Differential expression of tsRNAs and miRNAs in embryo culture medium: potential impact on embryo implantation.
Embryo culture medium
Embryo quality
Endometrial receptivity
miRNA
tsRNA
Journal
Journal of assisted reproduction and genetics
ISSN: 1573-7330
Titre abrégé: J Assist Reprod Genet
Pays: Netherlands
ID NLM: 9206495
Informations de publication
Date de publication:
Mar 2024
Mar 2024
Historique:
received:
30
08
2023
accepted:
15
01
2024
pubmed:
25
1
2024
medline:
25
1
2024
entrez:
25
1
2024
Statut:
ppublish
Résumé
Can small RNA derived from embryos in conditioned embryo culture medium (ECM) influence embryo implantation? We employed small RNA sequencing to investigate the expression profiles of transfer RNA-derived small RNA (tsRNA) and microRNA (miRNA) in ECM from high-quality and low-quality embryos. Quantitative real-time PCR was employed to validate the findings of small RNA sequencing. Additionally, we conducted bioinformatics analysis to predict the potential functions of these small RNAs in embryo implantation. To establish the role of tiRNA-1:35-Leu-TAG-2 in embryonic trophoblast cell adhesion, we utilized co-culture systems involving JAR and Ishikawa cells. Our analysis revealed upregulation of nine tsRNAs and four miRNAs in ECM derived from high-quality embryos, whereas 37 tsRNAs and 12 miRNAs exhibited upregulation in ECM from low-quality embryos. The bioinformatics analysis of tsRNA, miRNA, and mRNA pathways indicated that their respective target genes may play pivotal roles in both embryo development and endometrial receptivity. Utilizing tiRNA mimics, we demonstrated that the prominently expressed tiRNA-1:35-Leu-TAG-2 in the low-quality ECM group can be internalized by Ishikawa cells. Notably, transfection of tiRNA-1:35-Leu-TAG-2 into Ishikawa cells reduced the attachment rate of JAR spheroids. Our investigation uncovers significant variation in the expression profiles of tsRNAs and miRNAs between ECM derived from high- and low-quality embryos. Intriguingly, the release of tiRNA-1:35-Leu-TAG-2 by low-quality embryos detrimentally affects embryo implantation and endometrial receptivity. These findings provide fresh insights into understanding the molecular foundations of embryo-endometrial communication.
Identifiants
pubmed: 38270749
doi: 10.1007/s10815-024-03034-8
pii: 10.1007/s10815-024-03034-8
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
781-793Subventions
Organisme : Scientific Research Project of Hubei Provincial Health Commission
ID : WJ2021M162
Organisme : Zhongnan Hospital of Wuhan University
ID : CXPY2022010
Organisme : Basic and Clinical Medical Research Joint Fund of Zhongnan Hospital，Wuhan University
ID : ZNLH202206
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer Science+Business Media, LLC, part of Springer Nature.
Références
Brosens JJ, Salker MS, Teklenburg G, Nautiyal J, Salter S, Lucas ES, Steel JH, Christian M, Chan YW, Boomsma CM, et al. Uterine selection of human embryos at implantation. Sci Rep. 2014;4:3894.
doi: 10.1038/srep03894
pubmed: 24503642
pmcid: 3915549
Cimadomo D, Capalbo A, Ubaldi FM, Scarica C, Palagiano A, Canipari R, Rienzi L. The impact of biopsy on human embryo developmental potential during preimplantation genetic diagnosis. Biomed Res Int. 2016;2016:7193075.
doi: 10.1155/2016/7193075
pubmed: 26942198
pmcid: 4749789
Leaver M, Wells D. Non-invasive preimplantation genetic testing (niPGT): the next revolution in reproductive genetics? Hum Reprod Update. 2020;26:16–42.
doi: 10.1093/humupd/dmz033
pubmed: 31774124
Rubio C, Rodrigo L, Garcia-Pascual C, Peinado V, Campos-Galindo I, Garcia-Herrero S, Simon C. Clinical application of embryo aneuploidy testing by next-generation sequencing. Biol Reprod. 2019;101:1083–90.
