Transcriptome Profile of One-month-old Lambs' Granulosa Cells After Superstimulation

Overview

Journal Asian-Australas J Anim Sci

Specialty Veterinary Medicine

Date 2016 May 19

PMID 27189640

Citations 8

Authors

Yangsheng Wu

Jiapeng Lin

Xiaolin Li

Bing Han

Liqin Wang

Mingjun Liu

Juncheng Huang

Affiliations

Soon will be listed here.

Abstract

Objective: Superstimulatory treatment of one-month-old lambs can achieve synchronous development of numerous growing follicles. However, these growing follicles cannot complete maturation and ovulation. Oocyte maturation and competence are acquired during follicular development, in which granulosa cells play an essential role.

Methods: In this study, we applied RNA sequencing to analyze and compare gene expression between prepubertal and adult superstimulated follicle granulosa cells in sheep.

Results: There were more than 300 genes that significantly differed in expression. Among these differently expressed genes, many extracellular matrix genes (EGF containing Fibulin Like Extracellular Matrix Protein 1, pentraxin 3, adrenomedullin, and osteopontin) were significantly down-regulated in the superstimulated follicles. Ingenuity pathway and gene ontology analyses revealed that processes of axonal guidance, cell proliferation and DNA replication were expressed at higher levels in the prepubertal follicles. Epidermal growth factor, T-Box protein 2 and beta-estradiol upstream regulator were predicted to be active in prepubertal follicles. By comparison, tumor protein P53 and let-7 were most active in adult follicles.

Conclusion: These results may contribute to a better understanding of the mechanisms governing the development of granulosa cells in the growing follicle in prepubertal sheep.

Citing Articles

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Growth hormone treatment improves the development of follicles and oocytes in prepubertal lambs.

Liu K, Zhang L, Qi Q, Li J, Yan F, Hou J J Ovarian Res. 2023; 16(1):132.

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Banerjee P, Diniz W, Rodning S, Dyce P Front Genet. 2023; 14:1174145.

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Histone deacetylase inhibitor, panobinostat, exerts anti-proliferative effect with partial normalization from aberrant epigenetic states on granulosa cell tumor cell lines.

Hazama Y, Tsujioka T, Kitanaka A, Tohyama K, Shimoya K PLoS One. 2022; 17(7):e0271245.

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Transcriptomic comparison of ovarian granulosa cells between adult sheep and prepubertal lambs.

Tian H, Ren P, Liu K, Qiu C, Fan L, Li J BMC Genomics. 2022; 23(1):151.

PMID: 35189817 PMC: 8862527. DOI: 10.1186/s12864-022-08379-x.

References

Sonjaya H, Driancourt M . Ovarian follicles during infancy in Romanov and Ile-de-France ewe lambs. J Reprod Fertil. 1987; 81(1):241-8. DOI: 10.1530/jrf.0.0810241. View

Kang X, Liu G, Liu Y, Xu Q, Zhang M, Fang M . Transcriptome profile at different physiological stages reveals potential mode for curly fleece in Chinese tan sheep. PLoS One. 2013; 8(8):e71763. PMC: 3753335. DOI: 10.1371/journal.pone.0071763. View

Morton K . Developmental capabilities of embryos produced in vitro from prepubertal lamb oocytes. Reprod Domest Anim. 2008; 43 Suppl 2:137-43. DOI: 10.1111/j.1439-0531.2008.01153.x. View

Hatzirodos N, Irving-Rodgers H, Hummitzsch K, Harland M, Morris S, Rodgers R . Transcriptome profiling of granulosa cells of bovine ovarian follicles during growth from small to large antral sizes. BMC Genomics. 2014; 15:24. PMC: 3898003. DOI: 10.1186/1471-2164-15-24. View

Leoni G, Bebbere D, Succu S, Berlinguer F, Mossa F, Galioto M . Relations between relative mRNA abundance and developmental competence of ovine oocytes. Mol Reprod Dev. 2006; 74(2):249-57. DOI: 10.1002/mrd.20442. View

