Biopolym. Cell. 2015; 31(6):405-416.
http://dx.doi.org/10.7124/bc.0008FD
Reviews
Nitrosative events in atopic asthma pathogenesis
1Parilova O. O., 1Volodina T. T., 1Shandrenko S. G.
  1. Palladin Institute of Biochemistry, NAS of Ukraine
    9, Leontovycha Str., Kyiv, Ukraine, 01601

Abstract

The correlation between high exhaled nitric oxide levels and eosinophilic-mediated airway inflammation in patients with atopic asthma has been well documented. This generates prerequisites that a regulatory feedback mechanism exists between them. Therefore, the paper briefly describes evidence implementing biosynthesis, enzyme structural features, expression regulation of its isoforms and effects of nitric oxide, which have helped elucidate molecular mechanisms by which nitric oxide selectively promotes asthma exacerbation. In previous study we have demonstrated that airway infiltrate of immune cells contributes to NO synthesis in the respiratory tract during allergic inflammation under guinea pig model of acute asthma with multiple challenges. On the basis of these findings the authors posits that nitric oxide represents an additional signal of the induction of Th2 subset response and be considerably involved in the complex network of immune regulation distinctive for atopic asthma phenotype.
Keywords: nitric oxide, atopic asthma, nitric oxide synthases, allergic airway inflammation, eosinophilia
Full text: (PDF, in English)

References

[1] Busse WW, Lemanske RF Jr. Asthma. N Engl J Med. 2001;344(5):350-62.
[2] Schröder NW, Maurer M. The role of innate immunity in asthma: leads and lessons from mouse models. Allergy. 2007;62(6):579-90.
[3] Gaston B. The biochemistry of asthma. Biochim Biophys Acta. 2011;1810(11):1017-24.
[4] Asher MI, Montefort S, Björkstén B, Lai CK, Strachan DP, Weiland SK, Williams H; ISAAC Phase Three Study Group. Worldwide time trends in the prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and eczema in childhood: ISAAC Phases One and Three repeat multicountry cross-sectional surveys. Lancet. 2006;368(9537):733-43.
[5] Illi S, von Mutius E, Lau S, Niggemann B, Grüber C, Wahn U; Multicentre Allergy Study (MAS) group. Perennial allergen sensitisation early in life and chronic asthma in children: a birth cohort study. Lancet. 2006;368(9537):763-70.
[6] Ducharme FM. Inhaled corticosteroids versus leukotriene antagonists as first-line therapy for asthma: a systematic review of current evidence. Treat Respir Med. 2004;3(6):399-405.
[7] Colucci R, Fornai M, Tuccori M, Antonioli L, Pasqualetti G, Blandizzi C, Del Tacca M. Tolerability profiles of leukotriene receptor antagonists and long-acting beta2-adrenoceptor agonists in combination with inhaled corticosteroids for treatment of asthma: a review. J Asthma. 2007;44(6):411-22.
[8] Shorter JH, Nelson DD, McManus JB, Zahniser MS, Sama S, Milton DK. Clinical study of multiple breath biomarkers of asthma and COPD (NO, CO2, CO and N2O) by infrared laser spectroscopy. J Breath Res. 2011;5(3):037108.
[9] Moncada S, Higgs A. The L-arginine-nitric oxide pathway. N Engl J Med. 1993;329(27):2002-12.
[10] Ghosh S, Erzurum SC. Nitric oxide metabolism in asthma pathophysiology. Biochim Biophys Acta. 2011;1810(11):1008-16.
[11] Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. Nitric oxide in health and disease of the respiratory system. Physiol Rev. 2004;84(3):731-65.
[12] Dweik RA, Boggs PB, Erzurum SC, Irvin CG, Leigh MW, Lundberg JO, Olin AC, Plummer AL, Taylor DR; American Thoracic Society Committee on Interpretation of Exhaled Nitric Oxide Levels (FENO) for Clinical Applications. An official ATS clinical practice guideline: interpretation of exhaled nitric oxide levels (FENO) for clinical applications. Am J Respir Crit Care Med. 2011;184(5):602-15.
[13] American Thoracic Society; European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med. 2005;171(8):912-30.
