Magnetic labeling of natural lipid encapsulations with iron-based nanoparticles
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With superior biocompatibility and unique magnetic properties, iron-based nanoparticles (IBNP) are commonly encapsulated in cells and extracellular vesicles (EV) to allow for magnetic force controlled drug delivery and non-invasive tracking. Based on their natural source and similar morphology, we classify both cells and EVs as being natural lipid encapsulations (NLEs), distinguishing them from synthetic liposomes. Both their imaging contrast and drug effects are dominated by the amount of iron encapsulated in each NLE, demonstrating the importance of magnetic labeling efficiency. It is known that the membranes function as barriers to ensure that substances pass in and out in an orderly manner. The most important issue in increasing the cellular uptake of IBNPs is the interaction between the NLE membrane and IBNPs, which has been found to be affected by properties of the IBNPs as well as NLE heterogeneity. Two aspects are important for effective magnetic labelling: First, how to effectively drive membrane wrapping of the nanoparticles into the NLEs, and second, how to balance biosafety and nanoparticle uptake. In this review, we will provide a systematic overview of the magnetic labeling of NLEs with IBNPs. This article provides a summary of the applications of magnetically labeled NLEs and the labeling methods used for IBNPs. The review also analyzes the role of IBNPs physicochemical properties, especially their magnetic properties, and the heterogeneity of NLEs in the internalization pathway. At the same time, the future development of magnetically labeled NLEs is also discussed.
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Magnetic labeling of natural lipid encapsulations with iron-based nanoparticles
)
Abstract
With superior biocompatibility and unique magnetic properties, iron-based nanoparticles (IBNP) are commonly encapsulated in cells and extracellular vesicles (EV) to allow for magnetic force controlled drug delivery and non-invasive tracking. Based on their natural source and similar morphology, we classify both cells and EVs as being natural lipid encapsulations (NLEs), distinguishing them from synthetic liposomes. Both their imaging contrast and drug effects are dominated by the amount of iron encapsulated in each NLE, demonstrating the importance of magnetic labeling efficiency. It is known that the membranes function as barriers to ensure that substances pass in and out in an orderly manner. The most important issue in increasing the cellular uptake of IBNPs is the interaction between the NLE membrane and IBNPs, which has been found to be affected by properties of the IBNPs as well as NLE heterogeneity. Two aspects are important for effective magnetic labelling: First, how to effectively drive membrane wrapping of the nanoparticles into the NLEs, and second, how to balance biosafety and nanoparticle uptake. In this review, we will provide a systematic overview of the magnetic labeling of NLEs with IBNPs. This article provides a summary of the applications of magnetically labeled NLEs and the labeling methods used for IBNPs. The review also analyzes the role of IBNPs physicochemical properties, especially their magnetic properties, and the heterogeneity of NLEs in the internalization pathway. At the same time, the future development of magnetically labeled NLEs is also discussed.
References(190)
Lin, C. L.; Ho, Y. S. A bibliometric analysis of publications on pluripotent stem cell research. Cell J. 2015, 17, 59–70.
Petrou, P.; Gothelf, Y.; Argov, Z.; Gotkine, M.; Levy, Y. S.; Kassis, I.; Vaknin-Dembinsky, A.; Ben-Hur, T.; Offen, D.; Abramsky, O. et al. Safety and clinical effects of mesenchymal stem cells secreting neurotrophic factor transplantation in patients with amyotrophic lateral sclerosis results of phase 1/2 and 2A clinical trials. JAMA Neurol. 2016, 73, 337–344.
Yáñez-Mó, M.; Siljander, P. R. M.; Andreu, Z.; Zavec, A. B.; Borràs, F. E.; Buzas, E. I.; Buzas, K.; Casal, E.; Cappello, F.; Carvalho, J. et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles 2015, 4, 27066–27126.
Chen, X.; Ba, Y.; Ma, L. J.; Cai, X.; Yin, Y.; Wang, K. H.; Guo, J. G.; Zhang, Y. J.; Chen, J. N.; Guo, X. et al. Characterization of microRNAs in serum: A novel class of biomarkers for diagnosis of cancer and other diseases. Cell Res. 2008, 18, 997–1006.
Zaborowski, M. P.; Balaj, L.; Breakefield, X. O.; Lai, C. P. Extracellular vesicles: Composition, biological relevance, and methods of study. Bioscience 2015, 65, 783–797.
Allen, T. M.; Cullis, P. R. Liposomal drug delivery systems: From concept to clinical applications. Adv. Drug Deliv. Rev. 2013, 65, 36–48.
Riazifar, M.; Pone, E. J.; Lötvall, J.; Zhao, W. A. Stem cell extracellular vesicles: Extended messages of regeneration. Ann. Rev. Pharmacol. Toxicol. 2017, 57, 125–154.
György, B.; Hung, M. E.; Breakefield, X. O.; Leonard, J. N. Therapeutic applications of extracellular vesicles: Clinical promise and open questions. Ann. Rev. Pharmacol. Toxicol. 2015, 55, 439–464.
Chai, Z. L.; Hu, X. F.; Lu, W. Y. Cell membrane-coated nanoparticles for tumor-targeted drug delivery. Sci. China Mater. 2017, 60, 504–510.
Calò, A.; Reguera, D.; Oncins, G.; Persuy, M. A.; Sanz, G.; Lobasso, S.; Corcelli, A.; Pajot-Augy, E.; Gomila, G. Force measurements on natural membrane nanovesicles reveal a composition-independent, high young's modulus. Nanoscale 2014, 6, 2275–2285.
Chen, O.; Riedemann, L.; Etoc, F.; Herrmann, H.; Coppey, M.; Barch, M.; Farrar, C. T.; Zhao, J.; Bruns, O. T.; Wei, H. et al. Magneto-fluorescent core-shell supernanoparticles. Nat. Commun. 2014, 5, 5093-5101.
Key, J.; Leary, J. F. Nanoparticles for multimodal in vivo imaging in nanomedicine. Int. J. Nanomedicine 2014, 9, 711–726.
Chen, B.; Li, Y.; Zhang, X. Q.; Liu, F.; Liu, Y. L.; Ji, M.; Xiong, F.; Gu, N. An efficient synthesis of ferumoxytol induced by alternating-current magnetic field. Mater. Lett. 2016, 170, 93–96.
Duan, L.; Yang, F.; He, W.; Song, L. N.; Qiu, F.; Xu, N.; Xu, L.; Zhang, Y.; Hua, Z. C.; Gu, N. A multi-gradient targeting drug delivery system based on RGD-L-TRAIL-labeled magnetic microbubbles for cancer theranostics. Adv. Funct. Mater. 2016, 26, 8313–8324.
Ma, X. X.; Tao, H. Q.; Yang, K.; Feng, L. Z.; Cheng, L.; Shi, X. Z.; Li, Y. G.; Guo, L.; Liu, Z. A functionalized graphene oxide-iron oxide nanocomposite for magnetically targeted drug delivery, photothermal therapy, and magnetic resonance imaging. Nano Res. 2012, 5, 199–212.
