FREE SHIPPING over $40
OVER 9000 FIVE-STAR REVIEWS
5% OFF ALL SUBSCRIPTIONS
100% HAPPINESS GUARANTEE
Analyze Diet
0
Home / Equine Research Bank / Genes (Basel) / Non-Coding RNA Sequencing of Equine Endometrium During Mater...
Genes2019; 10(10); 821; doi: 10.3390/genes10100821

Non-Coding RNA Sequencing of Equine Endometrium During Maternal Recognition of Pregnancy.

Abstract: Maternal recognition of pregnancy (MRP) in the mare is not well defined. In a non-pregnant mare, prostaglandin F (PGF) is released on day 14 post-ovulation (PO) to cause luteal regression, resulting in loss of progesterone production. Equine MRP occurs prior to day 14 to halt PGF production. Studies have failed to identify a gene candidate for MRP, so attention has turned to small, non-coding RNAs. The objective of this study was to evaluate small RNA (<200 nucleotides) content in endometrium during MRP. Mares were used in a cross-over design with each having a pregnant and non-mated cycle. Each mare was randomly assigned to collection day 11 or 13 PO ( = 3/day) and endometrial biopsies were obtained. Total RNA was isolated and sequencing libraries were prepared using a small RNA library preparation kit and sequenced on a HiSeq 2000. EquCab3 was used as the reference genome and DESeq2 was used for statistical analysis. On day 11, 419 ncRNAs, representing miRNA, snRNA, snoRNA, scaRNA, and vaultRNA, were different between pregnancy statuses, but none on day 13. Equine endometrial ncRNAs with unknown structure and function were also identified. This study is the first to describe ncRNA transcriptome in equine endometrium. Identifying targets of these ncRNAs could lead to determining MRP.
Get Full Text
Publication Date: 2019-10-18 PubMed ID: 31635328PubMed Central: PMC6826835DOI: 10.3390/genes10100821Google 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
  • Research Support
  • Non-U.S. Gov't

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 article involves a study about maternal recognition of pregnancy (MRP) in mares, using non-coding RNAs to possibly determine pregnancy status.

Concept of Maternal Recognition of Pregnancy

  • The paper begins by explaining the concept of MRP in mares, which is yet to be fully understood. In a situation where the mare is not pregnant, prostaglandin F (PGF) is released on the 14th day following ovulation, triggering a process called luteal regression that results in ending the production of progesterone. For pregnant mares, MRP occurs before the 14th day to stop PGF production.
  • Previous studies could not identify a specific gene responsible for MRP, thus the focus of this research shifts to smaller, non-coding RNAs (ncRNAs).

Objectives and Methodology of the Study

  • The primary objective of this investigation was to assess the content of small RNA (<200 nucleotides) in the endometrium during MRP.
  • The researchers used a cross-over design, entailing both pregnant and non-mated cycles for each mare. The mares were randomized to belong to either day 11 or day 13 post-ovulation groups for endometrial biopsy collection.
  • A small RNA library preparation kit was utilized to prepare sequencing libraries from the total RNA, which were then sequenced on a HiSeq 2000.
  • The reference genome used in the research was EquCab3, with DESeq2 employed for statistical analysis.

Findings and Conclusion

  • On day 11, the researchers identified 419 ncRNAs, which represented a variety of RNA types such as miRNA, snRNA, snoRNA, scaRNA, and vaultRNA. These RNAs presented differing between pregnant and non-pregnant mares, while on day 13 there was no difference.
  • The researchers also detected equine endometrial ncRNAs with unidentified structures and functions.
  • As a first of its kind, the study described the ncRNA transcriptome within the equine endometrium.
  • The research points towards potential avenues for future studies, as identifying targets of these ncRNAs may provide valuable insights into MRP determination.

