Nitric oxide controls an inflammatory-like Ly6ChiPDCA1 + DC subset that regulates Th1 immune responses

Journal of Leukocyte Biology

Volumn 89, Issue 3, 2011, Pages 443-455

  Giordano, Daniela ^a   Li, Chang ^a   Suthar, Mehul S ^a   Draves, Kevin E ^a   Ma, Daphne Y ^a   Gale Jr , Michael ^a   Clark, Edward A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

NOS2 KO; Th17; TipDCs; West Nile virus

Indexed keywords

GAMMA INTERFERON; NITRIC OXIDE;

ARTICLE; AUTOIMMUNE DISEASE; CD4+ T LYMPHOCYTE; CELL PROTECTION; CELL TRANSFER; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; TH1 CELL; WILD TYPE;

ANIMALS; ANTIGENS, CD86; ANTIGENS, LY; ANTIGENS, SURFACE; APOPTOSIS REGULATORY PROTEINS; BIOLOGICAL MARKERS; CD4-POSITIVE T-LYMPHOCYTES; CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; DOWN-REGULATION; EPITOPES; IMMUNITY; INFLAMMATION; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; TH1 CELLS; TOLL-LIKE RECEPTORS; UP-REGULATION; WEST NILE FEVER; WEST NILE VIRUS;

MUS; WEST NILE VIRUS;

EID: 79952229169     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0610329     Document Type: Article

References (77)

