Therapeutic administration of the direct thrombin inhibitor argatroban reduces hepatic inflammation in mice with established fatty liver disease

American Journal of Pathology

Volumn 181, Issue 4, 2012, Pages 1287-1295

  Kassel, Karen M ^a   Sullivan, Bradley P ^a   Cui, Wei ^a   Copple, Bryan L ^a,b   Luyendyk, James P ^a,c  

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

^b MICHIGAN STATE UNIVERSITY   (United States)

^c MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; ARGATROBAN; COLLAGEN TYPE 1; COMPLEMENTARY DNA; LOW DENSITY LIPOPROTEIN RECEPTOR; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; THROMBIN; TRIACYLGLYCEROL;

ANIMAL EXPERIMENT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; DIET; HEPATITIS; HISTOPATHOLOGY; MACROPHAGE; MALE; MOUSE; NEUTROPHIL; NONALCOHOLIC FATTY LIVER; NONHUMAN; NUCLEOTIDE SEQUENCE; OSMOTIC PUMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; STELLATE CELL; WEIGHT GAIN; WESTERN DIET;

ANIMALS; CHEMOKINE CCL2; CHEMOKINE CXCL2; COLLAGEN; DIET; FATTY LIVER; FEEDING BEHAVIOR; GENE EXPRESSION REGULATION; INFLAMMATION; INTERCELLULAR ADHESION MOLECULE-1; LIPID METABOLISM; LIPIDS; LIVER; LIVER CIRRHOSIS; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; NEUTROPHILS; PIPECOLIC ACIDS; RECEPTORS, LDL; RNA, MESSENGER; THROMBIN; WEIGHT GAIN;

EID: 84866480350     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.06.011     Document Type: Article

References (57)