Cite This Article

APA
Klohonatz KM, Coleman SJ, Cameron AD, Hess AM, Reed KJ, Canovas A, Medrano JF, Islas-Trejo AD, Kalbfleisch T, Bouma GJ, Bruemmer JE. (2019). Non-Coding RNA Sequencing of Equine Endometrium During Maternal Recognition of Pregnancy. Genes (Basel), 10(10), 821. https://doi.org/10.3390/genes10100821

Publication

Genes
ISSN: 2073-4425
NlmUniqueID: 101551097
Country: Switzerland
Language: English
Volume: 10
Issue: 10
PII: 821

Researcher Affiliations

Klohonatz, Kristin M
  • Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523, USA. kmk5057@gmail.com.
Coleman, Stephen J
  • Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523, USA. stephen.coleman@colostate.edu.
Cameron, Ashley D
  • Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523, USA. adcamero@gmail.com.
Hess, Ann M
  • Department of Statistics and Bioinformatics, Colorado State University, Fort Collins, CO 80523, USA. ann.hess@colostate.edu.
Reed, Kailee J
  • Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523, USA. kailee.reed@colostate.edu.
Canovas, Angela
  • Department of Animal Science, University of California Davis, Davis, CA 95616, USA. acanovas@uoguelph.ca.
Medrano, Juan F
  • Department of Animal Science, University of California Davis, Davis, CA 95616, USA. jfmedrano@ucdavis.edu.
Islas-Trejo, Alma D
  • Department of Animal Science, University of California Davis, Davis, CA 95616, USA. adislas@ucdavis.edu.
Kalbfleisch, Ted
  • Department of Veterinary Science, Gluck Equine Research Center, University of Kentucky, Lexington, KY 40503, USA. ted.kalbfleisch@uky.edu.
Bouma, Gerrit J
  • Department of Biomedical Sciences, Animal Reproduction and Biotechnology Laboratory, Colorado State University, Fort Collins, CO 80523, USA. gerrit.bouma@colostate.edu.
Bruemmer, Jason E
  • Department of Animal Sciences, Colorado State University, Fort Collins, CO 80523, USA. jason.bruemmer@colostate.edu.
  • Department of Animal Sciences, 259 Animal Sciences, 1171 Campus Delivery Colorado State University, Fort Collins, CO 80523, USA. jason.bruemmer@colostate.edu.

MeSH Terms

  • Animals
  • Endometrium / metabolism
  • Female
  • Horses / genetics
  • Horses / metabolism
  • Horses / physiology
  • Pregnancy
  • Pregnancy, Animal / genetics
  • Pregnancy, Animal / metabolism
  • Pregnancy, Animal / physiology
  • RNA, Untranslated / genetics
  • RNA, Untranslated / metabolism
  • Transcriptome

Conflict of Interest Statement

The authors declare no conflict of interest.

