Strategies to improve the immunogenicity of anticancer vaccines based on dendritic cell/malignant cell fusions

OncoImmunology

Volumn 2, Issue 9, 2013, Pages

  Koido, Shigeo ^a   Homma, Sadamu ^a   Okamoto, Masato ^b   Namiki, Yoshihisa ^a   Takakura, Kazuki ^a   Uchiyama, Kan ^a   Kajihara, Mikio ^a   Arihiro, Seiji ^a   Imazu, Hiroo ^a   Arakawa, Hiroshi ^a   Kan, Shin ^a   Komita, Hideo ^a   Kamata, Yuko ^a   Ito, Masaki ^a   Ohkusa, Toshifumi ^a   Gong, Jianlin ^c   Tajiri, Hisao ^a  

^a JIKEI UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cytotoxic T lymphocyte; Dendritic cell; Fusion; Immunogenicity; Whole tumor cell

Indexed keywords

CANCER VACCINE; DENDRITIC CELL VACCINE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR AGONIST; TUMOR ANTIGEN;

ADVANCED CANCER; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; CANCER CELL; CANCER CHEMOTHERAPY; CANCER IMMUNOTHERAPY; CANCER PATIENT; CELL COUNT; CELL FUSION; CELL INTERACTION; CELL LYSATE; CELL SPECIFICITY; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DISEASE EXACERBATION; DRUG MECHANISM; DRUG SAFETY; HUMAN; IMMUNOGENICITY; IMMUNOMODULATION; INNATE IMMUNITY; LYMPHOCYTE FUNCTION; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; VACCINE PRODUCTION;

EID: 84890278140     PISSN: 21624011     EISSN: 2162402X     Source Type: Journal    
DOI: 10.4161/onci.25994     Document Type: Review

References (39)

