The potential role of miRNAs and regulation of their expression in the development of mare endometrial fibrosis.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
24 09 2023
24 09 2023
Historique:
received:
27
02
2023
accepted:
06
09
2023
medline:
26
9
2023
pubmed:
25
9
2023
entrez:
24
9
2023
Statut:
epublish
Résumé
Mare endometrial fibrosis (endometrosis), is one of the main causes of equine infertility. Despite the high prevalence, both ethology, pathogenesis and the nature of its progression remain poorly understood. Recent studies have shown that microRNAs (miRNAs) are important regulators in multiple cellular processes and functions under physiological and pathological circumstances. In this article, we reported changes in miRNA expression at different stages of endometrosis and the effect of transforming growth factor (TGF)-β1 on the expression of the most dysregulated miRNAs. We identified 1, 26, and 5 differentially expressed miRNAs (DEmiRs), in categories IIA (mild fibrosis), IIB (moderate fibrosis), and III (severe fibrosis) groups compared to category I (no fibrosis) endometria group, respectively (P
Identifiants
pubmed: 37743390
doi: 10.1038/s41598-023-42149-3
pii: 10.1038/s41598-023-42149-3
pmc: PMC10518347
doi:
Substances chimiques
Cytokines
0
MicroRNAs
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
15938Informations de copyright
© 2023. Springer Nature Limited.
Références
Schoniger, S. & Schoon, H. A. The healthy and diseased equine endometrium: A review of morphological features and molecular analyses. Animals 10, 40625. https://doi.org/10.3390/ani10040625 (2020).
doi: 10.3390/ani10040625
Bracher, V., Mathias, S. & Allen, W. R. Influence of chronic degenerative endometritis (endometrosis) on placental development in the mare. Equine Vet. J. 28, 180–188. https://doi.org/10.1111/j.2042-3306.1996.tb03771.x (1996).
doi: 10.1111/j.2042-3306.1996.tb03771.x
pubmed: 28976715
Kenney, R. M. Cyclic and pathologic changes of the mare endometrium as detected by biopsy, with a note on early embryonic death. J. Am. Vet. Med. Assoc. 172, 241–262 (1978).
pubmed: 621166
Hoffmann, C. et al. The equine endometrosis: New insights into the pathogenesis. Anim. Reprod. Sci. 111, 261–278. https://doi.org/10.1016/j.anireprosci.2008.03.019 (2009).
doi: 10.1016/j.anireprosci.2008.03.019
pubmed: 18468817
Lamceva, J., Uljanovs, R. & Strumfa, I. The main theories on the pathogenesis of endometriosis. Int. J. Mol. Sci. 24, 254. https://doi.org/10.3390/ijms24054254 (2023).
doi: 10.3390/ijms24054254
Liu, I. K. & Troedsson, M. H. The diagnosis and treatment of endometritis in the mare: Yesterday and today. Theriogenology 70, 415–420. https://doi.org/10.1016/j.theriogenology.2008.05.040 (2008).
doi: 10.1016/j.theriogenology.2008.05.040
pubmed: 18513792
Ricketts, S. W. & Alonso, S. The effect of age and parity on the development of equine chronic endometrial disease. Equine Vet. J. 23, 189–192. https://doi.org/10.1111/j.2042-3306.1991.tb02752.x (1991).
doi: 10.1111/j.2042-3306.1991.tb02752.x
pubmed: 1884699
Szostek-Mioduchowska, A. Z., Lukasik, K., Skarzynski, D. J. & Okuda, K. Effect of transforming growth factor-beta1 on alpha-smooth muscle actin and collagen expression in equine endometrial fibroblasts. Theriogenology 124, 9–17. https://doi.org/10.1016/j.theriogenology.2018.10.005 (2019).
doi: 10.1016/j.theriogenology.2018.10.005
pubmed: 30321755
Szostek-Mioduchowska, A. Z., Baclawska, A., Rebordao, M. R., Ferreira-Dias, G. & Skarzynski, D. J. Prostaglandins effect on matrix metallopeptidases and collagen in mare endometrial fibroblasts. Theriogenology 153, 74–84. https://doi.org/10.1016/j.theriogenology.2020.04.040 (2020).