Yigit, M. V.; Moore, A.; Medarova, Z. Magnetic nanoparticles for cancer diagnosis and therapy. Pharm. Res. 2012, 29, 1180–1188.
Peer, D.; Karp, J. M.; Hong, S.; FaroKhzad, O. C.; Margalit, R.; Langer, R. Nanocarriers as an emerging platform for cancer therapy. Nat. Nanotechnol. 2007, 2, 751–760.
Ding, Q.; Liu, D. F.; Guo, D. W.; Yang, F.; Pang, X. Y.; Che, R. C.; Zhou, N. Z.; Xie, J.; Sun, J. F.; Huang, Z. H. et al. Shape-controlled fabrication of magnetite silver hybrid nanoparticles with high performance magnetic hyperthermia. Biomaterials 2017, 124, 35–46.
Wang, M.; Thanou, M. Targeting nanoparticles to cancer. Pharmacol. Res. 2010, 62, 90–99.
Berman, S. M. C.; Walczak, P.; Bulte, J. W. M. Tracking stem cells using magnetic nanoparticles. Wiley Interdiscip. Rev. Nanomed. Nanobiotechnol. 2011, 3, 343–355.
Li, L.; Jiang, W.; Luo, K.; Song, H. M.; Lan, F.; Wu, Y.; Gu, Z. W. Superparamagnetic iron oxide nanoparticles as mri contrast agents for non-invasive stem cell labeling and tracking. Theranostics 2013, 3, 595–615.
Prashant, C.; Dipak, M.; Yang, C. T.; Chuang, K. H.; Jun, D.; Feng, S. S. Superparamagnetic iron oxide-loaded poly(lactic acid)-D-α-tocopherol polyethylene glycol 1000 succinate copolymer nanoparticles as mri contrast agent. Biomaterials 2010, 31, 5588–5597.
Kircher, M. F.; Gambhir, S. S.; Grimm, J. Noninvasive cell-tracking methods. Nat. Rev. Clin. Oncol. 2011, 8, 677–688.
Behzadi, S.; Serpooshan, V.; Tao, W.; Hamaly, M. A.; Alkawareek, M. Y.; Dreaden, E. C.; Brown, D.; Alkilany, A. M.; Farokhzad, O. C.; Mahmoudi, M. Cellular uptake of nanoparticles: Journey inside the cell. Chem. Soc. Rev. 2017, 46, 4218–4244.
Gupta, A. K.; Gupta, M. Synthesis and surface engineering of iron oxide nanoparticles for biomedical applications. Biomaterials 2005, 26, 3995–4021.
Mura, S.; Nicolas, J.; Couvreur, P. Stimuli-responsive nanocarriers for drug delivery. Nat. Mater. 2013, 12, 991–1003.
Katagiri, K.; Imai, Y.; Koumoto, K.; Kaiden, T.; Kono, K.; Aoshima, S. Magnetoresponsive on-demand release of hybrid liposomes formed from Fe3O4 nanoparticles and thermosensitive block copolymers. Small 2011, 7, 1683–1689.
Tassa, C.; Shaw, S. Y.; Weissleder, R. Dextran-coated iron oxide nanoparticles: A versatile platform for targeted molecular imaging, molecular diagnostics, and therapy. Acc. Chem. Res. 2011, 44, 842–852.
Silva, A. K. A.; Luciani, N.; Gazeau, F.; Aubertin, K.; Bonneau, S.; Chauvierre, C.; Letourneur, D.; Wilhelm, C. Combining magnetic nanoparticles with cell derived microvesicles for drug loading and targeting. Nanomed. -Nanotechnol. Biol. Med. 2015, 11, 645–655.
Tukmachev, D.; Lunov, O.; Zablotskii, V.; Dejneka, A.; Babic, M.; Syková, E.; Kubinová, Š. An effective strategy of magnetic stem cell delivery for spinal cord injury therapy. Nanoscale 2015, 7, 3954–3958.
Penland, N.; Choi, E.; Perla, M.; Park, J.; Kim, D. H. Facile fabrication of tissue-engineered constructs using nanopatterned cell sheets and magnetic levitation. Nanotechnology 2017, 28, 075103–075111.
Ho, V. H. B.; Müller, K. H.; Barcza, A.; Chen, R. J.; Slater, N. K. H. Generation and manipulation of magnetic multicellular spheroids. Biomaterials 2010, 31, 3095–3102.
Ito, A.; Ino, K.; Hayashida, M.; Kobayashi, T.; Matsunuma, H.; Kagami, H.; Ueda, M.; Honda, H. Novel methodology for fabrication of tissue-engineered tubular constructs using magnetite nanoparticles and magnetic force. Tissue Eng. 2005, 11, 1553–1561.
Whatley, B. R.; Li, X. W.; Zhang, N.; Wen, X. J. Magnetic-directed patterning of cell spheroids. J. Biomed. Mater. Res. Part A 2014, 102, 1537–1547.
Boehm-Sturm, P.; Mengler, L.; Wecker, S.; Hoehn, M.; Kallur, T. In vivo tracking of human neural stem cells with 19F magnetic resonance imaging. PLoS One 2011, 6, e29040–e29049.
Daadi, M. M.; Li, Z. J.; Arac, A.; Grueter, B. A.; Sofilos, M.; Malenka, R. C.; Wu, J. C.; Steinberg, G. K. Molecular and magnetic resonance imaging of human embryonic stem cell-derived neural stem cell grafts in ischemic rat brain. Mol. Ther. 2009, 17, 1282–1291.
Silva, A. K. A.; Wilhelm, C.; Kolosnjaj-Tabi, J.; Luciani, N.; Gazeau, F. Cellular transfer of magnetic nanoparticles via cell microvesicles: Impact on cell tracking by magnetic resonance imaging. Pharm. Res. 2012, 29, 1392–1403.
Kumari, S.; Swetha, M. G.; Mayor, S. Endocytosis unplugged: Multiple ways to enter the cell. Cell Res. 2010, 20, 256–275.
Mooren, O. L.; Galletta, B. J.; Cooper, J. A. Roles for actin assembly in endocytosis. Annu. Rev. Biochem. 2012, 81, 661–686.
Porat-Shliom, N.; Milberg, O.; Masedunskas, A.; Weigert, R. Multiple roles for the actin cytoskeleton during regulated exocytosis. Cell. Mol. Life Sci. 2013, 70, 2099–2121.
Lim, J. P.; Gleeson, P. A. Macropinocytosis: An endocytic pathway for internalising large gulps. Immunol. Cell Biol. 2011, 89, 836–843.
de Vries, E.; Tscherne, D. M.; Wienholts, M. J.; Cobos-Jiménez, V.; Scholte, F.; García-Sastre, A.; Rottier, P. J. M.; de Haan, C. A. M. Dissection of the influenza a virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS Pathog. 2011, 7, e1001329-e1001348.
