The interaction of nanostructured antimicrobials with biological systems: Cellular uptake, trafficking and potential toxicity

Food Science and Human Wellness

Volumn 9, Issue 1, 2020, Pages 8-20

  Brandelli, Adriano ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

Active packaging; Antimicrobial; Food safety; Nanobiotechnology; Nanoparticle toxicity

Indexed keywords

EID: 85077392395     PISSN: None     EISSN: 22134530     Source Type: Journal    
DOI: 10.1016/j.fshw.2019.12.003     Document Type: Review

References (117)

1. Cushen, M., Kerry, J., Morris, M., et al. Nanotechnologies in the food industry - recent developments, risks and regulation. Trends Food Sci. Technol. 24 (2012), 30–46.
2. Lee, B., Yun, Y., Park, K., Smart nanoparticles for drug delivery: boundaries and opportunities. Chem. Eng. Sci. 125 (2015), 158–164.
3. Kane, R.V., Stroock, A.D., Nanobiotechnology: protein-nanomaterial interactions. Biotechnol. Progr. 23 (2007), 316–319.
4. Sekhon, B.S., Food nanotechnology - an overview. Nanotechnol. Sci. Appl. 3 (2010), 1–15.
5. Dasgupta, N., Ranjan, S., Mundekkad, D., et al. Nanotechnology in agri-food: from field to plate. Food Res. Int. 69 (2015), 381–400.
6. McClements, D.J., Nanoscale nutrient delivery systems for food applications: Improving bioactive dispersibility, stability, and bioavailability. J. Food Sci. 80 (2015), 1602–1611.
7. Lopes, N.A., Brandelli, A., Nanostructures for delivery of natural antimicrobials in food. Crit. Rev. Food Sci. Nutr. 58 (2018), 2202–2212.
8. McClements, D.J., Xiao, H., Is nano safe in foods? Establishing the factors impacting the gastrointestinal fate and toxicity of organic and inorganic food-grade nanoparticles. Sci. Food, 1, 2017, 6.
9. Brandelli, A., Lopes, N.A., Boelter, J.F., Food applications of nanostructured antimicrobials. Grumezescu, A.M., (eds.) Food Preservation, 2017, Academic Press, London, 35–74.
10. Brandelli, A., Brum, L.F.W., Santos, J.H.Z., Nanostructured bioactive compounds for ecological food packaging. Environ. Chem. Lett. 15 (2017), 193–204.
11. Brandelli, A., Taylor, T.M., Nanostructured and nanoencapsulated natural antimicrobials for use in food products. Taylor, T.M., (eds.) Handbook of Natural Antimicrobials for Food Safety and Quality, 2015, Woodhead Publishing, Oxford, 229–257.
12. CLSI, Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically, CLSI Standard M07. 2018, Clinical and Laboratory Standards Institute, Wayne, PA.
13. EUCAST, Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin. Microbiol. Infect. 9 (2003), 9–15.
14. 2. Toxicol. In Vitro 25 (2011), 2147–2151.
15. Prabhu, S., Poulose, E.K., Silver nanoparticles: mechanism of antimicrobial action, synthesis, medical applications, and toxicity effects. Int. Nano Lett., 2, 2012, 32.
16. Rai, M., Ingle, A.P., Gupta, I., et al. Bioactivity of noble metal nanoparticles decorated with biopolymers and their applications in drug delivery. Int. J. Pharm. 496 (2015), 159–172.
17. Slavin, Y.N., Asnis, J., Häfeli, U.O., et al. Metal nanoparticles: understanding the mechanisms behind antibacterial activity. Int. J. Nanobiotechnology Pharm., 15, 2017, 65.
18. Sohal, I.K., O'Fallon, K.S., Gaines, P., et al. Ingested engineered nanomaterials: state of science in nanotoxicity testing and future research needs. Part. Fibre Toxicol., 15, 2018, 29.