doi: 10.1016/j.theriogenology.2020.04.040
pubmed: 32442743
Szostek-Mioduchowska, A. Z., Baclawska, A., Okuda, K. & Skarzynski, D. J. Effect of proinflammatory cytokines on endometrial collagen and metallopeptidase expression during the course of equine endometrosis. Cytokine 123, 154767. https://doi.org/10.1016/j.cyto.2019.154767 (2019).
doi: 10.1016/j.cyto.2019.154767
pubmed: 31265984
Szostek-Mioduchowska, A., Slowinska, M., Pacewicz, J., Skarzynski, D. J. & Okuda, K. Matrix metallopeptidase expression and modulation by transforming growth factor-beta1 in equine endometrosis. Sci. Rep. 10, 1119. https://doi.org/10.1038/s41598-020-58109-0 (2020).
doi: 10.1038/s41598-020-58109-0
pubmed: 31980722
pmcid: 6981191
Rebordao, M. R. et al. Neutrophil extracellular traps formation by bacteria causing endometritis in the mare. J. Reprod. Immunol. 106, 41–49. https://doi.org/10.1016/j.jri.2014.08.003 (2014).
doi: 10.1016/j.jri.2014.08.003
pubmed: 25218891
Alpoim-Moreira, J. et al. Metallopeptidades 2 and 9 genes epigenetically modulate equine endometrial fibrosis. Front. Vet. Sci. 9, 970003. https://doi.org/10.3389/fvets.2022.970003 (2022).
doi: 10.3389/fvets.2022.970003
pubmed: 36032279
pmcid: 9412240
Szóstek-Mioduchowska, A. et al. 5th International Conference on Uterine Disorders in Farm Animals: Endometritis as a Cause of Infertility in Domestic Animals 22.
Meng, X. M., Nikolic-Paterson, D. J. & Lan, H. Y. TGF-beta: The master regulator of fibrosis. Nat. Rev. Nephrol. 12, 325–338. https://doi.org/10.1038/nrneph.2016.48 (2016).
doi: 10.1038/nrneph.2016.48
pubmed: 27108839
O’Reilly, S. MicroRNAs in fibrosis: Opportunities and challenges. Arthritis Res. Ther. 18, 11. https://doi.org/10.1186/s13075-016-0929-x (2016).
doi: 10.1186/s13075-016-0929-x
pubmed: 26762516
pmcid: 4718015
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. 209, 37–44. https://doi.org/10.1016/j.vetimm.2019.02.006 (2019).
doi: 10.1016/j.vetimm.2019.02.006
pubmed: 30885304
Adwent, I. et al. The influence of adalimumab and cyclosporine A on the expression profile of the genes related to TGFbeta signaling pathways in keratinocyte cells treated with lipopolysaccharide A. Mediat. Inflamm. 2020, 3821279. https://doi.org/10.1155/2020/3821279 (2020).
doi: 10.1155/2020/3821279
O’Brien, J., Hayder, H., Zayed, Y. & Peng, C. Overview of microRNA biogenesis, mechanisms of actions, and circulation. Front. Endocrinol. 9, 402. https://doi.org/10.3389/fendo.2018.00402 (2018).
doi: 10.3389/fendo.2018.00402
Ma, Y. et al. MiR-130b increases fibrosis of HMC cells by regulating the TGF-beta1 pathway in diabetic nephropathy. J. Cell Biochem. 120, 4044–4056. https://doi.org/10.1002/jcb.27688 (2019).
doi: 10.1002/jcb.27688
pubmed: 30260005
Ye, M., Wang, S., Sun, P. & Qie, J. Integrated microRNA expression profile reveals dysregulated miR-20a-5p and miR-200a-3p in liver fibrosis. Biomed. Res. Int. 2021, 9583932. https://doi.org/10.1155/2021/9583932 (2021).
