Antitumor activity of new liposomal prodrug of mitomycin C in multidrug resistant solid tumor: Insights of the mechanism of action

References

• Angelini G, Gardella S, Ardy M, Ciriolo MR, Filomeni G, Di Trapani G, Clarke F, Sitia R, Rubartelli A. Antigen-presenting dendritic cells provide the reducing extracellular microenvironment required for T lymphocyte activation. Proc Natl Acad Sci USA 2002; 99: 1491–1496
   PubMed Web of Science ®Google Scholar
• Baban DF, Seymour LW. Control of tumour vascular permeability. Adv Drug Deliv Rev 1998; 34: 109–119
   PubMed Web of Science ®Google Scholar
• Baker AF, Dragovich T, Tate WR, Ramanathan RK, Roe D, Hsu CH, Kirkpatrick DL, Powis G. The antitumor thioredoxin-1 inhibitor PX-12 (1-methylpropyl 2-imidazolyl disulfide) decreases thioredoxin-1 and VEGF levels in cancer patient plasma. J Lab Clin Med 2006; 147: 83–90
   PubMed Web of Science ®Google Scholar
• Biaglow JE, Miller RA. The thioredoxin reductase/thioredoxin system: Novel redox targets for cancer therapy. Cancer Biol Ther 2005; 4: 6–13
   PubMed Web of Science ®Google Scholar
• Crenesse D, Laurens M, Heurteaux C, Cursio R, Saint-Paul MC, Schmid-Alliana A, Gugenheim J. Rat liver ischemia–reperfusion-induced apoptosis and necrosis are decreased by FK506 pretreatment. Eur J Pharmacol 2003; 473: 177–184
   PubMed Web of Science ®Google Scholar
• Dharap SS, Wang Y, Chandna P, Khandare JJ, Qiu B, Gunaseelan S, Sinko PJ, Stein S, Farmanfarmaian A, Minko T. Tumor-specific targeting of an anticancer drug delivery system by LHRH peptide. Proc Natl Acad Sci USA 2005; 102: 12962–12967
   PubMed Web of Science ®Google Scholar
• Dharap SS, Chandna P, Wang Y, Khandare JJ, Qiu B, Stein S, Minko T. Molecular targeting of BCL2 and BCLXL proteins by synthetic BH3 peptide enhances the efficacy of chemotherapy. J Pharmacol Exp Ther 2006; 316: 992–998
   PubMed Web of Science ®Google Scholar
• Fang J, Sawa T, Maeda H. Factors and mechanism of “EPR” effect and the enhanced antitumor effects of macromolecular drugs including SMANCS. Adv Exp Med Biol 2003; 519: 29–49
   PubMed Web of Science ®Google Scholar
• Gabizon AA, Shmeeda H, Zalipsky S. Pros and cons of the liposome platform in cancer drug targeting. J Liposome Res 2006a; 16: 175–183
   PubMed Web of Science ®Google Scholar
• Gabizon AA, Tzemach D, Horowitz AT, Shmeeda H, Yeh J, Zalipsky S. Reduced toxicity and superior therapeutic activity of a mitomycin C lipid-based prodrug incorporated in pegylated liposomes. Clin Cancer Res 2006b; 12: 1913–1920
   PubMed Web of Science ®Google Scholar
• Guo X, Szoka FC, Jr. Steric stabilization of fusogenic liposomes by a low-pH sensitive PEG–diortho ester–lipid conjugate. Bioconjug Chem 2001; 12: 291–300
   PubMed Web of Science ®Google Scholar
• Hsia TC, Lin CC, Wang JJ, Ho ST, Kao A. Relationship between chemotherapy response of small cell lung cancer and P-glycoprotein or multidrug resistance-related protein expression. Lung 2002; 180: 173–179
   PubMed Web of Science ®Google Scholar
• Hwang CY, Ryu YS, Chung MS, Kim KD, Park SS, Chae SK, Chae HZ, Kwon KS. Thioredoxin modulates activator protein 1 (AP-1) activity and p27Kip1 degradation through direct interaction with Jab1. Oncogene 2004; 23: 8868–8875
   PubMed Web of Science ®Google Scholar
• Ihnat MA, Nervi AM, Anthony SP, Kaltreider RC, Warren AJ, Pesce CA, Davis SA, Lariviere JP, Hamilton JW. Effects of mitomycin C and carboplatin pretreatment on multidrug resistance-associated P-glycoprotein expression and on subsequent suppression of tumor growth by doxorubicin and paclitaxel in human metastatic breast cancer xenografted nude mice. Oncol Res 1999; 11: 303–310
   PubMed Web of Science ®Google Scholar
• Khandare JJ, Chandna P, Wang Y, Pozharov VP, Minko T. Novel polymeric prodrug with multivalent components for cancer therapy. J Pharmacol Exp Ther 2006; 317: 929–937
