Small-size silver nanoparticles stimulate neutrophil oxidative burst through an increase of intracellular calcium levels

Freitas,Marisa; Lucas,Mariana; Sousa,Adelaide; Soares,Tânia; Ribeiro,Daniela; Carvalho,Félix; Fernandes,Eduarda

doi:10.3892/wasj.2020.46

Small-size silver nanoparticles stimulate neutrophil oxidative burst through an increase of intracellular calcium levels

Authors:
- Marisa Freitas
- Mariana Lucas
- Adelaide Sousa
- Tânia Soares
- Daniela Ribeiro
- Félix Carvalho
- Eduarda Fernandes
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Affiliations: LAQV, REQUIMTE, Laboratory of Applied Chemistry, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal, UCIBIO, REQUIMTE, Laboratory of Toxicology, Department of Biological Sciences, Faculty of Pharmacy, University of Porto, 4050-313 Porto, Portugal
Published online on: April 21, 2020 https://doi.org/10.3892/wasj.2020.46
Article Number: 5
Copyright: © Freitas et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Despite the widespread use of silver nanoparticles (AgNPs) in several daily consumer products, the putative human risks resulting from continuous exposure remain elusive, particularly with what concerns the reactivity of the immune system and the resulting pro-inflammatory effects. Neutrophils are considered one of the first and primary cell types that process systemic nanoparticles, mediating the host inflammatory and immunological response, involving the production of reactive oxygen and nitrogen species. The main objective of the present study was to evaluate the effect of polyvinylpyrrolidone (PVP) and citrate-coated AgNPs of different sizes (5, 10 and 50 nm) on oxidative burst, calcium levels and the viability of human neutrophils. It was observed that the effects of AgNPs were size and coating-dependent. The citrate-coated and 5-nm-sized AgNPs were the most cytotoxic and potent inducers of neutrophil oxidative burst. It was observed that AgNPs induced an increase in intracellular calcium levels, which are involved in the activation of protein kinase C (PKC), resulting in the assembly of NADPH oxidase subunits with the subsequent production of reactive oxygen species. This excessive production of reactive oxygen species most probably contributes to the AgNP-induced decrease in neutrophil viability. Overall, the data of the present study contribute to a better understanding of the pro-inflammatory mechanisms associated with the use of AgNPs.