1. S. Bellentani, G. Saccoccio, F. Masutti, L.S. Croce, G. Brandi, F. Sasso, G. Cristanini, C. Tiribelli Prevalence of and risk factors for hepatic steatosis in Northern Italy Ann Intern Med 132 2000 112 117 (Pubitemid 30044177)
2. D.G. Tiniakos, M.B. Vos, E.M. Brunt Nonalcoholic fatty liver disease: pathology and pathogenesis Annu Rev Pathol 5 2010 145 171
3. D.E. Kleiner, E.M. Brunt, M. Van Natta, C. Behling, M.J. Contos, O.W. Cummings, L.D. Ferrell, Y.C. Liu, M.S. Torbenson, A. Unalp-Arida, M. Yeh, A.J. McCullough, A.J. Sanyal Design and validation of a histological scoring system for nonalcoholic fatty liver disease Hepatology 41 2005 1313 1321 (Pubitemid 40770284)
4. J.M. Clark, F.L. Brancati, A.M. Diehl Nonalcoholic fatty liver disease Gastroenterology 122 2002 1649 1657 (Pubitemid 34533559)
5. G.C. Farrell, C.Z. Larter Nonalcoholic fatty liver disease: from steatosis to cirrhosis Hepatology 43 2006 S99 S112
6. S.L. Friedman Mechanisms of hepatic fibrogenesis Gastroenterology 134 2008 1655 1669 (Pubitemid 351615417)
7. A. Kotronen, H. Yki-Jarvinen Fatty liver: a novel component of the metabolic syndrome Arterioscler Thromb Vasc Biol 28 2008 27 38
8. C.E. Ndumele, K. Nasir, R.D. Conceicao, J.A. Carvalho, R.S. Blumenthal, R.D. Santos Hepatic steatosis obesity, and the metabolic syndrome are independently and additively associated with increased systemic inflammation Arterioscler Thromb Vasc Biol 31 2011 1927 1932
9. G. Targher, L. Bertolini, F. Poli, S. Rodella, L. Scala, R. Tessari, L. Zenari, G. Falezza Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients Diabetes 54 2005 3541 3546 (Pubitemid 43334347)
10. A. Bertola, S. Bonnafous, R. Anty, S. Patouraux, M.C. Saint-Paul, A. Iannelli, J. Gugenheim, J. Barr, J.M. Mato, Y. Le Marchand-Brustel, A. Tran, P. Gual Hepatic expression patterns of inflammatory and immune response genes associated with obesity and NASH in morbidly obese patients PLoS One 5 2010 e13577
11. Y. Tamura, M. Sugimoto, T. Murayama, M. Minami, Y. Nishikaze, H. Ariyasu, T. Akamizu, T. Kita, M. Yokode, H. Arai C-C chemokine receptor 2 inhibitor improves diet-induced development of insulin resistance and hepatic steatosis in mice J Atheroscler Thromb 17 2010 219 228
12. A. Rull, F. Rodriguez, G. Aragones, J. Marsillach, R. Beltran, C. Alonso-Villaverde, J. Camps, J. Joven Hepatic monocyte chemoattractant protein-1 is upregulated by dietary cholesterol and contributes to liver steatosis Cytokine 48 2009 273 279
13. R. Stienstra, F. Saudale, C. Duval, S. Keshtkar, J.E. Groener, N. van Rooijen, B. Staels, S. Kersten, M. Muller Kupffer cells promote hepatic steatosis via interleukin-1beta-dependent suppression of peroxisome proliferator-activated receptor alpha activity Hepatology 51 2010 511 522
14. W. Huang, A. Metlakunta, N. Dedousis, P. Zhang, I. Sipula, J.J. Dube, D.K. Scott, R.M. O'Doherty Depletion of liver Kupffer cells prevents the development of diet-induced hepatic steatosis and insulin resistance Diabetes 59 2010 347 357
15. S. Schenk, M. Saberi, J.M. Olefsky Insulin sensitivity: modulation by nutrients and inflammation J Clin Invest 118 2008 2992 3002
16. G. Tarantino, P. Colicchio, P. Conca, C. Finelli, M.N. Di Minno, M. Tarantino, D. Capone, F. Pasanisi Young adult obese subjects with and without insulin resistance: what is the role of chronic inflammation and how to weigh it non-invasively? J Inflamm (Lond) 6 2009 6
17. P.M. Ridker High-sensitivity C-reactive protein and cardiovascular risk: rationale for screening and primary prevention Am J Cardiol 92 2003 17K 22K
18. P. Calabro, E. Golia, E.T. Yeh CRP and the risk of atherosclerotic events Semin Immunopathol 31 2009 79 94
19. T. Lisman, R.J. Porte Rebalanced hemostasis in patients with liver disease: evidence and clinical consequences Blood 116 2010 878 885
20. P. Fritsch, M. Kleber, A. Rosenkranz, M. Fritsch, W. Muntean, H. Mangge, T. Reinehr Haemostatic alterations in overweight children: associations between metabolic syndrome, thrombin generation, and fibrinogen levels Atherosclerosis 212 2010 650 655
21. M. Romano, M.T. Guagnano, G. Pacini, S. Vigneri, A. Falco, M. Marinopiccoli, M.R. Manigrasso, S. Basili, G. Davi Association of inflammation markers with impaired insulin sensitivity and coagulative activation in obese healthy women J Clin Endocrinol Metab 88 2003 5321 5326 (Pubitemid 37452734)
