Дикарбонил-модифицированные липопротеиды низкой плотности - ключевые индукторы экспрессии генов LOX-1 и NOX1 в культивируемых эндотелиоцитах пупочной вены человека

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Аннотация

Впервые исследована экспрессия генов LOX-1 (лектин-подобного рецептора-1 для окисленных липопротеидов низкой плотности) и NOX1 (NADPH-оксидазы 1) в эндотелиоцитах пупочной вены человека (HUVECs) при культивировании в присутствии липопротеидов низкой плотности (ЛНП), модифицированных различными природными дикарбонилами. Установлено, что из исследованных дикарбонил-модифицированных ЛНП (модифицированные малоновым диальдегидом (МДА) ЛНП, глиоксаль-модифицированные ЛНП и метилглиоксаль-модифицированные ЛНП) наибольшую индукцию генов LOX-1 и NOX1, а также генов антиоксидантных ферментов и проапоптотических факторов в HUVECs вызывают МДА-модифицированные ЛНП. Обсуждается важная роль дикарбонил-модифицированных ЛНП в молекулярных механизмах повреждения стенки сосудов и дисфункции эндотелия.

Об авторах

В. З Ланкин

ФГБУ «НМИЦ кардиологии имени академика Е.И. Чазова» Минздрава России

121552 Москва, Россия

М. Г Шарапов

ФИЦ «Пущинский научный центр биологических исследований РАН», Институт биофизики клетки РАН

Email: sharapov.mg@yandex.ru
142290 Пущино, Московская обл., Россия

А. К Тихазе

ФГБУ «НМИЦ кардиологии имени академика Е.И. Чазова» Минздрава России

121552 Москва, Россия

Р. Г Гончаров

ФИЦ «Пущинский научный центр биологических исследований РАН», Институт биофизики клетки РАН

142290 Пущино, Московская обл., Россия

О. А Антонова

ФГБУ «НМИЦ кардиологии имени академика Е.И. Чазова» Минздрава России

121552 Москва, Россия

Г. Г Коновалова

ФГБУ «НМИЦ кардиологии имени академика Е.И. Чазова» Минздрава России

121552 Москва, Россия

В. И Новоселов

ФИЦ «Пущинский научный центр биологических исследований РАН», Институт биофизики клетки РАН

