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Biology of reproduction2010; 83(1); 102-113; doi: 10.1095/biolreprod.109.081612

Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy.

Abstract: Establishment and maintenance of pregnancy are critically dependent on embryo-maternal communication during the preimplantation period. To gain new insights into this complex process in the horse, transcriptional profiling of Day 13.5 pregnant and cyclic endometrial tissue samples was carried out using custom-designed microarrays. Selected array data were validated using quantitative RT-PCR, and proteins of interest were localized using immunohistochemistry. One hundred and six transcripts were up-regulated, whereas 47 transcripts showed lower expression levels in pregnant mares, that is, were down-regulated in pregnant mares. Half of the genes with known or inferred function are classically regulated by estrogens. Elevated transcript levels were found for genes involved in cell-cell signaling, heat shock response, and secretory proteins, among others. Solute carrier family 36 (proton/amino acid symporter), member 2, SLC36A2, was one of the most highly up-regulated genes, potentially reflecting the nutritional needs of the rapidly developing embryo. Among the genes showing lower expression in pregnant mares, estrogen receptor 1 was of particular interest because of its potential involvement in the initiation of luteolysis in cyclic mares. We hypothesize that either conceptus' estrogens or luteinizing hormone of uterine origin is involved in the observed down-regulation of estrogen receptor 1. Several of the genes identified in the current study are known to play a role in early pregnancy in species other than the horse. Thus, products of these commonly expressed genes likely contain universal activities for controlling endometrial receptivity to the conceptus, whereas other factors play unique roles within specific species in ensuring ongoing corpus luteum function. This is the first systematic study of endometrial transcriptome changes in response to the presence of an embryo during maternal recognition of pregnancy and an important step toward deciphering the embryo-maternal dialogue in equids.
Publication Date: 2010-03-24 PubMed ID: 20335638DOI: 10.1095/biolreprod.109.081612Google Scholar: Lookup
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  • Journal Article
  • Research Support
  • Non-U.S. Gov't
  • Validation Study

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 examines the changes in the horse’s endometrium during the time of maternal recognition of pregnancy, which is the communication between the embryo and the mare. The study utilized transcriptional profiling to identify the differences in gene expression.

Methodology and General Findings

  • The study used custom-designed microarrays for transcriptional profiling, allowing detailed observation of gene expression in Day 13.5 pregnant and cyclic endometrial tissue samples from horses.
  • Quantitative RT-PCR was used to validate the selected array data, while immunohistochemistry helped to identify proteins obtained from the gene data.
  • Of the gene transcripts tested, 106 were upregulated and 47 were downregulated in pregnant mares, indicating changes in gene expression levels during pregnancy.
  • Half of the genes that show known or inferred function were classified as being regulated by estrogens, a type of hormone that plays a significant role in pregnancy.

Specific Findings

  • The genes with elevated transcript levels were mainly involved in cell-cell signaling, heat shock response, and secretory proteins.
  • One of the highly upregulated genes was SLC36A2, which is part of the Solute carrier family 36, and may reflect the nutritional requirements of the growing embryo.
  • The study took particular note of the estrogen receptor 1 gene, which exhibited lower expression in pregnant mares. The researchers hypothesized that this could be due to its role in initiating luteolysis, a process involved in the menstrual cycle, in cyclic mares.

Conclusions and Implications

  • The research hypothesized that the reduced expression of the estrogen receptor 1 gene could be influenced by the estrogens from the conceptus or luteinizing hormone of uterine origin.
  • Some of the genes identified in this study are already known to play roles in early pregnancy in species other than horses. These findings suggest there could be common factors controlling endometrial receptivity to the conceptus across species.
  • The results of the first systematic study of the changes in endometrial transcriptome in response to the presence of the embryo provide significant contributions toward understanding the embryo-maternal dialogue in horses.

