Efficient nuclear drug translocation and improved drug efficacy mediated by acidity-responsive boronate-linked dextran/cholesterol nanoassembly

Biomaterials

Volumn 52, Issue 1, 2015, Pages 281-290

  Zhu, Jing Yi ^a   Lei, Qi ^a   Yang, Bin ^a   Jia, Hui Zhen ^a   Qiu, Wen Xiu ^a   Wang, Xuli ^b   Zeng, Xuan ^a   Zhuo, Ren Xi ^a   Feng, Jun ^a   Zhang, Xian Zheng ^a  

^a WUHAN UNIVERSITY   (China)

^b UNIVERSITY OF UTAH   (United States)

Author keywords

Acidity responsiveness; Boronate linking; Lysosomal acidity; Nanoassembly; Nuclear drug translocation; Tumor chemotherapy

Indexed keywords

CHEMOTHERAPY; CHOLESTEROL; DEXTRAN; MOBILE SECURITY; STABILITY; TUMORS;

ASSOCIATED MECHANISM; BORONATE; DOSE-DEPENDENT MANNER; NANO-ASSEMBLIES; NUCLEAR DRUG TRANSLOCATION; PHENYLBORONIC ACIDS; PHYSIOLOGICAL CONDITION; STRUCTURAL STABILITIES;

CATALYST ACTIVITY;

AMMONIUM CHLORIDE; BORONIC ACID DERIVATIVE; CHOLESTEROL; DEXTRAN; DOXORUBICIN; GLUCOSE; NANOPARTICLE; ANTINEOPLASTIC AGENT; BENZENEBORONIC ACID; BORON; CARBAMIC ACID DERIVATIVE; DRUG CARRIER; MICELLE;

ACIDITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER CHEMOTHERAPY; CANCER INHIBITION; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; CRITICAL MICELLE CONCENTRATION; CYTOTOXICITY; DISSOCIATION; DOSE RESPONSE; DRUG DELIVERY SYSTEM; DRUG SAFETY; DRUG UPTAKE; ENDOSOME; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; IN VIVO STUDY; LYSOSOME; MALE; MOUSE; NANOENCAPSULATION; NONHUMAN; PRIORITY JOURNAL; SERUM; TUMOR GROWTH; XENOGRAFT; ACTIVE TRANSPORT; ANIMAL; BAGG ALBINO MOUSE; CANCER TRANSPLANTATION; CHEMISTRY; CYTOPLASM; DRUG EFFECTS; FEMALE; HELA CELL LINE; METABOLISM; MICELLE; NANOMEDICINE; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; NUDE MOUSE; PARTICLE SIZE; TRANSMISSION ELECTRON MICROSCOPY;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; ANTINEOPLASTIC AGENTS; BORON; BORONIC ACIDS; CARBAMATES; CELL NUCLEUS; CHOLESTEROL; CYTOPLASM; DEXTRANS; DRUG CARRIERS; ENDOSOMES; FEMALE; HELA CELLS; HUMANS; LYSOSOMES; MAGNETIC RESONANCE SPECTROSCOPY; MICE; MICE, INBRED BALB C; MICE, NUDE; MICELLES; MICROSCOPY, ELECTRON, TRANSMISSION; NANOMEDICINE; NANOPARTICLES; NEOPLASM TRANSPLANTATION; PARTICLE SIZE;

EID: 84932599619     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.02.048     Document Type: Article

References (48)

