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Research Progress on Histone Deacetylases Regulating Programmed Cell Death in Atherosclerosis

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Abstract

Histone deacetylases (HDACs) are epigenetic modifying enzyme that is closely related to chromatin structure and gene transcription, and numerous studies have found that HDACs play an important regulatory role in atherosclerosis disease. Apoptosis, autophagy and programmed necrosis as the three typical programmed cell death modalities that can lead to cell loss and are closely related to the developmental process of atherosclerosis. In recent years, accumulating evidence has shown that the programmed cell death mediated by HDACs is increasingly important in the pathophysiology of atherosclerosis. This paper first gives a brief overview of HDACs, the mechanism of programmed cell death, and their role in atherosclerosis, and then further elaborates on the role and mechanism of HDACs in regulating apoptosis, autophagy, and programmed necrosis in atherosclerosis, respectively, to provide new effective measures and theoretical basis for the prevention and treatment of atherosclerosis.

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References

  1. Arnett DK, Blumenthal RS, Albert MA, et al. 2019 ACC/AHA guideline on the primary prevention of cardiovascular disease: a report of the American College of Cardiology/American Heart Association Task Force on clinical practice guidelines. Circulation. 2019;140(11):e596–646. https://doi.org/10.1161/cir.0000000000000678.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Narula N, Olin JW, Narula N. Pathologic disparities between peripheral artery disease and coronary artery disease. Arterioscler Thromb Vasc Biol. 2020;40(9):1982–9. https://doi.org/10.1161/atvbaha.119.312864.

    Article  CAS  PubMed  Google Scholar 

  3. Malekmohammad K, Sewell R, Rafieian-Kopaei M. Antioxidants and atherosclerosis: mechanistic aspects. Biomolecules. 2019;9:8. https://doi.org/10.3390/biom9080301.

    Article  CAS  Google Scholar 

  4. Yurdagul AJ. Crosstalk between macrophages and vascular smooth muscle cells in atherosclerotic plaque stability. Arterioscler Thromb Vasc Biol. 2022;42(4):372–80. https://doi.org/10.1161/atvbaha.121.316233.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Lin Y, Qiu T, Wei G, et al. Role of histone post-translational modifications in inflammatory diseases. Front Immunol. 2022;13:852272. https://doi.org/10.3389/fimmu.2022.852272.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Imai S, Armstrong CM, Kaeberlein M, et al. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000;403(6771):795–800. https://doi.org/10.1038/35001622.

    Article  CAS  PubMed  Google Scholar 

  7. Lecce L, Xu Y, V'Gangula B, et al. Histone deacetylase 9 promotes endothelial-mesenchymal transition and an unfavorable atherosclerotic plaque phenotype. J Clin Invest. 2021;131(15) https://doi.org/10.1172/jci131178.

  8. Zhao Y, Jia X, Yang X, et al. Deacetylation of Caveolin-1 by Sirt6 induces autophagy and retards high glucose-stimulated LDL transcytosis and atherosclerosis formation. Metabolism. 2022;131:155162. https://doi.org/10.1016/j.metabol.2022.155162.

    Article  CAS  PubMed  Google Scholar 

  9. Yao F, Jin Z, Zheng Z, et al. HDAC11 promotes both NLRP3/caspase-1/GSDMD and caspase-3/GSDME pathways causing pyroptosis via ERG in vascular endothelial cells. Cell Death Dis. 2022;8(1):112. https://doi.org/10.1038/s41420-022-00906-9.

    Article  CAS  Google Scholar 

  10. Liu C, Jiang Z, Pan Z, et al. The function, regulation and mechanism of programmed cell death of macrophages in atherosclerosis. Front Cell Dev Biol. 2021;9:809516. https://doi.org/10.3389/fcell.2021.809516.

    Article  PubMed  Google Scholar 

  11. D'Arcy MS. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int. 2019;43(6):582–92. https://doi.org/10.1002/cbin.11137.

