Depletion of apoptosis signal-regulating kinase 1 prevents bile duct ligation-induced necroinflammation and subsequent peribiliary fibrosis

American Journal of Pathology

Volumn 184, Issue 3, 2014, Pages 644-661

  Noguchi, Hirotsugu ^a   Yamada, Sohsuke ^a   Nabeshima, Atsunori ^a   Guo, Xin ^a   Tanimoto, Akihide ^b   Wang, Ke Yong ^a   Kitada, Shohei ^a   Tasaki, Takashi ^a   Takama, Tatsuo ^a   Shimajiri, Shohei ^a   Horlad, Hasita ^c   Komohara, Yoshihiro ^c   Izumi, Hiroto ^a   Kohno, Kimitoshi ^a   Ichijo, Hidenori ^d   Sasaguri, Yasuyuki ^a  

^a UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

^b KAGOSHIMA UNIVERSITY   (Japan)

^c KUMAMOTO UNIVERSITY   (Japan)

^d UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; MAP3K5 PROTEIN, MOUSE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE;

ANIMAL; APOPTOSIS; BILE DUCT; C57BL MOUSE; CELL PROLIFERATION; CHOLESTASIS; GENE DELETION; GENETICS; INFLAMMATION; LIVER; LIVER CELL; LIVER CIRRHOSIS; MALE; METABOLISM; MOUSE; PATHOLOGY; PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; BILE DUCTS; CELL PROLIFERATION; CHOLESTASIS; HEPATOCYTES; INFLAMMATION; LIVER; LIVER CIRRHOSIS; MALE; MAP KINASE KINASE KINASE 5; MAP KINASE KINASE KINASES; MICE; MICE, INBRED C57BL; PHOSPHORYLATION; SEQUENCE DELETION; SIGNAL TRANSDUCTION;

EID: 84894146670     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.11.030     Document Type: Article

References (42)

