FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Sci Rep / Bioinformatic analysis of endometrial miRNA expression profi...
Scientific reports2024; 14(1); 3900; doi: 10.1038/s41598-024-53499-x

Bioinformatic analysis of endometrial miRNA expression profile at day 26-28 of pregnancy in the mare.

Abstract: The establishment of the fetomaternal interface depends on precisely regulated communication between the conceptus and the uterine environment. Recent evidence suggests that microRNAs (miRNAs) may play an important role in embryo-maternal dialogue. This study aimed to determine the expression profile of endometrial miRNAs during days 26-28 of equine pregnancy. Additionally, the study aimed to predict target genes for differentially expressed miRNAs (DEmiRs) and their potential role in embryo attachment, adhesion, and implantation. Using next-generation sequencing, we identified 81 DEmiRs between equine endometrium during the pre-attachment period of pregnancy (day 26-28) and endometrium during the mid-luteal phase of the estrous cycle (day 10-12). The identified DEmiRs appear to have a significant role in regulating the expression of genes that influence cell fate and properties, as well as endometrial receptivity formation. These miRNAs include eca-miR-21, eca-miR-126-3p, eca-miR-145, eca-miR-451, eca-miR-491-5p, members of the miR-200 family, and the miRNA-17-92 cluster. The target genes predicted for the identified DEmiRs are associated with ion channel activity and sphingolipid metabolism. Furthermore, it was noted that the expression of mucin 1 and leukemia inhibitory factor, genes potentially regulated by the identified DEmiRs, was up-regulated at day 26-28 of pregnancy. This suggests that miRNAs may play a role in regulating specific genes to create a favorable uterine environment that is necessary for proper attachment, adhesion, and implantation of the embryo in mares.
© 2024. The Author(s).
Get Full Text
Publication Date: 2024-02-16 PubMed ID: 38365979PubMed Central: PMC10873421DOI: 10.1038/s41598-024-53499-xGoogle Scholar: Lookup
The Equine Research Bank provides access to a large database of publicly available scientific literature. Inclusion in the Research Bank does not imply endorsement of study methods or findings by Mad Barn.
LinkedInCopy
  • Journal Article

Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

The research focuses on identifying how microRNAs in a mare’s endometrium may influence the development of the embryo during days 26-28 of equine pregnancy. The study found key differentially expressed microRNAs and tied them to the regulation of important genes for embryo attachment and implantation.

Objective of the Research

  • The primary goal of this research was to investigate and understand the profile of microRNAs (miRNAs) within the endometrium of a mare during the 26th to 28th days of equine pregnancy. miRNAs are critical for cell fate, properties, and endometrial receptivity formation.
  • A secondary objective was to identify gene targets for the differentiated miRNAs and their potential role in the embryo’s adhesion, attachment, and implantation processes.

Methodology

  • The study used next-generation sequencing to identify differentially expressed miRNAs (DEmiRs) between the endometrium during the pre-attachment period of pregnancy (day 26-28) and the mid-luteal phase of the estrous cycle (day 10-12). A total of 81 DEmiRs were identified.
  • The researchers then made predictions of the target genes for the DEmiRs, focusing on how these genes might be connected with ion channel activity and sphingolipid metabolism.

Major Findings

  • Among the identified DEmiRs, miRNAs like eca-miR-21, eca-miR-126-3p, eca-miR-145, eca-miR-451, eca-miR-491-5p, members of the miR-200 family, and the miRNA-17-92 cluster were found to be significant in the regulation of genes that influenced cell fate and properties and endometrial receptivity formation.
  • The researchers observed that the expression of mucin 1 and leukemia inhibitory factor genes, which are potentially regulated by the identified DEmiRs, was up-regulated on the 26th to 28th days of pregnancy.
  • This increased expression suggests a potential role of miRNAs in facilitating a suitable uterine environment needed for the successful attachment, adhesion, and implantation of an embryo in mares.