doi: 10.1093/biolre/ioz019
pubmed: 30721942
Zhou W, Dimitriadis E. Secreted MicroRNA to predict embryo implantation outcome: from research to clinical diagnostic application. Front Cell Dev Biol. 2020;8:586510.
doi: 10.3389/fcell.2020.586510
pubmed: 33072767
pmcid: 7537741
Fang F, Li Z, Yu J, Long Y, Zhao Q, Ding X, Wu L, Shao S, Zhang L, Xiang W. MicroRNAs secreted by human embryos could be potential biomarkers for clinical outcomes of assisted reproductive technology. J Adv Res. 2021;31:25–34.
doi: 10.1016/j.jare.2021.01.003
pubmed: 34194830
pmcid: 8240345
Abu-Halima M, Khaizaran ZA, Ayesh BM, Fischer U, Khaizaran SA, Al-Battah F, Hammadeh M, Keller A, Meese E. MicroRNAs in combined spent culture media and sperm are associated with embryo quality and pregnancy outcome. Fertil Steril. 2020;113(970–980):e972.
Berkhout RP, Keijser R, Repping S, Lambalk CB, Afink GB, Mastenbroek S, Hamer G. High-quality human preimplantation embryos stimulate endometrial stromal cell migration via secretion of microRNA hsa-miR-320a. Hum Reprod. 2020;35:1797–807.
doi: 10.1093/humrep/deaa149
pubmed: 32644109
pmcid: 7398623
Russell SJ, Menezes K, Balakier H, Librach C. Comprehensive profiling of small RNAs in human embryo-conditioned culture media by improved sequencing and quantitative PCR methods. Syst Biol Reprod Med. 2020;66:129–39.
doi: 10.1080/19396368.2020.1716108
pubmed: 32053759
Kirkegaard K, Yan Y, Sørensen BS, Hardarson T, Hanson C, Ingerslev HJ, Knudsen UB, Kjems J, Lundin K, Ahlström A. Comprehensive analysis of soluble RNAs in human embryo culture media and blastocoel fluid. J Assist Reprod Genet. 2020;37:2199–209.
doi: 10.1007/s10815-020-01891-7
pubmed: 32681282
pmcid: 7492334
Huang P, Tu B, Liao HJ, Huang FZ, Li ZZ, Zhu KY, Dai F, Liu HZ, Zhang TY, Sun CZ. Elevation of plasma tRNA fragments as a promising biomarker for liver fibrosis in nonalcoholic fatty liver disease. Sci Rep. 2021;11:5886.
doi: 10.1038/s41598-021-85421-0
pubmed: 33723340
pmcid: 7961013
Tosar JP, Cayota A. Extracellular tRNAs and tRNA-derived fragments. RNA Biol. 2020;17:1149–67.
doi: 10.1080/15476286.2020.1729584
pubmed: 32070197
pmcid: 7549618
Tosar JP, Segovia M, Castellano M, Gambaro F, Akiyama Y, Fagundez P, Olivera A, Costa B, Possi T, Hill M, et al. Fragmentation of extracellular ribosomes and tRNAs shapes the extracellular RNAome. Nucleic Acids Res. 2020;48:12874–88.
doi: 10.1093/nar/gkaa674
pubmed: 32785615
pmcid: 7736827
Ivanov P, O’Day E, Emara MM, Wagner G, Lieberman J, Anderson P. G-quadruplex structures contribute to the neuroprotective effects of angiogenin-induced tRNA fragments. Proc Natl Acad Sci U S A. 2014;111:18201–6.
doi: 10.1073/pnas.1407361111
pubmed: 25404306
pmcid: 4280610
Martinez G. tRNA-derived small RNAs: new players in genome protection against retrotransposons. RNA Biol. 2018;15:170–5.
doi: 10.1080/15476286.2017.1403000
pubmed: 29120263
Buck VU, Kohlen MT, Sternberg AK, Rosing B, Neulen J, Leube RE, Classen-Linke I. Steroid hormones and human choriogonadotropin influence the distribution of alpha6-integrin and desmoplakin 1 in gland-like endometrial epithelial spheroids. Histochem Cell Biol. 2021;155:581–91.
