Hepatic sinusoidal cells in health and disease: Update from the 14th International Symposium

Liver International

Volumn 29, Issue 4, 2009, Pages 490-501

  Smedsrød, Bård ^a   Le Couteur, David ^b   Ikejima, Kenichi ^c   Jaeschke, Hartmut ^d   Kawada, Norifumi ^e   Naito, Makoto ^f   Knolle, Percy ^g   Nagy, Laura ^h   Senoo, Haruki ⁱ   Vidal Vanaclocha, Fernando ^j   Yamaguchi, Noriko ⁱ  

^a UNIVERSITY OF TROMSØ   (Norway)

^b Department of Microbiology and Infectious Diseases   (Australia)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^e OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^f NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^g UNIVERSITY OF BONN   (Germany)

^h CASE WESTERN RESERVE UNIVERSITY   (United States)

ⁱ AKITA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^j UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

more..

Author keywords

Hepatic stellate cell; Kupffer cell; Liver; Liver sinusoidal endothelial cell; Sinusoid

Indexed keywords

ADIPONECTIN; CYCLIC AMP; FC RECEPTOR IIB; FERRITIN; IRON; MANNOSE RECEPTOR; PARACETAMOL; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RETINOL; SCAVENGER RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN;

AGING; ALCOHOLIC FATTY LIVER; ANTIGEN PRESENTATION; CD8+ T LYMPHOCYTE; CHRONIC LIVER DISEASE; DRUG OVERDOSE; ENDOCYTOSIS; ENDOTHELIUM CELL; HUMAN; IMMUNOREGULATION; INFLAMMATION; KUPFFER CELL; LIVER CIRRHOSIS; LIVER DEVELOPMENT; LIVER FIBROSIS; LIVER METASTASIS; LIVER NECROSIS; LIVER REGENERATION; LIVER SINUSOID; LIVER TOXICITY; MACROPHAGE; MICROCIRCULATION; NATURAL KILLER CELL; NEUTROPHIL CHEMOTAXIS; NONALCOHOLIC FATTY LIVER; NONHUMAN; OXIDATIVE STRESS; OXYGEN TENSION; PRIMARY SCLEROSING CHOLANGITIS; REVIEW; STELLATE CELL; TUMOR VASCULARIZATION;

CONGRESSES AS TOPIC; HUMANS; KUPFFER CELLS; LIVER; LIVER DISEASES; LIVER NEOPLASMS; NORWAY;

EID: 62749148283     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/j.1478-3231.2009.01979.x     Document Type: Review

References (130)

