A new 2α,5α,10β,14β-tetraacetoxy-4(20),11-taxadiene (SIA) derivative overcomes paclitaxel resistance by inhibiting MAPK signaling and increasing paclitaxel accumulation in breast cancer cells

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Mei, Mei ^a   Xie, Dan ^a   Zhang, Yi ^a   Jin, Jing ^a   You, Feng ^a   Li, Yan ^a   Dai, Jungui ^a   Chen, Xiaoguang ^a  

^a INSTITUTE OF MATERIA MEDICA   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2ALPHA,5ALPHA,10BETA,14BETA TETRAACETOXY 4(10), 11 TAXADIENE; ANTINEOPLASTIC AGENT; MITOGEN ACTIVATED PROTEIN KINASE P38; MULTIDRUG RESISTANCE PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; NPB 304; PACLITAXEL; PROTEIN P53; UNCLASSIFIED DRUG; ACETIC ACID DERIVATIVE; DITERPENE; SINENXAN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER RESISTANCE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG STRUCTURE; DRUG SYNTHESIS; HUMAN; IC 50; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION; ANIMAL; BREAST TUMOR; CHEMISTRY; DISEASE MODEL; DRUG EFFECTS; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SCREENING; FEMALE; GENETICS; METABOLISM; SIGNAL TRANSDUCTION; SYNTHESIS; TUMOR CELL LINE;

ACETATES; ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; BREAST NEOPLASMS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DITERPENES; DRUG RESISTANCE, NEOPLASM; DRUG SYNERGISM; FEMALE; HUMANS; MAP KINASE SIGNALING SYSTEM; P-GLYCOPROTEIN; PACLITAXEL; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84905646935     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104317     Document Type: Article

References (58)

1. Mekhail TM, Markman M (2002) Paclitaxel in cancer therapy. Expert Opin Pharmacother 3: 755-766. (Pubitemid 34649705)
2. Blagosklonny MV, Fojo T (1999) Molecular effects of paclitaxel: myths and reality (a critical review). Int J Cancer 83: 151-156. (Pubitemid 29449089)
3. Horwitz SB (1994) Taxol (paclitaxel): mechanisms of action. Ann Oncol 5 Suppl 6: S3-6.
4. Geney R, Ungureanu l M, Li D, Ojima I (2002) Overcoming multidrug resistance in taxane chemotherapy. Clin Chem Lab Med 40: 918-925.
5. Baguley BC (2010) Multiple drug resistance mechanisms in cancer. Mol Biotechnol 46: 308-316.
6. Redmond KM, Wilson TR, Johnston PG, Longley DB (2008) Resistance mechanisms to cancer chemotherapy. Front Biosci 13: 5138-5154. (Pubitemid 351599664)
7. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Wong EW, et al. (2007) Roles of the Raf/MEK/ERK pathway in cell growth, malignant transformation and drug resistance. Biochim Biophys Acta 1773: 1263-1284. (Pubitemid 47125967)
8. McCubrey JA, Steelman LS, Chappell WH, Abrams SL, Franklin RA, et al. (2012) Ras/Raf/MEK/ERK and PI3K/PTEN/Akt/mTOR cascade inhibitors: how mutations can result in therapy resistance and how to overcome resistance. Oncotarget 3: 1068-1111.
9. Higgins CF (2007) Multiple molecular mechanisms for multidrug resistance transporters. Nature 446: 749-757.
10. Sparreboom A, Danesi R, Ando Y, Chan J, Figg WD (2003) Pharmacogenomics of ABC transporters and its role in cancer chemotherapy. Drug Resist Updat 6: 71-84. (Pubitemid 36565766)
11. McDaid HM, Horwitz SB (2001) Selective potentiation of paclitaxel (taxol)-induced cell death by mitogen-activated protein kinase kinase inhibition in human cancer cell lines. Mol Pharmacol 60: 290-301. (Pubitemid 32678294)
12. Steelman LS, Franklin RA, Abrams SL, Chappell W, Kempf CR, et al. (2011) Roles of the Ras/Raf/MEK/ERK pathway in leukemia therapy. Leukemia 25: 1080-1094.
