Research progress of the function of liver non-parenchymal cells in hepatic ischemia-reperfusion injury_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

CHEN Bangliang ,  MA Yong

Department of Hepatic Surgery, The First Affiliated Hospital of Harbin Medical University, Key Laboratory of Hepatosplenic Surgery, Ministry of Education, Harbin 150001, P. R. China;

Corresponding author：

MA Yong, Email: doctormy80@163.com

Keywords：

hepatic ischemia-reperfusion injury; Kupffer cell; sinusoidal endothelial cell; hepatic stellate cell; dendritic cell; review

DOI：

10.7507/1007-9424.201910051

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To investigate relationship between liver non-parenchymal cells and hepatic ischemia-reperfusion injury (HIRI).Method The relevant literatures on researches of the relationship between HIRI and liver non-parenchymal cells were analyzed and reviewed.Results During HIRI, hepatocytes could be severely damaged by aseptic inflammatory reaction and apoptosis. The liver non-parenchymal cells included Kupffer cells, sinusoidal endothelial cells, hepatic stellate cells, and dendritic cells, which could release a variety of cytokines and inflammatory mediators to promote the damage, and some liver non-parenchymal cells also had effect on reducing HIRI, for example: Kupffer cells could express heme oxygenase-1 to reduce HIRI, and hepatic stellate cells may participate in the repair process after HIRI. The role of liver non-parenchymal cells in HIRI was complex, but it also had potential therapeutic value.Conclusion Liver non-parenchymal cells can affect HIRI through a variety of mechanisms, which provide new goals and strategies for clinical reduction of HIRI.

Citation： CHEN Bangliang, MA Yong. Research progress of the function of liver non-parenchymal cells in hepatic ischemia-reperfusion injury. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2020, 27(6): 755-758. doi: 10.7507/1007-9424.201910051 Copy

