Multi-drug resistance in cancer chemotherapeutics: Mechanisms and lab approaches

Cancer Letters

Volumn 347, Issue 2, 2014, Pages 159-166

  Wu, Qiong ^a   Yang, Zhiping ^a   Nie, Yongzhan ^a   Shi, Yongquan ^a   Fan, Daiming ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Biomarker; Cancer; Chemotherapy; Lab approach; Mechanism; Multi drug resistance (MDR)

Indexed keywords

ABC TRANSPORTER; BLEOMYCIN; BONE MORPHOGENETIC PROTEIN 4; CISPLATIN; COLCHICINE; DIHYDROARTEMISININ; DOXORUBICIN; FLUOROURACIL; HERMES ANTIGEN; MICRORNA; MITOXANTRONE; OXALIPLATIN; PACLITAXEL; TAMOXIFEN; VINCRISTINE;

APOPTOSIS; AUTOPHAGY; CANCER CELL CULTURE; CANCER CHEMOTHERAPY; CANCER STEM CELL; CARCINOGENICITY; CELL RENEWAL; DNA DAMAGE; DNA REPAIR; DOWN REGULATION; DRUG SENSITIVITY; EPIGENETICS; HIGH THROUGHPUT SCREENING; HUMAN; HYPOXIA; LABORATORY TEST; MULTIDRUG RESISTANCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SHORT SURVEY; SIGNAL TRANSDUCTION;

BIOMARKER; CANCER; CHEMOTHERAPY; LAB APPROACH; MECHANISM; MULTI-DRUG RESISTANCE (MDR);

ANTINEOPLASTIC AGENTS; AUTOPHAGY; DRUG RESISTANCE, MULTIPLE; DRUG RESISTANCE, NEOPLASM; EPIGENESIS, GENETIC; HUMANS; MICRORNAS;

EID: 84898462370     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2014.03.013     Document Type: Review

References (80)

