Митохондриальный оксидативный стресс и болезни печени
https://doi.org/10.31146/1682-8658-ecg-228-8-143-157
Аннотация
Печень является важным органом обмена веществ и детоксикации и, следовательно, требует большого количества энергии, которая в основном вырабатывается митохондриями. Митохондриальный оксидативный стресс, который возникает, когда ферментативные и неферментативные антиоксиданты перегружаются активными формами кислорода (АФК), образующимися при различных патологических процессах. Это приводит к гепатоцеллюлярной дисфункции и, в конечном итоге, к фиброзу печени. Данный обзор посвящен современным представлениям патофизиологических основ митохондриального оксидативного стресса и его влиянию на развитие хронических заболеваний печени различной этиологии.
Об авторах
Г. В. Волынец
Федеральное государственное бюджетное образовательное учреждение высшего образования «Российский национальный исследовательский медицинский университет имени Н. И. Пирогова» Министерства здравоохранения Российской Федерации
Россия
Россия
А. И. Хавкин
ГБУЗ МО «Научно-исследовательский клинический институт детства Министерства здравоохранения Московской области»; Белгородский государственный исследовательский университет
Россия
Россия
Список литературы
1. Seen S. Chronic liver disease and oxidative stress - a narrative review. Expert Rev Gastroenterol Hepatol. 2021;15(9):1021-1035. https://doi.org/10.1080/17474124.2021.1949289.
2. Sepanlou S. G., Safiri S., Bisignano C. The global, regional, and national burden of cirrhosis by cause in 195 countries and territories, 1990-2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol. 2020;5(3):245-266. https://doi.org/10.1016/S2468-1253(19)30349-8.
3. Rui F., Yang H., Hu X., Xue Q., Xu Y., Shi J., Li J. Renaming NAFLD to MAFLD: advantages and potential changes in diagnosis, pathophysiology, treatment, and management. Infect Microb Dis. 2022;4(2):49-55. https://doi.org/10.1097/IM9.0000000000000089.
4. Anthony P. P., Ishak K. G., Nayak N. C., Poulsen H. E., Scheuer P. J., Sobin L. H. The morphology of cirrhosis. Recommendations on definition, nomenclature, and classification by a working group sponsored by the World Health Organization. J Clin Pathol. 1978;31(5):395-414. https://doi.org/10.1136/jcp.31.5.395.
5. Berumen J., Baglieri J., Kisseleva T., Mekeel K. Liver fibrosis: pathophysiology and clinical implications. WIREs Mech Dis. 2021;13(1): e1499. https://doi.org/10.1002/wsbm.1499.
6. Qian Z., Liang J., Huang R. et al. HBV integrations reshaping genomic structures promote hepatocellular carcinoma. Gut. 2024;73(7):1169-1182. https://doi.org/10.1136/gutjnl-2023-330414.
7. Wolfe W., Xiang Z., Yu X., Li P., Chen H., Yao M., Fe Yi., Huang Y., Yin Y., Xiao H. The challenge of applications of probiotics in gastrointestinal diseases. Advanced Gut & Microbiome Research. 2023. https://doi.org/10.1155/2023/1984200.
8. Marcellin P., Gane E., Buti M. et al. Regression of cirrhosis during treatment with tenofovir disoproxil fumarate for chronic hepatitis B: a 5-year open-label follow-up study. Lancet, 381 (9865) (2013), pp. 468-475 Y. Sun, J. Zhou, L. Wang, et al. New classification of liver biopsy assessment for fibrosis in chronic hepatitis B patients before and after treatment. Lancet. 2013;381(9865):468-75. https://doi.org/10.1016/S0140-6736(12)61425-1
9. Su TH, Kao JH, Liu CJ. Molecular mechanism and treatment of viral hepatitis-related liver fibrosis.Int J Mol Sci. 2014;15(6):10578-604. https://doi.org/10.3390/ijms150610578
10. Sun Y., Zhou J., Wang L. et al. New classification of liver biopsy assessment for fibrosis in chronic hepatitis B patients before and after treatment. Hepatology. 2017;65(5):1438-1450. https://doi.org/10.1002/hep.29009.
11. Wu J., Huang F., Ling Z. et al. Altered faecal microbiota on the expression of Th cells responses in the exacerbation of patients with hepatitis E infection. J Viral Hepat. 2020;27(11):1243-1252. https://doi.org/10.1111/jvh.13344.
12. Asrani S. K., Devarbhavi H., Eaton J., Kamath P. S. Burden of liver diseases in the world. J Hepatol. 2019;70(1):151-171. https://doi.org/10.1016/j.jhep.2018.09.014.
