Электронные сигареты и глутатион-зависимые механизмы клеточной защиты в контексте сохранения репродуктивного здоровья

1. Salari N., Rahimi S., Darvishi N., Abdolmaleki A., Mohammadi M. The global prevalence of E-cigarettes in youth: a comprehensive systematic review and meta-analysis. Public Health Pract. (Oxf). 2024; 7: 100506. https://dx.doi.org/10.1016/j.puhip.2024.100506
2. Jerzyński T., Stimson G.V., Shapiro H., Król G. Estimation of the global number of e-cigarette users in 2020. Harm Reduct. J. 2021; 18(1): 109. https://dx.doi.org/10.1186/s12954-021-00556-7
3. Kabéle M., Lyytinen G., Bosson J.A., Hedman L., Antoniewicz L., Lundbäck M. et al. Nicotine in E-cigarette aerosol may lead to pulmonary inflammation. Respir. Med. 2025; 242: 108101. https://dx.doi.org/10.1016/j.rmed.2025.108101
4. Kotoulas S.C., Katsaounou P., Riha R., Grigoriou I., Papakosta D., Spyratos D. et al. Electronic cigarettes and asthma: what do we know so far? J. Pers. Med. 2021; 11(8): 723. https://dx.doi.org/10.3390/jpm11080723
5. Roxlau E.T., Pak O., Hadzic S., Garcia-Castro C.F., Gredic M., Wu C.Y. et al. Nicotine promotes e-cigarette vapour-induced lung inflammation and structural alterations. Eur. Respir. J. 2023; 61(6): 2200951. https://dx.doi.org/10.1183/13993003.00951-2022
6. Wang Q., Lucas J.H., Pang C., Zhao R., Rahman I. Tobacco and menthol flavored nicotine-free electronic cigarettes induced inflammation and dysregulated repair in lung fibroblast and epithelium. Respir. Res. 2024; 25(1): 23. https://dx.doi.org/10.1186/s12931-023-02537-9
7. Majidid S., Weisbrod R.M., Fetterman J.L., Keith R.J., Rizvi S.H.M., Zhou Y. et al. Pod-based e-liquids impair human vascular endothelial cell function. PLoS One. 2023; 18(1): e0280674. https://dx.doi.org/10.1371/journal.pone.0280674
8. Mohammadi L., Han D.D., Xu F., Huang A., Derakhshandeh R., Rao P. et al. Chronic e-cigarette use impairs endothelial function on the physiological and cellular levels. Arterioscler. Thromb. Vasc. Biol. 2022; 42(11): 1333-50. https://dx.doi.org/10.1161/ATVBAHA.121.317749
9. El-Mahdy M.A., Mahgoup E.M., Ewees M.G., Eid M.S., Abdelghany T.M., Zweier J.L. Long-term electronic cigarette exposure induces cardiovascular dysfunction similar to tobacco cigarettes: role of nicotine and exposure duration. Am. J. Physiol. Heart. Circ. Physiol. 2021; 320(5): H2112-29. https://dx.doi.org/10.1152/ajpheart.00997.2020
10. El-Mahdy M.A., Ewees M.G., Eid M.S., Mahgoup E.M., Khaleel S.A., Zweier J.L. Electronic cigarette exposure causes vascular endothelial dysfunction due to NADPH oxidase activation and eNOS uncoupling. Am. J. Physiol. Heart. Circ. Physiol. 2022; 322(4): H549-67. https://dx.doi.org/10.1152/ajpheart.00460.2021
11. Rao P., Han D.D., Tan K., Mohammadi L., Derakhshandeh R., Navabzadeh M. et al. Comparable impairment of vascular endothelial function by a wide range of electronic nicotine delivery devices. Nicotine Tob. Res. 2022; 24(7): 1055-62. https://dx.doi.org/10.1093/ntr/ntac019
12. Evanoff N.G., Dengel D.R., Stockelman K.A., Fandl H., DeSouza N.M., Greiner J.J. et al. Circulating extracellular microvesicles associated with electronic cigarette use increase endothelial cell inflammation and reduce nitric oxide production. Exp. Physiol. 2024; 109(9): 1593-603. https://dx.doi.org/10.1113/EP091715
13. Mercier C., Pourchez J., Leclerc L., Forest V. In vitro toxicological evaluation of aerosols generated by a 4th generation vaping device using nicotine salts in an air-liquid interface system. Respir. Res. 2024; 25(1): 75. https://dx.doi.org/10.1186/s12931-024-02697-2