[14] Saleh D, Ernst P, Lim S, Barnes PJ, Giaid A. Increased formation of the potent oxidant peroxynitrite in the airways of asthmatic patients is associated with induction of nitric oxide synthase: effect of inhaled glucocorticoid. FASEB J. 1998;12(11):929-37.
[15] 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 U S A. 1991;88(17):7773-7.
[16] Lyons CR, Orloff GJ, Cunningham JM. Molecular cloning and functional expression of an inducible nitric oxide synthase from a murine macrophage cell line. J Biol Chem. 1992;267(9):6370-4.
[17] Xie QW, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Ding A, Troso T, Nathan C. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science. 1992;256(5054):225-8.
[18] Nunokawa Y, Ishida N, Tanaka S. Cloning of inducible nitric oxide synthase in rat vascular smooth muscle cells. Biochem Biophys Res Commun. 1993;191(1):89-94.
[19] Warner RL, Paine R 3rd, Christensen PJ, Marletta MA, Richards MK, Wilcoxen SE, Ward PA. Lung sources and cytokine requirements for in vivo expression of inducible nitric oxide synthase. Am J Respir Cell Mol Biol. 1995;12(6):649–61.
[20] Yates DH. Role of exhaled nitric oxide in asthma. Immunol Cell Biol. 2001;79(2):178-90.
[21] Bogdan C. Nitric oxide and the immune response. Nat Immunol. 2001;2(10):907-16.
[22] Clancy RM, Abramson SB. Nitric oxide: a novel mediator of inflammation. Proc Soc Exp Biol Med. 1995;210(2):93-101.
[23] Uetani K, Thomassen MJ, Erzurum SC. Nitric oxide synthase 2 through an autocrine loop via respiratory epithelial cell-derived mediator. Am J Physiol Lung Cell Mol Physiol. 2001;280(6):L1179-88.
[24] Fujii Y, Magder S, Cernacek P, Goldberg P, Guo Y, Hussain SN. Endothelin receptor blockade attenuates lipopolysaccharide-induced pulmonary nitric oxide production. Am J Respir Crit Care Med. 2000;161(3 Pt 1):982-9.
[25] Wang HH, Hsieh HL, Yang CM. Nitric oxide production by endothelin-1 enhances astrocytic migration via the tyrosine nitration of matrix metalloproteinase-9. J Cell Physiol. 2011;226(9):2244-56.
[26] Alderton WK, Cooper CE, Knowles RG. Nitric oxide synthases: structure, function and inhibition. Biochem J. 2001;357(Pt 3):593-615.
[27] Barnes PJ, Dweik RA, Gelb AF, Gibson PG, George SC, Grasemann H, Pavord ID, Ratjen F, Silkoff PE, Taylor DR, Zamel N. Exhaled nitric oxide in pulmonary diseases: a comprehensive review. Chest. 2010;138(3):682-92.
[28] Gaston B, Drazen JM, Loscalzo J, Stamler JS. The biology of nitrogen oxides in the airways. Am J Respir Crit Care Med. 1994;149(2 Pt 1):538-51.
[29] Pechkovsky DV, Zissel G, Goldmann T, Einhaus M, Taube C, Magnussen H, Schlaak M, Müller-Quernheim J. Pattern of NOS2 and NOS3 mRNA expression in human A549 cells and primary cultured AEC II. Am J Physiol Lung Cell Mol Physiol. 2002;282(4):L684-92.
[30] Hollá LI, Bucková D, Kuhrová V, Stejskalová A, Francová H, Znojil V, Vácha J. Prevalence of endothelial nitric oxide synthase gene polymorphisms in patients with atopic asthma. Clin Exp Allergy. 2002;32(8):1193-8.
[31] Maarsingh H, Leusink J, Bos IS, Zaagsma J, Meurs H. Arginase strongly impairs neuronal nitric oxide-mediated airway smooth muscle relaxation in allergic asthma. Respir Res. 2006;7:6.
[32] Zuo L, Koozechian MS, Chen LL. Characterization of reactive nitrogen species in allergic asthma. Ann Allergy Asthma Immunol. 2014;112(1):18-22.
