Modulation of NF-κB and hypoxia-inducible factor-1 by S-nitrosoglutathione does not alter allergic airway inflammation in mice

American Journal of Respiratory Cell and Molecular Biology

Volumn 44, Issue 6, 2011, Pages 813-823

  Olson, Nels ^a   Kasahara, David I ^a   Hristova, Milena ^a   Bernstein, Risa ^a   Janssen Heininger, Yvonne ^a   Van Der Vliet, Albert ^a  

^a UNIVERSITY OF VERMONT COLLEGE OF MEDICINE   (United States)

Author keywords

Asthma; Hypoxia inducible factor 1; Nitric oxide; Nuclear factor B; S nitrosothiols

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; OVALBUMIN; S NITROSOGLUTATHIONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DIFFERENTIATION; LUNG LAVAGE; MALE; METAPLASIA; MOUSE; MUCUS METAPLASIA; NONHUMAN; RESPIRATORY TRACT ALLERGY;

ANIMALS; BRONCHOALVEOLAR LAVAGE FLUID; HYPERSENSITIVITY; HYPOXIA-INDUCIBLE FACTOR 1; INFLAMMATION; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE DONORS; OVALBUMIN; S-NITROSOGLUTATHIONE;

ANIMALIA; MUS;

EID: 80051571620     PISSN: 10441549     EISSN: None     Source Type: Journal    
DOI: 10.1165/rcmb.2010-0035OC     Document Type: Article

References (60)

