Classical and alternative activation of rat hepatic sinusoidal endothelial cells by inflammatory stimuli

Experimental and Molecular Pathology

Volumn 94, Issue 1, 2013, Pages 160-167

  Liu, Yinglin ^a   Gardner, Carol R ^a   Laskin, Jeffrey D ^b   Laskin, Debra L ^a  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

Author keywords

Acetaminophen; Endothelial cells; INOS; Kupffer cells; Liver; Mannose receptor

Indexed keywords

ARGINASE 1; BETA CATENIN; GAMMA INTERFERON; GELATINASE A; GELATINASE B; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 4; LIPOPOLYSACCHARIDE; MANNOSE RECEPTOR; PARACETAMOL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COCULTURE; CONTROLLED STUDY; ENDOTHELIUM CELL; INFLAMMATION; KUPFFER CELL; LIVER CELL; LIVER TOXICITY; MACROPHAGE ACTIVATION; MALE; NONHUMAN; RAT; UPREGULATION;

ACETAMINOPHEN; ANIMALS; ARGINASE; BETA CATENIN; CELLS, CULTURED; COCULTURE TECHNIQUES; ENDOTHELIAL CELLS; HEPATOCYTES; INFLAMMATION; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-13; INTERLEUKIN-4; KUPFFER CELLS; LECTINS, C-TYPE; LIPOPOLYSACCHARIDES; LIVER; MACROPHAGE ACTIVATION; MALE; MANNOSE-BINDING LECTINS; MATRIX METALLOPROTEINASE 9; NITRIC OXIDE SYNTHASE TYPE II; PROLIFERATING CELL NUCLEAR ANTIGEN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CELL SURFACE;

RATTUS;

EID: 84870881596     PISSN: 00144800     EISSN: 10960945     Source Type: Journal    
DOI: 10.1016/j.yexmp.2012.10.015     Document Type: Article

References (67)