[33] Hecker M, Cattaruzza M, Wagner AH. Regulation of inducible nitric oxide synthase gene expression in vascular smooth muscle cells. Gen Pharmacol. 1999;32(1):9-16.
[34] Romanska HM, Polak JM, Coleman RA, James RS, Harmer DW, Allen JC, Bishop AE. iNOS gene upregulation is associated with the early proliferative response of human lung fibroblasts to cytokine stimulation. J Pathol. 2002;197(3):372-9.
[35] Ermert M, Ruppert C, Günther A, Duncker HR, Seeger W, Ermert L. Cell-specific nitric oxide synthase-isoenzyme expression and regulation in response to endotoxin in intact rat lungs. Lab Invest. 2002;82(4):425-41.
[36] Panaro MA, Brandonisio O, Acquafredda A, Sisto M, Mitolo V. Evidences for iNOS expression and nitric oxide production in the human macrophages. Curr Drug Targets Immune Endocr Metabol Disord. 2003;3(3):210-21.
[37] Prado CM, Leick-Maldonado EA, Yano L, Leme AS, Capelozzi VL, Martins MA, Tibério IF. Effects of nitric oxide synthases in chronic allergic airway inflammation and remodeling. Am J Respir Cell Mol Biol. 2006;35(4):457-65.
[38] del Pozo V, de Arruda-Chaves E, de Andrés B, Cárdaba B, López-Farré A, Gallardo S, Cortegano I, Vidarte L, Jurado A, Sastre J, Palomino P, Lahoz C. Eosinophils transcribe and translate messenger RNA for inducible nitric oxide synthase. J Immunol. 1997;158(2):859-64.
[39] Evans TJ, Buttery LD, Carpenter A, Springall DR, Polak JM, Cohen J. Cytokine-treated human neutrophils contain inducible nitric oxide synthase that produces nitration of ingested bacteria. Proc Natl Acad Sci U S A. 1996;93(18):9553-8.
[40] Webb JL, Polak JM, Evans TJ. Effect of adhesion on inducible nitric oxide synthase (iNOS) production in purified human neutrophils. Clin Exp Immunol. 2001;123(1):42-8.
[41] Lu L, Bonham CA, Chambers FG, Watkins SC, Hoffman RA, Simmons RL, Thomson AW. 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. 1996;157(8):3577-86.
[42] McCauley SD, Gilchrist M, Befus AD. Nitric oxide: a major determinant of mast cell phenotype and function. Mem Inst Oswaldo Cruz. 2005;100 Suppl 1:11-4.
[43] Gilchrist M, McCauley SD, Befus AD. Expression, localization, and regulation of NOS in human mast cell lines: effects on leukotriene production. Blood. 2004;104(2):462-9.
[44] Bidri M, Ktorza S, Vouldoukis I, Le Goff L, Debré P, Guillosson JJ, Arock M. Nitric oxide pathway is induced by Fc epsilon RI and up-regulated by stem cell factor in mouse mast cells. Eur J Immunol. 1997;27(11):2907-13.
[45] Inoue T, Suzuki Y, Yoshimaru T, Ra C. Nitric oxide protects mast cells from activation-induced cell death: the role of the phosphatidylinositol-3 kinase-Akt-endothelial nitric oxide synthase pathway. J Leukoc Biol. 2008;83(5):1218-29.
[46] Gilchrist M, Savoie M, Nohara O, Wills FL, Wallace JL, Befus AD. Nitric oxide synthase and nitric oxide production in vivo-derived mast cells. J Leukoc Biol. 2002;71(4):618-24.
[47] Lin TJ, Hirji N, Nohara O, Stenton GR, Gilchrist M, Befus AD. Mast cells express novel CD8 molecules that selectively modulate mediator secretion. J Immunol. 1998;161(11):6265-72.
[48] Suzuki Y, Inoue T, Ra C. Endothelial nitric oxide synthase is essential for nitric oxide generation, L-type Ca2+ channel activation and survival in RBL-2H3 mast cells. Biochim Biophys Acta. 2010;1803(3):372-85.