142290 Пущино, Московская обл., Россия

Список литературы

  1. Гончаров Р. Г., Шарапов М. Г. (2023) Ишемически-реперфузионные поражения: молекулярные механизмы патогенеза и способы их коррекции, Мол. Биол., 6, 1150-1174, doi: 10.31857/S0026898423060071.
  2. Dubois-Deruy, E., Peugnet, V., Turkieh, A., and Pinet, F. (2020) Oxidative stress in cardiovascular diseases, Antioxidants (Basel), 9, 864, doi: 10.3390/antiox9090864.
  3. Lankin, V. Z., and Tikhaze, A. K. (2003) Atherosclerosis as a free radical pathology and antioxidative therapy of this disease, Free Radicals NO and Inflammation, IOS Press, Amsterdam etc., 344, 218-231.
  4. 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.
  5. 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 (Basel), 11, 1565, doi: 10.3390/antiox11081565.
  6. 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.
  7. Spiteller, G. (2008) Peroxyl radicals are essential reagents in the oxidation steps of the Maillard reaction leading to generation of advanced glycation end products, Ann. NY Acad. Sci., 1126, 128-133, doi: 10.1196/annals.1433.031.
  8. Lankin, V. Z., Shadyro, O. I., Shumaev, K. B., Tikhaze, A. K., and Sladkova, A. A. (2019) Non-enzymatic methylglyoxal formation from glucose metabolites and generation of superoxide anion radical during methylglyoxal-dependend cross-links reaction, J. Antioxidant Activity, 1, 34-45, doi: 10.14302/issn.2471-2140.jaa-19-2997.
  9. 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.
  10. 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.
  11. Sharapov, M. G., Gudkov, S. V., and Lankin, V. Z. (2021) Hydroperoxide reducing enzymes in the regulation of free radical processes, Biochemistry (Moscow), 86, 1256-1274, doi: 10.1134/S0006297921100084.
  12. 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.
  13. Yla-Herttuala, S. (1994) Role of lipid and lipoprotein oxidation in the pathogenesis of atherosclerosis, Drugs Today, 30, 507-514.
  14. Steinberg, D. (1995) Role of oxydized LDL and antioxidants in atherosclerosis, Adv. Exp. Med. Biol., 369, 39-48, doi: 10.1007/978-1-4615-1957-7_5.
  15. 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.
  16. 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.
  17. Sharapov, M. G., Goncharov, R. G., Gordeeva, A. E., Novoselov, V. I., Antonova, O. A., Tikhaze, A. K., and Lankin, V. Z. (2016) Enzymatic antioxidant system of endotheliocytes, Dokl. Biochem. Biophys., 471, 410-412, doi: 10.1134/S1607672916060090.
  18. 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.
  19. Rubio-Gayosso, I., Platts, S. H., and Duling, B. R. (2006) Reactive oxygen species mediate modification of glycocalyx during ischemia-reperfusion injury, Am. J. Physiol. Heart Circ. Physiol., 290, H2247-H2256, doi: 10.1152/ajpheart.00796.2005.
  20. Pirillo, A., Norata, G. D., and Catapano, A. L. (2013) LOX-1, OxLDL, and atherosclerosis, Mediat. Inflamm., 2013, 152786, doi: 10.1155/2013/152786.
  21. 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.
  22. Chistiakov, D. A., Orekhov, A. N., and Bobryshev, Yu. V. (2016) LOX-1-mediated effects on vascular cells in atherosclerosis, Cell. Physiol. Biochem., 38, 1851-1859, doi: 10.1159/000443123.
  23. 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.
  24. 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.
  25. 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.
  26. Lankin, V. Z., Tikhaze, A. K., and Kumskova, E. M. (2012) Macrophages actively accumulate malonyldialdehyde-modified but not enzymatically oxidized low density lipoprotein, Mol. Cell. Biochem., 365, 93-98, doi: 10.1007/s11010-012-1247-5.
  27. Lankin, V. Z., Tikhaze, A. K., and Konovalova, G. G. (2023) Oxidized lipoproteins: definition of the term and pathophysiologic effects, Biochemistry (Moscow), 88, 1910-1919, doi: 10.1134/S0006297923110196.
  28. Antonov, A. S., Nikolaeva, M. A., Klueva, T. S., Romanov, Y. A., Babaev, V. R., Bystrevskaya, V. B., Perov, N. A., Repin, V. S., and Smirnov, V. N. (1986) Primary culture of endothelial cells from atherosclerotic human aorta. Part 1. Identification, morphological and ultrastructural characteristics of two endothelial cell subpopulations, Atherosclerosis, 59, 1-19, doi: 10.1016/0021-9150(86)90027-4.
  29. 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.
  30. Lowry, O. H., Rosebrough, N. J., Farr, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265-275, doi: 10.1016/S0021-9258(19)52451-6.
  31. 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.
  32. Tikhaze, A. K., Domogatsky, S. P., and Lankin, V. Z. (2021) Clearance of carbonyl-modified low-density lipoproteins in rabbits, Biochemistry (Moscow) Suppl. Ser. B Biomed. Chem., 15, 119-124, doi: 10.1134/S1990750821020104.
  33. 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.
  34. 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.
