Differential effects of arsenic trioxide on chemosensitization in human hepatic tumor and stellate cell lines

BMC Cancer

Volumn 12, Issue , 2012, Pages

  Rangwala, Fatima ^a   Williams, Kevin P ^b   Smith, Ginger R ^b   Thomas, Zainab ^b   Allensworth, Jennifer L ^c   Lyerly, H K ^c   Diehl, Anna M ^a   Morse, Michael A ^a,c   Devi, Gayathri R ^c  

^a 2606 Duke University Medical Center ^*  (United States)

^b NORTH CAROLINA CENTRAL UNIVERSITY   (United States)

^c DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

5 fluorouracil; Apoptosis; Arsenic trioxide; Hepatocellular carcinoma; High throughput assay; Sorafenib; Stroma

Indexed keywords

ARSENIC TRIOXIDE; FLUOROURACIL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SORAFENIB; STRESS ACTIVATED PROTEIN KINASE; THYMIDYLATE SYNTHASE;

ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CELL STRAIN HEPG2; CELL SURVIVAL; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG POTENTIATION; DRUG SENSITIVITY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; IC 50; REAL TIME POLYMERASE CHAIN REACTION; STELLATE CELL; TUMOR CELL; WESTERN BLOTTING;

ADULT; AMP-ACTIVATED PROTEIN KINASES; ANTINEOPLASTIC AGENTS; ARSENICALS; BLOTTING, WESTERN; CARCINOMA, HEPATOCELLULAR; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DRUG SYNERGISM; ENZYME ACTIVATION; FLUOROURACIL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GROWTH INHIBITORS; HEP G2 CELLS; HEPATIC STELLATE CELLS; HUMANS; INHIBITORY CONCENTRATION 50; LIVER NEOPLASMS; NIACINAMIDE; OXIDES; PHENYLUREA COMPOUNDS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THYMIDYLATE SYNTHASE; TIME FACTORS;

EID: 84865847635     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-12-402     Document Type: Article

References (41)