[49] Furuke K, Burd PR, Horvath-Arcidiacono JA, Hori K, Mostowski H, Bloom ET. Human NK cells express endothelial nitric oxide synthase, and nitric oxide protects them from activation-induced cell death by regulating expression of TNF-alpha. J Immunol. 1999;163(3):1473-80.
[50] Lancaster JR Jr. Nitroxidative, nitrosative, and nitrative stress: kinetic predictions of reactive nitrogen species chemistry under biological conditions. Chem Res Toxicol. 2006;19(9):1160-74.
[51] Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol. 2005;6(2):150-66.
[52] Martínez MC, Andriantsitohaina R. Reactive nitrogen species: molecular mechanisms and potential significance in health and disease. Antioxid Redox Signal. 2009;11(3):669-702.
[53] Alving K, Weitzberg E, Lundberg JM. Increased amount of nitric oxide in exhaled air of asthmatics. Eur Respir J. 1993;6(9):1368-70.
[54] Kharitonov SA, Yates D, Robbins RA, Logan-Sinclair R, Shinebourne EA, Barnes PJ. Increased nitric oxide in exhaled air of asthmatic patients. Lancet. 1994;343(8890):133-5.
[55] Massaro AF, Gaston B, Kita D, Fanta C, Stamler JS, Drazen JM. Expired nitric oxide levels during treatment of acute asthma. Am J Respir Crit Care Med. 1995;152(2):800-3.
[56] Yates DH, Kharitonov SA, Robbins RA, Thomas PS, Barnes PJ. Effect of a nitric oxide synthase inhibitor and a glucocorticosteroid on exhaled nitric oxide. Am J Respir Crit Care Med. 1995;152(3):892-6.
[57] Hamid Q, Springall DR, Riveros-Moreno V, Chanez P, Howarth P, Redington A, Bousquet J, Godard P, Holgate S, Polak JM. Induction of nitric oxide synthase in asthma. Lancet. 1993 Dec 18-25;342(8886-8887):1510-3.
[58] Guo FH, Comhair SA, Zheng S, Dweik RA, Eissa NT, Thomassen MJ, Calhoun W, Erzurum SC. Molecular mechanisms of increased nitric oxide (NO) in asthma: evidence for transcriptional and post-translational regulation of NO synthesis. J Immunol. 2000;164(11):5970-80.
[59] De Sanctis GT, MacLean JA, Hamada K, Mehta S, Scott JA, Jiao A, Yandava CN, Kobzik L, Wolyniec WW, Fabian AJ, Venugopal CS, Grasemann H, Huang PL, Drazen JM. Contribution of nitric oxide synthases 1, 2, and 3 to airway hyperresponsiveness and inflammation in a murine model of asthma. J Exp Med. 1999;189(10):1621-30.
[60] Feder LS, Stelts D, Chapman RW, Manfra D, Crawley Y, Jones H, Minnicozzi M, Fernandez X, Paster T, Egan RW, Kreutner W, Kung TT. Role of nitric oxide on eosinophilic lung inflammation in allergic mice. Am J Respir Cell Mol Biol. 1997;17(4):436-42.
[61] Xiong Y, Karupiah G, Hogan SP, Foster PS, Ramsay AJ. Inhibition of allergic airway inflammation in mice lacking nitric oxide synthase 2. J Immunol. 1999;162(1):445-52.
[62] Popov TA. Human exhaled breath analysis. Ann Allergy Asthma Immunol. 2011;106(6):451-6.
[63] Jatakanon A, Lim S, Kharitonov SA, Chung KF, Barnes PJ. Correlation between exhaled nitric oxide, sputum eosinophils, and methacholine responsiveness in patients with mild asthma. Thorax. 1998;53(2):91-5.
[64] Mattes J, Storm van’s Gravesande K, Reining U, Alving K, Ihorst G, Henschen M, Kuehr J. NO in exhaled air is correlated with markers of eosinophilic airway inflammation in corticosteroid-dependent childhood asthma. Eur Respir J. 1999;13(6):1391–5.
[65] Piacentini GL, Bodini A, Costella S, Vicentini L, Mazzi P, Sperandio S, Boner AL. Exhaled nitric oxide and sputum eosinophil markers of inflammation in asthmatic children. Eur Respir J. 1999;13(6):1386-90.