19. Fröhlich, E., Roblegg, E., Models for oral uptake of nanoparticles in consumer products. Toxicology 27 (2012), 10–17.
20. Bouwmeester, H., Dekkers, S., Noordam, M.Y., et al. Review of health safety aspects of nanotechnologies in food production. Regul. Toxicol. Pharmacol. 53 (2009), 52–62.
21. Cao, Y., Li, J., Liu, F., et al. Consideration of interaction between nanoparticles and food components for the safety assessment of nanoparticles following oral exposure: a review. Environ. Toxicol. Pharmacol. 46 (2016), 206–210.
22. Shang, L., Nienhaus, K., Nienhaus, G.U., Engineered nanoparticles interacting with cells: size matters. J. Nanobiotechnol., 12, 2014, 5.
23. Zhang, X.Q., Xu, X., Bertrand, N., et al. Interactions of nanomaterials and biological systems: implications to personalized medicine. Adv. Drug Deliv. Rev. 64 (2012), 1363–1384.
24. Lundqvist, M., Augustsson, C., Lilja, M., et al. The nanoparticle protein corona formed in human blood or human blood fractions. PLoS One, 12, 2017, e0175871.
25. Saha, K., Moyano, D.F., Rotello, V.M., Protein corona suppress the hemolytic activity of hydrophilic and hydrophobic nanoparticles. Mat. Horizons 1 (2014), 102–105.
26. Holpuch, A.S., Hummel, G.J., Tong, M., et al. Nanoparticles for local drug delivery to the oral mucosa: proof of principle studies. Pharm. Res. 27 (2010), 1224–1236.
27. Lai, S.K., O'Hanlon, D.E., Harrold, S., et al. Rapid transport of large polymeric nanoparticles in fresh undiluted human mucus. Proc. Natl. Acad. Sci. U.S.A. 104 (2007), 1482–1487.
28. Lai, S.K., Wang, Y.Y., Hanes, J., Mucus-penetrating nanoparticles for drug and gene delivery to mucosal tissues. Adv. Drug Deliv. Rev. 61 (2009), 158–171.
29. Thanki, K., Gangwal, R.P., Sangamwar, A.T., et al. Oral delivery of anticancer drugs: challenges and opportunities. J. Control. Release 170 (2013), 15–40.
30. Yue, Z.G., Wei, W., Lv, P.P., et al. Surface charge affects cellular uptake and intracellular trafficking of chitosan-based nanoparticles. Biomacromolecules 12 (2011), 2440–2446.
31. Yun, Y., Cho, Y.W., Park, K., Nanoparticles for oral delivery: targeted nanoparticles with peptidic ligands for oral protein delivery. Adv. Drug Deliv. Rev. 65 (2013), 822–832.
32. Malheiros, P.S., Daroit, D.J., Silveira, N.P., et al. Effect of nanovesicle-encapsulated nisin on growth of Listeria monocytogenes in milk. Food Microbiol. 27 (2010), 175–178.
33. Yang, W., Peters, J.I., R.O. Williams III, Inhalated nanoparticles - a current review. Int. J. Pharm. 356 (2008), 239–247.
34. Bilia, A.R., Guccione, C., Isacchi, B., et al. Essential oils loadedin nanosystems: a developing strategy for successful therapeutic approach. Evid Based Complemet Altern Med, 2014, 2014, 651593.
35. Palmer, B.C., DeLouise, L.A., Nanoparticle-enabled transdermal drug delivery system for enhanced dose control and tissue targeting. Molecules, 21, 2016, 1719.
36. Faraji, A.H., Wipf, P., Nanoparticles in cell drug delivery. Bioorg. Med. Chem. 17 (2009), 2950–2962.
37. Lundy, D.J., Chen, K.H., Toh, E.K.W., et al. Distribution of systemically administered nanoparticles reveals a size-dependent effect immediately following cardiac ischaemia-reperfusion injury. Sci. Rep., 6, 2016, 25613.
