MEK inhibition induced downregulation of MRP1 and MRP3 expression in experimental hepatocellular carcinoma

Cancer Cell International

Volumn 13, Issue 1, 2013, Pages

  Lin, Shibo ^a   Hoffmann, Katrin ^a   Xiao, Zhi ^b   Jin, Nan ^a   Galli, Uwe ^a   Mohr, Elvira ^a   Büchler, Markus W ^a   Schemmer, Peter ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b CENTRAL SOUTH UNIVERSITY   (China)

Author keywords

Hepatocellular carcinoma; MEK; MRP1; MRP3; Multidrug resistance

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 3 (3,5 DIBROMO 4 HYDROXYBENZYLIDENE) 1,3 DIHYDRO 5 IODO 2 INDOLONE; DOXORUBICIN; GEMCITABINE; MITOGEN ACTIVATED PROTEIN KINASE; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 3; RAF PROTEIN; SELUMETINIB;

ARTICLE; CANCER GROWTH; CELL VIABILITY; CONTROLLED STUDY; DOSE RESPONSE; DOWN REGULATION; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL CARCINOMA; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING;

EID: 84872156087     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-13-3     Document Type: Article

References (44)

1. Philip PA, Mahoney MR, Allmer C, Thomas J, Pitot HC, Kim G, Donehower RC, Fitch T, Picus J, Erlichman C. Phase II study of Erlotinib (OSI-774) in patients with advanced hepatocellular cancer. J Clin Oncol 2005, 23(27):6657-6663. 10.1200/JCO.2005.14.696, 16170173.
2. El-Serag HB, Rudolph KL. Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 2007, 132(7):2557-2576. 10.1053/j.gastro.2007.04.061, 17570226.
3. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin 2011, 61(2):69-90. 10.3322/caac.20107, 21296855.
4. El-Serag HB, Marrero JA, Rudolph L, Reddy KR. Diagnosis and treatment of hepatocellular carcinoma. Gastroenterology 2008, 134(6):1752-1763. 10.1053/j.gastro.2008.02.090, 18471552.
5. Davila JA, Duan Z, McGlynn KA, El-Serag HB. Utilization and Outcomes of Palliative Therapy for Hepatocellular Carcinoma: A Population-based Study in the United States. J Clin Gastroenterol 2012, 46(1):71-77. 10.1097/MCG.0b013e318224d669, 22157221.
6. Bruix J, Sherman M. Management of hepatocellular carcinoma: an update. Hepatology 2011, 53(3):1020-1022. 10.1002/hep.24199, 3084991, 21374666.
7. Llovet JM, Ricci S, Mazzaferro V, Hilgard P, Gane E, Blanc JF, de Oliveira AC, Santoro A, Raoul JL, Forner A, et al. Sorafenib in advanced hepatocellular carcinoma. N Engl J Med 2008, 359(4):378-390. 10.1056/NEJMoa0708857, 18650514.
8. Cheng AL, Kang YK, Chen Z, Tsao CJ, Qin S, Kim JS, Luo R, Feng J, Ye S, Yang TS, 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(1):25-34. 10.1016/S1470-2045(08)70285-7, 19095497.
9. Lai CL, Wu PC, Chan GC, Lok AS, Lin HJ. Doxorubicin versus no antitumor therapy in inoperable hepatocellular carcinoma. A prospective randomized trial. Cancer 1988, 62(3):479-483. 10.1002/1097-0142(19880801)62:3<479::AID-CNCR2820620306>3.0.CO;2-L, 2839280.
10. Fuchs CS, Clark JW, Ryan DP, Kulke MH, Kim H, Earle CC, Vincitore M, Mayer RJ, Stuart KE. A phase II trial of gemcitabine in patients with advanced hepatocellular carcinoma. Cancer 2002, 94(12):3186-3191. 10.1002/cncr.10607, 12115351.
11. Yeo W, Mok TS, Zee B, Leung TW, Lai PB, Lau WY, Koh J, Mo FK, Yu SC, Chan AT, et al. A randomized phase III study of doxorubicin versus cisplatin/interferon alpha-2b/doxorubicin/fluorouracil (PIAF) combination chemotherapy for unresectable hepatocellular carcinoma. J Natl Cancer Inst 2005, 97(20):1532-1538. 10.1093/jnci/dji315, 16234567.
12. Thomas MB, O'Beirne JP, Furuse J, Chan AT, Abou-Alfa G, Johnson P. Systemic therapy for hepatocellular carcinoma: cytotoxic chemotherapy, targeted therapy and immunotherapy. Ann Surg Oncol 2008, 15(4):1008-1014. 10.1245/s10434-007-9705-0, 18236117.
13. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer 2002, 2(1):48-58. 10.1038/nrc706, 11902585.
