Nanomedicine and nanotoxicology: the pros and cons for neurodegeneration and brain cancer

References

• 1 Clarke DD, Sokoloff L. Regulation of cerebral metabolic rate. In: Basic Neurochemistry: Molecular, Cellular and Medical Aspects (6th Edition). Siegel GJ, Agranoff BW, Albers RW et al. (Eds). Lippincott-Raven, PA, USA (1999).
  Google Scholar
• 2 Celardo I, Martins LM, Gandhi S. Unravelling mitochondrial pathways to Parkinson's disease. Br. J. Pharmacol. 171(8), 1943–1957 (2014).
  Medline CASGoogle Scholar
• 3 Kamat JP, Devasagayam TPA, Priyadarsini KI, Mohan H. Reactive oxygen species mediated membrane damage induced by fullerene derivatives and its possible biological implications. Toxicology 155(1–3), 55–61 (2000).
  Medline CASGoogle Scholar
• 4 Chaudhari N, Talwar P, Parimisetty A et al. A molecular web: endoplasmic reticulum stress, inflammation, and oxidative stress. Front. Cell Neurosci. 8, 213 (2014).
  MedlineGoogle Scholar
• 5 Abbott NJ, Patabendige AA, Dolman DE et al. Structure and function of the blood–brain barrier. Neurobiol. Dis. 37(1), 13–25 (2010).
  Medline CASGoogle Scholar
• 6 Eyal S, Hsiao P, Unadkat JD. Drug interactions at the blood–brain barrier: fact or fantasy? Pharmacol. Ther. 123(1), 80–104 (2009).
  Medline CASGoogle Scholar
• 7 Gelperina S, Maksimenko O, Khalansky A et al. Drug delivery to the brain using surfactant-coated poly (lactide-co-glycolide) nanoparticles: influence of the formulation parameters. Eur. J. Pharm. Biopharm. 74(2), 157–163 (2010).
  Medline CASGoogle Scholar
• 8 Petri B, Bootz A, Khalansky A et al. Chemotherapy of brain tumour using doxorubicin bound to surfactant-coated poly(butyl cyanoacrylate) nanoparticles: revisiting the role of surfactants. J. Control. Release 117(1), 51–58 (2007).
  Medline CASGoogle Scholar
• 9 Kreuter J, Shamenkov D, Petrov V et al. Apolipoprotein-mediated transport of nanoparticle-bound drugs across the blood–brain barrier. J. Drug Target 10(4), 317–325 (2002).
  Medline CASGoogle Scholar
• 10 Gendelman HE, Mosley RL, Boska MD, McMillan J. The promise of nanoneuromedicine. Nanomedicine 9(2), 171–176 (2014).
  CASGoogle Scholar
• 11 Pardridge WM. The blood–brain barrier: bottleneck in brain drug development. NeuroRx 2(1), 3–14 (2005).
  MedlineGoogle Scholar
• 12 Fuentes P, Catalan J. A clinical perspective: anti Tau's treatment in Alzheimer's disease. Curr. Alzheimer Res. 8(6), 686–688 (2011).
  Medline CASGoogle Scholar
• 13 Pardridge WM. Drug transport across the blood–brain barrier. J. Cereb. Blood Flow Metab. 32(11), 1959–1972 (2012).
  Medline CASGoogle Scholar
• 14 Gabathuler R. Approaches to transport therapeutic drugs across the blood–brain barrier to treat brain diseases. Neurobiol. Dis. 37(1), 48–57 (2010).
  Medline CASGoogle Scholar
• 15 Larsen JM, Martin DR, Byrne ME. Recent advances in delivery through the blood–brain barrier. Curr. Top. Med. Chem. 14(9), 1148–1160 (2014).
  Medline CASGoogle Scholar
• 16 Kreuter J. Drug delivery to the central nervous system by polymeric nanoparticles: what do we know? Adv. Drug Deliv. Rev. 71, 2–14 (2014).
  Medline CASGoogle Scholar
• 17 Kreuter J. Mechanism of polymeric nanoparticle-based drug transport across the blood–brain barrier (BBB). J. Microencapsul. 30(1), 49–54 (2013).