1. Nestle FO, Alijagic S, Gilliet M, Sun Y, Grabbe S, Dummer R, Burg G, Schadendorf D. Vaccination of melanoma patients with peptide- or tumor lysate-pulsed dendritic cells. Nat Med 1998; 4:328- 32; PMID:9500607; http://dx.doi.org/10.1038/ nm0398-328
2. Mackensen A, Herbst B, Chen JL, Köhler G, Noppen C, Herr W, Spagnoli GC, Cerundolo V, Lindemann A. 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; PMID:10760827; ht t p : / / d x . d o i . o r g /10 .10 0 2 / ( S ICI )10 9 7- 0215(20000501)86:3385::AID-IJC133.0.CO;2-T
3. Palucka AK, Ueno H, Connolly J, Kerneis-Norvell F, Blanck JP, Johnston DA, Fay J, Banchereau J. Dendritic cells loaded with killed allogeneic melanoma cells can induce objective clinical responses and MART-1 specific CD8+ T-cell immunity. J Immunother 2006; 29:545-57; PMID:16971810; http://dx.doi. org/10.1097/01.cji.0000211309.90621.8b
4. Nair SK, Boczkowski D, Morse M, Cumming RI, Lyerly HK, Gilboa E. Induction of primary carcinoembryonic antigen (CEA)-specific cytotoxic T lymphocytes in vitro using human dendritic cells transfected with RNA. Nat Biotechnol 1998; 16:364- 9; PMID:9555728; http://dx.doi.org/10.1038/ nbt0498-364
5. Koido S, Kashiwaba M, Chen D, Gendler S, Kufe D, Gong J. Induction of antitumor immunity by vaccination of dendritic cells transfected with MUC1 RNA. J Immunol 2000; 165:5713-9; PMID:11067929
6. Gong J, Chen D, Kashiwaba M, Kufe D. Induction of antitumor activity by immunization with fusions of dendritic and carcinoma cells. Nat Med 1997; 3:558- 61; PMID:9142127; http://dx.doi.org/10.1038/ nm0597-558
7. Koido S, Homma S, Okamoto M, Namiki Y, Takakura K, Uchiyama K, Kajihara M, Arihiro S, Imazu H, Arakawa H, et al. Fusions between dendritic cells and whole tumor cells as anticancer vaccines. Oncoimmunology 2013; 2:e24437; PMID:23762810; http://dx.doi.org/10.4161/ onci.24437
8. Koido S, Hara E, Homma S, Ohkusa T, Gong J, Tajiri H. Cancer immunotherapy by fusions of dendritic cells and tumor cells. Immunotherapy 2009; 1:49-62; PMID:20635973; http://dx.doi. org/10.2217/1750743X.1.1.49
9. Koido S, Hara E, Homma S, Namiki Y, Ohkusa T, Gong J, Tajiri H. Cancer vaccine by fusions of dendritic and cancer cells. Clin Dev Immunol 2009; 2009:1; PMID:20182533; http://dx.doi. org/10.1155/2009/657369
10. Koido S, Ohana M, Liu C, Nikrui N, Durfee J, Lerner A, Gong J. Dendritic cells fused with human cancer cells: morphology, antigen expression, and T cell stimulation. Clin Immunol 2004; 113:261- 9; PMID:15507391; http://dx.doi.org/10.1016/j. clim.2004.08.004
11. Koido S, Gong J. Characterization of structure and direct antigen presentation by dendritic/tumor-fused cells as cancer vaccines. Anticancer Res 2013; 33:347- 54; PMID:23393323
12. Koido S, Tanaka Y, Chen D, Kufe D, Gong J. The kinetics of in vivo priming of CD4 and CD8 T cells by dendritic/tumor fusion cells in MUC1-transgenic mice. J Immunol 2002; 168:2111-7; PMID:11859096
13. Koido S, Homma S, Hara E, Namiki Y, Takahara A, Komita H, Nagasaki E, Ito M, Ohkusa T, Gong J, et al. Regulation of tumor immunity by tumor/dendritic cell fusions. Clin Dev Immunol 2010; 2010:1; PMID:21048993; http://dx.doi. org/10.1155/2010/516768
14. Zheng R, Cohen PA, Paustian CA, Johnson TD, Lee WT, Shu S, Koski GK. Paired Toll-like receptor agonists enhance vaccine therapy through induction of interleukin-12. Cancer Res 2008; 68:4045-9; PMID:18519662; http://dx.doi.org/10.1158/0008- 5472.CAN-07-6669
15. Celis E. Toll-like receptor ligands energize peptide vaccines through multiple paths. Cancer Res 2007; 67:7945-7; PMID:17804699; http://dx.doi. org/10.1158/0008-5472.CAN-07-1652
16. Wang RF. Regulatory T cells and toll-like receptors in cancer therapy. Cancer Res 2006; 66:4987-90; PMID:16707417; http://dx.doi.org/10.1158/0008- 5472.CAN-05-4676
17. Napolitani G, Rinaldi A, Bertoni F, Sallusto F, Lanzavecchia A. Selected Toll-like receptor agonist combinations synergistically trigger a T helper type 1-polarizing program in dendritic cells. Nat Immunol 2005; 6:769-76; PMID:15995707; http://dx.doi. org/10.1038/ni1223
18. Nakazato H, Koike A, Saji S, Ogawa N, Sakamoto J; Study Group of Immunochemotherapy with PSK for Gastric Cancer. Efficacy of immunochemotherapy as adjuvant treatment after curative resection of gastric cancer. Lancet 1994; 343:1122-6; PMID:7910230; http://dx.doi.org/10.1016/S0140-6736(94)90233-X
19. Tanaka N, Gouchi A, Ohara T, Mannami T, Konaga E, Fuchimoto S, Okamura S, Sato K, Orita K; Cooperative Study Group of Preoperative Intratumoral Immunotherapy for Cancer. Intratumoral injection of a streptococcal preparation, OK-432, before surgery for gastric cancer. A randomized trial. Cancer 1994; 74:3097-103; PMID:7982173; http://dx.doi. org/10.1002/1097-0142(19941215)74:123097::AIDCNCR2820741206 3.0.CO;2-P
20. Koido S, Homma S, Okamoto M, Namiki Y, Takakura K, Takahara A, Odahara S, Tsukinaga S, Yukawa T, Mitobe J, et al. Combined TLR2/4- activated dendritic/tumor cell fusions induce augmented cytotoxic T lymphocytes. PLoS One 2013; 8:e59280; PMID:23555011; http://dx.doi. org/10.1371/journal.pone.0059280
