Advances of liver sinusoidal endothelial cells regulating hepatic sinusoidal microenvironment to promote liver regeneration_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

QING Zhe ,  ZENG Zhong

Organ Transplantation Center, The First Affiliated Hospital of Kunming Medical University, Kunming 650032, P. R. China;

Corresponding author：

ZENG Zhong, Email: zzong9933@163.com

Keywords：

liver sinusoidal endothelial cell; hepatic sinusoidal microenvironment; liver regeneration

DOI：

10.7507/1007-9424.202110002

Video：

Export PDF Favorites Scan Get Citation

Abstract Full text Figures/Tables Video References Cited by

Objective To summarize the research progress on the regulation of hepatic sinusoidal microenvironment to promote liver regeneration based on liver sinusoidal endothelial cells (LSECs), aiming to further clarify the mechanism of liver regeneration and provide new ideas and methods for clinical promotion of liver regeneration and prevention of liver failure. Method The basic and clinical research studies on LSECs and liver regeneration at home and abroad in recent years were searched and reviewed. Results Differentiated LSECs played an important role in liver regeneration, regulated the homeostasis of hepatic sinusoid microenvironment by paracrine and autocrine, and participated in the whole process of promoting liver regeneration, such as hepatocyte proliferation and neovascularization after acute and chronic liver injury. Conclusion In the process of liver regeneration after all kinds of acute and chronic liver injury, LSECs promote liver regeneration by regulating hepatic sinusoid microenvironment, which will provide new strategies and methods for clinical promotion of liver regeneration and prevention of liver failure after hepatectomy.

Citation： QING Zhe, ZENG Zhong. Advances of liver sinusoidal endothelial cells regulating hepatic sinusoidal microenvironment to promote liver regeneration. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2022, 29(7): 958-964. doi: 10.7507/1007-9424.202110002 Copy