1. Yang JD, Nakamura I, Roberts LR. The tumor microenvironment in hepatocellular carcinoma: current status and therapeutic targets. Semin Canc Biol 2011, 21:35-43.
2. Amann T, Bataille F, Spruss T, Muhlbauer M, Gabele E, Scholmerich J, Kiefer P, Bosserhoff AK, Hellerbrand C. Activated hepatic stellate cells promote tumorigenicity of hepatocellular carcinoma. Canc Sci 2009, 100:646-653.
3. Sancho-Bru P, Juez E, Moreno M, Khurdayan V, Morales-Ruiz M, Colmenero J, Arroyo V, Brenner DA, Gines P, Bataller R. Hepatocarcinoma cells stimulate the growth, migration and expression of pro-angiogenic genes in human hepatic stellate cells. Liver Int 2010, 30:31-41. 10.1111/j.1478-3231.2009.02161.x, 19929904.
4. Santamato A, Fransvea E, Dituri F, Caligiuri A, Quaranta M, Niimi T, Pinzani M, Antonaci S, Giannelli G. Hepatic stellate cells stimulate HCC cell migration via Laminin-5 production. Clin Sci (Lond) 2011, 121:159-168.
5. van Zijl F, Mair M, Csiszar A, Schneller D, Zulehner G, Huber H, Eferl R, Beug H, Dolznig H, Mikulits W. Hepatic tumor-stroma crosstalk guides epithelial to mesenchymal transition at the tumor edge. Oncogene 2009, 28:4022-4033. 10.1038/onc.2009.253, 2900602, 19718050.
6. Emadi A, Gore SD. Arsenic trioxide - An old drug rediscovered. Blood Rev 2010, 24:191-199. 10.1016/j.blre.2010.04.001, 2918685, 20471733.
7. Kito M, Akao Y, Ohishi N, Yagi K, Nozawa Y. Arsenic trioxide-induced apoptosis and its enhancement by buthionine sulfoximine in hepatocellular carcinoma cell lines. Biochem Biophys Res Commun 2002, 291:861-867. 10.1006/bbrc.2002.6525, 11866444.
8. Siu KP, Chan JY, Fung KP. Effect of arsenic trioxide on human hepatocellular carcinoma HepG2 cells: inhibition of proliferation and induction of apoptosis. Life Sci 2002, 71:275-285. 10.1016/S0024-3205(02)01622-3, 12034346.
9. Oketani M, Kohara K, Tuvdendorj D, Ishitsuka K, Komorizono Y, Ishibashi K, Arima T. Inhibition by arsenic trioxide of human hepatoma cell growth. Cancer Lett 2002, 183:147-153. 10.1016/S0304-3835(01)00800-X, 12065089.
10. Zhang T, Wang SS, Hong L, Wang XL, Qi QH. Arsenic trioxide induces apoptosis of rat hepatocellular carcinoma cells in vivo. J Exp Clin Cancer Res 2003, 22:61-68.
11. Kito M, Matsumoto K, Wada N, Sera K, Futatsugawa S, Naoe T, Nozawa Y, Akao Y. Antitumor effect of arsenic trioxide in murine xenograft model. Canc Sci 2003, 94:1010-1014.
12. Lin CC, Hsu C, Hsu CH, Hsu WL, Cheng AL, Yang CH. Arsenic trioxide in patients with hepatocellular carcinoma: a phase II trial. Invest New Drugs 2007, 25:77-84.
13. Subbarayan PR, Lee K, Ardalan B. Arsenic trioxide suppresses thymidylate synthase in 5-FU-resistant colorectal cancer cell line HT29 In Vitro re-sensitizing cells to 5-FU. Anticancer Res 2010, 30:1157-1162.
14. Lin DY, Lin SM, Liaw YF. Non-surgical treatment of hepatocellular carcinoma. J Gastroenterol Hepatol 1997, 12:S319-S328. 10.1111/j.1440-1746.1997.tb00516.x, 9407353.
15. Patt YZ, Hassan MM, Aguayo A, Nooka AK, Lozano RD, Curley SA, Vauthey JN, Ellis LM, Schnirer II, Wolff RA, et al. Oral capecitabine for the treatment of hepatocellular carcinoma, cholangiocarcinoma, and gallbladder carcinoma. Cancer 2004, 101:578-586. 10.1002/cncr.20368, 15274071.
16. Fleming GF, Schilsky RL, Schumm LP, Meyerson A, Hong AM, Vogelzang NJ, Ratain MJ. Phase I and pharmacokinetic study of 24-hour infusion 5-fluorouracil and leucovorin in patients with organ dysfunction. Ann Oncol 2003, 14:1142-1147. 10.1093/annonc/mdg302, 12853359.
17. Twelves C, Glynne-Jones R, Cassidy J, Schuller J, Goggin T, Roos B, Banken L, Utoh M, Weidekamm E, Reigner B. Effect of hepatic dysfunction due to liver metastases on the pharmacokinetics of capecitabine and its metabolites. Clin Cancer Res 1999, 5:1696-1702.
18. Sicklick JK, Li YX, Jayaraman A, Kannangai R, Qi Y, Vivekanandan P, Ludlow JW, Owzar K, Chen W, Torbenson MS, Diehl AM. Dysregulation of the Hedgehog pathway in human hepatocarcinogenesis. Carcinogenesis 2006, 27:748-757.
19. Syn WK, Choi SS, Liaskou E, Karaca GF, Agboola KM, Oo YH, Mi Z, Pereira TA, Zdanowicz M, Malladi P, et al. Osteopontin is induced by hedgehog pathway activation and promotes fibrosis progression in nonalcoholic steatohepatitis. Hepatology 2011, 53:106-115. 10.1002/hep.23998, 3025083, 20967826.
20. Choi SS, Witek RP, Yang L, Omenetti A, Syn WK, Moylan CA, Jung Y, Karaca GF, Teaberry VS, Pereira TA, et al. Activation of Rac1 promotes hedgehog-mediated acquisition of the myofibroblastic phenotype in rat and human hepatic stellate cells. Hepatology 2010, 52:278-290. 10.1002/hep.23649, 2920128, 20578145.
21. Xu L, Hui AY, Albanis E, Arthur MJ, O'Byrne SM, Blaner WS, Mukherjee P, Friedman SL, Eng FJ. Human hepatic stellate cell lines, LX-1 and LX-2: new tools for analysis of hepatic fibrosis. Gut 2005, 54:142-151. 10.1136/gut.2004.042127, 1774377, 15591520.
