blockade of B7-H1 improves myeloid dendritic cell-mediated antitumor immunity. Nat Med 2003;9:562-7.
53. Wakkach A, Fournier N, Brun V, Breittmayer JP, Cottrez F, Groux H. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 2003;18:605-17.
54. Wang L, Goillot E, Tepper RI. IL-10 inhibits alloreactive cytotoxic T lymphocyte generation in vivo. Cell Immunol 1994;159:152-69.
55. Beissert S, Hosoi J, Grabbe S, Asahina A, Granstein RD. IL-10 inhibits tumor antigen presentation by epidermal antigen-presenting cells. J Immunol 1995;154:1280-6.
56. Kurte M, Lopez M, Aguirre A, Escobar A, Aguillon JC, Charo J et al. A synthetic peptide homologous to functional domain of human IL-10 down-regulates expression of MHC class I and Transporter associated with Antigen Processing 1/2 in human melanoma cells. J Immunol 2004;173:1731-7.
57. Chen Q, Daniel V, Maher DW, Hersey P. Production of IL-10 by melanoma cells: examination of its role in immunosuppression mediated by melanoma. Int J Cancer 1994;56:755-60.
58. Kruger-Krasagakes S, Krasagakis K, Garbe C, Diamantstein T. Production of cytokines by human melanoma cells and melanocytes. Recent results in cancer research Fortschritte der Krebsforschung 1995;139:155-68.
59. Lattime EC, Mastrangelo MJ, Bagasra O, Li W, Berd D. Expression of cytokine mRNA in human melanoma tissues. Cancer Immunol Immunother 1995;41:151-6.
60. Enk AH, Jonuleit H, Saloga J, Knop J. Dendritic cells as mediators of tumor-induced tolerance in metastatic melanoma. Int J Cancer 1997;73:309-16.
61. Attia P, Maker AV, Haworth LR, Rogers-Freezer L, Rosenberg SA. Inability of a fusion protein of IL-2 and diphtheria toxin (Denileukin Diftitox, DAB389IL-2, ONTAK) to eliminate regulatory T lymphocytes in patients with melanoma. J Immunother (1997) 2005;28:582-92.
62. Schendel DJ, Falk CS, Nossner E, Maget B, Kressenstein S, Urlinger S et al. Gene transfer of human interferon gamma complementary DNA into a renal cell carcinoma line enhances MHC-restricted cytotoxic T lymphocyte recognition but suppresses non-MHC-restricted effector cell activity. Gene Ther 2000;7:950-9.
63. Meazza R, Comes A, Orengo AM, Ferrini S, Accolla RS. Tumor rejection by gene transfer of the MHC class II transactivator in murine mammary adenocarcinoma cells. Eur J Immunol 2003;33:1183-92.
64. George TC, Bilsborough J, Viney JL, Norment AM. High antigen dose and activated dendritic cells enable Th cells to escape regulatory T cell-mediated suppression in vitro. Eur J Immunol 2003;33:502-11.
65. Pasare C, Medzhitov R. Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science New York, NY 2003;299:1033-6.
66. Cyster JG. Leukocyte migration: scent of the T zone. Curr Biol 2000;10:R30-3.
67. Kirk CJ, Hartigan-O'Connor D, Nickoloff BJ, Chamberlain JS, Giedlin M, Aukerman L et al. T cell-dependent antitumor immunity mediated by secondary lymphoid tissue chemokine: augmentation of dendritic cell-based immunotherapy. Cancer Res 2001;61:2062-70.
68. Sharma S, Stolina M, Luo J, Strieter RM, Burdick M, Zhu LX et al. Secondary lymphoid tissue chemokine mediates T cell-dependent antitumor responses in vivo. J Immunol 2000;164:4558-63.
69. Hisada M, Yoshimoto T, Kamiya S, Magami Y, Miyaji H, Yoneto T et al. Synergistic antitumor effect by coexpression of chemokine CCL21/SLC and costimulatory molecule LIGHT. Cancer Gene Ther 2004;11:280-8.
70. Novak L, Igoucheva O, Cho S, Alexeev V. Characterization of the CCL21-mediated melanoma-specific immune responses and in situ melanoma eradication. Mol Cancer Ther 2007;6:1755-64.
71. Dudley ME, Rosenberg SA. Adoptive-cell-transfer therapy for the treatment of patients with cancer. Nature Rev 2003;3:666-75.
