Effects of dietary curcumin inhibit deltamethrin-induced oxidative stress, inflammation and cell apoptosis in Channa argus via Nrf2 and NF-κB signaling pathways

Highlights

• Del exposure could lead to body damage of C. argus.

• Optimum dietary curcumin could attenuate Del-induced oxidative stress of C. argus.

• Optimum dietary curcumin could improve Del-induced inflammation response of C. argus.

• Optimum dietary curcumin could improve Del-induced cell apoptosis of C. argus.

• Optimum dietary curcumin could improve Del-induced damage via Nrf2 and NF-κB signaling pathways.

Abstract

The current study evaluated the ameliorative effects of dietary curcumin (CUR) on oxidative stress, inflammation and cell apoptosis in Channa argus exposed to deltamethrin (DEL) for 28 d. This study was divided into five groups: the first group served as a control group, and the second, third, fourth and fifth groups were exposed to DEL (0.242 ppb) in water and fed CUR-supplemented diets at 0, 100, 200 and 400 mg/kg, respectively. The results showed that the biochemical parameter levels (ADA, COR, LDH, AST and ALT) and the innate immune parameter levels (LYS, CRP, MPO, C3, C4 and IgM) in the serum of fish exposed to DEL were notably increased (P < 0.05), and dietary supplementation with 200 and 400 mg/kg CUR in the DEL exposure period significantly reduced the levels of these parameters (P < 0.05). The levels of ROS, CAT, GSH, SOD, GSH-Px, GST and GSH-Rt in the gill, kidney, spleen, and liver of fish exposed to DEL were significantly decreased (P < 0.05), and there were notable increases (P < 0.05) in the 200 and 400 mg/kg CUR treatments. MDA content exhibited an opposite trend. The results of RT-qPCR analysis showed that dietary supplementation with CUR attenuated the inflammatory response of fish after DEL exposure by downregulating the expression of pro-inflammatory genes (NF-κB p65, IL-1β, IL-6, IL-8, IL-12 and TNF-α) in the liver and spleen and upregulating the expression of anti-inflammatory genes (TGF-β, IκBα and IL-10). Dietary supplementation with CUR was observed to improve the level of oxidative stress of fish after DEL exposure by downregulating the mRNA levels of Keap1 in the liver and spleen and upregulating the mRNA levels of Nrf2, Cu/Zn SOD, GSH-Px, GST and CAT. Dietary supplementation with CUR was determined to improve the cell apoptosis of fish after DEL exposure by downregulating the expression of pro-apoptotic genes (Bcl-2) in the liver and spleen and upregulating the expression of anti-apoptotic genes (Bax, Cas-3, Cas-8, Cas-9, and p53). In brief, the results of our study indicated that supplying optimal dietary CUR could attenuate deltamethrin-induced oxidative stress, inflammation and cell apoptosis in C. argus via the Nrf2 and NF-κB signaling pathways.

