Role of Kupffer cells in ischemia-reperfusion injury during liver transplantation_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CAO Zhumin ^1,2 , WU Xinyi ¹ , LIU Chang’an ¹ ,  GONG Jianping ¹

1. Department of Hepatobiliary Surgery, The Second Affiliated Hospital of Chongqing Medical University, Chongqing 400010, P. R. China;
2. Chongqing the Seventh People’s Hospital, Chongqing 400054, P. R. China;

Corresponding author：

GONG Jianping, Email: gongjianping11@126.com

Keywords：

Kupffer cells; liver transplantation; ischemia-reperfusion injury

DOI：

10.7507/1007-9424.202003039

Video：

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Objective To Analyze the relationship between Kupffer cells (KCs) and ischemia-reperfusion injury (IRI) during liver transplantation.Method The relevant studies in recent years on the KCs in the hepatic IRI during the liver transplantation were collected and summarized.Results Some recent studies had shown that both the congenital immunity and adaptive immunity were closely related to the occurrence and development of hepatic IRI and the activation of KCs. The KCs were the resident macrophage of the liver and played the key role in the aseptic inflammatory injury. The KCs could secrete various pro-inflammatory factors to aggravate the liver cell injury. On the other hand, the KCs could also improve the hepatic IRI by upregulating anti-inflammatory factors.Conclusions Hepatic IRI can activate the innate immune system and the adaptive immune system to cause the sterile inflammatory response of damaged liver cells. During hepatic IRI, the activated KCs can secrete pro-inflammatory factors and anti-inflammatory factors to play the dual roles of injury and protection.

Citation： CAO Zhumin, WU Xinyi, LIU Chang’an, GONG Jianping. Role of Kupffer cells in ischemia-reperfusion injury during liver transplantation. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(10): 1310-1313. doi: 10.7507/1007-9424.202003039 Copy

