Transgenic mice expressing cyclooxygenase-2 in hepatocytes reveal a minor contribution of this enzyme to chemical hepatocarcinogenesis

American Journal of Pathology

Volumn 178, Issue 3, 2011, Pages 1361-1373

  Izquierdo, Cristina Llorente ^a   Mayoral, Rafael ^a,b   Flores, Juana María ^c   García Palencia, Pilar ^c   Cucarella, Carme ^d   Boscá, Lisardo ^a,b   Casado, Marta ^a,b,d   Martín Sanz, Paloma ^a,b  

^a INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

^d INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA ACTIN; COLLAGEN; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; GELATINASE B; PROSTAGLANDIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CELL CULTURE; CELL GROWTH; FEMALE; FIBROGENESIS; HEPATITIS; HUMAN; HUMAN CELL; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LIVER FIBROSIS; LIVER HISTOLOGY; LIVER INJURY; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; NUDE MOUSE; PATHOGENESIS; PRECANCER; PRIORITY JOURNAL; PROTEIN EXPRESSION; STELLATE CELL; TRANSGENIC MOUSE; WILD TYPE;

EID: 79952754473     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2010.11.074     Document Type: Article

References (44)

1. Llovet JM, Bruix J: Molecular targeted therapies in hepatocellular carcinoma. Hepatology 2008, 48:1312-1327
2. Maeda S, Kamata H, Luo JL, Leffert H, Karin M: IKKbeta couples hepatocyte death to cytokine-driven compensatory proliferation that promotes chemical hepatocarcinogenesis. Cell 2005, 121:977-990 (Pubitemid 40884391)
3. Simmons DL, Botting RM, Hla T: Cyclooxygenase isozymes: the biology of prostaglandin synthesis and inhibition. Pharmacol Rev 2004, 56:387-437 (Pubitemid 39096597)
4. Ledwith BJ, Pauley CJ, Wagner LK, Rokos CL, Alberts DW, Manam S: Induction of cyclooxygenase-2 expression by peroxisome proliferators and non-tetradecanoylphorbol 12,13-myristate-type tumor promoters in immortalized mouse liver cells. J Biol Chem 1997, 272:3707-3714 (Pubitemid 27067016)
5. Martín-Sanz P, Callejas NA, Casado M, Díaz-Guerra MJ, Boscá L: Expression of cyclooxygenase-2 in foetal rat hepatocytes stimulated with lipopolysaccharide and pro-inflammatory cytokines. Br J Pharmacol 1998, 125:1313-1319
6. Callejas NA, Boscá L, Williams CS, Du BR, Martín-Sanz P: Regulation of cyclooxygenase 2 expression in hepatocytes by CCAAT/enhancer- binding proteins. Gastroenterology 2000, 119:493-501 (Pubitemid 30621999)
7. Pham H, Eibl G, Vincenti R, Chong B, Tai HH, Slice LW: 15-Hydroxyprostaglandin dehydrogenase suppresses K-RasV12-dependent tumor formation in Nu/Nu mice. Mol Carcinog 2008, 47:466-477 (Pubitemid 351822305)
8. Casado M, Callejas NA, Rodrigo J, Zhao X, Dey SK, Boscá L, Martín-Sanz P: Contribution of cyclooxygenase 2 to liver regeneration after partial hepatectomy. FASEB J 2001, 15:2016-2018
9. Rudnick DA, Perlmutter DH, Muglia LJ: Prostaglandins are required for CREB activation and cellular proliferation during liver regeneration. Proc Natl Acad Sci USA 2001, 98:8885-8890 (Pubitemid 32678122)
10. Yamamoto H, Kondo M, Nakamori S, Nagano H, Wakasa K, Sugita Y, Chang-De J, Kobayashi S, Damdinsuren B, Dono K, Umeshita K, Sekimoto M, Sakon M, Matsuura N, Monden M: JTE-522, a cyclooxygenase-2 inhibitor, is an effective chemopreventive agent against rat experimental liver fibrosis1. Gastroenterology 2003, 125:556-571 (Pubitemid 36929437)
11. Kern MA, Haugg AM, Koch AF, Schilling T, Breuhahn K, Walczak H, Fleischer B, Trautwein C, Michalski C, Schulze-Bergkamen H, Friess H, Stremmel W, Krammer PH, Schirmacher P, Müller M: Cyclooxygenase-2 inhibition induces apoptosis signaling via death receptors and mitochondria in hepatocellular carcinoma. Cancer Res 2006, 66:7059-7066 (Pubitemid 44197682)
