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Histopathological study of the maternal exposure to the biologically produced silver nanoparticles on different organs of the offspring

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Abstract

This research for the first time presents the possibility of crossing the biologically produced SNPs through the placenta to different organs of rat offspring. SNPs were produced using Fusarium oxysporum. After adding 1 mmol final concentration of silver nitrate solution to the culture supernatant and 5 min heating, SNPs were produced, and their production was proved using visible spectrum, transmission electron microscope (TEM), and X-ray diffraction (XRD) analyses. SNPs were washed, and their concentration determined using inductively coupled plasma (ICP) instrument. SNPs were used for 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay, and after determination of their half maximal inhibitory concentration (IC50) dose, their toxic and nontoxic doses were determined and used for in vivo studies. A total of 24 female rats, after detection of their vaginal plugs, were divided into 3 groups each having 8 members. A control group was treated with normal saline. The other two groups were treated by toxic and nontoxic doses of SNPs, respectively. After delivery and breastfeeding, the pups were scarified, and their organs were collected and analyzed using histological examinations. Results showed that SNPs had a maximum absorbance peak around 450 nm, with polygonal and round shapes. XRD results confirmed the presence of SNPs. The concentration of the SNPs after washing was 19 ppm/mL based on the ICP results. MTT assay results showed that SNPs had a dose-dependent toxic effect. Histopathological examination results showed that SNPs could pass through the placenta; both their nontoxic and toxic doses induced somehow mild alternations in the liver, kidney, testis, and ovary and had no effects on the brains of the rat offspring. In conclusions, the use of the biologically produced SNPs should be limited during pregnancy and breastfeeding.

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References

  • Ahmad A, Mukherjee P, Senapati S, Mandal D, Khan MI, Kumar R, Sastry M (2003) Extracellular biosynthesis of silver nanoparticles using the fungus Fusarium oxysporum. Colloids Surf B: Biointerfaces 28(4):313–318

    Article  CAS  Google Scholar 

  • Amiri S, Yousefi-Ahmadipour A, Hosseini M-J, Haj-Mirzaian A, Momeny M, Hosseini-Chegeni H, Mokhtari T, Kharrazi S, Hassanzadeh G, Amini SM (2018) Maternal exposure to silver nanoparticles are associated with behavioral abnormalities in adulthood: role of mitochondria and innate immunity in developmental toxicity. NeuroToxicology 66:66–77

    Article  CAS  Google Scholar 

  • Austin CA, Umbreit TH, Brown KM, Barber DS, Dair BJ, Francke-Carroll S, Feswick A, Saint-Louis MA, Hikawa H, Siebein KN (2012) Distribution of silver nanoparticles in pregnant mice and developing embryos. Nanotoxicology 6(8):912–922

    Article  CAS  Google Scholar 

  • Calderon-Garciduenas L, Villarreal-Calderon R, Valencia-Salazar G, Henriquez-Roldan C, Gutiérrez-Castrellón P, Torres-Jardon R, Osnaya-Brizuela N, Romero L, Torres-Jardón R, Solt A (2008) Systemic inflammation, endothelial dysfunction, and activation in clinically healthy children exposed to air pollutants. Inhal Toxicol 20(5):499–506

    Article  CAS  Google Scholar 

  • Chu M, Wu Q, Yang H, Yuan R, Hou S, Yang Y, Zou Y, Xu S, Xu K, Ji A (2010) Transfer of quantum dots from pregnant mice to pups across the placental barrier. Small 6(5):670–678

    Article  CAS  Google Scholar 

  • Dănilă O-O, Berghian AS, Dionisie V, Gheban D, Olteanu D, Tabaran F, Baldea I, Katona G, Moldovan B, Clichici S (2017) The effects of silver nanoparticles on behavior, apoptosis and nitro-oxidative stress in offspring Wistar rats. Nanomedicine 12(12):1455–1473

    Article  Google Scholar 

  • Del Bonis-O’Donnell JT, Chio L, Dorlhiac GF, McFarlane IR, Landry MP (2018) Advances in nanomaterials for brain microscopy. Nano Res 11(10):5144-72

  • Durán N, Marcato PD, Alves OL, De Souza GI, Esposito E (2005) Mechanistic aspects of biosynthesis of silver nanoparticles by several Fusarium oxysporum strains. J Nanobiotechnol 3(1):8

    Article  Google Scholar 

  • Ema M, Okuda H, Gamo M, Honda K (2017) A review of reproductive and developmental toxicity of silver nanoparticles in laboratory animals. Reprod Toxicol 67:149–164