13. Chen P., Yao L., Yuan M., Wang Z., Zhang Q., Jiang Y., Li L. Mitochondrial dysfunction: A promising therapeutic target for liver diseases. Genes Dis. 2023;11(3):101115. https://doi.org/10.1016/j.gendis.2023.101115.
14. Middleton P., Vergis N. Mitochondrial dysfunction and liver disease: role, relevance, and potential for therapeutic modulation. Therap Adv Gastroenterol. 2021;14: 17562848211031394. https://doi.org/10.1177/ 17562848211031394.
15. Reichert A. S., Neupert W. Mitochondriomics or what makes us breathe. Trends Genet. 2004;20(11):555-62. https://doi.org/10.1016/j.tig.2004.08.012.
16. Vercellino I., Sazanov L. A. The assembly, regulation and function of the mitochondrial respiratory chain. Nat Rev Mol Cell Biol. 2022;23(2):141-161. https://doi.org/10.1038/s41580-021-00415-0.
17. Vakifahmetoglu-Norberg H., Ouchida A. T., Norberg E. The role of mitochondria in metabolism and cell death. Biochem Biophys Res Commun. 2017;482(3):426-431. https://doi.org/10.1016/j.bbrc.2016.11.088.
18. Horbay R., Bilyy R. Mitochondrial dynamics during cell cycling. Apoptosis. 2016;21(12):1327-1335. https://doi.org/10.1007/s10495-016-1295-5.
19. Youle R. J., van der Bliek A. M. Mitochondrial fission, fusion, and stress. Science. 2012; 337: 1062-1065.
20. Adebayo M., Singh S., Singh A. P., Dasgupta S. Mitochondrial fusion and fission: The fine-tune balance for cellular homeostasis. FASEB J. 2021 Jun;35(6): e21620. https://doi.org/10.1096/fj.202100067R.
21. Meyer J. N., Leuthner T. C., Luz A. L. Mitochondrial fusion, fission, and mitochondrial toxicity. Toxicology. 2017 Nov 1;391:42-53. https://doi.org/10.1016/j.tox.2017.07.019.
22. Yu F., Abdelwahid E., Xu T., Hu L., Wang M., Li Y., Mogharbel B. F., de Carvalho K. A.T., Guarita-Souza L.C., An Y., Li P. The role of mitochondrial fusion and fission in the process of cardiac oxidative stress. Histol Histopathol. 2020 Jun;35(6):541-552. https://doi.org/10.14670/HH-18-191.
23. Mansouri A., Gattolliat C. H., Asselah T. Mitochondrial dysfunction and signaling in chronic liver diseases. Gastroenterology. 2018;155(3):629-647. https://doi.org/10.1053/j.gastro.2018.06.083.
24. Rezzani R., Franco C. Liver, oxidative stress and metabolic syndromes. Nutrients. 2021;13(2):301. https://doi.org/10.3390/nu13020301.
25. Sies H. Oxidative stress: a concept in redox biology and medicine. Redox Biol. 2015;4:180-3. https://doi.org/10.1016/j.redox.2015.01.002.
26. Zorov D. B., Juhaszova M., Yaniv Y., Nuss H. B., Wang S., Sollott S. J. Regulation and pharmacology of the mitochondrial permeability transition pore. Cardiovasc Res. 2009;83(2):213-25. https://doi.org/10.1093/cvr/cvp151.
27. Bernardi P., Petronilli V. The permeability transition pore as a mitochondrial calcium release channel: a critical appraisal. J Bioenerg Biomembr. 1996;28(2):131-8. https://doi.org/10.1007/BF02110643.
28. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem J. 1999;341 (Pt 2)(Pt 2):233-49.
29. Zorov D. B., Filburn C. R., Klotz L. O., Zweier J. L., Sollott S. J. Reactive oxygen species (ROS)-induced ROS release: a new phenomenon accompanying induction of the mitochondrial permeability transition in cardiac myocytes. J Exp Med. 2000;192(7):1001-14. https://doi.org/10.1084/jem.192.7.1001.
30. Zorov D. B., Juhaszova M., Sollott S. J. Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev. 2014;94(3):909-50. https://doi.org/10.1152/physrev.00026.2013.
31. Gill S. S., Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem. 2010;48(12):909-30. https://doi.org/10.1016/j.plaphy.2010.08.016.
