Overcoming the stability, toxicity, and biodegradation challenges of tumor stimuli-responsive inorganic nanoparticles for delivery of cancer therapeutics

References

• Dawidczyk CM, Kim C, Park JH, et al. State-of-the-art in design rules for drug delivery platforms: lessons learned from FDA-approved nanomedicines. J Control Release. 2014;187:133–144.
   PubMed Web of Science ®Google Scholar
• Maeda H, Nakamura H, Fang J. The EPR effect for macromolecular drug delivery to solid tumors: improvement of tumor uptake, lowering of systemic toxicity, and distinct tumor imaging in vivo. Adv Drug Deliv Rev. 2013;65:71–79.
   PubMed Web of Science ®Google Scholar
• Mura S, Nicolas J, Couvreur P. Stimuli-responsive nanocarriers for drug delivery. Nat Mater. 2013;12:991–1003.
   PubMed Web of Science ®Google Scholar
• Lyon PC, Gray MD, Mannaris C, et al. Safety and feasibility of ultrasound-triggered targeted drug delivery of doxorubicin from thermosensitive liposomes in liver tumours (TARDOX): a single-centre, open-label, phase 1 trial. Lancet Oncol. 2018;19:1027–1039.
   PubMed Web of Science ®Google Scholar
• Ganta S, Devalapally H, Shahiwala A, et al. A review of stimuli-responsive nanocarriers for drug and gene delivery. J Control Release. 2008;126:187–204.
   PubMed Web of Science ®Google Scholar
• Paris JL, Mannaris C, Cabañas MV, et al. Ultrasound-mediated cavitation-enhanced extravasation of mesoporous silica nanoparticles for controlled-release drug delivery. Chem Eng J. 2018;340:2–8.
   Web of Science ®Google Scholar
• Paris JL, Manzano M, Cabañas MV, et al. Mesoporous silica nanoparticles engineered for ultrasound-induced uptake by cancer cells. Nanoscale. 2018;10:6402–6408.
   PubMed Web of Science ®Google Scholar
• Wang S, Huang P, Chen X. Hierarchical targeting strategy for enhanced tumor tissue accumulation/retention and cellular internalization. Adv Mater. 2016;28:7340–7364.
   PubMed Web of Science ®Google Scholar
• Kwan JJ, Graham S, Myers R, et al. Ultrasound-induced inertial cavitation from gas-stabilizing nanoparticles. Phys Rev E. 2015;92:023019.
   Web of Science ®Google Scholar
• Mahmoudi M, Sant S, Wang B, et al. Superparamagnetic iron oxide nanoparticles (SPIONs): development, surface modification and applications in chemotherapy. Adv Drug Deliv Rev. 2011;63:24–46.
   PubMed Web of Science ®Google Scholar
• Liu J, Detrembleur C, De Pauw-Gillet M-C, et al. Gold nanorods coated with mesoporous silica shell as drug delivery system for remote near infrared light-activated release and potential phototherapy. Small. 2015;11:2323–2332.
   PubMed Web of Science ®Google Scholar
• Yang K, Feng L, Liu Z. Stimuli responsive drug delivery systems based on nano-graphene for cancer therapy. Adv Drug Deliv Rev. 2016;105:228–241.
   PubMed Web of Science ®Google Scholar
• Argyo C, Weiss V, Bräuchle C, et al. Multifunctional mesoporous silica nanoparticles as a universal platform for drug delivery. Chem Mater. 2014;26:435–451.
   Web of Science ®Google Scholar
• Butler KS, Durfee PN, Theron C, et al. Protocells: modular mesoporous silica nanoparticle-supported lipid bilayers for drug delivery. Small. 2016;12:2173–2185.
   PubMed Web of Science ®Google Scholar
• Fadeel B, Garcia-Bennett AE. Better safe than sorry: understanding the toxicological properties of inorganic nanoparticles manufactured for biomedical applications. Adv Drug Deliv Rev. 2010;62:362–374.
   PubMed Web of Science ®Google Scholar
• Mukherjee S, Patra CR. Therapeutic application of anti-angiogenic nanomaterials in cancers. Nanoscale. 2016;8:12444–12470.
   PubMed Web of Science ®Google Scholar
• Pankhurst QA, Connolly J, Jones SK, et al. Applications of magnetic nanoparticles in biomedicine. J Phys D Appl Phys. 2003;36:R167–R181.
   Web of Science ®Google Scholar
• Hu Y, Mignani S, Majoral J-P, et al. Construction of iron oxide nanoparticle-based hybrid platforms for tumor imaging and therapy. Chem Soc Rev. 2018;47:1874–1900.
   PubMed Web of Science ®Google Scholar
• Kunzmann A, Andersson B, Vogt C, et al. Efficient internalization of silica-coated iron oxide nanoparticles of different sizes by primary human macrophages and dendritic cells. Toxicol Appl Pharmacol. 2011;253:81–93.
   PubMed Web of Science ®Google Scholar
• Ankamwar B, Lai TC, Huang JH, et al. Biocompatibility of Fe 3 O 4 nanoparticles evaluated by in vitro cytotoxicity assays using normal, glia and breast cancer cells. Nanotechnology. 2010;21:075102.
   PubMed Web of Science ®Google Scholar
• Shubayev VI, Pisanic TR, Jin S. Magnetic nanoparticles for theragnostics. Adv Drug Deliv Rev. 2009;61:467–477.
   PubMed Web of Science ®Google Scholar
• Eaton JW, Qian M. Molecular bases of cellular iron toxicity. Free Radic Biol Med. 2002;32:833–840.
   PubMed Web of Science ®Google Scholar
• Huang -C-C, Liao Z-X, Lu H-M, et al. Cellular organelle-dependent cytotoxicity of iron oxide nanoparticles and its implications for cancer diagnosis and treatment: A mechanistic investigation. Chem Mater. 2016;28:9017–9025.
   Web of Science ®Google Scholar
• Singh N, Jenkins GJS, Asadi R, et al. Potential toxicity of superparamagnetic iron oxide nanoparticles (SPION). Nano Rev. 2010;1:5358.
