Sericin nanomicelles with enhanced cellular uptake and pH-triggered release of doxorubicin reverse cancer drug resistance

References

• Alexis F, Pridgen E, Molnar LK, Farokhzad OC. (2008). Factors affecting the clearance and biodistribution of polymeric nanoparticles. Mol Pharmaceutics 5:505–15.
   PubMed Web of Science ®Google Scholar
• Andre EM, Pensado A, Resnier P, et al. (2016). Characterization and comparison of two novel nanosystems associated with siRNA for cellular therapy. Int J Pharm 497:255–67.
   PubMed Web of Science ®Google Scholar
• Beddoes CM, Case CP, Briscoe WH. (2015). Understanding nanoparticle cellular entry: a physicochemical perspective. Adv Colloid Interface Sci 218:48–68.
   PubMed Web of Science ®Google Scholar
• Cabral H, Matsumoto Y, Mizuno K, et al. (2011). Accumulation of sub-100 nm polymeric micelles in poorly permeable tumours depends on size. Nature Nanotech 6:815–23.
   PubMed Web of Science ®Google Scholar
• Cao T, Zhang Y. (2016). Processing and characterization of silk sericin from Bombyx mori and its application in biomaterials and biomedicines. Mater Sci Eng C 61:940–52.
   PubMed Web of Science ®Google Scholar
• Chang L, Yuan Y, Li C, et al. (2016). Upregulation of SNHG6 regulates ZEB1 expression by competitively binding miR-101-3p and interacting with UPF1 in hepatocellular carcinoma. Cancer Lett 383:183–94.
   PubMed Web of Science ®Google Scholar
• Chen M, Shao Z, Chen X. (2012). Paclitaxel-loaded silk fibroin nanospheres. J Biomed Mater Res A 100:203–10.
   PubMed Web of Science ®Google Scholar
• Davis ME, Chen ZG, Shin DM. (2008). Nanoparticle therapeutics: an emerging treatment modality for cancer. Nat Rev Drug Discov 7:771–82.
   PubMed Web of Science ®Google Scholar
• Dewanjee S, Dua TK, Bhattacharjee N, et al. (2017). Natural products as alternative choices for P-glycoprotein (P-gp) inhibition. Molecules 22:871.
   Web of Science ®Google Scholar
• Fang J, Yong Q, Zhang K, et al. (2015). Novel injectable porous poly(g-benzyl-L- glutamate) microspheres for cartilage tissue engineering: preparation and evaluation. J Mater Chem B 3(3):1020–31.
   PubMed Web of Science ®Google Scholar
• Gabizon A, Meshorer A, Barenholz Y. (1986). Comparative long-term study of the toxicities of free and liposome-associated doxorubicin in mice after intravenous administration. J Natl Cancer Inst 77:459–69.
   PubMed Web of Science ®Google Scholar
• Goldman A, Kulkarni A, Kohandel M, et al. (2016). Rationally designed 2-in-1 nanoparticles can overcome adaptive resistance in cancer. ACS Nano 10:5823–34.
   PubMed Web of Science ®Google Scholar
• Gupta P, Garg T, Tanmay M, Arora S. (2015). Polymeric drug-delivery systems: role in P-gp efflux system inhibition. Crit Rev Ther Drug Carrier Syst 32:247–75.
   PubMed Web of Science ®Google Scholar
• He Q, Shi J. (2014). MSN anti-cancer nanomedicines: chemotherapy enhancement, overcoming of drug resistance, and metastasis inhibition. Adv Mater 26:391–411.
   PubMed Web of Science ®Google Scholar
• Hekmat A, Attar H, Seyf KA, et al. (2016). New oral formulation and in vitro evaluation of docetaxel-loaded nanomicelles. Molecules 21:1265.
