Tolerogen-induced interferon-producing killer dendritic cells (IKDCs) protect against EAE

Journal of Autoimmunity

Volumn 37, Issue 4, 2011, Pages 328-341

  Huarte, Eduardo ^a   Rynda Apple, Agnieszka ^a   Riccardi, Carol ^a   Skyberg, Jerod A ^a   Golden, Sarah ^a   Rollins, MaryClare F ^a   Ramstead, Andrew G ^a   Jackiw, Larissa O ^a   Maddaloni, Massimo ^a   Pascual, David W ^a  

^a MONTANA STATE UNIVERSITY   (United States)

Author keywords

EAE; HVEM; IKDC; T reg cells; Tolerance

Indexed keywords

HYBRID PROTEIN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN OLIGODENDROCYTE GLYCOPROTEIN; VIRUS PROTEIN;

ADOPTIVE TRANSFER; ALLERGIC ENCEPHALOMYELITIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CONTROLLED STUDY; DENDRITIC CELL; FEMALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REMISSION; REOVIRUS;

ADOPTIVE TRANSFER; ANIMALS; ANTIGENS, LY; CYTOTOXICITY, IMMUNOLOGIC; DENDRITIC CELLS; DISEASE PROGRESSION; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; IMMUNE TOLERANCE; INTERFERONS; LYMPHOCYTE ACTIVATION; MICE; MYELIN PROTEINS; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY B; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; RECOMBINANT FUSION PROTEINS; RECURRENCE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; VIRAL PROTEINS;

EID: 82955163021     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2011.09.005     Document Type: Article

References (69)