14. Liu Z., Zhang Y., Youn J.Y., Zhang Y., Makino A., Yuan J.X. et al. Flavored and nicotine-containing e-cigarettes induce impaired angiogenesis and diabetic wound healing via increased endothelial oxidative stress and reduced NO bioavailability. Antioxidants (Basel). 2022; 11(5): 904. https://dx.doi.org/10.3390/antiox11050904
15. Samsonov A., Urlacher S.S. Oxidative stress in children and adolescents: insights into human biology. Am. J. Hum. Biol. 2025; 37(1): e24200. https://dx.doi.org/10.1002/ajhb.24200
16. Thirion-Romero I., Pérez-Padilla R., Zabert G., Barrientos-Gutierrez I. Respiratory impact of electronic cigarettes and low-risk tobacco. Rev. Invest. Clin. 2019; 71(1): 17-27. https://dx.doi.org/10.24875/RIC.18002616
17. Wu Y.H., Chiang C.P. Adverse effects of electronic cigarettes on human health. J. Dent. Sci. 2024; 19(4): 1919-23. https://dx.doi.org/10.1016/j.jds.2024.07.030
18. Canistro D., Vivarelli F., Cirillo S., Marquillas C.B., Buschini A., Lazzaretti M. et al. E-cigarettes induce toxicological effects that can raise the cancer risk. Sci. Rep. 2017; 7(1): 2028. https://dx.doi.org/10.1038/s41598-017-02317-8
19. Serpa G.L., Renton N.D., Lee N., Crane M.J., Jamieson A.M. Electronic nicotine delivery system aerosol-induced cell death and dysfunction in macrophages and lung epithelial cells. Am. J. Respir. Cell. Mol. Biol. 2020; 63(3): 306-16. https://dx.doi.org/10.1165/rcmb.2019-0200OC
20. Zhou Y., Zhao X., Hu W., Ruan F., He C., Huang J. et al. Acute and subacute oral toxicity of propylene glycol enantiomers in mice and the underlying nephrotoxic mechanism. Environ. Pollut. 2021; 290: 118050. https://dx.doi.org/10.1016/j.envpol.2021.118050
21. National Academies of Sciences, Engineering, and Medicine. Public health consequences of e-cigarettes. Washington, DC: The National Academies Press; 2018. https://dx.doi.org/10.17226/24952
22. Komura M., Sato T., Yoshikawa H., Nitta N.A., Suzuki Y., Koike K. et al. Propylene glycol, a component of electronic cigarette liquid, damages epithelial cells in human small airways. Respir. Res. 2022; 23(1): 216. https://dx.doi.org/10.1186/s12931-022-02142-2
23. Lechasseur A., Mouchiroud M., Tremblay F., Bouffard G., Milad N., Pineault M. et al. Glycerol contained in vaping liquids affects the liver and aspects of energy homeostasis in a sex-dependent manner. Physiol. Rep. 2022; 10(2): e15146. https://dx.doi.org/10.14814/phy2.15146
24. Esteban-Lopez M., Perry M.D., Garbinski L.D., Manevski M., Andre M., Ceyhan Y. et al. Health effects and known pathology associated with the use of e-cigarettes. Toxicol. Reports. 2022; 9: 1357-68. https://dx.doi.org/10.1016/j.toxrep.2022.06.006
25. Marí M., de Gregorio E., de Dios C., Roca-Agujetas V., Cucarull B., Tutusaus A. et al. Mitochondrial glutathione: recent insights and role in disease. Antioxidants (Basel). 2020; 9(10): 909. https://dx.doi.org/10.3390/antiox9100909
26. Hermes-Lima M., Moreira D.C., Zenteno-Savín T., Cassier-Chauvat C., Marceau F., Farci S. et al. The glutathione system: a journey from cyanobacteria to higher eukaryotes. Antioxidants (Basel). 2023; 12(6): 1199 https://dx.doi.org/10.3390/antiox12061199
27. Жаворонок Т.В., Носарева О.Л., Помогаева А.П., Бутусова В.Н., Стариков Ю.В., Климанова Е.М., Петина Г.В., Степовая Е.А. Особенности детоксикации с участием ферментов микросомального окисления и глутатионзависимых ферментов при псевдотуберкулезе у детей. Бюллетень сибирской медицины. 2006; 1: 16-20.
