Identification and Characterization of CircRNAs in Peri-implantation Endometrium Between Yorkshire and Erhualian Pigs

Overview

Journal BMC Genomics

Publisher Biomed Central

Specialty Genetics

Date 2023 Jul 24

PMID 37488487

Authors

Chen Zhou

Xinyan Cheng

Fanming Meng

Yongzhong Wang

Wanyun Luo

Enqin Zheng

Gengyuan Cai

Zhenfang Wu

Zicong Li

Linjun Hong

Affiliations

Soon will be listed here.

Abstract

Background: One of the most critical periods for the loss of pig embryos is the 12th day of gestation when implantation begins. Recent studies have shown that non-coding RNAs (ncRNAs) play important regulatory roles during pregnancy. Circular RNAs (circRNAs) are a kind of ubiquitously expressed ncRNAs that can directly regulate the binding proteins or regulate the expression of target genes by adsorbing micro RNAs (miRNA).

Results: We used the Illumina Novaseq6,000 technology to analyze the circRNA expression profile in the endometrium of three Erhualian (EH12) and three Yorkshire (YK12) pigs on day 12 of gestation. Overall, a total of 22,108 circRNAs were identified. Of these, 4051 circRNAs were specific to EH12 and 5889 circRNAs were specific to YK12, indicating a high level of breed specificity. Further analysis showed that there were 641 significant differentially expressed circRNAs (SDEcircRNAs) in EH12 compared with YK12 (FDR < 0.05). Functional enrichment of differential circRNA host genes revealed many pathways and genes associated with reproduction and regulation of embryo development. Network analysis of circRNA-miRNA interactions further supported the idea that circRNAs act as sponges for miRNAs to regulate gene expression. The prediction of differential circRNA binding proteins further explored the potential regulatory pathways of circRNAs. Analysis of SDEcircRNAs suggested a possible reason for the difference in embryo survival between the two breeds at the peri-implantation stage.

Conclusions: Together, these data suggest that circRNAs are abundantly expressed in the endometrium during the peri-implantation period in pigs and are important regulators of related genes. The results of this study will help to further understand the differences in molecular pathways between the two breeds during the critical implantation period of pregnancy, and will help to provide insight into the molecular mechanisms that contribute to the establishment of pregnancy and embryo loss in pigs.

Citing Articles

Identification and Functional Analysis of circRNAs during Goat Follicular Development.

Liu J, Guo C, Fu J, Liu D, Liu G, Sun B Int J Mol Sci. 2024; 25(14).

PMID: 39062792 PMC: 11277404. DOI: 10.3390/ijms25147548.

Population dynamics of potentially harmful haplotypes: a pedigree analysis.

Arias K, Fernandez I, Gutierrez J, Alvarez I, Goyache F BMC Genomics. 2024; 25(1):487.

PMID: 38755557 PMC: 11097446. DOI: 10.1186/s12864-024-10407-x.

Novel Insights into the Circadian Rhythms Based on Long Noncoding and Circular RNA Profiling.

Tan X, Zhang J, Dong J, Huang M, Zhou Z, Wang D Int J Mol Sci. 2024; 25(2).

PMID: 38256234 PMC: 10816401. DOI: 10.3390/ijms25021161.

References

Li W, Xi Y, Xue S, Wang Y, Wu L, Liu H . Sequence analysis of microRNAs during pre-implantation between Meishan and Yorkshire pigs. Gene. 2017; 646:20-27. DOI: 10.1016/j.gene.2017.12.046. View

Ji Y, Lu X, Zhong Q, Liu P, An Y, Zhang Y . Transcriptional profiling of mouse uterus at pre-implantation stage under VEGF repression. PLoS One. 2013; 8(2):e57287. PMC: 3585347. DOI: 10.1371/journal.pone.0057287. View

Ibanez-Perez J, Diaz-Nunez M, Clos-Garcia M, Lainz L, Iglesias M, Diez-Zapirain M . microRNA-based signatures obtained from endometrial fluid identify implantative endometrium. Hum Reprod. 2022; 37(10):2375-2391. PMC: 9527456. DOI: 10.1093/humrep/deac184. View

Jean J, George E, Kaestner K, Brown L, Spira A, Joyce-Brady M . Transcription factor Klf4, induced in the lung by oxygen at birth, regulates perinatal fibroblast and myofibroblast differentiation. PLoS One. 2013; 8(1):e54806. PMC: 3553006. DOI: 10.1371/journal.pone.0054806. View

Gholizadeh M, Esmaeili-Fard S . Meta-analysis of genome-wide association studies for litter size in sheep. Theriogenology. 2021; 180:103-112. DOI: 10.1016/j.theriogenology.2021.12.025. View