1. Fojo A., Hamilton T.C., Young R.C., Ozols R.F. Multidrug resistance in ovarian cancer. Cancer 1987, 60:2075-2080.
2. Kaye S.B. The multidrug resistance phenotype. Br. J. Cancer 1988, 58:691-694.
3. Gillet J.P., Efferth T., Remacle J. Chemotherapy-induced resistance by ATP-binding cassette transporter genes. Biochim. Biophys. Acta 2007, 1775:237-262.
4. Lage H. ABC-transporters: implications on drug resistance from microorganisms to human cancers. Int. J. Antimicrob. Agents 2003, 22:188-199.
5. Dean M., Rzhetsky A., Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001, 11:1156-1166.
6. Shaffer B.C., Gillet J.P., Patel C., Baer M.R., Bates S.E., Gottesman M.M. Drug resistance: still a daunting challenge to the successful treatment of AML. Drug Resist. Update 2012, 15:62-69.
7. Azab F., Vali S., Abraham J., Potter N., Muz B., de la Puente P., Fiala M., Paasch J., Sultana Z., Tyagi A., Abbasi T., Vij R., Azab A.K. PI3KCA plays a major role in multiple myeloma and its inhibition with BYL719 decreases proliferation, synergizes with other therapies and overcomes stroma-induced resistance. Brit. J. Haematol. 2014.
8. Shao S., Huang X., Wang Y., He S., Xu X., Zhu X., Yang X., Ding Z., Yao L., Huang Y., Wang C. A role for activator of G-protein signaling 3 (AGS3) in multiple myeloma. Int. J. Hematol. 2014, 99:57-68.
9. Vinod B.S., Maliekal T.T., Anto R.J. Phytochemicals as chemosensitizers: from molecular mechanism to clinical significance. Antioxid. Redox Signal. 2013, 18:1307-1348.
10. O'Donovan T.R., O'Sullivan G.C., McKenna S.L. Induction of autophagy by drug-resistant esophageal cancer cells promotes their survival and recovery following treatment with chemotherapeutics. Autophagy 2011, 7:509-524.
11. Guo X.L., Hu F., Zhang S.S., Zhao Q.D., Zong C., Ye F., Guo S.W., Zhang J.W., Li R., Wu M.C., Wei L.X. Inhibition of p53 increases chemosensitivity to 5-FU in nutrient-deprived hepatocarcinoma cells by suppressing autophagy. Cancer Lett. 2014.
12. Xue Z., Yan H., Li J., Liang S., Cai X., Chen X., Wu Q., Gao L., Wu K., Nie Y., Fan D. Identification of cancer stem cells in vincristine preconditioned SGC7901 gastric cancer cell line. J. Cell. Biochem. 2012, 113:302-312.
13. Sarvi S., Mackinnon A.C., Avlonitis N., Bradley M., Rintoul R.C., Rassl D.M., Wang W., Forbes S.J., Gregory C.D., Sethi T. CD133+ cancer stem-like cells in small cell lung cancer are highly tumorigenic and chemoresistant but sensitive to a novel neuropeptide antagonist. Cancer Res. 2014.
14. Martin V., Sanchez-Sanchez A.M., Herrera F., Gomez-Manzano C., Fueyo J., Alvarez-Vega M.A., Antolin I., Rodriguez C. Melatonin-induced methylation of the ABCG2/BCRP promoter as a novel mechanism to overcome multidrug resistance in brain tumour stem cells. Br. J. Cancer 2013, 108:2005-2012.
15. Cheng W., Liu T., Wan X., Gao Y., Wang H. MicroRNA-199a targets CD44 to suppress the tumorigenicity and multidrug resistance of ovarian cancer-initiating cells. FEBS J. 2012, 279:2047-2059.
16. Wang F., Li T., Zhang B., Li H., Wu Q., Yang L., Nie Y., Wu K., Shi Y., Fan D. MicroRNA-19a/b regulates multidrug resistance in human gastric cancer cells by targeting PTEN. Biochem. Biophys. Res. Commun. 2013, 434:688-694.
17. Zhang L., Pickard K., Jenei V., Bullock M.D., Bruce A., Mitter R., Kelly G., Paraskeva C., Strefford J., Primrose J., Thomas G.J., Packham G., Mirnezami A.H. MiR-153 supports colorectal cancer progression via pleiotropic effects that enhance invasion and chemotherapeutic resistance. Cancer Res. 2013, 73:6435-6447.