Geiser, M. Update on macrophage clearance of inhaled micro-and nanoparticles. J. Aerosol Med. Pulm. Drug Deliv. 2010, 23, 207–217.
Yameen, B.; Choi, W. I.; Vilos, C.; Swami, A.; Shi, J. J.; Farokhzad, O. C. Insight into nanoparticle cellular uptake and intracellular targeting. J. Control. Release 2014, 190, 485–499.
Banerjee, A.; Berezhkovskii, A.; Nossal, R. Kinetics of cellular uptake of viruses and nanoparticles via clathrin-mediated endocytosis. Phys. Biol. 2016, 13, 016005–016018.
Harush-Frenkel, O.; Altschuler, Y.; Benita, S. Nanoparticle-cell interactions: Drug delivery implications. Crit. Rev. Ther. Drug Carr. Syst. 2008, 25, 485–544.
Pelkmans, L.; Kartenbeck, J.; Helenius, A. Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 2001, 3, 473–483.
Rodríguez, N. E.; Gaur, U.; Wilson, M. E. Role of caveolae in Leishmania chagasi phagocytosis and intracellular survival in macrophages. Cell Microbiol. 2006, 8, 1106–1120.
Li, W.; Chen, C. Y.; Ye, C.; Wei, T. T.; Zhao, Y. L.; Lao, F.; Chen, Z.; Meng, H.; Gao, Y. X.; Yuan, H. et al. The translocation of fullerenic nanoparticles into lysosome via the pathway of clathrin-mediated endocytosis. Nanotechnology 2008, 19, 145102.
Bryant, L. H.; Kim, S. J.; Hobson, M.; Milo, B.; Kovacs, Z. I.; Jikaria, N.; Lewis, B. K.; Aronova, M. A.; Sousa, A. A.; Zhang, G. F. et al. Physicochemical characterization of ferumoxytol, heparin and protamine nanocomplexes for improvedmagnetic labeling of stem cells. Nanomed. -Nanotechnol. Biol. Med. 2017, 13, 503–513.
Du, B. J.; Liu, J. H.; Ding, G. Y.; Han, X.; Li, D.; Wang, E. K.; Wang, J. Positively charged graphene/Fe3O4/polyethylenimine with enhanced drug loading and cellular uptake for magnetic resonance imaging and magnet-responsive cancer therapy. Nano Res. 2017, 10, 2280–2295.
Candeloro, P.; Tirinato, L.; Malara, N.; Fregola, A.; Casals, E.; Puntes, V.; Perozziello, G.; Gentile, F.; Coluccio, M. L.; Das, G. et al. Nanoparticle microinjection and raman spectroscopy as tools for nanotoxicology studies. Analyst 2011, 136, 4402–4408.
Walczak, P.; Ruiz-Cabello, J.; Kedziorek, D. A.; Gilad, A. A.; Lin, S. P.; Barnett, B.; Qin, L.; Levitsky, H.; Bulte, J. W. M. Magnetoelectroporation: Improved labeling of neural stem cells and leukocytes for cellular magnetic resonance imaging using a single FDA-approved agent. Nanomed. -Nanotechnol. Biol. Med. 2006, 2, 89–94.
Yang, F.; Li, M. X.; Cui, H. T.; Wang, T. T.; Chen, Z. W.; Song, L. N.; Gu, Z. X.; Zhang, Y.; Gu, N. Altering the response of intracellular reactive oxygen to magnetic nanoparticles using ultrasound and microbubbles. Sci. China. Mater. 2015, 58, 467–480.
Lee, C. H.; Chen, C. B.; Chung, T. H.; Lin, Y. S.; Lee, W. C. Cellular uptake of protein-bound magnetic nanoparticles in pulsed magnetic field. J. Nanosci. Nanotechnol. 2010, 10, 7965–7970.
Ye, D. W; Wang, Q. W; Zhang, W. G; Sun, J. F; Gu, N. Recent progress in magnetic labeling for stem cell, Chin. Sci. Bull. 2017, 62, 2301–2311.
Cui, Y. N.; Xu, Q. X.; Chow, P. K. H.; Wang, D. P.; Wang, C. H. Transferrin-conjugated magnetic silica plga nanoparticles loaded with doxorubicin and paclitaxel for brain glioma treatment. Biomaterials 2013, 34, 8511–8520.
Song, M.; Moon, W. K.; Kim, Y.; Lim, D.; Song, I. C.; Yoon, B. W. Labeling efficacy of superparamagnetic iron oxide nanoparticles to human neural stem cells: Comparison of ferumoxides, monocrystalline iron oxide, cross-linked iron oxide (CLIO)-NH2 and tat-CLIO. Korean J. Radiol. 2007, 8, 365–371.
Wang, C. H.; Qiao, L.; Zhang, Q.; Yan, H. S.; Liu, K. L. Enhanced cell uptake of superparamagnetic iron oxide nanoparticles through direct chemisorption of FITC-tat-PEG600-b-poly(glycerol monoacrylate). Int. J. Pharm. 2012, 430, 372–380.
Andreas, K.; Georgieva, R.; Ladwig, M.; Mueller, S.; Notter, M.; Sittinger, M.; Ringe, J. Highly efficient magnetic stem cell labeling with citrate-coated superparamagnetic iron oxide nanoparticles for MRI tracking. Biomaterials 2012, 33, 4515–4525.
Frank, J. A.; Miller, B. R.; Arbab, A. S.; Zywicke, H. A.; Jordan, E. K.; Lewis, B. K.; Bryant, L. H. Jr; Bulte, J. W. M. Clinically applicable labeling of mammalian and stem cells by combining superparamagnetic iron oxides and transfection agents. Radiology 2003, 228, 480–487.
Min, K. A.; Shin, M. C.; Yu, F. Q.; Yang, M. Z.; David, A. E.; Yang, V. C.; Rosania, G. R. Pulsed magnetic field improves the transport of iron oxide nanoparticles through cell barriers. ACS Nano 2013, 7, 2161–2171.
Xie, D. H.; Qiu, B. S.; Walczak, P.; Li, X. B.; Ruiz-Cabello, J.; Minoshima, S.; Bulte, J. W. M.; Yang, X. M. Optimization of magnetosonoporation for stem cell labeling. NMR Biomed. 2010, 23, 480–484.
Guduru, R.; Liang, P.; Runowicz, C.; Nair, M.; Atluri, V.; Khizroev, S. Magneto-electric nanoparticles to enable field-controlled high-specificity drug delivery to eradicate ovarian cancer cells. Sci. Rep. 2013, 3, 2953.
Vats, N.; Wilhelm, C.; Rautou, P. E.; Poirier-Quinot, M.; Péchoux, C.; Devue, C.; Boulanger, C. M.; Gazeau, F. Magnetic tagging of cell-derived microparticles: New prospects for imaging and manipulation of these mediators of biological information. Nanomedicine 2010, 5, 727–738.
