1932

Abstract

The versatile chemistry of nitrogen is important to pulmonary physiology. Indeed, almost all redox forms of nitrogen are relevant to pulmonary physiology and to pathophysiology. Here we review the relevance to pulmonary biology of () elemental nitrogen; () reduced forms of nitrogen such as amines, ammonia, and hydroxylamine; and () oxidized forms of nitrogen such as the nitroxyl anion, the nitric oxide free radical, and -nitrosothiols. Our focus is on oxidized nitrogen in the form of -nitrosothiol bond–containing species, which are now appreciated to be important to every type of cell-signaling process in the lung. We also review potential clinical applications of nitrogen oxide biochemistry. These principles are being translated into clinical practice as diagnostic techniques and therapies for a range of pulmonary diseases including asthma, cystic fibrosis, adult respiratory distress syndrome, primary ciliary dyskinesia, and pulmonary hypertension.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-physiol-021113-170352
2015-02-10
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/physiol/77/1/annurev-physiol-021113-170352.html?itemId=/content/journals/10.1146/annurev-physiol-021113-170352&mimeType=html&fmt=ahah

Literature Cited

  1. Joyce CJ, Williams AB. 1.  1999. Kinetics of absorption atelectasis during anesthesia: a mathematical model. J. Appl. Physiol. 86:1116–25 [Google Scholar]
  2. Schreiber F, Stief P, Gieseke A, Heisterkamp IM, Verstraete W. 2.  et al. 2010. Denitrification in human dental plaque. BMC Biol. 8:24 [Google Scholar]
  3. Mitsui T, Kato N, Kondo T. 3.  2000. Estimation of nitrate metabolism in intestinal tract by measuring breath nitrous oxide concentration in Chinese and Japanese. Dig. Dis. Sci. 45:1002–5 [Google Scholar]
  4. Gaston B, Ratjen F, Vaughan JW, Malhotra NR, Canady RG. 4.  et al. 2002. Nitrogen redox balance in the cystic fibrosis airway: effects of antipseudomonal therapy. Am. J. Respir. Crit. Care Med. 165:387–90 [Google Scholar]
  5. Marozkina NV, Gaston B. 5.  2011. Nitrogen balance in the ecosystem of the cystic fibrosis lung. Am. J. Respir. Crit. Care Med. 183:1290–92 [Google Scholar]
  6. Quinton PM. 6.  2010. Role of epithelial HCO3 transport in mucin secretion: lessons from cystic fibrosis. Am. J. Physiol. Cell Physiol. 299:C1222–33 [Google Scholar]
  7. Pezzulo AA, Tang XX, Hoegger MJ, Alaiwa MH, Ramachandran S. 7.  et al. 2012. Reduced airway surface pH impairs bacterial killing in the porcine cystic fibrosis lung. Nature 487:109–13 [Google Scholar]
  8. Hunt JF, Erwin E, Palmer L, Vaughan J, Malhotra N. 8.  et al. 2002. Expression and activity of pH-regulatory glutaminase in the human airway epithelium. Am. J. Respir. Crit. Care Med. 165:101–7 [Google Scholar]
  9. Ngamtrakulpanit L, Yu Y, Adjei A, Amoah G, Gaston B, Hunt J. 9.  2010. Identification of intrinsic airway acidification in pulmonary tuberculosis. Glob. J. Health Sci. 2:106–10 [Google Scholar]
  10. Kostikas K, Papatheodorou G, Ganas K, Psathakis K, Panagou P, Loukides S. 10.  2002. pH in expired breath condensate of patients with inflammatory airway diseases. Am. J. Respir. Crit. Care Med. 165:1364–70 [Google Scholar]
  11. Carraro S, Doherty J, Zaman K, Gainov I, Turner R. 11.  et al. 2006. S-Nitrosothiols regulate cell-surface pH buffering by airway epithelial cells during the human immune response to rhinovirus. Am. J. Physiol. Lung Cell. Mol. Physiol. 290:L827–32 [Google Scholar]
  12. Hattori Y, Campbell EB, Gross SS. 12.  1994. Argininosuccinate synthetase mRNA and activity are induced by immunostimulants in vascular smooth muscle. Role in the regeneration or arginine for nitric oxide synthesis. J. Biol. Chem. 269:9405–8 [Google Scholar]
  13. Engelen MP, Com G, Luiking YC, Deutz NE. 13.  2013. Stimulated nitric oxide production and arginine deficiency in children with cystic fibrosis with nutritional failure. J. Pediatr. 163:369–75 e1 [Google Scholar]
