Vaccination with antigen-transfected, NKT cell ligand-loaded, human cells elicits robust in situ immune responses by dendritic cells

Cancer Research

Volumn 73, Issue 1, 2013, Pages 62-73

  Shimizu, Kanako ^a,b   Mizuno, Takuya ^c   Shinga, Jun ^a   Asakura, Miki ^a   Kakimi, Kazuhiro ^d   Ishii, Yasuyuki ^b   Masuda, Kenichi ^g   Maeda, Tomoji ^h   Sugahara, Hidetoshi ^a   Sato, Yusuke ^a   Matsushita, Hirokazu ^d   Nishida, Keigo ^b   Hanada, Kenichi ⁱ   Dorrie, Jan ^j   Schaft, Niels ^j   Bickham, Kara ^k   Koike, Hisashi ^d,f   Ando, Tsuyoshi ^d   Nagai, Ryozo ^d,e   Fujii, Shin Ichiro ^a  

^a Institute of Physical and Chemical Research   (Japan)

^b INST OF PHYS AND CHEMICAL RESEARCH   (Japan)

^c YAMAGUCHI UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO HOSPITAL   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f PHARMACEUTICALS AND MEDICAL DEVICES AGENCY   (Japan)

^g Animal Allergy Clinical Laboratories   (Japan)

^h IWATE MEDICAL UNIVERSITY   (Japan)

ⁱ NIH   (Germany)

^j UNIVERSITY HOSPITAL ERLANGEN   (Germany)

^k Columbia University College of Physicians and Surgeons ^*  (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

CD1D ANTIGEN; MELAN A; MESSENGER RNA; TUMOR ANTIGEN; TUMOR CELL VACCINE;

ADAPTIVE IMMUNITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ARTIFICIAL ADJUVANT VECTOR CELL; CANCER IMMUNOTHERAPY; CELL ACTIVATION; CELL ACTIVITY; CELL STRAIN HEK293; CELL TYPE; CROSS PRESENTATION; DENDRITIC CELL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; INNATE IMMUNITY; MALE; MOUSE; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR IMMUNITY; VACCINATION;

ADAPTIVE IMMUNITY; ANIMALS; ANTIGENS, NEOPLASM; CANCER VACCINES; CROSS-PRIMING; DENDRITIC CELLS; DOGS; FLOW CYTOMETRY; HEK293 CELLS; HUMANS; IMMUNITY, INNATE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; NATURAL KILLER T-CELLS; TRANSFECTION;

EID: 84871969182     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-0759     Document Type: Article

References (50)