Cite This Article

APA
Sadowska A, Molcan T, Wójtowicz A, Lukasik K, Pawlina-Tyszko K, Gurgul A, Ferreira-Dias G, Skarzynski DJ, Szóstek-Mioduchowska A. (2024). Bioinformatic analysis of endometrial miRNA expression profile at day 26-28 of pregnancy in the mare. Sci Rep, 14(1), 3900. https://doi.org/10.1038/s41598-024-53499-x

Publication

Scientific reports
ISSN: 2045-2322
NlmUniqueID: 101563288
Country: England
Language: English
Volume: 14
Issue: 1
Pages: 3900
PII: 3900

Researcher Affiliations

Sadowska, Agnieszka
  • Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Tuwima Street 10, 10-748, Olsztyn, Poland.
Molcan, Tomasz
  • Molecular Biology Laboratory, Institute of Animal Reproduction and Food Research, Polish Academy of Sciences, Tuwima Street 10, 10-748, Olsztyn, Poland.
Wójtowicz, Anna
  • Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Tuwima Street 10, 10-748, Olsztyn, Poland.
Lukasik, Karolina
  • Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Tuwima Street 10, 10-748, Olsztyn, Poland.
Pawlina-Tyszko, Klaudia
  • Department of Animal Molecular Biology, National Research Institute of Animal Production, Sarego Street 2, 31-047, Kraków, Poland.
Gurgul, Artur
  • Center for Experimental and Innovative Medicine, University of Agriculture in Krakow, Mickiewicza Street 21, 31-120, Kraków, Poland.
Ferreira-Dias, Graca
  • CIISA-Center for Interdisciplinary Research in Animal Health, Faculty of Veterinary Medicine, University of Lisbon, 1300-477, Lisbon, Portugal.
  • Associate Laboratory for Animal and Veterinary Sciences (AL4AnimalS), 1300-477, Lisbon, Portugal.
Skarzynski, Dariusz J
  • Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Tuwima Street 10, 10-748, Olsztyn, Poland.
Szóstek-Mioduchowska, Anna
  • Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Tuwima Street 10, 10-748, Olsztyn, Poland. a.szostek-mioduchowska@pan.olsztyn.pl.

MeSH Terms

  • Pregnancy
  • Horses / genetics
  • Animals
  • Female
  • Embryo Implantation / genetics
  • Endometrium / metabolism
  • MicroRNAs / genetics
  • MicroRNAs / metabolism
  • Uterus / metabolism
  • Embryo, Mammalian / metabolism

Grant Funding

  • 2017/01/X/NZ5/01528 / Narodowe Centrum Nauki
  • 5/FBW/2021 / Department of Reproductive Immunology and Pathology, Institute of Animal Reproduction and Food Research of Polish Academy of Sciences, Olsztyn, Poland

Conflict of Interest Statement

The authors declare no competing interests.