32. Shu L., Hu C., Xu M. et al. ATAD3B is a mitophagy receptor mediating clearance of oxidative stress-induced damaged mitochondrial DNA. EMBO J. 2021;40(8): e106283. https://doi.org/10.15252/embj.2020106283.
33. Zhang Y., Qi H., Taylor R., Xu W., Liu L. F., Jin S. The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy. 2007;3(4):337-46. https://doi.org/10.4161/auto.4127.
34. Moore M. P., Cunningham R. P., Meers G. M. et al.Compromised hepatic mitochondrial fatty acid oxidation and reduced markers of mitochondrial turnover in human NAFLD. Hepatology. 2022;76(5):1452-1465. https://doi.org/10.1002/hep.32324.
35. Kameoka S., Adachi Y., Okamoto K., Iijima M., Sesaki H. Phosphatidic Acid and Cardiolipin Coordinate Mitochondrial Dynamics. Trends Cell Biol. 2018;28(1):67-76. https://doi.org/10.1016/j.tcb.2017.08.011.
36. Chan D. C. Mitochondrial Dynamics and Its Involvement in Disease. Annu Rev Pathol. 2020;15:235-259. https://doi.org/10.1146/annurev-pathmechdis-012419-032711.
37. de Brito O. M., Scorrano L. Mitofusin 2 tethers endoplasmic reticulum to mitochondria. Nature. 2008;456(7222):605-10. https://doi.org/10.1038/nature07534.
38. Sukhorukov V. S., Voronkova A. S., Baranich T. I. et al. Molecular Mechanisms of Interactions between Mitochondria and the Endoplasmic Reticulum: A New Look at How Important Cell Functions are Supported. Mol Biol (Mosk). 2022;56(1):69-82. https://doi.org/10.31857/S0026898422010098.
39. Vara-Perez M., Felipe-Abrio B., Agostinis P. Mitophagy in Cancer: A Tale of Adaptation. Cells. 2019;8(5):493. https://doi.org/10.3390/cells8050493.
40. Adebayo M., Singh S., Singh A. P., Dasgupta S. Mitochondrial fusion and fssion: The fne-tune balance for cellular homeostasis. FASEB J. 2021;35(6): e21620. https://doi.org/10.1096/fj.202100067R.
41. Ban T., Ishihara T., Kohno H. et al. Molecular basis of selective mitochondrial fusion by heterotypic action between OPA1 and cardiolipin. Nat Cell Biol. 2017;19(7):856-863. https://doi.org/10.1038/ncb3560.
42. Kameoka S., Adachi Y., Okamoto K., Iijima M., Sesaki H. Phosphatidic Acid and Cardiolipin Coordinate Mitochondrial Dynamics. Trends Cell Biol. 2018;28(1):67-76. https://doi.org/10.1016/j.tcb.2017.08.011.
43. Song Z., Ghochani M., McCaffery J.M., Frey T. G., Chan D. C. Mitofusins and OPA1 mediate sequential steps in mitochondrial membrane fusion. Mol Biol Cell. 2009;20(15):3525-32. https://doi.org/10.1091/mbc.e09-03-0252.
44. Cipolat S., Martins de Brito O., Dal Zilio B., Scorrano L. OPA1 requires mitofusin 1 to promote mitochondrial fusion. Proc Natl Acad Sci U S A. 2004;101(45):15927-32. https://doi.org/10.1073/pnas.0407043101.
45. Ehses S., Raschke I., Mancuso G. et al. Regulation of OPA1 processing and mitochondrial fusion by m-AAA protease isoenzymes and OMA1. J Cell Biol. 2009;187(7):1023-36. https://doi.org/10.1083/jcb.200906084.
46. Griparic L., Kanazawa T., van der Bliek A. M. Regulation of the mitochondrial dynamin-like protein Opa1 by proteolytic cleavage. J Cell Biol. 2007;178(5):757-64. https://doi.org/10.1083/jcb.200704112.
47. Duvezin-Caubet S., Jagasia R., Wagener J., et al. Proteolytic processing of OPA1 links mitochondrial dysfunction to alterations in mitochondrial morphology. J Biol Chem. 2006;281(49):37972-9. https://doi.org/10.1074/jbc.M606059200.
48. Mishra P., Carelli V., Manfredi G., Chan D. C. Proteolytic cleavage of Opa1 stimulates mitochondrial inner membrane fusion and couples fusion to oxidative phosphorylation. Cell Metab. 2014;19(4):630-41. https://doi.org/10.1016/j.cmet.2014.03.011.