Klein, S.; Sommer, A.; Distel, L. V. R.; Neuhuber, W.; Kryschi, C. Superparamagnetic iron oxide nanoparticles as radiosensitizer via enhanced reactive oxygen species formation. Biochem. Biophys. Res. Common. 2012, 425, 393–397.
Chen, Z. W.; Yin, J. J.; Zhou, Y. T.; Zhang, Y.; Song, L.; Song, M. J.; Hu, S. L.; Gu, N. Dual enzyme-like activities of iron oxide nanoparticles and their implication for diminishing cytotoxicity. ACS Nano 2012, 6, 4001–4012.
Geng, Y.; Dalhaimer, P.; Cai, S. S.; Tsai, R.; Tewari, M.; Minko, T.; Discher, D. E. Shape effects of filaments versus spherical particles in flow and drug delivery. Nat. Nanotechnol. 2007, 2, 249–255.
Park, J. H.; von Maltzahn, G.; Zhang, L. L.; Schwartz, M. P.; Ruoslahti, E.; Bhatia, S. N.; Sailor, M. J. Magnetic iron oxide nanoworms for tumor targeting and imaging. Adv. Mater. 2008, 20, 1630–1635.
Li, X.; Bao, M. M.; Weng, Y. Y.; Yang, K.; Zhang, W. D.; Chen, G. J. Glycopolymer-coated iron oxide nanoparticles: Shape-controlled synthesis and cellular uptake. J. Mat. Chem. B 2014, 2, 5569–5575.
Ulrich, S.; Hirsch, C.; Diener, L.; Wick, P.; Rossi, R. M.; Bannwarth, M. B.; Boesel, L. F. Preparation of ellipsoid-shaped supraparticles with modular compositions and investigation of shape-dependent cell-uptake. RSC Adv. 2016, 6, 89028–89039.
Liu, Z.; Cai, W. B.; He, L. N.; Nakayama, N.; Chen, K.; Sun, X. M.; Chen, X. Y.; Dai, H. J. In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice. Nat. Nanotechnol. 2007, 2, 47–52.
Sherwood, J.; Lovas, K.; Rich, M.; Yin, Q.; Lackey, K.; Bolding, M. S.; Bao, Y. Shape-dependent cellular behaviors and relaxivity of iron oxide-based T1 MRI contrast agents. Nanoscale 2016, 8, 17506–17515.
Sun, Z. Z.; Worden, M.; Wroczynskyj, Y.; Manna, P. K.; Thliveris, J. A.; van Lierop, J.; Hegmann, T.; Miller, D. W. Differential internalization of brick shaped iron oxide nanoparticles by endothelial cells. J. Mat. Chem. B 2016, 4, 5913–5920.
Yu, S. S.; Lau, C. M.; Thomas, S. N.; Jerome, W. G.; Maron, D. J.; Dickerson, J. H.; Hubbell, J. A.; Giorgio, T. D. Size-and charge-dependent non-specific uptake of pegylated nanoparticles by macrophages. Int. J. Nanomedicine 2012, 7, 799–813.
Trekker, J.; Leten, C.; Struys, T.; Lazenka, V. V.; Argibay, B.; Micholt, L.; Lambrichts, I.; Van Roy, W.; Lagae, L.; Himmelreich, U. Sensitive in vivo cell detection using size-optimized superparamagnetic nanoparticles. Biomaterials 2014, 35, 1627–1635.
Jun, Y. W.; Huh, Y. M.; Choi, J. S.; Lee, J. H.; Song, H. T.; Kim, S.; Yoon, S.; Kim, K. S.; Shin, J. S.; Suh, J. S. et al. Nanoscale size effect of magnetic nanocrystals and their utilization for cancer diagnosis via magnetic resonance imaging. J. Am. Chem. Soc. 2005, 127, 5732–5733.
Jun, Y. W.; Lee, J. H.; Cheon, J. Chemical design of nanoparticle probes for high-performance magnetic resonance imaging. Angew. Chem., Int. Ed. 2008, 47, 5122–5135.
Tanimoto, A.; Kuribayashi, S. Application of superparamagnetic iron oxide to imaging of hepatocellular carcinoma. Eur. J. Radiol. 2006, 58, 200–216.
Huang, J.; Bu, L. H.; Xie, J.; Chen, K.; Cheng, Z.; Li, X. G.; Chen, X. Y. Effects of nanoparticle size on cellular uptake and liver MRI with polyvinylpyrrolidone-coated iron oxide nanoparticles. ACS Nano 2010, 4, 7151–7160.
He, C. B.; Hu, Y. P.; Yin, L. C.; Tang, C.; Yin, C. H. Effects of particle size and surface charge on cellular uptake and biodistribution of polymeric nanoparticles. Biomaterials 2010, 31, 3657–3666.
Mendes, R. G.; Koch, B.; Bachmatiuk, A.; El-Gendy, A. A.; Krupskaya, Y.; Springer, A.; Klingeler, R.; Schmidt, O.; Buchner, B.; Sanchez, S. et al. Synthesis and toxicity characterization of carbon coated iron oxide nanoparticles with highly defined size distributions. Biochim. Biophys. Acta-Gen. Subj. 2014, 1840, 160–169.
Shang, L.; Nienhaus, K.; Nienhaus, G. U. Engineered nanoparticles interacting with cells: Size matters. J. Nanobiotechnol. 2014, 12, 5–16.
Sun, R.; Dittrich, J.; Le-Huu, M.; Mueller, M. M.; Bedke, J.; Kartenbeck, J.; Lehmann, W. D.; Krueger, R.; Bock, M.; Huss, R. et al. Physical and biological characterization of superparamagnetic iron oxide-and ultrasmall superparamagnetic iron oxide-labeled cells -a comparison. Invest. Radiol. 2005, 40, 504–513.
Jo, J.; Aoki, I.; Tabata, Y. Design of iron oxide nanoparticles with different sizes and surface charges for simple and efficient labeling of mesenchymal stem cells. J. Control. Release 2010, 142, 465–473.
Yuan, H. Y.; Li, J.; Bao, G.; Zhang, S. L. Variable nanoparticle-cell adhesion strength regulates cellular uptake. Phys. Rev. Lett. 2010, 105, 138101–138105.
Zhang, S. L.; Gao, H. J.; Bao, G. Physical principles of nanoparticle cellular endocytosis. ACS Nano 2015, 9, 8655–8671.
Deserno, M.; Bickel, T. Wrapping of a spherical colloid by a fluid membrane. Europhys. Lett. 2003, 62, 767–774.
Lin, X. B.; Li, Y.; Gu, N. Nanoparticle's size effect on its translocation across a lipid bilayer: A molecular dynamics simulation. J. Comput. Theor. Nanosci. 2010, 7, 269–276.