  Medline CASGoogle Scholar
• 18 Wohlfart S, Gelperina S, Kreuter J. Transport of drugs across the blood–brain barrier by nanoparticles. J. Control. Release 161(2), 264–273 (2012).
  Medline CASGoogle Scholar
• 19 Hervé F, Ghinea N, Scherrmann J-M. CNS delivery via adsorptive transcytosis. AAPS J. 10(3), 455–472 (2008).
  Medline CASGoogle Scholar
• 20 Yang H. Nanoparticle-mediated brain-specific drug delivery, imaging, and diagnosis. Pharm. Res. 27(9), 1759–1771 (2010).
  Medline CASGoogle Scholar
• 21 Anselmo AC, Mitragotri S. An overview of clinical and commercial impact of drug delivery systems. J. Control. Release 190, 15–28 (2014).
  Medline CASGoogle Scholar
• 22 BiOasis technologies attracts astrazeneca (AZN), abbvie (ABBV) to blood–brain barrier platform. http://www.midasletter.com/2015/01/bioasis-technologies-inc-blood-brain-barrier-platform-attracts-majors/.
  Google Scholar
• 23 Jain KK. Nanobiotechnology-based strategies for crossing the blood–brain barrier. Nanomedicine 7(8), 1225–1233 (2012).
  CASGoogle Scholar
• 24 Gozzi Alessandro, Swarz Adam, Valerio C et al. Use of short chain oligo-glycerolipids to improve BBB permeability: application to Manganese-Enhanced MRI (MEMRI). Presented at: roceedings of the International Society for Magnetic Resonance in Medicine Scientific Meeting and Exhibition. Toronto, Canada, 3–9 May 2008 (Abstract 527).
  Google Scholar
• 25 James K, Dewan SS, Lawson K, Nagavarapu U. Advanced drug delivery systems: mAb, RNAi, & breaking the blood–brain barrier. Drug Dev. Deliv. 14(9), 46–50 (2014).
  Google Scholar
• 26 Cerense. www.cerense.com/.
  Google Scholar
• 27 Gaillard PJ. Case study: to-BBB's G-Technology, getting the best from drug-delivery research with industry-academia partnerships. Ther. Deliv. 2(11), 1391–1394 (2011).
  MedlineGoogle Scholar
• 28 Business Wire. to-BBB announces positive data from Phase 1 clinical study. Business Wire (2014). www.businesswire.com/news/home/20140912005148/en/to-BBB-Announces-Positive-Data-Phase-1-Clinical#.VczqoLPjLMw.
  Google Scholar
• 29 Lanone S, Boczkowski J. Biomedical applications and potential health risks of nanomaterials: molecular mechanisms. Curr. Mol. Med. 6(6), 651–663 (2006).
  Medline CASGoogle Scholar
• 30 Buzea C, Pacheco II, Robbie K. Nanomaterials and nanoparticles: sources and toxicity. Biointerphases 2(4), MR17–MR71 (2007).
  MedlineGoogle Scholar
• 31 Devasena T, Francis AP. Alzheimers disease & parkinsonism. Brain 29, 31 (2015).
  Google Scholar
• 32 Halliwell B. Role of free radicals in the neurodegenerative diseases. Drugs Aging 18(9), 685–716 (2001).
  Medline CASGoogle Scholar
• 33 Blanka HK, Catherine CB, Seher G-A, Lucienne J-J. Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells. Biochem. J. 441(3), 813–821 (2012).
  MedlineGoogle Scholar
• 34 Bermudez E, Mangum JB, Asgharian B et al. Long-term pulmonary responses of three laboratory rodent species to subchronic inhalation of pigmentary titanium dioxide particles. Toxicol. Sci. 70(1), 86–97 (2002).
  Medline CASGoogle Scholar
• 35 Lee JH, Kim YS, Song KS et al. Biopersistence of silver nanoparticles in tissues from Sprague-Dawley rats. Part Fibre Toxicol. 10(36), 16968–16973 (2013).
  Google Scholar
• 36 Li Y, Li J, Yin J et al. Systematic influence induced by 3 nm titanium dioxide following intratracheal instillation of mice. J. Nanosci. Nanotechnol. 10(12), 8544–8549 (2010).
