Abstract
Nanomaterials have revolutionized many scientific fields and are widely applied to address environmental problems and to develop novel health care strategies. However, their mechanism of action is still poorly understood. Several nanomaterials for medical applications are based on quantum dots (QDs). Despite their amazing physico-chemical properties, quantum dots display significant adverse effects. In the present study, the effects of QDs on the motor nervous system of nematodes Caenorhabditis elegans have been investigated as a non-mammalian alternative model. We also explored the possibility of modifying the toxicity of QDs by coating with a cell-penetrating peptide gH625 and thus we analysed the effects determined by QDs-gH625 complexes on the nematodes. With this work, we have demonstrated, by in vivo experiments, that the peptide gH625 is able to reduce the side effects of metallic nanoparticle making them more suitable for medical applications.
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References
Acosta C et al. (2018) Toxicological assessment of mesoporous silica particles in the nematode Caenorhabditis elegans. Environ Res 166:61–70. https://doi.org/10.1016/j.envres.2018.05.018
de Alteriis E et al. (2018) Polymicrobial antibiofilm activity of the membranotropic peptide gH625 and its analogue. Microb Pathog 125:189–195. https://doi.org/10.1016/j.micpath.2018.09.027
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Carberry TP et al. (2012) Dendrimer functionalization with a membrane-interacting domain of herpes simplex virus type 1: towards intracellular delivery. Chemistry 18:13678–13685. https://doi.org/10.1002/chem.201202358
Chen N et al. (2012) The cytotoxicity of cadmium-based quantum dots. Biomaterials 33:1238–1244. https://doi.org/10.1016/j.biomaterials.2011.10.070
Cho SJ et al. (2007) Long-term exposure to CdTe quantum dots causes functional impairments in live cells. Langmuir 23:1974–1980. https://doi.org/10.1021/la060093j
Contreras EQ et al. (2013) Toxicity of quantum dots and cadmium salt to Caenorhabditis elegans after multigenerational exposure. Environ Sci Technol 47:1148–1154. https://doi.org/10.1021/es3036785
Falanga A et al. (2011) A peptide derived from herpes simplex virus type 1 glycoprotein H: membrane translocation and applications to the delivery of quantum dots. Nanomedicine 7:934. https://doi.org/10.1016/j.nano.2011.04.009
Falanga A et al. (2018) Enhanced uptake of gH625 by blood brain barrier compared to liver in vivo: characterization of the mechanism by an in vitro model and implications for delivery. Sci Rep 8:13836–13836. https://doi.org/10.1038/s41598-018-32095-w
Falanga A, Cantisani M, Pedone C, Galdiero S (2009) Membrane fusion and fission: enveloped viruses. Protein Pept Lett 16:751–759
Falanga A, Galdiero M, Galdiero S (2015) Membranotropic cell penetrating peptides: the outstanding journey. Int J Mol Sci 16:25323–25337. https://doi.org/10.3390/ijms161025323
Finkel T, Holbrook NJ (2000) Oxidants, oxidative stress and the biology of ageing. Nature 408:239. https://doi.org/10.1038/35041687
Fridovich I (1995) Superoxide radical and superoxide dismutases. Annu Rev Biochem 64:97–112. https://doi.org/10.1146/annurev.bi.64.070195.000525
Galdiero E et al. (2017) Daphnia magna and xenopus laevis as in vivo models to probe toxicity and uptake of quantum dots functionalized with gH625. Int J Nanomed 12:2717–2731. https://doi.org/10.2147/ijn.s127226
Galdiero S et al. (2010) The presence of a single N-terminal histidine residue enhances the fusogenic properties of a membranotropic peptide derived from herpes simplex virus type 1 glycoprotein H. J Biol Chem 285:17123–17136. https://doi.org/10.1074/jbc.M110.114819
Galdiero S et al. (2012) Structure and orientation of the gH625-644 membrane interacting region of herpes simplex virus type 1 in a membrane mimetic system. Biochemistry 51:3121–3128. https://doi.org/10.1021/bi201589m
Galdiero S, Falanga A, Morelli G, Galdiero M (2015) gH625: a milestone in understanding the many roles of membranotropic peptides. Biochim Biophys Acta 1848:16–25. https://doi.org/10.1016/j.bbamem.2014.10.006
Galstyan A et al. (2019) Blood-brain barrier permeable nano immunoconjugates induce local immune responses for glioma therapy. Nat Commun 10:3850. https://doi.org/10.1038/s41467-019-11719-3
Gao X et al. (2005) In vivo molecular and cellular imaging with quantum dots. Curr Opin Biotechnol 16:63–72. https://doi.org/10.1016/j.copbio.2004.11.003
Garsin DA et al. (2003) Long-lived C. elegans daf-2 mutants are resistant to bacterial pathogens. Science 300:1921. https://doi.org/10.1126/science.1080147
Guarnieri, D et al. (2015) Surface decoration with gH625-membranotropic peptides as a method to escape the endo-lysosomal compartment and reduce nanoparticle toxicity. Nanotechnology 26. https://doi.org/10.1088/0957-4484/26/41/415101
Hekimi S, Guarente L (2003) Genetics and the specificity of the aging process. Science 299:1351. https://doi.org/10.1126/science.1082358
