Features of cytokine expression under its modification with vaccine viral antigens (SARS-CoV-2 and Influenzavirus) and benzo(a)pyrene in experimental models in vitro

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Introduction. In this study, we estimated features of modifying effects produced by benzo(a)pyrene well as by vaccine antigens of the SARS-CoV-2 and Influenzavirus viruses on the cytokine profile indicators under experimental conditions in vitro.
Materials and methods. To assess the cytokine-producing function, there was studied a mixed population of immunocytes, which was cultured for 72 hours, followed by analyzing the cytokine profile by enzyme immunoassay. Benzo(a)pyrene and viral vaccine antigens S protein of SARS-CoV-2 and hemagglutinins
of Influenzaviruses of types A and B were used as inducing factors (modifiers).
Results. For exposure to benzo(a)pyrene in vitro there was noted multidirectional modification of cytokine mediator production with activation of IL-8 expression and suppression of IL-6 production (p=0.003–0.047). Similar changes in cytokine expression persisted under combined load with SARS-CoV-2 and Influenzavirus viral antigens. SARS-CoV-2 antigens predominantly stimulated the expression of cytokines (IL-1β, IL-10 and IL-8), while activation of the cytokine profile by Influenzavirus antigens was limited by an increase in IL-8 expression with its maximum achieved under combined (SARS-CoV-2 + Influenzavirus) viral load (p=0.002–0.047). Simultaneous introduction of benzo(a)pyrene and viral antigens into the cell culture involved an increase in expression of pro-inflammatory cytokines IL-1β and TNF-α (p=0.004–0.038).
Limitations. The limitations of the in vitro methodological approach are associated with ambiguity as regards translation and extrapolation of the results and conclusions obtained using cellular and subcellular models to processes formed within a macroorganism.
Conclusion. The results of the study clarify and supplement the ideas about participation of cytokine compartments of intercellular interactions in development of immune and inflammatory processes associated with persisting SARS-CoV-2 and Influenzavirus and modifying effects of benzo(a)pyrene. This made it possible to verify features of combined effects produced by chemical and biological factors in experimental models in vitro (imbalance in expression of IL-8 and IL-6), to identify markers of their effects for evaluating effectiveness of measures aimed at preventing socially significant viral infections under destabilization of the environment.

About the authors

Nina V. Zaitseva

Federal Scientific Center for Medical and Preventive Technologies for Health Risk Management

Email: znv@fcrisk.ru
DSc (Medicine), Professor, Academician of the RAS, Scientific Director of the Federal Scientific Center for Medical and Preventive Health Risk Management Technologies, Perm, 614045, Russian Federation

Ksenia G. Starkova

Federal Scientific Center for Medical and Preventive Technologies for Health Risk Management

Email: skg@fcrisk.ru
PhD (Biology), head of the Laboratory of immunology and allergology, Federal Scientific Center for Medical and Preventive Health Risk Management Technologies, Perm, 614045, Russian Federation

Oleg V. Dolgikh

Federal Scientific Center for Medical and Preventive Technologies for Health Risk Management

Email: oleg@fcrisk.ru
DSc (Medicine), Professor, Head of the Department of Immunobiological Diagnostic Methods of the Federal Scientific Center for Medical and Preventive Health Risk Management Technologies, Perm, 614045, Russian Federation

Alisa S. Shirinkina

Federal Scientific Center for Medical and Preventive Technologies for Health Risk Management

Email: shirinkina.ali@yandex.ru
researcher of the Department of Immunobiological Diagnostic Methods of the Federal Scientific Center for Medical and Preventive Health Risk Management Technologies, Perm, 614045, Russian Federation