14. Lee CH. Reversing agents for ATP-binding cassette drug transporters. Methods Mol Biol 2010, 596:325-340. 10.1007/978-1-60761-416-6_14, 19949930.
15. Hoffmann K, Shibo L, Xiao Z, Longerich T, Buchler MW, Schemmer P. Correlation of gene expression of ATP-binding cassette protein and tyrosine kinase signaling pathway in patients with hepatocellular carcinoma. Anticancer Res 2011, 31(11):3883-3890.
16. Hoffmann K, Xiao Z, Franz C, Mohr E, Serba S, Buchler MW, Schemmer P. Involvement of the epidermal growth factor receptor in the modulation of multidrug resistance in human hepatocellular carcinoma cells in vitro. Canc Cell Int 2011, 11:40.
17. Hwang YH, Choi JY, Kim S, Chung ES, Kim T, Koh SS, Lee B, Bae SH, Kim J, Park YM. Over-expression of c-raf-1 proto-oncogene in liver cirrhosis and hepatocellular carcinoma. Hepatol Res 2004, 29(2):113-121. 10.1016/j.hepres.2004.02.009, 15163433.
18. Ito Y, Sasaki Y, Horimoto M, Wada S, Tanaka Y, Kasahara A, Ueki T, Hirano T, Yamamoto H, Fujimoto J, et al. Activation of mitogen-activated protein kinases/extracellular signal-regulated kinases in human hepatocellular carcinoma. Hepatology 1998, 27(4):951-958. 10.1002/hep.510270409, 9537433.
19. Schmidt CM, McKillop IH, Cahill PA, Sitzmann JV. Increased MAPK expression and activity in primary human hepatocellular carcinoma. Biochem Biophys Res Commun 1997, 236(1):54-58. 10.1006/bbrc.1997.6840, 9223425.
20. Zhang Z, Zhou X, Shen H, Wang D, Wang Y. Phosphorylated ERK is a potential predictor of sensitivity to sorafenib when treating hepatocellular carcinoma: evidence from an in vitro study. BMC Med 2009, 7:41. 10.1186/1741-7015-7-41, 2738687, 19698189.
21. Hoffmann K, Franz C, Xiao Z, Mohr E, Serba S, Buchler MW, Schemmer P. Sorafenib modulates the gene expression of multi-drug resistance mediating ATP-binding cassette proteins in experimental hepatocellular carcinoma. Anticancer Res 2010, 30(11):4503-4508.
22. Tanami H, Imoto I, Hirasawa A, Yuki Y, Sonoda I, Inoue J, Yasui K, Misawa-Furihata A, Kawakami Y, Inazawa J. Involvement of overexpressed wild-type BRAF in the growth of malignant melanoma cell lines. Oncogene 2004, 23(54):8796-8804. 10.1038/sj.onc.1208152, 15467732.
23. Hatzivassiliou G, Song K, Yen I, Brandhuber BJ, Anderson DJ, Alvarado R, Ludlam MJ, Stokoe D, Gloor SL, Vigers G, et al. RAF inhibitors prime wild-type RAF to activate the MAPK pathway and enhance growth. Nature 2010, 464(7287):431-435. 10.1038/nature08833, 20130576.
24. Nies AT, Konig J, Pfannschmidt M, Klar E, Hofmann WJ, Keppler D. Expression of the multidrug resistance proteins MRP2 and MRP3 in human hepatocellular carcinoma. Int J Canc Suppl J Int Canc 2001, 94(4):492-499.
25. Vander Borght S, Komuta M, Libbrecht L, Katoonizadeh A, Aerts R, Dymarkowski S, Verslype C, Nevens F, Roskams T. Expression of multidrug resistance-associated protein 1 in hepatocellular carcinoma is associated with a more aggressive tumour phenotype and may reflect a progenitor cell origin. Liver Int 2008, 28(10):1370-1380. 10.1111/j.1478-3231.2008.01889.x, 19055643.
26. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144(5):646-674. 10.1016/j.cell.2011.02.013, 21376230.
27. Kim EK, Choi EJ. Pathological roles of MAPK signaling pathways in human diseases. Biochim Biophys Acta 2010, 1802(4):396-405. 10.1016/j.bbadis.2009.12.009, 20079433.
28. Klein PJ, Schmidt CM, Wiesenauer CA, Choi JN, Gage EA, Yip-Schneider MT, Wiebke EA, Wang Y, Omer C, Sebolt-Leopold JS. The effects of a novel MEK inhibitor PD184161 on MEK-ERK signaling and growth in human liver cancer. Neoplasia 2006, 8(1):1-8. 10.1593/neo.05373, 1601146, 16533420.
29. Deming D, Geiger P, Chen H, Vaccaro A, Kunnimalaiyaan M, Holen K. ZM336372, a Raf-1 activator, causes suppression of proliferation in a human hepatocellular carcinoma cell line. J Gastrointest Surg 2008, 12(5):852-857. 10.1007/s11605-008-0495-x, 18299943.
