RNA-Seq Profiling of Single Bovine Oocyte Transcript Abundance and Its Modulation by Cytoplasmic Polyadenylation

Overview

Journal Mol Reprod Dev

Specialties Molecular Biology
Reproductive Medicine

Date 2015 Jan 7

PMID 25560149

Citations 32

Authors

Juan M Reyes

James L Chitwood

Pablo J Ross

Affiliations

Soon will be listed here.

Abstract

Molecular changes occurring during mammalian oocyte maturation are partly regulated by cytoplasmic polyadenylation (CP) and affect oocyte quality, yet the extent of CP activity during oocyte maturation remains unknown. Single bovine oocyte RNA sequencing (RNA-Seq) was performed to examine changes in transcript abundance during in vitro oocyte maturation in cattle. Polyadenylated RNA from individual germinal-vesicle and metaphase-II oocytes was amplified and processed for Illumina sequencing, producing approximately 30 million reads per replicate for each sample type. A total of 10,494 genes were found to be expressed, of which 2,455 were differentially expressed (adjusted P < 0.05 and fold change >2) between stages, with 503 and 1,952 genes respectively increasing and decreasing in abundance. Differentially expressed genes with complete 3'-untranslated-region sequence (279 increasing and 918 decreasing in polyadenylated transcript abundance) were examined for the presence, position, and distribution of motifs mediating CP, revealing enrichment (85%) and lack thereof (18%) in up- and down-regulated genes, respectively. Examination of total and polyadenylated RNA abundance by quantitative PCR validated these RNA-Seq findings. The observed increases in polyadenylated transcript abundance within the RNA-Seq data are likely due to CP, providing novel insight into targeted transcripts and resultant differential gene expression profiles that contribute to oocyte maturation.

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References

Resuehr D, Spiess A . A real-time polymerase chain reaction-based evaluation of cDNA synthesis priming methods. Anal Biochem. 2003; 322(2):287-91. DOI: 10.1016/j.ab.2003.07.017. View

Cao Q, Richter J . Dissolution of the maskin-eIF4E complex by cytoplasmic polyadenylation and poly(A)-binding protein controls cyclin B1 mRNA translation and oocyte maturation. EMBO J. 2002; 21(14):3852-62. PMC: 126103. DOI: 10.1093/emboj/cdf353. View

Sagata N, Shiokawa K, Yamana K . A study on the steady-state population of poly(A)+RNA during early development of Xenopus laevis. Dev Biol. 1980; 77(2):431-48. DOI: 10.1016/0012-1606(80)90486-8. View

Bachvarova R, De Leon V, Johnson A, Kaplan G, Paynton B . Changes in total RNA, polyadenylated RNA, and actin mRNA during meiotic maturation of mouse oocytes. Dev Biol. 1985; 108(2):325-31. DOI: 10.1016/0012-1606(85)90036-3. View

Paynton B, Rempel R, Bachvarova R . Changes in state of adenylation and time course of degradation of maternal mRNAs during oocyte maturation and early embryonic development in the mouse. Dev Biol. 1988; 129(2):304-14. DOI: 10.1016/0012-1606(88)90377-6. View

McGrew L, Dworkin M, Richter J . Poly(A) elongation during Xenopus oocyte maturation is required for translational recruitment and is mediated by a short sequence element. Genes Dev. 1989; 3(6):803-15. DOI: 10.1101/gad.3.6.803. View

Gautier J, Minshull J, Lohka M, Glotzer M, Hunt T, Maller J . Cyclin is a component of maturation-promoting factor from Xenopus. Cell. 1990; 60(3):487-94. DOI: 10.1016/0092-8674(90)90599-a. View

Vassalli J, Huarte J, Belin D, Gubler P, Vassalli A, OConnell M . Regulated polyadenylation controls mRNA translation during meiotic maturation of mouse oocytes. Genes Dev. 1989; 3(12B):2163-71. DOI: 10.1101/gad.3.12b.2163. View

Varnum S, Wormington W . Deadenylation of maternal mRNAs during Xenopus oocyte maturation does not require specific cis-sequences: a default mechanism for translational control. Genes Dev. 1990; 4(12B):2278-86. DOI: 10.1101/gad.4.12b.2278. View

10.

