The role of nitric oxide in the regulation of adaptive immune responses

Inmunologia

Volumn 27, Issue 3, 2008, Pages 103-117

  Ibiza, S ^a   Serrador, Juan M ^a  

^a CENTRO NACIONAL DE INVESTIGACIONES CARDIOVASCULARES CNIC   (Spain)

Author keywords

cNOS; iNOS; Nitric oxide; T lymphocytes

Indexed keywords

ENDOTOXIN; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 1BETA; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTING CELL; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL FUNCTION; CYTOKINE PRODUCTION; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOREGULATION; MACROPHAGE; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

EID: 77956018310     PISSN: 02139626     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0213-9626(08)70058-1     Document Type: Review

References (129)

1. Hobbs AJ, Higgs A, Moncada S. Inhibition of nitric oxide synthase as a potential therapeutic target. Annu Rev Pharmacol Toxicol 1999;39:191-220. (Pubitemid 29222557)
2. Bogdan C. Nitric oxide and the immune response. Nat Immunol 2001; 2:907-16.
3. Knowles RG, Moncada S. Nitric oxide synthases in mammals. Biochem J 1994; 298:249-258.
4. Groves JT, Wang CC. Nitric oxide synthase: models and mechanisms. Curr Opin Chem Biol 2000; 4:687-695.
5. Dimmeler S, Fleming I, Fisslthaler B, Hermann C, Busse R, Zeiher AM. Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 1999; 399:601-605. (Pubitemid 29279182)
6. Fulton D, Gratton JP, McCabe TJ, Fontana J, Fujio Y, Walsh K, et al. Regulation of endothelium-derived nitric oxide production by the protein kinase Akt. Nature 1999; 399:597-601. (Pubitemid 29279181)
7. Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: Structure, function and inhibition. Biochem J 2001; 357:593-615. (Pubitemid 32735142)
8. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: Purview and parameters. Nat Rev Mol Cell Biol 2005; 6:150-166.
9. Bogdan C, Rollinghoff M, Diefenbach A. The role of nitric oxide in innate immunity. Immunol Rev 2000; 173:17-26. (Pubitemid 30095207)
10. 2+/calmodulin- dependent isoform in human B and T lymphocytes. Eur J Immunol 1996; 26:511-516.
11. Stuehr DJ, Cho HJ, Kwon NS, Weise MF, Nathan CF. Purification and characterization of the cytokine-induced macrophage nitric oxide synthase:An FAD- and FMN-containing flavoprotein. Proc Natl Acad Sci USA 1991; 88:7773-7777.
12. Schneemann M, Schoedon G. Species differences in macrophage NO production are important. Nat Immunol 2002; 3:102.
13. Schonhoff CM, Gaston B, Mannick JB. Nitrosylation of cytochrome c during apoptosis. J Biol Chem 2003; 278:18265-18270.
14. Diefenbach A, Schindler H, Donhauser N, Lorenz E, Laskay T, MacMicking J, et al. Type 1 interferon (IFNα/β) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite. Immunity 1998; 8:77-87. (Pubitemid 28097825)
15. Diefenbach A, Schindler H, Rollinghoff M, Yokoyama WM, Bogdan C. Requirement for type 2 NO synthase for IL-12 signaling in innate immunity. Science 1999; 284:951-955. (Pubitemid 29288431)
16. Kolb H, Kolb-Bachofen V. Nitric oxide in autoimmune disease: Cytotoxic or regulatory mediator? Immunol Today 1998; 19:556-561.
17. Niedbala W, Cai B, Liew FY. Role of nitric oxide in the regulation of T cell functions. Ann Rheum Dis 2006; 65 Suppl 3:iii37-40.
18. Mazzoni A, Bronte V, Visintin A, Spitzer JH, Apolloni E, Serafini P, et al. Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J Immunol 2002; 168:689-695.
