Celestine blue B as a sensor for hypochlorous acid and HOCL-modified proteins registration

Abstract

Objective — the study of hypochlorous acid (HOCl) and its derivatives production, which catalyzed by human neutrophil myeloperoxidase, using “turn-on” fluorescent sensor — celestine blue B.

Materials and methods. Neutrophils were isolated from the venous blood of healthy donors. Phorbol 12-myristate 13-acetate, N-formyl-methionyl-leucyl-phenylalanine, plant lectins, HOCl-modified proteins were used as agonists. N-acetylcysteine, 4-aminobenzoic acid hydrazide, isoniazid and ceruloplasmin were used as regulators of neutrophil myeloperoxidase activity and/or HOCl scavengers.

Results. Using a wide range of agonists and inhibitors, it has been shown that celestine blue B is oxidized in vitro by HOCl and its derivatives as a result of neutrophil myeloperoxidase activity. The oxidation of celestine blue B by HOCl-modified human serum albumin (HSA-Cl) and inhibition of this process by monoclonal antibody against HSA-Cl (IgM class) was also found.

Conclusion. Based on the developed method using celestine blue B, it is possible to conduct a sensitive analysis for the presence of HOCl-modified proteins (chloramines, etc.), to investigate the effect of various agonists and drugs on myeloperoxidase activity and exocytosis from the neutrophil granules.

Keywords

celestine blue B / HOCl / myeloperoxidase / neutrophils / fluorescence

References

[1] Winterbourn CC, Kettle AJ. Redox reactions and microbial killing in the neutrophil phagosome. Antioxid Redox Signal. 2013;18(6):642-660. https://doi.org/10.1089/ars. 2012.4827.

[2] Panasenko OM, Gorudko IV, Sokolov AV. Hypochlorous acid as a precursor of free radicals in living systems. Biochemistry (Mosc). 2013;78(13):1466-1489. https://doi.org/10.1134/S0006297913130075.

[3] Aratani Y. Myeloperoxidase: its role for host defense, inflammation, and neutrophil function. Arch Biochem Biophys. 2018;640:47-52. https://doi.org/10.1016/j.abb. 2018.01.004.

[4] Liu SR, Wu SP. Hypochlorous acid turn-on fluorescent probe based on oxidation of diphenyl selenide. Org Lett. 2013;15(4):878-881. https://doi.org/10.1021/ol400011u.

[5] Zhang R, Song B, Yuan J. Bioanalytical methods for hypochlorous acid detection: recent advances and challenges. Trends Analyt Chem. 2018;99:1-33. https://doi.org/10.1016/j.trac.2017.11.015.

[6] Bertozo LC, Zeraik ML, Ximenes VF. Dansylglycine, a fluorescent probe for specific determination of halogenating activity of myeloperoxidase and eosinophil peroxidase. Anal Biochem. 2017;532:29-37. https://doi.org/10.1016/j.ab.2017.05.029.

[7] Sokolov AV, Kostevich VA, Kozlov SO, et al. Kinetic method for assaying the halogenating activity of myeloperoxidase based on reaction of celestine blue B with taurine halogenamines. Free Radic Res. 2015;49(6):777-789. https://doi.org/10.3109/10715762.2015.1017478.

[8] Козлов С.О., Кудрявцев И.В., Грудинина Н.А., и др. Активированные нейтрофилы, продуцирующие HOCL, выявляющиеся при проточной цитометрии и конфокальной микроскопии с помощью целестинового синего В // Acta Biomedica Scientifica. – 2016. – Т. 1. – № 3–2. – С. 86–91. [Kozlov SO, Kudryavtsev IV, Grudinina NA, et al. Activated producing HOCL neutrophils revealed by flow cytometry and confocal microscopy with celestine blue B. Acta Biomedica Scientifica. 2016;1(3-2):86-91. (In Russ.)]. https://doi.org/10.12737/article_590823a4895537.04307905.

[9] Sokolov AV, Acquasaliente L, Kostevich VA, et al. Thrombin inhibits the anti-myeloperoxidase and ferroxidase functions of ceruloplasmin: relevance in rheumatoid arthritis. Free Radic Biol Med. 2015;86:279-294. https://doi.org/10.1016/j.freeradbiomed.2015.05.016.

[10] Михальчик Е.В., Смолина Н.В., Астамирова Т.С., и др. Альбумин сыворотки крови, модифицированный в условиях окислительного/галогенирующего стресса, усиливает люминолзависимую хемилюминесценцию нейтрофилов человека // Биофизика. – 2013. – Т. 58. – № 4. – C. 681–689. [Mikhalchik EV, Smolina NV, Astamirova TC, et al. Human serum albumin modified under oxidative/halogenative stress enhances luminol-dependent chemiluminescence of human neutrophils. Biophysics. 2013;58(4):530-536. (In Russ.)]. https://doi.org/10.1134/S0006350913040118.

[11] Gorudko IV, Grigorieva DV, Shamova EV, et al. Hypohalous acid-modified human serum albumin induces neutrophil NADPH oxidase activation, degranulation, and shape change. Free Radic Biol Med. 2014;68:326-334. https://doi.org/10.1016/j.freeradbiomed.2013.12.023.

[12] Freysd’ottir J. Production of monoclonal antibodies. Methods Mol Med. 2000;40:267-279. https://doi.org/10.1385/ 1-59259-076-4:267.

[13] Keshari RS, Verma A, Barthwal MK, Dikshit M. Reactive oxygen species-induced activation of ERK and p38 MAPK mediates PMA-induced NETs release from human neutrophils. J Cell Biochem. 2013;114(3):532-540. https://doi.org/10.1002/jcb.24391.