18. Xia L., Zhang D., Du R., Pan Y., Zhao L., Sun S., Hong L., Liu J., Fan D. MiR-15b and miR-16 modulate multidrug resistance by targeting BCL2 in human gastric cancer cells. Int. J. Cancer 2008, 123:372-379.
19. Shang Y., Zhang Z., Liu Z., Feng B., Ren G., Li K., Zhou L., Sun Y., Li M., Zhou J., An Y., Wu K., Nie Y., Fan D. MiR-508-5p regulates multidrug resistance of gastric cancer by targeting ABCB1 and ZNRD1. Oncogene 2013.
20. Chen Z., Ma T., Huang C., Zhang L., Lv X., Xu T., Hu T., Li J. MiR-27a modulates the MDR1/P-glycoprotein expression by inhibiting FZD7/beta-catenin pathway in hepatocellular carcinoma cells. Cell. Signal. 2013, 25:2693-2701.
21. Chen Q., Xia H.W., Ge X.J., Zhang Y.C., Tang Q.L., Bi F. Serum miR-19a predicts resistance to FOLFOX chemotherapy in advanced colorectal cancer cases. Asian Pac. J. Cancer Prev. 2013, 14:7421-7426.
22. Liu L., Ning X., Sun L., Zhang H., Shi Y., Guo C., Han S., Liu J., Sun S., Han Z., Wu K., Fan D. Hypoxia-inducible factor-1 alpha contributes to hypoxia-induced chemoresistance in gastric cancer. Cancer Sci. 2008, 99:121-128.
23. Liu L., Ning X., Sun L., Shi Y., Han S., Guo C., Chen Y., Sun S., Yin F., Wu K., Fan D. Involvement of MGr1-Ag/37LRP in the vincristine-induced HIF-1 expression in gastric cancer cells. Mol. Cell. Biochem. 2007, 303:151-160.
24. Liu L., Sun L., Zhang H., Li Z., Ning X., Shi Y., Guo C., Han S., Wu K., Fan D. Hypoxia-mediated up-regulation of MGr1-Ag/37LRP in gastric cancers occurs via hypoxia-inducible-factor 1-dependent mechanism and contributes to drug resistance. Int. J. Cancer 2009, 124:1707-1715.
25. Casorelli I., Bossa C., Bignami M. DNA damage and repair in human cancer: molecular mechanisms and contribution to therapy-related leukemias. Int. J. Environ. Res. Public Health 2012, 9:2636-2657.
26. Ziebarth A.J., Nowsheen S., Steg A.D., Shah M.M., Katre A.A., Dobbin Z.C., Han H.D., Lopez-Berestein G., Sood A.K., Conner M., Yang E.S., Landen C.N. Endoglin (CD105) contributes to platinum resistance and is a target for tumor-specific therapy in epithelial ovarian cancer. Clin. Cancer Res. 2013, 19:170-182.
27. Wray J., Williamson E.A., Sheema S., Lee S.H., Libby E., Willman C.L., Nickoloff J.A., Hromas R. Metnase mediates chromosome decatenation in acute leukemia cells. Blood 2009, 114:1852-1858.
28. Wray J., Williamson E.A., Royce M., Shaheen M., Beck B.D., Lee S.H., Nickoloff J.A., Hromas R. Metnase mediates resistance to topoisomerase II inhibitors in breast cancer cells. PLoS ONE 2009, 4:e5323.
29. Williamson E.A., Damiani L., Leitao A., Hu C., Hathaway H., Oprea T., Sklar L., Shaheen M., Bauman J., Wang W., Nickoloff J.A., Lee S.H., Hromas R. Targeting the transposase domain of the DNA repair component Metnase to enhance chemotherapy. Cancer Res. 2012, 72:6200-6208.
30. Ivanova T., Zouridis H., Wu Y., Cheng L.L., Tan I.B., Gopalakrishnan V., Ooi C.H., Lee J., Qin L., Wu J., Lee M., Rha S.Y., Huang D., Liem N., Yeoh K.G., Yong W.P., Teh B.T., Tan P. Integrated epigenomics identifies BMP4 as a modulator of cisplatin sensitivity in gastric cancer. Gut 2013, 62:22-33.
31. Oehme I., Linke J.P., Bock B.C., Milde T., Lodrini M., Hartenstein B., Wiegand I., Eckert C., Roth W., Kool M., Kaden S., Grone H.J., Schulte J.H., Lindner S., Hamacher-Brady A., Brady N.R., Deubzer H.E., Witt O. Histone deacetylase 10 promotes autophagy-mediated cell survival. Proc. Natl. Acad. Sci. USA 2013, 110:E2592-2601.
32. Lee E., Kim H., Lee I.H., Jon S. In vivo antitumor effects of chitosan-conjugated docetaxel after oral administration. J. Control Release 2009, 140:79-85.