1.	袁博, 瞿思铭, 黄汉飞, 等. 肝窦内皮细胞介导肝再生与纤维化平衡的研究进展. 中华肝胆外科杂志, 2021, 27(7): 545-548.
2.	祖广晨, 谭煜炜, 陈学敏, 等. 肝窦内皮细胞与肝再生的研究进展. 中华肝胆外科杂志, 2019, 25(7): 546-549.
3.	Ding BS, Nolan D J, Butler J M, et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature, 2010, 468(7321): 310-315.
4.	Lu J, Zhao YL, Zhang XQ, et al. The vascular endothelial growth factor signaling pathway regulates liver sinusoidal endothelial cells during liver regeneration after partial hepatectomy. Expert Rev Gastroenterol Hepatol, 2021, 15(2): 139-147.
5.	Cogger VC, Mcnerney GP, Nyunt T, et al. Three-dimensional structured illumination microscopy of liver sinusoidal endothelial cell fenestrations. J Struct Biol, 2010, 171(3): 382-388.
6.	Deleve LD, Maretti-Mira AC. Liver sinusoidal endothelial cell: an update. Semin Liver Dis, 2017, 37(4): 377-387.
7.	Sorensen KK, Simon-Santamaria J, Mccuskey RS, et al. Liver sinusoidal endothelial cells. Compr Physiol, 2015, 5(4): 1751-1774.
8.	May D, Djonov V, Zamir G, et al. A transgenic model for conditional induction and rescue of portal hypertension reveals a role of VEGF-mediated regulation of sinusoidal fenestrations. PLoS One, 2011, 6(7): e21478. doi: 10.1371/journal.pone.0021478.
9.	Deleve LD, Wang X, Hu L, et al. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol, 2004, 287(4): G757-G763. doi: 10.1152/ajpgi.00017.2004.
10.	Xie G, Wang X, Wang L, et al. Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats. Gastroenterology, 2012, 142(4): 918-927.
11.	Yokomori H, Oda M, Yoshimura K, et al. Vascular endothelial growth factor increases fenestral permeability in hepatic sinusoidal endothelial cells. Liver Int, 2003, 23(6): 467-475.
12.	Funyu J, Mochida S, Inao M, et al. VEGF can act as vascular permeability factor in the hepatic sinusoids through upregulation of porosity of endothelial cells. Biochem Biophys Res Commun, 2001, 280(2): 481-485.
13.	Wang L, Wang X, Wang L, et al. Hepatic vascular endothelial growth factor regulates recruitment of rat liver sinusoidal endothelial cell progenitor cells. Gastroenterology, 2012, 143(6): 1555-1563.
14.	Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol, 2004, 5(10): 836-847.
15.	Zhang XJ, Olsavszky V, Yin Y, et al. Angiocrine hepatocyte growth factor signaling controls physiological organ and body size and dynamic hepatocyte proliferation to prevent liver damage during regeneration. Am J Pathol, 2020, 190(2): 358-371.
16.	Qing Z, Huang H, Yang S, et al. Hypoxia maintains the fenestration of liver sinusoidal endothelial cells and promotes their proliferation through the SENP1/HIF-1alpha/VEGF signaling axis. Biochem Biophys Res Commun, 2021, 540: 42-50.
17.	Qu S, Yuan B, Zhang H, et al. Heme oxygenase 1 attenuates hypoxia-reoxygenation injury in mice liver sinusoidal endothelial cells. Transplantation, 2018, 102(3): 426-432.
18.	Poisson J, Lemoinne S, Boulanger C, et al. Liver sinusoidal endothelial cells: Physiology and role in liver diseases. J Hepatol, 2017, 66(1): 212-227.
19.	Golse N, Bucur PO, Adam R, et al. New paradigms in post-hepatectomy liver failure. J Gastrointest Surg, 2013, 17(3): 593-605.
20.	Yagi S, Hirata M, Miyachi Y, et al. Liver Regeneration after hepatectomy and partial liver transplantation. Int J Mol Sci, 2020, 21(21): 8414. doi: 10.3390/ijms21218414.
21.	Ito K, Ozasa H, Horikawa S. Effects of prior splenectomy on remnant liver after partial hepatectomy with Pringle maneuver in rats. Liver Int, 2005, 25(2): 438-444.
22.	Yoshizumi T, Taketomi A, Soejima Y, et al. The beneficial role of simultaneous splenectomy in living donor liver transplantation in patients with small-for-size graft. Transpl Int, 2008, 21(9): 833-842.
23.	Hu J, Srivastava K, Wieland M, et al. Endothelial cell-derived angiopoietin-2 controls liver regeneration as a spatiotemporal rheostat. Science, 2014, 343(6169): 416-419.
24.	DeLeve LD. Liver sinusoidal endothelial cells and liver regeneration. J Clin Invest, 2013, 123(5): 1861-1866.
25.	LeCouter J, Moritz DR, Li B, et al. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science, 2003, 299(5608): 890-893.
26.	Wang WL, Zheng XL, Li QS, et al. The effect of aging on VEGF/VEGFR2 signal pathway genes expression in rat liver sinusoidal endothelial cell. Mol Cell Biochem, 2021, 476(1): 269-277.