doi: 10.1155/2021/9583932
pubmed: 34235224
pmcid: 8218919
Zhang, W. et al. MicroRNA-26a protects the heart against hypertension-induced myocardial fibrosis. J. Am. Heart Assoc. 9, e017970. https://doi.org/10.1161/JAHA.120.017970 (2020).
doi: 10.1161/JAHA.120.017970
pubmed: 32865120
pmcid: 7726969
Kanehisa, M. Toward understanding the origin and evolution of cellular organisms. Protein Sci. 28, 1947–1951. https://doi.org/10.1002/pro.3715 (2019).
doi: 10.1002/pro.3715
pubmed: 31441146
pmcid: 6798127
Kanehisa, M., Furumichi, M., Sato, Y., Kawashima, M. & Ishiguro-Watanabe, M. KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 51, D587–D592. https://doi.org/10.1093/nar/gkac963 (2023).
doi: 10.1093/nar/gkac963
pubmed: 36300620
Kanehisa, M. & Goto, S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 28, 27–30. https://doi.org/10.1093/nar/28.1.27 (2000).
doi: 10.1093/nar/28.1.27
pubmed: 10592173
pmcid: 102409
Hinz, B. Masters and servants of the force: The role of matrix adhesions in myofibroblast force perception and transmission. Eur. J. Cell Biol. 85, 175–181. https://doi.org/10.1016/j.ejcb.2005.09.004 (2006).
doi: 10.1016/j.ejcb.2005.09.004
pubmed: 16546559
Bonnans, C., Chou, J. & Werb, Z. Remodelling the extracellular matrix in development and disease. Nat. Rev. Mol. Cell Biol. 15, 786–801. https://doi.org/10.1038/nrm3904 (2014).
doi: 10.1038/nrm3904
pubmed: 25415508
pmcid: 4316204
Yang, L. et al. Periostin facilitates skin sclerosis via PI3K/Akt dependent mechanism in a mouse model of scleroderma. PLoS ONE 7, e41994. https://doi.org/10.1371/journal.pone.0041994 (2012).
doi: 10.1371/journal.pone.0041994
pubmed: 22911870
pmcid: 3404023
Wei, L. et al. Asiatic acid attenuates CCl4-induced liver fibrosis in rats by regulating the PI3K/AKT/mTOR and Bcl-2/Bax signaling pathways. Int. Immunopharmacol. 60, 1–8. https://doi.org/10.1016/j.intimp.2018.04.016 (2018).
doi: 10.1016/j.intimp.2018.04.016
pubmed: 29702278
Qin, W., Cao, L. & Massey, I. Y. Role of PI3K/Akt signaling pathway in cardiac fibrosis. Mol. Cell Biochem. 476, 4045–4059. https://doi.org/10.1007/s11010-021-04219-w (2021).
doi: 10.1007/s11010-021-04219-w
pubmed: 34244974
Wang, J. et al. Targeting PI3K/AKT signaling for treatment of idiopathic pulmonary fibrosis. Acta Pharm. Sin. B 12, 18–32. https://doi.org/10.1016/j.apsb.2021.07.023 (2022).
doi: 10.1016/j.apsb.2021.07.023
pubmed: 35127370
Chang, R., Zheng, W., Sun, Y. & Xu, T. microRNA-1388-5p inhibits NF-kappaB signaling pathway in miiuy croaker through targeting IRAK1. Dev. Comp. Immunol. 119, 104025. https://doi.org/10.1016/j.dci.2021.104025 (2021).
doi: 10.1016/j.dci.2021.104025
pubmed: 33539892
Luedde, T. & Schwabe, R. F. NF-kappaB in the liver-linking injury, fibrosis and hepatocellular carcinoma. Nat. Rev. Gastroenterol. Hepatol. 8, 108–118. https://doi.org/10.1038/nrgastro.2010.213 (2011).
doi: 10.1038/nrgastro.2010.213
pubmed: 21293511
pmcid: 3295539
Domino, M. et al. Expression of genes involved in the NF-kappaB-dependent pathway of the fibrosis in the mare endometrium. Theriogenology 147, 18–24. https://doi.org/10.1016/j.theriogenology.2020.01.055 (2020).
doi: 10.1016/j.theriogenology.2020.01.055
pubmed: 32074495
Kenney, R. M. & Doig, P. A. Equine endometrial biopsy. Curr. Therapy Theriogenol. 723–729, 723–729 (1986).
