Myeloperoxidase-dependent lipid peroxidation promotes the oxidative modification of cytosolic proteins in phagocytic neutrophils

Journal of Biological Chemistry

Volumn 290, Issue 15, 2015, Pages 9896-9905

  Wilkie Grantham, Rachel P ^a   Magon, Nicholas J ^a   Harwood, D Tim ^a   Kettle, Anthony J ^a   Vissers, Margreet C ^a   Winterbourn, Christine C ^a   Hampton, Mark B ^b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN-ANTIBODY REACTIONS; CARBONYLATION; CHEMICAL ACTIVATION; LIPIDS; OXIDATION;

BUTYLATED HYDROXYTOLUENE; GLUTATHIONE ADDUCTS; LIPID PEROXIDATION; OXIDATIVE MODIFICATION; POST-TRANSLATIONAL MODIFICATIONS; PROTEIN CARBONYLATION; PROTEOMIC ANALYSIS; REACTIVE OXYGEN SPECIES;

PROTEINS;

CALGRANULIN; CALGRANULIN B; MYELOPEROXIDASE; 4-HYDROXY-2-NONENAL; 6-HYDROXY-2,5,7,8-TETRAMETHYLCHROMAN-2-CARBOXYLIC ACID; ALDEHYDE; BUTYLCRESOL; CHROMAN DERIVATIVE; PEROXIDASE; PROTEOME; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ARTICLE; BIOTINYLATION; CARBONYLATION; CENTRIFUGATION; CONTROLLED STUDY; ERYTHROCYTE; HUMAN; HUMAN CELL; LIPID PEROXIDATION; NEUTROPHIL; NONHUMAN; OPSONIZATION; OXIDATION; PHAGOCYTOSIS; PHAGOSOME; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN PROCESSING; PROTEIN PURIFICATION; PROTEOMICS; SEDIMENTATION; STAPHYLOCOCCUS AUREUS; CYTOSOL; DRUG EFFECTS; IMMUNOBLOTTING; MASS SPECTROMETRY; METABOLISM; OXIDATION REDUCTION REACTION; PROCEDURES; PROTEIN CARBONYLATION; TIME; TWO DIMENSIONAL GEL ELECTROPHORESIS;

ALDEHYDES; BUTYLATED HYDROXYTOLUENE; CALGRANULIN B; CHROMANS; CYTOSOL; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; HUMANS; IMMUNOBLOTTING; LEUKOCYTE L1 ANTIGEN COMPLEX; LIPID PEROXIDATION; NADPH OXIDASE; NEUTROPHILS; OXIDATION-REDUCTION; PEROXIDASE; PHAGOCYTOSIS; PROTEIN CARBONYLATION; PROTEOME; PROTEOMICS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TIME FACTORS;

EID: 84927127416     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.613422     Document Type: Article

References (39)