1. Martinez I, Nedredal GI, Oie CI, et al. The influence of oxygen tension on the structure and function of isolated liver sinusoidal endothelial cells. Comp Hepatol 2008; 7: 4.
2. 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 2006; 291: G1187-9.
3. 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 2004; 287: G757-63.
4. 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: G137-45.
5. Yokomori H, Yoshimura K, Funakoshi S, et al. Rho modulates hepatic sinusoidal endothelial fenestrae via regulation of the actin cytoskeleton in rat endothelial cells. Lab Invest 2004; 84: 857-64.
6. Carpenter B, Lin Y, Stoll S, et al. VEGF is crucial for the hepatic vascular development required for lipoprotein uptake. Development 2005; 132: 3293-303.
7. Le Couteur DG, Fraser R, Hilmer S, Rivory LP, McLean AJ. The hepatic sinusoid in aging and cirrhosis - effects on hepatic substrate disposition and drug clearance. Clin Pharmacokinet 2005; 44: 187-200.
8. Hilmer SN, Cogger VC, Fraser R, et al. Age-related changes in the hepatic sinusoidal endothelium impede lipoprotein transfer in the rat. Hepatology 2005; 42: 1349-54.
9. Warren A, Le Couteur DG, Fraser R, et al. T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology 2006; 44: 1182-90.
10. 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: 1193-9.
11. Smedsrod B, Pertoft H, Gustafson S, Laurent TC. Scavenger functions of the liver endothelial cell. Biochem J 1990; 266: 313-27.
12. Malovic I, Sorensen KK, Elvevold KH, et al. The mannose receptor on murine liver sinusoidal endothelial cells is the main denatured collagen clearance receptor. Hepatology 2007; 45: 1454-61.
13. Elvevold K, Simon-Santamaria J, Hasvold H, et al. Liver sinusoidal endothelial cells depend on mannose receptor-mediated recruitment of lysosomal enzymes for normal degradation capacity. Hepatology 2008; 48: 2007-15.
14. 2 -terminal propeptides of types I and III procollagen is a physiological function of the scavenger receptor in liver endothelial cells. J Exp Med 1994; 179: 405-12.
15. Smedsrod B, Melkko J, Araki N, Sano H, Horiuchi S. Advanced glycation end products are eliminated by scavenger-receptor-mediated endocytosis in hepatic sinusoidal Kupffer and endothelial cells. Biochem J 1997; 322(Part 2): 567-73.
16. McCourt PA, Smedsrod BH, Melkko J, Johansson S. Characterization of a hyaluronan receptor on rat sinusoidal liver endothelial cells and its functional relationship to scavenger receptors. Hepatology 1999; 30: 1276-86.
17. Hansen B, Arteta B, Smedsrod B. The physiological scavenger receptor function of hepatic sinusoidal endothelial and Kupffer cells is independent of scavenger receptor class A type I and II. Mol Cell Biochem 2002; 240: 1-8.
18. Hansen B, Longati P, Elvevold K, et al. Stabilin-1 and stabilin-2 are both directed into the early endocytic pathway in hepatic sinusoidal endothelium via interactions with clathrin/AP-2, independent of ligand binding. Exp Cell Res 2005; 303: 160-73.
19. Mousavi SA, Sporstol M, Fladeby C, et al. Receptor-mediated endocytosis of immune complexes in rat liver sinusoidal endothelial cells is mediated by Fc gammaRIIb2. Hepatology 2007; 46: 871-84.
20. Takizawa T, Anderson CL, Robinson JM. A novel Fc gamma R-defined, IgG-containing organelle in placental endothelium. J Immunol 2005; 175: 2331-9.
21. Seternes T, Sorensen K, Smedsrod B. Scavenger endothelial cells of vertebrates: A nonperipheral leukocyte system for high-capacity elimination of waste macromolecules. Proc Natl Acad Sci USA 2002; 99: 7594-7.
22. Martin-Armas M, Zykova S, Smedsrod B. Effects of CpG-oligonucleotides, poly I:C and LPS on Atlantic cod scavenger endothelial cells (SEC). Dev Comp Immunol 2008; 32: 100-7.
