N 3 (188) 2024. P. 57–64

THE STATE OF PARАOXONASE IN THE OXIDANT-ANTIOXIDANT SYSTEM IN COMORBIDITY OF CHRONIC OBSTRUCTIVE PULMONARY DISEASE (REVIEW ARTICLE)

N. P. Masik, О. I. Masik, V. V. Kylymchuk, O.I. Mazur, N. S. Nedorezaniuk, E. M. Znamirovska

National Pyrogov Memorial Medical University, Vinnytsia, Ukraine

DOI 10.32782/2226-2008-2024-3-10

The aim is to study the nature of changes in the oxidant-antioxidant system and the role of parаoxonase in COPD in comorbidity with cardiovascular diseases.

Materials and methods. Scientific literature was searched in the informative databases of Scopus, Web of Science, Medline, The Cochrane Library, Pubmed, ResearchGate, Google Scholar, and other Internet resources.

Results. Pathological changes in COPD are based on such universal mechanisms as chronic systemic inflammatory processes of low intensity (low-grade inflammation) and oxidative stress. Numerous studies confirm the interdependence between inflammation and oxidative stress. Increased formation and release of reactive oxygen species (ROS) in the damaged area leads to progressive strengthening of the processes of lipid peroxidation (LPO) and oxidative modification of proteins, their glycosylation, and an increase in the modified atherogenic fraction of lipoproteins. In the future, there will be an increase in hypoxic and ischemic changes in organs and tissues.

The activity of oxidative stress processes is regulated by the antioxidant system (AOS), one of the factors of which is the enzyme paraoxonase (PON), associated with mitochondria and mitochondrial-associated membranes, as the main source of free radicals. The human PON family includes three calcium-dependent esterases: PON1, PON2, and PON3, which have different functions and are located in different locations. PON1 and PON3 are found in high-density lipoprotein (HDL), whereas PON2 is an intracellular enzyme. All PONs exhibit antiinflammatory, antioxidant, anti-atherogenic, and detoxifying properties, and play a protective role in diseases associated with inflammation and oxidative stress, preventing atherosclerosis and cardiovascular diseases.

Conclusion. PON1 can be considered as a diagnostic marker of oxidant-antioxidant imbalance in COPD, associated with a predisposition to the development of cardiovascular diseases.

Key words: chronic obstructive pulmonary disease (COPD), comorbidity with cardiovascular diseases, inflammation, oxidative stress, antioxidant system, paraoxonase.

