Plasma extracellular vesicle miRNAs as potential biomarkers of superstimulatory response in cattle

. 2020 Nov 05 ; 10 (1) : 19130. [epub] 20201105

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33154526

Grantová podpora
13/IA/1983 Science Foundation Ireland - Ireland

Odkazy

PubMed 33154526
PubMed Central PMC7645755
DOI 10.1038/s41598-020-76152-9
PII: 10.1038/s41598-020-76152-9
Knihovny.cz E-zdroje

The ability to predict superstimulatory response would be a beneficial tool in assisted reproduction. Using small RNAseq technology, we profiled extracellular vesicle microRNA (EV-miRNA) abundance in the blood plasma of heifers exhibiting variable responses to superstimulation. Estrous synchronized crossbred beef heifers (n = 25) were superstimulated and blood samples were collected from each heifer on Day 7 of consecutive unstimulated (U) and superstimulated (S) cycles. A subset of high (H) and low (L) responders was selected depending on their response to superstimulation and EV-miRNA profiles were analysed at both time-points in each heifer. Approximately 200 known miRNAs were detected in each sample with 144 commonly detected in all samples. A total of 12 and 14 miRNAs were dysregulated in UH vs. UL and in SH vs. SL heifers, respectively. Interestingly, miR-206 and miR-6517 exhibited the same differential expression pattern in H compared to L heifers both before and after superstimulation. Pathway analysis indicated that circadian rhythm and signaling pathways were among the top pathways enriched with genes targeted by dysregulated miRNAs in H vs. L responding heifers. In conclusion, heifers with divergent ovarian responses exhibited differential expression of plasma EV-miRNAs which may be used as a potential biomarker to predict superstimulation response.

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Bó GA, Mapletoft RJ. Historical perspectives and recent research on superovulation in cattle. Theriogenology. 2014;81:38–48. doi: 10.1016/j.theriogenology.2013.09.020. PubMed DOI

Moore SG, Hasler JF. A 100-year review: reproductive technologies in dairy science. J. Dairy Sci. 2017;100:10314–10331. doi: 10.3168/jds.2017-13138. PubMed DOI

Wagner M, et al. Single-cell analysis of human ovarian cortex identifies distinct cell populations but no oogonial stem cells. Nat. Commun. 2020;11:1147. doi: 10.1038/s41467-020-14936-3. PubMed DOI PMC

Erickson BH. Development and senescence of the postnatal bovine ovary. J. Anim. Sci. 1966;25:800–805. doi: 10.2527/jas1966.253800x. PubMed DOI

Ireland JJ, et al. Does size matter in females? An overview of the impact of the high variation in the ovarian reserve on ovarian function and fertility, utility of anti-Müllerian hormone as a diagnostic marker for fertility and causes of variation in the ovarian reserve in cattle. Reprod. Fertil. Dev. 2011;23:1–14. doi: 10.1071/RD10226. PubMed DOI

Burns DS, Jimenez-Krassel F, Ireland JLH, Knight PG, Ireland JJ. Numbers of antral follicles during follicular waves in cattle: evidence for high variation among animals, very high repeatability in individuals, and an inverse association with serum follicle-stimulating hormone concentrations. Biol. Reprod. 2005;73:54–62. doi: 10.1095/biolreprod.104.036277. PubMed DOI

Monniaux D, et al. Anti-Müllerian hormone: a predictive marker of embryo production in cattle? Reprod. Fertil. Dev. 2010;22:1083. doi: 10.1071/RD09279. PubMed DOI

Rico C, et al. Determination of anti-Müllerian hormone concentrations in blood as a tool to select Holstein donor cows for embryo production: from the laboratory to the farm. Reprod. Fertil. Dev. 2012;24:932–944. doi: 10.1071/RD11290. PubMed DOI

Alward KJ, Bohlen JF. Overview of anti-Müllerian hormone (AMH) and association with fertility in female cattle. Reprod. Domest. Anim. 2020;55:3–10. doi: 10.1111/rda.13583. PubMed DOI

El-Sheikh Ali H, et al. Plasma anti-Müllerian hormone as a biomarker for bovine granulosa-theca cell tumors. Theriogenology. 2013;80:940–949. doi: 10.1016/j.theriogenology.2013.07.022. PubMed DOI

Yáñez-Mó M, et al. Biological properties of extracellular vesicles and their physiological functions. J. Extracell. Vesicles. 2015;4:1–60. doi: 10.3402/jev.v4.27066. PubMed DOI PMC

