Nonviral delivery of small interfering RNA into pancreas-associated immune cells prevents autoimmune diabetes

Molecular Therapy

Volumn 20, Issue 12, 2012, Pages 2315-2325

  Leconet, Wilhem ^a,c   Petit, Pierre ^b   Peraldi Roux, Sylvie ^b   Bresson, Damien ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^b CNRS   (France)

^c INSTITUT DE RECHERCHE EN CANCÉROLOGIE DE MONTPELLIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONATE 15 LIPOXYGENASE; CD11B ANTIGEN; CHEMOKINE RECEPTOR CXCR3; GAMMA INTERFERON INDUCIBLE PROTEIN 10; LIPID; LIPOSOME; MESSENGER RNA; POLYETHYLENEIMINE; PROGRAMMED DEATH 1 LIGAND 1; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARACHIDONATE 15 LIPOXYGENASE GENE; ARTICLE; AUTOIMMUNE DISEASE; CHEMOKINE RECEPTOR CXCR3 GENE; CONTROLLED STUDY; DOWN REGULATION; DRUG EFFECT; DRUG EFFICACY; DRUG TARGETING; FEMALE; GAMMA INTERFERON INDUCIBLE PROTEIN 10 GENE; GENE EXPRESSION REGULATION; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; INSULIN DEPENDENT DIABETES MELLITUS; MACROPHAGE; MOUSE; NONHUMAN; NONVIRAL GENE DELIVERY SYSTEM; NONVIRAL GENE THERAPY; PANCREAS; PHENOTYPE; PREVENTION STUDY; REGULATORY T LYMPHOCYTE; SHORT COURSE THERAPY; SIGNAL TRANSDUCTION; UPREGULATION; WILD TYPE;

MUS;

EID: 84870583382     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2012.190     Document Type: Article

References (50)