   PubMed Web of Science ®Google Scholar
• Hoosain FG, Choonara YE, Tomar LK, et al. (2015). Bypassing P-glycoprotein drug efflux mechanisms: possible applications in pharmacoresistant schizophrenia therapy. Biomed Res Int 2015:484963.
   PubMed Web of Science ®Google Scholar
• Hu D, Xu Z, Hu Z, et al. (2016). pH-Triggered charge-reversal silk sericin-based nanoparticles for enhanced cellular uptake and doxorubicin delivery. ACS Sustainable Chem Eng 5:1638–47.
   Web of Science ®Google Scholar
• Hua C, Dong CM, Wei Y. (2009). Versatile strategy for the synthesis of dendronlike polypeptide/linear poly(epsilon-caprolactone) block copolymers via click chemistry. Biomacromolecules 10:1140–8.
   PubMed Web of Science ®Google Scholar
• Huang Y, Jan J. (2014). Carboxylmethyl chitosan-graft-poly(γ-benzyl-l-glutamate) glycopeptides: synthesis and particle formation as encapsulants. Polymer 55:540–9.
   Web of Science ®Google Scholar
• Huang L, Tao K, Liu J, et al. (2016). Design and fabrication of multifunctional sericin nanoparticles for tumor targeting and pH-responsive subcellular delivery of cancer chemotherapy drugs. ACS Appl Mater Interfaces 8:6577–85.
   PubMed Web of Science ®Google Scholar
• Huwyler J, Cerletti A, Fricker G, et al. (2002). By-passing of P-glycoprotein using immunoliposomes. J Drug Target 10:73–9.
   PubMed Web of Science ®Google Scholar
• Jansen JA, de Boer TP, Wolswinkel R, et al. (2008). Lysosome mediated Kir2.1 breakdown directly influences inward rectifier current density. Biochem Biophys Res Commun 367:687–92.
   PubMed Web of Science ®Google Scholar
• Jin Y, Liu L, Zhang S, et al. (2016). Chromium alters lipopolysaccharide-induced inflammatory responses both in vivo and in vitro. Chemosphere 148:436–43.
   PubMed Web of Science ®Google Scholar
• Khire TS, Kundu J, Kundu SC, Yadavalli VK. (2010). The fractal self-assembly of the silk protein sericin. Soft Matter 6:2066.
   Web of Science ®Google Scholar
• Kibria G, Hatakeyama H, Harashima H. (2014). Cancer multidrug resistance: mechanisms involved and strategies for circumvention using a drug delivery system. Arch Pharm Res 37:4–15.
   PubMed Web of Science ®Google Scholar
• Kim HK, Noh YH, Nilius B, et al. (2017). Current and upcoming mitochondrial targets for cancer therapy. Semin Cancer Biol 47:154–67.
   PubMed Web of Science ®Google Scholar
• Kundu J, Chung YI, Kim YH, et al. (2010). Silk fibroin nanoparticles for cellular uptake and control release. Int J Pharm 388:242–50.
   PubMed Web of Science ®Google Scholar
• Lamboni L, Gauthier M, Yang G, Wang Q. (2015). Silk sericin: a versatile material for tissue engineering and drug delivery. Biotechnol Adv 33:1855–67.
   PubMed Web of Science ®Google Scholar
• Lammel A, Schwab M, Hofer M, et al. (2011). Recombinant spider silk particles as drug delivery vehicles. Biomaterials 32:2233–40.
   PubMed Web of Science ®Google Scholar
• Lammel AS, Hu X, Park SH, et al. (2010). Controlling silk fibroin particle features for drug delivery. Biomaterials 31:4583–91.
   PubMed Web of Science ®Google Scholar
• Lee H, Dam DH, Ha JW, et al. (2015). Enhanced human epidermal growth factor receptor 2 degradation in breast cancer cells by lysosome-targeting gold nanoconstructs. ACS Nano 9:9859–67.
