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Research Article

Effects of silver nanoparticles functionalized with Cornus mas L. extract on architecture and apoptosis in rat testicle

    Razvan Opris

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    ,
    Vlad Toma

    Department of Molecular Biology & Biotechnology, Faculty of Biology & Geology, ‘Babes-Bolyai’ University, 5–7 Clinicilor Street, 400006 Cluj-Napoca, Romania

    Department of Biochemistry & Experimental Biology, Institute of Biological Research, 48 Republicii Street, branch of NIRDBS Bucharest, 400015 Cluj-Napoca, Romania

    Department of Molecular & Biomolecular Physics, NIRD for Isotopic & Molecular Technologies, 101 Donath Street, 400293 Cluj-Napoca, Romania

    ,
    Diana Olteanu

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    ,
    Ioana Baldea

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    ,
    Alina Mihaela Baciu

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    ,
    Florica Imre Lucaci

    Physico-Chemical Analysis Center, Interdisciplinary Research Institute on Bio-Nano-Sciences, ‘Babes-Bolyai’ University, 42 Treboniu Laurian Street, 400271 Cluj-Napoca, Romania

    ,
    Alexandra Berghian-Sevastre

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    ,
    Corina Tatomir

    Departments of Radiobiology & Tumour Biology, ‘Ion Chiricuta’ Oncology Institute, 34-36 Republicii Street, 400015, Cluj-Napoca, Romania

    ,
    Bianca Moldovan

    Department of Chemistry, Faculty of Chemistry & Chemical Engineering, ‘Babes-Bolyai’ University, 11. Arany Janos, 400028 Cluj-Napoca, Romania

    ,
    Simona Clichici

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    ,
    Luminita David

    Department of Chemistry, Faculty of Chemistry & Chemical Engineering, ‘Babes-Bolyai’ University, 11. Arany Janos, 400028 Cluj-Napoca, Romania

    ,
    Adrian Florea

    *Author for correspondence:

    E-mail Address: aflorea@umfcluj.ro

    Department of Cell & Molecular Biology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy 6, Louis Pasteur Street, 400349, Cluj Napoca, Romania

    &
    Gabriela Adriana Filip

    Department of Physiology, ‘Iuliu Hatieganu’ University of Medicine & Pharmacy, 1–3 Clinicilor Street, 400006, Cluj-Napoca, Romania

    Published Online:https://doi.org/10.2217/nnm-2018-0193

    Aim: To assess ultrastructural changes, alterations in matrix metalloproteinase activity and apoptosis induced by silver nanoparticles (AgNPs) in the rat testicle. Materials & methods: For 45 days, two groups of animals received different doses of AgNPs (0.8 and 1.5 mg/kg b.w.), and a control group was given the buffer used as vehicle for AgNPs. At 7 and 15 days post-treatment, transmission electron microscopy, TUNEL assay, evaluation of NFkB, pNFkB, p53, Bcl-2 and Nrf2 expressions were performed on the removed testes. Results: Transmission electron microscopy revealed severe ultrastructural changes of interstitial tissue and seminiferous epithelium sustained by positive signal for apoptosis. The promatrix metalloproteinase-2 activity and NFkB, Bcl-2 expressions were increased, mainly at 7 days. Conclusion: AgNPs induced severe cell lesions identified even a long time after the exposure.

