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The Role of Halogenative Stress in Atherogenic Modification of Low-Density Lipoproteins

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Abstract

This review discusses formation of reactive halogen species (RHS) catalyzed by myeloperoxidase (MPO), an enzyme mostly present in leukocytes. An imbalance between the RHS production and body’s ability to remove or neutralize them leads to the development of halogenative stress. RHS reactions with proteins, lipids, carbohydrates, and antioxi-dants in the content of low-density lipoproteins (LDLs) of the human blood are described. MPO binds site-specifically to the LDL surface and modifies LDL properties and structural organization, which leads to the LDL conversion into proatherogenic forms captured by monocytes/macrophages, which causes accumulation of cholesterol and its esters in these cells and their transformation into foam cells, the basis of atherosclerotic plaques. The review describes the biomarkers of MPO enzymatic activity and halogenative stress, as well as the involvement of the latter in the development of atherosclerosis.

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Abbreviations

ApoB100:

apolipoprotein B-100

CP:

ceruloplas-min

CVD:

cardiovascular disease

HDL:

high-density lipopro-tein

LDL:

low-density lipoprotein

LDL-Br:

low-density lipoprotein modified by HOBr

LDL-Cl:

low-density lipopro-tein modified by HOCl

LPO:

lipid peroxidation

mLDL:

modified low-density lipoprotein

MPO:

myeloperoxidase

RHS:

reactive halogen species

VLDL:

very low-density lipoprotein

References

  1. Klimov, A. N., and Nikulicheva, N. G. (1999) Lipids and Lipoproteins Metabolism and Its Defects [in Russian], Piter, St. Petersburg.

    Google Scholar 

  2. Anichkov, N. N. (1965) Basic Theoretical Principles for Further Studies of the Problem of Atherosclerosis. Atherosclerosis [in Russian], Meditsina, Leningrad, pp. 14–21.

    Google Scholar 

  3. Gofman, J. W., Glazier, F., Tamplin, A., Strisower, B., and De Lalla, O. (1954) Lipoproteins, coronary heart disease, and atherosclerosis, Physiol. Rev., 34, 589–607.

    Article  CAS  PubMed  Google Scholar 

  4. De Lalla, O. F., and Gofman, J. W. (1954) Ultracentrifugal analysis of serum lipoproteins, Methods Biochem. Anal., 1, 459–478.

    Google Scholar 

  5. Tada, H., Kawashiri, M. A., Nohara, A., Inazu, A., Mabuchi, H., and Yamagishi, M. (2017) Impact of clinical signs and genetic diagnosis of familial hypercholes-terolemia on the prevalence of coronary artery disease in patients with severe hypercholesterolemia, Eur. Heart J., 38, 1573–1579.

    Article  CAS  PubMed  Google Scholar 

  6. Carew, T. E. (1989) Role of biologically modified low-density lipoprotein in atherosclerosis, Am. J. Cardiol., 64, 18G–22G.

    Article  CAS  PubMed  Google Scholar 

  7. Aviram, M. (1993) Modified forms of low-density lipopro-tein and atherosclerosis, Atherosclerosis, 98, 1–9.

    Article  CAS  PubMed  Google Scholar 

  8. Brown, M. S., and Goldstein, J. L. (1976) Receptor-mediated control of cholesterol metabolism, Science, 191, 150–154.

    Article  CAS  PubMed  Google Scholar 

  9. Goldstein, J. L., Ho, Y. K., Basu, S. K., and Brown, M. S. (1979) Binding site on macrophages that mediates uptake and degradation of acetylated low-density lipoprotein, producing massive cholesterol deposition, Proc. Natl. Acad. Sci. USA, 76, 333–337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Fogelman, A. M., Schechter, J. S., Hokom, M. Child, J. S., and Edwards, P. A. (1980) Malondialdehyde alteration of low-density lipoprotein leads to cholesterol accumulation in human monocyte-macrophages, Proc. Natl. Acad. Sci. USA, 77, 2214–2218.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Panasenko, O. M., Azizova, O. A., and Vladimirov, Yu. A. (1992) Peroxidation of blood lipoproteins and development of atherosclerosis, Sov. Med. Rev. B. Physicochem. Asp. Med., 3, 1–74.

    Google Scholar 

  12. Steinbrecher, U. P., Zhang, H., and Lougheed, M. (1990) Role of oxidatively modified LDL in atherosclerosis, Free Radic. Biol. Med., 9, 155–168.

    Article  CAS  PubMed  Google Scholar 

  13. Panasenko, O. M., Aksenov, D. V., Mel’nichenko, A. A., Suprun, I. V., Yanushevskaya, E. V., Vlasik, T. N., Sobenin, I. A., and Orekhov, A. N. (2005) Proteolysis of apoprotein B-100 impairs its topography on LDL surface and reduces LDL association resistance, Bull. Exp. Biol. Med., 140, 521–525.

    Article  CAS  PubMed  Google Scholar 

  14. Piha, M., Lindstedt, L., and Kovanen, P. T. (1995) Fusion of proteolyzed low-density lipoprotein in the fluid phase: a novel mechanism generating atherogenic lipoprotein particles, Biochemistry, 34, 10120–10129.

    Article  CAS  PubMed  Google Scholar 

  15. Aksenov, D. V., Mel’nichenko, A. A., Suprun, I. V., Yanushevskaya, E. V., Vlasik, T. N., Sobenin, I. A., Panasenko, O. M., and Orekhov, A. N. (2005) Phospholipid hydrolysis with phospholipases A2 and C impairs apolipoprotein B-100 conformation on the surface of low density lipoproteins by reducing their association resistance, Bull. Exp. Biol. Med., 140, 419–422.

    Article  CAS  PubMed  Google Scholar 

  16. Mel’nichenko, A. A., Tertov, V. V., Ivanova, O. A., Aksenov, D. V., Sobenin, I. A., Popov, E. V., Kaplun, V. V., Suprun, I. V., Panasenko, O. M., and Orekhov, A. N. (2005) Desialylation decreases the resistance of apoB-containing lipoproteins to aggregation and increases their atherogenic potential, Bull. Exp. Biol. Med., 140, 51–54.

    Article  PubMed  CAS  Google Scholar 

  17. Panasenko, O. M., Tertov, V. V., Melnichenko, A. A., Aksenov, D. V., Sobenin, I. A., Kaplun, V. V., Suprun, I. V., and Orekhov, A. N. (2006) Correlation between the athero-genic potential and particle size of apoB-containing lipoproteins deglycosylated with different enzymes, Biol. Membr. (Moscow), 23, 225–234.

    CAS  Google Scholar 

  18. Turk, Z., and Skrabalo, Z. (1987) The cell-interactive properties of glucosylated very-low-density and low-density lipoproteins, Cell Mol. Biol., 33, 345–354.

    CAS  PubMed  Google Scholar 

  19. Avogaro, P., Bon, G. B., and Cazzolato, G. (1988) Presence of a modified low-density lipoprotein in humans, Arteriosclerosis, 8, 79–87.

    Article  CAS  PubMed  Google Scholar 

  20. Tertov, V. V., Sobenin, I. A., Gabbasov, Z. A., Popov, E. G., Jaakkola, O., Solakivi, T., Nikkari, T., Smirnov, V. N., and Orekhov, A. N. (1992) Multiple-modified desialylated low density lipoproteins that cause intracellular lipid accumulation. Isolation, fractionation and characterization, Labor. Invest., 67, 665–675.

    CAS  Google Scholar 

  21. Austin, M. A., Breslow, J. L., Hennekens, C. H., Buring, J. E., Willett, W. C., and Krauss, R. M. (1988) Low-density lipoprotein subclass patterns and risk of myocardial infarction, JAMA, 260, 1917–1921.

