Cellular uptake, intracellular distribution and degradation of Her2-targeting silk nanospheres

References

• Duncan R, Richardson SC. Endocytosis and intracellular trafficking as gateways for nanomedicine delivery: opportunities and challenges. Mol Pharm. 2012;9(9):2380–2402.22844998
   PubMed Web of Science ®Google Scholar
• Maeda H. Tumor-selective delivery of macromolecular drugs via the EPR effect: background and future prospects. Bioconj Chem. 2010;21(5):797–802.
   PubMed Web of Science ®Google Scholar
• Maeda H. The link between infection and cancer: tumor vasculature, free radicals, and drug delivery to tumors via the EPR effect. Cancer Sci. 2013;104(7):779–789.23495730
   PubMed Web of Science ®Google Scholar
• Prabhakar U, Maeda H, Jain RK, et al. Challenges and key considerations of the enhanced permeability and retention effect for nanomedicine drug delivery in oncology. Cancer Res. 2013;73(8):2412–2417.23423979
   PubMed Web of Science ®Google Scholar
• Yameen B, Choi WI, Vilos C, Swami A, Shi J, Farokhzad OC. Insight into nanoparticle cellular uptake and intracellular targeting. J Control Release. 2014;190:485–499.24984011
   PubMed Web of Science ®Google Scholar
• Rajendran L, Knolker HJ, Simons K. Subcellular targeting strategies for drug design and delivery. Nat Rev Drug Discov. 2010;9(1):29–42. doi:10.1038/nrd289720043027
   PubMed Web of Science ®Google Scholar
• Shi J, Kantoff PW, Wooster R, Farokhzad OC. Cancer nanomedicine: progress, challenges and opportunities. Nat Rev Cancer. 2017;17(1):20–37. doi:10.1038/nrc.2016.10827834398
   PubMed Web of Science ®Google Scholar
• Seib FP. Silk nanoparticles - an emerging anticancer nanomedicine. AIMS Bioeng. 2017;4(2):239–258. doi:10.3934/bioeng.2017.2.239
   Google Scholar
• Aigner TB, DeSimone E, Scheibel T. Biomedical applications of recombinant silk-based materials. Adv Mater. 2018;30(19):e1704636. doi:10.1002/adma.v30.1929436028
   PubMed Web of Science ®Google Scholar
• Jastrzebska K, Kucharczyk K, Florczak A, Dondajewska E, Mackiewicz A, Dams-Kozlowska H. Silk as an innovative biomaterial for cancer therapy. Rep Pract Oncol Radiother. 2015;20(2):87–98. doi:10.1016/j.rpor.2014.11.01025859397
   PubMedGoogle Scholar
• Deptuch T, Dams-Kozlowska H. Silk materials functionalized via genetic engineering for biomedical applications. Materials. 2018;10(12):1417–1438. doi:10.3390/ma10121417
   Web of Science ®Google Scholar
• Florczak A, Mackiewicz A, Dams-Kozlowska H. Functionalized spider silk spheres as drug carriers for targeted cancer therapy. Biomacromolecules. 2014;15(8):2971–2981. doi:10.1021/bm500591p24963985
   PubMed Web of Science ®Google Scholar
• Florczak A, Jastrzebska K, Mackiewicz A, Dams-Kozlowska H. Blending two bioengineered spider silks to develop cancer targeting spheres. J Mater Chem B. 2017;5:3000–3011. doi:10.1039/C7TB00233E
   PubMed Web of Science ®Google Scholar
• Numata K, Mieszawska-Czajkowska AJ, Kvenvold LA, Kaplan DL. Silk-based nanocomplexes with tumor-homing peptides for tumor-specific gene delivery. Macromol Biosci. 2012;12(1):75–82. doi:10.1002/mabi.20110027422052706
   PubMed Web of Science ®Google Scholar
• Elsner MB, Herold HM, Muller-Herrmann S, Bargel H, Scheibel T. Enhanced cellular uptake of engineered spider silk particles. Biomater Sci. 2015;3(3):543–551. doi:10.1039/c4bm00401a26222296
   PubMedGoogle Scholar
• Schierling MB, Doblhofer E, Scheibel T. Cellular uptake of drug loaded spider silk particles. Biomater Sci. 2016;4(10):1515–1523. doi:10.1039/c6bm00435k27709129
   PubMedGoogle Scholar
• Florczak A, Jastrzebska K, Bialas W, Mackiewicz A, Dams-Kozlowska H. Optimization of spider silk sphere formation processing conditions to obtain carriers with controlled characteristics. J Biomed Mater Res A. 2018;106(12):3211–3221. doi:10.1002/jbm.a.3651630242958
   PubMedGoogle Scholar
• Urbanelli L, Ronchini C, Fontana L, Menard S, Orlandi R, Monaci P. Targeted gene transduction of mammalian cells expressing the HER2/neu receptor by filamentous phage. J Mol Biol. 2001;313(5):965–976. doi:10.1006/jmbi.2001.511111700053
   PubMedGoogle Scholar
• Jastrzebska K, Felcyn E, Kozak M, et al. The method of purifying bioengineered spider silk determines the silk sphere properties. Sci Rep. 2016;6:28106. doi:10.1038/srep2810627312998
