Cabozantinib reverses multidrug resistance of human hepatoma HepG2/adr cells by modulating the function of P-glycoprotein

Liver International

Volumn 35, Issue 3, 2015, Pages 1010-1023

  Xiang, Qing Feng ^a   Zhang, Dong Mei ^b   Wang, Jing Nan ^a   Zhang, Hong Wu ^a   Zheng, Zhe Yu ^a   Yu, Da Cheng ^a   Li, Ying Jie ^b   Xu, Jun ^b   Chen, Ya Jin ^a   Shang, Chang Zhen ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b JINAN UNIVERSITY   (China)

Author keywords

Cabozantinib; Chemotherapy; Hepatocellular carcinoma; Multidrug resistance; P glycoprotein

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CABOZANTINIB; CHOLECYSTOKININ OCTAPEPTIDE; DOXORUBICIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MULTIDRUG RESISTANCE PROTEIN; PROTEIN KINASE B; SCATTER FACTOR RECEPTOR; VERAPAMIL; VINCRISTINE; ANILIDE; MET PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; PYRIDINE DERIVATIVE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG BINDING SITE; DRUG MECHANISM; DRUG PROTEIN BINDING; ENZYME ACTIVITY; FEMALE; FLOW CYTOMETRY; FLUORESCENCE MICROSCOPE; GENE EXPRESSION; HEPG2 CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR DOCKING; MOUSE; MULTIDRUG RESISTANCE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN EXPRESSION; TUMOR XENOGRAFT; WESTERN BLOTTING; ANIMAL; BAGG ALBINO MOUSE; CARCINOMA, HEPATOCELLULAR; DRUG EFFECTS; DRUG RESISTANCE; DRUG SCREENING; HEK293 CELL LINE; LIVER NEOPLASMS; METABOLISM; NUDE MOUSE; RANDOMIZATION;

ANILIDES; ANIMALS; CARCINOMA, HEPATOCELLULAR; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HEK293 CELLS; HEP G2 CELLS; HUMANS; LIVER NEOPLASMS; MICE, INBRED BALB C; MICE, NUDE; MOLECULAR DOCKING SIMULATION; P-GLYCOPROTEIN; PROTO-ONCOGENE PROTEINS C-AKT; PROTO-ONCOGENE PROTEINS C-MET; PYRIDINES; RANDOM ALLOCATION; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84922704062     PISSN: 14783223     EISSN: 14783231     Source Type: Journal    
DOI: 10.1111/liv.12524     Document Type: Article

References (45)