23. Crossley AC. The ultrastructure and function of pericardial cells and other nephrocytes in an insect: Calliphora erythrocephala. Tissue Cell 1972; 4: 529-60.
24. Yoshida M, Nishikawa Y, Omori Y, et al. Involvement of signaling of VEGF and TGF-beta in differentiation of sinusoidal endothelial cells during culture of fetal rat liver cells. Cell Tissue Res 2007; 329: 273-82.
25. Keitel V, Reinehr R, Gatsios P, et al. The G-protein coupled bile salt receptor TGR5 is expressed in liver sinusoidal endothelial cells. Hepatology 2007; 45: 695-704.
26. Watanabe N, Takashimizu S, Nishizaki Y, et al. An endothelin A receptor antagonist induces dilatation of sinusoidal endothelial fenestrae: implications for endothelin-1 in hepatic microcirculation. J Gastroenterol 2007; 42: 775-82.
27. Yokomori H, Yoshimura K, Ohshima S, et al. The endothelin-1 receptor-mediated pathway is not involved in the endothelin-1-induced defenestration of liver sinusoidal endothelial cells. Liver Int 2006; 26: 1268-76.
28. Deleve LD, Wang X, Guo Y. Sinusoidal endothelial cells prevent rat stellate cell activation and promote reversion to quiescence. Hepatology 2008; 48: 920-30.
29. Qiao JG, Wu L, Lei DX, Wang L. Insulin promotes sinusoidal endothelial cell proliferation mediated by upregulation of vascular endothelial growth factor in regenerating rat liver after partial hepatectomy. World J Gastroenterol 2005; 11: 5978-83.
30. Falkowska-Hansen B, Falkowski M, Metharom P, Krunic D, Goerdt S. Clathrin-coated vesicles form a unique net-like structure in liver sinusoidal endothelial cells by assembling along undisrupted microtubules. Exp Cell Res 2007; 313: 1745-57.
31. 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: 1018-31.
32. Le Couteur DG, Warren A, Cogger VC, et al. Old age and the hepatic sinusoid. Anat Rec 2008; 291: 672-83.
33. Ito Y, Sorensen KK, Bethea NW, et al. Age-related changes in the hepatic microcirculation of mice. Exp Gerontol 2007; 48: 789-97.
34. Collardeau-Frachon S, Scoazec J. Vascular development and differentiation during human liver organogenesis. Anat Rec 2008; 291: 614-27.
35. McCuskey RS. The hepatic microvascular system in health and its response to toxicants. Anat Rec 2008; 291: 661-71.
36. Deleve LD. Hepatic microvasculature in liver injury. Semin Liver Dis 2007; 27: 390-400.
37. Cogger VC, Muller M, Fraser R, et al. The effects of oxidative stress on the liver sieve. J Hepatol 2004; 41: 370-76.
38. McCuskey RS, Ito Y, Robertson GR, et al. Hepatic microvascular dysfunction during evolution of dietary steatohepatitis in mice. Hepatology 2004; 40: 386-93.
39. Ohmura T, Enomoto K, Satoh H, Sawada N, Mori M. Establishment of a novel monoclonal antibody, SE-1, which specifically reacts with rat hepatic sinusoidal endothelial cells. J Histochem Cytochem 1993; 41: 1253-7.
40. Tokairin T, Nishikawa Y, Doi Y, et al. A highly specific isolation of rat sinusoidal endothelial cells by the immunomagnetic bead method using SE-1 monoclonal antibody. J Hepatol 2002; 36: 725-33.
41. Rivera CA. Risk factors and mechanisms of non-alcoholic steatohepatitis. Pathophysiology 2008; 15: 109-14.
42. Thurman II RG. Alcoholic liver injury involves activation of Kupffer cells by endotoxin. Am J Physiol 1998; 275: G605-11.
43. Nagy LE. Recent insights into the role of the innate immune system in the development of alcoholic liver disease. Exp Biol Med (Maywood) 2003; 228: 882-90.
44. Hritz I, Mandrekar P, Velayudham A, et al. The critical role of toll-like receptor (TLR) 4 in alcoholic liver disease is independent of the common TLR adapter MyD88. Hepatology 2008; 48: 1224-31.