1. Flodstrom-Tullberg M., Bryceson Y.T., Shi F.D., Hoglund P., Ljunggren H.G. Natural killer cells in human autoimmunity. Curr Opin Immunol 2009, 21:634-640.
2. Paust S., Senman B., von Andrian U.H. Adaptive immune responses mediated by natural killer cells. Immunol Rev 2010, 235:286-296.
3. Rabinovich B.A., Shannon J., Su R.C., Miller R.G. Stress renders T cell blasts sensitive to killing by activated syngeneic NK cells. J Immunol 2000, 165:2390-2397.
4. Marcenaro E., Della Chiesa M., Bellora F., Parolini S., Millo R., Moretta L., et al. IL-12 or IL-4 prime human NK cells to mediate functionally divergent interactions with dendritic cells or tumors. J Immunol 2005, 174:3992-3998.
5. Homann D., Jahreis A., Wolfe T., Hughes A., Coon B., van Stipdonk M.J., et al. CD40L blockade prevents autoimmune diabetes by induction of bitypic NK/DC regulatory cells. Immunity 2002, 16:403-415.
6. Pillarisetty V.G., Katz S.C., Bleier J.I., Shah A.B., Dematteo R.P. Natural killer dendritic cells have both antigen presenting and lytic function and in response to CpG produce IFN-γ via autocrine IL-12. J Immunol 2005, 174:2612-2618.
7. Chan C.W., Crafton E., Fan H.N., Flook J., Yoshimura K., Skarica M., et al. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat Med 2006, 12:207-213.
8. Taieb J., Chaput N., Menard C., Apetoh L., Ullrich E., Bonmort M., et al. A novel dendritic cell subset involved in tumor immunosurveillance. Nat Med 2006, 12:214-219.
9. GeurtsvanKessel C.H., Bergen I.M., Muskens F., Boon L., Hoogsteden H.C., Osterhaus A.D., et al. Both conventional and interferon killer dendritic cells have antigen-presenting capacity during influenza virus infection. PLoS One 2009, 4:e7187.
10. + cells identify them as a subset of NK cells. J Exp Med 2007, 204:2561-2568.
11. Caminschi I., Ahmet F., Heger K., Brady J., Nutt S.L., Vremec D., et al. Putative IKDCs are functionally and developmentally similar to natural killer cells, but not to dendritic cells. J Exp Med 2007, 204:2579-2590.
12. + interferon-producing killer dendritic cells are activated natural killer cells. J Exp Med 2007, 204:2569-2578.
13. Hanna J., Gonen-Gross T., Fitchett J., Rowe T., Daniels M., Arnon T.I., et al. Novel APC-like properties of human NK cells directly regulate T cell activation. J Clin Invest 2004, 114:1612-1623.
14. + lymphoid progenitors. Blood 2007, 109:4825-4931.
15. Pletneva M., Fan H., Park J.J., Radojcic V., Jie C., Yu Y., et al. IFN-producing killer dendritic cells are antigen-presenting cells endowed with T-cell cross-priming capacity. Cancer Res 2009, 69:6607-6614.
16. Himoudi N., Yan M., Bouma G., Morgenstern D., Wallace R., Seddon B., et al. Migratory and antigen presentation functions of IFN-producing killer dendritic cells. Cancer Res 2009, 69:6598-6606.
17. + subset and are licensed by tumor cells. Cancer Res 2009, 69:6590-6597.
18. Baxter A.G. The origin and application of experimental autoimmune encephalomyelitis. Nat Rev Immunol 2007, 7:904-912.
19. Legge K.L., Gregg R.K., Maldonado-Lopez R., Li L., Caprio J.C., Moser M., et al. On the role of dendritic cells in peripheral T cell tolerance and modulation of autoimmunity. J Exp Med 2002, 196:217-227.
20. Rynda A., Maddaloni M., Mierzejewska D., Ochoa-Repáraz J., Maslanka T., Crist K., et al. Low-dose tolerance is mediated by the microfold cell ligand, reovirus protein sigma1. J Immunol 2008, 180:5187-5200.
21. reg cells in protein σ1-mediated protection against murine experimental autoimmune encephalomyelitis (EAE). PLoS One 2010, 5:e8720.
22. Rynda-Apple A., Huarte E., Maddaloni M., Callis G., Skyberg J.A., Pascual D.W. Active immunization using a single dose immunotherapeutic abates established EAE via IL-10 and regulatory T cells. Eur J Immunol 2011, 41:313-323.
23. + T cells. J Immunol 2001, 166:4209-4215.
24. Zhang B., Yamamura T., Kondo T., Fujiwara M., Tabira T. Regulation of experimental autoimmune encephalomyelitis by natural killer (NK) cells. J Exp Med 1997, 186:1677-1687.
25. Al-Falahi Y., Sand K.L., Knudsen E., Damaj B.B., Rolin J., Maghazachi A.A. Splenic natural killer cell activity in two models of experimental neurodegenerative diseases. J Cell Mol Med 2009, 13:2693-2703.
