Nilotinib counteracts P-glycoprotein-mediated multidrug resistance and synergizes the antitumoral effect of doxorubicin in soft tissue sarcomas

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Villar, Victor Hugo ^a   Vögler, Oliver ^a   Martínez Serra, Jordi ^a,b   Ramos, Rafael ^a,b   Calabuig Fariñas, Silvia ^a,b   Gutiérrez, Antonio ^a,b   Barceló, Francisca ^a   Martín Broto, Javier ^a,b   Alemany, Regina ^a  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b HOSPITAL UNIVERSITARIO SON ESPASES   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; GLYCOPROTEIN P; IMATINIB; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MULTIDRUG RESISTANCE PROTEIN 1; NILOTINIB;

ANTINEOPLASTIC ACTIVITY; ANTIPROLIFERATIVE ACTIVITY; ARTICLE; CANCER CELL; CANCER INHIBITION; CELL COUNT; CONTROLLED STUDY; DRUG POTENCY; DRUG POTENTIATION; DRUG RETENTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; LEIOMYOSARCOMA; MAJOR CLINICAL STUDY; MOLECULAR MECHANICS; MULTIDRUG RESISTANCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; SOFT TISSUE SARCOMA; SYNOVIAL SARCOMA; UPREGULATION;

ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DOXORUBICIN; DRUG RESISTANCE, MULTIPLE; DRUG SYNERGISM; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; P-GLYCOPROTEIN; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; PYRIMIDINES; SARCOMA; SIGNAL TRANSDUCTION;

EID: 84861473905     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037735     Document Type: Article

References (44)

