Liver Sinusoidal Endothelial Cell: An Update

Abstract

This update focuses on two main topics. First, recent developments in our understanding of liver sinusoidal endothelial cell (LSEC) function will be reviewed, specifically elimination of blood-borne waste, immunological function of LSECs, interaction of LSECs with liver metastases, LSECs and liver regeneration, and LSECs and hepatic fibrosis. Second, given the current emphasis on rigor and transparency in biomedical research, the update discusses the need for standardization of methods to demonstrate identity and purity of isolated LSECs, pitfalls in methods that might lead to a selection bias in the types of LSECs isolated, and questions about long-term culture of LSECs. Various surface markers used for immunomagnetic selection are reviewed.

Keywords

liver sinusoidal endothelial cell - endocytosis - liver regeneration - liver fibrosis - cell isolation approaches

• References

• 1 Elvevold K, Smedsrød B, Martinez I. The liver sinusoidal endothelial cell: a cell type of controversial and confusing identity. Am J Physiol Gastrointest Liver Physiol 2008; 294 (02) G391-G400
• 2 Poisson J, Lemoinne S, Boulanger C. , et al. Liver sinusoidal endothelial cells: physiology and role in liver diseases. J Hepatol 2017; 66 (01) 212-227
• 3 Sørensen KK, Simon-Santamaria J, McCuskey RS, Smedsrød B. Liver sinusoidal endothelial cells. Compr Physiol 2015; 5 (04) 1751-1774
• 4 Sørensen KK, McCourt P, Berg T. , et al. The scavenger endothelial cell: a new player in homeostasis and immunity. Am J Physiol Regul Integr Comp Physiol 2012; 303 (12) R1217-R1230
• 5 Breiner KM, Schaller H, Knolle PA. Endothelial cell-mediated uptake of a hepatitis B virus: a new concept of liver targeting of hepatotropic microorganisms. Hepatology 2001; 34 (4 Pt 1): 803-808
• 6 Ganesan LP, Mohanty S, Kim J, Clark KR, Robinson JM, Anderson CL. Rapid and efficient clearance of blood-borne virus by liver sinusoidal endothelium. PLoS Pathog 2011; 7 (09) e1002281
• 7 Mates JM, Yao Z, Cheplowitz AM. , et al. Mouse liver sinusoidal endothelium eliminates hiv-like particles from blood at a rate of 100 million per minute by a second-order kinetic process. Front Immunol 2017; 8: 35
• 8 Simon-Santamaria J, Rinaldo CH, Kardas P. , et al. Efficient uptake of blood-borne BK and JC polyomavirus-like particles in endothelial cells of liver sinusoids and renal vasa recta. PLoS One 2014; 9 (11) e111762
• 9 Wisse E. An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J Ultrastruct Res 1970; 31 (01) 125-150
• 10 Fraser R, Bosanquet AG, Day WA. Filtration of chylomicrons by the liver may influence cholesterol metabolism and atherosclerosis. Atherosclerosis 1978; 29 (02) 113-123
• 11 Cogger VC, Hilmer SN, Sullivan D, Muller M, Fraser R, Le Couteur DG. Hyperlipidemia and surfactants: the liver sieve is a link. Atherosclerosis 2006; 189 (02) 273-281
• 12 Herrnberger L, Hennig R, Kremer W. , et al. Formation of fenestrae in murine liver sinusoids depends on plasmalemma vesicle-associated protein and is required for lipoprotein passage. PLoS One 2014; 9 (12) e115005
• 13 LE Couteur DG, Cogger VC, McCuskey RS. , et al. Age-related changes in the liver sinusoidal endothelium: a mechanism for dyslipidemia. Ann N Y Acad Sci 2007; 1114: 79-87
• 14 Steinberg D, Witztum JL. Oxidized low-density lipoprotein and atherosclerosis. Arterioscler Thromb Vasc Biol 2010; 30 (12) 2311-2316