    Article  PubMed  Google Scholar 

  12. Zhang X, Lu J, Zhang Q, et al. CircRNA RSF1 regulated ox-LDL induced vascular endothelial cells proliferation, apoptosis and inflammation through modulating miR-135b-5p/HDAC1 axis in atherosclerosis. Biol Res. 2021;54(1):11. https://doi.org/10.1186/s40659-021-00335-5.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yuan P, Hu Q, He X, et al. Laminar flow inhibits the Hippo/YAP pathway via autophagy and SIRT1-mediated deacetylation against atherosclerosis. Cell Death Dis. 2020;11(2):141. https://doi.org/10.1038/s41419-020-2343-1.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chen J, Zhang J, Wu J, et al. Low shear stress induced vascular endothelial cell pyroptosis by TET2/SDHB/ROS pathway. Free Radic Biol Med. 2021;162:582–91. https://doi.org/10.1016/j.freeradbiomed.2020.11.017.

    Article  CAS  PubMed  Google Scholar 

  15. Shvedunova M, Akhtar A. Modulation of cellular processes by histone and non-histone protein acetylation. Nat Rev Mol Cell Biol. 2022;23(5):329–49. https://doi.org/10.1038/s41580-021-00441-y.

    Article  CAS  PubMed  Google Scholar 

  16. Alaskhar AB, Khalaila R, Wolf J, et al. Histone modifications and their role in epigenetics of atopy and allergic diseases. Allergy Asthma Clin Immunol. 2018;14:39. https://doi.org/10.1186/s13223-018-0259-4.

    Article  CAS  Google Scholar 

  17. Gregoretti IV, Lee YM, Goodson HV. Molecular evolution of the histone deacetylase family: functional implications of phylogenetic analysis. J Mol Biol. 2004;338(1):17–31. https://doi.org/10.1016/j.jmb.2004.02.006.

    Article  CAS  PubMed  Google Scholar 

  18. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet. 2009;10(1):32–42. https://doi.org/10.1038/nrg2485.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Grootaert M, Finigan A, Figg NL, et al. SIRT6 protects smooth muscle cells from senescence and reduces atherosclerosis. Circ Res. 2021;128(4):474–91. https://doi.org/10.1161/circresaha.120.318353.

    Article  CAS  PubMed  Google Scholar 

  20. Asare Y, Campbell-James TA, Bokov Y, et al. Histone deacetylase 9 activates IKK to regulate atherosclerotic plaque vulnerability. Circ Res. 2020;127(6):811–23. https://doi.org/10.1161/circresaha.120.316743.

    Article  CAS  PubMed  Google Scholar 

  21. Slee EA, Adrain C, Martin SJ. Executioner caspase-3, -6, and -7 perform distinct, non-redundant roles during the demolition phase of apoptosis. J Biol Chem. 2001;276(10):7320–6. https://doi.org/10.1074/jbc.m008363200.

    Article  CAS  PubMed  Google Scholar 

  22. Goldar S, Khaniani MS, Derakhshan SM, et al. Molecular mechanisms of apoptosis and roles in cancer development and treatment. Asian Pac J Cancer Prev. 2015;16(6):2129–44. https://doi.org/10.7314/apjcp.2015.16.6.2129.

    Article  PubMed  Google Scholar 

  23. Liu H, Su D, Zhang J, et al. Author correction: improvement of pharmacokinetic profile of TRAIL via trimer-tag enhances its antitumor activity in vivo. Sci Rep. 2018;8(1):5266. https://doi.org/10.1038/s41598-018-23057-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Cavalcante GC, Schaan AP, Cabral GF, et al. A cell’s fate: an overview of the molecular biology and genetics of apoptosis. Int J Mol Sci. 2019;20(17) https://doi.org/10.3390/ijms20174133.

  25. Kong YY, Li GQ, Zhang WJ, et al. Nicotinamide phosphoribosyltransferase aggravates inflammation and promotes atherosclerosis in ApoE knockout mice. Acta Pharmacol Sin. 2019;40(9):1184–92. https://doi.org/10.1038/s41401-018-0207-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Gonçalves I, Singh P, Tengryd C, et al. sTRAIL-R2 (soluble TNF [tumor necrosis factor]-related apoptosis-inducing ligand receptor 2) a marker of plaque cell apoptosis and cardiovascular events. Stroke. 2019;50(8):1989–96. https://doi.org/10.1161/strokeaha.119.024379.

