Suppression of established hepatocarcinoma in adjuvant only immunotherapy: Alum triggers anti-tumor CD8 + T cell response

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Wang, Bo ^a   Wang, Xuanyi ^a   Wen, Yumei ^a   Fu, Jing ^b   Wang, Hongyang ^b   Ma, Zhangmei ^a   Shi, Yan ^c,d   Wang, Bin ^a  

^a FUDAN UNIVERSITY   (China)

^b Eastern Hepatobiliary Surgery Institute/Hospital   (China)

^c TSINGHUA UNIVERSITY   (China)

^d UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ALUMINUM POTASSIUM SULFATE; ALUMINUM SULFATE; CHEMOKINE; IMMUNOLOGICAL ADJUVANT;

ANIMAL; BIOSYNTHESIS; CARCINOMA, HEPATOCELLULAR; CD8+ T LYMPHOCYTE; DISEASE MODEL; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; IMMUNOLOGY; IMMUNOMODULATION; LIVER NEOPLASMS; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; NEUTROPHIL CHEMOTAXIS; PATHOLOGY; TUMOR CELL LINE;

ADJUVANTS, IMMUNOLOGIC; ALUM COMPOUNDS; ANIMALS; CARCINOMA, HEPATOCELLULAR; CD8-POSITIVE T-LYMPHOCYTES; CELL LINE, TUMOR; CHEMOKINES; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION REGULATION; HUMANS; IMMUNOMODULATION; LIVER NEOPLASMS; LYMPHOCYTE ACTIVATION; MICE; NEUTROPHIL INFILTRATION;

EID: 84949519380     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep17695     Document Type: Article

References (84)