    Article  CAS  PubMed  Google Scholar 

  22. Daugherty, A., Dunn, J. L., Rateri, D. L., and Heinecke, J. W. (1994) Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions, J. Clin. Invest., 94, 437–444.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Schindhelm, R. K., van der Zwan, L. P., Teerlink, T., and Scheffer, P. G. (2009) Myeloperoxidase: a useful biomarker for cardiovascular disease risk stratification? Clin. Chem., 55, 1462–1470.

    Article  CAS  PubMed  Google Scholar 

  24. Klebanoff, S. J. (2005) Myeloperoxidase: friend and foe, J. Leukoc. Biol., 77, 598–625.

    Article  CAS  PubMed  Google Scholar 

  25. Panasenko, O. M., Gorudko, I. V., and Sokolov, A. V. (2013) Hypochlorous acid as a precursor of free radicals in living systems, Biochemistry (Moscow), 78, 1466–1489.

    Article  CAS  Google Scholar 

  26. Panasenko, O. M., and Sergienko, V. I. (2010) Halogenative stress and its biomarkers, Vestn. Ross. Akad. Med. Nauk, No. 1, 22–39.

    Google Scholar 

  27. Sies, H. (1991) Role of reactive oxygen species in biological processes, Klin. Wochenschr., 69, 965–968.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Darley-Usmar, V., and Halliwell, B. (1996) Blood radicals: reactive nitrogen species, reactive oxygen species, transition metal ions, and the vascular system, Pharm. Res., 13, 649–662.

    Article  CAS  PubMed  Google Scholar 

  29. Fiedler, T. J., Davey, C. A., and Fenna, R. E. (2000) X-ray crystal structure and characterization of halide-binding sites of human myeloperoxidase at 1.8 Å resolution, J. Biol. Chem., 275, 11964–11971.

    Article  CAS  PubMed  Google Scholar 

  30. Schultz, J., and Kaminker, K. (1962) Myeloperoxidase of the leucocyte of normal human blood. 1. Content and localization, Arch. Biochem. Biophys., 96, 465–467.

    Article  CAS  PubMed  Google Scholar 

  31. Edwards, S. W. (1994) Biochemistry and Physiology of the Neutrophil, Cambridge University Press, Cambridge-New York-Melbourn, p. 299.

    Book  Google Scholar 

  32. Deby-Dupont, G., Deby, C., and Lamy, M. (1999). Neutrophil myeloperoxidase revisited: its role in health and disease, Intensivmed, 36, 500–513.

    Article  Google Scholar 

  33. Smith, R. J., Speziale, S. C., and Bowman, B. J. (1985) Properties of interleukin-1 as a complete secretogen for human neutrophils, Biochem. Biophys. Res. Commun., 130, 1233–1240.

    Article  CAS  PubMed  Google Scholar 

  34. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., and Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria, Science, 303, 1532–1535.

    Article  CAS  PubMed  Google Scholar 

  35. Lau, D., Mollnau, H., Eiserich, J. P., Freeman, B. A., Daiber, A., Gehling, U. M., Brummer, J., Rudolph, V., Munzel, T., Heitzer, T., Meinertz, T., and Baldus, S. (2005) Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins, Proc. Natl. Acad. Sci. USA, 102, 431–436.

    Article  CAS  PubMed  Google Scholar 

  36. Grigorieva, D. V., Gorudko, I. V., Sokolov, A. V., Kostevich, V. A., Vasilyev, V. B., Cherenkevich, S. N., and Panasenko, O. M. (2016) Myeloperoxidase stimulates neu-trophil degranulation, Bull. Exp. Biol. Med., 161, 495–500.

    Article  CAS  PubMed  Google Scholar 

  37. Gorudko, I. V., Grigorieva, D. V., Sokolov, A. V., Shamova, E. V., Kostevich, V. A., Kudryavtsev, I. V., Syromiatnikova, E. D., Vasilyev, V. B., Cherenkevich, S. N., and Panasenko, O. M. (2018) Neutrophil activation in response to monomeric myeloperoxidase, Biochem. Cell Biol., 96, 592–601.

    Article  CAS  PubMed  Google Scholar 

  38. El Kebir, D., Jozsef, L., Pan, W., and Filep, J. G. (2008) Myeloperoxidase delays neutrophil apoptosis through CD11b/CD18 integrins and prolongs inflammation, Circ. Res., 103, 352–359.

    Article  CAS  PubMed  Google Scholar 

  39. Morris, J. C. (1966) The acid ionization constant of HOCl from 5 to 35°, J. Phys. Chem., 70, 3798–3805.

    Article  CAS  Google Scholar 

  40. Furtmuller, P. G., Burner, U., and Obinger, C. (1998) Reaction of myeloperoxidase compound I with chloride, bromide, iodide, and thiocyanate, Biochemistry, 37, 17923–17930.

    Article  CAS  PubMed  Google Scholar 

  41. Pattison, D. I., and Davies, M. J. (2006) Reactions of myeloperoxidase-derived oxidants with biological substrates: gaining chemical insight into human inflammatory diseases, Curr. Med. Chem., 13, 3271–3290.

    Article  CAS  PubMed  Google Scholar 

  42. Panasenko, O. M., Briviba, K., Klotz, L.-O., and Sies, H. (1997) Oxidative modification and nitration of human low-density lipoproteins by the reaction of hypochlorous acid with nitrite, Arch. Biochem. Biophys, 343, 254–259.

    Article  CAS  PubMed  Google Scholar 

  43. Eiserich, J. P., Cross, C. E., Jones, A. D., Halliwell, B., and van der Vliet, A. (1996) Formation of nitrating and chlorinating species by reaction of nitrite with hypochlorous acid. A novel mechanism for nitric oxide-mediated protein modification, J. Biol. Chem., 271, 19199–19208.

    Article  CAS  PubMed  Google Scholar 

  44. Byun, J., Mueller, M., Fabjan, J. S., and Heinecke, J. W. (1999) Nitrogen dioxide radical generated by the myeloper-oxidase-hydrogen peroxide-nitrite system promotes lipid peroxidation of low density lipoproteins, FEBS Lett., 455, 243–246.

    Article  CAS  PubMed  Google Scholar 

  45. Furtmuller, P. G., Jantschko, W., Zederbauer, M., Jakopitsch, C., Arnhold, J., and Obinger, C. (2004) Kinetics of interconversion of redox intermediates of lac-toperoxidase, eosinophil peroxidase and myeloperoxidase, Jpn. J. Infect. Dis., 57, S30–S31.

    Google Scholar 

  46. Kulinsky, V. I. (1999) Reactive oxygen forms and oxidative modification of macromolecules: benefit, harm and defense, Soros Educ. J., 1, 2–7.

    Google Scholar 

  47. Halliwell, B., and Gutteridge, J. M. C. (1999) Free Radical in Biology and Medicine, Oxford University Press, Oxford, pp. 617–783.

    Google Scholar 

  48. Gaut, J. P., Yeh, G. C., Tran, H. D., Byun, J., Henderson, J. P., Richter, G. M., Brennan, M. L., Lusis, A. J., Belaaouaj, A., Hotchkiss, R. S., and Heinecke, J. W. (2001) Neutrophils employ the myeloperoxidase system to generate antimicrobial brominating and chlorinating oxi-dants during sepsis, Proc. Natl. Acad. Sci. USA, 98, 11961–11966.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Dunford, H. B., and Marquez-Curtis, L. A. (2002) Myeloperoxidase: kinetic evidence for formation of enzyme-bound chlorinating intermediate, Methods Enzymol., 354, 338–350.

    Article  CAS  PubMed  Google Scholar 

  50. Thukkani, A. K., Albert, C. J., Wildsmith, K. R., Messner, M. C., Martinson, B. D., Hsu, F. F., and Ford, D. A. (2003) Myeloperoxidase-derived reactive chlorinating species from human monocytes target plasmalogens in low density lipoprotein, J. Biol. Chem., 278, 36365–36372.