21. Ghorpade DS, Kaveri SV, Bayry J, Balaji KN. Cooperative regulation of NOTCH1 proteinphosphatidylinositol 3-kinase (PI3K) signaling by NOD1, NOD2, and TLR2 receptors renders enhanced refractoriness to transforming growth factor-beta (TGF-beta)- or cytotoxic T-lymphocyte antigen 4 (CTLA-4)-mediated impairment of human dendritic cell maturation. J Biol Chem 2011; 286:31347-60; PMID:21768114; http://dx.doi. org/10.1074/jbc.M111.232413
22. Terabe M, Ambrosino E, Takaku S, O'Konek JJ, Venzon D, Lonning S, McPherson JM, Berzofsky JA. Synergistic enhancement of CD8+ T cell-mediated tumor vaccine efficacy by an anti-transforming growth factor-beta monoclonal antibody. Clin Cancer Res 2009; 15:6560-9; PMID:19861451; http://dx.doi.org/10.1158/1078-0432.CCR-09-1066
23. Ueda R, Fujita M, Zhu X, Sasaki K, Kastenhuber ER, Kohanbash G, McDonald HA, Harper J, Lonning S, Okada H. Systemic inhibition of transforming growth factor-beta in glioma-bearing mice improves the therapeutic efficacy of glioma-associated antigen peptide vaccines. Clin Cancer Res 2009; 15:6551-9; PMID:19861464; http://dx.doi.org/10.1158/1078- 0432.CCR-09-1067
24. Conroy H, Galvin KC, Higgins SC, Mills KHG. Gene silencing of TGF-β1 enhances antitumor immunity induced with a dendritic cell vaccine by reducing tumor-associated regulatory T cells. Cancer Immunol Immunother 2012; 61:425-31; PMID:22193988; http://dx.doi.org/10.1007/s00262-011-1188-y
25. Zhang M, Berndt BE, Chen JJ, Kao JY. Expression of a soluble TGF-beta receptor by tumor cells enhances dendritic cell/tumor fusion vaccine efficacy. J Immunol 2008; 181:3690-7; PMID:18714045
26. Koido S, Hara E, Homma S, Mitsunaga M, Takahara A, Nagasaki E, Kawahara H, Watanabe M, Toyama Y, Yanagisawa S, et al. Synergistic induction of antigenspecific CTL by fusions of TLR-stimulated dendritic cells and heat-stressed tumor cells. J Immunol 2007; 179:4874-83; PMID:17878387
27. Koido S, Homma S, Okamoto M, Namiki Y, Takakura K, Takahara A, Odahara S, Tsukinaga S, Yukawa T, Mitobe J, et al. Augmentation of antitumor immunity by fusions of ethanol-treated tumor cells and dendritic cells stimulated via dual TLRs through TGF-β1 blockade and IL-12p70 production. PLoS One 2013; 8:e63498; PMID:23717436; http:// dx.doi.org/10.1371/journal.pone.0063498
28. Georgopoulos C, Welch WJ. Role of the major heat shock proteins as molecular chaperones. Annu Rev Cell Biol 1993; 9:601-34; PMID:8280473; http:// dx.doi.org/10.1146/annurev.cb.09.110193.003125
29. Somersan S, Larsson M, Fonteneau JF, Basu S, Srivastava P, Bhardwaj N. Primary tumor tissue lysates are enriched in heat shock proteins and induce the maturation of human dendritic cells. J Immunol 2001; 167:4844-52; PMID:11673488
30. Obeid M, Tesniere A, Ghiringhelli F, Fimia GM, Apetoh L, Perfettini JL, Castedo M, Mignot G, Panaretakis T, Casares N, et al. Calreticulin exposure dictates the immunogenicity of cancer cell death. Nat Med 2007; 13:54-61; PMID:17187072; http:// dx.doi.org/10.1038/nm1523
31. Bianchi ME, Beltrame M, Paonessa G. Specific recognition of cruciform DNA by nuclear protein HMG1. Science 1989; 243:1056-9; PMID:2922595; http://dx.doi.org/10.1126/science.2922595
32. Apetoh L, Ghiringhelli F, Tesniere A, Obeid M, Ortiz C, Criollo A, Mignot G, Maiuri MC, Ullrich E, Saulnier P, et al. Toll-like receptor 4-dependent contribution of the immune system to anticancer chemotherapy and radiotherapy. Nat Med 2007; 13:1050-9; PMID:17704786; http://dx.doi. org/10.1038/nm1622
33. Gong J, Zhang Y, Durfee J, Weng D, Liu C, Koido S, Song B, Apostolopoulos V, Calderwood SK. A heat shock protein 70-based vaccine with enhanced immunogenicity for clinical use. J Immunol 2010; 184:488-96; PMID:19949080; http://dx.doi. org/10.4049/jimmunol.0902255
34. Koido S, Hara E, Homma S, Torii A, Mitsunaga M, Yanagisawa S, Toyama Y, Kawahara H, Watanabe M, Yoshida S, et al. Streptococcal preparation OK-432 promotes fusion efficiency and enhances induction of antigen-specific CTL by fusions of dendritic cells and colorectal cancer cells. J Immunol 2007; 178:613-22; PMID:17182602
35. Gong J, Apostolopoulos V, Chen D, Chen H, Koido S, Gendler SJ, McKenzie IF, Kufe D. Selection and characterization of MUC1-specific CD8+ T cells from MUC1 transgenic mice immunized with dendritic-carcinoma fusion cells. Immunology 2000; 101:316-24; PMID:11106934; http://dx.doi. org/10.1046/j.1365-2567.2000.00101.x
36. Brahmer JR, Tykodi SS, Chow LQ, Hwu WJ, Topalian SL, Hwu P, Drake CG, Camacho LH, Kauh J, Odunsi K, et al. Safety and activity of anti-PD-L1 antibody in patients with advanced cancer. N Engl J Med 2012; 366:2455-65; PMID:22658128; http:// dx.doi.org/10.1056/NEJMoa1200694
37. Topalian SL, Hodi FS, Brahmer JR, Gettinger SN, Smith DC, McDermott DF, Powderly JD, Carvajal RD, Sosman JA, Atkins MB, et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. N Engl J Med 2012; 366:2443-54; PMID:22658127; http://dx.doi.org/10.1056/NEJMoa1200690
38. Zitvogel L, Kroemer G. Targeting PD-1/ PD-L1 interactions for cancer immunotherapy. Oncoimmunology 2012; 1:1223-5; PMID:23243584; http://dx.doi.org/10.4161/onci.21335
39. Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, Segal NH, Ariyan CE, Gordon RA, Reed K, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med 2013; 369:122-33; PMID:23724867; http://dx.doi. org/10.1056/NEJMoa1302369