1. Gregory, L., Willem, W. O., Laszlo, R., Jianjun, G. &Padmanee, S. et al. Harnessing the power of the immune system to target cancer. Medicine 64, 71-90 (2013).
2. Santoni, M., Conti, A., Andrikou, K., Bittoni, A. &Lanese, A. et al. Risk of pruritus in cancer patients treated with biological therapies: A systematic review and meta-analysis of clinical trials. Crit Rev Oncol Hematol (2015), 10.1016/j.critrevonc.2015.05.007.
3. Topalian, S. L., Hodi, F. S., Brahmer, J. R., Gettinger, S. N. &Smith, D. C. et al. Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. New Engl J Med 366(26), 2443-2454 (2012).
4. Schulze, H. J., Cribier, B., Requena, L., Reifenberger, J. &Ferr?diz, C. et al. Imiquimod 5% cream for the treatment of superficial basal cell carcinoma: results from a randomized vehicle-controlled phase III study in Europe. Brit J Dermatol 152(5), 939-947 (2005).
5. Rosenberg, S. A., Restifo, N. P., Yang, J. C., Morgan, R. A. &Dudley, M. E. Adoptive cell transfer: a clinical path to effective cancer immunotherapy. Nat Rev Cancer 8(4), 299-308 (2008).
6. Makkouk, A. &Weiner, G. J. Cancer immunotherapy and breaking immune tolerance: new approaches to an old challenge. Cancer Res 75(1), 5-10 (2015).
7. Dudley, M. E., Wunderlich, J. R., Robbins, P. F., Yang, J. C. &Hwu, P. et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science (New York, NY) 298(5594), 850-854 (2002).
8. Mark, E. D., John, R. W., James, C. Y., Richard, M. S. &Suzanne, L. T. et al. Adoptive Cell Transfer Therapy Following Non-Myeloablative but Lymphodepleting Chemotherapy for the Treatment of Patients With Refractory Metastatic Melanoma. J Clin Oncol 23(10), 2346-2357 (2005).
9. Morgan, R. A., Dudley, M. E., Wunderlich, J. R., Hughes, M. S. &Yang, J. C. et al. Cancer regression in patients after transfer of genetically engineered lymphocytes. Science (New York, NY) 314(5796), 126-129 (2006).
10. Pardoll, D. M. The blockade of immune checkpoints in cancer immunotherapy. Nat Rev Cancer 12(4), 252-264 (2012).
11. Attia, P. Autoimmunity Correlates With Tumor Regression in Patients With Metastatic Melanoma Treated With Anti-Cytotoxic T-Lymphocyte Antigen-4. J Clin Oncol 23(25), 6043-6053 (2005).
12. Hodi, S. F., O'Day, S. J., McDermott, D. F., Weber, R. W. &Sosman, J. A. et al. Improved survival with ipilimumab in patientswith metastatic melanoma. New Engl J Med 363(8), 711-723 (2010).
13. Robert, C., Thomas, L., Bondarenko, I., O'Day, S. &Weber, J. et al. Ipilimumab plus dacarbazine for previously untreated metastatic melanoma. N Engl J Med 364(26), 2517-2526 (2011).
14. Lyford-Pike, S., Peng, S., Young, G. D., Taube, J. M. &Westra, W. H. et al. Evidence for a role of the PD-1:PD-L1 pathway in immune resistance of HPV-associated head and neck squamous cell carcinoma. Cancer Res 73(6), 1733-1741 (2013).
15. Aebersold, P., Hyatt, C., Johnson, S., Hines, K. &Korcak, L. et al. Lysis of autologous melanoma cells by tumor-infiltrating lymphocytes: association with clinical response. J Natl Cancer Inst 83(13), 932-937 (1991).
16. Robbins, P. F., Dudley, M. E., Wunderlich, J., El-Gamil, M. &Li, Y. F. et al. Cutting edge: persistence of transferred lymphocyte clonotypes correlates with cancer regression in patients receiving cell transfer therapy. J Immunol 173(12), 7125-7130 (2004).
17. Geoffrey, Y. K., Jianda, Y., David, B. P., Sebastian, E. A. S. &Katherine, S. P. et al. Single institution experience with ipilimumab in advanced melanoma patients in the compassionate use setting. Cancer 116(7), 1767-1775 (2010).
18. Peter, A., Giao, Q. P., Ajay, V. M., Michael, R. R. &Martha, M. Q. et al. Autoimmunity Correlates With Tumor Regression in Patients With Metastatic Melanoma Treated With Anti-Cytotoxic T-Lymphocyte Antigen-4. J Clin Oncol 23(25), 6043-6053 (2005).
19. Villadangos, J. A. &Schnorrer, P. Intrinsic and cooperative antigen-presenting functions of dendritic-cell subsets in vivo. Nat Rev Immunol 7(7), 543-555 (2007).
20. Serafini, P., Borrello, I. &Bronte, V. Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 16(1), 53-65 (2006).
21. Yang, L., Pang, Y. &Moses, H. L. TGF-beta and immune cells: an important regulatory axis in the tumor microenvironment and progression. Trends Immunol 31(6), 220-227 (2010).