19. Hongo D, Bryson JS, Kaplan AM, Cohen DA. Endogenous nitric oxide protects against T cell-dependent lethality during graft-versus-host disease and idiopathic pneumonia syndrome. J Immunol 2004; 173:1744-1756.
20. Fiorucci S, Mencarelli A, Distrutti E, Baldoni M, del Soldato P, Morelli A. Nitric oxide regulates immune cell bioenergetic: a mechanism to understand immunomodulatory functions of nitric oxide-releasing anti-inflammatory drugs. J Immunol 2004; 173:874-882.
21. Sriskandan S, Evans TJ, Cohen J. Bacterial superantigen-induced human lymphocyte responses are nitric oxide dependent and mediated by IL-12 and IFN-γ. J Immunol 1996; 156:2430-2435.
22. Suschek CV, Schnorr O, Kolb-Bachofen V. The role of iNOS in chronic inflammatory processes in vivo: Is it damage-promoting, protective, or active at all? Curr Mol Med 2004; 4:763-775.
23. Guzik TJ, Korbut R, Adamek-Guzik T. Nitric oxide and superoxide in inflammation and immune regulation. J Physiol Pharmacol 2003; 54:469-487.
24. Thippeswamy T, McKay JS, Quinn JP, Morris R. Nitric oxide, a biological double-faced janus - Is this good or bad? Histol Histopathol 2006; 21:445-458.
25. Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol 2003; 24:302-306.
26. Florquin S, Amraoui Z, Dubois C, Decuyper J, Goldman M. The protective role of endogenously synthesized nitric oxide in staphylococcal enterotoxin B-induced shock in mice. J Exp Med 1994; 180:1153-1158. (Pubitemid 24256629)
27. Zech B, Kohl R, von Knethen A, Brune B. Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases. Biochem J 2003; 371:1055-1064. (Pubitemid 36578905)
28. Bogdan C. Nitric oxide and the regulation of gene expression. Trends Cell Biol 2001; 11:66-75. (Pubitemid 32144753)
29. Pfeilschifter J, Eberhardt W, Beck KF. Regulation of gene expression by nitric oxide. Pflugers Arch 2001; 442:479-486. (Pubitemid 32673312)
30. Michel T, Feron O. Nitric oxide synthases: which, where, how, and why? J Clin Invest 1997; 100:2146-2152.
31. Renno T, Hahne M, MacDonald HR. Proliferation is a prerequisite for bacterial superantigen-induced T cell apoptosis in vivo. J Exp Med 1995; 181:2283-2287.
32. McKay DM, Lu J, Jedrzkiewicz S, Ho W, Sharkey KA. Nitric oxide participates in the recovery of normal jejunal epithelial ion transport following exposure to the superantigen, Staphylococcus aureus enterotoxin B. J Immunol 1999; 163:4519-4526. (Pubitemid 29474522)
33. Rachlis A, Watson JL, Lu J, McKay DM. Nitric oxide reduces bacterial superantigen-immune cell activation and consequent epithelial abnormalities. J Leukoc Biol 2002; 72:339-346.
34. Bronte V, Zanovello P. Regulation of immune responses by Larginine metabolism. Nat Rev Immunol 2005; 5:641-654. (Pubitemid 41113195)
35. Rodriguez PC, Zea AH, Culotta KS, Zabaleta J, Ochoa JB, Ochoa AC. Regulation of T cell receptor CD3zeta chain expression by Larginine. J Biol Chem 2002; 277:21123-21129. (Pubitemid 34952247)
36. Bingisser RM, Tilbrook PA, Holt PG, Kees UR. Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway. J Immunol 1998; 160:5729-5734.
37. Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell 1996; 85:803-815. (Pubitemid 126334356)
38. Li CQ, Trudel LJ, Wogan GN. Nitric oxide-induced genotoxicity, mitochondrial damage, and apoptosis in human lymphoblastoid cells expressing wild-type and mutant p53. Proc Natl Acad Sci USA 2002; 99:10364-10369.
