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

Hobbs, 1999, Inhibition of nitric oxide synthase as a potential therapeutic target, Annu Rev Pharmacol Toxicol, 39, 191, 10.1146/annurev.pharmtox.39.1.191 Bogdan, 2001, Nitric oxide and the immune response, Nat Immunol, 2, 907, 10.1038/ni1001-907 Knowles, 1994, Nitric oxide synthases in mammals, Biochem J, 298, 249, 10.1042/bj2980249 Groves, 2000, Nitric oxide synthase: models and mechanisms, Curr Opin Chem Biol, 4, 687, 10.1016/S1367-5931(00)00146-0 Dimmeler, 1999, Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation, Nature, 399, 601, 10.1038/21224 Fulton, 1999, Regulation of endothelium-derived nitric oxide production by the protein kinase Akt, Nature, 399, 597, 10.1038/21218 Alderton, 2001, Nitric oxide synthases: Structure, function and inhibition, Biochem J, 357, 593, 10.1042/bj3570593 Hess, 2005, Protein S-nitrosylation: Purview and parameters, Nat Rev Mol Cell Biol, 6, 150, 10.1038/nrm1569 Bogdan, 2000, The role of nitric oxide in innate immunity, Immunol Rev, 173, 17, 10.1034/j.1600-065X.2000.917307.x Reiling, 1996, Nitric oxide synthase: expression of the endothelial Ca2+calmodulin-dependent isoform in human B and T lymphocytes, Eur J Immunol, 26, 511, 10.1002/eji.1830260302 Stuehr, 1991, Purification and characterization of the cytokine-induced macrophage nitric oxide synthase:An FAD- and FMN-containing flavoprotein, Proc Natl Acad Sci USA, 88, 7773, 10.1073/pnas.88.17.7773 Schneemann, 2002, Species differences in macrophage NO production are important, Nat Immunol, 3, 102, 10.1038/ni0202-102a Schonhoff, 2003, Nitrosylation of cytochrome c during apoptosis, J Biol Chem, 278, 18265, 10.1074/jbc.M212459200 Diefenbach, 1998, Type 1 interferon (IFNα/β) and type 2 nitric oxide synthase regulate the innate immune response to a protozoan parasite, Immunity, 8, 77, 10.1016/S1074-7613(00)80460-4 Diefenbach, 1999, Requirement for type 2 NO synthase for IL-12 signaling in innate immunity, Science, 284, 951, 10.1126/science.284.5416.951 Kolb, 1998, Nitric oxide in autoimmune disease: Cytotoxic or regulatory mediator?, Immunol Today, 19, 556, 10.1016/S0167-5699(98)01366-8 Niedbala, 2006, Role of nitric oxide in the regulation of T cell functions, Ann Rheum Dis, 65, iii37, 10.1136/ard.2006.058446 Mazzoni, 2002, Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism, J Immunol, 168, 689, 10.4049/jimmunol.168.2.689 Hongo, 2004, Endogenous nitric oxide protects against T cell-dependent lethality during graftversus- host disease and idiopathic pneumonia syndrome, J Immunol, 173, 1744, 10.4049/jimmunol.173.3.1744 Fiorucci, 2004, Nitric oxide regulates immune cell bioenergetic: a mechanism to understand immunomodulatory functions of nitric oxide-releasing anti-inflammatory drugs, J Immunol, 173, 874, 10.4049/jimmunol.173.2.874 Sriskandan, 1996, Bacterial superantigen-induced human lymphocyte responses are nitric oxide dependent and mediated by IL-12 and IFN-γ, J Immunol, 156, 2430, 10.4049/jimmunol.156.7.2430 Suschek, 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, 10.2174/1566524043359908 Guzik, 2003, Nitric oxide and superoxide in inflammation and immune regulation, J Physiol Pharmacol, 54, 469 Thippeswamy, 2006, Nitric oxide, a biological double-faced janus--Is this good or bad?, Histol Histopathol, 21, 445 Bronte, 2003, L-arginine metabolism in myeloid cells controls T-lymphocyte functions, Trends Immunol, 24, 302, 10.1016/S1471-4906(03)00132-7 Florquin, 1994, The protective role of endogenously synthesized nitric oxide in staphylococcal enterotoxin B-induced shock in mice, J Exp Med, 180, 1153, 10.1084/jem.180.3.1153 Zech, 2003, Nitric oxide donors inhibit formation of the Apaf-1/caspase-9 apoptosome and activation of caspases, Biochem J, 371, 1055, 10.1042/bj20021720 Bogdan, 2001, Nitric oxide and the regulation of gene