Liposomes loaded with a STING pathway ligand, cyclic di-GMP, enhance cancer immunotherapy against metastatic melanoma

Journal of Controlled Release

Volumn 216, Issue , 2015, Pages 149-157

  Nakamura, Takashi ^a   Miyabe, Hiroko ^a   Hyodo, Mamoru ^b   Sato, Yusuke ^a   Hayakawa, Yoshihiro ^b   Harashima, Hideyoshi ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

^b AICHI INSTITUTE OF TECHNOLOGY   (Japan)

Author keywords

Adjuvant; c di GMP; Cancer immunotherapy; Liposome; Melanoma; STING

Indexed keywords

ANTIBIOTICS; CELLS; CYTOLOGY; DERMATOLOGY; DISEASES; GLYCOPROTEINS; LIGANDS; LIPOSOMES; MAMMALS; MOLECULAR BIOLOGY; ONCOLOGY;

ADJUVANT; C-DI-GMP; CANCER IMMUNOTHERAPY; MELANOMA; STING;

C (PROGRAMMING LANGUAGE);

ANTINEOPLASTIC AGENT; BETA INTERFERON; CYCLIC DI GUANOSINE PHOSPHATE; CYCLIC GMP DERIVATIVE; GAMMA INTERFERON; GANGLIOSIDE GM1 ANTIBODY; INTERLEUKIN 6; LIPOSOME; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYCLIC GMP; CYTOKINE; LIGAND; LIPID; MEMBRANE PROTEIN; MPYS PROTEIN, HUMAN; PIPERIDINE DERIVATIVE; YSK05;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINEOPLASTIC ACTIVITY; ARTICLE; CANCER IMMUNOTHERAPY; CELL INFILTRATION; CONTROLLED STUDY; CYTOSOL; EFFECTOR CELL; FEMALE; INTERFERON PRODUCTION; LUNG METASTASIS; LYMPHOCYTE ACTIVATION; METASTATIC MELANOMA; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; SPLEEN CELL; TUMOR GROWTH; TUMOR MICROENVIRONMENT; ZETA POTENTIAL; ADJUVANT CHEMOTHERAPY; ANALOGS AND DERIVATIVES; ANIMAL; BLOOD; CHEMISTRY; DRUG DELIVERY SYSTEM; DRUG EFFECTS; IMMUNOTHERAPY; INTRAVENOUS DRUG ADMINISTRATION; LUNG; MACROPHAGE ACTIVATION; MELANOMA, EXPERIMENTAL; METABOLISM; METASTASIS; PATHOLOGY; PROCEDURES;

ANIMALS; CHEMOTHERAPY, ADJUVANT; CYCLIC GMP; CYTOKINES; CYTOSOL; DRUG DELIVERY SYSTEMS; IMMUNOTHERAPY; INJECTIONS, INTRAVENOUS; KILLER CELLS, NATURAL; LIGANDS; LIPIDS; LIPOSOMES; LUNG; MACROPHAGE ACTIVATION; MELANOMA, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; NEOPLASM METASTASIS; PIPERIDINES;

EID: 84940172128     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.08.026     Document Type: Article

References (35)