  14. Grasemann H, Pencharz PB. 14.  2013. Arginine metabolism in patients with cystic fibrosis. J. Pediatr. 163:317–19 [Google Scholar]
  15. DeMaster EG, Raij L, Archer SL, Weir EK. 15.  1989. Hydroxylamine is a vasorelaxant and a possible intermediate in the oxidative conversion of l-arginine to nitric oxide. Biochem. Biophys. Res. Commun. 163:527–33 [Google Scholar]
  16. Jensen DE, Belka GK, Du Bois GC. 16.  1998. S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem. J. 331:Part 2659–68 [Google Scholar]
  17. Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS. 17.  2001. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490–94 [Google Scholar]
  18. Leaf CD, Wishnok JS, Tannenbaum SR. 18.  1989. l-Arginine is a precursor for nitrate biosynthesis in humans. Biochem. Biophys. Res. Commun. 163:1032–37 [Google Scholar]
  19. Hibbs JB Jr, Vavrin Z, Taintor RR. 19.  1987. l-Arginine is required for expression of the activated macrophage effector mechanism causing selective metabolic inhibition in target cells. J. Immunol. 138:550–65 [Google Scholar]
  20. Bredt DS, Snyder SH. 20.  1990. Isolation of nitric oxide synthetase, a calmodulin-requiring enzyme. Proc. Natl. Acad. Sci. USA 87:682–85 [Google Scholar]
  21. Kobzik L, Bredt DS, Lowenstein CJ, Drazen J, Gaston B. 21.  et al. 1993. Nitric oxide synthase in human and rat lung: immunocytochemical and histochemical localization. Am. J. Respir. Cell Mol. Biol. 9:371–77 [Google Scholar]
  22. Asano K, Chee CB, Gaston B, Lilly CM, Gerard C. 22.  et al. 1994. Constitutive and inducible nitric oxide synthase gene expression, regulation, and activity in human lung epithelial cells. Proc. Natl. Acad. Sci. USA 91:10089–93 [Google Scholar]
  23. Guo FH, De Raeve HR, Rice TW, Stuehr DJ, Thunnissen FB, Erzurum SC. 23.  1995. Continuous nitric oxide synthesis by inducible nitric oxide synthase in normal human airway epithelium in vivo. Proc. Natl. Acad. Sci. USA 92:7809–13 [Google Scholar]
  24. Vodovotz Y, Russell D, Xie QW, Bogdan C, Nathan C. 24.  1995. Vesicle membrane association of nitric oxide synthase in primary mouse macrophages. J. Immunol. 154:2914–25 [Google Scholar]
  25. Fukuto JM, Bianco CL, Chavez TA. 25.  2009. Nitroxyl (HNO) signaling. Free Radic. Biol. Med. 47:1318–24 [Google Scholar]
  26. Tsukahara H, Ishida T, Mayumi M. 26.  1999. Gas-phase oxidation of nitric oxide: chemical kinetics and rate constant. Nitric Oxide 3:191–98 [Google Scholar]
  27. Liu X, Miller MJ, Joshi MS, Thomas DD, Lancaster JR Jr. 27.  1998. Accelerated reaction of nitric oxide with O2 within the hydrophobic interior of biological membranes. Proc. Natl. Acad. Sci. USA 95:2175–79 [Google Scholar]
  28. Fernhoff NB, Derbyshire ER, Underbakke ES, Marletta MA. 28.  2012. Heme-assisted S-nitrosation desensitizes ferric soluble guanylate cyclase to nitric oxide. J. Biol. Chem. 287:43053–62 [Google Scholar]
  29. Katsuki S, Arnold W, Mittal C, Murad F. 29.  1977. Stimulation of guanylate cyclase by sodium nitroprusside, nitroglycerin and nitric oxide in various tissue preparations and comparison to the effects of sodium azide and hydroxylamine. J. Cycl. Nucleotide Res. 3:23–35 [Google Scholar]
  30. Gaston B, Drazen JM, Jansen A, Sugarbaker DA, Loscalzo J. 30.  et al. 1994. Relaxation of human bronchial smooth muscle by S-nitrosothiols in vitro. J. Pharmacol. Exp. Ther. 268:978–84 [Google Scholar]
  31. Gaston B, Reilly J, Drazen JM, Fackler J, Ramdev P. 31.  et al. 1993. Endogenous nitrogen oxides and bronchodilator S-nitrosothiols in human airways. Proc. Natl. Acad. Sci. USA 90:10957–61 [Google Scholar]
  32. Perkins WJ, Pabelick C, Warner DO, Jones KA. 32.  1998. cGMP-independent mechanism of airway smooth muscle relaxation induced by S-nitrosoglutathione. Am. J. Physiol. Cell Physiol. 275:C468–74 [Google Scholar]
  33. Jansen A, Drazen J, Osborne JA, Brown R, Loscalzo J, Stamler JS. 33.  1992. The relaxant properties in guinea pig airways of S-nitrosothiols. J. Pharmacol. Exp. Ther. 261:154–60 [Google Scholar]