    Article  CAS  Google Scholar 

  • Fatemi M, Moshtaghian J, Ghaedi K (2017) Effects of silver nanoparticle on the developing liver of rat pups after maternal exposure. Iran J Pharm Res 16(2):685–693

    CAS  PubMed  PubMed Central  Google Scholar 

  • Fatemi M, Roodbari NH, Ghaedi K, Naderi G (2013) The effects of prenatal exposure to silver nanoparticles on the developing brain in neonatal rats. J Biol Res-Thessalon 20:233–242

    Google Scholar 

  • Fatemi Tabatabaie SR, Mehdiabadi B, Moori Bakhtiari N, Tabandeh MR (2017) Silver nanoparticle exposure in pregnant rats increases gene expression of tyrosine hydroxylase and monoamine oxidase in offspring brain. Drug Chem Toxicol 40(4):440–447

    Article  CAS  Google Scholar 

  • Genter MB, Newman NC, Shertzer HG, Ali SF, Bolon B (2012) Distribution and systemic effects of intranasally administered 25 nm silver nanoparticles in adult mice. Toxicol Pathol 40(7):1004–1013

    Article  Google Scholar 

  • Kumari M, Ernest V, Mukherjee A, Chandrasekaran N (2012) In vivo nanotoxicity assays in plant models: Reineke J. (eds) Nanotoxicity. Methods in Molecular Biology (Methods and Protocols) 926:399-410

  • Lee Y, Choi J, Kim P, Choi K, Kim S, Shon W, Park K (2012) A transfer of silver nanoparticles from pregnant rat to offspring. Toxicol Res 28(3):139–141

    Article  CAS  Google Scholar 

  • Ma X, Yang X, Wang Y, Liu J, Jin S, Li S, Liang X-J (2018) Gold nanoparticles cause size-dependent inhibition of embryonic development during murine pregnancy. Nano Res 11(6):3419-33

  • Manuel AR-L, Martinez-Cuevas PP, Rosas-Hernandez H, Oros-Ovalle C, Bravo-Sanchez M, Martinez-Castañon GA, Gonzalez C (2017) Evaluation of vascular tone and cardiac contractility in response to silver nanoparticles, using Langendorff rat heart preparation. Nanomedicine 13(4):1507–1518

    Article  Google Scholar 

  • Melnik E, Demin V, Demin V, Gmoshinski I, Tyshko N, Tutelyan V (2013) Transfer of silver nanoparticles through the placenta and breast milk during in vivo experiments on rats. Acta Naturae 5(18):107-115

  • Morishita Y, Yoshioka Y, Takimura Y, Shimizu Y, Namba Y, Nojiri N, Ishizaka T, Takao K, Yamashita F, Takuma K (2016) Distribution of silver nanoparticles to breast milk and their biological effects on breast-fed offspring mice. ACS Nano 10(9):8180–8191

    Article  CAS  Google Scholar 

  • Pourali P, Badiee SH, Manafi S, Noorani T, Rezaei A, Yahyaei B (2017) Biosynthesis of gold nanoparticles by two bacterial and fungal strains, Bacillus cereus and Fusarium oxysporum, and assessment and comparison of their nanotoxicity in vitro by direct and indirect assays. Electron J Biotechnol 29:86–93

    Article  CAS  Google Scholar 

  • Pourali P, Baserisalehi M, Afsharnezhad S, Behravan J, Ganjali R, Bahador N, Arabzadeh S (2013) The effect of temperature on antibacterial activity of biosynthesized silver nanoparticles. Biometals 26(1):189–196

    Article  CAS  Google Scholar 

  • Pourali P, Razavian Zadeh N, Yahyaei B (2016) Silver nanoparticles production by two soil isolated bacteria, Bacillus thuringiensis and Enterobacter cloacae, and assessment of their cytotoxicity and wound healing effect in rats. Wound Repair Regen 24(5):860–869

    Article  Google Scholar 

  • Pourali P, Yahyaei B (2016) Biological production of silver nanoparticles by soil isolated bacteria and preliminary study of their cytotoxicity and cutaneous wound healing efficiency in rat. J Trace Elem Med Biol 34:22–31

    Article  CAS  Google Scholar 

  • Pourali P, Yahyaei B, Afsharnezhad S (2018) Bio-synthesis of gold nanoparticles by Fusarium oxysporum and assessment of their conjugation possibility with two types of β-lactam antibiotics without any additional linkers. Microbiology 87(2):229–237