1. Schoenfeld DA, Rosenbaum C, Horton J, Wolter JM, Falkson G, et al. (1982) A comparison of adriamycin versus vincristine and adriamycin, and cyclophosphamide versus vincristine, actinomycin-D, and cyclophosphamide for advanced sarcoma. Cancer 50: 2757-2762.
2. Mealey KL, Barhoumi R, Rogers K, Kochevar DT, (1998) Doxorubicin induced expression of P-glycoprotein in a canine osteosarcoma cell line. Cancer Lett 126: 187-192.
3. Abolhoda A, Wilson AE, Ross H, Danenberg PV, Burt M, et al. (1999) Rapid activation of MDR1 gene expression in human metastatic sarcoma after in vivo exposure to doxorubicin. Clin Cancer Res 5: 3352-3356.
4. Nichols GL, (2003) Tyrosine kinase inhibitors as cancer therapy. Cancer Invest 21: 758-771.
5. Arora A, Scholar EM, (2005) Role of tyrosine kinase inhibitors in cancer therapy. J Pharmacol Exp Ther 315: 971-979.
6. Hochhaus A, O'Brien SG, Guilhot F, Druker BJ, Branford S, et al. (2009) Six-year follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia 23: 1054-1061.
7. Debiec-Rychter M, Dumez H, Judson I, Wasag B, Verweij J, et al. (2004) Use of c-KIT/PDGFRA mutational analysis to predict the clinical response to imatinib in patients with advanced gastrointestinal stromal tumours entered on phase I and II studies of the EORTC Soft Tissue and Bone Sarcoma Group. Eur J Cancer 40: 689-695.
8. Shah NP, Nicoll JM, Nagar B, Gorre ME, Paquette RL, et al. (2002) Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2: 117-125.
9. Gramza AW, Corless CL, Heinrich MC, (2009) Resistance to Tyrosine Kinase Inhibitors in Gastrointestinal Stromal Tumors. Clin Cancer Res 15: 7510-7518.
10. Demetri GD, van Oosterom AT, Garrett CR, Blackstein ME, Shah MH, et al. (2006) Efficacy and safety of sunitinib in patients with advanced gastrointestinal stromal tumour after failure of imatinib: a randomised controlled trial. Lancet 368: 1329-38.
11. Breccia M, Alimena G, (2010) Nilotinib: a second-generation tyrosine kinase inhibitor for chronic myeloid leukemia. Leuk Res 34: 129-134.
12. Quintas-Cardama A, Cortes J, (2008) Nilotinib: a phenylamino-pyrimidine derivative with activity against BCR-ABL, KIT and PDGFR kinases. Future Oncol 4: 611-621.
13. Prenen H, Guetens G, de Boeck G, Debiec-Rychter M, Manley P, et al. (2006) Cellular uptake of the tyrosine kinase inhibitors imatinib and AMN107 in gastrointestinal stromal tumor cell lines. Pharmacology 77: 11-16.
14. Swords R, Mahalingam D, Padmanabhan S, Carew J, Giles F, (2009) Nilotinib: optimal therapy for patients with chronic myeloid leukemia and resistance or intolerance to imatinib. Drug Des Devel Ther 3: 89-101.
15. Reichardt P, (2008) Novel approaches to imatinib- and sunitinib-resistant GIST. Curr Oncol Rep 10: 344-349.
16. Tiwari AK, Sodani K, Wang SR, Kuang YH, Ashby CR Jr, et al. (2009) Nilotinib (AMN107, Tasigna) reverses multidrug resistance by inhibiting the activity of the ABCB1/Pgp and ABCG2/BCRP/MXR transporters. Biochem Pharmacol 78: 153-161.
17. Gooskens SL, Oranje AP, van Adrichem LN, de Waard-van der Spek FB, den Hollander JC, et al. (2010) Imatinib mesylate for children with dermatofibrosarcoma protuberans (DFSP). Pediatr Blood Cancer 55: 369-373.
18. Homet Moreno B, Garralda Cabanas E, Hitt R, (2010) Tyrosine kinase inhibitors in treating soft tissue sarcomas: sunitinib in non-GIST sarcomas. Clin Transl Oncol 12: 468-472.
19. Steel GG, Peckham MJ, (1979) Exploitable mechanisms in combined radiotherapy-chemotherapy: the concept of additivity. Int J Radiat Oncol Biol Phys 5: 85-91.
20. Tallarida RJ, (2001) Drug synergism: its detection and applications. J Pharmacol Exp Ther 298: 865-872.
21. Serra JM, Gutierrez A, Alemany R, Navarro M, Ros T, et al. (2008) Inhibition of c-Myc down-regulation by sustained extracellular signal-regulated kinase activation prevents the antimetabolite methotrexate- and gemcitabine-induced differentiation in non-small-cell lung cancer cells. Mol Pharmacol 73: 1679-1687.
22. Gronchi A, Frustaci S, Mercuri M, Martin Broto J, Lopez-Pousa A, et al. (2010) Localized, high-risk soft tissue sarcomas (STS) of the extremities and trunk wall in adults: Three versus five cycles of full-dose anthracyclin and ifosfamide adjuvant chemotherapy: A phase III randomized trial from the Italian Sarcoma Group (ISG) and Spanish Sarcoma Group (GEIS). J Clin Oncol 28: 15s (suppl; abstr 10003).
23. Peng B, Lloyd P, Schran H, (2005) Clinical pharmacokinetics of imatinib. Clin Pharmacokinet 44: 879-894.
