Oxidative Stress and Its Role in Aflatoxin Toxicity: History
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Contributor:
Martha Cebile Jobe
,
Doctor M. N. Mthiyane
,
Phiwayinkosi V. Dludla
,
Sithandiwe E. Mazibuko-Mbeje
,
Damian C. Onwudiwe
,
Mulunda Mwanza

Aflatoxin B1 is a secondary metabolite with a potentially devastating effect in causing liver damage in broiler chickens, and this is mainly facilitated through the generation of oxidative stress and malonaldehyde build-up. In the past few years, significant progress has been made in controlling the invasion of aflatoxins.

  • aflatoxins
  • oxidative stress
  • phytochemicals
  • antioxidants
  • broilers

1. Introduction

Mycotoxins are classified as a wide range of harmful compounds, with aflatoxins, fumonisin, trichothecenes, ochratoxins, and zearalenone, with aflatoxin being the most studied. The harmful effects of mycotoxins have led regulatory entities, such as the Food Agriculture Organization and the World Health Organization, to establish regulatory measurements to monitor and control the levels of mycotoxins in foods and feed [1][2]. The term “mycotoxicosis” emerged for the first time in 1962 in a study of animal sickness, following the deaths of approximately 100,000 young turkeys in the United Kingdom in 1960 [3][4]. The toxin that caused poultry deaths was linked to Aspergillus flavus that was isolated from the feed; hence, the discovery of aflatoxins marked the beginning of contemporary mycotoxin study. Over the years, research and field investigations have revealed that mycotoxins, which are secondary metabolites produced by some fungal species, are responsible for both food spoilage and the development of many diseases [5][6]. Aflatoxin B1 (AFB1) is well-known among the different aflatoxin types because of its widespread occurrence, high toxicity, and economic implications across the world [7]. According to the guidelines of the International Agency for Research on Cancer (IARC), AFB1 is classified as Group 1 [8], with widely reported hepatotoxic, carcinogenic, teratogenic, and immunosuppressive effects in mammals and poultry at large [9][10][11][12].
This has led to a significant interest in understanding the health implications of aflatoxins, with the PubMed search showing over 1493 records on this carcinogen, suggesting a considerable growth of publications over the years [13][14][15]. At present, oxidative stress appears to be one of the prime mechanisms of AFB1-induced toxicity in various disease settings. Briefly, exposure to AFB1 can induce an abnormally increased formation of free radicals, hence generating lipid peroxidation through their reaction with lipid products in the body: a consequence that leads to massive cellular damage which ultimately causes death to both animals and humans [16][17]]. Even more specifically for animals, AFB1 can induce the overproduction of toxic reactive oxygen species (ROS), which can also contribute to the formation of oxidative stress [18][19]. Apparently, this process can activate the cytochrome P450 (CYP450) enzyme system and produce AFB1-8, 9-epoxide, a toxic metabolite of AFB1 [20]. As a result, the formation of DNA adducts can therefore lead to genetic changes and cause the transformation of liver hepatocytes, which is the major detoxification hub within the body [21].
Several physical, chemical, and biological methodologies have been explored to eliminate aflatoxins, as the control of mycotoxins is a critical aspect of nutrition research [22][23][24]. Consistently, several compounds have been used to reduce aflatoxin toxicity in poultry feed. Such compounds include zeolites [25], sodium bentonite [26], and mannose oligosaccharides [27]. On another hand, experimental results are recommending the use of phytochemicals because they can ameliorate aflatoxin toxicity in experimental models [28]. These compounds can act as modulators of gene expression and/or enzymatic activities of biotransformation enzymes involved in aflatoxin activation and detoxification [29][30][31][32]. Indeed, some plant products contain abundant phytochemicals that can be effective against aflatoxin toxicity in broilers [33]. This is especially relevant since phytochemicals are known to contain abundant antioxidant properties that are essential in protecting against oxidative stress-induced cellular damage [34][35]. For example, increasing interest has been placed on unravelling the therapeutic effects of phytochemicals like berberine [36], carvacrol, curcumin [37][38], proanthocyanidins [39][40], quercetin [41][42], resveratrol [43], and silymarin [44][45][46] in protecting against oxidative stress, leading to alleviation of cell damage in many experimental models [47][48]. In fact, such information has not been comprehensively reviewed in relation to aflatoxin-induced toxicity.

