Piperine inhibits aflatoxin B1 production in Aspergillus flavus by modulating fungal oxidative stress response

Caceres, Isaura; Khoury, Rhoda El; Bailly, Sylviane; Oswald, Isabelle P.; Puel, Olivier; Bailly, Jean-Denis

doi:10.1016/j.fgb.2017.08.005

Cited by 73 publications

(76 citation statements)

References 56 publications

(59 reference statements)

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“…After treatment with 3.5% ethanol, all catalase genes including Cat, Cat1, Cat2, CatA, and Cu, Zn superoxide dismutase gene sod1 were up-regulated, while only Mn superoxide dismutase gene mnSOD was down-regulated. Similarly, piperine exposure significantly induced decreased expression of veA together with the overexpression of several bZIP transcription factors genes like atfA, atfB, and ap-1 and genes encoding catalase such as catA, cat2, and superoxide dismutase like sod1 in A. flavus (Caceres et al, 2017). Moreover, this gene response was coupled with an obvious increase of catalase enzymatic activity (Caceres et al, 2017).…”

Section: Discussionmentioning

confidence: 95%

“…In the meantime, AFs biosynthesis is thought to protect the fungus against oxidative stress (Wang et al, 2019). Several previous studies have indicated that some AFs inhibitors can regulate the stress response system of fungi (Reverberi et al, 2005;Grintzalis et al, 2014;Sun et al, 2015;Caceres et al, 2017). After treatment with 3.5% ethanol, all catalase genes including Cat, Cat1, Cat2, CatA, and Cu, Zn superoxide dismutase gene sod1 were up-regulated, while only Mn superoxide dismutase gene mnSOD was down-regulated.…”

Section: Discussionmentioning

confidence: 99%

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Ethanol Inhibits Aflatoxin B1 Biosynthesis in Aspergillus flavus by Up-Regulating Oxidative Stress-Related Genes

et al. 2020

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As the most carcinogenic, toxic, and economically costly mycotoxins, aflatoxin B 1 (AFB 1) is primarily biosynthesized by Aspergillus flavus and Aspergillus parasiticus. Aflatoxin biosynthesis is related to oxidative stress and functions as a second line of defense from excessive reactive oxygen species. Here, we find that ethanol can inhibit fungal growth and AFB 1 production by A. flavus in a dose-dependent manner. Then, the ethanol's molecular mechanism of action on AFB 1 biosynthesis was revealed using a comparative transcriptomic analysis. RNA-Seq data indicated that all the genes except for aflC in the aflatoxin gene cluster were down-regulated by 3.5% ethanol. The drastic repression of aflatoxin structural genes including the complete inhibition of aflK and aflLa may be correlated with the down-regulation of the transcription regulator genes aflR and aflS in the cluster. This may be due to the repression of several global regulator genes and the subsequent overexpression of some oxidative stress-related genes. The suppression of several key aflatoxin genes including aflR, aflD, aflM, and aflP may also be associated with the decreased expression of the global regulator gene veA. In particular, ethanol exposure caused the decreased expression of stress response transcription factor srrA and the overexpression of bZIP transcription factor ap-1, C 2 H 2 transcription factors msnA and mtfA, together with the enhanced levels of anti-oxidant enzymatic genes including Cat, Cat1, Cat2, CatA, and Cu, Zn superoxide dismutase gene sod1. Taken together, these RNA-Seq data strongly suggest that ethanol inhibits AFB 1 biosynthesis by A. flavus via enhancing fungal oxidative stress response. In conclusion, this study served to reveal the anti-aflatoxigenic mechanisms of ethanol in A. flavus and to provide solid evidence for its use in controlling AFB 1 contamination.

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Section: Discussionmentioning

confidence: 95%

Section: Discussionmentioning

confidence: 99%

Ethanol Inhibits Aflatoxin B1 Biosynthesis in Aspergillus flavus by Up-Regulating Oxidative Stress-Related Genes

et al. 2020

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“…The aflatoxin production and fungal growth were inhibited by piperine in a dose-dependent manner. Expression analysis of the AF gene cluster demonstrated that almost all genes were down regulated (Caceres et al, 2017). Exposure to piperine also resulted in decreased transcript levels of the global regulator veA together with an overexpression of genes coding several basic leucine zipper (bZIP) transcription factors such as atfA, atfB and ap-1 and genes belonging to superoxide dismutase and catalase families (Caceres et al, 2017).…”

Section: Essential Oils Polyphenols and Alkaloidsmentioning

confidence: 99%

“…Expression analysis of the AF gene cluster demonstrated that almost all genes were down regulated (Caceres et al, 2017). Exposure to piperine also resulted in decreased transcript levels of the global regulator veA together with an overexpression of genes coding several basic leucine zipper (bZIP) transcription factors such as atfA, atfB and ap-1 and genes belonging to superoxide dismutase and catalase families (Caceres et al, 2017). In total, 366 and 87 genes of A. flavus were significantly up-and down-regulated, respectively, when the fungus underwent exposure to resveratrol, a polyphenol isolated from red wine .…”

Section: Essential Oils Polyphenols and Alkaloidsmentioning

confidence: 99%

Aflatoxins: biosynthesis, prevention and eradication

Šimončicová

Kaliňáková

Kryštofová

2017

Acta Chimica Slovaca

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Filamentous fungi belonging to Aspergilli genera produce many compounds through various biosynthetic pathways. These compounds include a spectrum of products with beneficial medical properties (lovastatin) as well as those that are toxic and/or carcinogenic which are called mycotoxins. Aspergillus flavus, one of the most abundant soil-borne fungi, is a saprobe that is able growing on many organic nutrient sources, such as peanuts, corn and cotton seed. In many countries, food contamination by A. flavus is a huge problem, mainly due to the production of the most toxic and carcinogenic compounds known as aflatoxins. In this paper, we briefly cover current progress in aflatoxin biosynthesis and regulation, pre-and postharvest preventive measures, and decontamination procedures.