28. Jin Y., Waly M., Jamurtas A., Chu L., Labarrere C.A., Net C. et al. Glutathione: a samsonian life-sustaining small molecule that protects against oxidative stress, ageing and damaging inflammation. Front. Nutr. 2022; 9: 1007816. https://dx.doi.org/10.3389/fnut.2022.1007816
29. Iskusnykh I.Y., Zakharova A.A., Pathak D. Glutathione in brain disorders and aging. Molecules. 2022; 27(1): 324. https://dx.doi.org/10.3390/molecules27010324
30. Danileviciute A., Grazuleviciene R., Paulauskas A., Nadisauskiene R., Nieuwenhuijsen M.J. Low level maternal smoking and infant birthweight reduction: Genetic contributions of GSTT1 and GSTM1 polymorphisms. BMC Pregnancy Childbirth. 2012; 12: 161. https://dx.doi.org/10.1186/1471-2393-12-161
31. Кан Н.Е., Беднягин Л.А., Тютюнник В.Л., Ховхаева П.А., Донников А.Е., Долгушина Н.В. Значимость полиморфизма генов системы детоксикации при преэклампсии. Акушерство и гинекология. 2016; 2: 8-13.
32. Беспалова О.Н. Генетика невынашивания беременности. Журнал акушерства и женских болезней. 2007; 1: 81-95.
33. Беспалова О.Н., Иващенко Т.Э., Тарасенко О.А., Малышева О.В., Баранов В.С., Айламазян Э.К. Плацентарная недостаточность и полиморфизм генов глютатион-S-трансфераз М1, Т1 и р1. Журнал акушерства и женских болезней. 2006; 2: 25-31.
34. Сыркашева А.Г., Долгушина Н.В., Франкевич В.Е., Донников А.Е. Влияние тяжелых металлов на эффективность программ вспомогательных репродуктивных технологий в зависимости от полиморфизма генов системы детоксикации. Акушерство и гинекология. 2021; 7: 95-101.
35. Hernández-Rodríguez J., López A.L., Montes S., Bonilla-Jaime H., Morales I., Limón-Morales O. et al. Delay in puberty indices of Wistar rats caused by Cadmium. Focus on the redox system in reproductive organs. Reprod. Toxicol. 2021; 99: 71-9. https://dx.doi.org/10.1016/j.reprotox.2020.11.010
36. Babalola A.A., Adelowo A.R., Da-silva O.F., Ikeji C.N., Owoeye O., Rocha J.B.T. et al. Attenuation of doxorubicin-induced hypothalamic-pituitary-testicular axis dysfunction by diphenyl diselenide involves suppression of hormonal deficits, oxido-inflammatory stress and caspase 3 activity in rats. J. Trace Elem. Med. Biol. 2023; 79: 127254. https://dx.doi.org/10.1016/j.jtemb.2023.127254
37. Baraka S.M., Hussien Y.A., Ahmed-Farid O.A., Hassan A., Saleh D.O. Acrylamide-induced hypothalamic-pituitary-gonadal axis disruption in rats: androgenic protective roles of apigenin by restoring testicular steroidogenesis through upregulation of 17β-HSD, CYP11A1 and CYP17A1. Food Chem. Toxicol. 2024; 194: 115078. https://dx.doi.org/10.1016/j.fct.2024.115078
38. Nkpaa K.W., Amadi B.A., Adedara I.A., Wegwu M.O., Farombi E.O. Ethanol exacerbates manganese – induced functional alterations along the hypothalamic-pituitary-gonadal axis of male rats. Neurosci Lett. 2018; 684(2): 47-54. https://dx.doi.org/10.1016/j.neulet.2018.07.007
39. Owumi S.E., Arunsi U.O., Otunla M.T., Oluwasuji I.O. Exposure to lead and dietary furan intake aggravates hypothalamus-pituitary-testicular axis toxicity in chronic experimental rats. J. Biomed. Res. 2022; 37(2): 100-14. https://dx.doi.org/10.7555/JBR.36.20220108
