Tumor-associated antigen/IL-21-transduced dendritic cell vaccines enhance immunity and inhibit immunosuppressive cells in metastatic melanoma

Gene Therapy

Volumn 21, Issue 5, 2014, Pages 457-467

  Aravindaram, K ^a   Wang, P H ^a   Yin, S Y ^b   Yang, N S ^b  

^a NATIONAL BUREAU OF PLANT GENETIC RESOURCES   (India)

^b AGRICULTURAL BIOTECHNOLOGY RESEARCH CENTER   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTINEOPLASTIC AGENT; DENDRITIC CELL HGP100 MIL 21 VACCINE; DENDRITIC CELL HGP100 VACCINE; DENDRITIC CELL MIL 21 VACCINE; DENDRITIC CELL VACCINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; CANCER VACCINE; INTERLEUKIN 21; INTERLEUKIN DERIVATIVE; RECOMBINANT VACCINE; TUMOR ANTIGEN;

ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER INHIBITION; CELL ENGINEERING; DENDRITIC CELL; DRUG MECHANISM; GENE EXPRESSION; IMMUNE RESPONSE; IMMUNITY; IMMUNOCOMPETENT CELL; IN VIVO STUDY; METASTATIC MELANOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; SURVIVAL RATE; T LYMPHOCYTE; TUMOR XENOGRAFT; ANIMAL; BAGG ALBINO MOUSE; BIOLOGICAL THERAPY; BIOSYNTHESIS; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; FEMALE; GENETICS; IMMUNOLOGY; LYMPHOCYTE DEPLETION; MELANOMA, EXPERIMENTAL; METASTASIS; MORTALITY; NATURAL KILLER CELL; REGULATORY T LYMPHOCYTE; TRANSPLANTATION;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CELL PROLIFERATION; CELL- AND TISSUE-BASED THERAPY; DENDRITIC CELLS; FEMALE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; INTERFERON-GAMMA; INTERLEUKINS; KILLER CELLS, NATURAL; LYMPHOCYTE DEPLETION; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; NEOPLASM METASTASIS; SURVIVAL RATE; T-LYMPHOCYTES, CYTOTOXIC; T-LYMPHOCYTES, REGULATORY; TUMOR NECROSIS FACTOR-ALPHA; VACCINES, SYNTHETIC;

EID: 84900032004     PISSN: 09697128     EISSN: 14765462     Source Type: Journal    
DOI: 10.1038/gt.2014.12     Document Type: Article

References (48)

1. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998; 392: 245-252.
2. Banchereau J, Ueno H, Dhodapkar M, Connolly J, Finholt JP, Klechevsky E et al. Immune and clinical outcomes in patients with stage IV melanoma vaccinated with peptide-pulsed dendritic cells derived from CD34+ progenitors and activated with type I interferon. J Immunother 2005; 28: 505-516.
3. Wang B, Zaidi N, He LZ, Zhang L, Kuroiwa JM, Keler T et al. Targeting of the nonmutated tumor antigen HER2/neu to mature dendritic cells induces an integrated immune response that protects against breast cancer in mice. Breast Cancer Res 2012; 14: R39.
4. Huang J, Zhang SN, Choi KJ, Choi IK, Kim JH, Lee M et al. Therapeutic and tumor-specific immunity induced by combination of dendritic cells and oncolytic adenovirus expressing IL-12 and 4-1BBL. Mol Ther 2009; 18: 264-274.
5. Lesterhuis W, de Vries IJ, Schuurhuis DH, Boullart AC, Jacobs JF, de Boer AJ et al. Vaccination of colorectal cancer patients with CEA-loaded dendritic cells: antigenspecific T cell responses in DTH skin tests. Ann Oncol 2006; 17: 974-980.
6. Brower V. Approval of provenge seen as first step for cancer treatment vaccines. J Natl Cancer Inst 2010; 102: 1108-1110.
7. Behboudi SMA, Gilbert SC, Nicoll CL, Hill AVS. Dendritic cells infected by recombinant modified vaccinia virus Ankara retain immunogenicity in vivo despite in vitro dysfunction. Vaccine 2004; 22: 4326-4331.
8. Kastenmuller W, Drexler I, Ludwig H, Erfle V, Peschel C, Bernhard H et al. Infection of human dendritic cells with recombinant vaccinia virus MVA reveals general persistence of viral early transcription but distinct maturation-dependent cytopathogenicity. Virology 2006; 350: 276-288.
9. Mossoba M, Walia JS, Rasaiah VI, Buxhoeveden N, Head R, Ying C et al. Tumor protection following vaccination with low doses of lentivirally transduced DCs expressing the self antigen erbB2. Mol Ther 2008; 16: 607-617.
10. Nabekura T, Otsu M, Nagasawa T, Nakauchi H, Onodera M. Potent vaccine therapy with dendritic cells genetically modified by the gene-silencing- resistant retroviral vector GCDNsap. Mol Ther 2006; 13: 301-309.
11. Van Tendeloo V, Snoeck HW, Lardon F, Vanham GLEE, Nijs G, Lenjou M et al. Nonviral transfection of distinct types of human dendritic cells: high-efficiency gene transfer by electrophoration into hematopoietic progenitor-but not monocyte-derived dendritic cells. Gene Ther 1998; 5: 700-707.
12. Yoshikawa T, Niwa T, Mizuguchi H, Okada N, Nakagawa S. Engineering of highly immunogenic long-lived DC vaccines by antiapoptotic protein gene transfer to enhance cancer vaccine potency. Gene Ther 2008; 15: 1321-1329.
13. Aravindaram K, Yu HH, Lan CW, Wang PH, Chen YH, Chen HM et al. Transgenic expression of human gp100 and RANTES at specific time points for suppression of melanoma. Gene Ther 2009; 16: 1329-1339.
14. Smith C, Dunbar PR, Mirza F, Palmowski MJ, Shepherd D, Gilbert SC et al. Recombinant modified vaccinia Ankara primes functionally activated CTL specific for a melanoma tumor antigen epitope in melanoma patients with a high risk of disease recurrence. Int J Cancer 2005; 113: 259-266.
15. Di Nicola M, Carlo-Stella C, Anichini A, Mortarini R, Guidetti A, Tragni G et al. Clinical protocol. Immunization of patients with malignant melanoma with autologous CD34(+) cell-derived dendritic cells transduced ex vivo with a recombinant replication-deficient vaccinia vector encoding the human tyrosinase gene: a phase I trial. Hum Gene Ther 2003; 14: 1347-1360.
16. 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: 5381-5390.
17. Schuurhuis D, Verdijk P, Schreibelt G, Aarntzen EHJG, Scharenborg N, de Boer A et al. In situ expression of tumor antigens by mRNA electroporated dendritic cells in lymph nodes of melanoma patients. Cancer Res 2009; 69: 2927-2934.
18. Neal Z, Bates MK, Albertini MR, Herweijer H. Hydrodynamic limb vein delivery of a xenogeneic DNA cancer vaccine effectively induces antitumor immunity. Mol Ther 2007; 15: 422-430.
19. Perricone M, Claussen KA, Smith KA, Kaplan JM, Piraino S, Shankara S et al. Immuno gene therapy for murine melanoma using recombinant adenoviral vectors expressing melanoma associated antigens. Mol Ther 2000; 1: 275-284.
20. Wan Y, Emtage P, Zhu Q, Foley R, Pilon A, Roberts B et al. Enhanced immune response to the melanoma antigen gp100 using recombinant adenovirustransduced dendritic cells. Cell Immunol 1999; 198: 131-138.
21. Zhai Y, Yang JC, Spiess P, Nishimura MI, Overwijk WW, Roberts B et al. Cloning and characterization of the genes encoding the murine homologues of the human melanoma antigens MART1 and gp100. J Immunother 1997; 20: 15-25.
22. Chaput N D, Bergot A-S, Cordier C, Ngo-Abdalla S, Klatzmann D. Regulatory T cells prevent CD8 T cell maturation by inhibiting CD4 Th cells at tumor sites. J Immunol 2007; 179: 4969-4978.
23. Schulze S, Kim HS, Fan Q, Kim DW, Kaufman HL. Local IL-21 promotes the therapeutic activity of effector T cells by decreasing regulatory T cells within the tumor microenvironment. Mol Ther 2009; 17: 380-388.
