Acquisition of docetaxel resistance in breast cancer cells reveals upregulation of ABCB1 expression as a key mediator of resistance accompanied by discrete upregulation of other specific genes and pathways

Tumor Biology

Volumn 36, Issue 6, 2015, Pages 4327-4338

  Hansen, Stine Ninel ^a   Westergaard, David ^a,b   Thomsen, Mathilde Borg Houlberg ^a   Vistesen, Mette ^a   Do, Khoa Nguyen ^a,b   Fogh, Louise ^a   Belling, Kirstine C ^a,b   Wang, Jun ^a,c   Yang, Huanming ^a,c   Gupta, Ramneek ^a,b   Ditzel, Henrik J ^a,d   Moreira, José ^a   Brünner, Nils ^a   Stenvang, Jan ^a   Schrohl, Anne Sofie ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c BGI SHENZHEN   (China)

^d UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

Author keywords

Breast cancer; Docetaxel; Gene set enrichment analysis; Microarray analysis; Pgp; Resistance

Indexed keywords

ABC TRANSPORTER; CANCER TESTIS ANTIGEN; CELL PROTEIN; DOCETAXEL; EPIRUBICIN; GLYCOPROTEIN; INTERFERON INDUCIBLE PROTEIN; MATRIX PROTEIN; MESSENGER RNA; MULTIDRUG RESISTANCE PROTEIN 1; OXALIPLATIN; TRANSCRIPTOME; UNCLASSIFIED DRUG; ABCB1 PROTEIN, HUMAN; MULTIDRUG RESISTANCE PROTEIN; TAXOID; TUMOR PROTEIN;

ABCB1 GENE; ARTICLE; BREAST CANCER; BREAST CANCER CELL LINE; CANCER CELL; CANCER CHEMOTHERAPY; CANCER INHIBITION; CANCER RESISTANCE; CELL SPECIFICITY; CHEMOSENSITIVITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CROSS RESISTANCE; EXTRACELLULAR MATRIX; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; MCF 7 CELL LINE; MDA MDA 231 CELL LINE; MOLECULAR GENETICS; PREDICTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FAMILY; UPREGULATION; ANTAGONISTS AND INHIBITORS; BIOSYNTHESIS; BREAST NEOPLASMS; CELL MEMBRANE PERMEABILITY; DRUG EFFECTS; DRUG RESISTANCE; FEMALE; GENETICS; MICROARRAY ANALYSIS; PATHOLOGY; SIGNAL TRANSDUCTION;

BREAST NEOPLASMS; CELL MEMBRANE PERMEABILITY; DRUG RESISTANCE, NEOPLASM; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCOPROTEINS; HUMANS; MCF-7 CELLS; MICROARRAY ANALYSIS; NEOPLASM PROTEINS; P-GLYCOPROTEINS; SIGNAL TRANSDUCTION; TAXOIDS;

EID: 84938991148     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-015-3072-4     Document Type: Article

