Engineering DNA nanoparticles as immunomodulatory reagents that activate regulatory T cells

Journal of Immunology

Volumn 188, Issue 10, 2012, Pages 4913-4920

  Huang, Lei ^a   Lemos, Henrique P ^a   Li, Ngqian ^a   Li, MingHui ^a   Chandler, Phillip R ^a   Baban, Babak ^a   McGaha, Tracy L ^a   Ravishankar, Buvana ^a   Lee, Jeffrey R ^a,b   Munn, David H ^a   Mellor, Andrew L ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA BETA INTERFERON RECEPTOR; CD19 ANTIGEN; DNA; ENZYME; GAMMA INTERFERON; IDO ENZYME; INTERFERON RECEPTOR; NANOPARTICLE; PLASMID DNA; POLYETHYLENEIMINE; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN SPECIFICITY; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; DRUG ACTIVITY; DRUG POTENCY; ENZYME ACTIVITY; FEMALE; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOSTIMULATION; INFLAMMATION; LYMPHOCYTE ACTIVATION; LYMPHOCYTE PROLIFERATION; LYMPHOID TISSUE; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; SIGNAL TRANSDUCTION; UPREGULATION;

ANIMALS; ARTHRITIS, EXPERIMENTAL; ARTHRITIS, RHEUMATOID; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; DNA, BACTERIAL; GENETIC ENGINEERING; IMMUNOLOGIC FACTORS; IMMUNOPHENOTYPING; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NANOPARTICLES; POLYDEOXYRIBONUCLEOTIDES; POLYETHYLENEIMINE; T-LYMPHOCYTES, REGULATORY;

EID: 84861175030     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1103668     Document Type: Article

References (35)