1. Bresson, D and von Herrath, M (2004). Mechanisms underlying type 1 diabetes. Drug Discov Today Dis Mech 1: 321-327.
2. van Belle, TL, Coppieters, KT and von Herrath, MG (2011). Type 1 diabetes: etiology, immunology, and therapeutic strategies. Physiol Rev 91: 79-118 (doi: 10.1152/ physrev.00003.2010).
3. .von Herrath, M, Sanda, S and Herold, K (2007). Type 1 diabetes as a relapsingremitting disease? Nat Rev Immunol 7: 988-994.
4. .von Herrath, M, Rottembourg, D and Bresson, D (2006). Progress in the development of immune-based therapies for type 1 diabetes mellitus. BioDrugs 20: 341-350.
5. .Kim, DH and Rossi, JJ (2007). Strategies for silencing human disease using RNA interference. Nat Rev Genet 8: 173-184.
6. .Davidson, BL and McCray, PB Jr (2011). Current prospects for RNA interference-based therapies. Nat Rev Genet 12: 329-340.
7. .Dallas, A and Vlassov, AV (2006). RNAi: a novel antisense technology and its therapeutic potential. Med Sci Monit 12: RA67-RA74.
8. .Lacotte, S, Brun, S, Muller, S and Dumortier, H (2009). CXCR3, inflammation, and autoimmune diseases. Ann N Y Acad Sci 1173: 310-317.
9. .Lee, EY, Lee, ZH and Song, YW (2009). CXCL10 and autoimmune diseases. Autoimmun Rev 8: 379-383.
10. .Kühn, H and O'Donnell, VB (2006). Inflammation and immune regulation by 12/15- lipoxygenases. Prog Lipid Res 45: 334-356.
11. .Gao, Y, Liu, XL and Li, XR (2011). Research progress on siRNA delivery with nonviral carriers. Int J Nanomedicine 6: 1017-1025.
12. .Bresson, D, Togher, L, Rodrigo, E, Chen, Y, Bluestone, JA, Herold, KC et al. (2006). Anti-CD3 and nasal proinsulin combination therapy enhances remission from recentonset autoimmune diabetes by inducing Tregs. J Clin Invest 116: 1371-1381.
13. .Rotondi, M, Chiovato, L, Romagnani, S, Serio, M and Romagnani, P (2007). Role of chemokines in endocrine autoimmune diseases. Endocr Rev 28: 492-520.
14. .Nicoletti, F, Conget, I, Di Mauro, M, Di Marco, R, Mazzarino, MC, Bendtzen, K et al. (2002). Serum concentrations of the interferon-gamma- inducible chemokine IP-10/ CXCL10 are augmented in both newly diagnosed Type I diabetes mellitus patients and subjects at risk of developing the disease. Diabetologia 45: 1107-1110.
15. .Roep, BO, Kleijwegt, FS, van Halteren, AG, Bonato, V, Boggi, U, Vendrame, F et al. (2010). Islet inflammation and CXCL10 in recent-onset type 1 diabetes. Clin Exp Immunol 159: 338-343.
16. .Morimoto, J, Yoneyama, H, Shimada, A, Shigihara, T, Yamada, S, Oikawa, Y et al. (2004). CXC chemokine ligand 10 neutralization suppresses the occurrence of diabetes in nonobese diabetic mice through enhanced beta cell proliferation without affecting insulitis. J Immunol 173: 7017-7024.
17. .Dobrian, AD, Lieb, DC, Cole, BK, Taylor-Fishwick, DA, Chakrabarti, SK and Nadler, JL (2011). Functional and pathological roles of the 12- and 15-lipoxygenases. Prog Lipid Res 50: 115-131.
18. .McDuffie, M, Maybee, NA, Keller, SR, Stevens, BK, Garmey, JC, Morris, MA et al. (2008). Nonobese diabetic (NOD) mice congenic for a targeted deletion of 12/15- lipoxygenase are protected from autoimmune diabetes. Diabetes 57: 199-208.
19. .Weisberg, SP and Leibel, RL (2008). An apparent role for Alox15 in the pathogenesis of diabetes in the NOD mouse: parsing the supporting genetic data. Diabetes 57: 1-2.
20. .Francisco, LM, Sage, PT and Sharpe, AH (2010). The PD-1 pathway in tolerance and autoimmunity. Immunol Rev 236: 219-242.
21. .Martinic, MM, Juedes, AE, Bresson, D, Homann, D, Skak, K, Huber, C et al. (2007). Minimal impact of a de novo-expressed beta-cell autoantigen on spontaneous diabetes development in NOD mice. Diabetes 56: 1059-1068.
22. .van Halteren, AG, Kardol, MJ, Mulder, A and Roep, BO (2005). Homing of human autoreactive T cells into pancreatic tissue of NOD-scid mice. Diabetologia 48: 75-82.
23. .Szanya, V, Ermann, J, Taylor, C, Holness, C and Fathman, CG (2002). The subpopulation of CD4+CD25+ splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7. J Immunol 169: 2461-2465.
24. Sarween, N, Chodos, A, Raykundalia, C, Khan, M, Abbas, AK and Walker, LS (2004). CD4+CD25+ cells controlling a pathogenic CD4 response inhibit cytokine differentiation, CXCR-3 expression, and tissue invasion. J Immunol 173: 2942-2951.
25. Sarkar, SA, Lee, CE, Victorino, F, Nguyen, TT, Walters, JA, Burrack, A et al. (2012). Expression and regulation of chemokines in murine and human type 1 diabetes. Diabetes 61: 436-446.
26. Hoerning, A, Koss, K, Datta, D, Boneschansker, L, Jones, CN, Wong, IY et al. (2011). Subsets of human CD4(+) regulatory T cells express the peripheral homing receptor CXCR3.Eur J Immunol 41: 2291-2302.