72. Dudley ME, Wunderlich JR, Shelton TE, Even J, Rosenberg SA. Generation of tumor-infiltrating lymphocyte cultures for use in adoptive transfer therapy for melanoma patients. J Immunother 2003;26:332-42.
73. Klebanoff CA, Gattinoni L, Torabi-Parizi R Kerstann K, Cardones AR, Finkelstein SE et al. Central memory self/tumor-reactive CDS+ T cells confer superior antitumor immunity compared with effector memory T cells. Proc Natl Acad Sci U S A 2005; 102:9571-6.
74. Barth RJ Jr., Mule JJ, Spiess PJ, Rosenberg SA. Interferon gamma and tumor necrosis factor have a role in tumor regressions mediated by murine CD8+ tumor-infiltrating lymphocytes. J Exp Med 1991;173:647-58.
75. Cameron RB, Spiess PJ, Rosenberg SA. Synergistic antitumor activity of tumor-infiltrating lymphocytes, interleukin 2, and local tumor irradiation. Studies on the mechanism of action. The J Exp Med 1990;171:249-63.
76. Cheever MA, Greenberg PD, Fefer A, Gillis S. Augmentation of the anti-tumor therapeutic efficacy of long-term cultured T lymphocytes by in vivo administration of purified interleukin 2. J Exp Med 1982;155:968-80.
77. Rosenberg SA, Spiess P, Lafreniere R. A new approach to the adoptive immunotherapy of cancer with tumor-infiltrating lymphocytes. Science New York, NY 1986;233:1318-21.
78. Itoh K, Tilden AB, Balch CM. Interleukin 2 activation of cytotoxic T-lymphocytes infiltrating into human metastatic melanomas. Cancer Res 1986;46:3011-7.
79. Topalian SL, Solomon D, Rosenberg SA. Tumor-specific cytolysis by lymphocytes infiltrating human melanomas. J Immunol 1989;142:3714-25.
80. Yannelli JR, Hyatt C, McConnell S, Hines K, Jacknin L, Parker L et al. Growth of tumor-infiltrating lymphocytes from human solid cancers: summary of a 5-year experience. Int J Cancer 1996;65:413-21.
81. Rosenberg SA, Yannelli JR, Yang JC, Topalian SL, Schwartzentruber DJ, Weber JS et al. Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2. J Natl Cancer Inst 1994;86:1159-66.
82. Liu S, Riley J, Rosenberg S, Parkhurst M. Comparison of common gamma-chain cytokines, interleukin-2, interleukin-7, and interleukin-15 for the in vitro generation of human tumor-reactive T lymphocytes for adoptive cell transfer therapy. J Immunother 2006;29:284-93.
83. Johnson LA, Heemskerk B, Powell DJ, Jr., Cohen CJ, Morgan RA, Dudley ME et al. Gene transfer of tumor-reactive TCR confers both high avidity and tumor reactivity to nonreactive peripheral blood mononuclear cells and tumor-infiltrating lymphocytes. J Immunol 2006;177:6548-59.
84. Shedlock DJ, Shen H. Requirement for CD4 T cell help in generating functional CD8 T cell memory. Science New York, NY 2003;300:337-9.
85. Wherry EJ, Teichgraber V, Becker TC, Masopust D, Kaech SM, Antia R et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003;4:225-34.
86. Castiglioni P, Gerloni M, Zanetti M. Genetically programmed B lymphocytes are highly efficient in inducing anti-virus protective immunity mediated by central memory CD8T cells. Vaccine 2004;23:699-708.
87. Vaccari M, Trindade CJ, Venzon D, Zanetti M, Franchini G. Vaccine-induced CD8+ central memory T cells in protection from simian AIDS. J Immunol 2005;175:3502-7.
88. Nauts HC, Fowler GA, Bogatko FH. A review of the influence of bacterial infection and of bacterial products (Coley's toxins) on malignant tumors in man; a critical analysis of 30 inoperable cases treated by Coley's mixed toxins, in which diagnosis was confirmed by microscopic examination selected for special study. Acta Med Scand Suppl 1953;276:1-103.
89. Halpern BN, Biozzi G, Stiffel C, Mouton D. Inhibition of tumour growth by administration of killed corynebacterium parvum. Nature 1966;212:853-4.
90. Key ME, Hanna MG, Jr. Mechanism of action of BCG-tumor cell vaccines in the generation of systemic tumor immunity. II. Influence of the local inflammatory response on immune reactivity. J Natl Cancer Inst 1981;67:863-9.