REFERENCES

  1. Global Strategy for the Diagnosis, Management and Prevention of Chronic Obstructive Pulmonary Disease: 2022 Report. Available from: https://chrome-extension://efaidnbmnnnibpcajpcglclefindmkaj/https://staging.goldcopd.org/wp-content/ uploads/2021/12/GOLD-REPORT-2022-v1.1-22Nov2021_WMV.pdf.
  2. Feshchenko YI, Gavrysyuk VK, Dziublyk AY et al. Adapted clinical guideline: chronic obstructive pulmonary disease. Pulmonol. J. 2020; 3: 5–36. doi: 10.31215/2306-4927-2020-109-3-5-36 (in Ukrainian).
  3. Cho WK, Lee CG, Kim LK. COPD as a Disease of Immunosenescence. Yonsei Med J. 2019; 60(5): 407–413. https://doi. org/10.3349/ymj.2019.60.5.407.
  4. Peiser C. COPD and Inflammation [Internet]. A Compendium of Chronic Obstructive Pulmonary Disease. IntechOpen; 2023. http://dx.doi.org/10.5772/intechopen.107863.
  5. Taler-Verčič A, Goličnik M, Bavec A. The Structure and Function of Paraoxonase-1 and Its Comparison to Paraoxonase-2 and -3. 2020; 25(24): 5980. doi: 10.3390/molecules25245980.
  6. Buklioska Ilievska D., Minov J, Bushev J, Kochovska Kamchevska N. Low-grade systemic inflammation in patients with stable chronic obstructive pulmonary disease. Respiratio Medical Journal. 2019; 9 (1–2): 70–76. Available from: http://hdl.net/20.500.12188/18434.
  7. Lemko OI, Haysak MO, Reshetar DV. Comorbid conditions at chronic obstructive pulmonary disease: the questions under investigation and discussion. Part I. Ukrainskyi terapevtychnyi zhurnal. 2021; 1: 85–92. doi: http://doi.org/10.30978/ UTJ2021-1-85 (in Ukrainian).
  8. Ivchuk VV, Kovalchuk TA. Oxidant and antioxidant system in chronic obstructive pulmonary disease occupational etiology. Medychna ta klinichna khimiia. 21(2): 61–67. doi: 10.11603/mcch.2410-681X.2019.v.i2.10295 (in Ukrainian).
  9. Mahmood T, Singh RK, Kant S et al. Prevalence and etiological profile of chronic obstructive pulmonary disease in nonsmokers. Lung India: Official Organ of Indian Chest Society. 2017, 34 (2), 122. doi: 10.4103/0970-2113.201298.
  10. Lisetska IS, Rozhko MM. Biochemical indicators of oral fluid as markers for assessing the state of antioxidant-prooxidant systems in teenagers and young adults who smoke. Ukrainian Journal of Perinatology and Pediatrics. 2023; 1(93): 51–56. doi: 10.15574/PP.2023.93.51 (in Ukrainian).
  11. Bila I, Dzydzan О, Brodyak I, Sybirna N. Agmatine preventes oxidative-nitrative stress in blood leukocytes under streptozotocin-induced diabetes mellitus. Open Life Sciences. 2019; 14: 299–310. doi: 10.1515/biol-2019-0033.
  12. Kovalyova OM, Pasiieshvili TM. Biological and medical value of antioxidant protection system of the human body. Medytsyna sohodni i zavtra. 90(1): 21–32. https://doi.org/10.35339/msz.2021.90.01.03 (in Ukrainian).
  13. Bilyayeva OO, Osadchaya OI, Kryzhevskyi YeYe, Bitinsh AR. Substantiation of the use of antioxidant therapy in the complex conservative treatment of diabetic foot syndrome. Med. Chasopys. 2022. 1 (147) – I/II 1–5. doi: 10.32471/ umj.1680-3051.147.225667 (in Ukrainian).
  14. Korzhov VI, Zhadan VM, Polianska MO et al. Oxidant and antioxidant systems of the blood in experimental pulmonary emphysema. Аsthma and allergy. 2022; 4: 38–44. doi: 10.31655/2307-3373-2022-4-38-44 (in Ukrainian).
  15. Lorey MB, Öörni K, Kovanen PT. Modified Lipoproteins Induce Arterial Wall Inflammation During Atherogenesis. Front Cardiovasc Med. 2022; 9: 841545. doi: 10.3389/fcvm.2022.841545.