45. Zhao XJ, Dong Q, Bindas J, et al. TRIF and IRF-3 binding to the TNF promoter results in macrophage TNF dysregulation and steatosis induced by chronic ethanol. J Immunol 2008; 181: 3049-56.
46. Huang H, Park PH, McMullen MR, Nagy LE. Mechanisms for the anti-inflammatory effects of adiponectin in macrophages. J Gastroenterol Hepatol 2008; 23(Suppl. 1): S50-3.
47. dela Pena A, Leclercq IA, Williams J, Farrell GC. NADPH oxidase is not an essential mediator of oxidative stress or liver injury in murine MCD diet-induced steatohepatitis. J Hepatol 2007; 46: 304-13.
48. Risoe PK, Wang Y, Stuestol JF, et al. Lipopolysaccharide attenuates mRNA levels of several adenylyl cyclase isoforms in vivo. Biochim Biophys Acta 2007; 1772: 32-9.
49. Gobejishvili L, Barve S, Joshi-Barve S, McClain C. Enhanced PDE4B expression augments LPS-inducible TNF expression in ethanol-primed monocytes: Relevance to alcoholic liver disease. Am J Physiol Gastrointest Liver Physiol 2008; 295: G718-24.
50. Leclercq IA, Da Silva Morais A, Schroyen B, Van Hul N, Geerts A. Insulin resistance in hepatocytes and sinusoidal liver cells: Mechanisms and consequences. J Hepatol 2007; 47: 142-56.
51. Jeong WI, Osei-Hyiaman D, Park O, et al. Paracrine activation of hepatic CB1 receptors by stellate cell-derived endocannabinoids mediates alcoholic fatty liver. Cell Metab 2008; 7: 227-35.
52. Osei-Hyiaman D, DePetrillo M, Pacher P, et al. Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Invest 2005; 115: 1298-305.
53. Lopez-Parra M, Titos E, Horrillo R, et al. Regulatory effects of arachidonate 5-lipoxygenase on hepatic microsomal TG transfer protein activity and VLDL-triglyceride and apoB secretion in obese mice. J Lipid Res 2008; 49: 2513-23.
54. Jaeschke H, Bajt ML. Intracellular signaling mechanisms of acetaminophen-induced liver cell death. Toxicol Sci 2006; 89: 31-41.
55. Jaeschke H. Role of inflammation in the mechanism of acetaminophen-induced hepatotoxicity. Expert Opin Drug Metab Toxicol 2005; 1: 389-97.
56. James LP, McCullough SS, Knight TR, Jaeschke H, Hinson JA. Acetaminophen toxicity in mice lacking NADPH oxidase activity: Role of peroxynitrite formation and mitochondrial oxidant stress. Free Radic Res 2003; 37: 1289-97.
57. Ju C, Reilly TP, Bourdi M, et al. Protective role of Kupffer cells in acetaminophen-induced hepatic injury in mice. Chem Res Toxicol 2002; 15: 1504-13.
58. Liu ZX, Govindarajan S, Kaplowitz N. Innate immune system plays a critical role in determining the progression and severity of acetaminophen hepatotoxicity. Gastroenterology 2004; 127: 1760-74.
59. Masson MJ, Carpenter LD, Graf ML, Pohl LR. Pathogenic role of natural killer T and natural killer cells in acetaminophen-induced liver injury in mice is dependent on the presence of dimethyl sulfoxide. Hepatology 2008; 48: 889-97.
60. Lawson JA, Farhood A, Hopper RD, Bajt ML, Jaeschke H. The hepatic inflammatory response after acetaminophen overdose: Role of neutrophils. Toxicol Sci 2000; 54: 509-16.
61. Cover C, Liu J, Farhood A, et al. Pathophysiological role of the acute inflammatory response during acetaminophen hepatotoxicity. Toxicol Appl Pharmacol 2006; 216: 98-107.
62. Liu ZX, Han D, Gunawan B, Kaplowitz N. Neutrophil depletion protects against murine acetaminophen hepatotoxicity. Hepatology 2006; 43: 1220-30.
63. Jaeschke H, Liu J. Neutrophil depletion protects against murine acetaminophen hepatotoxicity: Another perspective. Hepatology 2007; 45: 1588-9; author reply 89.
64. Bajt ML, Yan HM, Farhood A, Jaeschke H. Plasminogen activator inhibitor-1 limits liver injury and facilitates regeneration after acetaminophen overdose. Toxicol Sci 2008; 104: 419-27.