    Papers of special note have been highlighted as: • of interest

    References

    • 1 NIH. Nanotechnology. www.nih.gov/science/nanotechnology.
    • 2 Daniel MC, Astruc D. Gold nanoparticles: assembly, supramolecular chemistry, quantum-size-related properties, and applications toward biology, catalysis, and nanotechnology. J. Chem. Rev. 104, 293–346 (2004).
    • 3 Allain LR, Vo-Dinh T. Surface-enhanced Raman scattering detection of the breast cancer susceptibility gene BRCA1 using a silver-coated microarray platform. Anal. Chim. Acta 469, 149–154 (2002).
    • 4 Parveen S, Misra R, Sahoo SK. Nanoparticles: a boon to drug delivery, therapeutics, diagnostics and imaging. Nanomedicine 8, 147–166 (2012).
    • 5 www.nanotechproject.org/inventories/consumer/analysisanddraft/.
    • 6 Kleinauskas A, Rocha S, Sahu S, Sun YP, Juzenas P. Carboncore silver-shell nanodots as sensitizers for phototherapy and radiotherapy. Nanotechnology 4(32), 325103 (2013).
    • 7 Sondi I, Salopek-Sondi B. Silver nanoparticles as antimicrobial agent: a case study on E. coli as a model for gram-negative bacteria. J. Colloid Interface Sci. 275, 177–182 (2004).
    • 8 Galdiero S, Falanga A, Vitiello M, Cantisani M, Marra V, Galdiero M. Silver nanoparticles as potential antiviral agents. Molecules 16(10), 8894–8918 (2011).
    • 9 Rahman MF, Wang J, Patterson TA et al. Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol. Lett. 187(1), 15–21 (2009).
    • 10 Almofti MR, Ichikawa T, Yamashita K, Terada H, Shinohara Y. Silver ion induces a cyclosporine a-insensitive permeability transition in rat liver mitochondria and release of apoptogenic cytochrome C. J. Biochem. 134(1), 43–49 (2003).
    • 11 Mittal AK, Chisti Y, Banerjee UC. Synthesis of metallic nanoparticles using plant extracts. Biotechnol. Adv. 31, 346–356 (2013).
    • 12 Rafique M, Sadaf I, Rafique MS et al. A review on green synthesis of silver nanoparticles and their applications. Artif. Cells Nanomed. Biotechnol. 45(7), 1272–1291 (2017). • Summarizes the effects of silver nanoparticles.
    • 13 Moldovan B, Filip A, Clichici S, Suharoschi R, Bolfa P, David L. Antioxidant activity of Cornelian cherry (Cornus mas L.) fruits extract and the in vivo evaluation of its anti-inflammatory effects. J. Funct. Foods 26, 77–87 (2016).
    • 14 Hosseinpour-Jaghdani F, Shomali T, Gholipour-Shahraki S, Rahimi-Madiseh M, Rafieian-Kopae M. Cornus mas: a review on traditional uses and pharmacological properties. J. Complement. Integr. Med. 14(3), 0137 (2017).
    • 15 Kim YS, Kim JS, Cho HS et al. Twenty-eight-day oral toxicity, genotoxicity, and gender-related tissue distribution of silver nanoparticles in Sprague-Dawley rats. Inhal. Toxicol. 20, 575–583 (2008).
    • 16 Wen H, Dan M, Yang Y et al. Acute toxicity and genotoxicity of silver nanoparticle in rats. PLoS ONE 12(9), e0185554 (2017).
    • 17 Thakur M, Gupta H, Singh D et al. Histopathological and ultra structural effects of nanoparticles on rat testis following 90 days (Chronic study) of repeated oral administration. J. Nanobiotechnol. 12, 1–13 (2014). • One of the few studies on the ultrastructural effects following chronic exposure to silver nanoparticles.
    • 18 Filip A, Potara M, Florea A et al. Comparative evaluation by scanning confocal Raman spectroscopy and transmission electron microscopy of therapeutic effects of noble metal nanoparticles in experimental acute inflammation. RSC Adv. 5(83), 67435–67448 (2015).
    • 19 Pippenger CE, Browne RW, Armstrong D. Regulatory antioxidant enzymes. Meth. Molec. Biol. 108, 299–311 (1998).
    • 20 Conti M, Moran PC, Levillain P. Improved fluorimetric determination of malondialdehyde. Clin. Chem. 37, 1273–1275 (1991).
    • 21 Reznick AZ, Packer L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 233, 347–357 (1994).
    • 22 Danila OO, Sevastre Berghian A, Dionisie V et al. The effects of silver nanoparticles on behavior, apoptosis and nitro-oxidative stress in offspring Wistar rats. Nanomedicine 12, 1455–1473 (2017).
    • 23 Huang T, Xu XN, Huang ST. Synthesis and characterization of tunable rainbow colored colloidal silver nanoparticles using single-nanoparticle plasmonic microscopy and spectroscopy. J. Mater. Chem. 20, 9867–9876 (2010).
    • 24 Moldovan B, David L, Vulcu A et al. In vitro and in vivo anti-inflammatory properties of green synthesized silver nanoparticles using Viburnum opulus L. fruits extract. Mater. Sci. Eng. C Mater. Biol. Appl. 79, 720–727 (2017).