   PubMedGoogle Scholar
• Jastrzebska K, Florczak A, Kucharczyk K, et al. Delivery of chemotherapeutics using spheres made of bioengineered spider silks derived from MaSp1 and MaSp2 proteins. Nanomedicine (Lond). 2018;13(4):439–454. doi:10.2217/nnm-2017-027629338625
   PubMedGoogle Scholar
• Kozlowska AK, Florczak A, Smialek M, et al. Functionalized bioengineered spider silk spheres improve nuclease resistance and activity of oligonucleotide therapeutics providing a strategy for cancer treatment. Acta Biomater. 2017;59:221–233. doi:10.1016/j.actbio.2017.07.01428694238
   PubMed Web of Science ®Google Scholar
• Lammel A, Schwab M, Hofer M, Winter G, Scheibel T. Recombinant spider silk particles as drug delivery vehicles. Biomaterials. 2011;32(8):2233–2240. doi:10.1016/j.biomaterials.2010.11.06021186052
   PubMed Web of Science ®Google Scholar
• Hofer M, Winter G, Myschik J. Recombinant spider silk particles for controlled delivery of protein drugs. Biomaterials. 2012;33(5):1554–1562. doi:10.1016/j.biomaterials.2011.10.05322079006
   PubMedGoogle Scholar
• Totten JD, Wongpinyochit T, Seib FP. Silk nanoparticles: proof of lysosomotropic anticancer drug delivery at single-cell resolution. J Drug Target. 2017;25(9–10):865–872. doi:10.1080/1061186X.2017.136321228812388
   PubMed Web of Science ®Google Scholar
• Wongpinyochit T, Uhlmann P, Urquhart AJ, Seib FP. PEGylated silk nanoparticles for anticancer drug delivery. Biomacromolecules. 2015;16(11):3712–3722. doi:10.1021/acs.biomac.5b0100326418537
   PubMed Web of Science ®Google Scholar
• Dams-Kozlowska H, Majer A, Tomasiewicz P, Lozinska J, Kaplan DL, Mackiewicz A. Purification and cytotoxicity of tag-free bioengineered spider silk proteins. J Biomed Mater Res A. 2013;101(2):456–464. doi:10.1002/jbm.a.3435322865581
   PubMedGoogle Scholar
• Huemmerich D, Helsen CW, Quedzuweit S, Oschmann J, Rudolph R, Scheibel T. Primary structure elements of spider dragline silks and their contribution to protein solubility. Biochemistry. 2004;43(42):13604–13612. doi:10.1021/bi048983q15491167
   PubMed Web of Science ®Google Scholar
• Akagi T, Shima F, Akashi M. Intracellular degradation and distribution of protein-encapsulated amphiphilic poly(amino acid) nanoparticles. Biomaterials. 2011;32(21):4959–4967. doi:10.1016/j.biomaterials.2011.03.04921482432
   PubMedGoogle Scholar
• Conner SD, Schmid SL. Regulated portals of entry into the cell. Nature. 2003;422(6927):37–44. doi:10.1038/nature0145112621426
   PubMed Web of Science ®Google Scholar
• Chen Q, Long M, Qiu L, et al. Decoration of pH-sensitive copolymer micelles with tumor-specific peptide for enhanced cellular uptake of doxorubicin. Int J Nanomedicine. 2016;11:5415–5427. doi:10.2147/IJN.S11195027799766
   PubMedGoogle Scholar
• Xu S, Olenyuk BZ, Okamoto CT, Hamm-Alvarez SF. Targeting receptor-mediated endocytotic pathways with nanoparticles: rationale and advances. Adv Drug Deliv Rev. 2013;65(1):121–138. doi:10.1016/j.addr.2012.09.04123026636
   PubMed Web of Science ®Google Scholar
• Maitz MF, Sperling C, Wongpinyochit T, Herklotz M, Werner C, Seib FP. Biocompatibility assessment of silk nanoparticles: hemocompatibility and internalization by human blood cells. Nanomedicine. 2017;13(8):2633–2642. doi:10.1016/j.nano.2017.07.01228757180
   PubMedGoogle Scholar
• 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(43):7393–7398. doi:10.1002/adma.20140356225238148
   PubMedGoogle Scholar
• Vercauteren D, Vandenbroucke RE, Jones AT, et al. The use of inhibitors to study endocytic pathways of gene carriers: optimization and pitfalls. Mol Ther. 2010;18(3):561–569. doi:10.1038/mt.2009.28120010917
   PubMed Web of Science ®Google Scholar
• Harhaji-Trajkovic L, Arsikin K, Kravic-Stevovic T, et al. Chloroquine-mediated lysosomal dysfunction enhances the anticancer effect of nutrient deprivation. Pharm Res. 2012;29(8):2249–2263. doi:10.1007/s11095-012-0753-122538436
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Levine B. Methods in mammalian autophagy research. Cell. 2010;140(3):313–326. doi:10.1016/j.cell.2010.01.02820144757
   PubMed Web of Science ®Google Scholar
• Seglen O. Inhibitors of lysosomal function In: Methods in Enzymology. Vol. 96 Elsevier Inc; 1983.