65. Holt MP, Cheng L, Ju C. Identification and characterization of infiltrating macrophages in acetaminophen-induced liver injury. J Leukoc Biol 2008; 84: 1410-21.
66. Senoo H, Kojima N, Sato M. Vitamin A-storing cells (stellate cells). Vitam Horm 2007; 75: 131-59.
67. Straub BK, Stoeffel P, Heid H, Zimbelmann R, Schirmacher P. Differential pattern of lipid droplet-associated proteins and de novo perilipin expression in hepatocyte steatogenesis. Hepatology 2008; 47: 1936-46.
68. Nagatsuma K, Hayashi Y, Hano H, et al. Lecithin: Retinol acyltransferase protein is distributed in both hepatic stellate cells and endothelial cells of normal rodent and human liver. Liver Int 2009; 29: 47-54.
69. Mezaki Y, Yoshikawa K, Yamaguchi N, et al. Rat hepatic stellate cells acquire retinoid responsiveness after activation in vitro by post-transcriptional regulation of retinoic acid receptor alpha gene expression. Arch Biochem Biophys 2007; 465: 370-9.
70. Yoshikawa K, Imai K, Seki T, et al. Distribution of retinylester-storing stellate cells in the arrowtooth halibut, Atheresthes evermanni. Comp Biochem Physiol A Mol Integr Physiol 2006; 145: 280-6.
71. Wold HL, Wake K, Higashi N, et al. Vitamin A distribution and content in tissues of the lamprey, Lampetra japonica. Anat Rec 2004; 276: 134-42.
72. Irie T, Kajiwara S, Kojima N, Senoo H, Seki T. Retinal is the essential form of retinoid for storage and transport in the adult of the ascidian Halocynthia roretzi. Comp Biochem Physiol B Biochem Mol Biol 2004; 139: 597-606.
73. Bonis PA, Friedman SL, Kaplan MM. Is liver fibrosis reversible? N Engl J Med 2001; 344: 452-4.
74. Desmet VJ, Roskams T. Cirrhosis reversal: A duel between dogma and myth. J Hepatol 2004; 40: 860-7.
75. Rockey DC, Maher JJ, Jarnagin WR, Gabbiani G, Friedman SL. Inhibition of rat hepatic lipocyte activation in culture by interferon-gamma. Hepatology 1992; 16: 776-84.
76. Maubach G, Lim MC, Kumar S, Zhuo L. Expression and upregulation of cathepsin S and other early molecules required for antigen presentation in activated hepatic stellate cells upon IFN-gamma treatment. Biochim Biophys Acta 2007; 1773: 219-31.
77. Yavrom S, Chen L, Xiong S, et al. Peroxisome proliferator-activated receptor gamma suppresses proximal alpha1(I) collagen promoter via inhibition of p300-facilitated NF-I binding to DNA in hepatic stellate cells. J Biol Chem 2005; 280: 40650-9.
78. Cheng JH, She H, Han YP, et al. Wnt antagonism inhibits hepatic stellate cell activation and liver fibrosis. Am J Physiol Gastrointest Liver Physiol 2008; 294: G39-49.
79. Klein I, Cornejo JC, Polakos NK, et al. Kupffer cell heterogeneity: functional properties of bone marrow derived and sessile hepatic macrophages. Blood 2007; 110: 4077-85.
80. Azzi A, Gysin R, Kempna P, et al. Regulation of gene expression by alpha-tocopherol. Biol Chem 2004; 385: 585-91.
81. Kinoshita K, Iimuro Y, Otogawa K, et al. Adenovirus-mediated expression of BMP-7 suppresses the development of liver fibrosis in rats. Gut 2007; 56: 706-14.
82. Friedman SL. Seminars in medicine of the Beth Israel Hospital, Boston. The cellular basis of hepatic fibrosis. Mechanisms and treatment strategies. N Engl J Med 1993; 328: 1828-35.
83. Gressner AM, Bachem MG. Molecular mechanisms of liver fibrogenesis - a homage to the role of activated fat-storing cells. Digestion 1995; 56: 335-46.
84. Olaso E, Friedman SL. Molecular regulation of hepatic fibrogenesis. J Hepatol 1998; 29: 836-47.
85. Kawada N. The hepatic perisinusoidal stellate cell. Histol Histopathol 1997; 12: 1069-80.