doi: 10.1007/s00418-020-01960-z
pubmed: 33502623
pmcid: 8134296
DeVeale B, Liu L, Boileau R, Swindlehurst-Chan J, Marsh B, Freimer JW, Abate A, Blelloch R. G1/S restriction point coordinates phasic gene expression and cell differentiation. Nat Commun. 2022;13:3696.
doi: 10.1038/s41467-022-31101-0
pubmed: 35760790
pmcid: 9237072
Wade SL, Langer LF, Ward JM, Archer TK. MiRNA-mediated regulation of the SWI/SNF chromatin remodeling complex controls pluripotency and endodermal differentiation in human ESCs. Stem Cells. 2015;33:2925–35.
doi: 10.1002/stem.2084
pubmed: 26119756
Dong X, Sui C, Huang K, Wang L, Hu D, Xiong T, Wang R, Zhang H. MicroRNA-223-3p suppresses leukemia inhibitory factor expression and pinopodes formation during embryo implantation in mice. Am J Transl Res. 2016;8(2):1155–63.
pubmed: 27158401
pmcid: 4846958
Jing MY, Xie LD, Chen X, Zhou Y, Jin MM, He WH, Wang DM, Liu AX. Circ-CCNB1 modulates trophoblast proliferation and invasion in spontaneous abortion by regulating miR-223/SIAH1 axis. Endocrinology. 2022;163:8.
doi: 10.1210/endocr/bqac093
Nechooshtan G, Yunusov D, Chang K, Gingeras TR. Processing by RNase 1 forms tRNA halves and distinct Y RNA fragments in the extracellular environment. Nucleic Acids Res. 2020;48:8035–49.
doi: 10.1093/nar/gkaa526
pubmed: 32609822
pmcid: 7430647
Li X, Liu X, Zhao D, Cui W, Wu Y, Zhang C, Duan C. tRNA-derived small RNAs: novel regulators of cancer hallmarks and targets of clinical application. Cell Death Discov. 2021;7:249.
doi: 10.1038/s41420-021-00647-1
pubmed: 34537813
pmcid: 8449783
Yu M, Lu B, Zhang J, Ding J, Liu P, Lu Y. tRNA-derived RNA fragments in cancer: current status and future perspectives. J Hematol Oncol. 2020;13:121.
doi: 10.1186/s13045-020-00955-6
pubmed: 32887641
pmcid: 7487644
Ivanov P, Emara MM, Villen J, Gygi SP, Anderson P. Angiogenin-induced tRNA fragments inhibit translation initiation. Mol Cell. 2011;43:613–23.
doi: 10.1016/j.molcel.2011.06.022
pubmed: 21855800
pmcid: 3160621
Kim HK, Fuchs G, Wang S, Wei W, Zhang Y, Park H, Roy-Chaudhuri B, Li P, Xu J, Chu K, et al. A transfer-RNA-derived small RNA regulates ribosome biogenesis. Nature. 2017;552:57–62.
doi: 10.1038/nature25005
pubmed: 29186115
pmcid: 6066594
Koera K, Nakamura K, Nakao K, Miyoshi J, Toyoshima K, Hatta T, Otani H, Aiba A, Katsuki M. K-ras is essential for the development of the mouse embryo. Oncogene. 1997;15(10):1151–9.
doi: 10.1038/sj.onc.1201284
pubmed: 9294608
Liu J, Zhou Y, Tong L, Wang X, Li Y, Wang H. Developmental potential of different embryos on day 3: a retrospective study. J Obstet Gynaecol. 2022;42:3322–7.
doi: 10.1080/01443615.2022.2125291
pubmed: 36149236
Liu S, Cui H, Li Q, Zhang L, Na Q, Liu C. RhoGDI2 is expressed in human trophoblasts and involved in their migration by inhibiting the activation of RAC1. Biol Reprod. 2014;90:88.
