Differences in structural changes and pathophysiologic effects of low-density lipoproteins upon accumulation of acylhydroperoxy derivatives in their outer phospholipid monolayer or upon chemical modification of apoprotein b-100 by natural dicarbonyl
- Authors: Lankin V.Z1, Tikhaze A.K1, Konovalova G.G1
-
Affiliations:
- National Medical Research Center of Cardiology named after Academician E. I. Chazov, Ministry of Health of Russia
- Issue: Vol 88, No 11 (2023)
- Pages: 2314-2325
- Section: Regular articles
- URL: https://rjeid.com/0320-9725/article/view/665514
- DOI: https://doi.org/10.31857/S0320972523110209
- EDN: https://elibrary.ru/MNINOG
- ID: 665514
Cite item
Abstract
Nanoparticles of the lipid-transporting system of the organism - low-density lipoproteins (LDL) of blood plasma are easily subjected to free radical peroxidation with formation of their main modified forms - oxidized LDL itself (containing hydroperoxy-acyls in phospholipids of the outer layer of particles) and dicarbonyl-modified LDL (apoprotein B-100 of which was chemically modified by the Maillard reaction). Based on the study of free radical oxidation kinetics of LDL, it was found that the existing in the literature designation “oxidized lipoproteins” is incorrect because it does not reveal the nature of oxidative modification of LDL. It is shown that “atherogenic” LDL (particles of which are actively captured by cultured macrophages) are not the oxidized LDL (in which LOOH-derivatives of phospholipids are formed by enzymatic oxidation of of C-15 lipoxygenase of rabbit reticulocytes), but dicarbonyl-modified LDL. The important role of dicarbonyl-modified LDL in the molecular mechanisms of atherogenesis and endothelial dysfunction is discussed.
About the authors
V. Z Lankin
National Medical Research Center of Cardiology named after Academician E. I. Chazov, Ministry of Health of Russia
Email: lankin0309@mail.ru
121552 Moscow, Russia
A. K Tikhaze
National Medical Research Center of Cardiology named after Academician E. I. Chazov, Ministry of Health of Russia121552 Moscow, Russia
G. G Konovalova
National Medical Research Center of Cardiology named after Academician E. I. Chazov, Ministry of Health of Russia121552 Moscow, Russia
References
- Steinbrecher, U. P., Parthasarathy, S., Leake, D. S., Witztum, J. L., and Steinberg, D. (1984) Modification of low density lipoprotein by cells involves lipid peroxidation and degradation low density lipoprotein phospholipids, Proc. Natl. Acad. Sci. USA, 81, 3883-3887, doi: 10.1073/pnas.81.12.3883.
- Steinberg, D., Parthasarathy, S., Carew, T. E., Khoo, J. C., and Witztum, J. L. (1989) Beyond cholesterol. Modification of low density lipoprotein that increase its atherogenicity, New Engl. J. Med., 320, 915-924, doi: 10.1056/NEJM198904063201407.
- Kita, T., Ishii, K., Yokode, M., Kume, N., Nagano, Y., Arai, H., and Kawai, C. (1990) The role of oxidized low density lipoprotein in the pathogenesis of atherosclerosis, Eur. Heart J., 11, 122-127, doi: 10.1093/eurheartj/11.suppl_e.122.
- Witztum, J. L., and Steinberg, D. (1991) Role of oxidized low-density lipoprotein in atherogenesis, J. Clin. Invest., 88, 1785-1792, doi: 10.1172/JCI115499.
- Yla-Herttuala, S. (1994) Role of lipid and lipoprotein oxidation in the pathogenesis of atherosclerosis, Drugs Today, 30, 507-514.
- Lankin, V. Z., and Tikhaze, A. K. (2003) Atherosclerosis as a free radical pathology and antioxidative therapy of this disease, in: Free radicals, NO and Inflammation, IOS Press, Amsterdam, 344, pp. 218-231.
- Lankin, V. Z., and Tikhaze, A. K. (2017) Role of oxidative stress in the genesis of atherosclerosis and diabetes mellitus: a personal look back on 50 years of research, Curr. Aging Sci., 10, 18-25, doi: 10.2174/1874609809666160926142640.
- Lankin, V. Z., Tikhaze, A. K., and Melkumyants, A. M. (2022) Dicarbonyl-dependent modification of LDL as a key factor of endothelial dysfunction and atherosclerotic vascular wall damage, Antioxidants, 11, 1565, doi: 10.3390/antiox11081565.
- Lankin, V. Z., Tikhaze, A. K., and Melkumyants, A. M. (2023) Malondialdehyde as an important key factor of molecular mechanisms of vascular wall damage under heart diseases development, Int. J. Mol. Sci., 24, 128, doi: 10.3390/ijms24010128.