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“…Interestingly, bZIP transcription factor Yap-1Leu558Trp substitution in A. flavus is confirmed as being responsible for voriconazole-resistant phenotypes [32]. When A. flavus was exposed to piperine, transcript levels of bZIP transcription factors atfA, atfB and ap-1 were increased [33]. Genome analysis of A. flavus identified 22 bZIP-type TFs [34], however, the functions of most bZIP-type TFs are still not clear.In this study, the ortholog gene of bZIP-type TF rsmA, termed AflRsmA, was deleted and functionally characterized in A. flavus.…”

mentioning

confidence: 99%

The bZIP Transcription Factor AflRsmA Regulates Aflatoxin B1 Biosynthesis, Oxidative Stress Response and Sclerotium Formation in Aspergillus flavus

Wang

Zha

et al. 2020

Toxins

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Fungal secondary metabolites play important roles not only in fungal ecology but also in humans living as beneficial medicine or harmful toxins. In filamentous fungi, bZIP-type transcription factors (TFs) are associated with the proteins involved in oxidative stress response and secondary metabolism. In this study, a connection between a bZIP TF and oxidative stress induction of secondary metabolism is uncovered in an opportunistic pathogen Aspergillus flavus, which produces carcinogenic and mutagenic aflatoxins. The bZIP transcription factor AflRsmA was identified by a homology research of A. flavus genome with the bZIP protein RsmA, involved in secondary metabolites production in Aspergillus nidulans. The AflrsmA deletion strain (∆AflrsmA) displayed less sensitivity to the oxidative reagents tert-Butyl hydroperoxide (tBOOH) in comparison with wild type (WT) and AflrsmA overexpression strain (AflrsmA OE ), while AflrsmA OE strain increased sensitivity to the oxidative reagents menadione sodium bisulfite (MSB) compared to WT and ∆AflrsmA strains. Without oxidative treatment, aflatoxin B 1 (AFB 1 ) production of ∆AflrsmA strains was consistent with that of WT, but AflrsmA OE strain produced more AFB 1 than WT; tBOOH and MSB treatment decreased AFB 1 production of ∆AflrsmA compared to WT. Besides, relative to WT, ∆AflrsmA strain decreased sclerotia, while AflrsmA OE strain increased sclerotia. The decrease of AFB 1 by ∆AflrsmA but increase of AFB 1 by AflrsmA OE was on corn. Our results suggest that AFB 1 biosynthesis is regulated by AflRsmA by oxidative stress pathways and provide insights into a possible function of AflRsmA in mediating AFB 1 biosynthesis response host defense in pathogen A. flavus.Key Contribution: Without oxidative treatment, deletion of AflrsmA has no impact on aflatoxin B 1 (AFB 1 ) biosynthesis in comparison with the wild type strain. However, the AflrsmA disruptant produces less AFB 1 on corn seeds and on YGT medium containing oxidative reagent menadione sodium bisulfite or tert-Butyl hydroperoxide.Toxins 2020, 12, 271 2 of 17 basic leucine zipper (bZIP) domain. The bZIP-type transcription factor as one of the largest families of dimerizing TFs is widely distributed in the all eukaryotes genomes. The first bZIP-type TF was discovered in humans over 30 years ago [2]. Then, it was found that bZIP-type TFs are involved in metabolism, development, cell cycle, reproduction, and programmed cell death [1]. In plants, the functions of bZIP-type TFs include abiotic stress response, metabolism, mediating pathogen defense, hormone signaling, and senescence [3]. bZIP-type TFs are involved in various biological processes in fungi (described below).In Saccharomyces cerevisiae, the first bZIP-type TF called Yap (yeast activator protein) was found [4], then a subset of YAP TFs (YAP1-YAP8) have been well defined [5]. Several bZIP proteins have been reported in filamentous fungi, such as Aspergillus spp. [6-11], Neurospora crassa [12], plant pathogens Fusarium graminearum [13], Magnaporthe oryzae [14], and ...

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Piperine inhibits aflatoxin B1 production in Aspergillus flavus by modulating fungal oxidative stress response

Cited by 73 publications

References 56 publications

Ethanol Inhibits Aflatoxin B1 Biosynthesis in Aspergillus flavus by Up-Regulating Oxidative Stress-Related Genes

Ethanol Inhibits Aflatoxin B1 Biosynthesis in Aspergillus flavus by Up-Regulating Oxidative Stress-Related Genes

Aflatoxins: biosynthesis, prevention and eradication

The bZIP Transcription Factor AflRsmA Regulates Aflatoxin B1 Biosynthesis, Oxidative Stress Response and Sclerotium Formation in Aspergillus flavus

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