Gal, N.; Lassenberger, A.; Herrero-Nogareda, L.; Scheberl, A.; Charwat, V.; Kasper, C.; Reimhult, E. Interaction of size-tailored pegylated iron oxide nanoparticles with lipid membranes and cells. ACS Biomater. Sci. Eng. 2017, 3, 249–259.
Hu, Z. Y.; Zhang, H. Y.; Zhang, Y.; Wu, R. A.; Zou, H. F. Nanoparticle size matters in the formation of plasma protein coronas on Fe3O4 nanoparticles. Colloid Surf. B-Biointerfaces 2014, 121, 354–361.
Mahmoudi, M.; Sheibani, S.; Milani, A. S.; Rezaee, F.; Gauberti, M.; Dinarvand, R.; Vali, H. Crucial role of the protein corona for the specific targeting of nanoparticles. Nanomedicine 2015, 10, 215–226.
Punnakitikashem, P.; Chang, S. H.; Huang, C. W.; Liu, J. P.; Hao, Y. W. Design and fabrication of non-superparamagnetic high moment magnetic nanoparticles for bioapplications. J. Nanopart. Res. 2010, 12, 1101–1106.
Assa, F.; Jafarizadeh-Malmiri, H.; Ajamein, H.; Anarjan, N.; Vaghari, H.; Sayyar, Z.; Berenjian, A. A biotechnological perspective on the application of iron oxide nanoparticles. Nano Res. 2016, 9, 2203–2225.
Hamley, I. W. Nanotechnology with soft materials. Angew. Chem., Int. Ed. 2003, 42, 1692–1712.
Fayol, D.; Luciani, N.; Lartigue, L.; Gazeau, F.; Wilhelm, C. Managing magnetic nanoparticle aggregation and cellular uptake: A precondition for efficient stem-cell differentiation and mri tracking. Adv. Healthc. Mater. 2013, 2, 313–325.
Safi, M.; Sarrouj, H.; Sandre, O.; Mignet, N.; Berret, J. F. Interactions between sub-10-nm iron and cerium oxide nanoparticles and 3T3 fibroblasts: The role of the coating and aggregation state. Nanotechnology 2010, 21, 145103–145113.
Bae, J. E.; Huh, M. I.; Ryu, B. K.; Do, J. Y.; Jin, S. U.; Moon, M. J.; Jung, J. C.; Chang, Y.; Kim, E.; Chi, S. G. et al. The effect of static magnetic fields on the aggregation and cytotoxicity of magnetic nanoparticles. Biomaterials 2011, 32, 9401–9414.
Herve, K.; Douziech-Eyrolles, L.; Munnier, E.; Cohen-Jonathan, S.; Soucé, M.; Marchais, H.; Limelette, P.; Warmont, F.; Saboungi, M. L.; Dubois, P. et al. The development of stable aqueous suspensions of pegylated spions for biomedical applications. Nanotechnology 2008, 19, 465608–465615.
Gillich, T.; Acikgoz, C.; Isa, L.; Schluter, A. D.; Spencer, N. D.; Textor, M. Peg-stabilized core-shell nanoparticles: Impact of linear versus dendritic polymer shell architecture on colloidal properties and the reversibility of temperature-induced aggregation. ACS Nano 2013, 7, 316–329.
Mornet, S.; Portier, J.; Duguet, E. A method for synthesis and functionalization of ultrasmall superparamagnetic covalent carriers based on maghemite and dextran. J. Magn. Magn. Mater. 2005, 293, 127–134.
Duan, H. W.; Kuang, M.; Wang, X. X.; Wang, Y. A.; Mao, H.; Nie, S. M. Reexamining the effects of particle size and surface chemistry on the magnetic properties of iron oxide nanocrystals: New insights into spin disorder and proton relaxivity. J. Phys. Chem. C 2008, 112, 8127–8131.
Zhao, X. Q.; Shang, T.; Zhang, X. D.; Ye, T.; Wang, D. J.; Rei, L. Passage of magnetic tat-conjugated Fe3O4@SiO2 nanoparticles across in vitro blood-brain barrier. Nanoscale Res. Lett. 2016, 11, 451–463.
Zhang, J.; Chen, Y. C.; Li, X.; Liang, X. L.; Luo, X. J. The influence of different long-circulating materials on the pharmacokinetics of liposomal vincristine sulfate. Int. J. Nanomed. 2016, 11, 4187–4197.
Mosqueira, V. C. F.; Legrand, P.; Morgat, J. L.; Vert, M.; Mysiakine, E.; Gref, R.; Devissaguet, J. P.; Barratt, G. Biodistribution of long-circulating PEG-grafted nanocapsules in mice: Effects of peg chain length and density. Pharm. Res. 2001, 18, 1411–1419.
Mohamed, S. A.; Al-Harbi, M. H.; Almulaiky, Y. Q.; Ibrahim, I. H.; El-Shishtawy, R. M. Immobilization of horseradish peroxidase on Fe3O4 magnetic nanoparticles. Electron. J. Biotechnol. 2017, 27, 84–90.
Ahn, J.; Moon, D. S.; Lee, J. K. Arsonic acid as a robust anchor group for the surface modification of Fe3O4. Langmuir 2013, 29, 14912–14918.
Park, J.; Kadasala, N. R.; Abouelmagd, S. A.; Castanares, M. A.; Collins, D. S.; Wei, A.; Yeo, Y. Polymer-iron oxide composite nanoparticles for epr-independent drug delivery. Biomaterials 2016, 101, 285–295.
Dowaidar, M.; Abdelhamid, H. N.; Hällbrink, M.; Freimann, K.; Kurrikoff, K.; Zou, X. D.; Langel, Ü. Magnetic nanoparticle assisted self-assembly of cell penetrating peptides-oligonu-cleotides complexes for gene delivery. Sci. Rep. 2017, 7, 9159–9170.
Gao, L. P.; Yu, J.; Liu, Y.; Zhou, J. E.; Sun, L.; Wang, J.; Zhu, J. Z.; Peng, H.; Lu, W. Y.; Yu, L. et al. Tumor-penetrating peptide conjugated and doxorubicin loaded T1-T2 dual mode mri contrast agents nanoparticles for tumor theranostics. Theranostics 2018, 8, 92–108.
Li, X. M.; Ding, L. Y.; Xu, Y. L.; Wang, Y. L.; Ping, Q. N. Targeted delivery of doxorubicin using stealth liposomes modified with transferrin. Int. J. Pharm. 2009, 373, 116–123.
Stähl, S.; Gräslund, T.; Karlström, A. E.; Frejd, F. Y.; Nygren, P.Ä.; Löfblom, J. Affibody molecules in biotechnological and medical applications. Trends Biotechnol. 2017, 35, 691–712.
Chai, Z. L.; Hu, X. F.; Wei, X. L.; Zhan, C. Y.; Lu, L. W.; Jiang, K.; Su, B. X.; Ruan, H. T.; Ran, D. N.; Fang, R. H. et al. A facile approach to functionalizing cell membrane-coated nanoparticles with neurotoxin-derived peptide for brain-targeted drug delivery. J. Control. Release 2017, 264, 102–111.
