Characterization of animal models for primary sclerosing cholangitis (PSC)

Journal of Hepatology

Volumn 60, Issue 6, 2014, Pages 1290-1303

  Fickert, Peter ^a   Pollheimer, Marion J ^a   Beuers, Ulrich ^b   Lackner, Carolin ^a   Hirschfield, Gideon ^c   Housset, Chantal ^d   Keitel, Verena ^e   Schramm, Christoph ^f   Marschall, Hanns Ulrich ^g   Karlsen, Tom H ^h,i   Melum, Espen ^h   Kaser, Arthur ^j   Eksteen, Bertus ^c   Strazzabosco, Mario ^k,l   Manns, Michael ^m   Trauner, Michael ⁿ  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

^d SORBONNE UNIVERSITÉ   (France)

^e HEINRICH HEINE UNIVERSITY   (Germany)

^f UNIVERSITY OF HAMBURG   (Germany)

^g UNIVERSITY OF GOTHENBURG   (Sweden)

^h OSLO UNIVERSITY HOSPITAL   (Norway)

ⁱ UNIVERSITY OF BERGEN   (Norway)

^j UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^k UNIVERSITY OF MILANO BICOCCA   (Italy)

^l YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^m HANNOVER MEDICAL SCHOOL   (Germany)

ⁿ MEDICAL UNIVERSITY OF VIENNA   (Austria)

more..

Author keywords

Animal model; Bile acids; Biliary fibrosis; Cholangiopathies; Cholestatic liver disease; Primary sclerosing cholangitis

Indexed keywords

ANIMAL HOUSING; ANIMAL MODEL; BILE DUCT; CHOLANGIOGRAPHY; CHOLANGITIS; CHOLESTASIS; DIET; EXPERIMENTAL DISEASE; HUMAN; INFLAMMATORY BOWEL DISEASE; LABORATORY; LIVER FIBROSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PHENOTYPE; PRIMARY SCLEROSING CHOLANGITIS; PRIORITY JOURNAL; REVIEW; STANDARD; TIGHT JUNCTION; TISSUE SECTION; ANIMAL; CHOLANGITIS, SCLEROSING; DISEASE MODEL; PATHOLOGY; PATHOPHYSIOLOGY; AUTOIMMUNE DISEASE; BILE DUCT DILATATION; BILIARY TRACT FIBROSIS; BODY WEIGHT; CANCER RISK; CD4 CD8 RATIO; CELL PROLIFERATION; CELLULAR PARAMETERS; DUCTULAR REACTION; END STAGE LIVER DISEASE; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INNATE IMMUNITY; INTESTINE MUCOSA; LABORATORY TEST; LIVER CARCINOGENESIS; LIVER TRANSPLANTATION; LIVER WEIGHT; MORPHOMETRICS; MOUSE MODEL; ORGAN PRESERVATION; PATHOGENESIS; QUANTITATIVE ANALYSIS; SPLEEN WEIGHT; TISSUE PRESERVATION;

ANIMALS; CHOLANGITIS, SCLEROSING; DISEASE MODELS, ANIMAL; HUMANS;

EID: 84901234765     PISSN: 01688278     EISSN: 16000641     Source Type: Journal    
DOI: 10.1016/j.jhep.2014.02.006     Document Type: Review

References (130)