    Article  PubMed  Google Scholar 

  27. Singh R, Letai A, Sarosiek K. Regulation of apoptosis in health and disease: the balancing act of BCL-2 family proteins. Nat Rev Mol Cell Biol. 2019;20(3):175–93. https://doi.org/10.1038/s41580-018-0089-8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Shakeri R, Kheirollahi A, Davoodi J. Apaf-1: regulation and function in cell death. Biochimie. 2017;135:111–25. https://doi.org/10.1016/j.biochi.2017.02.001.

    Article  CAS  PubMed  Google Scholar 

  29. Xu Y, Zhang Y, Xu Y, et al. Activation of CD137 signaling promotes macrophage apoptosis dependent on p38 MAPK pathway-mediated mitochondrial fission. Int J Biochem Cell Biol. 2021;136:106003. https://doi.org/10.1016/j.biocel.2021.106003.

    Article  CAS  PubMed  Google Scholar 

  30. Gu L, Ye P, Li H, et al. Lunasin attenuates oxidant-induced endothelial injury and inhibits atherosclerotic plaque progression in ApoE−/− mice by up-regulating heme oxygenase-1via PI3K/Akt/Nrf2/ARE pathway. FASEB J. 2019;33(4):4836–50. https://doi.org/10.1096/fj.201802251r.

    Article  CAS  PubMed  Google Scholar 

  31. Groenendyk J, Sreenivasaiah PK, Kim DH, et al. Biology of endoplasmic reticulum stress in the heart. Circ Res. 2010;107(10):1185–97. https://doi.org/10.1161/circresaha.110.227033.

    Article  CAS  PubMed  Google Scholar 

  32. Li B, Yi P, Zhang B, et al. Differences in endoplasmic reticulum stress signalling kinetics determine cell survival outcome through activation of MKP-1. Cell Signal. 2011;23(1):35–45. https://doi.org/10.1016/j.cellsig.2010.07.019.

    Article  CAS  PubMed  Google Scholar 

  33. Yang Y, Liu L, Naik I, et al. Transcription factor C/EBP homologous protein in health and diseases. Front Immunol. 2017;8:1612. https://doi.org/10.3389/fimmu.2017.01612.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Song S, Tan J, Miao Y, et al. Crosstalk of autophagy and apoptosis: involvement of the dual role of autophagy under ER stress. J Cell Physiol. 2017;232(11):2977–84. https://doi.org/10.1002/jcp.25785.

    Article  CAS  PubMed  Google Scholar 

  35. Ge P, Gao M, Du J, et al. Downregulation of microRNA-512-3p enhances the viability and suppresses the apoptosis of vascular endothelial cells, alleviates autophagy and endoplasmic reticulum stress as well as represses atherosclerotic lesions in atherosclerosis by adjusting spliced/unspliced ratio of X-box binding protein 1 (XBP-1S/XBP-1U). Bioengineered. 2021;12(2):12469–81. https://doi.org/10.1080/21655979.2021.2006862.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Geng J, Xu H, Fu W, et al. Rosuvastatin protects against endothelial cell apoptosis in vitro and alleviates atherosclerosis in ApoE-/- mice by suppressing endoplasmic reticulum stress. Exp Ther Med. 2020;20(1):550–60. https://doi.org/10.3892/etm.2020.8733.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40(2):280–93. https://doi.org/10.1016/j.molcel.2010.09.023.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Li XQ, Wang J, Fang B, et al. Intrathecal antagonism of microglial TLR4 reduces inflammatory damage to blood-spinal cord barrier following ischemia/reperfusion injury in rats. Mol Brain. 2014;7:28. https://doi.org/10.1186/1756-6606-7-28.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Zhou T, Liang L, Liang Y, et al. Mild hypothermia protects hippocampal neurons against oxygen-glucose deprivation/reperfusion-induced injury by improving lysosomal function and autophagic flux. Exp Cell Res. 2017;358(2):147–60. https://doi.org/10.1016/j.yexcr.2017.06.010.