  16. Medina-Díaz IM, Ponce-Ruíz N, Rojas-García AE. et al. The Relationship between Cancer and Paraoxonase 1. Antioxidants (Basel). 2022; 11(4): 697. doi: 10.3390/antiox11040697.
  17. Khalil A, Fulop T, Berrougui H. Role of Paraoxonase1in the Regulation of High-Density Lipoprotein Functionality and in Cardiovascular Protection. Antioxid Redox Signal. 2021; 34(3): 191–200. doi: 10.1089/ars.2019.7998.
  18. Dziublyk OYa, Gumenyuk NI, Mhitaryan LS et al. Qualitative composition of blood lipoproteids in patients with inflammation of lower respiratory tract as a risk factor of atherosclerosis. Pulmonol. J. 2017; 3: 21–24 (in Ukrainian).
  19. Thompson EW, Demissei BG, Smith AM. et al. Paraoxonase-1 Activity in Breast Cancer Patients Treated with Doxorubicin with or Without Trastuzumab. JACC Basic Translational Science. 2022; 7(1): 1–10. doi: 10.1016/j.jacbts.2021.10.010.
  20. Lytvynets LY, Lytvynets-Golutiak UY, Lytvynets VY. Oksydatyvnyi stres i komponenty antyoksydantnoho zakhystu v mekhanizmakh formuvannia bronkhialnoi astmy u ditei. Naukovyi visnyk Uzhhorodskoho universytetu. Seriia «Medytsyna». 2022; 2(66), 106–110. doi: https://doi.org/10.32782/2415-8127.2022.66.20 (in Ukrainian).
  21. Watanabe J, Kotani K, Gugliucci A. Paraoxonase 1 and Chronic Obstructive Pulmonary Disease: A Meta-Analysis. Antioxidants (Basel). 2021; 10(12): 1891. doi: 10.3390/antiox10121891.
  22. Zinellu E, Zinellu A, Pau MC et al. Paraoxonase-1 in stable chronic obstructive pulmonary disease: a systematic review and meta-analysis. Minerva Respiratory Medicine. 2022; 61(3): 138–145. https://doi.org/10.23736/S2784-8477.22.01999-4.
  23. Aune D, Schlesinger S, Norat T, Riboli E. Tobacco smoking and the risk of heart failure: A systematic review and metaanalysis of prospective studies. Eur J Prev Cardiol. 2019; 26(3): 279–288. doi: 10.1177/2047487318806658.
  24. Shunmoogam N, Naidoo P, Chilton R. Paraoxonase (PON)-1: a brief overview on genetics, structure, polymorphisms and clinical relevance. Vasc Health Risk Manag. 2018; 14: 137–143. doi: 10.2147/VHRM.S165173.
  25. Zhou WC, Qu J, Xie SY, Sun Y, Yao HW. Mitochondrial Dysfunction in Chronic Respiratory Diseases: Implications for the Pathogenesis and Potential Therapeutics. Oxid Med Cell Longev. 2021; 2021: 5188306. doi: 10.1155/2021/5188306.
  26. Kamimura D, Cain LR, Mentz RJ. et al. Cigarette Smoking and Incident Heart Failure: Insights From the Jackson Heart Study. Circulation. 2018; 137(24): 2572–2582. doi: 10.1161/CIRCULATIONAHA.117.031912.
  27. Albrengues J, Shields MA, Ng D. et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. 2018; 361(6409): 4227. doi: 10.1126/science.aao4227.
  28. Min J, Yang D, Kim M. et al. Publisher Correction: Inflammation induces two types of inflammatory dendritic cells in inflamed lymph nodes. Exp Mol Med. 2018; 50(4): 1. doi: https://doi.org/10.1038/emm.2017.292.
  29. Stasenko AA. Mistsevyi imunitet: textbook. NNTs «Instytut biolohii ta medytsyny». Kyiv. 2021. 153 р. (in Ukrainian).
  30. Lee PL, Lee KY, Cheng TM. et al. Relationships of Haptoglobin Phenotypes with Systemic Inflammation and the Severity of Chronic Obstructive Pulmonary Disease. Sci Rep. 2019; 9(1): 189. doi: 10.1038/s41598-018-37406-9.
  31. Hu Y, Li J, Lou B. et al. The Role of Reactive Oxygen Species in Arsenic Toxicity. Biomolecules. 2020; 10(2): 240. https:// doi.org/10.3390/biom10020240.