Vickers KC, Palmisano BT, Shoucri BM, Shamburek RD, Remaley AT. MicroRNAs are transported in plasma and delivered to recipient cells by high-density lipoproteins. Nat. Cell Biol. 2011;13:423–433. doi: 10.1038/ncb2210. PubMed DOI PMC

Arroyo JD, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc. Natl. Acad. Sci. 2011;108:5003–5008. doi: 10.1073/pnas.1019055108. PubMed DOI PMC

Valadi H, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007;9:654–659. doi: 10.1038/ncb1596. PubMed DOI

Sohel MMH, et al. Exosomal and non-exosomal transport of extra-cellular microRNAs in follicular fluid: implications for bovine oocyte developmental competence. PLoS ONE. 2013;8:e78505. doi: 10.1371/journal.pone.0078505. PubMed DOI PMC

Nik Mohamed Kamal NNSB, Shahidan WNS. Non-exosomal and exosomal circulatory MicroRNAs: which are more valid as biomarkers? Front. Pharmacol. 2020;10:1500. doi: 10.3389/fphar.2019.01500. PubMed DOI PMC

Tesfaye D, et al. Potential role of microRNAs in mammalian female fertility. Reprod. Fertil. Dev. 2017;29:8–23. doi: 10.1071/RD16266. PubMed DOI

Navakanitworakul R, et al. Characterization and small RNA content of extracellular vesicles in follicular fluid of developing bovine antral follicles. Sci. Rep. 2016;6:1–14. doi: 10.1038/srep25486. PubMed DOI PMC

Martinez RM, et al. Extracellular microRNAs profile in human follicular fluid and IVF outcomes. Sci. Rep. 2018;8:17036. doi: 10.1038/s41598-018-35379-3. PubMed DOI PMC

Machtinger R, et al. Mirnas isolated from extracellular vesicles in follicular fluid and oocyte development potential. Fertil. Steril. 2015;104:e54. doi: 10.1016/j.fertnstert.2015.07.162. DOI

Machtinger R, et al. Extracellular microRNAs in follicular fluid and their potential association with oocyte fertilization and embryo quality: an exploratory study. J. Assist. Reprod. Genet. 2017;34:525–533. doi: 10.1007/s10815-017-0876-8. PubMed DOI PMC

Gatien J, et al. Metabolomic profile of oviductal extracellular vesicles across the estrous cycle in cattle. Int. J. Mol. Sci. 2019;20:6339. doi: 10.3390/ijms20246339. PubMed DOI PMC

Ioannidis J, Donadeu FX. Circulating microRNA profiles during the bovine oestrous cycle. PLoS ONE. 2016;11:e0158160. doi: 10.1371/journal.pone.0158160. PubMed DOI PMC

Nakamura K, et al. Effects of miR-98 in intrauterine extracellular vesicles on maternal immune regulation during the peri-implantation period in cattle. Sci. Rep. 2019;9:20330. doi: 10.1038/s41598-019-56879-w. PubMed DOI PMC

Nakamura K, Kusama K, Ideta A, Imakawa K, Hori M. IFNT-independent effects of intrauterine extracellular vesicles (EVs) in cattle. Reproduction. 2020;159:503–511. doi: 10.1530/REP-19-0314. PubMed DOI

Noferesti SS, et al. Controlled ovarian hyperstimulation induced changes in the expression of circulatory miRNA in bovine follicular fluid and blood plasma. J. Ovarian Res. 2015;8:81. doi: 10.1186/s13048-015-0208-5. PubMed DOI PMC

Forde N, et al. Endometrial response of beef heifers on day 7 following insemination to supraphysiological concentrations of progesterone associated with superovulation. Physiol. Genomics. 2012;44:1107–1115. doi: 10.1152/physiolgenomics.00092.2012. PubMed DOI

Walker WL, Nebel RL, McGilliard ML. Time of ovulation relative to mounting activity in dairy cattle. J. Dairy Sci. 1996;79:1555–1561. doi: 10.3168/jds.S0022-0302(96)76517-7. PubMed DOI

Randi F, McDonald M, Duffy P, Kelly AK, Lonergan P. The relationship between external auditory canal temperature and onset of estrus and ovulation in beef heifers. Theriogenology. 2018;110:175–181. doi: 10.1016/j.theriogenology.2018.01.001. PubMed DOI

Shah JS, Soon PS, Marsh DJ. Comparison of methodologies to detect low levels of hemolysis in serum for accurate assessment of serum microRNAs. PLoS ONE. 2016;11:e0153200. doi: 10.1371/journal.pone.0153200. PubMed DOI PMC

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17:10. doi: 10.14806/ej.17.1.200. DOI

Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10:R25. doi: 10.1186/gb-2009-10-3-r25. PubMed DOI PMC

Robinson MD, Oshlack A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 2010;11:R25. doi: 10.1186/gb-2010-11-3-r25. PubMed DOI PMC

Wu Y, Wei B, Liu H, Li T, Rayner S. MiRPara: a SVM-based software tool for prediction of most probable microRNA coding regions in genome scale sequences. BMC Bioinform. 2011;12:107. doi: 10.1186/1471-2105-12-107. PubMed DOI PMC

Agarwal V, Bell GW, Nam J-W, Bartel DP. Predicting effective microRNA target sites in mammalian mRNAs. Elife. 2015;4:e05005. doi: 10.7554/eLife.05005. PubMed DOI PMC

Ogata H, et al. KEGG: kyoto encyclopedia of genes and genomes. Nucl. Acids Res. 1999;27:29–34. doi: 10.1093/nar/27.1.29. PubMed DOI PMC

Shannon P. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–2504. doi: 10.1101/gr.1239303. PubMed DOI PMC

Bindea G, et al. ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics. 2009;25:1091–1093. doi: 10.1093/bioinformatics/btp101. PubMed DOI PMC

Chou C-H, et al. miRTarBase update 2018: a resource for experimentally validated microRNA-target interactions. Nucl. Acids Res. 2018;46:D296–D302. doi: 10.1093/nar/gkx1067. PubMed DOI PMC

Ioannidis J, Donadeu FX. Comprehensive analysis of blood cells and plasma identifies tissue-specific miRNAs as potential novel circulating biomarkers in cattle. BMC Genom. 2018;19:243. doi: 10.1186/s12864-018-4646-5. PubMed DOI PMC

Tsang EK, et al. Small RNA sequencing in cells and exosomes identifies eQTLs and 14q32 as a region of active export. G3 (Bethesda) 2017;7:31–39. doi: 10.1534/g3.116.036137. PubMed DOI PMC

Buschmann D, et al. Evaluation of serum extracellular vesicle isolation methods for profiling miRNAs by next-generation sequencing. J. Extracell. Vesicles. 2018;7:1481321. doi: 10.1080/20013078.2018.1481321. PubMed DOI PMC

Danielson KM, Rubio R, Abderazzaq F, Das S, Wang YE. High throughput sequencing of extracellular RNA from human plasma. PLoS ONE. 2017;12:e0164644. doi: 10.1371/journal.pone.0164644. PubMed DOI PMC

Nuzziello N, et al. Molecular characterization of peripheral extracellular vesicles in clinically isolated syndrome: preliminary suggestions from a pilot study. Med. Sci. 2017;5:19. PubMed PMC

Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J. Extracell. Vesicles. 2013;2:20389. doi: 10.3402/jev.v2i0.20389. PubMed DOI PMC

Mathieu M, Martin-Jaular L, Lavieu G, Théry C. Specificities of secretion and uptake of exosomes and other extracellular vesicles for cell-to-cell communication. Nat. Cell Biol. 2019;21:9–17. doi: 10.1038/s41556-018-0250-9. PubMed DOI

Hailay T, et al. Extracellular vesicle-coupled miRNA profiles in follicular fluid of cows with divergent post-calving metabolic status. Sci. Rep. 2019;9:12851. doi: 10.1038/s41598-019-49029-9. PubMed DOI PMC

Martinez RM, et al. Body mass index in relation to extracellular vesicle–linked microRNAs in human follicular fluid. Fertil. Steril. 2019;112:387–396.e3. doi: 10.1016/j.fertnstert.2019.04.001. PubMed DOI PMC

Borges Júnior E, et al. Serum microRNA profiling for the identification of predictive molecular markers of the response to controlled ovarian stimulation. JBRA Assist. Reprod. 2019 doi: 10.5935/1518-0557.20190070. PubMed DOI PMC

Adams BD, Furneaux H, White BA. The micro-ribonucleic acid (miRNA) miR-206 targets the human estrogen receptor-α (ERα) and represses ERα messenger RNA and protein expression in breast cancer cell lines. Mol. Endocrinol. 2007;21:1132–1147. doi: 10.1210/me.2007-0022. PubMed DOI

Hewitt S, Korach K. Oestrogen receptor knockout mice: roles for oestrogen receptors alpha and beta in reproductive tissues. Reproduction. 2003;125:143–149. doi: 10.1530/rep.0.1250143. PubMed DOI

Dupont S, et al. Effect of single and compound knockouts of estrogen receptors α (ERα) and β (ERβ) on mouse reproductive phenotypes. Development. 2000;127:4277–4291. PubMed