86. Okuyama H, Shimahara Y, Kawada N. The hepatic stellate cell in the post-genomic era. Histol Histopathol 2002; 17: 487-95.
87. Kim Y, Ratziu V, Choi SG, et al. Transcriptional activation of transforming growth factor beta1 and its receptors by the Kruppel-like factor Zf9/core promoter-binding protein and Sp1. Potential mechanisms for autocrine fibrogenesis in response to injury. J Biol Chem 1998; 273: 33750-8.
88. Dey A, Cederbaum AI. Alcohol and oxidative liver injury. Hepatology 2006; 43: S63-74.
89. Ramm GA, Ruddell RG. Hepatotoxicity of iron overload: Mechanisms of iron-induced hepatic fibrogenesis. Semin Liver Dis 2005; 25: 433-49.
90. Kato J, Kobune M, Nakamura T, et al. Normalization of elevated hepatic 8-hydroxy-2′-deoxyguanosine levels in chronic hepatitis C patients by phlebotomy and low iron diet. Cancer Res 2001; 61: 8697-702.
91. Kawada N, Kristensen DB, Asahina K, et al. Characterization of a stellate cell activation-associated protein (STAP) with peroxidase activity found in rat hepatic stellate cells. J Biol Chem 2001; 276: 25318-23.
92. Nakatani K, Okuyama H, Shimahara Y, et al. Cytoglobin/STAP, its unique localization in splanchnic fibroblast-like cells and function in organ fibrogenesis. Lab Invest 2004; 84: 91-101.
93. Xu R, Harrison PM, Chen M, et al. Cytoglobin overexpression protects against damage-induced fibrosis. Mol Ther 2006; 13: 1093-100.
94. Ogawa T, Tateno C, Asahina K, et al. Identification of vitamin A-free cells in a stellate cell-enriched fraction of normal rat liver as myofibroblasts. Histochem Cell Biol 2007; 127: 161-74.
95. Magness ST, Bataller R, Yang L, Brenner DA. A dual reporter gene transgenic mouse demonstrates heterogeneity in hepatic fibrogenic cell populations. Hepatology 2004; 40: 1151-9.
96. Knolle PA, Gerken G. Local control of the immune response in the liver. Immunol Rev 2000; 174: 21-34.
97. Crispe IN. Hepatic T cells and liver tolerance. Nat Rev Immunol 2003; 3: 51-62.
98. Polakos NK, Cornejo JC, Murray DA, et al. Kupffer cell-dependent hepatitis occurs during influenza infection. Am J Pathol 2006; 168: 1169-78; quiz 404-5.
99. Tu Z, Bozorgzadeh A, Pierce RH, et al. TLR-dependent cross talk between human Kupffer cells and NK cells. J Exp Med 2008; 205: 233-44.
100. Dunn C, Brunetto M, Reynolds G, et al. Cytokines induced during chronic hepatitis B virus infection promote a pathway for NK cell-mediated liver damage. J Exp Med 2007; 204: 667-80.
101. + NKT cells patrolling liver sinusoids. PLoS Biol 2005; 3: E113.
102. + gut-homing lymphocytes to the liver in primary sclerosing cholangitis. J Exp Med 2004; 200: 1511-7.
103. Adams DH, Eksteen B. Aberrant homing of mucosal T cells and extra-intestinal manifestations of inflammatory bowel disease. Nat Rev Immunol 2006; 6: 244-51.
104. Curbishley SM, Eksteen B, Gladue RP, Lalor P, Adams DH. CXCR 3 activation promotes lymphocyte transendothelial migration across human hepatic endothelium under fluid flow. Am J Pathol 2005; 167: 887-99.
105. 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: 1262-72.
106. + T lymphocytes but fail to promote survival. Eur J Immunol 1998; 28: 221-36.
107. Bowen DG, Zen M, Holz L, et al. The site of primary T cell activation is a determinant of the balance between intrahepatic tolerance and immunity. J Clin Invest 2004; 114: 701-12.
108. Callery MP, Kamei T, Flye MW. Kupffer cell blockade inhibits induction of tolerance by the portal venous route. Transplantation 1989; 47: 1092-4.
109. Winau F, Hegasy G, Weiskirchen R, et al. Ito cells are liver-resident antigen-presenting cells for activating T cell responses. Immunity 2007; 26: 117-29.