13. Liu KJ, He JH, Su XD, Sim HM, Xie JD, et al. (2013) Saracatinib (AZD0530) is a potent modulator of ABCB1-mediated multidrug resistance in vitro and in vivo. Int J Cancer 132: 224-235.
14. Zhou WJ, Zhang X, Cheng C, Wang F, Wang XK, et al. (2012) Crizotinib (PF-02341066) reverses multidrug resistance in cancer cells by inhibiting the function of P-glycoprotein. Br J Pharmacol 166: 1669-1683.
15. Haass NK, Sproesser K, Nguyen TK, Contractor R, Medina CA, et al. (2008) The mitogen-activated protein/extracellular signal-regulated kinase kinase inhibitor AZD6244 (ARRY-142886) induces growth arrest in melanoma cells and tumor regression when combined with docetaxel. Clin Cancer Res 14: 230-239. (Pubitemid 351378000)
16. Makin G, Dive C (2001) Modulating sensitivity to drug-induced apoptosis: the future for chemotherapy? Breast Cancer Res 3: 150-153. (Pubitemid 32390215)
17. Penson RT, Oliva E, Skates SJ, Glyptis T, Fuller AF, Jr., et al. (2004) Expression of multidrug resistance-1 protein inversely correlates with paclitaxel response and survival in ovarian cancer patients: a study in serial samples. Gynecol Oncol 93: 98-106. (Pubitemid 38429555)
18. Trock BJ, Leonessa F, Clarke R (1997) Multidrug resistance in breast cancer: a meta-analysis of MDR1/gp170 expression and its possible functional significance. J Natl Cancer Inst 89: 917-931. (Pubitemid 27282064)
19. Yu M, Ocana A, Tannock IF (2013) Reversal of ATP-binding cassette drug transporter activity to modulate chemoresistance: why has it failed to provide clinical benefit? Cancer Metastasis Rev 32: 211-227.
20. Amiri-Kordestani L, Basseville A, Kurdziel K, Fojo AT, Bates SE (2012) Targeting MDR in breast and lung cancer: discriminating its potential importance from the failure of drug resistance reversal studies. Drug Resist Updat 15: 50-61.
21. Dai J (2009) Chemo-enzymatic transformation of taxanes and their reversal activity towards MDR tumor cells. Curr Top Med Chem 9: 1625-1635.
22. Xie D, Zhang Y, Zou J, Yin D, Chen X, et al. (2011) Biotransformation of a taxadiene by ginkgo cell cultures and the tumor multi-drug resistant reversal activities of the metabolites. Chem Pharm Bull (Tokyo) 59: 1038-1041.
23. Zhang Y, Li H, Wang H, Su F, Qu R, et al. (2010) Syl611, a novel semisynthetic taxane derivative, reverses multidrug resistance by p-glycoprotein inhibition and facilitating inward transmembrane action. Cancer Chemother Pharmacol 66: 851-859.
24. Huang M, Zhao X, Zhang M, Gu J, Chen X, et al. (2010) Synthesis and structure-activity relationships of sinenxan A derivatives as multidrug resistance reversal agents. Bioorg Med Chem Lett 20: 5418-5421.
25. Chou TC, Guan Y, Soenen DR, Danishefsky SJ, Boger DL (2005) Potent reversal of multidrug resistance by ningalins and its use in drug combinations against human colon carcinoma xenograft in nude mice. Cancer Chemother Pharmacol 56: 379-390. (Pubitemid 41095401)
26. Zhou Q, Li Y, Jin J, Lang L, Zhu Z, et al. (2012) Lx2-32c, a novel taxane derivative, exerts anti-resistance activity by initiating intrinsic apoptosis pathway in vitro and inhibits the growth of resistant tumor in vivo. Biol Pharm Bull 35: 2170-2179.