References

This article includes 55 references
  1. McCracken JA, Custer EE, Lamsa JC. Luteolysis: a neuroendocrine-mediated event.. Physiol Rev 1999 Apr;79(2):263-323.
    doi: 10.1152/physrev.1999.79.2.263pubmed: 10221982google scholar: lookup
  2. Sharp DC, Thatcher MJ, Salute ME, Fuchs AR. 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 1997 Jan;109(1):137-44.
    doi: 10.1530/jrf.0.1090137pubmed: 9068425google scholar: lookup
  3. Rambags BP, Krijtenburg PJ, Drie HF, Lazzari G, Galli C, Pearson PL, Colenbrander B, Stout TA. Numerical chromosomal abnormalities in equine embryos produced in vivo and in vitro.. Mol Reprod Dev 2005 Sep;72(1):77-87.
    doi: 10.1002/mrd.20302pubmed: 15948165google scholar: lookup
  4. Allen WR, Stewart F. Equine placentation.. Reprod Fertil Dev 2001;13(7-8):623-34.
    doi: 10.1071/RD01063pubmed: 11999314google scholar: lookup
  5. Betteridge KJ, Eaglesome MD, Mitchell D, Flood PF, Beriault R. Development of horse embryos up to twenty two days after ovulation: observations on fresh specimens.. J Anat 1982 Aug;135(Pt 1):191-209.
    pmc: PMC1168142pubmed: 7130052
  6. Denker HW. Structural dynamics and function of early embryonic coats.. Cells Tissues Organs 2000;166(2):180-207.
    doi: 10.1159/000016732pubmed: 10729727google scholar: lookup
  7. Ginther OJ. Mobility of the early equine conceptus.. Theriogenology 1983 Apr;19(4):603-11.
    doi: 10.1016/0093-691X(83)90180-2pubmed: 16725808google scholar: lookup
  8. McDowell KJ, Sharp DC, Grubaugh W, Thatcher WW, Wilcox CJ. Restricted conceptus mobility results in failure of pregnancy maintenance in mares.. Biol Reprod 1988 Sep;39(2):340-8.
    doi: 10.1095/biolreprod39.2.340pubmed: 3179385google scholar: lookup
  9. Ginther OJ. Internal regulation of physiological processes through local venoarterial pathways: a review.. J Anim Sci 1974 Sep;39(3):550-64.
    doi: 10.2527/jas1974.393550xpubmed: 4213194google scholar: lookup
  10. Leith GS, Ginther OJ. Characterization of intrauterine mobility of the early equine conceptus.. Theriogenology 1984 Oct;22(4):401-8.
    doi: 10.1016/0093-691X(84)90460-6pubmed: 16725972google scholar: lookup
  11. Klohonatz KM, Nulton LC, Hess AM, Bouma GJ, Bruemmer JE. The role of embryo contact and focal adhesions during maternal recognition of pregnancy.. PLoS One 2019;14(3):e0213322.
    doi: 10.1371/journal.pone.0213322pmc: PMC6400379pubmed: 30835748google scholar: lookup
  12. Klohonatz KM, Coleman SJ, Islas-Trejo AD, Medrano JF, Hess AM, Kalbfleisch T, Thomas MG, Bouma GJ, Bruemmer JE. Coding RNA Sequencing of Equine Endometrium during Maternal Recognition of Pregnancy.. Genes (Basel) 2019 Sep 25;10(10).
    doi: 10.3390/genes10100749pmc: PMC6826732pubmed: 31557877google scholar: lookup
  13. Stout TA, Allen WR. Role of prostaglandins in intrauterine migration of the equine conceptus.. Reproduction 2001 May;121(5):771-5.
    doi: 10.1530/rep.0.1210771pubmed: 11427165google scholar: lookup
  14. Baker CB, Adams MH, McDowell KJ. Lack of expression of alpha or omega interferons by the horse conceptus.. J Reprod Fertil Suppl 1991;44:439-43.
    pubmed: 1724463
  15. Bazer FW, Thatcher WW. Theory of maternal recognition of pregnancy in swine based on estrogen controlled endocrine versus exocrine secretion of prostaglandin F2alpha by the uterine endometrium.. Prostaglandins 1977 Aug;14(2):397-400.
    doi: 10.1016/0090-6980(77)90185-Xpubmed: 897228google scholar: lookup