33. Sindac J.A., Barraza S.J., Dobry C.J., Xiang J., Blakely P.K., Irani D.N., Keep R.F., Miller D.J., Larsen S.D. Optimization of novel indole-2-carboxamide inhibitors of neurotropic alphavirus replication. J. Med. Chem. 2013, 56:9222-9241.
34. Drescher S., Schaeffeler E., Hitzl M., Hofmann U., Schwab M., Brinkmann U., Eichelbaum M., Fromm M.F. MDR1 gene polymorphisms and disposition of the P-glycoprotein substrate fexofenadine. Br. J. Clin. Pharmacol. 2002, 53:526-534.
35. Taipalensuu J., Tavelin S., Lazorova L., Svensson A.C., Artursson P. Exploring the quantitative relationship between the level of MDR1 transcript, protein and function using digoxin as a marker of MDR1-dependent drug efflux activity. Eur. J. Pharm. Sci. 2004, 21:69-75.
36. Li X.X., Dong Y., Wang W., Wang H.L., Chen Y.Y., Shi G.Y., Yi J., Wang J. Emodin as an effective agent in targeting cancer stem-like side population cells of gallbladder carcinoma. Stem Cells Dev. 2013, 22:554-566.
37. Kannan P., Telu S., Shukla S., Ambudkar S.V., Pike V.W., Halldin C., Gottesman M.M., Innis R.B., Hall M.D. The "specific" P-glycoprotein inhibitor Tariquidar is also a substrate and an inhibitor for breast cancer resistance protein (BCRP/ABCG2). ACS Chem. Neurosci. 2011, 2:82-89.
38. Nabekura T., Yamaki T., Hiroi T., Ueno K., Kitagawa S. Inhibition of anticancer drug efflux transporter P-glycoprotein by rosemary phytochemicals. Pharmacol. Res. 2010, 61:259-263.
39. Keppler D. Multidrug resistance proteins (MRPs, ABCCs): importance for pathophysiology and drug therapy. Handb. Exp. Pharmacol. 2011, 299-323.
40. Lebedeva I.V., Pande P., Patton W.F. Sensitive and specific fluorescent probes for functional analysis of the three major types of mammalian ABC transporters. PLoS ONE 2011, 6:e22429.
41. Kang J., Zhao G., Lin T., Tang S., Xu G., Hu S., Bi Q., Guo C., Sun L., Han S., Xu Q., Nie Y., Wang B., Liang S., Ding J., Wu K. A peptide derived from phage display library exhibits anti-tumor activity by targeting GRP78 in gastric cancer multidrug resistance cells. Cancer Lett. 2013, 339:247-259.
42. Li K., Sun Z., Zheng J., Lu Y., Bian Y., Ye M., Wang X., Nie Y., Zou H., Fan D. In-depth research of multidrug resistance related cell surface glycoproteome in gastric cancer. J. Proteomics 2013, 82:130-140.
43. Kato R., Hasegawa K., Achiwa Y., Okamoto H., Torii Y., Oe S., Udagawa Y. Predicting nedaplatin sensitivity of cervical cancer using the histoculture drug response assay. Eur. J. Gynaecol. Oncol. 2011, 32:381-386.
44. Furukawa T., Kubota T., Hoffman R.M. Clinical applications of the histoculture drug response assay. Clin. Cancer Res. 1995, 1:305-311.
45. Du J., Pan Y., Shi Y., Guo C., Jin X., Sun L., Liu N., Qiao T., Fan D. Overexpression and significance of prion protein in gastric cancer and multidrug-resistant gastric carcinoma cell line SGC7901/ADR. Int. J. Cancer 2005, 113:213-220.
46. H. Al-Ali, M. Blackmore, J.L. Bixby, V.P. Lemmon, High Content Screening with Primary Neurons, in: G.S. Sittampalam, N. Gal-Edd, M. Arkin, D. Auld, C. Austin, B. Bejcek, M. Glicksman, J. Inglese, V. Lemmon, Z. Li, J. McGee, O. McManus, L. Minor, A. Napper, T. Riss, O.J. Trask, J. Weidner, (Eds.), Assay Guidance Manual, Bethesda, MD, 2004.
47. Schmandke A., Pietro M.A., Schwab M.E. An open source based high content screening method for cell biology laboratories investigating cell spreading and adhesion. PLoS ONE 2013, 8:e78212.
48. Rosania G.R., Shedden K., Zheng N., Zhang X. Visualizing chemical structure-subcellular localization relationships using fluorescent small molecules as probes of cellular transport. J. Cheminform. 2013, 5:44.
