Manipulating immune tolerance with micro-RNA regulated gene therapy

Frontiers in Microbiology

Volumn 2, Issue NOV, 2011, Pages

  Goudy, Kevin Scott ^a   Annoni, Andrea ^a   Naldini, Luigi ^a,b   Roncarolo, Maria Grazia ^a,b  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

Author keywords

Gene therapy; Hepatocytes; Liver; Microrna; Regulatory cells; Tolerance; Transgene; Treg

Indexed keywords

EID: 84864367347     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2011.00221     Document Type: Short Survey

References (47)

1. Annoni, A., Brown, B. D., Cantore, A., Sergi, L. S., Naldini, L., and Roncarolo, M. G. (2009). In vivo delivery of a microRNA-regulated transgene induces antigen-specific regulatory T cells and promotes immunologic tolerance. Blood 114, 5152-5161.
2. Bainbridge, J. W., Smith, A. J., Barker, S. S., Robbie, S., Henderson, R., Balaggan, K., Viswanathan, A., Holder, G. E., Stockman, A., Tyler, N., Petersen-Jones, S., Bhattacharya, S. S., Thrasher, A. J., Fitzke, E W., Carter, B. J., Rubin, G. S., Moore, A. T., and Ali, R. R. (2008). Effect of gene therapy on visual function in Leber's congenital amaurosis. N. Engl. J. Med. 358, 2231-2239.
3. Brown, B. D., Cantore, A., Annoni, A., Sergi, L. S., Lombardo, A., Della Valle, P., D'angelo, A., and Naldini, L. (2007a). A microRNA-regulated lentiviral vector mediates stable correction of hemophilia B mice. Blood 110,4144-4152.
4. Brown, B. D., Gentner, B., Cantore, A., Colleoni, S., Amendola, M., Zingale, A., Baccarini, A., Lazzari, G., Galli, C., and Naldini, L. (2007b). Endogenous microRNA can be broadly exploited to regulate transgene expression according to tissue, lineage and differentiation state. Nat. Biotechnol. 25,1457-1467.
5. Brown, B. D., Sitia, G., Annoni, A., Hauben, E., Sergi, L. S., Zingale, A., Roncarolo, M. G., Guidotti, L. G., and Naldini, L. (2007c). In vivo administration of lentiviral vectors triggers a type I interferon response that restricts hepatocyte gene transfer and promotes vector clearance. Blood 109, 2797-2805.
6. Brown, B. D., and Naldini, L. (2009). Exploiting and antagonizing microRNA regulation for therapeutic and experimental applications. Nat. Rev. Genet. 10, 578-585.
7. Brown, B. D., Shi, C. X., Rawle, E E., Tinlin, S., Mckinven, A., Hough, C., Graham, F. L., and Lillicrap, D. (2004). Factors influencing therapeutic efficacy and the host immune response to helper-dependent adenoviral gene therapy in hemophilia A mice. J. Thromb. Haemost. 2, 111-118.
8. Brown, B. D., Venneri, M. A., Zingale, A., Sergi Sergi, L., and Naldini, L. (2006). Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat. Med. 12,585-591.
9. Chen, W., Jin, W., Hardegen, N., Lei, K. J., Li, L., Marinos, N., Mcgrady, G., and Wahl, S. M. (2003). Conversion of peripheral CD4 + CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886.
10. Chen,W.,andKonkel,J.E. (2010). TGF-beta and 'adaptive' Foxp3(+) regulatory T cells. J. Mol. Cell Biol. 2, 30-36.