   PubMed Web of Science ®Google Scholar
• Kinnula VL, Paakko P, Soini Y. Antioxidant enzymes and redox regulating thiol proteins in malignancies of human lung. FEBS Lett 2004; 569: 1–6
   PubMed Web of Science ®Google Scholar
• Kratz F, Warnecke A, Scheuermann K, Stockmar C, Schwab J, Lazar P, Druckes P, Esser N, Drevs J, Rognan D, Bissantz C, Hinderling C, Folkers G, Fichtner I, Unger C. Probing the cysteine-34 position of endogenous serum albumin with thiol-binding doxorubicin derivatives. Improved efficacy of an acid-sensitive doxorubicin derivative with specific albumin-binding properties compared to that of the parent compound. J Med Chem 2002; 45: 5523–5533
   PubMed Web of Science ®Google Scholar
• Lasic D, Martin F. STEALTH® Liposomes. CRC press, Boca Raton, FL 1995
   Google Scholar
• Lee Y, Vassilakos A, Feng N, Avolio T, Jin H, Viau S, Wang M, Courssaris B, Xiong K, Wright J, Young A. Anti-proliferative and anti-tumor effects of antisense oligonucleotide GTI-2601 targeted against human thioredoxin. Anticancer Drugs 2006; 17: 143–154
   PubMed Web of Science ®Google Scholar
• Lincoln DT, Ali Emadi EM, Tonissen KF. The thioredoxin–thioredoxin reductase system: Over-expression in human cancer. Anticancer Res 2003; 23: 2425–2433
   PubMed Web of Science ®Google Scholar
• Maeda H. The enhanced permeability and retention (EPR) effect in tumor vasculature: The key role of tumor-selective macromolecular drug targeting. Adv Enzyme Regul 2001; 41: 189–207
   PubMedGoogle Scholar
• 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; 46: 6387–6392
   PubMed Web of Science ®Google Scholar
• Minko T, Kopeckova P, Pozharov V, Kopecek J. HPMA copolymer bound adriamycin overcomes MDR1 gene encoded resistance in a human ovarian carcinoma cell line. J Control Release 1998; 54: 223–233
   PubMed Web of Science ®Google Scholar
• Minko T, Kopeckova P, Kopecek J. Comparison of the anticancer effect of free and HPMA copolymer-bound adriamycin in human ovarian carcinoma cells. Pharm Res 1999a; 16: 986–996
   PubMed Web of Science ®Google Scholar
• Minko T, Kopeckova P, Kopecek J. Chronic exposure to HPMA copolymer-bound adriamycin does not induce multidrug resistance in a human ovarian carcinoma cell line. J Control Release 1999b; 59: 133–148
   PubMed Web of Science ®Google Scholar
• Minko T, Kopeckova P, Kopecek J. Efficacy of the chemotherapeutic action of HPMA copolymer-bound doxorubicin in a solid tumor model of ovarian carcinoma. Int J Cancer 2000a; 86: 108–117
   PubMed Web of Science ®Google Scholar
• Minko T, Kopeckova P, Pozharov V, Jensen KD, Kopecek J. The influence of cytotoxicity of macromolecules and of VEGF gene modulated vascular permeability on the enhanced permeability and retention effect in resistant solid tumors. Pharm Res 2000b; 17: 505–514
   PubMed Web of Science ®Google Scholar
• Minko T, Pakunlu RI, Wang Y, Khandare JJ, Saad M. New generation of liposomal drugs for cancer. Anticancer Agents Med Chem 2006; 6: 537–552
   PubMedGoogle Scholar
• Nakamura H, Bai J, Nishinaka Y, Ueda S, Sasada T, Ohshio G, Imamura M, Takabayashi A, Yamaoka Y, Yodoi J. Expression of thioredoxin and glutaredoxin, redox-regulating proteins, in pancreatic cancer. Cancer Detect Prev 2000; 24: 53–60
   PubMedGoogle Scholar
• Nguyen P, Awwad RT, Smart DD, Spitz DR, Gius D. Thioredoxin reductase as a novel molecular target for cancer therapy. Cancer Lett 2006; 236: 164–174
   PubMed Web of Science ®Google Scholar
• Pakunlu RI, Wang Y, Tsao W, Pozharov V, Cook TJ, Minko T. Enhancement of the efficacy of chemotherapy for lung cancer by simultaneous suppression of multidrug resistance and antiapoptotic cellular defense: Novel multicomponent delivery system. Cancer Res. 2004; 64: 6214–6224
   PubMed Web of Science ®Google Scholar
• Pakunlu RI, Wang Y, Saad M, Khandare JJ, Starovoytov V, Minko T. In vitro and in vivo intracellular liposomal delivery of antisense oligonucleotides and anticancer drug. J Control Release 2006; 114: 153–162