1. Babior, B. M. (1999) NADPH oxidase: an update. Blood 93, 1464-1476
2. Hampton, M. B., Kettle, A. J., and Winterbourn, C. C. (1998) Inside the neutrophil phagosome: oxidants, myeloperoxidase, and bacterial killing. Blood 92, 3007-3017
3. Chapman, A. L., Hampton, M. B., Senthilmohan, R., Winterbourn, C. C., and Kettle, A. J. (2002) Chlorination of bacterial and neutrophil proteins during phagocytosis and killing of Staphylococcus aureus. J. Biol. Chem. 277, 9757-9762
4. Oliver, C. N. (1987) Inactivation of enzymes and oxidative modification of proteins by stimulated neutrophils. Arch. Biochem. Biophys. 253, 62-72
5. Chai, Y. C., Ashraf, S. S., Rokutan, K., Johnston, R. B., Jr., and Thomas, J. A. (1994) S-Thiolation of individual human neutrophil proteins including actin by stimulation of the respiratory burst: evidence against a role for glutathione disulfide. Arch. Biochem. Biophys. 310, 273-281
6. Requena, J. R., Chao, C. C., Levine, R. L., and Stadtman, E. R. (2001) Glutamic and aminoadipic semialdehydes are the main carbonyl products of metal-catalyzed oxidation of proteins. Proc. Natl. Acad. Sci. U.S.A. 98, 69-74
7. Vissers, M. C., and Winterbourn, C. C. (1991) Oxidative damage to fibronectin. I. The effects of the neutrophil myeloperoxidase system and HOCl. Arch. Biochem. Biophys. 285, 53-59
8. Uchida, K., and Stadtman, E. R. (1993) Covalent attachment of 4-hydroxynonenal to glyceraldehyde-3-phosphate dehydrogenase: a possible involvement of intra- and intermolecular cross-linking reaction. J. Biol. Chem. 268, 6388-6393
9. Böyum, A. (1968) Separation of leukocytes from blood and bone marrow. Introduction. Scand. J. Clin. Lab. Invest. Suppl. 97, 7
10. Hampton, M. B., Vissers, M. C., and Winterbourn, C. C. (1994) A single assay for measuring the rates of phagocytosis and bacterial killing by neutrophils. J. Leukoc. Biol. 55, 147-152
11. Buss, H., Chan, T. P., Sluis, K. B., Domigan, N. M., and Winterbourn, C. C. (1997) Protein carbonyl measurement by a sensitive ELISA method. Free Rad. Biol. Med. 23, 361-366
12. Chapman, A. L., Mocatta, T. J., Shiva, S., Seidel, A., Chen, B., Khalilova, I., Paumann-Page, M. E., Jameson, G. N., Winterbourn, C. C., and Kettle, A. J. (2013) Ceruloplasmin is an endogenous inhibitor of myeloperoxidase. J. Biol. Chem. 288, 6465-6477
13. Baty, J. W., Hampton, M. B., and Winterbourn, C. C. (2002) Detection of oxidant sensitive thiol proteins by fluorescence labeling and two-dimensional electrophoresis. Proteomics 2, 1261-1266
14. Yousefi, R., Imani, M., Ardestani, S. K., Saboury, A. A., Gheibi, N., and Ranjbar, B. (2007) 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. (Shanghai) 39, 795-802
15. Ilg, E. C., Troxler, H., Bürgisser, D. M., Kuster, T., Markert, M., Guignard, F., Hunziker, P., Birchler, N., and Heizmann, C. W. (1996) Amino acid sequence determination of human S100A12 (P6, calgranulin C, CGRP, CAAF1) by tandem mass spectrometry. Biochem. Biophys. Res. Commun. 225, 146-150
16. Zhang, R., Brennan, M. L., Shen, Z., MacPherson, J. C., Schmitt, D., Molenda, C. E., and Hazen, S. L. (2002) Myeloperoxidase functions as a major enzymatic catalyst for initiation of lipid peroxidation at sites of inflammation. J. Biol. Chem. 277, 46116-46122
17. Heinecke, J. W. (2002) Tyrosyl radical production by myeloperoxidase: a phagocyte pathway for lipid peroxidation and dityrosine cross-linking of proteins. Toxicology 177, 11-22
18. Esterbauer, H., Schaur, R. J., and Zollner, H. (1991) Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic. Biol. Med. 11, 81-128
19. Quinn, M. T., Linner, J. G., Siemsen, D., Dratz, E. A., Buescher, E. S., and Jesaitis, A. J. (1995) Immunocytochemical detection of lipid peroxidation in phagosomes of human neutrophils: correlation with expression of flavocytochrome b. J. Leukoc. Biol. 57, 415-421
20. Sahara, S., and Yamashima, T. (2010) Calpain-mediated Hsp70.1 cleavage in hippocampal CA1 neuronal death. Biochem. Biophys. Res. Commun. 393, 806-81121.