49. Del Dotto V., Mishra P., Vidoni S. et al. OPA1 Isoforms in the Hierarchical Organization of Mitochondrial Functions. Cell Rep. 2017;19(12):2557-2571. https://doi.org/10.1016/j.celrep.2017.05.073.
50. Youle R. J., van der Bliek A. M. Mitochondrial fission, fusion, and stress. Science. 2012;337(6098):1062-5. https://doi.org/10.1126/science.1219855.
51. Adebayo M., Singh S., Singh A. P., Dasgupta S. Mitochondrial fusion and fission: The fine-tune balance for cellular homeostasis. FASEB J. 2021;35(6): e21620. https://doi.org/10.1096/fj.202100067R.
52. Meyer J. N., Leuthner T. C., Luz A. L. Mitochondrial fusion, fission, and mitochondrial toxicity. Toxicology. 2017;391:42-53. https://doi.org/10.1016/j.tox.2017.07.019.
53. Yu F., Abdelwahid E., Xu T. et al. The role of mitochondrial fusion and fission in the process of cardiac oxidative stress. Histol Histopathol. 2020;35(6):541-552. https://doi.org/10.14670/HH-18-191.
54. Friedman J. R., Lackner L. L., West M., DiBenedetto J.R., Nunnari J., Voeltz G. K. ER tubules mark sites of mitochondrial division. Science. 2011;334(6054):358-62. https://doi.org/10.1126/science.1207385.
55. Chiu Y. H., Lin S. A., Kuo C. H., Li C. J. Molecular Machinery and Pathophysiology of Mitochondrial Dynamics. Front Cell Dev Biol. 2021;9:743892. https://doi.org/10.3389/fcell.2021.743892.
56. Jones A., Thornton C. Mitochondrial dynamics in the neonatal brain - a potential target following injury? Biosci Rep. 2022;42(3): BSR20211696. https://doi.org/10.1042/BSR20211696.
57. Kleele T., Rey T., Winter J. et al. Distinct fssion signatures predict mitochondrial degradation or biogenesis. Nature. 2021;593(7859):435-439. https://doi.org/10.1038/s41586-021-03510-6.
58. Narendra D. P., Youle R. J. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal. 2011;14(10):1929-38. https://doi.org/10.1089/ars.2010.3799.
59. Sprenger H. G., Langer T. The Good and the Bad of Mitochondrial Breakups. Trends Cell Biol. 2019;29(11):888-900. https://doi.org/10.1016/j.tcb.2019.08.003.
60. Li Y. J., Cao Y. L., Feng J. X. et al. Structural insights of human mitofusin-2 into mitochondrial fusion and CMT2A onset. Nat Commun. 2019;10(1):4914. https://doi.org/10.1038/s41467-019-12912-0.
61. Palmer C. S., Osellame L. D., Laine D., Koutsopoulos O. S., Frazier A. E., Ryan M. T. MiD49 and MiD51, new components of the mitochondrial fission machinery. EMBO Rep. 2011;12(6):565-73. https://doi.org/10.1038/embor.2011.54.
62. Smirnova E., Griparic L., Shurland D. L., van der Bliek A. M. Dynamin-related protein Drp1 is required for mitochondrial division in mammalian cells. Mol Biol Cell. 2001;12(8):2245-56. https://doi.org/10.1091/mbc.12.8.2245.
63. Guo R., Gu J., Zong S., Wu M., Yang M. Structure and mechanism of mitochondrial electron transport chain. Biomed J. 2018;41(1):9-20. https://doi.org/10.1016/j.bj.2017.12.001.
64. Macdonald P. J., Francy C. A., Stepanyants N. et al. Distinct Splice Variants of Dynamin-related Protein 1 Differentially Utilize Mitochondrial Fission Factor as an Effector of Cooperative GTPase Activity. J Biol Chem. 2016;291(1):493-507. https://doi.org/10.1074/jbc.M115.680181.
65. Francy C. A., Clinton R. W., Fröhlich C., Murphy C., Mears J. A. Cryo-EM Studies of Drp1 Reveal Cardiolipin Interactions that Activate the Helical Oligomer. Sci Rep. 2017;7(1):10744. https://doi.org/10.1038/s41598-017-11008-3
66. Yoon Y., Krueger E. W., Oswald B. J., McNiven M. A. The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynamin-like protein DLP1. Mol Cell Biol. 2003;23(15):5409-20. https://doi.org/10.1128/MCB.23.15.5409-5420.2003.
67. Yu R., Jin S. B., Lendahl U., Nistér M., Zhao J. Human Fis1 regulates mitochondrial dynamics through inhibition of the fusion machinery. EMBO J. 2019;38(8): e99748. https://doi.org/10.15252/embj.201899748.