expression, Trends Cell Biol, 11, 66, 10.1016/S0962-8924(00)01900-0 Pfeilschifter, 2001, Regulation of gene expression by nitric oxide, Pflugers Arch, 442, 479, 10.1007/s004240100586 Michel, 1997, Nitric oxide synthases: which, where, how, and why?, J Clin Invest, 100, 2146, 10.1172/JCI119750 Renno, 1995, Proliferation is a prerequisite for bacterial superantigen-induced T cell apoptosis in vivo, J Exp Med, 181, 2283, 10.1084/jem.181.6.2283 McKay, 1999, Nitric oxide participates in the recovery of normal jejunal epithelial ion transport following exposure to the superantigen Staphylococcus aureus enterotoxin B, J Immunol, 163, 4519, 10.4049/jimmunol.163.8.4519 Rachlis, 2002, Nitric oxide reduces bacterial superantigen-immune cell activation and consequent epithelial abnormalities, J Leukoc Biol, 72, 339, 10.1189/jlb.72.2.339 Bronte, 2005, Regulation of immune responses by Larginine metabolism, Nat Rev Immunol, 5, 641, 10.1038/nri1668 Rodriguez, 2002, Regulation of T cell receptor CD3zeta chain expression by Larginine, J Biol Chem, 277, 21123, 10.1074/jbc.M110675200 Bingisser, 1998, Macrophage-derived nitric oxide regulates T cell activation via reversible disruption of the Jak3/STAT5 signaling pathway, J Immunol, 160, 5729, 10.4049/jimmunol.160.12.5729 Boldin, 1996, Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO- 1- and TNF receptor-induced cell death, Cell, 85, 803, 10.1016/S0092-8674(00)81265-9 Li, 2002, Nitric oxide-induced genotoxicity, mitochondrial damage, and apoptosis in human lymphoblastoid cells expressing wild-type and mutant p53, Proc Natl Acad Sci USA, 99, 10364, 10.1073/pnas.162356399 Gordon, 2001, Nitric oxide induces murine thymocyte apoptosis by oxidative injury and a p53-dependent mechanism, J Leukoc Biol, 70, 87, 10.1189/jlb.70.1.87 Hara, 2005, S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding, Nat Cell Biol, 7, 665, 10.1038/ncb1268 Bosca, 2005, Nitric oxide and cell viability in inflammatory cells: A role for NO in macrophage function and fate, Toxicology, 208, 249, 10.1016/j.tox.2004.11.035 Liu, 1999, NO: An inhibitor of cell death, Cell Death Differ, 6, 937, 10.1038/sj.cdd.4400578 Dimmeler, 1998, Nitric oxide inhibits APO-1/Fas-mediated cell death, Cell Growth Differ, 9, 415 Bonfoco, 1995, 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, 92, 7162, 10.1073/pnas.92.16.7162 Mannick, 1999, Fas-induced caspase denitrosylation, Science, 284, 651, 10.1126/science.284.5414.651 Melino, 2000, Nitric oxide inhibits apoptosis via AP-1-dependent CD95L transactivation, Cancer Res, 60, 2377 Brune, 1999, Nitric oxide (NO): An effector of apoptosis, Cell Death Differ, 6, 969, 10.1038/sj.cdd.4400582 Matsumoto, 2003, Screening for nitric oxide-dependent protein-protein interactions, Science, 301, 657, 10.1126/science.1079319 Genaro, 1995, lymphocyte programmed cell death is prevented by nitric oxide release through mechanisms involving sustained Bcl-2 levels, J Clin Invest, 95, 1884, 10.1172/JCI117869 Sciorati, 1997, Autocrine nitric oxide modulates CD95-induced apoptosis in gammadelta T lymphocytes, J Biol Chem, 272, 23211, 10.1074/jbc.272.37.23211 Park, 2004, Inhibition of apoptosis signal-regulating kinase 1 by nitric oxide through a thiol redox mechanism, J Biol Chem, 279, 7584, 10.1074/jbc.M304183200 Leist, 1999, Nitric oxide inhibits execution of apoptosis at two distinct ATPdependent steps upstream and downstream of mitochondrial cytochrome c release, Biochem Biophys Res Commun, 258, 215, 10.1006/bbrc.1999.0491 Erusalimsky, 2007, Nitric oxide and mitochondrial signaling: from physiology to pathophysiology, Arterioscler Thromb Vasc Biol, 27, 2524, 10.1161/ATVBAHA.107.151167 Leist, 1999, Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis, Exp Cell Res, 249, 396, 10.1006/excr.1999.4514 Moncada, 2002, Does nitric oxide modulate mitochondrial energy generation