• 15 Li R, Oteiza A, Sørensen KK. , et al. Role of liver sinusoidal endothelial cells and stabilins in elimination of oxidized low-density lipoproteins. Am J Physiol Gastrointest Liver Physiol 2011; 300 (01) G71-G81
• 16 Hurtado-Roca Y, Bueno H, Fernandez-Ortiz A. , et al. Oxidized LDL is associated with metabolic syndrome traits independently of central obesity and insulin resistance. Diabetes 2017; 66 (02) 474-482
• 17 Houben T, Brandsma E, Walenbergh SM, Hofker MH, Shiri-Sverdlov R. Oxidized LDL at the crossroads of immunity in non-alcoholic steatohepatitis. Biochim Biophys Acta 2017; 1862 (04) 416-429
• 18 Krieger M. Charting the fate of the “good cholesterol”: identification and characterization of the high-density lipoprotein receptor SR-BI. Annu Rev Biochem 1999; 68: 523-558
• 19 Ganesan LP, Mates JM, Cheplowitz AM. , et al. Scavenger receptor B1, the HDL receptor, is expressed abundantly in liver sinusoidal endothelial cells. Sci Rep 2016; 6: 20646
• 20 van der Steeg WA, Holme I, Boekholdt SM. , et al. High-density lipoprotein cholesterol, high-density lipoprotein particle size, and apolipoprotein A-I: significance for cardiovascular risk: the IDEAL and EPIC-Norfolk studies. J Am Coll Cardiol 2008; 51 (06) 634-642
• 21 Bowe B, Xie Y, Xian H, Balasubramanian S, Zayed MA, Al-Aly Z. High density lipoprotein cholesterol and the risk of all-cause mortality among U.S. veterans. Clin J Am Soc Nephrol 2016; 11 (10) 1784-1793
• 22 März W, Kleber ME, Scharnagl H. , et al. HDL cholesterol: reappraisal of its clinical relevance. Clin Res Cardiol 2017; 106: 663-675
• 23 Park JK, Utsumi T, Seo YE. , et al. Cellular distribution of injected PLGA-nanoparticles in the liver. Nanomedicine (Lond) 2016; 12 (05) 1365-1374
• 24 Warren A, Cogger VC, Arias IM, McCuskey RS, Le Couteur DG. Liver sinusoidal endothelial fenestrations in caveolin-1 knockout mice. Microcirculation 2010; 17 (01) 32-38
• 25 Steffan AM, Gendrault JL, Kirn A. Increase in the number of fenestrae in mouse endothelial liver cells by altering the cytoskeleton with cytochalasin B. Hepatology 1987; 7 (06) 1230-1238
• 26 Wisse E, Jacobs F, Topal B, Frederik P, De Geest B. The size of endothelial fenestrae in human liver sinusoids: implications for hepatocyte-directed gene transfer. Gene Ther 2008; 15 (17) 1193-1199
• 27 Mathison JC, Ulevitch RJ. The clearance, tissue distribution, and cellular localization of intravenously injected lipopolysaccharide in rabbits. J Immunol 1979; 123 (05) 2133-2143
• 28 Yao Z, Mates JM, Cheplowitz AM. , et al. Blood-borne lipopolysaccharide is rapidly eliminated by liver sinusoidal endothelial cells via high-density lipoprotein. J Immunol 2016; 197 (06) 2390-2399
• 29 DeLeve LD, Wang X, Kanel GC, Atkinson RD, McCuskey RS. Prevention of hepatic fibrosis in a murine model of metabolic syndrome with nonalcoholic steatohepatitis. Am J Pathol 2008; 173 (04) 993-1001
• 30 Harte AL, da Silva NF, Creely SJ. , et al. Elevated endotoxin levels in non-alcoholic fatty liver disease. J Inflamm (Lond) 2010; 7 (01) 15
• 31 Michelena J, Altamirano J, Abraldes JG. , et al. Systemic inflammatory response and serum lipopolysaccharide levels predict multiple organ failure and death in alcoholic hepatitis. Hepatology 2015; 62 (03) 762-772