   PubMedGoogle Scholar
• Mahmoudi M, Laurent S, Shokrgozar MA, et al. Toxicity evaluations of superparamagnetic iron oxide nanoparticles: cell “Vision” versus physicochemical properties of nanoparticles. ACS Nano. 2011;5:7263–7276.
   PubMed Web of Science ®Google Scholar
• Müller K, Skepper JN, Posfai M, et al. Effect of ultrasmall superparamagnetic iron oxide nanoparticles (Ferumoxtran-10) on human monocyte-macrophages in vitro. Biomaterials. 2007;28:1629–1642.
   PubMed Web of Science ®Google Scholar
• Malvindi MA, De Matteis V, Galeone A, et al. Toxicity assessment of silica coated iron oxide nanoparticles and biocompatibility improvement by surface engineering. Xu B, editor. PLoS One. 2014;9:e85835.
   PubMed Web of Science ®Google Scholar
• Iqbal MZ, Ma X, Chen T, et al. Silica-coated super-paramagnetic iron oxide nanoparticles (SPIONPs): a new type contrast agent of T 1 magnetic resonance imaging (MRI). J Mater Chem B. 2015;3:5172–5181.
   PubMed Web of Science ®Google Scholar
• Hanot C, Choi Y, Anani T, et al. Effects of iron-oxide nanoparticle surface chemistry on uptake kinetics and cytotoxicity in CHO-K1 cells. Int J Mol Sci. 2015;17:54.
   Web of Science ®Google Scholar
• Patel D, Moon JY, Chang Y, et al. Poly(d,l-lactide-co-glycolide) coated superparamagnetic iron oxide nanoparticles: synthesis, characterization and in vivo study as MRI contrast agent. Colloids Surf A Physicochem Eng Aspects. 2008;313–314:91–94.
   Web of Science ®Google Scholar
• Carenza E, Jordan O, Martínez-San Segundo P, et al. Encapsulation of VEGF 165 into magnetic PLGA nanocapsules for potential local delivery and bioactivity in human brain endothelial cells. J Mater Chem B. 2015;3:2538–2544.
   PubMed Web of Science ®Google Scholar
• Saengruengrit C, Ritprajak P, Wanichwecharungruang S, et al. The combined magnetic field and iron oxide-PLGA composite particles: effective protein antigen delivery and immune stimulation in dendritic cells. J Colloid Interface Sci. 2018;520:101–111.
   PubMed Web of Science ®Google Scholar
• Zhang X, Zhang H, Liang X, et al. Iron oxide nanoparticles induce autophagosome accumulation through multiple mechanisms: lysosome impairment, mitochondrial damage, and ER stress. Mol Pharm. 2016;13:2578–2587.
   PubMed Web of Science ®Google Scholar
• Nosrati H, Sefidi N, Sharafi A, et al. Bovine Serum Albumin (BSA) coated iron oxide magnetic nanoparticles as biocompatible carriers for curcumin-anticancer drug. Bioorg Chem. 2018;76:501–509.
   PubMed Web of Science ®Google Scholar
• Jedlovszky-Hajdú A, Bombelli FB, Monopoli MP, et al. Surface coatings shape the protein corona of spions with relevance to their application in vivo. Langmuir. 2012;28:14983–14991.
   PubMed Web of Science ®Google Scholar
• Mahmoudi M, Shokrgozar MA, Behzadi S. Slight temperature changes affect protein affinity and cellular uptake/toxicity of nanoparticles. Nanoscale. 2013;5:3240.
   PubMed Web of Science ®Google Scholar
• Bao Y, Wen T, Samia ACS, et al. Magnetic nanoparticles: material engineering and emerging applications in lithography and biomedicine. J Mater Sci. 2016;51:513–553.
   PubMed Web of Science ®Google Scholar
• Patil U, Adireddy S, Jaiswal A, et al. In vitro/in vivo toxicity evaluation and quantification of iron oxide nanoparticles. Int J Mol Sci. 2015;16:24417–24450.
   PubMed Web of Science ®Google Scholar
• Yang L, Kuang H, Zhang W, et al. Size dependent biodistribution and toxicokinetics of iron oxide magnetic nanoparticles in mice. Nanoscale. 2015;7:625–636.
   PubMed Web of Science ®Google Scholar
• Feng Q, Liu Y, Huang J, et al. Uptake, distribution, clearance, and toxicity of iron oxide nanoparticles with different sizes and coatings. Sci Rep. 2018;8:2082.
   PubMed Web of Science ®Google Scholar
• Yu Q, Xiong X, Zhao L, et al. Biodistribution and toxicity assessment of superparamagnetic iron oxide nanoparticles in vitro and in vivo. Curr Med Sci. 2018;38:1096–1102.
   PubMed Web of Science ®Google Scholar
• Mardhian DF, Storm G, Bansal R, et al. Nano-targeted relaxin impairs fibrosis and tumor growth in pancreatic cancer and improves the efficacy of gemcitabine in vivo. J Control Release. 2018;290:1–10.
   PubMed Web of Science ®Google Scholar
• Kim H-J, Lee J-H, Kim S-J, et al. Roles of NADPH oxidases in cisplatin-induced reactive oxygen species generation and ototoxicity. J Neurosci. 2010;30:3933–3946.
   PubMed Web of Science ®Google Scholar
• Ma P, Xiao H, Yu C, et al. Enhanced cisplatin chemotherapy by iron oxide nanocarrier-mediated generation of highly toxic reactive oxygen species. Nano Lett. 2017;17:928–937.
   PubMed Web of Science ®Google Scholar
• Yan L, Amirshaghaghi A, Huang D, et al. Protoporphyrin IX (PpIX)-coated superparamagnetic iron oxide nanoparticle (SPION) nanoclusters for magnetic resonance imaging and photodynamic therapy. Adv Funct Mater. 2018;28:1707030.
   PubMed Web of Science ®Google Scholar
• Boisselier E, Astruc D. Gold nanoparticles in nanomedicine: preparations, imaging, diagnostics, therapies and toxicity. Chem Soc Rev. 2009;38:1759.
