Improved efficacy and reduced toxicity of doxorubicin encapsulated in sulfatide-containing nanoliposome in a glioma model

PLoS ONE

Volumn 9, Issue 7, 2014, Pages

  Lin, Jia ^a,b   Shigdar, Sarah ^a   Fang, Ding Zhi ^b   Xiang, Dognxi ^a   Wei, Ming Q ^c   Danks, Andrew ^d   Kong, Lingxue ^a   Li, Lianghong ^e   Qiao, Liang ^f   Duan, Wei ^a  

^a DEAKIN UNIVERSITY   (Australia)

^b SICHUAN UNIVERSITY   (China)

^c GRIFFITH UNIVERSITY   (Australia)

^d MONASH UNIVERSITY   (Australia)

^e DALIAN MEDICAL UNIVERSITY   (China)

^f UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; LIPOSOME; SULFATIDE; SULFATIDE CONTAINING NANOLIPOSOMAL DOXORUBICIN; SULFATIDE CONTAINING NANOLIPOSOME; TENASCIN; UNCLASSIFIED DRUG; ANTINEOPLASTIC ANTIBIOTIC; NANOPARTICLE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD CHEMISTRY; CIRCULATION TIME; CONTROLLED STUDY; CYTOTOXICITY; DRUG BIOAVAILABILITY; DRUG BLOOD LEVEL; DRUG CLEARANCE; DRUG DELIVERY SYSTEM; DRUG DISTRIBUTION; DRUG EFFICACY; DRUG RETENTION; DRUG STABILITY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; NANOENCAPSULATION; NONHUMAN; PROTEIN EXPRESSION; RAT; SINGLE DRUG DOSE; TUMOR MICROENVIRONMENT; ANIMAL; APOPTOSIS; BAGG ALBINO MOUSE; CHEMISTRY; CONFOCAL MICROSCOPY; DISEASE MODEL; DRUG EFFECTS; GLIOMA; KINETICS; MCF 7 CELL LINE; MORTALITY; MOUSE; PARTICLE SIZE; SPRAGUE DAWLEY RAT; TISSUE DISTRIBUTION; TUMOR CELL LINE; XENOGRAFT;

ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; APOPTOSIS; CELL LINE, TUMOR; DISEASE MODELS, ANIMAL; DOXORUBICIN; FEMALE; GLIOMA; HUMANS; KINETICS; LIPOSOMES; MALE; MCF-7 CELLS; MICE; MICE, INBRED BALB C; MICROSCOPY, CONFOCAL; NANOPARTICLES; PARTICLE SIZE; RATS; RATS, SPRAGUE-DAWLEY; SULFOGLYCOSPHINGOLIPIDS; TISSUE DISTRIBUTION; TRANSPLANTATION, HETEROLOGOUS;

EID: 84904968815     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0103736     Document Type: Article

References (69)

