Precision cancer immunotherapy: Optimizing dendritic cell-based strategies to induce tumor antigen-specific t-cell responses against individual patient tumors

Journal of Immunotherapy

Volumn 38, Issue 4, 2015, Pages 155-164

  Osada, Takuya ^a   Nagaoka, Koji ^b   Takahara, Masashi ^b   Yang, Xiao Yi ^a   Liu, Cong Xiao ^a   Guo, Hongtao ^a   Choudhury, Kingshuk Roy ^a   Hobeika, Amy ^a   Hartman, Zachary ^a   Morse, Michael A ^c   Lyerly, H Kim ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b MEDINET Co Ltd   (Japan)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

cancer vaccine; dendritic cell; electroporation; maturation; mRNA

Indexed keywords

AUTOANTIGEN; B7 ANTIGEN; CANCER VACCINE; CARCINOEMBRYONIC ANTIGEN; CD40 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CHEMOKINE RECEPTOR CCR7; DENDRITIC CELL VACCINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 4; MESSENGER RNA; PICIBANIL; PROSTAGLANDIN E2; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; ZOLEDRONIC ACID; BISPHOSPHONIC ACID DERIVATIVE; IMIDAZOLE DERIVATIVE;

ACCURACY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNIZATION; CANCER INHIBITION; CANCER PATIENT; CANCER SIZE; CELL EXPANSION; CELL LYSATE; CELL MATURATION; CELLULAR IMMUNITY; COLON CANCER; CONTROLLED STUDY; DENDRITIC CELL; DRUG POTENCY; ELECTROPORATION; ENZYME LINKED IMMUNOSORBENT ASSAY; GAMMA DELTA T LYMPHOCYTE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IN VITRO STUDY; IN VIVO STUDY; MIXED LYMPHOCYTE REACTION; MOUSE; NONHUMAN; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE; TUMOR IMMUNITY; ADOPTIVE IMMUNOTHERAPY; ANIMAL; C57BL MOUSE; CANCER TRANSPLANTATION; CELL DIFFERENTIATION; CELL PROLIFERATION; DRUG COMBINATION; HCT116 CELL LINE; IMMUNOLOGY; NEOPLASMS; PERSONALIZED MEDICINE; PROCEDURES; TRANSPLANTATION;

ANIMALS; ANTIGEN PRESENTATION; CANCER VACCINES; CARCINOEMBRYONIC ANTIGEN; CELL DIFFERENTIATION; CELL PROLIFERATION; DENDRITIC CELLS; DINOPROSTONE; DIPHOSPHONATES; DRUG THERAPY, COMBINATION; HCT116 CELLS; HUMANS; IMIDAZOLES; IMMUNOTHERAPY, ADOPTIVE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; NEOPLASMS; PICIBANIL; PRECISION MEDICINE; T-LYMPHOCYTES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84928468391     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0000000000000075     Document Type: Article

References (40)