• 32 Bigatello LM, Broitman SA, Fattori L. , et al. Endotoxemia, encephalopathy, and mortality in cirrhotic patients. Am J Gastroenterol 1987; 82 (01) 11-15
• 33 Lin RS, Lee FY, Lee SD. , et al. Endotoxemia in patients with chronic liver diseases: relationship to severity of liver diseases, presence of esophageal varices, and hyperdynamic circulation. J Hepatol 1995; 22 (02) 165-172
• 34 Ganesan LP, Kim J, Wu Y. , et al. FcγRIIb on liver sinusoidal endothelium clears small immune complexes. J Immunol 2012; 189 (10) 4981-4988
• 35 Mousavi SA, Sporstøl M, Fladeby C, Kjeken R, Barois N, Berg T. Receptor-mediated endocytosis of immune complexes in rat liver sinusoidal endothelial cells is mediated by FcgammaRIIb2. Hepatology 2007; 46 (03) 871-884
• 36 Areschoug T, Gordon S. Scavenger receptors: role in innate immunity and microbial pathogenesis. Cell Microbiol 2009; 11 (08) 1160-1169
• 37 Gazi U, Martinez-Pomares L. Influence of the mannose receptor in host immune responses. Immunobiology 2009; 214 (07) 554-561
• 38 Martin-Armas M, Simon-Santamaria J, Pettersen I, Moens U, Smedsrød B, Sveinbjørnsson B. Toll-like receptor 9 (TLR9) is present in murine liver sinusoidal endothelial cells (LSECs) and mediates the effect of CpG-oligonucleotides. J Hepatol 2006; 44 (05) 939-946
• 39 Uhrig A, Banafsche R, Kremer M. , et al. Development and functional consequences of LPS tolerance in sinusoidal endothelial cells of the liver. J Leukoc Biol 2005; 77 (05) 626-633
• 40 Wu J, Meng Z, Jiang M. , et al. Toll-like receptor-induced innate immune responses in non-parenchymal liver cells are cell type-specific. Immunology 2010; 129 (03) 363-374
• 41 Boaru SG, Borkham-Kamphorst E, Tihaa L, Haas U, Weiskirchen R. Expression analysis of inflammasomes in experimental models of inflammatory and fibrotic liver disease. J Inflamm (Lond) 2012; 9 (01) 49
• 42 Schurich A, Berg M, Stabenow D. , et al. Dynamic regulation of CD8 T cell tolerance induction by liver sinusoidal endothelial cells. J Immunol 2010; 184 (08) 4107-4114
• 43 Rubinstein D, Roska AK, Lipsky PE. Liver sinusoidal lining cells express class II major histocompatibility antigens but are poor stimulators of fresh allogeneic T lymphocytes. J Immunol 1986; 137 (06) 1803-1810
• 44 Lohse AW, Knolle PA, Bilo K. , et al. Antigen-presenting function and B7 expression of murine sinusoidal endothelial cells and Kupffer cells. Gastroenterology 1996; 110 (04) 1175-1181
• 45 Limmer A, Ohl J, Kurts C. , et al. Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat Med 2000; 6 (12) 1348-1354
• 46 Lalor PF, Edwards S, McNab G, Salmi M, Jalkanen S, Adams DH. Vascular adhesion protein-1 mediates adhesion and transmigration of lymphocytes on human hepatic endothelial cells. J Immunol 2002; 169 (02) 983-992
• 47 Diehl L, Schurich A, Grochtmann R, Hegenbarth S, Chen L, Knolle PA. Tolerogenic maturation of liver sinusoidal endothelial cells promotes B7-homolog 1-dependent CD8+ T cell tolerance. Hepatology 2008; 47 (01) 296-305
• 48 Limmer A, Ohl J, Wingender G. , et al. Cross-presentation of oral antigens by liver sinusoidal endothelial cells leads to CD8 T cell tolerance. Eur J Immunol 2005; 35 (10) 2970-2981
• 49 Berg M, Wingender G, Djandji D. , et al. Cross-presentation of antigens from apoptotic tumor cells by liver sinusoidal endothelial cells leads to tumor-specific CD8+ T cell tolerance. Eur J Immunol 2006; 36 (11) 2960-2970
