Advertisement

Multidrug Resistance in Solid Tumor and Its Reversal

  • Ho Lun Wong
  • Xiao Yu Wu
  • Reina Bendayan
Chapter

Chemotherapy was first used for the treatment of advanced lymphomas in the 1940s [1]. Since then several classes of chemotherapeutic compounds such as alkylating agents, antimetabolites, anthracyclines, plant alkaloids, and later topoisomerase inhibitors and taxanes have been identified or synthesized to treat various forms of cancer [2, 3]. Although numerous in vitro and animal studies have demonstrated their effectiveness in inducing cancer cell death (cytotoxic) or cell growth arrest (cytostatic), these promising anticancer activities seen in the controlled environment of the laboratory frequently do not translate well into the expected clinical outcomes[4–8].

Keywords

Drug Carrier Breast Cancer Resistance Protein Solid Lipid Nanoparticles Anticancer Compound Drug Resistance Reversal 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. 1.
    Goodman LS, Wintrobe MM, Dameshek W, Goodman MJ, Gilman A, McLennan MT. Nitrogen mustard therapy. JAMA 1946; 132: 126–132.Google Scholar
  2. 2.
    Hirsch J. An anniversary for cancer chemotherapy. JAMA 2006; 296: 1518–1520.PubMedGoogle Scholar
  3. 3.
    Ewesuedo RB, Ratain MJ. Principles of cancer chemotherapy. In: Vokes EE, Golomb HM (ed). Oncologic Therapies. Springer, New York. 2003; pp. 19–67.Google Scholar
  4. 4.
    Baird RD, Kaye SB. Drug resistance reversal – are we getting closer. Eur J Cancer 2003; 39: 2450–2461.PubMedGoogle Scholar
  5. 5.
    Mimeault M, Brand RE, Sasson AA, Batra SK. Recent advances on the molecular mechanisms involved in pancreatic cancer progression and therapies. Pancreas 2005; 31: 301–316.PubMedGoogle Scholar
  6. 6.
    Mimeault M, Batra SK. Recent advances on multiple tumorigenic cascades involved in prostatic cancer progress and targeting therapies. Carcinogenesis 2006; 24: 1–22.Google Scholar
  7. 7.
    Carrick S, Parker S, Wilcken N, Ghersi D, Marzo M, Simes J. Single agent versus combination chemotherapy for metastatic breast cancer. In: The Cochrane library (ed). The Cochrane Database of Systematic Reviews. John Wiley and Sons, Chichester, 2005.Google Scholar
  8. 8.
    Gieseler F, Rudolph P, Kloeppel G, Foelsch UR. Resistance mechanisms of gastrointestinal cancers: why does conventional chemotherapy fail? Int J Colorectal Disease 2003; 18: 470–480.Google Scholar
  9. 9.
    Balmer CM, Valley AW, Iannucci A. Cancer treatment and chemotherapy. In: DiPiro JT, Talbert RL, Yee GC et al. (ed). Pharmacotherapy: A Pathophysiologic Approach. McGraw-Hill, New York, 2005; pp. 2279–2328.Google Scholar
  10. 10.
    Scardinao PT, Weaver R, Hudson MA. Early detection of prostate cancer. Hum Pathol 1992; 23: 211–222.Google Scholar
  11. 11.
    NIH Consensus Development Conference Statement. Adjuvant therapy for breast cancer 2000, NIH. http://www.nih.gov. Accessed Sept. 25, 2008.
  12. 12.
    Biedler JL, Riehm H. Cellular resistance to actinomycin D in Chinese hamster cells in vitro: cross-resistance, radioautographic, and cytogenic studies. Cancer Res 1970; 30: 1174–1184.PubMedGoogle Scholar
  13. 13.
    Juliano RL, Ling V. A surface glycoprotein modulating drug permeability in Chinese hamster ovary cell mutants. Biochim Acta1976; 455: 152–162.Google Scholar
  14. 14.
    Glavinas H, Krajcsi P, Cserepes J, Sarkadi B. The role of ABC transporters in drug resistance, metabolism and toxicity. Curr Drug Deliv 2004; 1: 27–42.PubMedGoogle Scholar
  15. 15.
    Riordan JR, Ling V. Purification of P-glycoprotein from plasma membrane vesicles of Chinese hamster ovary cell mutants with reduced colchicine permeability. J Biol Chem 1979; 254: 12701–12705.PubMedGoogle Scholar
  16. 16.
    Riordan JR, Deuchars KK, Norbert AN, Noa A, Jeffrey T, Ling V. Amplification of P-glycoprotein genes in multidrug-resistant mammalian cell lines. Nature 1985; 316: 817–819.PubMedGoogle Scholar
  17. 17.
    Debenham PG, Kartner N, Siminovitch L, Riordan JR, Ling V. DNA-mediated transfer of multiple drug resistance and plasma membrane glycoprotein expression. Mol Cell Biol 1982; 2: 881–889.PubMedGoogle Scholar
  18. 18.
    Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, Stewart AJ, Kurz EU, Duncan AMV, Deeley RG. Overexpression of a transporter gene in a multidrug-resistant human lung-cancer cell-line. Science1992; 258: 1650–1654.PubMedGoogle Scholar
  19. 19.