1. Ahmad N., Gardner C.R., Yurkow E.J., Laskin D.L. Inhibition of macrophages with gadolinium chloride alters intercellular adhesion molecule-1 expression in the liver during acute endotoxemia in rats. Hepatology 1999, 29:728-736.
2. Antoine D.J., Mercer A.E., Williams D.P., Park B.K. Mechanism-based bioanalysis and biomarkers for hepatic chemical stress. Xenobiotica 2009, 39:565-577.
3. Antoine D.J., Jenkins R.E., Dear J.W., Williams D.P., McGill M.R., Sharpe M.R., Craig D.G., Simpson K.J., Jaeschke H., Park B.K. Molecular forms of HMGB1 and keratin-18 as mechanistic biomarkers for mode of cell death and prognosis during clinical acetaminophen hepatotoxicity. Journal of Hepatology 2012, 56:1070-1079.
4. Aoyama T., Paik Y.H., Seki E. Toll-like receptor signaling and liver fibrosis. Gastroenterology Research and Practice 2010, 2010:192543.
5. Blazka M.E., Germolec D.R., Simeonova P., Bruccoleri A., Pennypacker K.R., Luster M.I. Acetaminophen-induced hepatotoxicity is associated with early changes in NF-κB and NF-IL6 DNA binding activity. Journal of Inflammation 1995, 47:138-150.
6. Bourdi M., Masubuchi Y., Reilly T.P., Amouzadeh H.R., Martin J.L., George J.W., Shah A.G., Pohl L.R. Protection against acetaminophen-induced liver injury and lethality by interleukin 10: role of inducible nitric oxide synthase. Hepatology 2002, 35:289-298.
7. Bourdi M., Eiras D.P., Holt M.P., Webster M.R., Reilly T.P., Welch K.D., Pohl L.R. Role of IL-6 in an IL-10 and IL-4 double knockout mouse model uniquely susceptible to acetaminophen-induced liver injury. Chemical Research in Toxicology 2007, 20:208-216.
8. Chen L.C., Gordon R.E., Laskin J.D., Laskin D.L. Role of TLR-4 in liver macrophage and endothelial cell responsiveness during acute endotoxemia. Experimental and Molecular Pathology 2007, 83:311-326.
9. Chiu H., Gardner C.R., Dambach D.M., Durham S.K., Brittingham J.A., Laskin J.D., Laskin D.L. Role of tumor necrosis factor receptor 1 (p55) in hepatocyte proliferation during acetaminophen-induced toxicity in mice. Toxicology and Applied Pharmacology 2003, 193:218-227.
10. Cohen S.D., Khairallah E.A. Selective protein arylation and acetaminophen-induced hepatotoxicity. Drug Metabolism Reviews 1997, 29:59-77.
11. Dambach D.M., Watson L.M., Gray K.R., Durham S.K., Laskin D.L. Role of CCR2 in macrophage migration into the liver during acetaminophen-induced hepatotoxicity in the mouse. Hepatology 2002, 35:1093-1103.
12. Dambach D.M., Durham S.K., Laskin J.D., Laskin D.L. Distinct roles of NF-κB p50 in the regulation of acetaminophen-induced inflammatory mediator production and hepatotoxicity. Toxicology and Applied Pharmacology 2006, 211:157-165.
13. DeLeve L.D., Wang X., Kaplowitz N., Shulman H.M., Bart J.A., van der Hoek A. Sinusoidal endothelial cells as a target for acetaminophen toxicity. Direct action versus requirement for hepatocyte activation in different mouse strains. Biochemical Pharmacology 1997, 53:1339-1345.
14. Dragomir A.C., Laskin J.D., Laskin D.L. Macrophage activation by factors released from acetaminophen-injured hepatocytes: potential role of HMGB1. Toxicology and Applied Pharmacology 2011, 253:170-177.
15. Dragomir A.C., Laskin J.D., Laskin D.L. Role of galectin-3 in acetaminophen-induced hepatotoxicity and inflammatory mediator production. Toxicological Sciences 2012, 127:609-619.
16. Dragomir, A.C., Sun, R., Choi, H., Laskin, J.D., Laskin, D.L., in press. Role of galectin-3 in classical and alternative macrophage activation in the liver following acetaminophen intoxication. Journal of Immunology http://www.jimmunol.org/cgi/doi/10.4049/jimmunol.120185.
17. Elvevold K., Simon-Santamaria J., Hasvold H., McCourt P., Smedsrod B., Sorensen K.K. Liver sinusoidal endothelial cells depend on mannose receptor-mediated recruitment of lysosomal enzymes for normal degradation capacity. Hepatology 2008, 48:2007-2015.
18. Enomoto K., Nishikawa Y., Omori Y., Tokairin T., Yoshida M., Ohi N., Nishimura T., Yamamoto Y., Li Q. Cell biology and pathology of liver sinusoidal endothelial cells. Medical Electron Microscopy 2004, 37:208-215.
19. Feder L.S., Laskin D.L. Regulation of hepatic endothelial cell and macrophage proliferation and nitric oxide production by GM-CSF, M-CSF, and IL-1β following acute endotoxemia. Journal of Leukocyte Biology 1994, 55:507-513.
20. Feder L.S., Todaro J.A., Laskin D.L. Characterization of interleukin-1 and interleukin-6 production by hepatic endothelial cells and macrophages. Journal of Leukocyte Biology 1993, 53:126-132.
21. Gardner C.R., Laskin D.L. Sinusoidal Cells in Liver Injury and Repair. Hepatotoxicity: from Genomics to In Vitro and In Vivo Models 2007, 341-370. John Wiley & Sons, West Sussex. S.C. Sahu (Ed.).
22. Gardner C.R., Heck D.E., Yang C.S., Thomas P.E., Zhang X.J., DeGeorge G.L., Laskin J.D., Laskin D.L. Role of nitric oxide in acetaminophen-induced hepatotoxicity in the rat. Hepatology 1998, 27:748-754.