27.	De Rudder M, Dili A, Starkel P, et al. Critical role of LSEC in post-hepatectomy liver regeneration and failure. Int J Mol Sci, 2021, 22(15): 8053. doi: 10.3390/ijms22158053.
28.	Gracia-Sancho J, Caparros E, Fernandez-Iglesias A, et al. Role of liver sinusoidal endothelial cells in liver diseases. Nat Rev Gastroenterol Hepatol, 2021, 18(6): 411-431.
29.	Cannistra M, Ruggiero M, Zullo A, et al. Hepatic ischemia reperfusion injury: a systematic review of literature and the role of current drugs and biomarkers. Int J Surg, 2016, 33 Suppl 1: S57-S70.
30.	Miyashita T, Nakanuma S, Ahmed AK, et al. Ischemia reperfusion-facilitated sinusoidal endothelial cell injury in liver transplantation and the resulting impact of extravasated platelet aggregation. Eur Surg, 2016, 48: 92-98.
31.	Kojima H, Nakamura K, Kupiec-Weglinski JW. Therapeutic targets for liver regeneration after acute severe injury: a preclinical overview. Expert Opin Ther Targets, 2020, 24(1): 13-24.
32.	Canto C, Auwerx J. AMP-activated protein kinase and its downstream transcriptional pathways. Cell Mol Life Sci, 2010, 67(20): 3407-3423.
33.	Hoyer-Hansen M, Jaattela M. AMP-activated protein kinase: a universal regulator of autophagy. Autophagy, 2007, 3(4): 381-383.
34.	Kim HS, Montana V, Jang HJ, et al. Epigallocatechin gallate (EGCG) stimulates autophagy in vascular endothelial cells: a potential role for reducing lipid accumulation. J Biol Chem, 2013, 288(31): 22693-22705.
35.	Ghislat G, Patron M, Rizzuto R, et al. Withdrawal of essential amino acids increases autophagy by a pathway involving Ca2⁺/calmodulin-dependent kinase kinase-beta (CaMKK-beta). J Biol Chem, 2012, 287(46): 38625-38636.
36.	Massip-Salcedo M, Casillas-Ramirez A, Franco-Gou R, et al. Heat shock proteins and mitogen-activated protein kinases in steatotic livers undergoing ischemia-reperfusion: some answers. Am J Pathol, 2006, 168(5): 1474-1485.
37.	Ma H, Liu X, Zhang M, et al. Liver sinusoidal endothelial cells are implicated in multiple fibrotic mechanisms. Mol Biol Rep, 2021, 48(3): 2803-2815.
38.	Lafoz E, Ruart M, Anton A, et al. The endothelium as a driver of liver fibrosis and regeneration. Cells, 2020, 9(4): 929. doi: 10.3390/cells9040929.
39.	Li H. Intercellular crosstalk of liver sinusoidal endothelial cells in liver fibrosis, cirrhosis and hepatocellular carcinoma. Dig Liver Dis, 2021 Jul 31: S1590-8658(21)00375-3. doi: 10.1016/j.dld.2021.07.006. Online ahead of print.
40.	Di Pascoli M, Divi M, Rodriguez-Vilarrupla A, et al. Resveratrol improves intrahepatic endothelial dysfunction and reduces hepatic fibrosis and portal pressure in cirrhotic rats. J Hepatol, 2013, 58(5): 904-910.
41.	Yan Z, Qu K, Zhang J, et al. CD147 promotes liver fibrosis progression via VEGF-A/VEGFR2 signalling-mediated cross-talk between hepatocytes and sinusoidal endothelial cells. Clin Sci (Lond), 2015, 129(8): 699-710.
42.	Zhang DW, Zhao YX, Wei D, et al. HAb18G/CD147 promotes activation of hepatic stellate cells and is a target for antibody therapy of liver fibrosis. J Hepatol, 2012, 57(6): 1283-1291.
43.	Kambakamba P, Linecker M, Schneider M, et al. Novel benefits of remote ischemic preconditioning through VEGF-dependent protection from resection-induced liver failure in the mouse. Ann Surg, 2018, 268(5): 885-893.
44.	Piao J, Jeong J, Jung J, et al. Substance P promotes liver sinusoidal endothelium-mediated hepatic regeneration by NO/HGF regulation. J Interferon Cytokine Res, 2019, 39(3): 147-154.
45.	Bravo M, Raurell I, Hide D, et al. Restoration of liver sinusoidal cell phenotypes by statins improves portal hypertension and histology in rats with NASH. Sci Rep, 2019, 9(1): 20183. doi: 10.1038/s41598-019-56366-2.
46.	Guixé-Muntet S, de Mesquita FC, Vila S, et al. Cross-talk between autophagy and KLF2 determines endothelial cell phenotype and microvascular function in acute liver injury. J Hepatol, 2017, 66(1): 86-94.
47.	Meyer J, Balaphas A, Fontana P, et al. Platelet interactions with liver sinusoidal endothelial cells and hepatic stellate cells lead to hepatocyte proliferation. Cells, 2020, 9(5): 1243. doi: 10.3390/cells9051243.