22. Aird KM, Ding X, Baras A, Wei J, Morse MA, Clay T, Lyerly HK, Devi GR. Trastuzumab signaling in ErbB2-overexpressing inflammatory breast cancer correlates with X-linked inhibitor of apoptosis protein expression. Mol Cancer Ther 2008, 7:38-47.
23. Chou TC, Talalay P. Quantitative analysis of dose-effect relationships: the combined effects of multiple drugs or enzyme inhibitors. Adv Enzyme Regul 1984, 22:27-55.
24. Sicklick JK, Li YX, Choi SS, Qi Y, Chen W, Bustamante M, Huang J, Zdanowicz M, Camp T, Torbenson MS, et al. Role for hedgehog signaling in hepatic stellate cell activation and viability. Lab Invest 2005, 85:1368-1380. 10.1038/labinvest.3700349, 16170335.
25. Thomas ZI, Gibson W, Sexton JZ, Aird KM, Ingram SM, Aldrich A, Lyerly HK, Devi GR, Williams KP. Targeting GLI1 expression in human inflammatory breast cancer cells enhances apoptosis and attenuates migration. Br J Cancer 2011, 104:1575-1586. 10.1038/bjc.2011.133, 3101910, 21505458.
26. Choi SS, Omenetti A, Witek RP, Moylan CA, Syn WK, Jung Y, Yang L, Sudan DL, Sicklick JK, Michelotti GA, et al. Hedgehog pathway activation and epithelial-to-mesenchymal transitions during myofibroblastic transformation of rat hepatic cells in culture and cirrhosis. Am J Physiol Gastrointest Liver Physiol 2009, 297:G1093-G1106. 10.1152/ajpgi.00292.2009, 2850083, 19815628.
27. Rangwala F, Guy CD, Lu J, Suzuki A, Burchette JL, Abdelmalek MF, Chen W, Diehl AM. Increased production of sonic hedgehog by ballooned hepatocytes. J Pathol 2011, 224:401-410. 10.1002/path.2888, 21547909.
28. Vinas O, Bataller R, Sancho-Bru P, Gines P, Berenguer C, Enrich C, Nicolas JM, Ercilla G, Gallart T, Vives J, et al. Human hepatic stellate cells show features of antigen-presenting cells and stimulate lymphocyte proliferation. Hepatology 2003, 38:919-929.
29. Bataller R, Brenner DA. Liver fibrosis. J Clin Invest 2005, 115:209-218. 546435, 15690074.
30. Tomuleasa C, Soritau O, Fischer-Fodor E, Pop T, Susman S, Mosteanu O, Petrushev B, Aldea M, Acalovschi M, Irimie A, Kacso G. Arsenic trioxide plus cisplatin/interferon alpha-2b/doxorubicin/capecitabine combination chemotherapy for unresectable hepatocellular carcinoma. Hematol Oncol Stem Cell Ther 2011, 4:60-66.
31. Yuan Z, Wang F, Zhao Z, Zhao X, Qiu J, Nie C, Wei Y. BIM-mediated AKT phosphorylation is a Key modulator of arsenic trioxide-induced apoptosis in cisplatin-sensitive and -resistant ovarian cancer cells. PLoS One 2011, 6:e20586. 10.1371/journal.pone.0020586, 3105099, 21655183.
32. Liu ZM, Tseng JT, Hong DY, Huang HS. Suppression of TG-interacting factor sensitizes arsenic trioxide-induced apoptosis in human hepatocellular carcinoma cells. Biochem J 2011, 438:349-358. 10.1042/BJ20101653, 21649584.
33. Chiu HW, Ho YS, Wang YJ. Arsenic trioxide induces autophagy and apoptosis in human glioma cells in vitro and in vivo through downregulation of survivin. J Mol Med 2011, 89:927-941. 10.1007/s00109-011-0763-1, 21594580.
34. Sumi D, Shinkai Y, Kumagai Y. Signal transduction pathways and transcription factors triggered by arsenic trioxide in leukemia cells. Toxicol Appl Pharmacol 2010, 244:385-392. 10.1016/j.taap.2010.02.012, 20193703.
35. Shen ZX, Chen GQ, Ni JH, Li XS, Xiong SM, Qiu QY, Zhu J, Tang W, Sun GL, Yang KQ, et al. Use of arsenic trioxide (As2O3) in the treatment of acute promyelocytic leukemia (APL): II. Clinical efficacy and pharmacokinetics in relapsed patients. Blood 1997, 89:3354-3360.
36. Ardalan B, Subbarayan PR, Ramos Y, Gonzalez M, Fernandez A, Mezentsev D, Reis I, Duncan R, Podolsky L, Lee K, et al. A phase I study of 5-fluorouracil/leucovorin and arsenic trioxide for patients with refractory/relapsed colorectal carcinoma. Clin Cancer Res 2010, 16:3019-3027. 10.1158/1078-0432.CCR-09-2590, 20501625.
37. Podolsky L, Oh M, Subbarayan PR, Francheschi D, Livingstone A, Ardalan B. 5-Fluorouracil/Leucovorin and arsenic trioxide for patients with refractory/relapsed colorectal carcinoma: a clinical experience. Acta Oncol 2011, 50:602-605. 10.3109/0284186X.2010.524934, 20950119.
38. Bragado P, Armesilla A, Silva A, Porras A. Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 2007, 12:1733-1742. 10.1007/s10495-007-0082-8, 17505786.
39. El-Najjar N, Chatila M, Moukadem H, Vuorela H, Ocker M, Gandesiri M, Schneider-Stock R, Gali-Muhtasib H. Reactive oxygen species mediate thymoquinone-induced apoptosis and activate ERK and JNK signaling. Apoptosis 2010, 15:183-195. 10.1007/s10495-009-0421-z, 19882352.
40. Chan DW, Liu VW, Tsao GS, Yao KM, Furukawa T, Chan KK, Ngan HY. Loss of MKP3 mediated by oxidative stress enhances tumorigenicity and chemoresistance of ovarian cancer cells. Carcinogenesis 2008, 29:1742-1750. 10.1093/carcin/bgn167, 18632752.
41. Lampiasi N, Azzolina A, D'Alessandro N, Umezawa K, McCubrey JA, Montalto G, Cervello M. Antitumor effects of dehydroxymethylepoxyquinomicin, a novel nuclear factor-kappaB inhibitor, in human liver cancer cells are mediated through a reactive oxygen species-dependent mechanism. Mol Pharmacol 2009, 76:290-300. 10.1124/mol.109.055418, 19461054.