Plasmacytoid and conventional dendritic cells cooperate in crosspriming AAV capsid-specific CD8+ T cells

Blood

Volumn 129, Issue 24, 2017, Pages 3184-3195

  Rogers, Geoffrey L ^a   Shirley, Jamie L ^a   Zolotukhin, Irene ^a   Kumar, Sandeep R P ^a   Sherman, Alexandra ^a   Perrin, George Q ^a   Hoffman, Brad E ^a   Srivastava, Arun ^a   Basner Tschakarjan, Etiena ^b   Wallet, Mark A ^a   Terhorst, Cox ^c   Biswas, Moanaro ^a   Herzog, Roland W ^a  

^a UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^b CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; INTERFERON; MYELOID DIFFERENTIATION FACTOR 88; PATTERN RECOGNITION RECEPTOR; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TOLL LIKE RECEPTOR AGONIST; CAPSID PROTEIN; MYD88 PROTEIN, MOUSE; TLR9 PROTEIN, MOUSE;

ADENO ASSOCIATED VIRUS; ANIMAL CELL; ANIMAL TISSUE; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CONVENTIONAL DENDRITIC CELL; DENDRITIC CELL; GENE THERAPY; IMMUNE RESPONSE; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; VIRUS CAPSID; VIRUS GENOME; ANIMAL; DEPENDOPARVOVIRUS; GENETICS; IMMUNOLOGY; KNOCKOUT MOUSE; LYMPHOCYTE ACTIVATION; PLASMA CELL;

ANIMALS; CAPSID PROTEINS; CD8-POSITIVE T-LYMPHOCYTES; DENDRITIC CELLS; DEPENDOVIRUS; GENETIC THERAPY; LYMPHOCYTE ACTIVATION; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PLASMA CELLS; TOLL-LIKE RECEPTOR 9;

EID: 85021083587     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2016-11-751040     Document Type: Article

References (60)