1. Steinman RM, Banchereau J. Taking dendritic cells into medicine. Nature 2007;449:419-26.
2. Palucka K, Ueno H, Banchereau J. Recent developments in cancer vaccines. J Immunol 2011;186:1325-31.
3. Le DT, Pardoll DM, Jaffee EM. Cellular vaccine approaches. Cancer J 2010;16:304-10.
4. Kenter GG, Welters MJ, Valentijn AR, Lowik MJ, Berends-van der Meer DM, Vloon AP, et al. Vaccination against HPV-16 oncoproteins for vulvar intraepithelial neoplasia. N Engl J Med 2009;361:1838-47.
5. Widenmeyer M, Griesemann H, Stevanovic S, Feyerabend S, Klein R, Attig S, et al. Promiscuous survivin peptide induces robust CD4(+) T-cell responses in the majority of vaccinated cancer patients. Int J Cancer 2012;131:140-9.
6. Aoki M, Ueda S, Nishikawa H, Kitano S, Hirayama M, Ikeda H, et al. Antibody responses against NY-ESO-1 and HER2 antigens in patients vaccinated with combinations of cholesteryl pullulan (CHP)-NY-ESO-1 and CHP-HER2 with OK-432. Vaccine 2009;27:6854-61.
7. Gilboa E, Vieweg J. Cancer immunotherapy with mRNA-transfected dendritic cells. Immunol Rev 2004;199:251-63.
8. Schuler G. Dendritic cells in cancer immunotherapy. Eur J Immunol 2010;40:2123-30.
9. Boczkowski D, Nair SK, Snyder D, Gilboa E. Dendritic cells pulsed with RNA are potent antigen-presenting cells in vitro and in vivo. J Exp Med 1996;184:465-72.
10. Nair SK, Heiser A, Boczkowski D, Majumdar A, Naoe M, Lebkowski JS, et al. Induction of cytotoxic T cell responses and tumor immunity against unrelated tumors using telomerase reverse transcriptase RNA transfected dendritic cells. Nat Med 2000;6:1011-7.
11. Heiser A, Coleman D, Dannull J, Yancey D, Maurice MA, Lallas CD, et al. Autologous dendritic cells transfected with prostate-specific antigen RNA stimulate CTL responses against metastatic prostate tumors. J Clin Invest 2002;109:409-17.
12. Schaft N, Dorrie J, Thumann P, Beck VE, Muller I, Schultz ES, et al. Generation of an optimized polyvalent monocyte-derived dendritic cell vaccine by transfecting defined RNAs after rather than before maturation. J Immunol 2005;174:3087-97.
13. Kyte JA, Mu L, Aamdal S, Kvalheim G, Dueland S, Hauser M, et al. Phase I/II trial of melanoma therapy with dendritic cells transfected with autologous tumor-mRNA. Cancer Gene Ther 2006;13:905-18.
14. Dannull J, Nair S, Su Z, Boczkowski D, DeBeck C, Yang B, et al. Enhancing the immunostimulatory function of dendritic cells by transfection with mRNA encoding OX40 ligand. Blood 2005;105:3206-13.
15. Hess PR, Boczkowski D, Nair SK, Snyder D, Gilboa E. Vaccination with mRNAs encoding tumor-associated antigens and granulocyte-macrophage colony-stimulating factor efficiently primes CTL responses, but is insufficient to overcome tolerance to a model tumor/self antigen. Cancer Immunol Immunother 2006;55:672-83.
16. Bontkes HJ, Kramer D, Ruizendaal JJ, Kueter EW, van Tendeloo VF, Meijer CJ, et al. Dendritic cells transfected with interleukin-12 and tumor-associated antigen messenger RNA induce high avidity cytotoxic T cells. Gene Ther 2007;14:366-75.
17. Klebanoff CA, Acquavella N, Yu Z, Restifo NP. Therapeutic cancer vaccines: are we there yet? Immunol Rev 2011;239:27-44.
18. Duthie MS, Windish HP, Fox CB, Reed SG. Use of defined TLR ligands as adjuvants within human vaccines. Immunol Rev 2011;239:178-96.
19. Beer TM, Bernstein GT, Corman JM, Glode LM, Hall SJ, Poll WL, et al. Randomized trial of autologous cellular immunotherapy with sipuleucel-T in androgen-dependent prostate cancer. Clin Cancer Res 2011;17:4558-67.
20. Bonifaz LC, Bonnyay DP, Charalambous A, Darguste DI, Fujii S, Soares H, et al. In vivo targeting of antigens to the DEC-205 receptor on maturing dendritic cells improves T cell vaccination. J Exp Med 2004;199:815-24.
21. He LZ, Crocker A, Lee J, Mendoza-Ramirez J, Wang XT, Vitale LA, et al. Antigenic targeting of the human mannose receptor induces tumor immunity. J Immunol 2007;178:6259-67.
22. Sancho D, Mourao-Sa D, Joffre OP, Schulz O, Rogers NC, Pennington DJ, et al. Tumor therapy in mice via antigen targeting to a novel, DC-restricted C-type lectin. J Clin Invest 2008;118:2098-110.
23. Klechevsky E, Flamar AL, Cao Y, Blanck JP, Liu M, O'Bar A, et al. Cross-priming CD8+ T cells by targeting antigens to human dendritic cells through DCIR. Blood 2010;116:1685-97.
24. Fujii S, Shimizu K, Kronenberg M, Steinman RM. Prolonged interferon-γ producing NKT response induced with α- galactosylceramide-loaded dendritic cells. Nat Immunol 2002;3:867-74.
25. Motohashi S, Nagato K, Kunii N, Yamamoto H, Yamasaki K, Okita K, et al. A phase I-II study of α-galactosylceramide-pulsed IL-2/GM-CSF-cultured peripheral blood mononuclear cells in patients with advanced and recurrent non-small cell lung cancer. J Immunol 2009;182:2492-501.
26. Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM. Activation of natural killer T cells by α-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a co-administered protein. J q1Exp Med 2003;198:267-79.
