Journal of Cystic Fibrosis
Volume 9, Issue 2 , Pages 84-92 , March 2010

Myeloperoxidase-dependent oxidative metabolism of nitric oxide in the cystic fibrosis airway

  • Anna L.P. Chapman

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
    • Current address: Free Radical Research Group, Department of Pathology, University of Otago, Christchurch, New Zealand.
  • ,
  • Brian M. Morrissey

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
  • ,
  • Vihas T. Vasu

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
  • ,
  • Maya M. Juarez

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
  • ,
  • Jessica S. Houghton

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
  • ,
  • Chin-Shang Li

      Affiliations

    • Department of Public Health Sciences, Division of Biostatistics, School of Medicine, University of California, Davis, California 95616, USA
  • ,
  • Carroll E. Cross

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
    • Department of Physiology and Membrane Biology, University of California, Davis, California 95616, USA
  • ,
  • Jason P. Eiserich

      Affiliations

    • Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, California 95616, USA
    • Department of Physiology and Membrane Biology, University of California, Davis, California 95616, USA
    • Corresponding Author InformationCorresponding author. Department of Internal Medicine, Division of Pulmonary/Critical Care Medicine, University of California, Davis, Davis, California 95616 USA. Tel.: +1 530 752 4008; fax: +1 530 752 8632.

Received 30 January 2008 ,Revised 5 August 2009 ,Accepted 1 October 2009.