    Article  CAS  PubMed  Google Scholar 

  40. Ohsumi Y. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. 2001;2(3):211–6. https://doi.org/10.1038/35056522.

    Article  CAS  PubMed  Google Scholar 

  41. Bjorkoy G, Lamark T, Brech A, et al. p62/SQSTM1 forms protein aggregates degraded by autophagy and has a protective effect on huntingtin-induced cell death. J Cell Biol. 2005;171(4):603–14. https://doi.org/10.1083/jcb.200507002.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Xu J, Kitada M, Ogura Y, et al. Relationship between autophagy and metabolic syndrome characteristics in the pathogenesis of atherosclerosis. Front Cell Dev Biol. 2021;9:641852. https://doi.org/10.3389/fcell.2021.641852.

    Article  PubMed  PubMed Central  Google Scholar 

  43. Tang Y, Wu H, Shao B, et al. Celosins inhibit atherosclerosis in ApoE(-/-) mice and promote autophagy flow. J Ethnopharmacol. 2018;215:74–82. https://doi.org/10.1016/j.jep.2017.12.031.

    Article  CAS  PubMed  Google Scholar 

  44. Xiong Q, Yan Z, Liang J, et al. Polydatin alleviates high-fat diet induced atherosclerosis in apolipoprotein E-deficient mice by autophagic restoration. Phytomedicine. 2021;81:153301. https://doi.org/10.1016/j.phymed.2020.153301.

    Article  CAS  PubMed  Google Scholar 

  45. Dong Y, Chen H, Gao J, et al. Molecular machinery and interplay of apoptosis and autophagy in coronary heart disease. J Mol Cell Cardiol. 2019;136:27–41. https://doi.org/10.1016/j.yjmcc.2019.09.001.

    Article  CAS  PubMed  Google Scholar 

  46. Carresi C, Mollace R, Macri R, et al. Oxidative stress triggers defective autophagy in endothelial cells: role in atherothrombosis development. Antioxidants (Basel). 2021;10(3) https://doi.org/10.3390/antiox10030387.

  47. Kaczmarek A, Vandenabeele P, Krysko DV. Necroptosis: the release of damage-associated molecular patterns and its physiological relevance. Immunity. 2013;38(2):209–23. https://doi.org/10.1016/j.immuni.2013.02.003.

    Article  CAS  PubMed  Google Scholar 

  48. Deng J. Advanced research on the regulated necrosis mechanism in myocardial ischemia-reperfusion injury. Int J Cardiol. 2021;334:97–101. https://doi.org/10.1016/j.ijcard.2021.04.042.

    Article  PubMed  Google Scholar 

  49. Bertheloot D, Latz E, Franklin BS. Necroptosis, pyroptosis and apoptosis: an intricate game of cell death. Cell Mol Immunol. 2021;18(5):1106–21. https://doi.org/10.1038/s41423-020-00630-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Li M, Wang ZW, Fang LJ, et al. Programmed cell death in atherosclerosis and vascular calcification. Cell Death Dis. 2022;13(5):467. https://doi.org/10.1038/s41419-022-04923-5.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Karunakaran D, Geoffrion M, Wei L, et al. Targeting macrophage necroptosis for therapeutic and diagnostic interventions in atherosclerosis. Sci Adv. 2016;2(7):e1600224. https://doi.org/10.1126/sciadv.1600224.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lin J, Li H, Yang M, et al. A role of RIP3-mediated macrophage necrosis in atherosclerosis development. Cell Rep. 2013;3(1):200–10. https://doi.org/10.1016/j.celrep.2012.12.012.

    Article  CAS  PubMed  Google Scholar 

  53. Yu P, Zhang X, Liu N, et al. Pyroptosis: mechanisms and diseases. Signal Transduct Target Ther. 2021;6(1):128. https://doi.org/10.1038/s41392-021-00507-5.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Shi J, Zhao Y, Wang K, et al. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature. 2015;526(7575):660–5. https://doi.org/10.1038/nature15514.