22. Gr?oire, W., Nathalie, D., Danie, G. &Pierre van der, B. Immune Suppression in Tumors as a Surmountable Obstacle to Clinical Efficacy of Cancer Vaccines. Cancers (Basel) 3(3), 2904-2954 (2011).
23. Coffman, R. L., Sher, A. &Seder, R. A. Vaccine adjuvants: putting innate immunity to work. Immunity, 33(4), 492-503 (2010).
24. Thomas, M., Keiichi, O., Denis, B., Claire, M. &Catherine, S. et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med 17(8), 996-1002 (2011).
25. Tracy, L. F., Gilbert, N., Aswin, H., Melanie, D. D. &Ping, Z. et al. Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat Med 17(4), 479-487 (2011).
26. Etsushi, K., Ken, J. I., Satoshi, U., Keiichi, O. &Cevayir, C. et al. Silica Crystals and Aluminum Salts Regulate the Production of Prostaglandin in Macrophages via NALP3 Inflammasome-Independent Mechanisms. Immunity 34(4), 514-526 (2011).
27. Nesrua, F. O., Atuaolcl, S., Gillie, M. &Sunz, Y. Vaccination of melanoma patients with peptide-or tumor lysate-pulsed dendritic cells. Nat Med 4(3), 328-332 (1998).
28. Yu, J. S., Liu, G., Ying, H., Yong, W. H. &Black, K. L. et al. Vaccination with tumor lysate-pulsed dendritic cells elicits antigenspecific, cytotoxic T-cells in patients with malignant glioma. Cancer Res 64(14), 4973-4979 (2004).
29. Kantoff, P. W., Higano, C. S., Shore, N. D., Berger, E. R. &Small, E. J. et al. Sipuleucel-T immunotherapy for castration-resistant prostate cancer. New Engl J Med 363(5), 411-422 (2010).
30. Caminschi, I., Vremec, D., Ahmet, F., Lahoud, M. H. &Villadangos, J. A. et al. Antibody responses initiated by Clec9A-bearing dendritic cells in normal and Batf3 mice. Mol Immunol 50(1-2), 9-17 (2012).
31. Macho-Fernandez, E., Cruz, L. J., Ghinnagow, R., Fontaine, J. &Bialecki, E. et al. Targeted delivery of ? -galactosylceramide to CD8? + dendritic cells optimizes type I NKT cell-based antitumor responses. J Immunol 193(2), 961-969 (2014).
32. Zhang, Y., Hu, X., Hu, Y., Teng, K. &Zhang, K. et al. Anti-CD40-induced inflammatory E-cadherin+ dendritic cells enhance T cell responses and antitumour immunity in murine Lewis lung carcinoma. J Exp Clin Canc Res 34, 11 (2015).
33. Xia, X., Mai, J., Xu, R., Perez, J. E. &Guevara, M. L. et al. Porous silicon microparticle potentiates anti-tumor immunity by enhancing cross-presentation and inducing type I interferon response. Cell Rep 11(6), 957-966 (2015).
34. Luo, M., Shao, B., Nie, W., Wei, X.-W. W. &Li, Y.-L. L.et al. Antitumor and Adjuvant Activity of ? -carrageenan by Stimulating Immune Response in Cancer Immunotherapy. Sci Rep 5, 11062 (2015).
35. Ling, M. Y. [Establishment of a murine ascites hepatoma cell line H 22-F 25/L and its biological characteristics]. Zhonghua Zhong Liu Za Zhi 13(1), 13-15 (1991).
36. Dobrzanski, M. J. Expanding roles for CD4 T cells and their subpopulations in tumor immunity and therapy. Front Oncol 3, 63 (2013).
37. Wang, Y., Rathinam, R., Walch, A. &Alahari, S. K. ST14 (suppression of tumorigenicity 14) gene is a target for miR-27b, and the inhibitory effect of ST14 on cell growth is independent of miR-27b regulation. J Biol Chem 284(34), 23094-23106 (2009).
38. Wissmann, C., Wild, P. J., Kaiser, S., Roepcke, S. &Stoehr, R. et al. WIF1, a component of the Wnt pathway, is down-regulated in prostate, breast, lung, and bladder cancer. J Pathol 201(2), 204-212 (2003).
39. Britschgi, A., Trinh, E., Rizzi, M., Jenal, M. &Ress, A. et al. DAPK2 is a novel E2F1/KLF6 target gene involved in their proapoptotic function. Oncogene 27(43), 5706-5716 (2008).
40. Lee, K. K., Leung, A. K., Tang, M. K., Cai, D. Q. &Schneider, C. et al. Functions of the growth arrest specific 1 gene in the development of the mouse embryo. Dev Biol 234(1), 188-203 (2001).
41. Hogan, S. P., Rosenberg, H. F., Moqbel, R., Phipps, S. &Foster, P. S. et al. Eosinophils: biological properties and role in health and disease. Clin Exp Allergy 38(5), 709-750 (2008).
42. Domachowske, J. B., Dyer, K. D., Bonville, C. A. &Rosenberg, H. F. Recombinant human eosinophil-derived neurotoxin/RNase 2 functions as an effective antiviral agent against respiratory syncytial virus. J Infect Dis 177(6), 1458-1464 (1998).