References 

  1. Kerem B, Rommens JM, Buchanan JA, Markiewicz D, Cox TK, Chakravarti A, et al. Identification of the cystic fibrosis gene: genetic analysis. Science. 1989;245(4922):1073–1080
  2. Boyle MP. Strategies for identifying modifier genes in cystic fibrosis. Proc Am Thorac Soc. 2007;4(1):52–57
  3. Scheid P, Kempster L, Griesenbach U, Davies JC, Dewar A, Weber PP, et al. Inflammation in cystic fibrosis airways: relationship to increased bacterial adherence. Eur Respir J. 2001;17(1):27–35
  4. Carrabino S, Carpani D, Livraghi A, Di Cicco M, Costantini D, Copreni E, et al. Dysregulated interleukin-8 secretion and NF-kappaB activity in human cystic fibrosis nasal epithelial cells. J Cyst Fibros. 2006;5(2):113–119
  5. Moskwa P, Lorentzen D, Excoffon KJ, Zabner J, McCray PB, Nauseef WM, et al. A novel host defense system of airways is defective in cystic fibrosis. Am J Respir Crit Care Med. 2007;175(2):174–183
  6. Birrer P. Proteases and antiproteases in cystic fibrosis: pathogenetic considerations and therapeutic strategies. Respiration. 1995;62(Suppl 1):25–28
  7. Cantin AM, White TB, Cross CE, Forman HJ, Sokol RJ, Borowitz D. Antioxidants in cystic fibrosis. Conclusions from the CF antioxidant workshop, Bethesda, Maryland, November 11–12, 2003. Free Radic Biol Med. 2007;42(1):15–31
  8. Kharitonov SA, Barnes PJ. Clinical aspects of exhaled nitric oxide. Eur Respir J. 2000;16(4):781–792
  9. Grasemann H, Michler E, Wallot M, Ratjen F. Decreased concentration of exhaled nitric oxide (NO) in patients with cystic fibrosis. Pediatr Pulmonol. 1997;24(3):173–177
  10. Lundberg JO, Nordvall SL, Weitzberg E, Kollberg H, Alving K. Exhaled nitric oxide in paediatric asthma and cystic fibrosis. Arch Dis Child. 1996;75(4):323–326
  11. Dotsch J, Demirakca S, Terbrack HG, Huls G, Rascher W, Kuhl PG. Airway nitric oxide in asthmatic children and patients with cystic fibrosis. Eur Respir J. 1996;9(12):2537–2540
  12. Jones KL, Hegab AH, Hillman BC, Simpson KL, Jinkins PA, Grisham MB, et al. Elevation of nitrotyrosine and nitrate concentrations in cystic fibrosis sputum. Pediatr Pulmonol. 2000;30(2):79–85
  13. Zetterquist W, Marteus H, Kalm-Stephens P, Nas E, Nordvall L, Johannesson M, et al. Oral bacteria — the missing link to ambiguous findings of exhaled nitrogen oxides in cystic fibrosis. Respir Med. 2009;103(2):187–193
  14. Kelley TJ, Drumm ML. Inducible nitric oxide synthase expression is reduced in cystic fibrosis murine and human airway epithelial cells. J Clin Invest. 1998;102(6):1200–1207
  15. Morrissey BM, Schilling K, Weil JV, Silkoff PE, Rodman DM. Nitric oxide and protein nitration in the cystic fibrosis airway. Arch Biochem Biophys. 2002;406(1):33–39
  16. Fang FC. Perspectives series: host/pathogen interactions. Mechanisms of nitric oxide-related antimicrobial activity. J Clin Invest. 1997;99(12):2818–2825
  17. Meng QH, Springall DR, Bishop AE, Morgan K, Evans TJ, Habib S, et al. Lack of inducible nitric oxide synthase in bronchial epithelium: a possible mechanism of susceptibility to infection in cystic fibrosis. J Pathol. 1998;184(3):323–331
  18. Grasemann H, Gaston B, Fang K, Paul K, Ratjen F. Decreased levels of nitrosothiols in the lower airways of patients with cystic fibrosis and normal pulmonary function. J Pediatr. 1999;135(6):770–772
  19. 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(7):922–926
  20. Fragoso MA, Fernandez V, Forteza R, Randell SH, Salathe M, Conner GE. Transcellular thiocyanate transport by human airway epithelia. J Physiol. 2004;561(Pt 1):183–194
  21. Mohammed JR, Mohammed BS, Pawluk LJ, Bucci DM, Baker NR, Davis WB. Purification and cytotoxic potential of myeloperoxidase in cystic fibrosis sputum. J Lab Clin Med. 1988;112(6):711–720
  22. Van Der Vliet A, Nguyen MN, Shigenaga MK, Eiserich JP, Marelich GP, Cross CE. Myeloperoxidase and protein oxidation in cystic fibrosis. Am J Physiol, Lung Cell Mol Physiol. 2000;279(3):L537–L546
  23. Forteza R, Salathe M, Miot F, Conner GE. Regulated hydrogen peroxide production by Duox in human airway epithelial cells. Am J Respir Cell Mol Biol. 2005;32(5):462–469
  24. Babior BM. NADPH oxidase: an update. Blood. 1999;93(5):1464–1476
  25. Kim JS, Hackley GH, Okamoto K, Rubin BK. Sputum processing for evaluation of inflammatory mediators. Pediatr Pulmonol. 2001;32(2):152–158
