Beneficial effects of bioinspired silver nanoparticles on zebrafish embryos including a gene expression study

Sakthi Devi R; Agnishwar Girigoswami; Shanmugaraja Meenakshi; Balasubramanian Deepika; Karthick Harini; Pemula Gowtham; Pragya Pallavi; Koyeli Girigoswami

doi:10.5599/admet.2102

Authors

Sakthi Devi R Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0003-2632-1286
Agnishwar Girigoswami Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0003-0475-2544
Shanmugaraja Meenakshi Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0002-7944-5840
Balasubramanian Deepika Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0003-4441-7863
Karthick Harini Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0002-8538-2049
Pemula Gowtham Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0002-6794-1214
Pragya Pallavi Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0001-6422-9697
Koyeli Girigoswami Medical Bionanotechnology, Faculty of Allied Health Sciences, Chettinad Hospital & Research Institute (CHRI), Chettinad Academy of Research and Education (CARE), Kelambakkam, Chennai-603 103, India https://orcid.org/0000-0003-1554-5241

DOI:

https://doi.org/10.5599/admet.2102

Keywords:

green synthesis, biocompatibility, nanoparticle toxicity, fish embryo, zebrafish hatching (ZHE1 and ZHE2)

Abstract

Background and purpose: Many sectors use nanoparticles and dispose of them in the aquatic environment without deciding the fate of these particles. Experimental approach: To identify a benign species of nanoparticles which can cause minimum harm to the aquatic environment, a comparative study was done with chemically synthesized silver nanoparticles (AgNPs) and green tea mediated synthesis (GT/AgNP) in both in vitro using human alveolar cancer cell line (A549) and normal cell line (L132), and in in vivo with zebrafish embryos. Key results: The in vitro studies revealed that GT/AgNPs were less toxic to normal cells than cancer cells. The GT/AgNPs showed high biocompatibility for zebrafish embryos monitored microscopically for their developmental stages and by cumulative hatchability studies. The reduced hatchability found in the AgNPs-treated group was correlated by differential gene expression of zebrafish hatching enzymes (ZHE) (ZHE1 and ZHE2). Conclusion: The results indicated that nanoparticles can affect the hatching of zebrafish embryos and elicit toxicity at the gene level.

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References

S. Dawadi, S. Katuwal, A. Gupta, U. Lamichhane, R. Thapa, S. Jaisi, G. Lamichhane, D.P. Bhattarai, N. Parajuli. Current research on silver nanoparticles: Synthesis, characterization, and applications. Journal of Nanomaterials 2021 (2021) 6687290. https://doi.org/10.1155/2021/6687290.

P.G. Jamkhande, N.W. Ghule, A.H. Bamer, M.G. Kalaskar. Metal nanoparticles synthesis: An overview on methods of preparation, advantages and disadvantages, and applications. Journal of Drug Delivery Science and Technology 53 (2019) 101174. https://doi.org/10.1016/j.jddst.2019.101174.

D.A. Mosselhy, W. He, D. Li, Y. Meng, Q. Feng. Silver nanoparticles: in vivo toxicity in zebrafish embryos and a comparison to silver nitrate. Journal of Nanoparticle Research 18 (2016) 222. https://doi.org/10.1007/s11051-016-3514-y.

L. Qiang, Z.H. Arabeyyat, Q. Xin, V.N. Paunov, I.J. Dale, R.I. Lloyd Mills, J.M. Rotchell, J. Cheng. Silver nanoparticles in Zebrafish (Danio rerio) embryos: Uptake, growth and molecular responses. International Journal of Molecular Sciences 21 (2020) 1876. https://doi.org/10.3390/ijms21051876.

D. Boyle, G.G. Goss. Effects of silver nanoparticles in early life-stage zebrafish are associated with particle dissolution and the toxicity of soluble silver. NanoImpact 12 (2018) 1-8. https://doi.org/10.1016/j.impact.2018.08.006.

J. Maheswari, M.R. Anjum, M. Sankari, G. Narasimha, S.B.N. Krishna, B. Kishori. Green synthesis, characterization and biological activities of silver nanoparticles synthesized from Neolamarkia cadamba. ADMET and DMPK 11 (2023) 573-585. https://doi.org/10.5599/admet.1793

T. Aavula, V. Narasimman, S. Ramachandran, R. Murugan, M. Ponnusamy, G.P. Pazhani. Antioxidant and Teratogenic Activities of Formulated Agar Extracted from Brown Seaweed Turbinaria conoides against Zebrafish Larvae. Evidence-Based Complementary and Alternative Medicine 2022 (2022) 3520336. https://doi.org/10.1155/2022/3520336.

B. Yashwanth, R. Pamanji, J.V. Rao. Toxicomorphomics and toxicokinetics of quinalphos on embryonic development of zebrafish (Danio rerio) and its binding affinity towards hatching enzyme, ZHE1. Aquatic Toxicology 180 (2016) 155-163. https://doi.org/10.1016/j.aquatox.2016.09.018.