1. Kawakami, S., Y. Ito, P. Charoensit, F. Yamashita, and M. Hashida. 2006. Evaluation of proinflammatory cytokine production induced by linear and branched polyethylenimine/plasmid DNA complexes in mice. J. Pharmacol. Exp. Ther. 317: 1382-1390. (Pubitemid 43764145)
2. Intra, J., and A. K. Salem. 2008. Characterization of the transgene expression generated by branched and linear polyethylenimine-plasmid DNA nanoparticles in vitro and after intraperitoneal injection in vivo. J. Control. Release 130: 129-138.
3. Günther, M., J. Lipka, A. Malek, D. Gutsch, W. Kreyling, and A. Aigner. 2011. Polyethylenimines for RNAi-mediated gene targeting in vivo and siRNA delivery to the lung. Eur. J. Pharm. Biopharm. 77: 438-449.
4. Chen, H., P. Li, Y. Yin, X. Cai, Z. Huang, J. Chen, L. Dong, and J. Zhang. 2010. The promotion of type 1 T helper cell responses to cationic polymers in vivo via toll-like receptor-4 mediated IL-12 secretion. Biomaterials 31: 8172-8180.
5. Rodrigo-Garzón, M., P. Berraondo, L. Ochoa, J. J. Zulueta, and G. González- Aseguinolaza. 2010. Antitumoral efficacy of DNA nanoparticles in murine models of lung cancer and pulmonary metastasis. Cancer Gene Ther. 17: 20-27.
6. Leslie, M. 2011. Immunology. Regulatory T cells get their chance to shine. Science 332: 1020-1021.
7. Phillips, B., M. Trucco, and N. Giannoukakis. 2011. Current state of type 1 diabetes immunotherapy: incremental advances, huge leaps, or more of the same? Clin. Dev. Immunol. 2011: 432016.
8. Baban, B., P. R. Chandler, B. A. Johnson, III, L. Huang, M. Li, M. L. Sharpe, L. M. Francisco, A. H. Sharpe, B. R. Blazar, D. H. Munn, and A. L. Mellor. 2011. Physiologic control of IDO competence in splenic dendritic cells. J. Immunol. 187: 2329-2335.
9. Baban, B., P. R. Chandler, M. D. Sharma, J. Pihkala, P. A. Koni, D. H. Munn, and A. L. Mellor. 2009. IDO activates regulatory T cells and blocks their conversion into Th17-like T cells. J. Immunol. 183: 2475-2483.
10. Munn, D. H., M. D. Sharma, D. Hou, B. Baban, J. R. Lee, S. J. Antonia, J. L. Messina, P. Chandler, P. A. Koni, and A. L. Mellor. 2004. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J. Clin. Invest. 114: 280-290. (Pubitemid 39071633)
11. Sharma, M. D., B. Baban, P. Chandler, D. Y. Hou, N. Singh, H. Yagita, M. Azuma, B. R. Blazar, A. L. Mellor, and D. H. Munn. 2007. Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2,3-dioxygenase. J. Clin. Invest. 117: 2570-2582. (Pubitemid 47494358)
12. Sharma, M. D., D. Y. Hou, B. Baban, P. A. Koni, Y. He, P. R. Chandler, B. R. Blazar, A. L. Mellor, and D. H. Munn. 2010. Reprogrammed foxp3(+) regulatory T cells provide essential help to support cross-presentation and CD8(+) T cell priming in naive mice. Immunity 33: 942-954.
13. Jasperson, L. K., C. Bucher, A. Panoskaltsis-Mortari, A. L. Mellor, D. H. Munn, and B. R. Blazar. 2009. Inducing the tryptophan catabolic pathway, indoleamine 2,3-dioxygenase (IDO), for suppression of graft-versus-host disease (GVHD) lethality. Blood 114: 5062-5070.
14. Grohmann, U., C. Orabona, F. Fallarino, C. Vacca, F. Calcinaro, A. Falorni, P. Candeloro, M. L. Belladonna, R. Bianchi, M. C. Fioretti, and P. Puccetti. 2002. CTLA-4-Ig regulates tryptophan catabolism in vivo. Nat. Immunol. 3: 1097-1101. (Pubitemid 35363664)
15. Ciorba, M. A., E. E. Bettonville, K. G. McDonald, R. Metz, G. C. Prendergast, R. D. Newberry, and W. F. Stenson. 2010. Induction of IDO-1 by immunostimulatory DNA limits severity of experimental colitis. J. Immunol. 184: 3907-3916.
16. Liu, H., L. Liu, K. Liu, P. Bizargity, W. W. Hancock, and G. A. Visner. 2009. Reduced cytotoxic function of effector CD8+ T cells is responsible for indoleamine 2,3-dioxygenase-dependent immune suppression. J. Immunol. 183: 1022-1031.
17. Johnson, B. A., III, B. Baban, and A. L. Mellor. 2009. Targeting the immunoregulatory indoleamine 2,3 dioxygenase pathway in immunotherapy. Immunotherapy 1: 645-661.
18. Laich, A., G. Neurauter, B. Widner, and D. Fuchs. 2002. More rapid method for simultaneous measurement of tryptophan and kynurenine by HPLC. Clin. Chem. 48: 579-581. (Pubitemid 34174597)