    Article  CAS  PubMed  Google Scholar 

  51. Albert, C. J., Crowley, J. R., Hsu, F. F., Thukkani, A. K., and Ford, D. A. (2002) Reactive brominating species produced by myeloperoxidase target the vinyl ether bond of plasmalogens: disparate utilization of sodium halides in the production of alpha-halo fatty aldehydes, J. Biol. Chem., 277, 4694–4703.

    Article  CAS  PubMed  Google Scholar 

  52. Panasenko, O. M., Gorudko, I. V., Kovaleva, A. M., Gusev, S. A., Sergienko, V. I., and Matishev, D. G. (2010) Production and properties of reactive halogen species in carcinogenesis, Vestnik Uzhn. Nauch. Tsentra RAN, 6, 73–90.

    Google Scholar 

  53. Rudiger, J., Bobrowski, N., Liotta, M., and Hoffmann, T. (2017) Development and application of a sampling method for the determination of reactive halogen species in volcanic gas emissions, Anal. Bioanal. Chem., 409, 5975–5985.

    Article  PubMed  CAS  Google Scholar 

  54. Ronsein, G. E., Winterbourn, C. C., Di Mascio, P., and Kettle, A. J. (2014) Cross-linking methionine and amine residues with reactive halogen species, Free Radic. Biol. Med., 70, 278–287.

    Article  CAS  PubMed  Google Scholar 

  55. Pattison, D. I., and Davies, M. J. (2001) Absolute rate constants for the reaction of hypochlorous acid with protein side chains and peptide bonds, Chem. Res. Toxicol., 14, 1453–1464.

    Article  CAS  PubMed  Google Scholar 

  56. Pattison, D. I., and Davies, M. J. (2004) Kinetic analysis of the reactions of hypobromous acid with protein components: implications for cellular damage and use of 3-bro-motyrosine as a marker of oxidative stress, Biochemistry, 43, 4799–4809.

    Article  CAS  PubMed  Google Scholar 

  57. Malle, E., Marsche, G., Arnhold, J., and Davies, M. J. (2006) Modification of low-density lipoprotein by myeloper-oxidase-derived oxidants and reagent hypochlorous acid, Biochim. Biophys. Acta, 1761, 392–415.

    Article  CAS  PubMed  Google Scholar 

  58. Pattison, D. I., Hawkins, C. L., and Davies, M. J. (2003) Hypochlorous acid-mediated oxidation of lipid components and antioxidants present in low-density lipoproteins: absolute rate constants, product analysis, and computational modeling, Chem. Res. Toxicol., 16, 439–449.

    Article  CAS  PubMed  Google Scholar 

  59. Skaff, O., Pattison, D. I., and Davies, M. J. (2007) Kinetics of hypobromous acid-mediated oxidation of lipid components and antioxidants, Chem. Res. Toxicol., 20, 1980–1988.

    Article  CAS  PubMed  Google Scholar 

  60. Hazell, L. J., van den Berg, J. J., and Stocker, R. (1994) Oxidation of low-density lipoprotein by hypochlorite causes aggregation that is mediated by modification of lysine residues rather than lipid oxidation, Biochem. J., 302, 297–304.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Jerlich, A., Horakova, L., Fabjan, J. S., Giessauf, A., Jurgens, G., and Schaur, R. J. (1999) Correlation of low-density lipoprotein modification by myeloperoxidase with hypochlorous acid formation, Int. J. Clin. Lab. Res., 29, 155–161.

    Article  CAS  PubMed  Google Scholar 

  62. Yang, C. Y., Gu, Z. W., Yang, M., Lin, S. N., Garcia-Prats, A. J., Rogers, L. K., Welty, S. E., and Smith, C. V. (1999) Selective modification of ApoB100 in the oxidation of low density lipoproteins by myeloperoxidase in vitro, J. Lipid Res., 40, 686–698.

    CAS  PubMed  Google Scholar 

  63. Delporte, C., Boudjeltia, K. Z., Noyon, C., Furtmuller, P. G., Nuyens, V., Slomianny, M. C., Madhoun, P., Desmet, J. M., Raynal, P., Dufour, D., Koyani, C. N., Reye, F., Rousseau, A., Vanhaeverbeek, M., Ducobu, J., Michalski, J. C., Neve, J., Vanhamme, L., Obinger, C., Malle, E., and Van Antwerpen, P. (2014) Impact of myeloperoxidase-LDL interactions on enzyme activity and subsequent post-translational oxidative modifications of ApoB100, J. Lipid Res., 55, 747–757.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hawkins, C. L., and Davies, M. J. (2005) The role of reactive N-bromo species and radical intermediates in hypo-bromous acid-induced protein oxidation, Free Radic. Biol. Med., 9, 900–912.

    Article  CAS  Google Scholar 

  65. Hawkins, C. L., Pattison, D. I., and Davies, M. J. (2003) Hypochlorite-induced oxidation of amino acids, peptides and proteins, Amino Acids, 25, 259–274.

    Article  CAS  PubMed  Google Scholar 

  66. Fu, X., Mueller, D. M., and Heinecke, J. W. (2002) Generation of intramolecular and intermolecular sulfe-namides, sulfinamides, and sulfonamides by hypochlorous acid: a potential pathway for oxidative cross-linking of low-density lipoprotein by myeloperoxidase, Biochemistry, 41, 1293–1301.

    Article  CAS  PubMed  Google Scholar 

  67. Heinecke, J. W., Li, W., Francis, G. A., and Goldstein, J. A. (1993) Tyrosyl radical generated by myeloperoxidase catalyzes the oxidative cross-linking of proteins, J. Clin. Invest., 91, 2866–2872.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Thomas, E. L. (1979) Myeloperoxidase, hydrogen peroxide, chloride antimicrobial system: nitrogen-chlorine derivatives of bacterial components in bactericidal action against Escherichia coli, Infect. Immun., 23, 522–531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Hawkins, C. L., and Davies, M. J. (1998) Reaction of HOCl with amino acids and peptides: EPR evidence for rapid rearrangement and fragmentation reactions of nitrogen-centered radicals. J. Chem. Soc. Perkin Trans., 2, 1937–1945.

    Article  Google Scholar 

  70. Podrez, E. A., Febbraio, M., Sheibani, N., Schmitt, D., Silverstein, R. L., Hajjar, D. P., Cohen, P. A., Frazier, W. A., Hoff, H. F., and Hazen, S. L. (2000) Macrophage scavenger receptor CD36 is the major receptor for LDL modified by monocyte-generated reactive nitrogen species, J. Clin. Invest., 105, 1095–1108.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Panasenko, O. M., Arnhold, J., and Sergienko, V. I. (2002) Impairment of membrane lipids by hypochlorite, Biol. Membr. (Moscow), 19, 403–434.

    CAS  Google Scholar 

  72. Panasenko, O. M., Arnhold, J., Sergienko, V. I., Arnold, K., and Vladimirov, Yu. A. (1996) Stoichiometry of hypochlorite interaction with unsaturated bonds of phos-phatidylcholine and free fatty acids in liposomes, Membr. Cell Biol., 10, 291–302.

    Google Scholar 

  73. Winterbourn, C. C., van den Berg, J. J., Roitman, E., and Kuypers, F. A. (1992) Chlorohydrin formation from unsat-urated fatty acids reacted with hypochlorous acid, Arch. Biochem. Biophys., 296, 547–555.

    Article  CAS  PubMed  Google Scholar 

  74. Spalteholz, H., Panasenko, O. M., and Arnhold, J. (2006) Formation of reactive halide species by myeloperoxidase and eosinophil peroxidase, Arch. Biochem. Biophys., 445, 225–234.

    Article  CAS  PubMed  Google Scholar 

  75. Panasenko, O. M., Vakhrusheva, T., Tretyakov, V., Spalteholz, H., and Arnhold, J. (2007) Influence of chloride on modification of unsaturated phosphatidylcholines by the myeloperoxidase/hydrogen peroxide/bromide system, Chem. Phys. Lipids, 149, 40–51.

