Integrated nanovaccine with microRNA-148a inhibition reprograms tumor-associated dendritic cells by modulating miR-148a/DNMT1/SOCS1 axis

Journal of Immunology

Volumn 197, Issue 4, 2016, Pages 1231-1241

  Liu, Lanlan ^a   Yi, Huqiang ^a   Wang, Ce ^a   He, Huamei ^a   Li, Ping ^a   Pan, Hong ^a   Sheng, Nan ^a   Ji, Manyi ^a   Cai, Lintao ^a   Ma, Yifan ^a  

^a SHENZHEN INSTITUTES OF ADVANCED TECHNOLOGY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER VACCINE; DNA METHYLTRANSFERASE 1; LIPOPOLYSACCHARIDE; MICRORNA; MICRORNA 148A; NANOVACCINE; OVALBUMIN; POLYINOSINIC POLYCYTIDYLIC ACID; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 3; TOLL LIKE RECEPTOR 4; UNCLASSIFIED DRUG; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; MIRN148 MICRORNA, MOUSE; SOCS1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW; CANCER IMMUNIZATION; CELL MATURATION; CONTROLLED STUDY; DENDRITIC CELL; DRUG DOSE COMPARISON; DRUG EFFICACY; FEMALE; GENE EXPRESSION; GENE REPRESSION; IN VIVO STUDY; MELANOMA B16; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NANOENCAPSULATION; NONHUMAN; NUCLEAR REPROGRAMMING; PRIORITY JOURNAL; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SPLEEN; SUPPRESSOR CELL; SURVIVAL TIME; TUMOR ASSOCIATED DENDRITIC CELL; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; TUMOR REGRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL REPROGRAMMING TECHNIQUE; DNA METHYLATION; DRUG EFFECTS; EXPERIMENTAL MELANOMA; GENE THERAPY; IMMUNOLOGY; METABOLISM; NANOTECHNOLOGY; PROCEDURES; REAL TIME POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CANCER VACCINES; CELLULAR REPROGRAMMING TECHNIQUES; DENDRITIC CELLS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; GENETIC THERAPY; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICRORNAS; NANOTECHNOLOGY; REAL-TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SUPPRESSOR OF CYTOKINE SIGNALING 1 PROTEIN;

EID: 84983738980     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600182     Document Type: Article

References (53)

