Targeted siRNA silencing of indoleamine 2, 3-dioxygenase in antigen-presenting cells using mannose-conjugated liposomes: A novel strategy for treatment of melanoma

Journal of Immunotherapy

Volumn 37, Issue 2, 2014, Pages 123-134

  Chen, Di ^a,c   Koropatnick, James ^a,b,c   Jiang, Nan ^a   Zheng, Xiufen ^a,b   Zhang, Xusheng ^a   Wang, Hongmei ^d   Yuan, Keng ^d   Siu, King Sun ^a,c   Shunnar, Aminah ^a   Way, Colin ^a,c   Min, Wei Ping ^a,b,c,d  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^c LONDON REGIONAL CANCER PROGRAM   (Canada)

^d NANCHANG UNIVERSITY   (China)

Author keywords

antigen presenting cells; IDO; liposome; mannose; siRNA

Indexed keywords

ANIMALS; ANTIGEN-PRESENTING CELLS; ANTIGENS, NEOPLASM; DENDRITIC CELLS; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; LECTINS, C-TYPE; LIPOSOMES; LYMPH NODES; LYMPHOCYTE ACTIVATION; MANNOSE-BINDING LECTINS; MELANOMA; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; NEOPLASM TRANSPLANTATION; RECEPTORS, CELL SURFACE; RNA INTERFERENCE; RNA, SMALL INTERFERING; SKIN NEOPLASMS; SPLEEN; T-LYMPHOCYTES; TUMOR BURDEN;

EID: 84894435140     PISSN: 15249557     EISSN: 15374513     Source Type: Journal    
DOI: 10.1097/CJI.0000000000000022     Document Type: Article

References (55)