  16. Klein C, Scoggin KE, Ealy AD, Troedsson MH. Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.. Biol Reprod 2010 Jul;83(1):102-13.
    doi: 10.1095/biolreprod.109.081612pubmed: 20335638google scholar: lookup
  17. Klohonatz KM, Hess AM, Hansen TR, Squires EL, Bouma GJ, Bruemmer JE. Equine endometrial gene expression changes during and after maternal recognition of pregnancy.. J Anim Sci 2015 Jul;93(7):3364-76.
    doi: 10.2527/jas.2014-8826pubmed: 26440005google scholar: lookup
  18. Tachibana Y, Nakano Y, Nagaoka K, Kikuchi M, Nambo Y, Haneda S, Matsui M, Miyake Y, Imakawa K. Expression of endometrial immune-related genes possibly functioning during early pregnancy in the mare.. J Reprod Dev 2013;59(1):85-91.
    doi: 10.1262/jrd.2012-142pmc: PMC3943239pubmed: 23138119google scholar: lookup
  19. Klohonatz KM, Cameron AD, Hergenreder JR, da Silveira JC, Belk AD, Veeramachaneni DN, Bouma GJ, Bruemmer JE. Circulating miRNAs as Potential Alternative Cell Signaling Associated with Maternal Recognition of Pregnancy in the Mare.. Biol Reprod 2016 Dec;95(6):124.
    doi: 10.1095/biolreprod.116.142935pubmed: 27760749google scholar: lookup
  20. He L, Hannon GJ. MicroRNAs: small RNAs with a big role in gene regulation.. Nat Rev Genet 2004 Jul;5(7):522-31.
    doi: 10.1038/nrg1379pubmed: 15211354google scholar: lookup
  21. Kenney RM. Cyclic and pathologic changes of the mare endometrium as detected by biopsy, with a note on early embryonic death.. J Am Vet Med Assoc 1978 Feb 1;172(3):241-62.
    pubmed: 621166
  22. Afgan E, Baker D, Batut B, van den Beek M, Bouvier D, Cech M, Chilton J, Clements D, Coraor N, Grüning BA, Guerler A, Hillman-Jackson J, Hiltemann S, Jalili V, Rasche H, Soranzo N, Goecks J, Taylor J, Nekrutenko A, Blankenberg D. The Galaxy platform for accessible, reproducible and collaborative biomedical analyses: 2018 update.. Nucleic Acids Res 2018 Jul 2;46(W1):W537-W544.
    doi: 10.1093/nar/gky379pmc: PMC6030816pubmed: 29790989google scholar: lookup
  23. Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. Babraham Bioinformatics; Cambrige, UK: 2010.
  24. Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report.. Bioinformatics 2016 Oct 1;32(19):3047-8.
    doi: 10.1093/bioinformatics/btw354pmc: PMC5039924pubmed: 27312411google scholar: lookup
  25. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data.. Bioinformatics 2014 Aug 1;30(15):2114-20.
    doi: 10.1093/bioinformatics/btu170pmc: PMC4103590pubmed: 24695404google scholar: lookup
  26. Kalbfleisch TS, Rice ES, DePriest MS Jr, Walenz BP, Hestand MS, Vermeesch JR, O Connell BL, Fiddes IT, Vershinina AO, Saremi NF, Petersen JL, Finno CJ, Bellone RR, McCue ME, Brooks SA, Bailey E, Orlando L, Green RE, Miller DC, Antczak DF, MacLeod JN. Improved reference genome for the domestic horse increases assembly contiguity and composition.. Commun Biol 2018;1:197.
    doi: 10.1038/s42003-018-0199-zpmc: PMC6240028pubmed: 30456315google scholar: lookup
  27. Patro R, Duggal G, Love MI, Irizarry RA, Kingsford C. Salmon provides accurate, fast, and bias-aware transcript expression estimates using dual-phase inference. bioRxiv 2016:021592.
    doi: 10.1101/021592google scholar: lookup
  28. Hunt SE, McLaren W, Gil L, Thormann A, Schuilenburg H, Sheppard D, Parton A, Armean IM, Trevanion SJ, Flicek P, Cunningham F. Ensembl variation resources.. Database (Oxford) 2018 Jan 1;2018.
    doi: 10.1093/database/bay119pmc: PMC6310513pubmed: 30576484google scholar: lookup
  29. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2.. Genome Biol 2014;15(12):550.