   Google Scholar
• Zou F, Schafer N, Palesch D, et al. Regulation of cathepsin G reduces the activation of proinsulin-reactive T cells from type 1 diabetes patients. PLoS One. 2011;6(8):e22815. doi:10.1371/journal.pone.002281521850236
   PubMedGoogle Scholar
• Jung M, Lee J, Seo HY, Lim JS, Kim EK. Cathepsin inhibition-induced lysosomal dysfunction enhances pancreatic beta-cell apoptosis in high glucose. PLoS One. 2015;10(1):e0116972. doi:10.1371/journal.pone.011697225625842
   PubMed Web of Science ®Google Scholar
• Ohkuma S, Poole B. Fluorescence probe measurement of the intralysosomal pH in living cells and the perturbation of pH by various agents. Proc Nat Acad Sci USA. 1978;75(7):3327–3331. doi:10.1073/pnas.75.7.332728524
   PubMed Web of Science ®Google Scholar
• Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9(8):581–593. doi:10.1038/nri256719498381
   PubMed Web of Science ®Google Scholar
• Sun Y, Liu J. Potential of cancer cell-derived exosomes in clinical application: a review of recent research advances. Clin Ther. 2014;36(6):863–872. doi:10.1016/j.clinthera.2014.04.01824863262
   PubMed Web of Science ®Google Scholar
• Chalmin F, Ladoire S, Mignot G, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120(2):457–471. doi:10.1172/JCI4048320093776
   PubMed Web of Science ®Google Scholar
• Savina A, Furlan M, Vidal M, Colombo MI. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J Biol Chem. 2003;278(22):20083–20090. doi:10.1074/jbc.M30164220012639953
   PubMed Web of Science ®Google Scholar
• Orci L, Tagaya M, Amherdt M, et al. Brefeldin A, a drug that blocks secretion, prevents the assembly of non-clathrin-coated buds on Golgi cisternae. Cell. 1991;64(6):1183–1195. doi:10.1016/0092-8674(91)90273-22004424
   PubMedGoogle Scholar
• Misumi Y, Misumi Y, Miki K, Takatsuki A, Tamura G, Ikehara Y. Novel blockade by brefeldin A of intracellular transport of secretory proteins in cultured rat hepatocytes. J Biol Chem. 1986;261(24):11398–11403.2426273
   PubMed Web of Science ®Google Scholar
• Liu W, Baker SS, Trinidad J, et al. Inhibition of lysosomal enzyme activities by proton pump inhibitors. J Gastroenterol. 2013;48(12):1343–1352. doi:10.1007/s00535-013-0774-523478938
   PubMed Web of Science ®Google Scholar
• Lee CM, Tannock IF. Inhibition of endosomal sequestration of basic anticancer drugs: influence on cytotoxicity and tissue penetration. Br J Cancer. 2006;94(6):863–869. doi:10.1038/sj.bjc.660301016495919
   PubMedGoogle Scholar
• Cao Y, Wang B. Biodegradation of silk biomaterials. Int J Mol Sci. 2009;10(4):1514–1524. doi:10.3390/ijms1004151419468322
   PubMed Web of Science ®Google Scholar
• Thurber AE, Omenetto FG, Kaplan DL. In vivo bioresponses to silk proteins. Biomaterials. 2015;71:145–157. doi:10.1016/j.biomaterials.2015.08.03926322725
   PubMed Web of Science ®Google Scholar
• Liu B, Song YW, Jin L, et al. Silk structure and degradation. Colloids Surf B Biointerfaces. 2015;131:122–128. doi:10.1016/j.colsurfb.2015.04.04025982316
   PubMed Web of Science ®Google Scholar
• Brown J, Lu CL, Coburn J, Kaplan DL. Impact of silk biomaterial structure on proteolysis. Acta Biomater. 2015;11:212–221. doi:10.1016/j.actbio.2014.09.01325240984
   PubMedGoogle Scholar
• Horan RL, Antle K, Collette AL, et al. In vitro degradation of silk fibroin. Biomaterials. 2005;26(17):3385–3393. doi:10.1016/j.biomaterials.2004.09.02015621227
   PubMed Web of Science ®Google Scholar
• Wang Y, Rudym DD, Walsh A, et al. In vivo degradation of three-dimensional silk fibroin scaffolds. Biomaterials. 2008;29(24–25):3415–3428. doi:10.1016/j.biomaterials.2008.05.00218502501
   PubMed Web of Science ®Google Scholar
• Li M, Ogiso M, Minoura N. Enzymatic degradation behavior of porous silk fibroin sheets. Biomaterials. 2003;24(2):357–365.12419638
   PubMed Web of Science ®Google Scholar
• Wongpinyochit T, Johnston BF, Seib FP. Degradation behavior of silk nanoparticles - enzyme responsiveness. ACS Biomater Sci Eng. 2018;4:942–951. doi:10.1021/acsbiomaterials.7b01021
   PubMed Web of Science ®Google Scholar