1.	Lu TF, Yang TH, Zhong CP, <italic>et al</italic>. Dual effect of hepatic macrophages on liver ischemia and reperfusion injury during liver transplantation. Immune Netw, 2018, 18(3): e24.
2.	Krenkel O, Tacke F. Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol, 2017, 17(5): 306-321.
3.	Bonnardel J, T'Jonck W, Gaublomme D, <italic>et al</italic>. Stellate cells, hepatocytes, and endothelial cells imprint the Kupffer cell identity on monocytes colonizing the liver macrophage. Immunity, 2019, 51(4): 638-654.e9.
4.	Vago JP, Galvão I, Negreiros-Lima JL, <italic>et al</italic>. Glucocorticoid-induced leucine zipper modulates macrophage polarization and apoptotic cell clearance. Pharmacol Res, 2020, 159: 104842.
5.	Mardani F, Seifi B, Mohammadi A, <italic>et al</italic>. Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol, 2018, 233(9): 6425-6440.
6.	Jones AE, Divakaruni AS. Macrophage activation as an archetype of mitochondrial repurposing. Mol Aspects Med, 2020, 71: 100838.
7.	Oliveira THC, Marques PE, Proost P, <italic>et al</italic>. Neutrophils: a cornerstone of liver ischemia and reperfusion injury. Lab Invest, 2018, 98(1): 51-62.
8.	Mihm S. Danger-associated molecular patterns (DAMPs): molecular triggers for sterile inflammation in the liver. Int J Mol Sci, 2018, 19(10): 3104.
9.	Ni DL, Wei H, Chen WY, <italic>et al</italic>. Ceria nanoparticles meet hepatic ischemia-reperfusion injury: The perfect imperfection. Adv Mater, 2019, 31(40): e1902956.
10.	Kahn J, Schemmer P. Control of ischemia-reperfusion injury in liver transplantation: potentials for increasing the donor pool. Visc Med, 2018, 34(6): 444-448.
11.	Zheng DF, Li ZT, Wei XF, <italic>et al</italic>. Role of miR-148a in mitigating hepatic ischemia-reperfusion injury by repressing the TLR4 signaling pathway <italic>via</italic> targeting CaMKⅡα <italic>in vivo</italic> and <italic>in vitro</italic>. Cell Physiol Biochem, 2018, 49(5): 2060-2072.
12.	Cheng MX, Huang P, He Q, <italic>et al</italic>. Liver X receptors activation attenuates ischemia reperfusion injury of liver graft in rats. J Invest Surg, 2019, 32(4): 298-303.
13.	刘文平, 张永川, 张映林. 丹参酮ⅡA 在小鼠肝脏缺血再灌注损伤模型中的保护作用及机制. 中国普外基础与临床杂志, 2020, 27(3): 298-303.
14.	Khambu B, Yan S, Huda N, <italic>et al</italic>. Role of high-mobility group box-1 in liver pathogenesis. Int J Mol Sci, 2019, 20(21): 5314.
15.	Lai X, Gong JH, Wang WM, <italic>et al</italic>. Acetyl-3-aminoethyl salicylate ameliorates hepatic ischemia/reperfusion injury and liver graft survival through a high-mobility group box 1/toll-like receptor 4-dependent mechanism. Liver Transpl, 2019, 25(8): 1220-1232.
16.	Wen SH, Li X, Ling YH, <italic>et al</italic>. HMGB1-associated necroptosis and Kupffer cells M1 polarization underlies remote liver injury induced by intestinal ischemia/reperfusion in rats. FASEB J, 2020, 34(3): 4384-4402.
17.	Zhao GY, Fu C, Wang L, <italic>et al</italic>. Down-regulation of nuclear HMGB1 reduces ischemia-induced HMGB1 translocation and release and protects against liver ischemia-reperfusion injury. Sci Rep, 2017, 7: 46272.
18.	Cochet F, Peri F. The role of carbohydrates in the lipopolysaccharide (LPS)/toll-like receptor 4 (TLR4) signalling. Int J Mol Sci, 2017, 18(11): 2318.
19.	Kopp F, Kupsch S, Schromm AB. Lipopolysaccharide-binding protein is bound and internalized by host cells and colocalizes with LPS in the cytoplasm: Implications for a role of lbp in intracellular LPS-signaling. Biochim Biophys Acta, 2016, 1863(4): 660-672.