[66] Donohue JF, Jain N. Exhaled nitric oxide to predict corticosteroid responsiveness and reduce asthma exacerbation rates. Respir Med. 2013;107(7):943-52.
[67] Haldar P, Brightling CE, Hargadon B, Gupta S, Monteiro W, Sousa A, Marshall RP, Bradding P, Green RH, Wardlaw AJ, Pavord ID. Mepolizumab and exacerbations of refractory eosinophilic asthma. N Engl J Med. 2009;360(10):973-84.
[68] Corren J, Lemanske RF, Hanania NA, Korenblat PE, Parsey MV, Arron JR, Harris JM, Scheerens H, Wu LC, Su Z, Mosesova S, Eisner MD, Bohen SP, Matthews JG. Lebrikizumab treatment in adults with asthma. N Engl J Med. 2011;365(12):1088-98.
[69] Warke TJ, Fitch PS, Brown V, Taylor R, Lyons JD, Ennis M, Shields MD. Exhaled nitric oxide correlates with airway eosinophils in childhood asthma. Thorax. 2002;57(5):383-7.
[70] Bousquet J, Chanez P, Lacoste JY, Barnéon G, Ghavanian N, Enander I, Venge P, Ahlstedt S, Simony-Lafontaine J, Godard P, et al. Eosinophilic inflammation in asthma. N Engl J Med. 1990;323(15):1033-9.
[71] Meurs H, Maarsingh H, Zaagsma J. Arginase and asthma: novel insights into nitric oxide homeostasis and airway hyperresponsiveness. Trends Pharmacol Sci. 2003;24(9):450-5.
[72] Yeadon M, Price R. Induction of calcium-independent nitric oxide synthase by allergen challenge in sensitized rat lung in vivo. Br J Pharmacol. 1995;116(6):2545-6.
[73] Parilova OO, Shandrenko SG. Interconnection between nitric oxide formation and hypersensitivity parameters under guinea pig model of acute asthma with multiple challenges. Ukr Biochem J. 2015;87(5):113–23.
[74] Trifilieff A, Fujitani Y, Mentz F, Dugas B, Fuentes M, Bertrand C. Inducible nitric oxide synthase inhibitors suppress airway inflammation in mice through down-regulation of chemokine expression. J Immunol. 2000;165(3):1526-33.
[75] Pautz A, Art J, Hahn S, Nowag S, Voss C, Kleinert H. Regulation of the expression of inducible nitric oxide synthase. Nitric Oxide. 2010;23(2):75-93.
[76] Alving K, Malinovschi A. Basic aspects of exhaled nitric oxide. European Respiratory Monograph. Plymouth, UK, Latimer Trend & So Ltd, European Respiratory Society; 2010; 69:1–31.
[77] Chibana K, Trudeau JB, Mustovich AT, Hu H, Zhao J, Balzar S, Chu HW, Wenzel SE. IL-13 induced increases in nitrite levels are primarily driven by increases in inducible nitric oxide synthase as compared with effects on arginases in human primary bronchial epithelial cells. Clin Exp Allergy. 2008;38(6):936-46.
[78] Bove PF, van der Vliet A. Nitric oxide and reactive nitrogen species in airway epithelial signaling and inflammation. Free Radic Biol Med. 2006;41(4):515-27.
[79] Mgbemena V, Segovia JA, Chang TH, Tsai SY, Cole GT, Hung CY, Bose S. Transactivation of inducible nitric oxide synthase gene by Kruppel-like factor 6 regulates apoptosis during influenza A virus infection. J Immunol. 2012;189(2):606-15.
[80] Ilmarinen-Salo P, Moilanen E, Kinnula VL, Kankaanranta H. Nitric oxide-induced eosinophil apoptosis is dependent on mitochondrial permeability transition (mPT), JNK and oxidative stress: apoptosis is preceded but not mediated by early mPT-dependent JNK activation. Respir Res. 2012;13:73.
[81] Curran AD. The role of nitric oxide in the development of asthma. Int Arch Allergy Immunol. 1996;111(1):1-4.