1. Joffre, O., Nolte, M. A., Sporri, R., Reis e Sousa, C. (2009) Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 227, 234-247.
2. Steinman, R. M., Banchereau, J. (2007) Taking dendritic cells into medicine. Nature 449, 419-426. (Pubitemid 47509552)
3. Díaz, N. L., Arvelaez, F. A., Zerpa, O., Tapia, F. J. (2006) Inducible nitric oxide synthase and cytokine pattern in lesions of patients with American cutaneous leishmaniasis. Clin. Exp. Dermatol. 31, 114-117.
4. Fernández-Ruiz, V., Lopez-Moratalla, N., Gonzalez, A. (2005) Production of nitric oxide and self-nitration of proteins during monocyte differentiation to dendritic cells. J. Physiol. Biochem. 61, 517-525.
5. Guzik, T. J., Korbut, R., Adamek-Guzik, T. (2003) Nitric oxide and superoxide in inflammation and immune regulation. J. Physiol. Pharmacol. 54, 469-487. (Pubitemid 38029745)
6. Bogdan, C. (2001) Nitric oxide and the immune response. Nat. Immunol. 2, 907-916.
7. Bagley, K. C., Abdelwahab, S. F., Tuskan, R. G., Lewis, G. K. (2006) Cholera toxin indirectly activates human monocyte-derived dendritic cells in vitro through the production of soluble factors, including prostaglandin E(2) and nitric oxide. Clin. Vaccine Immunol. 13, 106-115.
8. Marigo, I., Dolcetti, L., Serafini, P., Zanovello, P., Bronte, V. (2008) Tumor- induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol. Rev. 222, 162-179. (Pubitemid 351430364)
9. MacMicking, J. D., Nathan, C., Hom, G., Chartrain, N., Fletcher, D. S., Trumbauer, M., Stevens, K., Xie, Q. W., Sokol, K., Hutchinson, N., et al. (1995) Altered responses to bacterial infection and endotoxic shock in mice lacking inducible nitric oxide synthase. Cell 81, 641-650.
10. Wei, X. Q., Charles, I. G., Smith, A., Ure, J., Feng, G. J., Huang, F. P., Xu, D., Muller, W., Moncada, S., Liew, F. Y. (1995) Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 375, 408-411.
11. Sahrbacher, U. C., Lechner, F., Eugster, H. P., Frei, K., Lassmann, H., Fontana, A. (1998) Mice with an inactivation of the inducible nitric oxide synthase gene are susceptible to experimental autoimmune encephalomyelitis. Eur. J. Immunol. 28, 1332-1338.
12. Kolb, H., Kolb-Bachofen, V. (1998) Nitric oxide in autoimmune disease: cytotoxic or regulatory mediator? Immunol. Today 19, 556-561. (Pubitemid 28557118)
13. Fenyk-Melody, J. E., Garrison, A. E., Brunnert, S. R., Weidner, J. R., Shen, F., Shelton, B. A., Mudgett, J. S. (1998) Experimental autoimmune encephalomyelitis is exacerbated in mice lacking the NOS2 gene. J. Immunol. 160, 2940-2946. (Pubitemid 28136750)
14. Dalton, D. K., Wittmer, S. (2005) Nitric-oxide-dependent and independent mechanisms of protection from CNS inflammation during Th1-mediated autoimmunity: evidence from EAE in iNOS KO mice. J. Neuroimmunol. 160, 110-121. (Pubitemid 40248600)
15. Huang, F. P., Niedbala, W., Wei, X. Q., Xu, D., Feng, G. J., Robinson, J. H., Lam, C., Liew, F. Y. (1998) Nitric oxide regulates Th1 cell development through the inhibition of IL-12 synthesis by macrophages. Eur. J. Immunol. 28, 4062-4070. (Pubitemid 28558636)
16. Xiong, H., Zhu, C., Li, F., Hegazi, R., He, K., Babyatsky, M., Bauer, A. J., Plevy, S. E. (2004) Inhibition of interleukin-12 p40 transcription and NF-κB activation by nitric oxide in murine macrophages and dendritic cells. J. Biol. Chem. 279, 10776-10783. (Pubitemid 38372691)
17. Giordano, D., Magaletti, D. M., Clark, E. A. (2006) Nitric oxide and cGMP protein kinase (cGK) regulate dendritic-cell migration toward the lymph-node-directing chemokine CCL19. Blood 107, 1537-1545. (Pubitemid 43242392)
18. O'Neill, D. W., Bhardwaj, N. (2007) Exploiting dendritic cells for active immunotherapy of cancer and chronic infections. Mol. Biotechnol. 36, 131-141. (Pubitemid 350135919)