1. T.F. Gajewski, J. Louahed, and V.G. Brichard Gene signature in melanoma associated with clinical activity: a potential clue to unlock cancer immunotherapy Cancer J. 16 2010 399 403
2. O. Hamid, H. Schmidt, A. Nissan, L. Ridolfi, S. Aamdal, J. Hansson, M. Guida, D.M. Hyams, H. Gomez, L. Bastholt, S.D. Chasalow, and D. Berman A prospective phase II trial exploring the association between tumor microenvironment biomarkers and clinical activity of ipilimumab in advanced melanoma J. Transl. Med. 9 2011 204
3. H. Harlin, Y. Meng, A.C. Peterson, Y. Zha, M. Tretiakova, C. Slingluff, M. McKee, and T.F. Gajewski Chemokine expression in melanoma metastases associated with CD8 + T-cell recruitment Cancer Res. 69 2009 3077 3085
4. R.R. Ji, S.D. Chasalow, L. Wang, O. Hamid, H. Schmidt, J. Cogswell, S. Alaparthy, D. Berman, M. Jure-Kunkel, N.O. Siemers, J.R. Jackson, and V. Shahabi An immune-active tumor microenvironment favors clinical response to ipilimumab Cancer Immunol. Immunother. 61 2012 1019 1031
5. S. Spranger, R.M. Spaapen, Y. Zha, J. Williams, Y. Meng, T.T. Ha, and T.F. Gajewski Up-regulation of PD-L1, IDO, and T(regs) in the melanoma tumor microenvironment is driven by CD8(+) T cells Sci. Transl. Med. 5 2013 200ra116
6. S.R. Woo, M.B. Fuertes, L. Corrales, S. Spranger, M.J. Furdyna, M.Y. Leung, R. Duggan, Y. Wang, G.N. Barber, K.A. Fitzgerald, M.L. Alegre, and T.F. Gajewski STING-dependent cytosolic DNA sensing mediates innate immune recognition of immunogenic tumors Immunity 41 2014 830 842
7. X. Cai, Y.H. Chiu, and Z.J. Chen The cGAS-cGAMP-STING pathway of cytosolic DNA sensing and signaling Mol. Cell 54 2014 289 296
8. P. Ross, H. Weinhouse, Y. Aloni, D. Michaeli, P. Weinberger-Ohana, R. Mayer, S. Braun, E. de Vroom, G.A. van der Marel, J.H. van Boom, and M. Benziman Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid Nature 325 1987 279 281
9. P. Ross, R. Mayer, H. Weinhouse, D. Amikam, Y. Huggirat, M. Benziman, E. de Vroom, A. Fidder, P. de Paus, L.A. Sliedregt, and et al. The cyclic diguanylic acid regulatory system of cellulose synthesis in Acetobacter xylinum. Chemical synthesis and biological activity of cyclic nucleotide dimer, trimer, and phosphothioate derivatives J. Biol. Chem. 265 1990 18933 18943
10. D.K. Karaolis, T.K. Means, D. Yang, M. Takahashi, T. Yoshimura, E. Muraille, D. Philpott, J.T. Schroeder, M. Hyodo, Y. Hayakawa, B.G. Talbot, E. Brouillette, and F. Malouin Bacterial c-di-GMP is an immunostimulatory molecule J. Immunol. 178 2007 2171 2181
11. D.L. Burdette, K.M. Monroe, K. Sotelo-Troha, J.S. Iwig, B. Eckert, M. Hyodo, Y. Hayakawa, and R.E. Vance STING is a direct innate immune sensor of cyclic di-GMP Nature 478 2011 515 518
12. K. Parvatiyar, Z. Zhang, R.M. Teles, S. Ouyang, Y. Jiang, S.S. Iyer, S.A. Zaver, M. Schenk, S. Zeng, W. Zhong, Z.J. Liu, R.L. Modlin, Y.J. Liu, and G. Cheng The helicase DDX41 recognizes the bacterial secondary messengers cyclic di-GMP and cyclic di-AMP to activate a type I interferon immune response Nat. Immunol. 13 2012 1155 1161
13. H. Miyabe, M. Hyodo, T. Nakamura, Y. Sato, Y. Hayakawa, and H. Harashima A new adjuvant delivery system ‘cyclic di-GMP/YSK05 liposome' for cancer immunotherapy J. Control. Release 184 2014 20 27
14. Y. Sato, H. Hatakeyama, Y. Sakurai, M. Hyodo, H. Akita, and H. Harashima A pH-sensitive cationic lipid facilitates the delivery of liposomal siRNA and gene silencing activity in vitro and in vivo J. Control. Release 163 2012 267 276
15. T. Nakamura, R. Moriguchi, K. Kogure, and H. Harashima Incorporation of polyinosine-polycytidylic acid enhances cytotoxic T cell activity and antitumor effects by octaarginine-modified liposomes encapsulating antigen, but not by octaarginine-modified antigen complex Int. J. Pharm. 441 2013 476 481
16. M. Ahmad, R.C. Rees, and S.A. Ali Escape from immunotherapy: possible mechanisms that influence tumor regression/progression Cancer Immunol. Immunother. 53 2004 844 854
