Sorafenib treatment during partial hepatectomy reduces tumorgenesis in an inflammation-associated liver cancer model

Oncotarget

Volumn 7, Issue 4, 2016, Pages 4860-4870

  Zahavi, Tamar ^a   Lanton, Tali ^a   Divon, Mali Salmon ^b   Salmon, Asher ^a   Peretz, Tamar ^a   Galun, Eithan ^a   Axelrod, Jonathan H ^a   Sonnenblick, Amir ^a  

^a HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^b ARIEL UNIVERSITY   (Israel)

Author keywords

Hepatectomy; Liver cancer; Mdr2 knockout; Sorafenib; Stellate cells

Indexed keywords

SORAFENIB; ANTINEOPLASTIC AGENT; CARBANILAMIDE DERIVATIVE; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN; NICOTINAMIDE; P-GLYCOPROTEIN 2;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER MODEL; CELL ACTIVATION; CHRONIC HEPATITIS; CONTROLLED STUDY; DNA REPAIR; DRUG EFFICACY; DRUG SAFETY; LIVER CANCER; LIVER CARCINOGENESIS; LIVER FIBROSIS; LIVER REGENERATION; MOUSE; NONHUMAN; PARTIAL HEPATECTOMY; SHORT COURSE THERAPY; SIGNAL TRANSDUCTION; STELLATE CELL; ANALOGS AND DERIVATIVES; ANIMAL; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELL TRANSFORMATION; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; ENZYME IMMUNOASSAY; GENETICS; HEPATITIS; INFLAMMATION; KNOCKOUT MOUSE; LIVER NEOPLASMS; LIVER RESECTION; PATHOLOGY; PHYSIOLOGY; PROTEIN MICROARRAY; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; HEPATECTOMY; HEPATITIS; IMMUNOENZYME TECHNIQUES; INFLAMMATION; LIVER NEOPLASMS; LIVER REGENERATION; MICE; MICE, KNOCKOUT; NIACINAMIDE; P-GLYCOPROTEINS; PHENYLUREA COMPOUNDS; PROTEIN ARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

EID: 84957989883     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.6638     Document Type: Article

References (39)