22. E. Sola, S. Navarro, P. Medina, A. Vaya, A. Estelles, A. Hernandez-Mijares, F. Espana Activated protein C levels in obesity and weight loss influence Thromb Res 123 2009 697 700
23. G. Targher, G. Zoppini, P. Moghetti, C.P. Day Disorders of coagulation and hemostasis in abdominal obesity: emerging role of fatty liver Semin Thromb Hemost 36 2010 41 48
24. K.M. Kassel, A.P. Owens III, C.E. Rockwell, B.P. Sullivan, R. Wang, O. Tawfik, G. Li, G.L. Guo, N. Mackman, J.P. Luyendyk Protease-activated receptor 1 and hematopoietic cell tissue factor are required for hepatic steatosis in mice fed a Western Diet Am J Pathol 179 2011 2278 2289
25. T. Iwaki, M.J. Sandoval-Cooper, M. Brechmann, V.A. Ploplis, F.J. Castellino A fibrinogen deficiency accelerates the initiation of LDL cholesterol-driven atherosclerosis via thrombin generation and platelet activation in genetically predisposed mice Blood 107 2006 3883 3891 (Pubitemid 43726792)
26. A. Owens III, F. Passam, S. Antoniak, S. Marshall, A. McDaniel, L. Rudel, J. Williams, B. Hubbard, J. Dutton, J. Wang, P. Tobias, L. Curtiss, A. Daugherty, D. Kirchhofer, J. Luyendyk, P. Moriarty, S. Nagaraja, B. Furie, B. Furie, D. Johns, R. Temel, N. Mackman Monocyte tissue factor-dependent activation of coagulation in hypercholesterolemic mice and monkeys is inhibited by simvastatin J Clin Invest 122 2012 558 568
27. T. Kitaoka, Y. Hua, G. Xi, J.T. Hoff, R.F. Keep Delayed argatroban treatment reduces edema in a rat model of intracerebral hemorrhage Stroke 33 2002 3012 3018 (Pubitemid 35462880)
28. M. Mihara, K. Aihara, Y. Ikeda, S. Yoshida, M. Kinouchi, K. Kurahashi, Y. Fujinaka, M. Akaike, T. Matsumoto Inhibition of thrombin action ameliorates insulin resistance in type 2 diabetic db/db mice Endocrinology 151 2010 513 519
29. Owoo G, Burgos RA, inventors; Bayer Int, assignee. 2008 Feb 29. Argatroban formulations and methods for making and using same. United States patent US 7,915,290 B2
30. Y. Tanaka, L.M. Aleksunes, R.L. Yeager, M.A. Gyamfi, N. Esterly, G.L. Guo, C.D. Klaassen NF-E2-related factor 2 inhibits lipid accumulation and oxidative stress in mice fed a high-fat diet J Pharmacol Exp Ther 325 2008 655 664 (Pubitemid 351574806)
31. J.P. Luyendyk, B.P. Sullivan, G.L. Guo, R. Wang Tissue factor-deficiency and protease activated receptor-1-deficiency reduce inflammation elicited by diet-induced steatohepatitis in mice Am J Pathol 176 2010 177 186
32. S. Clement, C. Juge-Aubry, A. Sgroi, S. Conzelmann, V. Pazienza, B. Pittet-Cuenod, C.A. Meier, F. Negro Monocyte chemoattractant protein-1 secreted by adipose tissue induces direct lipid accumulation in hepatocytes Hepatology 48 2008 799 807
33. M. Endo, T. Masaki, M. Seike, H. Yoshimatsu TNF-alpha induces hepatic steatosis in mice by enhancing gene expression of sterol regulatory element binding protein-1c (SREBP-1c) Exp Biol Med (Maywood) 232 2007 614 621 (Pubitemid 46683386)
34. B.M. De Taeye, T. Novitskaya, O.P. McGuinness, L. Gleaves, M. Medda, J.W. Covington, D.E. Vaughan Macrophage TNF-alpha contributes to insulin resistance and hepatic steatosis in diet-induced obesity Am J Physiol Endocrinol Metab 293 2007 E713 E725
35. S.S. Rensen, Y. Slaats, J. Nijhuis, A. Jans, V. Bieghs, A. Driessen, E. Malle, J.W. Greve, W.A. Buurman Increased hepatic myeloperoxidase activity in obese subjects with nonalcoholic steatohepatitis Am J Pathol 175 2009 1473 1482
36. L. Yang, R.M. Froio, T.E. Sciuto, A.M. Dvorak, R. Alon, F.W. Luscinskas ICAM-1 regulates neutrophil adhesion and transcellular migration of TNF-alpha-activated vascular endothelium under flow Blood 106 2005 584 592 (Pubitemid 40981255)
37. J. Lee, G. Cacalano, T. Camerato, K. Toy, M.W. Moore, W.I. Wood Chemokine binding and activities mediated by the mouse IL-8 receptor J Immunol 155 1995 2158 2164
38. A.A. Gupte, J.Z. Liu, Y. Ren, L.J. Minze, J.R. Wiles, A.R. Collins, C.J. Lyon, D. Pratico, M.J. Finegold, S.T. Wong, P. Webb, J.D. Baxter, D.D. Moore, W.A. Hsueh Rosiglitazone attenuates age- and diet-associated nonalcoholic steatohepatitis in male low-density lipoprotein receptor knockout mice Hepatology 52 2010 2001 2011