1. E.V. Loftus Jr., G.C. Harewood, C.G. Loftus, W.J. Tremaine, W.S. Harmsen, and A.R. Zinsmeister et al. PSC-IBD: a unique form of inflammatory bowel disease associated with primary sclerosing cholangitis Gut 54 2005 91 96
2. U. Broome, R. Olsson, L. Lööf, G. Bodemar, R. Hultcrantz, and A. Danielsson et al. Natural history and prognostic factors in 305 Swedish patients with primary sclerosing cholangitis Gut 38 1996 610 615
3. R.W. Chapman, B.A. Arborgh, J.M. Rhodes, J.A. Summerfield, R. Dick, and P.J. Scheuer et al. Primary sclerosing cholangitis: a review of its clinical features, cholangiography, and hepatic histology Gut 21 1980 870 877
4. R.H. Wiesner, P.M. Grambsch, E.R. Dickson, J. Ludwig, R.L. MacCarty, and E.B. Hunter et al. Primary sclerosing cholangitis: natural history, prognostic factors and survival analysis Hepatology 10 1989 430 436
5. O. Fausa, E. Schrumpf, and K. Elgjo Relationship of inflammatory bowel disease and primary sclerosing cholangitis Semin Liver Dis 11 1991 31 39
6. European Association for the Study of the Liver EASL Clinical Practice Guidelines: management of cholestatic liver diseases J Hepatol 51 2009 237 267
7. E. Krones, I. Graziadei, M. Trauner, and P. Fickert Evolving concepts in primary sclerosing cholangitis Liver Int 32 2012 352 369
8. J. Fevery, L. Henckaerts, R. Van Oirbeek, S. Vermeire, P. Rutgeerts, and F. Nevens et al. Malignancies and mortality in 200 patients with primary sclerosering cholangitis: a long-term single-centre study Liver Int 32 2012 214 222
9. A. Bergquist, A. Ekbom, R. Olsson, D. Kornfeldt, L. Lööf, and A. Danielsson et al. Hepatic and extrahepatic malignancies in primary sclerosing cholangitis J Hepatol 36 2002 321 327
10. T.J. Weismüller, J. Wedemeyer, S. Kubicka, C.P. Strassburg, and M.P. Manns The challenges in primary sclerosing cholangitis-aetiopathogenesis, autoimmunity, management and malignancy J Hepatol 48 2008 S38 S57
11. M. Strazzabosco, L. Fabris, and C. Spirli Pathophysiology of cholangiopathies J Clin Gastroenterol 39 2005 S90 S102
12. T.H. Karlsen, A. Franke, E. Melum, A. Kaser, J.R. Hov, and T. Balschun et al. Genome-wide association analysis in primary sclerosing cholangitis Gastroenterology 138 2010 1102 1111
13. P.J. Trivedi, and G.M. Hirschfield Review article: overlap syndromes and autoimmune liver disease Aliment Pharmacol Ther 36 2012 517 533
14. J.M. Vierling Animal models for primary sclerosing cholangitis Best Pract Res Clin Gastroenterol 15 2001 591 610
15. M.J. Pollheimer, M. Trauner, and P. Fickert Will we ever model PSC? - "It's hard to be a PSC model!" Clin Res Hepatol Gastroenterol 35 2011 792 804
16. P. Fickert Time to say goodbye to the drug or the model? - Why do drugs fail to live up to their promise in bile duct ligated mice? J Hepatol 60 2014 12 15
17. P. Fickert, M.J. Pollheimer, C.H. Österreicher, and M. Trauner Animal models of cholestasis in animal models for the study of human diseases 2013 Academic Press p. 331-410
18. R. Chapman, J. Fevery, A. Kalloo, D.M. Nagorney, K.M. Boberg, B. Shneider, and G.J. Gores American Association for the Study of Liver Diseases. Diagnosis and management of primary sclerosing cholangitis Hepatology 51 2010 660 678
19. S. Hohenester, U. Beuers, J.F. Medina, and R.P. Elferink Antimitochondrial antibodies may be insufficiently specific to define primary biliary cirrhosis-like disease in mouse models Hepatology 58 2013 828 830
20. Y. Zhang, and C.D. Klaassen Effects of feeding bile acids and a bile acid sequestrant on hepatic bile acid composition in mice J Lipid Res 51 2010 3230 3242
