Inhibition of Cyclic Adenosine Monophosphate (cAMP)-response Element-binding Protein (CREB)-binding Protein (CBP)/β-Catenin Reduces Liver Fibrosis in Mice

EBioMedicine

Volumn 2, Issue 11, 2015, Pages 1751-1758

  Osawa, Yosuke ^a   Oboki, Keisuke ^b   Imamura, Jun ^a   Kojika, Ekumi ^a   Hayashi, Yukiko ^a   Hishima, Tsunekazu ^a   Saibara, Toshiji ^c   Shibasaki, Futoshi ^b   Kohara, Michinori ^b   Kimura, Kiminori ^a  

^a TOKYO METROPOLITAN KOMAGOME HOSPITAL   (Japan)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^c KOCHI MEDICAL SCHOOL   (Japan)

Author keywords

Beta catenin; Fibrosis; Hepatic stellate cell; Liver; Macrophage

Indexed keywords

ANTIFIBROTIC AGENT; BETA CATENIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GELATINASE A; GELATINASE B; NEUTROPHIL COLLAGENASE; PRI 724; SURVIVIN; UNCLASSIFIED DRUG; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BILE DUCT LIGATION; CELL DEATH; CELL VIABILITY; CONTROLLED STUDY; ENZYME INHIBITION; FLUORESCENCE ACTIVATED CELL SORTING; HISTOLOGY; LIVER FIBROSIS; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; WESTERN BLOTTING; ZYMOGRAPHY; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE MODEL; DRUG EFFECTS; HEPATIC STELLATE CELL; LIVER CIRRHOSIS; MACROPHAGE; METABOLISM; PATHOLOGY;

ANIMALS; BETA CATENIN; CELL DEATH; CREB-BINDING PROTEIN; DISEASE MODELS, ANIMAL; HEPATIC STELLATE CELLS; LIVER CIRRHOSIS; MACROPHAGES; MALE; MICE; SIGNAL TRANSDUCTION;

EID: 84958903782     PISSN: None     EISSN: 23523964     Source Type: Journal    
DOI: 10.1016/j.ebiom.2015.10.010     Document Type: Article

References (47)