References

This article includes 85 references
  1. Stout T. Embryo-maternal communication during the first 4 weeks of equine pregnancy.. Theriogenology 2016;86:349–354.
    doi: 10.1016/j.theriogenology.2016.04.048pubmed: 27156682google scholar: lookup
  2. Smits K. Maternal recognition of pregnancy in the horse: Are microRNAs the secret messengers?. Int. J. Mol. Sci. 2020;21:419.
    doi: 10.3390/ijms21020419pmc: PMC7014256pubmed: 31936511google scholar: lookup
  3. Ginther OJ. Equine embryo mobility. A friend of theriogenologists.. J. Equine. Vet. Sci. 2021;106:103747.
    doi: 10.1016/j.jevs.2021.103747pubmed: 34670705google scholar: lookup
  4. Bauersachs S, Wolf E. Transcriptome analyses of bovine, porcine and equine endometrium during the pre-implantation phase.. Anim. Reprod. Sci. 2012;134:84–94.
    doi: 10.1016/j.anireprosci.2012.08.015pubmed: 22917876google scholar: lookup
  5. Wilsher S, Gower S, Allen WR. Persistence of an immunoreactive MUC1 protein at the feto-maternal interface throughout pregnancy in the mare.. Reprod. Fertil. Dev. 2013;25:753–761.
    doi: 10.1071/RD12152pubmed: 22951049google scholar: lookup
  6. Allen WR, Wilsher S. A review of implantation and early placentation in the mare.. Placenta 2009;30:1005–1015.
    doi: 10.1016/j.placenta.2009.09.007pubmed: 19850339google scholar: lookup
  7. Bauersachs S, Wolf E. Uterine responses to the preattachment embryo in domestic ungulates: Recognition of pregnancy and preparation for implantation.. Annu. Rev. Anim. Biosci. 2015;3:489–511.
    doi: 10.1146/annurev-animal-022114-110639pubmed: 25387113google scholar: lookup
  8. Ali A. MicroRNA–mRNA networks in pregnancy complications: A comprehensive downstream analysis of potential biomarkers.. Int. J. Mol. Sci. 2021;22:2313.
    doi: 10.3390/ijms22052313pmc: PMC7956714pubmed: 33669156google scholar: lookup
  9. Rottiers V, Näär AM. MicroRNAs in metabolism and metabolic disorders.. Nat. Rev. Mol. Cell. Biol. 2012;13:239–250.
    doi: 10.1038/nrm3313pmc: PMC4021399pubmed: 22436747google scholar: lookup
  10. Ponsuksili S. Differential expression of miRNAs and their target mRNAs in endometria prior to maternal recognition of pregnancy associates with endometrial receptivity for in vivo-and in vitro-produced bovine embryos.. Biol. Reprod. 2014;91:135.
    doi: 10.1095/biolreprod.114.121392pubmed: 25253731google scholar: lookup
  11. Zhang L. MiR-26a promoted endometrial epithelium cells (EECs) proliferation and induced stromal cells (ESCs) apoptosis via the PTEN-PI3K/AKT pathway in dairy goats.. J. Cell. Physiol. 2018;233:4688–4706.
    doi: 10.1002/jcp.26252pubmed: 29115668google scholar: lookup
  12. Li Q, Liu W, Chiu PCN, Yeung WSB. Mir-let-7a/g enhances uterine receptivity via suppressing Wnt/β-catenin under the modulation of ovarian hormones.. Reprod. Sci. 2020;27:1164–1174.
    doi: 10.1007/s43032-019-00115-3pubmed: 31942710google scholar: lookup
  13. Su L. Expression patterns of microRNAs in porcine endometrium and their potential roles in embryo implantation and placentation.. PLoS ONE 2014;9:e87867.
    doi: 10.1371/journal.pone.0087867pmc: PMC3914855pubmed: 24505325google scholar: lookup
  14. Hua R. Small RNA-seq analysis of extracellular vesicles from porcine uterine flushing fluids during peri-implantation.. Gene 2021;766:145117.
    doi: 10.1016/j.gene.2020.145117pubmed: 32920039google scholar: lookup
  15. Veit TD, Chies JAB. Tolerance versus immune response—microRNAs as important elements in the regulation of the HLA-G gene expression.. Transpl. Immunol. 2009;20:229–231.
    doi: 10.1016/j.trim.2008.11.001pubmed: 19038339google scholar: lookup
  16. Kose M. Expression pattern of microRNAs in ovine endometrium during the peri-implantation.. Theriogenology 2022;191:35–46.
    doi: 10.1016/j.theriogenology.2022.07.015pubmed: 35944411google scholar: lookup