17. S. Morgado, B. Sanchez-Correa, J.G. Casado, E. Duran, I. Gayoso, F. Labella, R. Solana, and R. Tarazona NK cell recognition and killing of melanoma cells is controlled by multiple activating receptor-ligand interactions J. Innate Immun. 3 2011 365 373
18. M.K. Erdmann Immunity unleashed in melanoma Lancet Oncol. 11 2010 108 109
19. T. Nakamura, D. Yamazaki, J. Yamauchi, and H. Harashima The nanoparticulation by octaarginine-modified liposome improves alpha-galactosylceramide-mediated antitumor therapy via systemic administration J. Control. Release 171 2013 216 224
20. T. Abe, and G.N. Barber Cytosolic-DNA-mediated, STING-dependent proinflammatory gene induction necessitates canonical NF-kappaB activation through TBK1 J. Virol. 88 2014 5328 5341
21. E.O. Long Tumor cell recognition by natural killer cells Semin. Cancer Biol. 12 2002 57 61
22. C. Gregoire, L. Chasson, C. Luci, E. Tomasello, F. Geissmann, E. Vivier, and T. Walzer The trafficking of natural killer cells Immunol. Rev. 220 2007 169 182
23. S. Habu, H. Fukui, K. Shimamura, M. Kasai, Y. Nagai, K. Okumura, and N. Tamaoki In vivo effects of anti-asialo GM1. I. Reduction of NK activity and enhancement of transplanted tumor growth in nude mice J. Immunol. 127 1981 34 38
24. T. Ebihara, M. Azuma, H. Oshiumi, J. Kasamatsu, K. Iwabuchi, K. Matsumoto, H. Saito, T. Taniguchi, M. Matsumoto, and T. Seya Identification of a polyI:C-inducible membrane protein that participates in dendritic cell-mediated natural killer cell activation J. Exp. Med. 207 2010 2675 2687
25. F. Gerosa, B. Baldani-Guerra, C. Nisii, V. Marchesini, G. Carra, and G. Trinchieri Reciprocal activating interaction between natural killer cells and dendritic cells J. Exp. Med. 195 2002 327 333
26. T. Akazawa, T. Ebihara, M. Okuno, Y. Okuda, M. Shingai, K. Tsujimura, T. Takahashi, M. Ikawa, M. Okabe, N. Inoue, M. Okamoto-Tanaka, H. Ishizaki, J. Miyoshi, M. Matsumoto, and T. Seya Antitumor NK activation induced by the Toll-like receptor 3-TICAM-1 (TRIF) pathway in myeloid dendritic cells Proc. Natl. Acad. Sci. U. S. A. 104 2007 252 257
27. S. Chiba, H. Ikushima, H. Ueki, H. Yanai, Y. Kimura, S. Hangai, J. Nishio, H. Negishi, T. Tamura, S. Saijo, Y. Iwakura, and T. Taniguchi Recognition of tumor cells by Dectin-1 orchestrates innate immune cells for anti-tumor responses Elife 3 2014 e04177
28. E. Ambegia, S. Ansell, P. Cullis, J. Heyes, L. Palmer, and I. MacLachlan Stabilized plasmid-lipid particles containing PEG-diacylglycerols exhibit extended circulation lifetimes and tumor selective gene expression Biochim. Biophys. Acta 1669 2005 155 163
29. S. Kim, K. Iizuka, H.L. Aguila, I.L. Weissman, and W.M. Yokoyama In vivo natural killer cell activities revealed by natural killer cell-deficient mice Proc. Natl. Acad. Sci. U. S. A. 97 2000 2731 2736
30. S. Coca, J. Perez-Piqueras, D. Martinez, A. Colmenarejo, M.A. Saez, C. Vallejo, J.A. Martos, and M. Moreno The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma Cancer 79 1997 2320 2328
31. C.C. Chang, M. Campoli, and S. Ferrone Classical and nonclassical HLA class I antigen and NK cell-activating ligand changes in malignant cells: current challenges and future directions Adv. Cancer Res. 93 2005 189 234
32. E. Vivier, D.H. Raulet, A. Moretta, M.A. Caligiuri, L. Zitvogel, L.L. Lanier, W.M. Yokoyama, and S. Ugolini Innate or adaptive immunity? The example of natural killer cells Science 331 2011 44 49
33. A. Diefenbach, E.R. Jensen, A.M. Jamieson, and D.H. Raulet Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity Nature 413 2001 165 171
34. M.J. Smyth, J. Swann, E. Cretney, N. Zerafa, W.M. Yokoyama, and Y. Hayakawa NKG2D function protects the host from tumor initiation J. Exp. Med. 202 2005 583 588
35. L. Deng, H. Liang, M. Xu, X. Yang, B. Burnette, A. Arina, X.D. Li, H. Mauceri, M. Beckett, T. Darga, X. Huang, T.F. Gajewski, Z.J. Chen, Y.X. Fu, and R.R. Weichselbaum STING-dependent cytosolic DNA sensing promotes radiation-induced type I interferon-dependent antitumor immunity in immunogenic tumors Immunity 41 2014 843 852