Qin, Y. et al. Salvia miltiorrhiza-derived Sal-miR-58 induces autophagy and attenuates inflammation in vascular smooth muscle cells. Mol. Ther. Nucleic Acids 21, 492–511. https://doi.org/10.1016/j.omtn.2020.06.015 (2020).
doi: 10.1016/j.omtn.2020.06.015
pubmed: 32679544
pmcid: 7360890
Jiang, X. P., Ai, W. B., Wan, L. Y., Zhang, Y. Q. & Wu, J. F. The roles of microRNA families in hepatic fibrosis. Cell Biosci. 7, 34. https://doi.org/10.1186/s13578-017-0161-7 (2017).
doi: 10.1186/s13578-017-0161-7
pubmed: 28680559
pmcid: 5496266
Zhao, M. et al. MicroRNA-34a: A novel therapeutic target in fibrosis. Front. Physiol. 13, 895242. https://doi.org/10.3389/fphys.2022.895242 (2022).
doi: 10.3389/fphys.2022.895242
pubmed: 35795649
pmcid: 9250967
He, Y., Huang, C., Lin, X. & Li, J. MicroRNA-29 family, a crucial therapeutic target for fibrosis diseases. Biochimie 95, 1355–1359. https://doi.org/10.1016/j.biochi.2013.03.010 (2013).
doi: 10.1016/j.biochi.2013.03.010
pubmed: 23542596
Roderburg, C. et al. Micro-RNA profiling reveals a role for miR-29 in human and murine liver fibrosis. Hepatology 53, 209–218. https://doi.org/10.1002/hep.23922 (2011).
doi: 10.1002/hep.23922
pubmed: 20890893
Huang, D. et al. Inhibiting effect of miR-29 on proliferation and migration of uterine leiomyoma via the STAT3 signaling pathway. Aging (Albany NY) 14, 1307–1320. https://doi.org/10.18632/aging.203873 (2022).
doi: 10.18632/aging.203873
pubmed: 35113040
Mott, J. L., Kobayashi, S., Bronk, S. F. & Gores, G. J. mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 26, 6133–6140. https://doi.org/10.1038/sj.onc.1210436 (2007).
doi: 10.1038/sj.onc.1210436
pubmed: 17404574
pmcid: 2432524
Cargnello, M. & Roux, P. P. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol. Mol. Biol. Rev. 75, 50–83. https://doi.org/10.1128/MMBR.00031-10 (2011).
doi: 10.1128/MMBR.00031-10
pubmed: 21372320
pmcid: 3063353
Ihn, H. Pathogenesis of fibrosis: Role of TGF-beta and CTGF. Curr. Opin. Rheumatol. 14, 681–685. https://doi.org/10.1097/00002281-200211000-00009 (2002).
doi: 10.1097/00002281-200211000-00009
pubmed: 12410091
Derynck, R. & Zhang, Y. E. Smad-dependent and Smad-independent pathways in TGF-beta family signalling. Nature 425, 577–584. https://doi.org/10.1038/nature02006 (2003).
doi: 10.1038/nature02006
pubmed: 14534577
Mia, M. M. & Singh, M. K. New insights into Hippo/YAP signaling in fibrotic diseases. Cells 11, 2065. https://doi.org/10.3390/cells11132065 (2022).
doi: 10.3390/cells11132065
pubmed: 35805148
pmcid: 9265296
Jorgenson, A. J. et al. TAZ activation drives fibroblast spheroid growth, expression of profibrotic paracrine signals, and context-dependent ECM gene expression. Am. J. Physiol. Cell Physiol. 312, C277–C285. https://doi.org/10.1152/ajpcell.00205.2016 (2017).