  26. Eiserich JP, Baldus S, Brennan ML, Ma W, Zhang C, Tousson A, et al. Myeloperoxidase, a leukocyte-derived vascular NO oxidase. Science. 2002;296(5577):2391–2394
  27. Fahy JV, Liu J, Wong H, Boushey HA. Analysis of cellular and biochemical constituents of induced sputum after allergen challenge: a method for studying allergic airway inflammation. J Allergy Clin Immunol. 1994;93(6):1031–1039
  28. Society AT, Society ER. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide. Am J Respir Cell Mol Biol. 2005;171:912–930
  29. Suresh V, Shelley DA, Shin HW, George SC. Effect of heterogeneous ventilation and nitric oxide production on exhaled nitric oxide profiles. J Appl Physiol. 2008;104(6):1743–1752
  30. Suri R, Paraskakis E, Bush A. Alveolar, but not bronchial nitric oxide production is elevated in cystic fibrosis. Pediatr Pulmonol. 2007;42(12):1215–1221
  31. Hubert D, Aubourg F, Fauroux B, Trinquart L, Sermet I, Lenoir G, et al. Exhaled nitric oxide in cystic fibrosis: relationships with airway and lung vascular impairments. Eur Respir J. 2009;34(1):117–124
  32. Zetterquist W, Pedroletti C, Lundberg JO, Alving K. Salivary contribution to exhaled nitric oxide. Eur Respir J. 1999;13(2):327–333
  33. Abu-Soud HM, Hazen SL. Nitric oxide is a physiological substrate for mammalian peroxidases. J Biol Chem. 2000;275(48):37524–37532
  34. Gerson C, Sabater J, Scuri M, Torbati A, Coffey R, Abraham JW, et al. The lactoperoxidase system functions in bacterial clearance of airways. Am J Respir Cell Mol Biol. 2000;22(6):665–671
  35. Abu-Soud HM, Hazen SL. Nitric oxide modulates the catalytic activity of myeloperoxidase. J Biol Chem. 2000;275(8):5425–5430
  36. Thomas EL, Jefferson MM, Joyner RE, Cook GS, King CC. Leukocyte myeloperoxidase and salivary lactoperoxidase: identification and quantitation in human mixed saliva. J Dent Res. 1994;73(2):544–555
  37. Eiserich JP, Hristova M, Cross CE, Jones AD, Freeman BA, Halliwell B, et al. Formation of nitric oxide-derived inflammatory oxidants by myeloperoxidase in neutrophils. Nature. 1998;391(6665):393–397
  38. Linnane SJ, Keatings VM, Costello CM, Moynihan JB, O'Connor CM, Fitzgerald MX, et al. Total sputum nitrate plus nitrite is raised during acute pulmonary infection in cystic fibrosis. Am J Respir Crit Care Med. 1998;158(1):207–212
  39. Wooldridge JL, Deutsch GH, Sontag MK, Osberg I, Chase DR, Silkoff PE, et al. NO pathway in CF and non-CF children. Pediatr Pulmonol. 2004;37(4):338–350
  40. Yoon SS, Coakley R, Lau GW, Lymar SV, Gaston B, Karabulut AC, et al. Anaerobic killing of mucoid Pseudomonas aeruginosa by acidified nitrite derivatives under cystic fibrosis airway conditions. J Clin Invest. 2006;116(2):436–446
  41. Grasemann H, Kurtz F, Ratjen F. Inhaled l-arginine improves exhaled nitric oxide and pulmonary function in patients with cystic fibrosis. Am J Respir Crit Care Med. 2006;174(2):208–212
  42. Bousquet J, Chanez P, Lacoste JY, Barneon G, Ghavanian N, Enander I, et al. Eosinophilic inflammation in asthma. N Engl J Med. 1990;323(15):1033–1039
  43. Konstan MW, Hilliard KA, Norvell TM, Berger M. Bronchoalveolar lavage findings in cystic fibrosis patients with stable, clinically mild lung disease suggest ongoing infection and inflammation. Am J Respir Crit Care Med. 1994;150(2):448–454
  44. Danel C, Erzurum SC, McElvaney NG, Crystal RG. Quantitative assessment of the epithelial and inflammatory cell populations in large airways of normals and individuals with cystic fibrosis. Am J Respir Crit Care Med. 1996;153(1):362–368
  45. 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):515–527
  46. Fischer H, Schwarzer C, Illek B. Vitamin C controls the cystic fibrosis transmembrane conductance regulator chloride channel. Proc Natl Acad Sci U S A. 2004;101(10):3691–3696
  47. van Dalen CJ, Winterbourn CC, Senthilmohan R, Kettle AJ. Nitrite as a substrate and inhibitor of myeloperoxidase. Implications for nitration and hypochlorous acid production at sites of inflammation. J Biol Chem. 2000;275(16):11638–11644
  48. Turi JL, Yang F, Garrick MD, Piantadosi CA, Ghio AJ. The iron cycle and oxidative stress in the lung. Free Radic Biol Med. 2004;36(7):850–857

PII: S1569-1993(09)00126-X

doi: 10.1016/j.jcf.2009.10.001

Journal of Cystic Fibrosis
Volume 9, Issue 2 , Pages 84-92 , March 2010