References (46)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D. Global cancer statistics. CA Cancer J Clin. 2011;61:69–90.
2. Mouridsen HT, Bjerre KD, Christiansen P, Jensen MB, Moller S. Improvement of prognosis in breast cancer in Denmark 1977-2006, based on the nationwide reporting to the DBCG Registry. Acta Oncol. 2008;47:525–36.
3. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013;63:11–30.
4. Gennari A, Conte P, Rosso R, Orlandini C, Bruzzi P. Survival of metastatic breast carcinoma patients over a 20-year period: a retrospective analysis based on individual patient data from six consecutive studies. Cancer. 2005;104:1742–50.
5. El Saghir NS, Tfayli A, Hatoum HA, Nachef Z, Dinh P, Awada A. Treatment of metastatic breast cancer: state-of-the-art, subtypes and perspectives. Crit Rev Oncol Hematol. 2011;80:433–49.
6. Diaz JF, Andreu JM. Assembly of purified GDP-tubulin into microtubules induced by taxol and taxotere: reversibility, ligand stoichiometry, and competition. Biochemistry. 1993;32:2747–55.
7. Fabbri F, Carloni S, Brigliadori G, Zoli W, Lapalombella R, Marini M. Sequential events of apoptosis involving docetaxel, a microtubule-interfering agent: a cytometric study. BMC Cell Biol. 2006;7:6.
8. Terrano DT, Upreti M, Chambers TC. Cyclin-dependent kinase 1-mediated Bcl-xL/Bcl-2 phosphorylation acts as a functional link coupling mitotic arrest and apoptosis. Mol Cell Biol. 2010;30:640–56.
9. Trock BJ, Leonessa F, Clarke R. Multidrug resistance in breast cancer: a meta-analysis of MDR1/gp170 expression and its possible functional significance. J Natl Cancer Inst. 1997;89:917–31.
10. Noguchi S. Predictive factors for response to docetaxel in human breast cancers. Cancer Sci. 2006;97:813–20.
11. Linn SC, Pinedo HM, van Ark-Otte J, van der Valk P, Hoekman K, Honkoop AH, et al. Expression of drug resistance proteins in breast cancer, in relation to chemotherapy. Int J Cancer. 1997;71:787–95.
12. Carter A, Dann EJ, Katz T, Shechter Y, Oliven A, Regev R, et al. Cells from chronic myelogenous leukaemia patients at presentation exhibit multidrug resistance not mediated by either MDR1 or MRP1. Br J Haematol. 2001;114:581–90.
13. Chintamani, Singh JP, Mittal MK, Saxena S, Bansal A, Bhatia A, et al. Role of p-glycoprotein expression in predicting response to neoadjuvant chemotherapy in breast cancer—a prospective clinical study. World J Surg Oncol. 2005;3:61.
14. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB. Evaluation of a tetrazolium-based semiautomated colorimetric assay: assessment of chemosensitivity testing. Cancer Res. 1987;47:936–42.
15. Bolstad BM, Irizarry RA, Astrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19:185–93.
16. Smyth GK: Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004;3:Article3
17. Smyth GK, Speed T. Normalization of cDNA microarray data. Methods. 2003;31:265–73.
18. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
19. Hochberg Y, Benjamini Y. More powerful procedures for multiple significance testing. Stat Med. 1990;9:811–8.
20. Mootha VK, Lindgren CM, Eriksson KF, Subramanian A, Sihag S, Lehar J, et al. PGC-1alpha-responsive genes involved in oxidative phosphorylation are coordinately downregulated in human diabetes. Nat Genet. 2003;34:267–73.
21. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A. 2005;102:15545–50.
22. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Res. 2012;40:D109–14.
23. Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28:27–30.
24. Liu B, Sun D, Xia W, Hung MC, Yu D. Cross-reactivity of C219 anti-p170(mdr-1) antibody with p185(c-erbB2) in breast cancer cells: cautions on evaluating p170(mdr-1). J Natl Cancer Inst. 1997;89:1524–9.
25. Hernandez-Vargas H, Palacios J, Moreno-Bueno G. Molecular profiling of docetaxel cytotoxicity in breast cancer cells: uncoupling of aberrant mitosis and apoptosis. Oncogene. 2007;26:2902–13.