  34. Lilly CM, Stamler JS, Gaston B, Meckel C, Loscalzo J, Drazen JM. 34.  1993. Modulation of vasoactive intestinal peptide pulmonary relaxation by NO in tracheally superfused guinea pig lungs. Am. J. Physiol. Lung Cell. Mol. Physiol. 265:L410–15 [Google Scholar]
  35. Bannenberg G, Xue J, Engman L, Cotgreave I, Moldeus P, Ryrfeldt A. 35.  1995. Characterization of bronchodilator effects and fate of S-nitrosothiols in the isolated perfused and ventilated guinea pig lung. J. Pharmacol. Exp. Ther. 272:1238–45 [Google Scholar]
  36. Gaston B, Drazen JM, Loscalzo J, Stamler JS. 36.  1994. The biology of nitrogen oxides in the airways. Am. J. Respir. Crit. Care Med. 149:538–51 [Google Scholar]
  37. Snyder AH, McPherson ME, Hunt JF, Johnson M, Stamler JS, Gaston B. 37.  2002. Acute effects of aerosolized S-nitrosoglutathione in cystic fibrosis. Am. J. Respir. Crit. Care Med. 165:922–26 [Google Scholar]
  38. Moya MP, Gow AJ, McMahon TJ, Toone EJ, Cheifetz IM. 38.  et al. 2001. S-Nitrosothiol repletion by an inhaled gas regulates pulmonary function. Proc. Natl. Acad. Sci. USA 98:5792–97 [Google Scholar]
  39. Estevez AG, Jordan J. 39.  2002. Nitric oxide and superoxide, a deadly cocktail. Ann. N. Y. Acad. Sci. 962:207–11 [Google Scholar]
  40. Nathan CF, Hibbs JB Jr. 40.  1991. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 3:65–70 [Google Scholar]
  41. Broillet MC, Firestein S. 41.  1996. Direct activation of the olfactory cyclic nucleotide–gated channel through modification of sulfhydryl groups by NO compounds. Neuron 16:377–85 [Google Scholar]
  42. Jeffers A, Xu X, Huang KT, Cho M, Hogg N. 42.  et al. 2005. Hemoglobin mediated nitrite activation of soluble guanylyl cyclase. Comp. Biochem. Physiol. A 142:130–35 [Google Scholar]
  43. Hopmann KH, Cardey B, Gladwin MT, Kim-Shapiro DB, Ghosh A. 43.  2011. Hemoglobin as a nitrite anhydrase: modeling methemoglobin-mediated N2O3 formation. Chemistry 17:6348–58 [Google Scholar]
  44. Straub AC, Lohman AW, Billaud M, Johnstone SR, Dwyer ST. 44.  et al. 2012. Endothelial cell expression of haemoglobin α regulates nitric oxide signalling. Nature 491:473–77 [Google Scholar]
  45. Angelo M, Singel DJ, Stamler JS. 45.  2006. An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc. Natl. Acad. Sci. USA 103:8366–71 [Google Scholar]
  46. Herold S, Rock G. 46.  2005. Mechanistic studies of S-nitrosothiol formation by NO*/O2 and by NO*/methemoglobin. Arch. Biochem. Biophys. 436:386–96 [Google Scholar]
  47. Bunn HF, Nathan DG, Dover GJ, Hebbel RP, Platt OS. 47.  et al. 2010. Pulmonary hypertension and nitric oxide depletion in sickle cell disease. Blood 116:687–92 [Google Scholar]
  48. Hebbel RP. 48.  2011. Reconstructing sickle cell disease: a data-based analysis of the “hyperhemolysis paradigm” for pulmonary hypertension from the perspective of evidence-based medicine. Am. J. Hematol. 86:123–54 [Google Scholar]
  49. Gustafsson LE, Leone AM, Persson MG, Wiklund NP, Moncada S. 49.  1991. Endogenous nitric oxide is present in the exhaled air of rabbits, guinea pigs and humans. Biochem. Biophys. Res. Commun. 181:852–57 [Google Scholar]
  50. Ricciardolo FL, Sterk PJ, Gaston B, Folkerts G. 50.  2004. Nitric oxide in health and disease of the respiratory system. Physiol. Rev. 84:731–65 [Google Scholar]
  51. Stamler JS, Singel DJ, Loscalzo J. 51.  1992. Biochemistry of nitric oxide and its redox-activated forms. Science 258:1898–902 [Google Scholar]
  52. Foster MW, Hess DT, Stamler JS. 52.  2009. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol. Med. 15:391–404 [Google Scholar]
  53. Gow AJ, Chen Q, Hess DT, Day BJ, Ischiropoulos H, Stamler JS. 53.  2002. Basal and stimulated protein S-nitrosylation in multiple cell types and tissues. J. Biol. Chem. 277:9637–40 [Google Scholar]
  54. Paige JS, Xu G, Stancevic B, Jaffrey SR. 54.  2008. Nitrosothiol reactivity profiling identifies S-nitrosylated proteins with unexpected stability. Chem. Biol. 15:1307–16 [Google Scholar]