1.	Konishi T, Lentsch AB. Hepatic ischemia/reperfusion: mechanisms of tissue injury, repair, and regeneration. Gene Expr, 2017, 17(4): 277-287.
2.	Li J, Li RJ, Lv GY, et al. The mechanisms and strategies to protect from hepatic ischemia-reperfusion injury. Eur Rev Med Pharmacol Sci, 2015, 19(11): 2036-2047.
3.	Kalogeris T, Baines CP, Krenz M, et al. Ischemia/reperfusion. Compr Physiol, 2016, 7(1): 113-170.
4.	Seo W, Jeong WI. Hepatic non-parenchymal cells: master regulators of alcoholic liver disease? World J Gastroenterol, 2016, 22(4): 1348-1356.
5.	Li X, Wu Y, Zhang W, et al. Pre-conditioning with tanshinone ⅡA attenuates the ischemia/reperfusion injury caused by liver grafts via regulation of HMGB1 in rat Kupffer cells. Biomed Pharmacother, 2017, 89: 1392-1400.
6.	Xu X, Wang M, Li JZ, et al. Tauroursodeoxycholic acid alleviates hepatic ischemia reperfusion injury by suppressing the function of Kupffer cells in mice. Biomed Pharmacother, 2018, 106: 1271-1281.
7.	Anzell AR, Maizy R, Przyklenk K, et al. Mitochondrial quality control and disease: insights into ischemia-reperfusion injury. Mol Neurobiol, 2018, 55(3): 2547-2564.
8.	Chen K, Li JJ, Li SN, et al. 15-Deoxy-Δ12,14-prostaglandin J2 alleviates hepatic ischemi-reperfusion injury in mice via inducing antioxidant response and inhibiting apoptosis and autophagy. Acta Pharmacol Sin, 2017, 38(5): 672-687.
9.	Karatzas T, Neri AA, Baibaki ME, et al. Rodent models of hepatic ischemia-reperfusion injury: time and percentage-related pathophysiological mechanisms. J Surg Res, 2014, 191(2): 399-412.
10.	Elias-Miró M, Jiménez-Castro MB, Rodés J, et al. Current knowledge on oxidative stress in hepatic ischemia/reperfusion. Free Radic Res, 2013, 47(8): 555-568.
11.	Suyavaran A, Ramamurthy C, Mareeswaran R, et al. TNF-α suppression by glutathione preconditioning attenuates hepatic ischemia reperfusion injury in young and aged rats. Inflamm Res, 2015, 64(1): 71-81.
12.	Zhang J, Xu P, Song P, et al. CCL2-CCR2 signaling promotes hepatic ischemia/reperfusion injury. J Surg Res, 2016, 202(2): 352-362.
13.	Qin CC, Liu YN, Hu Y, et al. Macrophage inflammatory protein-2 as mediator of inflammation in acute liver injury. World J Gastroenterol, 2017, 23(17): 3043-3052.
14.	Gao J, Jiang Z, Wang S, et al. Endoplasmic reticulum stress of Kupffer cells involved in the conversion of natural regulatory T cells to Th17 cells in liver ischemia-reperfusion injury. J Gastroenterol Hepatol, 2016, 31(4): 883-889.
15.	Chies AB, Nakazato PCG, Spadella MA, et al. Rivastigmine prevents injury induced by ischemia and reperfusion in rat liver. Acta Cir Bras, 2018, 33(9): 775-784.
16.	Ni M, Fu H, Huang F, et al. Vagus nerve attenuates hepatocyte apoptosis upon ischemia-reperfusion via α7 nicotinic acetylcholine receptor on Kupffer cells in mice. Anesthesiology, 2016, 125(5): 1005-1016.
17.	Shiraishi S, Cho S, Akiyama D, et al. Sevoflurane has postconditioning as well as preconditioning properties against hepatic warm ischemia-reperfusion injury in rats. J Anesth, 2019, 33(3): 390-398.
18.	Li S, Takahara T, Fujino M, et al. Astaxanthin prevents ischemia-reperfusion injury of the steatotic liver in mice. PLoS One, 2017, 12(11): e0187810.
19.	Yun N, Cho HI, Lee SM. Impaired autophagy contributes to hepatocellular damage during ischemia/reperfusion: heme oxygenase-1 as a possible regulator. Free Radic Biol Med, 2014, 68: 168-177.
20.	Xu D, Chen L, Chen X, et al. 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.
21.	Yazdani HO, Chen HW, Tohme S, et al. IL-33 exacerbates liver sterile inflammation by amplifying neutrophil extracellular trap formation. J Hepatol, 2018, 68(1): 130-139.
22.	Neumann K, Schiller B, Tiegs G. NLRP3 inflammasome and IL-33: novel players in sterile liver inflammation. Int J Mol Sci, 2018, 19(9): E2732.
23.	Xie F, Li ZP, Wang HW, et al. Evaluation of liver ischemia-reperfusion injury in rabbits using a nanoscale ultrasound contrast agent targeting ICAM-1. PLoS One, 2016, 11(4): e0153805.