K. Sano, K. Inohaya, M. Kawaguchi, N. Yoshizaki, I. Iuchi, S. Yasumasu. Purification and characterization of zebrafish hatching enzyme–an evolutionary aspect of the mechanism of egg envelope digestion. The FEBS journal 275 (2008) 5934-5946. https://doi.org/10.1111/j.1742-4658.2008.06722.x.

S. Yasumasu, M. Kawaguchi, S. Ouchi, K. Sano, K. Murata, H. Sugiyama, T. Akema, I. Iuchi. Mechanism of egg envelope digestion by hatching enzymes, HCE and LCE in medaka, Oryzias latipes. The Journal of Biochemistry 148 (2010) 439-448. https://doi.org/10.1093/jb/mvq086.

J. Kavya, G. Amsaveni, M. Nagalakshmi, K. Girigoswami, R. Murugesan, A. Girigoswami. Silver nanoparticles induced lowering of BCl2/Bax causes Dalton's Lymphoma tumour cell death in mice. Journal of Bionanoscience 7 (2013) 276-281. https://doi.org/10.1166/jbns.2013.1135.

V. Keerthana, A. Girigoswami, S. Jothika, D. Kavitha, A. Gopikrishna, T. Somanathan, K. Girigoswami. Synthesis, Characterization and Applications of GO–TiO2 Nanocomposites in Textile Dye Remediation. Iranian Journal of Science and Technology, Transactions A: Science 46 (2022) 1149-1161. https://doi.org/10.1007/s40995-022-01337-y.

P. Thomas, A.C. Sekhar, R. Upreti, M.M. Mujawar, S.S. Pasha. Optimization of single plate-serial dilution spotting (SP-SDS) with sample anchoring as an assured method for bacterial and yeast cfu enumeration and single colony isolation from diverse samples. Biotechnology Reports 8 (2015) 45-55. https://doi.org/10.1016/j.btre.2015.08.003.

S.K. Metkar, A. Girigoswami, D.D. Bondage, U.G. Shinde, K. Girigoswami. The potential of lumbrokinase and serratiopeptidase for the degradation of Aβ 1–42 peptide–an in vitro and in silico approach. International Journal of Neuroscience (2022). https://doi.org/10.1080/00207454.2022.2089137.

K. Liu, P.-c. Liu, R. Liu, X. Wu. Dual AO/EB staining to detect apoptosis in osteosarcoma cells compared with flow cytometry. Medical Science Monitor Basic Research 21 (2015) 15-20. https://doi.org/10.12659/MSMBR.893327.

K. Girigoswami, S.H. Ku, J. Ryu, C.B. Park. A synthetic amyloid lawn system for high-throughput analysis of amyloid toxicity and drug screening. Biomaterials 29 (2008) 2813-2819. https://doi.org/10.1016/j.biomaterials.2008.03.022.

K. Girigoswami, M. Viswanathan, R. Murugesan, A. Girigoswami. Studies on polymer-coated zinc oxide nanoparticles: UV-blocking efficacy and in vivo toxicity. Materials Science and Engineering C 56 (2015) 501-510. https://doi.org/10.1016/j.msec.2015.07.017.

R. Ghosh, K. Girigoswami. NADH dehydrogenase subunits are overexpressed in cells exposed repeatedly to H2O2. Mutation Research/Fundamental Molecular Mechanisms of Mutagenesis 638 (2008) 210-215. https://doi.org/10.1016/j.mrfmmm.2007.08.008.

S.M. Peterson, J.L. Freeman. RNA isolation from embryonic zebrafish and cDNA synthesis for gene expression analysis. JoVE (Journal of Visualized Experiments) 30 (2009) e1470. https://doi.org/10.3791/1470.

K. Jyoti, M. Baunthiyal, A. Singh. Characterization of silver nanoparticles synthesized using Urtica dioica Linn. leaves and their synergistic effects with antibiotics. Journal of Radiation Research and Applied Sciences 9 (2016) 217-227.

G. Agraharam, A. Girigoswami, K. Girigoswami. Nanoencapsulated myricetin to improve antioxidant activity and bioavailability: a study on zebrafish embryos. Chemistry 4 (2021) 1-17. https://doi.org/10.3390/chemistry4010001.

B. Deepika, A. Gopikrishna, A. Girigoswami, M.N. Banu, K. Girigoswami. Applications of Nanoscaffolds in Tissue Engineering. Current Pharmacology Reports 8 (2022) 171-187. https://doi.org/10.1007/s40495-022-00284-x.

A. Girigoswami, K. Girigoswami. Potential Applications of Nanoparticles in Improving the Outcome of Lung Cancer Treatment. Genes 14 (2023) 1370. https://doi.org/10.3390/genes14071370.