27. Li Y, Tang K, Zhang H, Zhang Y, Zhou W, et al. (2011) Function of Aurora kinase A in Taxol-resistant breast cancer and its correlation with P-gp. Mol Med Rep 4: 739-746.
28. You F, Hu J, Li X, Li Y (2013) The elimination of MTC-220, a novel anti-tumor agent of conjugate of paclitaxel and muramyl dipeptide analogue, in rats. Cancer Chemother Pharmacol 71: 1453-1462.
29. Vogelstein B, Lane D, Levine AJ (2000) Surfing the p53 network. Nature 408: 307-310.
30. Oren M (2003) Decision making by p53: life, death and cancer. Cell Death Differ 10: 431-442.
31. Dent P, Jarvis WD, Birrer MJ, Fisher PB, Schmidt-Ullrich RK, et al. (1998) The roles of signaling by the p42/p44 mitogen-activated protein (MAP) kinase pathway; a potential route to radio- and chemo-sensitization of tumor cells resulting in the induction of apoptosis and loss of clonogenicity. Leukemia 12: 1843-1850. (Pubitemid 28554457)
32. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273: 18623-18632. (Pubitemid 28334795)
33. Marengo B, De Ciucis CG, Ricciarelli R, Furfaro AL, Colla R, et al. (2013) p38MAPK inhibition: a new combined approach to reduce neuroblastoma resistance under etoposide treatment. Cell Death Dis 4: e589.
34. Milone MR, Pucci B, Bruzzese F, Carbone C, Piro G, et al. (2013) Acquired resistance to zoledronic acid and the parallel acquisition of an aggressive phenotype are mediated by p38-MAP kinase activation in prostate cancer cells. Cell Death Dis 4: e641.
35. He D, Zhao XQ, Chen XG, Fang Y, Singh S, et al. (2013) BIRB796, the inhibitor of p38 mitogen-activated protein kinase, enhances the efficacy of chemotherapeutic agents in ABCB1 overexpression cells. PLoS One 8: e54181.
36. Thomas H, Coley HM (2003) Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting p-glycoprotein. Cancer Control 10: 159-165. (Pubitemid 36437822)
37. Brooks TA, Minderman H, O'Loughlin KL, Pera P, Ojima I, et al. (2003) Taxane-based reversal agents modulate drug resistance mediated by P-glycoprotein, multidrug resistance protein, and breast cancer resistance protein. Mol Cancer Ther 2: 1195-1205.
38. Ojima I, Borella CP, Wu X, Bounaud PY, Oderda CF, et al. (2005) Design, synthesis and structure-activity relationships of novel taxane-based multidrug resistance reversal agents. J Med Chem 48: 2218-2228. (Pubitemid 40396349)
39. Torres K, Horwitz SB (1998) Mechanisms of Taxol-induced cell death are concentration dependent. Cancer Res 58: 3620-3626. (Pubitemid 28376560)
40. Banerjee M, Singh P, Panda D (2010) Curcumin suppresses the dynamic instability of microtubules, activates the mitotic checkpoint and induces apoptosis in MCF-7 cells. FEBS J 277: 3437-3448.
41. Milross CG, Mason KA, Hunter NR, Chung WK, Peters LJ, et al. (1996) Relationship of mitotic arrest and apoptosis to antitumor effect of paclitaxel. J Natl Cancer Inst 88: 1308-1314. (Pubitemid 26301619)
42. Bello E, Taraboletti G, Colella G, Zucchetti M, Forestieri D, et al. (2013) The tyrosine kinase inhibitor E-3810 combined with paclitaxel inhibits the growth of advanced-stage triple-negative breast cancer xenografts. Mol Cancer Ther 12: 131-140.
43. Santarpia L, Lippman SM, El-Naggar AK (2012) Targeting the MAPK-RASRAF signaling pathway in cancer therapy. Expert Opin Ther Targets 16: 103-119.