91. Eilber FR, Townsend CM, Jr., Morton DL. Results of BCG adjuvant immunotherapy for melanoma of the head and neck. Am J Surg 1976;132:476-9.
92. Morton D, Eilber FR, Malmgren RA, Wood WC. Immunological factors which influence response to immunotherapy in malignant melanoma. Surgery 1970;68:158-63; discussion 63-4.
93. Wallack MK, Steplewski Z, Koprowski H, Rosato E, George J, Hulihan B et al. A new approach in specific, active immunotherapy. Cancer 1977;39:560-4.
94. Kaufman HL, Deraffele G, Mitcham J, Moroziewicz D, Cohen SM, Hurst-Wicker KS et al. Targeting the local tumor microenvironment with vaccinia virus expressing B7.1 for the treatment of melanoma. J Clin Invest 2005;115:1903-12.
95. Di Nicola M, Carlo-Stella C, Mortarini R, Baldassari P, Guidetti A, Gallino GF et al. Boosting T cell-mediated immunity to tyrosinase by vaccinia virus-transduced, CD34(+)-derived dendritic cell vaccination: a phase I trial in metastatic melanoma. Clin Cancer Res 2004;10:5381-90.
96. Adamina M, Weber WP, Rosenthal R, Schumacher R, Zajac P, Guller U et al. Heterologous prime-boost immunotherapy of melanoma patients with Influenza virosomes, and recombinant Vaccinia virus encoding 5 melanoma epitopes and 3 co-stimulatory molecules. A multi-centre phase I/II open labeled clinical trial. Contemp Clin Trials 2008;29:165-81.
97. Ulmer JB, Donnelly JJ, Parker SE, Rhodes GH, Feigner PL, Dwarki VJ et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science New York, NY 1993;259:1745-9.
98. Alexeev V, Uitto J. DNA pharmaceuticals for skin diseases. In: Schleff M. DNA pharmaceuticals: formulation and delivery in gene therapy, DNA vaccination and immunotherapy. Verlag: Wiley-VCH; 2005. pp. 173-87.
99. Peachman KK, Rao M, Alving CR. Immunization with DNA through the skin. Methods San Diego, CA 2003;31:232-42.
100. Bergman PJ, McKnight J, Novosad A, Charney S, Farrelly J, Craft D et al. Long-term survival of dogs with advanced malignant melanoma after DNA vaccination with xenogeneic human tyrosinase: a phase I trial. Clin Cancer Res 2003;9:1284-90.
101. Liao JC, Gregor P, Wolchok JD, Orlandi F, Craft D, Leung C et al. Vaccination with human tyrosinase DNA induces antibody responses in dogs with advanced melanoma. Cancer Immun 2006;6:8.
102. Pavlenko M, Roos AK, Lundqvist A, Palmborg A, Miller AM, Ozenci V et al. A phase I trial of DNA vaccination with a plasmid expressing prostate-specific antigen in patients with hormone-refractory prostate cancer. Br J Cancer 2004;91:688-94.
103. Kang TH, Lee JH, Song CK, Han HD, Shin BC, Pai SI et al. Epigallocatechin-3-gallate enhances CD8+ T cell-mediated antitumor immunity induced by DNA vaccination. Cancer Res 2007;67:802-11.
104. Nchinda G, Kuroiwa J, Oks M, Trumpfheller C, Park CG, Huang Y et al. The efficacy of DNA vaccination is enhanced in mice by targeting the encoded protein to dendritic cells. J Clin Invest 2008;118:1427-36.
105. Peng X, Treml J, Paterson Y. Adjuvant properties of listeriolysin O protein in a DNA vaccination strategy. Cancer Immunol Immunother 2007;56:797-806.
106. Shi FF, Gunn GR, Snyder LA, Goletz TJ. Intradermal vaccination of MUC1 transgenic mice with MUC1/IL-18 plasmid DNA suppresses experimental pulmonary metastases. Vaccine 2007;25:3338-46.
107. Tan GH, Li YN, Huang FY, Wang H, Bai RZ, Jang J. Combination of recombinant xenogeneic endoglin DNA and protein vaccination enhances anti-tumor effects. Immunol Invest 2007;36:423-40.
108. Zhang X, Yu C, Zhao J, Fu L, Yi S, Liu S et al. Vaccination with a DNA vaccine based on human PSCA and HSP70 adjuvant enhances the antigen-specific CD8+ T-cell response and inhibits the PSCA+ tumors growth in mice. J Gene Med 2007;9:715-26.