- Lankin, V. Z., Tikhaze, A. K., and Kosach, V. Ya. (2022) Comparative susceptibility to oxidation of different classes of blood plasma lipoproteins, Biochemistry (Moscow), 87, 1335-1341, doi: 10.1134/S0006297922110128.
- Milne, G. L., Seal, J. R., Havrilla, C. M., Wijtmans, M., and Porter, N. A. (2005) Identification and analysis of products formed from phospholipids in the free radical oxidation of human low density lipoproteins, J. Lipid Res., 46, 307-319, doi: 10.1194/jlr.M400311-JLR200.
- Noguchi, N., Numano, R., Kaneda, H., and Niki, E. (1998) Oxidation of lipids in low density lipoprotein particles, Free Radic. Res., 29, 43-52, doi: 10.1080/10715769800300061.
- Эмануэль Н. М., Денисов Е. Т., Майзус З. К. (1965) Цепные реакции окисления углеводородов в жидкой фазе, Наука, Москва, с. 375.
- Lankin, V. Z., Tikhaze, A. K., and Osis, Yu. G. (2002) Modeling the cascade of enzymatic reactions in liposomes including successive free radical peroxidation, reduction, and hydrolysis of phospholipid polyenoic acyls for studying the effect of these processes on the structuraldynamic parameters of the membranes, Biochemistry (Moscow), 67, 566-574, doi: 10.1023/a:1015502429453.
- Estévez, M., Padilla, P., Carvalho, L., Martín, L., Carrapiso, A., and Delgado, J. (2019) Malondialdehyde interferes with the formation and detection of primary carbonyls in oxidized proteins, Redox Biol., 26, 101277, doi: 10.1016/j.redox.2019.101277.
- Tertov, V. V., Kaplun, V. V., Dvoryantsev, S. N., and Orekhov, A. N. (1995) Apolipoprotein B-bound lipids as a marker for evaluation of low density lipoprotein oxidation in vivo, Biochem. Biophys. Res. Commun., 214, 608-613, doi: 10.1006/bbrc.1995.2329.
- Schewe, T., Wiesncr, R., and Rapoport, S. M. (1981) Lipoxygenase from rabbit reticulocytes, Methods Enzymol., 71, 430-441, doi: 10.1016/0076-6879(81)71054-1.
- Requena, J. R., Fu, M. X., Ahmed, M. U., Jenkins, A. J., Lyons, T. J., Baynes, J. W., and Thorpe, S. R. (1997) Quantification of malondialdehyde and 4-hydroxynonenal adducts to lysine residues in native and oxidized human low-density lipoprotein, Biochem. J., 322, 317-325, doi: 10.1042/bj3220317.
- Fogelman, A. M., Shechter, I., Seager, J., Hokom, M., Child, J. S., and Edwards, P. A. (1980) Malondialdehyde alteration of low density lipoproteins leads to cholesteryl ester accumulation in human monocyte-macrophages, Proc. Natl. Acad. Sci. USA, 77, 2214-2218, doi: 10.1073/pnas.77.4.2214.
- Sigurdardottir, V., Fagerberg, B., and Hulthe, J. (2002) Circulating oxidized low-density lipoprotein (LDL) is associated with risk factors of the metabolic syndrome and LDL size in clinically healthy 58 year old men (AIR Study), J. Int. Med., 252, 440-447, doi: 10.1046/j.1365-2796.2002.01054.x.
- Lankin, V. Z., Konovalova, G. G., Domogatsky, S. P., Tikhaze, A. K., Klots, I. N., and Ezhov, M. V. (2023) Clearance and utilization of dicarbonyl-modified LDL in monkeys and humans, Int. J. Mol. Sci., 24, 10471, doi: 10.3390/ijms241310471.
- Schalkwijk, C. G., Vermeer, M. A., Stehouwer, C. D., te Koppele, J., Princen, H. M., and van Hinsbergh, V. W. (1998) Effect of methylglyoxal on the physico-chemical and biological properties of low-density lipoprotein, Biochim. Biophys. Acta, 1394, 187-198, doi: 10.1016/s0005-2760(98)00112-x.
- Patel, R. P., and Darley-Usmar, V. (1999) Molecular mechanisms of the copper dependent oxidation of low-density lipoprotein, Free Radic. Res., 30, 1-9, doi: 10.1080/10715769900300011.
- Lankin, V. Z., Konovalova, G. G., Tikhaze, A. K., Shumaev, K. B., Kumskova, E. M., and Viigimaa, M. (2014) The initiation of the free radical peroxidation of low-density lipoproteins by glucose and its metabolite methylglyoxal: a common molecular mechanism of vascular wall injures in atherosclerosis and diabetes, Mol. Cell. Biochem., 395, 241-252, doi: 10.1007/s11010-014-2131-2.