38. Letchford, K., Burt, H., A review of the formation and classification of amphiphilic block copolymer nanoparticulate structures: micelles, nanospheres, nanocapsules and polymersomes. Eur. J. Pharm. Biopharm. 65 (2007), 259–269.
39. Jiang, W., Kim, B.Y.S., Rutka, J.T., et al. Nanoparticle-mediated cellular response is size-dependent. Nature Nanotechnol. 3 (2008), 145–150.
40. Faroozandeh, P., Aziz, A.A., Insight into cellular uptake and intracellular trafficking of nanoparticles. Nanoscale Res. Lett., 13, 2018, 339.
41. Mitchell, M.J., Chen, C.S., Ponmudi, V., et al. E-selectin liposomal and nanotube-targeted delivery of doxorubicin to circulating tumor cells. J. Control. Release 160 (2012), 609–617.
42. Delehantry, J.B., Boeneman, K., Bradburne, C.E., et al. Peptides for specific intracellular delivery and targeting nanoparticles: implications for developing nanoparticle-mediated drug delivery. Ther. Deliv. 1 (2010), 411–433.
43. Trbojevich, R.A., Torres, A.M., Biological synthesis, pharmacokinetics and toxicity of different metal nanoparticles. Rai, M., Shegokar, R., (eds.) Metal Nanoparticles in Pharma, 2018, Springer, Cham, 451–468.
44. Park, K., Toxicokinetic differences and toxicities of silver nanoparticles and silver ions in rats after single oral administration. J. Toxicol. Environ. Health A 76 (2013), 1246–1260.
45. Park, K., Park, E.J., Chun, I.K., et al. Bioavailability and toxicokinetics of citrate-coated silver nanoparticles in rats. Arch. Pharm. Res. 34 (2011), 153–158.
46. Pujalté, I., Dieme, D., Haddad, S., et al. Toxicokinetics of titanium dioxide (TiO2) nanoparticles after inhalation in rats. Toxicol. Lett. 265 (2017), 77–85.
47. Chung, H.E., Yu, J., Baek, M., et al. Toxicokinetics of zinc oxide nanoparticles in rats. J. Phys. Conf. Ser., 429, 2013, 012037.
48. + uptake. J. Membr. Biol. 236 (2010), 15–26.
49. Vaucher, R.A., Motta, A.S., Brandelli, A., Evaluation of the in vitro cytotoxicity of the antimicrobial peptide P34. Cell Biol. Int. 34 (2010), 317–323.
50. Radaic, A., Pugliese, G.O., Campese, G.C., et al. Studying the interactions between nanoparticles and biological systems. Quim(November), 2016, 1236–1244.
51. Preta, G., Cronin, J.G., Sheldon, I.M., Dynasore - not just a dynamin inhibitor. Cell Commun. Signal, 13, 2015, 24.
52. Mayor, S., Parton, R.G., Donaldson, J.G., Clathrin-independent pathways of endocytosis. Cold Spring Harb. Perspect. Biol., 6, 2014, a016758.
53. Rosendale, M., Perrais, D., Imaging in focus: imaging the dynamics of endocytosis. Int. J. Biochem. Cell Biol. 93 (2017), 41–45.
54. Zhang, S., Gao, H., Bao, G., Physical principles of nanoparticle cellular endocytosis. ACS Nano 9 (2015), 8655–8671.
55. Contini, C., Schneemilch, M., Gaisford, S., et al. Nanoparticle-membrane interactions. J. Exp. Nanosci. 13 (2018), 62–81.
56. Deserno, M., Elastic deformation of a fluid membrane upon colloid binding. Phys. Rev. E, 69, 2004, 031903.
57. Kaksonen, M., Roux, A., Mechanisms of chlatrin-mediated endocytosis. Nature Rev. Mol. Cell. Biol. 19 (2018), 313–326.