    Article  CAS  Google Scholar 

  • Pourali P, Yahyaei B, Ajoudanifar H, Taheri R, Alavi H, Hoseini A (2014) Impregnation of the bacterial cellulose membrane with biologically produced silver nanoparticles. Curr Microbiol 69(6):785–793

    Article  CAS  Google Scholar 

  • Rahman M, Wang J, Patterson T, Saini U, Robinson B, Newport G, Murdock R, Schlager J, Hussain S, Ali S (2009) Expression of genes related to oxidative stress in the mouse brain after exposure to silver-25 nanoparticles. Toxicol Lett 187(1):15–21

    Article  CAS  Google Scholar 

  • Ramirez-Lee MA, Espinosa-Tanguma R, Mejía-Elizondo R, Medina-Hernández A, Martinez-Castañon GA, Gonzalez C (2017) Effect of silver nanoparticles upon the myocardial and coronary vascular function in isolated and perfused diabetic rat hearts. Nanomedicine 13(8):2587–2596

    Article  CAS  Google Scholar 

  • Rezaei A, Pourali P, Yahyaei B (2016) Assessment the cytotoxicity effects of gold Nanoaprticles Produced by Bacillus Cereus In Hepg2 Cell Line. Iran J Public Health 29(3):291-301

  • Söderstjerna E, Johansson F, Klefbohm B, Johansson UE (2013) Gold-and silver nanoparticles affect the growth characteristics of human embryonic neural precursor cells. PLoS One 8(3):e58211

    Article  Google Scholar 

  • Takeda K, Suzuki K-i, Ishihara A, Kubo-Irie M, Fujimoto R, Tabata M, Oshio S, Nihei Y, Ihara T, Sugamata M (2009) Nanoparticles transferred from pregnant mice to their offspring can damage the genital and cranial nerve systems. J Health Sci 55(1):95–102

    Article  CAS  Google Scholar 

  • Wei L, Tang J, Zhang Z, Chen Y, Zhou G, Xi T (2010) Investigation of the cytotoxicity mechanism of silver nanoparticles in vitro. Biomed Mater 5(4):044103

    Article  Google Scholar 

  • Wu J, Yu C, Tan Y, Hou Z, Li M, Shao F, Lu X (2015) Effects of prenatal exposure to silver nanoparticles on spatial cognition and hippocampal neurodevelopment in rats. Environ Res 138:67–73

    Article  CAS  Google Scholar 

  • Yahyaei B, Arabzadeh S, Pourali P (2014) An alternative method for biological production of silver and gold nanoparticles. JPAM 8:4495–4501

    Google Scholar 

  • Yahyaei B, Peyvandi N, Akbari H, Arabzadeh S, Afsharnezhad S, Ajoudanifar H, Pourali P (2016) Production, assessment, and impregnation of hyaluronic acid with silver nanoparticles that were produced by streptococcus pyogenes for tissue engineering applications. Appl Biol Chem 59(2):227–237

    Article  CAS  Google Scholar 

  • Yahyaei B, Pourali P (2019) One step conjugation of some chemotherapeutic drugs to the biologically produced gold nanoparticles and assessment of their anticancer effects. Sci Rep 9(1):10242

    Article  Google Scholar 

  • Yang H, Sun C, Fan Z, Tian X, Yan L, Du L, Liu Y, Chen C, Liang X-j, Anderson GJ (2012) Effects of gestational age and surface modification on materno-fetal transfer of nanoparticles in murine pregnancy. Sci Rep 2:847

    Article  Google Scholar 

  • Zhang X-D, Wu H-Y, Wu D, Wang Y-Y, Chang J-H, Zhai Z-B, Meng A-M, Liu P-X, Zhang L-A, Fan F-Y (2010) Toxicologic effects of gold nanoparticles in vivo by different administration routes. Int J Nanomedicine 5:771

    Article  CAS  Google Scholar 

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BY designed and performed experiments, analyzed data, and co-wrote the paper. FA, TH, and NK performed experiments. PP, MN, and SA performed experiments and analyzed data. All authors read and approved the manuscript.

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Correspondence to Behrooz Yahyaei.

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Pourali, P., Nouri, M., Ameri, F. et al. Histopathological study of the maternal exposure to the biologically produced silver nanoparticles on different organs of the offspring. Naunyn-Schmiedeberg's Arch Pharmacol 393, 867–878 (2020). https://doi.org/10.1007/s00210-019-01796-y

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