  Medline CASGoogle Scholar
• 37 Wang J, Liu Y, Jiao F et al. Time-dependent translocation and potential impairment on central nervous system by intranasally instilled TiO₂ nanoparticles. Toxicology 254(1), 82–90 (2008).
  Medline CASGoogle Scholar
• 38 Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225(4667), 1168–1170 (1984).
  Medline CASGoogle Scholar
• 39 Ball MJ, Hachinski V, Fox A et al. A new definition of Alzheimer's disease: a hippocampal dementia. Lancet 325(8419), 14–16 (1985).
  Google Scholar
• 40 Ze Y, Zheng L, Zhao X et al. Molecular mechanism of titanium dioxide nanoparticles-induced oxidative injury in the brain of mice. Chemosphere 92(9), 1183–1189 (2013).
  Medline CASGoogle Scholar
• 41 Nrf2 antioxidant stress response: managing its ‘Dark Side’ (2015). www.caymanchem.com/app/template/Article.vm/article/2168.
  Google Scholar
• 42 Huerta-García E, Pérez-Arizti JA, Márquez-Ramírez SG et al. Titanium dioxide nanoparticles induce strong oxidative stress and mitochondrial damage in glial cells. Free Radic. Biol. Med. 73, 84–94 (2014).
  Medline CASGoogle Scholar
• 43 Lawrence T. The nuclear factor NF-κB pathway in inflammation. Cold Spring Harb. Perspect. Biol. 1(6), a001651 (2009).
  MedlineGoogle Scholar
• 44 Montiel-Dávalos A, Ventura-Gallegos JL, Alfaro-Moreno E et al. TiO₂ nanoparticles induce dysfunction and activation of human endothelial cells. Chem. Res. Toxicol. 25(4), 920–930 (2012).
  Medline CASGoogle Scholar
• 45 Xue Y, Wu J, Sun J. Four types of inorganic nanoparticles stimulate the inflammatory reaction in brain microglia and damage neurons in vitro. Toxicol. Lett. 214(2), 91–98 (2012).
  Medline CASGoogle Scholar
• 46 Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J. Interferon Cytokine Res. 29(6), 313–326 (2009).
  Medline CASGoogle Scholar
• 47 Graeber MB. Changing face of microglia. Science 330(6005), 783–788 (2010).
  Medline CASGoogle Scholar
• 48 Anthony DC, Pitossi FJ. Special issue commentary: the changing face of inflammation in the brain. Mol. Cell. Neurosci. 53, 1–5 (2013).
  Medline CASGoogle Scholar
• 49 Block ML, Zecca L, Hong JS. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8(1), 57–69 (2007).
  Medline CASGoogle Scholar
• 50 Wang Y, Wang B, Zhu MT et al. Microglial activation, recruitment and phagocytosis as linked phenomena in ferric oxide nanoparticle exposure. Toxicol. Lett. 205(1), 26–37 (2011).
  Medline CASGoogle Scholar
• 51 Zhang XD, Wu HY, Wu D et al. Toxicologic effects of gold nanoparticles in vivo by different administration routes. Int. J. Nanomedicine 5, 771 (2010).
  Medline CASGoogle Scholar
• 52 Sonavane G, Tomoda K, Makino K. Biodistribution of colloidal gold nanoparticles after intravenous administration: effect of particle size. Colloids Surf. B Biointerfaces 66(2), 274–280 (2008).
  Medline CASGoogle Scholar
• 53 Yu LE, Lanry Yung LY, Ong CN et al. Translocation and effects of gold nanoparticles after inhalation exposure in rats. NanoToxicology 1(3), 235–242 (2007).
  CASGoogle Scholar
• 54 Siddiqi NJ, Abdelhalim MA, El-Ansary AK et al. Identification of potential biomarkers of gold nanoparticle toxicity in rat brains. J. Neuroinflammation 9, 123 (2012).
  Medline CASGoogle Scholar
• 55 Kregel KC. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J. Appl. Physiol. 92(5), 2177–2186 (2002).