doi: 10.1152/ajpcell.00205.2016
pubmed: 27881410
Engelman, J. A., Luo, J. & Cantley, L. C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 7, 606–619. https://doi.org/10.1038/nrg1879 (2006).
doi: 10.1038/nrg1879
pubmed: 16847462
Li, M. et al. Icaritin inhibits skin fibrosis through regulating AMPK and Wnt/beta-catenin Signaling. Cell Biochem. Biophys. 79, 231–238. https://doi.org/10.1007/s12013-020-00952-z (2021).
doi: 10.1007/s12013-020-00952-z
pubmed: 33125640
Goffin, J. M. et al. Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J. Cell Biol. 172, 259–268. https://doi.org/10.1083/jcb.200506179 (2006).
doi: 10.1083/jcb.200506179
pubmed: 16401722
pmcid: 2063555
Cordova-Rivas, S. et al. 5p and 3p strands of miR-34 family members have differential effects in cell proliferation, migration, and invasion in cervical cancer cells. Int. J. Mol. Sci. 20, 545. https://doi.org/10.3390/ijms20030545 (2019).
doi: 10.3390/ijms20030545
pubmed: 30696040
pmcid: 6387060
Tarasov, V. et al. Differential regulation of microRNAs by p53 revealed by massively parallel sequencing: miR-34a is a p53 target that induces apoptosis and G1-arrest. Cell Cycle 6, 1586–1593. https://doi.org/10.4161/cc.6.13.4436 (2007).
doi: 10.4161/cc.6.13.4436
pubmed: 17554199
Zhang, L. & Yang, F. Tanshinone IIA improves diabetes-induced renal fibrosis by regulating the miR-34-5p/Notch1 axis. Food Sci. Nutr. 10, 4019–4040. https://doi.org/10.1002/fsn3.2998 (2022).
doi: 10.1002/fsn3.2998
pubmed: 36348805
pmcid: 9632221
Huang, Y., Qi, Y., Du, J. Q. & Zhang, D. F. MicroRNA-34a regulates cardiac fibrosis after myocardial infarction by targeting Smad4. Expert Opin. Ther. Targets 18, 1355–1365. https://doi.org/10.1517/14728222.2014.961424 (2014).
doi: 10.1517/14728222.2014.961424
pubmed: 25322725
Li, W. Q. et al. The rno-miR-34 family is upregulated and targets ACSL1 in dimethylnitrosamine-induced hepatic fibrosis in rats. FEBS J. 278, 1522–1532. https://doi.org/10.1111/j.1742-4658.2011.08075.x (2011).
doi: 10.1111/j.1742-4658.2011.08075.x
pubmed: 21366874
Sharp, D. C., Thatcher, M. J., Salute, M. E. & Fuchs, A. R. Relationship between endometrial oxytocin receptors and oxytocin-induced prostaglandin F2 alpha release during the oestrous cycle and early pregnancy in pony mares. J. Reprod. Fertil. 109, 137–144. https://doi.org/10.1530/jrf.0.1090137 (1997).
doi: 10.1530/jrf.0.1090137
pubmed: 9068425
Chen, C. et al. Mesenchymal stem cell transplantation in tight-skin mice identifies miR-151-5p as a therapeutic target for systemic sclerosis. Cell Res. 27, 559–577. https://doi.org/10.1038/cr.2017.11 (2017).
doi: 10.1038/cr.2017.11
pubmed: 28106077
pmcid: 5385608
Jeong, D. et al. miR-25 tough decoy enhances cardiac function in heart failure. Mol. Ther. 26, 718–729. https://doi.org/10.1016/j.ymthe.2017.11.014 (2018).
doi: 10.1016/j.ymthe.2017.11.014
pubmed: 29273502
Sun, B. et al. miR-205 suppresses pulmonary fibrosis by targeting GATA3 through inhibition of endoplasmic reticulum stress. Curr. Pharm. Biotechnol. 21, 720–726. https://doi.org/10.2174/1389201021666191210115614 (2020).