and apoptosis?, Nat Rev Mol Cell Biol, 3, 214, 10.1038/nrm762 Mannick, 2004, NO means no and yes: Regulation of cell signaling by protein nitrosylation, Free Radic Res, 38, 1, 10.1080/10715760310001629065 Beckman, 1996, Nitric oxide, superoxide, and peroxynitrite: The good, the bad, and ugly, Am J Physiol, 271, C1424, 10.1152/ajpcell.1996.271.5.C1424 Szabo, 1996, DNA strand breakage and activation of poly-ADP ribosyltransferase: A cytotoxic pathway triggered by peroxynitrite, Free Radic Biol Med, 21, 855, 10.1016/0891-5849(96)00170-0 Schindler, 2001, NO as a signaling molecule: Effects on kinases, Int Immunopharmacol, 1, 1443, 10.1016/S1567-5769(01)00089-3 Reynaert, 2004, Nitric oxide represses inhibitory κB kinase through Snitrosylation, Proc Natl Acad Sci USA, 101, 8945, 10.1073/pnas.0400588101 Marshall, 2002, Nitrosative stress-induced apoptosis through inhibition of NF-κB, J Biol Chem, 277, 34223, 10.1074/jbc.M201638200 Lander, 1995, Novogrodsky A. p21ras as a common signaling target of reactive free radicals and cellular redox stress, J Biol Chem, 270, 21195, 10.1074/jbc.270.36.21195 De Martin, 2000, The transcription factor NF-kB and the regulation of vascular cell function, Arterioscler Thromb Vasc Biol, 20, E83 Hickey, 1997, Role of nitric oxide in regulation of leucocyteendothelial cell interactions, Exp Physiol, 82, 339, 10.1113/expphysiol.1997.sp004029 Hickey, 2001, Inducible nitric oxide synthase (iNOS) and regulation of leucocyte/endothelial cell interactions: studies in iNOS-deficient mice, Acta Physiol Scand, 173, 119, 10.1046/j.1365-201X.2001.00892.x Nikitovic, 1998, Inhibition of AP-1 DNA binding by nitric oxide involving conserved cysteine residues in Jun and Fos, Biochem Biophys Res Commun, 242, 109, 10.1006/bbrc.1997.7930 Klatt, 1999, Nitric oxide inhibits c-Jun DNA binding by specifically targeted S-glutathionylation, J Biol Chem, 274, 15857, 10.1074/jbc.274.22.15857 Zouki, 2001, Peroxynitrite mediates cytokine-induced IL-8 gene expression and production by human leukocytes, J Leukoc Biol, 69, 815, 10.1189/jlb.69.5.815 Chu, 1998, 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, 248, 871, 10.1006/bbrc.1998.9062 Connelly, 2005, 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, 280, 10040, 10.1074/jbc.M411991200 Blesson, 2002, Analysis of the mechanisms of human cytotoxic T lymphocyte response inhibition by NO, Int Immunol, 14, 1169, 10.1093/intimm/dxf081 Fiedler, 2002, Inhibition of calcineurin-NFAT hypertrophy signaling by cGMP-dependent protein kinase type I in cardiac myocytes, Proc Natl Acad Sci USA, 99, 11363, 10.1073/pnas.162100799 Mannick, 1994, Nitric oxide produced by human B lymphocytes inhibits apoptosis and Epstein- Barr virus reactivation, Cell, 79, 1137, 10.1016/0092-8674(94)90005-1 Beltran, 2002, Inhibition of mitochondrial respiration by endogenous nitric oxide: a critical step in Fas signaling, Proc Natl Acad Sci USA, 99, 8892, 10.1073/pnas.092259799 Cherla, 2001, Stromal cell-derived factor 1 α-induced chemotaxis in T cells is mediated by nitric oxide signaling pathways, J Immunol, 166, 3067, 10.4049/jimmunol.166.5.3067 Vig, 2004, Inducible nitric oxide synthase in T cells regulates T cell death and immune memory, J Clin Invest, 113, 1734, 10.1172/JCI20225 Taylor-Robinson, 1994, Regulation of the immune response by nitric oxide differentially produced by T helper type 1 and T helper type 2 cells, Eur J Immunol, 24, 980, 10.1002/eji.1830240430 Barreiro Arcos, 2006, Thyroid hormones increase inducible nitric oxide synthase gene expression downstream from PKC-ξin murine tumor T lymphocytes, Am J Physiol Cell Physiol, 291, C327, 10.1152/ajpcell.00316.2005 Mori, 1999, 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, 94, 2862, 10.1182/blood.V94.8.2862.420k24_2862_2870 Jimenez, 2001, Regulation of human immunodeficiency virus type 1 replication