24. Guo X, Ma N, Wang J, Song J, Bu X, et al. (2008) Increased p38-MAPK is responsible for chemotherapy resistance in human gastric cancer cells. BMC Cancer 8: 375.
25. Lu M, Xiao L, Hu J, Deng S, Xu Y, (2008) Targeting of p38 mitogen-activated protein kinases to early growth response gene 1 (EGR-1) in the human paclitaxel-resistance ovarian carcinoma cells. J Huazhong Univ Sci Technolog Med Sci 28: 451-455.
26. Montemurro M, Schoffski P, Reichardt P, Gelderblom H, Schutte J, et al. (2009) Nilotinib in the treatment of advanced gastrointestinal stromal tumours resistant to both imatinib and sunitinib. Eur J Cancer 45: 2293-2297.
27. Manley PW, Stiefl N, Cowan-Jacob SW, Kaufman S, Mestan J, et al. (2010) Structural resemblances and comparisons of the relative pharmacological properties of imatinib and nilotinib. Bioorg Med Chem 18: 6977-6986.
28. Potti A, Ganti AK, Foster H, Knox S, Hebert BJ, et al. (2004) Immunohistochemical detection of HER-2/neu, c-kit (CD117) and vascular endothelial growth factor (VEGF) overexpression in soft tissue sarcomas. Anticancer Res 24: 333-337.
29. Lubieniecka JM, Nielsen TO, (2005) cDNA microarray-based translational research in soft tissue sarcoma. J Surg Oncol 92: 267-271.
30. Mahadevan D, Cooke L, Riley C, Swart R, Simons B, et al. (2007) A novel tyrosine kinase switch is a mechanism of imatinib resistance in gastrointestinal stromal tumors. Oncogene 26: 3909-3919.
31. Gonzalez I, Andreu EJ, Panizo A, Inoges S, Fontalba A, et al. (2004) Imatinib inhibits proliferation of Ewing tumor cells mediated by the stem cell factor/KIT receptor pathway, and sensitizes cells to vincristine and doxorubicin-induced apoptosis. Clin Cancer Res 10: 751-761.
32. DeAngelo DJ, Attar EC, (2010) Use of dasatinib and nilotinib in imatinib-resistant chronic myeloid leukemia: translating preclinical findings to clinical practice. Leuk Lymphoma 51: 363-375.
33. Manley PW, Drueckes P, Fendrich G, Furet P, Liebetanz J, et al. (2010) Extended kinase profile and properties of the protein kinase inhibitor nilotinib. Biochim Biophys Acta 1804 445-453.
34. Peng CL, Guo W, Ji T, Ren T, Yang Y, et al. (2009) Sorafenib induces growth inhibition and apoptosis in human synovial sarcoma cells via inhibiting the RAF/MEK/ERK signaling pathway. Cancer Biol Ther 8: 1729-1736.
35. Watanabe T, Tsuda M, Tanaka S, Ohba Y, Kawaguchi H, et al. (2009) Adaptor protein Crk induces Src-dependent activation of p38 MAPK in regulation of synovial sarcoma cell proliferation. Mol Cancer Res 7: 1582-1592.
36. White DL, Saunders VA, Dang P, Engler J, Zannettino AC, et al. (2006) OCT-1-mediated influx is a key determinant of the intracellular uptake of imatinib but not nilotinib (AMN107): reduced OCT-1 activity is the cause of low in vitro sensitivity to imatinib. Blood 108: 697-704.
37. 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.
38. O'Connor R, (2007) The pharmacology of cancer resistance. Anticancer Res 27: 1267-1272.
39. Davies A, Jordanides NE, Giannoudis A, Lucas CM, Hatziieremia S, et al. (2009) Nilotinib concentration in cell lines and primary CD34(+) chronic myeloid leukemia cells is not mediated by active uptake or efflux by major drug transporters. Leukemia 23: 1999-2006.
40. Hamada A, Miyano H, Watanabe H, Saito H, (2003) Interaction of imatinib mesilate with human P-glycoprotein. J Pharmacol Exp Ther 307: 824-828.
41. Milano A, Apice G, Ferrari E, Fazioli F, de Rosa V, et al. (2006) New emerging drugs in soft tissue sarcoma. Crit Rev Oncol Hematol 59: 74-84.
42. Le Cesne A, Judson I, Crowther D, Rodenhuis S, Keizer HJ, et al. (2000) Randomized phase III study comparing conventional-dose doxorubicin plus ifosfamide versus high-dose doxorubicin plus ifosfamide plus recombinant human granulocyte-macrophage colony-stimulating factor in advanced soft tissue sarcomas: A trial of the European Organization for Research and Treatment of Cancer/Soft Tissue and Bone Sarcoma Group. J Clin Oncol 18: 2676-2684.
43. Gottesman MM, Pastan I, (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62: 385-427.
44. Maurel J, Martins AS, Poveda A, Lopez-Guerrero JA, Cubedo R, et al. (2010) Imatinib plus low-dose doxorubicin in patients with advanced gastrointestinal stromal tumors refractory to high-dose imatinib: a phase I-II study by the Spanish Group for Research on Sarcomas. Cancer 116: 3692-3701.