Neuronal nitric oxide synthase modulates maturation of human dendritic cells

Journal of Immunology

Volumn 184, Issue 11, 2010, Pages 6025-6034

  Adler, Henric S ^a   Simon, Alexandra ^a   Graulich, Edith ^a   Habermeier, Alice ^a   Bacher, Nicole ^a   Friebe, Andreas ^b   Closs, Ellen I ^a   Steinbrink, Kerstin ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARGININE; CD83 ANTIGEN; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GUANYLATE CYCLASE; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITRIC OXIDE SYNTHASE; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR; CYTOKINE; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE;

ARTICLE; AUTOCRINE EFFECT; CELL CULTURE; CELL DIFFERENTIATION; CELL MATURATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; ENZYME REGULATION; HUMAN; HUMAN CELL; NERVE CELL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION; BIOSYNTHESIS; CELL LINE; CELL SEPARATION; CYTOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; IMMUNOBLOTTING; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CELL DIFFERENTIATION; CELL LINE; CELL SEPARATION; CYTOKINES; DENDRITIC CELLS; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HUMANS; IMMUNOBLOTTING; LYMPHOCYTE ACTIVATION; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE I; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 77953402823     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.0901327     Document Type: Article

References (45)

1. Nathan, C., and Q. W. Xie. 1994. Nitric oxide synthases: roles, tolls, and controls. Cell 78: 915-918.
2. Bogdan, C. 2001. Nitric oxide and the immune response. Nat. Immunol. 2: 907-916.
3. Niedbala, W., B. Cai, and F. Y. Liew. 2006. Role of nitric oxide in the regulation of T cell functions. Ann. Rheum. Dis. 65: 37-40.
4. Niedbala, W., X. Q. Wei, C. Campbell, D. Thomson, M. Komai-Koma, and F. Y. Liew. 2002. Nitric oxide preferentially induces type 1 T cell differentiation by selectively up-regulating IL-12 receptor b 2 expression via cGMP. Proc. Natl. Acad. Sci. USA 99: 16186-16191.
5. MacMicking, J. D., R. J. North, R. LaCourse, J. S. Mudgett, S. K. Shah, and C. F. Nathan. 1997. Identification of nitric oxide synthase as a protective locus against tuberculosis. Proc. Natl. Acad. Sci. USA 94: 5243-5248.
6. Suschek, C. V., O. Schnorr, and V. Kolb-Bachofen. 2004. The role of iNOS in chronic inflammatory processes in vivo: is it damage-promoting, protective, or active at all? Curr. Mol. Med. 4: 763-775.
7. Lowes, M. A., F. Chamian, M. V. Abello, J. Fuentes-Duculan, S. L. Lin, R. Nussbaum, I. Novitskaya, H. Carbonaro, I. Cardinale, T. Kikuchi, et al. 2005. Increase in TNF-a and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc. Natl. Acad. Sci. USA 102: 19057-19062.
8. Guttman-Yassky, E., M. A. Lowes, J. Fuentes-Duculan, J. Whynot, I. Novitskaya, I. Cardinale, A. Haider, A.Khatcherian, J. A. Carucci, R. Bergman, and J. G. Krueger. 2007.Major differences in inflammatory dendritic cells and their products distinguish atopic dermatitis from psoriasis. J. Allergy Clin. Immunol. 119: 1210-1217.
9. Nestle, F. O., D. H. Kaplan, and J. Barker. 2009. Psoriasis. N. Engl. J. Med. 361: 496-509.
10. Ardavín, C., G. Martínez del Hoyo, P. Martín, F. Anjuère, C. F. Arias, A. R.Marín, S. Ruiz, V. Parrillas, and H. Hernández. 2001. Origin and differentiation of dendritic cells. Trends Immunol. 22: 691-700.
11. Steinman, R. M. Dendritic cells: understanding immunogenicity. 2007. Eur. J. Immunol. l37: S53-60.
12. Ardavín, C. 2003. Origin, precursors and differentiation of mouse dendritic cells. Nat. Rev. Immunol. 3: 582-590.
13. Jonuleit, H., U. Kühn, G. Müller, K. Steinbrink, L. Paragnik, E. Schmitt, J. Knop, and A. H. Enk. 1997. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur. J. Immunol. 27: 3135-3142.
14. Nishioka, Y., H. Wen, K. Mitani, P. D. Robbins, M. T. Lotze, S. Sone, and H. Tahara. 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.
15. Fernández-Ruiz, V., A. González, and N. López-Moratalla. 2004. Effect of nitric oxide in the differentiation of human monocytes to dendritic cells. Immunol. Lett. 93: 87-95.
16. Morita, R., T. Uchiyama, and T. Hori. 2005. Nitric oxide inhibits IFN-α production of human plasmacytoid dendritic cells partly via a guanosine 3′,5′-cyclic monophosphate-dependent pathway. J. Immunol. 175: 806-812. (Pubitemid 41094962)
17. Stuehr, D. J. 1999. Mammalian nitric oxide synthases. Biochim. Biophys. Acta 1411: 217-230.
18. Alderton, W. K., C. E. Cooper, and R. G. Knowles. 2001. Nitric oxide synthases: structure, function and inhibition. Biochem. J. 357: 593-615.
19. Förstermann, U., J. P. Boissel, and H. Kleinert. 1998. Expressional control of the 'constitutive' isoforms of nitric oxide synthase (NOS I and NOS III). FASEB J. 12: 773-790.