11. De Palma, M., Montini, E., Santoni De Sio, F. R., Benedicenti, F., Gentile, A., Medico, E., and Naldini, L. (2005). Promoter trapping reveals significant differences in integration site selection between MLV and HIV vectors in primary hematopoietic cells. Blood 105,2307-2315.
12. Erhardt, A., Biburger, M., Papadopoulos, T., and Tiegs, G. (2007). IL-10, regulatory T cells, and Kupffer cells mediate tolerance in concanavalin A-induced liver injury in mice. Hepatology 45, 475-485.
13. Fehervari,Z., and Sakaguchi, S. (2004a). CD4+ Tregs and immune control. J. Clin. Invest. 114,1209-1217.
14. Fehervari, Z., and Sakaguchi, S. (2004b). Control of Foxp3+ CD25+CD4+ regulatory cell activation and function by dendritic cells. Int. Immunol. 16,1769-1780.
15. Follenzi, A., Santambrogio, L., and Annoni, A. (2007). Immune responses to lentiviral vectors. Curr. GeneTher. 7,306-315.
16. Gregori, S., Tomasoni, D., Pacciani, V., Scirpoli, M., Battaglia, M., Magnani, C. F., Hauben, E., and Roncarolo, M. G. (2010). Differentiation of type 1 T regulatory cells (Tr1) by tolerogenic DC-10 requires the IL- 10-dependentILT4/HLA-G pathway. Blood 116,935-944.
17. Haribhai, D., Williams, J. B., Jia, S., Nickerson, D., Schmitt, E. G., Edwards, B., Ziegelbauer, J., Yassai, M., Li, S. H., Relland, L. M., Wise, P. M., Chen, A., Zheng, Y. Q., Simpson, P. M., Gorski, J., Salzman, N. H., Hessner, M. J., Chatila, T. A., and Williams, C. B. (2011). A requisite role for induced regulatory T cells in tolerance based on expanding antigen receptor diversity. Immunity 35, 109-122.
18. Hauswirth, W. W., Aleman, T. S., Kaushal, S., Cideciyan, A. V., Schwartz, S. B., Wang, L., Conlon, T. J., Boye, S. L., Flotte, T. R., Byrne, B. J., and Jacobson, S. G. (2008). Treatment of leber congenital amaurosis due to RPE65 mutations by ocular subretinal injection of adeno-associated virus gene vector: short-term results of a phase I trial. Hum. Gene Ther. 19, 979-990.
19. Herzog, R. W (2007). Immune responses to AAV capsid: are mice not humans after all? Mol Ther. 15, 649-650.
20. Jurkin, J., Schichl, Y. M., Koeffel, R., Bauer, T., Richter, S., Konradi, S., Gesslbauer, B., and Strobl, H. (2010). miR-146a is differentially expressed by myeloid dendritic cell subsets and desensitizes cells to TLR2-dependent activation. J. Immunol. 184,4955-4965.
21. Kang, Y., Xie, L., Tran, D. T., Stein, C. S., Hickey, M., Davidson, B. L., and Mccray, P. B. Jr. (2005). Persistent expression of factor VIII in vivo following non primate lentiviral gene transfer. Blood 106, 1552-1558.
22. Kaplitt, M. G., Feigin, A., Tang, C., Fitzsimons, H. L., Mattis, P., Lawlor, P. A., Bland, R. J., Young, D., Strybing, K., Eidelberg, D., and During, M. J. (2007). Safety and tolerability of gene therapy with an adeno-associated virus (AAV) borne GAD gene for Parkinson's disease: an open label, phase I trial. Lancet 369, 2097-2105.
23. Kelly, E. J., and Russell, S. J. (2009). MicroRNAs and the regulation of vector tropism. Mol Ther. 17, 409-416.
24. Knolle, P. A., Germann, T., Treichel, U., Uhrig, A., Schmitt, E., Hegenbarth, S., Lohse, A. W., and Gerken, G. (1999). Endotoxin down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells. J. Immunol. 162, 1401-1407.