58. Willmann, W., Dringen, R., Monitoring the cytoskeleton-dependent intracellular trafficking of fluorescent iron oxide nanoparticles by nanoparticle pulse-chase experiments in C6 glioma cells. Neurochem. Res. 43 (2018), 2055–2071.
59. Iversen, T.G., Skotland, T., Sandvig, K., Endocytosis and intracellular transport of nanoparticles: present knowledge and needs for future studies. Nano Today 6 (2011), 176–185.
60. Ivanov, A.I., Pharmacological inhibitors of endocytic pathways: is it specific enough to be useful?. Methods Mol. Biol. 440 (2008), 15–33.
61. Ding, L., Yao, C., Yin, X., et al. Size, shape and protein corona determine cellular uptake and removal mechanisms of gold nanoparticles. Small, 14, 2018, 1801451.
62. Wu, M., Guo, H., Liu, L., et al. Size-dependent cellular uptake and localization profiles of silver nanoparticles. Int. J. Nanomedicine 14 (2019), 4247–4259.
63. Jiang, X.M., Wang, L.M., Chen, C.Y., Cellular uptake, intracellular trafficking and biological responses of gold nanoparticles. J. Chin. Chem. Soc. 58 (2011), 273–281.
64. Invitrogen, Probes for endocytosis, receptors and ion channels. Molecular Probes Handbook, 11th edition, 2010, 739–772.
65. Houtari, J., Helenius, A., Endosome maturation. EMBO J. 30 (2011), 3481–3500.
66. Zhang, J., Chang, D., Yang, Y., et al. Systematic investigation on the intracellular trafficking network of polymeric nanoparticles. Nanoscale 9 (2017), 3269–3282.
67. Peñaloza, J.P., Marquez-Miranda, V., Cabana-Brunod, M., et al. Intracellular trafficking and cellular uptake mechanism of PHBV nanoparticles for targeted delivery in epithelial cell lines. Int. J. Nanobiotechnology Pharm., 15, 2017, 1.
68. Sun, X., Cheng, C., Zhang, J., et al. Intracellular trafficking network and autophagy of PHBHHx nanoparticles and their implications for drug delivery. Sci. Rep., 9, 2019, 9585.
69. Shukla, R., Bansal, V., Chaudhary, M., et al. Biocompatibility of gold nanoparticles and their endocytic fate inside the cellular compartment: a microscopic overview. Langmuir 21 (2005), 10644–10654.
70. Cupic, K.I., Rennick, J.J., Johnston, A.P.R., et al. Controlling endosomal escape using nanoparticle composition: current progress and future perspectives. Nanomedicine 14 (2019), 215–223.
71. Smith, S.A., Shelby, L.I., Johnston, A.P.R., et al. The endosomal escape of nanoparticles: towards more efficient cellular delivery. Bioconjugate Chem. 30 (2019), 263–272.
72. Schültz, I., López-Hernández, T., Gao, Q., et al. Lysosomal dysfunction caused by cellular accumulation of silica nanoparticles. J. Biol. Chem. 291 (2016), 14170–14184.
73. Tiede, K., Boxall, A.B.A., Tear, S.P., et al. Detection and characterization of engineered nanoparticles in food and the environment. Food Addit. Contam. 25 (2008), 795–821.
74. Vass, I.Z., Deák, Z., Paul, K., et al. Interaction of nanoparticles with biological systems. Acta Biol Szeged 59 (2015), 225–245.
75. Brandelli, A., Toxicity and safety evaluation of nanoclays. Rai, M., Biswas, J.K., (eds.) Nanomaterials: Ecotoxicity, Safety, and Public Perception, 2018, Springer, Cham, 57–76.
76. Francis, A.P., Davasena, T., Toxicity of carbon nanotubes: a review. Toxicol. Ind. Health 34 (2018), 200–210.
77. Kunzmann, A., Andersson, B., Thurnherr, T., et al. Toxicology of engineered nanomaterials: focus on biocompatibility, biodistribution and biodegradation. Biochim. Biophys. Acta 1810 (2011), 361–373.