39. Gordon SA, Abou-Jaoude W, Hoffman RA, McCarthy SA, Kim Y-M, Zhang XR, et al. Nitric oxide induces murine thymocyte apoptosis by oxidative injury and a p53-dependent mechanism. J Leukoc Biol 2001; 70:87-95. (Pubitemid 32613667)
40. Hara MR, Agrawal N, Kim SF, Cascio MB, Fujimuro M, Ozeki Y, et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 2005; 7:665-674. (Pubitemid 40975747)
41. Bosca L, Zeini M, Traves PG, Hortelano S. Nitric oxide and cell viability in inflammatory cells: A role for NO in macrophage function and fate. Toxicology 2005; 208:249-258. (Pubitemid 40187335)
42. Liu L, Stamler JS. NO: An inhibitor of cell death. Cell Death Differ 1999; 6:937-942.
43. Dimmeler S, Haendeler J, Sause A, Zeiher AM. Nitric oxide inhibits APO-1/Fas-mediated cell death. Cell Growth Differ 1998; 9:415-422. (Pubitemid 28345880)
44. Bonfoco E, Krainc D, Ankarcrona M, Nicotera P, Lipton SA. Apoptosis and necrosis: Two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci USA 1995; 92:7162-7166.
45. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, et al. Fas-induced caspase denitrosylation. Science 1999; 284:651-654.
46. Melino G, Bernassola F, Catani MV, Rossi A, Corazzari M, Sabatini S, et al. Nitric oxide inhibits apoptosis via AP-1-dependent CD95L transactivation. Cancer Res 2000; 60:2377-2383. (Pubitemid 30262426)
47. Brune B, von Knethen A, Sandau KB. Nitric oxide (NO): An effector of apoptosis. Cell Death Differ 1999; 6:969-975.
48. Matsumoto A, Comatas KE, Liu L, Stamler JS. Screening for nitric oxide-dependent protein-protein interactions. Science 2003; 301:657-661. (Pubitemid 36927951)
49. Genaro AM, Hortelano S, Alvarez A, Martinez C, Bosca L. Splenic B lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels. J Clin Invest 1995; 95:1884-1890.
50. Sciorati C, Rovere P, Ferrarini M, Heltai S, Manfredi AA, Clementi E. Autocrine nitric oxide modulates CD95-induced apoptosis in gammadelta T lymphocytes. J Biol Chem 1997; 272:23211-23215. (Pubitemid 27392455)
51. Park HS, Yu JW, Cho JH, Kim MS, Huh SH, Ryoo K, Choi EJ. Inhibition of apoptosis signal-regulating kinase 1 by nitric oxide through a thiol redox mechanism. J Biol Chem 2004; 279:7584-7590.
52. Leist M, Single B, Naumann H, Fava E, Simon B, Kuhnle S, Nicotera P. Nitric oxide inhibits execution of apoptosis at two distinct ATP-dependent steps upstream and downstream of mitochondrial cytochrome c release. Biochem Biophys Res Commun 1999; 258:215-221.
53. Erusalimsky JD, Moncada S. Nitric oxide and mitochondrial signaling: from physiology to pathophysiology. Arterioscler Thromb Vasc Biol 2007; 27:2524-2531.
54. Leist M, Single B, Naumann H, Fava E, Simon B, Kuhnle S, Nicotera P. Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. Exp Cell Res 1999; 249:396-403.
55. Moncada S, Erusalimsky JD. Does nitric oxide modulate mitochondrial energy generation and apoptosis? Nat Rev Mol Cell Biol 2002; 3:214-220.
56. Mannick JB, Schonhoff CM. NO means no and yes: Regulation of cell signaling by protein nitrosylation. Free Radic Res 2004; 38:1-7.
57. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly. Am J Physiol 1996; 271:C1424-1437.