[82] Abbas AK, Murphy KM, Sher A. Functional diversity of helper T lymphocytes. Nature. 1996;383(6603):787-93.
[83] Ouyang W, Ranganath SH, Weindel K, Bhattacharya D, Murphy TL, Sha WC, Murphy KM. Inhibition of Th1 development mediated by GATA-3 through an IL-4-independent mechanism. Immunity. 1998;9(5):745-55.
[84] Ferber IA, Lee HJ, Zonin F, Heath V, Mui A, Arai N, O'Garra A. GATA-3 significantly downregulates IFN-gamma production from developing Th1 cells in addition to inducing IL-4 and IL-5 levels. Clin Immunol. 1999;91(2):134-44.
[85] Chang RH, Feng MH, Liu WH, Lai MZ. Nitric oxide increased interleukin-4 expression in T lymphocytes. Immunology. 1997;90(3):364-9.
[86] 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 U S A. 2002;99(25):16186-91.
[87] Bauer H, Jung T, Tsikas D, Stichtenoth DO, Frölich 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(2):205-11.
[88] 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(4):2715-20.
[89] Adler KB, Fischer BM, Li H, Chloe NH, Wright DT. Hyper secretion of cumin is response to inflammatory mediators by guinea pig tracheal epithelial cells in vitro is blocked by inhibition of nitric oxide synthesis. Am J Respir Cell Mol Biol. 1995;13:526–530.
[90] Angeli P, Prado CM, Xisto DG, Silva PL, Pássaro CP, Nakazato HD, Leick-Maldonado EA, Martins MA, Rocco PR, Tibério IF. Effects of chronic L-NAME treatment lung tissue mechanics, eosinophilic and extracellular matrix responses induced by chronic pulmonary inflammation. Am J Physiol Lung Cell Mol Physiol. 2008;294(6):L1197-205.
[91] Prado CM, Leick-Maldonado EA, Kasahara DI, Capelozzi VL, Martins MA, Tibério IF. Effects of acute and chronic nitric oxide inhibition in an experimental model of chronic pulmonary allergic inflammation in guinea pigs. Am J Physiol Lung Cell Mol Physiol. 2005;289(4):L677-83.
[92] Iijima H, Duguet A, Eum SY, Hamid Q, Eidelman DH. Nitric oxide and protein nitration are eosinophil dependent in allergen-challenged mice. Am J Respir Crit Care Med. 2001;163(5):1233-40.
[93] Starling CM, Prado CM, Leick-Maldonado EA, Lanças T, Reis FG, Aristóteles LR, Dolhnikoff M, Martins MA, Tibério IF. Inducible nitric oxide synthase inhibition attenuates lung tissue responsiveness and remodeling in a model of chronic pulmonary inflammation in guinea pigs. Respir Physiol Neurobiol. 2009;165(2-3):185-94.
[94] Karpuzoglu E, Ahmed SA. Estrogen regulation of nitric oxide and inducible nitric oxide synthase (iNOS) in immune cells: implications for immunity, autoimmune diseases, and apoptosis. Nitric Oxide. 2006;15(3):177-86.
[95] Thomassen MJ, Buhrow LT, Connors MJ, Kaneko FT, Erzurum SC, Kavuru MS. Nitric oxide inhibits inflammatory cytokine production by human alveolar macrophages. Am J Respir Cell Mol Biol. 1997;17(3):279-83.
[96] Raychaudhuri B, Dweik R, Connors MJ, Buhrow L, Malur A, Drazba J, Arroliga AC, Erzurum SC, Kavuru MS, Thomassen MJ. Nitric oxide blocks nuclear factor-kappaB activation in alveolar macrophages. Am J Respir Cell Mol Biol. 1999;21(3):311-6.
[97] Sato E, Simpson KL, Grisham MB, Koyama S, Robbins RA. Reactive nitrogen and oxygen species attenuate interleukin- 8-induced neutrophil chemotactic activity in vitro. J Biol Chem. 2000;275(15):10826-30.
[98] Kim YM, Talanian RV, Billiar TR. Nitric oxide inhibits apoptosis by preventing increases in caspase-3-like activity via two distinct mechanisms. J Biol Chem. 1997;272(49):31138-48.