|
|
|
| Effects of Low Oxygen Tension on Transcriptome of Yak (Bos grunniens) Cumulus Cells |
| LI Rui-Zhe1,2, XU Jing-Tao2, SUN Yong-Gang2, MA Zhi-Jie2, CHEN Sheng-Mei2, LUO Yu-Zhu1,* |
1 College of Animal Science and Technology, Gansu Agricultural University, Lanzhou 730070, China;
2 Qinghai Academy of Animal Science and Veterinary Medicine, Xining 810016, China |
|
|
|
|
Abstract Cumulus cells are important supporting cells of oocytes. Quality of cumulus cells influences in vitro maturation and developmental competence of oocytes. Low oxygen tension was beneficial for in vitro maturation and developmental competence of yak (Bos grunniens) oocytes, whereas whether the beneficial effects were exerted through cumulus cells has not been reported. In order to investigate the effects of low oxygen tension on transcriptome of yak cumulus cells, maturation of yak cumulus-oocyte complex (COC) was carried out at 5% and 20% O2, respectively. Then cumulus cells were collected for RNA-seq, screening of differentially expressed genes (DEGs) and qRT-PCR verification. The results showed that 8 yak cumulus cell transcriptomic libraries were obtained and total data size was 56.17 Gb; gene expression analysis showed that a total of 13 584 genes were expressed of the two groups and 270 DEGs were identified, among which 229 DEGs were up-regulated in 5% O2 and 41 DEGs were up-regulated in 20% O2; Gene Ontology (GO) and KEGG pathway analysis showed that DEGs were mostly enriched in glycolysis, cumulus cell expansion and cumulus-oocyte signaling et al.; 6 711 new genes and 7 209 new transcripts, among which 829 new transcripts had protein coding potential, were found in unannotated region of the yak reference genome. qRT-PCR results were consistent with the sequencing data. Taken together, above results indicated that low oxygen tension might induce yak cumulus cells to have a similar transcriptomic profile to those matured in vivo and therefore promote the maturation and developmental competence of yak oocytes. The present study provides a reference for further study of the effect of oxygen tension on the mechanism of cumulus cell-oocyte interaction in the process of in vitro maturation of yak oocytes.
|
|
Received: 01 July 2020
Published: 01 April 2021
|
|
|
|
Corresponding Authors:
* luoyz@gsau.edu.cn
|
|
|
|
[1] Andrade G M, da Silveira J C, Perrini C, et al.2017. The role of the PI3K-Akt signaling pathway in the developmental competence of bovine oocytes[J]. PLOS ONE, 12(9): e0185045.
[2] Bennemann J, Grothmann H, Wrenzycki C.2018. Reduced oxygen concentration during in vitro oocyte maturation alters global DNA methylation in the maternal pronucleus of subsequent zygotes in cattle[J]. Molecular Reproduction and Development, 85(11): 849-857.
[3] Bermejo-Alvarez P, Lonergan P, Rizos D, et al.2010. Low oxygen tension during IVM improves bovine oocyte competence and enhances anaerobic glycolysis[J]. Reproductive BioMedicine Online, 20(3): 341-349.
[4] Carabatsos M J, Sellitto C, Goodenough D A, et al.2000. Oocyte-granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence[J]. Developmental Biology, 226(2): 167-179.
[5] Chen S, Zhou Y, Chen Y, et al.2018. Fastp: An ultra-fast all-in-one FASTQ preprocessor[J]. Bioinformatics, 34(17): i884-i890.
[6] Cillo F, Brevini T A, Antonini S, et al.2007. Association between human oocyte developmental competence and expression levels of some cumulus genes[J]. Reproduction, 134(5): 645-650.
[7] de Munck N, Janssens R, Segers I, et al.2019. Influence of ultra-low oxygen (2%) tension on in vitro human embryo development[J]. Human Reproduction, 34(2): 228-234.
[8] Demiray S B, Goker E N T, Tavmergen E, et al.2019. Differential gene expression analysis of human cumulus cells[J]. Clinical and Experimental Reproductive Medicine, 46(2): 76-86.