    doi: 10.1186/s13059-014-0550-8pmc: PMC4302049pubmed: 25516281google scholar: lookup
  30. Catalanotto C, Cogoni C, Zardo G. MicroRNA in Control of Gene Expression: An Overview of Nuclear Functions.. Int J Mol Sci 2016 Oct 13;17(10).
    doi: 10.3390/ijms17101712pmc: PMC5085744pubmed: 27754357google scholar: lookup
  31. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals.. Nat Rev Mol Cell Biol 2009 Feb;10(2):126-39.
    doi: 10.1038/nrm2632pubmed: 19165215google scholar: lookup
  32. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH, Kim VN. MicroRNA genes are transcribed by RNA polymerase II.. EMBO J 2004 Oct 13;23(20):4051-60.
    doi: 10.1038/sj.emboj.7600385pmc: PMC524334pubmed: 15372072google scholar: lookup
  33. Kim YK, Kim VN. Processing of intronic microRNAs.. EMBO J 2007 Feb 7;26(3):775-83.
    doi: 10.1038/sj.emboj.7601512pmc: PMC1794378pubmed: 17255951google scholar: lookup
  34. Meister G, Landthaler M, Patkaniowska A, Dorsett Y, Teng G, Tuschl T. Human Argonaute2 mediates RNA cleavage targeted by miRNAs and siRNAs.. Mol Cell 2004 Jul 23;15(2):185-97.
    doi: 10.1016/j.molcel.2004.07.007pubmed: 15260970google scholar: lookup
  35. Chendrimada TP, Finn KJ, Ji X, Baillat D, Gregory RI, Liebhaber SA, Pasquinelli AE, Shiekhattar R. MicroRNA silencing through RISC recruitment of eIF6.. Nature 2007 Jun 14;447(7146):823-8.
    doi: 10.1038/nature05841pubmed: 17507929google scholar: lookup
  36. Lange-Consiglio A, Lazzari B, Pizzi F, Stella A, Girani A, Quintè A, Cremonesi F, Capra E. Different Culture Times Affect MicroRNA Cargo in Equine Amniotic Mesenchymal Cells and Their Microvesicles.. Tissue Eng Part C Methods 2018 Oct;24(10):596-604.
    doi: 10.1089/ten.tec.2018.0205pubmed: 30234462google scholar: lookup
  37. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends.. J Cell Biol 2013 Feb 18;200(4):373-83.
    doi: 10.1083/jcb.201211138pmc: PMC3575529pubmed: 23420871google scholar: lookup
  38. Yáñez-Mó M, Siljander PR, Andreu Z, Zavec AB, Borràs FE, Buzas EI, Buzas K, Casal E, Cappello F, Carvalho J, Colás E, Cordeiro-da Silva A, Fais S, Falcon-Perez JM, Ghobrial IM, Giebel B, Gimona M, Graner M, Gursel I, Gursel M, Heegaard NH, Hendrix A, Kierulf P, Kokubun K, Kosanovic M, Kralj-Iglic V, Krämer-Albers EM, Laitinen S, Lässer C, Lener T, Ligeti E, Linē A, Lipps G, Llorente A, Lötvall J, Manček-Keber M, Marcilla A, Mittelbrunn M, Nazarenko I, Nolte-'t Hoen EN, Nyman TA, O'Driscoll L, Olivan M, Oliveira C, Pállinger É, Del Portillo HA, Reventós J, Rigau M, Rohde E, Sammar M, Sánchez-Madrid F, Santarém N, Schallmoser K, Ostenfeld MS, Stoorvogel W, Stukelj R, Van der Grein SG, Vasconcelos MH, Wauben MH, De Wever O. Biological properties of extracellular vesicles and their physiological functions.. J Extracell Vesicles 2015;4:27066.
    doi: 10.3402/jev.v4.27066pmc: PMC4433489pubmed: 25979354google scholar: lookup
  39. Twenter HM, Belk AD, Klohonatz KM, Bass LD, Bouma GJ, Bruemmer JE. An investigation into miRNAs in the equine epididymis as potential regulators of spermatozoal maturation. J. Equine Vet. Sci. 2017;48:61–68.
    doi: 10.1016/j.jevs.2016.07.023google scholar: lookup
  40. Navakanitworakul R, Hung WT, Gunewardena S, Davis JS, Chotigeat W, Christenson LK. Characterization and Small RNA Content of Extracellular Vesicles in Follicular Fluid of Developing Bovine Antral Follicles.. Sci Rep 2016 May 9;6:25486.
    doi: 10.1038/srep25486pmc: PMC4860563pubmed: 27158133google scholar: lookup
