Oxidation of calprotectin by hypochlorous acid prevents chelation of essential metal ions and allows bacterial growth: Relevance to infections in cystic fibrosis

Free Radical Biology and Medicine

Volumn 86, Issue , 2015, Pages 133-144

  Magon, Nicholas J ^a   Turner, Rufus ^a   Gearry, Richard B ^a   Hampton, Mark B ^a   Sly, Peter D ^a   Kettle, Anthony J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Calprotectin; Dehydromethionine; Hypochlorous acid; Methionine; Methionine sulfoxide; Nutritional immunity; S100A8; S100A9

Indexed keywords

CALGRANULIN; HYPOCHLOROUS ACID; MANGANESE; METAL ION; METHIONINE; METHIONINE SULFOXIDE; MONOMER; MYELOPEROXIDASE; ZINC ION; PROTEIN BINDING;

AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL GROWTH; CELL ISOLATION; CHELATION; CHILD; CLINICAL ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING; CYSTIC FIBROSIS; DISEASE CONTROL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; INFECTION; LUNG LAVAGE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NEUTROPHIL; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PHAGOCYTOSIS; PRESCHOOL CHILD; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS INFECTION; RECURRENT INFECTION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; AMINO ACID SEQUENCE; CHEMISTRY; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; INFANT; MICROBIOLOGY; MOLECULAR GENETICS; OXIDATION REDUCTION REACTION; PHYSIOLOGY;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

AMINO ACID SEQUENCE; CHILD, PRESCHOOL; CYSTIC FIBROSIS; HUMANS; HYPOCHLOROUS ACID; INFANT; LEUKOCYTE L1 ANTIGEN COMPLEX; MOLECULAR SEQUENCE DATA; NEUTROPHILS; OXIDATION-REDUCTION; OXIDATIVE STRESS; PROTEIN BINDING; PSEUDOMONAS AERUGINOSA; STAPHYLOCOCCUS AUREUS;

EID: 84936760059     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.05.022     Document Type: Article

References (46)