1. Bove PF, van der Vliet A. Nitric oxide and reactive nitrogen species in airway epithelial signaling and inflammation. Free Rad Biol Med 2006;41:515-527. (Pubitemid 44080515)
2. Gaston B, Drazen JM, Loscalzo J, Stamler JS. The biology of nitrogen oxides in the airways. Am J Respir Crit Care Med 1994;149:538-551. (Pubitemid 24069009)
3. Xiong Y, Karupiah G, Hogan SP, Foster PS, Ramsay AJ. Inhibition of allergic airway inflammation in mice lacking nitric oxide synthase. J Immunol 1999;162:445-452. (Pubitemid 29018952)
4. Feder LS, Stelts D, Chapman RW, Manfra D, Crawley Y, Jones H, Minnicozzi M, Fernandez X, Paster T, Egan RW, et al. Role of nitric oxide on eosinophilic lung inflammation in allergic mice. Am J Respir Cell Mol Biol 1997;17:436-442. (Pubitemid 127500976)
5. 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-B activation in alveolar macrophages. Am J Respir Cell Mol Biol 1999;21:311-316. (Pubitemid 129517185)
6. Okamoto T, Gohil K, Finkelstein EI, Bove P, Akaike T, van der Vliet A. Multiple contributing roles for NOS2 in LPS-induced acute airway inflammation in mice. Am J Physiol Lung Cell Mol Physiol 2004;286:L198-L209. (Pubitemid 38055876)
7. De Sanctis GT, MacLean JA, Hamada K, Mehta S, Scott JA, Jiao A, Yandava CN, Kobzik L, Wolyniec WW, Fabian AJ, et al. Contribution of nitric oxide synthases 1, 2, and 3 to airway hyperresponsiveness and inflammation in a murine model of asthma. J Exp Med 1999;189:1621-1630.
8. Poynter ME, Irvin CG, Janssen-Heininger YM. Rapid activation of nuclear factor-κB in airway epithelium in a murine model of allergic airway inflammation. Am J Pathol 2002;160:1325-1334. (Pubitemid 34411636)
9. Marshall HE, Stamler JS. Inhibition of NF-κB by S-nitrosylation. Biochemistry 2001;40:1688-1693.
10. Reynaert NL, Ckless K, Korn SH, Vos N, Guala AS, Wouters EF, van der Vliet A, Janssen-Heininger YM. Nitric oxide represses inhibitory κB kinase through S-nitrosylation. Proc Natl Acad Sci USA 2004;101: 8841-8842.
11. Gaston B, Sears S, Woods J, Hunt J, Ponaman M, McMahon T, Stamler JS. Bronchodilator S-nitrosothiol deficiency in asthmatic respiratory failure. Lancet 1998;351:1317-1319. (Pubitemid 28195909)
12. Que LG, Yang Z, Stamler JS, Lugogo NL, Kraft M. S-nitrosoglutathione reductase: an important regulator in human asthma. Am J Respir Crit Care Med 2009;180:226-231.
13. Richardson G, Benjamin N. Potential therapeutic uses for S-nitrosothiols. Clin Sci (Lond) 2002;102:99-105. (Pubitemid 34177806)
14. Snyder AH, McPherson ME, Hunt JF, Johnson M, Stamler JS, Gaston B. Acute effects of aerosolized S-nitrosoglutathione in cystic fibrosis. Am J Respir Crit Care Med 2002;165:922-926. (Pubitemid 34774658)
15. Marshall HE, Potts EN, Kelleher ZT, Stamler JS, Foster WM, Auten RL. Protection from lipopolysaccharide-induced lung injury by augmentation of airway S-nitrosothiols. Am J Respir Crit Care Med 2009;180:11-18.
16. Lee SY, Kwon S, Kim KH, Moon HS, Song JS, Park SH, Kim YK. Expression of vascular endothelial growth factor and hypoxia-inducible factor in the airway of asthmatic patients. Ann Allergy Asthma Immunol 2006;97:794-799. (Pubitemid 46032432)
17. Brüne B, Zhou J. Nitric oxide and superoxide: interference with hypoxic signaling. Cardiovasc Res 2007;75:275-282. (Pubitemid 46961919)
18. Ckless K, Lampert A, Reiss J, Kasahara D, Poynter ME, Irvin CG, Lundblad LK, Norton R, van der Vliet A, Janssen-Heininger YM. Inhibition of arginase activity enhances inflammation in mice with allergic airway disease, in association with increases in protein S-nitrosylation and tyrosine nitration. J Immunol 2008;181:4255-4264.
19. Poynter ME, Irvin CG, Janssen-Heininger YM. A prominent role for airway epithelial NF-κB activation in lipopolysaccharide-induced airway inflammation. J Immunol 2003;170:6257-6265. (Pubitemid 36682611)
20. Kasahara DI, Poynter ME, Othman Z, Hemenway D, van der Vliet A. Acrolein inhalation suppresses lipopolysaccharide-induced inflammatory cytokine production but does not affect acute airways neutrophilia. J Immunol 2008;181:736-745.
21. Jaffrey SR, Erdjument-Bromage H, Ferris CD, Tempst P, Snyder SH. Protein S-nitrosylation: a physiological signal for neuronal nitric oxide. Nat Cell Biol 2001;3:193-197. (Pubitemid 32118373)