• 50 Böttcher JP, Schanz O, Garbers C. , et al. IL-6 trans-signaling-dependent rapid development of cytotoxic CD8+ T cell function. Cell Reports 2014; 8 (05) 1318-1327
• 51 Wittlich M, Dudek M, Böttcher JP. , et al. Liver sinusoidal endothelial cell cross-priming is supported by CD4 T cell-derived IL-2. J Hepatol 2017; 66 (05) 978-986
• 52 Knolle PA, Uhrig A, Hegenbarth S. , et al. IL-10 down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells through decreased antigen uptake via the mannose receptor and lowered surface expression of accessory molecules. Clin Exp Immunol 1998; 114 (03) 427-433
• 53 Knolle PA, Germann T, Treichel U. , et al. Endotoxin down-regulates T cell activation by antigen-presenting liver sinusoidal endothelial cells. J Immunol 1999; 162 (03) 1401-1407
• 54 Carambia A, Frenzel C, Bruns OT. , et al. Inhibition of inflammatory CD4 T cell activity by murine liver sinusoidal endothelial cells. J Hepatol 2013; 58 (01) 112-118
• 55 Xu X, Jin R, Li M. , et al. Liver sinusoidal endothelial cells induce tolerance of autoreactive CD4+ recent thymic emigrants. Sci Rep 2016; 6: 19861
• 56 Carambia A, Freund B, Schwinge D. , et al. TGF-β-dependent induction of CD4⁺CD25⁺Foxp3⁺ Tregs by liver sinusoidal endothelial cells. J Hepatol 2014; 61 (03) 594-599
• 57 Carambia A, Freund B, Schwinge D. , et al. Nanoparticle-based autoantigen delivery to Treg-inducing liver sinusoidal endothelial cells enables control of autoimmunity in mice. J Hepatol 2015; 62 (06) 1349-1356
• 58 Kruse N, Neumann K, Schrage A. , et al. Priming of CD4+ T cells by liver sinusoidal endothelial cells induces CD25low forkhead box protein 3- regulatory T cells suppressing autoimmune hepatitis. Hepatology 2009; 50 (06) 1904-1913
• 59 Patten DA, Wilson GK, Bailey D. , et al. Human liver sinusoidal endothelial cells promote intracellular crawling of lymphocytes during recruitment: A new step in migration. Hepatology 2017; 65 (01) 294-309
• 60 Kariya T, Ueta H, Xu XD. , et al. Direct evidence for activated CD8+ T cell transmigration across portal vein endothelial cells in liver graft rejection. J Gastroenterol 2016; 51 (10) 985-998
• 61 Mamdouh Z, Mikhailov A, Muller WA. Transcellular migration of leukocytes is mediated by the endothelial lateral border recycling compartment. J Exp Med 2009; 206 (12) 2795-2808
• 62 Oo YH, Weston CJ, Lalor PF. , et al. Distinct roles for CCR4 and CXCR3 in the recruitment and positioning of regulatory T cells in the inflamed human liver. J Immunol 2010; 184 (06) 2886-2898
• 63 Neumann K, Erben U, Kruse N. , et al. Chemokine Transfer by liver sinusoidal endothelial cells contributes to the recruitment of CD4+ T cells into the murine liver. PLoS One 2015; 10 (06) e0123867
• 64 Schrage A, Wechsung K, Neumann K. , et al. Enhanced T cell transmigration across the murine liver sinusoidal endothelium is mediated by transcytosis and surface presentation of chemokines. Hepatology 2008; 48 (04) 1262-1272
• 65 Oo YH, Banz V, Kavanagh D. , et al. CXCR3-dependent recruitment and CCR6-mediated positioning of Th-17 cells in the inflamed liver. J Hepatol 2012; 57 (05) 1044-1051
• 66 Yang H, Li N, Du Y. , et al. Neutrophil adhesion and crawling dynamics on liver sinusoidal endothelial cells under shear flow. Exp Cell Res 2017; 351 (01) 91-99