    Doyle LA, Ross DD. Multidrug resistance mediated by the breast cancer resistance protein BCRP (ABCG2). Oncogene 2003; 22: 7340–7358.PubMedGoogle Scholar
  20. 20.
    Mellor HR, Callaghan R. Resistance to chemotherapy in cancer: A complex and integrated cellular response. Pharmacology 2008; 81: 275–300.PubMedGoogle Scholar
  21. 21.
    Chien AJ, Moasser MM. Cellular mechanisms of resistance to anthracyclines and taxanes in cancer: Intrinsic and acquired. Semin Oncol 2008; 35: S1–S14.PubMedGoogle Scholar
  22. 22.
    Mimeault M, Hauke R, Batra SK. Recent advances on the molecular mechanisms involved in the drug resistance of cancer cells and novel targeting therapies. Clin Pharmacol Therapeutics 2008; 83: 673–691.Google Scholar
  23. 23.
    Thomas H, Coley HM. Overcoming multidrug resistance in cancer: an update on the clinical strategy of inhibiting P-glycoprotein. Cancer Control 2003; 10: 159–165.PubMedGoogle Scholar
  24. 24.
    Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Natl Rev Cancer 2003; 2: 48–58.Google Scholar
  25. 25.
    Dean M, Rzhetsky A, Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res 2001; 11: 1156–1166.PubMedGoogle Scholar
  26. 26.
    Dean M. The human ATP-binding cassette (ABC) transporter superfamily. National Library of Medicine (US), NCBI. http://www.ncbi.nlm.nih.gov/bookshelf/br.fcgi?book=mono_001&part=A137. 2002, Accessed 4 October 2008.
  27. 27.
    Hollenstein K, Frei DC, Locher KP. Structure of an ABC transporter in complex with its binding protein. Nature 2007; 446: 213–216.PubMedGoogle Scholar
  28. 28.
    Davidson AL, Maloney PC. ABC transporters: how small machines do a big job. Trends Microbiol 2007; 15: 448–455.PubMedGoogle Scholar
  29. 29.
    Tamura A, Watanabe M, Saito H, Nakagawa H, Kamachi T, Okura I, Ishikawa T. Functional validation of the genetic polymorphisms of human ATP-binding cassette (ABC) transporter ABCG2: identification of alleles that are defective in porphyrin transport. Mol Pharmacol 2006; 70: 287–296.PubMedGoogle Scholar
  30. 30.
    Fromm MF. The influence of MDR1 polymorphisms on P-glycoprotein expression and function in humans. Adv Drug Deliv Rev 2003; 54: 1295–1310.Google Scholar
  31. 31.
    Gottesman MM. Mechanisms of cancer drug resistance. Ann Rev Med 2002; 53: 615–627.PubMedGoogle Scholar
  32. 32.
    Ambudkar SV, Kimchi-Sarfaty C, Sauna ZE, Gottesman MM. P-glycoprotein: from genomics to mechanism. Oncogene 2003; 22: 7468–7485.PubMedGoogle Scholar
  33. 33.
    Varadi A, Szakacs G, Bakos E, Sarkadi B. P-glycoprotein and the mechanism of multidrug resistance. Novartis Foundation Symposium 2002; 243: 54–65.PubMedGoogle Scholar
  34. 34.
    Eckford PD, Sharom FJ. The reconstituted P-glycoprotein multidrug transporter is a flippase for glucosylceramide and other simple glycosphingolipids. Biochem J 2005; 389: 517–526.PubMedGoogle Scholar
  35. 35.
    Al-Shawi MK, Omote H. The remarkable transport mechanism of P-glycoprotein: a multidrug transporter. J Bioenerg Biomembr 2006; 37: 489–496.Google Scholar
  36. 36.
    Orlowski S, Martin S, Escargueil A. P-glycoprotein and ‘lipid rafts’: some ambiguous mutual relationships (floating on them, building them or meeting them by chance?) Cell Mol Life Sci 2006; 63: 1038–1059.PubMedGoogle Scholar
  37. 37.
    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: 265–283.PubMedGoogle Scholar
  38. 38.
    Jeffrey P, Summerfield SG. Challenges for blood–brain barrier (BBB) screening. Xenobiotica 2007; 37: 1135–1151.PubMedGoogle Scholar
  39. 39.
    Gedeon C, Behravan J, Koren G, Piquette-Miller M. Transport of glyburide by placental ABC transporters: implications in fetal drug exposure. Placenta 2006; 27: 1096–1010.PubMedGoogle Scholar
  40. 40.
    Melaine N, Liénard M, Dorval I, Le Goascogne C, Lejeune H, Jégou B. Multidrug resistance genes and P-glycoprotein in the testis of the rat, mouse, guinea pig, and human. Biol Reprod 2002; 67: 1699–1707.PubMedGoogle Scholar
  41. 41.
    Bunting KD, Zhou S, Lu T, Brian P. Enforced P-glycoprotein pump function in murine bone marrow cells results in expansion of side population stem cells in vitro and repopulating cells in vivo. Blood 2000; 96: 902–909.PubMedGoogle Scholar
  42. 42.
    Johnstone RW, Ruefli AA, Smyth MJ. Multiple physiological functions for multidrug transporter P-glycoprotein. Tr Biochem Sci 2000; 25: 1–6.Google Scholar
  43. 43.