1. 袁博, 瞿思铭, 黄汉飞, 等. 肝窦内皮细胞介导肝再生与纤维化平衡的研究进展. 中华肝胆外科杂志, 2021, 27(7): 545-548.
2. 祖广晨, 谭煜炜, 陈学敏, 等. 肝窦内皮细胞与肝再生的研究进展. 中华肝胆外科杂志, 2019, 25(7): 546-549.
3. Ding BS, Nolan D J, Butler J M, et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature, 2010, 468(7321): 310-315.
4. Lu J, Zhao YL, Zhang XQ, et al. The vascular endothelial growth factor signaling pathway regulates liver sinusoidal endothelial cells during liver regeneration after partial hepatectomy. Expert Rev Gastroenterol Hepatol, 2021, 15(2): 139-147.
5. Cogger VC, Mcnerney GP, Nyunt T, et al. Three-dimensional structured illumination microscopy of liver sinusoidal endothelial cell fenestrations. J Struct Biol, 2010, 171(3): 382-388.
6. Deleve LD, Maretti-Mira AC. Liver sinusoidal endothelial cell: an update. Semin Liver Dis, 2017, 37(4): 377-387.
7. Sorensen KK, Simon-Santamaria J, Mccuskey RS, et al. Liver sinusoidal endothelial cells. Compr Physiol, 2015, 5(4): 1751-1774.
8. May D, Djonov V, Zamir G, et al. A transgenic model for conditional induction and rescue of portal hypertension reveals a role of VEGF-mediated regulation of sinusoidal fenestrations. PLoS One, 2011, 6(7): e21478. doi: 10.1371/journal.pone.0021478.
9. Deleve LD, Wang X, Hu L, et al. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol, 2004, 287(4): G757-G763. doi: 10.1152/ajpgi.00017.2004.
10. Xie G, Wang X, Wang L, et al. Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats. Gastroenterology, 2012, 142(4): 918-927.
11. Yokomori H, Oda M, Yoshimura K, et al. Vascular endothelial growth factor increases fenestral permeability in hepatic sinusoidal endothelial cells. Liver Int, 2003, 23(6): 467-475.
12. Funyu J, Mochida S, Inao M, et al. VEGF can act as vascular permeability factor in the hepatic sinusoids through upregulation of porosity of endothelial cells. Biochem Biophys Res Commun, 2001, 280(2): 481-485.
13. Wang L, Wang X, Wang L, et al. Hepatic vascular endothelial growth factor regulates recruitment of rat liver sinusoidal endothelial cell progenitor cells. Gastroenterology, 2012, 143(6): 1555-1563.
14. Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol, 2004, 5(10): 836-847.
15. Zhang XJ, Olsavszky V, Yin Y, et al. Angiocrine hepatocyte growth factor signaling controls physiological organ and body size and dynamic hepatocyte proliferation to prevent liver damage during regeneration. Am J Pathol, 2020, 190(2): 358-371.
16. Qing Z, Huang H, Yang S, et al. Hypoxia maintains the fenestration of liver sinusoidal endothelial cells and promotes their proliferation through the SENP1/HIF-1alpha/VEGF signaling axis. Biochem Biophys Res Commun, 2021, 540: 42-50.
17. Qu S, Yuan B, Zhang H, et al. Heme oxygenase 1 attenuates hypoxia-reoxygenation injury in mice liver sinusoidal endothelial cells. Transplantation, 2018, 102(3): 426-432.
18. Poisson J, Lemoinne S, Boulanger C, et al. Liver sinusoidal endothelial cells: Physiology and role in liver diseases. J Hepatol, 2017, 66(1): 212-227.
19. Golse N, Bucur PO, Adam R, et al. New paradigms in post-hepatectomy liver failure. J Gastrointest Surg, 2013, 17(3): 593-605.
20. Yagi S, Hirata M, Miyachi Y, et al. Liver Regeneration after hepatectomy and partial liver transplantation. Int J Mol Sci, 2020, 21(21): 8414. doi: 10.3390/ijms21218414.
21. Ito K, Ozasa H, Horikawa S. Effects of prior splenectomy on remnant liver after partial hepatectomy with Pringle maneuver in rats. Liver Int, 2005, 25(2): 438-444.
22. Yoshizumi T, Taketomi A, Soejima Y, et al. The beneficial role of simultaneous splenectomy in living donor liver transplantation in patients with small-for-size graft. Transpl Int, 2008, 21(9): 833-842.
23. Hu J, Srivastava K, Wieland M, et al. Endothelial cell-derived angiopoietin-2 controls liver regeneration as a spatiotemporal rheostat. Science, 2014, 343(6169): 416-419.
24. DeLeve LD. Liver sinusoidal endothelial cells and liver regeneration. J Clin Invest, 2013, 123(5): 1861-1866.
25. LeCouter J, Moritz DR, Li B, et al. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science, 2003, 299(5608): 890-893.
26. Wang WL, Zheng XL, Li QS, et al. The effect of aging on VEGF/VEGFR2 signal pathway genes expression in rat liver sinusoidal endothelial cell. Mol Cell Biochem, 2021, 476(1): 269-277.
27. De Rudder M, Dili A, Starkel P, et al. Critical role of LSEC in post-hepatectomy liver regeneration and failure. Int J Mol Sci, 2021, 22(15): 8053. doi: 10.3390/ijms22158053.