[14] Ganji SH, Kamanna VS, Kashyap ML. Niacin decreases leukocyte myeloperoxidase: mechanistic role of redox agents and Src/p38MAP kinase. Atherosclerosis. 2014;235(2):554-561. https://doi.org/10.1016/j.atherosclerosis.2014.05.948.

[15] Lindemann O, Strodthoff C, Horstmann M, et al. TRPC1 regulates fMLP-stimulated migration and chemotaxis of neutrophil granulocytes. Biochim Biophys Acta Mol Cell Res. 2015;1853(9):2122-2130. https://doi.org/10.1016/j.bbamcr.2014.12.037.

[16] Grigorieva DV, Gorudko IV, Kostevich VA, et al. Myeloperoxidase exocytosis from activated neutrophils in the presence of heparin. Biochemistry (Moscow). Supplement Series B: Biomedical Chemistry. 2018;12(2):136-142. https://doi.org/10.1134/S199075081802004X.

[17] Huang J, Smith F, Panizzi P. Ordered cleavage of myeloperoxidase ester bonds releases active site heme leading to inactivation of myeloperoxidase by benzoic acid hydrazide analogs. Arch Biochem Biophys. 2014;548:74-85. https://doi.org/10.1016/j.abb.2014.02.014.

[18] Forbes LV, Furtmüller PG, Khalilova I, et al. Isoniazid as a substrate and inhibitor of myeloperoxidase: identification of amine adducts and the influence of superoxide dismutase on their formation. Biochem Pharmacol. 2012;84(7):949-960. https://doi.org/10.1016/j.bcp.2012.07.020.

[19] Sokolov AV, Kostevich VA, Varfolomeeva EY, et al. Capacity of ceruloplasmin to scavenge products of the respiratory burst of neutrophils is not altered by the products of reactions catalyzed by myeloperoxidase. Biochem. Cell Biol. 2018;96(4):457-467. https://doi.org/10.1139/bcb-2017-0277.

[20] Varfolomeeva EY, Semenova EV, Sokolov AV, et al. Ceruloplasmin decreases respiratory burst reaction during pregnancy. Free Radic Res. 2016;50(8):909-919. https://doi.org/10.1080/10715762.2016.1197395.

[21] Storkey C, Davies MJ, Pattison DI. Reevaluation of the rate constants for the reaction of hypochlorous acid (HOCL) with cysteine, methionine, and peptide derivatives using a new competition kinetic approach. Free Radic Biol Med. 2014;73:60-66. https://doi.org/10.1016/j.freeradbiomed.2014.04.024.

[22] Van Damme EJ. History of plant lectin research. Methods Mol Biol. 2014;1200:3-13. https://doi.org/10.1007/978-1-4939-1292-6_1.

[23] Кобелев А.В., Сироткин А.С. Лектины: обзор свойств и перспектив использования в биотехнологии // Вестник биотехнологии и физико-химической биологии им. Ю.А. Овчинникова. – 2018. – Т. 14. – № 2. – С. 60–67. [Kobelev AV, Sirotkin AS. Lectins: a review of properties and prospects for use in biotechnology. Yu.A. Ovchinnikov bulletin of biotechnology and physical and chemical biology. 2018;14(2):60-67. (In Russ.)]

[24] Pereira-da-Silva G, Caroline FC, Roque-Barreira MC. Neutrophil activation induced by plant lectins: modulation of inflammatory processes. Inflamm Allergy Drug Targets. 2012;11(6):433-441. https://doi.org/10.2174/ 187152812803589985.

[25] Timoshenko AV, Gorudko IV, Gabius HJ. Lectins from medicinal plants: Bioeffectors with diverse activities. In: Phytochemicals – Biosynthesis, Function and Application. Ed. by R. Jetter. Vol. 44. Cham: Springer; 2014. P. 43-56. https://doi.org/10.1007/978-3-319-04045-5_3.

[26] Луценко В.Е., Григорьева Д.В., Черенкевич С.Н., и др. Флуоресцентный метод оценки функциональной активности нейтрофилов // Актуальные вопросы биологической физики и химии. – 2018. – Т. 3. – № 3. – С. 612–618. [Lutsenko VE, Grigorieva DV, Cherenkevich SN, et al. Fluorescent method for estiment neutrophils functional activity. Aktual’nye voprosy biologicheskoj fiziki i khimii. 2018;3(3):612-618. (In Russ.)]

[27] Gorudko IV, Vakhrusheva TV, Mukhortova AV, et al. The priming effect of halogenated phospholipids on the functional responses of human neutrophils. Biochemistry (Moscow). Supplement Series A: Membrane and Cell Biology. 2010;4(3):262-271. https://doi.org/10.1134/S1990747810030037.

[28] Salavej P, Spalteholz H, Arnhold J. Modification of amino acid residues in human serum albumin by myeloperoxidase. Free Radic Biol Med. 2006;40(3):516-525. https://doi.org/10.1016/j.freeradbiomed.2005.09.007.

[29] Vlasova II, Sokolov AV, Kostevich VA, et al. Myeloperoxidase-induced oxidation of albumin and ceruloplasmin: role of tyrosines. Biochemistry (Moscow). 2019;84(6):652-662. https://doi.org/10.1134/S0006297919060087.

RIGHTS & PERMISSIONS

Lutsenko V.E., Grigorieva D.V., Gorudko I.V., Cherenkevich S.N., Gorbunov N.N., Kostevich V.A., Panasenko O.M., Sokolov A.V.