    Ronaldson PT, Bendayan M, Gingras D, Piquette-Miller M, Bendayan R. Cellular localization and functional expression of P-glycoprotein in rat astrocyte cultures. J Neurochem 2004; 89: 788–800.PubMedGoogle Scholar
  44. 44.
    Babakhanian K, Bendayan M, Bendayan R. Localization of P-glycoprotein at the nuclear envelope of rat brain cells. Biochem Biophys Res Commun 2007; 361: 301–306.PubMedGoogle Scholar
  45. 45.
    Allen JD, Brinkhuis RF, van Deemter L, Wijnholds J, Schinkel AH. Extensive contribution of the multidrug transporters P-glycoprotein and Mrp1 to basal drug resistance. Cancer Res 2000; 60: 5761–5766.PubMedGoogle Scholar
  46. 46.
    Leonessa F, Green D, Licht T, Wijinholds J, Schinkel AH. MDA435/LCC6/WT and MDA435/LCC6/mdr1: ascites models of human breast cancer. Br J Cancer 1996; 73: 154–161.PubMedGoogle Scholar
  47. 47.
    Arceci RJ. Can multidrug resistance mechanisms be modified? Brit J Haematol 2000; 110: 285–291.Google Scholar
  48. 48.
    Endicott JA, Ling V. The biochemistry of P-glycoprotein-mediated multidrug resistance. Ann Rev Biochem 1989; 58: 137–171.PubMedGoogle Scholar
  49. 49.
    Johnson WW. P-glycoprotein-mediated efflux as a major factor in the variance of absorption and distribution of drugs: modulation of chemotherapy resistance. Methods Find Exp Clin Pharmacol 2002; 24: 501–514.PubMedGoogle Scholar
  50. 50.
    Campone M, Vavasseur F, Le Cabellec MT, Meflah K, Vallette FM, Oliver L. Induction of chemoresistance in HL-60 cells concomitantly causes a resistance to apoptosis and the synthesis of P-glycoprotein. Leukemia 2001; 15: 1377–1387.PubMedGoogle Scholar
  51. 51.
    Hahn SM, Russo A, Cook JA, Mitchell JB. A multidrug-resistant breast cancer line induced by weekly exposure to doxorubicin. Int J Oncol 1999; 14: 273–279.PubMedGoogle Scholar
  52. 52.
    Mayer R, Kartenbeck J, Buchler M, Jedlitschky G, Leier I, Keppler D. Expression of the MRP gene-encoded conjugate export pump in liver and its selective absence from the canalicular membrane in transport- deficient mutant hepatocytes. J Cell Biol 1995; 131: 137–150.PubMedGoogle Scholar
  53. 53.
    Evers R, Kool M, van Deemter L, Janssen H, Calafat J, Oomen LC, Paulusma CC, Oude Elferink RP, Baas F, Schinkel AH, Borst P. Drug export activity of the human canalicular multispecific organic anion transporter in polarized kidney MDCK cells expressing cMOAT (MRP2) cDNA. J Clin Invest 1998; 101: 1310–1319.PubMedGoogle Scholar
  54. 54.
    Doyle LA, Yang W, Abruzzo LV. A multidrug resistance transporter from human MCF-7 breast cancer cells. Proc Natl Acad Sci USA 1998; 95: 15665–15670.PubMedGoogle Scholar
  55. 55.
    Maliepaard M, Scheffer GL, Faneyte IF, van Gastelen MA, Pijnenborg AC, Schinkel AH, van De Vijver MJ, Scheper RJ, Schellens JH. Subcellular localization and distribution of the breast cancer resistance protein transporter in normal human tissues. Cancer Res 2001; 61: 3458–3464.PubMedGoogle Scholar
  56. 56.
    Diestra JE, Scheffer GL, Catala II, Maliepaard M, Schellens JH, Scheper RJ, Germà-Lluch JR, Izquierdo MA. Frequent expression of the multi-drug resistance-associated protein BCRP/MXR/ABCP/ABCG2 in human tumours detected by the BXP-21 monoclonal antibody in paraffin-embedded material. J Pathol 2002; 198: 213–219.PubMedGoogle Scholar
  57. 57.
    Brangi M, Litman T, Ciotti M, Nishiyama K, Kohlhagen G, Takimoto C, Robey R, Pommier Y, Fojo T, Bates SE. Camptothecin resistance: role of the ATP-binding cassette (ABC), mitoxantrone-resistance half-transporter (MXR), and potential for glucuronidation in MXR-expressing cells. Cancer Res 1999; 59: 5938–5946.PubMedGoogle Scholar
  58. 58.
    Maliepaard M, van Gastelen MA, de Jong LA, Pluim D, van Waardenburg RC, Ruevekamp-Helmers MC, Floot BG, Schellens JH. Overexpression of the BCRP/MXR/ABCP gene in a topotecan-selected ovarian tumor cell line. Cancer Res 1999; 59: 4559–4563.PubMedGoogle Scholar
  59. 59.