Osaka, T.; Nakanishi, T.; Shanmugam, S.; Takahama, S.; Zhang, H. Effect of surface charge of magnetite nanoparticles on their internalization into breast cancer and umbilical vein endothelial cells. Colloid Surf. B-Biointerfaces 2009, 71, 325–330.
Wang, X. Q.; Zhang, H. R.; Jing, H. J.; Cui, L. Q. Highly efficient labeling of human lung cancer cells using cationic poly-L-lysine-assisted magnetic iron oxide nanoparticles. Nano-Micro Lett. 2015, 7, 374–384.
Bull, E.; Madani, S. Y.; Sheth, R.; Seifalian, A.; Green, M.; Seifalian, A. M. Stem cell tracking using iron oxide nanoparticles. Int. J. Nanomed. 2014, 9, 1641–1653.
Santhosh, P. B.; Velikonja, A.; Perutkova, Š.; Gongadze, E.; Kulkarni, M.; Genova, J.; Eleršič, K.; Iglič, A.; Kralj-Iglič, V.; Ulrih, N. P. Influence of nanoparticle-membrane electrostatic interactions on membrane fluidity and bending elasticity. Chem. Phys. Lipids 2014, 178, 52–62.
Lin, J. Q.; Zhang, H. W.; Chen, Z.; Zheng, Y. G. Penetration of lipid membranes by gold nanoparticles: Insights into cellular uptake, cytotoxicity, and their relationship. ACS Nano 2010, 4, 5421–5429.
Nangia, S.; Sureshkumar, R. Effects of nanoparticle charge and shape anisotropy on translocation through cell membranes. Langmuir 2012, 28, 17666–17671.
Li, S.; Malmstadt, N. Deformation and poration of lipid bilayer membranes by cationic nanoparticles. Soft Matter 2013, 9, 4969–4976.
Deen, W. M.; Bohrer, M. P.; Epstein, N. B. Effects of molecular size and configuration on diffusion in microporous membranes. AIChE J. 1981, 27, 952–959.
Hong, S. P.; Leroueil, P. R.; Janus, E. K.; Peters, J. L.; Kober, M. M.; Islam, M. T.; Orr, B. G.; Baker, J. R.; Holl, M. M. B. Interaction of polycationic polymers with supported lipid bilayers and cells: Nanoscale hole formation and enhanced membrane permeability. Bioconjugate Chem. 2006, 17, 728–734.
Wang, T. T.; Bai, J.; Jiang, X.; Nienhaus, G. U. Cellular uptake of nanoparticles by membrane penetration: A study combining confocal microscopy with ftir spectroelectrochemistry. ACS Nano 2012, 6, 1251–1259.
Han, X.; Deng, Z. C.; Yang, Z.; Wang, Y. L.; Zhu, H. H.; Chen, B. D.; Cui, Z.; Ewing, R. C.; Shi, D. L. Biomarkerless targeting and photothermal cancer cell killing by surface-electrically-charged superparamagnetic Fe3O4 composite nanoparticles. Nanoscale 2017, 9, 1457–1465.
Pu, L.; Xu, J. B.; Sun, Y. M.; Fang, Z.; Chan-Park, M. B.; Duan, H. W. Cationic polycarbonate-grafted superparamagnetic nanoparticles with synergistic dual-modality antimicrobial activity. Biomater. Sci. 2016, 4, 871–879.
Sakulkhu, U.; Mahmoudi, M.; Maurizi, L.; Coullerez, G.; Hofmann-Amtenbrink, M.; Vries, M.; Motazacker, M.; Rezaee, F.; Hofmann, H. Significance of surface charge and shell material of superparamagnetic iron oxide nanoparticle (SPION) based core/shell nanoparticles on the composition of the protein corona. Biomater. Sci. 2015, 3, 265–278.
Fleischer, C. C.; Payne, C. K. Nanoparticle-cell interactions: Molecular structure of the protein corona and cellular outcomes. Acc. Chem. Res. 2014, 47, 2651–2659.
Carter, D. C.; Ho, J. X. Structure of serum-albumin. Adv. Protein Chem. 1994, 45, 153–203.
Mu, Q. X.; Li, Z. W.; Li, X.; Mishra, S. R.; Zhang, B.; Si, Z. K.; Yang, L.; Jiang, W.; Yan, B. Characterization of protein clusters of diverse magnetic nanoparticles and their dynamic interactions with human cells. J. Phys. Chem. C 2009, 113, 5390–5395.
Serda, R. E.; Blanco, E.; Mack, A.; Stafford, S. J.; Amra, S.; Li, Q. P.; van de Ven, A.; Tanaka, T.; Torchilin, V. P.; Wiktorowicz, J. E. et al. Proteomic analysis of serum opsonins impacting biodistribution and cellular association of porous silicon microparticles. Mol. Imaging 2011, 10, 43–55.
McConnell, K. I.; Shamsudeen, S.; Meraz, I. M.; Mahadevan, T. S.; Ziemys, A.; Rees, P.; Summers, H. D.; Serda, R. E. Reduced cationic nanoparticle cytotoxicity based on serum masking of surface potential. J. Biomed. Nanotechnol. 2016, 12, 154–164.
Babič, M.; Horák, D.; Trchová, M.; Jendelová, P.; Glogarová, K.; Lesny, P.; Herynek, V.; Hájek, M.; Syková, E. Poly(L-lysine)-modified iron oxide nanoparticles for stem cell labeling. Bioconjugate Chem. 2008, 19, 740–750.
Kokkinopoulou, M.; Simon, J.; Landfester, K.; Mailänder, V.; Lieberwirth, I. Visualization of the protein corona: Towards a biomolecular understanding of nanoparticle-cell-interactions. Nanoscale 2017, 9, 8858–8870.
Gref, R.; Lück, M.; Quellec, P.; Marchand, M.; Dellacherie, E.; Harnisch, S.; Blunk, T.; Müller, R. H. 'Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): Influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloid Surf. B-Biointerfaces 2000, 18, 301–313.
Ritz, S.; Schöttler, S.; Kotman, N.; Baier, G.; Musyanovych, A.; Kuharev, J.; Landfester, K.; Schild, H.; Jahn, O.; Tenzer, S. et al. Protein corona of nanoparticles: Distinct proteins regulate the cellular uptake. Biomacromolecules 2015, 16, 1311–1321.
Rogers, W. J.; Basu, P. Factors regulating macrophage endocytosis of nanoparticles: Implications for targeted magnetic resonance plaque imaging. Atherosclerosis 2005, 178, 67–73.
Ayala, V.; Herrera, A. P.; Latorre-Esteves, M.; Torres-Lugo, M.; Rinaldi, C. Effect of surface charge on the colloidal stability and in vitro uptake of carboxymethyl dextran-coated iron oxide nanoparticles. J. Nanopart. Res. 2013, 15, 2180–2186.