  Medline CASGoogle Scholar
• 56 Porter AG, Jänicke RU. Emerging roles of caspase-3 in apoptosis. Cell Death Differ. 6(2), 99–104 (1999).
  Medline CASGoogle Scholar
• 57 Li JJ, Hartono D, Ong CN, Bay B-H, Yung L-YL. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 31(23), 5996–6003 (2010).
  Medline CASGoogle Scholar
• 58 Codreanu SG, Ullery JC, Zhu J et al. Alkylation damage by lipid electrophiles targets functional protein systems. Mol. Cell Proteomics 13(3), 849–859 (2014).
  Medline CASGoogle Scholar
• 59 Jilani A, Ramotar D, Slack C et al. Molecular cloning of the human gene, PNKP, encoding a polynucleotide kinase 3’-phosphatase and evidence for its role in repair of DNA strand breaks caused by oxidative damage. J. Biol. Chem. 274(34), 24176–24186 (1999).
  Medline CASGoogle Scholar
• 60 Funk CD, FitzGerald GA. COX-2 inhibitors and cardiovascular risk. J. Cardiovasc. Pharmacol. 50(5), 470–479 (2007).
  Medline CASGoogle Scholar
• 61 Maier-Hauff K, Ulrich F, Nestler D et al. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J. Neurooncol. 103(2), 317–324 (2011).
  MedlineGoogle Scholar
• 62 Hare D, Ayton S, Bush A, Lei P. A delicate balance: iron metabolism and diseases of the brain. Front. Aging Neurosci. 5, 34 (2013).
  MedlineGoogle Scholar
• 63 Wang B, Feng WY, Wang M et al. Transport of intranasally instilled fine Fe₂O₃ particles into the brain: micro-distribution, chemical states, and histopathological observation. Biol. Trace Elem. Res. 118(3), 233–243 (2007).
  Medline CASGoogle Scholar
• 64 Wu J, Ding T, Sun J. Neurotoxic potential of iron oxide nanoparticles in the rat brain striatum and hippocampus. NeuroToxicology 34, 243–253 (2013).
  Medline CASGoogle Scholar
• 65 Kim JS, Yoon TJ, Yu KN et al. Toxicity and tissue distribution of magnetic nanoparticles in mice. Toxicol. Sci. 89(1), 338–347 (2006).
  Medline CASGoogle Scholar
• 66 Liu CH, Ren JQ, You Z et al. Noninvasive detection of neural progenitor cells in living brains by MRI. FASEB J. 26(4), 1652–1662 (2012).
  Medline CASGoogle Scholar
• 67 Jain TK, Reddy MK, Morales MA, Leslie-Pelecky DL, Labhasetwar V. Biodistribution, clearance, and biocompatibility of iron oxide magnetic nanoparticles in rats. Mol. Pharm. 5(2), 316–327 (2008).
  Medline CASGoogle Scholar
• 68 Wang J, Chen Y, Chen B et al. Pharmacokinetic parameters and tissue distribution of magnetic Fe(₃)O(₄) nanoparticles in mice. Int. J. Nanomedicine 5, 861–866 (2010).
  Medline CASGoogle Scholar
• 69 Kumari M, Rajak S, Singh SP et al. Biochemical alterations induced by acute oral doses of iron oxide nanoparticles in Wistar rats. Drug Chem. Toxicol. 36(3), 296–305 (2013).
  Medline CASGoogle Scholar
• 70 Kim Y, Kong SD, Chen LH, Pisanic TR, Jin S, Shubayev VI. in vivo nanoneurotoxicity screening using oxidative stress and neuroinflammation paradigms. Nanomed. Nanotechnol. Biol. Med. 9(7), 1057–1066 (2013).
  CASGoogle Scholar
• 71 Liochev SI, Fridovich I. The Haber–Weiss cycle – 70 years later: an alternative view. Redox Rep. Commun. Free Radic. Res. 7(1), 55–57; author reply 59–60 (2002).
  Medline CASGoogle Scholar
• 72 Manke A, Wang L, Rojanasakul Y. Mechanisms of nanoparticle-induced oxidative stress and toxicity. BioMed. Res. Int. 2013, e942916 (2013).