   PubMed Web of Science ®Google Scholar
• Umair M, Javed I, Rehman M, et al. Nanotoxicity of inert materials: the case of gold, silver and iron. J Pharm Pharm Sci. 2016;19:161.
   PubMed Web of Science ®Google Scholar
• Han MS, Lytton-Jean AKR, Oh B-K, et al. Colorimetric Screening of DNA-Binding Molecules with Gold Nanoparticle Probes. Angew Chemie Int Ed. 2006;45:1807–1810.
   PubMed Web of Science ®Google Scholar
• Medley CD, Smith JE, Tang Z, et al. Gold nanoparticle-based colorimetric assay for the direct detection of cancerous cells. Anal Chem. 2008;80:1067–1072.
   PubMed Web of Science ®Google Scholar
• Guisasola E, Baeza A, Asín L, et al. Heating at the nanoscale through drug-delivery devices: fabrication and synergic effects in cancer treatment with nanoparticles. Small Methods. 2018;2:1800007.
   Web of Science ®Google Scholar
• Kim F, Song JH, Yang P. Photochemical synthesis of gold nanorods. J Am Chem Soc. 2002;124:14316–14317.
   PubMed Web of Science ®Google Scholar
• Yu, Chang -S-S, C-L L, et al. Gold nanorods: electrochemical synthesis and optical properties. J Phys Chem B. 1997;101:6661–6664.
   Web of Science ®Google Scholar
• Gole A, Murphy CJ. Seed-mediated synthesis of gold nanorods: role of the size and nature of the seed. Chem Mater. 2004;16:3633–3640.
   Web of Science ®Google Scholar
• Takahashi H, Niidome Y, Niidome T, et al. Modification of gold nanorods using phosphatidylcholine to reduce cytotoxicity. Langmuir. 2006;22:2–5.
   PubMed Web of Science ®Google Scholar
• Hauck TS, Ghazani AA, Chan WCW. Assessing the effect of surface chemistry on gold nanorod uptake, toxicity, and gene expression in mammalian cells. Small. 2008;4:153–159.
   PubMed Web of Science ®Google Scholar
• Rayavarapu RG, Petersen W, Hartsuiker L, et al. In vitro toxicity studies of polymer-coated gold nanorods. Nanotechnology. 2010;21:145101.
   PubMed Web of Science ®Google Scholar
• Pan Y, Neuss S, Leifert A, et al. Size-dependent cytotoxicity of gold nanoparticles. Small. 2007;3:1941–1949.
   PubMed Web of Science ®Google Scholar
• Pan Y, Leifert A, Ruau D, et al. Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small. 2009;5:2067–2076.
   PubMed Web of Science ®Google Scholar
• Mironava T, Hadjiargyrou M, Simon M, et al. Gold nanoparticles cellular toxicity and recovery: effect of size, concentration and exposure time. Nanotoxicology. 2010;4:120–137.
   PubMed Web of Science ®Google Scholar
• Albanese A, Chan WCW. Effect of gold nanoparticle aggregation on cell uptake and toxicity. ACS Nano. 2011;5:5478–5489.
   PubMed Web of Science ®Google Scholar
• Chithrani BD, Ghazani AA, Chan WCW. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano Lett. 2006;6:662–668.
   PubMed Web of Science ®Google Scholar
• Singh A, Shukla R, Hassan S, et al. Cytotoxicity and cellular internalization studies of biogenic gold nanotriangles in animal cell lines. Int J Green Nanotechnol. 2011;3:251–263.
   Google Scholar
• Favi PM, Gao M, Johana Sepúlveda Arango L, et al. Shape and surface effects on the cytotoxicity of nanoparticles: gold nanospheres versus gold nanostars. J Biomed Mater Res Part A. 2015;103:3449–3462.
   PubMed Web of Science ®Google Scholar
• Schaeublin NM, Braydich-Stolle LK, Schrand AM, et al. Surface charge of gold nanoparticles mediates mechanism of toxicity. Nanoscale. 2011;3:410.
   PubMed Web of Science ®Google Scholar
• Bertrand N, Leroux J-C. The journey of a drug-carrier in the body: an anatomo-physiological perspective. J Control Release. 2012;161:152–163.
   PubMed Web of Science ®Google Scholar
• Choi K, Riviere JE, Monteiro-Riviere NA. Protein corona modulation of hepatocyte uptake and molecular mechanisms of gold nanoparticle toxicity. Nanotoxicology. 2017;11:64–75.
   PubMed Web of Science ®Google Scholar
• Johnston HJ, Hutchison G, Christensen FM, et al. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol. 2010;40:328–346.
   PubMed Web of Science ®Google Scholar
• Simpson CA, Salleng KJ, Cliffel DE, et al. In vivo toxicity, biodistribution, and clearance of glutathione-coated gold nanoparticles. Nanomedicine Nanotechnology, Biol Med. 2013;9:257–263.
   PubMed Web of Science ®Google Scholar
• Thakor AS, Luong R, Paulmurugan R, et al. The fate and toxicity of raman-active silica-gold nanoparticles in mice. Sci Transl Med. 2011;3: 79ra33–79ra33.
   PubMed Web of Science ®Google Scholar
• Lasagna-Reeves C, Gonzalez-Romero D, Barria MA, et al. Bioaccumulation and toxicity of gold nanoparticles after repeated administration in mice. Biochem Biophys Res Commun. 2010;393:649–655.
   PubMed Web of Science ®Google Scholar
• Villaverde G, Gómez-Graña S, Guisasola E, et al. Targeted chemo-photothermal therapy: a nanomedicine approximation to selective melanoma treatment. Part Part Syst Charact. 2018;35:1800148.
   Web of Science ®Google Scholar
• Kreyling WG, Abdelmonem AM, Ali Z, et al. In vivo integrity of polymer-coated gold nanoparticles. Nat Nanotechnol. 2015;10:619–623.
   PubMed Web of Science ®Google Scholar
• Rengan AK, Bukhari AB, Pradhan A, et al. In vivo analysis of biodegradable liposome gold nanoparticles as efficient agents for photothermal therapy of cancer. Nano Lett. 2015;15:842–848.