- Caldiroli, A., Auxilia, A. M., Capuzzi, E., Clerici, M., and Buoli, M. (2020) Malondialdehyde and bipolar disorder: A short comprehensive review of available literature, J. Affect Disord., 274, 31-37, doi: 10.1016/j.jad.2020.05.001.
- Bilenko, M. V., Khil'chenko, A. V., Konovalova, G. G., and Lankin, V. Z. (2003) Effect of antioxidant probucol on cell-mediated LDL oxidation in vitro and in vivo, Bull. Exp. Biol. Med., 136, 126-128, doi: 10.1023/a:1026398319379.
- 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, Lab. Invest., 67, 665-675.
- Hara, A., and Radin, N. S. (1978) Lipid extraction of tissues with a low-toxicity solvent, Anal. Biochem., 90, 420-426, doi: 10.1016/0003-2697(78)90046-5.
- Lankin, V., Viigimaa, M., Tikhaze, A., Kumskova, E., Konovalova, G., Abina, J., Zemtsovskaya, G., Kotkina, T., Yanushevskaya, E., and Vlasik, T. (2011) Cholesterol-rich low density lipoproteins are also more oxidized, Mol. Cell. Biochem., 355, 187-191, doi: 10.1007/s11010-011-0853-y.
- Viigimaa, M., Abina, J., Zemtsovskaya, G., Tikhaze, A., Konovalova, G., Kumskova, E., and Lankin, V. (2010) Malondialdehyde - modified low-density lipoproteins as biomarker for atherosclerosis, Blood Press, 19, 164-168, doi: 10.3109/08037051.2010.484158.
- Galle, J., Schneider, R., Heinloth, A., Wanner, C., Galle, P. R., Conzelmann, E., Dimmeler, S., and Heermeier, K. (1999) Lp(a) and LDL induce apoptosis in human endothelial cells and in rabbit aorta: role of oxidative stress, Kidney Int., 55, 1450-1461, doi: 10.1046/j.1523-1755.1999.00351.x.
- Zhao, R., Ma, X., Xie, X., and Shen, G. X. (2009) Involvement of NADPH oxidase in oxidized LDL-induced upregulation of heat shock factor-1 and plasminogen activator inhibitor-1 in vascular endothelial cells, Am. J. Physiol. Endocrinol. Metab., 297, E104-E111, doi: 10.1152/ajpendo.91023.2008.
- Furman, C., Martin-Nizard, F., Fruchart, J. C., Duriez, P., and Teissier, E. (1999) Differential toxicities of air (mO-LDL) or copper-oxidized LDLs (Cu-LDL) toward endothelial cells, J. Biochem. Mol. Toxicol., 13, 316-323, doi: 10.1002/(sici)1099-0461(1999)13:6<316::aid-jbt5>3.0.co;2-o.
- Sangle, G. V., Zhao, R., and Shen, G. X. (2008) Transmembrane signaling pathway mediates oxidized low-density lipoprotein-induced expression of plasminogen activator inhibitor-1 in vascular endothelial cells, Am. J. Physiol. Endocrinol. Metab., 295, E1243-E1254, doi: 10.1152/ajpendo.90415.2008.
- Lankin, V. Z., Antonovsky, V. L., and Tikhaze, A. K. (2004) Regulation of free radical lipoperoxidation and organic peroxides metabolism during normal station and pathologies, in Peroxides at the Beginning of the Third Millennium: Synthesis, Properties, Application, Nova Science Publishers, Inc., NY, pp. 85-111.
- Lankin, V. Z., Tikhaze, A. K., Kapel'ko, V. I., Shepel'kova, G. S., Shumaev, K. B., Panasenko, O. M., Konovalova, G. G., and Belenkov, Y. N. (2007) Mechanisms of oxidative modification of low density lipoproteins under conditions of oxidative and carbonyl stress, Biochemistry (Moscow), 72, 1081-1090, doi: 10.1134/S0006297907100069.
- Lankin, V. Z., Tikhaze, A. K., Konovalova, G. G., Kumskova, E. M., and Shumaev, K. B. (2010) Aldehyde-dependent modification of low density lipoproteins, in Handbook of Lipoprotein Research, Nova Science Publishers, Inc., NY, pp. 85-107.
- Lankin, V. Z., Shumaev, K. B., Tikhaze, A. K., and Kurganov, B. I. (2017) Influence of dicarbonyls on kinetic characteristics of glutathione peroxidase, Dokl. Biochem. Biophys., 475, 287-290, doi: 10.1134/S1607672917040123.