  17. Klohonatz KM. Circulating miRNAs as potential alternative cell signaling associated with maternal recognition of pregnancy in the mare.. Biol. Reprod. 2016;95:124.
    doi: 10.1095/biolreprod.116.142935pubmed: 27760749google scholar: lookup
  18. Klohonatz KM. Non-coding RNA sequencing of equine endometrium during maternal recognition of pregnancy.. Genes 2019;10:821.
    doi: 10.3390/genes10100821pmc: PMC6826732pubmed: 31557877google scholar: lookup
  19. Klein C. Transcriptional profiling of equine endometrium before, during and after capsule disintegration during normal pregnancy and after oxytocin-induced luteostasis in non-pregnant mares.. PLoS ONE 2021;16:e0257161.
    doi: 10.1371/journal.pone.0257161pmc: PMC8494348pubmed: 34614002google scholar: lookup
  20. Liang J, Wang S, Wang Z. Role of microRNAs in embryo implantation.. Reprod. Biol. Endocrinol. 2017;15:90.
    doi: 10.1186/s12958-017-0309-7pmc: PMC5699189pubmed: 29162091google scholar: lookup
  21. Fakhr Y, Brindley DN, Hemmings DG. Physiological and pathological functions of sphingolipids in pregnancy.. Cell. Signal. 2021;85:110041.
    doi: 10.1016/j.cellsig.2021.110041pubmed: 33991614google scholar: lookup
  22. Mizugishi K. Maternal disturbance in activated sphingolipid metabolism causes pregnancy loss in mice.. J. Clin. Investig. 2007;117:2993–3006.
    doi: 10.1172/JCI30674pmc: PMC1978422pubmed: 17885683google scholar: lookup
  23. Adada M, Canals D, Hannun YA, Obeid LM. Sphingolipid regulation of ezrin, radixin, and moesin proteins family: Implications for cell dynamics.. Biochim. Biophys. Acta. 2014;1841:727–737.
    doi: 10.1016/j.bbalip.2013.07.002pmc: PMC3888837pubmed: 23850862google scholar: lookup
  24. Lessey BA. Adhesion molecules and implantation.. J. Reprod. Immunol. 2002;55:101–112.
    doi: 10.1016/S0165-0378(01)00139-5pubmed: 12062825google scholar: lookup
  25. Geekiyanage H, Chan C. MicroRNA-137/181c regulates serine palmitoyltransferase and in turn amyloid beta, novel targets in sporadic Alzheimers disease.. J. Neurosci. 2011;31:14820–14830.
    doi: 10.1523/JNEUROSCI.3883-11.2011pmc: PMC3200297pubmed: 21994399google scholar: lookup
  26. Chen MB. MicroRNA-101 down-regulates sphingosine kinase 1 in colorectal cancer cells.. Biochem. Biophys. Res. Commun. 2015;463:954–960.
    doi: 10.1016/j.bbrc.2015.06.041pubmed: 26071354google scholar: lookup
  27. Takehara M, Bandou H, Kobayashi K, Nagahama M. Clostridium perfringens α-toxin specifically induces endothelial cell death by promoting ceramide-mediated apoptosis.. Anaerobe 2020;65:102262.
    doi: 10.1016/j.anaerobe.2020.102262pubmed: 32828915google scholar: lookup
  28. Slater M, Murphy CR, Barden JA. Purinergic receptor expression in the apical plasma membrane of rat uterine epithelial cells during implantation.. Cell Calcium 2002;31:201–207.
    doi: 10.1016/S0143-4160(02)00033-7pubmed: 12098222google scholar: lookup
  29. Slater M, Murphy CR, Barden JA. Tenascin, E-cadherin and P2X calcium channel receptor expression is increased during rat blastocyst implantation.. Histochem. J. 2002;34:13–19.
    doi: 10.1023/A:1021335606896pubmed: 12365795google scholar: lookup
  30. Sadeghi H, Taylor HS. HOXA10 regulates endometrial GABAAπ receptor expression and membrane translocation.. Am. J. Physiol. Endocrinol. Metab. 2010;298:E889–E893.
    doi: 10.1152/ajpendo.00577.2009pmc: PMC3774337pubmed: 20103740google scholar: lookup
  31. Chan HC, Chen H, Ruan Y, Sun T. Physiology and pathophysiology of the epithelial barrier of the female reproductive tract: Role of ion channels.. Adv. Exp. Med. Biol. 2012;763:193–217.
    doi: 10.1007/978-1-4614-4711-5_10pubmed: 23397626google scholar: lookup
  32. Ruan Y, Chen H, Chan HC. Ion channels in the endometrium: Regulation of endometrial receptivity and embryo implantation.. Hum. Reprod. Update. 2014;20:517–529.