49. Persson M., Loye A.F., Mow T., Hornberg J.J. A high content screening assay to predict human drug-induced liver injury during drug discovery. J. Pharmacol. Toxicol. Methods 2013, 68:302-313.
50. Vaz G.M., Paszko E., Davies A.M., Senge M.O. High content screening as high quality assay for biological evaluation of photosensitizers in vitro. PLoS ONE 2013, 8:e70653.
51. Lincke C.R., Broeks A., The I., Plasterk R.H., Borst P. The expression of two P-glycoprotein (Pgp) genes in transgenic Caenorhabditis elegans is confined to intestinal cells. EMBO J. 1993, 12:1615-1620.
52. Juranka P.F., Zastawny R.L., Ling V. P-glycoprotein: multidrug-resistance and a superfamily of membrane-associated transport proteins. FASEB J. 1989, 3:2583-2592.
53. Langer R., Ott K., Feith M., Lordick F., Specht K., Becker K., Hofler H. High pretherapeutic thymidylate synthetase and MRP-1 protein levels are associated with nonresponse to neoadjuvant chemotherapy in oesophageal adenocarcinoma patients. J. Surg. Oncol. 2010, 102:503-508.
54. Shi H., Lu D., Shu Y., Shi W., Lu S., Wang K. Expression of multidrug-resistance-related proteins P-glycoprotein, glutathione-S-transferases, topoisomerase-II and lung resistance protein in primary gastric cardiac adenocarcinoma. Cancer Invest. 2008, 26:344-351.
55. Zhao L., Pan Y., Gang Y., Wang H., Jin H., Tie J., Xia L., Zhang Y., He L., Yao L., Qiao T., Li T., Liu Z., Fan D. Identification of GAS1 as an epirubicin resistance-related gene in human gastric cancer cells with a partially randomized small interfering RNA library. J. Biol. Chem. 2009, 284:26273-26285.
56. Weinkauf M., Hutter G., Zimmermann Y., Hartmann E., Rosenwald A., Dreyling M. Combined RNA-expression and 2D-PAGE-screening identifies comprehensive interaction networks affected after bortezomib or enzastaurin exposure of mantle cell lymphoma. Talanta 2010, 80:1539-1544.
57. Park S.H., Wang X., Liu R., Lam K.S., Weiss R.H. High throughput screening of a small molecule one-bead-one-compound combinatorial library to identify attenuators of p21 as chemotherapy sensitizers. Cancer Biol. Ther. 2008, 7:2015-2022.
58. Kopetz S. Right drug for the right patient. Am. Soc. Clin. Oncol. Educ. Book 2013, 115-120.
59. Hudson B.D., Kulp K.S., Loots G.G. Prostate cancer invasion and metastasis: insights from mining genomic data. Brief Funct. Genom. 2013, 12:397-410.
60. Xu C.Z., Xie J., Jin B., Chen X.W., Sun Z.F., Wang B.X., Dong P. Gene and microRNA expression reveals sensitivity to paclitaxel in laryngeal cancer cell line. Int. J. Clin. Exp. Pathol. 2013, 6:1351-1361.
61. Galvani E., Toffalorio F., Peters G.J., De Pas T., Giovannetti E. Clinical Application of Pharmacogenetics of non-small cell lung cancer (NSCLC): time to "work it out"?. Curr. Pharm. Des. 2013.
62. Stewart A., Steiner J., Mellows G., Laguda B., Norris D., Bevan P. Phase I trial of XR9576 in healthy volunteers demonstrates modulation of P-glycoprotein in CD56+ lymphocytes after oral and intravenous administration. Clin. Cancer Res. 2000, 6:4186-4191.
63. Agrawal M., Abraham J., Balis F.M., Edgerly M., Stein W.D., Bates S., Fojo T., Chen C.C. Increased 99m Tc-sestamibi accumulation in normal liver and drug-resistant tumors after the administration of the glycoprotein inhibitor, XR9576. Clin. Cancer Res. 2003, 9:650-656.
64. Pusztai L., Wagner P., Ibrahim N., Rivera E., Theriault R., Booser D., Symmans F.W., Wong F., Blumenschein G., Fleming D.R., Rouzier R., Boniface G., Hortobagyi G.N. Phase II study of tariquidar, a selective P-glycoprotein inhibitor, in patients with chemotherapy-resistant, advanced breast carcinoma. Cancer 2005, 104:682-691.