   PubMed Web of Science ®Google Scholar
• Bunggulawa EJ, Wang W, Yin T, et al. Recent advancements in the use of exosomes as drug delivery systems. J Nanobiotechnology. 2018;16:81.
   PubMed Web of Science ®Google Scholar
• Betzer O, Perets N, Angel A, et al. In vivo neuroimaging of exosomes using gold nanoparticles. ACS Nano. 2017;11:10883–10893.
   PubMed Web of Science ®Google Scholar
• Cheng X, Sun R, Yin L, et al. Light-triggered assembly of gold nanoparticles for photothermal therapy and photoacoustic imaging of tumors in vivo. Adv Mater. 2017;29:1604894.
   Web of Science ®Google Scholar
• Shen H, Zhang L, Liu M, et al. Biomedical applications of graphene. Theranostics. 2012;2:283–294.
   PubMed Web of Science ®Google Scholar
• Seabra AB, Paula AJ, de Lima R, et al. Nanotoxicity of graphene and graphene oxide. Chem Res Toxicol. 2014;27:159–168.
   PubMed Web of Science ®Google Scholar
• Ou L, Song B, Liang H, et al. Toxicity of graphene-family nanoparticles: a general review of the origins and mechanisms. Part Fibre Toxicol. 2016;13:57.
   PubMed Web of Science ®Google Scholar
• Jastrzębska AM, Kurtycz P, Olszyna AR. Recent advances in graphene family materials toxicity investigations. J Nanopart Res. 2012;14:1320.
   PubMed Web of Science ®Google Scholar
• Yang K, Li Y, Tan X, et al. Behavior and toxicity of graphene and its functionalized derivatives in biological systems. Small. 2013;9:1492–1503.
   PubMed Web of Science ®Google Scholar
• Gurunathan S, Han JW, Eppakayala V, et al. Green synthesis of graphene and its cytotoxic effects in human breast cancercells. Int J Nanomedicine. 2013;8:1015.
   PubMed Web of Science ®Google Scholar
• Vallabani NVS, Mittal S, Shukla R, et al. Toxicity of graphene in normal human lung cells (BEAS-2B). J Biomed Nanotechnol. 2011;7:106–107.
   PubMed Web of Science ®Google Scholar
• Zhang L, Xia J, Zhao Q, et al. Functional graphene oxide as a nanocarrier for controlled loading and targeted delivery of mixed anticancer drugs. Small. 2010;6:537–544.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Ali SF, Dervishi E, et al. Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. ACS Nano. 2010;4:3181–3186.
   PubMed Web of Science ®Google Scholar
• Chang Y, Yang S-T, Liu J-H, et al. In vitro toxicity evaluation of graphene oxide on A549 cells. Toxicol Lett. 2011;200:201–210.
   PubMed Web of Science ®Google Scholar
• Qiao Y, An J, Ma L. Single cell array based assay for in vitro genotoxicity study of nanomaterials. Anal Chem. 2013;85:4107–4112.
   PubMed Web of Science ®Google Scholar
• Robinson JT, Tabakman SM, Liang Y, et al. Ultrasmall reduced graphene oxide with high near-infrared absorbance for photothermal therapy. J Am Chem Soc. 2011;133:6825–6831.
   PubMed Web of Science ®Google Scholar
• Feng L, Liu Z. Graphene in biomedicine: opportunities and challenges. Nanomedicine. 2011;6:317–324.
   PubMed Web of Science ®Google Scholar
• Liu Z, Robinson JT, Sun X, et al. PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J Am Chem Soc. 2008;130:10876–10877.
   PubMed Web of Science ®Google Scholar
• Sun X, Liu Z, Welsher K, et al. Nano-graphene oxide for cellular imaging and drug delivery. Nano Res. 2008;1:203–212.
   PubMed Web of Science ®Google Scholar
• Sasidharan A, Panchakarla LS, Sadanandan AR, et al. Hemocompatibility and macrophage response of pristine and functionalized graphene. Small. 2012;8:1251–1263.
   PubMed Web of Science ®Google Scholar
• Singh SK, Singh MK, Kulkarni PP, et al. Amine-modified graphene: thrombo-protective safer alternative to graphene oxide for biomedical applications. ACS Nano. 2012;6:2731–2740.
   PubMed Web of Science ®Google Scholar
• Zhang X, Yin J, Peng C, et al. Distribution and biocompatibility studies of graphene oxide in mice after intravenous administration. Carbon N Y. 2011;49:986–995.
   Web of Science ®Google Scholar
• Liao K, Lin Y, Macosko CW, et al. Cytotoxicity of graphene oxide and graphene in human erythrocytes and skin fibroblasts. ACS Appl Mater Interfaces. 2011;3:2607–2615.
   PubMed Web of Science ®Google Scholar
• Wen K-P, Chen Y-C, Chuang C-H, et al. Accumulation and toxicity of intravenously-injected functionalized graphene oxide in mice. J Appl Toxicol. 2015;35:1211–1218.
   PubMed Web of Science ®Google Scholar
• Schinwald A, Murphy FA, Jones A, et al. Graphene-based nanoplatelets: a new risk to the respiratory system as a consequence of their unusual aerodynamic properties. ACS Nano. 2012;6:736–746.
   PubMed Web of Science ®Google Scholar
• Zhang S, Yang K, Feng L, et al. In vitro and in vivo behaviors of dextran functionalized graphene. Carbon N Y. 2011;49:4040–4049.
   Web of Science ®Google Scholar
• Wang K, Ruan J, Song H, et al. Biocompatibility of Graphene Oxide. Nanoscale Res Lett. 2011;6:8.
   PubMed Web of Science ®Google Scholar
• Gollavelli G, Ling Y-C. Multi-functional graphene as an in vitro and in vivo imaging probe. Biomaterials. 2012;33:2532–2545.
   PubMed Web of Science ®Google Scholar
• Zanni E, De Bellis G, Bracciale MP, et al. Graphite nanoplatelets and Caenorhabditis elegans : insights from an in vivo model. Nano Lett. 2012;12:2740–2744.