doi: 10.1095/biolreprod.113.111153
pubmed: 24554735
Tu Z, Wang Q, Cui T, Wang J, Ran H, Bao H, Lu J, Wang B, Lydon JP, DeMayo F, et al. Uterine RAC1 via Pak1-ERM signaling directs normal luminal epithelial integrity conducive to on-time embryo implantation in mice. Cell Death Differ. 2016;23:169–81.
doi: 10.1038/cdd.2015.98
pubmed: 26184908
Du ZQ, Liang H, Liu XM, Liu YH, Wang C, Yang CX. Single cell RNA-seq reveals genes vital to in vitro fertilized embryos and parthenotes in pigs. Sci Rep. 2021;11:14393.
doi: 10.1038/s41598-021-93904-3
pubmed: 34257377
pmcid: 8277874
Kaneko Y, Lecce L, Day ML, Murphy CR. Focal adhesion kinase localizes to sites of cell-to-cell contact in vivo and increases apically in rat uterine luminal epithelium and the blastocyst at the time of implantation. J Morphol. 2012;273:639–50.
doi: 10.1002/jmor.20010
pubmed: 22322452
Harden SL, Zhou J, Gharanei S, Diniz-da-Costa M, Lucas ES, Cui L, Murakami K, Fang J, Chen Q, Brosens JJ, Lee YH. Exometabolomic analysis of decidualizing human endometrial stromal and perivascular cells. Front Cell Dev Biol. 2021;9:626619.
doi: 10.3389/fcell.2021.626619
pubmed: 33585482
pmcid: 7876294
Paule S, Nebl T, Webb AI, Vollenhoven B, Rombauts LJ, Nie G. Proprotein convertase 5/6 cleaves platelet-derived growth factor A in the human endometrium in preparation for embryo implantation. Mol Hum Reprod. 2015;21:262–70.
doi: 10.1093/molehr/gau109
pubmed: 25429785
Purnell ET, Warner CM, Kort HI, Mitchell-Leef D, Elsner CW, Shapiro DB, Massey JB, Roudebush WE. Influence of the preimplantation embryo development (Ped) gene on embryonic platelet-activating factor (PAF) levels. J Assist Reprod Genet. 2006;23:269–73.
doi: 10.1007/s10815-006-9039-z
pubmed: 16799834
pmcid: 2530821
Stepanjuk A, Koel M, Pook M, Saare M, Jaager K, Peters M, Krjutskov K, Ingerpuu S, Salumets A. MUC20 expression marks the receptive phase of the human endometrium. Reprod Biomed Online. 2019;39:725–36.
doi: 10.1016/j.rbmo.2019.05.004
pubmed: 31519421
Moharrami T, Ai J, Ebrahimi-Barough S, Nouri M, Ziadi M, Pashaiefar H, Yazarlou F, Ahmadvand M, Najafi S, Modarressi MH. Influence of follicular fluid and seminal plasma on the expression of endometrial receptivity genes in endometrial cells. Cell J. 2021;22:457–66.
pubmed: 32347039
Elnaggar A, Farag AH, Gaber ME, Hafeez MA, Ali MS, Atef AM. AlphaVBeta3 integrin expression within uterine endometrium in unexplained infertility: a prospective cohort study. BMC Womens Health. 2017;17:90.
doi: 10.1186/s12905-017-0438-3
pubmed: 28950833
pmcid: 5615471
Jiang C, Gong W, Chen R, Ke H, Qu X, Yang W, Cheng Z. RhoA/ROCK/ARHGAP26 signaling in the eutopic and ectopic endometrium is involved in clinical characteristics of adenomyosis. J Int Med Res. 2018;46:5019–29.
doi: 10.1177/0300060518789038
pubmed: 30387365
pmcid: 6300968
Pfendler KC, Yoon J, Taborn GU, Kuehn MR, Iannaccone PM. Nodal and bone morphogenetic protein 5 interact in murine mesoderm formation and implantation. Genesis. 2000;28(1):1–14.
doi: 10.1002/1526-968X(200009)28:1<1::AID-GENE10>3.0.CO;2-X
pubmed: 11020711