1. H. Miyoshi, C. Rust, P.J. Roberts, L.J. Burgart, and G.J. Gores Hepatocyte apoptosis after bile duct ligation in the mouse involves Fas Gastroenterology 117 1999 669 677 (Pubitemid 29409254)
2. A. Canbay, H. Higuchi, S.F. Bronk, M. Taniai, T.J. Sebo, and G.J. Gores Fas enhances fibrogenesis in the bile duct ligated mouse: a link between apoptosis and fibrosis Gastroenterology 123 2002 1323 1330
3. J.H. Yoon, and G.J. Gores Death receptor-mediated apoptosis and the liver J Hepatol 37 2002 400 410 (Pubitemid 34969958)
4. A. Canbay, P. Taimr, N. Torok, H. Higuchi, S. Friedman, and G.J. Gores Apoptotic body engulfment by a human stellate cell line is profibrogenic Lab Invest 83 2003 655 663 (Pubitemid 36618044)
5. M.H. Schoemaker, W.M. Gommans, L. Conde de la Rosa, M. Homan, P. Klok, C. Trautwein, H. van Goor, K. Poelstra, H.J. Haisma, P.L. Jansen, and H. Moshage Resistance of rat hepatocytes against bile acid-induced apoptosis in cholestatic liver injury is due to nuclear factor-kappa B activation J Hepatol 39 2003 153 161 (Pubitemid 36920549)
6. J.S. Gujral, J. Liu, A. Farhood, and H. Jaeschke Reduced oncotic necrosis in Fas receptor-deficient C57BL/6J-lpr mice after bile duct ligation Hepatology 40 2004 998 1007 (Pubitemid 39288134)
7. P. Fickert, M. Trauner, A. Fuchsbichler, G. Zollner, M. Wagner, H.U. Marschall, K. Zatloukal, and H. Denk Oncosis represents the main type of cell death in mouse models of cholestasis J Hepatol 42 2005 378 385 (Pubitemid 40254253)
8. P.D. Nalapareddy, S. Schüngel, J.Y. Hong, M.P. Manns, H. Jaeschke, and A. Vogel The BH3-only protein bid does not mediate death-receptor-induced liver injury in obstructive cholestasis Am J Pathol 175 2009 1077 1085
9. C. Mitchell, M. Mahrouf-Yorgov, A. Mayeuf, M.A. Robin, A. Mansouri, B. Fromenty, and H. Gilgenkrantz Overexpression of Bcl-2 in hepatocytes protects against injury but does not attenuate fibrosis in a mouse model of chronic cholestatic liver disease Lab Invest 91 2011 273 282
10. K.N. Lazaridis, M. Strazzabosco, and N.F. Larusso The cholangiopathies: disorders of biliary epithelia Gastroenterology 127 2004 1565 1577 (Pubitemid 39457780)
11. K. Yahagi, M. Ishii, K. Kobayashi, Y. Ueno, Y. Mano, H. Niitsuma, T. Igarashi, and T. Toyota Primary culture of cholangiocytes from normal mouse liver In Vitro Cell Dev Biol Anim 34 1998 512 514 (Pubitemid 29071747)
12. G. Alpini, S. Glaser, Y. Ueno, L. Pham, P.V. Podila, A. Caligiuri, G. LeSage, and N.F. LaRusso Heterogeneity of the proliferative capacity of rat cholangiocytes after bile duct ligation Am J Physiol Gastrointest Liver Physiol 274 1998 G767 G775
13. G. LeSage, S. Glaser, L. Marucci, A. Benedetti, J.L. Phinizy, R. Rodgers, A. Caligiuri, E. Papa, Z. Tretjak, A.M. Jezequel, L.A. Holcomb, and G. Alpini Acute carbon tetrachloride feeding induces damage of large but not small cholangiocytes from BDL rat liver Am J Physiol Gastrointest Liver Physiol 276 1999 G1289 G1301 (Pubitemid 29251929)
14. S. Glaser, E. Gaudio, A. Rao, L.M. Pierce, P. Onori, A. Franchitto, H.L. Francis, D.E. Dostal, J.K. Venter, S. DeMorrow, R. Mancinelli, G. Carpino, D. Alvaro, S.E. Kopriva, J.M. Savage, and G. Alpini Morphological and functional heterogeneity of the mouse intrahepatic biliary epithelium Lab Invest 89 2009 456 469
15. H. Ichijo, E. Nishida, K. Irie, P.T. Digike, M. Saitoh, T. Moriguchi, M. Takagi, K. Matsumoto, K. Miyazono, and Y. Gotoh Induction of apoptosis by ASK1, mammalian MAPKKK that activates SAPK/JNK and p38 signaling pathways Science 275 1997 90 94 (Pubitemid 27020316)