26. Xu W., Fazekas G., Hara H., Tabira T. Mechanism of natural killer (NK) cell regulatory role in experimental autoimmune encephalomyelitis. J Neuroimmunol 2005, 163:24-30.
27. Hao J., Liu R., Piao W., Zhou Q., Vollmer T.L., Campagnolo D.I., et al. Central nervous system (CNS)-resident natural killer cells suppress Th17 responses and CNS autoimmune pathology. J Exp Med 2010, 207:1907-1921.
28. Huang D., Shi F.D., Jung S., Pien G.C., Wang J., Salazar-Mather T.P., et al. The neuronal chemokine CX3CL1/fractalkine selectively recruits NK cells that modify experimental autoimmune encephalomyelitis within the central nervous system. FASEB J 2006, 20:896-905.
29. Hammarberg H., Lidman O., Lundberg C., Eltayeb S.Y., Gielen A.W., Muhallab S., et al. Neuroprotection by encephalomyelitis: rescue of mechanically injured neurons and neurotrophin production by CNS-infiltrating T and natural killer cells. J Neurosci 2000, 20:5283-5291.
30. Takahashi K., Miyake S., Kondo T., Terao K., Hatakenaka M., Hashimoto S., et al. Natural killer type 2 bias in remission of multiple sclerosis. J Clin Invest 2001, 107:R23-R29.
31. Munschauer F.E., Hartrich L.A., Stewart C.C., Jacobs L. Circulating natural killer cells but not cytotoxic T lymphocytes are reduced in patients with active relapsing multiple sclerosis and little clinical disability as compared to controls. J Neuroimmunol 1995, 62:177-181.
32. Batoulis H., Addicks K., Kuerten S. Emerging concepts in autoimmune encephalomyelitis beyond the CD4/T(H)1 paradigm. Ann Anat 2010, 192:179-193.
33. Spits H., Lanier L.L. Natural killer or dendritic: what's in a name?. Immunity 2007, 26:11-16.
34. Winkler-Pickett R., Young H.A., Cherry J.M., Diehl J., Wine J., Back T., et al. In vivo regulation of experimental autoimmune encephalomyelitis by NK cells: alteration of primary adaptive responses. J Immunol 2008, 180:4495-4506.
35. bright subset. Blood 2001, 97:3146-3151.
36. Airas L., Saraste M., Rinta S., Elovaara I., Huang Y.H., Wiendl H. Immunoregulatory factors in multiple sclerosis patients during and after pregnancy: relevance of natural killer cells. Clin Exp Immunol 2008, 151:235-243.
37. + T cells by NK cells via the Qa-1-NKG2A inhibitory pathway. Immunity 2007, 26:593-604.
38. neg cells are responsible for natural cytotoxicity against tumor targets. Leukemia 2005, 19:835-840.
39. Greenwald R.J., Freeman G.J., Sharpe A.H. The B7 family revisited. Annu Rev Immunol 2005, 23:515-548.
40. Carter L.L., Leach M.W., Azoitei M.L., Cui J., Pelker J.W., Jussif J., et al. PD-1/PD-L1, but not PD-1/PD-L2, interactions regulate the severity of experimental autoimmune encephalomyelitis. J Neuroimmunol 2007, 182:124-134.
41. + T cell frequency varies for different epitopes and predicts repertoire diversity and response magnitude. Immunity 2007, 27:203-213.
42. Huarte E., Sarobe P., Lu J., Casares N., Lasarte J.J., Dotor J., et al. Enhancing immunogenicity of a CTL epitope from carcinoembryonic antigen by selective amino acid replacements. Clin Cancer Res 2002, 8:2336-2344.
43. + T cell responses. J Exp Med 2011, 208:81-90.
44. Feng X., Yan J., Wang Y., Zierath J.R., Nordenskjold M., Henter J.I., et al. The proteasome inhibitor bortezomib disrupts tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) expression and natural killer (NK) cell killing of TRAIL receptor-positive multiple myeloma cells. Mol Immunol 2010, 47:2388-2396.
45. Murphy T.L., Murphy K.M. Slow down and survive: enigmatic immunoregulation by BTLA and HVEM. Annu Rev Immunol 2010, 28:389-411.
46. Ochoa-Repáraz J., Mielcarz D.W., Begum-Haque S., Kasper L.H. Gut, bugs, and brain: role of commensal bacteria in the control of central nervous system disease. Ann Neurol 2011, 69:240-247.
47. Steinman L., Zamvil S.S. Virtues and pitfalls of EAE for the development of therapies for multiple sclerosis. Trends Immunol 2005, 26:565-571.
48. Fontoura P., Garren H. Multiple sclerosis therapies: molecular mechanisms and future. Results Probl Cell Differ 2010, 51:259-285.