    Article  CAS  PubMed  Google Scholar 

  55. Hoseini Z, Sepahvand F, Rashidi B, et al. NLRP3 inflammasome: Its regulation and involvement in atherosclerosis. J Cell Physiol. 2018;233(3):2116–32. https://doi.org/10.1002/jcp.25930.

    Article  CAS  PubMed  Google Scholar 

  56. Wu X, Zhang H, Qi W, et al. Nicotine promotes atherosclerosis via ROS-NLRP3-mediated endothelial cell pyroptosis. Cell Death Dis. 2018;9(2):171. https://doi.org/10.1038/s41419-017-0257-3.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Oh S, Son M, Park CH, et al. The reducing effects of pyrogallol-phloroglucinol-6,6-bieckol on high-fat diet-induced pyroptosis in endothelial and vascular smooth muscle cells of mice aortas. Mar Drugs. 2020;18(12) https://doi.org/10.3390/md18120648.

  58. Xu T, Ding W, Ji X, et al. Molecular mechanisms of ferroptosis and its role in cancer therapy. J Cell Mol Med. 2019;23(8):4900–12. https://doi.org/10.1111/jcmm.14511.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Wu X, Li Y, Zhang S, et al. Ferroptosis as a novel therapeutic target for cardiovascular disease. Theranostics. 2021;11(7):3052–9. https://doi.org/10.7150/thno.54113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Xiao L, Luo G, Guo X, et al. Macrophage iron retention aggravates atherosclerosis: evidence for the role of autocrine formation of hepcidin in plaque macrophages. Biochim Biophys Acta Mol Cell Biol Lipids. 2020;1865(2):158531. https://doi.org/10.1016/j.bbalip.2019.158531.

    Article  CAS  PubMed  Google Scholar 

  61. Fu F, Lai Q, Hu J, et al. Ruscogenin alleviates myocardial ischemia-induced ferroptosis through the activation of BCAT1/BCAT2. Antioxidants (Basel). 2022;11(3) https://doi.org/10.3390/antiox11030583.

  62. Su G, Yang W, Wang S, et al. SIRT1-autophagy axis inhibits excess iron-induced ferroptosis of foam cells and subsequently increases IL-1Beta and IL-18. Biochem Biophys Res Commun. 2021;561:33–9. https://doi.org/10.1016/j.bbrc.2021.05.011.

    Article  CAS  PubMed  Google Scholar 

  63. Kruger-Genge A, Blocki A, Franke RP, et al. Vascular endothelial cell biology: an update. Int J Mol Sci. 2019;20(18) https://doi.org/10.3390/ijms20184411.

  64. Shiotsugu S, Okinaga T, Habu M, et al. The biological effects of interleukin-17A on adhesion molecules expression and foam cell formation in atherosclerotic lesions. J Interferon Cytokine Res. 2019;39(11):694–702. https://doi.org/10.1089/jir.2019.0034.

    Article  CAS  PubMed  Google Scholar 

  65. Liu H, Wang H, Ma J, et al. MicroRNA-146a-3p/HDAC1/KLF5/IKBalpha signal axis modulates plaque formation of atherosclerosis mice. Life Sci. 2021;284:119615. https://doi.org/10.1016/j.lfs.2021.119615.

    Article  CAS  PubMed  Google Scholar 

  66. Wang H, Sugimoto K, Lu H, et al. HDAC1-mediated deacetylation of HIF1alpha prevents atherosclerosis progression by promoting miR-224-3p-mediated inhibition of FOSL2. Mol Ther Nucleic Acids. 2021;23:577–91. https://doi.org/10.1016/j.omtn.2020.10.044.

    Article  CAS  PubMed  Google Scholar 

  67. Khanahmadi M, Manafi B, Tayebinia H, et al. Downregulation of Sirt1 is correlated to upregulation of p53 and increased apoptosis in epicardial adipose tissue of patients with coronary artery disease. EXCLI J. 2020;19:1387–98. https://doi.org/10.17179/excli2020-2423.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Hao Y, Yang Z, Li Q, et al. 5-Heptadecylresorcinol protects against atherosclerosis in apolipoprotein E-deficient mice by modulating SIRT3 signaling: the possible beneficial effects of whole grain consumption. Mol Nutr Food Res. 2022;66(9):e2101114. https://doi.org/10.1002/mnfr.202101114.