  55. Marozkina NV, Gaston B. 55.  2012. S-Nitrosylation signaling regulates cellular protein interactions. Biochim. Biophys. Acta 1820:722–29 [Google Scholar]
  56. Zhang H, Xu Y, Joseph J, Kalyanaraman B. 56.  2005. Intramolecular electron transfer between tyrosyl radical and cysteine residue inhibits tyrosine nitration and induces thiyl radical formation in model peptides treated with myeloperoxidase, H2O2, and NO2: EPR SPIN trapping studies. J. Biol. Chem. 280:40684–98 [Google Scholar]
  57. Mannick JB, Schonhoff C, Papeta N, Ghafourifar P, Szibor M. 57.  et al. 2001. S-Nitrosylation of mitochondrial caspases. J. Cell Biol. 154:1111–16 [Google Scholar]
  58. Abrams AJ, Farooq A, Wang G. 58.  2011. S-Nitrosylation of ApoE in Alzheimer's disease. Biochemistry 50:3405–7 [Google Scholar]
  59. Smith BC, Fernhoff NB, Marletta MA. 59.  2012. Mechanism and kinetics of inducible nitric oxide synthase auto-S-nitrosation and inactivation. Biochemistry 51:1028–40 [Google Scholar]
  60. Schmidt HH, Hofmann H, Schindler U, Shutenko ZS, Cunningham DD, Feelisch M. 60.  1996. No NO from NO synthase. Proc. Natl. Acad. Sci. USA 93:14492–97 [Google Scholar]
  61. Kim SF, Huri DA, Snyder SH. 61.  2005. Inducible nitric oxide synthase binds, S-nitrosylates, and activates cyclooxygenase-2. Science 310:1966–70 [Google Scholar]
  62. Whalen EJ, Foster MW, Matsumoto A, Ozawa K, Violin JD. 62.  et al. 2007. Regulation of β-adrenergic receptor signaling by S-nitrosylation of G-protein-coupled receptor kinase 2. Cell 129:511–22 [Google Scholar]
  63. Gonzalez DR, Treuer A, Sun QA, Stamler JS, Hare JM. 63.  2009. S-Nitrosylation of cardiac ion channels. J. Cardiovasc. Pharmacol. 54:188–95 [Google Scholar]
  64. Rosenfeld RJ, Bonaventura J, Szymczyna BR, MacCoss MJ, Arvai AS. 64.  et al. 2010. Nitric-oxide synthase forms N-NO-pterin and S-NO-cys: implications for activity, allostery, and regulation. J. Biol. Chem. 285:31581–89 [Google Scholar]
  65. Ozawa K, Whalen EJ, Nelson CD, Mu Y, Hess DT. 65.  et al. 2008. S-Nitrosylation of β-arrestin regulates β-adrenergic receptor trafficking. Mol. Cell 31:395–405 [Google Scholar]
  66. Stamler JS, Toone EJ, Lipton SA, Sucher NJ. 66.  1997. (S)NO signals: translocation, regulation, and a consensus motif. Neuron 18:691–96 [Google Scholar]
  67. Perez-Mato I, Castro C, Ruiz FA, Corrales FJ, Mato JM. 67.  1999. Methionine adenosyltransferase S-nitrosylation is regulated by the basic and acidic amino acids surrounding the target thiol. J. Biol. Chem. 274:17075–79 [Google Scholar]
  68. Matsushita K, Morrell CN, Cambien B, Yang SX, Yamakuchi M. 68.  et al. 2003. Nitric oxide regulates exocytosis by S-nitrosylation of N-ethylmaleimide-sensitive factor. Cell 115:139–50 [Google Scholar]
  69. Gaston B, Singel D, Doctor A, Stamler JS. 69.  2006. S-Nitrosothiol signaling in respiratory biology. Am. J. Respir. Crit. Care Med. 173:1186–93 [Google Scholar]
  70. Marozkina NV, Wei C, Yemen S, Wallrabe H, Nagji AS. 70.  et al. 2012. S-Nitrosoglutathione reductase in human lung cancer. Am. J. Respir. Cell Mol. Biol. 46:63–70 [Google Scholar]
  71. Inoue K, Akaike T, Miyamoto Y, Okamoto T, Sawa T. 71.  et al. 1999. Nitrosothiol formation catalyzed by ceruloplasmin. Implication for cytoprotective mechanism in vivo. J. Biol. Chem. 274:27069–75 [Google Scholar]
  72. Fang K, Johns R, Macdonald T, Kinter M, Gaston B. 72.  2000. S-Nitrosoglutathione breakdown prevents airway smooth muscle relaxation in the guinea pig. Am. J. Physiol. Lung Cell. Mol. Physiol. 279:L716–21 [Google Scholar]
  73. Benhar M, Forrester MT, Hess DT, Stamler JS. 73.  2008. Regulated protein denitrosylation by cytosolic and mitochondrial thioredoxins. Science 320:1050–54 [Google Scholar]
  74. Haendeler J, Hoffmann J, Tischler V, Berk BC, Zeiher AM, Dimmeler S. 74.  2002. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat. Cell Biol. 4:743–49 [Google Scholar]
  75. Bateman RL, Rauh D, Tavshanjian B, Shokat KM. 75.  2008. Human carbonyl reductase 1 is an S-nitrosoglutathione reductase. J. Biol. Chem. 283:35756–62 [Google Scholar]