1. Halder S, Ng R, Agbandje-McKenna M. Parvoviruses: structure and infection. Future Virol. 2012;7(3):253-278.
2. Mingozzi F, High KA. Therapeutic in vivo gene transfer for genetic disease using AAV: progress and challenges. Nat Rev Genet. 2011;12(5): 341-355.
3. Gaudet D, Méthot J, Déry S, et al. Efficacy and long-term safety of alipogene tiparvovec (AAV1-LPLS447X) gene therapy for lipoprotein lipase deficiency: an open-label trial. Gene Ther. 2013; 20(4):361-369.
4. Bennett J, Wellman J, Marshall KA, et al. Safety and durability of effect of contralateral-eye administration of AAV2 gene therapy in patients with childhood-onset blindness caused by RPE65 mutations: a follow-on phase 1 trial. Lancet. 2016; 388(10045):661-672.
5. Manno CS, Pierce GF, Arruda VR, et al. Successful transduction of liver in hemophilia by AAV-Factor IX and limitations imposed by the host immune response [published correction appears in Nat Med. 2006;12(5):592]. Nat Med. 2006; 12(3):342-347.
6. Nathwani AC, Tuddenham EG, Rangarajan S, et al. Adenovirus-associated virus vectormediated gene transfer in hemophilia B. N Engl J Med. 2011;365(25):2357-2365.
7. Nathwani AC, Reiss UM, Tuddenham EG, et al. Long-term safety and efficacy of factor IX gene therapy in hemophilia B. N Engl J Med. 2014; 371(21):1994-2004.
8. Brantly ML, Chulay JD, Wang L, et al. Sustained transgene expression despite T lymphocyte responses in a clinical trial of rAAV1-AAT gene therapy [published correction appears in Proc Natl Acad Sci USA. 2009;106(41):17606]. Proc Natl Acad Sci USA. 2009;106(38):16363-16368.
9. Mueller C, Chulay JD, Trapnell BC, et al. Human treg responses allow sustained recombinant adeno-associated virus-mediated transgene expression. J Clin Invest. 2013;123(12): 5310-5318.
10. Mingozzi F, Meulenberg JJ, Hui DJ, et al. AAV-1-mediated gene transfer to skeletal muscle in humans results in dose-dependent activation of capsid-specific T cells. Blood. 2009;114(10): 2077-2086.
11. Herzog RW. Hemophilia gene therapy: caught between a cure and an immune response. Mol Ther. 2015;23(9):1411-1412.
12. Kawai T, Akira S. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity. 2011;34(5):637-650.
13. Zhu J, Huang X, Yang Y. The TLR9-MyD88 pathway is critical for adaptive immune responses to adeno-associated virus gene therapy vectors in mice. J Clin Invest. 2009;119(8):2388-2398.
14. Rogers GL, Martino AT, Aslanidi GV, Jayandharan GR, Srivastava A, Herzog RW. Innate immune responses to AAV vectors. Front Microbiol. 2011;2:194.
15. Martino AT, Suzuki M, Markusic DM, et al. The genome of self-complementary adeno-associated viral vectors increases toll-like receptor 9-dependent innate immune responses in the liver. Blood. 2011;117(24):6459-6468.
16. Rogers GL, Martino AT, Zolotukhin I, Ertl HC, Herzog RW. Role of the vector genome and underlying factor IX mutation in immune responses to AAV gene therapy for hemophilia B. J Transl Med. 2014;12(1):25.
17. Hösel M, Broxtermann M, Janicki H, et al. Toll-like receptor 2-mediated innate immune response in human nonparenchymal liver cells toward adenoassociated viral vectors. Hepatology. 2012;55(1): 287-297.
18. Rogers GL, Suzuki M, Zolotukhin I, et al. Unique roles of TLR9-and MyD88-dependent and-independent pathways in adaptive immune responses to AAV-mediated gene transfer. J Innate Immun. 2015;7(3):302-314.
19. Faust SM, Bell P, Cutler BJ, et al. CpG-depleted adeno-associated virus vectors evade immune detection. J Clin Invest. 2013;123(7):2994-3001.
20. Martino AT, Basner-Tschakarjan E, Markusic DM, et al. Engineered AAV vector minimizes in vivo targeting of transduced hepatocytes by capsidspecific CD81 T cells. Blood. 2013;121(12): 2224-2233.
21. Li C, He Y, Nicolson S, et al. Adeno-associated virus capsid antigen presentation is dependent on endosomal escape. J Clin Invest. 2013;123(3): 1390-1401.
22. Wang L, Figueredo J, Calcedo R, Lin J, Wilson JM. Cross-presentation of adeno-associated virus serotype 2 capsids activates cytotoxic T cells but does not render hepatocytes effective cytolytic targets. Hum Gene Ther. 2007;18(3):185-194.
23. Sasai M, Linehan MM, Iwasaki A. Bifurcation of toll-like receptor 9 signaling by adaptor protein 3. Science. 2010;329(5998):1530-1534.
24. Bhat N, Fitzgerald KA. Recognition of cytosolic DNA by cGAS and other STING-dependent sensors. Eur J Immunol. 2014;44(3):634-640.
25. Jung S, Unutmaz D, Wong P, et al. In vivo depletion of CD11c1 dendritic cells abrogates priming of CD81 T cells by exogenous cellassociated antigens. Immunity. 2002;17(2): 211-220.
26. Perrin GQ, Zolotukhin I, Sherman A, et al. Dynamics of antigen presentation to transgene product-specific CD41 T cells and of treg induction upon hepatic AAV gene transfer. Mol Ther Methods Clin Dev. 2016;3:16083.
27. Corti M, Elder M, Falk D, et al. B-cell depletion is protective against anti-AAV capsid immune response: a human subject case study. Mol Ther Methods Clin Dev. 2014;1. Article 14033.
28. Sack BK, Merchant S, Markusic DM, et al. Transient B cell depletion or improved transgene expression by codon optimization promote tolerance to factor VIII in gene therapy. PLoS One. 2012;7(5):e37671.
29. Biswas M, Sarkar D, Kumar SR, et al. Synergy between rapamycin and FLT3 ligand enhances plasmacytoid dendritic cell-dependent induction of CD41CD251FoxP31 treg. Blood. 2015;125(19): 2937-2947.
30. Pinto AK, Daffis S, Brien JD, et al. A temporal role of type I interferon signaling in CD81 T cell maturation during acute West Nile virus infection. PLoS Pathog. 2011;7(12):e1002407.
31. Ertl HC, High KA. Impact of AAV capsid-specific T-cell responses on design and outcome of clinical gene transfer trials with recombinant adeno-associated viral vectors: an evolving controversy. Hum Gene Ther. 2017;28(4): 328-337.