  35. Sharapov, M. G., Glushkova, O. V., Parfenyuk, S. B., Gudkov, S. V., Lunin, S. M., and Novoselova, E. G. (2021) The role of TLR4/NF-κB signaling in the radioprotective effects of exogenous Prdx6, Arch. Biochem. Biophys., 702, 108830, doi: 10.1016/j.abb.2021.108830.
  36. Schmittgen, T. D., and Livak, K. J. (2008) Analyzing real-time PCR data by the comparative CT method, Nat. Protoc., 3, 1101-1108, doi: 10.1038/nprot.2008.73.
  37. Bradford, M. M. (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248-254, doi: 10.1006/abio.1976.9999.
  38. Sharapov, M. G., Goncharov, R. G., Parfenyuk, S. B., and Glushkova, O. V. (2022) Effect of peroxiredoxin 6 on p53 transcription factor level, Biochemistry (Moscow), 87, 839-849, doi: 10.1134/S0006297922080156.
  39. Aoyama, T., Fujiwara, H., Masaki, T., and Sawamura, T. (1999) Induction of lectin-like oxidized LDL receptor by oxidized LDL and lysophosphatidylcholine in cultured endothelial cells, J. Mol. Cell. Cardiol., 31, 2101-2114, doi: 10.1006/jmcc.1999.1041.
  40. Hong, D., Bai, Y. P., Gao, H. C., Wang, X., Li, L. F., Zhang, G. G., and Hu, C. P. (2014) Ox-LDL induces endothelial cell apoptosis via the LOX-1-dependent endoplasmic reticulum stress pathway, Atherosclerosis, 235, 310-317, doi: 10.1016/j.atherosclerosis.2014.04.028.
  41. Wang, Y. C., Lee, A. S., Lu, L. S., Ke, L. Y., Chen, W. Y., Dong, J. W., Lu, J., Chen, Z., Chu, C. S., Chan, H. C., Kuzan, T. Y., Tsai, M. H., Hsu, W. L., Dixon, R. A. F., Sawamura, T., Chang, K. C., and Chen, C. H. (2018) Human electronegative LDL induces mitochondrial dysfunction and premature senescence of vascular cells in vivo, Aging cell, 17, e12792, doi: 10.1111/acel.12792.
  42. Bagci, E. Z., Vodovotz, Y., Billiar, T. R., Ermentrout, G. B., and Bahar, I. (2006) Bistability in apoptosis: roles of bax, bcl-2, and mitochondrial permeability transition pores, Biophys. J., 90, 1546-1559, doi: 10.1529/biophysj.105.068122.
  43. Batty, M., Bennett, M. R., and Yu, E. (2022) The role of oxidative stress in atherosclerosis, Cells, 11, 3843, doi: 10.3390/cells11233843.
  44. Kohlgrüber, S., Upadhye, A., Dyballa-Rukes, N., McNamara, C. A., and Altschmied, J. (2017) Regulation of transcription factors by reactive oxygen species and nitric oxide in vascular physiology and pathology, Antioxid. Redox Signal, 26, 679-699, doi: 10.1089/ars.2016.6946.
  45. Leonarduzzi, G., Sottero, B., and Poli, G. (2010) Targeting tissue oxidative damage by means of cell signaling modulators: the antioxidant concept revisited, Pharmacol. Ther., 128, 336-374, doi: 10.1016/j.pharmthera.2010.08.003.
  46. Szalóki, N., Krieger, J. W., Komáromi, I., Tóth, K., and Vámosi, G. (2015) Evidence for homodimerization of the c-Fos transcription factor in live cells revealed by fluorescence microscopy and computer modeling, Mol. Cell. Biol., 35, 3785-3798, doi: 10.1128/MCB.00346-15.
  47. Hirota, K., Matsui, M., Iwata, S., Nishiyama, A., Mori, K., and Yodoi, J. (1997) AP-1 transcriptional activity is regulated by a direct association between thioredoxin and Ref-1, Proc. Natl. Acad. Sci. USA, 94, 3633-3638, doi: 10.1073/pnas.94.8.3633.
  48. Shi, T., and Dansen, T. B. (2020) Reactive oxygen species induced p53 activation: DNA damage, redox signaling, or both? Antioxid. Redox Signal., 33, 839-859, doi: 10.1089/ars.2020.8074.
  49. Ji, Z., He, L., Regev, A., and Struhl, K. (2019) Inflammatory regulatory network mediated by the joint action of NF-κB, STAT3, and AP-1 factors is involved in many human cancers, Proc. Natl. Acad. Sci. USA, 116, 9453-9462, doi: 10.1073/pnas.1821068116.
  50. Kielian, T., Haney, A., Mayes, P. M., Garg, S., and Esen, N. (2005) Toll-like receptor 2 modulates the proinflammatory milieu in Staphylococcus aureus-induced brain abscess, Infect. Immun., 73, 7428-7435, doi: 10.1128/IAI.73.11.7428-7435.
  51. Ohgi, K., Kajiya, H., Goto-T, K., Okamoto, F., Yoshinaga, Y., Okabe, K., and Sakagami, R. (2018) Toll-like receptor 2 activation primes and upregulates osteoclastogenesis via lox-1, Lipids Health Dis., 17, 132, doi: 10.1186/s12944-018-0787-4.
  52. Lee, W.-J., Ou, H.-C., Hsu, W.-C., Chou, M.-M., Tseng, J.-J., Hsu, S.-L., Tsai, K.-L., and Sheu, W. H.-S. (2010) Ellagic acid inhibits oxidized LDL-mediated LOX-1 expression, ROS generation, and inflammation in human endothelial cells, J. Vasc. Surg., 52, 1290-1300, doi: 10.1016/j.jvs.2010.04.085.
  53. Chan, S. H., Hung, C. H., Shih, J. Y., Chu, P. M., Cheng, Y. H., Lin, H. C., Hsieh, P. L., and Tsai, K. L. (2018) Exercise intervention attenuates hyperhomocysteinemia-induced aortic endothelial oxidative injury by regulating SIRT1 through mitigating NADPH oxidase/LOX-1 signaling, Redox Biol., 14, 116-125, doi: 10.1016/j.redox.2017.08.016.
  54. 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.
  55. 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.
  56. 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.
  57. 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.
  58. 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.2Yla-HerttualaL010.03.031.

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