Subcortical maternal complex (SCMC) expression during folliculogenesis is affected by oocyte donor age in sheep

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GAMETE BIOLOGY

Subcortical maternal complex (SCMC) expression during folliculogenesis is affected by oocyte donor age in sheep D. Bebbere 1

&

A. Abazari-Kia 1,2 & S. Nieddu 1 & B. Melis Murgia 1 & D. F. Albertini 3 & S. Ledda 1

Received: 17 April 2020 / Accepted: 25 June 2020 # Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Purpose The age-associated decline in female fertility is largely ascribable to the decrease in oocyte quality. The subcortical maternal complex (SCMC) is a multiprotein complex essential for early embryogenesis and female fertility and functionally conserved across mammals. The present work evaluated expression dynamics of its components during folliculogenesis in relation to maternal age in sheep. Methods The expression of the SCMC components (KHDC3/FILIA, NLRP2, NLRP5/MATER, OOEP/FLOPED, PADI6, TLE6 and ZBED3) was analyzed by real-time PCR in pools of growing oocytes (GO) of different diameters (70–90 μm (S), 90–110 μm (M), or 110–130 μm (L)) derived from non-hormonally treated adult (Ad; age < 4 years), prepubertal (Pr; age 40 days), or aged ewes (age > 6 years). Results Specific expression patterns associated with donor age were observed during folliculogenesis for all genes, except ZBED3. In oocytes of adult donors, the synthesis of NLRP2, NLRP5, PADI6, and ZBED3 mRNAs was complete in S GO, while FILIA, TLE6, and OOEP were actively transcribed at this stage. Conversely, Pr GO showed active transcription of all mRNAs, except for ZBED3, during the entire window of oocyte growth. Notably, aged GO showed a completely inverse pattern, with a decrease of NLRP2, TLE6, FILIA, and PADI6 mRNA abundance during the latest stage of oocyte growth (L GO). Interestingly, MATER showed high expression variability, suggesting large inter-oocyte differences. Conclusion Our study describes the SCMC expression dynamics during sheep oogenesis and reports age-specific patterns that are likely involved in the age-related decline of oocyte quality. Keywords KHDC3/FILIA . NLRP2 . NLRP5/MATER . OOEP/FLOPED . PADI6 . TLE6 . ZBED3 . Reproductive ageing . Oocyte developmental competence

Introduction Transcription and translation are uncoupled during oocyte maturation and early embryonic development; the molecules that support this developmental window are stored as mRNAs in the oocyte during its growth, and gene expression regulation occurs at the post-transcriptional level. The molecular

* D. Bebbere [email protected] 1

Department of Veterinary Medicine, University of Sassari, Sassari, Italy

2

Department of Animal Science, College of Agriculture and Natural Resources, University of Tehran, Karaj, Tehran, Iran

3

The Center for Human Reproduction, New York, NY, USA

endowment of the oocyte, or transcriptome, is therefore crucial to complete the complex mechanisms underlying oocyte to embryo transition, including nuclear reprogramming to totipotency and activation of the embryonic genome (EGA). As a result, the storage of maternal molecules during oogenesis is a major determinant o