  32. Kryghna SI, Kievvskaia YiО, Kozar VV. The state of immunologic resistance in terms of experimental bacterial rhinitis and its pharmacological correction. Visnyik problem biologii I meditciny. 2018; 2(143): 137–140 (in Ukrainian).
  33. Albar Z, Albakri M, Hajjari J, et al. Inflammatory Markers and Risk of Heart Failure with Reduced to Preserved Ejection Fraction. Am J Cardiol. 2022; 167: 68–75. doi: 10.1016/j.amjcard.2021.11.045.
  34. Aimo A, Castiglione V, Borrelli C. et al. Oxidative stress and inflammation in the evolution of heart failure: From pathophysiology to therapeutic strategies. Eur J Prev Cardiol. 2020; 27(5): 494b510. doi: 10.1177/2047487319870344.
  35. Pasiyeshvili LM, Zhelezniakova NM, Pasiieshvili TM. Antioxidant system: norm and pathology. Skhidnoievropeiskyi zhurnal vnutrishnoi ta simeinoi medytsyny. 2021; 1: 40–46. doi: 10.15407/internalmed2021.01.040 (in Russian).
  36. Camps J, García-Heredia A, Hernández-Aguilera A, Joven J. Paraoxonases, mitochondrial dysfunction and non-communicable diseases. Chemico-Biological Interactions. 2016; 259(B): 382–387. https://doi.org/10.1016/j.cbi.2016.04.005.
  37. Cavallero A, Puccini P, Aprile V et al. Presence, enzymatic activity, and subcellular localization of paraoxonases 1, 2, and 3 in human lung tissues. Life Sciences. Volume 311, Part A, 2022. 121147. ISSN 0024-3205. https://doi.org/10.1016/j. lfs.2022.121147.
  38. Xu JH, Lu SJ, Wu P, et al. Molecular mechanism whereby paraoxonase-2 regulates coagulation activation through endothelial tissue factor in rat haemorrhagic shock model. Wound J. 2020; 17: 735–741. https://doi.org/10.1111/iwj.13329.
  39. Belovol AN, Topchiy II, Kirienko OM, Denisenko VP, Kirienko DA. Determination state of oxidative stress, pon1 activity and lipid spectrum in patients with diabetic nephropathies and hypertension disease. Eksperymentalna i klinichna medytsyna. 2018; 79 (2–3): 71–78. Available from: https://ecm.knmu.edu.ua/article/view/403 (in Ukrainian).
  40. Zhao XJ, Liu LC, Guo C. et al. Hepatic paraoxonase 1 ameliorates dysfunctional high-density lipoprotein and atherosclerosis in scavenger receptor class B type I deficient mice. Ann Transl Med 2021; 9(13): 1063. doi: 10.21037/atm-21-682.
  41. Durrington PN, Bashir B, Soran H. Paraoxonase 1 and atherosclerosis. Cardiovasc. Med. 2023; 10: 1065967. doi: 10.3389/fcvm.2023.1065967.
  42. Yemchenko Ya. The role of PPAR in the pathogenesis of psoriasis and obesity. VISNYK Ukrainska medychna stomatolohichna akademiia. 2019; 2(66): 224–229. doi: 10.31718/2077-1096.19.2.224 (in Ukrainian).
  43. Vatashchuk M, Hurza V, Bayliak M. Adapting of Spectrophotometric Assay of Paraoxonase Activity with 4-Nitrophenylacetate for Murine Plasma and Liver. Journal of Vasyl Stefanyk Precarpathian National University. 2023; 9(4): 6–14. doi: https: // doi.org/10.15330/jpnu.9.4.6-14.
  44. Vavlukis M, Vavlukis A, Krsteva K, Topuzovska S. Paraoxonase 1 gene polymorphisms in lipid oxidation and atherosclerosis development. Front Genet. 2022; 13: 966413. doi: 10.3389/fgene.2022.966413.
  45. Kunachowicz D, Ściskalska M, Kepinska M. Modulatory Effect of Lifestyle-Related, Environmental and Genetic Factors on Paraoxonase-1 Activity: A Review. Int J Environ Res Public Health. 2023; 20(4): 2813. doi: 10.3390/ijerph20042813.
  46. Mackness M, Sozmen EY. A critical review on human serum Paraoxonase-1 in the literature: truths and misconceptions. Turkish Journal of Biochemistry. 2021; 46(1): 3–8. https://doi.org/10.1515/tjb-2020-0186.