  MedlineGoogle Scholar
• 73 Pelicano H, Carney D, Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 7(2), 97–110 (2004).
  Medline CASGoogle Scholar
• 74 Eidi H, Joubert O, Némos C et al. Drug delivery by polymeric nanoparticles induces autophagy in macrophages. Int. J. Pharm. 422(1–2), 495–503 (2012).
  Medline CASGoogle Scholar
• 75 Arnoult D, Grodet A, Lee YJ, Estaquier J, Blackstone C. Release of OPA1 during apoptosis participates in the rapid and complete release of cytochrome c and subsequent mitochondrial fragmentation. J. Biol. Chem. 280(42), 35742–35750 (2005).
  Medline CASGoogle Scholar
• 76 Nakamura K, Nemani VM, Azarbal F et al. Direct membrane association drives mitochondrial fission by the Parkinson disease-associated protein alpha-synuclein. J. Biol. Chem. 286(23), 20710–20726 (2011).
  Medline CASGoogle Scholar
• 77 Wang H, Joseph JA. Quantifying cellular oxidative stress by dichlorofluorescein assay using microplate reader. Free Radic. Biol. Med. 27(5–6), 612–616 (1999).
  Medline CASGoogle Scholar
• 78 Lockman PR, Koziara JM, Mumper RJ, Allen DD. Nanoparticle surface charges alter blood–brain barrier integrity and permeability. J. Drug Target. 12(9–10), 635–641 (2004).
  Medline CASGoogle Scholar
• 79 Yuan ZY, Hu YL, Gao JQ. Brain localization and neurotoxicity evaluation of polysorbate 80-modified chitosan nanoparticles in rats. PLoS ONE 10(8), e0134722 (2015).
  MedlineGoogle Scholar
• 80 Hu YL, Gao JQ. Potential neurotoxicity of nanoparticles. Int. J. Pharm. 394(1–2), 115–121 (2010).
  Medline CASGoogle Scholar
• 81 Zhao M, Hu J, Zhang L et al. Study of amphotericin B magnetic liposomes for brain targeting. Int. J. Pharm. 475(1–2), 9–16 (2014).
  Medline CASGoogle Scholar
• 82 Kolter M, Ott M, Hauer C, Reimold I, Fricker G. Nanotoxicity of poly(n-butylcyano-acrylate) nanoparticles at the blood–brain barrier, in human whole blood and in vivo. J. Control. Release 197, 165–179 (2015).
  Medline CASGoogle Scholar
• 83 Paris I, Segura-Aguilar J. The role of metal ions in dopaminergic neuron degeneration in Parkinsonism and Parkinson's disease. Monatshefte Für Chem. 142(4), 365–374 (2011).
  CASGoogle Scholar
• 84 Halliwell B. Oxidative stress and neurodegeneration: where are we now? J. Neurochem. 97(6), 1634–1658 (2006).
  Medline CASGoogle Scholar
• 85 Mizushima N. Autophagy: process and function. Genes Dev. 21(22), 2861–2873 (2007).
  Medline CASGoogle Scholar
• 86 Ravikumar B, Futter M, Jahreiss L et al. Mammalian macroautophagy at a glance. J. Cell Sci. 122(Pt 11), 1707–1711 (2009).
  Medline CASGoogle Scholar
• 87 Komatsu M, Ichimura Y. Selective autophagy regulates various cellular functions. Genes Cells Devoted Mol. Cell. Mech. 15(9), 923–933 (2010).
  Medline CASGoogle Scholar
• 88 Stern ST, Adiseshaiah PP, Crist RM. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part. Fibre Toxicol. 9(1), 20 (2012).
  Medline CASGoogle Scholar
• 89 Gelino S, Hansen M. Autophagy - an emerging anti-aging mechanism. J. Clin. Exp. Pathol. 12(Suppl. 4), pii: 006 (2012).
  Google Scholar
• 90 Ichimura Y, Komatsu M. Selective degradation of p62 by autophagy. Semin. Immunopathol. 32(4), 431–436 (2010).
  MedlineGoogle Scholar
• 91 Wu YN, Yang LX, Shi XY et al. The selective growth inhibition of oral cancer by iron core-gold shell nanoparticles through mitochondria-mediated autophagy. Biomaterials 32(20), 4565–4573 (2011).