78. Römer, I., Briffa, S.M., Dasilva, Y.A.R., et al. Impact of particle size, oxidation state and capping agent of different cerium dioxide nanoparticles on the phosphate-induced transformations at different pH and concentration. PLoS One, 14, 2019, e0217483.
79. Vandebriel, R.J., de Jong, W.H., A review of mammalian toxicity of ZnO nanoparticles. Nanotechnol. Sci. Appl. 5 (2012), 61–71.
80. Pandurangan, M., Kim, D.H., In vitro toxicity of zinc oxide nanoparticles: a review. J. Nanopart. Res., 17, 2015, 158.
81. Warheit, D.B., Hazard and risk assessment strategies for nanoparticles exposure: how far we come in the past 10 years?. F1000 Res., 7, 2018, 376.
82. Geiser, M., Jeannet, N., Fierz, M., et al. Evaluation adverse effects of inhaled nanoparticles by realistic in vitro technology. Nanomaterials, 7, 2017, 49.
83. Sukhanova, A., Bozrova, S., Sokolov, P., et al. Dependence of nanoparticle toxicity on their physical and chemical properties. Nanoscale Res. Lett., 13, 2018, 44.
84. Mourdikoudis, S., Pallares, R.M., Thanh, N.T.K., Characterization techniques for nanoparticles: comparison and complementarity upon studying nanoparticle properties. Nanoscale 10 (2018), 12871–12934.
85. Ponce, A., Mejía-Rosales, S., José-Yacamán, M., Scanning transmission electron microscopy methods for analysis of nanoparticles. Methods Mol. Biol. 906 (2012), 453–471.
86. Brown, A., Hondow, N., Electron microscopy of nanoparticles in cells. Summers, H., (eds.) Frontiers of Nanoscience, Vol. 5 Nanomedicine, 2013, Elsevier, London, 95–120.
87. Leroueil, P.R., Hong, S., Mecke, A., et al. Nanoparticle interaction with biological membranes: does nanotechnology presents a Janus face?. Acc. Chem. Res. 40 (2007), 335–342.
88. Madaan, K., Kumar, S., Poonia, N., et al. Dendrimers in drug delivery and targeting: drug-dendrimer interactions and toxicity issues. J. Pharm. Bioallied Sci. 6 (2014), 139–150.
89. Kong, B., Seog, J.Y., Graham, L.M., et al. Experimental consideration on the cytotoxicity of nanoparticles. Nanomedicine 6 (2011), 926–941.
90. Kumar, V., Sharma, N., Maitra, S.S., In vitro and in vivo toxicity assessment of nanoparticles. Int. Nano Lett. 7 (2017), 243–256.
91. Kroll, A., Dierker, C., Rommel, C., et al. Cytotoxicity screening of 23 engineered nanomaterials using a test matrix of ten cell lines and three different assays. Part. Fibre Toxicol., 8, 2011, 9.
92. Holder, A.L., Goth-Goldstein, R., Lucas, D., et al. Particle-induced artifacts in the MTT and LDH viability assays. Chem. Res. Toxicol. 25 (2012), 1885–1892.
93. Pujalté, I., Passagne, I., Brouillaud, B., et al. Cytotoxicity and oxidative stress induced by different metallic nanoparticles on human kidney cells. Part. Fibre Toxicol., 8, 2011, 10.
94. Zhao, J., Riediker, M., Detecting the oxidative reactivity of nanoparticles: a new protocol for reducing artifacts. J. Nanopart. Res., 16, 2014, 2493.
95. Hackenberg, S., Scherzed, A., Kessler, M., et al. Silver nanoparticles: evaluation of DNA damage, toxicity and functional impairment in human mesenchymal stem cells. Toxicol. Lett. 201 (2011), 27–33.