1. Coussens LM, Werb Z. Inflammation and cancer. Nature. 2002; 420:860-867.
2. Berasain C, Castillo J, Perugorria MJ, Latasa MU, Prieto J, Avila MA. Inflammation and Liver Cancer: New Molecular Links. Ann N Y Acad Sci. 2009; 1155:206-221.
3. Marrero JA. Multidisciplinary management of hepatocellular carcinoma: where are we today? Semin Liver Dis. 2013; 33:S3-10.
4. Schwartz M, Roayaie S, Konstadoulakis M. Strategies for the management of hepatocellular carcinoma. Nat Clin Pract Oncol. 2007; 4:424-432.
5. Livraghi T, Mäkisalo H, Line P-D. Treatment options in hepatocellular carcinoma today. Scand J Surg SJS Off Organ Finn Surg Soc Scand Surg Soc. 2011; 100:22-29.
6. Llovet JM. Updated treatment approach to hepatocellular carcinoma. J Gastroenterol. 2005; 40:225-235.
7. Adachi E, Maeda T, Matsumata T, Shirabe K, Kinukawa N, Sugimachi K, Tsuneyoshi M. Risk factors for intrahepatic recurrence in human small hepatocellular carcinoma. Gastroenterology. 1995; 108:768-775.
8. Imamura H, Matsuyama Y, Tanaka E, Ohkubo T, Hasegawa K, Miyagawa S, Sugawara Y, Minagawa M, Takayama T, Kawasaki S, Makuuchi M. Risk factors contributing to early and late phase intrahepatic recurrence of hepatocellular carcinoma after hepatectomy. J Hepatol. 2003; 38:200-207.
9. Yamamoto J, Kosuge T, Takayama T, Shimada K, Yamasaki S, Ozaki H, Yamaguchi N, Makuuchi M: Recurrence of hepatocellular carcinoma after surgery. Br J Surg. 1996; 83:1219-1222.
10. Kumada T, Nakano S, Takeda I, Sugiyama K, Osada T, Kiriyama S, Sone Y, Toyoda H, Shimada S, Takahashi M, Sassa T. Patterns of recurrence after initial treatment in patients with small hepatocellular carcinoma. Hepatol Baltim Md. 1997; 25:87-92.
11. Ercolani G, Grazi GL, Ravaioli M, Del Gaudio M, Gardini A, Cescon M, Varotti G, Cetta F, Cavallari A. Liver resection for hepatocellular carcinoma on cirrhosis: univariate and multivariate analysis of risk factors for intrahepatic recurrence. Ann Surg. 2003; 237:536-543.
12. Poon RT-P, Fan ST, Lo CM, Liu CL, Wong J. Long-term survival and pattern of recurrence after resection of small hepatocellular carcinoma in patients with preserved liver function: implications for a strategy of salvage transplantation. Ann Surg. 2002; 235:373-382.
13. Abdel Wahab M, Sultan A, el-Ghawalby N, Fathy O, Abu Zeid M, Abu el-Enin A, Abdallah T, Foad A, Kandeel T, el-Shobari M, el-Fiky A, el-Ebidy G, Gadel Hak N, et al. Hepatic resection in cirrhotic liver for treatment of hepatocellular carcinoma in Egyptian patients. Experience with 140 cases in a single center. Hepatogastroenterology. 2004; 51:559-563.
14. Hoshida Y, Villanueva A, Kobayashi M, Peix J, Chiang DY, Camargo A, Gupta S, Moore J, Wrobel MJ, Lerner J, Reich M, Chan JA, Glickman JN, et al. Gene expression in fixed tissues and outcome in hepatocellular carcinoma. N Engl J Med. 2008; 359:1995-2004.
15. Farazi PA, DePinho RA. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer. 2006; 6:674-687.
16. Picardo A, Karpoff HM, Ng B, Lee J, Brennan MF, Fong Y. Partial hepatectomy accelerates local tumor growth: Potential roles of local cytokine activation. Surgery. 1998; 124:57-64.
17. Asaga T, Suzuki K, Umeda M, Sugimasa Y, Takemiya S, Okamoto T. The enhancement of tumor growth after partial hepatectomy and the effect of sera obtained from hepatectomized rats on tumor cell growth. Jpn J Surg. 1991; 21:669-675.
18. De Jong KP, Lont HE, Bijma AM, Brouwers MA, de Vries EG, van Veen ML, Marquet RL, Slooff MJ, Terpstra OT. The effect of partial hepatectomy on tumor growth in rats: in vivo and in vitro studies. Hepatol Baltim Md. 1995; 22:1263-1272.
19. Lammert F, Wang DQ-H, Hillebrandt S, Geier A, Fickert P, Trauner M, Matern S, Paigen B, Carey MC. Spontaneous cholecysto-and hepatolithiasis inMdr2 mice: A model for low phospholipid-associated cholelithiasis. Hepatology. 2004; 39:117-128.