1. Alexis F, Rhee JW, Richie JP, Radovic-Moreno AF, Langer R, et al. (2008) New frontiers in nanotechnology for cancer treatment. Urol Oncol 26: 74-85.
2. Bawarski WE, Chidlowsky E, Bharali DJ, Mousa SA (2008) Emerging nanopharmaceuticals. Nanomedicine 4: 273-282.
3. Peer D, Karp JM, Seungpyo H, Farokhzad OC, Margalit R, et al. (2007) Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2: 751-760. (Pubitemid 350223348)
4. Sapra P, Tyagi P, Allen TM (2005) Ligand-targeted liposomes for cancer treatment. Curr Drug Deliv 2: 369-381. (Pubitemid 41277769)
5. Ganta S, Devalapally H, Shahiwala A, Amiji M (2008) A review of stimuli-responsive nanocarriers for drug and gene delivery. J Control Release 126: 187-204.
6. Townson K, Greenshields KN, Veitch J, Nicholl D, Eckhardt M, et al. (2007) Sulfatide binding properties of murine and human antiganglioside antibodies. Glycobiology 17: 1156-1166. (Pubitemid 47604723)
7. Orend G, Chiquet-Ehrismann R (2006) Tenascin-C induced signaling in cancer. Cancer Lett 244: 143-163. (Pubitemid 44508708)
8. Shao K, Hou Q, Duan W, Go ML, Wong KP, et al. (2006) Intracellular drug delivery by sulfatide-mediated liposomes to gliomas. J Control Release 115: 150-157. (Pubitemid 44559706)
9. Foti C, Florean C, Pezzutto A, Roncaglia P, Tomasella A, et al. (2009) Characterization of caspase-dependent and caspase-independent deaths in glioblastoma cells treated with inhibitors of the ubiquitin-proteasome system. Molecular cancer therapeutics 8: 3140-3150.
10. Wu X, Li QT (1999) Hydration and stability of sulfatide-containing phosphatidylethanolamine small unilamellar vesicles. Biochim Biophys Acta 1416: 285-294. (Pubitemid 29065444)
11. Adamsky K, Schilling J, Garwood J, Faissner A, Peles E (2001) Glial tumor cell adhesion is mediated by binding of the FNIII domain of receptor protein tyrosine phosphatase beta (RPTPbeta) to tenascin C. Oncogene 20: 609-618. (Pubitemid 32156185)
12. Alvarez-Cedron L, Sayalero ML, Lanao JM (1999) High-performance liquid chromatographic validated assay of doxorubicin in rat plasma and tissues. J Chromatogr B Biomed Sci Appl 721: 271-278. (Pubitemid 29142349)
13. Stewart JCM (1980) Colorimetric determination of phospholipids with ammonium ferrothiocyanate. Anal Biochem 104: 10-14.
14. Rai S, Paliwal R, Vaidya B, Khatri K, Goyal AK, et al. (2008) Targeted delivery of doxorubicin via estrone-appended liposomes. J Drug Target 16: 455-463. (Pubitemid 352015814)
15. Song H, Zhang J, Han Z, Zhang X, Li Z, et al. (2006) Pharmacokinetic and cytotoxic studies of pegylated liposomal daunorubicin. Cancer Chemother Pharmacol 57: 591-598. (Pubitemid 43237843)
16. Zhang FY, Du GJ, Zhang L, Zhang CL, Lu WL, et al. (2009) Naringenin enhances the anti-tumor effect of doxorubicin through selectively inhibiting the activity of multidrug resistance-associated proteins but not P-glycoprotein. Pharm Res 26: 914-925.
17. Jung SH, Jung SH, Seong H, Cho SH, Jeong KS, et al. (2009) Polyethylene glycol-complexed cationic liposome for enhanced cellular uptake and anticancer activity. Int J Pharm 382: 254-261.
18. Xiong XB, Huang Y, Lu WL, Zhang H, Zhang X, et al. (2005) Enhanced intracellular uptake of sterically stabilized liposomal Doxorubicin in vitro resulting in improved antitumor activity in vivo. Pharm Res 22: 933-939. (Pubitemid 40898103)
19. Xiong XB, Huang Y, Lu WL, Zhang X, Zhang H, et al. (2005) Enhanced intracellular delivery and improved antitumor efficacy of doxorubicin by sterically stabilized liposomes modified with a synthetic RGD mimetic. J Control Release 107: 262-275. (Pubitemid 41316289)