   PubMed Web of Science ®Google Scholar
• Liu J, Li Q, Zhang J, et al. (2017). Safe and effective reversal of cancer multidrug resistance using sericin-coated mesoporous silica nanoparticles for lysosome-targeting delivery in mice. Small 13:1602567.
   Web of Science ®Google Scholar
• Lv S, Ji L, Chen B, et al. (2018). Histone methyltransferase KMT2D sustains prostate carcinogenesis and metastasis via epigenetically activating LIFR and KLF4. Oncogene 37:1354–68.
   PubMed Web of Science ®Google Scholar
• Mandal BB, Kundu SC. (2009). Self-assembled silk sericin/poloxamer nanoparticles as nanocarriers of hydrophobic and hydrophilic drugs for targeted delivery. Nanotechnology 20:355101.
   PubMed Web of Science ®Google Scholar
• Markman JL, Rekechenetskiy A, Holler E, Ljubimova JY. (2013). Nanomedicine therapeutic approaches to overcome cancer drug resistance. Adv Drug Deliv Rev 65:1866–79.
   PubMed Web of Science ®Google Scholar
• Mayor S, Pagano RE. (2007). Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8:603–12.
   PubMed Web of Science ®Google Scholar
• Merrifield CJ, Kaksonen M. (2014). Endocytic accessory factors and regulation of clathrin-mediated endocytosis. Cold Spring Harb Perspect Biol 6:a16733.
   Web of Science ®Google Scholar
• Qu Q, Ma X, Zhao Y. (2015). Targeted delivery of doxorubicin to mitochondria using mesoporous silica nanoparticle nanocarriers. Nanoscale 7:16677–86.
   PubMed Web of Science ®Google Scholar
• Rajagopal A, Simon SM. (2003). Subcellular localization and activity of multidrug resistance proteins. Mol Biol Cell 14:3389–99.
   PubMed Web of Science ®Google Scholar
• Rashidi M, Bandala-Sanchez E, Lawlor KE, et al. (2018). CD52 inhibits Toll-like receptor activation of NF-kappaB and triggers apoptosis to suppress inflammation. Cell Death Differ 25:392–405.
   PubMed Web of Science ®Google Scholar
• Seib FP, Jones GT, Rnjak-Kovacina J, et al. (2013). pH-dependent anticancer drug release from silk nanoparticles. Adv Healthc Mater 2:1606–11.
   PubMed Web of Science ®Google Scholar
• Shapira A, Livney YD, Broxterman HJ, Assaraf YG. (2011). Nanomedicine for targeted cancer therapy: towards the overcoming of drug resistance. Drug Resist Update 14:150–63.
   PubMed Web of Science ®Google Scholar
• Siegel RL, Miller KD, Jemal A. (2016). Cancer statistics, 2016. CA Cancer J Clin 66:7–30.
   PubMed Web of Science ®Google Scholar
• Upadhyay KK, Meins JFL, Misra A, et al. (2009). Biomimetic doxorubicin loaded polymersomes from hyaluronan-block-poly(γ-benzyl glutamate) copolymers. Biomacromolecules 10:2802–8.
   PubMed Web of Science ®Google Scholar
• Vepari C, Kaplan DL. (2007). Silk as a biomaterial. Prog Polym Sci 32:991–1007.
   PubMed Web of Science ®Google Scholar
• Walker WA, Tarannum M, Vivero-Escoto JL. (2016). Cellular endocytosis and trafficking of cholera toxin B-modified mesoporous silica nanoparticles. J Mater Chem B Mater B 4:1254–62.
   PubMed Web of Science ®Google Scholar
• Wang S, Xu T, Yang Y, Shao Z. (2015). Colloidal stability of silk fibroin nanoparticles coated with cationic polymer for effective drug delivery. ACS Appl Mater Interfaces 7:21254–62.