  41. Stark GR, Darnell JE Jr. The JAK-STAT pathway at twenty.. Immunity 2012 Apr 20;36(4):503-14.
    doi: 10.1016/j.immuni.2012.03.013pmc: PMC3909993pubmed: 22520844google scholar: lookup
  42. O'Shea JJ, Plenge R. JAK and STAT signaling molecules in immunoregulation and immune-mediated disease.. Immunity 2012 Apr 20;36(4):542-50.
    doi: 10.1016/j.immuni.2012.03.014pmc: PMC3499974pubmed: 22520847google scholar: lookup
  43. Croker BA, Kiu H, Nicholson SE. SOCS regulation of the JAK/STAT signalling pathway.. Semin Cell Dev Biol 2008 Aug;19(4):414-22.
    doi: 10.1016/j.semcdb.2008.07.010pmc: PMC2597703pubmed: 18708154google scholar: lookup
  44. Rawlings JS, Rosler KM, Harrison DA. The JAK/STAT signaling pathway.. J Cell Sci 2004 Mar 15;117(Pt 8):1281-3.
    doi: 10.1242/jcs.00963pubmed: 15020666google scholar: lookup
  45. da Silveira JC, Veeramachaneni DN, Winger QA, Carnevale EM, Bouma GJ. Cell-secreted vesicles in equine ovarian follicular fluid contain miRNAs and proteins: a possible new form of cell communication within the ovarian follicle.. Biol Reprod 2012 Mar;86(3):71.
    doi: 10.1095/biolreprod.111.093252pubmed: 22116803google scholar: lookup
  46. Vlachos IS, Zagganas K, Paraskevopoulou MD, Georgakilas G, Karagkouni D, Vergoulis T, Dalamagas T, Hatzigeorgiou AG. DIANA-miRPath v3.0: deciphering microRNA function with experimental support.. Nucleic Acids Res 2015 Jul 1;43(W1):W460-6.
    doi: 10.1093/nar/gkv403pmc: PMC4489228pubmed: 25977294google scholar: lookup
  47. Matera AG, Terns RM, Terns MP. Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs.. Nat Rev Mol Cell Biol 2007 Mar;8(3):209-20.
    doi: 10.1038/nrm2124pubmed: 17318225google scholar: lookup
  48. Delpu Y, Larrieu D, Gayral M, Arvanitis D, Dufresne M, Cordelier P, Torrisani J. Drug Discovery in Cancer Epigenetics. Elsevier; Amsterdam, The Netherlands: 2016. Noncoding RNAs: Clinical and therapeutic applications; pp. 305–326.
  49. Weinberg Z, Ruzzo WL. Faster genome annotation of non-coding RNA families without loss of accuracy. In Proceedings of The Eighth Annual International Conference on Resaerch in Computational Molecular Biology; San Diego, CA, USA. 27–31 March 2004; pp. 243–251.
  50. Newman AJ. The role of U5 snRNP in pre-mRNA splicing.. EMBO J 1997 Oct 1;16(19):5797-800.
    doi: 10.1093/emboj/16.19.5797pmc: PMC1170210pubmed: 9312037google scholar: lookup
  51. Kandels-Lewis S, Séraphin B. Involvement of U6 snRNA in 5' splice site selection.. Science 1993 Dec 24;262(5142):2035-9.
    doi: 10.1126/science.8266100pubmed: 8266100google scholar: lookup
  52. Kaida D, Berg MG, Younis I, Kasim M, Singh LN, Wan L, Dreyfuss G. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation.. Nature 2010 Dec 2;468(7324):664-8.
    doi: 10.1038/nature09479pmc: PMC2996489pubmed: 20881964google scholar: lookup
  53. Cuthbert JM, Russell SJ, White KL, Benninghoff AD. The maternal-to-zygotic transition in bovine in vitro-fertilized embryos is associated with marked changes in small non-coding RNAs†.. Biol Reprod 2019 Feb 1;100(2):331-350.
    doi: 10.1093/biolre/ioy190pubmed: 30165428google scholar: lookup
  54. Scott MS, Ono M. From snoRNA to miRNA: Dual function regulatory non-coding RNAs.. Biochimie 2011 Nov;93(11):1987-92.
    doi: 10.1016/j.biochi.2011.05.026pmc: PMC3476530pubmed: 21664409google scholar: lookup
  55. Deryusheva S, Gall JG. scaRNAs and snoRNAs: Are they limited to specific classes of substrate RNAs?. RNA 2019 Jan;25(1):17-22.
    doi: 10.1261/rna.068593.118pmc: PMC6298559pubmed: 30301832google scholar: lookup