  76. Trujillo M, Alvarez MN, Peluffo G, Freeman BA, Radi R. 76.  1998. Xanthine oxidase–mediated decomposition of S-nitrosothiols. J. Biol. Chem. 273:7828–34 [Google Scholar]
  77. Johnson MA, Macdonald TL, Mannick JB, Conaway MR, Gaston B. 77.  2001. Accelerated S-nitrosothiol breakdown by amyotrophic lateral sclerosis mutant copper,zinc-superoxide dismutase. J. Biol. Chem. 276:39872–78 [Google Scholar]
  78. Ramachandran N, Root P, Jiang XM, Hogg PJ, Mutus B. 78.  2001. Mechanism of transfer of NO from extracellular S-nitrosothiols into the cytosol by cell-surface protein disulfide isomerase. Proc. Natl. Acad. Sci. USA 98:9539–44 [Google Scholar]
  79. Kornberg MD, Sen N, Hara MR, Juluri KR, Nguyen JV. 79.  et al. 2010. GAPDH mediates nitrosylation of nuclear proteins. Nat. Cell Biol. 12:1094–100 [Google Scholar]
  80. Gaston B, Stamler JS. 80.  1997. Nitrogen oxides and lung function. The Lung: Scientific Foundations J West, R Crystal, E Weibel, P Barnes 239–53 Philadelphia: Lippincott-Raven [Google Scholar]
  81. Jaffrey SR. 81.  2005. Detection and characterization of protein nitrosothiols. Methods Enzymol. 396:105–18 [Google Scholar]
  82. Hogg N, Singh RJ, Konorev E, Joseph J, Kalyanaraman B. 82.  1997. S-Nitrosoglutathione as a substrate for γ-glutamyl transpeptidase. Biochem. J. 323:Part 2477–81 [Google Scholar]
  83. Holder AA, Marshall SC, Wang PG, Kwak CH. 83.  2003. The mechanism of the decomposition of a bronchodilator, S-nitroso-N-acetyl-d,l-penicillamine (SNAP), by a bronchoconstrictor, aqueous sulfite: detection of the N-nitrosohydroxylamine-N-sulfonate ion. Bull. Korean Chem. Soc. 3:350–56 [Google Scholar]
  84. Doctor A, Platt R, Sheram ML, Eischeid A, McMahon T. 84.  et al. 2005. Hemoglobin conformation couples erythrocyte S-nitrosothiol content to O2 gradients. Proc. Natl. Acad. Sci. USA 102:5709–14 [Google Scholar]
  85. Pawloski JR, Hess DT, Stamler JS. 85.  2001. Export by red blood cells of nitric oxide bioactivity. Nature 409:622–26 [Google Scholar]
  86. Zhang Y, Hogg N. 86.  2004. The mechanism of transmembrane S-nitrosothiol transport. Proc. Natl. Acad. Sci. USA 101:7891–96 [Google Scholar]
  87. Lipton AJ, Johnson MA, Macdonald T, Lieberman MW, Gozal D, Gaston B. 87.  2001. S-Nitrosothiols signal the ventilatory response to hypoxia. Nature 413:171–74 [Google Scholar]
  88. Zaman K, Hanigan MH, Smith A, Vaughan J, Macdonald T. 88.  et al. 2006. Endogenous S-nitrosoglutathione modifies 5-lipoxygenase expression in airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 34:387–93 [Google Scholar]
  89. Marshall HE, Hess DT, Stamler JS. 89.  2004. S-Nitrosylation: physiological regulation of NF-κB. Proc. Natl. Acad. Sci. USA 101:8841–42 [Google Scholar]
  90. Reynaert NL, Ckless K, Korn SH, Vos N, Guala AS. 90.  et al. 2004. Nitric oxide represses inhibitory κB kinase through S-nitrosylation. Proc. Natl. Acad. Sci. USA 101:8945–50 [Google Scholar]
  91. Zaman K, Palmer LA, Doctor A, Hunt JF, Gaston B. 91.  2004. Concentration-dependent effects of endogenous S-nitrosoglutathione on gene regulation by specificity proteins Sp3 and Sp1. Biochem. J. 380:67–74 [Google Scholar]
  92. Hara MR, Snyder SH. 92.  2006. Nitric oxide-GAPDH-Siah: a novel cell death cascade. Cell. Mol. Neurobiol. 26:527–38 [Google Scholar]
  93. Marozkina NV, Yemen S, Borowitz M, Liu L, Plapp M. 93.  et al. 2010. Hsp 70/Hsp 90 organizing protein as a nitrosylation target in cystic fibrosis therapy. Proc. Natl. Acad. Sci. USA 107:11393–98 [Google Scholar]
  94. Palmer LA, Doctor A, Chhabra P, Sheram ML, Laubach VE. 94.  et al. 2007. S-Nitrosothiols signal hypoxia-mimetic vascular pathology. J. Clin. Investig. 117:2592–601 [Google Scholar]
  95. Nott A, Watson PM, Robinson JD, Crepaldi L, Riccio A. 95.  2008. S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455:411–15 [Google Scholar]