1. Batrakova E.V., Gendelman H.E., Kabanov A.V. Cell-mediated drug delivery. Expert Opin Drug Deliv 2011, 8:415-433.
2. Nair M., Guduru R., Liang P., Hong J., Sagar V., Khizroev S. Externally controlled on-demand release of anti-HIV drug using magneto-electric nanoparticles as carriers. Nat Commun 2013, 4:1707.
3. Jia H., Zhu J., Wang X., Cheng H., Chen G., Zhao Y., et al. Aboronate-linked linear-hyperbranched polymeric nanovehicle for pH-dependent tumor-targeted drug delivery. Biomaterials 2014, 35:5240-5249.
4. Yang B., Lv Y., Zhu J., Han Y., Jia H., Chen W., et al. ApH-responsive drug nanovehicle constructed by reversible attachment of cholesterol to PEGylated poly(L-lysine) via catechol-boronic acid ester formation. Acta Biomater 2014, 10:3686-3695.
5. Zhao Z., Yao X., Zhang Z., Chen L., He C., Chen X. Boronic acid shell-crosslinked dextran-b-PLA micelles for acid-responsive drug delivery. Macromol Biosci 2014, 14:1609-1618.
6. Li L., Bai Z., Levkin P.A. Boronate-dextran: an acid-responsive biodegradable polymer for drug delivery. Biomaterials 2013, 34:8504-8510.
7. Maruyama K. Intracellular targeting delivery of liposomal drugs to solid tumors based on EPR effects. Adv Drug Deliv Rev 2011, 63:161-169.
8. Gillies E.R., Fréchet J.M.J. pH-Responsive copolymer assemblies for controlled release of doxorubicin. Bioconjug Chem 2005, 16:361-368.
9. Hickman J.A. Apoptosis induced by anticancer drugs. Cancer Metastasis Rev 1992, 11:121-139.
10. Burrow S.M., Phoenix D.A., Wainwright M., Tobin M.J. Intracellular localisation studies of doxorubicin and Victoria Blue BO in EMT6-S and EMT6-R cells using confocal microscopy. Cytotechnology 2002, 39:15-25.
11. Zhang J., Zhou F., Wu X., Zhang X., Chen Y., Zha B.S., et al. Cellular pharmacokinetic mechanisms of adriamycin resistance and its modulation by 20(S)-ginsenoside Rh2 in MCF-7/Adr cells. Br J Pharmacol 2012, 165:120-134.
12. Yao X., Chen L., Chen X., He C., Zheng H., Chen X. Intercellular pH-responsive histidine modified dextran-g-cholesterol micelle for anticancer drug delivery. Colloids Surf B Biointerfaces 2014, 121:36-43.
13. Liu Z., Jiao Y., Wang Y., Zhou C., Zhang Z. Polysaccharides-based nanoparticles as drug delivery systems. Adv Drug Deliv Rev 2008, 60:1650-1662.
14. He L., Fullenkamp D.E., Rivera J.G., Messersmith P.B. pH responsive self-healing hydrogels formed by boronate-catechol complexation. Chem Commun 2011, 47:7497-7499.
15. Su J., Chen F., Cryns V.L., Messersmith P.B. Catechol polymers for pH-responsive, targeted drug delivery to cancer cells. JAm Chem Soc 2011, 133:11850-11853.
16. Chen W., Cheng Y., Wang B. Dual-responsive boronate crosslinked micelles for targeted drug delivery. Angew Chem Int Ed 2012, 51:5293-5295.
17. Li Y., Xiao W., Xiao K., Berti L., Luo J., Tseng H.P., et al. Well-defined, reversible boronate crosslinked nanocarriers for targeted drug delivery in response to acidic pH values and cis-diols. Angew Chem Int Ed 2012, 124:2918-2923.
18. Ellis G.A., Palte M.J., Raines R.T. Boronate-mediated biologic delivery. JAm Chem Soc 2012, 134:3631-3634.
19. Yang B., Jia H., Wang X., Chen S., Zhang X., Zhuo R., et al. Self-assembled vehicle construction via boronic acid coupling and host-guest interaction for serum-tolerant DNA transport and pH-responsive drug delivery. Adv Healthc Mater 2014, 3:596-608.
20. Li Y.L., Zhu L., Liu Z., Cheng R., Meng F., Cui J.H., et al. Reversibly stabilized multifunctional dextran nanoparticles efficiently deliver doxorubicin into the nuclei of cancer cells. Angew Chem Int Ed 2009, 48:9914-9918.
21. Kheirolomoom A., Ferrara K.W. Cholesterol transport from liposomal delivery vehicles. Biomaterials 2007, 28:4311-4320.
22. Karpa M.J., Duggan P.J., Griffin G.J., Freudigmann S.J. Competitive transport of reducing sugars through a lipophilic membrane facilitated by aryl boron acids. Tetrahedron 1997, 53:3669-3678.
23. Li Z.Y., Wang H.Y., Li C., Zhang X.L., Wu X.J., Qin S.Y., et al. Porphyrin-functionalized amphiphilic diblock copolypeptides for photodynamic therapy. JPolym Sci A Polym Chem 2011, 49:286-292.
24. Besheer A., Hause G., Kressler J., Mäder K. Hydrophobically modified hydroxyethyl starch: synthesis, characterization, and aqueous self-assembly into nano-sized polymeric micelles and vesicles. Biomacromolecules 2007, 8:359-367.