21. Y. Alnouti, I.L. Csanaky, and C.D. Klaassen Quantitative-profiling of bile acids and their conjugates in mouse liver, bile, plasma, and urine using LC-MS/MS J Chromatogr B Analyt Technol Biomed Life Sci 873 2008 209 217
22. J. Huang, S.P. Bathena, I.L. Csanaky, and Y. Alnouti Simultaneous characterization of bile acids and their sulfate metabolites in mouse liver, plasma, bile, and urine using LC-MS/MS J Pharm Biomed Anal 55 2011 1111 1119
23. L. Humbert, M.A. Maubert, C. Wolf, H. Duboc, M. Mahé, and D. Farabos et al. Bile acid profiling in human biological samples: comparison of extraction procedures and application to normal and cholestatic patients J Chromatogr B Analyt Technol Biomed Life Sci 15 2012 135 145
24. T. Goto, K.T. Myint, K. Sato, O. Wada, G. Kakiyama, and T. Iida et al. LC/ESI-tandem mass spectrometric determination of bile acid 3-sulfates in human urine 3beta-Sulfooxy-12alpha-hydroxy-5beta-cholanoic acid is an abundant nonamidated sulfate J Chromatogr B Analyt Technol Biomed Life Sci 846 2007 69 77
25. B.C. Portmann, and Y. Nakamura Diseases of the bile ducts A.D. Burt, B.C. Portmann, L.D. Ferrell, MacSween's pathology of the liver 5th ed. 2007 Churchill Livingstone Elsevier Philadelphia 517 581
26. B. Portmann, and Y. Zen Inflammatory disease of the bile ducts-cholangiopathies: liver biopsy challenge and clinicopathological correlation Histopathology 60 2012 236 248
27. M.E. Thorpe, P.J. Scheuer, and S. Sherlock Primary sclerosing cholangitis, the biliary tree, and ulcerative colitis Gut 8 1967 435 448
28. J.H. Lefkowitch Primary sclerosing cholangitis Arch Intern Med 142 1982 1157 1160
29. V.J. Desmet Histopathology of chronic cholestasis and adult ductopenic syndrome Clin Liver Dis 2 1998 249 264 [viii]
30. J.H. Lefkowitch Scheuer's liver biopsy interpretation 8th ed. 2010 Saunders/Elsevier Edinburgh p. 47-74
31. V.J. Desmet Histopathology of cholestasis Verh Dtsch Ges Pathol 79 1995 233 240
32. F. Seibold, P. Weber, R. Klein, P.A. Berg, and K.H. Wiedmann Clinical significance of antibodies against neutrophils in patients with inflammatory bowel disease and primary sclerosing cholangitis Gut 33 1992 657 662
33. D.S. Bansi, K.A. Fleming, and R.W. Chapman Importance of antineutrophil cytoplasmic antibodies in primary sclerosing cholangitis and ulcerative colitis: prevalence, titre, and IgG subclass Gut 38 1996 384 389
34. B. Terjung, and H.J. Worman Anti-neutrophil antibodies in primary sclerosing cholangitis Best Pract Res Clin Gastroenterol 15 2001 629 642
35. C. Schwarze, B. Terjung, P. Lilienweiss, U. Beuers, V. Herzog, and T. Sauerbruch et al. IgA class antineutrophil cytoplasmic antibodies in primary sclerosing cholangitis and autoimmune hepatitis Clin Exp Immunol 133 2003 283 289
36. J.H. Aron, and C.L. Bowlus The immunobiology of primary sclerosing cholangitis Semin Immunopathol 31 2009 383 397
37. R. Fiorotto, R. Scirpo, M. Trauner, L. Fabris, R. Hoque, and C. Spirli et al. Loss of CFTR affects biliary epithelium innate immunity and causes TLR4-NF-κB-mediated inflammatory response in mice Gastroenterology 141 2011 1498 1508
38. C. Spirlì, L. Fabris, E. Duner, R. Fiorotto, G. Ballardini, and T. Roskams et al. Cytokine-stimulated nitric oxide production inhibits adenylyl cyclase and cAMP-dependent secretion in cholangiocytes Gastroenterology 124 2003 737 753
39. C. Spirlì, M.H. Nathanson, R. Fiorotto, E. Duner, L.A. Denson, and J.M. Sanz et al. Proinflammatory cytokines inhibit secretion in rat bile duct epithelium Gastroenterology 121 2001 156 169