25. Landgraf, P., Rusu, M., Sheridan, R., Sewer,A.,Iovino,N.,Aravin,A.,Pfeffer, S., Rice, A., Kamphorst, A. O., Landthaler, M., Lin, C., Socci, N. D., Hermida, L., Fulci, V., Chiaretti, S., Foa, R., Schliwka, J., Fuchs, U., Novosel, A., Muller, R. U., Schermer, B., Bissels, U., Inman, J., Phan, Q., Chien, M., Weir, D. B., Choksi, R., De Vita, G., Frezzetti, D., Trompeter, H. I., Hornung, V., Teng, G., Hartmann, G., Palkovits, M., Di Lauro, R., Wernet, P., Macino, G., Rogler, C. E., Nagle, J. W., Ju, J., Papavasiliou, F. N., Benzing, T., Lichter, P., Tam,W.,Brownstein,M. J., Bosio,A., Borkhardt,A.,Russo, J. J., Sander, C., Zavolan,M.,andTuschl,T. (2007). A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129,1401-1414.
26. Lau,A.H., and Thomson, A. W (2003). Dendritic cells and immune regulation in the liver. Gut 52, 307-314.
27. Levings, M. K., Gregori, S., Tresoldi, E., Cazzaniga, S., Bonini, C., and Roncarolo, M. G. (2005). Differentiation of Tr1 cells by immature dendritic cells requires IL-10 but not CD25+CD4+ Tr cells. Blood 105, 1162-1169.
28. Li, C., Hirsch, M., Asokan, A., Zeithaml, B., Ma, H., Kafri, T., and Samulski, R. J. (2007). Adeno-associated virus type 2 (AAV2) capsid-specific cyto-toxic T lymphocytes eliminate only vector-transduced cells coexpressing the AAV2 capsid in vivo. J. Virol. 81, 7540-7547.
29. Limmer, A., Ohl, J., Kurts, C., Ljunggren, H. G.,Reiss,Y.,Groettrup,M., Momburg, F., Arnold, B., and Knolle, P. A. (2000). Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat. Med. 6, 1348-1354.
30. Lowenstein, P. R., Mandel, R. J., Xiong, W. D., Kroeger, K., and Castro, M. G. (2007). Immune responses to ade-novirus and adeno-associated vectors used for gene therapy of brain diseases: the role of immunological synapses in understanding the cell biology of neuroimmune interactions. Curr. Gene Ther. 7, 347-360.
31. Luth, S., Huber, S., Schramm, C., Buch, T., Zander, S., Stadelmann, C., Bruck, W., Wraith, D. C., Herkel, J., and Lohse, A. W. (2008). Ectopic expression of neural autoantigen in mouse liver suppresses experimental autoimmune neuroinflammation by inducing antigen-specific Tregs. J. Clin. Invest. 118, 3403-3410.
32. Matrai, J., Cantore, A., Bartholomae, C. C., Annoni, A., Wang, W., Acosta-Sanchez, A., Samara-Kuko, E., De Waele, L., Ma, L., Genovese, P., Damo, M., Arens, A., Goudy, K., Nichols, T. C., Von Kalle, C., Mk, L. C., Roncarolo, M. G., Schmidt, M., Vandendriessche, T., and Naldini, L. (2011). Hepatocyte-targeted expression by integrase-defective lentiviral vectors induces antigen-specific tolerance in mice with low genotoxic risk. Hepatology 53, 1696-1707.
33. Matsui, H., Hegadorn, C., Ozelo, M., Burnett, E., Tuttle, A., Labelle, A., Mccray, P. B. Jr., Naldini, L., Brown, B., Hough, C., and Lillicrap, D. (2011). A microRNA-regulated and GP64-pseudotyped lentiviral vector mediates stable expression of FVIII in amurine model of Hemophilia A. Mol Ther. 19, 723-730.
34. Mingozzi, F., and High, K. A. (2011). Immune Responses to AAV in Clinical Trials. Curr. Gene Ther. 11, 321-330.