25. Pan L., Liu J., He Q., Wang L., Shi J. Overcoming multidrug resistance of cancer cells by direct intranuclear drug delivery using TAT-conjugated mesoporous silica nanoparticles. Biomaterials 2013, 34:2719-2730.
26. Goren D., Horowitz A.T., Tzemach D., Tarshish M., Zalipsky S., Gabizon A. Nuclear delivery of doxorubicin via folate-targeted liposomes with bypass of multidrug-resistance efflux pump. Clin Cancer Res 2000, 6:1949-1957.
27. Springsteen G., Wang B. Adetailed examination of boronic acid-diol complexation. Tetrahedron 2002, 58:5291-5300.
28. Tomsho J.W., Benkovic S.J. Elucidation of the mechanism of the reaction between phenylboronic acid and a model diol, Alizarin Red S. JOrg Chem 2012, 77:2098-2106.
29. Chen C.S., Xu X.D., Wang Y., Yang J., Jia H.Z., Cheng H., et al. Apeptide nanofibrous indicator for eye-detectable cancer cell identification. Small 2013, 9:920-926.
30. Jain R.K. Delivery of molecular medicine to solid tumors: lessons from invivo imaging of gene expression and function. JControl Release 2001, 74:7-25.
31. Kataoka K., Harada A., Nagasaki Y. Block copolymer micelles for drug delivery: design, characterization and biological significance. Adv Drug Deliv Rev 2001, 47:113-131.
32. Ge Z., Liu S. Functional block copolymer assemblies responsive to tumor and intracellular microenvironments for site-specific drug delivery and enhanced imaging performance. Chem Soc Rev 2013, 42:7289-7325.
33. Görlich D., Kutay U. Transport between the cell nucleus and the cytoplasm. Annu Rev Cell Biol 1999, 15:607-660.
34. Puertollano R., Alonso M.A. MAL, an integral element of the apical sorting machinery, is an itinerant protein that cycles between the trans-Golgi network and the plasma membrane. Mol Biol Cell 1999, 10:3435-3447.
35. Hao M.M., Mukherjee S., Sun Y., Maxfield F.R. Effects of cholesterol depletion and increased lipid unsaturation on the properties of endocytic membranes. JBiol Chem 2004, 279:14171-14178.
36. Minotti G., Menna P., Salvatorelli E., Cairo G., Gianni L. Anthracyclines: molecular advances and pharmacologic developments in antitumor activity and cardiotoxicity. Pharmacol Rev 2004, 56:185-229.
37. Kiyomiya K., Matsuo S., Kurebe M. Mechanism of specific nuclear transport of adriamycin the mode of nuclear translocation of adriamycin-proteasome complex. Cancer Res 2001, 61:2467-2471.
38. Nakanishi T., Fukushima S., Okamoto K., Suzuki M., Matsumura Y., Yokoyama M., et al. Development of the polymer micelle carrier system for doxorubicin. JControl Release 2001, 74:295-302.
39. Childs A.C., Phaneuf S.L., Dirks A.J., Phillips T., Leeuwenburgh C. Doxorubicin treatment invivo causes cytochrome C release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2: Bax ratio. Cancer Res 2002, 62:4592-4598.
40. Goldstein J.L., Anderson R.G.W., Brown M.S. Coated pits, coated vesicles, and receptor-mediated endocytosis. Nature 1979, 279:679-685.
41. Peetla C., Vijayaraghavalu S., Labhasetwar V. Biophysics of cell membrane lipids in cancer drug resistance: implications for drug transport and drug delivery with nanoparticles. Adv Drug Deliv Rev 2013, 65:1686-1698.
42. Xu S., Olenyuk B.Z., Okamoto C.T., Hamm-Alvarez S.F. Targeting receptor-mediated endocytotic pathways with nanoparticles: rationale and advances. Adv Drug Deliv Rev 2013, 65:121-138.
43. Yamamoto T., Davis C.G., Brown M.S., Schneider W.J., Casey M.L., Goldstein J.L., et al. The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell 1984, 39:27-38.
44. Lee M., Rentz J., Han S.O., Bull D.A., Kim S.W. Water-soluble lipopolymer as an efficient carrier for gene delivery to myocardium. Gene Ther 2003, 10:585-593.
45. Möbius W., Donselaar E.V., Ohno-Iwashita Y., Shimada Y., Heijnen H.F.G., Slot J.W., et al. Recycling compartments and the internal vesicles of multivesicular bodies harbor most of the cholesterol found in the endocytic pathway. Traffic 2003, 4:222-231.
46. Mellet C.O., Fernández J.M.G., Benito J.M. Cyclodextrin-based gene delivery systems. Chem Soc Rev 2011, 40:1586-1608.
47. Tian Y., Jiang X., Chen X., Shao Z., Yang W. Doxorubicin-loaded magnetic silk fibroin nanoparticles for targeted therapy of multidrug-resistant cancer. Adv Mater 2014, 26:7393-7398.
48. Tang S., Yin Q., Zhang Z., Gu W., Chen L., Yu H., et al. Co-delivery of doxorubicin and RNA using pH-sensitive poly (β-amino ester) nanoparticles for reversal of multidrug resistance of breast cancer. Biomaterials 2014, 35:6047-6059.