16. K. Tobiume, A. Matsuzawa, T. Takahashi, H. Nishitoh, K. Morita, K. Takeda, O. Minowa, K. Miyazono, T. Noda, and H. Ichijo ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis EMBO Rep 2 2001 222 228 (Pubitemid 32273301)
17. S. Yamada, Y. Ding, A. Tanimoto, K.Y. Wang, X. Guo, Z. Li, T. Tasaki, A. Nabesima, Y. Murata, S. Shimajiri, K. Kohno, H. Ichijo, and Y. Sasaguri Apoptosis signal-regulating kinase 1 deficiency accelerates hyperlipidemia- induced atheromatous plaques via suppression of macrophage apoptosis Arterioscler Thromb Vasc Biol 31 2011 1555 1564
18. T. Watanabe, K. Otsu, T. Takeda, O. Yamaguchi, S. Hikoso, K. Kashiwase, Y. Higuchi, M. Taniike, A. Nakai, Y. Matsumura, K. Nishida, H. Ichijo, and M. Hori Apoptosis signal-regulating kinase 1 is involved not only in apoptosis but also in non-apoptotic cardiomyocyte death Biochem Biophys Res Commun 333 2005 562 567 (Pubitemid 40848328)
19. Q. Liu, M.A. Sargent, A.J. York, and J.D. Molkentin ASK1 regulates cardiomyocyte death but not hypertrophy in transgenic mice Circ Res 105 2009 1110 1117
20. T. Tasaki, S. Yamada, X. Guo, A. Tanimoto, K.Y. Wang, A. Nabeshima, S. Kitada, H. Noguchi, S. Kimura, S. Shimajiri, K. Kohno, H. Ichijo, and Y. Sasaguri Apoptosis signal-regulating kinase 1 deficiency attenuates vascular injury-induced neointimal hyperplasia by suppressing apoptosis in smooth muscle cells Am J Pathol 182 2013 597 609
21. P.S. Makena, V.K. Gorantla, M.C. Ghosh, L. Bezawada, K. Kandasamy, L. Balazs, C.L. Luellen, K.E. Thompson, K. Parthasarathi, H. Ichijo, C.M. Waters, and S.E. Sinclair Deletion of apoptosis signal-regulating kinase-1 prevents ventilator-induced lung injury in mice Am J Respir Cell Mol Biol 46 2012 461 469
22. S. Yamada, K.Y. Wang, A. Tanimoto, J. Fan, S. Shimajiri, S. Kitajima, M. Morimoto, M. Tsutui, T. Watanabe, K. Yasumoto, and Y. Sasaguri Matrix metalloproteinase 12 accelerates the initiation of atherosclerosis and stimulates the progression of fatty streaks to fibrous plaques in transgenic rabbits Am J Pathol 172 2008 1419 1429 (Pubitemid 351671554)
23. Y. Ding, S. Yamada, K.Y. Wang, S. Shimajiri, X. Guo, A. Tanimoto, Y. Murata, S. Kitajima, T. Watanabe, H. Izumi, K. Kohno, and Y. Sasaguri Overexpression of peroxiredoxin 4 protects against high-dose streptozotocin-induced diabetes by suppressing oxidative stress and cytokines in transgenic mice Antioxid Redox Signal 13 2010 1477 1490
24. X. Guo, S. Yamada, A. Tanimoto, Y. Ding, K.Y. Wang, S. Shimajiri, Y. Murata, S. Kimura, T. Tasaki, A. Nabeshima, T. Watanabe, K. Kohno, and Y. Sasaguri Overexpression of peroxiredoxin 4 attenuates atherosclerosis in apolipoprotein E knockout mice Antioxid Redox Signal 17 2012 1362 1375
25. A. Nabeshima, S. Yamada, X. Guo, A. Tanimoto, K.Y. Wang, S. Shimajiri, S. Kimura, T. Tasaki, H. Noguchi, S. Kitada, T. Watanabe, J. Fujii, K. Kohno, and Y. Sasaguri Peroxiredoxin 4 protects against nonalcoholic steatohepatitis and type 2 diabetes in a nongenetic mouse model Antioxid Redox Signal 19 2013 1983 1998
26. R. Mancinelli, A. Franchitto, E. Gaudio, P. Onori, S. Glaser, H. Francis, J. Venter, S. Demorrow, G. Carpino, S. Kopriva, M. White, G. Fava, D. Alvaro, and G. Alpini After damage of large bile ducts by gamma-aminobutyric acid, small ducts replenish the biliary tree by amplification of calcium-dependent signaling and de novo acquisition of large cholangiocyte phenotypes Am J Pathol 176 2010 1790 1800
27. H. Horlad, Y. Fujiwara, K. Takemura, K. Ohnishi, T. Ikeda, H. Tsukamoto, H. Mizuta, Y. Nishimura, M. Takeya, and Y. Komohara Corosolic acid impairs tumor development and lung metastasis by inhibiting the immunosuppressive activity of myeloid-derived suppressor cells Mol Nutr Food Res 57 2013 1046 1054