   PubMed Web of Science ®Google Scholar
• Zhang W, Wang C, Li Z, et al. Unraveling stress-induced toxicity properties of graphene oxide and the underlying mechanism. Adv Mater. 2012;24:5391–5397.
   PubMed Web of Science ®Google Scholar
• Syama S, Mohanan PV. Safety and biocompatibility of graphene: A new generation nanomaterial for biomedical application. Int J Biol Macromol. 2016;86:546–555.
   PubMed Web of Science ®Google Scholar
• Zhu C, Guo S, Fang Y, et al. Reducing sugar: new functional molecules for the green synthesis of graphene nanosheets. ACS Nano. 2010;4:2429–2437.
   PubMed Web of Science ®Google Scholar
• Gao J, Liu F, Liu Y, et al. Environment-friendly method to produce graphene that employs vitamin C and amino acid. Chem Mater. 2010;22:2213–2218.
   Web of Science ®Google Scholar
• Urbas K, Aleksandrzak M, Jedrzejczak M, et al. Chemical and magnetic functionalization of graphene oxide as a route to enhance its biocompatibility. Nanoscale Res Lett. 2014;9:656.
   PubMed Web of Science ®Google Scholar
• Chong Y, Ma Y, Shen H, et al. The in vitro and in vivo toxicity of graphene quantum dots. Biomaterials. 2014;35:5041–5048.
   PubMed Web of Science ®Google Scholar
• Jasim DA, Boutin H, Fairclough M, et al. Thickness of functionalized graphene oxide sheets plays critical role in tissue accumulation and urinary excretion: A pilot PET/CT study. Appl Mater Today. 2016;4:24–30.
   Web of Science ®Google Scholar
• Yang K, Zhang S, Zhang G, et al. Graphene in mice: ultrahigh in vivo tumor uptake and efficient photothermal therapy. Nano Lett. 2010;10:3318–3323.
   PubMed Web of Science ®Google Scholar
• Miao W, Shim G, Lee S, et al. Safety and tumor tissue accumulation of pegylated graphene oxide nanosheets for co-delivery of anticancer drug and photosensitizer. Biomaterials. 2013;34:3402–3410.
   PubMed Web of Science ®Google Scholar
• Yang K, Gong H, Shi X, et al. In vivo biodistribution and toxicology of functionalized nano-graphene oxide in mice after oral and intraperitoneal administration. Biomaterials. 2013;34:2787–2795.
   PubMed Web of Science ®Google Scholar
• Yan L, Wang Y, Xu X, et al. Can graphene oxide cause damage to eyesight?. Chem Res Toxicol. 2012;25:1265–1270.
   PubMed Web of Science ®Google Scholar
• Kiew SF, Kiew LV, Lee HB, et al. Assessing biocompatibility of graphene oxide-based nanocarriers: A review. J Control Release. 2016;226:217–228.
   PubMed Web of Science ®Google Scholar
• Kim Y-K, Kim M-H, Min D-H. Biocompatible reduced graphene oxide prepared by using dextran as a multifunctional reducing agent. Chem Commun. 2011;47:3195–3197.
   PubMed Web of Science ®Google Scholar
• Wate PS, Banerjee SS, Jalota-Badhwar A, et al. Cellular imaging using biocompatible dendrimer-functionalized graphene oxide-based fluorescent probe anchored with magnetic nanoparticles. Nanotechnology. 2012;23:415101.
   PubMed Web of Science ®Google Scholar
• Hong BJ, Compton OC, An Z, et al. successful stabilization of graphene oxide in electrolyte solutions: enhancement of biofunctionalization and cellular uptake. ACS Nano. 2012;6:63–73.
   PubMed Web of Science ®Google Scholar
• Cheng C, Nie S, Li S, et al. Biopolymer functionalized reduced graphene oxide with enhanced biocompatibility via mussel inspired coatings/anchors. J Mater Chem B. 2013;1:265–275.
   PubMed Web of Science ®Google Scholar
• Xu M, Zhu J, Wang F, et al. Improved in vitro and in vivo biocompatibility of graphene oxide through surface modification: poly(Acrylic Acid)-functionalization is superior to PEGylation. ACS Nano. 2016;10:3267–3281.
   PubMed Web of Science ®Google Scholar
• Croissant JG, Fatieiev Y, Khashab NM. Degradability and clearance of silicon, organosilica, silsesquioxane, silica mixed oxide, and mesoporous silica nanoparticles. Adv Mater. 2017;29:1604634.
   Web of Science ®Google Scholar
• Santos HA, Mäkilä E, Airaksinen AJ, et al. Porous silicon nanoparticles for nanomedicine: preparation and biomedical applications. Nanomedicine. 2014;9:535–554.
   PubMed Web of Science ®Google Scholar
• Xu W, Rytkönen J, Rönkkö S, et al. A nanostopper approach to selectively engineer the surfaces of mesoporous silicon. Chem Mater. 2014;26:6734–6742.
   Web of Science ®Google Scholar
• Kafshgari MH, Delalat B, Tong WY, et al. Oligonucleotide delivery by chitosan-functionalized porous silicon nanoparticles. Nano Res. 2015;8:2033–2046.
   Web of Science ®Google Scholar
• Godin B, Gu J, Serda RE, et al. Tailoring the degradation kinetics of mesoporous silicon structures through PEGylation. J Biomed Mater Res A. 2010;94:1236–1243.
   PubMed Web of Science ®Google Scholar
• Hou H, Nieto A, Ma F, et al. Tunable sustained intravitreal drug delivery system for daunorubicin using oxidized porous silicon. J Control Release. 2014;178:46–54.
   PubMed Web of Science ®Google Scholar
• Martinez JO, Chiappini C, Ziemys A, et al. Engineering multi-stage nanovectors for controlled degradation and tunable release kinetics. Biomaterials. 2013;34:8469–8477.
   PubMed Web of Science ®Google Scholar
• Hon NK, Shaposhnik Z, Diebold ED, et al. Tailoring the biodegradability of porous silicon nanoparticles. J Biomed Mater Res Part A. 2012;100A:3416–3421.