43. Zvi, G. F., Jing, S., Samuel, K., Veena, K. &Guanjun, C. et al. Polarization of Tumor-Associated Neutrophil Phenotype by TGF-? : "N1" versus "N2" TAN. Cancer Cell 16(3), 183-194 (2009).
44. Marcello, A., David, A. M., Friederike, J., Bruno, I. &Laurence, F. et al. Neutrophils mediate antibody-induced antitumor effects in mice. Blood 2013.
45. Zvi, G., Erik, H., Elizabeth, A. C., Tari, A. K. &Larry, N. et al. Tumor Entrained Neutrophils Inhibit Seeding in the Premetastatic Lung. Cancer Cell 20(3), 300-314 (2011).
46. Glenny, A. T., Pope, C. G., Hilda, W. &Wallace, U. Immunological notes. XVII. The antigenic value of toxoid precipitated by potassium alum. J Path and Bac 29(1), 31-40 (1926).
47. Meldrum, M. "A calculated risk": the Salk polio vaccine field trials of 1954. BMJ, 317(7167), 1233-1236 (1998).
48. Fujimaki, H., Ozawa, M., Imai, T., Kubota, K. &Watanabe, N. Adjuvant effects of aluminum silicate on IgE and IgG1 antibody production in mice. Int Arch Allergy Appl Immunol 75(4), 351-356 (1984).
49. Letvin, N. L., Bloom, B. R. &Hoffman, S. L. Prospects for vaccines to protect against AIDS, tuberculosis, and malaria. JAMA 285(5), 606-611 (2001).
50. Richards, R. L., Hayre, M. D., Hockmeyer, W. T. &Alving, C. R. Liposomes, lipid A, and aluminum hydroxide enhance the immune response to a synthetic malaria sporozoite antigen. Infect Immun 56(3), 682-686 (1988).
51. Meraldi, V., Romero, J. F., Kensil, C. &Corradin, G. A strong CD8+ T cell response is elicited using the synthetic polypeptide from the C-terminus of the circumsporozoite protein of Plasmodium berghei together with the adjuvant QS-21: quantitative and phenotypic comparison with the vaccine model of irradiated sporozoites. Vaccine 23(21), 2801-2812 (2005).
52. Glenny, A. T., Buttle, G. A. H. &Muriel, F. S. Rate of disappearance of diphtheria toxoid injected into rabbits and guinea -pigs: Toxoid precipitated with alum. The Journal of Pathology and Bacteriology 34(2), 267-275 (1931).
53. Munks, M. W., McKee, A. S., Macleod, M. K., Powell, R. L. &Degen, J. L. et al. Aluminum adjuvants elicit fibrin-dependent extracellular traps in vivo. Blood 116(24), 5191-5199 (2010).
54. Sharon, H., Robert, A. B., Vivienne, B. G., Abigail, H. P. &Paul, G. et al. Antigen depot is not required for alum adjuvanticity. FASEB J 26(3), 1272-1279 (2012).
55. Hanfen, L., Stephen, B. W., Jenny, P. T. &Fabio, R. Cutting edge: inflammasome activation by alum and alum's adjuvant effect are mediated by NLRP3. J Immunol 181(1), 17-21 (2008).
56. Veit, H., Franz, B., Annett, H., Eivind, O. S. &Hajime, K. et al. Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9(8), 847-856 (2008).
57. Stephanie, C. E., Oscar, R. C., William, O. C., Fayyaz, S. S. &Richard, A. F. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature, 453(7198), 1122-1126 (2008).
58. Amy, S. M., Michael, W. M., Megan, K. L. M., Courtney, J. F. &Nico Van, R. et al. Alum Induces Innate Immune Responses through Macrophage and Mast Cell Sensors, But These Sensors Are Not Required for Alum to Act As an Adjuvant for Specific Immunity. J Immunol 183(7), 4403-4414 (2009).
59. Flach, T. L., Ng, G., Hari, A., Desrosiers, M. D. &Zhang, P. et al. Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat Med 17(4), 479-487 (2011).
60. Franchi, L. &Nunez, G. The Nlrp3 inflammasome is critical for aluminium hydroxide-mediated IL-1beta secretion but dispensable for adjuvant activity. Eur J Immunol 38(8), 2085-2089 (2008).
61. Kool, M., Soullie, T., van Nimwegen, M., Willart, M. A. &Muskens, F. et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med, 205(4), 869-882 (2008).
62. McKee, A. S., Munks, M. W., MacLeod, M. K., Fleenor, C. J. &Van Rooijen, N. et al. Alum induces innate immune responses through macrophage and mast cell sensors, but these sensors are not required for alum to act as an adjuvant for specific immunity. J Immunol 183(7), 4403-4414 (2009).
63. Seubert, A., Calabro, S., Santini, L., Galli, B. &Genovese, A. et al. Adjuvanticity of the oil-in-water emulsion MF59 is independent of Nlrp3 inflammasome but requires the adaptor protein MyD88. Proc Natl Acad Sci USA 108(27), 11169-11174 (2011).
64. Tracy, L. F., Gilbert, N., Aswin, H., Melanie, D. D. &Ping, Z. et al. Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat Med 17(4), 479-487 (2011).