58. Szabo C. DNA strand breakage and activation of poly-ADP ribosyltransferase: A cytotoxic pathway triggered by peroxynitrite. Free Radic Biol Med 1996; 21:855-869.
59. Schindler H, Bogdan C. NO as a signaling molecule: Effects on kinases. Int Immunopharmacol 2001; 1:1443-1455.
60. Reynaert NL, Ckless K, Korn SH, Vos N, Guala AS, Wouters EF, et al. Nitric oxide represses inhibitory κB kinase through Snitrosylation. Proc Natl Acad Sci USA 2004; 101:8945-8950.
61. Marshall HE, Stamler JS. Nitrosative stress-induced apoptosis through inhibition of NF-κ B. J Biol Chem 2002; 277:34223-34228.
62. Lander HM, Ogiste JS, Teng KK, Novogrodsky A. p21ras as a common signaling target of reactive free radicals and cellular redox stress. J Biol Chem 1995; 270:21195-21198.
63. De Martin R, Hoeth M, Hofer-Warbinek R, Schmid JA. The transcription factor NF-κ B and the regulation of vascular cell function. Arterioscler Thromb Vasc Biol 2000; 20:E83-88.
64. Hickey MJ, Kubes P. Role of nitric oxide in regulation of leucocyte-endothelial cell interactions. Exp Physiol 1997; 82:339-348.
65. Hickey MJ, Granger DN, Kubes P. Inducible nitric oxide synthase (iNOS) and regulation of leucocyte/endothelial cell interactions: studies in iNOS-deficient mice. Acta Physiol Scand 2001; 173:119-126.
66. Nikitovic D, Holmgren A, Spyrou G. Inhibition of AP-1 DNA binding by nitric oxide involving conserved cysteine residues in Jun and Fos. Biochem Biophys Res Commun 1998; 242:109-112.
67. Klatt P, Molina EP, Lamas S. Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation. J Biol Chem 1999; 274:15857-15864.
68. Zouki C, Jozsef L, Ouellet S, Paquette Y, Filep JG. Peroxynitrite mediates cytokine-induced IL-8 gene expression and production by human leukocytes. J Leukoc Biol 2001; 69:815-824.
69. Chu SC, Marks-Konczalik J, Wu HP, Banks TC, Moss J. Analysis of the cytokine-stimulated human inducible nitric oxide synthase (iNOS) gene: Characterization of differences between human and mouse iNOS promoters. Biochem Biophys Res Commun 1998; 248:871-878.
70. Connelly L, Madhani M, Hobbs AJ. Resistance to endotoxic shock in endothelial nitric-oxide synthase (eNOS) knock-out mice: A pro-inflammatory role for eNOS-derived NO in vivo. J Biol Chem 2005; 280:10040-10046.
71. Blesson S, Thiery J, Gaudin C, Stancou JP, Kolb JL, Moreau J, et al. Analysis of the mechanisms of human cytotoxic T lymphocyte response inhibition by NO. Int Immunol 2002; 14:1169-1178.
72. Fiedler B, Lohmann SM, Smolenski A, Linnemuller S, Pieske B, Schroder F, et al. Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes. Proc Natl Acad Sci USA 2002; 99:11363-1136.
73. Mannick JB, Asano K, Izumi K, Kieff E, Stamler JS. Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein-Barr virus reactivation. Cell 1994; 79:1137-1146.
74. Beltran B, Quintero M, Garcia-Zaragoza E, O'Connor E, Esplugues JV, Moncada S. Inhibition of mitochondrial respiration by endogenous nitric oxide: a critical step in Fas signaling. Proc Natl Acad Sci USA 2002; 99:8892-8897.
75. Cherla RP, Ganju RK. Stromal cell-derived factor 1 α-induced chemotaxis in T cells is mediated by nitric oxide signaling pathways. J Immunol 2001; 166:3067-3074.