Sinkevicius KW, et al. Characterization of the ovarian and reproductive abnormalities in prepubertal and adult estrogen non-responsive estrogen receptor α knock-in (ENERKI) mice. Steroids. 2009;74:913–919. doi: 10.1016/j.steroids.2009.06.012. PubMed DOI PMC

Zou X, et al. Comprehensive analysis of mRNAs and miRNAs in the ovarian follicles of uniparous and multiple goats at estrus phase. BMC Genom. 2020;21:267. doi: 10.1186/s12864-020-6671-4. PubMed DOI PMC

Lv H, Sun Y, Zhang Y. MiR-133 is involved in estrogen deficiency-induced osteoporosis through modulating osteogenic differentiation of mesenchymal stem cells. Med. Sci. Monit. 2015;21:1527–1534. doi: 10.12659/MSM.894323. PubMed DOI PMC

Dai A, et al. MicroRNA-133b stimulates ovarian estradiol synthesis by targeting Foxl2. FEBS Lett. 2013;587:2474–2482. doi: 10.1016/j.febslet.2013.06.023. PubMed DOI

Matsuzaka Y, et al. Characterization and functional analysis of extracellular vesicles and muscle-abundant miRNAs (miR-1, miR-133a, and miR-206) in C2C12 myocytes and mdx mice. PLoS ONE. 2016;11:e0167811. doi: 10.1371/journal.pone.0167811. PubMed DOI PMC

Mizuno H, et al. Identification of muscle-specific micrornas in serum of muscular dystrophy animal models: promising novel blood-based markers for muscular dystrophy. PLoS ONE. 2011;6:e18388. doi: 10.1371/journal.pone.0018388. PubMed DOI PMC

Matsuzaka Y, et al. Three novel serum biomarkers, miR-1, miR-133a, and miR-206 for Limb-girdle muscular dystrophy, facioscapulohumeral muscular dystrophy, and Becker muscular dystrophy. Environ. Health Prev. Med. 2014;19:452–458. doi: 10.1007/s12199-014-0405-7. PubMed DOI PMC

Sahu B, et al. Response to controlled ovarian stimulation and oocyte quality in women with myotonic dystrophy type I. J. Assist. Reprod. Genet. 2008;25:1–5. doi: 10.1007/s10815-007-9193-y. PubMed DOI PMC

Feyereisen E, et al. Myotonic dystrophy: does it affect ovarian follicular status and responsiveness to controlled ovarian stimulation? Hum. Reprod. 2006;21:175–182. doi: 10.1093/humrep/dei310. PubMed DOI

Zhang Q, et al. MicroRNA-181a suppresses mouse granulosa cell proliferation by targeting activin receptor IIA. PLoS ONE. 2013;8:e59667. doi: 10.1371/journal.pone.0059667. PubMed DOI PMC

Salilew-Wondim D, et al. The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle. PLoS ONE. 2014;9:e106795. doi: 10.1371/journal.pone.0106795. PubMed DOI PMC

Donadeu FX, Schauer SN, Sontakke SD. Involvement of miRNAs in ovarian follicular and luteal development. J. Endocrinol. 2012;215:323–334. doi: 10.1530/JOE-12-0252. PubMed DOI

Huang J, et al. Solexa sequencing of novel and differentially expressed microRNAs in testicular and ovarian tissues in Holstein Cattle. Int. J. Biol. Sci. 2011;7:1016–1026. doi: 10.7150/ijbs.7.1016. PubMed DOI PMC

Miles JR, et al. MicroRNA expression profile in bovine cumulus-oocyte complexes: Possible role of let-7 and miR-106a in the development of bovine oocytes. Anim. Reprod. Sci. 2012;130:16–26. doi: 10.1016/j.anireprosci.2011.12.021. PubMed DOI

Hossain M, et al. Identification and characterization of miRNAs expressed in the bovine ovary. BMC Genom. 2009;10:443. doi: 10.1186/1471-2164-10-443. PubMed DOI PMC

Gecaj RM, et al. The dynamics of microRNA transcriptome in bovine corpus luteum during its formation, function, and regression. Front. Genet. 2017;8:213. doi: 10.3389/fgene.2017.00213. PubMed DOI PMC

Santos PH, et al. Effect of superstimulation on the expression of microRNAs and genes involved in steroidogenesis and ovulation in Nelore cows. Theriogenology. 2018;110:192–200. doi: 10.1016/j.theriogenology.2017.12.045. PubMed DOI