1. Jemal A, Siegel R, Xu J, Ward E. Cancer statistics, 2010. CA Cancer J Clin 2010; 60: 277-300.
2. Wong R, Frenette C. Updates in the management of hepatocellular carcinoma. Gastroenterol Hepatol (N Y) 2011; 7: 16-24.
3. Zhu AX. Systemic therapy of advanced hepatocellular carcinoma: how hopeful should we be? Oncologist 2006; 11: 790-800.
4. Zollner G, Wagner M, Fickert P, et al. Hepatobiliary transporter expression in human hepatocellular carcinoma. Liver Int 2005; 25: 367-79.
5. Li B, Ye T, Zhao L, et al. Effects of multidrug resistance, antisense RNA on the chemosensitivity of hepatocellular carcinoma cells. Hepatobiliary Pancreat Dis Int 2006; 5: 552-9.
6. Leonard GD, Fojo T, Bates SE. The role of ABC transporters in clinical practice. Oncologist 2003; 8: 411-24.
7. Ward AB, Szewczyk P, Grimard V, et al. Structures of P-glycoprotein reveal its conformational flexibility and an epitope on the nucleotide-binding domain. Proc Natl Acad Sci U S A 2013; 110: 13386-91.
8. Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM. P-glycoprotein: from genomics to mechanism. Oncogene 2003; 22: 7468-85.
9. Kato A, Miyazaki M, Ambiru S, et al. Multidrug resistance gene (MDR-1) expression as a useful prognostic factor in patients with human hepatocellular carcinoma after surgical resection. J Surg Oncol 2001; 78: 110-5.
10. Soini Y, Virkajarvi N, Raunio H, Paakko P. Expression of P-glycoprotein in hepatocellular carcinoma: a potential marker of prognosis. J Clin Pathol 1996; 49: 470-3.
11. Traxler P, Bold G, Buchdunger E, et al. Tyrosine kinase inhibitors: from rational design to clinical trials. Med Res Rev 2001; 21: 499-512.
12. Bronte F, Bronte G, Cusenza S, et al. Targeted therapies in hepatocellular carcinoma. Curr Med Chem 2014; 21: 966-74.
13. Dancey JE, Chen HX. Strategies for optimizing combinations of molecularly targeted anticancer agents. Nat Rev Drug Discov 2006; 5: 649-59.
14. Jagiello-Gruszfeld A, Tjulandin S, Dobrovolskaya N, et al. A single-arm phase II trial of first-line paclitaxel in combination with lapatinib in HER2-overexpressing metastatic breast cancer. Oncology 2010; 79: 129-35.
15. Abou-Alfa GK, Johnson P, Knox JJ, et al. Doxorubicin plus sorafenib vs doxorubicin alone in patients with advanced hepatocellular carcinoma: a randomized trial. JAMA 2010; 304: 2154-60.
16. Dai CL, Tiwari AK, Wu CP, et al. Lapatinib (Tykerb, GW572016) reverses multidrug resistance in cancer cells by inhibiting the activity of ATP-binding cassette subfamily B member 1 and G member 2. Cancer Res 2008; 68: 7905-14.
17. Shi Z, Peng XX, Kim IW, et al. Erlotinib (Tarceva, OSI-774) antagonizes ATP-binding cassette subfamily B member 1 and ATP-binding cassette subfamily G member 2-mediated drug resistance. Cancer Res 2007; 67: 11012-20.
18. Shukla S, Robey RW, Bates SE, Ambudkar SV. Sunitinib (Sutent, SU11248), a small-molecule receptor tyrosine kinase inhibitor, blocks function of the ATP-binding cassette (ABC) transporters P-glycoprotein (ABCB1) and ABCG2. Drug Metab Dispos 2009; 37: 359-65.
19. Hoffmann K, Franz C, Xiao Z, et al. Sorafenib modulates the gene expression of multi-drug resistance mediating ATP-binding cassette proteins in experimental hepatocellular carcinoma. Anticancer Res 2010; 30: 4503-8.
20. Wei Y, Ma Y, Zhao Q, et al. New use for an old drug: inhibiting ABCG2 with sorafenib. Mol Cancer Ther 2012; 11: 1693-702.
21. Gao JJ, Inagaki Y, Xue X, Qu XJ, Tang W. c-Met: a potential therapeutic target for hepatocellular carcinoma. Drug Discov Ther 2011; 5: 2-11.
22. Zhang SZ, Pan FY, Xu JF, et al. Knockdown of c-Met by adenovirus-delivered small interfering RNA inhibits hepatocellular carcinoma growth in vitro and in vivo. Mol Cancer Ther 2005; 4: 1577-84.
23. Salvi A, Arici B, Portolani N, et al. In vitro c-met inhibition by antisense RNA and plasmid-based RNAi down-modulates migration and invasion of hepatocellular carcinoma cells. Int J Oncol 2007; 31: 451-60.