19. Van Duivenvoorde, L. M., van Mierlo, G. J., Boonman, Z. F., Toes, R. E. (2006) Dendritic cells: vehicles for tolerance induction and prevention of autoimmune diseases. Immunobiology 211, 627-632.
20. Palucka, A. K., Ueno, H., Fay, J. W., Banchereau, J. (2007) Taming cancer by inducing immunity via dendritic cells. Immunol. Rev. 220, 129-150. (Pubitemid 350045575)
21. Randolph, G. J., Inaba, K., Robbiani, D. F., Steinman, R. M., Muller, W. A. (1999) Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity 11, 753-761. (Pubitemid 30030714)
22. Domínguez, P. M., Ardavin, C. (2010) Differentiation and function of mouse monocyte-derived dendritic cells in steady state and inflammation. Immunol. Rev. 234, 90-104.
23. Serbina, N. V., Pamer, E. G. (2006) Monocyte emigration from bone marrow during bacterial infection requires signals mediated by chemokine receptor CCR2. Nat. Immunol. 7, 311-317.
24. León, B., Lopez-Bravo, M., Ardavin, C. (2007) Monocyte-derived dendritic cells formed at the infection site control the induction of protective T helper 1 responses against Leishmania. Immunity 26, 519-531. (Pubitemid 46602998)
25. Shortman, K., Naik, S. H. (2007) Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 7, 19-30. (Pubitemid 46020824)
26. Serbina, N. V., Jia, T., Hohl, T. M., Pamer, E. G. (2008) Monocyte-mediated defense against microbial pathogens. Annu. Rev. Immunol. 26, 421-452. (Pubitemid 351600381)
27. León, B., Ardavin, C. (2008) Monocyte-derived dendritic cells in innate and adaptive immunity. Immunol. Cell Biol. 86, 320-324. (Pubitemid 351667991)
28. Serbina, N. V., Salazar-Mather, T. P., Biron, C. A., Kuziel, W. A., Pamer, E. G. (2003) TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19, 59-70. (Pubitemid 36859901)
29. Tezuka, H., Abe, Y., Iwata, M., Takeuchi, H., Ishikawa, H., Matsushita, M., Shiohara, T., Akira, S., Ohteki, T. (2007) Regulation of IgA production by naturally occurring TNF/iNOS-producing dendritic cells. Nature 448, 929-933. (Pubitemid 47312771)
30. Bluth, M. J., Zaba, L. C., Moussai, D., Suarez-Farinas, M., Kaporis, H., Fan, L., Pierson, K. C., White, T. R., Pitts-Kiefer, A., Fuentes-Duculan, J., Guttman-Yassky, E., Krueger, J. G., Lowes, M. A., Carucci, J. A. (2009) Myeloid dendritic cells from human cutaneous squamous cell carcinoma are poor stimulators of T-cell proliferation. J. Invest. Dermatol. 129, 2451-2462.
31. Bacci, S., Pieri, L., Buccoliero, A. M., Bonelli, A., Taddei, G., Romagnoli, P. (2008) Smooth muscle cells, dendritic cells and mast cells are sources of TNFα and nitric oxide in human carotid artery atherosclerosis. Thromb. Res. 122, 657-667.
32. Lowes, M. A., Chamian, F., Abello, M. V., Fuentes-Duculan, J., Lin, S. L., Nussbaum, R., Novitskaya, I., Carbonaro, H., Cardinale, I., Kikuchi, T., Gilleaudeau, P., Sullivan-Whalen, M., Wittkowski, K. M., Papp, K., Garovoy, M., Dummer, W., Steinman, R. M., Krueger, J. G. (2005) Increase in TNF-α and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc. Natl. Acad. Sci. USA 102, 19057-19062. (Pubitemid 43049565)
33. Hoffman, R. A., Mahidhara, R. S., Wolf-Johnston, A. S., Lu, L., Thomson, A. W., Simmons, R. L. (2002) Differential modulation of CD4 and CD8 T-cell proliferation by induction of nitric oxide synthesis in antigen presenting cells. Transplantation 74, 836-845.
34. Powell, T. J., Jenkins, C. D., Hattori, R., MacPherson, G. G. (2003) Rat bone marrow-derived dendritic cells, but not ex vivo dendritic cells, secrete nitric oxide and can inhibit T-cell proliferation. Immunology 109, 197-208. (Pubitemid 36683610)
35. Suthar, M. S., Ma, D. Y., Thomas, S., Lund, J. M., Zhang, N., Daffis, S., Rudensky, A. Y., Bevan, M. J., Clark, E. A., Kaja, M. K., Diamond, M. S., Gale Jr., M. (2010) IPS-1 is essential for the control of West Nile virus infection and immunity. PLoS Pathog. 6, e1000757.