    doi: 10.1093/humupd/dmu006pubmed: 24591147google scholar: lookup
  33. Wang Z. miRNA in the regulation of ion channel/transporter expression.. Compreh. Physiol. 2013;3:599–653.
    doi: 10.1002/cphy.c110002pubmed: 23720324google scholar: lookup
  34. Berrout J. TRPA1-FGFR2 binding event is a regulatory oncogenic driver modulated by miRNA-142-3p.. Nat. Commun. 2017;8:947.
    doi: 10.1038/s41467-017-00983-wpmc: PMC5643494pubmed: 29038531google scholar: lookup
  35. Gross C, Tiwari D. Regulation of ion channels by microRNAs and the implication for epilepsy.. Curr. Neurol. Neurosci. Rep. 2018;18:60.
    doi: 10.1007/s11910-018-0870-2pmc: PMC6092942pubmed: 30046905google scholar: lookup
  36. Lessey BA, Young SL. What exactly is endometrial receptivity?. Fertil. Steril. 2019;111:611–617.
    doi: 10.1016/j.fertnstert.2019.02.009pubmed: 30929718google scholar: lookup
  37. Liu W. MicroRNA and embryo implantation.. Am. J. Reprod. Immunol. 2016;75:263–271.
    doi: 10.1111/aji.12470pubmed: 26707514google scholar: lookup
  38. Li W. Sequence analysis of microRNAs during pre-implantation between Meishan and Yorkshire pigs.. Gene 2018;646:20–27.
    doi: 10.1016/j.gene.2017.12.046pubmed: 29287711google scholar: lookup
  39. Yang Y. Expression of mmu-miR-96 in the endometrium during early pregnancy and its regulatory effects on stromal cell apoptosis via Bcl2.. Mol. Med. Rep. 2017;15:1547–1554.
    doi: 10.3892/mmr.2017.6212pmc: PMC5364990pubmed: 28259902google scholar: lookup
  40. Zang X. Differential microRNA expression involved in endometrial receptivity of goats.. Biomolecules 2021;11:472.
    doi: 10.3390/biom11030472pmc: PMC8004627pubmed: 33810054google scholar: lookup
  41. Huang C. Increased Krüppel-like factor 12 impairs embryo attachment via downregulation of leukemia inhibitory factor in women with recurrent implantation failure.. Cell. Death. Discov. 2018;4:23.
    doi: 10.1038/s41420-018-0088-8pmc: PMC6079092pubmed: 30109142google scholar: lookup
  42. Maccani MA, Padbury JF, Marsit CJ. miR-16 and miR-21 expression in the placenta is associated with fetal growth.. PLoS ONE 2011;6:e21210.
    doi: 10.1371/journal.pone.0021210pmc: PMC3115987pubmed: 21698265google scholar: lookup
  43. Burghardt RC. Integrins and extracellular matrix proteins at the maternal-fetal interface in domestic animals.. Cells Tissues Organs 2002;172:202–217.
    doi: 10.1159/000066969pubmed: 12476049google scholar: lookup
  44. Hill L, Browne G, Tulchinsky E. ZEB/miR-200 feedback loop: At the crossroads of signal transduction in cancer.. Int. J. Cancer. 2013;132:745–754.
    doi: 10.1002/ijc.27708pubmed: 22753312google scholar: lookup
  45. Wang XM. Role and mechanisms of action of microRNA-21 as regards the regulation of the WNT/β-catenin signaling pathway in the pathogenesis of non-alcoholic fatty liver disease.. Int. J. Mol. Med. 2019;44:2201–2212.
    pmc: PMC6844630pubmed: 31638173
  46. Li Z, Jia J, Gou J, Zhao X, Yi T. MicroRNA-451 plays a role in murine embryo implantation through targeting Ankrd46, as implicated by a microarray-based analysis.. Fertil. Steril. 2015;103:834–4.e4.
    doi: 10.1016/j.fertnstert.2014.11.024pubmed: 25542822google scholar: lookup
  47. Azhari F. The role of the serum exosomal and endometrial microRNAs in recurrent implantation failure.. J. Matern. Fetal. Neonatal. Med. 2022;35:815–825.
    doi: 10.1080/14767058.2020.1849095pubmed: 33249960google scholar: lookup
  48. Liu X. Up-regulation of miR-145 may contribute to repeated implantation failure after IVF-embryo transfer by targeting PAI-1.. Reprod. Biomed. Online. 2020;40:627–636.
    doi: 10.1016/j.rbmo.2020.01.018pubmed: 32205015google scholar: lookup