30. Huynh H, Soo KC, Chow PK, Tran E. Targeted inhibition of the extracellular signal-regulated kinase kinase pathway with AZD6244 (ARRY-142886) in the treatment of hepatocellular carcinoma. Mol Cancer Ther 2007, 6(1):138-146. 10.1158/1535-7163.MCT-06-0436, 17237274.
31. Huynh H, Chow PK, Soo KC. AZD6244 and doxorubicin induce growth suppression and apoptosis in mouse models of hepatocellular carcinoma. Mol Cancer Ther 2007, 6(9):2468-2476. 10.1158/1535-7163.MCT-07-0162, 17876044.
32. O'Neil BH, Goff LW, Kauh JS, Strosberg JR, Bekaii-Saab TS, Lee RM, Kazi A, Moore DT, Learoyd M, Lush RM, et al. Phase II study of the mitogen-activated protein kinase 1/2 inhibitor selumetinib in patients with advanced hepatocellular carcinoma. J Clin Oncol 2011, 29(17):2350-2356. 10.1200/JCO.2010.33.9432, 3107750, 21519015.
33. Wang XK, Fu LW. Interaction of tyrosine kinase inhibitors with the MDR- related ABC transporter proteins. Curr Drug Metab 2010, 11(7):618-628. 10.2174/138920010792927316, 20812904.
34. Dohse M, Scharenberg C, Shukla S, Robey RW, Volkmann T, Deeken JF, Brendel C, Ambudkar SV, Neubauer A, Bates SE. Comparison of ATP-binding cassette transporter interactions with the tyrosine kinase inhibitors imatinib, nilotinib, and dasatinib. Drug Metab Dispos 2010, 38(8):1371-1380. 10.1124/dmd.109.031302, 2913625, 20423956.
35. Katayama K, Yoshioka S, Tsukahara S, Mitsuhashi J, Sugimoto Y. Inhibition of the mitogen-activated protein kinase pathway results in the down-regulation of P-glycoprotein. Mol Cancer Ther 2007, 6(7):2092-2102. 10.1158/1535-7163.MCT-07-0148, 17620438.
36. Zheng LS, Wang F, Li YH, Zhang X, Chen LM, Liang YJ, Dai CL, Yan YY, Tao LY, Mi YJ, et al. Vandetanib (Zactima, ZD6474) antagonizes ABCC1- and ABCG2-mediated multidrug resistance by inhibition of their transport function. PLoS One 2009, 4(4):e5172. 10.1371/journal.pone.0005172, 2669214, 19390592.
37. Chaudhary PM, Roninson IB. Induction of multidrug resistance in human cells by transient exposure to different chemotherapeutic drugs. J Natl Cancer Inst 1993, 85(8):632-639. 10.1093/jnci/85.8.632, 8096875.
38. Dreuw A, Hermanns HM, Heise R, Joussen S, Rodriguez F, Marquardt Y, Jugert F, Merk HF, Heinrich PC, Baron JM. Interleukin-6-type cytokines upregulate expression of multidrug resistance-associated proteins in NHEK and dermal fibroblasts. J Invest Dermatol 2005, 124(1):28-37. 10.1111/j.0022-202X.2004.23499.x, 15654950.
39. Imai Y, Ohmori K, Yasuda S, Wada M, Suzuki T, Fukuda K, Ueda Y. Breast cancer resistance protein/ABCG2 is differentially regulated downstream of extracellular signal-regulated kinase. Cancer Sci 2009, 100(6):1118-1127. 10.1111/j.1349-7006.2009.01154.x, 19514121.
40. Gomez-Martinez A, Garcia-Morales P, Carrato A, Castro-Galache MD, Soto JL, Carrasco-Garcia E, Garcia-Bautista M, Guaraz P, Ferragut JA, Saceda M. Post-transcriptional regulation of P-glycoprotein expression in cancer cell lines. Mol Cancer Res 2007, 5(6):641-653. 10.1158/1541-7786.MCR-06-0177, 17579122.
41. Ros JE, Libbrecht L, Geuken M, Jansen PL, Roskams TA. High expression of MDR1, MRP1, and MRP3 in the hepatic progenitor cell compartment and hepatocytes in severe human liver disease. J Pathol 2003, 200(5):553-560. 10.1002/path.1379, 12898590.
42. Garcia R, Franklin RA, McCubrey JA. EGF induces cell motility and multi-drug resistance gene expression in breast cancer cells. Cell Cycle 2006, 5(23):2820-2826. 10.4161/cc.5.23.3535, 17172846.
43. Wu J, Dent P, Jelinek T, Wolfman A, Weber MJ, Sturgill TW. Inhibition of the EGF-activated MAP kinase signaling pathway by adenosine 3',5'-monophosphate. Science 1993, 262(5136):1065-1069. 10.1126/science.7694366, 7694366.
44. Hirsch-Ernst KI, Ziemann C, Schmitz-Salue C, Foth H, Kahl GF. Modulation of P-glycoprotein and mdr1b mRNA expression by growth factors in primary rat hepatocyte culture. Biochem Biophys Res Commun 1995, 215(1):179-185. 10.1006/bbrc.1995.2450, 7575588.