  96. Joksovic PM, Doctor A, Gaston B, Todorovic SM. 96.  2007. Functional regulation of T-type calcium channels by S-nitrosothiols in the rat thalamus. J. Neurophysiol. 97:2712–21 [Google Scholar]
  97. Colasanti M, Persichini T, Venturini G, Ascenzi P. 97.  1999. S-Nitrosylation of viral proteins: molecular bases for antiviral effect of nitric oxide. IUBMB Life 48:25–31 [Google Scholar]
  98. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M. 98.  et al. 1999. Fas-induced caspase denitrosylation. Science 284:651–54 [Google Scholar]
  99. Jain L, Chen XJ, Brown LA, Eaton DC. 99.  1998. Nitric oxide inhibits lung sodium transport through a cGMP-mediated inhibition of epithelial cation channels. Am. J. Physiol. Lung Cell. Mol. Physiol. 274:L475–84 [Google Scholar]
  100. Kamosinska B, Radomski MW, Duszyk M, Radomski A, Man SF. 100.  1997. Nitric oxide activates chloride currents in human lung epithelial cells. Am. J. Physiol. Lung Cell. Mol. Physiol. 272:L1098–104 [Google Scholar]
  101. Duta V, Duta F, Puttagunta L, Befus AD, Duszyk M. 101.  2006. Regulation of basolateral Cl channels in airway epithelial cells: the role of nitric oxide. J. Membr. Biol. 213:165–74 [Google Scholar]
  102. Howard M, Fischer H, Roux J, Santos BC, Gullans SR. 102.  et al. 2003. Mammalian osmolytes and S-nitrosoglutathione promote ΔF508 cystic fibrosis transmembrane conductance regulator (CFTR) protein maturation and function. J. Biol. Chem. 278:35159–67 [Google Scholar]
  103. Zaman K, Carraro S, Doherty J, Henderson EM, Lendermon E. 103.  et al. 2006. S-Nitrosylating agents: a novel class of compounds that increase cystic fibrosis transmembrane conductance regulator expression and maturation in epithelial cells. Mol. Pharmacol. 70:1435–42 [Google Scholar]
  104. Atochina-Vasserman EN, Gow AJ, Abramova H, Guo CJ, Tomer Y. 104.  et al. 2009. Immune reconstitution during Pneumocystis lung infection: disruption of surfactant component expression and function by S-nitrosylation. J. Immunol. 182:2277–87 [Google Scholar]
  105. Gaston B, Sears S, Woods J, Hunt J, Ponaman M. 105.  et al. 1998. Bronchodilator S-nitrosothiol deficiency in asthmatic respiratory failure. Lancet 351:1317–19 [Google Scholar]
  106. Baraona E, Abittan CS, Dohmen K, Moretti M, Pozzato G. 106.  et al. 2001. Gender differences in pharmacokinetics of alcohol. Alcohol. Clin. Exp. Res. 25:502–7 [Google Scholar]
  107. Brown-Steinke K, deRonde K, Yemen S, Palmer LA. 107.  2010. Gender differences in S-nitrosoglutathione reductase activity in the lung. PLOS ONE 5:e14007 [Google Scholar]
  108. Que LG, Liu L, Yan Y, Whitehead GS, Gavett SH. 108.  et al. 2005. Protection from experimental asthma by an endogenous bronchodilator. Science 308:1618–21 [Google Scholar]
  109. Moore PE, Ryckman KK, Williams SM, Patel N, Summar ML, Sheller JR. 109.  2009. Genetic variants in GSNOR and ADRB2 influence response to albuterol in African-American children with severe asthma. Pediatr. Pulmonol. 44:649–54 [Google Scholar]
  110. Liu L, Yan Y, Zeng M, Zhang J, Hanes MA. 110.  et al. 2004. Essential roles of S-nitrosothiols in vascular homeostasis and endotoxic shock. Cell 116:617–28 [Google Scholar]
  111. Evangelista AM, Rao VS, Filo AR, Marozkina NV, Doctor A. 111.  et al. 2010. Direct regulation of striated muscle myosins by nitric oxide and endogenous nitrosothiols. PLOS ONE 5:e11209 [Google Scholar]
  112. Davisson RL, Travis MD, Bates JN, Lewis SJ. 112.  1996. Hemodynamic effects of l- and d-S-nitrosocysteine in the rat. Stereoselective S-nitrosothiol recognition sites. Circ. Res. 79:256–62 [Google Scholar]
  113. Pabelick CM, Warner DO, Perkins WJ, Jones KA. 113.  2000. S-Nitrosoglutathione-induced decrease in calcium sensitivity of airway smooth muscle. Am. J. Physiol. Lung Cell. Mol. Physiol. 278:L521–27 [Google Scholar]
  114. Bhandari V, Choo-Wing R, Chapoval SP, Lee CG, Tang C. 114.  et al. 2006. Essential role of nitric oxide in VEGF-induced, asthma-like angiogenic, inflammatory, mucus, and physiologic responses in the lung. Proc. Natl. Acad. Sci. USA 103:11021–26 [Google Scholar]
