Research advances of pyroptosis in hepatic ischemia-reperfusion injury_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CHEN Dong ,  MA Yong

Department of Hepatic Minimal Invasive Surgery, The First Affiliated Hospital of Harbin Medical University, Harbin 150001, P. R. China;

Corresponding author：

MA Yong, Email: doctormy80@163.com

Keywords：

pyroptosis; hepatic ischemia-reperfusion injury; interleukin-1β; caspase-1; caspase-11

DOI：

10.7507/1007-9424.202103130

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research advances of pyroptosis in hepatic ischamia-reperfusion injury (IRI).Method The literatures about the studies of mechanism of pyroptosis in hepatic IRI were retrieved and analyzed.Results Pyroptosis, also known as inflammatory necrocytosis, was proven to play an important role in the hepatic IRI. When hepatic ischemia-reperfusion occurred, the classical pathway of pyroptosis dependenting on caspase-1 and the non-classical pathway of pyroptosis dependenting on caspase-11 were initiated by specific stimulants, and leaded to the activation of gasdermin D, releases of proinflammatory factors such as interleukin-1β, interleukin-18, etc., and the recruitment and activation of neutrophils. Consequently, pyroptosis caused more severe hepatic inflammation and aggravated existing cell injury and dysfunction of liver during hepatic IRI.Conclusions Pyroptosis plays an important role in liver IRI. Further researches about mechanism of pyroptosis will be beneficial to the prevention and treatment of the pyroptosis of related diseases.

Citation： CHEN Dong, MA Yong. Research advances of pyroptosis in hepatic ischemia-reperfusion injury. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(2): 243-247. doi: 10.7507/1007-9424.202103130 Copy