  47. Bacchetti T, Ferretti G, Carbone F, Ministrini S. Dysfunctional high-density lipoprotein: The role of myeloperoxidase and paraoxonase-1. Med. Chem. 2021; 28: 2842–2850. doi: 10.2174/0929867327999200716112353.
  48. Lipkan NG, Kuchmenko OB, Mkhitaryan LS. Inductive No-synthase activity and citrulline content in blood serum as markers of immuno-inflammatory activation and oxidative stress under chronic heart failure. Bulletin of Medical and Biological Research. 2021; 4(10): 46–52. doi: 10.11603/bmbr.2706-6290.2021.4.12492 (in Ukrainian)
  49. Soomro S. Oxidative Stress and Inflammation. Open Journal of Immunology. 2019; 9(1): 1–20. doi: 10.4236/oji.2019.91001.
  50. Parween F, Gupta RD. Insights into the role of paraoxonase 2 in human pathophysiology. J Biosci. 2022; 47: 4. https://doi. org/10.1007/s12038-021-00234-7.
  51. Manco G, Porzio E, Carusone TM. Human Paraoxonase-2 (PON2): Protein Functions and Modulation. Antioxidants. 2021; 10(2):256. https://doi.org/10.3390/antiox10020256.
  52. Li W, Kennedy D, Shao Z et al. Paraoxonase 2 prevents the development of heart failure. Free Radic. Biol. Med. 2018; 121: 117–126. https://doi.org/10.1016/j.freeradbiomed.2018.04.583.
  53. Shih DM, Meng Y, Sallam T et al. PON2 Deficiency Leads to Increased Susceptibility to Diet-Induced Obesity. Antioxidants (Basel). 2019; 8(1): 19. https://doi.org/10.3390/antiox8010019.
  54. Nagarajan A, Dogra SK, Sun L. et al. Paraoxonase 2 Facilitates Pancreatic Cancer Growth and Metastasis by Stimulating GLUT1-Mediated Glucose Transport. Mol Cell. 2017; 67(4): 685–701. doi: 10.1016/j.molcel.2017.07.014.
  55. Ritta MC, Baldez AM, Oliveira IO et al. Paraoxonase 1 serum activity in women: the effects of menopause, the C(-107)T polymorphism and food intake. Arch Endocrinol Metab. 2019; 63(3): 272–279. doi: 10.20945/2359-3997000000130.
  56. Yang X, Yang C, Friesel RE, Liaw L. Sprouty1 has a protective role in atherogenesis and modifies the migratory and inflammatory phenotype of vascular smooth muscle cells. 2023; 373: 17–28. doi: 10.1016/j. atherosclerosis.2023.04.007.
  57. Mahrooz A, Mackness M. Epigenetics of paraoxonases. Opin. Lipidol. 2020; 31: 200–205. doi: 10.1097/ MOL.0000000000000687.
  58. Djekic S, Vekic J, Zeljkovic A. et al. HDL Subclasses and the Distribution of Paraoxonase-1 Activity in Patients with ST-Segment Elevation Acute Myocardial Infarction. Int J Mol Sci. 2023; 24(11): 9384. doi: 10.3390/ijms24119384.
  59. Sansbury LB, Rothnie KJ, Bains C, Compton C, Anley G, Ismaila AS. Healthcare, Medication Utilization and Outcomes of Patients with COPD by GOLD Classification in England. J. Chron. Obstruct. Pulmon. Dis. 2021; 16: 2591–2604.
  60. Mehvari F, Imanparast F, Mohaghegh P, Alimoradian A. et al. Protective effects of paraoxonase-1, vitamin E and selenium, and oxidative stress index on the susceptibility of lowdensity lipoprotein to oxidation in diabetic patients with/without coronary artery disease. Eur J Med Res. 2023; 28(1): 300. doi: 10.1186/s40001-023-01254-9.
  61. Varadhan S, Venkatachalam R, Perumal SM, Ayyamkulamkara SS. Evaluation of Oxidative Stress Parameters and Antioxidant Status in Coronary Artery Disease Patients. Arch Razi Inst. 2022; 77(2): 853–859. doi: 10.22092/ARI.2022.357069.1965.
  62. Kotani K, Sakane N, Gugliucci A. Serum paraoxonase activity in familial hypercholesterolaemia. Arch Med Sci Atheroscler Dis. 2023; 8: 11–12. doi: 10.5114/amsad/160952.
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