40. X. Bo, U. Broome, M. Remberger, and S. Sumitran-Holgersson Tumour necrosis factor alpha impairs function of liver derived T lymphocytes and natural killer cells in patients with primary sclerosing cholangitis Gut 49 2001 131 141
41. T.L. Whiteside, S. Lasky, L. Si, and D.H. Van Thiel Immunologic analysis of mononuclear cells in liver tissues and blood of patients with primary sclerosing cholangitis Hepatology 5 1985 468 474
42. E. Hashimoto, K.D. Lindor, H.A. Homburger, E.R. Dickson, A.J. Czaja, and R.H. Wiesner et al. Immunohistochemical characterization of hepatic lymphocytes in primary biliary cirrhosis in comparison with primary sclerosing cholangitis and autoimmune chronic active hepatitis Mayo Clin Proc 68 1993 1049 1055
43. S. Zeissig, T. Olszak, E. Melum, R.S. Blumberg, J.R. Hov, and A. Lleo et al. Analyzing antigen recognition by natural killer T cells Methods Mol Biol 960 2013 557 572
44. B. Lee, M. Sharron, L.J. Montaner, D. Weissman, and R.W. Doms Quantification of CD4, CCR5, and CXCR4 levels on lymphocyte subsets, dendritic cells, and differentially conditioned monocyte-derived macrophages Proc Natl Acad Sci U S A 96 1999 5215 5220
45. M.J. Pollheimer, E. Halilbasic, P. Fickert, and M. Trauner Pathogenesis of primary sclerosing cholangitis Best Pract Res Clin Gastroenterol 25 2011 727 739
46. M. Yasoshima, Y. Nakanuma, K. Tsuneyama, J. Van de Water, and M.E. Gershwin Immunohistochemical analysis of adhesion molecules in the micro-environment of portal tracts in relation to aberrant expression of PDC-E2 and HLA-DR on the bile ducts in primary biliary cirrhosis J Pathol 175 1995 319 325
47. S. Bloom, K. Fleming, and R. Chapman Adhesion molecule expression in primary sclerosing cholangitis and primary biliary cirrhosis Gut 36 1995 604 609
48. A.T. Borchers, S. Shimoda, C. Bowlus, C.L. Keen, and M.E. Gershwin Lymphocyte recruitment and homing to the liver in primary biliary cirrhosis and primary sclerosing cholangitis Semin Immunopathol 31 2009 309 322
49. D.H. Adams, S.G. Hubscher, J. Shaw, G.D. Johnson, C. Babbs, and R. Rothlein et al. Increased expression of intercellular adhesion molecule 1 on bile ducts in primary biliary cirrhosis and primary sclerosing cholangitis Hepatology 14 1991 426 431
50. P. Dillon, D. Belchis, T. Tracy, R. Cilley, L. Hafer, and T. Krummel Increased expression of intercellular adhesion molecules in biliary atresia Am J Pathol 145 1994 263 267
51. A.J. Grant, S. Goddard, J. Ahmed-Choudhury, G. Reynolds, D.G. Jackson, and M. Briskin et al. Hepatic expression of secondary lymphoid chemokine (CCL21) promotes the development of portal-associated lymphoid tissue in chronic inflammatory liver disease Am J Pathol 160 2002 1445 1455
52. A.J. Grant, P.F. Lalor, M. Salmi, S. Jalkanen, and D.H. Adams Homing of mucosal lymphocytes to the liver in the pathogenesis of hepatic complications of inflammatory bowel disease Lancet 359 2002 150 157
53. A.J. Grant, P.F. Lalor, S.G. Hubscher, M. Briskin, and D.H. Adams MAdCAM-1 expressed in chronic inflammatory liver disease supports mucosal lymphocyte adhesion to hepatic endothelium (MAdCAM-1 in chronic inflammatory liver disease) Hepatology 33 2001 1065 1072
54. K.J. Hillan, K.E. Hagler, R.N. MacSween, A.M. Ryan, M.E. Renz, and H.H. Chiu et al. Expression of the mucosal vascular addressin, MAdCAM-1, in inflammatory liver disease Liver 19 1999 509 518
55. B. Eksteen, A.J. Grant, A. Miles, S.M. Curbishley, P.F. Lalor, and S.G. Hubscher et al. Hepatic endothelial CCL25 mediates the recruitment of CCR9+ gut-homing lymphocytes to the liver in primary sclerosing cholangitis J Exp Med 200 2004 1511 1517