    Article  CAS  PubMed  Google Scholar 

  76. Carr, A. C., Winterbourn, C. C., and van den Berg, J. J. (1996) Peroxidase-mediated bromination of unsaturated fatty acids to form bromohydrins, Arch. Biochem. Biophys., 327, 227–233.

    Article  CAS  PubMed  Google Scholar 

  77. Panasenko, O. M., Spalteholz, H., Schiller, J., and Arnhold, J. (2006) Leukocytic myeloperoxidase-mediated formation of bromohydrins and lysophospholipids from unsaturated phosphatidylcholines, Biochemistry (Moscow), 71, 571–580.

    Article  CAS  Google Scholar 

  78. Panasenko, O. M., Osipov, A. N., Schiller, J., and Arnhold, J. (2002) Interaction of exogenous hypochlorite or hypochlorite produced by myeloperoxidase + H2O2 + Cl- system with unsaturated phosphatidylcholines, Biochemistry (Moscow), 67, 889–900.

    Article  CAS  Google Scholar 

  79. Panasenko, O. M., Spalteholz, H., Schiller, J., and Arnhold, J. (2003). Myeloperoxidase-induced formation of chlorohydrins and lysophospholipids from unsaturated phosphatidylcholines, Free Radic. Biol. Med., 34, 553–562.

    Article  CAS  PubMed  Google Scholar 

  80. Panasenko, O. M., Spalteholz, H., Schiller, J., and Arnhold, J. (2004) Myeloperoxidase mediated destruction of unsaturated phosphatidylcholines in liposomes, Biol. Membr. (Moscow), 21, 138–150.

    CAS  Google Scholar 

  81. Spalteholz, H., Wenske, K., Panasenko, O. M., Schiller, J., and Arnhold, J. (2004) Evaluation of products upon the reaction of hypochlorous acid with unsaturated phos-phatidylcholines, Chem. Phys. Lipids, 129, 85–96.

    Article  CAS  PubMed  Google Scholar 

  82. Arnhold, J., Osipov, A. N., Spalteholz, H., Panasenko, O. M., and Schiller, J. (2002) Formation of lysophospholipids from unsaturated phosphatidylcholines under the influence of hypochlorous acid, Biochim. Biophys. Acta, 1572, 91–100.

    Article  CAS  PubMed  Google Scholar 

  83. Arnhold, J., Osipov, A. N., Spalteholz, H., Panasenko, O. M., and Schiller, J. (2001) Effects of hypochlorous acid on unsaturated phosphatidylcholines, Free Radic. Biol. Med., 31, 1111–1119.

    Article  CAS  PubMed  Google Scholar 

  84. Engelmann, B., Brautigam, C., and Thiery, J. (1994) Plasmalogen phospholipids as potential protectors against lipid peroxidation of low density lipoproteins, Biochem. Biophys. Res. Commun., 204, 1235–1242.

    Article  CAS  PubMed  Google Scholar 

  85. Albert, C. J., Crowley, J. R., Hsu, F. F., Thukkani, A. K., and Ford, D. A. (2001) Reactive chlorinating species produced by myeloperoxidase target the vinyl ether bond of plasmalogens. Identification of 2-chlorohexadecanal, J. Biol. Chem., 276, 23733–23741.

    Article  CAS  PubMed  Google Scholar 

  86. Leßig, J., Schiller, J., Arnhold, J., and Fuchs, B. (2007) Hypochlorous acid-mediated generation of glycerophos-phocholine from unsaturated plasmalogen glycerophos-phocholine lipids, J. Lipid Res., 48, 1316–1324.

    Article  PubMed  CAS  Google Scholar 

  87. Messner, M. C., Albert, C. J., Hsu, F., and Ford, D. A. (2006) Selective plasmenylcholine oxidation by hypo-chlorous acid: formation of lysophosphatidylcholine chlorohydrins, Chem. Phys. Lipids, 144, 34–44.

    Article  CAS  PubMed  Google Scholar 

  88. Skaff, O., Pattison, D. I., and Davies, M. J. (2008) The vinyl ether linkages of plasmalogens are favored targets for myeloperoxidase-derived oxidants: a kinetic study, Biochemistry, 47, 8237–8245.

    Article  CAS  PubMed  Google Scholar 

  89. Schiller, J., Zschornig, O., Petkovic, M., Muller, M., Arnhold, J., and Arnold, K. (2001) Lipid analysis of human HDL and LDL by MALDI-TOF mass spectrometry and 31P-NMR, J. Lipid Res., 42, 1501–1508.

    CAS  PubMed  Google Scholar 

  90. Zakiev, E. R., Sukhorukov, V. N., Melnichenko, A. A., Sobenin, I. A., Ivanova, E. A., and Orekhov, A. N. (2016) Lipid composition of circulating multiple-modified low-density lipoprotein, Lipids Health Dis., 15, 134.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Thukkani, A. K., McHowat, J., Hsu, F. F., Brennan, M. L., Hazen, S. L., and Ford, D. A. (2003) Identification of alpha-chloro fatty aldehydes and unsaturated lysophos-phatidylcholine molecular species in human atherosclerotic lesions, Circulation, 108, 3128–3133.

    Article  CAS  PubMed  Google Scholar 

  92. Siess, W., Zangl, K. J., Essler, M., Bauer, M., Brandl, R., Corrinth, C., Bittman, R., Tigyi, G., and Aepfelbacher, M. (1999) Lysophosphatidic acid mediates the rapid activation of platelets and endothelial cells by mildly oxidized low density lipoprotein and accumulates in human atherosclerotic lesions, Proc. Nat. Acad. Sci. USA, 96, 6931–6936.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Nusshold, C., Kollroser, M., Kofeler, H., Rechberger, G., Reicher, H., Ullen, A., Bernhart, E., Waltl, S., Kratzer, I., Hermetter, A., Hackl, H., Trajanoski, Z., Hrzenjak, A., Malle, E., and Sattler, W. (2010) Hypochlorite modification of sphingomyelin generates chlorinated lipid species that induce apoptosis and proteome alterations in dopaminergic PC12 neurons in vitro, Free Radic. Biol. Med., 48, 1588–600.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Spalteholz, H., Wenske, K., and Arnhold, J. (2005) Interaction of hypohalous acids and heme peroxidases with unsaturated phosphatidylcholines, Biofactors, 24, 67–76.

    Article  CAS  PubMed  Google Scholar 

  95. Heinecke, J. W., Li, W., Mueller, D. M., Bohrer, A., and Turk, J. (1994) Cholesterol chlorohydrin synthesis by the myeloperoxidase-hydrogen peroxide-chloride system: potential markers for lipoproteins oxidatively damaged by phagocytes, Biochemistry, 33, 10127–10136.

    Article  CAS  PubMed  Google Scholar 

  96. Carr, A. C., van den Berg, J. J., and Winterbourn, C. C. (1996) Chlorination of cholesterol in cell membranes by hypochlorous acid, Arch. Biochem. Biophys., 332, 63–69.

    Article  CAS  PubMed  Google Scholar 

  97. Hazen, S. L., Hsu, F. F., Duffin, K., and Heinecke, J. W. (1996) Molecular chlorine generated by the myeloperoxi-dase-hydrogen peroxide-chloride system of phagocytes converts low density lipoprotein cholesterol into a family of chlorinated sterols, J. Biol. Chem., 271, 23080–23088.

    Article  CAS  PubMed  Google Scholar 

  98. Van den Berg, J. J., Winterbourn, C. C., and Kuypers, F. A. (1993) Hypochlorous acid-mediated modification of cholesterol and phospholipid: analysis of reaction products by gas chromatography-mass spectrometry, J. Lipid Res., 34, 2005–2012.

    CAS  PubMed  Google Scholar 

  99. Sergienko, V. I., Panasenko, O. M., and Murina, M. A. (1999) Development and introduction of electrochemical methods of detoxication in medicine, Efferent. Ter., 5,No.4, 8–17.