28. J.S. Gujral, A. Farhood, M.L. Bajt, and H. Jaeschke Neutrophils aggravate acute liver injury during obstructive cholestasis in bile duct-ligated mice Hepatology 38 2003 355 363 (Pubitemid 36919856)
29. N. Kinnman, C. Francoz, V. Barbu, D. Wendum, C. Rey, R. Hultcrantz, R. Poupon, and C. Housset The myofibroblastic conversion of peribiliary fibrogenic cells distinct from hepatic stellate cells is stimulated by platelet-derived growth factor during liver fibrogenesis Lab Invest 83 2003 163 173 (Pubitemid 36255362)
30. K.Y. Wang, A. Tanimoto, S. Yamada, X. Guo, Y. Ding, T. Watanabe, T. Watanabe, K. Kohno, K. Hirano, H. Tsukada, and Y. Sasaguri Histamine regulation in glucose and lipid metabolism via histamine receptors: model for nonalcoholic steatohepatitis in mice Am J Pathol 177 2010 713 723
31. Y. Yasuniwa, H. Izumi, K.Y. Wang, S. Shimajiri, Y. Sasaguri, K. Kawai, H. Kasai, T. Shimada, K. Miyake, E. Kashiwagi, G. Hirano, A. Kidani, M. Akiyama, B. Han, Y. Wu, and I. Ieiri Circadian disruption accelerates tumor growth and angio/stromagenesis through a Wnt signaling pathway PLoS One 5 2010 e15330
32. B.L. Woolbright, and H. Jaeschke Novel insight into mechanisms of cholestatic liver injury World J Gastroenterol 18 2012 4985 4993
33. S.A. Gradilone, A.I. Masyuk, P.L. Splinter, J.M. Banales, B.Q. Huang, P.S. Tietz, T.V. Masyuk, and N.F. Larusso Cholangiocyte cilia express TRPV4 and detect changes in luminal tonicity inducing bicarbonate secretion Proc Natl Acad Sci U S A 104 2007 19138 19143
34. P. Georgiev, W. Jochum, S. Heinrich, J.H. Jang, A. Nocito, F. Dahm, and P.A. Clavien Characterization of time-related changes after experimental bile duct ligation Br J Surg 95 2008 646 656
35. B. Grasl-Kraupp, B. Ruttkay-Nedecky, H. Koudelka, K. Bukowska, W. Bursch, and R. Schulte-Hermann In situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death: a cautionary note Hepatology 21 1995 1465 1468
36. J. Da Silva, B. Pierrat, J.L. Mary, and W. Lesslauer Blockade of p38 mitogen-activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes J Biol Chem 272 1997 28373 28380 (Pubitemid 27517783)
37. A.M. Badger, M.N. Cook, M.W. Lark, T.M. Newman-Tarr, B.A. Swift, A.H. Nelson, F.C. Barone, and S. Kumar SB 203580 inhibits p38 mitogen-activated protein kinase, nitric oxide production, and inducible nitric oxide synthase in bovine cartilage-derived chondrocytes J Immunol 161 1998 467 473 (Pubitemid 28285556)
38. H. Bai, N. Zhang, Y. Xu, Q. Chen, M. Khan, J.J. Potter, S.K. Nayar, T. Cornish, G. Alpini, S. Bronk, D. Pan, and R.A. Anders Yes-associated protein regulates the hepatic response after bile duct ligation Hepatology 56 2012 1097 1107
39. R.F. Schwabe, C.A. Bradham, T. Uehara, E. Hatano, B.L. Bennett, R. Schoonhoven, and D.A. Brenner c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration Hepatology 37 2003 824 832 (Pubitemid 36397393)
40. T. Cantz, M.P. Manns, and M. Ott Stem cells in liver regeneration and therapy Cell Tissue Res 331 2008 271 282 (Pubitemid 350265492)
41. K. Hayashi, M. Takahashi, K. Kimura, W. Nishida, H. Saga, and K. Sobue Changes in the balance of phosphoinositide 3-kinase/protein kinase B (Akt) and the mitogen-activated protein kinases (ERK/p38 MAPK) determine a phenotype of visceral and vascular smooth muscle cells J Cell Biol 145 1999 727 740 (Pubitemid 29240851)
42. P. Lefebvre, B. Cariou, F. Lien, F. Kuipers, and B. Staels Role of bile acids and bile acid receptors in metabolic regulation Physiol Rev 89 2009 147 191 Technology Technology Technology