110. + T cells results in antigen-specific T-cell tolerance. Nat Med 2000; 6: 1348-54.
111. + T cells is predominantly ICAM-1/LFA-1 dependent in mice. Hepatology 2005; 42: 1063-71.
112. + T cell tolerance. Hepatology 2008; 47: 296-305.
113. 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: 2970-81.
114. 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: 2960-70.
115. Jessup JM, Battle P, Waller H, et al. Reactive nitrogen and oxygen radicals formed during hepatic ischemia-reperfusion kill weakly metastatic colorectal cancer cells. Cancer Res 1999; 59: 1825-9.
116. 2 production by hepatic sinusoidal endothelium in response to B16 melanoma cell adhesion. J Cell Physiol 1996; 167: 314-23.
117. Bayon LG, Izquierdo MA, Sirovich I, et al. Role of Kupffer cells in arresting circulating tumor cells and controlling metastatic growth in the liver. Hepatology 1996; 23: 1224-31.
118. Timmers M, Vekemans K, Vermijlen D, et al. Interactions between rat colon carcinoma cells and Kupffer cells during the onset of hepatic metastasis. Int J Cancer 2004; 112: 793-802.
119. Vekemans K, Timmers M, Vermijlen D, et al. CC531s colon carcinoma cells induce apoptosis in rat hepatic endothelial cells by the Fas/ FasL-mediated pathway. Liver Int 2003; 23: 283-93.
120. Jessup JM, Samara R, Battle P, Laguinge LM. Carcinoembryonic antigen promotes tumor cell survival in liver through an IL-10-dependent pathway. Clin Exp Metastasis 2004; 21: 709-17.
121. Mendoza L, Carrascal T, De Luca M, et al. Hydrogen peroxide mediates vascular cell adhesion molecule-1 expression from interleukin-18-activated hepatic sinusoidal endothelium: Implications for circulating cancer cell arrest in the murine liver. Hepatology 2001; 34: 298-310.
122. Vidal-Vanaclocha F, Fantuzzi G, Mendoza L, et al. IL-18 regulates IL-1beta-dependent hepatic melanoma metastasis via vascular cell adhesion molecule-1. Proc Natl Acad Sci USA 2000; 97: 734-9.
123. Auguste P, Fallavollita L, Wang N, et al. The host inflammatory response promotes liver metastasis by increasing tumor cell arrest and extravasation. Am J Pathol 2007; 170: 1781-92.
124. Mendoza L, Valcarcel M, Carrascal T, et al. Inhibition of cytokine-induced microvascular arrest of tumor cells by recombinant endostatin prevents experimental hepatic melanoma metastasis. Cancer Res 2004; 64: 304-10.
125. Wang N, Thuraisingam T, Fallavollita L, et al. The secretory leukocyte protease inhibitor is a type 1 insulin-like growth factor receptor-regulated protein that protects against liver metastasis by attenuating the host proinflammatory response. Cancer Res 2006; 66: 3062-70.
126. Zubia A, Mendoza L, Vivanco S, et al. Application of stereocontrolled stepwise [3+2] cycloadditions to the preparation of inhibitors of alpha(4)beta(1)-integrin-mediated hepatic melanoma metastasis. Angew Chem Int Ed Engl 2005; 44: 2903-7.
127. Olaso E, Salado C, Egilegor E, et al. Proangiogenic role of tumor-activated hepatic stellate cells in experimental melanoma metastasis. Hepatology 2003; 37: 674-85.
128. Mueller L, Goumas FA, Affeldt M, et al. Stromal fibroblasts in colorectal liver metastases originate from resident fibroblasts and generate an inflammatory microenvironment. Am J Pathol 2007; 171: 1608-18.
129. Vermeulen PB, Colpaert C, Salgado R, et al. Liver metastases from colorectal adenocarcinomas grow in three patterns with different angiogenesis and desmoplasia. J Pathol 2001; 195: 336-42.
130. Solaun MS, Mendoza L, De Luca M, et al. Endostatin inhibits murine colon carcinoma sinusoidal-type metastases by preferential targeting of hepatic sinusoidal endothelium. Hepatology 2002; 35: 1104-16.