    Google Scholar 

  100. Vissers, M. C., Carr, A. C., and Chapman, A. L. (1998) Comparison of human red cell lysis by hypochlorous and hypobromous acids: insights into the mechanism of lysis, Biochem. J., 330, 131–138.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Panasenko, O. M. (1997). The mechanism of the hypochlorite-induced lipid peroxidation, Biofactors, 6, 181–190.

    Article  CAS  PubMed  Google Scholar 

  102. Stelmaszynska, T., Kukovetz, E., Egger, G., and Schaur, R. J. (1992) Possible involvement of myeloperoxidase in lipid peroxidation, Int. J. Biochem., 24, 121–128.

    Article  CAS  PubMed  Google Scholar 

  103. Evgina, S. A., Panasenko, O. M., Sergienko, V. I., and Vladimirov, Yu. A. (1992) Peroxidation of human plasma lipoproteins induced by hypochlorite, Biol. Membr. (Moscow), 6, 1247–1254.

    Google Scholar 

  104. Hazell, L. J., Davies, M. J., and Stocker, R. (1999) Secondary radicals derived from chloramines of apolipoprotein B-100 contribute to HOCl-induced lipid peroxidation of low-density lipoproteins, Biochem. J., 339, 489–495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Panasenko, O. M., Evgina, S. A., Aidyraliev, R. K., Sergienko, V. I., and Vladimirov, Yu. A. (1994) Peroxidation of human blood lipoproteins induced by exogenous hypochlorite or hypochlorite generated in the system of “myeloperoxidase + H2O2 + Cl-”, Free Radic. Biol. Med., 16, 143–148.

    Article  CAS  PubMed  Google Scholar 

  106. Panasenko, O. M., Evgina, S. A., Driomina, E. S., Sharov, V. S., Sergienko, V. I., and Vladimirov, Yu. A. (1995) Hypochlorite induces lipid peroxidation in blood lipopro-teins and phospholipid liposomes, Free Radic. Biol. Med., 19, 133–140.

    Article  CAS  PubMed  Google Scholar 

  107. Panasenko, O. M., Arnhold, J., Arnhold, K., Vladimirov, Iu. A., and Sergienko, V. I. (1996) Comparative study of the kinetics of phospholipid liposome peroxidation, induced by hypochlorite and in the Fe2+ + ascorbate system, Biofizika, 41, 334–341.

    CAS  PubMed  Google Scholar 

  108. Gorbatenkova, E. A., Artmann, G. M., and Panasenko, O. M. (2000) Hypochlorous acid and human blood low density lipoproteins modified by hypochlorous acid increase erythrocyte adhesion to endothelial cells, Membr. Cell Biol., 13, 537–546.

    CAS  PubMed  Google Scholar 

  109. Panasenko, O. M., Evgina, S. A., and Sergienko, V. I. (1993) Capacity of hypochlorite to penetrate into the lipid phase of human blood lipoproteins, Bull. Exp. Biol. Med., 115, 358–360.

    Article  CAS  Google Scholar 

  110. Panasenko, O. M., Panasenko, O. O., Briviba, K., and Sies, H. (1997) Hypochlorite destroys carotenoids in low density lipoproteins thus decreasing their resistance to per-oxidative modification, Biochemistry (Moscow), 62, 1140–1145.

    CAS  Google Scholar 

  111. Chekanov, A. V., Osipov, A. N., Vladimirov, Iu. A., Sergienko, V. I., and Panasenko, O. M. (2007) A comparative spin trapping study of hypobromous and hypochlorous acids interaction with tert-butyl hydroperoxide, Biofizika, 52, 5–13.

    CAS  PubMed  Google Scholar 

  112. Rice-Evans, C., Leake, D., Bruckdorfer, K. R., and Diplock, A. T. (1996) Practical approaches to low density lipoprotein oxidation: whys, wherefores and pitfalls, Free Radic. Res., 25, 285–311.

    Article  CAS  PubMed  Google Scholar 

  113. Osipov, A. N., Panasenko, O. M., Chekanov, A. V., and Arnhold, J. (2002) Interaction of tert-butyl hydroperoxide with hypochlorous acid. A spin trapping and chemilumi-nescence study, Free Radic. Res., 36, 749–754.

    Article  CAS  PubMed  Google Scholar 

  114. Panasenko, O. M., Osipov, A. N., Chekanov, A. V., Arnhold, J., and Sergienko, V. I. (2002) Peroxyl radical is produced upon the interaction of hypochlorite with tert-butyl hydroperoxide, Biochemistry (Moscow), 67, 880–888.

    Article  CAS  Google Scholar 

  115. Chekanov, A. V., Panasenko, O. M., Osipov, A. N., Arnhold, J., Kazarinov, K. D., Vladimirov, Iu. A., and Sergienko, V. I. (2002) Interaction of tert-butyl hydroperoxide with hypochlorite induces peroxyl radicals. A chemiluminescence study, Biofizika, 47, 787–794.

    CAS  PubMed  Google Scholar 

  116. Chekanov, A. V., Panasenko, O. M., Osipov, A. N., Matveeva, N. S., Kazarinov, K. D., Vladimirov, Iu. A., and Sergienko, V. I. (2005) The interaction of hypochlorite with fatty acid hydroperoxides results in the generation of free radicals, Biofizika, 50, 13–19.

    CAS  PubMed  Google Scholar 

  117. Panasenko, O. M., Chekanov, A. V., Arnhold, J., Sergienko, V. I., Osipov, A. N., and Vladimirov, Y. A. (2005) Generation of free radicals during decomposition of hydroperoxide in the presence of myeloperoxidase or activated neutrophils, Biochemistry (Moscow), 70, 998–1004.

    Article  CAS  Google Scholar 

  118. Chekanov, A. V., Osipov, A. N., Vladimirov, Yu. A., Sergienko, V. I., and Panasenko, O. M. (2006) Interaction of hypobromite with tert-butyl hydroperoxide. Role in phospholipid liposome peroxidation, Biol. Membr. (Moscow), 23, 426–432.

    CAS  Google Scholar 

  119. Noguchi, N., Nakada, A., Itoh, Y., Watanabe, A., and Niki, E. (2002) Formation of active oxygen species and lipid peroxidation induced by hypochlorite, Arch. Biochem. Biophys., 397, 440–447.

    Article  CAS  PubMed  Google Scholar 

  120. Miyamoto, S., Martinez, G. R., Rettori, D., Augusto, O., Medeiros, M. H. G., and Di Mascio, P. (2006) Linoleic acid hydroperoxide reacts with hypochlorous acid, generating peroxyl radical intermediates and singlet molecular oxygen, Proc. Natl. Acad. Sci. USA, 103, 293–298.

    Article  CAS  PubMed  Google Scholar 

  121. Crisby, M., Henareh, L., and Agewall, S. (2014) Relationship between oxidized LDL, IgM, and IgG autoantibodies to ox-LDL levels with recurrent cardiovascular events in Swedish patients with previous myocardial infarction, Angiology, 65, 932–936.

    Article  CAS  PubMed  Google Scholar 

  122. Holvoet, P., Vanhaecke, J., Janssens, S., Van de Werf, F., and Collen, D. (1998) Oxidized LDL and malondialde-hyde-modified LDL in patients with acute coronary syndromes and stable coronary artery disease, Circulation, 98, 1487–1489.

    Article  CAS  PubMed  Google Scholar 

  123. Osipov, A. N., Briukhanova, E. V., Vakhrusheva, T. V., Panasenko, O. M., and Vladimirov, Iu. A. (1997) Effect of hypochlorite and hydrogen peroxide on the ability of hemoglobin to stimulate lipid peroxidation of low-density lipoproteins, Biofizika, 42, 400–407.

    CAS  PubMed  Google Scholar 

  124. Yakutova, E. Sh., Dremina, Ye. S., Yevgina, S. A., Osipov, A. N., Sharov, V. S., Panasenko, O. M., and Vladimirov, Yu. A. (1994) Formation of free radicals on interaction of hypochlorite with iron (II) ions, Biophysics, 39, 241–245.