    Ross DD, Yang W, Abruzzo LV, Dalton WS, Schneider E, Lage H, Dietel M, Greenberger L, Cole SP, Doyle LA. Atypical multidrug resistance: breast cancer resistance protein messenger RNA expression in mitoxantrone-selected cell lines. J Natl Cancer Inst 1999; 91: 429–433.PubMedGoogle Scholar
  60. 60.
    Krishnamurthy P, Schuetz JD. Role of ABCG2/BCRP in biology and medicine. Annu Rev Pharmcol Toxicol 2006; 46: 381–410.Google Scholar
  61. 61.
    Sugimoto Y, Tsukahara S, Ishikawa E, Mitsuhashi J. Breast cancer resistance protein: molecular target for anticancer drug resistance and pharmacokinetics/pharmacodynamics. Cancer Sci 2005; 96: 457–465.PubMedGoogle Scholar
  62. 62.
    Boonstra R, Timmer-Bosscha H, van Echten-Arends J, van der Kolk DM, van den Berg A, de Jong B, Tew KD, Poppema S, de Vries EGE. Mitoxantrone resistance in a small cell lung cancer cell line is associated with ABCA2 upregulation. Brit J Cancer 2004; 90: 2411–2417.PubMedGoogle Scholar
  63. 63.
    Mack JT, Beljanski V, Tew KD, Townsend DM. The ATP-binding cassette transporter ABCA2 as a mediator of intracellular trafficking. Biomed Pharmacother 2006; 60: 587–592.PubMedGoogle Scholar
  64. 64.
    Efferth T, Gillet JP, Sauerbrey A, Bertholet V, de Longueville FO, Remacle J, Steinbach D. Expression profiling of ATP-binding cassette transporters in childhood T-cell acute lymphoblastic leukemia. Mol Cancer Ther 2006; 5: 1986–1994.PubMedGoogle Scholar
  65. 65.
    Steinbach D, Gillet JP, Sauerbrey A, Bernd Gruhn, Dawczynski K, Bertholet V, de Longueville F, Zintl F, Remacle J, Efferth T. ABCA3 as a possible cause of drug resistance in childhood acute myeloid leukemia. Clin Cancer Res 2006; 12: 4357–4363.PubMedGoogle Scholar
  66. 66.
    Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005; 5: 275–284.PubMedGoogle Scholar
  67. 67.
    Klopman G, Shi LM, Ramu A. Quantitative structure–activity relationship of multidrug resistance reversal agents. Mol Pharmacol 1997; 52: 323–334.PubMedGoogle Scholar
  68. 68.
    Roe M, Folkes A, Ashworth P Brumwell J, Chima L, Hunjan S, Pretswell I, Dangerfield W, Ryder H, Charlton P. Reversal of P-glycoprotein mediated multidrug resistance by novel anthranilamide derivatives. Bioorg Med Chem Lett 1999; 9: 595–600.PubMedGoogle Scholar
  69. 69.
    Starling JJ, Shepard RL, Cao J, Law KL, Norman BH, Kroin JS, Ehlhardt WJ, Baughman TM, Winter MA, Bell MG, Shih C, Gruber J, Elmquist WF, Dantzig AH. Pharmacological characterization of LY335979: A potent cyclopropyldibenzosuberane modulator of P-glycoprotein. Adv Enzyme Regul 1997; 37: 335–347.PubMedGoogle Scholar
  70. 70.
    van Zuylen L, Nooter K, Sparreboom A, Verweij J. Development of multidrug-resistance convertors: sense or nonsense? Invest New Drugs 2000; 18: 205–220.PubMedGoogle Scholar
  71. 71.
    Newman MJ, Rodarte JC, Benbatoul KD, Romano SJ, Zhang C, Krane S, Moran EJ, Uyeda RT, Dixon R, Guns ES, Mayer LD. Discovery and characterization of OC144-093, a novel inhibitor of P-glycoprotein-mediated multidrug resistance. Cancer Res 2000; 60: 2964–2972.PubMedGoogle Scholar
  72. 72.
    Wallstab A, Koester M, Bohme M, Keppler D. Selective inhibition of MDR1 P-glycoprotein-mediated transport by the acridone carboxamide derivative GG918. Br J Cancer 1999; 79: 1053–1060.PubMedGoogle Scholar
  73. 73.
    Coley HM, Verrill MW, Gregson SE. Incidence of P-glycoprotein over expression and multidrug resistance (MDR) reversal in adult soft tissue sarcoma. Eur J Cancer 2000; 36: 881–888.PubMedGoogle Scholar
  74. 74.
    Mistry P, Stewart AJ, Dangerfield W, Okiji S, Liddle C, Bootle D, Plumb JA, Templeton D, Charlton P. In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576. Cancer Res 2001; 61: 749–758.PubMedGoogle Scholar
  75. 75.
    Agrawal M, Abraham J, Balis FM, Edgerly M, Stein WD, Bates S, Fojo T, Chen CC. 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.PubMedGoogle Scholar
  76. 76.
    Bakker M, van der Graaf WT, Piers DA, Franssen EJ, Groen HJ, Smit EF, Kool W, Hollema H, Muller EA, deVries EG. 99mTc-Sestamibi scanning with SDZ PSC 833 as a functional detection method for resistance modulation in patients with solid tumours. Anticancer Res 1999; 19: 2349–2353.PubMedGoogle Scholar
  77. 77.
