The influence of P-glycoprotein expression and its inhibitors on the distribution of doxorubicin in breast tumors

BMC Cancer

Volumn 9, Issue , 2009, Pages 356-

  Patel, Krupa J ^a   Tannock, Ian F ^a,b  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; GLYCOPROTEIN P; GLYCOPROTEIN P INHIBITOR; VALSPODAR; VERAPAMIL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BREAST CANCER; BREAST TUMOR; CELL HETEROGENEITY; CONTROLLED STUDY; DRUG DISTRIBUTION; DRUG PENETRATION; FEMALE; IMAGE ANALYSIS; IMMUNOFLUORESCENCE; IN VIVO STUDY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; TUMOR GROWTH;

EID: 70450270719     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/1471-2407-9-356     Document Type: Article

References (49)

1. Baguley BC, Finlay GJ. Pharmacokinetic/cytokinetic principles in the chemotherapy of solid tumours. Clinical and experimental pharmacology & physiology 1995, 22(11):825-828. 10.1111/j.1440-1681.1995.tb01943.x, 8593737.
2. Durand RE. Slow penetration of anthracyclines into spheroids and tumors: a therapeutic advantage?. Cancer chemotherapy and pharmacology 1990, 26(3):198-204. 10.1007/BF02897199, 2357767.
3. Erlanson M, Daniel-Szolgay E, Carlsson J. Relations between the penetration, binding and average concentration of cytostatic drugs in human tumour spheroids. Cancer chemotherapy and pharmacology 1992, 29(5):343-353. 10.1007/BF00686002, 1551172.
4. Kerr DJ, Kaye SB. Aspects of cytotoxic drug penetration, with particular reference to anthracyclines. Cancer chemotherapy and pharmacology 1987, 19(1):1-5. 10.1007/BF00296245, 3545523.
5. Tunggal JK, Cowan DS, Shaikh H, Tannock IF. Penetration of anticancer drugs through solid tissue: a factor that limits the effectiveness of chemotherapy for solid tumors. Clin Cancer Res 1999, 5(6):1583-1586.
6. Lankelma J, Dekker H, Luque FR, Luykx S, Hoekman K, Valk P, van Diest PJ, Pinedo HM. Doxorubicin gradients in human breast cancer. Clin Cancer Res 1999, 5(7):1703-1707.
7. Primeau AJ, Rendon A, Hedley D, Lilge L, Tannock IF. The distribution of the anticancer drug Doxorubicin in relation to blood vessels in solid tumors. Clin Cancer Res 2005, 11(24 Pt 1):8782-8788. 10.1158/1078-0432.CCR-05-1664, 16361566.
8. Juranka PF, Zastawny RL, Ling V. P-glycoprotein: multidrug-resistance and a superfamily of membrane-associated transport proteins. Faseb J 1989, 3(14):2583-2592.
9. Ling V. Charles F. Kettering Prize. P-glycoprotein and resistance to anticancer drugs. Cancer 1992, 69(10):2603-2609. 10.1002/1097-0142(19920515)69:10<2603::AID-CNCR2820691034>3.0.CO;2-E, 1348966.
10. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nature reviews 2002, 2(1):48-58. 10.1038/nrc706, 11902585.
11. Goldstein LJ, Galski H, Fojo A, Willingham M, Lai SL, Gazdar A, Pirker R, Green A, Crist W, Brodeur GM. Expression of a multidrug resistance gene in human cancers. J Natl Cancer Inst 1989, 81(2):116-124. 10.1093/jnci/81.2.116, 2562856.
12. Bradley G, Ling V. P-glycoprotein, multidrug resistance and tumor progression. Cancer Metastasis Rev 1994, 13(2):223-233. 10.1007/BF00689638, 7923552.
13. Chico I, Kang MH, Bergan R, Abraham J, Bakke S, Meadows B, Rutt A, Robey R, Choyke P, Merino M. Phase I study of infusional paclitaxel in combination with the P-glycoprotein antagonist PSC 833. J Clin Oncol 2001, 19(3):832-842.
14. Bates S, Kang M, Meadows B, Bakke S, Choyke P, Merino M, Goldspiel B, Chico I, Smith T, Chen C. A Phase I study of infusional vinblastine in combination with the P-glycoprotein antagonist PSC 833 (valspodar). Cancer 2001, 92(6):1577-1590. 10.1002/1097-0142(20010915)92:6<1577::AID-CNCR1484>3.0.CO;2-H, 11745237.
15. Ferry DR, Traunecker H, Kerr DJ. Clinical trials of P-glycoprotein reversal in solid tumours. Eur J Cancer 1996, 32A(6):1070-1081. 10.1016/0959-8049(96)00091-3, 8763349.
16. Krishna R, Mayer LD. Multidrug resistance (MDR) in cancer. Mechanisms, reversal using modulators of MDR and the role of MDR modulators in influencing the pharmacokinetics of anticancer drugs. Eur J Pharm Sci 2000, 11(4):265-283. 10.1016/S0928-0987(00)00114-7, 11033070.