56. B. Eksteen, J.R. Mora, E.L. Haughton, N.C. Henderson, L. Lee-Turner, and E.J. Villablanca et al. Gut homing receptors on CD8 T cells are retinoic acid dependent and not maintained by liver dendritic or stellate cells Gastroenterology 137 2009 320 329
57. B. Wang, B.M. Dolinski, N. Kikuchi, D.R. Leone, M.G. Peters, and P.H. Weinreb et al. Role of alphavbeta6 integrin in acute biliary fibrosis Hepatology 46 2007 1404 1412
58. E. Patsenker, Y. Popov, F. Stickel, A. Jonczyk, S.L. Goodman, and D. Schuppan Inhibition of integrin alphavbeta6 on cholangiocytes blocks transforming growth factor-beta activation and retards biliary fibrosis progression Gastroenterology 135 2008 660 670
59. V.J. Desmet Ductal plates in hepatic ductular reactions. Hypothesis and implications III. Implications for liver pathology Virchows Arch 458 2011 271 279
60. L. Fabris, and M. Strazzabosco Epithelial-mesenchymal interactions in biliary diseases Semin Liver Dis 31 2011 11 32
61. L. Fabris, M. Cadamuro, M. Guido, C. Spirli, R. Fiorotto, and M. Colledan et al. Analysis of liver repair mechanisms in Alagille syndrome and biliary atresia reveals a role for notch signaling Am J Pathol 171 2007 641 653
62. J. Liu, A.N. Eischeid, and X.M. Chen Col1A1 production and apoptotic resistance in TGF-β1-induced epithelial-to-mesenchymal transition-like phenotype of 603B cells PLoS One 7 2012 e51371
63. E.B. Alabraba, V. Lai, L. Boon, S.J. Wigmore, D.H. Adams, and S.C. Afford Coculture of human liver macrophages and cholangiocytes leads to CD40-dependent apoptosis and cytokine secretion Hepatology 47 2008 552 562
64. D. Alvaro, P. Onori, V.D. Metalli, G. Svegliati-Baroni, F. Folli, and A. Franchitto et al. Intracellular pathways mediating estrogen-induced cholangiocyte proliferation in the rat Hepatology 36 2002 297 304
65. S.M. Cruickshank, J. Southgate, P.J. Selby, and L.K. Trejdosiewicz Expression and cytokine regulation of immune recognition elements by normal human biliary epithelial and established liver cell lines in vitro J Hepatol 29 1998 550 558
66. V. Cardinale, Y. Wang, G. Carpino, C.B. Cui, M. Gatto, and M. Rossi et al. Multipotent stem/progenitor cells in human biliary tree give rise to hepatocytes, cholangiocytes, and pancreatic islets Hepatology 54 2011 2159 2172
67. R. Chapman, and S. Cullen Etiopathogenesis of primary sclerosing cholangitis World J Gastroenterol 14 2008 3350 3359
68. J.J. Van den Oord, R. Sciot, and V.J. Desmet Expression of MHC products by normal and abnormal bile duct epithelium J Hepatol 3 1986 310 317
69. K.N. Lazaridis, M. Strazzabosco, and N.F. Larusso The cholangiopathies: disorders of biliary epithelia Gastroenterology 127 2004 1565 1577
70. T. Ishikawa, V.M. Factor, J.U. Marquardt, C. Raggi, D. Seo, and M. Kitade et al. Hepatocyte growth factor/c-met signaling is required for stem-cell-mediated liver regeneration in mice Hepatology 55 2012 1215 1226
71. R.G. Wells The role of matrix stiffness in hepatic stellate cell activation and liver fibrosis J Clin Gastroenterol 39 2005 158 161
72. T. Kisseleva, M. Cong, Y. Paik, D. Scholten, C. Jiang, and C. Benner et al. Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis Proc Natl Acad Sci U S A 109 2012 9448 9453
73. J.S. Troeger, I. Mederacke, G.Y. Gwak, D.H. Dapito, X. Mu, and C.C. Hsu et al. Deactivation of hepatic stellate cells during liver fibrosis resolution in mice Gastroenterology 143 2012 1073 1083
74. S. Lemoinne, A. Cadoret, H. El Mourabit, D. Thabut, and C. Housset Origins and functions of liver myofibroblasts Biochim Biophys Acta 1832 2013 948 954
75. M. Penz-Österreicher, C.H. Österreicher, and M. Trauner Fibrosis in autoimmune and cholestatic liver disease Best Pract Res Clin Gastroenterol 25 2011 245 258