  49. Sirohi VK, Gupta K, Kapoor R, Dwivedi A. MicroRNA-145 targets Smad1 in endometrial stromal cells and regulates decidualization in rat.. J. Mol. Med. 2019;97:509–522.
    doi: 10.1007/s00109-019-01744-6pubmed: 30729278google scholar: lookup
  50. Zeinali T, Mansoori B, Mohammadi A, Baradaran B. Regulatory mechanisms of miR-145 expression and the importance of its function in cancer metastasis.. Biomed. Pharmacother. 2019;109:195–207.
    doi: 10.1016/j.biopha.2018.10.037pubmed: 30396077google scholar: lookup
  51. Meseguer M, Pellicer A, Simón C. MUC1 and endometrial receptivity.. Mol. Hum. Reprod. 1998;4:1089–1098.
    doi: 10.1093/molehr/4.12.1089pubmed: 9872358google scholar: lookup
  52. Samuel CA, Allen WR, Steven DH. Studies on the development of the equine placenta. I. Development of the microcotyledons.. J. Reprod. Fertil. 1974;41:441–445.
    doi: 10.1530/jrf.0.0410441pubmed: 4452985google scholar: lookup
  53. Carson DD. Mucin expression and function in the female reproductive tract.. Hum. Reprod. Update. 1998;4:459–464.
    doi: 10.1093/humupd/4.5.459pubmed: 10027596google scholar: lookup
  54. Hey NA, Aplin JD. Sialyl-Lewis x and Sialyl-Lewis a are associated with MUC1 in human endometrium.. Glycoconj. J. 1996;13:769–779.
    doi: 10.1007/BF00702341pubmed: 8910004google scholar: lookup
  55. Chen X. TDP-43 regulates cancer-associated microRNAs.. Protein. Cell. 2018;9:848–866.
    doi: 10.1007/s13238-017-0480-9pmc: PMC6160384pubmed: 28952053google scholar: lookup
  56. Li W. SP1-upregulated LBX2-AS1 promotes the progression of glioma by targeting the miR-491-5p/LIF axis.. J. Cancer. 2021;12:6989–7002.
    doi: 10.7150/jca.63289pmc: PMC8558668pubmed: 34729101google scholar: lookup
  57. Lv Y. miRNA and target gene expression in menstrual endometria and early pregnancy decidua.. Eur. J. Obstet. Gynecol. Reprod. Biol. 2016;197:27–30.
    doi: 10.1016/j.ejogrb.2015.11.003pubmed: 26699100google scholar: lookup
  58. Wu D, Guo J, Qi B, Xiao H. TGF-β1 induced proliferation, migration, and ECM accumulation through the SNHG11/miR-34b/LIF pathway in human pancreatic stellate cells.. Endocr. J. 2021;68:1347–1357.
    doi: 10.1507/endocrj.EJ21-0176pubmed: 34261825google scholar: lookup
  59. Kimber SJ. Leukemia inhibitory factor in implantation and uterine biology.. Reproduction 2005;130:131–145.
    doi: 10.1530/rep.1.00304pubmed: 16049151google scholar: lookup
  60. de Ruijter-Villani M, Deelen C, Stout TAE. Expression of leukaemia inhibitory factor at the conceptus? Maternal interface during preimplantation development and in the endometrium during the oestrous cycle in the mare.. Reprod. Fertil. Dev. 2015;28:1642–1651.
    doi: 10.1071/RD14334pubmed: 25881292google scholar: lookup
  61. Rosario GX, Stewart CL. The multifaceted actions of leukaemia inhibitory factor in mediating uterine receptivity and embryo implantation.. Am. J. Reprod. Immunol. 2016;75:246–255.
    doi: 10.1111/aji.12474pubmed: 26817565google scholar: lookup
  62. Yue X. Leukemia inhibitory factor promotes EMT through STAT3-dependent miR-21 induction.. Oncotarget 2016;7:3777–3790.
    doi: 10.18632/oncotarget.6756pmc: PMC4826169pubmed: 26716902google scholar: lookup
  63. Harvey MB. Proteinase expression in early mouse embryos is regulated by leukaemia inhibitory factor and epidermal growth factor.. Development 1995;121:1005–1014.
    doi: 10.1242/dev.121.4.1005pubmed: 7743917google scholar: lookup
  64. Kenney RM, Doig PA. Equine endometrial biopsy.. In: Morrow DA, editor. Current Therapy in Theriogenology. Saunders; 1986. pp. 723–729.
  65. Wójtowicz A. The potential role of miRNAs and regulation of their expression in the development of mare endometrial fibrosis.. Sci. Rep. 2023;13:15938.
    doi: 10.1038/s41598-023-42149-3pmc: PMC10518347pubmed: 37743390google scholar: lookup
  66. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. .