22. Forrester MT, Foster MW, Stamler JS. Assessment and application of the biotin switch technique for examining protein S-nitrosylation under conditions of pharmacologically induced oxidative stress. J Biol Chem 2007;282:13977-13983. (Pubitemid 47100466)
23. Tsikas D, Denker K, Frolich JC. Artifactual-free analysis of S-nitrosoglutathione and S-nitroglutathione by neutral-pH, anion-pairing, high-performance liquid chromatography: study on peroxynitrite-mediated S-nitration of glutathione to S-nitroglutathione under physiological conditions. J Chromatogr A 2001;915:107-116. (Pubitemid 32289330)
24. Donovan CE, Mark DA, He HZ, Liou HC, Kobzik L, Wang Y, De Sanctis GT, Perkins DL, Finn PW. NF-κB/rel transcription factors: C-rel promotes airway hyperresponsiveness and allergic pulmonary inflammation. J Immunol 1999;163:6827-6833.
25. Yang L, Cohn L, Zhang DH, Homer R, Ray A, Ray P. Essential role of nuclear factor-κB in the induction of eosinophilia in allergic airway inflammation. J Exp Med 1998;188:1739-1750. (Pubitemid 28516118)
26. Kelleher ZT, Matsumoto A, Stamler JS, Marshall HE. NOS2 regulation of NF-κB by S-nitrosylation of p65. J BiolChem2007;282:30667-30672. (Pubitemid 350035227)
27. Long AJ, Sypek JP, Askew R, Fish SC, Mason LE, Williams CM, Goldman SJ. Gob-5 contributes to goblet cell hyperplasia and modulates pulmonary tissue inflammation. Am J Respir Cell Mol Biol 2006;35:357-365. (Pubitemid 44353404)
28. Higgins DF, Kimura K, Bernhardt WM, Shrimanker N, Akai Y, Hohenstein B, Saito Y, Johnson RS, Kretzler M, Cohen CD, et al. Hypoxia promotes fibrogenesis in vivo via HIF-1 stimulation of epithelial-to-mesenchymal transition. J Clin Invest 2007;117:3810-3820. (Pubitemid 350224091)
29. Karhausen J, Furuta GT, Tomaszewski JE, Johnson RS, Colgan SP, Haase VH. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J Clin Invest 2004;114:1098-1106. (Pubitemid 39578699)
30. Lee KS, Kim SR, Park SJ, Park HS, Min KH, Jin SM, Lee MK, Kim UH, Lee YC. Peroxisome proliferator activated receptor-γ modulates reactive oxygen species generation and activation of nuclear factork-κB and hypoxia-inducible factor-1α in allergic airway disease of mice. J Allergy Clin Immunol 2006;118:120-127. (Pubitemid 43949584)
31. Huerta-Yepez S, Baay-Guzman GJ, Garcia-Zepeda R, Hernandez-Pando R, Vega MI, Gonzalez-Bonilla C, Bonavida B. 2-Methoxyestradiol (2-ME) reduces the airway inflammation and remodeling in an experimental mouse model. Clin Immunol 2008;129:313-324.
32. Hjoberg J, Shore S, Kobzik L, Okinaga S, Hallock A, Vallone J, Subramaniam V, De Sanctis GT, Elias JA, Drazen JM, et al. Expression of nitric oxide synthase-2 in the lungs decreases airway resistance and responsiveness. J Appl Physiol 2004;97:249-259. (Pubitemid 38802526)
33. 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;165:1526-1533. (Pubitemid 30604588)
34. Alcorn JF, Ckless K, Brown AL, Guala AS, Kolls JK, Poynter ME, Irvin CG, Van Der Vliet A, Janssen-Heininger YM. Strain-dependent activation of NF-κB in the airway epithelium and its role in allergic airway inflammation. Am J Physiol Lung Cell Mol Physiol 2010;298:57-66.
35. Broide DH, Lawrence T, Doherty T, Cho JY, Miller M, McElwain K, McElwain S, Karin M. Allergen-induced peribronchial fibrosis and mucus production mediated by κB kinase β-dependent genes in airway epithelium. Proc Natl Acad Sci USA 2005;102:17723-17728. (Pubitemid 41803564)
36. Poynter ME, Cloots R, van Woerkom T, Butnor KJ, Vacek P, Taatjes DJ, Irvin CG, Janssen-Heininger YM. Nf-κB activation in airways modulates allergic inflammation but not hyperresponsiveness. J Immunol 2004;173:7003-7009. (Pubitemid 39541089)
37. delaTorre A, Schroeder RA, Bartlett ST, Kuo PC. Differential effects of nitric oxide-mediated S-nitrosylation on p50 and c-Jun DNA binding. Surgery 1998;124:137-141; discussion 141-132.
38. Dweik RA, Comhair SA, Gaston B, Thunnissen FB, Farver C, Thomassen MJ, Kavuru M, Hammel J, Abu-Soud HM, Erzurum SC. No chemical events in the human airway during the immediate and late antigen-induced asthmatic response. Proc Natl Acad Sci USA 2001;98:2622-2627. (Pubitemid 32209532)