44. Sebolt-Leopold JS, Herrera R (2004) Targeting the mitogen-activated protein kinase cascade to treat cancer. Nat Rev Cancer 4: 937-947. (Pubitemid 39626217)
45. Kohno M, Pouyssegur J (2006) Targeting the ERK signaling pathway in cancer therapy. Ann Med 38: 200-211. (Pubitemid 43675585)
46. Cossa G, Gatti L, Cassinelli G, Lanzi C, Zaffaroni N, et al. (2013) Modulation of sensitivity to antitumor agents by targeting the MAPK survival pathway. Curr Pharm Des 19: 883-894.
47. Tortora G, Bianco R, Daniele G, Ciardiello F, McCubrey JA, et al. (2007) Overcoming resistance to molecularly targeted anticancer therapies: Rational drug combinations based on EGFR and MAPK inhibition for solid tumours and haematologic malignancies. Drug Resist Updat 10: 81-100. (Pubitemid 47031052)
48. McDaid HM, Lopez-Barcons L, Grossman A, Lia M, Keller S, et al. (2005) Enhancement of the therapeutic efficacy of taxol by the mitogen-activated protein kinase kinase inhibitor CI-1040 in nude mice bearing human heterotransplants. Cancer Res 65: 2854-2860. (Pubitemid 40490089)
49. MacKeigan JP, Collins TS, Ting JP (2000) MEK inhibition enhances paclitaxel-induced tumor apoptosis. J Biol Chem 275: 38953-38956. (Pubitemid 32058904)
50. Kim K, Kong SY, Fulciniti M, Li X, Song W, et al. (2010) Blockade of the MEK/ERK signalling cascade by AS703026, a novel selective MEK1/2 inhibitor, induces pleiotropic anti-myeloma activity in vitro and in vivo. Br J Haematol 149: 537-549.
51. Jazirehi AR, Vega MI, Chatterjee D, Goodglick L, Bonavida B (2004) Inhibition of the Raf-MEK1/2-ERK1/2 signaling pathway, Bcl-xL down-regulation, and chemosensitization of non-Hodgkin's lymphoma B cells by Rituximab. Cancer Res 64: 7117-7126. (Pubitemid 39331025)
52. Boldt S, Weidle UH, Kolch W (2002) The role of MAPK pathways in the action of chemotherapeutic drugs. Carcinogenesis 23: 1831-1838. (Pubitemid 35355933)
53. Barancik M, Bohacova V, Kvackajova J, Hudecova S, Krizanova O, et al. (2001) SB203580, a specific inhibitor of p38-MAPK pathway, is a new reversal agent of P-glycoprotein-mediated multidrug resistance. Eur J Pharm Sci 14: 29-36. (Pubitemid 32655412)
54. Lage H (2008) An overview of cancer multidrug resistance: a still unsolved problem. Cell Mol Life Sci 65: 3145-3167.
55. Perez-Tomas R (2006) Multidrug resistance: retrospect and prospects in anti-cancer drug treatment. Curr Med Chem 13: 1859-1876.
56. Thews O, Dillenburg W, Rosch F, Fellner M (2013) PET imaging of the impact of extracellular pH and MAP kinases on the p-glycoprotein (Pgp) activity. Adv Exp Med Biol 765: 279-286.
57. Sauvant C, Nowak M, Wirth C, Schneider B, Riemann A, et al. (2008) Acidosis induces multi-drug resistance in rat prostate cancer cells (AT1) in vitro and in vivo by increasing the activity of the p-glycoprotein via activation of p38. Int J Cancer 123: 2532-2542.
58. Thews O, Dillenburg W, Fellner M, Buchholz HG, Bausbacher N, et al. (2010) Activation of P-glycoprotein (Pgp)-mediated drug efflux by extracellular acidosis: in vivo imaging with 68Ga-labelled PET tracer. Eur J Nucl Med Mol Imaging 37: 1935-1942.