40. Adeoye O., Olawumi J., Opeyemi A., Christiania O. Review on the role of glutathione on oxidative stress and infertility. JBRA Assist. Reprodist. 2018; 22(1): 61-6. https://dx.doi.org/10.5935/1518-0557.20180003
41. Ploeger C.G., Hansen K., Bayles A., Burger A., Hansen J., Jenkins T. Changes in sperm glutathione and glutathione redox states correlate to poor sperm qualitative measures. Reprod. Med. 2025; 6(2): 13. https://dx.doi.org/10.3390/reprodmed6020013
42. Li Q., Chao T., Wang Y., He P., Zhang L., Wang J. Metabolomics and transcriptomics analyses reveal the complex molecular mechanisms by which the hypothalamus regulates sexual development in female goats. BMC Genomics. 2025; 26(1): 303. https://dx.doi.org/10.1186/s12864-025-11492-2
43. Yan F., Zhao Q., Li Y., Zheng Z., Kong X., Shu C. et al. The role of oxidative stress in ovarian aging: a review. J. Ovarian Res. 2022; 15(1): 100. https://dx.doi.org/10.1186/s13048-022-01032-x
44. Lava Kumar S., Kushawaha B., Mohanty A., Kumari A., Kumar A., Beniwal R. et al. Glutathione peroxidase (GPX1) - Selenocysteine metabolism preserves the follicular fluid’s (FF) redox homeostasis via IGF-1- NMD cascade in follicular ovarian cysts (FOCs). Biochim. Biophys. Acta Mol. Basis Dis. 2024; 1870(6): 167235. https://dx.doi.org/10.1016/j.bbadis.2024.167235
45. Assiri M.A., Al Jumayi S.R., Alsuhaymi S., Emwas A.H., Jaremko M., Alsaleh N.B. et al. Electronic cigarette vapor disrupts key metabolic pathways in human lung epithelial cells. Saudi Pharm. J. 2024; 32(1): 101897. https://dx.doi.org/10.1016/j.jsps.2023.101897
46. Jeon J., Zhang Q., Chepaitis P.S., Greenwald R., Black M., Wright C. Toxicological assessment of particulate and metal hazards associated with vaping frequency and device age. Toxics. 2023; 11(2): 155. https://dx.doi.org/10.3390/toxics11020155
47. Fung N.H., Wang H., Vlahos R., Wilson N., Lopez A.F., Owczarek C.M. et al. Targeting the human βc receptor inhibits inflammatory myeloid cells and lung injury caused by acute cigarette smoke exposure. Respirology. 2022; 27(8): 617-29. https://dx.doi.org/10.1111/resp.14297
48. Wang J., Zhang T., Johnston C.J., Kim S.Y., Gaffrey M.J., Chalupa D. et al. Protein thiol oxidation in the rat lung following e-cigarette exposure. Redox Biol. 2020; 37: 101758. https://dx.doi.org/10.1016/j.redox.2020.101758
49. Alzoubi K.H., Khabour O.F., Al-Sawalha N.A., Karaoghlanian N., Shihadeh A., Eissenberg T. Time course of changes in inflammatory and oxidative biomarkers in lung tissue of mice induced by exposure to electronic cigarette aerosol. Toxicol. Rep. 2022; 9: 1484-90. https://dx.doi.org/10.1016/j.toxrep.2022.07.001
50. Górna I., Napierala M., Florek E. Electronic cigarette use and metabolic syndrome development: a critical review. Toxics. 2020; 8(4): 105. https://dx.doi.org/10.3390/toxics8040105
51. Bonner E., Chang Y., Christie E., Colvin V., Cunningham B., Elson D. et al. The chemistry and toxicology of vaping. Pharmacol. Ther. 2021; 225: 107837. https://dx.doi.org/10.1016/j.pharmthera.2021.107837
