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Beauvericin alters the expression of genes coding for key proteins of the mitochondrial chain in ovine cumulus-oocyte complexes

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Abstract

Beauvericin (BEA) is a member of the enniatin family of mycotoxins which has received increasing interest because of frequent occurrence in food and feed. By its ionophoric properties, BEA is able to alter membrane ion permeability uncoupling oxidative phosphorylation. It was also shown to alter oocyte mitochondrial function. In this study, the effects of BEA at 0.5, 1, ,3 and 5 μmol/L on expression of genes coding for key proteins of the mitochondrial chain in ovine oocytes and cumulus cells were evaluated at different time points of in vitro maturation (IVM), germinal vesicle (GV; t = 0), metaphase I (MI; t = 7 h), and metaphase II (MII; t = 24 h). The expression of nuclear (TFAM, NDUFA12, UQCRH, COX4, ATP5O) and mitochondrial (ND1, COX1, COX2, ATP6, ATP8) genes coding for proteins of Complexes I, III, IV, and V was analyzed by qRT-PCR. After BEA exposure, perturbed expression of all genes was observed in cumulus cells and in oocytes at the MI stage (7 h IVM). Expression of ND1, UQCRH, COX4 and ATP5O was downregulated in cumulus cells and upregulated in oocytes starting from 0.5 μmol/L BEA. Expression of TFAM, NDUFA12, COX1, COX2, ATP6, and ATP8 was upregulated starting from 1 μmol/L in cumulus cells and from 3 μmol/L in oocytes. Cumulus cells and oocytes displayed different gene expression patterns upon BEA exposure. The downregulation in cumulus cells of four genes coding for proteins of mitochondrial complexes could represent a major toxic event induced by BEA on the cumulus-oocyte complex which may result in mitochondrial functional alteration.

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Abbreviations

ABC:

ATP-binding cassette

ATP:

Adenosine triphosphate

ATP5O:

ATP synthase O subunit

ATP6:

ATP synthase 6

ATP8:

ATP synthase 8

BEA:

Beauvericin

COC:

Cumulus-oocyte complex

COX:

Cytochrome c oxidase

EFSA:

European Food Safety Authority

GV:

Germinal vesicle

IVM:

In vitro maturation

MI:

Metaphase I

MII:

Metaphase II

mtDNA:

Mitochondrial DNA

ND:

NADH dehydrogenase

NDUFA12:

NADH: ubiquinone oxidoreductase subunit A12

OXPHOS:

Oxidative phosphorylation

TFAM:

Mitochondrial transcription factor A

UQCRH:

Ubiquinol-cytochrome c reductase hinge protein

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Funding

This study was funded by UE-FSE-FSER, PON RI 2014-2020 Action I.1—“Innovative doctoral of industrial interest”—a.a. 2016/2017, XXXII cycle, PhD Program “Functional and Applied Genomics and Proteomics—DOT1302781”—Grant No. 2. A.M. was also supported by the Research Grant No. VERI00086 in the framework of the Project “Demetra” (Dipartimenti di Eccellenza 2018-22; CUP code: C46C18000530001) funded by the Italian Ministry for Education, University and Research.

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Correspondence to Antonella Mastrorocco.

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Mastrorocco, A., Ciani, E., Nicassio, L. et al. Beauvericin alters the expression of genes coding for key proteins of the mitochondrial chain in ovine cumulus-oocyte complexes. Mycotoxin Res 37, 1–9 (2021). https://doi.org/10.1007/s12550-020-00409-5

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  • DOI: https://doi.org/10.1007/s12550-020-00409-5

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