24. Rakhmilevich A, Imboden M, Hao Z, Macklin MD, Roberts T, Wright KM et al. Effective particle-Mediated vaccination against mouse melanoma by coadministration of plasmid DNA encoding gp100 and granulocyte-Macrophage colonystimulating factor. Clin Can Res 2001; 7: 952-961.
25. Trevor K, Hersh EM, Brailey J, Balloul JM, Acres B. Transduction of human dendritic cells with a recombinant modified vaccinia ankara virus encoding MUC1 and IL2. Cancer Immunol Immunother 2001; 50: 397-407.
26. Szabo S, Kim ST, Costa GL, Zhang X, Fathman CG, Glimcher LH. A novel transcription factor, T-bet directs Th1 lineage commitment. Cell 2000; 100: 655-669.
27. Gabrilovich DaN S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 2009; 9: 162-174.
28. Shevach E. Mechanisms of Foxp3+ T regulatory cell-Mediated suppression. Immunity 2009; 30: 636-645.
29. Yang Z, Zang B, Li D, Lv M, Huang C, Shen GX et al. Mast cells mobilize myeloidderived suppressor cells and Treg cells in tumor microenvironment via IL-17 pathway in murine hepatocarcinoma model. PLoS One 2010; 5: 1-9.
30. Tatsumi T, Gambotto A, Robbins PD, Storkus WJ. Interleukin 18 gene transfer expands the repertoire of antitumor Th1-type immunity elicited by dendritic cell-based vaccines in association with enhanced therapeutic efficacy. Cancer Res 2002; 62: 5853-5858.
31. Yang S, Vervaert CE, Burch J, Grichnik J, Seigler HF, Darrow TL. Murine dendritic cells transfected with human gp100 elicit both antigen specific CD8+ and CD4+ T-cell responses and are more effective than DNA vaccines at generating antitumor immunity. Int J Cancer 1999; 83: 532-540.
32. Li YaY C. IL-21 mediated Foxp3 suppression leads to enhanced generation of antigen-specific CD8+ cytotoxic T lymphocytes. Blood 2008; 111: 229-235.
33. Kowalczyk A, Wierzbicki A, Gil M, Bambach B, Kaneko Y, Rokita H. Induction of protective immune responses against NXS2 neuroblastoma challenge in mice by immunotherapy with GD2 mimotope vaccine and IL-15 and IL-21 gene delivery. Cancer Immunol Immunother 2007; 56: 1443-1458.
34. Brandt K B, Foster DC, Rckert R. Interleukin-21 inhibits dendritic cell activation and maturation. Blood 2003; 102: 4090-4098.
35. Tao RLL, Huang W, Zheng L. Activation of human dendritic cells by recombinant modified vaccinia virus Ankara vectors encoding Survivin and IL-2 genes in vitro. Hum Gene Ther 2010; 98: 98-108.
36. Ma HL, Konz RF, Senices M, Young DA, Grusby MJ, Collins M et al. IL-21 activates both innate and adaptive immunity to generate potent antitumor responses that require perforin but are independent of IFN-?. J Immunol 2003; 171: 608-615.
37. Kaka AS SD, Hartmaier R, Leen AM, Lu A, Bear A, Rooney CM et al. Genetic modification of T cells with IL-21 enhances antigen presentation and generation of central memory tumor-specific cytotoxic T-lymphocytes. J Immunother 2009; 32: 726-736.
38. Zeng R SR, Finkelstein SE, Oh S, Kovanen PE, Hinrichs CS, Pise-Masison CA et al. Synergy of IL-21 and IL-15 in regulating CD8+ T cell expansion and function. J Exp Med 2005; 201: 139-148.
39. Ansn S BM, Berezovskaya A, Murray AP, Stevenson K, Nadler LM, Hirano N. Dissociation of its opposing immunologic effects is critical for the optimization of antitumor CD8+ T-cell responses induced by interleukin 21. Cancer Res 2008; 14: 6125-6136.
40. Spolski R LW. Cytokine mediators of Th17 function. Eur J Immunol 2009; 39: 658-661.
41. Albertini M, Emler CA, Schell K, Tans KJ, King DM, Sheehy MJ. Dual expression of human leukocyte antigen molecules and the B7-1 costimulatory molecule (CD80) on human melanoma cells after particle-Mediated gene transfer. Cancer Gene Ther 1996; 3: 192-201.
42. Wyatt L, Shors ST, Murphy BR, Moss B. Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine 1996; 14: 1451-1458.
43. Earl P, Moss B, Wyatt LS, Carroll MW. Generation of recombinant vaccinia viruses. In: Ausubel FM, Brent R, Kingston RE, Moore DD, Seidmen ZG, Smith ZA, Skuhl LX (eds). Current Protocols in Molecular Biology. John Wiley and Sons: NewYork, NY, USA, 1998, pp 16.17.1-16.19.11.
44. Labeur M, Roters B, Pers B, Mehling A, Luger TA, Schwarz T et al. Generation of tumor immunity by bone marrow-derived dendritic cells correlates with dendritic cell maturation stage. J Immunol 1999; 162: 168-175.
45. Nagerson D, Panelli M, Dudley ME, Finkelstein SE, Rosenberg SA, Marincola FM. Biased epitope selection by recombinant vaccinia-virus (rVV)-infected mature or immature dendritic cells. Gene Ther 2003; 10: 1754-1765.
46. Yin SY, Wang CY, Yang NS. Interleukin-4 enhances trafficking and functional activities of GM-CSF-stimulated mouse myeloid-derived dendritic cells at late differentiation stage. Exp Cell Res 2011; 317: 2210-2221.
47. Loges S, Clausen H, Reichelt U, Bubenheim M, Erbersdobler A, Schurr P et al. Determination of microvessel density by quantitative real-time PCR in esophageal cancer: correlation with histologic methods, angiogenic growth factor expression, and lymph node metastasis. Clin Cancer Res 2007; 13: 76-80.
48. Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A et al. 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res 2010; 70: 3052-3061