12. Mayoral R, Fernández-Martinez A, Boscá L, Martin-Sanz P: Prostaglandin E2 promotes migration and adhesion in hepatocellular carcinoma cells. Carcinogenesis 2005, 26:753-761 (Pubitemid 41214337)
13. Cheng AS, Yu J, Lai PB, Chan HL, Sung JJ: COX-2 mediates hepatitis B virus X protein abrogation of p53-induced apoptosis. Biochem Biophys Res Commun 2008, 374:175-180
14. Núñez O, Fernández-Martínez A, Majano PL, Apolinario A, Gómez-Gonzalo M, Benedicto I, López-Cabrera M, Boscá L, Clemente G, García-Monzón C, Martín-Sanz P: Increased intrahepatic cyclooxygenase 2, matrix metalloproteinase 2, and matrix metalloproteinase 9 expression is associated with progressive liver disease in chronic hepatitis C virus infection: role of viral core and NS5A proteins. Gut 2004, 53:1665-1672
15. Cusimano A, Fodera D, Lampiasi N, Azzolina A, Notarbartolo M, Giannitrapani L, D'Alessandro N, Montalto G, Cervello M: Prostaglandin E2 receptors and COX enzymes in human hepatocellular carcinoma: role in the regulation of cell growth. Ann N Y Acad Sci 2009, 1155:300-308
16. Cha YI, DuBois RN: NSAIDs and cancer prevention: targets down-stream of COX-2. Annu Rev Med 2007, 58:239-252 (Pubitemid 46706512)
17. Calvisi DF, Factor VM, Ladu S, Conner EA, Thorgeirsson SS: Disruption of beta-catenin pathway or genomic instability define two distinct categories of liver cancer in transgenic mice. Gastroenterology 2004, 126:1374-1386 (Pubitemid 38552801)
18. Luedde T, Beraza N, Kotsikoris V, van Loo G, Nenci A, De Vos R, Roskams T, Trautwein C, Pasparakis M: Deletion of NEMO/IKK-gamma in liver parenchymal cells causes steatohepatitis and hepatocellular carcinoma. Cancer Cell 2007, 11:119-132 (Pubitemid 46209851)
19. Pikarsky E, Porat RM, Stein I, Abramovitch R, Amit S, Kasem S, Gutkovich-Pyest E, Urieli-Shoval S, Galun E, Ben-Neriah Y: NF-kappaB functions as a tumour promoter in inflammation-associated cancer. Nature 2004, 431:461-466 (Pubitemid 39329586)
20. Haybaeck J, Zeller N, Wolf MJ, Weber A, Wagner U, Kurrer MO, Bremer J, Iezzi G, Graf R, Clavien PA, Thimme R, Blum H, Nedospasov SA, Zatloukal K, Ramzan M, Ciesek S, Pietschmann T, Marche PN, Karin M, Kopf M, Browning JL, Aguzzi A, Heikenwalder M: A lymphotoxin-driven pathway to hepatocellular carcinoma. Cancer Cell 2009, 16:295-308
21. Casado M, Mollá B, Roy R, Fernández-Martínez A, Cucarella C, Mayoral R, Boscá L, Martín-Sanz P: Protection against Fas-induced liver apoptosis in transgenic mice expressing cyclooxygenase 2 in hepatocytes. Hepatology 2007, 45:631-638 (Pubitemid 46450614)
22. Goldsworthy TL, Fransson-Steen R: Quantitation of the cancer process in C57BL/6J, B6C3F1 and C3H/HeJ mice. Toxicol Pathol 2002, 30:97-105
23. Kern MA, Schoneweiss MM, Sahi D, Bahlo M, Haugg AM, Kasper HU, Dienes HP, Kaferstein H, Breuhahn K, Schirmacher P: Cyclooxygenase-2 inhibitors suppress the growth of human hepatocellular carcinoma implants in nude mice. Carcinogenesis 2004, 25:1193-1199 (Pubitemid 38968047)
24. De la Cueva E, García-Cao I, Herranz M, López P, García-Palencia P, Flores JM, Serrano M, Fernández-Piqueras J, Martín-Caballero J. Tumorigenic activity of p21Waf1/Cip1 in thymic lymphoma. Oncogene 2006, 25:4128-4132 (Pubitemid 44024876)
25. Freeman JE, Stirling D, Russell AL, Wolf CR: cDNA sequence, deduced amino acid sequence, predicted gene structure and chemical regulation of mouse Cyp2e1. Biochem J 1992, 281:689-695
26. Martín-Sanz P, Mayoral R, Casado M, Boscá L: COX-2 in liver, from regeneration to hepatocarcinogenesis: what we have learned from animal models? World J Gastroenterol 2010, 16:1430-1435
27. Mayoral R, Mollá B, Flores JM, Boscá L, Casado M, Martín-Sanz P: Constitutive expression of cyclo-oxygenase 2 transgene in hepatocytes protects against liver injury. Biochem J 2008, 416:337-346