36. Inaba, K., Inaba, M., Romani, N., Aya, H., Deguchi, M., Ikehara, S., Muramatsu, S., Steinman, R. M. (1992) Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 176, 1693-1702.
37. Xu, Y., Zhan, Y., Lew, A. M., Naik, S. H., Kershaw, M. H. (2007) Differential development of murine dendritic cells by GM-CSF versus Flt3 ligand has implications for inflammation and trafficking. J. Immunol. 179, 7577-7584.
38. Lu, L., Bonham, C. A., Chambers, F. G., Watkins, S. C., Hoffman, R. A., Simmons, R. L., Thomson, A. W. (1996) Induction of nitric oxide synthase in mouse dendritic cells by IFN-γ, endotoxin, and interaction with allogeneic T cells: nitric oxide production is associated with dendritic cell apoptosis. J. Immunol. 157, 3577-3586. (Pubitemid 126449172)
39. Falcone, S., Perrotta, C., De Palma, C., Pisconti, A., Sciorati, C., Capobianco, A., Rovere-Querini, P., Manfredi, A. A., Clementi, E. (2004) Activation of acid sphingomyelinase and its inhibition by the nitric oxide/cyclic guanosine 3′,5′-monophosphate pathway: key events in Escherichia coli-elicited apoptosis of dendritic cells. J. Immunol. 173, 4452-4463. (Pubitemid 39280675)
40. Naik, S. H., Proietto, A. I., Wilson, N. S., Dakic, A., Schnorrer, P., Fuchsberger, M., Lahoud, M. H., O'Keeffe, M., Shao, Q. X., Chen, W. F., Villadangos, J. A., Shortman, K., Wu, L. (2005) Cutting edge: generation of splenic CD8+ and CD8- dendritic cell equivalents in Fms-like tyrosine kinase 3 ligand bone marrow cultures. J. Immunol. 174, 6592-6597. (Pubitemid 40705619)
41. Gilliet, M., Boonstra, A., Paturel, C., Antonenko, S., Xu, X. L., Trinchieri, G., O'Garra, A., Liu, Y. J. (2002) The development of murine plasmacytoid dendritic cell precursors is differentially regulated by FLT3-ligand and granulocyte/macrophage colony-stimulating factor. J. Exp. Med. 195, 953-958. (Pubitemid 34286765)
42. Dillon, S., Agrawal, S., Banerjee, K., Letterio, J., Denning, T. L., Oswald- Richter, K., Kasprowicz, D. J., Kellar, K., Pare, J., van Dyke, T., Ziegler, S., Unutmaz, D., Pulendran, B. (2006) Yeast zymosan, a stimulus for TLR2 and dectin-1, induces regulatory antigen-presenting cells and immunological tolerance. J. Clin. Invest. 116, 916-928.
43. Blasius, A. L., Giurisato, E., Cella, M., Schreiber, R. D., Shaw, A. S., Colonna, M. (2006) Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 177, 3260-3265. (Pubitemid 44277845)
44. Stanford, A., Chen, Y., Zhang, X. R., Hoffman, R., Zamora, R., Ford, H. R. (2001) Nitric oxide mediates dendritic cell apoptosis by downregulating inhibitors of apoptosis proteins and upregulating effector caspase activity. Surgery 130, 326-332. (Pubitemid 32721687)
45. Wong, S. H., Santambrogio, L., Strominger, J. L. (2004) Caspases and nitric oxide broadly regulate dendritic cell maturation and surface expression of class II MHC proteins. Proc. Natl. Acad. Sci. USA 101, 17783-17788. (Pubitemid 40051964)
46. Nishioka, Y., Wen, H., Mitani, K., Robbins, P. D., Lotze, M. T., Sone, S., Tahara, H. (2003) Differential effects of IL-12 on the generation of alloreactive CTL mediated by murine and human dendritic cells: a critical role for nitric oxide. J. Leukoc. Biol. 73, 621-629. (Pubitemid 38040475)
47. Wang, Q., McLoughlin, R. M., Cobb, B. A., Charrel-Dennis, M., Zaleski, K. J., Golenbock, D., Tzianabos, A. O., Kasper, D. L. (2006) A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 203, 2853-2863. (Pubitemid 46026163)
48. Ivanov, S., Dragoi, A. M., Wang, X., Dallacosta, C., Louten, J., Musco, G., Sitia, G., Yap, G. S., Wan, Y., Biron, C. A., Bianchi, M. E., Wang, H., Chu, W. M. (2007) A novel role for HMGB1 in TLR9-mediated inflammatory responses to CpG-DNA. Blood 110, 1970-1981. (Pubitemid 47443911)