References

  1. GBD 2016 Lower Respiratory Infections Collaborators. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of lower respiratory infections in 195 countries, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect. Dis. 2018; 18(11): 1191–210. https://doi.org/10.1016/S1473-3099(18)30310-4
  2. Rahman S., Montero M.T.V., Rowe K., Kirton R., Kunik F.Jr. Epidemiology, pathogenesis, clinical presentations, diagnosis and treatment of COVID-19: a review of current evidence. Expert Rev. Clin. Pharmacol. 2021; 14(5): 601–21. https://doi.org/10.1080/17512433.2021.1902303
  3. Khorramdelazad H., Kazemi M.H., Najafi A., Keykhaee M., Zolfaghari Emameh R., Falak R. Immunopathological similarities between COVID-19 and influenza: Investigating the consequences of co-infection. Microb. Pathog. 2021; 152: 104554. https://doi.org/10.1016/j.micpath.2020.104554
  4. Chang D., Dela Cruz C., Sharma L. Beneficial and detrimental effects of cytokines during Influenza and COVID-19. Viruses. 2024; 16(2): 308. https://doi.org/10.3390/v16020308
  5. Pacheco-Hernández L.M., Ramírez-Noyola J.A., Gómez-García I.A., Ignacio-Cortés S., Zúñiga J., Choreño-Parra J.A. Comparing the cytokine storms of COVID-19 and pandemic Influenza. J. Interferon Cytokine Res. 2022; 42(8): 369–92. https://doi.org/10.1089/jir.2022.0029
  6. Зайцева Н.В., Май И.В., Рейс Ж., Спенсер П.С., Кирьянов Д.А., Камалтдинов М.Р. К оценке дополнительной заболеваемости населения COVID-19 в условиях загрязнения атмосферного воздуха: методические подходы и некоторые практические результаты. Анализ риска здоровью. 2021; (3): 14–28. https://doi.org/10.21668/health.risk/2021.3.02 https://elibrary.ru/ulmefu
  7. Loaiza-Ceballos M.C., Marin-Palma D., Zapata W., Hernandez J.C. Viral respiratory infections and air pollutants. Air Qual. Atmos. Health. 2022; 15(1): 105–14. https://doi.org/10.1007/s11869-021-01088-6
  8. Weaver A.K., Head J.R., Gould C.F., Carlton E.J., Remais J.V. Environmental factors influencing COVID-19 incidence and severity. Annu. Rev. Public Health. 2022; 43: 271–91. https://doi.org/10.1146/annurev-publhealth-052120-101420
  9. Monoson A., Schott E., Ard K., Kilburg-Basnyat B., Tighe R.M., Pannu S., et al. Air pollution and respiratory infections: the past, present, and future. Toxicol. Sci. 2023; 192(1): 3–14. https://doi.org/10.1093/toxsci/kfad003
  10. Rzymski P., Poniedziałek B., Rosińska J., Rogalska M., Zarębska-Michaluk D., Rorat M., et al. The association of airborne particulate matter and benzo[a]pyrene with the clinical course of COVID-19 in patients hospitalized in Poland. Environ. Pollut. 2022; 306: 119469. https://doi.org/10.1016/j.envpol.2022.119469
  11. Bukowska B., Mokra K., Michałowicz J. Benzo[a]pyrene – environmental occurrence, human exposure, and mechanisms of toxicity. Int. J. Mol. Sci. 2022; 23(11): 6348. https://doi.org/10.3390/ijms23116348
  12. Долгих О.В., Никоношина Н.А. Риск формирования дисбаланса популяционного состава лимфоцитов и специфической сенсибилизации у детей, проживающих в условиях аэрогенной экспозиции бенз(а)пиреном в Арктической зоне России. Анализ риска здоровью. 2023; (4): 68–75. https://doi.org/10.21668/health.risk/2023.4.06 https://elibrary.ru/rlmmrl
  13. Liu W., Zhao Y., Fan J., Shen J., Tang H., Tang W., et al. Smoke and spike: benzo[a]pyrene enhances SARS-CoV-2 infection by boosting NR4A2-induced ACE2 and TMPRSS2 expression. Adv. Sci. (Weinh). 2023; 10(26): e2300834. https://doi.org/10.1002/advs.202300834
  14. Schmidt J.R., Haupt J., Riemschneider S., Kämpf C., Löffler D., Blumert C., et al. Transcriptomic signatures reveal a shift towards an anti-inflammatory gene expression profile but also the induction of type I and type II interferon signaling networks through aryl hydrocarbon receptor activation in murine macrophages. Front. Immunol. 2023; 14: 1156493. https://doi.org/10.3389/fimmu.2023.1156493
  15. Yu Y.Y., Jin H., Lu Q. Effect of polycyclic aromatic hydrocarbons on immunity. J. Transl. Autoimmun. 2022; 5: 100177. https://doi.org/10.1016/j.jtauto.2022.100177
  16. Fueldner C., Kohlschmidt J., Riemschneider S., Schulze F., Zoldan K., Esser C., et. al. Benzo(a)pyrene attenuates the pattern-recognition-receptor induced proinflammatory phenotype of murine macrophages by inducing IL-10 expression in an aryl hydrocarbon receptor-dependent manner. Toxicology. 2018; 409: 80–90. https://doi.org/10.1016/j.tox.2018.07.011
  17. Bock K.W. Aryl hydrocarbon receptor (AHR)-mediated inflammation and resolution: Non-genomic and genomic signaling. Biochem. Pharmacol. 2020; 182: 114220. https://doi.org/10.1016/j.bcp.2020.114220
  18. Ryabkova V.A., Churilov L.P., Shoenfeld Y. Influenza infection, SARS, MERS and COVID-19: Cytokine storm – The common denominator and the lessons to be learned. Clin. Immunol. 2021; 223: 108652. https://doi.org/10.1016/j.clim.2020.108652
  19. Choreño-Parra J.A., Jiménez-Álvarez L.A., Cruz-Lagunas A., Rodríguez-Reyna T.S., Ramírez-Martínez G., Sandoval-Vega M., et al. Clinical and immunological factors that distinguish COVID-19 from pandemic Influenza A (H1N1). Front. Immunol. 2021; 12: 593595. https://doi.org/10.3389/fimmu.2021.593595
  20. Essa S., Shamsah M., Alsarraf A.H., Esmaeil A., Al-Shammasi A., Raghupathy R. Influence of SARS-CoV-2 infection on cytokine production by mitogen-stimulated peripheral blood mononuclear cells and neutrophils in COVID-19 intensive care unit patients. Microorganisms. 2022; 10(11): 2194. https://doi.org/10.3390/microorganisms10112194
  21. Mudd P.A., Crawford J.C., Turner J.S., Souquette A., Reynolds D., Bender D., et al. Distinct inflammatory profiles distinguish COVID-19 from influenza with limited contributions from cytokine storm. Sci. Adv. 2020; 6(50): eabe3024. https://doi.org/10.1126/sciadv.abe3024
  22. Zsichla L., Müller V. Risk factors of severe COVID-19: a review of host, viral and environmental factors. Viruses. 2023; 15(1): 175. https://doi.org/10.3390/v15010175

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2025


СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77 - 37884 от 02.10.2009.