    Google Scholar 

  125. Savenkova, M. L., Mueller, D. M., and Heinecke, J. W. (1994) Tyrosyl radical generated by myeloperoxidase is a physiological catalyst for the initiation of lipid peroxidation in low density lipoprotein, J. Biol. Chem., 269, 20394–20400.

    CAS  PubMed  Google Scholar 

  126. Kawai, Y., Kiyokawa, H., Kimura, Y., Kato, Y., Tsuchiya, K., and Terao, J. (2006) Hypochlorous acid-derived modification of phospholipids: characterization of aminophos-pholipids as regulatory molecules for lipid peroxidation, Biochemistry, 45, 14201–14211.

    Article  CAS  PubMed  Google Scholar 

  127. Arnhold, J., Panasenko, O. M., Schiller, J., Vladimirov, Yu. A., and Arnold, K. (1995) The action of hypochlorous acid on phosphatidylcholine liposomes in dependence on the content of double bonds. Stoichiometry and NMR analysis, Chem. Phys. Lipids, 78, 55–64.

    Article  CAS  PubMed  Google Scholar 

  128. Panasenko, O. M., Arnhold, J., Vladimirov, Yu. A., Arnold, K., and Sergienko, V. I. (1997) Hypochlorite-induced peroxidation of egg yolk phosphatidylcholine is mediated by hydroperoxides, Free Radic. Res., 27, 1–12.

    Article  CAS  PubMed  Google Scholar 

  129. Richter, G., Schober, C., Suß, R., Fuchs, B., Birkemeyer, C., and Schiller, J. (2008) Comparison of the positive and negative ion electrospray ionization and matrix-assisted laser desorption ionization-time-of-flight mass spectra of the reaction products of phosphatidylethanolamines and hypochlorous acid, Anal. Biochem., 376, 157–159.

    Article  CAS  PubMed  Google Scholar 

  130. Carr, A. C., van den Berg, J. J., and Winterbourn, C. C. (1998) Differential reactivities of hypochlorous and hypo-bromous acids with purified Escherichia coli phospholipid: formation of haloamines and halohydrins, Biochim. Biophys. Acta, 1392, 254–264.

    Article  CAS  PubMed  Google Scholar 

  131. Tertov, V. V., Orekhov, A. N., Sobenin, I. A., Morrisett, J. D., Gotto, A. M., and Guevara, J. G., (1993) Carbohydrate composition of protein and lipid components in sialic acid-rich and -poor low-density lipoproteins from subjects with and without coronary artery disease, J. Lipid Res., 34, 365–375.

    CAS  PubMed  Google Scholar 

  132. Taniguchi, T., Ishikawa, Y., Tsunemitsu, M., and Fukuzaki, H. (1989) The structures of asparagine-linked sugar chains of human apolipoprotein B-100, Arch. Biochem. Biophys., 273, 197–205.

    Article  CAS  PubMed  Google Scholar 

  133. Prutz, W. A. (1996) Hypochlorous acid interactions with thiols, nucleotides, DNA, and other biological substrates, Arch. Biochem. Biophys., 332, 110–120.

    Article  CAS  PubMed  Google Scholar 

  134. Schiller, J., Arnhold, J., and Arnold, K. (1995) Action of hypochlorous acid on polymeric components of cartilage. Use of 13C NMR spectroscopy, Z. Naturforsch., 50, 721–728.

    Article  CAS  Google Scholar 

  135. Schiller, J., Arnhold, J., and Arnold, K. (1995) NMR studies of the action of hypochlorous acid on native pig articular cartilage, Eur. J. Biochem., 233, 672–676.

    Article  CAS  PubMed  Google Scholar 

  136. Hawkins, C. L., and Davies, M. J. (1998) Degradation of hyaluronic acid, poly- and monosaccharides, and model compounds by hypochlorite: evidence for radical intermediates and fragmentation, Free Radic. Biol. Med., 24, 1396–1410.

    Article  CAS  PubMed  Google Scholar 

  137. Rees, M. D., Hawkins, C. L., and Davies, M. J. (2003) Hypochlorite-mediated fragmentation of hyaluronan, chondroitin sulfates, and related N-acetyl glycosamines: evidence for chloramide intermediates, free radical transfer reactions, and site-specific fragmentation, J. Am. Chem. Soc., 125, 13719–13733.

    Article  CAS  PubMed  Google Scholar 

  138. Rees, M. D., Mcniven, T. N., and Davies, M. J. (2007) Degradation of extracellular matrix and its components by hypobromous acid, Biochem. J., 401, 587–596.

    Article  CAS  PubMed  Google Scholar 

  139. Rees, M. D., Hawkins, C. L., and Davies, M. J. (2004) Hypochlorite and superoxide radicals can act synergisti-cally to induce fragmentation of hyaluronan and chon-droitin sulphates, Biochem. J., 381, 175–184.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Rees, M. D., and Davies, M. J. (2006) Heparan sulfate degradation via reductive homolysis of its N-chloro-deriv-atives, Am. Chem. Soc., 128, 3085–3097.

    Article  CAS  Google Scholar 

  141. Tertov, V. V., Kaplun, V. V., Sobenin, I. A., and Orekhov, A. N. (1998) Low-density lipoprotein modification occurring in human plasma. Possible mechanism of in vivo lipopro-tein desialylation as a primary step of atherogenic modification, Atherosclerosis, 138, 183–195.

    Article  CAS  PubMed  Google Scholar 

  142. Sukhorukov, V. N., Karagodin, V. P., and Orekhov, A. N. (2016) Atherogenic modification of low-density lipopro-teins, Biomed. Khim., 62, 391–402.

    Article  CAS  PubMed  Google Scholar 

  143. Tertov, V. V., Nikonova, E. Y., Nifant’ev, N. E., Bovin, N. V., and Orekhov, A. N. (2002) Human plasma trans-siali-dase donor and acceptor specificity, Biochemistry (Moscow), 67, 908–913.

    Article  CAS  Google Scholar 

  144. Estrbauer, H., Puhl, H., Waeg, G., Krebs, A., Tatzber, F., and Rabol, H. (1993) Vitamin E and atherosclerosis - an overview, in Vitamin E (Mino, M., Nakamura, H., Diplock, A. T., and Keyden, H. J., eds.) Japan Scientific Societies Press, Tokyo, pp. 233–241.

    Google Scholar 

  145. Hazell, L. J., and Stocker, R. (1993) Oxidation of low-density lipoprotein with hypochlorite causes transformation of the lipoprotein into a high-uptake form for macrophages, Biochem. J., 290, 165–172.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Albrich, J. M., McCarthy, C. A., and Hurst, J. K. (1981) Biological reactivity of hypochlorous acid: implications for microbicidal mechanisms of leukocyte myeloperoxidase, Proc. Natl. Acad. Sci. USA, 78, 210–214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. Hazell, L. J., and Stocker, R. (1997) a-Tocopherol does not inhibit hypochlorite-induced oxidation of apolipopro-tein B-100 of low-density lipoprotein, FEBS Lett., 414, 541–544.

    Article  CAS  PubMed  Google Scholar 

  148. Panasenko, O. M., Evgina, S. A., and Sergienko, V. I. (1993) A spin-probe study of the structural change in human blood lipoproteins under the action of sodium hypochlorite, Bull. Exp. Biol. Med., 116, 153–155.

    CAS  Google Scholar 

  149. Panasenko, O. M. (1998) Hypochlorite and Oxidative Modification of Human Blood Lipoproteins: Ph. D. Thesis, Biological Sciences [in Russian], Research Institute of Physico-Chemical Medicine, Moscow.

    Google Scholar 

  150. Panasenko, O. M., Borin, M. L., Azizova, O. A., and Arnol’d, K. (1985) Determination of the surface charge of lipoproteins and its changes during lipid peroxidation, Biofizika, 30, 822–827.