76. C.H. Österreicher, M. Penz-Österreicher, S.I. Grivennikov, M. Guma, E.K. Koltsova, and C. Datz et al. Fibroblast-specific protein 1 identifies an inflammatory subpopulation of macrophages in the liver Proc Natl Acad Sci U S A 108 2011 308 313
77. M. Pinzani Epithelial-mesenchymal transition in chronic liver disease: fibrogenesis or escape from death? J Hepatol 55 2011 459 465
78. J.H. Lefkowitch Special stains in diagnostic liver pathology Semin Diagn Pathol 23 2006 190 198
79. L.C. Junqueira, G. Bignolas, and R.R. Brentani Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections Histochem J 11 1979 447 455
80. W. Jimenez, A. Parés, J. Caballería, D. Heredia, M. Bruguera, and M. Torres et al. Measurement of fibrosis in needle liver biopsies: evaluation of a colorimetric method Hepatology 5 1985 815 818
81. W. Malkusch, B. Rehn, and J. Bruch Advantages of Sirius Red staining for quantitative morphometric collagen measurements in lungs Exp Lung Res 21 1995 67 77
82. L.C. Junqueira, G.S. Montes, and E.M. Sanchez The influence of tissue section thickness on the study of collagen by the Picrosirius-polarization method Histochemistry 74 1982 153 156
83. D.M. Bolarin, and E.C. Azinge Biochemical markers, extracellular components in liver fibrosis and cirrhosis Niger Q J Hosp Med 17 2007 42 52
84. T. Kisseleva, and D.A. Brenner Inactivation of myofibroblasts during regression of liver fibrosis Cell Cycle 12 2013 381 382
85. S. Sakisaka, T. Kawaguchi, E. Taniguchi, S. Hanada, K. Sasatomi, and H. Koga et al. Alterations in tight junctions differ between primary biliary cirrhosis and primary sclerosing cholangitis Hepatology 33 2001 1460 1468
86. P. Fickert, A. Fuchsbichler, M. Wagner, G. Zollner, A. Kaser, and H. Tilg et al. Regurgitation of bile acids from leaky bile ducts causes sclerosing cholangitis in Mdr2 (Abcb4) knockout mice Gastroenterology 127 2004 261 274
87. M. Muendoerfer, U.F. Schaefer, P. Koenig, J.S. Walk, P. Loos, and S. Balbach et al. Online monitoring of transepithelial electrical resistance (TEER) in an apparatus for combined dissolution and permeation testing Int J Pharm 392 2010 134 140
88. J.H. Tabibian, S.I. Macura, S.P. O'Hara, J.L. Fidler, J.F. Glockner, and N. Takahashi et al. Micro-computed tomography and nuclear magnetic resonance imaging for noninvasive, live-mouse cholangiography Lab Invest 93 2013 733 743
89. P. Fickert, G. Zollner, A. Fuchsbichler, C. Stumptner, A.H. Weiglein, and F. Lammert et al. Ursodeoxycholic acid aggravates bile infarcts in bile duct-ligated and Mdr2 knockout mice via disruption of cholangioles Gastroenterology 123 2002 1238 1251
90. S.M. Wiener, R.F. Hoyt Jr., J.R. Deleonardis, R.R. Clevenger, K.R. Jeffries, and K. Nagashima et al. Manometric changes during retrograde biliary infusion in mice Am J Physiol Gastrointest Liver Physiol 279 2000 G49 G66
91. S. Lyoumi, M. Abitbol, D. Rainteau, Z. Karim, F. Bernex, and V. Oustric et al. Protoporphyrin retention in hepatocytes and Kupffer cells prevents sclerosing cholangitis in erythropoietic protoporphyria mouse model Gastroenterology 141 2011 1509 1519
92. W.S. Garrett, C.A. Gallini, T. Yatsunenko, M. Michaud, A. DuBois, and M.L. Delaney et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis Cell Host Microbe 8 2010 292 300
93. C.O. Elson, K.W. Beagley, A.T. Sharmanov, K. Fujihashi, H. Kiyono, and G.S. Tennyson et al. Hapten-induced model of murine inflammatory bowel disease: mucosa immune responses and protection by tolerance J Immunol 157 1996 2174 2185