1. Aranda, F., E. Vacchelli, A. Eggermont, J. Galon, C. Sautès-Fridman, E. Tartour, L. Zitvogel, G. Kroemer, and L. Galluzzi. 2013. Trial Watch: peptide vaccines in cancer therapy. Oncoimmunology 2: E26621.
2. Watkins, S. K., Z. Zhu, E. Riboldi, K. A. Shafer-Weaver, K. E. Stagliano, M. M. Sklavos, S. Ambs, H. Yagita, and A. A. Hurwitz. 2011. FOXO3 programs tumor-associated DCs to become tolerogenic in human and murine prostate cancer. J. Clin. Invest. 121: 1361-1372.
3. Norian, L. A., P. C. Rodriguez, L. A. O'Mara, J. Zabaleta, A. C. Ochoa, M. Cella, and P. M. Allen. 2009. Tumor-infiltrating regulatory dendritic cells inhibit CD8+ T cell function via L-arginine metabolism. Cancer Res. 69: 3086-3094.
4. Hargadon, K. M. 2013. Tumor-altered dendritic cell function: implications for anti-tumor immunity. Front. Immunol. 4: 192.
5. Shurin, G. V., Y. Ma, and M. R. Shurin. 2013. Immunosuppressive mechanisms of regulatory dendritic cells in cancer. Cancer Microenviron. 6: 159-167.
6. Luo, Z., C. Wang, H. Yi, P. Li, H. Pan, L. Liu, L. Cai, and Y. Ma. 2015. Nanovaccine loaded with poly I:C and STAT3 siRNA robustly elicits anti-tumor immune responses through modulating tumor-associated dendritic cells in vivo. Biomaterials 38: 50-60.
7. Topalian, S. L., J. D. Wolchok, T. A. Chan, I. Mellman, K. Palucka, J. Banchereau, S. A. Rosenberg, and K. Dane Wittrup. 2015. Immunotherapy: The path to win the war on cancer? Cell 161: 185-186.
8. Baxevanis, C. N., I. F. Voutsas, and O. E. Tsitsilonis. 2013. Toll-like receptor agonists: current status and future perspective on their utility as adjuvants in improving anticancer vaccination strategies. Immunotherapy 5: 497-511.
9. Tran Janco, J. M., P. Lamichhane, L. Karyampudi, and K. L. Knutson. 2015. Tumorinfiltrating dendritic cells in cancer pathogenesis. J. Immunol. 194: 2985-2991.
10. Idoyaga, J., J. Moreno, and L. Bonifaz. 2007. Tumor cells prevent mouse dendritic cell maturation induced by TLR ligands. Cancer Immunol. Immunother. 56: 1237-1250.
11. Djuranovic, S., A. Nahvi, and R. Green. 2011. A parsimonious model for gene regulation by miRNAs. Science 331: 550-553.
12. Bartel, D. P. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
13. O'Connell, R. M., D. S. Rao, A. A. Chaudhuri, and D. Baltimore. 2010. Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10: 111-122.
14. Xia, J., X. Guo, J. Yan, and K. Deng. 2014. The role of miR-148a in gastric cancer. J. Cancer Res. Clin. Oncol. 140: 1451-1456.
15. Lombard, A. P., B. A. Mooso, S. J. Libertini, R. M. Lim, R. M. Nakagawa, K. D. Vidallo, N. C. Costanzo, P. M. Ghosh, and M. Dmudryj. 2015. The miR- 148a dependent apoptosis of bladder cancer cells is mediated in part by the epigenetic modifier DNMT1. Mol. Carcinog. 55: 757-767.
16. Li, C., P. J. Ebert, and Q. J. Li. 2013. T cell receptor (TCR) and transforming growth factor b (TGF-b) signaling converge on DNA (cytosine-5)- methyltransferase to control forkhead box protein 3 (foxp3) locus methylation and inducible regulatory T cell differentiation. J. Biol. Chem. 288: 19127-19139.
17. Liu, X., Z. Zhan, L. Xu, F. Ma, D. Li, Z. Guo, N. Li, and X. Cao. 2010. MicroRNA-148/152 impair innate response and antigen presentation of TLRtriggered dendritic cells by targeting CaMKIIa. J. Immunol. 185: 7244-7251.
18. Wolffe, A. P., and M. A. Matzke. 1999. Epigenetics: Regulation through repression. Science 286: 481-486.
19. Gal-Yam, E. N., Y. Saito, G. Egger, and P. A. Jones. 2008. Cancer epigenetics: modifications, screening, and therapy. Annu. Rev. Med. 59: 267-280.
20. Lay, F. D., Y. Liu, T. K. Kelly, H. Witt, P. J. Farnham, P. A. Jones, and B. P. Berman. 2015. The role of DNA methylation in directing the functional organization of the cancer epigenome. Genome Res. 25: 467-477.