    CAS  PubMed  Google Scholar 

  151. Panasenko, O. M., Evgina, S. A., Nikitin, S. V., and Sergienko, V. I. (1995) The effect of hypochlorite on electrical surface properties of human blood lipoproteins, Biofizika, 40, 545–550.

    CAS  PubMed  Google Scholar 

  152. Jerlich, A., Fabjan, J. S., Tschabuschnig, S., Smirnova, A. V., Horakova, L., Hayn, M., Auer, H., Guttenberger, H., Leis, H. J., Tatzber, F., Waeg, G., and Schaur, R. J. (1998) Human low density lipoprotein as a target of hypochlorite generated by myeloperoxidase, Free Radic. Biol. Med., 24, 1139–1148.

    Article  CAS  PubMed  Google Scholar 

  153. Panasenko, O. M., Melnichenko, A. A., Aksenov, D. V., Vakhrusheva, T. V., Suprun, I. V., Yanushevskaya, E. V., Vlasik, T. N., Sobenin, I. A., and Orekhov, A. N. (2004) Myeloperoxidase increases atherogenic potential of human blood low density lipoproteins by modifying their surface and lowering the resistance to association, Biol. Membr. (Moscow), 21, 498–505.

    CAS  Google Scholar 

  154. Guyton, J. R., and Klemp, K. F. (1994) Development of the atherosclerotic core region. Chemical and ultrastructural analysis of microdissected atherosclerotic lesions from human aorta, Arterioscler. Thromb., 14, 1305–1314.

    Article  CAS  PubMed  Google Scholar 

  155. Tirziu, D., Dobrian, A., Tasca, C., Simionescu, M., and Simionescu, N. (1995) Intimal thickenings of human aorta contain modified reassembled lipoproteins, Atherosclerosis, 112, 101–114.

    Article  CAS  PubMed  Google Scholar 

  156. O’Connell, A. M., Gieseg, S. P., and Stanley, K. K. (1994) Hypochlorite oxidation causes cross-linking of Lp(a), Biochim. Biophys. Acta, 1225, 180–186.

    Article  PubMed  Google Scholar 

  157. Panasenko, O. M., Azizova, O. A., Arnold, K., and Borin, M. L. (1987) Alterations of surface charges of plasma lipoproteins in ischemic heart disease, Biomed. Biochim. Acta, 46, 97–102.

    CAS  PubMed  Google Scholar 

  158. Carr, A. C., Myzak, M. C., Stocker, R., McCall, M. R., and Frei, B. (2000) Myeloperoxidase binds to low-density lipoprotein: potential implications for atherosclerosis, FEBS Lett., 487, 176–180.

    Article  CAS  PubMed  Google Scholar 

  159. Sokolov, A. V., Chekanov, A. V., Kostevich, V. A., Aksenov, D. V., Vasilyev, V. B., and Panasenko, O. M. (2011) Revealing binding sites for myeloperoxidase on the surface of human low density lipoproteins, Chem. Phys. Lipids, 164, 49–53.

    Article  CAS  PubMed  Google Scholar 

  160. Sokolov, A. V., Ageeva, K. V., Cherkalina, O. S., Pulina, M. O., Zakharova, E. T., Prozorovskii, V. N., Aksenov, D. V., Vasilyev, V. B., and Panasenko, O. M. (2010) Identification and properties of complexes formed by myeloperoxidase with lipoproteins and ceruloplasmin, Chem. Phys. Lipids, 163, 347–355.

    Article  CAS  PubMed  Google Scholar 

  161. Sokolov, A. V., Kostevich, V. A., Runova, O. L., Gorudko, I. V., Vasilyev, V. B., Cherenkevich, S. N., and Panasenko, O. M. (2014) Proatherogenic modification of LDL by surface-bound myeloperoxidase, Chem. Phys. Lipid, 180, 72–80.

    Article  CAS  Google Scholar 

  162. Segelmark, M., Persson, B., Hellmark, T., and Wieslander, J. (1997) Binding and inhibition of myeloperoxidase (MPO): a major function of ceruloplasmin? Clin. Exp. Immunol., 108, 167–174.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  163. Sokolov, A. V., Ageeva, K. V., Pulina, M. O., Cherkalina, O. S., Samygina, V. R., Vlasova, I. I., Panasenko, O. M., Zakharova, E. T., and Vasilyev, V. B. (2008) Ceruloplasmin and myeloperoxidase in complex affect the enzymatic properties of each other, Free Radic. Res., 42, 989–998.

    Article  CAS  PubMed  Google Scholar 

  164. Panasenko, O. M., Chekanov, A. V., Vlasova, I. I., Sokolov, A. V., Ageeva, K. V., Pulina, M. O., Cherkalina, O. S., and Vasil’ev, V. B. (2008) A study of the effect of ceruloplasmin and lactoferrin on the chlorination activity of leukocytic myeloperoxidase using the chemiluminescence method, Biophysics, 53, 268–272.

    Article  Google Scholar 

  165. Karakas, M., and Koenig, W. (2012) Myeloperoxidase production by macrophage and risk of atherosclerosis, Curr. Atheroscler. Rep., 14, 277–283.

    Article  CAS  PubMed  Google Scholar 

  166. Zhang, R., Brennan, M. L., Fu, X., Aviles, R. J., Pearce, G. L., Penn, M. S., Topol, E. J., Sprecher, D. L., and Hazen, S. L. (2001) Association between myeloperoxidase levels and risk of coronary artery disease, JAMA, 286, 2136–2142.

    Article  CAS  PubMed  Google Scholar 

  167. Chen, L. Q., Rohatgi, A., Ayers, C. R., Das, S. R., Khera, A., Berry, J. D., McGuire, D. K., de and Lemos, J. A. (2011) Race-specific associations of myeloperoxidase with atherosclerosis in a population-based sample: the Dallas Heart Study, Atherosclerosis, 219, 833–838.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  168. Karakas, M., Koenig, W., Zierer, A., Herder, C., Rottbauer, W., Baumert, J., Meisinger, C., and Thorand, B. (2012) Myeloperoxidase is associated with incident coronary heart disease independently of traditional risk factors: results from the MONICA/KORA Augsburg study, J. Intern. Med., 271, 43–50.

    Article  CAS  PubMed  Google Scholar 

  169. Sugiyama, S., Okada, Y., Sukhova, G. K., Virmani, R., Heinecke, J. W., and Libby, P. (2001) Macrophage myeloperoxidase regulation by granulocyte macrophage colony-stimulating factor in human atherosclerosis and implications in acute coronary syndromes, Am. J. Pathol., 158, 879–891.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  170. Cheng, M. L., Chen, C. M., Gu, P. W., Ho, H. Y., and Chiu, D. T. (2008) Elevated levels of myeloperoxidase, white blood cell count and 3-chlorotyrosine in Taiwanese patients with acute myocardial infarction, Clin. Biochem., 41, 554–560.

    Article  CAS  PubMed  Google Scholar 

  171. Ho, H. Y., Cheng, M. L., Chen, C. M., Gu, P. W., Wang, Y. L., Li, J. M., and Chiu, D. T. (2008) Oxidative damage markers and antioxidants in patients with acute myocardial infarction and their clinical significance, Biofactors, 34, 135–145.

    Article  CAS  PubMed  Google Scholar 

  172. Hazen, S. L., and Heinecke, J. W. (1997) 3-Chlorotyrosine, a specific marker of myeloperoxidase-cat-alyzed oxidation, is markedly elevated in low density lipoprotein isolated from human atherosclerotic intima, J. Clin. Invest., 99, 2075–2081.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  173. Hazen, S. L., Crowley, J. R., Mueller, D. M., and Heinecke, J. W. (1997) Mass spectrometric quantification of 3-chlorotyrosine in human tissues with attomole sensitivity: a sensitive and specific marker for myeloperoxidase-catalyzed chlorination at sites of inflammation, Free Radic. Biol. Med., 23, 909–916.