    Article  CAS  PubMed  Google Scholar 

  69. Seimon T, Tabas I. Mechanisms and consequences of macrophage apoptosis in atherosclerosis. J Lipid Res. 2009;50:S382–7. https://doi.org/10.1194/jlr.r800032-jlr200.

    Article  PubMed  PubMed Central  Google Scholar 

  70. Hoeksema MA, Gijbels MJ, Van den Bossche J, et al. Targeting macrophage Histone deacetylase 3 stabilizes atherosclerotic lesions. EMBO Mol Med. 2014;6(9):1124–32. https://doi.org/10.15252/emmm.201404170.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Seneviratne A, Hulsmans M, Holvoet P, et al. Biomechanical factors and macrophages in plaque stability. Cardiovasc Res. 2013;99(2):284–93. https://doi.org/10.1093/cvr/cvt097.

    Article  CAS  PubMed  Google Scholar 

  72. Zhang B, Ma Y, Xiang C. SIRT2 decreases atherosclerotic plaque formation in low-density lipoprotein receptor-deficient mice by modulating macrophage polarization. Biomed Pharmacother. 2018;97:1238–42. https://doi.org/10.1016/j.biopha.2017.11.061.

    Article  CAS  PubMed  Google Scholar 

  73. Zhang L, Chen J, He Q, et al. MicroRNA-217 is involved in the progression of atherosclerosis through regulating inflammatory responses by targeting sirtuin 1. Mol Med Rep. 2019;20(4):3182–90. https://doi.org/10.3892/mmr.2019.10581.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Grootaert M, Moulis M, Roth L, et al. Vascular smooth muscle cell death, autophagy and senescence in atherosclerosis. Cardiovasc Res. 2018;114(4):622–34. https://doi.org/10.1093/cvr/cvy007.

    Article  CAS  PubMed  Google Scholar 

  75. Clarke MC, Figg N, Maguire JJ, et al. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12(9):1075–80. https://doi.org/10.1038/nm1459.

    Article  CAS  PubMed  Google Scholar 

  76. Flynn PD, Byrne CD, Baglin TP, et al. Thrombin generation by apoptotic vascular smooth muscle cells. Blood. 1997;89(12):4378–84. https://doi.org/10.1182/blood.V89.12.4378.

    Article  CAS  PubMed  Google Scholar 

  77. Gorenne I, Kumar S, Gray K, et al. Vascular smooth muscle cell sirtuin 1 protects against DNA damage and inhibits atherosclerosis. Circulation. 2013;127(3):386–96. https://doi.org/10.1161/circulationaha.112.124404.

    Article  CAS  PubMed  Google Scholar 

  78. Yuan L, Wang D, Wu C. Protective effect of liquiritin on coronary heart disease through regulating the proliferation of human vascular smooth muscle cells via upregulation of sirtuin1. Bioengineered. 2022;13(2):2840–50. https://doi.org/10.1080/21655979.2021.2024687.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Wang H, He F, Liang B, et al. p53-dependent LincRNA-p21 protects against proliferation and anti-apoptosis of vascular smooth muscle cells in atherosclerosis by upregulating SIRT7 via MicroRNA-17-5p. J Cardiovasc Transl Res. 2021;14(3):426–40. https://doi.org/10.1007/s12265-020-10074-9.

    Article  PubMed  Google Scholar 

  80. Phadwal K, Feng D, Zhu D, et al. Autophagy as a novel therapeutic target in vascular calcification. Pharmacol Ther. 2020;206:107430. https://doi.org/10.1016/j.pharmthera.2019.107430.

    Article  CAS  PubMed  Google Scholar 

  81. Torisu T, Torisu K, Lee IH, et al. Autophagy regulates endothelial cell processing, maturation and secretion of von Willebrand factor. Nat Med. 2013;19(10):1281–7. https://doi.org/10.1038/nm.3288.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Wu Q, Hu Y, Jiang M, et al. Effect of autophagy regulated by Sirt1/FoxO1 pathway on the release of factors promoting thrombosis from vascular endothelial cells. Int J Mol Sci. 2019;20(17) https://doi.org/10.3390/ijms20174132.