Fujihara M, Comizzoli P, Keefer C, Wildt D, Songsasen N . Epidermal growth factor (EGF) sustains in vitro primordial follicle viability by enhancing stromal cell proliferation via MAPK and PI3K pathways in the prepubertal, but not adult, cat ovary. Biol Reprod. 2014; 90(4):86. DOI: 10.1095/biolreprod.113.115089. View

Kelly J, Kleemann D, Walker S . Enhanced efficiency in the production of offspring from 4- to 8-week-old lambs. Theriogenology. 2005; 63(7):1876-90. DOI: 10.1016/j.theriogenology.2004.09.010. View

Dias F, Khan M, Sirard M, Adams G, Singh J . Differential gene expression of granulosa cells after ovarian superstimulation in beef cattle. Reproduction. 2013; 146(2):181-91. DOI: 10.1530/REP-13-0114. View

Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg S . TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 2013; 14(4):R36. PMC: 4053844. DOI: 10.1186/gb-2013-14-4-r36. View

10.

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

11.

Mortazavi A, Williams B, McCue K, Schaeffer L, Wold B . Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008; 5(7):621-8. DOI: 10.1038/nmeth.1226. View

12.

Leoni G, Palmerini M, Satta V, Succu S, Pasciu V, Zinellu A . Differences in the Kinetic of the First Meiotic Division and in Active Mitochondrial Distribution between Prepubertal and Adult Oocytes Mirror Differences in their Developmental Competence in a Sheep Model. PLoS One. 2015; 10(4):e0124911. PMC: 4403920. DOI: 10.1371/journal.pone.0124911. View

13.

Hiradate Y, Ohtake J, Hoshino Y, Tanemura K, Sato E . Adrenomedullin: a possible regulator of germinal vesicle breakdown. Biochem Biophys Res Commun. 2011; 415(4):691-5. DOI: 10.1016/j.bbrc.2011.10.139. View

14.

Hamel M, Dufort I, Robert C, Gravel C, Leveille M, Leader A . Identification of differentially expressed markers in human follicular cells associated with competent oocytes. Hum Reprod. 2008; 23(5):1118-27. DOI: 10.1093/humrep/den048. View

15.

Gou K, Guan H, Bai J, Cui X, Wu Z, Yan F . Field evaluation of juvenile in vitro embryo transfer (JIVET) in sheep. Anim Reprod Sci. 2008; 112(3-4):316-24. DOI: 10.1016/j.anireprosci.2008.05.008. View

16.

Yamashita Y, Shimada M . The release of EGF domain from EGF-like factors by a specific cleavage enzyme activates the EGFR-MAPK3/1 pathway in both granulosa cells and cumulus cells during the ovulation process. J Reprod Dev. 2012; 58(5):510-4. DOI: 10.1262/jrd.2012-056. View

17.

Khan D, Guillemette C, Sirard M, Richard F . Characterization of FSH signalling networks in bovine cumulus cells: a perspective on oocyte competence acquisition. Mol Hum Reprod. 2015; 21(9):688-701. DOI: 10.1093/molehr/gav032. View

18.

Primig M . The bioinformatics tool box for reproductive biology. Biochim Biophys Acta. 2012; 1822(12):1880-95. DOI: 10.1016/j.bbadis.2012.05.018. View

19.

Amiridis G, Cseh S . Assisted reproductive technologies in the reproductive management of small ruminants. Anim Reprod Sci. 2012; 130(3-4):152-61. DOI: 10.1016/j.anireprosci.2012.01.009. View

20.

Berkholtz C, Lai B, Woodruff T, Shea L . Distribution of extracellular matrix proteins type I collagen, type IV collagen, fibronectin, and laminin in mouse folliculogenesis. Histochem Cell Biol. 2006; 126(5):583-92. PMC: 2659665. DOI: 10.1007/s00418-006-0194-1. View