27. + T cell responses to soluble antigen in vivo through direct interaction with dendritic cells. J Immunol 2003;171:5140-7.
28. Fujii S, Shimizu K, Hemmi H, Fukui M, Bonito AJ, Chen G, et al. Glycolipid α-C-galactosylceramide is a distinct inducer of dendritic cell function during innate and adaptive immune responses of mice. Proc Natl Acad Sci U S A 2006;103:11252-7.
29. Youn HJ, Ko SY, Lee KA, Ko HJ, Lee YS, Fujihashi K, et al. A single intranasal immunization with inactivated influenza virus and α-galactosylceramide induces long-term protective immunity without redirecting antigen to the central nervous system. Vaccine 2007;25:5189-98.
30. Guillonneau C, Mintern JD, Hubert FX, Hurt AC, Besra GS, Porcelli S, et al. Combined NKT cell activation and in fluenza virus vaccination boosts memory CTL generation and protective immunity. Proc Natl Acad Sci U S A 2009;106:3330-5.
31. Lindqvist M, Persson J, Thorn K, Harandi AM. The mucosal adjuvant effect of α-galactosylceramide for induction of protective immunity to sexually transmitted viral infection. J Immunol 2009;182:6435-43.
32. Shimizu K, Goto A, Fukui M, Taniguchi M, Fujii S. Tumor cells loaded with α-galactosylceramide Induce innate NKT and NK cell-dependent resistance to tumor implantation in mice. J Immunol 2007;178:2853-61.
33. Fujii S, Goto A, Shimizu K. Antigen mRNA-transfected, allogeneic fibroblasts loaded with NKT-cell ligand confer antitumor immunity. Blood 2009;113:4262-72.
34. Shimizu K, Kurosawa Y, Taniguchi M, Steinman RM, Fujii S. Cross-presentation of glycolipid from tumor cells loaded with α-galactosylceramide leads to potent and long-lived T cell mediated immunity via dendritic cells. J Exp Med 2007;204:2641- 53.
35. Fujii S. Exploiting dendritic cells and natural killer T cells in immunotherapy against malignancies. Trends Immunol 2008;29:242-9.
36. Chung Y, Qin H, Kang CY, Kim S, Kwak LW, Dong C. An NKT-mediated autologous vaccine generates CD4 T-cell dependent potent antilymphoma immunity. Blood 2007;110:2013-9.
37. Karaki S, Kariyone A, Kato N, Kano K, Iwakura Y, Takiguchi M. HLA-B51 transgenic mice as recipients for production of polymorphic HLA-A, B-specific antibodies. Immunogenetics 1993;37:139-42.
38. Hosoi A, Takeda Y, Sakuta K, Ueha S, Kurachi M, Kimura K, et al. Dendritic cell vaccine with mRNA targeted to the proteasome by polyubiquitination. Biochem Biophys Res Commun 2008;371:242-6.
39. + T cells by exogenous cell-associated antigens. Immunity 2002;17:211-20.
40. Johnson LA,Morgan RA, Dudley ME, Cassard L, Yang JC, Hughes MS, et al. Gene therapy with human and mouse T-cell receptors mediates cancer regression and targets normal tissues expressing cognate antigen. Blood 2009;114:535-46.
41. Yasuda N, Masuda K, Tsukui T, Teng A, Ishii Y. Identification of canine natural CD3-positive T cells expressing an invariant T-cell receptor alpha chain. Vet Immunol Immunopathol 2009;132:224-31.
42. Shimizu K, Hidaka M, Kadowaki N, Makita N, Konishi N, Fujimoto K, et al. Evaluation of the function of human invariant NKT cells from cancer patients using α-galactosylceramide-loaded murine dendritic cells. J Immunol 2006;177:3484-92.
43. Palucka AK, Ueno H, Connolly J, Kerneis-Norvell F, Blanck JP, Johnston DA, et al. 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.
44. von Euw EM, Barrio MM, Furman D, Levy EM, Bianchini M, Peguillet I, et al. A phase I clinical study of vaccination of melanoma patients with dendritic cells loaded with allogeneic apoptotic/necrotic melanoma cells. Analysis of toxicity and immune response to the vaccine and of IL-10 -1082 promoter genotype as predictor of disease progression. J Transl Med 2008;6:6.
45. Nemunaitis J, Jahan T, Ross H, Sterman D, Richards D, Fox B, et al. Phase 1/2 trial of autologous tumor mixed with an allogeneic GVAX vaccine in advanced-stage non-small-cell lung cancer. Cancer Gene Ther 2006;13:555-62.
46. Small EJ, Sacks N, Nemunaitis J, Urba WJ, Dula E, Centeno AS, et al. Granulocyte macrophage colony-stimulating factor-secreting allogeneic cellular immunotherapy for hormone-refractory prostate cancer. Clin Cancer Res 2007;13:3883-91.
47. Brehm MA, Shultz LD, Greiner DL. Humanized mouse models to study human diseases. Curr Opin Endocrinol Diabetes Obes 2010;17:120-5.
48. Strowig T, Gurer C, Ploss A, Liu YF, Arrey F, Sashihara J, et al. Priming of protective T cell responses against virus-induced tumors in mice with human immune system components. J Exp Med 2009;206:1423-34.
49. Paoloni M, Khanna C. Translation of new cancer treatments from pet dogs to humans. Nat Rev Cancer 2008;8:147-56.
50. Chang DH,Osman K, Connolly J, Kukreja A, Krasovsky J, Pack M, et al. Sustained expansion of NKT cells and antigen-specific T cells after injection of α-galactosyl-ceramide loaded mature dendritic cells in cancer patients. J Exp Med 2005;201:1503-17.