27. .Ukena, SN, Velaga, S, Geffers, R, Grosse, J, Baron, U, Buchholz, S et al. (2011). Human regulatory T cells in allogeneic stem cell transplantation. Blood 118: e82-e92.
28. .Eksteen, B, Miles, A, Curbishley, SM, Tselepis, C, Grant, AJ, Walker, LS et al. (2006). Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10. J Immunol 177: 593-603.
29. Hasegawa, H, Inoue, A, Kohno, M, Lei, J, Miyazaki, T, Yoshie, O et al. (2008). Therapeutic effect of CXCR3-expressing regulatory T cells on liver, lung and intestinal damages in a murine acute GVHD model. Gene Ther 15: 171-182.
30. Oikawa, Y, Shimada, A, Yamada, Y, Okubo, Y, Katsuki, T, Shigihara, T et al. (2010). CXC chemokine ligand 10 DNA vaccination plus Complete Freund's Adjuvant reverses hyperglycemia in non-obese diabetic mice. Rev Diabet Stud 7: 209-224.
31. Shigihara, T, Shimada, A, Oikawa, Y, Yoneyama, H, Kanazawa, Y, Okubo, Y et al. (2005). CXCL10 DNA vaccination prevents spontaneous diabetes through enhanced beta cell proliferation in NOD mice. J Immunol 175: 8401-8408.
32. Groom, JR and Luster, AD (2011). CXCR3 ligands: redundant, collaborative and antagonistic functions. Immunol Cell Biol 89: 207-215.
33. Aboumrad, E, Madec, AM and Thivolet, C (2007). The CXCR4/CXCL12 (SDF-1) signalling pathway protects non-obese diabetic mouse from autoimmune diabetes. Clin Exp Immunol 148: 432-439.
34. Atkinson, MA and Wilson, SB (2002). Fatal attraction: chemokines and type 1 diabetes. J Clin Invest 110: 1611-1613.
35. Chen, XS, Sheller, JR, Johnson, EN and Funk, CD (1994). Role of leukotrienes revealed by targeted disruption of the 5-lipoxygenase gene. Nature 372: 179-182.
36. Chen, W, Bluestone, JA and Herold, KC (2005). Achieving antigen-specific tolerance in diabetes: regulating specifically. Int Rev Immunol 24: 287-305.
37. Chen, M, Yang, ZD, Smith, KM, Carter, JD and Nadler, JL (2005). Activation of 12- lipoxygenase in proinflammatory cytokine-mediated beta cell toxicity. Diabetologia 48: 486-495.
38. Garcia, MR, Ledgerwood, L, Yang, Y, Xu, J, Lal, G, Burrell, B et al. (2010). Monocytic suppressive cells mediate cardiovascular transplantation tolerance in mice. J Clin Invest 120: 2486-2496.
39. Cheng, X, Zhao, Z, Ventura, E, Gran, B, Shindler, KS and Rostami, A (2007). The PD-1/PD-L pathway is up-regulated during IL-12-induced suppression of EAE mediated by IFN-gamma. J Neuroimmunol 185: 75-86.
40. Wang, L, Pino-Lagos, K, de Vries, VC, Guleria, I, Sayegh, MH and Noelle, RJ (2008). Programmed death 1 ligand signaling regulates the generation of adaptive Foxp3+CD4+ regulatory T cells. Proc Natl Acad Sci USA 105: 9331-9336.
41. Loke, P and Allison, JP (2003). PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc Natl Acad Sci USA 100: 5336-5341.
42. Akirav, EM, Baquero, MT, Opare-Addo, LW, Akirav, M, Galvan, E, Kushner, JA et al. (2011). Glucose and inflammation control islet vascular density and beta-cell function in NOD mice: control of islet vasculature and vascular endothelial growth factor by glucose. Diabetes 60: 876-883.
43. Inaba, S, Nagahara, S, Makita, N, Tarumi, Y, Ishimoto, T, Matsuo, S et al. (2012). Atelocollagen-mediated systemic delivery prevents immunostimulatory adverse effects of siRNA in mammals. Mol Ther 20: 356-366.
44. Wong, FS and Wen, L (2008). IFN-alpha can both protect against and promote the development of type 1 diabetes. Ann N Y Acad Sci 1150: 187-189.
45. Zhang, J, Huang, Z, Sun, R, Tian, Z and Wei, H (2012). IFN-gamma induced by IL-12 administration prevents diabetes by inhibiting pathogenic IL-17 production in NOD mice. J Autoimmun 38: 20-28 (doi: 10.1016/j.jaut.2011.11.017).
46. .Lonez, C, Vandenbranden, M and Ruysschaert, JM (2008). Cationic liposomal lipids: from gene carriers to cell signaling. Prog Lipid Res 47: 340-347.
47. .Sioud, M and Sørensen, DR (2003). Cationic liposome-mediated delivery of siRNAs in adult mice. Biochem Biophys Res Commun 312: 1220-1225.
48. .Lundberg, P, Welander, PV, Edwards, CK 3rd, van Rooijen, N and Cantin, E (2007). Tumor necrosis factor (TNF) protects resistant C57BL/6 mice against herpes simplex virus-induced encephalitis independently of signaling via TNF receptor 1 or 2. J Virol 81: 1451-1460.
49. Lundberg, P, Yang, HJ, Jung, SJ, Behlke, MA, Rose, SD and Cantin, EM (2012). Protection against TNFa-dependent liver toxicity by intraperitoneal liposome delivered DsiRNA targeting TNFa in vivo. J Control Release 160: 194-199.
50. Mamchak, AA, Manenkova, Y, Leconet, W, Zheng, Y, Chan, JR, Stokes, CL et al. (2012). Preexisting autoantibodies predict efficacy of oral insulin to cure autoimmune diabetes in combination with anti-CD3.Diabetes 61: 1490-1499.