49. Pérez, O., Bracho, G., Lastre, M., Mora, N., del Campo, J., Gil, D., Zayas, C., Acevedo, R., Gonzalez, D., Lopez, J. A., Taboada, C., Turtle, C., Solis, R. L. (2004) Novel adjuvant based on a proteoliposome-derived cochleate structure containing native lipopolysaccharide as a pathogen-associated molecular pattern. Immunol. Cell Biol. 82, 603-610. (Pubitemid 39563961)
50. Haider, A. S., Lowes, M. A., Suarez-Farinas, M., Zaba, L. C., Cardinale, I., Khatcherian, A., Novitskaya, I., Wittkowski, K. M., Krueger, J. G. (2008) Identification of cellular pathways of "type 1," Th17 T cells, and TNF-and inducible nitric oxide synthase-producing dendritic cells in autoimmune inflammation through pharmacogenomic study of cyclosporine A in psoriasis. J. Immunol. 180, 1913-1920.
51. Corinti, S., Pastore, S., Mascia, F., Girolomoni, G. (2003) Regulatory role of nitric oxide on monocyte-derived dendritic cell functions. J. Interferon Cytokine Res. 23, 423-431. (Pubitemid 37034580)
52. Paolucci, C., Burastero, S. E., Rovere-Querini, P., De Palma, C., Falcone, S., Perrotta, C., Capobianco, A., Manfredi, A. A., Clementi, E. (2003) Synergism of nitric oxide and maturation signals on human dendritic cells occurs through a cyclic GMP-dependent pathway. J. Leukoc. Biol. 73, 253-262. (Pubitemid 36158300)
53. Copin, R., De Baetselier, P., Carlier, Y., Letesson, J. J., Muraille, E. (2007) MyD88-dependent activation of B220-CD11b+LY-6C+ dendritic cells during Brucella melitensis infection. J. Immunol. 178, 5182-5191. (Pubitemid 46595302)
54. De Trez, C., Magez, S., Akira, S., Ryffel, B., Carlier, Y., Muraille, E. (2009) iNOS-producing inflammatory dendritic cells constitute the major infected cell type during the chronic Leishmania major infection phase of C57BL/6 resistant mice. PLoS Pathog. 5, e1000494.
55. Lin, K. L., Suzuki, Y., Nakano, H., Ramsburg, E., Gunn, M. D. (2008) CCR2+ monocyte-derived dendritic cells and exudate macrophages produce influenza-induced pulmonary immune pathology and mortality. J. Immunol. 180, 2562-2572.
56. Aldridge Jr., J. R., Moseley, C. E., Boltz, D. A., Negovetich, N. J., Reynolds, C., Franks, J., Brown, S. A., Doherty, P. C., Webster, R. G., Thomas, P. G. (2009) TNF/iNOS-producing dendritic cells are the necessary evil of lethal influenza virus infection. Proc. Natl. Acad. Sci. USA 106, 5306-5311.
57. Bosschaerts, T., Guilliams, M., Stijlemans, B., Morias, Y., Engel, D., Tacke, F., Herin, M., De Baetselier, P., Beschin, A. (2010) Tip-DC development during parasitic infection is regulated by IL-10 and requires CCL2/CCR2, IFN-γ and MyD88 signaling. PLoS Pathog. 6, e1001045.
58. Getts, D. R., Terry, R. L., Getts, M. T., Muller, M., Rana, S., Shrestha, B., Radford, J., Van Rooijen, N., Campbell, I. L., King, N. J. (2008) Ly6c+ "inflammatory monocytes" are microglial precursors recruited in a pathogenic manner in West Nile virus encephalitis. J. Exp. Med. 205, 2319-2337.
59. Lobigs, M., Mullbacher, A., Wang, Y., Pavy, M., Lee, E. (2003) Role of type I and type II interferon responses in recovery from infection with an encephalitic flavivirus. J. Gen. Virol. 84, 567-572. (Pubitemid 36267129)
60. Samuel, M. A., Diamond, M. S. (2006) Pathogenesis of West Nile virus infection: a balance between virulence, innate and adaptive immunity, and viral evasion. J. Virol. 80, 9349-9360. (Pubitemid 44435614)
61. Willenborg, D. O., Staykova, M., Fordham, S., O'Brien, N., Linares, D. (2007) The contribution of nitric oxide and interferon γ to the regulation of the neuro-inflammation in experimental autoimmune encephalomyelitis. J. Neuroimmunol. 191, 16-25. (Pubitemid 350060995)
62. Bierly, A. L., Shufesky, W. J., Sukhumavasi, W., Morelli, A. E., Denkers, E. Y. (2008) Dendritic cells expressing plasmacytoid marker PDCA-1 are Trojan horses during Toxoplasma gondii infection. J. Immunol. 181, 8485-8491.
63. Tam, M. A., Wick, M. J. (2006) Differential expansion, activation and effector functions of conventional and plasmacytoid dendritic cells in mouse tissues transiently infected with Listeria monocytogenes. Cell. Microbiol. 8, 1172-1187. (Pubitemid 43871651)