28. Gracia-Sancho J, Caparros E, Fernandez-Iglesias A, et al. Role of liver sinusoidal endothelial cells in liver diseases. Nat Rev Gastroenterol Hepatol, 2021, 18(6): 411-431.
29. Cannistra M, Ruggiero M, Zullo A, et al. Hepatic ischemia reperfusion injury: a systematic review of literature and the role of current drugs and biomarkers. Int J Surg, 2016, 33 Suppl 1: S57-S70.
30. Miyashita T, Nakanuma S, Ahmed AK, et al. Ischemia reperfusion-facilitated sinusoidal endothelial cell injury in liver transplantation and the resulting impact of extravasated platelet aggregation. Eur Surg, 2016, 48: 92-98.
31. Kojima H, Nakamura K, Kupiec-Weglinski JW. Therapeutic targets for liver regeneration after acute severe injury: a preclinical overview. Expert Opin Ther Targets, 2020, 24(1): 13-24.
32. Canto C, Auwerx J. AMP-activated protein kinase and its downstream transcriptional pathways. Cell Mol Life Sci, 2010, 67(20): 3407-3423.
33. Hoyer-Hansen M, Jaattela M. AMP-activated protein kinase: a universal regulator of autophagy. Autophagy, 2007, 3(4): 381-383.
34. Kim HS, Montana V, Jang HJ, et al. Epigallocatechin gallate (EGCG) stimulates autophagy in vascular endothelial cells: a potential role for reducing lipid accumulation. J Biol Chem, 2013, 288(31): 22693-22705.
35. Ghislat G, Patron M, Rizzuto R, et al. Withdrawal of essential amino acids increases autophagy by a pathway involving Ca2⁺/calmodulin-dependent kinase kinase-beta (CaMKK-beta). J Biol Chem, 2012, 287(46): 38625-38636.
36. Massip-Salcedo M, Casillas-Ramirez A, Franco-Gou R, et al. Heat shock proteins and mitogen-activated protein kinases in steatotic livers undergoing ischemia-reperfusion: some answers. Am J Pathol, 2006, 168(5): 1474-1485.
37. Ma H, Liu X, Zhang M, et al. Liver sinusoidal endothelial cells are implicated in multiple fibrotic mechanisms. Mol Biol Rep, 2021, 48(3): 2803-2815.
38. Lafoz E, Ruart M, Anton A, et al. The endothelium as a driver of liver fibrosis and regeneration. Cells, 2020, 9(4): 929. doi: 10.3390/cells9040929.
39. Li H. Intercellular crosstalk of liver sinusoidal endothelial cells in liver fibrosis, cirrhosis and hepatocellular carcinoma. Dig Liver Dis, 2021 Jul 31: S1590-8658(21)00375-3. doi: 10.1016/j.dld.2021.07.006. Online ahead of print.
40. Di Pascoli M, Divi M, Rodriguez-Vilarrupla A, et al. Resveratrol improves intrahepatic endothelial dysfunction and reduces hepatic fibrosis and portal pressure in cirrhotic rats. J Hepatol, 2013, 58(5): 904-910.
41. Yan Z, Qu K, Zhang J, et al. CD147 promotes liver fibrosis progression via VEGF-A/VEGFR2 signalling-mediated cross-talk between hepatocytes and sinusoidal endothelial cells. Clin Sci (Lond), 2015, 129(8): 699-710.
42. Zhang DW, Zhao YX, Wei D, et al. HAb18G/CD147 promotes activation of hepatic stellate cells and is a target for antibody therapy of liver fibrosis. J Hepatol, 2012, 57(6): 1283-1291.
43. Kambakamba P, Linecker M, Schneider M, et al. Novel benefits of remote ischemic preconditioning through VEGF-dependent protection from resection-induced liver failure in the mouse. Ann Surg, 2018, 268(5): 885-893.
44. Piao J, Jeong J, Jung J, et al. Substance P promotes liver sinusoidal endothelium-mediated hepatic regeneration by NO/HGF regulation. J Interferon Cytokine Res, 2019, 39(3): 147-154.
45. Bravo M, Raurell I, Hide D, et al. Restoration of liver sinusoidal cell phenotypes by statins improves portal hypertension and histology in rats with NASH. Sci Rep, 2019, 9(1): 20183. doi: 10.1038/s41598-019-56366-2.
46. Guixé-Muntet S, de Mesquita FC, Vila S, et al. Cross-talk between autophagy and KLF2 determines endothelial cell phenotype and microvascular function in acute liver injury. J Hepatol, 2017, 66(1): 86-94.
47. Meyer J, Balaphas A, Fontana P, et al. Platelet interactions with liver sinusoidal endothelial cells and hepatic stellate cells lead to hepatocyte proliferation. Cells, 2020, 9(5): 1243. doi: 10.3390/cells9051243.

Previous Article
Research progress on relation of immune cell infiltration and prognosis of hepatocellular carcinoma
Next Article
Research progress of Hippo signaling pathway in triple negative breast cancer

CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Advances of liver sinusoidal endothelial cells regulating hepatic sinusoidal microenvironment to promote liver regeneration

Abstract Full text Figures/Tables Video References Cited by

Previous Article

Next Article

Format

Content