28. Yu J, Hui AY, Chu ES, Cheng AS, Go MY, Chan HL, Leung WK, Cheung KF, Ching AK, Chui YL, Chan KK, Sung JJ: Expression of a cyclo-oxygenase-2 transgene in murine liver causes hepatitis. Gut 2007, 56:991-999 (Pubitemid 46999086)
29. Han C, Li G, Lim K, DeFrances MC, Gandhi CR, Wu T: Transgenic expression of cyclooxygenase-2 in hepatocytes accelerates endotoxin-induced acute liver failure. J Immunol 2008, 181:8027-8035
30. Li G, Han C, Xu L, Lim K, Isse K, Wu T: Cyclooxygenase-2 prevents fas-induced liver injury through up-regulation of epidermal growth factor receptor. Hepatology 2009, 50:834-843
31. Hui AY, Leung WK, Chan HL, Chan FK, Go MY, Chan KK, Tang BD, Chu ES, Sung JJ: Effect of celecoxib on experimental liver fibrosis in rat. Liver Int 2006, 26:125-136
32. Paik YH, Kim JK, Lee JI, Kang SH, Kim DY, An SH, Lee SJ, Lee DK, Han KH, Chon CY, Lee SI, Lee KS, Brenner DA: Celecoxib induces hepatic stellate cell apoptosis through inhibition of Akt activation and suppresses hepatic fibrosis in rats. Gut 2009, 58:1517-1527
33. Yu J, Wu CW, Chu ES, Hui AY, Cheng AS, Go MY, Ching AK, Chui YL, Chan HL, Sung JJ: Elucidation of the role of COX-2 in liver fibrogenesis using transgenic mice. Biochem Biophys Res Commun 2008, 372:571-577
34. Choi EM, Kim SR, Lee EJ, Han JA: Cyclooxygenase-2 functionally inactivates p53 through a physical interaction with p53. Biochim Biophys Acta 2009, 1793:1354-1365
35. Fernández-Martínez A, Mollá B, Mayoral R, Boscá L, Casado M, Martín-Sanz P: Cyclo-oxygenase 2 expression impairs serum-withdrawal- induced apoptosis in liver cells. Biochem J 2006, 398:371-380
36. Sakurai T, He G, Matsuzawa A, Yu GY, Maeda S, Hardiman G, Karin M: Hepatocyte necrosis induced by oxidative stress and IL-1 alpha release mediate carcinogen-induced compensatory proliferation and liver tumorigenesis. Cancer Cell 2008, 14:156-165
37. Schwabe RF, Bradham CA, Uehara T, Hatano E, Bennett BL, Schoonhoven R, Brenner DA: c-Jun-N-terminal kinase drives cyclin D1 expression and proliferation during liver regeneration. Hepatology 2003, 37:824-832 (Pubitemid 36397393)
38. Sakurai T, Maeda S, Chang L, Karin M: Loss of hepatic NF-kappa B activity enhances chemical hepatocarcinogenesis through sustained c-Jun N-terminal kinase 1 activation. Proc Natl Acad Sci USA 2006, 103:10544-10551 (Pubitemid 44078014)
39. Tanabe T, Tohnai N: Cyclooxygenase isozymes and their gene structures and expression. Prostaglandins Other Lipid Mediat 2002, 68-69:95-114. (Pubitemid 35247390)
40. Kim YM, Park SY, Pyo H: Cyclooxygenase-2 (COX-2) negatively regulates expression of epidermal growth factor receptor and causes resistance to gefitinib in COX-2-overexpressing cancer cells. Mol Cancer Res 2009, 7:1367-1377
41. He G, Yu GY, Temkin V, Ogata H, Kuntzen C, Sakurai T, Sieghart W, Peck-Radosavljevic M, Leffert HL, Karin M: Hepatocyte IKKbeta/NF-kappaB inhibits tumor promotion and progression by preventing oxidative stress-driven STAT3 activation. Cancer Cell 2010, 17:286-297
42. Trikha M, Corringham R, Klein B, Rossi JF: Targeted anti-interleukin-6 monoclonal antibody therapy for cancer: a review of the rationale and clinical evidence. Clin Cancer Res 2003, 9:4653-4665 (Pubitemid 37323267)
43. Han C, Demetris AJ, Stolz DB, Xu L, Lim K, Wu T: Modulation of Stat3 activation by the cytosolic phospholipase A2alpha and cyclooxygenase-2- controlled prostaglandin E2 signaling pathway. J Biol Chem 2006, 281:24831-24846 (Pubitemid 44274256)
44. Schulze-Bergkamen H, Brenner D, Krueger A, Suess D, Fas SC, Frey CR, Dax A, Zink D, Büchler P, Müller M, Krammer PH: Hepatocyte growth factor induces Mcl-1 in primary human hepatocytes and inhibits CD95-mediated apoptosis via Akt. Hepatology 2004, 39:645-654 (Pubitemid 38337644)