   Web of Science ®Google Scholar
• Park J-H, Gu L, von Maltzahn G, et al. Biodegradable luminescent porous silicon nanoparticles for in vivo applications. Nat Mater. 2009;8:331–336.
   PubMed Web of Science ®Google Scholar
• Martinez JO, Evangelopoulos M, Chiappini C, et al. Degradation and biocompatibility of multistage nanovectors in physiological systems. J Biomed Mater Res Part A. 2014;102:3540–3549.
   PubMed Web of Science ®Google Scholar
• Tolstik E, Osminkina LA, Matthäus C, et al. Studies of silicon nanoparticles uptake and biodegradation in cancer cells by Raman spectroscopy. Nanomedicine Nanotechnology, Biol Med. 2016;12:1931–1940.
   PubMed Web of Science ®Google Scholar
• Tzur-Balter A, Shatsberg Z, Beckerman M, et al. Mechanism of erosion of nanostructured porous silicon drug carriers in neoplastic tissues. Nat Commun. 2015;6:6208.
   PubMed Web of Science ®Google Scholar
• Wang C-F, Mäkilä EM, Kaasalainen MH, et al. Copper-free azide–alkyne cycloaddition of targeting peptides to porous silicon nanoparticles for intracellular drug uptake. Biomaterials. 2014;35:1257–1266.
   PubMed Web of Science ®Google Scholar
• Shahbazi MA, Hamidi M, Mäkilä EM, et al. The mechanisms of surface chemistry effects of mesoporous silicon nanoparticles on immunotoxicity and biocompatibility. Biomaterials. 2013;34:7776–7789.
   PubMed Web of Science ®Google Scholar
• Ivanov S, Zhuravsky S, Yukina G, et al. In vivo toxicity of intravenously administered silica and silicon nanoparticles. Materials. 2012;5:1873–1889.
   Web of Science ®Google Scholar
• Sarparanta M, Bimbo LM, Rytkoänen J, et al. Intravenous delivery of hydrophobin-functionalized porous silicon nanoparticles: stability, plasma protein adsorption and biodistribution. Mol Pharm. 2012;9:654–663.
   PubMed Web of Science ®Google Scholar
• Sarparanta MP, Bimbo LM, Mäkilä EM, et al. The mucoadhesive and gastroretentive properties of hydrophobin-coated porous silicon nanoparticle oral drug delivery systems. Biomaterials. 2012;33:3353–3362.
   PubMed Web of Science ®Google Scholar
• Shahbazi M, Almeida PV, Mäkilä E, et al. Functionalized porous silicon nanoparticles for enhanced stability and cellular internalization. Macromol Rapid Commun. 2014;35:624–629.
   PubMed Web of Science ®Google Scholar
• Xia B, Zhang W, Shi J, et al. Engineered stealth porous silicon nanoparticles via surface encapsulation of bovine serum albumin for prolonging blood circulation in vivo. ACS Appl Mater Interfaces. 2013;5:11718–11724.
   PubMed Web of Science ®Google Scholar
• Paris JL, Colilla M, Izquierdo-Barba I, et al. Tuning mesoporous silica dissolution in physiological environments: a review. J Mater Sci. 2017;52:8761–8771.
   Web of Science ®Google Scholar
• Vallet-Regí M, Rámila A, Del Real RP, et al. A new property of MCM-41: drug delivery system. Chem Mater. 2001;13:308–311.
   Web of Science ®Google Scholar
• Vallet-Regí M, Ruiz-Hernández E. Bioceramics: from bone regeneration to cancer nanomedicine. Adv Mater. 2011;23:5177–5218.
   PubMed Web of Science ®Google Scholar
• Villaverde G, Alfranca A, Gonzalez‐Murillo Á, et al. Molecular scaffolds as double‐targeting agents for the diagnosis and treatment of neuroblastoma. Angew Chemie. 2019;131:3099–3104.
   Google Scholar
• Mora-Raimundo P, Lozano D, Manzano M, et al. Nanoparticles to Knockdown osteoporosis-related gene and promote osteogenic marker expression for osteoporosis treatment. ACS Nano. 2019;13:5451–5464.
   PubMed Web of Science ®Google Scholar
• Baeza A, Colilla M, Vallet-Regí M. Advances in mesoporous silica nanoparticles for targeted stimuli-responsive drug delivery. Expert Opin Drug Deliv. 2015;12:319–337.
   PubMed Web of Science ®Google Scholar
• Baeza A, Ruiz-Molina D, Vallet-Regí M. Recent advances in porous nanoparticles for drug delivery in antitumoral applications: inorganic nanoparticles and nanoscale metal-organic frameworks. Expert Opin Drug Deliv. 2017;14:783–796.
   PubMed Web of Science ®Google Scholar
• Martínez-Carmona M, Lozano D, Baeza A, et al. A novel visible light responsive nanosystem for cancer treatment. Nanoscale. 2017;9:15967–15973.
   PubMed Web of Science ®Google Scholar
• Martínez-Carmona M, Baeza A, Rodriguez-Milla MA, et al. Mesoporous silica nanoparticles grafted with a light-responsive protein shell for highly cytotoxic antitumoral therapy. J Mater Chem B. 2015;3:5746–5752.
   PubMed Web of Science ®Google Scholar
• Guisasola E, Asín L, Beola L, et al. Beyond traditional hyperthermia: in vivo cancer treatment with magnetic-responsive mesoporous silica nanocarriers. ACS Appl Mater Interfaces. 2018;10:12518–12525.
   PubMed Web of Science ®Google Scholar
• Baeza A, Guisasola E, Ruiz-Hernández E, et al. Magnetically triggered multidrug release by hybrid mesoporous silica nanoparticles. Chem Mater. 2012;24:517–524.
   Web of Science ®Google Scholar
• Guisasola E, Baeza A, Talelli M, et al. Magnetic-responsive release controlled by hot spot effect. Langmuir. 2015;31:12777–12782.