  115. Moya MP, Gow AJ, Califf RM, Goldberg RN, Stamler JS. 115.  2002. Inhaled ethyl nitrite gas for persistent pulmonary hypertension of the newborn. Lancet 360:141–43 [Google Scholar]
  116. Gaston B, May WJ, Sullivan S, Yemen S, Marozkina NV. 116.  et al. 2014. Essential role of hemoglobin β-93-cysteine in posthypoxia facilitation of breathing in conscious mice. J. Appl. Physiol. 116:1290–99 [Google Scholar]
  117. Reynolds JD, Bennett KM, Cina AJ, Diesen DL, Henderson MB. 117.  et al. 2013. S-Nitrosylation therapy to improve oxygen delivery of banked blood. Proc. Natl. Acad. Sci. USA 110:11529–34 [Google Scholar]
  118. Li D, Shirakami G, Zhan X, Johns RA. 118.  2000. Regulation of ciliary beat frequency by the nitric oxide–cyclic guanosine monophosphate signaling pathway in rat airway epithelial cells. Am. J. Respir. Cell Mol. Biol. 23:175–81 [Google Scholar]
  119. Fischer A, Mundel P, Mayer B, Preissler U, Philippin B, Kummer W. 119.  1993. Nitric oxide synthase in guinea pig lower airway innervation. Neurosci. Lett. 149:157–60 [Google Scholar]
  120. Melamed Y, Shupak A, Bitterman H. 120.  1992. Medical problems associated with underwater diving. N. Engl. J. Med. 326:30–35 [Google Scholar]
  121. Rabin HR, Surette MG. 121.  2012. The cystic fibrosis airway microbiome. Curr. Opin. Pulm. Med. 18:622–27 [Google Scholar]
  122. Elsayed NM. 122.  1994. Toxicity of nitrogen dioxide: an introduction. Toxicology 89:161–74 [Google Scholar]
  123. Haddad IY, Pataki G, Hu P, Galliani C, Beckman JS, Matalon S. 123.  1994. Quantitation of nitrotyrosine levels in lung sections of patients and animals with acute lung injury. J. Clin. Investig. 94:2407–13 [Google Scholar]
  124. Afshari A, Brok J, Moller AM, Wetterslev J. 124.  2010. Inhaled nitric oxide for acute respiratory distress syndrome (ARDS) and acute lung injury in children and adults. Cochrane Database Syst. Rev. 2010:CD002787 [Google Scholar]
  125. Wang D, Li MH, Hsu K, Shen CY, Chen HI, Lin YC. 125.  1992. Air embolism–induced lung injury in isolated rat lungs. J. Appl. Physiol. 72:1235–42 [Google Scholar]
  126. Marshall HE, Potts EN, Kelleher ZT, Stamler JS, Foster WM, Auten RL. 126.  2009. Protection from lipopolysaccharide-induced lung injury by augmentation of airway S-nitrosothiols. Am. J. Respir. Crit. Care Med. 180:11–18 [Google Scholar]
  127. Lim KH, Ancrile BB, Kashatus DF, Counter CM. 127.  2008. Tumour maintenance is mediated by eNOS. Nature 452:646–49 [Google Scholar]
  128. Wei W, Li B, Hanes MA, Kakar S, Chen X, Liu L. 128.  2010. S-Nitrosylation from GSNOR deficiency impairs DNA repair and promotes hepatocarcinogenesis. Sci. Transl. Med. 2:19ra3 [Google Scholar]
  129. Dweik RA, Comhair SA, Gaston B, Thunnissen FB, Farver C. 129.  et al. 2001. NO chemical events in the human airway during the immediate and late antigen-induced asthmatic response. Proc. Natl. Acad. Sci. USA 98:2622–27 [Google Scholar]
  130. Guo FH, Uetani K, Haque SJ, Williams BR, Dweik RA. 130.  et al. 1997. Interferon γ and interleukin 4 stimulate prolonged expression of inducible nitric oxide synthase in human airway epithelium through synthesis of soluble mediators. J. Clin. Investig. 100:829–38 [Google Scholar]
  131. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA. 131.  et al. 1998. Formation of nitric oxide–derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature 391:393–97 [Google Scholar]
  132. Alving K, Weitzberg E, Lundberg JM. 132.  1993. Increased amount of nitric oxide in exhaled air of asthmatics. Eur. Respir. J. 6:1368–70 [Google Scholar]
  133. Gaston B, Massaro A, Drazen J, Chee CBE, Wohl MEB, Stamler JS. 133.  1994. Expired nitric oxide concentrations are elevated in patients with asthma. The Biology of Nitric Oxide 3: Physiological and Clinical Aspects, ed. S Moncada, pp. 497–500. London: Portland Press Proc. [Google Scholar]