• 67 Aspinall AI, Curbishley SM, Lalor PF. , et al. CX(3)CR1 and vascular adhesion protein-1-dependent recruitment of CD16(+) monocytes across human liver sinusoidal endothelium. Hepatology 2010; 51 (06) 2030-2039
• 68 Onoe T, Ohdan H, Tokita D. , et al. Liver sinusoidal endothelial cells tolerize T cells across MHC barriers in mice. J Immunol 2005; 175 (01) 139-146
• 69 Liu WL, Tang L, Zhang G. , et al. Characterization of a novel C-type lectin-like gene, LSECtin - Demonstration of carbohydrate binding and expression in sinusoidal endothelial cells of liver and lymph node. J Biol Chem 2004; 279 (18) 18748-18758
• 70 Na H, Liu X, Li X. , et al. Novel roles of DC-SIGNR in colon cancer cell adhesion, migration, invasion, and liver metastasis. J Hematol Oncol 2017; 10 (01) 28
• 71 Zuo Y, Ren S, Wang M. , et al. Novel roles of liver sinusoidal endothelial cell lectin in colon carcinoma cell adhesion, migration and in-vivo metastasis to the liver. Gut 2013; 62 (08) 1169-1178
• 72 Maher JJ. Cell-specific expression of hepatocyte growth factor in liver.Upregulation in sinusoidal endothelial cells after carbon tetrachloride. J Clin Invest 1993; 91 (05) 2244-2252
• 73 Nanji AA, Tahan SR, Wei Y, Sadrzadeh SM. Hepatic sinusoidal endothelial cell G1/S arrest correlates with severity of alcoholic liver injury in the rat. Gastroenterology 1994; 107 (03) 818-823
• 74 Taniguchi E, Sakisaka S, Matsuo K, Tanikawa K, Sata M. Expression and role of vascular endothelial growth factor in liver regeneration after partial hepatectomy in rats. J Histochem Cytochem 2001; 49 (01) 121-130
• 75 LeCouter J, Moritz DR, Li B. , et al. Angiogenesis-independent endothelial protection of liver: role of VEGFR-1. Science 2003; 299 (5608): 890-893
• 76 Greene AK, Wiener S, Puder M. , et al. Endothelial-directed hepatic regeneration after partial hepatectomy. Ann Surg 2003; 237 (04) 530-535
• 77 Ding BS, Nolan DJ, Butler JM. , et al. Inductive angiocrine signals from sinusoidal endothelium are required for liver regeneration. Nature 2010; 468 (7321): 310-315
• 78 DeLeve LD, Wang X, Wang L. VEGF-sdf1 recruitment of CXCR7+ bone marrow progenitors of liver sinusoidal endothelial cells promotes rat liver regeneration. Am J Physiol Gastrointest Liver Physiol 2016; 310 (09) G739-G746
• 79 DeLeve LD. Liver sinusoidal endothelial cells and liver regeneration. J Clin Invest 2013; 123 (05) 1861-1866
• 80 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 (06) 1555-1563.e2
• 81 Wang L, Wang X, Xie G, Wang L, Hill CK, DeLeve LD. Liver sinusoidal endothelial cell progenitor cells promote liver regeneration in rats. J Clin Invest 2012; 122 (04) 1567-1573
• 82 Steffan AM, Gendrault JL, McCuskey RS, McCuskey PA, Kirn A. Phagocytosis, an unrecognized property of murine endothelial liver cells. Hepatology 1986; 6: 830-836
• 83 Harb R, Xie G, Lutzko C. , et al. Bone marrow progenitor cells repair rat hepatic sinusoidal endothelial cells after liver injury. Gastroenterology 2009; 137 (02) 704-712
• 84 Ding BS, Cao Z, Lis R. , et al. Divergent angiocrine signals from vascular niche balance liver regeneration and fibrosis. Nature 2014; 505 (7481): 97-102
• 85 Yu Y, Liang Y, Liu X. , et al. Id1 modulates endothelial progenitor cells function through relieving the E2-2-mediated repression of FGFR1 and VEGFR2 in vitro. Mol Cell Biochem 2016; 411 (1–2): 289-298