  83. Fetterman JL, Holbrook M, Flint N, et al. Restoration of autophagy in endothelial cells from patients with diabetes mellitus improves nitric oxide signaling. Atherosclerosis. 2016;247:207–17. https://doi.org/10.1016/j.atherosclerosis.2016.01.043.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Cai X, She M, Xu M, et al. GLP-1 treatment protects endothelial cells from oxidative stress-induced autophagy and endothelial dysfunction. Int J Biol Sci. 2018;14(12):1696–708. https://doi.org/10.7150/ijbs.27774.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Liao X, Sluimer JC, Wang Y, et al. Macrophage autophagy plays a protective role in advanced atherosclerosis. Cell Metab. 2012;15(4):545–53. https://doi.org/10.1016/j.cmet.2012.01.022.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Luo Y, Lu S, Gao Y, et al. Araloside C attenuates atherosclerosis by modulating macrophage polarization via Sirt1-mediated autophagy. Aging (Albany NY). 2020;12(2):1704–24. https://doi.org/10.18632/aging.102708.

    Article  CAS  PubMed  Google Scholar 

  87. Ma S, Chen J, Feng J, et al. Melatonin ameliorates the progression of atherosclerosis via mitophagy activation and NLRP3 inflammasome inhibition. Oxid Med Cell Longev. 2018;2018:9286458. https://doi.org/10.1155/2018/9286458.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wang T, Sun C, Hu L, et al. Sirt6 stabilizes atherosclerosis plaques by promoting macrophage autophagy and reducing contact with endothelial cells. Biochem Cell Biol. 2020;98(2):120–9. https://doi.org/10.1139/bcb-2019-0057.

    Article  CAS  PubMed  Google Scholar 

  89. Kockx MM, De Meyer GR, Muhring J, et al. Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation. 1998;97(23):2307–15. https://doi.org/10.1161/01.cir.97.23.2307.

    Article  CAS  PubMed  Google Scholar 

  90. Osonoi Y, Mita T, Azuma K, et al. Defective autophagy in vascular smooth muscle cells enhances cell death and atherosclerosis. Autophagy. 2018;14(11):1991–2006. https://doi.org/10.1080/15548627.2018.1501132.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Chen Z, Ouyang C, Zhang H, et al. Vascular smooth muscle cell-derived hydrogen sulfide promotes atherosclerotic plaque stability via TFEB (transcription factor EB)-mediated autophagy. Autophagy. 2022;18(10):2270–87. https://doi.org/10.1080/15548627.2022.2026097.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Han T, Zhao H, Xie L, et al. Deacetylation of cGAS by HDAC1 regulates vascular calcification by promoting autophagy. Life Sci. 2020:118930. https://doi.org/10.1016/j.lfs.2020.118930.

  93. Wei X, Xie F, Zhou X, et al. Role of pyroptosis in inflammation and cancer. Cell Mol Immunol. 2022;19(9):971–92. https://doi.org/10.1038/s41423-022-00905-x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. Qian Z, Zhao Y, Wan C, et al. Pyroptosis in the initiation and progression of atherosclerosis. Front Pharmacol. 2021;12:652963. https://doi.org/10.3389/fphar.2021.652963.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Yao F, Lv X, Jin Z, et al. Sirt6 inhibits vascular endothelial cell pyroptosis by regulation of the Lin28b/let-7 pathway in atherosclerosis. Int Immunopharmacol. 2022;110:109056. https://doi.org/10.1016/j.intimp.2022.109056.

    Article  CAS  PubMed  Google Scholar 

  96. Jin X, Fu W, Zhou J, et al. Oxymatrine attenuates oxidized low-density lipoprotein-induced HUVEC injury by inhibiting NLRP3 inflammasome-mediated pyroptosis via the activation of the SIRT1/Nrf2 signaling pathway. Int J Mol Med. 2021;48(4) https://doi.org/10.3892/ijmm.2021.5020.