23. Gardner C.R., Laskin J.D., Dambach D.M., Chiu H., Durham S.K., Zhou P., Bruno M., Gerecke D.R., Gordon M.K., Laskin D.L. Exaggerated hepatotoxicity of acetaminophen in mice lacking tumor necrosis factor receptor-1. Potential role of inflammatory mediators. Toxicology and Applied Pharmacology 2003, 192:119-130.
24. Gardner G.R., Mishin V., Hankey P., Laskin J.D., Laskin D.L. Regulation of alternative macrophage activation in the liver following acetaminophen intoxication by stem cell-derived tyrosine kinase. Toxicology and Applied Pharmacology 2012, 262:139-148.
25. Gieling R.G., Elsharkawy A.M., Caamano J.H., Cowie D.E., Wright M.C., Ebrahimkhani M.R., Burt A.D., Mann J., Raychaudhuri P., Liou H.C., Oakley F., Mann D.A. The c-Rel subunit of nuclear factor-κB regulates murine liver inflammation, wound-healing, and hepatocyte proliferation. Hepatology 2010, 51:922-931.
26. Gratchev A., Kzhyshkowska J., Kothe K., Muller-Molinet I., Kannookadan S., Utikal J., Goerdt S. Mφ1 and Mφ2 can be re-polarized by Th2 or Th1 cytokines, respectively, and respond to exogenous danger signals. Immunobiology 2006, 211:473-486.
27. Hogaboam C.M., Bone-Larson C.L., Steinhauser M.L., Matsukawa A., Gosling J., Boring L., Charo I.F., Simpson K.J., Lukacs N.W., Kunkel S.L. Exaggerated hepatic injury due to acetaminophen challenge in mice lacking C-C chemokine receptor 2. American Journal of Pathology 2000, 156:1245-1252.
28. Holt M.P., Cheng L., Ju C. Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. Journal of Leukocyte Biology 2008, 84:1410-1421.
29. Ikeda A., Ueki S., Nakao A., Tomiyama K., Ross M.A., Stolz D.B., Geller D.A., Murase N. Liver graft exposure to carbon monoxide during cold storage protects sinusoidal endothelial cells and ameliorates reperfusion injury in rats. Liver Transplantation 2009, 15:1458-1468.
30. Ishibashi H., Nakamura M., Komori A., Migita K., Shimoda S. Liver architecture, cell function, and disease. Seminars in Immunopathology 2009, 31:399-409.
31. Jia C. Advances in the regulation of liver regeneration. Expert Reviews in Gastroenterology and Hepatology 2011, 5:105-121.
32. Ju C., Reilly T.P., Bourdi M., Radonovich M.F., Brady J.N., George J.W., Pohl L.R. Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chemical Research in Toxicology 2002, 15:1504-1513.
33. Karlmark K.R., Zimmermann H.W., Roderburg C., Gassler N., Wasmuth H.E., Luedde T., Trautwein C., Tacke F. The fractalkine receptor CXC3R1 protects against liver fibrosis by controlling differentiation and survival of infiltrating hepatic monocytes. Hepatology 2010, 52:1769-1782.
34. Kosugi I., Muro H., Shirasawa H., Ito I. Endocytosis of soluble IgG immune complex and its transport to lysosomes in hepatic sinusoidal endothelial cells. Journal of Hepatology 1992, 16:106-114.
35. Lalor P.F., Lai W.K., Curbishley S.M., Shetty S., Adams D.H. Human hepatic sinusoidal endothelial cells can be distinguished by expression of phenotypic markers related to their specialised functions in vivo. World Journal of Gastroenterology 2006, 12:5429-5439.
36. Laskin D.L. Macrophages and inflammatory mediators in chemical toxicity: a battle of forces. Chemical Research in Toxicology 2009, 22:1376-1385.
37. Laskin D.L., Pilaro A.M., Ji S. Potential role of activated macrophages in acetaminophen hepatotoxicity. II. Mechanism of macrophage accumulation and activation. Toxicology and Applied Pharmacology 1986, 86:216-226.
38. Laskin D.L., Gardner C.R., Price V.F., Jollow D.J. Modulation of macrophage functioning abrogates the acute hepatotoxicity of acetaminophen. Hepatology 1995, 21:1045-1050.
39. Lohwasser C., Neureiter D., Popov Y., Bauer M., Schuppan D. Role of the receptor for advanced glycation end products in hepatic fibrosis. World Journal of Gastroenterology 2009, 15:5789-5798.
40. Løvdal T., Andersen E., Brech A., Berg T. Fc receptor mediated endocytosis of small soluble immunoglobulin G immune complexes in Kupffer cells and endothelial cells from rat liver. Journal of Cell Science 2000, 113:3255-3266.
41. Maher J.J. Cell-specific expression of hepatocyte growth factor in liver. Upregulation in sinusoidal endothelial cells after carbon tetrachloride. Journal of Clinical Investigation 1993, 91:2244-2252.
42. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Frontiers in Bioscience 2008, 13:453-461.
43. Martinez-Pomares L., Wienke D., Stillion R., McKenzie E.J., Arnold J.N., Harris J., McGreal E., Sim R.B., Isacke C.M., Gordon S. Carbohydrate-independent recognition of collagens by the macrophage mannose receptor. European Journal of Immunology 2006, 36:1074-1082.
44. Martin-Murphy B.V., Holt M.P., Ju C. The role of damage associated molecular pattern molecules in acetaminophen-induced liver injury in mice. Toxicology Letters 2010, 192:387-394.