• 86 Yu Y, Liang Y, Yin C. , et al. Inhibitor of DNA-binding 1 promotes endothelial progenitor cell proliferation and migration by suppressing E2-2 through the helix-loop-helix domain. Int J Mol Med 2016; 38 (05) 1549-1557
• 87 Xia X, Yu Y, Zhang L, Ma Y, Wang H. Inhibitor of DNA binding 1 regulates cell cycle progression of endothelial progenitor cells through induction of Wnt2 expression. Mol Med Rep 2016; 14 (03) 2016-2024
• 88 Schaffner F, Poper H. Capillarization of hepatic sinusoids in man. Gastroenterology 1963; 44: 239-242
• 89 Horn T, Christoffersen P. Sinusoidal endothelial cells: a SEM investigation of the fenestration in normal and diseased human liver. In: Bioulac Sage P, Balabaud C. , eds. Sinusoids in Human Liver: Health and Disease. Rijswijk, The Netherlands: The Kupffer Cell Foundation; 1988
• 90 Horn T, Christoffersen P, Henriksen JH. Alcoholic liver injury: defenestration in noncirrhotic livers--a scanning electron microscopic study. Hepatology 1987; 7 (01) 77-82
• 91 Fraser R, Rogers GWT, Bowler LM, Day WA, Dobbs BR. Defenestration and vitamin A status in a rat model of cirrhosis. In: Wisse E, Knook DL, McCuskey RS. , eds. Cells of the hepatic sinusoid. Vol 3. Leiden: Kupffer Cell Foundation; 1991: 195-198
• 92 Deleve LD, Wang X, Guo Y. Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology 2008; 48 (03) 920-930
• 93 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 (04) 918-927.e6
• 94 DeLeve LD, Wang X, Hu L, McCuskey MK, McCuskey RS. Rat liver sinusoidal endothelial cell phenotype is maintained by paracrine and autocrine regulation. Am J Physiol Gastrointest Liver Physiol 2004; 287 (04) G757-G763
• 95 Rockey DC, Chung JJ. Reduced nitric oxide production by endothelial cells in cirrhotic rat liver: endothelial dysfunction in portal hypertension. Gastroenterology 1998; 114 (02) 344-351
• 96 Shah V, Toruner M, Haddad F. , et al. Impaired endothelial nitric oxide synthase activity associated with enhanced caveolin binding in experimental cirrhosis in the rat. Gastroenterology 1999; 117 (05) 1222-1228
• 97 Failli P, DeFRANCO RM, Caligiuri A. , et al. Nitrovasodilators inhibit platelet-derived growth factor-induced proliferation and migration of activated human hepatic stellate cells. Gastroenterology 2000; 119 (02) 479-492
• 98 Marrone G, Russo L, Rosado E. , et al. The transcription factor KLF2 mediates hepatic endothelial protection and paracrine endothelial-stellate cell deactivation induced by statins. J Hepatol 2013; 58 (01) 98-103
• 99 Marrone G, Maeso-Díaz R, García-Cardena G. , et al. KLF2 exerts antifibrotic and vasoprotective effects in cirrhotic rat livers: behind the molecular mechanisms of statins. Gut 2015; 64 (09) 1434-1443
• 100 Jarnagin WR, Rockey DC, Koteliansky VE, Wang SS, Bissell DM. Expression of variant fibronectins in wound healing: cellular source and biological activity of the EIIIA segment in rat hepatic fibrogenesis. J Cell Biol 1994; 127 (6 Pt 2): 2037-2048
• 101 Olsen AL, Sackey BK, Marcinkiewicz C, Boettiger D, Wells RG. Fibronectin extra domain-A promotes hepatic stellate cell motility but not differentiation into myofibroblasts. Gastroenterology 2012; 142 (04) 928-937.e3
• 102 Koyama Y, Wang P, Liang S. , et al. Mesothelin/mucin 16 signaling in activated portal fibroblasts regulates cholestatic liver fibrosis. J Clin Invest 2017; 127 (04) 1254-1270