20. Lu, L., C. A. Bonham, F. G. Chambers, S. C. Watkins, R. A. Hoffman, R. L. Simmons, and A. W. Thomson. 1996. Induction of nitric oxide synthase in mouse dendritic cells by IFN-gamma, endotoxin, and interaction with allogeneic T cells: nitric oxide production is associated with dendritic cell apoptosis. J. Immunol. 157: 3577-3586.
21. Huang, D., D. T. Cai, R. Y. R. Chua, D. M. Kemeny, and S. H. Wong. 2008. Nitric-oxide synthase 2 interacts with CD74 and inhibits its cleavage by caspase during dendritic cell development. J. Biol. Chem. 283: 1713-1722.
22. Serbina, N. V., T. P. Salazar-Mather, C. A. Biron, W. A. Kuziel, and E. G. Pamer. 2003. TNF/iNOS-producing dendritic cells mediate innate immune defense against bacterial infection. Immunity 19: 59-70.
23. Fernández-Ruiz, V., N. López-Moratalla, and A. González. 2005. Production of nitric oxide and self-nitration of proteins during monocyte differentiation to dendritic cells. J. Physiol. Biochem. 61: 517-525.
24. Bagley, K. C., S. F. Abdelwahab, R. G. Tuskan, and G. K. Lewis. 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.
25. Lindemann, S., C. Gierer, and H. Darius. 2003. Prostacyclin inhibits adhesion of polymorphonuclear leukocytes to human vascular endothelial cells due to adhesion molecule independent regulatory mechanisms. Basic Res. Cardiol. 98: 8-15.
26. Adler, H., S. Kubsch, E. Graulich, S. Ludwig, J. Knop, and K. Steinbrink. 2007. Activation of MAP kinase p38 is critical for the regulatory function of anergic T cells induced by tolerogenic dendritic cells. Blood 109: 4351-4359.
27. Ishii, K., H. Sheng, T. D. Warner, U. Förstermann, and F. A. Murad. 1991. A simple and sensitive bioassay method for detection of EDRF with RFL-6 rat lung fibroblasts. Am. J. Physiol. 261: H598-H603.
28. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426.
29. Closs, E. I. 2002. Expression, regulation and function of carrier proteins for cationic amino acids. Curr. Opin. Nephrol. Hypertens. 11: 99-107.
30. Closs, E. I., J. P. Boissel, A. Habermeier, and A. Rotmann. 2006. Structure and function of cationic amino acid transporters (CATs). J. Membr. Biol. 213: 67-77.
31. Bronte, V., and P. Zanovello. 2005. Regulation of immune responses by Larginine metabolism. Nat. Rev. Immunol. 5: 641-654.
32. Munder, M., K. Eichmann, J. M. Morán, F. Centeno, G. Soler, and M. Modolell. 1999. Th1/Th2-regulated expression of arginase isoforms in murine macrophages and dendritic cells. J. Immunol. 163: 3771-3777. (Pubitemid 29450901)
33. Munder, M., F. Mollinedo, J. Calafa, J. Canchado, C. Gil-Lamaignere, J. M. Fuentes, C. Luckner, G. Doschko, and G. Soler, K. Eichmann K,F. M. Müller, A. D. Ho, M. Goerner, and M. Modolell. 2005. Arginase I is constitutively expressed in human granulocytes and participates in fungicidal activity. Blood 105:2549-2556.
34. Zhu, J., and W. E. Paul. 2008. CD4 T cells: fates, functions, and faults. Blood 112: 1557-1569.
35. Paolucci, C., P. Rovere, C. De Nadai, A. A. Manfredi, and E. Clementi. 2000. Nitric oxide inhibits the tumor necrosis factor a -regulated endocytosis of human dendritic cells in a cyclic GMP-dependent way. J. Biol. Chem. 275: 19638-19644.
36. Paolucci, C., S. E. Burastero, P. Rovere-Querini, C. De Palma, S. Falcone, C. Perrotta, A. Capobianco, A. A. Manfredi, and E. Clementi. 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.
37. Moncada, S., and E. A. Higgs. 1995. Molecular mechanisms and therapeutic strategies related to nitric oxide. FASEB J. 9: 1319-1330.
38. Niedbala, W., X. Q. Wei, D. Piedrafita, D. Xu, and F. Y. Liew. 1999. Effects of nitric oxide on the induction and differentiation of Th1 cells. Eur. J. Immunol. 29: 2498-2505.
39. Steinbrink, K., M. Wölfl, H. Jonuleit, J. Knop, and A. H. Enk. 1997. Induction of tolerance by IL-10-treated dendritic cells. J. Immunol. 159: 4772-4780.
40. Vignali, D. A., L. W. Collison, and C. J. Workman. 2008. How regulatory T cells work. Nat. Rev. Immunol. 8: 523-532.
41. Steinbrink, K., K. Mahnke, S. Grabbe, A. H. Enk, and H. Jonuleit. 2009. Myeloid dendritic cell: From sentinel of immunity to key player of peripheral tolerance? Hum. Immunol. 70: 289-293.
42. Eksioglu, E. A., S. Eisen, and V. Reddy. 2010. Dendritic cells as therapeutic agents against cancer. Front. Biosci. 15: 321-347.
43. Bonham, C. A., L. Lu, Y. Li, R. A. Hoffman, R. L. Simmons, and A. W. Thomson. 1996. Nitric oxide production by mouse bone marrow-derived dendritic cells: implications for the regulation of allogeneic T cell responses. Transplantation 62: 1871-1877.
44. Williams, M. S., S. Noguchi, P. A. Henkart, and Y. Osawa. 1998. Nitric oxide synthase plays a signaling role in TCR-triggered apoptotic death. J. Immunol. 161: 6526-6531.
45. van der Veen, R. C., T. A. Dietlin, L. Pen, and J. D. Gray. 1999. Nitric oxide inhibits the proliferation of T-helper 1 and 2 lymphocytes without reduction in cytokine secretion. Cell. Immunol. 193: 194-201.