  Medline CASGoogle Scholar
• 92 Ueng TH, Kang JJ, Wang HW, Cheng YW, Chiang LY. Suppression of microsomal cytochrome P450-dependent monooxygenases and mitochondrial oxidative phosphorylation by fullerenol, a polyhydroxylated fullerene C60. Toxicol. Lett. 93(1), 29–37 (1997).
  Medline CASGoogle Scholar
• 93 Shcharbin D, Jokiel M, Klajnert B, Bryszewska M. Effect of dendrimers on pure acetylcholinesterase activity and structure. Bioelectrochem. Amst. Neth. 68(1), 56–59 (2006).
  Medline CASGoogle Scholar
• 94 Ravikumar B, Sarkar S, Davies JE et al. Regulation of mammalian autophagy in physiology and pathophysiology. Physiol. Rev. 90(4), 1383–1435 (2010).
  Medline CASGoogle Scholar
• 95 Bellettato CM, Scarpa M. Pathophysiology of neuropathic lysosomal storage disorders. J. Inherit. Metab. Dis. 33(4), 347–362 (2010).
  Medline CASGoogle Scholar
• 96 Aldenhoven M, Sakkers RJB, Boelens J, de Koning TJ, Wulffraat NM. Musculoskeletal manifestations of lysosomal storage disorders. Ann. Rheum. Dis. 68(11), 1659–1665 (2009).
  Medline CASGoogle Scholar
• 97 Nel AE, Mädler L, Velegol D et al. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 8(7), 543–557 (2009).
  Medline CASGoogle Scholar
• 98 Rivera-Gil P, Jimenez de Aberasturi D, Wulf V et al. The challenge to relate the physicochemical properties of colloidal nanoparticles to their cytotoxicity. Acc. Chem. Res. 46(3), 743–749 (2013).
  Medline CASGoogle Scholar
• 99 Hussain S, Thomassen LC, Ferecatu I et al. Carbon black and titanium dioxide nanoparticles elicit distinct apoptotic pathways in bronchial epithelial cells. Part. Fibre Toxicol. 7, 10 (2010).
  MedlineGoogle Scholar
• 100 Meunier E, Coste A, Olagnier D et al. Double-walled carbon nanotubes trigger IL-1β release in human monocytes through NLRP3 inflammasome activation. Nanomed. Nanotechnol. Biol. Med. 8(6), 987–995 (2012).
  CASGoogle Scholar
• 101 Franchi L, Eigenbrod T, Muñoz-Planillo R, Nuñez G. The inflammasome: a caspase-1-activation platform that regulates immune responses and disease pathogenesis. Nat. Immunol. 10(3), 241–247 (2009).
  Medline CASGoogle Scholar
• 102 Hamilton RF, Wu N, Porter D, Buford M, Wolfarth M, Holian A. Particle length-dependent titanium dioxide nanomaterials toxicity and bioactivity. Part. Fibre Toxicol. 6, 35 (2009).
  MedlineGoogle Scholar
• 103 Lunov O, Syrovets T, Loos C et al. Amino-functionalized polystyrene nanoparticles activate the NLRP3 inflammasome in human macrophages. ACS Nano 5(12), 9648–9657 (2011).
  Medline CASGoogle Scholar
• 104 Futerman AH, van Meer G. The cell biology of lysosomal storage disorders. Nat. Rev. Mol. Cell Biol. 5(7), 554–565 (2004).
  Medline CASGoogle Scholar
• 105 Kroemer G, Jäättelä M. Lysosomes and autophagy in cell death control. Nat. Rev. Cancer 5(11), 886–897 (2005).
  Medline CASGoogle Scholar
• 106 Loos B, Engelbrecht AM, Lockshin RA, Klionsky DJ, Zakeri Z. The variability of autophagy and cell death susceptibility: unanswered questions. Autophagy 9(9), 1270–1285 (2013).
  Medline CASGoogle Scholar
• 107 Harhaji L, Isakovic A, Raicevic N et al. Multiple mechanisms underlying the anticancer action of nanocrystalline fullerene. Eur. J. Pharmacol. 568(1–3), 89–98 (2007).