68. Serasinghe M. N., Chipuk J. E. Mitochondrial Fission in Human Diseases. Handb Exp Pharmacol. 2017;240:159-188. https://doi.org/10.1007/164_2016_38.
69. Korobova F., Ramabhadran V., Higgs H. N. An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science. 2013;339(6118):464-7. https://doi.org/10.1126/science.1228360.
70. Kunkel G. H., Chaturvedi P., Tyagi S. C. Mitochondrial pathways to cardiac recovery: TFAM. Heart Fail Rev. 2016;21(5):499-517. https://doi.org/10.1007/s10741-016-9561-8.
71. Popov L. D. Mitochondrial biogenesis: An update. J Cell Mol Med. 2020;24(9):4892-4899. https://doi.org/10.1111/jcmm.15194.
72. Hu C., Zhang X., Wei W., Zhang N., Wu H., Ma Z., Li L., Deng W., Tang Q. Matrine attenuates oxidative stress and cardiomyocyte apoptosis in doxorubicin-induced cardiotoxicity via maintaining AMPK α/UCP2 pathway. Acta Pharm Sin B. 2019;9(4):690-701. https://doi.org/10.1016/j.apsb.2019.03.003
73. Schlaepfer I. R., Joshi M. CPT1A-mediated fat oxidation, mechanisms, and therapeutic potential. Endocrinology. 2020;161(2): bqz046. https://doi.org/10.1210/endocr/bqz046.
74. St-Pierre J., Drori S., Uldry M. et al. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell. 2006;127(2):397-408. https://doi.org/10.1016/j.cell.2006.09.024.
75. Han D., Dara L., Win S., Than T. A., Yuan L., Abbasi S. Q., Liu Z. X., Kaplowitz N. Regulation of drug-induced liver injury by signal transduction pathways: critical role of mitochondria. Trends Pharmacol Sci. 2013;34(4):243-53. https://doi.org/10.1016/j.tips.2013.01.009.
76. Li P. A., Hou X., Hao S. Mitochondrial biogenesis in neurodegeneration. J Neurosci Res. 2017;95(10):2025-2029. https://doi.org/10.1002/jnr.24042.
77. Dominy J. E., Puigserver P. Mitochondrial biogenesis through activation of nuclear signaling proteins. Cold Spring Harb Perspect Biol. 2013;5(7): a015008. https://doi.org/10.1101/cshperspect.a015008
78. Liu L., Li Y., Wang J. et al. Mitophagy receptor FUNDC1 is regulated by PGC-1α/NRF1 to fine tune mitochondrial homeostasis. EMBO Rep. 2021;22(3): e50629. https://doi.org/10.15252/embr.202050629.
79. Lin Q., Li S., Jiang N., Shao X. et al. PINK1-parkin pathway of mitophagy protects against contrast-induced acute kidney injury via decreasing mitochondrial ROS and NLRP3 inflammasome activation. Redox Biol. 2019;26:101254. https://doi.org/10.1016/j.redox.2019.101254
80. Rakovic A., Grünewald A., Kottwitz J., Brüggemann N., Pramstaller P. P., Lohmann K., Klein C. Mutations in PINK1 and Parkin impair ubiquitination of Mitofusins in human fibroblasts. PLoS One. 2011;6(3): e16746. https://doi.org/10.1371/journal.pone.0016746.
81. Vara-Perez M., Maes H., Van Dingenen S., Agostinis P. BNIP3 contributes to the glutamine-driven aggressive behavior of melanoma cells. Biol Chem. 2019;400(2):187-193. https://doi.org/10.1515/hsz-2018-0208.
82. Levine B., Kroemer G. Biological Functions of Autophagy Genes: A Disease Perspective. Cell. 2019;176(1-2):11-42. https://doi.org/10.1016/j.cell.2018.09.048.
83. Rogov V., Dötsch V., Johansen T., Kirkin V.Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53(2):167-78. https://doi.org/10.1016/j.molcel.2013.12.014.
84. Wild P., McEwan D.G., Dikic I. The LC3 interactome at a glance. J Cell Sci. 2014;127(Pt 1):3-9. https://doi.org/10.1242/jcs.140426.
85. Galluzzi L., Baehrecke E. H., Ballabio A. et al. Molecular definitions of autophagy and related processes. EMBO J. 2017;36(13):1811-1836. https://doi.org/10.15252/embj.201796697.