20. Li X, Ding L, Xu Y, Wang Y, Ping Q (2009) Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int J Pharm 373: 116-123.
21. Cheng C, Haouala A, Krueger T, Mithieux F, Perentes JY, et al. (2009) Drug uptake in a rodent sarcoma model after intravenous injection or isolated lung perfusion of free/liposomal doxorubicin. Interact Cardiovasc Thorac Surg 8: 635-638.
22. Lopes de Menezes DE, Hudon N, McIntosh N, Mayer LD (2000) Molecular and pharmacokinetic properties associated with the therapeutics of bcl-2 antisense oligonucleotide G3139 combined with free and liposomal doxorubicin. Clin Cancer Res 6: 2891-2902. (Pubitemid 30482132)
23. Tang N, Du G, Wang N, Liu C, Hang H, et al. (2007) Improving penetration in tumors with nanoassemblies of phospholipids and doxorubicin. J Natl Cancer Inst 99: 1004-1015. (Pubitemid 47232602)
24. Koh E, Nakamura T, Takahashi H (2004) Troponin-T and brain natriuretic peptide as predictors for adriamycin-induced cardiomyopathy in rats. Circ J 68: 163-167. (Pubitemid 38197255)
25. Fritze A, Hens F, Kimpfler A, Schubert R, Peschka-Suss R (2006) Remote loading of doxorubicin into liposomes driven by a transmembrane phosphate gradient. Biochim Biophys Acta 1758: 1633-1640. (Pubitemid 44466698)
26. Hancox RA, Allen MD, Holliday DL, Edwards DR, Pennington CJ, et al. (2009) Tumour-associated tenascin-C isoforms promote breast cancer cell invasion and growth by matrix metalloproteinase-dependent and independent mechanisms. Breast cancer research: BCR 11: R24.
27. Chen Z, Deng J, Zhao Y, Tao T (2012) Cyclic RGD peptide-modified liposomal drug delivery system: enhanced cellular uptake in vitro and improved pharmacokinetics in rats. Int J Nanomedicine 7: 3803-3811.
28. Shmeeda H, Amitay Y, Gorin J, Tzemach D, Mak L, et al. (2010) Delivery of zoledronic acid encapsulated in folate-targeted liposome results in potent in vitro cytotoxic activity on tumor cells. J Control Release 146: 76-83.
29. Rahman A, Carmichael D, Harris M, Roh JK (1986) Comparative pharmacokinetics of free doxorubicin and doxorubicin entrapped in cardiolipin liposomes. Cancer Res 46: 2295-2299. (Pubitemid 16120685)
30. Wei G, Xiao S, Si D, Liu C (2008) Improved HPLC method for doxorubicin quantification in rat plasma to study the pharmacokinetics of micelle-encapsulated and liposome-encapsulated doxorubicin formulations. Biomed Chromatogr 22: 1252-1258.
31. Sugiyama I, Sadzuka Y (2011) Correlation of fixed aqueous layer thickness around PEG-modified liposomes with in vivo efficacy of antitumor agent-containing liposomes. Curr Drug Discov Technol 8: 357-366.
32. Singal PK, Iliskovic N (1998) Doxorubicin-induced cardiomyopathy. N Engl J Med 339: 900-905. (Pubitemid 28446849)
33. Herman EH, Zhang J, Lipshultz SE, Rifai N, Chadwick D, et al. (1999) Correlation between serum levels of cardiac troponin-T and the severity of the chronic cardiomyopathy induced by doxorubicin. J Clin Oncol 17: 2237-2243. (Pubitemid 29318858)
34. Zhu Q, Feng C, Liao W, Zhang Y, Tang S (2013) Target delivery of MYCN siRNA by folate-nanoliposomes delivery system in a metastatic neuroblastoma model. Cancer cell international 13: 65.
35. Lin J, Yu Y, Shigdar S, Fang DZ, Du JR, et al. (2012) Enhanced antitumor efficacy and reduced systemic toxicity of sulfatide-containing nanoliposomal doxorubicin in a xenograft model of colorectal cancer. PloS one 7: e49277.
36. Reardon DA, Zalutsky MR, Bigner DD (2007) Antitenascin-C monoclonal antibody radioimmunotherapy for malignant glioma patients. Expert Rev Anticancer Ther 7: 675-687. (Pubitemid 46805563)