17. Krishna R, Mayer LD. Liposomal doxorubicin circumvents PSC 833-free drug interactions, resulting in effective therapy of multidrug-resistant solid tumors. Cancer research 1997, 57(23):5246-5253.
18. Krishna R, St-Louis M, Mayer LD. Increased intracellular drug accumulation and complete chemosensitization achieved in multidrug-resistant solid tumors by co-administering valspodar (PSC 833) with sterically stabilized liposomal doxorubicin. Int J Cancer 2000, 85(1):131-141. 10.1002/(SICI)1097-0215(20000101)85:1<131::AID-IJC23>3.0.CO;2-R, 10585596.
19. Wang JC, Liu XY, Lu WL, Chang A, Zhang Q, Goh BC, Lee HS. Pharmacokinetics of intravenously administered stealth liposomal doxorubicin modulated with verapamil in rats. Eur J Pharm Biopharm 2006, 62(1):44-51. 10.1016/j.ejpb.2005.06.004, 16126379.
20. Tunggal JK, Melo T, Ballinger JR, Tannock IF. The influence of expression of P-glycoprotein on the penetration of anticancer drugs through multicellular layers. Int J Cancer 2000, 86(1):101-107. 10.1002/(SICI)1097-0215(20000401)86:1<101::AID-IJC16>3.0.CO;2-I, 10728602.
21. Martin C, Walker J, Rothnie A, Callaghan R. The expression of P-glycoprotein does influence the distribution of novel fluorescent compounds in solid tumour models. British journal of cancer 2003, 89(8):1581-1589. 2394330, 14562035, 10.1038/sj.bjc.6601300.
22. Kyle AH, Huxham LA, Yeoman DM, Minchinton AI. Limited tissue penetration of taxanes: a mechanism for resistance in solid tumors. Clin Cancer Res 2007, 13(9):2804-2810. 10.1158/1078-0432.CCR-06-1941, 17473214.
23. Less JR, Skalak TC, Sevick EM, Jain RK. Microvascular architecture in a mammary carcinoma: branching patterns and vessel dimensions. Cancer research 1991, 51(1):265-273.
24. Stephens TC, Peacock JH. Tumour volume response, initial cell kill and cellular repopulation in B16 melanoma treated with cyclophosphamide and 1-(2-chloroethyl)-3-cyclohexyl-1-nitrosourea. British journal of cancer 1977, 36(3):313-321. 2025422, 921888.
25. Milas L, Nakayama T, Hunter N, Jones S, Lin TM, Yamada S, Thames H, Peters L. Dynamics of tumor cell clonogen repopulation in a murine sarcoma treated with cyclophosphamide. Radiother Oncol 1994, 30(3):247-253. 10.1016/0167-8140(94)90465-0, 8209009.
26. Davis AJ, Tannock JF. Repopulation of tumour cells between cycles of chemotherapy: a neglected factor. The lancet oncology 2000, 1:86-93. 10.1016/S1470-2045(00)00019-X, 11905673.
27. Wu L, Tannock IF. Effect of the selective estrogen receptor modulator arzoxifene on repopulation of hormone-responsive breast cancer xenografts between courses of chemotherapy. Clin Cancer Res 2005, 11(22):8195-8200. 10.1158/1078-0432.CCR-05-1258, 16299252.
28. Wu L, Tannock IF. Repopulation in murine breast tumors during and after sequential treatments with cyclophosphamide and 5-fluorouracil. Cancer research 2003, 63(9):2134-2138.
29. Huxham LA, Kyle AH, Baker JH, Nykilchuk LK, Minchinton AI. Microregional effects of gemcitabine in HCT-116 xenografts. Cancer research 2004, 64(18):6537-6541. 10.1158/0008-5472.CAN-04-0986, 15374965.
30. Sakata K, Kwok TT, Gordon GR, Waleh NS, Sutherland RM. Resistance to verapamil sensitization of multidrug-resistant cells grown as multicellular spheroids. Int J Cancer 1994, 59(2):282-286. 10.1002/ijc.2910590222, 7927930.
31. Zacherl J, Hamilton G, Thalhammer T, Riegler M, Cosentini EP, Ellinger A, Bischof G, Schweitzer M, Teleky B, Koperna T. Inhibition of P-glycoprotein-mediated vinblastine transport across HCT-8 intestinal carcinoma monolayers by verapamil, cyclosporine A and SDZ PSC 833 in dependence on extracellular pH. Cancer Chemother Pharmacol 1994, 34(2):125-132. 10.1007/BF00685929, 7910786.
32. Wartenberg M, Frey C, Diedershagen H, Ritgen J, Hescheler J, Sauer H. Development of an intrinsic P-glycoprotein-mediated doxorubicin resistance in quiescent cell layers of large, multicellular prostate tumor spheroids. Int J Cancer 1998, 75(6):855-863. 10.1002/(SICI)1097-0215(19980316)75:6<855::AID-IJC7>3.0.CO;2-U, 9506530.
33. Ouar Z, Bens M, Vignes C, Paulais M, Pringel C, Fleury J, Cluzeaud F, Lacave R, Vandewalle A. Inhibitors of vacuolar H+-ATPase impair the preferential accumulation of daunomycin in lysosomes and reverse the resistance to anthracyclines in drug-resistant renal epithelial cells. The Biochemical journal 2003, 370(Pt 1):185-193. 1223162, 12435274, 10.1042/BJ20021411.