35. Mingozzi, F., Maus, M. V., Hui, D. J., Sabatino, D. E., Murphy, S. L., Rasko, J. E., Ragni, M. V., Manno, C. S., Sommer, J., Jiang, H., Pierce, G. F., Ertl, H. C., and High, K. A. (2007). CD8(+) T-cell responses to adeno-associated virus capsid in humans. Nat. Med. 13,419-422.
36. Nayak, S., Cao, O., Hoffman, B. E., Cooper, M., Zhou, S., Atkinson, M. A., and Herzog, R. W. (2009). Prophylactic immune tolerance induced by changing the ratio of antigen-specific effector to regulatory T cells. J. Thromb. Haemost. 7, 1523-1532.
37. Osborn, M. J., Mcelmurry, R. T., Lees, C. J., Defeo, A. P., Chen, Z. Y., Kay, M. A., Naldini, L., Freeman, G., Tolar, J., and Blazar, B. R. (2011). Minicircle DNA-based gene therapy coupled with immune modulation permits long-term expression of alpha-L-iduronidase in mice with mucopolysaccharidosis type I. Mol. Ther. 19,450-460.
38. Petriv, O. I., Kuchenbauer, F., Delaney, A. D., Lecault, V., White, A., Kent, D., Marmolejo, L., Heuser, M., Berg, T., Copley, M., Ruschmann, J., Sekulovic, S., Benz, C., Kuroda, E., Ho, V., Antignano, F., Halim, T., Giambra, V., Krystal, G., Takei, C. J., Weng, A. P., Piret, J., Eaves, C., Marra, M. A., Humphries, R. K., and Hansen, C. L. (2010). Comprehensive microRNA expression profiling of the hematopoietic hierarchy. Proc. Natl.Acad. Sci. U.S.A. 107, 15443-15448.
39. Prasad, S. A., Norbury, C. C., Chen, W., Bennink, J. R., and Yewdell, J. W. (2001). Cutting edge: recombinant adenoviruses induce CD8 T cell responses to an inserted protein whose expression is limited to non immune cells. J. Immunol. 166, 4809-4812.
40. Sakaguchi, S., Yamaguchi, T., Nomura, T., and Ono, M. (2008). Regulatory T cells and immune tolerance. Cell 133, 775-787.
41. Sawa, Y., Arima, Y., Ogura, H., Kitabayashi, C., Jiang, J. J., Fukushima, T., Kamimura, D., Hirano, T., and Murakami, M. (2009). Hepatic interleukin-7 expression regulates T cell responses. Immunity 30, 447-457.
42. Seyfert-Margolis, V., and Turka, L. A. (2008). Marking a path to transplant tolerance. J. Clin. Invest. 118, 2684-2686.
43. Taganov, K. D., Boldin, M. P., Chang, K. J., and Baltimore, D. (2006). NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl Acad. Sci. U.S.A. 103, 12481-12486.
44. Unger, W. W., Laban, S., Kleijwegt, F. S., Van Der Slik, A. R., and Roep, B. O. (2009). Induction of Treg by monocyte-derived DC modulated by vitamin D3 or dexamethasone: differential role for PD-L1. Eur. J. Immunol. 39,3147-3159.
45. Vandendriessche, T., Thorrez, L., Acosta-Sanchez, A., Petrus, I., Wang, L., Ma, L., L, D. E. W., Iwasaki, Y., Gillijns, V., Wilson, J. M., Collen, D., and Chuah, M. K. (2007). Efficacy and safety of adeno-associated viral vectors based on serotype 8 and 9 vs. lentiviral vectors for hemophilia B gene therapy. J. Thromb. Haemost. 5, 16-24.
46. Wakkach, A., Fournier, N., Brun, V., Breittmayer, J. P., Cottrez, F., and Groux, H. (2003). Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 18, 605-617.
47. Warren, A., Le Couteur, D. G., Fraser, R., Bowen, D. G., Mccaughan, G. W., and Bertolino, P. (2006). T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology 44,1182-1190.