94. A. Kaser, A.H. Lee, A. Franke, J.N. Glickman, S. Zeissig, and H. Tilg et al. XBP1 links ER stress to intestinal inflammation and confers genetic risk for human inflammatory bowel disease Cell 134 2008 743 756
95. L. Jostins, S. Ripke, R.K. Weersma, R.H. Duerr, D.P. McGovern, and K.Y. Hui et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease Nature 49 2012 119 124
96. P. Newell, A. Villanueva, S.L. Friedman, K. Koike, and J.M. Llovet Experimental models of hepatocellular carcinoma J Hepatol 48 2008 858 879
97. M. Katzenellenbogen, O. Pappo, H. Barash, N. Klopstock, L. Mizrahi, and D. Olam et al. Multiple adaptive mechanisms to chronic liver disease revealed at early stages of liver carcinogenesis in the Mdr2-knockout mice Cancer Res 66 2006 4001 4010
98. J. Bolker Model organisms: there's more to life than rats and flies Nature 491 2012 31 33
99. H. Geerts Of mice and men: bridging the translational disconnect in CNS drug discovery CNS Drugs 23 2009 915 926
100. A.M. Arenas-Gamboa, J.J. Bearss, G.B. Hubbard, B.F. Porter, M.A. Owston, and E.J. Dick Jr. et al. Sclerosing cholangitis in baboons (Papio spp) resembling primary sclerosing cholangitis of humans Vet Pathol 49 2012 524 527
101. M. Mourelle, A. Salas, J. Vilaseca, F. Guarner, and J.R. Malagelada Induction of chronic cholangitis in the rat by trinitrobenzene sulfonic acid J Hepatol 22 1995 219 225
102. T. Orth, M. Neurath, P. Schirmacher, P.R. Galle, and W.J. Mayet A novel rat model of chronic fibrosing cholangitis induced by local administration of a hapten reagent into the dilated BD is associated with increased TNF-alpha production and autoantibodies J Hepatol 33 2000 862 872
103. M. Goetz, H.A. Lehr, M.F. Neurath, P.R. Galle, and T. Orth Long-term evaluation of a rat model of chronic cholangitis resembling human primary sclerosing cholangitis Scand J Immunol 58 2003 533 540
104. K. Tjandra, K.A. Sharkey, and M.G. Swain Progressive development of a Th1-type hepatic cytokine profile in rats with experimental cholangitis Hepatology 31 2000 280 290
105. S.N. Lichtman, J. Wang, and R.L. Clark A microcholangiographic study of liver disease models in rats Acad Radiol 2 1995 515 521
106. P. Fickert, U. Stöger, A. Fuchsbichler, T. Moustafa, H.U. Marschall, and A.H. Weiglein et al. A new xenobiotic-induced mouse model of sclerosing cholangitis and biliary fibrosis Am J Pathol 171 2007 525 536
107. M. Marzioni, S. Saccomanno, L. Agostinelli, C. Rychlicki, S. De Minicis, and I. Pierantonelli et al. PDX-1/Hes-1 interactions determine cholangiocyte proliferative response to injury in rodents: possible implications for sclerosing cholangitis J Hepatol 58 2013 750 756
108. P. Fickert, A. Fuchsbichler, H.U. Marschall, M. Wagner, G. Zollner, and R. Krause et al. Lithocholic acid feeding induces segmental bile duct obstruction and destructive cholangitis in mice Am J Pathol 168 2006 410 422
109. J.J. Smit, A.H. Schinkel, R.P. Oude Elferink, A.K. Groen, E. Wagenaar, and L. van Deemter et al. Homozygous disruption of the murine mdr2 P-glycoprotein gene leads to a complete absence of phospholipid from bile and to liver disease Cell 75 1993 451 462
110. P.R. Durie, G. Kent, M.J. Phillips, and C.A. Ackerley Characteristic multiorgan pathology of cystic fibrosis in a long-living cystic fibrosis transmembrane regulator knockout murine model Am J Pathol 164 2004 1481 1493
111. P.G. Blanco, M.M. Zaman, O. Junaidi, S. Sheth, R.K. Yantiss, and I.A. Nasser et al. Induction of colitis in cftr-/- mice results in bile duct injury Am J Physiol Gastrointest Liver Physiol 287 2004 G491 G496