Ge, Y. Q.; Zhang, Y.; Xia, J. G.; Ma, M.; He, S. Y.; Nie, F.; Gu, N. Effect of surface charge and agglomerate degree of magnetic iron oxide nanoparticles on kb cellular uptake in vitro. Colloid Surf. B-Biointerfaces 2009, 73, 294–301.
Jahn, M. R.; Nawroth, T.; Fütterer, S.; Wolfrum, U.; Kolb, U.; Langguth, P. Iron oxide/hydroxide nanoparticles with negatively charged shells show increased uptake in CaCO-2 cells. Mol. Pharmaceutics 2012, 9, 1628–1637.
Xu, Y. L.; Sherwood, J. A.; Lackey, K. H.; Qin, Y.; Bao, Y. P. The responses of immune cells to iron oxide nanoparticles. J. Appl. Toxicol. 2016, 36, 543–553.
Srivastava, I.; Misra, S. K.; Ostadhossein, F.; Daza, E.; Singh, J.; Pan, D. Surface chemistry of carbon nanoparticles functionally select their uptake in various stages of cancer cells. Nano Res. 2017, 10, 3269–3284.
Yang, Y.; Wang, Q. Q.; Song, L. N.; Liu, X.; Zhao, P.; Zhang, F. M.; Gu, N.; Sun, J. F. Uptake of magnetic nanoparticles for adipose-derived stem cells with multiple passage numbers. Sci. China. Mater. 2017, 60, 892–902.
Wahajuddin; Arora, S. Superparamagnetic iron oxide nanoparticles: Magnetic nanoplatforms as drug carriers. Int. J. Nanomedicine 2012, 7, 3445–3471.
Lu, Y. C.; Chang, F. Y.; Tu, S. J.; Chen, J. P.; Ma, Y. H. Cellular uptake of magnetite nanoparticles enhanced by NdFeB magnets in staggered arrangement. J. Magn. Magn. Mater. 2017, 427, 71–80.
Widder, K. J.; Senyei, A. E.; Scarpelli, D. G. Magnetic microspheres–A model system for site specific drug delivery in vivo. Exp. Biol. Med. 1978, 158, 141–146.
Lamkowsky, M. C.; Geppert, M.; Schmidt, M. M.; Dringen, R. Magnetic field-induced acceleration of the accumulation of magnetic iron oxide nanoparticles by cultured brain astrocytes. J. Biomed. Mater. Res. Part A 2012, 100A, 323–334.
MacDonald, C.; Barbee, K.; Polyak, B. Force dependent internalization of magnetic nanoparticles results in highly loaded endothelial cells for use as potential therapy delivery vectors. Pharm. Res. 2012, 29, 1270–1281.
Barnes, A. L.; Wassel, R. A.; Mondalek, F.; Chen, K. J.; Dormer, K. J.; Kopke, R. D. Magnetic characterization of superparamagnetic nanoparticles pulled through model membranes. BioMagnetic Res. Technol. 2007, 5, 1.
Chaudhary, S.; Smith, C. A.; del Pino, P.; de la Fuente, J. M.; Mullin, M.; Hursthouse, A.; Stirling, D.; Berry, C. C. Elucidating the function of penetratin and a static magnetic field in cellular uptake of magnetic nanoparticles. Pharma-ceuticals 2013, 6, 204–222.
Towhidi, L.; Firoozabadi, S. M. P.; Mozdarani, H.; Miklavcic, D. Lucifer yellow uptake by CHO cells exposed to magnetic and electric pulses. Radiol. Oncol. 2012, 46, 119–125.
Chen, C. B.; Chen, J. Y.; Lee, W. C. Fast transfection of mammalian cells using superparamagnetic nanoparticles under strong magnetic field. J. Nanosci. Nanotechnol. 2009, 9, 2651–2659.
Antov, Y.; Barbul, A.; Mantsur, H.; Korenstein, R. Electroendocytosis: Exposure of cells to pulsed low electric fields enhances adsorption and uptake of macromolecules. Biophys. J. 2005, 88, 2206–2223.
Mahrour, N.; Pologea-Moraru, R.; Moisescu, M. G.; Orlowski, S.; Levêque, P.; Mir, L. M. In vitro increase of the fluid-phase endocytosis induced by pulsed radiofrequency electromagnetic fields: Importance of the electric field component. Biochim. Biophys. Acta-Biomembr. 2005, 1668, 126–137.
Novickij, V.; Grainys, A.; Novickij, J.; Markovskaja, S. Irreversible magnetoporation of micro-organisms in high pulsed magnetic fields. IET Nanobiotechnol. 2014, 8, 157–162.
Novickij, V.; Grainys, A.; Švediene, J.; Markovskaja, S.; Paškevičius, A.; Novickij, J. Microsecond pulsed magnetic field improves efficacy of antifungal agents on pathogenic microorganisms. Bioelectromagnetics 2014, 35, 347–353.
Zhang, Z. H.; Lin, X. B.; Gu, N. Effects of temperature and peg grafting density on the translocation of pegylated nanoparticles across asymmetric lipid membrane. Colloid Surf. B-Biointerfaces 2017, 160, 92–100.
Mailänder, V.; Lorenz, M. R.; Holzapfel, V.; Musyanovych, A.; Fuchs, K.; Wiesneth, M.; Walther, P.; Landfester, K.; Schrezenmeier, H. Carboxylated superparamagnetic iron oxide particles label cells intracellularly without transfection agents. Mol. Imaging Biol. 2008, 10, 138–146.
Gal, N.; Massalha, S.; Samuelly-Nafta, O.; Weihs, D. Effects of particle uptake, encapsulation, and localization in cancer cells on intracellular applications. Med. Eng. Phys. 2015, 37, 478–483.
Perevedentseva, E.; Hong, S. F.; Huang, K. J.; Chiang, I. T.; Lee, C. Y.; Tseng, Y. T.; Cheng, C. L. Nanodiamond internalization in cells and the cell uptake mechanism. J. Nanopart. Res. 2013, 15, 1834–1846.
Srinivasan, A. R.; Lakshmikuttyamma, A.; Shoyele, S. A. Investigation of the stability and cellular uptake of self-associated monoclonal antibody (MAb) nanoparticles by non-small lung cancer cells. Mol. Pharmaceutics 2013, 10, 3275–3284.
Rappoport, J. Z.; Simon, S. M. Endocytic trafficking of activated egfr is AP-2 dependent and occurs through preformed clathrin spots. J. Cell Sci. 2009, 122, 1301–1305.
Kawauchi, T. Cell adhesion and its endocytic regulation in cell migration during neural development and cancer metastasis. Int. J. Mol. Sci. 2012, 13, 4564–4590.
Bitsikas, V.; Corrêa, I. R. Jr.; Nichols, B. J. Clathrin-indepen-dent pathways do not contribute significantly to endocytic flux. eLife 2014, 3, e03970–e03996.