1. L. Feuchtbaum, J. Carter, S. Dowray, R.J. Currier, and F. Lorey Birth prevalence of disorders detectable through newborn screening by race/ethnicity Genet. Med. 14 2012 937 945
2. H. Grasemann, and F. Ratjen Early lung disease in cystic fibrosis Lancet Resp. Med. 1 2013 148 157
3. P.D. Sly, C.L. Gangell, L. Chen, R.S. Ware, S. Ranganathan, L.S. Mott, C.P. Murray, and S.M. Stick Risk factors for bronchiectasis in children with cystic fibrosis N. Engl. J. Med. 368 2013 1963 1970
4. D.G. Yoo, M. Floyd, M. Winn, S.M. Moskowitz, and B. Rada NET formation induced by Pseudomonas aeruginosa cystic fibrosis isolates measured as release of myeloperoxidase-DNA and neutrophil elastase-DNA complexes Immunol. Lett. 160 2014 186 194
5. J. Edgeworth, M. Gorman, R. Bennett, P. Freemont, and N. Hogg Identification of p8,14 as a highly abundant heterodimeric calcium binding protein complex of myeloid cells J. Biol. Chem. 266 1991 7706 7713
6. V. van Heyningen, C. Hayward, J. Fletcher, and C. McAuley Tissue localization and chromosomal assignment of a serum protein that tracks the cystic fibrosis gene Nature 315 1985 513 515
7. B.D. Corbin, E.H. Seeley, A. Raab, J. Feldmann, M.R. Miller, V.J. Torres, K.L. Anderson, B.M. Dattilo, P.M. Dunman, R. Gerads, R.M. Caprioli, W. Nacken, W.J. Chazin, and E.P. Skaar Metal chelation and inhibition of bacterial growth in tissue abscesses Science 319 2008 962 965
8. B.E. Golden, P.A. Clohessy, G. Russell, and M.K. Fagerhol Calprotectin as a marker of inflammation in cystic fibrosis Arch. Dis. Child. 74 1996 136 139
9. S.J. Klebanoff, A.J. Kettle, H. Rosen, C.C. Winterbourn, and W.M. Nauseef Myeloperoxidase: a front-line defender against phagocytosed microorganisms J. Leukoc. Biol. 93 2013 185 198
10. E. Thomson, S. Brennan, R. Senthilmohan, C.L. Gangell, A.L. Chapman, P.D. Sly, and A.J. Kettle Identifying peroxidases and their oxidants in the early pathology of cystic fibrosis Free Radic. Biol. Med. 49 2010 1354 1360
11. S.Y. Lim, M.J. Raftery, J. Goyette, K. Hsu, and C.L. Geczy Oxidative modifications of S100 proteins: functional regulation by redox J. Leukoc. Biol. 86 2009 577 587
12. J.C. Morris The acid ionization constant of HOCl from 5 to 35°J. Phys. Chem. 70 1966 3798 3805
13. K. Agner Peroxidase oxidation of chloride ions Proc. 4th Int. Cong. Biochem. 15 1958 64
14. R.J. Beers, and I.W. Sizer A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase J. Biol. Chem. 195 1952 133 140
15. U.K. Laemmli Cleavage of structural proteins during the assembly of the head of bacteriophage T4 Nature 227 1970 680 685
16. A. Böyum Isolation of mononuclear cells and granulocytes from human blood. Isolation of mononuclear cells by one centrifugation; and of granulocytes by combined centrifugation and sedimentation at 1 g Scand. J. Clin. Lab. Invest. 21 1968 77 89
17. R. Yousefi, M. Imani, S.K. Ardestani, A.A. Saboury, N. Gheibi, and B. Ranjbar Human calprotectin: effect of calcium and zinc on its secondary and tertiary structures, and role of pH in its thermal stability Acta Biochim. Biophys. Sin. 39 2007 795 802
18. A.V. Peskin, R. Turner, G.J. Maghzal, C.C. Winterbourn, and A.J. Kettle Oxidation of methionine to dehydromethionine by reactive halogen species generated by neutrophils Biochemistry 48 2009 10175 10182
19. S.M. Damo, T.E. Kehl-Fie, N. Sugitani, M.E. Holt, S. Rathi, W.J. Murphy, Y. Zhang, C. Betz, L. Hench, G. Fritz, E.P. Skaar, and W.J. Chazin Molecular basis for manganese sequestration by calprotectin and roles in the innate immune response to invading bacterial pathogens Proc. Natl. Acad. Sci. USA 110 2013 3841 3846
20. J.A. Hayden, M.B. Brophy, L.S. Cunden, and E.M. Nolan High-affinity manganese coordination by human calprotectin is calcium-dependent and requires the histidine-rich site formed at the dimer interface J. Am. Chem. Soc. 135 2013 775 787
21. G.E. Reid, K.D. Roberts, E.A. Kapp, and R.I. Simpson Statistical and mechanistic approaches to understanding the gas-phase fragmentation behavior of methionine sulfoxide containing peptides J. Proteome Res. 3 2004 751 759
22. P. Roepstorff, and J. Fohlman Proposal for a common nomenclature for sequence ions in mass spectra of peptides Biomed. Mass Spectrom. 11 1984 601
23. L.R. DeChatelet, P.S. Shirley, and R.B.J. Johnston Effect of phorbol myristate acetate on the oxidative metabolism of human polymorphonuclear leukocytes Blood 47 1976 545 554
24. U. Burner, C. Obinger, M. Paumann, P.G. Furtmuller, and A.J. Kettle Transient and steady-state kinetics of the oxidation of substituted benzoic acid hydrazides by myeloperoxidase J. Biol. Chem. 274 1999 9494 9502