[9] di Giacomo M, Camaioni A, Klinger F G, et al.2016. Cyclic AMP-elevating agents promote cumulus cell survival and hyaluronan matrix stability, thereby prolonging the time of mouse oocyte fertilizability[J]. Journal of Biological Chemistry, 291(8): 3821-3836.
[10] Gaspar R C, Arnold D R, Correa C A, et al.2015. Oxygen tension affects histone remodeling of in vitro-produced embryos in a bovine model[J]. Theriogenology, 83(9): 1408-1415.
[11] Gu L, Liu H, Gu X, et al.2015. Metabolic control of oocyte development: linking maternal nutrition and reproductive outcomes[J]. Cellular and Molecular Life Sciences, 72(2): 251-271.
[12] Huang X, Hao C, Shen X, et al.2013. Differences in the transcriptional profiles of human cumulus cells isolated from MI and MII oocytes of patients with polycystic ovary syndrome[J]. Reproduction, 145(6): 597-608.
[13] Kagan H M, Li W.2003. Lysyl oxidase: properties, specificity, and biological roles inside and outside of the cell[J]. Journal of Cellular Biochemistry, 88(4): 660-672.
[14] Kang J T, Atikuzzaman M, Kwon D K, et al.2012. Developmental competence of porcine oocytes after in vitro maturation and in vitro culture under different oxygen concentrations[J]. Zygote, 20(1): 1-8.
[15] Kang Y J, Yang D C, Kong L, et al.2017. CPC2: A fast and accurate coding potential calculator based on sequence intrinsic features[J]. Nucleic Acids Research, 45(W1): W12-W16.
[16] Kelley R L, Gardner D K.2016. Combined effects of individual culture and atmospheric oxygen on preimplantation mouse embryos in vitro[J]. Reproductive Biomedicine Online, 33(5): 537-549.
[17] Kirkegaard K, Hindkjaer J J, Ingerslev H J.2013. Effect of oxygen concentration on human embryo development evaluated by time-lapse monitoring[J]. Fertility and Sterility, 99(3): 738-744, e1-e4.
[18] Liao Y, Smyth G K, Shi W.2019. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads[J]. Nucleic Acids Research, 47(8): e47.
[19] Lonergan P, Fair T.2016. Maturation of oocytes in vitro[J]. Annual Review of Animal Biosciences, 4: 255-268.
[20] Love M I, Huber W, Anders S.2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2[J]. Genome Biology, 15(12): 550.
[21] Morin S J.2017. Oxygen tension in embryo culture: does a shift to 2% O2 in extended culture represent the most physiologic system?[J]. Journal of Assisted Reproduction and Genetics, 34(3): 309-314.
[22] Pertea G, Pertea M.2020. GFF Utilities: GffRead and GffCompare[J]. F1000 Research, 9: 304. DOI: 10.12688/f1000research.23297.1
[23] Pertea M, Kim D, Pertea G M, et al.2016. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown[J]. Nature Protocols, 11(9): 1650-1667.
[24] Richards J S, Liu Z, Shimada M.2015. Knobil and Neill's Physiology of Reproduction (Fourth Edition) Chapter 22-Ovulation [M]. Academic Press, San Diego. pp. 997-1021.
[25] Su Y-Q, Sugiura K, Eppig J J.2009. Mouse oocyte control of granulosa cell development and function: Paracrine regulation of cumulus cell metabolism[J]. Seminars in Reproductive Medicine, 27(1): 32-42.
[26] Sutton-McDowall M L, Gilchrist R B, Thompson J G.2010. The pivotal role of glucose metabolism in determining oocyte developmental competence[J]. Reproduction, 139(4): 685-695.
[27] Uyar A, Torrealday S, Seli E.2013. Cumulus and granulosa cell markers of oocyte and embryo quality[J]. Fertility and Sterility, 99(4): 979-997.
[28] Xiong X R, Lan D L, Li J, et al.2019. Identification of differential abundances of mRNA transcript in cumulus cells and CCND1 associated with yak oocyte developmental competence[J]. Animal Reproduction Science, 208: 106135. |
|
|
|