45. McCloskey T.W., Todaro J.A., Laskin D.L. Lipopolysaccharide treatment of rats alters antigen expression and oxidative metabolism in hepatic macrophages and endothelial cells. Hepatology 1992, 16:191-203.
46. McCuskey R.S. The hepatic microvascular system in health and its response to toxicants. Anatomical Record (Hoboken) 2008, 291:661-671.
47. McCuskey R.S., Bethea N.W., Wong J., McCuskey M.K., Abril E.R., Wang X., Ito Y., DeLeve L.D. Ethanol binging exacerbates sinusoidal endothelial and parenchymal injury elicited by acetaminophen. Journal of Hepatology 2005, 42:371-377.
48. Michael S.L., Pumford N.R., Mayeux P.R., Niesman M.R., Hinson J.A. Pretreatment of mice with macrophage inactivators decreases acetaminophen hepatotoxicity and the formation of reactive oxygen and nitrogen species. Hepatology 1999, 30:186-195.
49. Murray P.J., Wynn T.A. Obstacles and opportunities for understanding macrophage polarization. Journal of Leukocyte Biology 2011, 89:557-563.
50. Neta R., Sayers T.J., Oppenheim J.J. Relationship of TNF to interleukins. Immunology Series 1992, 56:499-566.
51. Palmes D., Minin E., Budny T., Uhlmann D., Armann B., Stratmann U., Herbst H., Spiegel H.U. The endothelin/nitric oxide balance determines small-for-size liver injury after reduced-size rat liver transplantation. Virchows Archiv 2005, 447:731-741.
52. Porcheray F., Viaud S., Rimaniol A.C., Leone C., Samah B., Dereuddre-Bosquet N., Dormont D., Gras G. Macrophage activation switching: an asset for the resolution of inflammation. Clinical and Experimental Immunology 2005, 142:481-489.
53. Ramadori G., Moriconi F., Malik I., Dudas J. Physiology and pathophysiology of liver inflammation, damage and repair. Journal of Physiology and Pharmacology 2008, 59(Suppl. 1):107-117.
54. Ryan P.M., Bourdi M., Korrapati M.C., Proctor W.R., Vasquez R.A., Yee S.B., Quinn T.D., Chakraborty M., Pohl L.R. Endogenous interleukin-4 regulates glutathione synthesis following acetaminophen-induced liver injury in mice. Chemical Research in Toxicology 2012, 25:83-93.
55. Sano A., Taylor M.E., Leaning M.S., Summerfield J.A. Uptake and processing of glycoproteins by isolated rat hepatic endothelial and Kupffer cells. Journal of Hepatology 1990, 10:211-216.
56. Sell S. Heterogeneity and plasticity of hepatocyte lineage cells. Hepatology 2001, 33:738-750.
57. Sica A., Mantovani A. Macrophage plasticity and polarization: in vivo veritas. Journal of Clinical Investigation 2012, 122:787-795.
58. Tacke F., Luedde T., Trautwein C. Inflammatory pathways in liver homeostasis and liver injury. Clinical Reviews in Allergy & Immunology 2009, 36:4-12.
59. Thiele G.M., Duryee M.J., Freeman T.L., Sorrell M.F., Willis M.S., Tuma D.J., Klassen L.W. Rat sinusoidal liver endothelial cells (SECs) produce pro-fibrotic factors in response to adducts formed from the metabolites of ethanol. Biochemical Pharmacology 2005, 70:1593-1600.
60. Tygstrup N., Jensen S.A., Krog B., Dalhoff K. Expression of liver-specific functions in rat hepatocytes following sublethal and lethal acetaminophen poisoning. Journal of Hepatology 1996, 25:183-190.
61. Uhrig A., Banafsche R., Kremer M., Hegenbarth S., Hamann A., Neurath M., Gerken G., Limmer A., Knolle P.A. Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver. Journal of Leukocyte Biology 2005, 77:626-633.
62. Usui M., Kuriyama N., Kisawada M., Hamada T., Mizuno S., Sakurai H., Tabata M., Imai H., Okamoto K., Uemoto S., Isaji S. Tissue factor expression demonstrates severe sinusoidal endothelial cell damage during rejection after living-donor liver transplantation. Journal of Hepatobiliary and Pancreatic Surgery 2009, 16:513-520.
63. Wu R.Q., Xu Y.X., Song X.H., Chen L.J., Meng X.J. Adhesion molecule and proinflammatory cytokine gene expression in hepatic sinusoidal endothelial cells following cecal ligation and puncture. World Journal of Gastroenterology 2001, 7:128-130.
64. Xie G., Wang L., Wang X., DeLeve L.D. Isolation of periportal, midlobular, and centrilobular rat liver sinusoidal endothelial cells enables study of zonated drug toxicity. American Journal of Physiology - Gastrointestinal and Liver Physiology 2010, 299:G1204-G1210.
65. Xie G., Wang X., Wang L., Wang L., Atkinson R.D., Kanel G.C., Gaarde W.A., Deleve L.D. Role of differentiation of liver sinusoidal endothelial cells in progression and regression of hepatic fibrosis in rats. Gastroenterology 2012, 142:918-927.
66. Xu C.S., Chen X.G., Chang C.F., Wang G.P., Wang W.B., Zhang L.X., Zhu Q.S., Wang L. Analysis of time-course gene expression profiles of sinusoidal endothelial cells during liver regeneration in rats. Molecular and Cellular Biochemistry 2011, 350:215-227.
67. Yee S.B., Bourdi M., Masson M.J., Pohl L.R. Hepatoprotective role of endogenous interleukin-13 in a murine model of acetaminophen-induced liver disease. Chemical Research in Toxicology 2007, 20:734-744.