112. L. Meerman, N.R. Koopen, V. Bloks, H. Van Goor, R. Havinga, and B.G. Wolthers et al. Biliary fibrosis associated with altered bile composition in a mouse model of erythropoietic protoporphyria Gastroenterology 117 1999 696 705
113. L. Libbrecht, L. Meerman, F. Kuipers, T. Roskams, V. Desmet, and P. Jansen Liver pathology and hepatocarcinogenesis in a long-term mouse model of erythropoietic protoporphyria J Pathol 199 2003 191 200
114. J. Stephens, M. Cosyns, M. Jones, and A. Hayward Liver and bile duct pathology following Cryptosporidium parvum infection of immunodeficient mice Hepatology 30 1999 27 35
115. B.L. Ungar, J.A. Burris, C.A. Quinn, and F.D. Finkelman New mouse models for chronic Cryptosporidium infection in immunodeficient hosts Infect Immun 58 1990 961 969
116. J.R. Mead, M.J. Arrowood, R.W. Sidwell, and M.C. Healey Chronic Cryptosporidium parvum infections in congenitally immunodeficient SCID and nude mice J Infect Dis 163 1991 1297 1304
117. E.M. Ponnuraj, and A.R. Hayward Requirement for TNF-Tnfrsf1 signalling for sclerosing cholangitis in mice chronically infected by Cryptosporidium parvum Clin Exp Immunol 128 2002 416 420
118. J.M. Ward, M.R. Anver, D.C. Haines, and R.E. Benveniste Chronic active hepatitis in mice caused by Helicobacter hepaticus Am J Pathol 145 1994 959 968
119. P. Avenaud, B. Le Bail, K. Mayo, A. Marais, R. Fawaz, and P. Bioulac-Sage et al. Natural history of Helicobacter hepaticus infection in conventional A/J mice, with special reference to liver involvement Infect Immun 71 2003 3667 3672
120. P. Georgiev, W. Jochum, S. Heinrich, J.H. Jang, A. Nocito, and F. Dahm et al. Characterization of time-related changes after experimental bile duct ligation Br J Surg 95 2008 646 656
121. S.N. Lichtman, and R.B. Sartor Hepatobiliary injury associated with experimental small-bowel bacterial overgrowth in rats Immunol Res 10 1991 528 531
122. S. Yamada, M. Ishii, L.S. Liang, T. Yamamoto, and T. Toyota Small duct cholangitis induced by N-formyl L-methionine L-leucin L-tyrosine in rats J Gastroenterol 29 1994 631 636
123. S. Yamada, M. Ishii, N. Kisara, R. Nagatomi, and T. Toyota Macrophages are essential for lymphocyte infiltration in formyl peptide-induced cholangitis in rat liver Liver 19 1999 253 258
124. Y. Numata, S. Tazuma, T. Nishioka, Y. Ueno, and K. Chayama Immune response in mouse experimental cholangitis associated with colitis induced by dextran sulfate sodium J Gastroenterol Hepatol 19 2004 910 915
125. K. Tjandra, T. Le, and M.G. Swain Experimental colitis attenuates development of toxin-induced cholangitis in rats Dig Dis Sci 47 2002 1216 1223
126. A. Nonomura, N. Kono, H. Minato, and Y. Nakanuma Diffuse biliary tract involvement mimicking primary sclerosing cholangitis in an experimental model of chronic graft-vs.-host disease in mice Pathol Int 48 1998 421 427
127. T. Orth, M. Neurath, P. Schirmacher, U. Treichel, Meyer zum Büschenfelde, and W. Mayet Anti-neutrophil cytoplasmic antibodies in a rat model of trinitrobenzenesulphonic acid-induced liver injury Eur J Clin Invest 29 1999 929 939
128. M. Beaussier, D. Wendum, L. Fouassier, C. Rey, V. Barbu, and E. Lasnier et al. Adaptive bile duct proliferative response in experimental bile duct ischemia J Hepatol 42 2005 257 265
129. J. Buxbaum, P. Qian, C. Khuu, B.L. Shneider, D.I. Daikh, and M.E. Gershwin et al. Novel model of antigen-specific induction of bile duct injury Gastroenterology 131 2006 1899 1906
130. D. Seidel, I. Eickmeier, A.A. Kühl, A. Hamann, C. Loddenkemper, and E. Schott CD8 T cells primed in the gut-associated lymphoid tissue induce immune-mediated cholangitis in mice Hepatology 2013 10.1002/hep.26702