21. Zhang, X., A. Ulm, H. K. Somineni, S. Oh, M. T. Weirauch, H. X. Zhang, X. Chen, M. A. Lehn, E. M. Janssen, and H. Ji. 2014. DNA methylation dynamics during ex vivo differentiation and maturation of human dendritic cells. Epigenetics Chromatin 7: 21.
22. Deng, J., N. Gao, Y. Wang, H. Yi, S. Fang, Y. Ma, and L. Cai. 2012. Selfassembled cationic micelles based on PEG-PLL-PLLeu hybrid polypeptides as highly effective gene vectors. Biomacromolecules 13: 3795-3804.
23. Herman, J. G., J. R. Graff, S. Myöhänen, B. D. Nelkin, and S. B. Baylin. 1996. Methylation-specific PCR: A novel PCR assay for methylation status of CpG islands. Proc. Natl. Acad. Sci. USA 93: 9821-9826.
24. Wang, C., Y. Zhuang, Y. Zhang, Z. Luo, N. Gao, P. Li, H. Pan, L. Cai, and Y. Ma. 2012. Toll-like receptor 3 agonist complexed with cationic liposome augments vaccine-elicited antitumor immunity by enhancing TLR3-IRF3 signaling and type I interferons in dendritic cells. Vaccine 30: 4790-4799.
25. Harimoto, H., M. Shimizu, Y. Nakagawa, K. Nakatsuka, A. Wakabayashi, C. Sakamoto, and H. Takahashi. 2013. Inactivation of tumor-specific CD8? CTLs by tumor-infiltrating tolerogenic dendritic cells. Immunol. Cell Biol. 91: 545-555.
26. Stepanek, I., M. Indrova, J. Bieblova, J. Fucikova, R. Spisek, J. Bubenik, and M. Reinis. 2011. Effects of 5-azacytidine and trichostatin A on dendritic cell maturation. J. Biol. Regul. Homeost. Agents 25: 517-529.
27. Frikeche, J., A. Clavert, J. Delaunay, E. Brissot, M. Grégoire, B. Gaugler, and M. Mohty. 2011. Impact of the hypomethylating agent 5-azacytidine on dendritic cells function. Exp. Hematol. 39: 1056-1063.
28. Lujambio, A., G. A. Calin, A. Villanueva, S. Ropero, M. Sánchez-Céspedes, D. Blanco, L. M. Montuenga, S. Rossi, M. S. Nicoloso, W. J. Faller, et al. 2008. A microRNA DNA methylation signature for human cancer metastasis. Proc. Natl. Acad. Sci. USA 105: 13556-13561.
29. Kinjyo, I., T. Hanada, K. Inagaki-Ohara, H. Mori, D. Aki, M. Ohishi, H. Yoshida, M. Kubo, and A. Yoshimura. 2002. SOCS1/JAB is a negative regulator of LPS induced macrophage activation. Immunity 17: 583-591.
30. Dai, X., K. Sayama, K. Yamasaki, M. Tohyama, Y. Shirakata, Y. Hanakawa, S. Tokumaru, Y. Yahata, L. Yang, A. Yoshimura, and K. Hashimoto. 2006. SOCS1-negative feedback of STAT1 activation is a key pathway in the dsRNA induced innate immune response of human keratinocytes. J. Invest. Dermatol. 126: 1574-1581.
31. Luo, Z., P. Li, J. Deng, N. Gao, Y. Zhang, H. Pan, L. Liu, C. Wang, L. Cai, and Y. Ma. 2013. Cationic polypeptide micelle-based antigen delivery system: A simple and robust adjuvant to improve vaccine efficacy. J. Control. Release 170: 259-267.
32. Hurwitz, A. A., and S. K. Watkins. 2012. Immune suppression in the tumor microenvironment: A role for dendritic cell-mediated tolerization of T cells. Cancer Immunol. Immunother. 61: 289-293.
33. Alizadeh, D., and N. Larmonier. 2014. Chemotherapeutic targeting of cancerinduced immunosuppressive cells. Cancer Res. 74: 2663-2668.
34. Restifo, N. P., M. E. Dudley, and S. A. Rosenberg. 2012. Adoptive immunotherapy for cancer: harnessing the T cell response. Nat. Rev. Immunol. 12: 269-281.
35. Pampena, M. B., and E. M. Levy. 2015. Natural killer cells as helper cells in dendritic cell cancer vaccines. Front. Immunol. 6: 13.
36. Fraszczak, J., M. Trad, N. Janikashvili, D. Cathelin, D. Lakomy, V. Granci, A. Morizot, S. Audia, O. Micheau, L. Lagrost, et al. 2010. Peroxynitritedependent killing of cancer cells and presentation of released tumor antigens by activated dendritic cells. J. Immunol. 184: 1876-1884.
37. Nefedova, Y., M. Huang, S. Kusmartsev, R. Bhattacharya, P. Cheng, R. Salup, R. Jove, and D. Gabrilovich. 2004. Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. J. Immunol. 172: 464-474.