   PubMed Web of Science ®Google Scholar
• Powis G, Mustacich D, Coon A. The role of the redox protein thioredoxin in cell growth and cancer. Free Radic Biol Med 2000; 29: 312–322
   PubMed Web of Science ®Google Scholar
• Powis G, Wipf P, Lynch SM, Birmingham A, Kirkpatrick DL. Molecular pharmacology and antitumor activity of palmarumycin-based inhibitors of thioredoxin reductase. Mol Cancer Ther 2006; 5: 630–636
   PubMed Web of Science ®Google Scholar
• Sato N, Iwata S, Nakamura K, Hori T, Mori K, Yodoi J. Thiol-mediated redox regulation of apoptosis. Possible roles of cellular thiols other than glutathione in T cell apoptosis. J Immunol 1995; 154: 3194–3203
   PubMed Web of Science ®Google Scholar
• Senter P, Pierce W, Greenfield R. Development of drug release strategy based on the reductive fragmentation of benzyl carbamate disulfide. J Org Chem 1990; 55: 2975–2978
   Web of Science ®Google Scholar
• Sharma R, Awasthi YC, Yang Y, Sharma A, Singhal SS, Awasthi S. Energy dependent transport of xenobiotics and its relevance to multidrug resistance. Curr Cancer Drug Targets 2003; 3: 89–107
   PubMed Web of Science ®Google Scholar
• Soderberg A, Sahaf B, Rosen A. Thioredoxin reductase, a redox-active selenoprotein, is secreted by normal and neoplastic cells: Presence in human plasma. Cancer Res 2000; 60: 2281–2289
   PubMed Web of Science ®Google Scholar
• Streicher KL, Sylte MJ, Johnson SE, Sordillo LM. Thioredoxin reductase regulates angiogenesis by increasing endothelial cell-derived vascular endothelial growth factor. Nutr Cancer 2004; 50: 221–231
   PubMed Web of Science ®Google Scholar
• Szakacs G, Jakab K, Antal F, Sarkadi B. Diagnostics of multidrug resistance in cancer. Pathol Oncol Res 1998; 4: 251–257
   PubMedGoogle Scholar
• Szoka FC, Jr. The future of liposomal drug delivery. Biotechnol Appl Biochem 1990; 12: 496–500
   PubMed Web of Science ®Google Scholar
• Torchilin VP. Drug targeting. Eur J Pharm Sci 2000; 11(Suppl 2)S81–S91
   PubMed Web of Science ®Google Scholar
• van Veen HW, Konings WN. The ABC family of multidrug transporters in microorganisms. Biochim Biophys Acta 1998; 1365: 31–36
   PubMed Web of Science ®Google Scholar
• Vicent MJ, Duncan R. Polymer conjugates: Nanosized medicines for treating cancer. Trends Biotechnol 2006; 24: 39–47
   PubMed Web of Science ®Google Scholar
• Wang Y, Minko T. A novel cancer therapy: Combined liposomal hypoxia inducible factor 1 alpha antisense oligonucleotides and an anticancer drug. Biochem Pharmacol 2004; 68: 2031–2042
   PubMed Web of Science ®Google Scholar
• Welsh SJ, Bellamy WT, Briehl MM, Powis G. The redox protein thioredoxin-1 (Trx-1) increases hypoxia-inducible factor 1alpha protein expression: Trx-1 overexpression results in increased vascular endothelial growth factor production and enhanced tumor angiogenesis. Cancer Res 2002; 62: 5089–5095
   PubMed Web of Science ®Google Scholar
• Working P, Newman M, Huang S, Mayhew E, Vaage, Lasic D. Pharmacokinetics, biodistribution and therapeutic efficacy of doxorubicin encapsulated in STEALTH® liposomes (DOXIL). J Liposome Res 1994; 4: 667–687
   Google Scholar
• Xiong XB, Huang Y, Lu WL, Zhang X, Zhang H, Nagai T, Zhang Q. Enhanced intracellular delivery and improved antitumor efficacy of doxorubicin by sterically stabilized liposomes modified with a synthetic RGD mimetic. J Control Release 2005; 107: 262–275
   PubMed Web of Science ®Google Scholar
• Zalipsky S, Gabizon A. 2002. Conjugate having a cleavable linkage for use in a liposome, US patent 6,365,179 B1
   Google Scholar
• Zalipsky S, Kiwan R, Qazen M, Flaherty T, Engbers C, Guo L, Zomorodi K, Feng W, Yeh J, Horowits A, Indap M, Gabizon A. New lipsomal prodrug of mitomycin C. Int'l Symp Control Rel Biact Mater 2001; 2001: 437–438
   Google Scholar