1.	Dai Q, Jiang W, Liu H, et al. Kupffer cell-targeting strategy for the protection of hepatic ischemia/reperfusion injury. Nanotechnology, 2021 Jan 20. Online ahead of print. doi: 10.1088/1361-6528/abde02.
2.	王小莹, 申丽娟, 刘作金. 细胞焦亡与肝脏缺血再灌注损伤. 重庆医学, 2019, 48(18): 3184-3187.
3.	Broz P, Pelegrín P, Shao F. The gasdermins, a protein family executing cell death and inflammation. Nat Rev Immunol, 2020, 20(3): 143-157.
4.	Li J, Zhao J, Xu M, et al. Blocking GSDMD processing in innate immune cells but not in hepatocytes protects hepatic ischemia-reperfusion injury. Cell Death Dis, 2020, 11(4): 244. doi: 10.1038/s41419-020-2437-9.
5.	Kim HY, Kim SJ, Lee SM. Activation of NLRP3 and AIM2 inflammasomes in Kupffer cells in hepatic ischemia/reperfusion. FEBS J, 2015, 282(2): 259-270.
6.	Weber ANR, Bittner ZA, Shankar S, et al. Recent insights into the regulatory networks of NLRP3 inflammasome activation. J Cell Sci, 2020, 133(23): jcs248344. doi:10.1242/jcs.248344.
7.	Swanson KV, Deng M, Ting JP. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol, 2019, 19(8): 477-489.
8.	Zhao N, Li CC, Di B, et al. Recent advances in the NEK7-licensed NLRP3 inflammasome activation: mechanisms, role in diseases and related inhibitors. J Autoimmun, 2020, 113: 102515. doi: 10.1016/j.jaut.2020.102515.
9.	Liu G, Chen X, Wang Q, et al. NEK7: a potential therapy target for NLRP3-related diseases. Biosci Trends, 2020, 14(2): 74-82.
10.	Vande Walle L, Lamkanfi M. Pyroptosis. Curr Biol, 2016, 26(13): R568-R572.
11.	Conos SA, Lawlor KE, Vaux DL, et al. Cell death is not essential for caspase-1-mediated interleukin-1β activation and secretion. Cell Death Differ, 2016, 23(11): 1827-1838.
12.	Hafner-Bratkovič I, Sušjan P, Lainšček D, et al. NLRP3 lacking the leucine-rich repeat domain can be fully activated via the canonical inflammasome pathway. Nat Commun, 2018, 9(1): 5182. doi: 10.1038/s41467-018-07573-4.
13.	Karmakar M, Katsnelson M, Malak HA, et al. Neutrophil IL-1β processing induced by pneumolysin is mediated by the NLRP3/ASC inflammasome and caspase-1 activation and is dependent on K⁺ efflux. J Immunol, 2015, 194(4): 1763-1775.
14.	Evavold CL, Ruan J, Tan Y, et al. The pore-forming protein gasdermin D regulates interleukin-1 secretion from living macrophages. Immunity, 2018, 48(1): 35-44.
15.	Li Z, Zhao F, Cao Y, et al. DHA attenuates hepatic ischemia reperfusion injury by inhibiting pyroptosis and activating PI3K/Akt pathway. Eur J Pharmacol, 2018, 835: 1-10.
16.	Hua S, Ma M, Fei X, et al. Glycyrrhizin attenuates hepatic ischemia-reperfusion injury by suppressing HMGB1-dependent GSDMD-mediated Kupffer cells pyroptosis. Int Immunopharmacol, 2019, 68: 145-155.
17.	Zhong W, Rao Z, Rao J, et al. Aging aggravated liver ischemia and reperfusion injury by promoting STING-mediated NLRP3 activation in macrophages. Aging Cell, 2020, 19(8): e13186. doi: 10.1111/acel.13186.
18.	Lin Q, Li S, Jiang N, 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. doi: 10.1016/j.redox.2019.101254.
19.	Xu Y, Tang Y, Lu J, et al. PINK1-mediated mitophagy protects against hepatic ischemia/reperfusion injury by restraining NLRP3 inflammasome activation. Free Radic Biol Med, 2020, 160: 871-886.
20.	Lozano-Ruiz B, González-Navajas JM. The emerging relevance of AIM2 in liver disease. Int J Mol Sci, 2020, 21(18): 6535. doi: 10.3390/ijms21186535.
21.	Konishi T, Lentsch AB. Hepatic ischemia/reperfusion: mechanisms of tissue injury, repair, and regeneration. Gene Expr, 2017, 17(4): 277-287.
22.	Sharma M, de Alba E. Structure, activation and regulation of NLRP3 and AIM2 inflammasomes. Int J Mol Sci, 2021, 22(2): 872. doi: 10.3390/ijms22020872.
23.	Lugrin J, Martinon F. The AIM2 inflammasome: sensor of pathogens and cellular perturbations. Immunol Rev, 2018, 281(1): 99-114.
24.	Czigany Z, Hata K, Lai W, et al. A dual protective effect of intestinal remote ischemic conditioning in a rat model of total hepatic ischemia. J Clin Med, 2019, 8(10): 1546. doi: 10.3390/jcm8101546.
25.	罗炳生, 刘靖华. LPS 的胞内受体 Caspase-11 的研究进展. 生物化学与生物物理进展, 2018, 45(3): 289-296.
26.	Abu Khweek A, Amer AO. Pyroptotic and non-pyroptotic effector functions of caspase-11. Immunol Rev, 2020, 297(1): 39-52.
27.	Sherif IO, Al-Shaalan NH. Vildagliptin attenuates hepatic ischemia/reperfusion injury via the TLR4/NF-κB signaling pathway. Oxid Med Cell Longev, 2018, 2018: 3509091. doi: 10.1155/2018/3509091.
28.	Kayagaki N, Stowe IB, Lee BL, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature, 2015, 526(7575): 666-671.
29.	Mazgaeen L, Gurung P. Recent advances in lipopolysaccharide recognition systems. Int J Mol Sci, 2020, 21(2): 379. doi: 10.3390/ijms21020379.
30.	Yang D, He Y, Muñoz-Planillo R, et al. Caspase-11 requires the pannexin-1 channel and the purinergic P2X7 pore to mediate pyroptosis and endotoxic shock. Immunity, 2015, 43(5): 923-932.
31.	Pellegrini C, Antonioli L, Lopez-Castejon G, et al. Canonical and non-canonical activation of NLRP3 inflammasome at the crossroad between immune tolerance and intestinal inflammation. Front Immunol, 2017, 8: 36. doi: 10.3389/fimmu.2017.00036.
32.	Yi YS. Functional crosstalk between non-canonical caspase-11 and canonical NLRP3 inflammasomes during infection-mediated inflammation. Immunology, 2020, 159(2): 142-155.
33.	Aizawa E, Karasawa T, Watanabe S, et al. GSDME-dependent incomplete pyroptosis permits selective IL-1α release under caspase-1 inhibition. iScience, 2020, 23(5): 101070. doi: 10.1016/j.isci.2020.101070.
34.	Mandal P, Feng Y, Lyons JD, et al. Caspase-8 collaborates with caspase-11 to drive tissue damage and execution of endotoxic sh ock. Immunity, 2018, 49(1): 42-55.
35.	Zhang L, Liu H, Jia L, et al. Exosomes mediate hippocampal and cortical neuronal injury induced by hepatic ischemia-reperfusion injury through activating pyroptosis in rats. Oxid Med Cell Longev, 2019, 2019: 3753485. doi: 10.1155/2019/3753485.
36.	Zhao H, Huang H, Alam A, et al. VEGF mitigates histone-induced pyroptosis in the remote liver injury associated with renal allograft ischemia-reperfusion injury in rats. Am J Transplant, 2018, 18(8): 1890-1903.