    Peck RA, Hewett J, Harding MW, Wang YM, Chaturvedi PR, Bhatnagar A, Ziessman H, Atkins F, Hawkins MJ. Phase I and pharmacokinetic study of the novel MDR1 and MRP1 inhibitor biricodar administered alone and in combination with doxorubicin. J Clin Oncol 2001; 19: 3130–3141.PubMedGoogle Scholar
  78. 78.
    Fischer V, Rodriguez-Gascon A, Heitz F, Tynes R, Hauck C, Cohen D, Vickers AEM. The multidrug resistance modulator valspodar (PSC 833) is metabolized by human cytochrome P450 3A: Implications for drug-drug interactions and pharmacological activity of the main metabolite. Drug Metab Dispos 1998; 26: 802–811.PubMedGoogle Scholar
  79. 79.
    Wandel C, Kim RB, Kajiji S, Guengerich FP, Wilkinson GR, Wood AJJ. P-glycoprotein and cytochrome P450 3A inhibition: dissociation of inhibitory potencies. Cancer Res 1999; 59: 3944–3948.PubMedGoogle Scholar
  80. 80.
    Nobili S, Landini I, Giglioni B, Mini E. Pharmacological strategies for overcoming multidrug resistance. Current Drug Targets 2006; 7: 861–879.PubMedGoogle Scholar
  81. 81.
    Duhem C, Ries F, Dicato M. What does Multidrug Resistance (MDR) Expression Mean in the Clinic? The Oncologist 1996; 1: 151–158.PubMedGoogle Scholar
  82. 82.
    Sonneveld P, Suciu S, Weijermans P, Beksac M, Neuwirtova R, Solbu G, Lokhorst H, Van der lelie J, Dohner H, Gerhartz H, Segeren CM, Willemze R, Lowenberg B. Cyclosporin A combined with vincristine, doxorubicin and dexamethasone (VAD) compared with VAD alone in patients with advanced refractory multiple myeloma: an EORTC-HOVON randomized phase III study (06914). Br J Haematol 2001; 115: 895–902.PubMedGoogle Scholar
  83. 83.
    Baer MR, George SL, Dodge RK, O'Loughlin KL, Minderman H, Caligiuri MA, Anastasi J, Powell BL, Kolitz JE, Schiffer CA, Bloomfield CD, Larson RA. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: Cancer and Leukemia Group B Study 9720. Blood 2002; 100: 1224–1232.PubMedGoogle Scholar
  84. 84.
    Toppmeyer D, Seidman AD, Pollak M, Russell C, Tkaczuk K, Verma S, Overmoyer B, Garg V, Ette E, Harding MW, Demetri GD. Safety and efficacy of the multidrug resistance inhibitor Incel (biricodar; VX-710) in combination with paclitaxel for advanced breast cancer refractory to paclitaxel. Clin Cancer Res 2002; 8: 670–678.PubMedGoogle Scholar
  85. 85.
    Stavrovskaya AA. Cellular mechanisms of multidrug resistance of tumor cells. Biochemistry 2000; 65: 95–106.PubMedGoogle Scholar
  86. 86.
    Sparreboom A, Planting AS, Jewell RC, van der Burg ME, van der Gaast A, de Bruijin P, Loos WJ, Nooter K, Chndler LH, Paul EM, Wissel PS, Verweij J. Clinical pharmacokinetics of doxorubicin in combination with GF120918, a potent inhibitor of MDR1 P-glycoprotein. Anticancer Drugs 1999; 10: 719–728.PubMedGoogle Scholar
  87. 87.
    Aszalos A, Ladanyi A, Bocsi J, Szende B. Induction of apoptosis in MDR1 expressing cells by daunorubicin with combinations of suboptimal concentrations of P-glycoprotein modulators. Cancer Let 2001; 167: 157–162.Google Scholar
  88. 88.
    Matsumura Y, Maeda H. A new concept for macromolecular therapeutics in cancer chemotherapy: Mechanism of tumoritropic accumulation of proteins and the antitumor agent SMANCS. Cancer Res 1986; 6: 193–210.Google Scholar
  89. 89.
    Northfelt DW, Dezube BJ, Thommes JA, Miller BJ, Fischl MA, Friedman-Kien A, Kaplan LD, Du Mond C, Mamelok RD, Henry DH. Efficacy of pegylated-liposomal doxorubicin in the treatment of AIDS-related Kaposi’s sarcoma after failure of standard chemotherapy. J Clin Oncol 1997; 15: 653–659.PubMedGoogle Scholar
  90. 90.
    Park JW. Liposome-based drug delivery in breast cancer treatment. Breast Cancer Res 2002; 4: 95–99.PubMedGoogle Scholar
  91. 91.
    Popovic N, Brundin P. Therapeutic potential of controlled drug delivery systems in neurodegenerative diseases. Int J Pharmaceut 2006; 314: 120–126.Google Scholar
  92. 92.
    Koziara JM, Lockman PR, Allen DD, Mumper RJ. Paclitaxel nanoparticles for the potential treatment of brain tumors. J Control Release 2004; 99: 259–269.PubMedGoogle Scholar
  93. 93.