76. Vig M, Srivastava S, Kandpal U, Sade H, Lewis V, Sarin A, et al. Inducible nitric oxide synthase in T cells regulates T cell death and immune memory. J Clin Invest 2004; 113:1734-1742.
77. Taylor-Robinson AW, Liew FY, Severn A, Xu D, McSorley SJ, Garside P, et al. Regulation of the immune response by nitric oxide differentially produced by T helper type 1 and T helper type 2 cells. Eur J Immunol 1994; 24:980-984.
78. Barreiro Arcos ML, Gorelik G, Klecha A, Genaro AM, Cremaschi GA. Thyroid hormones increase inducible nitric oxide synthase gene expression downstream from PKC-ζ in murine tumor T lymphocytes. Am J Physiol Cell Physiol 2006; 291:C327-336.
79. Mori N, Nunokawa Y, Yamada Y, Ikeda S, Tomonaga M, Yamamoto N. Expression of human inducible nitric oxide synthase gene in T-cell lines infected with human T-cell leukemia virus type-I and primary adult T-cell leukemia cells. Blood 1999; 94: 2862-2870.
80. Jimenez JL, Gonzalez-Nicolas J, Alvarez S, Fresno M, Munoz- Fernandez MA. Regulation of human immunodeficiency virus type 1 replication in human T lymphocytes by nitric oxide. J Virol 2001; 75:4655-4663.
81. Koh KP, Wang Y, Yi T, Shiao SL, Lorber MI, Sessa WC, Tellides G, Pober JS. T cell-mediated vascular dysfunction of human allografts results from IFN-γ dysregulation of NO synthase. J Clin Invest 2004; 114:846-856.
82. Choy JC, Wang Y, Tellides G, Pober JS. Induction of inducible NO synthase in bystander human T cells increases allogeneic responses in the vasculature. Proc Natl Acad Sci USA 2007; 104:1313-1318.
83. Esaki T, Hayashi T, Muto E, Yamada K, Kuzuya M, Iguchi A. Expression of inducible nitric oxide synthase in T lymphocytes and macrophages of cholesterol-fed rabbits. Atherosclerosis 1997; 128:39-46. (Pubitemid 27065259)
84. Bustamante J, Bersier G, Badin RA, Cymeryng C, Parodi A, Boveris A. Sequential NO production by mitochondria and endoplasmic reticulum during induced apoptosis. Nitric Oxide 2002; 6:333-341.
85. Ibiza S, Victor VM, Bosca I, Ortega A, Urzainqui A, O'Connor J, et al. Endothelial nitric oxide synthase regulates T cell receptor signaling at the immunological synapse. Immunity 2006; 24:753-765.
86. 2+- and redox-dependent production of nitric oxide. J Immunol 2003; 171:5188-5197.
87. 2+ signaling profile of lupus T cells. J Immunol 2004; 173:3676-3683.
88. Averna M, Stifanese R, De Tullio R, Salamino F, Bertuccio M, Pontremoli S, Melloni E. Proteolytic degradation of nitric oxide synthase isoforms by calpain is modulated by the expression levels of HSP90. Febs J 2007; 274:6116-6127.
89. Williams MS, Noguchi S, Henkart PA, Osawa Y. Nitric oxide synthase plays a signaling role in TCR-triggered apoptotic death. J Immunol 1998; 161:6526-6531.
90. Koncz A, Pasztoi M, Mazan M, Fazakas F, Buzas E, Falus A, Nagy G. Nitric oxide mediates T cell cytokine production and signal transduction in histidine decarboxylase knockout mice. J Immunol 2007; 179:6613-6619.
91. Horvath BV, Szalai C, Mandi Y, Laszlo V, Radvany Z, Darvas Z, Falus A. Histamine and histamine-receptor antagonists modify gene expression and biosynthesis of interferon gamma in peripheral human blood mononuclear cells and in CD19-depleted cell subsets. Immunol Lett 1999; 70:95-99.