1. Dai Q, Jiang W, Liu H, et al. Kupffer cell-targeting strategy for the protection of hepatic ischemia/reperfusion injury. Nanotechnology, 2021 Jan 20. Online ahead of print. doi: 10.1088/1361-6528/abde02.
2. 王小莹, 申丽娟, 刘作金. 细胞焦亡与肝脏缺血再灌注损伤. 重庆医学, 2019, 48(18): 3184-3187.
3. Broz P, Pelegrín P, Shao F. The gasdermins, a protein family executing cell death and inflammation. Nat Rev Immunol, 2020, 20(3): 143-157.
4. Li J, Zhao J, Xu M, et al. Blocking GSDMD processing in innate immune cells but not in hepatocytes protects hepatic ischemia-reperfusion injury. Cell Death Dis, 2020, 11(4): 244. doi: 10.1038/s41419-020-2437-9.
5. Kim HY, Kim SJ, Lee SM. Activation of NLRP3 and AIM2 inflammasomes in Kupffer cells in hepatic ischemia/reperfusion. FEBS J, 2015, 282(2): 259-270.
6. Weber ANR, Bittner ZA, Shankar S, et al. Recent insights into the regulatory networks of NLRP3 inflammasome activation. J Cell Sci, 2020, 133(23): jcs248344. doi:10.1242/jcs.248344.
7. Swanson KV, Deng M, Ting JP. The NLRP3 inflammasome: molecular activation and regulation to therapeutics. Nat Rev Immunol, 2019, 19(8): 477-489.
8. Zhao N, Li CC, Di B, et al. Recent advances in the NEK7-licensed NLRP3 inflammasome activation: mechanisms, role in diseases and related inhibitors. J Autoimmun, 2020, 113: 102515. doi: 10.1016/j.jaut.2020.102515.
9. Liu G, Chen X, Wang Q, et al. NEK7: a potential therapy target for NLRP3-related diseases. Biosci Trends, 2020, 14(2): 74-82.
10. Vande Walle L, Lamkanfi M. Pyroptosis. Curr Biol, 2016, 26(13): R568-R572.
11. Conos SA, Lawlor KE, Vaux DL, et al. Cell death is not essential for caspase-1-mediated interleukin-1β activation and secretion. Cell Death Differ, 2016, 23(11): 1827-1838.
12. Hafner-Bratkovič I, Sušjan P, Lainšček D, et al. NLRP3 lacking the leucine-rich repeat domain can be fully activated via the canonical inflammasome pathway. Nat Commun, 2018, 9(1): 5182. doi: 10.1038/s41467-018-07573-4.
13. Karmakar M, Katsnelson M, Malak HA, et al. Neutrophil IL-1β processing induced by pneumolysin is mediated by the NLRP3/ASC inflammasome and caspase-1 activation and is dependent on K⁺ efflux. J Immunol, 2015, 194(4): 1763-1775.
14. Evavold CL, Ruan J, Tan Y, et al. The pore-forming protein gasdermin D regulates interleukin-1 secretion from living macrophages. Immunity, 2018, 48(1): 35-44.
15. Li Z, Zhao F, Cao Y, et al. DHA attenuates hepatic ischemia reperfusion injury by inhibiting pyroptosis and activating PI3K/Akt pathway. Eur J Pharmacol, 2018, 835: 1-10.
16. Hua S, Ma M, Fei X, et al. Glycyrrhizin attenuates hepatic ischemia-reperfusion injury by suppressing HMGB1-dependent GSDMD-mediated Kupffer cells pyroptosis. Int Immunopharmacol, 2019, 68: 145-155.
17. Zhong W, Rao Z, Rao J, et al. Aging aggravated liver ischemia and reperfusion injury by promoting STING-mediated NLRP3 activation in macrophages. Aging Cell, 2020, 19(8): e13186. doi: 10.1111/acel.13186.
18. Lin Q, Li S, Jiang N, 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. doi: 10.1016/j.redox.2019.101254.
19. Xu Y, Tang Y, Lu J, et al. PINK1-mediated mitophagy protects against hepatic ischemia/reperfusion injury by restraining NLRP3 inflammasome activation. Free Radic Biol Med, 2020, 160: 871-886.