in human T lymphocytes by nitric oxide, J Virol, 75, 4655, 10.1128/JVI.75.10.4655-4663.2001 Koh, 2004, T cell-mediated vascular dysfunction of human allografts results from IFN-γdysregulation of NO synthase, J Clin Invest, 114, 846, 10.1172/JCI21767 Choy, 2007, Induction of inducible NO synthase in bystander human T cells increases allogeneic responses in the vasculature, Proc Natl Acad Sci USA, 104, 1313, 10.1073/pnas.0607731104 Esaki, 1997, Expression of inducible nitric oxide synthase in T lymphocytes and macrophages of cholesterol-fed rabbits, Atherosclerosis, 128, 39, 10.1016/S0021-9150(96)05976-X Bustamante, 2002, Sequential NO production by mitochondria and endoplasmic reticulum during induced apoptosis, Nitric Oxide, 6, 333, 10.1006/niox.2001.0420 Ibiza, 2006, Endothelial nitric oxide synthase regulates T cell receptor signaling at the immunological synapse, Immunity, 24, 753, 10.1016/j.immuni.2006.04.006 Nagy, 2003, T cell activation-induced mitochondrial. hyperpolarization is mediated by Ca2- and redox-dependent. production of nitric oxide, J Immunol, 171, 5188, 10.4049/jimmunol.171.10.5188 Nagy, 2004, Nitric oxidedependent mitochondrial biogenesis generates Ca2+ signaling profile of lupus T cells, J Immunol, 173, 3676, 10.4049/jimmunol.173.6.3676 Averna, 2007, Proteolytic degradation of nitric oxide synthase isoforms by calpain is modulated by the expression levels of HSP90, Febs J, 274, 6116, 10.1111/j.1742-4658.2007.06133.x Williams, 1998, Nitric oxide synthase plays a signaling role in TCR-triggered apoptotic death, J Immunol, 161, 6526, 10.4049/jimmunol.161.12.6526 Koncz, 2007, Nitric oxide mediates T cell cytokine production and signal transduction in histidine decarboxylase knockout mice, J Immunol, 179, 6613, 10.4049/jimmunol.179.10.6613 Horvath, 1999, 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, 70, 95, 10.1016/S0165-2478(99)00126-1 Haddad, 2003, 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, 198, 369, 10.1084/jem.20020691 Norman, 2008, Interferon-γlimits Th1 lymphocyte adhesion to inflamed endothelium: A. nitric oxide regulatory feedback mechanism, Eur J Immunol, 38, 1368, 10.1002/eji.200737847 Mason, 1992, T-cell subsets in autoimmunity, Curr Opin Immunol, 4, 728, 10.1016/0952-7915(92)90053-H Huang, 1998, Nitric oxide regulates Th1 cell development through the inhibition of IL-12 synthesis by macrophages, Eur J Immunol, 28, 4062, 10.1002/(SICI)1521-4141(199812)28:12<4062::AID-IMMU4062>3.0.CO;2-K Wei, 1995, Altered immune responses in mice lacking inducible nitric oxide synthase, Nature, 375, 408, 10.1038/375408a0 McInnes, 1998, Septic arthritis following Staphylococcus aureus infection in mice lacking inducible nitric oxide synthase, J Immunol, 160, 308, 10.4049/jimmunol.160.1.308 Tarrant, 1999, 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, 189, 219, 10.1084/jem.189.2.219 Niedbala, 2002, 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, 99, 16186, 10.1073/pnas.252464599 Chang, 1997, Nitric oxide increased interleukin-4 expression in T lymphocytes, Immunology, 90, 364, 10.1111/j.1365-2567.1997.00364.x Okuda, 1996, Nitric oxide induces apoptosis in mouse splenic T lymphocytes, Immunol Lett, 52, 135, 10.1016/0165-2478(96)02597-7 Bauer, 1997, Nitric oxide inhibits the secretion of T-helper 1- and T-helper 2-associated cytokines in activated human T cells, Immunology, 90, 205, 10.1046/j.1365-2567.1997.00161.x Eriksson, 2005, Human bronchial epithelium controls TH2 responses by TH1-induced, nitric oxide-mediated STAT5 dephosphorylation: Implications for the pathogenesis of asthma, J Immunol, 175, 2715, 10.4049/jimmunol.175.4.2715 Murphy, 2002, The lineage decisions of helper T cells, Nat Rev Immunol, 2, 933, 10.1038/nri954 Yamashita, 2005, Ras-ERK MAPK cascade regulates GATA3 stability and Th2 differentiation through ubiquitin-proteasome