Citations

This article has been cited 6 times.
  1. Luna-Ramirez RI, Limesand SW, Goyal R, Pendleton AL, Rincón G, Zeng X, Luna-Nevárez G, Reyna-Granados JR, Luna-Nevárez P. Blood Transcriptomic Analyses Reveal Functional Pathways Associated with Thermotolerance in Pregnant Ewes Exposed to Environmental Heat Stress.. Genes (Basel) 2023 Aug 6;14(8).
    doi: 10.3390/genes14081590pubmed: 37628641google scholar: lookup
  2. Vegas AR, Podico G, Canisso IF, Bollwein H, Fröhlich T, Bauersachs S, Almiñana C. Dynamic regulation of the transcriptome and proteome of the equine embryo during maternal recognition of pregnancy.. FASEB Bioadv 2022 Dec;4(12):775-797.
    doi: 10.1096/fba.2022-00063pubmed: 36479207google scholar: lookup
  3. Rudolf Vegas A, Hamdi M, Podico G, Bollwein H, Fröhlich T, Canisso IF, Bauersachs S, Almiñana C. Uterine extracellular vesicles as multi-signal messengers during maternal recognition of pregnancy in the mare.. Sci Rep 2022 Sep 16;12(1):15616.
    doi: 10.1038/s41598-022-19958-zpubmed: 36114358google scholar: lookup
  4. Werry N, Russell SJ, Gillis DJ, Miller S, Hickey K, Larmer S, Lohuis M, Librach C, LaMarre J. Characteristics of miRNAs Present in Bovine Sperm and Associations With Differences in Fertility.. Front Endocrinol (Lausanne) 2022;13:874371.
    doi: 10.3389/fendo.2022.874371pubmed: 35663333google scholar: lookup
  5. Rudolf Vegas A, Podico G, Canisso IF, Bollwein H, Almiñana C, Bauersachs S. Spatiotemporal endometrial transcriptome analysis revealed the luminal epithelium as key player during initial maternal recognition of pregnancy in the mare.. Sci Rep 2021 Nov 16;11(1):22293.
    doi: 10.1038/s41598-021-01785-3pubmed: 34785745google scholar: lookup
  6. Smits K, Gansemans Y, Tilleman L, Van Nieuwerburgh F, Van De Velde M, Gerits I, Ververs C, Roels K, Govaere J, Peelman L, Deforce D, Van Soom A. Maternal Recognition of Pregnancy in the Horse: Are MicroRNAs the Secret Messengers?. Int J Mol Sci 2020 Jan 9;21(2).
    doi: 10.3390/ijms21020419pubmed: 31936511google scholar: lookup
Subscribe to our newsletter
Join 99,344 horse owners like you who receive our email updates on horse health and nutrition.