   PubMed Web of Science ®Google Scholar
• Paris JL, Cabañas MV, Manzano M, et al. Polymer-grafted mesoporous silica nanoparticles as ultrasound-responsive drug carriers. ACS Nano. 2015;9:11023–11033.
   PubMed Web of Science ®Google Scholar
• Martínez-Carmona M, Lozano D, Colilla M, et al. Selective topotecan delivery to cancer cells by targeted pH-sensitive mesoporous silica nanoparticles. RSC Adv. 2016;6:50923–50932.
   Web of Science ®Google Scholar
• Hu C, Huang P, Zheng Z, et al. A facile strategy to prepare an enzyme-responsive mussel mimetic coating for drug delivery based on mesoporous silica nanoparticles. Langmuir. 2017;33:5511–5518.
   PubMed Web of Science ®Google Scholar
• Wu M, Meng Q, Chen Y, et al. Large pore-sized hollow mesoporous organosilica for redox-responsive gene delivery and synergistic cancer chemotherapy. Adv Mater. 2016;28:1963–1969.
   PubMed Web of Science ®Google Scholar
• Lin YS, Abadeer N, Haynes CL. Stability of small mesoporous silica nanoparticles in biological media. Chem Commun. 2011;47:532–534.
   PubMed Web of Science ®Google Scholar
• Murugadoss S, Lison D, Godderis L, et al. Toxicology of silica nanoparticles: an update. Arch Toxicol. 2017;91:2967–3010.
   PubMed Web of Science ®Google Scholar
• Kim I-Y, Joachim E, Choi H, et al. Toxicity of silica nanoparticles depends on size, dose, and cell type. Nanomedicine Nanotechnology, Biol Med. 2015;11:1407–1416.
   PubMed Web of Science ®Google Scholar
• Kim D, Lin YS, Haynes CL. On-chip evaluation of shear stress effect on cytotoxicity of mesoporous silica nanoparticles. Anal Chem. 2011;83:8377–8382.
   PubMed Web of Science ®Google Scholar
• Heidegger S, Gößl D, Schmidt A, et al. Immune response to functionalized mesoporous silica nanoparticles for targeted drug delivery. Nanoscale. 2016;8:938–948.
   PubMed Web of Science ®Google Scholar
• Lin Y-S, Haynes CL. Impacts of mesoporous silica nanoparticle size, pore ordering, and pore integrity on hemolytic activity. J Am Chem Soc. 2010;132:4834–4842.
   PubMed Web of Science ®Google Scholar
• Slowing II, Wu CW, Vivero-Escoto JL, et al. Mesoporous silica nanoparticles for reducing hemolytic activity towards mammalian red blood cells. Small. 2009;5:57–62.
   PubMed Web of Science ®Google Scholar
• Urata C, Yamada H, Wakabayashi R, et al. Aqueous colloidal mesoporous nanoparticles with ethenylene-bridged silsesquioxane frameworks. J Am Chem Soc. 2011;133:8102–8105.
   PubMed Web of Science ®Google Scholar
• Liu T, Li L, Teng X, et al. Single and repeated dose toxicity of mesoporous hollow silica nanoparticles in intravenously exposed mice. Biomaterials. 2011;32:1657–1668.
   PubMed Web of Science ®Google Scholar
• Fu C, Liu T, Li L, et al. The absorption, distribution, excretion and toxicity of mesoporous silica nanoparticles in mice following different exposure routes. Biomaterials. 2013;34:2565–2575.
   PubMed Web of Science ®Google Scholar
• Hudson SP, Padera RF, Langer R, et al. The biocompatibility of mesoporous silicates. Biomaterials. 2008;29:4045–4055.
   PubMed Web of Science ®Google Scholar
• Villaverde G, Baeza A, Melen GJ, et al. A new targeting agent for the selective drug delivery of nanocarriers for treating neuroblastoma. J Mater Chem B. 2015;3:4831–4842.
   PubMed Web of Science ®Google Scholar
• Dogra P, Adolphi NL, Wang Z, et al. Establishing the effects of mesoporous silica nanoparticle properties on in vivo disposition using imaging-based pharmacokinetics. Nat Commun. 2018;9:4551.
   PubMed Web of Science ®Google Scholar
• Yu T, Greish K, McGill LD, et al. Influence of geometry, porosity, and surface characteristics of silica nanoparticles on acute toxicity: their vasculature effect and tolerance threshold. ACS Nano. 2012;6:2289–2301.
   PubMed Web of Science ®Google Scholar
• Lee S, Kim MS, Lee D, et al. The comparative immunotoxicity of mesoporous silica nanoparticles and colloidal silica nanoparticles in mice. Int J Nanomedicine. 2013;8:147–158.
   PubMed Web of Science ®Google Scholar
• Li L, Tang F, Liu H, et al. In vivo delivery of silica nanorattle encapsulated docetaxel for liver cancer therapy with low toxicity and high efficacy. ACS Nano. 2011;5:679.
   Web of Science ®Google Scholar
• He Q, Shi J, Zhu M, et al. The three-stage in vitro degradation behavior of mesoporous silica in simulated body fluid. Microporous Mesoporous Mater. 2010;131:314–320.
   Web of Science ®Google Scholar
• Braun K, Pochert A, Beck M, et al. Dissolution kinetics of mesoporous silica nanoparticles in different simulated body fluids. J Sol-Gel Sci Technol. 2016;79:319–327.
   Web of Science ®Google Scholar
• Yamada H, Urata C, Aoyama Y, et al. Preparation of colloidal mesoporous silica nanoparticles with different diameters and their unique degradation behavior in static aqueous systems. Chem Mater. 2012;24:1462–1471.
   Web of Science ®Google Scholar
• Hao N, Liu H, Li L, et al. In vitro degradation behavior of silica nanoparticles under physiological conditions. J Nanosci Nanotechnol. 2012;12:6346–6354.
   PubMed Web of Science ®Google Scholar
• Huang X, Young NP, Townley HE. Characterization and comparison of mesoporous silica particles for optimized drug delivery. Nanomater Nanotechnol. 2014;4:2.
