Ochratoxin A affects oocyte maturation and subsequent embryo developmental dynamics in the juvenile sheep model
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ORIGINAL ARTICLE
Ochratoxin A affects oocyte maturation and subsequent embryo developmental dynamics in the juvenile sheep model Maria Elena Dell’Aquila 1 & Shafaq Asif 2 & Letizia Temerario 1 & Antonella Mastrorocco 1,2 & Giuseppina Marzano 1,3 & Nicola Antonio Martino 1,4 & Giovanni Michele Lacalandra 5 & Bernard AJ Roelen 6 Augusto Carluccio 2 & Domenico Robbe 2 & Fiorenza Minervini 7
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Received: 23 March 2020 / Revised: 12 September 2020 / Accepted: 18 September 2020 # The Author(s) 2020
Abstract The genotoxic and nephrotoxic mycotoxin Ochratoxin A (OTA) has also been reported to have adverse effects on oocyte maturation and embryo development. Previous studies on the effects of OTA on female fertility have used micromolar concentrations, but no information is available to date on effects in a more relevant nanomolar range. This study used a juvenile sheep model to evaluate the effects of oocyte exposure to low levels of OTA on maturation, fertilization, and embryo development. Further, it was investigated whether different mechanisms of action of OTA could be responsible for varying toxic effects at different levels of exposure. Cumulus-oocyte-complexes (COCs) were exposed to 10 μmol/L–0.1 nmol/L OTA during in vitro maturation and evaluated for cumulus viability, oocyte maturation, and bioenergetic/oxidative status. COCs were subjected to in vitro fertilization, embryo culture, and embryo quality assessment via morphology, viability, bioenergetic/oxidative status, and time-lapse monitoring. At micromolar concentrations, OTA induced cytotoxic effects, by reducing cumulus expansion and oocyte maturation. OTA altered temporospatial dynamics of zygote pronuclear formation and embryo morphokinetics. Blastocysts, even morphologically normal, were found to undergo collapse events, which were probably related to boosted blastocyst mitochondrial activity. At nanomolar concentrations, OTA did not affect COC morpho-functional parameters, but impaired oocyte ability to prevent polyspermy and increased blastocyst apoptosis. In conclusion, in the female germ cell, cytotoxic nonspecific effects characterize OTA-induced toxicity at high exposure levels, whereas fine tuning-mode effects, not associated with altered cell viability and integrity, characterize OTA toxic action at low levels. Keywords Ochratoxin A . Juvenile sheep oocyte . In vitro maturation . In vitro fertilization . Bioenergetic/oxidative status . Time-lapse embryo monitoring
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s12550-020-00410-y) contains supplementary material, which is available to authorized users. * Maria Elena Dell’Aquila [email protected] 1
Department of Biosciences, Biotechnologies and Biopharmaceutics, University of Bari Aldo Moro, Str. Prov. Casamassima Km 3, 70010 Valenzano, Bari, Italy
2
Faculty of Veterinary Medicine, University of Teramo, SP18, 64100 Teramo, Italy
3
Department of Mathematics and Physics E. de Giorgi, University of Salento, Via per Arnesano, 73100 Lecc
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