20.	Bai H, Wen J, Gong JP, <italic>et al</italic>. Blockade of the Notch1/Jagged1 pathway in Kupffer cells aggravates ischemia-reperfusion injury of orthotopic liver transplantation in mice. Autoimmunity, 2019, 52(4): 176-184.
21.	Li J, Ke WB, Zhou Q, <italic>et al</italic>. Tumour necrosis factor-α promotes liver ischaemia-reperfusion injury through the PGC-1α/Mfn2 pathway. J Cell Mol Med, 2014, 18(9): 1863-1873.
22.	Su L, Li N, Tang H, <italic>et al</italic>. Kupffer cell-derived TNF-α promotes hepatocytes to produce CXCL1 and mobilize neutrophils in response to necrotic cells. Cell Death Dis, 2018, 9(3): 323.
23.	Al-Saeedi M, Liang R, Schultze DP, <italic>et al</italic>. Glycine protects partial liver grafts from Kupffer cell-dependent ischemia-reperfusion injury without negative effect on regeneration. Amino Acids, 2019, 51(6): 903-911.
24.	Yue S, Zhu JJ, Zhang M, <italic>et al</italic>. The myeloid heat shock transcription factor 1/β-catenin axis regulates NLR family, pyrin domain-containing 3 inflammasome activation in mouse liver ischemia/reperfusion injury. Hepatology, 2016, 64(5): 1683-1698.
25.	Jin YT, Li CY, Xu DW, et al. Jagged1-mediated myeloid Notch1 signaling activates HSF1/Snail and controls NLRP3 inflammasome activation in liver inflammatory injury. Cell Mol Immunol, 2019 Oct 31. doi: 10.1038/s41423-019-0318-x.
26.	Chen N, Ou ZB, Zhang WF, <italic>et al</italic>. Cathepsin B regulates non-canonical NLRP3 inflammasome pathway by modulating activation of caspase-11 in Kupffer cells. Cell Prolif, 2018, 51(6): e12487.
27.	Cheng MX, Cao D, Chen Y, <italic>et al</italic>. α-ketoglutarate attenuates ischemia-reperfusion injury of liver graft in rats. Biomed Pharmacother, 2019, 111: 1141-1146.
28.	Roth K, Rockwell CE, Copple BL. Differential sensitivity of Kupffer cells and hepatic monocyte-derived macrophages to bacterial lipopolysaccharide. Clin Exp Gastroenterol Hepatol, 2019, 1(1): 106.
29.	Kageyama S, Hirao H, Nakamura K, et al. Recipient HO-1 inducibility is essential for posttransplant hepatic HO-1 expression and graft protection: From bench-to-bedside. Am J Transplant, 2019, 19(2): 356-367.
30.	Xu DW, Chen LL, Chen XS, <italic>et al</italic>. The triterpenoid CDDO-imidazolide ameliorates mouse liver ischemia-reperfusion injury through activating the Nrf2/HO-1 pathway enhanced autophagy. Cell Death Dis, 2017, 8(8): e2983.
31.	Zhang M, Nakamura K, Kageyama S, <italic>et al</italic>. Myeloid HO-1 modulates macrophage polarization and protects against ischemia-reperfusion injury. JCI Insight, 2018, 3(19): e120596.
32.	Hirao H, Dery KJ, Kageyama S, Net al. Heme oxygenase-1 in liver transplant ischemia-reperfusion injury: From bench-to-bedside. Free Radic Biol Med, 2020: S0891-5849(19)31510-2.
33.	Rao J, Cheng F, Yang S, <italic>et al</italic>. Ag-specific CD4 T cells promote innate immune responses in liver ischemia reperfusion injury. Cell Mol Immunol, 2019, 16(1): 98-100.
34.	Li P, He K, Li J, <italic>et al</italic>. The role of Kupffer cells in hepatic diseases. Mol Immunol, 2017, 85: 222-229.
35.	Wu H, Xu X, Li J, <italic>et al</italic>. TIM-4 blockade of KCs combined with exogenous TGF-β injection helps to reverse acute rejection and prolong the survival rate of mice receiving liver allografts. Int J Mol Med, 2018, 42(1): 346-358.
36.	Li Y, Ma D, Wang Z, <italic>et al</italic>. MicroRNA-155 deficiency in Kupffer cells ameliorates liver ischemia-reperfusion injury in mice. Transplantation, 2017, 101(7): 1600-1608.