65. Amy, S. M., Matthew, A. B., Michael, W. M., Lei, J. &John, W. K. et al. Host DNA released in response to aluminum adjuvant enhances MHC class II-mediated antigen presentation and prolongs CD4 T-cell interactions with dendritic cells. Proc Natl Acad Sci USA 110(12), 31 (2013).
66. Kuroda, E., Ishii, K. J., Uematsu, S., Ohata, K. &Coban, C. et al. Silica crystals and aluminum salts regulate the production of prostaglandin in macrophages via NALP3 inflammasome-independent mechanisms. Immunity 34(4), 514-526 (2011).
67. Rieser, C., Bock, G., Klocker, H., Bartsch, G. &Thurnher, M. Prostaglandin E2 and tumor necrosis factor alpha cooperate to activate human dendritic cells: synergistic activation of interleukin 12 production. J Exp Med 186(9), 1603-1608 (1997).
68. Luft, T., Jefford, M., Luetjens, P., Toy, T. &Hochrein, H. et al. Functionally distinct dendritic cell (DC) populations induced by physiologic stimuli: prostaglandin E(2) regulates the migratory capacity of specific DC subsets. Blood 100(4), 1362-1372 (2002).
69. Mori, A., Oleszycka, E., Sharp, F. A., Coleman, M. &Ozasa, Y. et al. The vaccine adjuvant alum inhibits IL-12 by promoting PI3 kinase signaling while chitosan does not inhibit IL-12 and enhances Th1 and Th17 responses. Eur J Immunol 42(10), 2709-2719 (2012).
70. Kool, M., Willart, M. A., van Nimwegen, M., Bergen, I. &Pouliot, P. et al. An unexpected role for uric acid as an inducer of T helper 2 cell immunity to inhaled antigens and inflammatory mediator of allergic asthma. Immunity 34(4), 527-540 (2011).
71. Hu, D. E., Moore, A. M., Thomsen, L. L. &Brindle, K. M. Uric acid promotes tumor immune rejection. Cancer Res, 64(15), 5059-5062 (2004).
72. Shi, Y., Evans, J. E. &Rock, K. L. Molecular identification of a danger signal that alerts the immune system to dying cells. Nature 425(6957), 516-521 (2003).
73. Reis e Sousa, C. &Germain, R. N. Major histocompatibility complex class I presentation of peptides derived from soluble exogenous antigen by a subset of cells engaged in phagocytosis. J Exp Med 182(3), 841-851 (1995).
74. Castellino, F., Boucher, P. E., Eichelberg, K., Mayhew, M. &Rothman, J. E. et al. Receptor-mediated uptake of antigen/heat shock protein complexes results in major histocompatibility complex class I antigen presentation via two distinct processing pathways. J Exp Med 191(11), 1957-1964 (2000).
75. Hari, A., Zhang, Y., Tu, Z., Detampel, P. &Stenner, M. et al. Activation of NLRP3 inflammasome by crystalline structures via cell surface contact. Sci Rep 4, 7281 (2014).
76. Wang, X. Y., Yao, X., Wan, Y. M., Wang, B. &Xu, J. Q. et al. Responses to multiple injections with alum alone compared to injections with alum adsorbed to proteins in mice. Immunol Lett 149(1-2), 88-92 (2013).
77. Xu, D. Z., Zhao, K., Guo, L. M., Li, L. J. &Xie, Q. et al. A randomized controlled phase IIb trial of antigen-antibody immunogenic complex therapeutic vaccine in chronic hepatitis B patients. PLoS One 3(7), e2565 (2008).
78. Mirjam, K., Thomas, S., Menno van, N., Monique, A. W. &Femke, M. et al. Alum adjuvant boosts adaptive immunity by inducing uric acid and activating inflammatory dendritic cells. J Exp Med, 205(4), 869-882 (2008).
79. Mosca, F., Tritto, E., Muzzi, A., Monaci, E. &Bagnoli, F. et al. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA 105(30), 10501-10506 (2008).
80. Harris, J. R., Soliakov, A., Lewis, R. J., Depoix, F. &Watkinson, A. et al. Alhydrogel(R) adjuvant, ultrasonic dispersion and protein binding: a TEM and analytical study. Micron 43(2-3), 192-200 (2012).
81. Pape, K. A., Khoruts, A., Mondino, A. &Jenkins, M. K. Inflammatory cytokines enhance the in vivo clonal expansion and differentiation of antigen-activated CD4 T cells. J Immunol 159(2), 591-598 (1997).
82. Darcy, P. K., Neeson, P., Yong, C. S. &Kershaw, M. H. Manipulating immune cells for adoptive immunotherapy of cancer. Curr Opin Immunol 27, 46-52 (2014).
83. Palucka, K. &Banchereau, J. Cancer immunotherapy via dendritic cells. Nat Rev Cancer 12(4), 265-277 (2012).
84. Palucka, K. &Banchereau, J. Dendritic-cell-based therapeutic cancer vaccines. Immunity 39(1), 38-48 (2013).