37. Mayer LD, Tai LC, Ko DS, Masin D, Ginsberg RS, et al. (1989) Influence of vesicle size, lipid composition, and drug-to-lipid ratio on the biological activity of liposomal doxorubicin in mice. Cancer Res 49: 5922-5930. (Pubitemid 19274148)
38. Hussain S, Plückthun A, Allen TM, Zangemeister-Wittke U (2007) Antitumor activity of an epithelial cell adhesion molecule targeted nanovesicular drug delivery system. Mol Cancer Ther 6: 3019-3027. (Pubitemid 350206780)
39. Hernández J, Martí A, Estelrich J (1991) Interaction of doxorubicin with lipid systems. Bioconjug Chem 2: 398-402.
40. Lim HJ, Masin D, Madden TD, Bally MB (1997) Influence of drug release characteristics on the therapeutic activity of liposomal mitoxantrone. J Pharmacol Exp Ther 281: 566-573. (Pubitemid 27203116)
41. Huang Y, Chen X-M, Zhao B-X, Ke X-Y, Zhao B-J, et al. (2010) Antiangiogenic Activity of Sterically Stabilized Liposomes Containing Paclitaxel (SSL-PTX): In Vitro and In Vivo. AAPS PharmSciTech 11: 752-759.
42. Sadzuka Y, Nakade A, Tsuruda T, Sonobe T (2003) Study on the characterization of mixed polyethyleneglycol modified liposomes containing doxorubicin. J Control Release 91: 271-280. (Pubitemid 36976760)
43. Ishida T, Takanashi Y, Doi H, Yamamoto I, Kiwada H (2002) Encapsulation of an antivasospastic drug, fasudil, into liposomes, and in vitro stability of the fasudil-loaded liposomes. International journal of pharmaceutics 232: 59-67. (Pubitemid 34076754)
44. Wang J, Goh B, Lu W, Zhang Q, Chang A, et al. (2005) In vitro cytotoxicity of Stealth liposomes co-encapsulating doxorubicin and verapamil on doxorubicin-resistant tumor cells. Biol Pharm Bull 28: 822-828. (Pubitemid 40740648)
45. Li B, Xu H, Li Z, Yao M, Xie M, et al. (2012) Bypassing multidrug resistance in human breast cancer cells with lipid/polymer particle assemblies. Int J Nanomedicine 7: 187-197.
46. Allen TM, Cheng WWK, Hare JI, Laginha KM (2006) Pharmacokinetics and Pharmacodynamics of Lipidic Nano-Particles in Cancer. Anticancer Agents Med Chem 6: 513-523. (Pubitemid 44697110)
47. Cabanes A, Even-Chen S, Zimberoff J, Barenholz Y, Kedar E, et al. (1999) Enhancement of antitumor activity of polyethylene glycol-coated liposomal doxorubicin with soluble and liposomal interleukin 2. Clin Cancer Res 5: 687-693. (Pubitemid 29131981)
48. Unezaki S, Maruyama K, Takahashi N, Koyama M, Yuda T, et al. (1994) Enhanced delivery and antitumor activity of doxorubicin using long-circulating thermosensitive liposomes containing amphipathic polyethylene glycol in combination with local hyperthermia. Pharm Res 11: 1180-1185. (Pubitemid 24259860)
49. Xu L, Anchordoquy T (2011) Drug delivery trends in clinical trials and translational medicine: challenges and opportunities in the delivery of nucleic acid-based therapeutics. J Pharm Sci 100: 38-52.
50. Wu J, Lu Y, Lee A, Pan X, Yang X, et al. (2007) Reversal of multidrug resistance by transferrin-conjugated liposomes co-encapsulating doxorubicin and verapamil. J Pharm Pharm Sci 10: 350-357. (Pubitemid 350065179)
51. Tokarska-Schlattner M, Zaugg M, da Silva R, Lucchinetti E, Schaub MC, et al. (2005) Acute toxicity of doxorubicin on isolated perfused heart: response of kinases regulating energy supply. Am J Physiol Heart Circ Physiol 289: H37-47. (Pubitemid 40934080)
52. Bagchi D, Sen CK, Ray SD, Das DK, Bagchi M, et al. (2003) Molecular mechanisms of cardioprotection by a novel grape seed proanthocyanidin extract. Mutat Res 523-524: 87-97. (Pubitemid 36293235)