34. Giaccone G, Linn SC, Welink J, Catimel G, Stieltjes H, Vijgh WJ, Eeltink C, Vermorken JB, Pinedo HM. A dose-finding and pharmacokinetic study of reversal of multidrug resistance with SDZ PSC 833 in combination with doxorubicin in patients with solid tumors. Clin Cancer Res 1997, 3(11):2005-2015.
35. Colley MWV, SE G. Incidence of P-glycoprotein over epxression and multidrug resistance (MDR) reversal in adult soft tissue sarcoma. European Journal of Cancer 2000, 36:881-888. 10.1016/S0959-8049(00)00032-0, 10785593.
36. Tidefelt U, Sundman-Engberg B, Paul C. Intracellular uptake and cytotoxic effect in vitro of doxorubicin and epirubicin in human leukemic and normal hematopoietic cells. Cancer chemotherapy and pharmacology 1991, 29(1):7-12. 10.1007/BF00686328, 1742852.
37. Mayer LD, Lim KT, Hartley D. Identification of two distinct intracellular sites that contribute to the modulation of multidrug resistance in P388/ADR cells expressing P-glycoprotein. Journal of experimental therapeutics & oncology 2002, 2(2):107-120. 10.1046/j.1359-4117.2002.1009x.x, 12415627.
38. Ward JP, King JR. Mathematical modelling of drug transport in tumour multicell spheroids and monolayer cultures. Math Biosci 2003, 181(2):177-207. 10.1016/S0025-5564(02)00148-7, 12445761.
39. Sinek JP, Sanga S, Zheng X, Frieboes HB, Ferrari M, Cristini V. Predicting drug pharmacokinetics and effect in vascularized tumors using computer simulation. Journal of mathematical biology 2009, 58(4-5):485-510. 10.1007/s00285-008-0214-y, 18781304.
40. El-Kareh AW, Secomb TW. Two-mechanism peak concentration model for cellular pharmacodynamics of Doxorubicin. Neoplasia (New York, NY) 2005, 7(7):705-713.
41. Jackson TL. Intracellular accumulation and mechanism of action of doxorubicin in a spatio-temporal tumor model. J Theor Biol 2003, 220(2):201-213. 10.1006/jtbi.2003.3156, 12468292.
42. Alarcon T, Byrne HM, Maini PK. A mathematical model of the effects of hypoxia on the cell-cycle of normal and cancer cells. J Theor Biol 2004, 229(3):395-411. 10.1016/j.jtbi.2004.04.016, 15234206.
43. Alarcon T, Byrne HM, Maini PK. Towards whole-organ modelling of tumour growth. Progress in biophysics and molecular biology 2004, 85(2-3):451-472. 10.1016/j.pbiomolbio.2004.02.004, 15142757.
44. Frieboes HB, Edgerton ME, Fruehauf JP, Rose FR, Worrall LK, Gatenby RA, Ferrari M, Cristini V. Prediction of drug response in breast cancer using integrative experimental/computational modeling. Cancer research 2009, 69(10):4484-4492. 10.1158/0008-5472.CAN-08-3740, 19366802.
45. Belpomme D, Gauthier S, Pujade-Lauraine E, Facchini T, Goudier MJ, Krakowski I, Netter-Pinon G, Frenay M, Gousset C, Marie FN. Verapamil increases the survival of patients with anthracycline-resistant metastatic breast carcinoma. Ann Oncol 2000, 11(11):1471-1476. 10.1023/A:1026556119020, 11142488.
46. Carlson RW, O'Neill AM, Goldstein LJ, Sikic BI, Abramson N, Stewart JA, Davidson NE, Wood WC. A pilot phase II trial of valspodar modulation of multidrug resistance to paclitaxel in the treatment of metastatic carcinoma of the breast (E1195): a trial of the Eastern Cooperative Oncology Group. Cancer investigation 2006, 24(7):677-681. 10.1080/07357900600981349, 17118777.
47. Ries F, Dicato M. Treatment of advanced and refractory breast cancer with doxorubicin, vincristine and continuous infusion of verapamil. A phase I-II clinical trial. Medical oncology and tumor pharmacotherapy 1991, 8(1):39-43.
48. Taylor CW, Dalton WS, Mosley K, Dorr RT, Salmon SE. Combination chemotherapy with cyclophosphamide, vincristine, adriamycin, and dexamethasone (CVAD) plus oral quinine and verapamil in patients with advanced breast cancer. Breast Cancer Res Treat 1997, 42(1):7-14. 10.1023/A:1005716214718, 9116320.
49. ten Tije AJ, Synold TW, Spicer D, Verweij J, Doroshow JH, Sparreboom A. Effect of valspodar on the pharmacokinetics of unbound paclitaxel. Invest New Drugs 2003, 21(3):291-298. 10.1023/A:1025412509730, 14578679.