49. Bright natural killer cells in the peripheral blood of multiple sclerosis patients treated with interferon-beta. Neurol Sci 2007, 28:121-126.
50. Kastrukoff L.F., Lau A., Wee R., Zecchini D., White R., Paty D.W. Clinical relapses of multiple sclerosis are associated with 'novel' valleys in natural killer cell functional activity. J Neuroimmunol 2003, 145:103-114.
51. bright natural killer cells mediate immunomodulatory effects of IL-2Rα-targeted therapy (daclizumab) in multiple sclerosis. Proc Natl Acad Sci U S A 2006, 103:5941-5946.
52. Bielekova B., Howard T., Packer A.N., Richert N., Blevins G., Ohayon J., et al. Effect of anti-CD25 antibody daclizumab in the inhibition of inflammation and stabilization of disease progression in multiple sclerosis. Arch Neurol 2009, 66:483-489.
53. Rio J., Nos C., Tintoré M., Téllez N., Galán I., Pelayo R., et al. Defining the response to interferon-β in relapsing-remitting multiple sclerosis patients. Ann Neurol 2006, 59:344-352.
54. Axtell R.C., de Jong B.A., Boniface K., van der Voort L.F., Bhat R., De Sarno P., et al. T helper type 1 and 17 cells determine efficacy of interferon-β in multiple sclerosis and experimental encephalomyelitis. Nat Med 2010, 16:406-412.
55. Warabi Y., Matsumoto Y., Hayashi H. Interferon beta-1b exacerbates multiple sclerosis with severe optic nerve and spinal cord demyelination. J Neurol Sci 2007, 252:57-61.
56. Begum-Haque S., Christy M., Ochoa-Reparaz J., Nowak E.C., Mielcarz D., Haque A., et al. Augmentation of regulatory B cell activity in experimental allergic encephalomyelitis by glatiramer acetate. J Neuroimmunol 2011.
57. Carter N.J., Keating G.M. Glatiramer acetate: a review of its use in relapsing-remitting multiple sclerosis and in delaying the onset of clinically definite multiple sclerosis. Drugs 2010, 70:1545-1577.
58. Hauser S.L., Waubant E., Arnold D.L., Vollmer T., Antel J., Fox R.J., et al. B-cell depletion with rituximab in relapsing-remitting multiple sclerosis. N Engl J Med 2008, 358:676-688.
59. Rose J.W., Watt H.E., White A.T., Carlson N.G. Treatment of multiple sclerosis with an anti-interleukin-2 receptor monoclonal antibody. Ann Neurol 2004, 56:864-867.
60. Coles A., Deans J., Compston A. Campath-1H treatment of multiple sclerosis: lessons from the bedside for the bench. Clin Neurol Neurosurg 2004, 106:270-274.
61. Perona-Wright G., Mohrs K., Szaba F.M., Kummer L.W., Madan R., Karp C.L., et al. Systemic but not local infections elicit immunosuppressive IL-10 production by natural killer cells. Cell Host Microbe 2009, 6:503-512.
62. Cheung T.C., Steinberg M.W., Oborne L.M., Macauley M.G., Fukuyama S., Sanjo H., et al. Unconventional ligand activation of herpesvirus entry mediator signals cell survival. Proc Natl Acad Sci U S A 2009, 106:6244-6249.
63. + T-cell immunity to reject established tumors. Blood 2006, 107:1342-1351.
64. Gonzalez L.C., Loyet K.M., Calemine-Fenaux J., Chauhan V., Wranik B., Ouyang W., et al. A coreceptor interaction between the CD28 and TNF receptor family members B and T lymphocyte attenuator and herpesvirus entry mediator. Proc Natl Acad Sci U S A 2005, 102:1116-1121.
65. Sakoda Y., Park J.J., Zhao Y., Kuramasu A., Geng D., Liu Y., et al. Dichotomous regulation of GVHD through bidirectional functions of the BTLA-HVEM pathway. Blood 2011, 117:2506-2514.
66. Hubert P., Jacobs N., Caberg J.H., Boniver J., Delvenne P. The cross-talk between dendritic and regulatory T cells: good or evil?. J Leukoc Biol 2007, 82:781-794.
67. Della Chiesa M., Vitale M., Carlomagno S., Ferlazzo G., Moretta L., Moretta A. The natural killer cell-mediated killing of autologous dendritic cells is confined to a cell subset expressing CD94/NKG2A, but lacking inhibitory killer Ig-like receptors. Eur J Immunol 2003, 33:1657-1666.
68. Mailloux A.W., Young M.R. NK-dependent increases in CCL22 secretion selectively recruits regulatory T cells to the tumor microenvironment. J Immunol 2009, 182:2753-2765.
69. Schreiner B., Bailey S.L., Shin T., Chen L., Miller S.D. PD-1 ligands expressed on myeloid-derived APC in the CNS regulate T-cell responses in EAE. Eur J Immunol 2008, 38:2706-2717.