  134. Hansel TT, Kharitonov SA, Donnelly LE, Erin EM, Currie MG. 134.  et al. 2003. A selective inhibitor of inducible nitric oxide synthase inhibits exhaled breath nitric oxide in healthy volunteers and asthmatics. FASEB J. 17:1298–300 [Google Scholar]
  135. De Sanctis GT, MacLean JA, Hamada K, Mehta S, Scott JA. 135.  et al. 1999. Contribution of nitric oxide synthases 1, 2, and 3 to airway hyperresponsiveness and inflammation in a murine model of asthma. J. Exp. Med. 189:1621–30 [Google Scholar]
  136. Petsky HL, Cates CJ, Lasserson TJ, Li AM, Turner C. 136.  et al. 2012. A systematic review and meta-analysis: tailoring asthma treatment on eosinophilic markers (exhaled nitric oxide or sputum eosinophils). Thorax 67:199–208 [Google Scholar]
  137. Liu L, Urban P, Hunt JF, Wilkinson P, Laning K, Gaston B. 137.  2010. Changes in exhaled nitric oxide and breath pH during fluticasone wean in asthma. Respiration 79:193–99 [Google Scholar]
  138. Dweik RA, Sorkness RL, Wenzel S, Hammel J, Curran-Everett D. 138.  et al. 2010. Use of exhaled nitric oxide measurement to identify a reactive, at-risk phenotype among patients with asthma. Am. J. Respir. Crit. Care Med. 181:1033–41 [Google Scholar]
  139. Que LG, Yang Z, Stamler JS, Lugogo NL, Kraft M. 139.  2009. S-Nitrosoglutathione reductase: an important regulator in human asthma. Am. J. Respir. Crit. Care Med. 180:226–31 [Google Scholar]
  140. Liu L, Teague WG, Erzurum S, Fitzpatrick A, Mantri S. 140.  et al. 2011. Determinants of exhaled breath condensate pH in a large population with asthma. Chest 139:328–36 [Google Scholar]
  141. Gaston B, Kelly R, Urban P, Liu L, Henderson EM. 141.  et al. 2006. Buffering airway acid decreases exhaled nitric oxide in asthma. J. Allergy Clin. Immunol. 118:817–22 [Google Scholar]
  142. Yoon SS, Coakley R, Lau GW, Lymar SV, Gaston B. 142.  et al. 2006. Anaerobic killing of mucoid Pseudomonas aeruginosa by acidified nitrite derivatives under cystic fibrosis airway conditions. J. Clin. Investig. 116:436–46 [Google Scholar]
  143. Grasemann H, Gaston B, Fang K, Paul K, Ratjen F. 143.  1999. Decreased levels of nitrosothiols in the lower airways of patients with cystic fibrosis and normal pulmonary function. J. Pediatr. 135:770–72 [Google Scholar]
  144. Grasemann H, Al-Saleh S, Scott JA, Shehnaz D, Mehl A. 144.  et al. 2011. Asymmetric dimethylarginine contributes to airway nitric oxide deficiency in patients with cystic fibrosis. Am. J. Respir. Crit. Care Med. 183:1363–68 [Google Scholar]
  145. Piacentini GL, Bodini A, Peroni D, Rigotti E, Pigozzi R. 145.  et al. 2008. Nasal nitric oxide for early diagnosis of primary ciliary dyskinesia: practical issues in children. Respir. Med. 102:541–47 [Google Scholar]
  146. Noone PG, Leigh MW, Sannuti A, Minnix SL, Carson JL. 146.  et al. 2004. Primary ciliary dyskinesia: diagnostic and phenotypic features. Am. J. Respir. Crit. Care Med. 169:459–67 [Google Scholar]
  147. Balfour-Lynn IM, Laverty A, Dinwiddie R. 147.  1996. Reduced upper airway nitric oxide in cystic fibrosis. Arch. Dis. Child. 75:319–22 [Google Scholar]
  148. Nakano H, Ide H, Imada M, Osanai S, Takahashi T. 148.  et al. 2000. Reduced nasal nitric oxide in diffuse panbronchiolitis. Am. J. Respir. Crit. Care Med. 162:2218–20 [Google Scholar]
  149. Degano B, Valmary S, Serrano E, Brousset P, Arnal JF. 149.  2011. Expression of nitric oxide synthases in primary ciliary dyskinesia. Hum. Pathol. 42:1855–61 [Google Scholar]
  150. McMahon TJ, Moon RE, Luchsinger BP, Carraway MS, Stone AE. 150.  et al. 2002. Nitric oxide in the human respiraotry cycle. Nat. Med. 8:711–17 [Google Scholar]
  151. McMahon TJ, Ahearn GS, Moya MP, Gow AJ, Huang YC. 151.  et al. 2005. A nitric oxide processing defect of red blood cells created by hypoxia: deficiency of S-nitrosohemoglobin in pulmonary hypertension. Proc. Natl. Acad. Sci. USA 102:14801–6 [Google Scholar]
/content/journals/10.1146/annurev-physiol-021113-170352
Loading
/content/journals/10.1146/annurev-physiol-021113-170352
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error