1. Lu TF, Yang TH, Zhong CP, <italic>et al</italic>. Dual effect of hepatic macrophages on liver ischemia and reperfusion injury during liver transplantation. Immune Netw, 2018, 18(3): e24.
2. Krenkel O, Tacke F. Liver macrophages in tissue homeostasis and disease. Nat Rev Immunol, 2017, 17(5): 306-321.
3. Bonnardel J, T'Jonck W, Gaublomme D, <italic>et al</italic>. Stellate cells, hepatocytes, and endothelial cells imprint the Kupffer cell identity on monocytes colonizing the liver macrophage. Immunity, 2019, 51(4): 638-654.e9.
4. Vago JP, Galvão I, Negreiros-Lima JL, <italic>et al</italic>. Glucocorticoid-induced leucine zipper modulates macrophage polarization and apoptotic cell clearance. Pharmacol Res, 2020, 159: 104842.
5. Mardani F, Seifi B, Mohammadi A, <italic>et al</italic>. Macrophage plasticity, polarization, and function in health and disease. J Cell Physiol, 2018, 233(9): 6425-6440.
6. Jones AE, Divakaruni AS. Macrophage activation as an archetype of mitochondrial repurposing. Mol Aspects Med, 2020, 71: 100838.
7. Oliveira THC, Marques PE, Proost P, <italic>et al</italic>. Neutrophils: a cornerstone of liver ischemia and reperfusion injury. Lab Invest, 2018, 98(1): 51-62.
8. Mihm S. Danger-associated molecular patterns (DAMPs): molecular triggers for sterile inflammation in the liver. Int J Mol Sci, 2018, 19(10): 3104.
9. Ni DL, Wei H, Chen WY, <italic>et al</italic>. Ceria nanoparticles meet hepatic ischemia-reperfusion injury: The perfect imperfection. Adv Mater, 2019, 31(40): e1902956.
10. Kahn J, Schemmer P. Control of ischemia-reperfusion injury in liver transplantation: potentials for increasing the donor pool. Visc Med, 2018, 34(6): 444-448.
11. Zheng DF, Li ZT, Wei XF, <italic>et al</italic>. Role of miR-148a in mitigating hepatic ischemia-reperfusion injury by repressing the TLR4 signaling pathway <italic>via</italic> targeting CaMKⅡα <italic>in vivo</italic> and <italic>in vitro</italic>. Cell Physiol Biochem, 2018, 49(5): 2060-2072.
12. Cheng MX, Huang P, He Q, <italic>et al</italic>. Liver X receptors activation attenuates ischemia reperfusion injury of liver graft in rats. J Invest Surg, 2019, 32(4): 298-303.
13. 刘文平, 张永川, 张映林. 丹参酮ⅡA 在小鼠肝脏缺血再灌注损伤模型中的保护作用及机制. 中国普外基础与临床杂志, 2020, 27(3): 298-303.
14. Khambu B, Yan S, Huda N, <italic>et al</italic>. Role of high-mobility group box-1 in liver pathogenesis. Int J Mol Sci, 2019, 20(21): 5314.
15. Lai X, Gong JH, Wang WM, <italic>et al</italic>. Acetyl-3-aminoethyl salicylate ameliorates hepatic ischemia/reperfusion injury and liver graft survival through a high-mobility group box 1/toll-like receptor 4-dependent mechanism. Liver Transpl, 2019, 25(8): 1220-1232.
16. Wen SH, Li X, Ling YH, <italic>et al</italic>. HMGB1-associated necroptosis and Kupffer cells M1 polarization underlies remote liver injury induced by intestinal ischemia/reperfusion in rats. FASEB J, 2020, 34(3): 4384-4402.
17. Zhao GY, Fu C, Wang L, <italic>et al</italic>. Down-regulation of nuclear HMGB1 reduces ischemia-induced HMGB1 translocation and release and protects against liver ischemia-reperfusion injury. Sci Rep, 2017, 7: 46272.
18. Cochet F, Peri F. The role of carbohydrates in the lipopolysaccharide (LPS)/toll-like receptor 4 (TLR4) signalling. Int J Mol Sci, 2017, 18(11): 2318.
19. Kopp F, Kupsch S, Schromm AB. Lipopolysaccharide-binding protein is bound and internalized by host cells and colocalizes with LPS in the cytoplasm: Implications for a role of lbp in intracellular LPS-signaling. Biochim Biophys Acta, 2016, 1863(4): 660-672.