32. Chabicovsky M, Prieschl-Grassauer E, Seipelt J, et al. Pre-clinical safety evaluation of pyrrolidine dithiocarbamate. Basic Clin Pharmacol Toxicol. 2010;107(3):758-767.
33. Browne EP. Regulation of B-cell responses by toll-like receptors. Immunology. 2012;136(4): 370-379.
34. Agudo J, Ruzo A, Kitur K, Sachidanandam R, Blander JM, Brown BDA. A TLR and non-TLR mediated innate response to lentiviruses restricts hepatocyte entry and can be ameliorated by pharmacological blockade. Mol Ther. 2012; 20(12):2257-2267.
35. Zhu J, Huang X, Yang Y. Innate immune response to adenoviral vectors is mediated by both toll-like receptor-dependent and-independent pathways. J Virol. 2007;81(7): 3170-3180.
36. Nair-Gupta P, Baccarini A, Tung N, et al. TLR signals induce phagosomal MHC-I delivery from the endosomal recycling compartment to allow cross-presentation. Cell. 2014;158(3):506-521.
37. Brewitz A, Eickhoff S, Dähling S, et al. CD81 T cells orchestrate pDC-XCR11 dendritic cell spatial and functional cooperativity to optimize priming. Immunity. 2017;46(2):205-219.
38. Fonteneau JF, Larsson M, Beignon AS, et al. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol. 2004;78(10):5223-5232.
39. Rossetti M, Gregori S, Hauben E, et al. HIV-1-derived lentiviral vectors directly activate plasmacytoid dendritic cells, which in turn induce the maturation of myeloid dendritic cells. Hum Gene Ther. 2011;22(2):177-188.
40. Kuwajima S, Sato T, Ishida K, Tada H, Tezuka H, Ohteki T. Interleukin 15-dependent crosstalk between conventional and plasmacytoid dendritic cells is essential for CpG-induced immune activation. Nat Immunol. 2006;7(7):740-746.
41. Piccioli D, Sammicheli C, Tavarini S, et al. Human plasmacytoid dendritic cells are unresponsive to bacterial stimulation and require a novel type of cooperation with myeloid dendritic cells for maturation. Blood. 2009;113(18):4232-4239.
42. Bakdash G, Schreurs I, Schreibelt G, Tel J. Crosstalk between dendritic cell subsets and implications for dendritic cell-based anticancer immunotherapy. Expert Rev Clin Immunol. 2014; 10(7):915-926.
43. Alloatti A, Kotsias F, Magalhaes JG, Amigorena S. Dendritic cell maturation and crosspresentation: timing matters! Immunol Rev. 2016;272(1):97-108.
44. van Endert P. Intracellular recycling and crosspresentation by MHC class I molecules. Immunol Rev. 2016;272(1):80-96.
45. Stahnke S, Lux K, Uhrig S, et al. Intrinsic phospholipase A2 activity of adeno-associated virus is involved in endosomal escape of incoming particles. Virology. 2011;409(1):77-83.
46. Finn JD, Hui D, Downey HD, et al. Proteasome inhibitors decrease AAV2 capsid derived peptide epitope presentation on MHC class I following transduction. Mol Ther. 2010;18(1):135-142.
47. Pien GC, Basner-Tschakarjan E, Hui DJ, et al. Capsid antigen presentation flags human hepatocytes for destruction after transduction by adeno-associated viral vectors. J Clin Invest. 2009;119(6):1688-1695.
48. Zhong L, Zhao W, Wu J, et al. A dual role of EGFR protein tyrosine kinase signaling in ubiquitination of AAV2 capsids and viral secondstrand DNA synthesis. Mol Ther. 2007;15(7): 1323-1330.
49. Zhong L, Li B, Jayandharan G, et al. Tyrosinephosphorylation of AAV2 vectors and its consequences on viral intracellular trafficking and transgene expression. Virology. 2008; 381(2):194-202.
50. Zhong L, Li B, Mah CS, et al. Next generation of adeno-associated virus 2 vectors: point mutations in tyrosines lead to high-efficiency transduction at lower doses [published correction appears in Proc Natl Acad Sci USA. 2008;105(31):11032]. Proc Natl Acad Sci USA. 2008;105(22):7827-7832.
51. Welsh RM, Bahl K, Marshall HD, Urban SL. Type 1 interferons and antiviral CD8 T-cell responses. PLoS Pathog. 2012;8(1):e1002352.
52. Pantel A, Teixeira A, Haddad E, Wood EG, Steinman RM, Longhi MP. Direct type I IFN but not MDA5/TLR3 activation of dendritic cells is required for maturation and metabolic shift to glycolysis after poly IC stimulation. PLoS Biol. 2014;12(1):e1001759.
53. Spadaro F, Lapenta C, Donati S, et al. IFN-a enhances cross-presentation in human dendritic cells by modulating antigen survival, endocytic routing, and processing. Blood. 2012;119(6): 1407-1417.
54. de Ruiter PE, Boor PP, de Jonge J, et al. Prednisolone does not affect direct-acting antivirals against hepatitis C, but inhibits interferon-alpha production by plasmacytoid dendritic cells. Transpl Infect Dis. 2015;17(5): 707-715.
55. Wu TL, Li H, Faust SM, et al. CD81 T cell recognition of epitopes within the capsid of adenoassociated virus 8-based gene transfer vectors depends on vectors' genome. Mol Ther. 2014; 22(1):42-51.
56. Kumar SR, Hoffman BE, Terhorst C, de Jong YP, Herzog RW. The balance between CD81 T cellmediated clearance of AAV-encoded antigen in the liver and tolerance is dependent on the vector dose. Mol Ther. 2017;25(4):880-891.
57. Jayandharan GR, Aslanidi G, Martino AT, et al. Activation of the NF-kappaB pathway by adeno-associated virus (AAV) vectors and its implications in immune response and gene therapy. Proc Natl Acad Sci USA. 2011;108(9): 3743-3748.
58. Doerfler PA, Nayak S, Corti M, Morel L, Herzog RW, Byrne BJ. Targeted approaches to induce immune tolerance for Pompe disease therapy. Mol Ther Methods Clin Dev. 2016;3:15053.
59. Suárez-Fariñas M, Arbeit R, Jiang W, Ortenzio FS, Sullivan T, Krueger JG. Suppression of molecular inflammatory pathways by toll-like receptor 7, 8, and 9 antagonists in a model of IL-23-induced skin inflammation. PLoS One. 2013;8(12):e84634.
60. Mutwiri GK, Nichani AK, Babiuk S, Babiuk LA. Strategies for enhancing the immunostimulatory effects of CpG oligodeoxynucleotides. J Control Release. 2004;97(1):1-17.