39. Liu L, Hausladen A, Zeng M, Que L, Heitman J, Stamler JS. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 2001;410:490-494. (Pubitemid 32240051)
40. Que LG, Liu L, Yan Y, Whitehead GS, Gavett SH, Schwartz DA, Stamler JS. Protection from experimental asthma by an endogenous bronchodilator. Science 2005;308:1618-1621. (Pubitemid 40807509)
41. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004;4:617-629. (Pubitemid 39025047)
42. Guo J, Lu W, Shimoda LA, Semenza GL, Georas SN. Enhanced interferon-γ gene expression in T cells and reduced ovalbumin-dependent lung eosinophilia in hypoxia-inducible factor-1α-deficient mice. Int Arch Allergy Immunol 2009;149:98-102.
43. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, Gallo RL, Hurtado-Ziola N, Nizet V, Johnson RS. HIF-1α expression regulates the bactericidal capacity of phagocytes. J Clin Invest 2005;115:1806-1815. (Pubitemid 40979719)
44. Walmsley SR, Print C, Farahi N, Peyssonnaux C, Johnson RS, Cramer T, Sobolewski A, Condliffe AM, Cowburn AS, Johnson N, et al. Hypoxia-induced neutrophil survival is mediated by HIF-1α-dependent NF-κB activity. J Exp Med 2005;201:105-115. (Pubitemid 40130088)
45. Rosenberger P, Schwab JM, Mirakaj V, Masekowsky E, Mager A, Morote-Garcia JC, Unertl K, Eltzschig HK. Hypoxia-inducible factor-dependent induction of netrin-1 dampens inflammation caused by hypoxia. Nat Immunol 2009;10:195-202.
46. Evans CM, Kim K, Tuvim MJ, Dickey BF. Mucus hypersecretion in asthma: causes and effects. Curr Opin Pulm Med 2009;15:4-11.
47. Lee KS, Kim SR, Park HS, Park SJ, Min KH, Lee KY, Choe YH, Hong SH, Han HJ, Lee YR, et al. A novel thiol compound, N-acetylcysteine amide, attenuates allergic airway disease by regulating activation of NF-κB and hypoxia-inducible factor-1α. Exp Mol Med 2007;39:756-768.
48. Li F, Sonveaux P, Rabbani ZN, Liu S, Yan B, Huang Q, Vujaskovic Z, Dewhirst MW, Li CY. Regulation of HIF-1α stability through S-nitrosylation. Mol Cell 2007;26:63-74. (Pubitemid 46550936)
49. Yasinska IM, Sumbayev VV. S-nitrosation of cys-800 of HIF-1α protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett 2003;549:105-109. (Pubitemid 36959853)
50. Carver DJ,Gaston B, Deronde K, Palmer LA. Akt-mediated activation of HIF-1 in pulmonary vascular endothelial cells by S-nitrosoglutathione. Am J Respir Cell Mol Biol 2007;37:255-263. (Pubitemid 350067605)
51. Sogawa K, Numayama-Tsuruta K, Ema M, Abe M, Abe H, Fujii-Kuriyama Y. Inhibition of hypoxia-inducible factor-1 activity by nitric oxide donors in hypoxia. Proc Natl Acad Sci USA 1998;95:7368-7373. (Pubitemid 28293258)
52. Hagen T, Taylor CT, Lam F, Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF-1α. Science 2003;302:1975-1978. (Pubitemid 37523507)
53. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, Nizet V, Johnson RS, Haddad GG, Karin M. Nf-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α. Nature 2008;453:807-811. (Pubitemid 351793778)
54. van Uden P, Kenneth NS, Rocha S. Regulation of hypoxia-inducible factor-1α by NF-κB. Biochem J 2008;412:477-484.
55. Ricciardolo FL, Gaston B, Hunt J. Acid stress in the pathology of asthma. J Allergy Clin Immunol 2004;113:610-619. (Pubitemid 38530413)
56. Hesslinger C, Strub A, Boer R, Ulrich WR, Lehner MD, Braun C. Inhibition of inducible nitric oxide synthase in respiratory diseases. Biochem Soc Trans 2009;37:886-891.
57. Bove PF, Hristova M, Wesley UV, Olson N, Lounsbury KM, van der Vliet A. Inflammatory levels of nitric oxide inhibit airway epithelial cell migration by inhibition of the kinase ERK1/2 and activation of hypoxia-inducible factor21α. J Biol Chem 2008;283:17919-17928.
58. Tuder RM, Yun JH, Bhunia A, Fijalkowska I. Hypoxia and chronic lung disease. J Mol Med 2007;85:1317-1324. (Pubitemid 350234100)
59. Zhou J, Schmid T, Brune B. Tumor necrosis factor-α causes accumulation of a ubiquitinated form of hypoxia inducible factor-1α through a nuclear factor-κB-dependent pathway. Mol Biol Cell 2003;14:2216-2225. (Pubitemid 36724315)
60. Frede S, Freitag P, Otto T, Heilmaier C, Fandrey J. The proinflammatory cytokine interleukin 1β and hypoxia cooperatively induce the expression of adrenomedullin in ovarian carcinoma cells through hypoxia inducible factor 1 activation. Cancer Res 2005;65:4690-4697. (Pubitemid 40740805)