24.	Peralta C, Jiménez-Castro MB, Gracia-Sancho J. Hepatic ischemia and reperfusion injury: effects on the liver sinusoidal milieu. J Hepatol, 2013, 59(5): 1094-1106.
25.	Jawad R, D’souza M, Selenius LA, et al. Morphological alterations and redox changes associated with hepatic warm ischemia-reperfusion injury. World J Hepatol, 2017, 9(34): 1261-1269.
26.	Teoh NC, Ajamieh H, Wong HJ, et al. Microparticles mediate hepatic ischemia-reperfusion injury and are the targets of Diannexin (ASP8597). PLoS One, 2014, 9(9): e104376.
27.	Takamura H, Nakanuma S, Hayashi H, et al. Severe veno-occlusive disease/sinusoidal obstruction syndrome after deceased-donor and living-donor liver transplantation. Transplant Proc, 2014, 46(10): 3523-3535.
28.	Nakanuma S, Miyashita T, Hayashi H, et al. Extravasated platelet aggregation in liver zone 3 may correlate with the progression of sinusoidal obstruction syndrome following living donor liver transplantation: a case report. Exp Ther Med, 2015, 9(4): 1119-1124.
29.	Ito T, Kuriyama N, Kato H, et al. Sinusoidal protection by sphingosine-1-phosphate receptor 1 agonist in liver ischemia-reperfusion injury. J Surg Res, 2018, 222: 139-152.
30.	Hessheimer AJ, Escobar B, Muñoz J, et al. Somatostatin therapy protects porcine livers in small-for-size liver transplantation. Am J Transplant, 2014, 14(8): 1806-1816.
31.	Banan B, Xiao Z, Watson R, et al. Novel strategy to decrease reperfusion injuries and improve function of cold-preserved livers using normothermic ex vivo liver perfusion machine. Liver Transpl, 2016, 22(3): 333-343.
32.	Weiskirchen S, Tag CG, Sauer-Lehnen S, et al. Isolation and culture of primary murine hepatic stellate cells. Methods Mol Biol, 2017, 1627: 165-191.
33.	Feng M, Wang Q, Wang H, et al. Adoptive transfer of hepatic stellate cells ameliorates liver ischemia reperfusion injury through enriching regulatory T cells. Int Immunopharmacol, 2014, 19(2): 267-274.
34.	Beck-Schimmer B, Roth Z’graggen B, Booy C, et al. Sevoflurane protects hepatocytes from ischemic injury by reducing reactive oxygen species signaling of hepatic stellate cells: translational fin-dings based on a clinical trial. Anesth Analg, 2018, 127(4): 1058-1065.
35.	Stewart RK, Dangi A, Huang C, et al. A novel mouse model of dep-letion of stellate cells clarifies their role in ischemia/reperfusion- and endotoxin-induced acute liver injury. J Hepatol, 2014, 60(2): 298-305.
36.	Marcos R. Depletion of hepatic stellate cells: have Kupffer cells lost their bad neighbor? J Hepatol, 2014, 61(3): 714-715.
37.	Konishi T, Schuster RM, Lentsch AB. Proliferation of hepatic stellate cells, mediated by YAP and TAZ, contributes to liver repair and regeneration after liver ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol, 2018, 314(4): G471-G482.
38.	Konishi T, Schuster RM, Lentsch AB. Liver repair and regeneration after ischemia-reperfusion injury is associated with prolonged fibrosis. Am J Physiol Gastrointest Liver Physiol, 2019, 316(3): G323-G331.
39.	Yoshida O, Kimura S, Jackson EK, et al. CD39 expression by hepatic myeloid dendritic cells attenuates inflammation in liver transplant ischemia-reperfusion injury in mice. Hepatology, 2013, 58(6): 2163-2175.
40.	Castellaneta A, Yoshida O, Kimura S, et al. Plasmacytoid dendritic cell-derived IFN-α promotes murine liver ischemia/reperfusion injury by induction of hepatocyte IRF-1. Hepatology, 2014, 60(1): 267-277.
41.	Funken D, Ishikawa-Ankerhold H, Uhl B, et al. In situ targeting of dendritic cells sets tolerogenic environment and ameliorates CD4⁺ T-cell response in the postischemic liver. FASEB J, 2017, 31(11): 4796-4808.
42.	Li J, Zhao X, Liu X, et al. Disruption of TIM-4 in dendritic cell ameliorates hepatic warm IR injury through the induction of regulatory T cells. Mol Immunol, 2015, 66(2): 117-125.