    Wong HL, Rauth AM, Bendayan R, Manias JL, Ramaswamy M, Liu Z, Erhan SZ, Wu XY. A new polymer-lipid hybrid nanoparticle system increases cytotoxicity of doxorubicin against multidrug resistant human breast cancer cells. Pharm Res 2006; 23: 1574–1585.PubMedGoogle Scholar
  94. 94.
    Mamot C, Drummond DC, Hong K, Kirpotin DB, Park JW. Liposome-based approaches to overcome anticancer drug resistance. Drug Res Update 2003; 6: 271–279.Google Scholar
  95. 95.
    Hagiwara A, Sakakura C, Shirasu M, Togawa T, Sonoyama Y, Fujiyama J, Ebihara Y, Itoh T, Yamagishi H. Intraperitoneal injection of dextran sulfate as an anti-adherent drug for the prevention of peritoneal metastasis of cancer shows low toxicity in animals. Anti-Cancer Drugs 2000; 11: 393–399.PubMedGoogle Scholar
  96. 96.
    Hu YP, Jarillon S, Dubernet C, Couvreur P, Robert J. On the mechanism of action of doxorubicin encapsulation in nanospheres for the reversal of multidrug resistance. Cancer Chemother Pharmacol 1996; 37: 556–560.PubMedGoogle Scholar
  97. 97.
    Drori S, Eytan GD, Assaraf YG. Potentiation of anticancer-drug cytotoxicity by multidrug-resistance chemosensitizers involves alterations in membrane fluidity leading to increased membrane permeability. Eur J Biochem 1995; 228: 1020–1029.PubMedGoogle Scholar
  98. 98.
    Riehm H, Biedler JL. Potentiation of drug effect by Tween 80 in Chinese Hamster cells resistant to actinomycin D and daunomycin. Cancer Res 1972; 32: 1195–1200.PubMedGoogle Scholar
  99. 99.
    Kabanov AV, Batrakova EV, Alakhov VY. Pluronic block copolymers for overcoming drug resistance in cancer. Adv Drug Del Rev 2002; 54: 759–779.Google Scholar
  100. 100.
    Doige CA, Yu X, Sharom FJ. The effects of lipids and detergents on ATPase activity of P-glycoprotein. Biochim Biophys Acta 1993; 1146: 65–72.PubMedGoogle Scholar
  101. 101.
    Liu Z, Bendayan R, Wu XY. Triton-X-100-modified polymer and microspheres for reversal of multidrug resistance. J Pharm Pharmacol 2001; 53: 1–12.Google Scholar
  102. 102.
    Batrakova EV, Han HY, Miller DW, Kabanov AV. Effects of pluronic P85 unimers and micelles on drug permeability in polarized BBMEC and Caco-2 cells. Pharm Res 1998; 15: 1525–1532.PubMedGoogle Scholar
  103. 103.
    Alakhov VY, Kabanov AV. Block copolymeric biotransport carriers as versatile vehicles for drug delivery. Exp Opin Invest Drugs 1998; 7: 1453–1473.Google Scholar
  104. 104.
    Alakhov VY, Moskaleva EY, Batrakova EV. Hypersensitization of multidrug resistant human ovarian carcinoma cells by pluronic P85 block copolymer. Bioconjug Chem 1996; 7: 209–216.PubMedGoogle Scholar
  105. 105.
    Kabonov AV, Batrakova EV, Alakhov VY. An essential relationship between ATP depletion and chemosensitizing activity of pluronic block copolymers. J Control Release 2003; 91: 75–83.Google Scholar
  106. 106.
    Batrakova EV, Li S, Vinogradov SV, Alakhov VY, Miller DW, Kabanov AV. Mechanism of pluronic effect on p-glycoprotein efflux system in blood brain barrier: contributions of energy depletion and membrane fluidization. J Pharmacol Exp Ther 2001; 299: 483–493.PubMedGoogle Scholar
  107. 107.
    Ugazio E, Cavali R, Gasco MR. Incorporation of cyclosporin A in solid lipid nanoparticles (SLN). Int J Pharm 2002; 241: 341–344.PubMedGoogle Scholar
  108. 108.
    Lo YL, Liu FI, Cheung JY. Effect of PSC 833 liposomes and intralipid on the transport of epirubicin in Caco-2 cells and rat intestines. J Control Release 2001; 76: 1–10.PubMedGoogle Scholar
  109. 109.
    Wong HL, Bendayan R, Rauth AM, Wu XY. Development of solid lipid nanoparticles containing ionically-complexed chemotherapeutic drugs and chemosensitizers. J Pharm Sci 2004; 93: 1993–2004.PubMedGoogle Scholar
  110. 110.
    Wong HL, Rauth AM, Bendayan R, Wu XY. Combinational treatment with doxorubicin and GG918 (Elacridar) using polymer-lipid hybrid nanoparticles (PLN) and evaluation of strategies for multidrug-resistance reversal in human breast cancer cells. J Control Release 2006; 116: 275–284.PubMedGoogle Scholar
  111. 111.
    Shuhendler AJ, O’Brien P, Rauth AM, Wu XY. On the synergistic effect of doxorubicin and mitomycin C against breast cancer cells. Drug Metabol Drug Interactions 2008; 22: 201–233.Google Scholar
  112. 112.