• 103 Lua I, Li Y, Zagory JA. , et al. Characterization of hepatic stellate cells, portal fibroblasts, and mesothelial cells in normal and fibrotic livers. J Hepatol 2016; 64 (05) 1137-1146
• 104 Mederacke I, Hsu CC, Troeger JS. , et al. Fate tracing reveals hepatic stellate cells as dominant contributors to liver fibrosis independent of its aetiology. Nat Commun 2013; 4: 2823
• 105 Cogger VC, Arias IM, Warren A. , et al. The response of fenestrations, actin, and caveolin-1 to vascular endothelial growth factor in SK Hep1 cells. Am J Physiol Gastrointest Liver Physiol 2008; 295 (01) G137-G145
• 106 Voyta JC, Via DP, Butterfield CE, Zetter BR. Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. J Cell Biol 1984; 99 (06) 2034-2040
• 107 Van Berkel TJ, De Rijke YB, Kruijt JK. Different fate in vivo of oxidatively modified low density lipoprotein and acetylated low density lipoprotein in rats. Recognition by various scavenger receptors on Kupffer and endothelial liver cells. J Biol Chem 1991; 266 (04) 2282-2289
• 108 Kamps JA, Kruijt JK, Kuiper J, van Berkel TJ. Characterization of the interaction of acetylated LDL and oxidatively modified LDL with human liver parenchymal and Kupffer cells in culture. Arterioscler Thromb 1992; 12 (09) 1079-1087
• 109 Katz SC, Pillarisetty VG, Bleier JI, Shah AB, DeMatteo RP. Liver sinusoidal endothelial cells are insufficient to activate T cells. J Immunol 2004; 173 (01) 230-235
• 110 De Sanctis JB, Blanca I, Bianco NE. Expression of different lipoprotein receptors in natural killer cells and their effect on natural killer proliferative and cytotoxic activity. Immunology 1995; 86 (03) 399-407
• 111 Meyer J, Gonelle-Gispert C, Morel P, Bühler L. Methods for isolation and purification of murine liver sinusoidal endothelial cells: a systematic review. PLoS One 2016; 11 (03) e0151945
• 112 Xie G, Wang L, Wang X, Wang L, DeLeve LD. Isolation of periportal, midlobular, and centrilobular rat liver sinusoidal endothelial cells enables study of zonated drug toxicity. Am J Physiol Gastrointest Liver Physiol 2010; 299 (05) G1204-G1210
• 113 Barberá-Guillem E, Rocha M, Alvarez A, Vidal-Vanaclocha F. Differences in the lectin-binding patterns of the periportal and perivenous endothelial domains in the liver sinusoids. Hepatology 1991; 14 (01) 131-139
• 114 Strauss O, Phillips A, Ruggiero K, Bartlett A, Dunbar PR. Immunofluorescence identifies distinct subsets of endothelial cells in the human liver. Sci Rep 2017; 7: 44356
• 115 Asumendi A, Alvarez A, Martinez I, Smedsrød B, Vidal-Vanaclocha F. Hepatic sinusoidal endothelium heterogeneity with respect to mannose receptor activity is interleukin-1 dependent. Hepatology 1996; 23 (06) 1521-1529
• 116 Rocha M, Lentini A, Asumendi A. , et al. In situ and in vitro correlation between mannose receptor expression and fenestration pattern in endothelial cells selected from different zones of liver lobule. In: Macrophage Mannose Receptor: Leiden, The Netherlands: The Kupffer Cell Foundation; 1993
• 117 Scoazec JY, Racine L, Couvelard A, Flejou JF, Feldmann G. Endothelial cell heterogeneity in the normal human liver acinus: in situ immunohistochemical demonstration. Liver 1994; 14 (03) 113-123
• 118 Vidal-Vanaclocha F, Barbera-Guillem E. Fenestration patterns in endothelial cells of rat liver sinusoids. J Ultrastruct Res 1985; 90: 115-123