52. Osadchuk L., Kleshchev M., Osadchuk A. Effects of cigarette smoking on semen quality, reproductive hormone levels, metabolic profile, zinc and sperm DNA fragmentation in men: results from a population-based study. Front. Endocrinol. (Lausanne). 2023; 14: 1255304. https://dx.doi.org/10.3389/fendo.2023.1255304
53. Kim H.K., Choi W.Y., Lee J.I., Kim T.J. Impact of conventional cigarette and electronic cigarette use on sperm quality and IVF/ICSI outcomes. Sci. Rep. 2025; 15(1): 23714. https://dx.doi.org/10.1038/s41598-025-09495-w
54. Laldinsangi C. Toxic effects of smokeless tobacco on female reproductive health: a review. Curr. Res. Toxicol. 2022; 3: 100066. https://dx.doi.org/10.1016/j.crtox.2022.100066
55. Holmboe S.A., Priskorn L., Jensen T.K., Skakkebaek N.E., Andersson A.M., Jørgensen N. Use of e-cigarettes associated with lower sperm counts in a cross-sectional study of young men from the general population. Hum. Reprod. 2020; 35(7): 1693-701. https://dx.doi.org/10.1093/humrep/deaa089
56. Kaur G., Gaurav A., Lamb T., Perkins M., Muthumalage T., Rahman I. Current perspectives on characteristics, compositions, and toxicological effects of e-cigarettes containing tobacco and menthol / mint flavors. Front. Physiol. 2020; 11: 613948. https://dx.doi.org/10.3389/fphys.2020.613948
57. Wang H., Tian Y., Fu Y., Ma S., Xu X., Wang W. et al. Testicular tissue response following a 90-day subchronic exposure to HTP aerosols and cigarette smoke in rats. Toxicol. Res. (Camb). 2023; 12(5): 902-12. https://dx.doi.org/10.1093/toxres/tfad085
58. Nahak T.M., I Gusti Ngurah Pramesemara. Electronic cigarettes on sperm quality: review in animal and human study. Indonesian Andrology and Biomedical Journal. 2023; 4(2): 71-8. https://dx.doi.org/10.20473/iabj.v4i2.48503
59. Rahali D., Jrad-Lamine A., Dallagi Y., Bdiri Y., Ba N., El May M. et al. Semen parameter alteration, histological changes and role of oxidative stress in adult rat epididymis on exposure to electronic cigarette refill liquid. Chin. J. Physiol. 2018; 61(2): 75-84. https://dx.doi.org/10.4077/CJP.2018.BAG521
60. Chen K., Wu L., Liu Q., Tan F., Wang L., Zhao D. et al. Glutathione improves testicular spermatogenesis through inhibiting oxidative stress, mitochondrial damage, and apoptosis induced by copper deposition in mice with Wilson disease. Biomed. Pharmacother. 2023; 158: 114107. . https://dx.doi.org/10.1016/j.biopha.2022.114107
61. Galanti F., Licata E., Paciotti G., Gallo M., Riccio S., Miriello D. et al. Impact of different typologies of smoking on ovarian reserve and oocyte quality in women performing ICSI cycles: an observational prospective study. Eur. Rev. Med. Pharmacol. Sci. 2023; 27(11): 5190-9. https://dx.doi.org/10.26355/eurrev_202306_32637
62. Chen T., Wu M., Dong Y., Kong B., Cai Y., Hei C. et al. Effect of e-cigarette refill liquid on follicular development and estrogen secretion in rats. Tob. Induc. Dis. 2022; 20(4): 36. https://dx.doi.org/10.18332/tid/146958
63. Chen T., Wu M., Dong Y., Ren H., Wang M., Kong B. et al. Ovarian toxicity of e-cigarette liquids: effects of components and high and low nicotine concentration e-cigarette liquid in vitro. Tob. Induc. Dis. 2023; 21: 128. https://dx.doi.org/10.18332/tid/170631
