Sulfite-mediated Oxidation of Myeloperoxidase to a Free Radical: Immuno-spin Trapping Detection in Human Neutrophils

Overview

Journal Free Radic Biol Med

Specialties Biochemistry
Biology
General Medicine

Date 2013 Feb 5

PMID 23376232

Citations 8

Authors

Kalina Ranguelova

Annette B Rice

Olivier M Lardinois

Mathilde Triquigneaux

Natacha Steinckwich

Leesa J Deterding

Stavros Garantziotis

Ronald P Mason

Affiliations

Soon will be listed here.

Abstract

Previous studies focused on catalyzed oxidation of (bi)sulfite, leading to the formation of the reactive sulfur trioxide ((•)SO3(-)), peroxymonosulfate ((-)O3SOO(•)), and sulfate (SO4(•-)) anion radicals, which can damage target proteins and oxidize them to protein radicals. It is known that these very reactive sulfur- and oxygen-centered radicals can be formed by oxidation of (bi)sulfite by peroxidases. Myeloperoxidase (MPO), an abundant heme protein secreted from activated neutrophils that play a central role in host defense mechanisms, allergic reactions, and asthma, is a likely candidate for initiating the respiratory damage caused by sulfur dioxide. The objective of this study was to examine the oxidative damage caused by (bi)sulfite-derived free radicals in human neutrophils through formation of protein radicals. We used immuno-spin trapping and confocal microscopy to study the protein oxidations driven by sulfite-derived radicals. We found that the presence of sulfite can cause MPO-catalyzed oxidation of MPO to a protein radical in phorbol 12-myristate 13-acetate-activated human neutrophils. We trapped the MPO-derived radicals in situ using the nitrone spin trap 5,5-dimethyl-1-pyrroline N-oxide and detected them immunologically as nitrone adducts in cells. Our present study demonstrates that myeloperoxidase initiates (bi)sulfite oxidation leading to MPO radical damage, possibly leading to (bi)sulfite-exacerbated allergic reactions.

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References

GUNNISON A, Jacobsen D . Sulfite hypersensitivity. A critical review. CRC Crit Rev Toxicol. 1987; 17(3):185-214. DOI: 10.3109/10408448709071208. View

LESTER M . Sulfite sensitivity: significance in human health. J Am Coll Nutr. 1995; 14(3):229-32. DOI: 10.1080/07315724.1995.10718500. View

Taylor S, Higley N, Bush R . Sulfites in foods: uses, analytical methods, residues, fate, exposure assessment, metabolism, toxicity, and hypersensitivity. Adv Food Res. 1986; 30:1-76. DOI: 10.1016/s0065-2628(08)60347-x. View

Ranguelova K, Rice A, Khajo A, Triquigneaux M, Garantziotis S, Magliozzo R . Formation of reactive sulfite-derived free radicals by the activation of human neutrophils: an ESR study. Free Radic Biol Med. 2012; 52(8):1264-71. PMC: 3313009. DOI: 10.1016/j.freeradbiomed.2012.01.016. View

Boyum A . Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968; 97:77-89. View

Smith J . Neutrophils, host defense, and inflammation: a double-edged sword. J Leukoc Biol. 1994; 56(6):672-86. DOI: 10.1002/jlb.56.6.672. View

Johnson J, Waud W, Rajagopalan K, Duran M, Beemer F, WADMAN S . Inborn errors of molybdenum metabolism: combined deficiencies of sulfite oxidase and xanthine dehydrogenase in a patient lacking the molybdenum cofactor. Proc Natl Acad Sci U S A. 1980; 77(6):3715-9. PMC: 349689. DOI: 10.1073/pnas.77.6.3715. View

Furtmuller P, Arnhold J, Jantschko W, Pichler H, Obinger C . Redox properties of the couples compound I/compound II and compound II/native enzyme of human myeloperoxidase. Biochem Biophys Res Commun. 2003; 301(2):551-7. DOI: 10.1016/s0006-291x(02)03075-9. View

GUNNISON A, PALMES E . S-sulfonates in human plasma following inhalation of sulfur dioxide. Am Ind Hyg Assoc J. 1974; 35(5):288-91. DOI: 10.1080/0002889748507036. View

10.

Bassoe C, Li N, Ragheb K, Lawler G, Sturgis J, Robinson J . Investigations of phagosomes, mitochondria, and acidic granules in human neutrophils using fluorescent probes. Cytometry B Clin Cytom. 2002; 51(1):21-9. DOI: 10.1002/cyto.b.10003. View

11.

Lu D, Grinstein S . ATP and guanine nucleotide dependence of neutrophil activation. Evidence for the involvement of two distinct GTP-binding proteins. J Biol Chem. 1990; 265(23):13721-9. View

12.

Rossi F . The O2- -forming NADPH oxidase of the phagocytes: nature, mechanisms of activation and function. Biochim Biophys Acta. 1986; 853(1):65-89. DOI: 10.1016/0304-4173(86)90005-4. View

13.

Ramirez D, Chen Y, Mason R . Immunochemical detection of hemoglobin-derived radicals formed by reaction with hydrogen peroxide: involvement of a protein-tyrosyl radical. Free Radic Biol Med. 2003; 34(7):830-9. DOI: 10.1016/s0891-5849(02)01437-5. View

14.

Barnes P . Reactive oxygen species and airway inflammation. Free Radic Biol Med. 1990; 9(3):235-43. DOI: 10.1016/0891-5849(90)90034-g. View

15.

Klebanoff S . Myeloperoxidase: friend and foe. J Leukoc Biol. 2005; 77(5):598-625. DOI: 10.1189/jlb.1204697. View

16.

Shih V, Abroms I, Johnson J, Carney M, Mandell R, Robb R . Sulfite oxidase deficiency. Biochemical and clinical investigations of a hereditary metabolic disorder in sulfur metabolism. N Engl J Med. 1977; 297(19):1022-8. DOI: 10.1056/NEJM197711102971902. View

17.

Furtmuller P, Obinger C, Hsuanyu Y, Dunford H . Mechanism of reaction of myeloperoxidase with hydrogen peroxide and chloride ion. Eur J Biochem. 2000; 267(19):5858-64. DOI: 10.1046/j.1432-1327.2000.01491.x. View

18.

Mottley C, Mason R . Sulfate anion free radical formation by the peroxidation of (Bi)sulfite and its reaction with hydroxyl radical scavengers. Arch Biochem Biophys. 1988; 267(2):681-9. DOI: 10.1016/0003-9861(88)90077-x. View

19.

Cohen H, Fridovich I . Hepatic sulfite oxidase. Purification and properties. J Biol Chem. 1971; 246(2):359-66. View

20.

Ranguelova K, Chatterjee S, Ehrenshaft M, Ramirez D, Summers F, Kadiiska M . Protein Radical Formation Resulting from Eosinophil Peroxidase-catalyzed Oxidation of Sulfite. J Biol Chem. 2010; 285(31):24195-205. PMC: 2911282. DOI: 10.1074/jbc.M109.069054. View