1. Akhmetshina A., Palumbo K., Dees C., Bergmann C., Venalis P., Zerr P., Horn A., Kireva T., Beyer C., Zwerina J., Schneider H., Sadowski A., Riener M.O., Macdougald O.A., Distler O., Schett G., Distler J.H. Activation of canonical Wnt signalling is required for TGF-beta-mediated fibrosis. Nat. Commun. 2012, 3:735.
2. Amini-Nik S., Cambridge E., Yu W., Guo A., Whetstone H., Nadesan P., Poon R., Hinz B., Alman B.A. Beta-catenin-regulated myeloid cell adhesion and migration determine wound healing. J. Clin. Invest. 2014, 124:2599-2610.
3. Bataller R., Brenner D.A. Hepatic stellate cells as a target for the treatment of liver fibrosis. Semin. Liver Dis. 2001, 21:437-451.
4. Bataller R., Brenner D.A. Liver fibrosis. J. Clin. Invest. 2005, 115:209-218.
5. Beers M.F., Morrisey E.E. The three R's of lung health and disease: repair, remodeling, and regeneration. J. Clin. Invest. 2011, 121:2065-2073.
6. Chen L., Li J., Zhang J., Dai C., Liu X., Wang J., Gao Z., Guo H., Wang R., Lu S., Wang F., Zhang H., Chen H., Fan X., Wang S., Qin Z. S100A4 promotes liver fibrosis via activation of hepatic stellate cells. J. Hepatol. 2015, 62:156-164.
7. Cheng J.H., She H., Han Y.P., Wang J., Xiong S., Asahina K., Tsukamoto H. Wnt antagonism inhibits hepatic stellate cell activation and liver fibrosis. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294:G39-G49.
8. Cheon S.S., Cheah A.Y., Turley S., Nadesan P., Poon R., Clevers H., Alman B.A. Beta-catenin stabilization dysregulates mesenchymal cell proliferation, motility, and invasiveness and causes aggressive fibromatosis and hyperplastic cutaneous wounds. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:6973-6978.
9. Chilosi M., Poletti V., Zamo A., Lestani M., Montagna L., Piccoli P., Pedron S., Bertaso M., Scarpa A., Murer B., Cancellieri A., Maestro R., Semenzato G., Doglioni C. Aberrant Wnt/beta-catenin pathway activation in idiopathic pulmonary fibrosis. Am. J. Pathol. 2003, 162:1495-1502.
10. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006, 127:469-480.
11. Dees C., Distler J.H. Canonical Wnt signalling as a key regulator of fibrogenesis - implications for targeted therapies?. Exp. Dermatol. 2013, 22:710-713.
12. Duffield J.S., Forbes S.J., Constandinou C.M., Clay S., Partolina M., Vuthoori S., Wu S., Lang R., Iredale J.P. Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair. J. Clin. Invest. 2005, 115:56-65.
13. Friedman S.L. Molecular regulation of hepatic fibrosis, an integrated cellular response to tissue injury. J. Biol. Chem. 2000, 275:2247-2250.
14. Friedman S.L. Mac the knife? Macrophages - the double-edged sword of hepatic fibrosis. J. Clin. Invest. 2005, 115:29-32.
15. Hao S., He W., Li Y., Ding H., Hou Y., Nie J., Hou F.F., Kahn M., Liu Y. Targeted inhibition of beta-catenin/CBP signaling ameliorates renal interstitial fibrosis. J. Am. Soc. Nephrol. 2011, 22:1642-1653.
16. Harty M.W., Papa E.F., Huddleston H.M., Young E., Nazareth S., Riley C.A., Ramm G.A., Gregory S.H., Tracy T.F. Hepatic macrophages promote the neutrophil-dependent resolution of fibrosis in repairing cholestatic rat livers. Surgery 2008, 143:667-678.
17. Hecht A., Vleminckx K., Stemmler M.P., Van Roy F., Kemler R. The p300/CBP acetyltransferases function as transcriptional coactivators of beta-catenin in vertebrates. EMBO J. 2000, 19:1839-1850.
18. Henderson W.R., Chi E.Y., Ye X., Nguyen C., Tien Y.T., Zhou B., Borok Z., Knight D.A., Kahn M. Inhibition of Wnt/beta-catenin/CREB binding protein (CBP) signaling reverses pulmonary fibrosis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:14309-14314.
19. Huang W.C., Sala-Newby G.B., Susana A., Johnson J.L., Newby A.C. Classical macrophage activation up-regulates several matrix metalloproteinases through mitogen activated protein kinases and nuclear factor-kappaB. PLoS One 2012, 7.
20. Iimuro Y., Brenner D.A. Matrix metalloproteinase gene delivery for liver fibrosis. Pharm. Res. 2008, 25:249-258.
21. Iredale J.P., Benyon R.C., Pickering J., Mccullen M., Northrop M., Pawley S., Hovell C., Arthur M.J. Mechanisms of spontaneous resolution of rat liver fibrosis. Hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors. J. Clin. Invest. 1998, 102:538-549.
22. Issa R., Williams E., Trim N., Kendall T., Arthur M.J., Reichen J., Benyon R.C., Iredale J.P. Apoptosis of hepatic stellate cells: involvement in resolution of biliary fibrosis and regulation by soluble growth factors. Gut 2001, 48:548-557.
23. Kim M.H., Albertsson P., Xue Y., Nannmark U., Kitson R.P., Goldfarb R.H. Expression of neutrophil collagenase (MMP-8) in Jurkat T leukemia cells and its role in invasion. Anticancer Res. 2001, 21:45-50.
24. Kimura K., Sekiguchi S., Hayashi S., Hayashi Y., Hishima T., Nagaki M., Kohara M. Role of interleukin-18 in intrahepatic inflammatory cell recruitment in acute liver injury. J. Leukoc. Biol. 2011, 89:433-442.
25. Lenz H.J., Kahn M. Safely targeting cancer stem cells via selective catenin coactivator antagonism. Cancer Sci. 2014, 105:1087-1092.