2. An Overview of Oxidative Stress and Its Role in Aflatoxin Toxicity

Oxidative stress defines an imbalance between the production of free radicals, including ROS, and the counteractive protective effects of intracellular antioxidant systems. Thus far, many studies have been published informing on the important role oxidative stress plays in the development and progression of various diseases [49][50][51]. While free radicals are essential for an efficient physiological process, their overproduction has been linked with the pathological state, through their attack on essential biomolecules including proteins, carbohydrates, lipids, and nucleic acids [52][53]. This process is known to have a devastating outcome in vital biochemical processes and cell signaling mechanisms that eventually render cellular damage. For example, lipid peroxidation, due to oxidants such as free radicals pouncing on lipids containing carbon–carbon double bonds [54], has long been linked to liver damage in broiler chickens poisoned with the antibiotic monensin, which is derived from the bacterium Streptomyces cinnamonensis [55]. Indeed, many internal and external factors are implicated in the production of free radicals that accelerate oxidative damage. In broiler chickens, for example, aflatoxin or its metabolites are directly induced through enhanced production of free radicals and lipid peroxides, resulting in cell damage [56][57]. An aspect of particular interest is hepatotoxicity, since liver CYP450 enzyme systems can metabolize aflatoxins, leading to chain activation of other free radical species like superoxide radicals and hydrogen peroxide [37][58]. In brief, it is well established that aflatoxin can be metabolized in the liver to its reactive form, AFB1-8,9-epoxide, which produces adducts upon reacting with both DNA and protein [59]. Subsequently, this process is instrumental in exacerbating apoptosis and facilitating cellular damage.
Consumption of AFB1-contaminated feed has been linked to toxicity in broilers [60], immunosuppression [61], and increased disease susceptibility [58][62]. The harmful effect of aflatoxins was examined using in vivo and in vitro experimental models see Table 1, reporting on the development of oxidative stress that is consistent with the exacerbation of hepatoxicity [63][64]. The weakening of antioxidant defences in murine livers, human lymphocytes, and bovine peripheral blood mononuclear cells, due to AFB1-induced generation of free radicals, has also been reported [65][66][67]. Oxidative stress in broilers has also been linked to the accumulation of AFB1 absorbed from the gastrointestinal tract causing toxicity in the liver, the main detoxification organ [10]. Following liver damage, the metabolism of proteins, carbohydrates, and lipids is hampered. An increase in free radical production due to AFB1 leads to lipid peroxidation in broiler chickens [68][69], with concomitant depletion of tissue/cellular sulphydryl forms of thiols. Glutathione (GSH) is the most important non-enzymatic antioxidant and should be considered an early biological marker of oxidative stress [70]. The conjugation of active AFB1 with GSH, which is mediated by glutathione S-transferases (GST), is a crucial process in the detoxification and excretion of this toxin [71]. Concerning that, poultry species have phase-I liver enzymes for activating AFB1 but weak phase-II GST enzyme productivity for detoxifying AFB1 and its toxic metabolites [72]. Importantly, AFB1 mainly causes an increase in malondialdehyde (MDA) concentrations, which may lead to a decrease in enzymatic antioxidants such as catalase (CAT), glutathione peroxidase (GPx), and superoxide dismutase (SOD) [37]. The current report discusses published information on the role of oxidative stress in broiler chickens, especially how it is influenced by the aflatoxin-contaminated diet or exposure to it. Moreover, it remains essential to understand whether the activation of nuclear factor erythroid 2-related factor 2 (Nrf2), the main intracellular antioxidant response mechanism, can ameliorate or protect against oxidative stress in relation to aflatoxins [33][62][73]. Importantly, Nrf2 can be activated by some phytochemicals and this mechanism is known to control the expression of a group of antioxidants and detoxification genes that give a protective role against oxidative stress and has been established against multiple diseases such as cancer, pulmonary disease, and inflammation [74][75].
Table 1. Summary of the literature reporting on the impact of the oxidative stress caused by aflatoxins in broiler chickens.
Reference Experimental Model Dosage and Treatment Duration Findings
[76] Broilers (aged 35 d) Received 100 µg/kg for 4 weeks Aflatoxin B1 (AFB1) significantly decreased the relative body weights of bursa of Fabricius, antioxidant enzyme activities of total superoxide dismutase (SOD), catalase (CAT), glutathione peroxidase (GPx), glutathione transferase (GST), and total antioxidation capacity, while it increased the malonaldehyde (MDA) content.
[63] Avian broilers (aged 120 d) Received 100 µg/kg for 4 weeks Antioxidant capacity (CAT, GPx, and glutathione (GSH) were reduced, and lipid peroxidation MDA and DNA damage (8-OHdG) were increased.Administration of AFB1-induced liver injury and decreased total protein and albumin concentrations. Induced hepatotoxicity by increasing alanine aminotransferase and aspartate aminotransferase activities. Also, mRNA and activity of enzymes responsible for the bioactivation of AFB1 into AFBO, which included cytochrome P450 (CYP450) A1, 1A2, 2A6, and 3A4, were negatively affected in liver microsomes after 2-week exposure to AFB1.
[77] Culture media (Primary broiler hepatocytes) Received 0.5, 1, 2.5, and 5 µmol/L AFB1 evoked mitochondrial generation of reactive oxygen species (ROS). AFB1 also increased the percentage of apoptotic cells and the expression of caspase-9 and caspase-3. This was also consistent with the impairment of mitochondrial functions, activated ROS, induced apoptosis, and upregulated messenger RNA (mRNA) expression of nuclear factor erythroid 2-related factor 2 (Nrf2). Whereas, the mRNA expressions of nicotinamide adenine dinucleotide phosphate (NADPH), quinone oxidoreductase 1, SOD, and heme oxygenase 1 were reduced.

This entry is adapted from the peer-reviewed paper 10.3390/molecules28145369

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