20. Lozano-Ruiz B, González-Navajas JM. The emerging relevance of AIM2 in liver disease. Int J Mol Sci, 2020, 21(18): 6535. doi: 10.3390/ijms21186535.
21. Konishi T, Lentsch AB. Hepatic ischemia/reperfusion: mechanisms of tissue injury, repair, and regeneration. Gene Expr, 2017, 17(4): 277-287.
22. Sharma M, de Alba E. Structure, activation and regulation of NLRP3 and AIM2 inflammasomes. Int J Mol Sci, 2021, 22(2): 872. doi: 10.3390/ijms22020872.
23. Lugrin J, Martinon F. The AIM2 inflammasome: sensor of pathogens and cellular perturbations. Immunol Rev, 2018, 281(1): 99-114.
24. Czigany Z, Hata K, Lai W, et al. A dual protective effect of intestinal remote ischemic conditioning in a rat model of total hepatic ischemia. J Clin Med, 2019, 8(10): 1546. doi: 10.3390/jcm8101546.
25. 罗炳生, 刘靖华. LPS 的胞内受体 Caspase-11 的研究进展. 生物化学与生物物理进展, 2018, 45(3): 289-296.
26. Abu Khweek A, Amer AO. Pyroptotic and non-pyroptotic effector functions of caspase-11. Immunol Rev, 2020, 297(1): 39-52.
27. Sherif IO, Al-Shaalan NH. Vildagliptin attenuates hepatic ischemia/reperfusion injury via the TLR4/NF-κB signaling pathway. Oxid Med Cell Longev, 2018, 2018: 3509091. doi: 10.1155/2018/3509091.
28. Kayagaki N, Stowe IB, Lee BL, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature, 2015, 526(7575): 666-671.
29. Mazgaeen L, Gurung P. Recent advances in lipopolysaccharide recognition systems. Int J Mol Sci, 2020, 21(2): 379. doi: 10.3390/ijms21020379.
30. Yang D, He Y, Muñoz-Planillo R, et al. Caspase-11 requires the pannexin-1 channel and the purinergic P2X7 pore to mediate pyroptosis and endotoxic shock. Immunity, 2015, 43(5): 923-932.
31. Pellegrini C, Antonioli L, Lopez-Castejon G, et al. Canonical and non-canonical activation of NLRP3 inflammasome at the crossroad between immune tolerance and intestinal inflammation. Front Immunol, 2017, 8: 36. doi: 10.3389/fimmu.2017.00036.
32. Yi YS. Functional crosstalk between non-canonical caspase-11 and canonical NLRP3 inflammasomes during infection-mediated inflammation. Immunology, 2020, 159(2): 142-155.
33. Aizawa E, Karasawa T, Watanabe S, et al. GSDME-dependent incomplete pyroptosis permits selective IL-1α release under caspase-1 inhibition. iScience, 2020, 23(5): 101070. doi: 10.1016/j.isci.2020.101070.
34. Mandal P, Feng Y, Lyons JD, et al. Caspase-8 collaborates with caspase-11 to drive tissue damage and execution of endotoxic sh ock. Immunity, 2018, 49(1): 42-55.
35. Zhang L, Liu H, Jia L, et al. Exosomes mediate hippocampal and cortical neuronal injury induced by hepatic ischemia-reperfusion injury through activating pyroptosis in rats. Oxid Med Cell Longev, 2019, 2019: 3753485. doi: 10.1155/2019/3753485.
36. Zhao H, Huang H, Alam A, et al. VEGF mitigates histone-induced pyroptosis in the remote liver injury associated with renal allograft ischemia-reperfusion injury in rats. Am J Transplant, 2018, 18(8): 1890-1903.

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Research advances of pyroptosis in hepatic ischemia-reperfusion injury

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