   PubMed Web of Science ®Google Scholar
• Wang YY, Zhang DD, Kong YY, et al. (2016). CS/PAA@TPGS/PLGA nanoparticles with intracellular pH-sensitive sequential release for delivering drug to the nucleus of MDR cells. Colloids Surf B Biointerfaces 145:716–27.
   PubMed Web of Science ®Google Scholar
• Wang Z, Sheng R, Luo T, et al. (2017). Synthesis and self-assembly of diblock glycopolypeptide analogues PMAgala-b-PBLG as multifunctional biomaterials for protein recognition, drug delivery and hepatoma cell targeting. Polym Chem 8:472–84.
   Web of Science ®Google Scholar
• Wang Z, Zhang Y, Zhang J, et al. (2014). Exploring natural silk protein sericin for regenerative medicine: an injectable, photoluminescent, cell-adhesive 3D hydrogel. Sci Rep 4:7064.
   PubMed Web of Science ®Google Scholar
• Xia XX, Wang M, Lin Y, et al. (2014). Hydrophobic drug-triggered self-assembly of nanoparticles from silk-elastin-like protein polymers for drug delivery. Biomacromolecules 15:908–14.
   PubMed Web of Science ®Google Scholar
• Xu R, Zhang G, Mai J, et al. (2016). An injectable nanoparticle generator enhances delivery of cancer therapeutics. Nat Biotechnol 34:414–8.
   PubMed Web of Science ®Google Scholar
• Xu G, Shi H, Ren L, et al. (2015). Enhancing the anti-colon cancer activity of quercetin by self-assembled micelles. Int J Nanomedicine 10:2051–63.
   PubMed Web of Science ®Google Scholar
• Yang M, Shuai Y, Zhou G, et al. (2014). Tuning molecular weights of Bombyx mori (B. mori) silk sericin to modify its assembly structures and materials formation. ACS Appl Mater Interfaces 6:13782–9.
   PubMed Web of Science ®Google Scholar
• Yang D, Wang T, Su Z, et al. (2016). Reversing cancer multidrug resistance in xenograft models via orchestrating multiple actions of functional mesoporous silica nanoparticles. ACS Appl Mater Interfaces 8:22431–41.
   PubMed Web of Science ®Google Scholar
• Yin Q, Shen J, Zhang Z, et al. (2013). Reversal of multidrug resistance by stimuli-responsive drug delivery systems for therapy of tumor. Adv Drug Deliv Rev 65:1699–715.
   PubMed Web of Science ®Google Scholar
• Zhang P, Zhang H, He W, et al. (2016). Disulfide-linked amphiphilic polymer-docetaxel conjugates assembled redox-sensitive micelles for efficient antitumor drug delivery. Biomacromolecules 17:1621–32.
   PubMed Web of Science ®Google Scholar
• Zhang XD, Wu D, Shen X, et al. (2012). In vivo renal clearance, biodistribution, toxicity of gold nanoclusters. Biomaterials 33:4628–38.
   PubMed Web of Science ®Google Scholar
• Zhaorigetu S, Sasaki M, Kato N. (2007). Consumption of sericin suppresses colon oxidative stress and aberrant crypt foci in 1,2-dimethylhydrazine-treated rats by colon undigested sericin. J Nutr Sci Vitaminol (Tokyo) 53:297–300.
   PubMed Web of Science ®Google Scholar
• Zhaorigetu S, Yanaka N, Sasaki M, et al. (2003). Inhibitory effects of silk protein, sericin on UVB-induced acute damage and tumor promotion by reducing oxidative stress in the skin of hairless mouse. J Photochem Photobiol B 71:11–7.
   PubMed Web of Science ®Google Scholar
• Zhaorigetu S, Yanaka N, Sasaki M, et al. (2003). Silk protein, sericin, suppresses DMBA-TPA-induced mouse skin tumorigenesis by reducing oxidative stress, inflammatory responses and endogenous tumor promoter TNF-alpha. Oncol Rep 10:537–43.
   PubMed Web of Science ®Google Scholar