   Web of Science ®Google Scholar
• Cauda V, Schlossbauer A, Bein T. Bio-degradation study of colloidal mesoporous silica nanoparticles: effect of surface functionalization with organo-silanes and poly(ethylene glycol). Microporous Mesoporous Mater. 2010;132:60–71.
   Web of Science ®Google Scholar
• Li X, Zhang L, Dong X, et al. Preparation of mesoporous calcium doped silica spheres with narrow size dispersion and their drug loading and degradation behavior. Microporous Mesoporous Mater. 2007;102:151–158.
   Web of Science ®Google Scholar
• Yu L, Chen Y, Wu M, et al. “Manganese extraction” strategy enables tumor-sensitive biodegradability and theranostics of nanoparticles. J Am Chem Soc. 2016;138:9881–9894.
   PubMed Web of Science ®Google Scholar
• Fontecave T, Sanchez C, Azaïs T, et al. Chemical modification as a versatile tool for tuning stability of silica based mesoporous carriers in biologically relevant conditions. Chem Mater. 2012;24:4326–4336.
   Web of Science ®Google Scholar
• Maggini L, Cabrera I, Ruiz-Carretero A, et al. Breakable mesoporous silica nanoparticles for targeted drug delivery. Nanoscale. 2016;8:7240–7247.
   PubMed Web of Science ®Google Scholar
• Chen Y, Meng Q, Wu M, et al. Hollow mesoporous organosilica nanoparticles: a generic intelligent framework-hybridization approach for biomedicine. J Am Chem Soc. 2014;136:16326–16334.
   PubMed Web of Science ®Google Scholar
• Cauda V, Argyo C, Bein T. Impact of different PEGylation patterns on the long-term bio-stability of colloidal mesoporous silica nanoparticles. J Mater Chem. 2010;20:8693–8699.
   Web of Science ®Google Scholar
• Shen D, Yang J, Li X, et al. Biphase stratification approach to three-dimensional dendritic biodegradable mesoporous silica nanospheres. Nano Lett. 2014;14:923–932.
   PubMed Web of Science ®Google Scholar
• Möller K, Bein T. Degradable drug carriers: vanishing mesoporous silica nanoparticles. Chem Mater. 2019;31:4364–4378.
   Web of Science ®Google Scholar
• Zhang Q, Wang X, Li PZ, et al. Biocompatible, uniform, and redispersible mesoporous silica nanoparticles for cancer-targeted drug delivery in vivo. Adv Funct Mater. 2014;24:2450–2461.
   Web of Science ®Google Scholar
• He Q, Zhang Z, Gao F, et al. In vivo biodistribution and urinary excretion of mesoporous silica nanoparticles: effects of particle size and PEGylation. Small. 2011;7:271–280.
   PubMed Web of Science ®Google Scholar
• Huang X, Li L, Liu T, et al. The shape effect of mesoporous silica nanoparticles on biodistribution, clearance, and biocompatibility in vivo. ACS Nano. 2011;5:5390–5399.
   PubMed Web of Science ®Google Scholar
• Li L, Liu T, Fu C, et al. Biodistribution, excretion, and toxicity of mesoporous silica nanoparticles after oral administration depend on their shape. Nanomedicine Nanotechnology, Biol Med. 2015;11:1915–1924.
   PubMed Web of Science ®Google Scholar
• Tarn D, Ashley CE, Xue M, et al. Mesoporous silica nanoparticle nanocarriers: biofunctionality and biocompatibility. Acc Chem Res. 2013;46:792–801.
   PubMed Web of Science ®Google Scholar
• Desai D, Zhang J, Sandholm J, et al. Lipid bilayer-gated mesoporous silica nanocarriers for tumor-targeted delivery of zoledronic acid in vivo. Mol Pharm. 2017;14:3218–3227.
   PubMed Web of Science ®Google Scholar
• Gonzalez Porras MA, Durfee PN, Gregory AM, et al. A novel approach for targeted delivery to motoneurons using cholera toxin-B modified protocells. J Neurosci Methods. 2016;273:160–174.
   PubMed Web of Science ®Google Scholar
• Ashley CE, Carnes EC, Epler KE, et al. Delivery of small interfering RNA by peptide-targeted mesoporous silica nanoparticle-supported lipid bilayers. ACS Nano. 2012;6:2174–2188.
   PubMed Web of Science ®Google Scholar
• Epler K, Padilla D, Phillips G, et al. Delivery of ricin toxin A-chain by peptide-targeted mesoporous silica nanoparticle-supported lipid bilayers. Adv Healthc Mater. 2012;1:348–353.
   PubMed Web of Science ®Google Scholar
• Sharifabad ME, Mercer T, Sen T. Drug-loaded liposome-capped mesoporous core–shell magnetic nanoparticles for cellular toxicity study. Nanomedicine. 2016;11:2753–2755.
   PubMed Web of Science ®Google Scholar
• Han N, Zhao Q, Wan L, et al. Hybrid lipid-capped mesoporous silica for stimuli-responsive drug release and overcoming multidrug resistance. ACS Appl Mater Interfaces. 2015;7:3342–3351.
   PubMed Web of Science ®Google Scholar
• Villegas MR, Baeza A, Noureddine A, et al. Multifunctional protocells for enhanced penetration in 3D extracellular tumoral matrices. Chem Mater. 2018;30:112–120.
   Web of Science ®Google Scholar
• Villegas MR, Baeza A, Vallet-Regí M. Hybrid collagenase nanocapsules for enhanced nanocarrier penetration in tumoral tissues. ACS Appl Mater Interfaces. 2015;7:24075–24081.
   PubMed Web of Science ®Google Scholar
• Akin D, Sturgis J, Ragheb K, et al. Bacteria-mediated delivery of nanoparticles and cargo into cells. Nat Nanotechnol. 2007;2:441–449.
   PubMed Web of Science ®Google Scholar
• Bonvalot S, Le Pechoux C, De Baere T, et al. First-in-human study testing a new radioenhancer using nanoparticles (NBTXR3) activated by radiation therapy in patients with locally advanced soft tissue sarcomas. Clin Cancer Res. 2017;23:908–917.
   PubMed Web of Science ®Google Scholar