1. Banchereau J, Steinman R. Dendritic cells and the control of immunity. Nature. 1998; 392: 245-252.
2. Mueller D, Jenkins M, Schwartz R. Clonal expansion versus functional clonal inactivation: a costimulatory signaling pathway determines the outcome of T cell antigen receptor capacity. Annu Rev Immunol. 1989; 7: 445-480.
3. Liu Y, Linsley P. Costimulation of T cell growth. Curr Opin Immunol. 1992; 4: 265-270.
4. Larsen CP1, Ritchie SC, Hendrix R, et al. Regulation of immunostimulatory function and costimulatory molecule (B7-1 and B7-2) expression on murine dendritic cells. J Immunol. 1994; 152: 5208-5219.
5. Maecker HT, Auffermann-Gretzinger S, Nomura LE, et al. Detection of CD4 T-cell responses to a tumor vaccine by cytokine flow cytometry. Clin Cancer Res. 2001; 7(suppl): 902s-908s.
6. Li Y, Bendandi M, Deng Y, et al. Tumor-specific recognition of human myeloma cells by idiotype induced CD8(+) T cells. Blood. 2000; 96: 2828-2833.
7. Morse MA, Niedzwiecki D, Marshall JL, et al. A randomized phase II study of immunization with dendritic cells modified with poxvectors encoding CEA and MUC1 compared with the same poxvectors plus GM-CSF for resected metastatic colorectal cancer. Ann Surg. 2013; 258: 879-886.
8. Nair SK, Morse M, Boczkowski D, et al. Induction of tumorspecific cytotoxic T lymphocytes in cancer patients by autologous tumor RNA-transfected dendritic cells. Ann Surg. 2002; 235: 540-549.
9. Alfaro C, Perez-Gracia JL, Suarez N, et al. Pilot clinical trial of type 1 dendritic cells loaded with autologous tumor lysates combined with GM-CSF, pegylated IFN, and cyclophosphamide for metastatic cancer patients. J Immunol. 2011; 187: 6130-6142.
10. Wolfraim LA, Takahara M, Viley AM, et al. Clinical scale electroloading of mature dendritic cells with melanoma whole tumor cell lysate is superior to conventional lysate co-incubation in triggering robust in vitro expansion of functional antigenspecific CTL. Int Immunopharmacol. 2013; 15: 488-497.
11. Kyte JA, Mu L, Aamdal S, et al. Phase I/II trial of melanoma therapy with dendritic cells transfected with autologous tumormRNA. Cancer Gene Ther. 2006; 13: 905-918.
12. Wilgenhof S, Van Nuffel AM, Corthals J, et al. Therapeutic vaccination with an autologous mRNA electroporated dendritic cell vaccine in patients with advanced melanoma. J Immunother. 2011; 34: 448-456.
13. Sousa-Canavez JM, Canavez FC, Leite KR, et al. Therapeutic dendritic cell vaccine preparation using tumor RNA transfection: a promising approach for the treatment of prostate cancer. Genet Vaccines Ther. 2008; 6: 2.
14. Ponsaerts P, Van den Bosch G, Cools N, et al. Messenger RNA electroporation of human monocytes, followed by rapid in vitro differentiation, leads to highly stimulatory antigenloaded mature dendritic cells. J Immunol. 2002; 169: 1669-1675.
15. Ferlazzo G, Semino C, Melioli G. HLA class I molecule expression is upregulated during maturation of dendritic cells, protecting them from natural killer cell-mediated lysis. Immunol Lett. 2001; 76: 37-41.
16. MacAry PA, Lindsay M, Scott MA, et al. Mobilization of MHC class Imolecules from late endosomes to the cell surface following activation of CD34-derived human Langerhans cells. Proc Natl Acad Sci USA. 2001; 98: 3982-3987.
17. Townsend SE, Allison JP. Tumor rejection after direct costimulation of CD8+ T cells by B7-transfected melanoma cells. Science. 1993; 259: 368-370.
18. Inaba K, Witmer-Pack M, Inaba M, et al. The tissue distribution of the B7-2 costimulator in mice: abundant expression on dendritic cells in situ and during maturation in vitro. J Exp Med. 1994; 180: 1849-1860.
19. Jonuleit H, Kuhn U, Muller G, 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: 3135-3142.
20. Itoh T, Ueda Y, Okugawa K, et al. Streptococcal preparation OK432 promotes functional maturation of human monocytederived dendritic cells. Cancer Immunol Immunother. 2003; 52: 207-214.
