Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age

Cadmium (Cd), a highly toxic pollutant, impairs oocyte fertilization, through oxidative damage on cumulus cells (CCs). This study analysed the transcriptomic profile of CCs of cumulus-oocyte complexes (COCs) from adult and prepubertal sheep, exposed to Cd nanomolar concentration during in vitro matu...

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Main Authors: Nicola Antonio Martino, Ernesto Picardi, Elena Ciani, Anna Maria D’Erchia, Luisa Bogliolo, Federica Ariu, Antonella Mastrorocco, Letizia Temerario, Luigi Mansi, Valeria Palumbo, Graziano Pesole, Maria Elena Dell’Aquila
Format: Article
Language:English
Published: MDPI AG 2023-02-01
Series:Biology
Subjects:
Online Access:https://www.mdpi.com/2079-7737/12/2/249
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author Nicola Antonio Martino
Ernesto Picardi
Elena Ciani
Anna Maria D’Erchia
Luisa Bogliolo
Federica Ariu
Antonella Mastrorocco
Letizia Temerario
Luigi Mansi
Valeria Palumbo
Graziano Pesole
Maria Elena Dell’Aquila
author_facet Nicola Antonio Martino
Ernesto Picardi
Elena Ciani
Anna Maria D’Erchia
Luisa Bogliolo
Federica Ariu
Antonella Mastrorocco
Letizia Temerario
Luigi Mansi
Valeria Palumbo
Graziano Pesole
Maria Elena Dell’Aquila
author_sort Nicola Antonio Martino
collection DOAJ
description Cadmium (Cd), a highly toxic pollutant, impairs oocyte fertilization, through oxidative damage on cumulus cells (CCs). This study analysed the transcriptomic profile of CCs of cumulus-oocyte complexes (COCs) from adult and prepubertal sheep, exposed to Cd nanomolar concentration during in vitro maturation. In both age-groups, CCs of matured oocytes underwent RNA-seq, data analysis and validation. Differentially expressed genes (DEGs) were identified in adult (<i>n</i> = 99 DEGs) and prepubertal (<i>n</i> = 18 DEGs) CCs upon Cd exposure. Transcriptomes of adult CCs clustered separately between Cd-exposed and control samples, whereas prepubertal ones did not as observed by Principal Component Analysis. The transcriptomic signature of Cd-induced CC toxicity was identified by gene annotation and literature search. Genes associated with previous studies on ovarian functions and/or Cd effects were confirmed and new genes were identified, thus implementing the knowledge on their involvement in such processes. Enrichment and validation analysis showed that, in adult CCs, Cd acted as endocrine disruptor on DEGs involved in hormone biosynthesis, cumulus expansion, regulation of cell signalling, growth and differentiation and oocyte maturation, whereas in prepubertal CCs, Cd affected DEGs involved in CC development and viability and CC-oocyte communications. In conclusion, these DEGs could be used as valuable non-invasive biomarkers for oocyte competence.
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spelling doaj.art-924c1a4d974045ffb9835dbaa97af9312023-11-16T19:13:44ZengMDPI AGBiology2079-77372023-02-0112224910.3390/biology12020249Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult AgeNicola Antonio Martino0Ernesto Picardi1Elena Ciani2Anna Maria D’Erchia3Luisa Bogliolo4Federica Ariu5Antonella Mastrorocco6Letizia Temerario7Luigi Mansi8Valeria Palumbo9Graziano Pesole10Maria Elena Dell’Aquila11Department of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Veterinary Medicine, University of Sassari, Via Vienna n. 2, 07100 Sassari, ItalyDepartment of Veterinary Medicine, University of Sassari, Via Vienna n. 2, 07100 Sassari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyDepartment of Biosciences, Biotechnologies & Environment, University of Bari Aldo Moro, Via Edoardo Orabona, 70125 Bari, ItalyCadmium (Cd), a highly toxic pollutant, impairs oocyte fertilization, through oxidative damage on cumulus cells (CCs). This study analysed the transcriptomic profile of CCs of cumulus-oocyte complexes (COCs) from adult and prepubertal sheep, exposed to Cd nanomolar concentration during in vitro maturation. In both age-groups, CCs of matured oocytes underwent RNA-seq, data analysis and validation. Differentially expressed genes (DEGs) were identified in adult (<i>n</i> = 99 DEGs) and prepubertal (<i>n</i> = 18 DEGs) CCs upon Cd exposure. Transcriptomes of adult CCs clustered separately between Cd-exposed and control samples, whereas prepubertal ones did not as observed by Principal Component Analysis. The transcriptomic signature of Cd-induced CC toxicity was identified by gene annotation and literature search. Genes associated with previous studies on ovarian functions and/or Cd effects were confirmed and new genes were identified, thus implementing the knowledge on their involvement in such processes. Enrichment and validation analysis showed that, in adult CCs, Cd acted as endocrine disruptor on DEGs involved in hormone biosynthesis, cumulus expansion, regulation of cell signalling, growth and differentiation and oocyte maturation, whereas in prepubertal CCs, Cd affected DEGs involved in CC development and viability and CC-oocyte communications. In conclusion, these DEGs could be used as valuable non-invasive biomarkers for oocyte competence.https://www.mdpi.com/2079-7737/12/2/249adult sheepprepubertal lambcumulus celltranscriptomeRNA-sequencingcadmium
spellingShingle Nicola Antonio Martino
Ernesto Picardi
Elena Ciani
Anna Maria D’Erchia
Luisa Bogliolo
Federica Ariu
Antonella Mastrorocco
Letizia Temerario
Luigi Mansi
Valeria Palumbo
Graziano Pesole
Maria Elena Dell’Aquila
Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age
Biology
adult sheep
prepubertal lamb
cumulus cell
transcriptome
RNA-sequencing
cadmium
title Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age
title_full Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age
title_fullStr Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age
title_full_unstemmed Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age
title_short Cumulus Cell Transcriptome after Cumulus-Oocyte Complex Exposure to Nanomolar Cadmium in an In Vitro Animal Model of Prepubertal and Adult Age
title_sort cumulus cell transcriptome after cumulus oocyte complex exposure to nanomolar cadmium in an in vitro animal model of prepubertal and adult age
topic adult sheep
prepubertal lamb
cumulus cell
transcriptome
RNA-sequencing
cadmium
url https://www.mdpi.com/2079-7737/12/2/249
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