• 119 Wisse E, De Zanger RB, Charels K, Van Der Smissen P, McCuskey RS. The liver sieve: considerations concerning the structure and function of endothelial fenestrae, the sinusoidal wall and the space of Disse. Hepatology 1985; 5 (04) 683-692
• 120 Wack KE, Ross MA, Zegarra V, Sysko LR, Watkins SC, Stolz DB. Sinusoidal ultrastructure evaluated during the revascularization of regenerating rat liver. Hepatology 2001; 33 (02) 363-378
• 121 DeLeve LD, Wang X, McCuskey MK, McCuskey RS. Rat liver endothelial cells isolated by anti-CD31 immunomagnetic separation lack fenestrae and sieve plates. Am J Physiol Gastrointest Liver Physiol 2006; 291 (06) G1187-G1189
• 122 Protocol for the preparation of mouse liver Kupffer cells and liver sinusoidal endothelial cells. Available at: http://hdl.handle.net/10037/4575 . Accessed November 20, 2017
• 123 Smedsrød B, Pertoft H. Preparation of pure hepatocytes and reticuloendothelial cells in high yield from a single rat liver by means of Percoll centrifugation and selective adherence. J Leukoc Biol 1985; 38 (02) 213-230
• 124 Pertoft H, Smedsrod B. Separation and characterization of liver cells. In: Pretlow II TG, Pretlow TP. , eds. Cell Separation: Methods and Selected Applications. Cambridge, MA: Academic Press; 1987: 1-24
• 125 Huebert RC, Jagavelu K, Liebl AF. , et al. Immortalized liver endothelial cells: a cell culture model for studies of motility and angiogenesis. Lab Invest 2010; 90 (12) 1770-1781
• 126 Vonnahme FJ. The Human Liver- A Scanning Electron Microscopic Atlas. Basel: Karger; 1993
• 127 Bardin N, Francès V, Lesaule G, Horschowski N, George F, Sampol J. Identification of the S-Endo 1 endothelial-associated antigen. Biochem Biophys Res Commun 1996; 218 (01) 210-216
• 128 Schrage A, Loddenkemper C, Erben U. , et al. Murine CD146 is widely expressed on endothelial cells and is recognized by the monoclonal antibody ME-9F1. Histochem Cell Biol 2008; 129 (04) 441-451
• 129 Despoix N, Walzer T, Jouve N. , et al. Mouse CD146/MCAM is a marker of natural killer cell maturation. Eur J Immunol 2008; 38 (10) 2855-2864
• 130 March S, Hui EE, Underhill GH, Khetani S, Bhatia SN. Microenvironmental regulation of the sinusoidal endothelial cell phenotype in vitro. Hepatology 2009; 50 (03) 920-928
• 131 Su K, Yang H, Li X. , et al. Expression profile of FcgammaRIIb on leukocytes and its dysregulation in systemic lupus erythematosus. J Immunol 2007; 178 (05) 3272-3280
• 132 Minhajat R, Mori D, Yamasaki F, Sugita Y, Satoh T, Tokunaga O. Organ-specific endoglin (CD105) expression in the angiogenesis of human cancers. Pathol Int 2006; 56 (12) 717-723
• 133 Theuerkauf I, Zhou H, Fischer HP. Immunohistochemical patterns of human liver sinusoids under different conditions of pathologic perfusion. Virchows Arch 2001; 438 (05) 498-504
• 134 Lalor PF, Lai WK, Curbishley SM, Shetty S, Adams DH. Human hepatic sinusoidal endothelial cells can be distinguished by expression of phenotypic markers related to their specialised functions in vivo. World J Gastroenterol 2006; 12 (34) 5429-5439
• 135 Klein D, Demory A, Peyre F. , et al. Wnt2 acts as a cell type-specific, autocrine growth factor in rat hepatic sinusoidal endothelial cells cross-stimulating the VEGF pathway. Hepatology 2008; 47 (03) 1018-1031
• 136 Krause P, Markus PM, Schwartz P. , et al. Hepatocyte-supported serum-free culture of rat liver sinusoidal endothelial cells. J Hepatol 2000; 32 (05) 718-726