    • 25 Park MV, Neigh AM, Vermeulen JP et al. The effect of particle size on the cytotoxicity, inflammation, developmental toxicity and genotoxicity of silver nanoparticles. Biomaterials 32, 9810–9817 (2011). • Finds that smaller sized nanoparticles inflict more damage.
    • 26 Park EJ, Yi J, Kim Y, Choi K, Park K. Silver nanoparticles induce cytotoxicity by a Trojan-horse type mechanism. Toxicol. In Vitro 24(3), 872–187 (2010).
    • 27 Lee JH, Kim YS, Song KS et al. Biopersistence of silver nanoparticles in tissues from Sprague–Dawley rats. Part Fibre Toxicol. 10, 36 (2013). • Shows increased accumulation of silver nanoparticles in the testicle after subchronic oral administration.
    • 28 EL Badawy AM, Silva RG, Morris B, Scheckel KG, Suidan MT, Tolaymat TM. Surface charge-dependent toxicity of silver nanoparticles. Environ. Sci. Technol. 45, 283–287 (2011).
    • 29 Katsnelson BA, Privalova LI, Gurvich VB et al. Comparative in vivo assessment of some adverse bioeffects of equidimensional gold and silver nanoparticles and the attenuation of nanosilver's effects with a complex of innocuous bioprotectors. Int. J. Mol. Sci. 14, 2449–2483 (2013).
    • 30 Sani M, Sebai H, Ghanem-Boughanmi N, Boughattas NA, Ben-Attia M. Circadian (about 24-hour) variation in malondialdehyde content and catalase activity of mouse erythrocytes. Redox Rep. 20(1), 26–32 (2015).
    • 31 Hunt CR, Sim JE, Sullivan SJ et al. Genomic instability and catalase gene amplification induced by chronic exposure to oxidative stress. Cancer Res. 58, 3986–3992 (1998).
    • 32 Kaido M, Mori K, Koide O. Testicular damage caused by inhalation of ethylene oxide in rats: light and electron microscopic studies. Toxicol. Pathol. 20(1), 32–43 (1992).
    • 33 Gras-Kraupp B, Ruttkay-Nedecky B, Koudelka H, Bukowska K, Bursch W, Schulte-Herma R. In situ detection of fragmented DNA (TUNEL assay) to discriminate among apoptosis, necrosis, and auto cell death: a cautionary note. Hepatology 21(5), 1465–1468 (1995). • Shows that TUNEL assay is not specific enough to reveal cell apoptosis.
    • 34 www.ncbi.nlm.nih.gov/gene/4313.
    • 35 Schreck R, Albermann K, Baeuerle PA. Nuclear factor KB: an oxidative stress-responsive transcription factor of eukaryotic cells (a review). Free Radic. Res. Commun. 17(4), 221–237 (1992).
    • 36 Czabotar PE, Lessene G, Strasser A, Adams JM. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 15(1), 49–63 (2014).
    • 37 www.thermofisher.com/ro/en/home/life-science/antibodies/antibodies-learning-center/antibodies-resource-library/cell-signaling-pathways/p53-mediated-apoptosis-pathway.html. • Very good schematic representations of cell signalling pathways.
    • 38 Ma Q. Role of Nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53, 401–426 (2013).
    • 39 Kim AS, Chae CH, Kim J, Choi JY, Kim SG, Baciut G. Silver nanoparticles induce apoptosis through the toll-like receptor 2 pathway. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. 113(6), 789–798 (2012).
    • 40 Hedger MP. Toll-like receptors and signalling in spermatogenesis and testicular responses to inflammation – a perspective. J. Reprod. Immunol. 88, 130–141 (2011). • Reveals a signalling pathway through which silver nanoparticles induce cell apoptosis.
    • 41 Stepkowski TM, Brzóska K, Kruszewski M. Silver nanoparticles induced changes in the expression of NF-kB related genes are cell type specific and related to the basal activity of NF-kB. Toxicol. In Vitro 28(4), 473–478 (2014).
    • 42 Braydich-Stolle LK, Lucas B, Schrand A et al. Silver nanoparticles disrupt GDNF/Fyn kinase signalling in spermatogonial stem cells. Toxicol. Sci. 116(2), 577–589 (2010).
    • 43 Lee J, Richburg JH, Shipp EB, Meistrich ML, Boekelheide K. The Fas system, a regulator of testicular germ cell apoptosis, is differentially up-regulated in Sertoli cell versus germ cell injury of the testis. Endocrinology 140(2), 852–858 (1999). • Shows that only Sertoli cells can produce Fas-ligand.
    • 44 Koji T, Hishikawa Y, Ando H, Nakanishi Y, Kobayashi N. Expression of Fas and Fas ligand in lormal and ischemia-reperfusion testes: Involvement of the Fas system in the induction of germ cell apoptosis in the damaged mouse testis. Biol. Reprod. 64, 946–954 (2001).