65. Xie D., Zhang Y., Zou J., Yin D., Chen X., Dai J. Biotransformation of a taxadiene by ginkgo cell cultures and the tumor multi-drug resistant reversal activities of the metabolites. Chem. Pharm. Bull. (Tokyo) 2011, 59:1038-1041.
66. Gu Y., Fan S., Xiong Y., Peng B., Zheng G., Yu Y., Ouyang Y., He Z. Cloning and functional characterization of TCRP1, a novel gene mediating resistance to cisplatin in an oral squamous cell carcinoma cell line. FEBS Lett. 2011, 585:881-887.
67. Kurimoto S., Kashiwada Y., Lee K.H., Takaishi Y. Triterpenes and a triterpene glucoside from Dysoxylum cumingianum. Phytochemistry 2011, 72:2205-2211.
68. Zhou F., Mei H., Wu Q., Jin R. Expression of histone H2AX phosphorylation and its potential to modulate adriamycin resistance in K562/A02 cell line. J. Huazhong. Univ. Sci. Technol. Med. Sci. 2011, 31:154-158.
69. Eid S.Y., El-Readi M.Z., Wink M. Synergism of three-drug combinations of sanguinarine and other plant secondary metabolites with digitonin and doxorubicin in multi-drug resistant cancer cells. Phytomedicine 2012, 19:1288-1297.
70. Yin F., Shi Y.Q., Zhao W.P., Xiao B., Miao J.Y., Fan D.M. Suppression of P-gp induced multiple drug resistance in a drug resistant gastric cancer cell line by overexpression of Fas. World J. Gastroenterol. 2000, 6:664-670.
71. Huang H.Y., Niu J.L., Zhao L.M., Lu Y.H. Reversal effect of 2',4'-dihydroxy-6'-methoxy-3',5'-dimethylchalcone on multi-drug resistance in resistant human hepatocellular carcinoma cell line BEL-7402/5-FU. Phytomedicine 2011, 18:1086-1092.
72. Sun J., Yeung C.A., Co N.N., Tsang T.Y., Yau E., Luo K., Wu P., Wa J.C., Fung K.P., Kwok T.T., Liu F. Clitocine reversal of P-glycoprotein associated multi-drug resistance through down-regulation of transcription factor NF-kappaB in R-HepG2 cell line. PLoS ONE 2012, 7:e40720.
73. Lu J.J., Chen S.M., Ding J., Meng L.H. Characterization of dihydroartemisinin-resistant colon carcinoma HCT116/R cell line. Mol. Cell. Biochem. 2012, 360:329-337.
74. Huang X.C., Sun Y.L., Salim A.A., Chen Z.S., Capon R.J. Parguerenes: marine red alga bromoditerpenes as inhibitors of P-glycoprotein (ABCB1) in multidrug resistant human cancer cells. Biochem. Pharmacol. 2013, 85:1257-1268.
75. Deng Q., Li Z.P., Huang C.M., Liu Z., Zhong R.M., Li A.J., Bi F., Tang Q.L. Effect and mechanism of DNMT inhibitor on the reversal of multidrug resistance in human colon cancer cell line sw620/L-OHP. Sichuan Da Xue Xue Bao Yi Xue Ban 2010, 41:975-979.
76. Liu X., Qiao L., Xie D., Zhang Y., Zou J., Chen X., Dai J. Microbial transformation of ginsenoside-Rg(1) by Absidia coerulea and the reversal activity of the metabolites towards multi-drug resistant tumor cells. Fitoterapia 2011, 82:1313-1317.
77. Mamidipudi V., Shi T., Brady H., Surapaneni S., Chopra R., Aukerman S.L., Heise C., Sung V. Increased cellular accumulation and distribution of amrubicin contribute to its activity in anthracycline-resistant cancer cells. Cancer Chemother. Pharmacol. 2012, 69:965-976.
78. Liang B., Kong D., Liu Y., Liang N., He M., Ma S., Liu X. Autophagy inhibition plays the synergetic killing roles with radiation in the multi-drug resistant SKVCR ovarian cancer cells. Radiat. Oncol. 2012, 7:213.
79. Eid S.Y., El-Readi M.Z., Wink M. Digitonin synergistically enhances the cytotoxicity of plant secondary metabolites in cancer cells. Phytomedicine 2012, 19:1307-1314.
80. Iangcharoen P., Punfa W., Yodkeeree S., Kasinrerk W., Ampasavate C., Anuchapreeda S., Limtrakul P. Anti-P-glycoprotein conjugated nanoparticles for targeting drug delivery in cancer treatment. Arch. Pharm. Res. 2011, 34:1679-1689.