53. Mercuro G, Cadeddu C, Piras A, Dessì M, Madeddu C, et al. (2007) Early epirubicin-induced myocardial dysfunction revealed by serial tissue Doppler echocardiography: correlation with inflammatory and oxidative stress markers. Oncologist 12: 1124-1133. (Pubitemid 350007024)
54. Cosan D, Basaran A, Gunes HV, Degirmenci I, Aral E (2008) The effect of doxorubicin on rats that received toxic and carcinogenic benzo(a)pyrene. Folia Histochem Cytobiol 46: 367-372.
55. Yokogawa K, Ido A, Kurihara T, Mano Y, Nomura M, et al. (2006) Serum aminotransferase activity as a predictor for estimation of total clearance of hepatically metabolized drugs in rats with acute hepatic failure. Biol Pharm Bull 29: 141-145. (Pubitemid 43036711)
56. Charrois GJ, Allen TM (2003) Rate of biodistribution of STEALTH liposomes to tumor and skin: influence of liposome diameter and implications for toxicity and therapeutic activity. Biochim Biophys Acta 1609: 102-108. (Pubitemid 36044071)
57. Farr KP, Safwat A (2011) Palmar-plantar erythrodysesthesia associated with chemotherapy and its treatment. Case Rep Oncol 4: 229-235.
58. Goren D, Horowitz AT, Zalipsky S, Woodle MC, Yarden Y, et al. (1996) Targeting of stealth liposomes to erbB-2 (Her/2) receptor: in vitro and in vivo studies. Br J Cancer 74: 1749-1756. (Pubitemid 26401894)
59. Elbayoumi TA, Torchilin VP (2009) Tumor-targeted nanomedicines: enhanced antitumor efficacy in vivo of doxorubicin-loaded, long-circulating liposomes modified with cancer-specific monoclonal antibody. Clin Cancer Res 15: 1973-1980.
60. Campbell RB (2006) Tumor Physiology and Delivery of Nanopharmaceuticals. Anticancer Agents Med Chem 6: 503-512.
61. Drummond DC, Meyer O, Hong K, Kirpotin DB, Papahadjopoulos D (1999) Optimizing liposomes for delivery of chemotherapeutic agents to solid tumors. Pharmacol Rev 51: 691-743.
62. Tanaka T, Mangala LS, Vivas-Mejia PE, Nieves-Alicea R, Mann AP, et al. (2010) Sustained small interfering RNA delivery by mesoporous silicon particles. Cancer research 70: 3687-3696.
63. Chen MH, Chang CH, Chang YJ, Chen LC, Yu CY, et al. (2010) MicroSPECT/CT imaging and pharmacokinetics of 188Re-(DXR)-liposome in human colorectal adenocarcinoma-bearing mice. Anticancer Res 30: 65-72.
64. Cui J, Li C, Wang C, Li Y, Zhang L, et al. (2008) Repeated injection of pegylated liposomal antitumour drugs induces the disappearance of the rapid distribution phase. The Journal of pharmacy and pharmacology 60: 1651-1657.
65. Liu F, Chen Z, Wang J, Shao X, Cui Z, et al. (2008) Overexpression of cell surface cytokeratin 8 in multidrug-resistant MCF-7/MX cells enhances cell adhesion to the extracellular matrix. Neoplasia 10: 1275-1284.
66. Fernando NT, Koch M, Rothrock C, Gollogly LK, D'Amore PA, et al. (2008) Tumor escape from endogenous, extracellular matrix-associated angiogenesis inhibitors by up-regulation of multiple proangiogenic factors. Clin Cancer Res 14: 1529-1539. (Pubitemid 351413938)
67. Quemener C, Gabison EE, Naïmi B, Lescaille G, Bougatef F, et al. (2007) Extracellular matrix metalloproteinase inducer up-regulates the urokinase-type plasminogen activator system promoting tumor cell invasion. Cancer Res 67: 9-15. (Pubitemid 46142753)
68. Mackie EJ, Tucker RP (1999) The tenascin-C knockout revisited. J Cell Sci 112: 3847-3853. (Pubitemid 30119755)
69. Adams M, Jones JL, Walker RA, Pringle JH, Bell SC (2002) Changes in tenascin-C isoform expression in invasive and preinvasive breast disease. Cancer Res 62: 3289-3297. (Pubitemid 34602427)