21. Dalle-Donne, I., Carini, M., Vistoli, G., Gamberoni, L., Giustarini, D., Colombo, R., Maffei Facino, R., Rossi, R., Milzani, A., and Aldini, G. (2007) Actin Cys374 as a nucleophilic target of unsaturated aldehydes.Free Radic. Biol. Med.42, 583-598
22. Aldini, G., Dalle-Donne, I., Vistoli, G., Maffei Facino, R., and Carini, M. (2005) Covalent modification of actin by 4-hydroxy-trans-2-nonenal (HNE): LC-ESI-MS/MS evidence for Cys374 Michael adduction. J. Mass Spectrom. 40, 946-954
23. Guignard, F., Mauel, J., and Markert, M. (1996) Phosphorylation of my-eloid-related proteins MRP-14 and MRP-8 during human neutrophil activation. Eur. J. Biochem. 241, 265-271
24. Roulin, K., Hagens, G., Hotz, R., Saurat, J. H., Veerkamp, J. H., and Siegenthaler, G. (1999) 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, 410-421
25. Kerkhoff, C., Klempt, M., Kaever, V., and Sorg, C. (1999) The two calciumbinding proteins, S100A8 and S100A9, are involved in the metabolism of arachidonic acid in human neutrophils. J. Biol. Chem. 274, 32672-32679
26. Klempt, M., Melkonyan, H., Nacken, W., Wiesmann, D., Holtkemper, U., and Sorg, C. (1997) The heterodimer of the Ca2+-binding proteins MRP8 and MRP14 binds to arachidonic acid. FEBS Lett. 408, 81-84
27. Lemarchand, P., Vaglio, M., Mauël, J., and Markert, M. (1992) Translocation of a small cytosolic calcium-binding protein (MRP-8) to plasma membrane correlates with human neutrophil activation. J. Biol. Chem. 267, 19379-19382
28. Doussiere, J., Bouzidi, F., and Vignais, P. V. (2002) The S100A8/A9 protein as a partner for the cytosolic factors of NADPH oxidase activation in neutrophils. Eur. J. Biochem. 269, 3246-3255
29. Kerkhoff, C., Nacken, W., Benedyk, M., Dagher, M. C., Sopalla, C., and Doussiere, J. (2005) The arachidonic acid-binding protein S100A8/A9 promotes NADPH oxidase activation by interaction with p67phox and Rac-2. FASEB J. 19, 467-469
30. Bouzidi, F., and Doussiere, J. (2004) Binding of arachidonic acid to my-eloid-related proteins (S100A8/A9) enhances phagocytic NADPH oxidase activation. Biochem. Biophys. Res. Commun. 325, 1060-1065
31. Harrison, C. A., Raftery, M. J., Walsh, J., Alewood, P., Iismaa, S. E., Thliveris, S., and Geczy, C. L. (1999) Oxidation regulates the inflammatory properties of the murine S100 protein S100A8. J. Biol. Chem. 274, 8561-8569
32. Lusitani, D., Malawista, S. E., and Montgomery, R. R. (2003) Calprotectin, an abundant cytosolic protein from human polymorphonuclear leukocytes, inhibits the growth of Borrelia burgdorferi. Infect. Immun. 71, 4711-4716
33. Sohnle, P. G., Hunter, M. J., Hahn, B., and Chazin, W. J. (2000) Zincreversible antimicrobial activity of recombinant calprotectin (migration inhibitory factor-related proteins 8 and 14). J. Infect. Dis. 182, 1272-1275
34. Lim, S. Y., Raftery, M. J., Goyette, J., and Geczy, C. L. (2010) SGlutathionylation regulates inflammatory activities of S100A9. J. Biol. Chem. 285, 14377-14388
35. Mantovani, A., Cassatella, M. A., Costantini, C., and Jaillon, S. (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 11, 519-531
36. Parker, H., Dragunow, M., Hampton, M. B., Kettle, A. J., and Winterbourn, C. C. (2012) Requirements for NADPH oxidase and myeloperoxidase in neutrophil extracellular trap formation differ depending on the stimulus. J. Leukoc. Biol. 92, 841-849
37. Poullis, A., Foster, R., Mendall, M. A., and Fagerhol, M. K. (2003) Emerging role of calprotectin in gastroenterology. J. Gastroenterol. Hepatol. 18, 756-762
38. Røseth, A. G., Schmidt, P. N., and Fagerhol, M. K. (1999) Correlation between faecal excretion of indium-111-labelled granulocytes and calprotectin, a granulocyte marker protein, in patients with inflammatory bowel disease. Scand. J. Gastroenterol. 34, 50-54
39. Corbin, B. D., Seeley, E. H., Raab, A., Feldmann, J., Miller, M. R., Torres, V. J., Anderson, K. L., Dattilo, B. M., Dunman, P. M., Gerads, R., Caprioli, R. M., Nacken, W., Chazin, W. J., and Skaar, E. P. (2008) Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 319, 962-965