- Sharapov, M. G., Gudkov, S. V., Lankin, V. Z., and Novoselov, V. I. (2021) Role of glutathione peroxidases and peroxiredoxins in free radical-induced pathologies, Biochemistry (Moscow), 86, 1418-1433, doi: 10.1134/S0006297921110067.
- Lankin, V. Z., Konovalova, G. G., Tikhaze, A. K., Shumaev, K. B., Belova (Kumskova), E. M., Grechnikova, M. A., and Viigimaa, M. (2016) Aldehyde inhibition of antioxidant enzymes in the blood of diabetic patients, J. Diabetes, 8, 398-404, doi: 10.1111/1753-0407.12309.
- Lankin, V. Z., Sharapov, M. G., Goncharov, R. G., Tikhaze, A. K., and Novoselov, V. I. (2019) Natural dicarbonyls inhibit peroxidase activity of peroxiredoxins, Dokl. Biochem. Biophys., 485, 132-134, doi: 10.1134/S1607672919020157.
- Yu, X. H., Fu, Y. C., Zhang, D. W., Yin, K., and Tang, C. K. (2013) Foam cells in atherosclerosis, Clin. Chim. Acta, 424, 245-252, doi: 10.1016/j.cca.2013.06.006.
- Estruch, M., Sanchez-Quesada, J. L., Ordonez Llanos, J., and Benitez, S. (2013) Electronegative LDL: a circulating modified LDL with a role in inflammation, Mediat. Inflamm., 2013, 181324, doi: 10.1155/2013/181324.
- Puig, N., Montolio, L., Camps-Renom, P., Navarra, L., Jiménez-Altayó, F., Jiménez- Xarrié, E., Sánchez-Quesada, J. L., and Benitez, S. (2020) Electronegative LDL promotes inflammation and triglyceride accumulation in macrophages, Cells, 9, 583, doi: 10.3390/cells9030583.
- Pirillo, A., Norata, G. D., and Catapano, A. L. (2013) LOX-1, OxLDL, and atherosclerosis, Mediat. Inflamm., 2013, 152786, doi: 10.1155/2013/152786.
- Lubrano, V., and Balzan, S. (2014) LOX-1 and ROS, inseparable factors in the process of endothelial damage, Free Radic. Res., 48, 841-848, doi: 10.3109/10715762.2014.929122.
- Kattoor, A. J., Kanuri, S. H., and Mehta, J. L. (2019) Role of Ox-LDL and LOX-1 in atherogenesis, Curr. Med. Chem., 26, 1693-1700, doi: 10.2174/0929867325666180508100950.
- Akhmedov, A., Sawamura, T., Chen, C. H., Kraler, S., Vdovenko, D., and Lüscher, T. F. (2021) Lectin - like oxidized low-density lipoprotein receptor-1 (LOX-1): a crucial driver of atherosclerotic cardiovascular disease, Eur. Heart J., 42, 1797-1807, doi: 10.1093/eurheartj/ehaa770.
- Duprat, F., Robles, C., Castillo, M. P., Rivas, Y., Mondaca, M., Jara, N., Roa, F., Bertinat, R., Toledo, J., Paz, C., and González-Chavarría, I. (2023) LOX-1 activation by oxLDL induces AR and AR-V7 expression via NF-κB and STAT3 signaling pathways reducing enzalutamide cytotoxic effects, Int. J.Mol. Sci., 24, 5082, doi: 10.3390/ijms24065082.
- Ланкин В. З., Шарапов М. Г., Гончаров Р. Г., Антонова О. А., Коновалова Г. Г., Тихазе А. К., Косач В. Я. (2023) Молекулярные механизмы повреждения стенки сосудов и дисфункции эндотелия. Обоснование новых подходов к антиоксидантной терапии. Тезисы конф. "Кардиология на марше", Кардиологический вестник (спец. выпуск), 16-17.
- Galvani, S., Coatrieux, C., Elbaz, M., Grazide, M. H., Thiers, J. C., Parini, A., Uchida, K., Kamar, N., Rostaing, L., Baltas, M., Salvayre, R., and Nègre-Salvayre, A. (2008) Carbonyl scavenger and antiatherogenic effects of hydrazine derivatives, Free. Radic. Biol. Med., 45, 1457-1467, doi: 10.1016/j.freeradbiomed.2008.08.026.
- Belkheiri, N., Bouguerne, B., Bedos-Belval, F., Duran, H., Bernis, C., Salvayre, R., Nègre-Salvayre, A., and Baltas, M. (2010) Synthesis and antioxidant activity evaluation of a syringic hydrazones family, Eur. J. Med. Chem., 45, 3019-3026, doi: 10.1016/j.ejmech.2010.03.031.
Supplementary files