P. Pallavi, K. Harini, S. Crowder, D. Ghosh, P. Gowtham, K. Girigoswami, A. Girigoswami. Rhodamine-Conjugated Anti-Stokes Gold Nanoparticles with Higher ROS Quantum Yield as Theranostic Probe to Arrest Cancer and MDR Bacteria. Applied Biochemistry and Biotechnology 195 (2023) 6979-6993. https://doi.org/10.1007/s12010-023-04475-0.

S.S. Ps, A. Guha, B. Deepika, S. Udayakumar, M. Nag, D. Lahiri, A. Girigoswami, K. Girigoswami. Nanocargos designed with synthetic and natural polymers for ovarian cancer management. Naunyn-Schmiedeberg's Archives of Pharmacology 396 (2023) 407–3415. https://doi.org/10.1007/s00210-023-02608-0.

N. Akhtar, S.K. Metkar, A. Girigoswami, K. Girigoswami. ZnO nanoflower based sensitive nano-biosensor for amyloid detection. Materials Science and Engineering C 78 (2017) 960-968. https://doi.org/j.msec.2017.04.118.

S. Nishakavya, A. Girigoswami, A. Gopikrishna, R. Deepa, A. Divya, S. Ajith, K. Girigoswami. Size attenuated copper doped zirconia nanoparticles enhances in vitro antimicrobial properties. Applied Biochemistry and Biotechnology 194 (2022) 3435-3452. https://doi.org/10.1007/s12010-022-03875-y.

S. Lal, R. Verma, A. Chauhan, J. Dhatwalia, I. Guleria, S. Ghotekar, S. Thakur, K. Mansi, R. Kumar, A. Kumari. Antioxidant, antimicrobial, and photocatalytic activity of green synthesized ZnO-NPs from Myrica esculenta fruits extract. Inorganic Chemistry Communications 141 (2022) 109518. https://doi.org/10.1016/j.inoche.2022.109518.

N.R. Jagannathan, Potential of Magnetic Resonance (MR) Methods in Clinical Cancer Research, in Biomedical Translational Research, R.C. Sobti, A. SobtiSpringer, Eds., 2022, p. 339-360. https://doi.org/10.1007/978-981-16-4345-3_21.

P. Sharmiladevi, K. Girigoswami, V. Haribabu, A. Girigoswami. Nano-enabled theranostics for cancer. Materials Advances 2 (2021) 2876-2891. https://doi.org/10.1039/D1MA00069A.

R. Sakthi Devi, A. Girigoswami, M. Siddharth, K. Girigoswami. Applications of gold and silver nanoparticles in theranostics. Applied Biochemistry and Biotechnology 194 (2022) 4187-4219. https://doi.org/10.1007/s12010-022-03963-z.

N. Durán, M. Durán, C.E.d. Souza. Silver and silver chloride nanoparticles and their anti-tick activity: a mini review. Journal of the Brazilian Chemical Society 28 (2017) 927-932. https://doi.org/10.21577/0103-5053.20170045

M. Akter, M.T. Sikder, M.M. Rahman, A.A. Ullah, K.F.B. Hossain, S. Banik, T. Hosokawa, T. Saito, M. Kurasaki. A systematic review on silver nanoparticles-induced cytotoxicity: Physicochemical properties and perspectives. Journal of Advanced Research 9 (2018) 1-16. https://doi.org/10.1016/j.jare.2017.10.008.

C. Liao, Y. Li, S.C. Tjong. Bactericidal and cytotoxic properties of silver nanoparticles. International Journal of Molecular Sciences 20 (2019) 449. https://doi.org/10.3390/ijms20020449.

F. Safari, M. Rabieepor, F. Jamalomidi, Z. Baghaeifar, L. Khodaei. Evaluation of Anti-cancer and Pro-apoptotic Activities of Iranian Green Tea Extract Against A549, PC3, and MCF-7 Cancer Cell Lines. International Journal of Basic Science in Medicine 4 (2019) 113-118. https://doi.org/10.15171/ijbsm.2019.21.

S. Mashjoor, M. Alishahi, Z. Tulaby Dezfuly. In vivo Comparative Toxicity of Silver Nanoparticles and Bio-productivity in Zebrafish (Embryo and Adult Stages). Modares Journal of Biotechnology 9 (2018) 465-472. https://doi.org/biot.modares.ac.ir/article-22-15751-en.html.

S. Cambier, M. Røgeberg, A. Georgantzopoulou, T. Serchi, C. Karlsson, S. Verhaegen, T.-G. Iversen, C. Guignard, M. Kruszewski, L. Hoffmann. Fate and effects of silver nanoparticles on early life-stage development of zebrafish (Danio rerio) in comparison to silver nitrate. Science of The Total Environment 610 (2018) 972-982. https://doi.org/10.1016/j.scitotenv.2017.08.115.

G. Tortella, O. Rubilar, N. Durán, M. Diez, M. Martínez, J. Parada, A. Seabra. Silver nanoparticles: Toxicity in model organisms as an overview of its hazard for human health and the environment. Journal of Hazardous Materials 390 (2020) 121974. https://doi.org/10.1016/j.jhazmat.2019.121974.