Introduction

In recent decades, with the rapid development of intensive agriculture and the chemical industry, an increasing number of farm chemicals have been produced and widely used in agriculture, medicine and industry around the world (Jin et al., 2015; Sehonova et al., 2018; Aliko et al., 2018). As a common pesticide that is widely used worldwide, pyrethroids have successively replaced organochlorine, organophosphorus and carbamate pesticides due to their low toxicity, low persistence, high efficacy and biological action (Guardiola et al., 2014; Sapana and Gupta, 2014; Velíšek et al., 2007). According to prior reports, pyrethroids accounted for 38% of the worldwide pesticide market share in 2015, and their usage increased thereafter (Singh et al., 2016; Chen et al., 2016). Deltamethrin (DEL) (C₂₂H₁₉Br₂NO₃), a synthetic pyrethroid pesticide, is widely used in agriculture, forestry and aquaculture (Milam et al., 2000; Bradbury and Coats, 1989; Parvez and Raisuddin, 2006). However, DEL applied to cultivated fields can be washed or permeated into both surface water and groundwater, which would increase the concentration of drug residues in aquatic environments and harm the health of aquatic animals (Ramwell et al., 2004; Koprucu et al., 2006; Siegler et al., 2015). According to a previous report, DEL has been detected in the Ebro River Delta at concentrations ranging from 2 ng/L to 58.8 ng/L (Feo et al., 2010). A DEL concentration of up to 4 μg/L was detected in a stream in Cintra, Brazil (Belluta et al., 2010). DEL concentrations ranging from 0.033 to 0.45 μg/L have been detected in the Indus and Ravi rivers (Mahboob et al., 2015). Moreover, in the Indus River, Pakistan, DEL concentrations in the muscle of Cyprinus carpio ranged from 0.490 to 0.839 μg/g, whereas it ranged from 0.214 to 0.318 μg/g in the sampled sediments (Jabeen et al., 2015). The average concentrations of DEL in the muscle of omnivorous and carnivorous fish in Sichuan, Chongqing, Anhui and Hubei provinces in China were 1.72 and 0.76 μg/kg, respectively (Xu, 2017). Previously obtained evidence has demonstrated that DEL exposure could induce immunosuppression, oxidative stress and tissue damage in aquatic animals, such as Channa punctata, Danio rerio, Carassius carassius, Penaeus monodon, Oreochromis niloticus, Eriocheir sinensis, Cyprinus carpio, Sparus aurata L. and Gobiocypris rarus (Atif et al., 2005; Awoyemi et al., 2019; Abdel-Daim et al., 2015; Hong et al., 2018; Haverinen and Vornanen, 2016; Tu et al., 2012; Jindal et al., 2019; Guardiola et al., 2014; Zhang et al., 2020). Therefore, it is urgently important to identify a method to decrease the damaging effects of DEL on aquaculture ecosystems.

Currently, Chinese herbs and medicinal plant extracts have been investigated as alternatives to chemical drugs to alleviate toxicity in aquaculture because of their unique biological properties, including antibacterial, antioxidant, immunostimulant and antiparasite activities (Kong et al., 2020a, Kong et al., 2021; Jindal et al., 2019). Curcumin (CUR, C₂₁H₂OO₆), also known as diferuloymethane, is a hydrophobic polyphenol compound extracted from the rhizome of turmeric (Curcuma longa L.) (Mathai, 1976; Hatcher et al., 2008; Oliveira et al., 2016) and widely used as a green and natural spice, colorant, preservative and flavoring in the food industry. CUR has a wide range of biological properties, such as antioxidation, anti-inflammatory, antibacterial, antiviral, antitumor, lipid-lowering, liver and gallbladder protecting and digestion promoting actions (Al-Reza et al., 2010; Gul and Bakht, 2015; Sahne et al., 2016; Akram et al., 2010; Noorafshan and Ashkani-Esfahani, 2013; Negi et al., 1999). Moreover, a number of studies have investigated the effects of CUR on aquatic animals, such as crucian carp (Carassius auratus) (Jiang et al., 2016), Jian carp (Cyprinus carpio var. Jian) (Cao et al., 2015), grass carp (Ctenopharyngodon idellus) (Liu et al., 2017; Ming et al., 2020), Nile tilapia (Oreochromis niloticus) (Mahmoud et al., 2017; Mohamed et al., 2020), and silver catfish (Rhamdia quelen) (Baldissera et al., 2018). However, little is known about the effects of dietary CUR on DEL-induced oxidative stress, inflammation and cell apoptosis in fish.

Channa argus (C. argus), an economically important fish, is widely farmed in Asia (Courtenay and Williams, 2004). Aquaculture environmental pollution has considerably harmed the healthy growth of C. argus (Kong et al., 2020b). Some studies have indicated that CUR improves the inflammatory response of fish after exposure to toxic substances or bacteria by inhibiting the nuclear factor kappa B (NF-κB) signaling pathway (Ming et al., 2020; Cao et al., 2015). In light of these findings, this study investigated the ameliorative effects of dietary CUR on C. argus exposed to DEL; specifically, antioxidant levels, cell apoptosis, immunity, and the expression of genes associated with the nuclear factor erythroid 2-related factor 2 (Nrf2) and NF-κB signaling pathways were examined.