    Article  CAS  PubMed  Google Scholar 

  174. Bergt, C., Pennathur, S., Fu, X., Byun, J., O’Brien, K., McDonald, T. O., Singh, P., Anantharamaiah, G. M., Chait, A., Brunzell, J., Geary, R. L., Oram, J. F., and Heinecke, J. W. (2004) The myeloperoxidase product hypochlorous acid oxidizes HDL in the human artery wall and impairs ABCA1-dependent cholesterol transport, Proc. Natl. Acad. Sci. USA, 101, 13032–13037.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  175. Pennathur, S., Bergt, C., Shao, B., Byun, J., Kassim, S. Y., Singh, P., Green, P. S., McDonald, T. O., Brunzell, J., Chait, A., Oram, J. F., O’brien, K., Geary, R. L., and Heinecke, J. W. (2004) Human atherosclerotic intima and blood of patients with established coronary artery disease contain high density lipoprotein damaged by reactive nitrogen species, J. Biol. Chem., 279, 42977–42983.

    Article  CAS  PubMed  Google Scholar 

  176. Zheng, L., Nukuna, B., Brennan, M. L., Sun, M., Goormastic, M., Settle, M., Schmitt, D., Fu, X., Thomson, L., Fox, P. L., Ischiropoulos, H., Smith, J. D., Kinter, M., and Hazen, S. L. (2004) Apolipoprotein A-I is a selective target for myeloperoxidase-catalyzed oxidation and functional impairment in subjects with cardiovascular disease, J. Clin. Invest., 114, 529–541.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  177. Rudolph, V., Andrie, R. P., Rudolph, T. K., Friedrichs, K., Klinke, A., Hirsch-Hoffmann, B., Schwoerer, A. P., Lau, D., Fu, X., Klingel, K., Sydow, K., Didie, M., Seniuk, A., von Leitner, E. C., Szoecs, K., Schrickel, J. W., Treede, H., Wenzel, U., Lewalter, T., Nickenig, G., Zimmermann, W. H., Meinertz, T., Boger, R. H., Reichenspurner, H., Freeman, B. A., Eschenhagen, T., Ehmke, H., Hazen, S. L., Willems, S., and Baldus, S. (2010) Myeloperoxidase acts as a profibrotic mediator of atrial fibrillation, Nat. Med., 16, 470–474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  178. Malle, E., Hazell, L., Stocker, R., Sattler, W., Esterbauer, H., and Waeg, G. (1995) Immunologic detection and measurement of hypochlorite-modified LDL with specific monoclonal antibodies, Arterioscler. Thromb. Vasc. Biol., 15, 982–989.

    Article  CAS  PubMed  Google Scholar 

  179. Hazell, L. J., Arnold, L., Flowers, D., Waeg, G., Malle, E., and Stocker, R. (1996) Presence of hypochlorite-mod-ified proteins in human atherosclerotic lesions, J. Clin. Invest., 97, 1535–1544.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  180. Hazell, L. J., Baernthaler, G., and Stocker, R. (2001) Correlation between intima-to-media ratio, apolipopro-tein B-100, myeloperoxidase, and hypochlorite-oxidized proteins in human atherosclerosis, Free Radic. Biol. Med., 31, 1254–1262.

    Article  CAS  PubMed  Google Scholar 

  181. Jerlich, A., Pitt, A. R., Schaur, R. J., and Spickett, C. M. (2000) Pathways of phospholipid oxidation by HOCl in human LDL detected by LC-MS, Free Radic. Biol. Med., 28, 673–682.

    Article  CAS  PubMed  Google Scholar 

  182. Messner, M. C., Albert, C. J., McHowat, J., and Ford, D. A. (2008) Identification of lysophosphatidylcholine-chlorohydrin in human atherosclerotic lesions, Lipids, 43, 243–249.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  183. Domigan, N. N., Carr, A. C., Lewis, J. G., Elder, P. A., and Winterbourn, C. C. (1997) A monoclonal antibody recognizing the chlorohydrin derivates of oleic acid for probing hypochlorous acid involvement in tissue injury, Redox Rep., 3, 111–117.

    Article  CAS  PubMed  Google Scholar 

  184. Thukkani, A. K., Martinson, B. D., Albert, C. J., Vogler, G. A., and Ford, D. A. (2005) Neutrophil-mediated accumulation of 2-ClHDA during myocardial infarction: 2-ClHDA-mediated myocardial injury, Am. J. Physiol. Heart Circ. Physiol., 288, H2955–H2964.

    Article  CAS  PubMed  Google Scholar 

  185. Takeshita, J., Byun, J., Nhan, T. Q., Pritchard, D. K., Pennathur, S., Schwartz, S. M., Chait, A., and Heinecke, J. W. (2006) Myeloperoxidase generates 5-chlorouracil in human atherosclerotic tissue: a potential pathway for somatic mutagenesis by macrophages, J. Biol. Chem., 281, 3096–3104.

    Article  CAS  PubMed  Google Scholar 

  186. Sokolov, A. V., Kostevich, V. A., Vasilyev, V. B., and Panasenko, O. M. (2018) Hypohalous acids modified lipoproteins as biomarkers of halogenative stress at cardiovascular diseases, in Molecular, Membrane and Cellular Basis of Biosystem Functioning (Volotovsky, I. D., ed.) Izdvo BGU, Minsk, p. 171.

    Google Scholar 

  187. Sokolov, A. V., Kostevich, V. A., Gorbunov, N. V., Grigorieva, D. V., Gorudko, I. V., Vasilyev, V. B., and Panasenko, O. M. (2018) A link between active myeloper-oxidase and chlorinated ceruloplasmin in blood plasma of patients with cardiovascular diseases, Med. Immunol. (Russia), 20, 699–710.

    Article  Google Scholar 

  188. Liu, L., Wang, Y. X., Zhou, J., Long, F., Sun, H. W., Liu, Y., Chen, Y. Z., and Jiang, C. L. (2005) Rapid non-genomic inhibitory effects of glucocorticoids on human neutrophil degranulation, Inflamm. Res., 54, 37–41.

    Article  CAS  PubMed  Google Scholar 

  189. Vlasova, I. I., Arnhold, J., Osipov, A. N., and Panasenko, O. M. (2006) pH-dependent regulation of myeloperoxi-dase activity, Biochemistry (Moscow), 71, 667–677.

    Article  CAS  Google Scholar 

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Funding

Funding The authors’ studies cited in this review were supported by the Russian Foundation for Basic Research (projects 17-04-00530 and 18-515-00004) and Russian Science Foundation (project 17-75-30064).

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Authors and Affiliations

  1. Federal Research and Clinical Center of Physico-Chemical Medicine, Federal Medical Biological Agency, 119435, Moscow, Russia

    O. M. Panasenko, T. I. Torkhovskaya & A. V. Sokolov

  2. Orekhovich Institute of Biomedical Chemistry, 119121, Moscow, Russia

    T. I. Torkhovskaya

  3. Belarusian State University, 220030, Minsk, Belarus

    I. V. Gorudko

  4. Institute of Experimental Medicine, 197376, St. Petersburg, Russia

    A. V. Sokolov

Authors
  1. O. M. Panasenko
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  2. T. I. Torkhovskaya
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  3. I. V. Gorudko
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  4. A. V. Sokolov
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Correspondence to O. M. Panasenko.

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Compliance with ethical standards. This article does not contain any studies involving animals or human participants performed by any of the authors.

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Russian Text © The Author(s), 2020, published in Uspekhi Biologicheskoi Khimii, 2020, Vol. 60, pp. 75-122.

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Panasenko, O.M., Torkhovskaya, T.I., Gorudko, I.V. et al. The Role of Halogenative Stress in Atherogenic Modification of Low-Density Lipoproteins. Biochemistry Moscow 85 (Suppl 1), 34–55 (2020). https://doi.org/10.1134/S0006297920140035

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  • DOI: https://doi.org/10.1134/S0006297920140035

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