96. Selvaraj, V., Bodapati, S., Murray, E., et al. Cytotoxicity and genotoxicity caused by yttrium oxide nanoparticles in HEK293 cells. Int. J. Nanomedicine 12 (2014), 1379–1391.
97. Teeguarden, J.G., Hinderliter, P.M., Orr, G., et al. Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol. Sci. 95 (2007), 300–312.
98. Kalbassi, M.R., Johari, S.A., Soltani, M., et al. Particle size and agglomeration affect the toxicity level of silver nanoparticle types in aquatic environment. Ecopersia 1 (2013), 273–290.
99. Liyanage, D.D., Thamali, R.J.K.A., Kumbalatara, A.A.K., et al. An analysis of nanoparticle settling times in liquids. J. Nanomater., 2016, 2016, 7061838.
100. Hinderliter, P.M., Minard, K.R., Orr, G., et al. ISDD: a computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part. Fibre Toxicol., 7, 2010, 36.
101. Fernandes, M.R., Pedroso, A.R., Animal experimentation: a look into ethics, welfare and alternative methods. Rev. Assoc. Med. Bras. 63 (2017), 923–928.
102. Wen, H., Dan, M., Yang, Y., et al. Acute toxicity and genotoxicity of silver nanoparticle in rats. PLoS One, 12, 2017, e0185554.
103. Festing, S., Wilkinson, R., The ethics of animal research. Talking point on the use of animals in scientific research. EMBO Rep. 9 (2007), 526–530.
104. Wilson-Sanders, S.E., Invertebrate models for biomedical research, testing, and education. ILAR J. 52 (2011), 126–152.
105. Gonzalez-Moragas, L., Roig, A., Laromaine, A., C. elegans as a tool for in vivo nanoparticle assessment. Adv. Colloid Interface Sci. 219 (2015), 10–26.
106. Wu, T., Xu, H., Liang, X., et al. Caernorhabditis elegans as a complete model organism for biosafety assessments of nanoparticles. Chemosphere 221 (2019), 708–726.
107. Wang, J., Zhu, X., Chen, Y., et al. Application of embryonic and adult zebrafish in nanotoxicology assessment. Methods Mol. Biol. 926 (2012), 317–329.
108. 2 nanoparticles to study the effect of particle size on zebrafish embryo toxicity. Analyst 139 (2014), 964–972.
109. Sayed, A.E.H., Soliman, H.A.M., Developmental toxicity and DNA damaging properties of silver nanoparticles in the catfish (Clarias gariepinus). Mutat. Res. 822 (2017), 34–40.
110. Yang, Y., Qin, Z., Zeng, W., et al. Toxicity assessment of nanoparticles in various systems and organs. Nanotechnol. Rev. 6 (2017), 279–289.
111. van der Zande, M., Vandebriel, R.J., Van Doren, E., et al. Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano 6 (2012), 7427–7442.
112. Sharma, V., Singh, P., Pandey, A.K., et al. Induction of oxidative stress, DNA damage and apoptosis in mouse liver after sub-acute oral exposure to zinc oxide nanoparticles. Mutat. Res. 745 (2012), 84–91.
113. Chen, Z., Wang, Y., Zhuo, L., et al. Interaction of titanium dioxide nanoparticles with glucose on young rats after oral administration. Nanomedicine 11 (2015), 1633–1642.
114. Bettini, S., Boutet-Robinet, E., Cartier, C., et al. Food-grade TiO2 impairs intestinal and systemic homeostasis, initiates preneoplasic lesions and promotes aberrant crypt development in the rat colon. Sci. Rep., 7, 2017, 40373.
115. 2. Food Res. Int. 95 (2017), 38–45.
116. Hadrup, N., Lam, H.R., Oral toxicity of silver ions, silver nanoparticles and colloidal silver - a review. Regul. Toxicol. Pharmacol. 68 (2014), 1–7.
117. Saunders, M., Hutchison, G., Carreira, S.C., Reproductive toxicity of nanomaterials. Therapy, 40, 2015, 44.