39. S. Subramanian, L. Goodspeed, S. Wang, J. Kim, L. Zeng, G.N. Ioannou, W.G. Haigh, M.M. Yeh, K.V. Kowdley, K.D. O'Brien, S. Pennathur, A. Chait Dietary cholesterol exacerbates hepatic steatosis and inflammation in obese LDL receptor-deficient mice J Lipid Res 52 2011 1626 1635
40. G. Targher, M. Chonchol, L. Miele, G. Zoppini, I. Pichiri, M. Muggeo Nonalcoholic fatty liver disease as a contributor to hypercoagulation and thrombophilia in the metabolic syndrome Semin Thromb Hemost 35 2009 277 287
41. M. Cigolini, G. Targher, G. Agostino, M. Tonoli, M. Muggeo, G. De Sandre Liver steatosis and its relation to plasma haemostatic factors in apparently healthy men: role of the metabolic syndrome Thromb Haemost 76 1996 69 73 (Pubitemid 26254319)
42. V. Bieghs, P.J. Van Gorp, K. Wouters, T. Hendrikx, M.J. Gijbels, B.M. van, J. Bakker, C.J. Binder, D. Lutjohann, B. Staels, M.H. Hofker, R. Shiri-Sverdlov LDL receptor knock-out mice are a physiological model particularly vulnerable to study the onset of inflammation in non-alcoholic fatty liver disease PLoS One 7 2012 e30668
43. A.E. Obstfeld, E. Sugaru, M. Thearle, A.M. Francisco, C. Gayet, H.N. Ginsberg, E.V. Ables, A.W. Ferrante Jr. C-C chemokine receptor 2 (CCR2) regulates the hepatic recruitment of myeloid cells that promote obesity-induced hepatic steatosis Diabetes 59 2010 916 925
44. S.S. Rensen, Y. Slaats, A. Driessen, C.J. Peutz-Kootstra, J. Nijhuis, R. Steffensen, J.W. Greve, W.A. Buurman Activation of the complement system in human nonalcoholic fatty liver disease Hepatology 50 2009 1809 1817
45. J.W. Haukeland, J.K. Damas, Z. Konopski, E.M. Loberg, T. Haaland, I. Goverud, P.A. Torjesen, K. Birkeland, K. Bjoro, P. Aukrust Systemic inflammation in nonalcoholic fatty liver disease is characterized by elevated levels of CCL2 J Hepatol 44 2006 1167 1174
46. K.M. Kassel, A.P. Owens III, C.E. Rockwell, B.P. Sullivan, R. Wang, O. Tawfik, G. Li, G.L. Guo, N. Mackman, J.P. Luyendyk Protease-activated receptor 1 and hematopoietic cell tissue factor are required for hepatic steatosis in mice fed a Western diet Am J Pathol 179 2011 2278 2289
47. S. Vermeire, G. Van Assche, P. Rutgeerts C-reactive protein as a marker for inflammatory bowel disease Inflamm Bowel Dis 10 2004 661 665 (Pubitemid 39276479)
48. L. Boring, J. Gosling, M. Cleary, I.F. Charo Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis Nature 394 1998 894 897 (Pubitemid 28410911)
49. M. Namiki, S. Kawashima, T. Yamashita, M. Ozaki, T. Hirase, T. Ishida, N. Inoue, K. Hirata, A. Matsukawa, R. Morishita, Y. Kaneda, M. Yokoyama Local overexpression of monocyte chemoattractant protein-1 at vessel wall induces infiltration of macrophages and formation of atherosclerotic lesion: synergism with hypercholesterolemia Arterioscler Thromb Vasc Biol 22 2002 115 120 (Pubitemid 34076241)
50. J.L. Goldstein, W.R. Hazzard, H.G. Schrott, E.L. Bierman, A.G. Motulsky Hyperlipidemia in coronary heart disease I. Lipid levels in 500 survivors of myocardial infarction J Clin Invest 52 1973 1533 1543
51. H. Ten Cate Tissue factor-driven thrombin generation and inflammation in atherosclerosis Thromb Res 129 Suppl 2 2012 S38 S40
52. B. Sun, M. Karin Obesity, inflammation, and liver cancer J Hepatol 56 2012 704 713
53. R. Kohli, M. Kirby, S.A. Xanthakos, S. Softic, A.E. Feldstein, V. Saxena, P.H. Tang, L. Miles, M.V. Miles, W.F. Balistreri, S.C. Woods, R.J. Seeley High-fructose, medium chain trans fat diet induces liver fibrosis and elevates plasma coenzyme Q9 in a novel murine model of obesity and nonalcoholic steatohepatitis Hepatology 52 2010 934 944
54. L.D. DeLeve, X. Wang, G.C. Kanel, R.D. Atkinson, R.S. McCuskey Prevention of hepatic fibrosis in a murine model of metabolic syndrome with nonalcoholic steatohepatitis Am J Pathol 173 2008 993 1001
55. S. Fiorucci, E. Antonelli, E. Distrutti, B. Severino, R. Fiorentina, M. Baldoni, G. Caliendo, V. Santagada, A. Morelli, G. Cirino PAR1 antagonism protects against experimental liver fibrosis Role of proteinase receptors in stellate cell activation Hepatology 39 2004 365 375 (Pubitemid 38222177)
56. S.L. Hernandez-Gea V and Friedman Pathogenesis of liver fibrosis Annu Rev Pathol 6 2011 425 456
57. J.I. Weitz Factor Xa and thrombin as targets for new oral anticoagulants Thromb Res 127 Suppl 2 2011 S5 S12