26. Ajabnoor GM, Crook T, Coley HM. Paclitaxel resistance is associated with switch from apoptotic to autophagic cell death in MCF-7 breast cancer cells. Cell Death Dis. 2012;3:e260.
27. Iseri OD, Kars MD, Gunduz U. Two different docetaxel resistant MCF-7 sublines exhibited different gene expression pattern. Mol Biol Rep. 2012;39:3505–16.
28. Kars MD, Iseri OD, Gunduz U. A microarray based expression profiling of paclitaxel and vincristine resistant MCF-7 cells. Eur J Pharmacol. 2011;657:4–9.
29. Iseri OD, Kars MD, Arpaci F, Gunduz U. Gene expression analysis of drug-resistant MCF-7 cells: implications for relation to extracellular matrix proteins. Cancer Chemother Pharmacol. 2010;65:447–55.
30. Kars MD, Iseri OD, Gunduz U. Drug resistant breast cancer cells overexpress ETS1 gene. Biomed Pharmacother. 2010;64:458–62.
31. Villeneuve DJ, Hembruff SL, Veitch Z, Cecchetto M, Dew WA, Parissenti AM. cDNA microarray analysis of isogenic paclitaxel- and doxorubicin-resistant breast tumor cell lines reveals distinct drug-specific genetic signatures of resistance. Breast Cancer Res Treat. 2006;96:17–39.
32. Duan Z, Lamendola DE, Duan Y, Yusuf RZ, Seiden MV. Description of paclitaxel resistance-associated genes in ovarian and breast cancer cell lines. Cancer Chemother Pharmacol. 2005;55:277–85.
33. Wu CP, Hsieh CH, Wu YS. The emergence of drug transporter-mediated multidrug resistance to cancer chemotherapy. Mol Pharm. 2011;8:1996–2011.
34. Vera-Ramirez L, Sanchez-Rovira P, Ramirez-Tortosa CL, Quiles JL, Ramirez-Tortosa M, Lorente JA. Transcriptional shift identifies a set of genes driving breast cancer chemoresistance. PLoS ONE. 2013;8:e53983.
35. Hembruff SL, Laberge ML, Villeneuve DJ, Guo B, Veitch Z, Cecchetto M, et al. Role of drug transporters and drug accumulation in the temporal acquisition of drug resistance. BMC Cancer. 2008;8:318.
36. Guarneri V, Dieci MV, Conte P. Relapsed triple-negative breast cancer: challenges and treatment strategies. Drugs. 2013;73:1257–65.
37. Duan Z, Duan Y, Lamendola DE, Yusuf RZ, Naeem R, Penson RT, et al. Overexpression of MAGE/GAGE genes in paclitaxel/doxorubicin-resistant human cancer cell lines. Clin Cancer Res. 2003;9:2778–85.
38. Cappell KM, Sinnott R, Taus P, Maxfield K, Scarbrough M, Whitehurst AW. Multiple cancer testis antigens function to support tumor cell mitotic fidelity. Mol Cell Biol. 2012;32:4131–40.
39. Materna V, Surowiak P, Kaplenko I, Spaczynski M, Duan Z, Zabel M, et al. Taxol-resistance-associated gene-3 (TRAG-3/CSAG2) expression is predictive for clinical outcome in ovarian carcinoma patients. Virchows Arch. 2007;450:187–94.
40. Grigoriadis A, Caballero OL, Hoek KS, da Silva L, Chen YT, Shin SJ, et al. CT-X antigen expression in human breast cancer. Proc Natl Acad Sci U S A. 2009;106:13493–8.
41. Chen YT, Ross DS, Chiu R, Zhou XK, Chen YY, Lee P, et al. Multiple cancer/testis antigens are preferentially expressed in hormone-receptor negative and high-grade breast cancers. PLoS ONE. 2011;6:e17876.
42. Hellman M, Tossavainen H, Rappu P, Heino J, Permi P. Characterization of intrinsically disordered prostate associated gene (PAGE5) at single residue resolution by NMR spectroscopy. PLoS ONE. 2011;6:e26633.
43. Aoudjit F, Vuori K. Integrin signaling in cancer cell survival and chemoresistance. Chemother Res Pract. 2012;2012:283181.
44. Groth-Pedersen L, Jaattela M. Combating apoptosis and multidrug resistant cancers by targeting lysosomes. Cancer Lett. 2013;332:265–74.
45. Nomura T, Katunuma N. Involvement of cathepsins in the invasion, metastasis and proliferation of cancer cells. J Med Invest. 2005;52:1–9.
46. Zhang XJ, Chen S, Huang KX, Le WD. Why should autophagic flux be assessed? Acta Pharmacol Sin. 2013;34:595–9.