92. Haddad W, Cooper CJ, Zhang Z, Brown B, Zhu Y, Issekutz A, et al. P-selectin and P-selectin glycoprotein ligand 1 are major determinants for Th1 cell recruitment to nonlymphoid effector sites in the intestinal lamina propria. J Exp Med 2003; 198:369-377.
93. Norman MU, Zbytnuik L, Kubes P. Interferon-γ limits Th1 lymphocyte adhesion to inflamed endothelium: A nitric oxide regulatory feedback mechanism. Eur J Immunol 2008; 38:1368-1380.
94. Mason D, Fowell D. T-cell subsets in autoimmunity. Curr Opin Immunol 1992; 4:728-732.
95. Huang FP, Niedbala W, Wei XQ, Xu D, Feng GJ, Robinson JH, et al. Nitric oxide regulates Th1 cell development through the inhibition of IL-12 synthesis by macrophages. Eur J Immunol 1998; 28:4062-4070.
96. Wei XQ, Charles IG, Smith A, Jan Ure J, Feng GJ, Huang FP et al. Altered immune responses in mice lacking inducible nitric oxide synthase. Nature 1995; 375:408-411.
97. McInnes IB, Leung B, Wei XQ, Gemmell CC, Liew FY. Septic arthritis following Staphylococcus aureus infection in mice lacking inducible nitric oxide synthase. J Immunol 1998; 160:308-315.
98. Tarrant TK, Silver PB, Wahlsten JL, Rizzo LV, Chan CC, Wiggert B, Caspi RR. Interleukin 12 protects from a T helper type 1-mediated autoimmune disease, experimental autoimmune uveitis, through a mechanism involving interferon gamma, nitric oxide, and apoptosis. J Exp Med 1999; 189:219-230.
99. Niedbala W, Wei XQ, Campbell C, Thomson D, Komai-Koma M, Liew FY. Nitric oxide preferentially induces type 1 T cell differentiation by selectively up-regulating IL-12 receptor beta 2 expression via cGMP. Proc Natl Acad Sci USA 2002; 99:16186-16191.
100. Chang RH, Feng MH, Liu WH, Lai MZ. Nitric oxide increased interleukin-4 expression in T lymphocytes. Immunology 1997; 90:364-369.
101. Okuda Y, Sakoda S, Shimaoka M, Yanagihara T. Nitric oxide induces apoptosis in mouse splenic T lymphocytes. Immunol Lett 1996; 52:135-138.
102. Bauer H, Jung T, Tsikas D, Stichtenoth DO, Frolich JC, Neumann C. Nitric oxide inhibits the secretion of T-helper 1- and T-helper 2-associated cytokines in activated human T cells. Immunology 1997; 90:205-211.
103. Eriksson U, Egermann U, Bihl MP, Gambazzi F, Tamm M, Holt PG, Bingisser RM. Human bronchial epithelium controls TH2 responses by TH1-induced, nitric oxide-mediated STAT5 dephosphorylation: Implications for the pathogenesis of asthma. J Immunol 2005; 175:2715-2720.
104. Murphy KM, Reiner SL. The lineage decisions of helper T cells. Nat Rev Immunol 2002; 2:933-944.
105. Yamashita M, Shinnakasu R, Asou H, Asou H, Kimura M, Hasegawa A, et al. Ras-ERK MAPK cascade regulates GATA3 stability and Th2 differentiation through ubiquitin-proteasome pathway. J Biol Chem 2005; 280:29409-24919.
106. Lander HM, Hajjar DP, Hempstead BL, Mirza UA, Chait BT, Campbell S, Quilliam LA. A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J Biol Chem 1997; 272:4323-4326.
107. - precursors. J Immunol 2002; 169:4183-4189.
108. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J Exp Med 2003; 198:1875-1886.
109. - T cells. J Clin Invest 2003; 112:1437-1443.
110. + T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000; 192:1213-1222.
111. Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P, et al. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 2006; 7:83-92.