Xie S, Batnasan E, Zhang Q, Li Y. MicroRNA expression is altered in granulosa cells of ovarian hyperresponders. Reprod. Sci. 2016;23:1001–1010. doi: 10.1177/1933719115625849. PubMed DOI

McBride D, et al. Identification of miRNAs associated with the follicular–luteal transition in the ruminant ovary. Reproduction. 2012;144:221–233. doi: 10.1530/REP-12-0025. PubMed DOI

Donadeu FX, et al. Relationships between size, steroidogenesis and miRNA expression of the bovine corpus luteum. Theriogenology. 2020;145:226–230. doi: 10.1016/j.theriogenology.2019.10.033. PubMed DOI

Toloubeydokhti T, et al. The expression of microRNA (miRNA), mir-17, mir-211 and mir-542 and their target genes, StAR, IL-1b and Cox2 in follicular cells derived from women undergoing ART. Fertil. Steril. 2007;88:S165–S166. doi: 10.1016/j.fertnstert.2007.07.576. DOI

de Ávila ACFCM, et al. Estrous cycle impacts microRNA content in extracellular vesicles that modulate bovine cumulus cell transcripts during in vitro maturation†. Biol. Reprod. 2020;102:362–375. doi: 10.1093/biolre/ioz177. PubMed DOI

Prasasya RD, Mayo KE. Regulation of Follicle Formation and Development by Ovarian Signaling Pathways. In: Leung PCK, Adashi EY, editors. The Ovary. Amsterdam: Elsevier; 2019. pp. 23–49.

Kawamura K, et al. Hippo signaling disruption and Akt stimulation of ovarian follicles for infertility treatment. Proc. Natl. Acad. Sci. USA. 2013;110:17474–17479. doi: 10.1073/pnas.1312830110. PubMed DOI PMC

Grosbois J, Demeestere I. Dynamics of PI3K and Hippo signaling pathways during in vitro human follicle activation. Hum. Reprod. 2018;33:1705–1714. doi: 10.1093/humrep/dey250. PubMed DOI

Zhang B, et al. MicroRNA mediating networks in granulosa cells associated with ovarian follicular development. Biomed Res. Int. 2017;2017:1–18. PubMed PMC

Santonocito M, et al. Molecular characterization of exosomes and their microRNA cargo in human follicular fluid: bioinformatic analysis reveals that exosomal microRNAs control pathways involved in follicular maturation. Fertil. Steril. 2014;102:1751–1761.e1. doi: 10.1016/j.fertnstert.2014.08.005. PubMed DOI

Sellix MT. Circadian clock function in the mammalian ovary. J. Biol. Rhythms. 2015;30:7–19. doi: 10.1177/0748730414554222. PubMed DOI

Shimizu T, et al. Expressions of the circadian genes Per2, Bmal1, Clock and Cry1 during the different stages of follicular development and their regulation by FSH in bovine granulosa cells from small follicles. Livest. Sci. 2012;145:292–297. doi: 10.1016/j.livsci.2012.01.012. DOI

Gräs S, Georg B, Jørgensen HL, Fahrenkrug J. Expression of the clock genes Per1 and Bmal1 during follicle development in the rat ovary. Effects of gonadotropin stimulation and hypophysectomy. Cell Tissue Res. 2012;350:539–548. doi: 10.1007/s00441-012-1489-2. PubMed DOI

Kojima S, Shingle DL, Green CB. Post-transcriptional control of circadian rhythms. J. Cell Sci. 2011;124:311–320. doi: 10.1242/jcs.065771. PubMed DOI PMC

Tao SC, Guo SC. Extracellular vesicles: potential participants in circadian rhythm synchronization. Int. J. Biol. Sci. 2018;14:1610–1620. doi: 10.7150/ijbs.26518. PubMed DOI PMC

Zhou W, Li Y, Wang X, Wu L, Wang Y. MiR-206-mediated dynamic mechanism of the mammalian circadian clock. BMC Syst. Biol. 2011;5:141. doi: 10.1186/1752-0509-5-141. PubMed DOI PMC

Knarr M, Nagaraj AB, Kwiatkowski LJ, DiFeo A. miR-181a modulates circadian rhythm in immortalized bone marrow and adipose derived stromal cells and promotes differentiation through the regulation of PER3. Sci. Rep. 2019;9:1–13. doi: 10.1038/s41598-018-36425-w. PubMed DOI PMC

Gao Q, Zhou L, Yang SY, Cao JM. A novel role of microRNA 17–5p in the modulation of circadian rhythm. Sci. Rep. 2016;6:1–12. doi: 10.1038/s41598-016-0001-8. PubMed DOI PMC

R Core Team . R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing; 2019.

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