Hodgkin J, Doniach T (1997) Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146:149–164
Hsu P-CL, O’Callaghan M, Al-Salim N, Hurst MRH (2012) Quantum dot nanoparticles affect the reproductive system of Caenorhabditis elegans. Environ Toxicol Chem 31:2366–2374. https://doi.org/10.1002/etc.1967
Iachetta G et al. (2019) gH625-liposomes as tool for pituitary adenylate cyclase-activating polypeptide brain delivery. Sci Rep. 9:9183–9183. https://doi.org/10.1038/s41598-019-45137-8
Jamieson T et al. (2007) Biological applications of quantum dots. Biomaterials 28:4717–4732. https://doi.org/10.1016/j.biomaterials.2007.07.014
Khosravi-Katuli K et al. (2018) Effects of ZnO nanoparticles in the Caspian roach (Rutilus rutilus caspicus). Sci Total Environ 626:30–41. https://doi.org/10.1016/j.scitotenv.2018.01.085
Li D et al. (2019) Cross-linked poly(ethylene glycol) shells for nanoparticles: enhanced stealth effect and colloidal stability. Langmuir 35:8799–8805. https://doi.org/10.1021/acs.langmuir.9b01325
Li Y et al. (2013) High concentration of vitamin E decreases thermosensation and thermotaxis learning and the underlying mechanisms in the nematode Caenorhabditis elegans. PLoS One 8:e71180. https://doi.org/10.1371/journal.pone.0071180
Ma H, Bertsch PM, Glenn TC, Kabengi NJ, Williams PL (2009) Toxicity of manufactured zinc oxide nanoparticles in the nematode Caenorhabditis elegans. Environ Toxicol Chem 28:1324–1330. https://doi.org/10.1897/08-262.1
Mallo GV et al. (2002) Inducible antibacterial defense system in C. elegans. Curr Biol 12:1209–1214. https://doi.org/10.1016/S0960-9822(02)00928-4
Martin-Serrano, A, Gomez, R, Ortega, P & de la Mata, FJ (2019) Nanosystems as vehicles for the delivery of antimicrobial peptides (AMPs). Pharmaceutics 11. https://doi.org/10.3390/pharmaceutics11090448
McMahan RS, Lee V, Parks WC, Kavanagh TJ, Eaton DL (2014) In vitro approaches to assessing the toxicity of quantum dots. Methods Mol Biol 1199:155–163. https://doi.org/10.1007/978-1-4939-1280-3_12
Medintz IL, Uyeda HT, Goldman ER, Mattoussi H (2005) Quantum dot bioconjugates for imaging, labelling and sensing. Nat Mater 4:435. https://doi.org/10.1038/nmat1390
Oral R, Pagano G, Siciliano A, Toscanesi M, Gravina M, Di Nunzio A, Palumbo A, Thomas PJ, Tommasi F, Burić P, Lyons DM, Guida M, Trifuoggi M (2019) Soil pollution and toxicity in an area affected by emissions from a bauxite processing plant and a power plant in Gardanne (southern France). Ecotoxicol Environ Saf 170:55–61. https://doi.org/10.1016/j.ecoenv.2018.11.122
Pellico, J et al. (2019) Unambiguous detection of atherosclerosis using bioorthogonal nanomaterials. Nanomedicine https://doi.org/10.1016/j.nano.2018.12.015
Qu Y et al. (2011) Full assessment of fate and physiological behavior of quantum dots utilizing Caenorhabditis elegans as a model organism. Nano Lett 11:3174–3183. https://doi.org/10.1021/nl201391e
Roh J-Y, Park Y-K, Park K, Choi J (2010) Ecotoxicological investigation of CeO2 and TiO2 nanoparticles on the soil nematode Caenorhabditis elegans using gene expression, growth, fertility, and survival as endpoints. Environ Toxicol Pharmacol 29:167–172. https://doi.org/10.1016/j.etap.2009.12.003
Troemel ER et al. (2006) p38 MAPK regulates expression of immune response genes and contributes to longevity in C. elegans. PLOS Genet 2:e183. https://doi.org/10.1371/journal.pgen.0020183
Ulusoy M et al. (2016) Evaluation of CdTe/CdS/ZnS core/shell/shell quantum dot toxicity on three-dimensional spheroid cultures. Toxicol Res 5:126–135. https://doi.org/10.1039/c5tx00236b
Valiante S et al. (2015) Peptide gH625 enters into neuron and astrocyte cell lines and crosses the blood-brain barrier in rats. Int J Nanomed 10:1885–1898. https://doi.org/10.2147/ijn.s77734
Wang H, Wick RL, Xing B (2009) Toxicity of nanoparticulate and bulk ZnO, Al2O3 and TiO2 to the nematode Caenorhabditis elegans. Environ Pollut 157:1171–1177. https://doi.org/10.1016/j.envpol.2008.11.004
Winnik FM, Maysinger D (2013) Quantum dot cytotoxicity and ways to reduce it. Acc Chem Res 46:672–680. https://doi.org/10.1021/ar3000585
Wu, L et al. (2019) Enzyme-responsive multifunctional peptide coating of gold nanorods improves tumor targeting and photothermal therapy efficacy. Acta Biomater. https://doi.org/10.1016/j.actbio.2019.01.026
Zhao Y et al. (2015) Quantum dots exposure alters both development and function of D-type GABAergic motor neurons in nematode Caenorhabditis elegans. Toxicol Res 4:399–408. https://doi.org/10.1039/c4tx00207e
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Galdiero, E., Siciliano, A., Lombardi, L. et al. Quantum dots functionalized with gH625 attenuate QDs oxidative stress and lethality in Caenorhabditis elegans: a model system. Ecotoxicology 29, 156–162 (2020). https://doi.org/10.1007/s10646-019-02158-3
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DOI: https://doi.org/10.1007/s10646-019-02158-3