    Shuhendler AJ, Chung R, Manias J, Connor A, Rauth AM, Wu XY. A novel doxorubicin-mitomycin C co-encapsulated nanoparticle formulation exhibits anti-cancer synergy in multidrug resistant human breast cancer cells. Breast Cancer Res Treatment, submitted in 2008.Google Scholar
  113. 113.
    Dass CR, Choong PFM. Selective gene delivery for cancer therapy using cationic liposomes: In vivo proof of applicability. J Control Release 2006; 113: 155–163.PubMedGoogle Scholar
  114. 114.
    Behlke M. Progress towards in vivo use of siRNAs. Mol Therapy 2006; 13: 645–670.Google Scholar
  115. 115.
    Qun (Tony) Liu. Enzyme Microencapsulation and Its Application for Overcoming Multidrug Resistance in Breast Cancer Treatment, Ph.D.Thesis, University of Toronto, Toronto, Canada, 2008.Google Scholar
  116. 116.
    Khalil IA, Kogure K, Akita H. Uptake pathways and subsequent intracellular trafficking in nonviral gene delivery. Pharmacol Rev 2006; 58: 32–45.PubMedGoogle Scholar
  117. 117.
    Kreuter J, Ramge P, Petrov V, Hamm S, Gelperina SE, Engelhardt B, Alyautdin R, von Briesen H, Begley DJ. Direct evidence that polysorbate-80-coated poly (butylcyanoacrylate) nanoparticles deliver drugs to the CNS via specific mechanisms requiring prior binding of drug to the nanoparticles. Pharm Res 2003; 20: 409–416.PubMedGoogle Scholar
  118. 118.
    Kreuter J, Shamenkov D, Petrov V, Ramge P, Cychutek K, Koch-Brandt C, Alyautdin R. Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood–brain barrier. J Drug Target 2002; 10: 317–325.PubMedGoogle Scholar
  119. 119.
    Steiniger SC, Kreuter J, Khalansky AS, Skidan IN, Bobruskin AI, Smirnova ZS, Severin SE, Uhl R, Kock M, Geiger KD, Gelperina SE. Chemotherapy of glioblastoma in rats using doxorubicin-loaded nanoparticles. Int J Cancer 2004; 109: 59–767.Google Scholar
  120. 120.
    Pelkmans L, Kartenbeck J, Helenius A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat Cell Biol 2001; 3: 473–483.PubMedGoogle Scholar
  121. 121.
    Amyere M, Mettlen M, van der Smissen P, Platek A, Payrastre B, Veithen A, Courtoy PJ. Origin, originality, functions, subversions and molecular signaling of macropinocytosis. Int J Med Microbiol 2002; 291: 487–494.PubMedGoogle Scholar
  122. 122.
    Kaplan IM, Wadia JS, Dowdy SF. Cationic TAT peptide transduction domain enters cells by macropinocytosis. J Control Release 2005; 102: 247–253.PubMedGoogle Scholar
  123. 123.
    Khalil IA, Kogure K, Futaki S, Harashima H. High density of octaarginine stimulates macropinocytosis leading to efficient intracellular trafficking for gene expression. J Biol Chem 2006; 6: 3544–3551.Google Scholar
  124. 124.
    Cho KC, Kim SH, Jeong JH, Park TG. Folate receptor-mediated gene delivery using folate-poly(ethylene glycol)-poly(L-lysine) conjugate. Macromol Biosci 2005; 5: 512–519.PubMedGoogle Scholar
  125. 125.
    Zhang H, Yee D, Wang C. Quantum Dots for Cancer Diagnosis and Therapy. Biol Clin Perspectives 2008; 3: 83–91.Google Scholar
  126. 126.
    Stevens PJ, Sekido M, Lee RJ. A folate-receptor-targeted lipid nanoparticle formulation for a lipophilic paclitaxel prodrug. Pharm Res 2004; 21: 2153–2157.PubMedGoogle Scholar
  127. 127.
    Wong HL, Bendayan R, Rauth AM, Xue HY, Babakhanian K, Wu XY. Amechanistic study of enhanced doxorubicin uptake and retention in multidrug resistant breast cancer cells using a polymer-lipid hybrid nanoparticle (PLN) system. J Pharmacol Exp Ther 2006; 317: 1372–1381.PubMedGoogle Scholar
  128. 128.
    Kopecek J, Kopeckova P, Minko T, Lu ZR. HPMA copolymer–anticancer drug conjugates: design, activity, and mechanism of action. Eur J Pharm Biopharm 2000; 50: 61–81.PubMedGoogle Scholar
  129. 129.
    Kopecek J, Kopeckova P, Minko T, Lu ZR, Peterson CM. Water soluble polymers in tumor targeted delivery. J Control Release 2001; 74: 147–158.PubMedGoogle Scholar
  130. 130.
    Bonnet D, Dick JE. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730–737.PubMedGoogle Scholar
  131. 131.
    Li C, Heidt DG, Dalerba P, Burant CF, Zhang L, Adsay V, Wicha M, Clarke MF, Simeone DM. Identification of pancreatic cancer stem cells. Cancer Res 2007; 67: 1030–1037.PubMedGoogle Scholar
  132. 132.
    Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, Squire J, Dirks PB. Identification of a cancer stem cell in human brain tumors. Cancer Res 2003; 63: 5821–5828.PubMedGoogle Scholar
  133. 133.
    O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature 2007; 445: 106–110.PubMedGoogle Scholar
  134. 134.
    Donnenberg VS, Donnenberg AD. Multiple drug resistance in cancer revisited: the cancer stem cell hypothesis. J Clin Pharmacol 2005; 45: 872–877.PubMedGoogle Scholar
  135. 135.
    Hirschmann-Jax C, Foster AE, Wulf GG. A distinct “side population” of cells with high drug efflux capacity in human tumor cells. Proc Natl Acad Sci USA 2004; 101: 14228–14233.PubMedGoogle Scholar
  136. 136.
    Gouaze V, Yu JY, Bleicher RJ, Han TY, Liu YY, Wang H, Michael M, Gottesman MM, Bitterman A, Giuliano AE, Cabot MC. Overexpression of glucosylceramide synthase and P-glycoprotein in cancer cells selected for resistance to natural product chemotherapy. Mol Cancer Ther 2004; 3: 633–639.PubMedGoogle Scholar
  137. 137.
    Gouaze V, Liu YY, Prickett CS, Yu JY, Giuliano AE, Cabot MC. Glucosylceramide synthase blockade down-regulates P-glycoprotein and resensitizes multidrug-resistant breast cancer cells to anticancer drugs. Cancer Res 2005; 65: 3861–3867.PubMedGoogle Scholar
  138. 138.
    Sun YL, Zhou GY, Li KN, Gao P, Zhang QH, Zhen JH, Bai YH, Zhang XF. Suppression of glucosylceramide synthase by RNA interference reverses multidrug resistance in human breast cancer cells. Neoplasma 2006; 53: 1–8.PubMedGoogle Scholar
  139. 139.
    Nakamura Y, Oka M, Soda H, Shiozawa K, Yoshikawa M, Itoh A, Ikegami Y, Tsurutani J, Nakatomi K, Kitazaki T, Doi S, Yoshida H, Kohno Sn. Gefitinib (“Iressa” ZD1839), an epidermal growth factor receptor tyrosine kinase inhibitor, reverses breast cancer resistance protein/ABCG2-mediated drug resistance. Cancer Res 2005; 65: 1541–1546.PubMedGoogle Scholar
  140. 140.
    Yanase K, Tsukahara S, Asada S, Ishikawa E, Imai Y, Sugimoto Y. Gefitinib reverses breast cancer resistance protein-mediated drug resistance. Mol Cancer Ther 2004; 3: 1119–1125.PubMedGoogle Scholar
  141. 141.
    Fantappiè O, Solazzo M, Lasagna N, Platini F, Tessitore L, Mazzant R. P-glycoprotein mediates celecoxib-induced apoptosis in multiple drug-resistant cell lines. Cancer Res 2007; 67: 4915–4923.PubMedGoogle Scholar
  142. 142.
    Tredan O, Galmarini CM, Patel K, Tannock IF. Drug resistance and the solid tumor microenvironment. J Natl Cancer Inst 2007; 99: 1441–1454.PubMedGoogle Scholar
  143. 143.
    Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Haner B Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A, Gilbertson RJ. A perivascular niche for brain tumor stem cells. Cancer Cell 2007; 11: 69–82.PubMedGoogle Scholar
  144. 144.
    Kim JJ, Tannock IF. Repopulation of cancer cells during therapy: An important cause of treatment failure. Nat Rev Cancer 2005; 5: 516–525.PubMedGoogle Scholar
  145. 145.
    Wong HL, Rauth AM, Bendayan R, Wu XY. Evaluation of the in vivo efficacy, toxicity and lymphatic drainage of loco-regional administered polymer-lipid hybrid nanoparticles (PLN) loaded with doxorubicin in a murine solid tumor model. Eur J Pharm Biopharm 2007; 65: 300–308.PubMedGoogle Scholar
  146. 146.
    Jang SH, Wientjes MG, Au JL. Enhancement of paclitaxel delivery to solid tumors by apoptosis-inducing pretreatment: effect of treatment schedule. J Pharmacol Exp Ther 2001; 296: 1035–1042.PubMedGoogle Scholar
  147. 147.
    Winkler F, Kozin SV, Tong RT, Chae S, Booth M, Garkavtsev I, Xu L, Hicklin D, Fukumura D, Tomaso ED. Kinetics of vascular normalization by VEGFR2 blockade governs brain tumor response to radiation: role of oxygenation, angiopoietin-1, and matrix metalloproteinases. Cancer Cell 2004; 6: 553–563.PubMedGoogle Scholar
  148. 148.
    Brown E, Mckee T, diTomaso, Pluen A, Seed B, Boucher Y, Rakesh K. Jain RK. Dynamic imaging of collagen and its modulation in tumors in vivo using second-harmonic generation. Nat Med 2003; 9: 796–800.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.School of Pharmacy, Temple UniversityPhiladelphiaUSA
  2. 2.Leslie Dan Faculty of PharmacyUniversity of TorontoOntarioCanada M5S 2S2
  3. 3.Leslie Dan Faculty of PharmacyUniversity of TorontoOntarioCanada M5S 2S2

Personalised recommendations