  97. Cochain C, Zernecke A. Macrophages in vascular inflammation and atherosclerosis. Pflugers Arch. 2017;469(3-4):485–99. https://doi.org/10.1007/s00424-017-1941-y.

    Article  CAS  PubMed  Google Scholar 

  98. Xu S, Chen H, Ni H, et al. Targeting HDAC6 attenuates nicotine-induced macrophage pyroptosis via NF-kappaB/NLRP3 pathway. Atherosclerosis. 2021;317:1–9. https://doi.org/10.1016/j.atherosclerosis.2020.11.021.

    Article  CAS  PubMed  Google Scholar 

  99. Lai B, Wu CH, Wu CY, et al. Ferroptosis and autoimmune diseases. Front Immunol. 2022;13:916664. https://doi.org/10.3389/fimmu.2022.916664.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Naito Y, Masuyama T, Ishihara M. Iron and cardiovascular diseases. J Cardiol. 2021;77(2):160–5. https://doi.org/10.1016/j.jjcc.2020.07.009.

    Article  PubMed  Google Scholar 

  101. Song S, Ding Y, Dai GL, et al. Sirtuin 3 deficiency exacerbates diabetic cardiomyopathy via necroptosis enhancement and NLRP3 activation. Acta Pharmacol Sin. 2021;42(2):230–41. https://doi.org/10.1038/s41401-020-0490-7.

    Article  CAS  PubMed  Google Scholar 

  102. Sohrabi Y, Reinecke H. RIPK1 targeting protects against obesity and atherosclerosis. Trends Endocrinol Metab. 2021;32(7):420–2. https://doi.org/10.1016/j.tem.2021.03.009.

    Article  CAS  PubMed  Google Scholar 

  103. Colijn S, Muthukumar V, Xie J, et al. Cell-specific and athero-protective roles for RIPK3 in a murine model of atherosclerosis. Dis Model Mech. 2020, 13(1) https://doi.org/10.1242/dmm.041962.

  104. Ma C, Wu H, Yang G, et al. Calycosin ameliorates atherosclerosis by enhancing autophagy via regulating the interaction between KLF2 and MLKL in apolipoprotein E gene-deleted mice. Br J Pharmacol. 2022;179(2):252–69. https://doi.org/10.1111/bph.15720.

    Article  CAS  PubMed  Google Scholar 

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Funding

This work was supported by the National Natural Science Foundation of China (82170260).

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Author notes

  1. Gang Zhou and Yanfang Liu contributed equally to this work.

Authors and Affiliations

  1. Institute of Cardiovascular Disease, China Three Gorges University, Yichang, 443003, China

    Gang Zhou, Yanfang Liu, Hui Wu, Dong Zhang, Qingzhuo Yang & Yi Li

  2. Department of Central Experimental Laboratory, Yichang Central People’s Hospital, Yichang, 443003, China

    Gang Zhou, Yanfang Liu, Dong Zhang, Qingzhuo Yang & Yi Li

  3. HuBei Clinical Research Center for Ischemic Cardiovascular Disease, Yichang, 443003, China

    Gang Zhou, Yanfang Liu, Hui Wu, Dong Zhang, Qingzhuo Yang & Yi Li

  4. Department of Cardiology, Yichang Central People’s Hospital, Yiling Road 183, Yichang, 443003, Hubei, China

    Hui Wu

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  1. Gang Zhou
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Contributions

Zhou Gang: conceptualization. Liu Yanfang: data curation, writing—original draft preparation. Zhang Dong: visualization, investigation. Yang Qingzhuo, Li Yi: production of matching images. Wu Hui: supervision. Zhou Gang, Liu Yanfang: writing—reviewing and editing.

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Correspondence to Hui Wu.

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Zhou, G., Liu, Y., Wu, H. et al. Research Progress on Histone Deacetylases Regulating Programmed Cell Death in Atherosclerosis. J. of Cardiovasc. Trans. Res. 17, 308–321 (2024). https://doi.org/10.1007/s12265-023-10444-z

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