Sapkota D, Chintala H, Wu F, Fliesler S, Hu Z, Mu X . Onecut1 and Onecut2 redundantly regulate early retinal cell fates during development. Proc Natl Acad Sci U S A. 2014; 111(39):E4086-95. PMC: 4191802. DOI: 10.1073/pnas.1405354111. View

Ren Q, Guan S, Fu J, Wang A . Expression of tissue inhibitor of metalloproteinases-3 messenger RNA and protein in porcine endometrium during implantation. Mol Biol Rep. 2010; 38(6):3829-37. DOI: 10.1007/s11033-010-0498-z. View

Takahashi H, Yuge K, Matsubara S, Ohkuchi A, Kuwata T, Usui R . Differential expression of ADAM (a disintegrin and metalloproteinase) genes between human first trimester villous and extravillous trophoblast cells. J Nippon Med Sch. 2014; 81(3):122-9. DOI: 10.1272/jnms.81.122. View

Ohinata Y, Tsukiyama T . Establishment of trophoblast stem cells under defined culture conditions in mice. PLoS One. 2014; 9(9):e107308. PMC: 4159327. DOI: 10.1371/journal.pone.0107308. View

10.

Tu J, Yang H, Chen Y, Chen H, Li Z, Li L . Current and Future Roles of Circular RNAs in Normal and Pathological Endometrium. Front Endocrinol (Lausanne). 2021; 12:668073. PMC: 8187767. DOI: 10.3389/fendo.2021.668073. View

11.

Song Y, Zhang L, Liu X, Niu M, Cui J, Che S . Analyses of circRNA profiling during the development from pre-receptive to receptive phases in the goat endometrium. J Anim Sci Biotechnol. 2019; 10:34. PMC: 6482587. DOI: 10.1186/s40104-019-0339-4. View

12.

Zhang S, Zeng X, Ren M, Mao X, Qiao S . Novel metabolic and physiological functions of branched chain amino acids: a review. J Anim Sci Biotechnol. 2017; 8:10. PMC: 5260006. DOI: 10.1186/s40104-016-0139-z. View

13.

Kim H, Kim Y, Yoon J, Yang S, Park M, Seol D . Estrogen induces EGR1 to fine-tune its actions on uterine epithelium by controlling PR signaling for successful embryo implantation. FASEB J. 2017; 32(3):1184-1195. DOI: 10.1096/fj.201700854RR. View

14.

Simmen R, Zhang X, Zhang D, Wang Y, Michel F, Simmen F . Expression and regulatory function of the transcription factor Sp1 in the uterine endometrium at early pregnancy: implications for epithelial phenotype. Mol Cell Endocrinol. 2000; 159(1-2):159-70. DOI: 10.1016/s0303-7207(99)00191-4. View

15.

Kim T, Yoo J, Wang Z, Lydon J, Khatri S, Hawkins S . ARID1A Is Essential for Endometrial Function during Early Pregnancy. PLoS Genet. 2015; 11(9):e1005537. PMC: 4574948. DOI: 10.1371/journal.pgen.1005537. View

16.

Young K, Kraeling R, Bazer F . Effect of pregnancy and exogenous ovarian steroids on endometrial prolactin receptor ontogeny and uterine secretory response in pigs. Biol Reprod. 1990; 43(4):592-9. DOI: 10.1095/biolreprod43.4.592. View

17.

Wessels J, Linton N, Croy B, Tayade C . A review of molecular contrasts between arresting and viable porcine attachment sites. Am J Reprod Immunol. 2007; 58(6):470-80. DOI: 10.1111/j.1600-0897.2007.00534.x. View

18.

Hu Y, Huo Z, Liu C, Liu S, Zhang N, Yin K . Functional study of one nucleotide mutation in pri-miR-125a coding region which related to recurrent pregnancy loss. PLoS One. 2014; 9(12):e114781. PMC: 4257728. DOI: 10.1371/journal.pone.0114781. View

19.

Gu T, Zhu M, Schroyen M, Qu L, Nettleton D, Kuhar D . Endometrial gene expression profiling in pregnant Meishan and Yorkshire pigs on day 12 of gestation. BMC Genomics. 2014; 15:156. PMC: 3940021. DOI: 10.1186/1471-2164-15-156. View

20.

Tao L, He X, Wang F, Pan L, Wang X, Gan S . Identification of genes associated with litter size combining genomic approaches in Luzhong mutton sheep. Anim Genet. 2021; 52(4):545-549. DOI: 10.1111/age.13078. View