38. Maurya, N., R. Gujar, M. Gupta, V. Yadav, S. Verma, and P. Sen. 2014. Immunoregulation of dendritic cells by the receptor T cell Ig and mucin protein-3 via Bruton's tyrosine kinase and c-Src. J. Immunol. 193: 3417-3425.
39. Chiba, S., M. Baghdadi, H. Akiba, H. Yoshiyama, I. Kinoshita, H. Dosaka-Akita, Y. Fujioka, Y. Ohba, J. V. Gorman, J. D. Colgan, et al. 2012. Tumor-infiltrating DCs suppress nucleic acid-mediated innate immune responses through interactions between the receptor TIM-3 and the alarmin HMGB1. Nat. Immunol. 13: 832-842.
40. Smyth, L. A., D. A. Boardman, S. L. Tung, R. Lechler, and G. Lombardi. 2015. MicroRNAs affect dendritic cell function and phenotype. Immunology 144: 197-205.
41. Karrich, J. J., L. C. Jachimowski, M. Libouban, A. Iyer, K. Brandwijk, E. W. Taanman-Kueter, M. Nagasawa, E. C. de Jong, C. H. Uittenbogaart, and B. Blom. 2013. MicroRNA-146a regulates survival and maturation of human plasmacytoid dendritic cells. Blood 122: 3001-3009.
42. Sun, Y., J. Sun, T. Tomomi, E. Nieves, N. Mathewson, H. Tamaki, R. Evers, and P. Reddy. 2013. PU.1-dependent transcriptional regulation of miR-142 contributes to its hematopoietic cell-specific expression and modulation of IL-6. J. Immunol. 190: 4005-4013.
43. Zheng, J., H. Y. Jiang, J. Li, H. C. Tang, X. M. Zhang, X. R. Wang, J. T. Du, H. B. Li, and G. Xu. 2012. MicroRNA-23b promotes tolerogenic properties of dendritic cells in vitro through inhibiting Notch1/NF-kB signalling pathways. Allergy 67: 362-370.
44. Xue, X., T. Feng, S. Yao, K. J. Wolf, C. G. Liu, X. Liu, C. O. Elson, and Y. Cong. 2011. Microbiota downregulates dendritic cell expression of miR-10a, which targets IL-12/IL-23p40. J. Immunol. 187: 5879-5886.
45. Pyfferoen, L., P. Mestdagh, K. Vergote, N. De Cabooter, J. Vandesompele, B. N. Lambrecht, and K. Y. Vermaelen. 2014. Lung tumours reprogram pulmonary dendritic cell immunogenicity at the microRNA level. Int. J. Cancer 135: 2868-2877.
46. Min, S., X. Liang, M. Zhang, Y. Zhang, S. Mei, J. Liu, J. Liu, X. Su, S. Cao, X. Zhong, et al. 2013. Multiple tumor-associated microRNAs modulate the survival and longevity of dendritic cells by targeting YWHAZ and Bcl2 signaling pathways. J. Immunol. 190: 2437-2446.
47. Xu, Q., Y. Jiang, Y. Yin, Q. Li, J. He, Y. Jing, Y. T. Qi, Q. Xu, W. Li, B. Lu, et al. 2013. A regulatory circuit of miR-148a/152 and DNMT1 in modulating cell transformation and tumor angiogenesis through IGF-IR and IRS1. J. Mol. Cell Biol. 5: 3-13.
48. Cheng, C., C. Huang, T. T. Ma, E. B. Bian, Y. He, L. Zhang, and J. Li. 2014. SOCS1 hypermethylation mediated by DNMT1 is associated with lipopolysaccharide-induced inflammatory cytokines in macrophages. Toxicol. Lett. 225: 488-497.
49. Rothschild, S. I. 2014. MicroRNA therapies in cancer. Mol. Cell. Ther. 2: 7.
50. Yin, H., R. L. Kanasty, A. A. Eltoukhy, A. J. Vegas, J. R. Dorkin, and D. G. Anderson. 2014. Non-viral vectors for gene-based therapy. Nat. Rev. Genet. 15: 541-555.
51. Cui, T. X., I. Kryczek, L. Zhao, E. Zhao, R. Kuick, M. H. Roh, L. Vatan, W. Szeliga, Y. Mao, D. G. Thomas, et al. 2013. Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2. Immunity 39: 611-621.
52. Wan, S., E. Zhao, I. Kryczek, L. Vatan, A. Sadovskaya, G. Ludema, D. M. Simeone, W. Zou, and T. H. Welling. 2014. Tumor-associated macrophages produce interleukin 6 and signal via STAT3 to promote expansion of human hepatocellular carcinoma stem cells. Gastroenterology 147: 1393-1404.
53. Kalinski, P., A. Giermasz, Y. Nakamura, P. Basse, W. J. Storkus, J. M. Kirkwood, and R. B. Mailliard. 2005. Helper role of NK cells during the induction of anticancer responses by dendritic cells. Mol. Immunol. 42: 535-539.