doi: 10.2174/1389201021666191210115614
pubmed: 31820686
Yuan, H. & Gao, J. The role of miR370 in fibrosis after myocardial infarction. Mol. Med. Rep. 15, 3041–3047. https://doi.org/10.3892/mmr.2017.6397 (2017).
doi: 10.3892/mmr.2017.6397
pubmed: 28350072
pmcid: 5428907
Mullenbrock, S. et al. Systems analysis of transcriptomic and proteomic profiles identifies novel regulation of fibrotic programs by miRNAs in pulmonary fibrosis fibroblasts. Genes 9, 120588. https://doi.org/10.3390/genes9120588 (2018).
doi: 10.3390/genes9120588
Fujisawa, C. et al. The role for miR-146b-5p in the attenuation of dermal fibrosis and angiogenesis by targeting PDGFRalpha in skin wounds. J. Investig. Dermatol. 142, 1990–2002. https://doi.org/10.1016/j.jid.2021.11.037 (2022).
doi: 10.1016/j.jid.2021.11.037
pubmed: 34929177
Gong, L. et al. S1PR3 deficiency alleviates radiation-induced pulmonary fibrosis through the regulation of epithelial–mesenchymal transition by targeting miR-495-3p. J. Cell Physiol. 235, 2310–2324. https://doi.org/10.1002/jcp.29138 (2020).
doi: 10.1002/jcp.29138
pubmed: 31489649
Tu, Z. et al. Loss of miR-146b-5p promotes T cell acute lymphoblastic leukemia migration and invasion via the IL-17A pathway. J. Cell Biochem. 120, 5936–5948. https://doi.org/10.1002/jcb.27882 (2019).
doi: 10.1002/jcb.27882
pubmed: 30362152
Guo, B., Hui, Q., Xu, Z., Chang, P. & Tao, K. miR-495 inhibits the growth of fibroblasts in hypertrophic scars. Aging (Albany NY) 11, 2898–2910. https://doi.org/10.18632/aging.101965 (2019).
doi: 10.18632/aging.101965
pubmed: 31085805
Liao, Y. et al. Therapeutic silencing miR-146b-5p improves cardiac remodeling in a porcine model of myocardial infarction by modulating the wound reparative phenotype. Protein Cell 12, 194–212. https://doi.org/10.1007/s13238-020-00750-6 (2021).
doi: 10.1007/s13238-020-00750-6
pubmed: 32845445
Friedman, S. L., Sheppard, D., Duffield, J. S. & Violette, S. Therapy for fibrotic diseases: Nearing the starting line. Sci. Transl. Med. 5, 167. https://doi.org/10.1126/scitranslmed.3004700 (2013).
doi: 10.1126/scitranslmed.3004700
Mehal, W. Z., Iredale, J. & Friedman, S. L. Scraping fibrosis: Expressway to the core of fibrosis. Nat. Med. 17, 552–553. https://doi.org/10.1038/nm0511-552 (2011).
doi: 10.1038/nm0511-552
pubmed: 21546973
pmcid: 3219752
Yanguas, S. C. et al. Experimental models of liver fibrosis. Arch. Toxicol. 90, 1025–1048. https://doi.org/10.1007/s00204-015-1543-4 (2016).
doi: 10.1007/s00204-015-1543-4
pubmed: 26047667
Witwer, K. W. Circulating microRNA biomarker studies: Pitfalls and potential solutions. Clin. Chem. 61, 56–63. https://doi.org/10.1373/clinchem.2014.221341 (2015).
doi: 10.1373/clinchem.2014.221341
pubmed: 25391989
Christopher, A. F. et al. MicroRNA therapeutics: Discovering novel targets and developing specific therapy. Perspect. Clin. Res. 7, 68–74. https://doi.org/10.4103/2229-3485.179431 (2016).
doi: 10.4103/2229-3485.179431
pubmed: 27141472
pmcid: 4840794
Condrat, C. E. et al. miRNAs as biomarkers in disease: Latest findings regarding their role in diagnosis and prognosis. Cells 9, 20276. https://doi.org/10.3390/cells9020276 (2020).