1. Konishi T, Lentsch AB. Hepatic ischemia/reperfusion: mechanisms of tissue injury, repair, and regeneration. Gene Expr, 2017, 17(4): 277-287.
2. Li J, Li RJ, Lv GY, et al. The mechanisms and strategies to protect from hepatic ischemia-reperfusion injury. Eur Rev Med Pharmacol Sci, 2015, 19(11): 2036-2047.
3. Kalogeris T, Baines CP, Krenz M, et al. Ischemia/reperfusion. Compr Physiol, 2016, 7(1): 113-170.
4. Seo W, Jeong WI. Hepatic non-parenchymal cells: master regulators of alcoholic liver disease? World J Gastroenterol, 2016, 22(4): 1348-1356.
5. Li X, Wu Y, Zhang W, et al. Pre-conditioning with tanshinone ⅡA attenuates the ischemia/reperfusion injury caused by liver grafts via regulation of HMGB1 in rat Kupffer cells. Biomed Pharmacother, 2017, 89: 1392-1400.
6. Xu X, Wang M, Li JZ, et al. Tauroursodeoxycholic acid alleviates hepatic ischemia reperfusion injury by suppressing the function of Kupffer cells in mice. Biomed Pharmacother, 2018, 106: 1271-1281.
7. Anzell AR, Maizy R, Przyklenk K, et al. Mitochondrial quality control and disease: insights into ischemia-reperfusion injury. Mol Neurobiol, 2018, 55(3): 2547-2564.
8. Chen K, Li JJ, Li SN, et al. 15-Deoxy-Δ12,14-prostaglandin J2 alleviates hepatic ischemi-reperfusion injury in mice via inducing antioxidant response and inhibiting apoptosis and autophagy. Acta Pharmacol Sin, 2017, 38(5): 672-687.
9. Karatzas T, Neri AA, Baibaki ME, et al. Rodent models of hepatic ischemia-reperfusion injury: time and percentage-related pathophysiological mechanisms. J Surg Res, 2014, 191(2): 399-412.
10. Elias-Miró M, Jiménez-Castro MB, Rodés J, et al. Current knowledge on oxidative stress in hepatic ischemia/reperfusion. Free Radic Res, 2013, 47(8): 555-568.
11. Suyavaran A, Ramamurthy C, Mareeswaran R, et al. TNF-α suppression by glutathione preconditioning attenuates hepatic ischemia reperfusion injury in young and aged rats. Inflamm Res, 2015, 64(1): 71-81.
12. Zhang J, Xu P, Song P, et al. CCL2-CCR2 signaling promotes hepatic ischemia/reperfusion injury. J Surg Res, 2016, 202(2): 352-362.
13. Qin CC, Liu YN, Hu Y, et al. Macrophage inflammatory protein-2 as mediator of inflammation in acute liver injury. World J Gastroenterol, 2017, 23(17): 3043-3052.
14. Gao J, Jiang Z, Wang S, et al. Endoplasmic reticulum stress of Kupffer cells involved in the conversion of natural regulatory T cells to Th17 cells in liver ischemia-reperfusion injury. J Gastroenterol Hepatol, 2016, 31(4): 883-889.
15. Chies AB, Nakazato PCG, Spadella MA, et al. Rivastigmine prevents injury induced by ischemia and reperfusion in rat liver. Acta Cir Bras, 2018, 33(9): 775-784.
16. Ni M, Fu H, Huang F, et al. Vagus nerve attenuates hepatocyte apoptosis upon ischemia-reperfusion via α7 nicotinic acetylcholine receptor on Kupffer cells in mice. Anesthesiology, 2016, 125(5): 1005-1016.
17. Shiraishi S, Cho S, Akiyama D, et al. Sevoflurane has postconditioning as well as preconditioning properties against hepatic warm ischemia-reperfusion injury in rats. J Anesth, 2019, 33(3): 390-398.
18. Li S, Takahara T, Fujino M, et al. Astaxanthin prevents ischemia-reperfusion injury of the steatotic liver in mice. PLoS One, 2017, 12(11): e0187810.
19. Yun N, Cho HI, Lee SM. Impaired autophagy contributes to hepatocellular damage during ischemia/reperfusion: heme oxygenase-1 as a possible regulator. Free Radic Biol Med, 2014, 68: 168-177.
20. Xu D, Chen L, Chen X, et al. 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.
21. Yazdani HO, Chen HW, Tohme S, et al. IL-33 exacerbates liver sterile inflammation by amplifying neutrophil extracellular trap formation. J Hepatol, 2018, 68(1): 130-139.
22. Neumann K, Schiller B, Tiegs G. NLRP3 inflammasome and IL-33: novel players in sterile liver inflammation. Int J Mol Sci, 2018, 19(9): E2732.
23. Xie F, Li ZP, Wang HW, et al. Evaluation of liver ischemia-reperfusion injury in rabbits using a nanoscale ultrasound contrast agent targeting ICAM-1. PLoS One, 2016, 11(4): e0153805.