21. Nakahara S, Tsunoda T, Baba T, et al. Dendritic cells stimulated with a bacterial product, OK-432, efficiently induce cytotoxic T lymphocytes specific to tumor rejection peptide. Cancer Res. 2003; 63: 4112-4118.
22. Chen YJ, Chao KS, Yang YC, et al. Zoledronic acid, an aminobisphosphonate, modulates differentiation and maturation of human dendritic cells. Immunopharmacol Immunotoxicol. 2009; 31: 499-508.
23. Kitawaki T, Kadowaki N, Fukunaga K, et al. A phase I/IIa clinical trial of immunotherapy for elderly patients with acute myeloid leukaemia using dendritic cells co-pulsed with WT1 peptide and zoledronate. Br J Haematol. 2011; 153: 796-799.
24. Fiore F, Castella B, Nuschak B, et al. Enhanced ability of dendritic cells to stimulate innate and adaptive immunity on short-term incubation with zoledronic acid. Blood. 2007; 110: 921-927.
25. Lutz MB, Kukutsch N, Ogilvie AL, et al. An advanced culture method for generating large quantities of highly pure dendritic cells from mouse bone marrow. J Immunol Methods. 1999; 223: 77-92.
26. Skipper H, Schabel F. Quantitative and cytokinetic studies in experimental tumor systems. In: Holland J, Frei E, eds. Cancer Medicine. Philadelphia, PA: Lea and Febiger; 1982: 636-648.
27. Takahara M, Miyai M, Tomiyama M, et al. Copulsing tumor antigen-pulsed dendritic cells with zoledronate efficiently enhance the expansion of tumor antigen-specific CD8+ T cells via Vg9 gdT cell activation. J Leukocyte Biol. 2008; 83: 742-754.
28. Ponsaerts P, Van Tendeloo VFI, Berneman ZN. Cancer immunotherapy using RNA-loaded dendritic cells. Clin Exp Immunol. 2003; 134: 378-384.
29. Gilboa E, Vieweg J. Cancer immunotherapy with mRNAtransfected dendritic cells. Immunol Rev. 2004; 199: 251-263.
30. Heiser A, Coleman D, Dannull J, et al. Autologous dendritic cells transfected with prostate-specific antigen RNA stimulate CTL responses against metastatic prostate tumors. J Clin Invest. 2002; 109: 409-417.
31. Boczkowski D, Nair SK, Snyder D, et al. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med. 1996; 184: 465-472.
32. Zheng L, Huang XL, Fan Z, et al. Delivery of liposomeencapsulated HIV type 1 proteins to human dendritic cells for stimulation of HIV type 1-specific memory cytotoxic T lymphocyte responses. AIDS Res Hum Retroviruses. 1999; 15: 1011-1020.
33. Lu D, Benjamin R, Kim M, et al. Optimization of methods to achieve mRNA-mediated transfection of tumor cells in vitro and in vivo employing cationic liposome vectors. Cancer Gene Ther. 1994; 1: 245-252.
34. Van Tendeloo V, Ponsaerts P, Lardon F, et al. Highly efficient gene delivery by mRNA electroporation in human hematopoietic cells: superiority to lipofection and passive pulsing of mRNA and to electroporation of plasmid cDNA for tumor antigen loading of dendritic cells. Blood. 2001; 98: 49-56.
35. Van Tendeloo VF, Van de Velde A, Van Driessche A, et al. Induction of complete and molecular remissions in acute myeloid leukemia by Wilms' tumor 1 antigen-targeted dendritic cell vaccination. Proc Natl Acad Sci USA. 2010; 107: 13824-13829.
36. Grunebach F, Muller MR, Brossart P. New developments in dendritic cell-based vaccinations: RNA translated into clinics. Cancer Immunol Immunother. 2005; 54: 517-525.
37. Rosenberg SA, Sherry RM, Morton KE, 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: 6169-6176.
38. Zajac AJ, Blattman JN, Murali-Krishna K, et al. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med. 1998; 188: 2205-2213.
39. Toes RE, Ossendorp F, Offringa R, et al. CD4 T cells and their role in antitumor immune responses. J Exp Med. 1999; 189: 753-756.
40. Prins RM, Wang X, Soto H, et al. Comparison of gliomaassociated antigen peptide-loaded versus autologous tumor lysate-loaded dendritic cell vaccination in malignant glioma patients. J Immunother. 2013; 36: 152-157.