doi: 10.3390/cells9020276
Hanna, J., Hossain, G. S. & Kocerha, J. The potential for microRNA therapeutics and clinical research. Front. Genet. 10, 478. https://doi.org/10.3389/fgene.2019.00478 (2019).
doi: 10.3389/fgene.2019.00478
pubmed: 31156715
pmcid: 6532434
Szostek, A. Z., Lukasik, K., Galvao, A. M., Ferreira-Dias, G. M. & Skarzynski, D. J. Impairment of the interleukin system in equine endometrium during the course of endometrosis. Biol. Reprod. 89, 79. https://doi.org/10.1095/biolreprod.113.109447 (2013).
doi: 10.1095/biolreprod.113.109447
pubmed: 23946535
Snider, T. A., Sepoy, C. & Holyoak, G. R. Equine endometrial biopsy reviewed: Observation, interpretation, and application of histopathologic data. Theriogenology 75, 1567–1581. https://doi.org/10.1016/j.theriogenology.2010.12.013 (2011).
doi: 10.1016/j.theriogenology.2010.12.013
pubmed: 21356552
Szostek-Mioduchowska, A. Z. et al. Effects of cortisol on prostaglandin F2alpha secretion and expression of genes involved in the arachidonic acid metabolic pathway in equine endometrium—In vitro study. Theriogenology 173, 221–229. https://doi.org/10.1016/j.theriogenology.2021.08.009 (2021).
doi: 10.1016/j.theriogenology.2021.08.009
pubmed: 34399386
Szostek, A. Z. et al. Effects of cell storage and passage on basal and oxytocin-regulated prostaglandin secretion by equine endometrial epithelial and stromal cells. Theriogenology 77, 1698–1708. https://doi.org/10.1016/j.theriogenology.2011.12.015 (2012).
doi: 10.1016/j.theriogenology.2011.12.015
pubmed: 22357062
Huang, H. et al. The microRNA MiR-29c alleviates renal fibrosis via TPM1-mediated suppression of the Wnt/beta-catenin pathway. Front. Physiol. 11, 331. https://doi.org/10.3389/fphys.2020.00331 (2020).
doi: 10.3389/fphys.2020.00331
pubmed: 32346368
pmcid: 7171049
Wang, X. et al. Upregulated miR-29c suppresses silica-induced lung fibrosis through the Wnt/beta-catenin pathway in mice. Hum. Exp. Toxicol. 37, 944–952. https://doi.org/10.1177/0960327117741750 (2018).
doi: 10.1177/0960327117741750
pubmed: 29216763
Zhao, S. & Fernald, R. D. Comprehensive algorithm for quantitative real-time polymerase chain reaction. J. Comput. Biol. 12, 1047–1064. https://doi.org/10.1089/cmb.2005.12.1047 (2005).
doi: 10.1089/cmb.2005.12.1047
pubmed: 16241897
Andersen, C. L., Jensen, J. L. & Orntoft, T. F. Normalization of real-time quantitative reverse transcription-PCR data: A model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets. Cancer Res. 64, 5245–5250. https://doi.org/10.1158/0008-5472.CAN-04-0496 (2004).
doi: 10.1158/0008-5472.CAN-04-0496
pubmed: 15289330
Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet. J. 17, 3. https://doi.org/10.14806/ej.17.1.200 (2011).
doi: 10.14806/ej.17.1.200
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359. https://doi.org/10.1038/nmeth.1923 (2012).
doi: 10.1038/nmeth.1923
pubmed: 22388286
pmcid: 3322381
Kozomara, A., Birgaoanu, M. & Griffiths-Jones, S. miRBase: From microRNA sequences to function. Nucleic Acids Res. 47, D155–D162. https://doi.org/10.1093/nar/gky1141 (2019).