24. Peralta C, Jiménez-Castro MB, Gracia-Sancho J. Hepatic ischemia and reperfusion injury: effects on the liver sinusoidal milieu. J Hepatol, 2013, 59(5): 1094-1106.
25. Jawad R, D’souza M, Selenius LA, et al. Morphological alterations and redox changes associated with hepatic warm ischemia-reperfusion injury. World J Hepatol, 2017, 9(34): 1261-1269.
26. Teoh NC, Ajamieh H, Wong HJ, et al. Microparticles mediate hepatic ischemia-reperfusion injury and are the targets of Diannexin (ASP8597). PLoS One, 2014, 9(9): e104376.
27. Takamura H, Nakanuma S, Hayashi H, et al. Severe veno-occlusive disease/sinusoidal obstruction syndrome after deceased-donor and living-donor liver transplantation. Transplant Proc, 2014, 46(10): 3523-3535.
28. Nakanuma S, Miyashita T, Hayashi H, et al. Extravasated platelet aggregation in liver zone 3 may correlate with the progression of sinusoidal obstruction syndrome following living donor liver transplantation: a case report. Exp Ther Med, 2015, 9(4): 1119-1124.
29. Ito T, Kuriyama N, Kato H, et al. Sinusoidal protection by sphingosine-1-phosphate receptor 1 agonist in liver ischemia-reperfusion injury. J Surg Res, 2018, 222: 139-152.
30. Hessheimer AJ, Escobar B, Muñoz J, et al. Somatostatin therapy protects porcine livers in small-for-size liver transplantation. Am J Transplant, 2014, 14(8): 1806-1816.
31. Banan B, Xiao Z, Watson R, et al. Novel strategy to decrease reperfusion injuries and improve function of cold-preserved livers using normothermic ex vivo liver perfusion machine. Liver Transpl, 2016, 22(3): 333-343.
32. Weiskirchen S, Tag CG, Sauer-Lehnen S, et al. Isolation and culture of primary murine hepatic stellate cells. Methods Mol Biol, 2017, 1627: 165-191.
33. Feng M, Wang Q, Wang H, et al. Adoptive transfer of hepatic stellate cells ameliorates liver ischemia reperfusion injury through enriching regulatory T cells. Int Immunopharmacol, 2014, 19(2): 267-274.
34. Beck-Schimmer B, Roth Z’graggen B, Booy C, et al. Sevoflurane protects hepatocytes from ischemic injury by reducing reactive oxygen species signaling of hepatic stellate cells: translational fin-dings based on a clinical trial. Anesth Analg, 2018, 127(4): 1058-1065.
35. Stewart RK, Dangi A, Huang C, et al. A novel mouse model of dep-letion of stellate cells clarifies their role in ischemia/reperfusion- and endotoxin-induced acute liver injury. J Hepatol, 2014, 60(2): 298-305.
36. Marcos R. Depletion of hepatic stellate cells: have Kupffer cells lost their bad neighbor? J Hepatol, 2014, 61(3): 714-715.
37. Konishi T, Schuster RM, Lentsch AB. Proliferation of hepatic stellate cells, mediated by YAP and TAZ, contributes to liver repair and regeneration after liver ischemia-reperfusion injury. Am J Physiol Gastrointest Liver Physiol, 2018, 314(4): G471-G482.
38. Konishi T, Schuster RM, Lentsch AB. Liver repair and regeneration after ischemia-reperfusion injury is associated with prolonged fibrosis. Am J Physiol Gastrointest Liver Physiol, 2019, 316(3): G323-G331.
39. Yoshida O, Kimura S, Jackson EK, et al. CD39 expression by hepatic myeloid dendritic cells attenuates inflammation in liver transplant ischemia-reperfusion injury in mice. Hepatology, 2013, 58(6): 2163-2175.
40. Castellaneta A, Yoshida O, Kimura S, et al. Plasmacytoid dendritic cell-derived IFN-α promotes murine liver ischemia/reperfusion injury by induction of hepatocyte IRF-1. Hepatology, 2014, 60(1): 267-277.
41. Funken D, Ishikawa-Ankerhold H, Uhl B, et al. In situ targeting of dendritic cells sets tolerogenic environment and ameliorates CD4⁺ T-cell response in the postischemic liver. FASEB J, 2017, 31(11): 4796-4808.
42. Li J, Zhao X, Liu X, et al. Disruption of TIM-4 in dendritic cell ameliorates hepatic warm IR injury through the induction of regulatory T cells. Mol Immunol, 2015, 66(2): 117-125.

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CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Research progress of the function of liver non-parenchymal cells in hepatic ischemia-reperfusion injury

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