26. Monga S.P. Role of Wnt/beta-catenin signaling in liver metabolism and cancer. Int. J. Biochem. Cell Biol. 2011, 43:1021-1029.
27. Osawa Y., Hoshi M., Yasuda I., Saibara T., Moriwaki H., Kozawa O. Tumor necrosis factor-alpha promotes cholestasis-induced liver fibrosis in the mouse through tissue inhibitor of metalloproteinase-1 production in hepatic stellate cells. PLoS One 2013, 8.
28. Osawa Y., Seki E., Adachi M., Suetsugu A., Ito H., Moriwaki H., Seishima M., Nagaki M. Role of acid sphingomyelinase of Kupffer cells in cholestatic liver injury in mice. Hepatology 2010, 51:237-245.
29. Osawa Y., Seki E., Adachi M., Taura K., Kodama Y., Siegmund S.V., Schwabe R.F., Brenner D.A. Systemic mediators induce fibrogenic effects in normal liver after partial bile duct ligation. Liver Int. 2006, 26:1138-1147.
30. Osawa Y., Suetsugu A., Matsushima-Nishiwaki R., Yasuda I., Saibara T., Moriwaki H., Seishima M., Kozawa O. Liver acid sphingomyelinase inhibits growth of metastatic colon cancer. J. Clin. Invest. 2013, 123:834-843.
31. Pellicoro A., Ramachandran P., Iredale J.P., Fallowfield J.A. Liver fibrosis and repair: immune regulation of wound healing in a solid organ. Nat. Rev. Immunol. 2014, 14:181-194.
32. Pesce J.T., Ramalingam T.R., Mentink-Kane M.M., Wilson M.S., El Kasmi K.C., Smith A.M., Thompson R.W., Cheever A.W., Murray P.J., Wynn T.A. Arginase-1-expressing macrophages suppress Th2 cytokine-driven inflammation and fibrosis. PLoS Pathog. 2009, 5.
33. Prikk K., Maisi P., Pirila E., Reintam M.A., Salo T., Sorsa T., Sepper R. Airway obstruction correlates with collagenase-2 (MMP-8) expression and activation in bronchial asthma. Lab. Investig. 2002, 82:1535-1545.
34. Ramachandran P., Pellicoro A., Vernon M.A., Boulter L., Aucott R.L., Ali A., Hartland S.N., Snowdon V.K., Cappon A., Gordon-Walker T.T., Williams M.J., Dunbar D.R., Manning J.R., Van Rooijen N., Fallowfield J.A., Forbes S.J., Iredale J.P. Differential Ly-6C expression identifies the recruited macrophage phenotype, which orchestrates the regression of murine liver fibrosis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E3186-E3195.
35. Santer F.R., Hoschele P.P., Oh S.J., Erb H.H., Bouchal J., Cavarretta I.T., Parson W., Meyers D.J., Cole P.A., Culig Z. Inhibition of the acetyltransferases p300 and CBP reveals a targetable function for p300 in the survival and invasion pathways of prostate cancer cell lines. Mol. Cancer Ther. 2011, 10:1644-1655.
36. Shapiro S.D., Kobayashi D.K., Pentland A.P., Welgus H.G. Induction of macrophage metalloproteinases by extracellular matrix. Evidence for enzyme- and substrate-specific responses involving prostaglandin-dependent mechanisms. J. Biol. Chem. 1993, 268:8170-8175.
37. Sisson T.H., Maher T.M., Ajayi I.O., King J.E., Higgins P.D., Booth A.J., Sagana R.L., Huang S.K., White E.S., Moore B.B., Horowitz J.C. Increased survivin expression contributes to apoptosis-resistance in IPF fibroblasts. Adv. Biosci. Biotechnol. 2012, 3:657-664.
38. Song E., Ouyang N., Horbelt M., Antus B., Wang M., Exton M.S. Influence of alternatively and classically activated macrophages on fibrogenic activities of human fibroblasts. Cell. Immunol. 2000, 204:19-28.
39. Takemaru K.I., Moon R.T. The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J. Cell Biol. 2000, 149:249-254.
40. Teo J.L., Kahn M. The Wnt signaling pathway in cellular proliferation and differentiation: A tale of two coactivators. Adv. Drug Deliv. Rev. 2010, 62:1149-1155.
41. Troeger J.S., Mederacke I., Gwak G.Y., Dapito D.H., Mu X., Hsu C.C., Pradere J.P., Friedman R.A., Schwabe R.F. Deactivation of hepatic stellate cells during liver fibrosis resolution in mice. Gastroenterology 2012, 143:1073-1083.
42. Wahlgren J., Maisi P., Sorsa T., Sutinen M., Tervahartiala T., Pirila E., Teronen O., Hietanen J., Tjaderhane L., Salo T. Expression and induction of collagenases (MMP-8 and -13) in plasma cells associated with bone-destructive lesions. J. Pathol. 2001, 194:217-224.
43. Wells R.G. The portal fibroblast: not just a poor man's stellate cell. Gastroenterology 2014, 147:41-47.
44. Wick G., Grundtman C., Mayerl C., Wimpissinger T.F., Feichtinger J., Zelger B., Sgonc R., Wolfram D. The immunology of fibrosis. Annu. Rev. Immunol. 2013, 31:107-135.
45. Wielockx B., Lannoy K., Shapiro S.D., Itoh T., Itohara S., Vandekerckhove J., Libert C. Inhibition of matrix metalloproteinases blocks lethal hepatitis and apoptosis induced by tumor necrosis factor and allows safe antitumor therapy. Nat. Med. 2001, 7:1202-1208.
46. Wright M.C., Issa R., Smart D.E., Trim N., Murray G.I., Primrose J.N., Arthur M.J., Iredale J.P., Mann D.A. Gliotoxin stimulates the apoptosis of human and rat hepatic stellate cells and enhances the resolution of liver fibrosis in rats. Gastroenterology 2001, 121:685-698.
47. Wynn T.A., Ramalingam T.R. Mechanisms of fibrosis: therapeutic translation for fibrotic disease. Nat. Med. 2012, 18:1028-1040.