24. Xie B, Xing R, Chen P, et al. Down-regulation of c-Met expression inhibits human HCC cells growth and invasion by RNA interference. J Surg Res 2010; 162: 231-8.
25. Zhou WJ, Zhang X, Cheng C, et al. Crizotinib (PF-02341066) reverses multidrug resistance in cancer cells by inhibiting the function of P-glycoprotein. Br J Pharmacol 2012; 166: 1669-83.
26. Elisei R, Schlumberger MJ, Muller SP, et al. Cabozantinib in progressive medullary thyroid cancer. J Clin Oncol 2013; 31: 3639-46.
27. Zhang Y, Guessous F, Kofman A, Schiff D, Abounader R. XL-184, a MET, VEGFR-2 and RET kinase inhibitor for the treatment of thyroid cancer, glioblastoma multiforme and NSCLC. IDrugs 2010; 13: 112-21.
28. Verslype C, Cohn AL, Kelley RK, et al. Activity of cabozantinib (XL184) in hepatocellular carcinoma: results from a phase II randomized discontinuation trial (RDT). J Clin Oncol 2012; 30: 4007.
29. Sennino B, Ishiguro-Oonuma T, Wei Y, et al. Suppression of tumor invasion and metastasis by concurrent inhibition of c-Met and VEGF signaling in pancreatic neuroendocrine tumors. Cancer Discov 2012; 2: 270-87.
30. Zhang DM, Shu C, Chen JJ, et al. BBA, a derivative of 23-hydroxybetulinic acid, potently reverses ABCB1-mediated drug resistance in vitro and in vivo. Mol Pharm 2012; 9: 3147-59.
31. Ford JM, Hait WN. Pharmacology of drugs that alter multidrug resistance in cancer. Pharmacol Rev 1990; 42: 155-99.
32. Aller SG, Yu J, Ward A, et al. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009; 323: 1718-22.
33. Minderman H, O'Loughlin KL, Pendyala L, Baer MR. VX-710 (biricodar) increases drug retention and enhances chemosensitivity in resistant cells overexpressing P-glycoprotein, multidrug resistance protein, and breast cancer resistance protein. Clin Cancer Res 2004; 10: 1826-34.
34. Limtrakul P, Khantamat O, Pintha K. Inhibition of P-glycoprotein activity and reversal of cancer multidrug resistance by Momordica charantia extract. Cancer Chemother Pharmacol 2004; 54: 525-30.
35. You H, Ding W, Dang H, Jiang Y, Rountree CB. c-Met represents a potential therapeutic target for personalized treatment in hepatocellular carcinoma. Hepatology 2011; 54: 879-89.
36. Ng IO, Liu CL, Fan ST, Ng M. Expression of P-glycoprotein in hepatocellular carcinoma. A determinant of chemotherapy response. Am J Clin Pathol 2000; 113: 355-63.
37. Kurzrock R, Sherman SI, Ball DW, et al. Activity of XL184 (Cabozantinib), an oral tyrosine kinase inhibitor, in patients with medullary thyroid cancer. J Clin Oncol 2011; 29: 2660-6.
38. Xiang QF, Wang F, Su XD, et al. Effect of BIBF 1120 on reversal of ABCB1-mediated multidrug resistance. Cell Oncol (Dordr) 2011; 34: 33-44.
39. Cheng C, Liu ZG, Zhang H, et al. Enhancing chemosensitivity in ABCB1- and ABCG2-overexpressing cells and cancer stem-like cells by an aurora kinase inhibitor CCT129202. Mol Pharm 2012; 9: 1971-82.
40. Tao LY, Liang YJ, Wang F, et al. Cediranib (recentin, AZD2171) reverses ABCB1- and ABCC1-mediated multidrug resistance by inhibition of their transport function. Cancer Chemother Pharmacol 2009; 64: 961-9.
41. Liu KJ, He JH, Su XD, et al. Saracatinib (AZD0530) is a potent modulator of ABCB1-mediated multidrug resistance in vitro and in vivo. Int J Cancer 2013; 132: 224-35.
42. Mi Y, Lou L. ZD6474 reverses multidrug resistance by directly inhibiting the function of P-glycoprotein. Br J Cancer 2007; 97: 934-40.
43. Choi J, Yip-Schneider M, Albertin F, et al. The effect of doxorubicin on MEK-ERK signaling predicts its efficacy in HCC. J Surg Res 2008; 150: 219-26.
44. Liang J, Ge F, Guo C, et al. Inhibition of PI3K/Akt partially leads to the inhibition of PrP(C)-induced drug resistance in gastric cancer cells. FEBS J 2009; 276: 685-94.
45. McCubrey JA, Steelman LS, Chappell WH, et al. Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 2007; 1773: 1263-84.