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1	Beyene HD, Werkneh AA, Bezabh HK and Ambaye TG: Synthesis paradigm and applications of silver nanoparticles (AgNPs), a review. Sustain Mater Technol. 13:18–23. 2017.
2	Vance ME, Kuiken T, Vejerano EP, McGinnis SP, Hochella MF Jr, Rejeski D and Hull MS: Nanotechnology in the real world: Redeveloping the nanomaterial consumer products inventory. Beilstein J Nanotechnol. 6:1769–1780. 2015.PubMed/NCBI View Article : Google Scholar
3	Williams KM, Gokulan K, Cerniglia CE and Khare S: Size and dose dependent effects of silver nanoparticle exposure on intestinal permeability in an in vitro model of the human gut epithelium. J Nanobiotechnol. 14(62)2016.PubMed/NCBI View Article : Google Scholar
4	Bouwmeester H, Dekkers S, Noordam MY, Hagens WI, Bulder AS, de Heer C, ten Voorde SE, Wijnhoven SW, Marvin HJ and Sips AJ: Review of health safety aspects of nanotechnologies in food production. Regul Toxicol Pharmacol. 53:52–62. 2009.PubMed/NCBI View Article : Google Scholar
5	Luo YH, Chang LW and Lin P: Metal-based nanoparticles and the immune system: Activation, inflammation, and potential applications. Biomed Res Int. 2015(143720)2015.PubMed/NCBI View Article : Google Scholar
6	Freitas M, Lima JL and Fernandes E: Optical probes for detection and quantification of neutrophils' oxidative burst. A review. Anal Chim Acta. 649:8–23. 2009.PubMed/NCBI View Article : Google Scholar
7	Ribeiro D, Freitas M, Lima JL and Fernandes E: Proinflammatory pathways: The modulation by flavonoids. Med Chem Rev. 35:877–936. 2015.PubMed/NCBI View Article : Google Scholar
8	Recordati C, De Maglie M, Bianchessi S, Argentiere S, Cella C, Mattiello S, Cubadda F, Aureli F, D'Amato M, Raggi A, et al: Tissue distribution and acute toxicity of silver after single intravenous administration in mice: Nano-specific and size-dependent effects. Part Fibre Toxicol. 13(12)2016.PubMed/NCBI View Article : Google Scholar
9	Seiffert J, Hussain F, Wiegman C, Li F, Bey L, Baker W, Porter A, Ryan MP, Chang Y, Gow A, et al: Pulmonary toxicity of instilled silver nanoparticles: Influence of size, coating and rat strain. PLoS One. 10(e0119726)2015.PubMed/NCBI View Article : Google Scholar
10	Park EJ, Bae E, Yi J, Kim Y, Choi K, Lee SH, Yoon J, Lee BC and Park K: Repeated-dose toxicity and inflammatory responses in mice by oral administration of silver nanoparticles. Environ Toxicol Pharmacol. 30:162–168. 2010.PubMed/NCBI View Article : Google Scholar
11	Park EJ, Choi K and Park K: Induction of inflammatory responses and gene expression by intratracheal instillation of silver nanoparticles in mice. Arch Pharm Res. 34:299–307. 2011.PubMed/NCBI View Article : Google Scholar
12	Alessandrini F, Vennemann A, Gschwendtner S, Neumann AU, Rothballer M, Seher T, Wimmer M, Kublik S, Traidl-Hoffmann C, Schloter M, et al: Pro-inflammatory versus immunomodulatory effects of silver nanoparticles in the lung: The critical role of dose, size and surface modification. Nanomaterials (Basel). 7(pii: E300)2017.PubMed/NCBI View Article : Google Scholar
13	Poirier M, Simard JC, Antoine F and Girard D: Interaction between silver nanoparticles of 20 nm (AgNP20) and human neutrophils: Induction of apoptosis and inhibition of de novo protein synthesis by AgNP20 aggregates. J Appl Toxicol. 34:404–412. 2014.PubMed/NCBI View Article : Google Scholar
14	Poirier M, Simard JC and Girard D: Silver nanoparticles of 70 nm and 20 nm affect differently the biology of human neutrophils. J Immunotoxicol. 13:375–385. 2016.PubMed/NCBI View Article : Google Scholar
15	Soares T, Ribeiro D, Proenca C, Chisté RC, Fernandes E and Freitas M: Size-dependent cytotoxicity of silver nanoparticles in human neutrophils assessed by multiple analytical approaches. Life Sci. 145:247–254. 2016.
16	Freitas M, Porto G, Lima JL and Fernandes E: Isolation and activation of human neutrophils in vitro. The importance of the anticoagulant used during blood collection. Clin Biochem. 41:570–575. 2008.PubMed/NCBI View Article : Google Scholar
17	Ribeiro D, Freitas M, Rocha S, Lima J, Carvalho F and Fernandes E: Calcium pathways in human neutrophils-the extended effects of thapsigargin and ML-9. Cells. 7(pii: E204)2018.PubMed/NCBI View Article : Google Scholar
18	Freitas M, Costa VM, Ribeiro D, Couto D, Porto G, Carvalho F and Fernandes E: Acetaminophen prevents oxidative burst and delays apoptosis in human neutrophils. Toxicol Lett. 219:170–177. 2013.PubMed/NCBI View Article : Google Scholar
19	Ng LG, Ostuni R and Hidalgo A: Heterogeneity of neutrophils. Nat Rev Immunol. 19:255–265. 2019.PubMed/NCBI View Article : Google Scholar
20	Silva RM, Anderson DS, Franzi LM, Peake JL, Edwards PC, Van Winkle LS and Pinkerton KE: Pulmonary effects of silver nanoparticle size, coating, and dose over time upon intratracheal instillation. Toxicol Sci. 144:151–162. 2015.PubMed/NCBI View Article : Google Scholar
21	Gliga AR, Skoglund S, Wallinder IO, Fadeel B and Karlsson HL: Size-dependent cytotoxicity of silver nanoparticles in human lung cells: The role of cellular uptake, agglomeration and Ag release. Part Fibre Toxicol. 11(11)2014.PubMed/NCBI View Article : Google Scholar
22	Belambri SA, Rolas L, Raad H, Hurtado-Nedelec M, Dang PM and El-Benna J: NADPH oxidase activation in neutrophils: Role of the phosphorylation of its subunits. Eur J Clin Invest. 48 (Suppl 2)(e12951)2018.PubMed/NCBI View Article : Google Scholar
23	Babior BM: The leukocyte NADPH oxidase. Isr Med Assoc J. 4:1023–1024. 2002.PubMed/NCBI
24	Manda-Handzlik A and Demkow U: Neutrophils: The role of oxidative and nitrosative stress in health and disease. Adv Exp Med Biol. 857:51–60. 2015.PubMed/NCBI View Article : Google Scholar
25	Hsiao IL, Hsieh YK, Wang CF, Chen IC and Huang YJ: Trojan-horse mechanism in the cellular uptake of silver nanoparticles verified by direct intra- and extracellular silver speciation analysis. Environ Sci Technol. 49:3813–3821. 2015.PubMed/NCBI View Article : Google Scholar
26	Wang H, Qiao X, Chen J, Wang X and Ding S: Mechanisms of PVP in the preparation of silver nanoparticles. Mater Chem Phys. 94:449–453. 2005.
27	Henglein A and Giersig M: Formation of colloidal silver nanoparticles: Capping action of citrate. J Phys Chem B. 103:9533–9539. 1999.
28	Wang X, Ji Z, Chang CH, Zhang H, Wang M, Liao YP, Lin S, Meng H, Li R, Sun B, et al: Use of coated silver nanoparticles to understand the relationship of particle dissolution and bioavailability to cell and lung toxicological potential. Small. 10:385–398. 2014.PubMed/NCBI View Article : Google Scholar
29	Cosentino-Gomes D, Rocco-Machado N and Meyer-Fernandes JR: Cell signaling through protein kinase C oxidation and activation. Int J Mol Sci. 13:10697–10721. 2012.PubMed/NCBI View Article : Google Scholar
30	Bertram A and Ley K: Protein kinase C isoforms in neutrophil adhesion and activation. Arch Immunol Ther Exp (Warsz). 59:79–87. 2011.PubMed/NCBI View Article : Google Scholar
31	Tintinger GR, Theron AJ, Steel HC, Cockeran R, Pretorius L and Anderson R: Protein kinase C promotes restoration of calcium homeostasis to platelet activating factor-stimulated human neutrophils by inhibition of phospholipase. C. J Inflamm (Lond). 6(29)2009.PubMed/NCBI View Article : Google Scholar
32	Nguyen KC, Seligy VL, Massarsky A, Moon TW, Rippstein P, Tan J and Tayabali AF: Comparison of toxicity of uncoated and coated silver nanoparticles. J Phys Conf Ser. 429(012025)2013.