  67. Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads.. EMBnet.journal 2011;17:10–12.
    doi: 10.14806/ej.17.1.200google scholar: lookup
  68. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2.. Nat. Methods. 2012;9:357–359.
    doi: 10.1038/nmeth.1923pmc: PMC3322381pubmed: 22388286google scholar: lookup
  69. Kozomara A, Birgaoanum M, Griffiths-Jones S. miRBase: From microRNA sequences to function.. Nucleic. Acids. Res. 2019;47:D155–D162.
    doi: 10.1093/nar/gky1141pmc: PMC6323917pubmed: 30423142google scholar: lookup
  70. Friedländer MR, Mackowiak SD, Li N, Chen W, Rajewsky N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades.. Nucleic. Acids. Res. 2012;40:37–52.
    doi: 10.1093/nar/gkr688pmc: PMC3245920pubmed: 21911355google scholar: lookup
  71. Wickham S. ggplot2: Elegant Graphics for Data Analysis.. Springer; 2016.
  72. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol. 2014;15:550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  73. Gerlach W, Giegerich R. GUUGle: A utility for fast exact matching under RNA complementary rules including G-U base pairing.. Bioinformatics 2016;22:762–764.
    doi: 10.1093/bioinformatics/btk041pubmed: 16403789google scholar: lookup
  74. John B. Human MicroRNA targets.. PLoS Biol. 2004;2:e363.
    doi: 10.1371/journal.pbio.0020363pmc: PMC521178pubmed: 15502875google scholar: lookup
  75. Kertesz M, Iovino N, Unnerstall U, Gaulm U, Segal E. The role of site accessibility in microRNA target recognition.. Nat. Genet. 2007;39:1278–1284.
    doi: 10.1038/ng2135pubmed: 17893677google scholar: lookup
  76. Miranda KC. A pattern-based method for the identification of MicroRNA binding sites and their corresponding heteroduplexes.. Cell. 2006;126:1203–1217.
    doi: 10.1016/j.cell.2006.07.031pubmed: 16990141google scholar: lookup
  77. Krüger J, Rehmsmeier M. RNAhybrid: MicroRNA target prediction easy, fast and flexible.. Nucleic. Acids. Res. 2006;34:W451–454.
    doi: 10.1093/nar/gkl243pmc: PMC1538877pubmed: 16845047google scholar: lookup
  78. Lukasik A, Wójcikowski M, Zielenkiewicz P. Tools4miRs—one place to gather all the tools for miRNA analysis.. Bioinformatics 2016;32:2722–2724.
    doi: 10.1093/bioinformatics/btw189pmc: PMC5013900pubmed: 27153626google scholar: lookup
  79. Yu G, Wang LG, Han Y, He QY. clusterProfiler: An R package for comparing biological themes among gene clusters.. OMICS 2012;16:284–287.
    doi: 10.1089/omi.2011.0118pmc: PMC3339379pubmed: 22455463google scholar: lookup
  80. Yun G, Wang LG, Yan GR, He QY. DOSE: An R/Bioconductor package for disease ontology semantic and enrichment analysis.. Bioinformatics 2015;31:608–609.
    doi: 10.1093/bioinformatics/btu684pubmed: 25677125google scholar: lookup
  81. Durinck S, Spellman PT, Birney E, Huber W. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt.. Nat. Protoc. 2009;4:1184–1191.
    doi: 10.1038/nprot.2009.97pmc: PMC3159387pubmed: 19617889google scholar: lookup
  82. Morgan M, Shepherd L. AnnotationHub: Client to access AnnotationHub resources.. R package version 3.4.0 (2022).
  83. Kolde R. Pheatmap: pretty heatmaps.. R package version 1. vol. 2, 747 (2012).
  84. Zhao S, Fernald RD. Comprehensive algorithm for quantitative real-time polymerase chain reaction.. J. Comput. Biol. 2005;12:1047–1064.
    doi: 10.1089/cmb.2005.12.1047pmc: PMC2716216pubmed: 16241897google scholar: lookup
  85. Ibrahim S, Szostek-Mioduchowska A, Skarzynski D. Expression profiling of selected miRNAs in equine endometrium in response to LPS challenge in vitro: A new understanding of the inflammatory immune response.. Vet. Immunol. Immunopathol. 2019;209:37–44.
    doi: 10.1016/j.vetimm.2019.02.006pubmed: 30885304google scholar: lookup

Citations

This article has been cited 0 times.
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.