  Medline CASGoogle Scholar
• 108 Stern ST, Zolnik BS, McLeland CB, Clogston J, Zheng J, McNeil SE. Induction of autophagy in porcine kidney cells by quantum dots: a common cellular response to nanomaterials? Toxicol. Sci. 106(1), 140–152 (2008).
  Medline CASGoogle Scholar
• 109 Chen Y, Yang L, Feng C, Wen L-P. Nano neodymium oxide induces massive vacuolization and autophagic cell death in non-small cell lung cancer NCI-H460 cells. Biochem. Biophys. Res. Commun. 337(1), 52–60 (2005).
  Medline CASGoogle Scholar
• 110 Seleverstov O, Zabirnyk O, Zscharnack M et al. Quantum dots for human mesenchymal stem cells labeling. A size-dependent autophagy activation.. Nano Lett. 6(12), 2826–2832 (2006).
  Medline CASGoogle Scholar
• 111 He C, Klionsky DJ. Regulation mechanisms and signalling pathways of autophagy. Annu. Rev. Genet. 43, 67–93 (2009).
  Medline CASGoogle Scholar
• 112 Calzolai L, Franchini F, Gilliland D, Rossi F. Protein–nanoparticle interaction: identification of the ubiquitin–gold nanoparticle interaction site. Nano Lett. 10(8), 3101–3105 (2010).
  Medline CASGoogle Scholar
• 113 Li H, Li Y, Jiao J, Hu HM. Alpha-alumina nanoparticles induce efficient autophagy-dependent cross-presentation and potent antitumour response. Nat. Nanotechnol. 6(10), 645–650 (2011).
  Medline CASGoogle Scholar
• 114 Zheng YT, Shahnazari S, Brech A, Lamark T, Johansen T, Brumell JH. The adaptor protein p62/SQSTM1 targets invading bacteria to the autophagy pathway. J. Immunol. Baltim. MD 183(9), 5909–5916 (2009).
  Medline CASGoogle Scholar
• 115 Mizushima N, Noda T, Ohsumi Y. Apg16p is required for the function of the Apg12p-Apg5p conjugate in the yeast autophagy pathway. EMBO J. 18(14), 3888–3896 (1999).
  Medline CASGoogle Scholar
• 116 Berry CC, Wells S, Charles S, Curtis ASG. Dextran and albumin derivatised iron oxide nanoparticles: influence on fibroblasts in vitro. Biomaterials. 24(25), 4551–4557 (2003).
  Medline CASGoogle Scholar
• 117 Gupta AK, Gupta M, Yarwood SJ, Curtis ASG. Effect of cellular uptake of gelatin nanoparticles on adhesion, morphology and cytoskeleton organisation of human fibroblasts. J. Control. Release 95(2), 197–207 (2004).
  Medline CASGoogle Scholar
• 118 Goldberg AL, Dice JF. Intracellular protein degradation in mammalian and bacterial cells. Annu. Rev. Biochem. 43(0), 835–869 (1974).
  Medline CASGoogle Scholar
• 119 Xiong R, Siegel D, Ross D. The activation sequence of cellular protein handling systems after proteasomal inhibition in dopaminergic cells. Chem. Biol. Interact. 204(2), 116–124 (2013).
  Medline CASGoogle Scholar
• 120 Muchowski PJ, Wacker JL. Modulation of neurodegeneration by molecular chaperones. Nat. Rev. Neurosci. 6(1), 11–22 (2005).
  Medline CASGoogle Scholar
• 121 Lehman NL. The ubiquitin proteasome system in neuropathology. Acta Neuropathol. (Berl.) 118(3), 329–347 (2009).
  Medline CASGoogle Scholar
• 122 Ventruti A, Cuervo AM. Autophagy and neurodegeneration. Curr. Neurol. Neurosci. Rep. 7(5), 443–451 (2007).
  Medline CASGoogle Scholar
• 123 Komatsu M, Waguri S, Chiba T et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441(7095), 880–884 (2006).