Choi T, Aoki F, Mori M, Yamashita M, Nagahama Y, Kohmoto K . Activation of p34cdc2 protein kinase activity in meiotic and mitotic cell cycles in mouse oocytes and embryos. Development. 1991; 113(3):789-95. DOI: 10.1242/dev.113.3.789. View

11.

Gebauer F, Xu W, Cooper G, Richter J . Translational control by cytoplasmic polyadenylation of c-mos mRNA is necessary for oocyte maturation in the mouse. EMBO J. 1994; 13(23):5712-20. PMC: 395537. DOI: 10.1002/j.1460-2075.1994.tb06909.x. View

12.

Gebauer F, Richter J . Mouse cytoplasmic polyadenylylation element binding protein: an evolutionarily conserved protein that interacts with the cytoplasmic polyadenylylation elements of c-mos mRNA. Proc Natl Acad Sci U S A. 1996; 93(25):14602-7. PMC: 26180. DOI: 10.1073/pnas.93.25.14602. View

13.

Kondo T, Yanagawa T, Yoshida N, Yamashita M . Introduction of cyclin B induces activation of the maturation-promoting factor and breakdown of germinal vesicle in growing zebrafish oocytes unresponsive to the maturation-inducing hormone. Dev Biol. 1997; 190(1):142-52. DOI: 10.1006/dbio.1997.8673. View

14.

de Moor C, Richter J . Cytoplasmic polyadenylation elements mediate masking and unmasking of cyclin B1 mRNA. EMBO J. 1999; 18(8):2294-303. PMC: 1171312. DOI: 10.1093/emboj/18.8.2294. View

15.

de Moor C, Meijer H, Lissenden S . Mechanisms of translational control by the 3' UTR in development and differentiation. Semin Cell Dev Biol. 2005; 16(1):49-58. DOI: 10.1016/j.semcdb.2004.11.007. View

16.

Traverso J, Donnay I, Lequarre A . Effects of polyadenylation inhibition on meiosis progression in relation to the polyadenylation status of cyclins A2 and B1 during in vitro maturation of bovine oocytes. Mol Reprod Dev. 2005; 71(1):107-14. DOI: 10.1002/mrd.20247. View

17.

Tremblay K, Vigneault C, McGraw S, Sirard M . Expression of cyclin B1 messenger RNA isoforms and initiation of cytoplasmic polyadenylation in the bovine oocyte. Biol Reprod. 2004; 72(4):1037-44. DOI: 10.1095/biolreprod.104.034793. View

18.

Bettegowda A, Patel O, Ireland J, Smith G . Quantitative analysis of messenger RNA abundance for ribosomal protein L-15, cyclophilin-A, phosphoglycerokinase, beta-glucuronidase, glyceraldehyde 3-phosphate dehydrogenase, beta-actin, and histone H2A during bovine oocyte maturation and early.... Mol Reprod Dev. 2005; 73(3):267-78. DOI: 10.1002/mrd.20333. View

19.

Graindorge A, Thuret R, Pollet N, Osborne H, Audic Y . Identification of post-transcriptionally regulated Xenopus tropicalis maternal mRNAs by microarray. Nucleic Acids Res. 2006; 34(3):986-95. PMC: 1361620. DOI: 10.1093/nar/gkj492. View

20.

Assou S, Anahory T, Pantesco V, Le Carrour T, Pellestor F, Klein B . The human cumulus--oocyte complex gene-expression profile. Hum Reprod. 2006; 21(7):1705-19. PMC: 2377388. DOI: 10.1093/humrep/del065. View