20. Bai H, Wen J, Gong JP, <italic>et al</italic>. Blockade of the Notch1/Jagged1 pathway in Kupffer cells aggravates ischemia-reperfusion injury of orthotopic liver transplantation in mice. Autoimmunity, 2019, 52(4): 176-184.
21. Li J, Ke WB, Zhou Q, <italic>et al</italic>. Tumour necrosis factor-α promotes liver ischaemia-reperfusion injury through the PGC-1α/Mfn2 pathway. J Cell Mol Med, 2014, 18(9): 1863-1873.
22. Su L, Li N, Tang H, <italic>et al</italic>. Kupffer cell-derived TNF-α promotes hepatocytes to produce CXCL1 and mobilize neutrophils in response to necrotic cells. Cell Death Dis, 2018, 9(3): 323.
23. Al-Saeedi M, Liang R, Schultze DP, <italic>et al</italic>. Glycine protects partial liver grafts from Kupffer cell-dependent ischemia-reperfusion injury without negative effect on regeneration. Amino Acids, 2019, 51(6): 903-911.
24. Yue S, Zhu JJ, Zhang M, <italic>et al</italic>. The myeloid heat shock transcription factor 1/β-catenin axis regulates NLR family, pyrin domain-containing 3 inflammasome activation in mouse liver ischemia/reperfusion injury. Hepatology, 2016, 64(5): 1683-1698.
25. Jin YT, Li CY, Xu DW, et al. Jagged1-mediated myeloid Notch1 signaling activates HSF1/Snail and controls NLRP3 inflammasome activation in liver inflammatory injury. Cell Mol Immunol, 2019 Oct 31. doi: 10.1038/s41423-019-0318-x.
26. Chen N, Ou ZB, Zhang WF, <italic>et al</italic>. Cathepsin B regulates non-canonical NLRP3 inflammasome pathway by modulating activation of caspase-11 in Kupffer cells. Cell Prolif, 2018, 51(6): e12487.
27. Cheng MX, Cao D, Chen Y, <italic>et al</italic>. α-ketoglutarate attenuates ischemia-reperfusion injury of liver graft in rats. Biomed Pharmacother, 2019, 111: 1141-1146.
28. Roth K, Rockwell CE, Copple BL. Differential sensitivity of Kupffer cells and hepatic monocyte-derived macrophages to bacterial lipopolysaccharide. Clin Exp Gastroenterol Hepatol, 2019, 1(1): 106.
29. Kageyama S, Hirao H, Nakamura K, et al. Recipient HO-1 inducibility is essential for posttransplant hepatic HO-1 expression and graft protection: From bench-to-bedside. Am J Transplant, 2019, 19(2): 356-367.
30. Xu DW, Chen LL, Chen XS, <italic>et al</italic>. The triterpenoid CDDO-imidazolide ameliorates mouse liver ischemia-reperfusion injury through activating the Nrf2/HO-1 pathway enhanced autophagy. Cell Death Dis, 2017, 8(8): e2983.
31. Zhang M, Nakamura K, Kageyama S, <italic>et al</italic>. Myeloid HO-1 modulates macrophage polarization and protects against ischemia-reperfusion injury. JCI Insight, 2018, 3(19): e120596.
32. Hirao H, Dery KJ, Kageyama S, Net al. Heme oxygenase-1 in liver transplant ischemia-reperfusion injury: From bench-to-bedside. Free Radic Biol Med, 2020: S0891-5849(19)31510-2.
33. Rao J, Cheng F, Yang S, <italic>et al</italic>. Ag-specific CD4 T cells promote innate immune responses in liver ischemia reperfusion injury. Cell Mol Immunol, 2019, 16(1): 98-100.
34. Li P, He K, Li J, <italic>et al</italic>. The role of Kupffer cells in hepatic diseases. Mol Immunol, 2017, 85: 222-229.
35. Wu H, Xu X, Li J, <italic>et al</italic>. TIM-4 blockade of KCs combined with exogenous TGF-β injection helps to reverse acute rejection and prolong the survival rate of mice receiving liver allografts. Int J Mol Med, 2018, 42(1): 346-358.
36. Li Y, Ma D, Wang Z, <italic>et al</italic>. MicroRNA-155 deficiency in Kupffer cells ameliorates liver ischemia-reperfusion injury in mice. Transplantation, 2017, 101(7): 1600-1608.

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Role of Kupffer cells in ischemia-reperfusion injury during liver transplantation

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