doi: 10.1093/nar/gky1141
pubmed: 30423142
Friedlander, M. R., Mackowiak, S. D., Li, N., Chen, W. & Rajewsky, N. miRDeep2 accurately identifies known and hundreds of novel microRNA genes in seven animal clades. Nucleic Acids Res. 40, 37–52. https://doi.org/10.1093/nar/gkr688 (2012).
doi: 10.1093/nar/gkr688
pubmed: 21911355
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550. https://doi.org/10.1186/s13059-014-0550-8 (2014).
doi: 10.1186/s13059-014-0550-8
pubmed: 25516281
pmcid: 4302049
Du, K. et al. Integrated analysis of microRNAs, circular RNAs, long non-coding RNAs, and mRNAs revealed competing endogenous RNA networks involved in brown adipose tissue whitening in rabbits. BMC Genom. 23, 779. https://doi.org/10.1186/s12864-022-09025-2 (2022).
doi: 10.1186/s12864-022-09025-2
He, J. et al. Integrated analysis of miRNAs and mRNA profiling reveals the potential roles of miRNAs in sheep hair follicle development. BMC Genom. 23, 722. https://doi.org/10.1186/s12864-022-08954-2 (2022).
doi: 10.1186/s12864-022-08954-2
Lukasik, A., Wojcikowski, M. & Zielenkiewicz, P. Tools4miRs—One place to gather all the tools for miRNA analysis. Bioinformatics 32, 2722–2724. https://doi.org/10.1093/bioinformatics/btw189 (2016).
doi: 10.1093/bioinformatics/btw189
pubmed: 27153626
pmcid: 5013900
John, B. et al. Human microRNA targets. PLoS Biol. 2, e363. https://doi.org/10.1371/journal.pbio.0020363 (2004).
doi: 10.1371/journal.pbio.0020363
pubmed: 15502875
pmcid: 521178
Kertesz, M., Iovino, N., Unnerstall, U., Gaul, U. & Segal, E. The role of site accessibility in microRNA target recognition. Nat. Genet. 39, 1278–1284. https://doi.org/10.1038/ng2135 (2007).
doi: 10.1038/ng2135
pubmed: 17893677
Miranda, K. C. et al. A pattern-based method for the identification of microRNA binding sites and their corresponding heteroduplexes. Cell 126, 1203–1217. https://doi.org/10.1016/j.cell.2006.07.031 (2006).
doi: 10.1016/j.cell.2006.07.031
pubmed: 16990141
Kruger, J. & Rehmsmeier, M. RNAhybrid: MicroRNA target prediction easy, fast and flexible. Nucleic Acids Res. 34, W451–W454. https://doi.org/10.1093/nar/gkl243 (2006).
doi: 10.1093/nar/gkl243
pubmed: 16845047
pmcid: 1538877
Yu, G., Wang, L. G., Han, Y. & He, Q. Y. clusterProfiler: An R package for comparing biological themes among gene clusters. OMICS 16, 284–287. https://doi.org/10.1089/omi.2011.0118 (2012).
doi: 10.1089/omi.2011.0118
pubmed: 22455463
pmcid: 3339379
Yu, G., Wang, L. G., Yan, G. R. & He, Q. Y. DOSE: An R/bioconductor package for disease ontology semantic and enrichment analysis. Bioinformatics 31, 608–609. https://doi.org/10.1093/bioinformatics/btu684 (2015).
doi: 10.1093/bioinformatics/btu684
pubmed: 25677125
Durinck, S., Spellman, P. T., Birney, E. & Huber, W. Mapping identifiers for the integration of genomic datasets with the R/Bioconductor package biomaRt. Nat. Protoc. 4, 1184–1191. https://doi.org/10.1038/nprot.2009.97 (2009).
doi: 10.1038/nprot.2009.97
pubmed: 19617889
pmcid: 3159387
Munz, M. et al. Qtlizer: Comprehensive QTL annotation of GWAS results. Sci. Rep. 10, 20417. https://doi.org/10.1038/s41598-020-75770-7 (2020).
doi: 10.1038/s41598-020-75770-7
pubmed: 33235230
pmcid: 7687904