64. Liu B., Xu G., Rong S., Santillan D.A., Santillan M.K., Snetselaar L.G. et al. National estimates of e-cigarette use among pregnant and nonpregnant women of reproductive age in the United States, 2014-2017. JAMA Pediatr. 2019; 173(6): 600-2. https://dx.doi.org/10.1001/jamapediatrics.2019.0658
65. Ammar L., Tindle H.A., Miller A.M., Adgent M.A., Nian H., Ryckman K.K. et al. Electronic cigarette use during pregnancy and the risk of adverse birth outcomes: a cross-sectional surveillance study of the US Pregnancy Risk Assessment Monitoring System (PRAMS) population. PLoS One. 2023; 18(10): e0287348. https://dx.doi.org/10.1371/journal.pone.0287348
66. Orzabal M.R., Lunde-Young E.R., Ramirez J.I., Howe S.Y.F., Naik V.D., Lee J. et al. Chronic exposure to e-cig aerosols during early development causes vascular dysfunction and offspring growth deficits. Transl. Res. 2019; 207: 70-82. https://dx.doi.org/10.1016/j.trsl.2019.01.001
67. Ashour A.A., Alhussain H., Rashid U Bin, Abughazzah L., Gupta I., Malki A. et al. E-cigarette liquid provokes significant embryotoxicity and inhibits angiogenesis. Toxics. 2020; 8(2): 38. https://dx.doi.org/10.3390/toxics8020038
68. Wetendorf M., Randall L.T., Lemma M.T., Hurr S.H., Pawlak J.B., Tarran R. et al. E-cigarette exposure delays implantation and causes reduced weight gain in female offspring exposed in utero. J. Endocr. Soc. 2019; 3(10): 1907-16. https://dx.doi.org/10.1210/js.2019-00216
69. Noël A., Hansen S., Zaman A., Perveen Z., Pinkston R., Hossain E. et al. In utero exposures to electronic-cigarette aerosols impair the Wnt signaling during mouse lung development. Am. J. Physiol. Lung Cell. Mol. Physiol. 2020; 318(4):L705-22. https://dx.doi.org/10.1152/ajplung.00408.2019
70. Lee J., Orzabal M.R., Naik V.D., Ramadoss J. Impact of e-cigarette vaping aerosol exposure in pregnancy on mTOR signaling in rat fetal hippocampus. Front. Neurosci. 2023; 17: 1217127. https://dx.doi.org/10.3389/fnins.2023.1217127
71. Chen Z., Chen W., Li Y., Moos M., Xiao D., Wang C. Single-nucleus chromatin accessibility and RNA sequencing reveal impaired brain development in prenatally e-cigarette exposed neonatal rats. iScience. 2022; 25(8): 104686. https://dx.doi.org/10.1016/j.isci.2022.104686
72. Church J.S., Chace-Donahue F., Blum J.L., Ratner J.R., Zelikoff J.T., Schwartzer J.J. Neuroinflammatory and behavioral outcomes measured in adult offspring of mice exposed prenatally to e-cigarette aerosols. Environ. Health Perspect. 2020; 128(4): 047006-1-14. https://dx.doi.org/10.1289/EHP6067
73. Walayat A., Hosseini M., Nepal C., Li Y., Chen W., Chen Z. et al. Maternal e-cigarette exposure alters DNA methylome, site-specific CpG and CH methylation, and transcriptomic signatures in the neonatal brain. Sci. Rep. 2024; 14(1): 24263. https://dx.doi.org/10.1038/s41598-024-75986-x
74. Walayat A., Li Y., Zhang Y., Fu Y., Liu B., Shao X.M. et al. Fetal e-cigarette exposure programs a neonatal brain hypoxic-ischemic sensitive phenotype via altering DNA methylation patterns and autophagy signaling pathway. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2021; 321(5): R791-801. https://dx.doi.org/10.1152/ajpregu.00207.2021

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