112. + T cell proliferation via an IFN-γ and nitric oxide-dependent mechanism. J Immunol 2001; 167:4293-4302.
113. Sawitzki B, Kingsley CI, Oliveira V, Karim M, Herber M, Wood KJ. IFN-γ production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo. J Exp Med 2005; 201:1925-1935.
114. Wood KJ, Sawitzki B. Interferon gamma: A crucial role in the function of induced regulatory T cells in vivo. Trends Immunol 2006;27:183-187.
115. - cells with tolerogenic properties. Transplantation 2007; 83:474-484.
116. Chen C, Lee W, Zhong L, Liu C. Regulatory T cells can mediate their function through the stimulation of APCs to produce Immunosuppressive nitric oxide. J Immunol 2006; 176:3449-3460.
117. - T cells via p53, IL-2, and OX40. Proc Natl Acad Sci USA 2007; 104:15478-15483.
118. Shi YF, Bissonnette RP, Parfrey N, Szalay M, Kubo RT, Green DR. In vivo administration of monoclonal antibodies to the CD3 T cell receptor complex induces cell death (apoptosis) in immature thymocytes. J Immunol 1991; 146:3340-3346.
119. Matthys P, Froyen G, Verdot L, Huang S, Sobis H, Van Damme J, et al. IFN-gamma receptor-deficient mice are hypersensitive to the anti-CD3-induced cytokine release syndrome and thymocyte apoptosis. Protective role of endogenous nitric oxide. J Immunol 1995; 155:3823-3829.
120. Tai XG, Toyo-oka K, Yamamoto N, Yashiro Y, Mu J, Hamaoka T, Fujiwara H. Expression of an inducible type of nitric oxide (NO) synthase in the thymus and involvement of NO in deletion of TCR-stimulated double-positive thymocytes. J Immunol 1997; 158:4696-4703.
121. Aiello S, Noris M, Piccinini G, Tomasoni S, Casiraghi F, Bonazzola S, et al. Thymic dendritic cells express inducible nitric oxide synthase and generate nitric oxide in response to self- and alloantigens. J Immunol 2000; 164:4649-4658.
122. Fehsel K, Kroncke KD, Meyer KL, Huber H, Wahn V, Kolb-Bachofen V. Nitric oxide induces apoptosis in mouse thymocytes. J Immunol 1995; 155:2858-2865.
123. Tatemichi M, Tazawa H, Masuda M, Saleem M, Wada S, Donehower LA, Ohgaki H, Ohshima H. Suppression of thymic lymphomas and increased nonthymic lymphomagenesis in Trp53-deficient mice lacking inducible nitric oxide synthase gene. Int J Cancer 2004; 111:819-828.
124. Cruz MT, Carmo A, Carvalho AP, Lopes MC. Calcium-dependent nitric oxide synthase activity in rat thymocytes. Biochem Biophys Res Commun 1998; 248:98-103.
125. Moulian N, Truffault F, Gaudry-Talarmain YM, Serraf A, Berrih-Aknin S. In vivo and in vitro apoptosis of human thymocytes are associated with nitrotyrosine formation. Blood 2001; 97:3521-3530.
126. Brito C, Naviliat M, Tiscornia AC, Vuillier F, Gualco G, Dighiero G, et al. Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death. J Immunol 1999; 162:3356-3366.
127. Ten Broeke R, De Crom R, Van Haperen R, Verweij V, Leusink-Muis T, Van Ark I, et al. Overexpression of endothelial nitric oxide synthase suppresses features of allergic asthma in mice. Respir Res 2006; 7:58.
128. Lowenstein CJ, Michel T. What's in a name? eNOS and anaphylactic shock. J Clin Invest 2006; 116:2075-2078.
129. Cauwels A, Janssen B, Buys E, Sips P, Brouckaert P. Anaphylactic shock depends on PI3K and eNOS-derived NO. J Clin Invest 2006; 116:2244-2251.