19. Hoshi, M., K. Saito, A. Hara, A. Taguchi, H. Ohtaki, R. Tanaka, H. Fujigaki, Y. Osawa, M. Takemura, H. Matsunami, et al. 2010. The absence of IDO upregulates type I IFN production, resulting in suppression of viral replication in the retrovirus-infected mouse. J. Immunol. 185: 3305-3312.
20. Tyring, S., W. R. Fleischmann, Jr., and S. Baron. 1986. A convenient microassay for cytolysis and cytostasis. Methods Enzymol. 119: 574-579. (Pubitemid 16025160)
21. Hou, D. Y., A. J. Muller, M. D. Sharma, J. DuHadaway, T. Banerjee, M. Johnson, A. L. Mellor, G. C. Prendergast, and D. H. Munn. 2007. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyltryptophan correlates with antitumor responses. Cancer Res. 67: 792-801. (Pubitemid 46192220)
22. Mellor, A. L., B. Baban, P. R. Chandler, A. Manlapat, D. J. Kahler, and D. H. Munn. 2005. Cutting edge: CpG oligonucleotides induce splenic CD19+ dendritic cells to acquire potent indoleamine 2,3-dioxygenase-dependent T cell regulatory functions via IFN Type 1 signaling. J. Immunol. 175: 5601-5605. (Pubitemid 41508038)
23. Johnson, B. A., III, D. J. Kahler, B. Baban, P. R. Chandler, B. Kang, M. Shimoda, P. A. Koni, J. Pihkala, B. Vilagos, M. Busslinger, et al. 2010. Blymphoid cells with attributes of dendritic cells regulate T cells via indoleamine 2,3-dioxygenase. Proc. Natl. Acad. Sci. USA 107: 10644-10648.
24. McGaha, T. L., Y. Chen, B. Ravishankar, N. van Rooijen, and M. C. Karlsson. 2011. Marginal zone macrophages suppress innate and adaptive immunity to apoptotic cells in the spleen. Blood 117: 5403-5412.
25. Baban, B., P. Chandler, D. McCool, B. Marshall, D. H. Munn, and A. L. Mellor. 2004. Indoleamine 2,3-dioxygenase expression is restricted to fetal trophoblast giant cells during murine gestation and is maternal genome specific. J. Reprod. Immunol. 61: 67-77. (Pubitemid 38446980)
26. Lemos, H. P., R. Grespan, S. M. Vieira, T. M. Cunha, W. A. Verri, Jr., K. S. Fernandes, F. O. Souto, I. B. McInnes, S. H. Ferreira, F. Y. Liew, and F. Q. Cunha. 2009. Prostaglandin mediates IL-23/IL-17-induced neutrophil migration in inflammation by inhibiting IL-12 and IFNgamma production. Proc. Natl. Acad. Sci. USA 106: 5954-5959.
27. Teige, A., R. Bockermann, M. Hasan, K. E. Olofsson, Y. Liu, and S. Issazadeh- Navikas. 2010. CD1d-dependent NKT cells play a protective role in acute and chronic arthritis models by ameliorating antigen-specific Th1 responses. J. Immunol. 185: 345-356.
28. Baban, B., A. M. Hansen, P. R. Chandler, A. Manlapat, A. Bingaman, D. J. Kahler, D. H. Munn, and A. L. Mellor. 2005. A minor population of splenic dendritic cells expressing CD19 mediates IDO-dependent T cell suppression via type I IFN signaling following B7 ligation. Int. Immunol. 17: 909-919. (Pubitemid 41417958)
29. Pestka, S., S. V. Kotenko, G. Muthukumaran, L. S. Izotova, J. R. Cook, and G. Garotta. 1997. The interferon gamma (IFN-gamma) receptor: a paradigm for the multichain cytokine receptor. Cytokine Growth Factor Rev. 8: 189-206. (Pubitemid 28077927)
30. Ehst, B. D., E. Ingulli, and M. K. Jenkins. 2003. Development of a novel transgenic mouse for the study of interactions between CD4 and CD8 T cells during graft rejection. Am. J. Transplant. 3: 1355-1362. (Pubitemid 37288079)
31. Huang, L., B. Baban, B. A. Johnson, III, and A. L. Mellor. 2010. Dendritic cells, indoleamine 2,3 dioxygenase and acquired immune privilege. Int. Rev. Immunol. 29: 133-155.
32. Ishikawa, H., Z. Ma, and G. N. Barber. 2009. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461: 788-792.
33. Yang, P., H. An, X. Liu, M. Wen, Y. Zheng, Y. Rui, and X. Cao. 2010. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat. Immunol. 11: 487-494.
34. Fernandes-Alnemri, T., J. W. Yu, C. Juliana, L. Solorzano, S. Kang, J. Wu, P. Datta, M. McCormick, L. Huang, E. McDermott, et al. 2010. The AIM2 inflammasome is critical for innate immunity to Francisella tularensis. Nat. Immunol. 11: 385-393.
35. Barbalat, R., S. E. Ewald, M. L. Mouchess, and G. M. Barton. 2011. Nucleic acid recognition by the innate immune system. Annu. Rev. Immunol. 29: 185-214.