86. Pickrell A. M., Youle R. J. The roles of PINK1, parkin, and mitochondrial fidelity in Parkinson’s disease. Neuron. 2015;85(2):257-73. https://doi.org/10.1016/j.neuron.2014.12.007.
87. Wang Q., Bu Q., Liu M. et al. XBP1-mediated activation of the STING signalling pathway in macrophages contributes to liver fibrosis progression. JHEP Rep. 2022;4(11):100555. https://doi.org/10.1016/j.jhepr.2022.100555.
88. Wu N. N., Wang L., Wang L., Xu X., Lopaschuk G. D., Zhang Y., Ren J. Site-specific ubiquitination of VDAC1 restricts its oligomerization and mitochondrial DNA release in liver fibrosis. Exp Mol Med. 2023;55(1):269-280. https://doi.org/10.1038/s12276-022-00923-9.
89. Lamanilao G. G., Dogan M., Patel P. S. et al. Key hepatoprotective roles of mitochondria in liver regeneration. Am J Physiol Gastrointest Liver Physiol. 2023;324(3): G207-G218. https://doi.org/10.1152/ajpgi.00220.2022.
90. Arduini A., Serviddio G., Escobar J., Tormos A. M., Bellanti F., Viña J., Monsalve M., Sastre J. Mitochondrial biogenesis fails in secondary biliary cirrhosis in rats leading to mitochondrial DNA depletion and deletions. Am J Physiol Gastrointest Liver Physiol. 2011;301(1): G119-27. https://doi.org/10.1152/ajpgi.00253.2010.
91. Larosche I., Lettéron P., Fromenty B., Vadrot N., Abbey-Toby A., Feldmann G., Pessayre D., Mansouri A. Tamoxifen inhibits topoisomerases, depletes mitochondrial DNA, and triggers steatosis in mouse liver. J Pharmacol Exp Ther. 2007;321(2):526-35. https://doi.org/10.1124/jpet.106.114546.
92. Liang Y. J., Teng W., Chen C. L. et al. Clinical Implications of HBV PreS/S Mutations and the Effects of PreS2 Deletion on Mitochondria, Liver Fibrosis, and Cancer Development. Hepatology. 2021;74(2):641-655. https://doi.org/10.1002/hep.31789.
93. Sekine S., Ito K., Watanabe H., Nakano T. et al. Mitochondrial iron accumulation exacerbates hepatic toxicity caused by hepatitis C virus core protein. Toxicol Appl Pharmacol. 2015;282(3):237-43. https://doi.org/10.1016/j.taap.2014.12.004.
94. Dionisio N., Garcia-Mediavilla M.V., Sanchez-Campos S. et al. Hepatitis C virus NS5A and core proteins induce oxidative stress-mediated calcium signalling alterations in hepatocytes. J Hepatol. 2009;50(5):872-82. https://doi.org/10.1016/j.jhep.2008.12.026
95. Pal S., Polyak S. J., Bano N., Qiu W. C., Carithers R. L., Shuhart M., Gretch D. R., Das A. Hepatitis C virus induces oxidative stress, DNA damage and modulates the DNA repair enzyme NEIL1. J Gastroenterol Hepatol. 2010;25(3):627-34. https://doi.org/10.1111/j.1440-1746.2009.06128.x.
96. Smirnova O. A., Ivanova O. N., Bartosch B. et al. Hepatitis C Virus NS5A Protein Triggers Oxidative Stress by Inducing NADPH Oxidases 1 and 4 and Cytochrome P450 2E1. Oxid Med Cell Longev. 2016;2016:8341937. https://doi.org/10.1155/2016/8341937.
97. Hara Y., Hino K., Okuda M., Furutani T. et al. Hepatitis C virus core protein inhibits deoxycholic acid-mediated apoptosis despite generating mitochondrial reactive oxygen species. J Gastroenterol. 2006;41(3):257-268.
98. Ríos-Ocampo W.A., Daemen T., Buist-Homan M., Faber K. N., Navas M. C., Moshage H. Hepatitis C virus core or NS3/4A protein expression preconditions hepatocytes against oxidative stress and endoplasmic reticulum stress. Redox Rep. 2019;24(1):17-26. https://doi.org/10.1080/13510002.2019.1596431.
99. Seo Y. L., Heo S., Jang K. L. Hepatitis C virus core protein overcomes H2O2-induced apoptosis by downregulating p14 expression via DNA methylation. J Gen Virol. 2015;96(Pt 4):822-832. https://doi.org/10.1099/vir.0.000032.
