Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology
Tinospora cordifolia ameliorated titanium dioxide nanoparticle-induced toxicity via regulating oxidative stress-activated MAPK and NRF2/Keap1 signaling pathways in Nile tilapia (Oreochromis niloticus)
Graphical abstract
Introduction
Titanium dioxide nanoparticle (TNP) is the most widely used common constituent of various personal, domestic, and food products (Luo et al., 2014). TNP adheres to the bacterial cell surface causing the generation of reactive oxygen species (ROS), disruption of the membrane integrity, leakage of cellular contents, and bacterial death (Foster et al., 2011). Due to this bactericidal effect, TNP can be applied in fish ponds to prevent or mitigate bacterial disease outbreaks (Cheng et al., 2008; Cheng et al., 2009; Jovanović et al., 2015). Unfortunately, various studies demonstrated that TNP is immunotoxic and exposure to TNP causes molecular, biochemical, physiological, and histological alterations in fish (Ramsden and Smith, 2009; Chen et al., 2011; Jovanovic and Palic, 2012; Purushothaman et al., 2014) resulting in increased mortality and morbidity during the subsequent challenge by bacterial pathogens (Jovanović et al., 2015). TNP can be absorbed by the gill, skin, and intestine of fish (Handy et al., 2008; Fırat and Bozat, 2019). Thus, environmental contamination by TNP could negatively affect fish survival during disease outbreaks.
Excessive generation of free radicals plays a vital role in mediating nanotoxicity (Khanna et al., 2015; Ferraro et al., 2020) which leads to damage of biological macromolecules and cell death. Plants and phytochemicals are the richest sources of antioxidants capable of scavenging the free radicals thereby decreasing the stress responses and increasing the immune responses, growth, and the nutritional value of farmed fish (Reverter et al., 2017). Several in vitro and in vivo studies with various nanoparticles and different antioxidants have shown to prevent oxidative stress-induced toxicity (Guo et al., 2013; Sarkar and Sil, 2014; Gonzalez-Esquivel et al., 2015; Abdel-Daim et al., 2019; Abdou et al., 2019; Alkaladi, 2019; Tayemeh et al., 2020).
Tinospora cordifolia (Family - Menispermaceae) commonly known, as “Amruth” or “Guduchi”, is a large, deciduous extensively spreading climbing shrub native to India. T. cordifolia is an important herb valued in Ayurveda for its rejuvenating, immune-boosting and detoxifying properties. It is useful in the treatment of several ailments including fevers, diabetes, jaundice, urinary problems, skin diseases, chronic diarrhea, heart diseases, leprosy, helminthiasis, and rheumatoid arthritis (Upadhyay et al., 2010). The whole plant of T. cordifolia contains furanolactone, diterpenoid lactones, cleodrane derivatives, columbin tinosporides, tinosporin, jateorine, berberine, disaccharides, choline, cordifolide, and cordifol, which has biological actions such as vasorelaxant, anti-oxidant, anti-inflammatory, immune-modulatory, anti-microbial, anti-hypertensive, hepato-protective, and anti-viral (Reddy et al., 2009; Alexander et al., 2010; Saha and Ghosh, 2012; Joshi and Kaur, 2016; Tiwari et al., 2018; Sharma et al., 2019). Currently, there are no reported studies on the efficacy of T. cordifolia to overcome nanotoxicity in the aquatic environment.
The present investigation was aimed to elucidate the mechanism of toxicity caused by TNP; and to evaluate the efficacy of T. cordifolia supplemented feed on TNP-induced alterations in growth performance, biochemical, inflammatory, pathological, and signaling pathways and to study the disease resistance against Aeromonas hydrophila in Nile tilapia (Oreochromis niloticus).
Section snippets
Chemicals
Titanium dioxide nanoparticle (TNP anatase, nanopowder, <25 nm, 99.7% purity), ethyl 3-aminobenzoate methanesulfonate (MS-222 98%), Folin–Ciocalteu reagent, gallic acid, aluminium chloride, quercetin, ascorbic acid, phosphomolybdenum, 2,2-diphenyl-1-picrylhydrazyl (DPPH), Griess reagent, DL-alanine, 2-oxoglutarate, 2, 4 dinitrophenyl hydrazine (DNPH), l-aspartate, para-nitrophenyl phosphate, triton X-100, and 2′,7′ dichloro-dihydro-fluorescein diacetate (DCFH-DA) were purchased from Sigma
Results and discussion
The generation of free radicals and oxidative damage are the major contributors of nanotoxicity. Thus, a prophylactic approach to control this may be an effectual tool to combat nanotoxicity. A cost-effective approach for the prevention and treatment of nanotoxicity that does not compromise with the bactericidal effect of TNP is considerable. The present study evaluated TNP-induced toxicity in Nile tilapia and the efficacy of TCE to alleviate the oxidative stress parameters, inflammatory
Conclusion
TNP induced sub-lethal effects that were appreciably decreased by TCE supplemented feed. Dietary supplementation with TCE attenuated TNP-induced oxidative stress mediated by regulation of the NRF2/Keap1 antioxidant pathway and ERK/p38 cell survival pathway to restrain the generation of ROS. The study also suggests that TCE can promote growth and reduce the adverse effects caused by environmental stress by improving the antioxidant defense system, inflammatory response, and disease resistance of
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgement
The first author thanks Kerala State Council for Science, Technology and Environment, Woman Scientist Division – Project grant no. 1107/2017/KSCSTE for financial assistance. We thank the authorities of Kerala University of Fisheries Science and Technology for providing all the necessary facilities for conducting the experiments.
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