1. Lob S,Ko nigsrainer A. Role of IDO in organ transplantation: promises and difficulties. Int Rev Immunol. 2009;28:185-206.
2. Macchiarulo A, Camaioni E, Nuti R, et al. Highlights at the gate of tryptophan catabolism: a review on the mechanisms of activation and regulation of indoleamine 2,3-dioxygenase (IDO), a novel target in cancer disease. Amino Acids. 2008;37: 219-229.
3. Lee GK, Park HJ, Macleod M, et al. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology. 2002;107:452-460.
4. Munn DH, Shafizadeh E, Attwood JT, et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med. 1999;189:1363-1372.
5. Fallarino F, Grohmann U, Vacca C, et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ. 2002;9:1069-1077.
6. Lob S, Ko nigsrainer A, Rammensee H-G, et al. Inhibitors of indoleamine-2,3-dioxygenase for cancer therapy: can we see the wood for the trees? Nat Rev Cancer. 2009;9:445-452.
7. Chen W, Liang X, Peterson AJ, et al. The indoleamine 2,3- dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol. 2008;181:5396-5404.
8. Munn DH. Expression of indoleamine 2,3-dioxygenase by plasmacytoid dendritic cells in tumor-draining lymph nodes. J Clini Investig. 2004;114:280-290.
9. Mao C-P, Lin Y-Y, Hung C-F, et al. Immunological research using RNA interference technology. Immunology. 2007;121: 295-307.
10. Tiemann K, Rossi JJ. RNAi-based therapeutics-current status, challenges and prospects. EMBO Mol Med. 2009;1: 142-151.
11. Ritprajak P, Hashiguchi M, Azuma M. Topical application of cream-emulsified CD86 siRNA ameliorates allergic skin disease by targeting cutaneous dendritic cells. Mol Ther. 2008; 16:1323-1330.
12. Keler T, Ramakrishna V, Fanger MW. Mannose receptortargeted vaccines. Expert Opin Biol Ther. 2004;4:1953-1962.
13. Figdor CG, van Kooyk Y, Adema GJ. C-type lectin receptors on dendritic cells and Langerhans cells. Nat Rev Immunol. 2002;2:77-84.
14. Gijzen K, Cambi A, Torensma R, et al. C-type lectins on dendritic cells and their interaction with pathogen-derived and endogenous glycoconjugates. Curr Protein Pept Sci. 2006;7: 283-294.
15. Taylor P, Gordon S, Martinezpomares L. The mannose receptor: linking homeostasis and immunity through sugar recognition. Trend Immunol. 2005;26:104-110.
16. Engering AJ, Cella M, Fluitsma D, et al. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells. Eur J Immunol. 1997; 27:2417-2425.
17. Flynn JL, Chan J. Immunology of tuberculosis. Annu Rev Immunol. 2001;19:93-129.
18. Irache JM, Salman HH, Gamazo C, et al. Mannose-targeted systems for the delivery of therapeutics. Expert Opin Drug Deliv. 2008;5:703-724.
19. Reddy P, Sun Y, Toubai T, et al. Histone deacetylase inhibition modulates indoleamine 2,3-dioxygenase-dependent DC functions and regulates experimental graft-versus-host disease in mice. J Clin Invest. 2008;118:2562-2573.
20. Hill JA, Ichim TE, Kusznieruk KP, et al. Immune modulation by silencing IL-12 production in dendritic cells using small interfering RNA. J Immunol. 2003;171:691-696.
21. Li SD, Huang L. Targeted delivery of antisense oligodeoxynucleotide and small interference RNA into lung cancer cells. Mol Pharm. 2006;3:579-588.
22. Zheng X, Suzuki M, Zhang X, et al. RNAi-mediated CD40- CD154 interruption promotes tolerance in autoimmune arthritis. Arthritis Res Ther. 2010;12:1-10.
23. Schnurr M, Galambos P, Scholz C, et al. Tumor cell lysatepulsed human dendritic cells induce a T-cell response against pancreatic carcinoma cells: an in vitro model for the assessment of tumor vaccines. Cancer Res. 2001;61:6445-6450.
24. Burnett JC, Rossi JJ, Tiemann K. Current progress of siRNA/ shRNA therapeutics in clinical trials. Biotechnol J. 2011;6: 1130-1146.
25. Weitman SD, Lark RH, Coney LR, et al. Distribution of the folate receptor GP38 in normal and malignant cell lines and tissues. Cancer Res. 1992;52:3396-3401.
26. Kamaly N, Kalber T, Thanou M, et al. Folate receptor targeted bimodal liposomes for tumor magnetic resonance imaging. Bioconjug Chem. 2009;20:648-655.
27. Schroeder A, Levins CG, Cortez C, et al. Lipid-based nanotherapeutics for siRNA delivery. J Intern Med. 2010;267: 9-21.
28. Engering AJ CM, Fluitsma D, Brockhaus M, et al. The mannose receptor functions as a high capacity and broad specificity antigen receptor in human dendritic cells.pdf. Eur J Immunol. 1997;27:2417-2425.