64. Dogan, R. N., Elhofy, A., Karpus, W. J. (2008) Production of CCL2 by central nervous system cells regulates development of murine experimental autoimmune encephalomyelitis through the recruitment of TNF- and iNOS-expressing macrophages and myeloid dendritic cells. J. Immunol. 180, 7376-7384.
65. Bailey, S. L., Schreiner, B., McMahon, E. J., Miller, S. D. (2007) CNS myeloid DCs presenting endogenous myelin peptides "preferentially" polarize CD4+ T(H)-17 cells in relapsing EAE. Nat. Immunol. 8, 172-180.
66. Huang, Y. M., Yang, J. S., Xu, L. Y., Link, H., Xiao, B. G. (2000) Autoantigen-pulsed dendritic cells induce tolerance to experimental allergic encephalomyelitis (EAE) in Lewis rats. Clin. Exp. Immunol. 122, 437-444. (Pubitemid 32002204)
67. Xiao, B. G., Duan, R. S., Link, H., Huang, Y. M. (2003) Induction of peripheral tolerance to experimental autoimmune myasthenia gravis by acetylcholine receptor-pulsed dendritic cells. Cell. Immunol. 223, 63-69. (Pubitemid 36945550)
68. Salazar, L., Aravena, O., Abello, P., Escobar, A., Contreras-Levicoy, J., Rojas-Colonelli, N., Catalan, D., Aguirre, A., Zuniga, R., Pesce, B., Gonzalez, C., Cepeda, R., Cuchacovich, M., Molina, M. C., Salazar-Onfray, F., Delgado, M., Toes, R. E., Aguillon, J. C. (2008) Modulation of established murine collagen-induced arthritis by a single inoculation of short-term lipopolysaccharide-stimulated dendritic cells. Ann. Rheum. Dis. 67, 1235-1241.
69. Yamazaki, S., Inaba, K., Tarbell, K. V., Steinman, R. M. (2006) Dendritic cells expand antigen-specific Foxp3+ CD25+ CD4+ regulatory T cells including suppressors of alloreactivity. Immunol. Rev. 212, 314-329. (Pubitemid 44116717)
70. Taieb, A., Breitinger, J. J., Unadkat, J. V., Shufesky, W. J., Morelli, A. E., Thomson, A. W., Lee, W. P., Feili-Hariri, M. (2007) Intrinsic ability of GM+IL-4 but not Flt3L-induced rat dendritic cells to promote allogeneic T cell hyporesponsiveness. Clin. Immunol. 123, 176-189. (Pubitemid 46590068)
71. Mazzoni, A., Bronte, V., Visintin, A., Spitzer, J. H., Apolloni, E., Serafini, P., Zanovello, P., Segal, D. M. (2002) Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J. Immunol. 168, 689-695. (Pubitemid 34049569)
72. Rössner, S., Voigtlander, C., Wiethe, C., Hanig, J., Seifarth, C., Lutz, M. B. (2005) Myeloid dendritic cell precursors generated from bone marrow suppress T cell responses via cell contact and nitric oxide production in vitro. Eur. J. Immunol. 35, 3533-3544. (Pubitemid 43025534)
73. Xu, L., Huang, Y., Yang, J., Van Der Meide, P. H., Levi, M., Wahren, B., Link, H., Xiao, B. (1999) Dendritic cell-derived nitric oxide is involved in IL-4-induced suppression of experimental allergic encephalomyelitis (EAE) in Lewis rats. Clin. Exp. Immunol. 118, 115-121. (Pubitemid 29479792)
74. Wood, K. J., Sawitzki, B. (2006) Interferon γ: a crucial role in the function of induced regulatory T cells in vivo. Trends Immunol. 27, 183-187.
75. Zhang, M., Tang, H., Guo, Z., An, H., Zhu, X., Song, W., Guo, J., Huang, X., Chen, T., Wang, J., Cao, X. (2004) Splenic stroma drives mature dendritic cells to differentiate into regulatory dendritic cells. Nat. Immunol. 5, 1124-1133. (Pubitemid 39549626)
76. Feng, G., Gao, W., Strom, T. B., Oukka, M., Francis, R. S., Wood, K. J., Bushell, A. (2008) Exogenous IFN-γ ex vivo shapes the alloreactive T-cell repertoire by inhibition of Th17 responses and generation of functional Foxp3+ regulatory T cells. Eur. J. Immunol. 38, 2512-2527.
77. Tang, H., Guo, Z., Zhang, M., Wang, J., Chen, G., Cao, X. (2006) Endothelial stroma programs hematopoietic stem cells to differentiate into regulatory dendritic cells through IL-10. Blood 108, 1189-1197. (Pubitemid 44232014)