Cite This Article

APA
Klein C, Scoggin KE, Ealy AD, Troedsson MH. (2010). Transcriptional profiling of equine endometrium during the time of maternal recognition of pregnancy. Biol Reprod, 83(1), 102-113. https://doi.org/10.1095/biolreprod.109.081612

Publication

ISSN: 1529-7268
NlmUniqueID: 0207224
Country: United States
Language: English
Volume: 83
Issue: 1
Pages: 102-113

Researcher Affiliations

Klein, Claudia
  • Department of Veterinary Science, University of Kentucky, Lexington, KY, USA. claudia.klein@uky.edu
Scoggin, Kirsten E
    Ealy, Alan D
      Troedsson, Mats H T

        MeSH Terms

        • Animals
        • Computational Biology
        • Endometrium / metabolism
        • Estrous Cycle / metabolism
        • Female
        • Gene Expression Profiling
        • Horses / metabolism
        • Humans
        • Immunohistochemistry
        • Oligonucleotide Array Sequence Analysis
        • Pregnancy / metabolism
        • Reverse Transcriptase Polymerase Chain Reaction

        Citations

        This article has been cited 33 times.
        1. Newcombe JR, Cuervo-Arango J, Wilsher S. The Timing of the Maternal Recognition of Pregnancy Is Specific to Individual Mares.. Animals (Basel) 2023 May 22;13(10).
          doi: 10.3390/ani13101718pubmed: 37238148google 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. Gibson C, de Ruijter-Villani M, Stout TAE. Insulin-like growth factor system components expressed at the conceptus-maternal interface during the establishment of equine pregnancy.. Front Vet Sci 2022;9:912721.
          doi: 10.3389/fvets.2022.912721pubmed: 36176700google scholar: lookup
        4. 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
        5. Diel de Amorim M, Klein C, Foster R, Dong L, Lopez-Rodriguez MF, Card C. Expression of Oxytocin/Neurophysin I and Oxytocinase in the Equine Conceptus from Day 8 to Day 21 Post-Ovulation.. Animals (Basel) 2022 Mar 22;12(7).
          doi: 10.3390/ani12070799pubmed: 35405789google scholar: lookup
        6. Lawson EF, Grupen CG, Baker MA, Aitken RJ, Swegen A, Pollard CL, Gibb Z. Conception and early pregnancy in the mare: lipidomics the unexplored frontier.. Reprod Fertil 2022 Jan 1;3(1):R1-R18.
          doi: 10.1530/RAF-21-0104pubmed: 35350651google scholar: lookup
        7. Segabinazzi LGTM, Roberts BN, Peterson EW, Ambrosia R, Bergfelt D, Samper J, French H, Gilbert RO. Early Pregnancy in Jennies in the Caribbean: Corpus Luteum Development and Progesterone Production, Uterine and Embryo Dynamics, Conceptus Growth and Maturation.. Animals (Basel) 2022 Jan 6;12(2).
          doi: 10.3390/ani12020127pubmed: 35049751google scholar: lookup
        8. 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
        9. Klein C, Bruce P, Hammermueller J, Hayes T, Lillie B, Betteridge K. 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(10):e0257161.
          doi: 10.1371/journal.pone.0257161pubmed: 34614002google scholar: lookup
        10. Weber KS, Wagener K, Blanco M, Bauersachs S, Bollwein H. A comparative analysis of the intrauterine transcriptome in fertile and subfertile mares using cytobrush sampling.. BMC Genomics 2021 May 22;22(1):377.
          doi: 10.1186/s12864-021-07701-3pubmed: 34022808google scholar: lookup
        11. Swegen A. Maternal recognition of pregnancy in the mare: does it exist and why do we care?. Reproduction 2021 May 5;161(6):R139-R155.
          doi: 10.1530/REP-20-0437pubmed: 33957605google scholar: lookup