pathway, J Biol Chem, 280, 24919, 10.1074/jbc.M502333200 Lander, 1997, A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction, J Biol Chem, 272, 4323, 10.1074/jbc.272.7.4323 Zheng, 2002, Generation ex vivo of TGF-®-producing regulatory T cells from CD4+CD25– precursors, J Immunol, 169, 4183, 10.4049/jimmunol.169.8.4183 Chen, 2003, Conversion of peripheral CD4+CD25– naive T cells to CD4+CD25+ regulatory T cells by TGF-®induction of transcription factor Foxp3, J Exp Med, 198, 1875, 10.1084/jem.20030152 Walker, 2003, Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25–T cells, J Clin Invest, 112, 1437, 10.1172/JCI19441 Jonuleit, 2000, Induction of interleukin 10-producing, nonproliferating CD4+T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells, J Exp Med, 192, 1213, 10.1084/jem.192.9.1213 Tang, 2006, Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice, Nat Immunol, 7, 83, 10.1038/ni1289 Atochina, 2001, A schistosome-expressed immunomodulatory glycoconjugate expands peritoneal Gr1+macrophages that suppress naive CD4+T cell proliferation via an IFN-γand nitric oxide-dependent mechanism, J Immunol, 167, 4293, 10.4049/jimmunol.167.8.4293 Sawitzki, 2005, IFN-γproduction by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo, J Exp Med, 201, 1925, 10.1084/jem.20050419 Wood, 2006, Interferon gamma: A crucial role in the function of induced regulatory T cells in vivo, Trends Immunol, 27, 183, 10.1016/j.it.2006.02.008 Aiello, 2007, DnIKK2-transfected dendritic cells induce a novel population of inducible nitric oxide synthase-expressing CD4CD25–cells with tolerogenic properties, Transplantation, 83, 474, 10.1097/01.tp.0000251808.91901.c3 Chen, 2006, Regulatory T cells can mediate their function through the stimulation of APCs to produce Immunosuppressive nitric oxide, J Immunol, 176, 3449, 10.4049/jimmunol.176.6.3449 Niedbala, 2007, Nitric oxide induces CD4+CD25+ Foxp3 regulatory T cells from CD4+CD25–T cells via p53 IL-2, and OX40, Proc Natl Acad Sci USA, 104, 15478, 10.1073/pnas.0703725104 Shi, 1991, In vivo administration of monoclonal antibodies to the CD3 T cell receptor complex induces cell death (apoptosis) in immature thymocytes, J Immunol, 146, 3340, 10.4049/jimmunol.146.10.3340 Matthys, 1995, 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, 155, 3823, 10.4049/jimmunol.155.8.3823 Tai, 1997, 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, 158, 4696, 10.4049/jimmunol.158.10.4696 Aiello, 2000, Thymic dendritic cells express inducible nitric oxide synthase and generate nitric oxide in response to self- and alloantigens, J Immunol, 164, 4649, 10.4049/jimmunol.164.9.4649 Fehsel, 1995, Nitric oxide induces apoptosis in mouse thymocytes, J Immunol, 155, 2858, 10.4049/jimmunol.155.6.2858 Tatemichi, 2004, Suppression of thymic lymphomas and increased nonthymic lymphomagenesis in Trp53-deficient mice lacking inducible nitric oxide synthase gene, Int J Cancer, 111, 819, 10.1002/ijc.20350 Cruz, 1998, Calcium-dependent nitric oxide synthase activity in rat thymocytes, Biochem Biophys Res Commun, 248, 98, 10.1006/bbrc.1998.8865 Moulian, 2001, In vivo and in vitro apoptosis of human thymocytes are associated with nitrotyrosine formation, Blood, 97, 3521, 10.1182/blood.V97.11.3521 Brito, 1999, Peroxynitrite inhibits T lymphocyte activation and proliferation by promoting impairment of tyrosine phosphorylation and peroxynitrite-driven apoptotic death, J Immunol, 162, 3356, 10.4049/jimmunol.162.6.3356 Ten Broeke, 2006, Overexpression of endothelial nitric oxide synthase suppresses features of allergic asthma in mice, Respir Res, 7, 58, 10.1186/1465-9921-7-58 Lowenstein, 2006, What's in a name?. eNOS and anaphylactic shock, J Clin Invest, 116, 2075, 10.1172/JCI29406 Cauwels, 2006, Anaphylactic shock depends on PI3K and eNOS-derived NO, J Clin Invest, 116, 2244, 10.1172/JCI25426