100. Miura K., Taura K., Kodama Y., Schnabl B., Brenner D. A. Hepatitis C virus-induced oxidative stress suppresses hepcidin expression through increased histone deacetylase activity. Hepatology. 2008;48(5):1420-9. https://doi.org/10.1002/hep.22486.
101. Medvedev R., Ploen D., Spengler C., Elgner F., Ren H., Bunten S., Hildt E. HCV-induced oxidative stress by inhibition of Nrf2 triggers autophagy and favors release of viral particles. Free Radic Biol Med. 2017;110:300-315. https://doi.org/10.1016/j.freeradbiomed.2017.06.021.
102. Anticoli S., Amatore D., Matarrese P., De Angelis M., Palamara A. T., Nencioni L., Ruggieri A. Counteraction of HCV-induced oxidative stress concurs to establish chronic infection in liver cell cultures. Oxid Med Cell Longev. 2019;2019:6452390. https://doi.org/10.1155/2019/6452390.
103. Zai W., Hu K., Ye J. et al. Long-Term Hepatitis B Virus Infection Induces Cytopathic Effects in Primary Human Hepatocytes, and Can Be Partially Reversed by Antiviral Therapy. Microbiol Spectr. 2022;10(1): e0132821. https://doi.org/10.1128/spectrum.01328-21
104. Kim S. J., Khan M., Quan J., Till A., Subramani S., Siddiqui A. Hepatitis B virus disrupts mitochondrial dynamics: induces fission and mitophagy to attenuate apoptosis. PLoS Pathog. 2013;9(12): e1003722. https://doi.org/10.1371/journal.ppat.1003722.
105. Kim S. J., Syed G. H., Khan M., Chiu W. W., Sohail M. A., Gish R. G., Siddiqui A. Hepatitis C virus triggers mitochondrial fission and attenuates apoptosis to promote viral persistence. Proc Natl Acad Sci U S A. 2014;111(17):6413-8. https://doi.org/10.1073/pnas.1321114111.
106. Duygu F., Karsen H., Aksoy N., Taskin A. Relationship of oxidative stress in hepatitis B infection activity with HBV DNA and fibrosis. Ann Lab Med. 2012;32(2):113-8. https://doi.org/10.3343/alm.2012.32.2.113.
107. Lin Y. T., Liu W., He Y., Wu Y. L., Chen W. N., Lin X. J., Lin X. Hepatitis B virus X protein increases 8-Oxo-7,8-Dihydro-2’-Deoxyguanosine (8-Oxodg) level via repressing MTH1/ MTH2 expression in hepatocytes. Cell Physiol Biochem. 2018;51(1):80-96. https://doi.org/10.1159/000495166.
108. Jung S. Y., Kim Y. J. C-terminal region of HBx is crucial for mitochondrial DNA damage. Cancer Lett. 2013;331(1):76-83. https://doi.org/10.1016/j.canlet.2012.12.004.
109. Poungpairoj P., Whongsiri P., Suwannasin S., Khlaiphuengsin A., Tangkijvanich P., Boonla C. Increased oxidative stress and RUNX3 hypermethylation in patients with hepatitis B virus-associated hepatocellular carcinoma (HCC) and induction of RUNX3 hypermethylation by reactive oxygen species in HCC cells. Asian Pac J Cancer Prev. 2015;16(13):5343-8. https://doi.org/10.7314/apjcp.2015.16.13.5343.
110. Domínguez-Pérez M., Simoni-Nieves A., Rosales P. et al. Cholesterol burden in the liver induces mitochondrial dynamic changes and resistance to apoptosis. J Cell Physiol. 2019;234(5):7213-7223. https://doi.org/10.1002/jcp.27474.
111. Galloway C. A., Lee H., Brookes P. S., Yoon Y. Decreasing mitochondrial fission alleviates hepatic steatosis in a murine model of nonalcoholic fatty liver disease. Am J Physiol Gastrointest Liver Physiol. 2014;307(6): G632-41. https://doi.org/10.1152/ajpgi.00182.2014.
112. Steffen J., Ngo J., Wang S. P. et al. The mitochondrial fission protein Drp1 in liver is required to mitigate NASH and prevents the activation of the mitochondrial ISR. Mol Metab. 2022;64:101566. https://doi.org/10.1016/j.molmet.2022.101566.
113. Piccinin E., Villani G., Moschetta A. Metabolic aspects in NAFLD, NASH and hepatocellular carcinoma: the role of PGC1 coactivators. Nat Rev Gastroenterol Hepatol. 2019;16(3):160-174. https://doi.org/10.1038/s41575-018-0089-3.