Yalçin, S.; Özluer, Ö.; Gündüz, U. Nanoparticle-based drug delivery in cancer: The role of cell membrane structures. Ther. Deliv. 2016, 7, 773–781.
Sahay, G.; Kim, J. O.; Kabanov, A. V.; Bronich, T. K. The exploitation of differential endocytic pathways in normal and tumor cells in the selective targeting of nanoparticulate chemotherapeutic agents. Biomaterials 2010, 31, 923–933.
Sigismund, S.; Confalonieri, S.; Ciliberto, A.; Polo, S.; Scita, G.; Di Fiore, P. P. Endocytosis and signaling: Cell logistics shape the eukaryotic cell plan. Physiol. Rev. 2012, 92, 273–366.
Zink, D.; Fischer, A. H.; Nickerson, J. A. Nuclear structure in cancer cells. Nat. Rev. Cancer 2004, 4, 677–687.
Lekka, M.; Pogoda, K.; Gostek, J.; Klymenko, O.; Prauzner-Bechcicki, S.; Wiltowska-Zuber, J.; Jaczewska, J.; Lekki, J.; Stachura, Z. Cancer cell recognition–Mechanical phenotype. Micron 2012, 43, 1259–1266.
Alibert, C.; Goud, B.; Manneville, J. B. Are cancer cells really softer than normal cells? Biol. Cell 2017, 109, 167–189.
Grady, M. E.; Composto, R. J.; Eckmann, D. M. Cell elasticity with altered cytoskeletal architectures across multiple cell types. J. Mech. Behav. Biomed. 2016, 61, 197–207.
Yilmaz, M.; Christofori, G. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 2009, 28, 15–33.
Elkhatib, N.; Bresteau, E.; Baschieri, F.; Rioja, A. L.; van Niel, G.; Vassilopoulos, S.; Montagnac, G. Tubular clathrin/AP-2 lattices pinch collagen fibers to support 3D cell migration. Science 2017, 356, 1138–1148.
Subra, C.; Grand, D.; Laulagnier, K.; Stella, A.; Lambeau, G.; Paillasse, M.; De Medina, P.; Monsarrat, B.; Perret, B.; Silvente-Poirot, S. et al. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J. Lipid Res. 2010, 51, 2105–2120.
Vlassov, A. V.; Magdaleno, S.; Setterquist, R.; Conrad, R. Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim. Biophys. Acta-Gen. Subj. 2012, 1820, 940–948.
Kourembanas, S. Exosomes: Vehicles of intercellular signaling, biomarkers, and vectors of cell therapy. Annu. Rev. Physiol. 2015, 77, 13–27.
Naqvi, S.; Samim, M.; Abdin, M.; Ahmed, F. J.; Maitra, A.; Prashant, C.; Dinda, A. K. Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress. Int. J. Nanomedinice 2010, 5, 983–989.
Hu, L. Z.; Wickline, S. A.; Hood, J. L. Magnetic resonance imaging of melanoma exosomes in lymph nodes. Magn. Reson. Med. 2015, 74, 266–271.
Gould, S. J.; Raposo, G. As we wait: Coping with an imperfect nomenclature for extracellular vesicles. J. Extracell. Vesicles 2013, 2. 20389–20391.
Jovic, M.; Sharma, M.; Rahajeng, J.; Caplan, S. The early endosome: A busy sorting station for proteins at the crossroads. Histol. Histopathol. 2010, 25, 99–112.
Busato, A.; Bonafede, R.; Bontempi, P.; Scambi, I.; Schiaffino, L.; Benati, D.; Malatesta, M.; Sbarbati, A.; Marzola, P.; Mariotti, R. Magnetic resonance imaging of ultrasmall superparamagnetic iron oxide-labeled exosomes from stem cells: A new method to obtain labeled exosomes. Int. J. Nanomedicine 2016, 11, 2481–2490.
Busato, A.; Bonafede, R.; Bontempi, P.; Scambi, I.; Schiaffino, L.; Benati, D.; Malatesta, M.; Sbarbati, A.; Marzola, P.; Mariotti, R. Labeling and magnetic resonance imaging of exosomes isolated from adipose stem cells. Curr. Protoc. Cell Biol. 2017, 75, 1–15.
Zhao, J. Y.; Chen, G.; Gu, Y. P.; Cui, R.; Zhang, Z. L.; Yu, Z. L.; Tang, B.; Zhao, Y. F.; Pang, D. W. Ultrasmall magnetically engineered Ag2Se quantum dots for instant efficient labeling and whole-body high-resolution multimodal real-time tracking of cell-derived microvesicles. J. Am. Chem. Soc. 2016, 138, 1893–1903.
Grange, C.; Tapparo, M.; Bruno, S.; Chatterjee, D.; Quesenberry, P. J.; Tetta, C.; Camussi, G. Biodistribution of mesenchymal stem cell-derived extracellular vesicles in a model of acute kidney injury monitored by optical imaging. Int. J. Mol. Med. 2014, 33, 1055–1063.
Zhu, L.; Dong, D.; Yu, Z. L.; Zhao, Y. F.; Pang, D. W.; Zhang, Z. L. Folate-engineered microvesicles for enhanced target and synergistic therapy toward breast cancer. ACS Appl. Mater. Interfaces 2017, 9, 5100–5108.
Ridder, K.; Keller, S.; Dams, M.; Rupp, A. K.; Schlaudraff, J.; Del Turco, D.; Starmann, J.; Macas, J.; Karpova, D.; Devraj, K. et al. Extracellular vesicle-mediated transfer of genetic information between the hematopoietic system and the brain in response to inflammation. PLoS Biol. 2014, 12, e1001874–e1001889.
Feng, D.; Zhao, W. L.; Ye, Y. Y.; Bai, X. C.; Liu, R. Q.; Chang, L. F.; Zhou, Q.; Sui, S. F. Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010, 11, 675–687.
Nanbo, A.; Kawanishi, E.; Yoshida, R.; Yoshiyama, H. Exosomes derived from epstein-barr virus-infected cells are internalized via caveola-dependent endocytosis and promote phenotypic modulation in target cells. J. Virol. 2013, 87, 10334–10347.
Christianson, H. C.; Svensson, K. J.; van Kuppevelt, T. H.; Li, J. P.; Belting, M. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc. Natl. Acad. Sci. USA 2013, 110, 17380–17385.
Macario, A. J. L.; Cappello, F.; Zummo, G.; de Macario, E. C. Chaperonopathies of senescence and the scrambling of interactions between the chaperoning and the immune systems. Ann. NY Acad. Sci. 2010, 1197, 85–93.
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Acknowledgements
This work was supported by the National Basic Research Program of China (Nos. 2013CB733804 and 2013CB934400), the National Key Research and Development Program of China (No. 2017YFA0104301), the National Natural Science Foundation of China for Key Project of Inter-national Cooperation (No. 61420106012), and the Collaborative Innovation Center of Suzhou Nano Science and Technology (No. SX21400213).
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