  Medline CASGoogle Scholar
• 124 Olzmann JA, Chin L-S. Parkin-mediated K63-linked polyubiquitination: a signal for targeting misfolded proteins to the aggresome-autophagy pathway. Autophagy 4(1), 85–87 (2008).
  Medline CASGoogle Scholar
• 125 Chin LS, Olzmann JA, Li L. Parkin-mediated ubiquitin signalling in aggresome formation and autophagy. Biochem. Soc. Trans. 38(Pt 1), 144 (2010).
  Medline CASGoogle Scholar
• 126 Chari RVJ. Targeted cancer therapy: conferring specificity to cytotoxic drugs. Acc. Chem. Res. 41(1), 98–107 (2008).
  Medline CASGoogle Scholar
• 127 Lalatsa A, Moreira Leite D, Pilkington GJ. Nanomedicines and the future of glioma. Oncol. News 10(2), 51–57 (2015).
  Google Scholar
• 128 Taggart LE, McMahon SJ, Currell FJ, Prise KM, Butterworth KT. The role of mitochondrial function in gold nanoparticle mediated radiosensitisation. Cancer Nanotechnol. 5(1), 5 (2014).
  MedlineGoogle Scholar
• 129 Khan MI, Mohammad A, Patil G, Naqvi SAH, Chauhan LKS, Ahmad I. Induction of ROS, mitochondrial damage and autophagy in lung epithelial cancer cells by iron oxide nanoparticles. Biomaterials 33(5), 1477–1488 (2012).
  Medline CASGoogle Scholar
• 130 Zhou SF. Structure, function and regulation of P-glycoprotein and its clinical relevance in drug disposition. Xenobiotica 38(7–8), 802–832 (2008).
  Medline CASGoogle Scholar
• 131 Rosenfeldt MT, Ryan KM. The role of autophagy in tumour development and cancer therapy. Expert Rev. Mol. Med. 11, e36 (2009).
  MedlineGoogle Scholar
• 132 Amaravadi RK, Lippincott-Schwartz J, Yin XM et al. Principles and current strategies for targeting autophagy for cancer treatment. Clin. Cancer Res. 17(4), 654–666 (2011).
  Medline CASGoogle Scholar
• 133 Wu YN, Chen DH, Shi X-Y et al. Cancer-cell-specific cytotoxicity of non-oxidized iron elements in iron core-gold shell NPs. Nanomedicine 7(4), 420–427 (2011).
  MedlineGoogle Scholar
• 134 Wang S, Li Y, Fan J et al. The role of autophagy in the neurotoxicity of cationic PAMAM dendrimers. Biomaterials 35(26), 7588–7597 (2014).
  Medline CASGoogle Scholar
• 135 Nixon RA, Wegiel J, Kumar A et al. Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J. Neuropathol. Exp. Neurol. 64(2), 113–122 (2005).
  MedlineGoogle Scholar
• 136 Anglade P, Vyas S, Javoy-Agid F et al. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol. 12(1), 25–31 (1997).
  Medline CASGoogle Scholar
• 137 Xilouri M, Stefanis L. Autophagic pathways in Parkinson disease and related disorders. Expert Rev. Mol. Med. 13, e8 (2011).
  MedlineGoogle Scholar
• 138 Ravikumar B, Vacher C, Berger Z et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36(6), 585–595 (2004).
  Medline CASGoogle Scholar
• 139 Hara T, Nakamura K, Matsui M et al. Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441(7095), 885–889 (2006).
  Medline CASGoogle Scholar
• 140 Boland B, Kumar A, Lee S et al. Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. J. Neurosci. 28(27), 6926–6937 (2008).
  Medline CASGoogle Scholar
• 141 Tanida I, Yamasaki M, Komatsu M, Ueno T. The FAP motif within human ATG7, an autophagy-related E1-like enzyme, is essential for the E2-substrate reaction of LC3 lipidation. Autophagy 8(1), 88–97 (2012).
  Medline CASGoogle Scholar
• 142 UK CR. Statistics and outlook for brain tumours (2015). www.cancerresearchuk.org/about-cancer/type/brain-tumour/treatment/statistics-and-outlook-for-brain-tumours#glioma.
  Google Scholar