114. Afonso M. B., Islam T., Magusto J. et al. RIPK3 dampens mitochondrial bioenergetics and lipid droplet dynamics in metabolic liver disease. Hepatology. 2023;77(4):1319-1334. https://doi.org/10.1002/hep.32756.
115. Lagouge M., Argmann C., Gerhart-Hines Z. et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell. 2006;127(6):1109-22. https://doi.org/10.1016/j.cell.2006.11.013.
116. Moore M. P., Cunningham R. P., Meers G. M. et al.Compromised hepatic mitochondrial fatty acid oxidation and reduced markers of mitochondrial turnover in human NAFLD. Hepatology. 2022;76(5):1452-1465. https://doi.org/10.1002/hep.32324.
117. Morris E. M., Meers G. M., Booth F. W., Fritsche K. L., Hardin C. D., Thyfault J. P., Ibdah J. A. PGC-1α overexpression results in increased hepatic fatty acid oxidation with reduced triacylglycerol accumulation and secretion. Am J Physiol Gastrointest Liver Physiol. 2012;303(8): G979-92. https://doi.org/10.1152/ajpgi.00169.2012.
118. Miao H., Ouyang H., Guo Q., Wei M., Lu B., Kai G., Ji L. Chlorogenic acid alleviated liver fibrosis in methionine and choline deficient diet-induced nonalcoholic steatohepatitis in mice and its mechanism. J Nutr Biochem. 2022;106:109020. https://doi.org/10.1016/j.jnutbio.2022.109020.
119. Liu R., Zhang H., Zhang Y. et al. Peroxisome proliferator-activated receptor gamma coactivator-1 alpha acts as a tumor suppressor in hepatocellular carcinoma. Tumour Biol. 2017;39(4):1010428317695031. https://doi.org/10.1177/1010428317695031.
120. Wang B., Hsu S. H., Frankel W., Ghoshal K., Jacob S. T. Stat3-mediated activation of microRNA-23a suppresses gluconeogenesis in hepatocellular carcinoma by down-regulating glucose-6-phosphatase and peroxisome proliferator-activated receptor gamma, coactivator 1 alpha. Hepatology. 2012;56(1):186-97. https://doi.org/10.1002/hep.25632.
121. Xu J., Ji L., Ruan Y. et al. UBQLN1 mediates sorafenib resistance through regulating mitochondrial biogenesis and ROS homeostasis by targeting PGC1β in hepatocellular carcinoma. Signal Transduct Target Ther. 2021;6(1):190. https://doi.org/10.1038/s41392-021-00594-4.
122. Kang J. W., Hong J. M., Lee S. M. Melatonin enhances mitophagy and mitochondrial biogenesis in rats with carbon tetrachloride-induced liver fibrosis. J Pineal Res. 2016;60(4):383-93. https://doi.org/10.1111/jpi.12319.
123. Han D., Johnson H. S., Rao M. P. et al. Mitochondrial remodeling in the liver following chronic alcohol feeding to rats. Free Radic Biol Med. 2017;102:100-110. https://doi.org/10.1016/j.freeradbiomed.2016.11.020.
124. Palma E., Ma X., Riva A. et al. Dynamin-1-Like Protein Inhibition Drives Megamitochondria Formation as an Adaptive Response in Alcohol-Induced Hepatotoxicity. Am J Pathol. 2019;189(3):580-589. https://doi.org/10.1016/j.ajpath.2018.11.008.
125. Ma X., Chen A., Melo L. et al. Loss of hepatic DRP1 exacerbates alcoholic hepatitis by inducing megamitochondria and mitochondrial maladaptation. Hepatology. 2023;77(1):159-175. https://doi.org/10.1002/hep.32604.
126. Han D., Ybanez M. D., Johnson H. S. et al. Dynamic adaptation of liver mitochondria to chronic alcohol feeding in mice: biogenesis, remodeling, and functional alterations. J Biol Chem. 2012;287(50):42165-79. https://doi.org/10.1074/jbc.M112.377374.
Рецензия
Для цитирования:
Волынец Г.В., Хавкин А.И. Митохондриальный оксидативный стресс и болезни печени. Экспериментальная и клиническая гастроэнтерология. 2024;(8):143-157. https://doi.org/10.31146/1682-8658-ecg-228-8-143-157
For citation:
Volynets G.V., Khavkin A.I. Mitochondrial oxidative stress and liver disease. Experimental and Clinical Gastroenterology. 2024;(8):143-157. (In Russ.) https://doi.org/10.31146/1682-8658-ecg-228-8-143-157
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