29. Terness P, Bauer TM, Rose L, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med. 2002;196:447-457.
30. Katz JB, Muller AJ, Prendergast GC. Indoleamine 2,3- dioxygenase in T-cell tolerance and tumoral immune escape. Immunol Rev. 2008;222:206-221.
31. Prendergast GC, Metz R, Muller AJ. IDO recruits Tregs in melanoma. Cell Cycle. 2009;8:1818-1819.
32. Prendergast GC. Immune escape as a fundamental trait of cancer: focus on IDO. Oncogene. 2008;27:3889-3900.
33. Hou DY, Muller AJ, Sharma MD, et al. Inhibition of indoleamine 2,3-dioxygenase in dendritic cells by stereoisomers of 1-methyl-tryptophan correlates with antitumor responses. Cancer Res. 2007;67:792-801.
34. Grohmann U, Fallarino F, Bianchi R, et al. IL-6 inhibits the tolerogenic function of CD8 alpha+ dendritic cells expressing indoleamine 2,3-dioxygenase. J Immunol. 2001;167:708-714.
35. Lee JH, Chen Y, Chan JL, et al. Molecular analysis of melanoma-induced sentinel lymph node immune dysfunction. Cancer Immunol Immunother. 2011;60:685-692.
36. Gajewski TF. Failure at the effector phase: immune barriers at the level of the melanoma tumor microenvironment. Clin Cancer Res. 2007;13:5256-5261.
37. Yano J, Hirabayashi K, Nakagawa S, et al. Antitumor activity of small interfering RNA/cationic liposome complex in mouse models of cancer. Clin Cancer Res. 2004;10:7721-7726.
38. Davidson BL, McCray PB. Current prospects for RNA interference-based therapies. Nat Rev Genet. 2011;12: 329-340.
39. Jiang N, Zhang X, Zheng X, et al. Targeted gene silencing of TLR4 using liposomal nanoparticles for preventing liver ischemia reperfusion injury. Am J Transplant. 2011;11: 1835-1844.
40. Hattori Y, Kawakami S, Suzuki S, et al. Enhancement of immune responses by DNA vaccination through targeted gene delivery using mannosylated cationic liposome formulations following intravenous administration in mice. Biochem Biophys Res Commun. 2004;317:992-999.
41. Engering A, Geijtenbeek TB, van Vliet SJ, et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol. 2002;168:2118-2126.
42. Barenholz A, Hovav AH, Fishman Y, et al. A peptide mimetic of the mycobacterial mannosylated lipoarabinomannan: characterization and potential applications. J Med Microbiol. 2007;56:579-586.
43. Uyttenhove C, Pilotte L, Theate I, et al. Evidence for a tumoral immune resistance mechanism based on tryptophan degradation by indoleamine 2,3-dioxygenase. Nat Med. 2003;9:1269-1274.
44. Lee Jr. Pattern of recruitment of immunoregulatory antigenpresenting cells in malignant melanoma. Lab Investig. 2003;83:1457-1466.
45. Di Pucchio T, Chatterjee B, Smed-So rensen A, et al. Direct proteasome-independent cross-presentation of viral antigen by plasmacytoid dendritic cells on major histocompatibility complex class I. Nature Immunology. 2008;9:551-557.
46. MacKenzie CR, Hadding U, Daubener W. Interferon-gammainduced activation of indoleamine 2,3-dioxygenase in cord blood monocyte-derived macrophages inhibits the growth of group B streptococci. J Infect Dis. 1998;178:875-878.
47. Leonhardt RM, Lee SJ, Kavathas PB, et al. Severe tryptophan starvation blocks onset of conventional persistence and reduces reactivation of Chlamydia trachomatis. Infect Immun. 2007;75: 5105-5117.
48. Munn DH, Shafizadeh E, Attwood JT, et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med. 1999;189:1363-1372.
49. Lee GK, Park HJ, Macleod M, et al. Tryptophan deprivation sensitizes activated T cells to apoptosis prior to cell division. Immunology. 2002;107:452-460.
50. Grohmann U, Fallarino F, Bianchi R, et al. IL-6 inhibits the tolerogenic function of CD8 alpha+ dendritic cells expressing indoleamine 2,3-dioxygenase. J Immunol. 2001;167:708-714.
51. Munn DH, Sharma MD, Baban B, et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity. 2005; 22:633-642.
52. Frumento G, Rotondo R, Tonetti M, et al. Tryptophanderived catabolites are responsible for inhibition of t and natural killer cell proliferation induced by indoleamine 2,3- dioxygenase. J Exp Med. 2002;196:459-468.
53. Fallarino F, Grohmann U, Vacca C, et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ. 2002;9:1069-1077.
54. Espinosa E, Berrocal A, Lopez Martin JA, et al. Advances in cutaneous melanoma. Clin Transl Oncol. 2012;14:325-332.
55. Akasaki Y, Liu G, Chung NH, et al. Induction of a CD4+ T regulatory type 1 response by cyclooxygenase-2-overexpressing glioma. J Immunol. 2004;173:4352-4359.