20. Mauad TH, van Nieuwkerk CM, Dingemans KP, Smit JJ, Schinkel AH, Notenboom RG, van den Bergh Weerman MA, Verkruisen RP, Groen AK, Oude Elferink RP. Mice with homozygous disruption of the mdr2 P-glycoprotein gene. A novel animal model for studies of nonsuppurative inflammatory cholangitis and hepatocarcinogenesis. Am J Pathol. 1994; 145:1237-1245.
21. Barash H, R. Gross E, Edrei Y, Ella E, Israel A, Cohen I, Corchia N, Ben-Moshe T, Pappo O, Pikarsky E, Goldenberg D, Shiloh Y, Galun E, et al. Accelerated carcinogenesis following liver regeneration is associated with chronic inflammation-induced double-strand DNA breaks. Proc Natl Acad Sci. 2010; 107:2207-2212.
22. Wilhelm SM. BAY 43-9006 Exhibits Broad Spectrum Oral Antitumor Activity and Targets the RAF/MEK/ERK Pathway and Receptor Tyrosine Kinases Involved in Tumor Progression and Angiogenesis. Cancer Res. 2004; 64:7099-7109.
23. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc J-F, de Oliveira AC, Santoro A, Raoul J-L, Forner A, Schwartz M, Porta C, Zeuzem S, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med. 2008; 359:378-390.
24. Cheng A-L, Kang Y-K, Chen Z, Tsao C-J, Qin S, Kim JS, Luo R, Feng J, Ye S, Yang T-S, Xu J, Sun Y, Liang H, et al. Efficacy and safety of sorafenib in patients in the Asia-Pacific region with advanced hepatocellular carcinoma: a phase III randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2009; 10:25-34.
25. Taub R. Liver regeneration: from myth to mechanism. Nat Rev Mol Cell Biol. 2004; 5:836-847.
26. Hora C, Romanque P, Dufour J-FF. Effect of sorafenib on murine liver regeneration. Hepatology. 2011; 53:577-586.
27. Feng Y-X, Wang T, Deng Y-Z, Yang P, Li J-J, Guan D-X, Yao F, Zhu Y-Q, Qin Y, Wang H, Li N, Wu M-C, Wang H-Y, et al. Sorafenib suppresses postsurgical recurrence and metastasis of hepatocellular carcinoma in an orthotopic mouse model. Hepatology. 2011; 53:483-492.
28. Luo W, Friedman MS, Shedden K, Hankenson KD, Woolf PJ. GAGE: generally applicable gene set enrichment for pathway analysis. BMC Bioinformatics. 2009; 10:161.
29. Kinner A, Wu W, Staudt C, Iliakis G. γH2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res. 2008; 36:5678-5694.
30. Straus D. Genetic evidence for the involvement of the lck tyrosine kinase in signal transduction through the T cell antigen receptor. Cell. 1992; 70:585-593.
31. Zhang DY, Friedman SL. Fibrosis-dependent mechanisms of hepatocarcinogenesis. Hepatology. 2012; 56:769-775.
32. Wang Y, Gao J, Zhang D, Zhang J, Ma J, Jiang H. New insights into the antifibrotic effects of sorafenib on hepatic stellate cells and liver fibrosis. J Hepatol. 2010; 53:132-144.
33. Su T-H, Shiau C-W, Jao P, Liu C-H, Liu C-J, Tai W-T, Jeng Y-M, Yang H-C, Tseng T-C, Huang H-P, Cheng H-R, Chen P-J, Chen K-F, et al. Sorafenib and its derivative SC-1 exhibit antifibrotic effects through signal transducer and activator of transcription 3 inhibition. Proc Natl Acad Sci U S A. 2015; 112:7243-7248.
34. Chen Y-L, Lv J, Ye X-L, Sun M-Y, Xu Q, Liu C-H, Min L-H, Li H-P, Liu P, Ding X. Sorafenib inhibits transforming growth factor β1-Mediated Epithelial-Mesenchymal Transition and apoptosis in mouse hepatocytes. Hepatology. 2011; 53:1708-1718.
35. Bruix J, Takayama T, Mazzaferro V, Chau G-Y, Yang J, Kudo M, Cai J, Poon RT, Han K-H, Tak WY, Lee HC, Song T, Roayaie S, et al. Adjuvant sorafenib for hepatocellular carcinoma after resection or ablation (STORM): a phase 3, randomised, double-blind, placebo-controlled trial. Lancet Oncol. 2015; 16:1344-1354.
36. Greene AK, Puder M. Partial Hepatectomy in the Mouse: Technique and Perioperative Management. J Invest Surg. 2003; 16:99-102.
37. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14:R36.
38. Anders S, Pyl PT, Huber W. HTSeq-a Python framework to work with high-throughput sequencing data. Bioinforma Oxf Engl. 2015; 31:166-169.
39. Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinforma Oxf Engl. 2010; 26:139-140.