25. L.V. Forbes, T. Sjogren, F. Auchere, D.W. Jenkins, B. Thong, D. Laughton, P. Hemsley, G. Pairaudeau, R. Turner, H. Eriksson, J.F. Unitt, and A.J. Kettle Potent reversible inhibition of myeloperoxidase by aromatic hydroxamates J. Biol. Chem. 288 2013 36636 36647
26. S.Y. Lim, M.J. Raftery, J. Goyette, and C.L. Geczy S-Glutathionylation regulates inflammatory activities of S100A9 J. Biol. Chem. 285 2010 14377 14388
27. A.J. Kettle, T. Chan, I. Osberg, R. Senthilmohan, A.L. Chapman, T.J. Mocatta, and J.S. Wagener Myeloperoxidase and protein oxidation in the airways of young children with cystic fibrosis Am. J. Respir. Crit. Care Med. 170 2004 1317 1323
28. R.D. Gray, A. Duncan, D. Noble, M. Imrie, D.S. O'Reilly, J.A. Innes, D.J. Porteous, A.P. Greening, and A.C. Boyd Sputum trace metals are biomarkers of inflammatory and suppurative lung disease Chest 137 2010 635 641
29. E.R. Stadtman, and R.L. Levine Free radical-mediated oxidation of free amino acids and amino acid residues in proteins Amino Acids 25 2003 207 218
30. S.Y. Lim, M.J. Raftery, and C.L. Geczy Oxidative modifications of DAMPs suppress inflammation: the case for S100A8 and S100A9 Antioxid. Redox Signal. 15 2011 2235 2248
31. G.E. Ronsein, C.C. Winterbourn, P. Di Mascio, and A.J. Kettle Cross-linking methionine and amine residues with reactive halogen species Free Radic. Biol. Med. 70 2014 278 287
32. L.H. Gomes, M.J. Raftery, W.X. Yan, J.D. Goyette, P.S. Thomas, and C.L. Geczy S100A8 and S100A9-oxidant scavengers in inflammation Free Radic. Biol. Med. 58 2013 170 186
33. K. Roulin, G. Hagens, R. Hotz, J.H. Saurat, J.H. Veerkamp, and G. Siegenthaler The fatty acid-binding heterocomplex FA-p34 formed by S100A8 and S100A9 is the major fatty acid carrier in neutrophils and translocates from the cytosol to the membrane upon stimulation Exp. Cell Res. 247 1999 410 421
34. C. Kerkhoff, W. Nacken, M. Benedyk, M.C. Dagher, C. Sopalla, and J. Doussiere The arachidonic acid-binding protein S100A8/A9 promotes NADPH oxidase activation by interaction with p67phox and Rac-2 FASEB J 19 2005 467 469
35. J. Doussiere, F. Bouzidi, and P.V. Vignais The S100A8/A9 protein as a partner for the cytosolic factors of NADPH oxidase activation in neutrophils Eur. J. Biochem. 269 2002 3246 3255
36. H.Y. Sroussi, J. Berline, P. Dazin, P. Green, and J.M. Palefsky S100A8 triggers oxidation-sensitive repulsion of neutrophils J. Dent. Res. 85 2006 829 833
37. H.Y. Sroussi, J. Berline, and J.M. Palefsky Oxidation of methionine 63 and 83 regulates the effect of S100A9 on the migration of neutrophils in vitro J. Leukoc. Biol. 81 2007 818 824
38. C. Ryckman, K. Vandal, P. Rouleau, M. Talbot, and P.A. Tessier Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion J. Immunol. 170 2003 3233 3242
39. A.N. Atallah, A. Puchnick, D. Wu, D.C. Shigueoka, G.M. Silva dos Santos, H.P. Lemos Jr, J.E. Mourao, and W. Iared Remarks about systematic reviews of diagnostic tests Sao Paulo Med. J 130 2012 279 281
40. H.Y. Sroussi, G.A. Kohler, N. Agabian, D. Villines, and J.M. Palefsky Substitution of methionine 63 or 83 in S100A9 and cysteine 42 in S100A8 abrogate the antifungal activities of S100A8/A9: potential role for oxidative regulation FEMS Immunol. Med. Microbiol. 55 2009 55 61
41. D. Basso, E. Greco, P. Fogar, P. Pucci, A. Flagiello, G. Baldo, S. Giunco, A. Valerio, F. Navaglia, C.F. Zambon, A. Falda, S. Pedrazzoli, and M. Plebani Pancreatic cancer-derived S-100A8 N-terminal peptide: a diabetes cause? Clin. Chim. Acta 372 2006 120 128
42. C.C. Winterbourn, M.B. Hampton, J.H. Livesey, and A.J. Kettle Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing J. Biol. Chem. 281 2006 39860 39869
43. R.P. Wilkie-Grantham, N.J. Magon, D.T. Harwood, A.J. Kettle, M.C. Vissers, C.C. Winterbourn, and M.B. Hampton Myeloperoxidase-dependent lipid peroxidation promotes the oxidative modification of cytosolic proteins in phagocytic neutrophils J. Biol. Chem. 2015
44. A.J. Kettle, A.M. Albrett, A.L. Chapman, N. Dickerhof, L.V. Forbes, I. Khalilova, and R. Turner Measuring chlorine bleach in biology and medicine Biochim. Biophys. Acta 1840 2014 781 793
45. A.J. Kettle, R. Turner, C.L. Gangell, D.T. Harwood, I.S. Khalilova, A.L. Chapman, C.C. Winterbourn, and P.D. Sly Oxidation contributes to low glutathione in the airways of children with cystic fibrosis Eur. Respir. J. 44 2014 122 129
46. A.K. Tiden, T. Sjogren, M. Svesson, A. Bernlind, R. Senthilmohan, F. Auchere, H. Norman, P. Markgren, S. Gustavsson, S. Schmidt, S. Lunquist, L.V. Forbes, N.J. Magon, G.N. Jameson, H. Eriksson, and A.J. Kettle 2-Thioxanthines are suicide inhibitors of myeloperoxidase that block oxidative stress during inflammation J. Biol. Chem. 286 2011 37578 37589