        12. Camacho CA, Santos GO, Caballeros JE, Cazales N, Ramirez CJ, Vidigal PMP, Ramos HJO, Barros E, Mattos RC. Uterine infusion of conceptus fragments changes the protein profile from cyclic mares.. Anim Reprod 2020 Nov 25;17(4):e20200552.
          doi: 10.1590/1984-3143-AR2020-0552pubmed: 33791032google scholar: lookup
        13. Bauersachs S, Almiñana C. Embryo-Maternal Interactions Underlying Reproduction in Mammals.. Int J Mol Sci 2020 Jul 10;21(14).
          doi: 10.3390/ijms21144872pubmed: 32664189google scholar: lookup
        14. Gibson C, de Ruijter-Villani M, Bauersachs S, Stout TAE. Asynchronous Embryo Transfer Followed by Comparative Transcriptomic Analysis of Conceptus Membranes and Endometrium Identifies Processes Important to the Establishment of Equine Pregnancy.. Int J Mol Sci 2020 Apr 7;21(7).
          doi: 10.3390/ijms21072562pubmed: 32272720google scholar: lookup
        15. Johnson C, Dance A, Kovalchuk I, Kastelic J, Thundathil J. Enhanced pre-pubertal nutrition upregulates mitochondrial function in testes and sperm of post-pubertal Holstein bulls.. Sci Rep 2020 Feb 10;10(1):2235.
          doi: 10.1038/s41598-020-59067-3pubmed: 32042017google scholar: lookup
        16. 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
        17. Klohonatz KM, Coleman SJ, Cameron AD, Hess AM, Reed KJ, Canovas A, Medrano JF, Islas-Trejo AD, Kalbfleisch T, Bouma GJ, Bruemmer JE. Non-Coding RNA Sequencing of Equine Endometrium During Maternal Recognition of Pregnancy.. Genes (Basel) 2019 Oct 18;10(10).
          doi: 10.3390/genes10100821pubmed: 31635328google scholar: lookup
        18. 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/genes10100749pubmed: 31557877google scholar: lookup
        19. Boakari YL, Ali HE, Dini P, Loux S, Fernandes CB, Scoggin K, Esteller-Vico A, Lawrence L, Ball B. A High Protein Model Alters the Endometrial Transcriptome of Mares.. Genes (Basel) 2019 Jul 30;10(8).
          doi: 10.3390/genes10080576pubmed: 31366166google scholar: lookup
        20. Johnson C, Dance A, Kovalchuk I, Kastelic J, Thundathil J. Enhanced early-life nutrition upregulates cholesterol biosynthetic gene expression and Sertoli cell maturation in testes of pre-pubertal Holstein bulls.. Sci Rep 2019 Apr 23;9(1):6448.
          doi: 10.1038/s41598-019-42686-wpubmed: 31015481google scholar: lookup
        21. Kim YJ, Kim YY, Kim DW, Joo JK, Kim H, Ku SY. Profile of MicroRNA Expression in Endometrial Cell during In Vitro Culture According to Progesterone Concentration.. Tissue Eng Regen Med 2017 Oct;14(5):617-629.
          doi: 10.1007/s13770-017-0080-zpubmed: 30603515google scholar: lookup
        22. Smits K, Willems S, Van Steendam K, Van De Velde M, De Lange V, Ververs C, Roels K, Govaere J, Van Nieuwerburgh F, Peelman L, Deforce D, Van Soom A. Proteins involved in embryo-maternal interaction around the signalling of maternal recognition of pregnancy in the horse.. Sci Rep 2018 Mar 27;8(1):5249.
          doi: 10.1038/s41598-018-23537-6pubmed: 29588480google scholar: lookup
        23. Aurich C, Budik S. Early pregnancy in the horse revisited - does exception prove the rule?. J Anim Sci Biotechnol 2015;6:50.
          doi: 10.1186/s40104-015-0048-6pubmed: 26635959google scholar: lookup
        24. López-Úbeda R, García-Vázquez FA, Romar R, Gadea J, Muñoz M, Hunter RH, Coy P. Oviductal Transcriptome Is Modified after Insemination during Spontaneous Ovulation in the Sow.. PLoS One 2015;10(6):e0130128.
          doi: 10.1371/journal.pone.0130128pubmed: 26098421google scholar: lookup
        25. Zhao H, Sui L, Miao K, An L, Wang D, Hou Z, Wang R, Guo M, Wang Z, Xu J, Wu Z, Tian J. Comparative analysis between endometrial proteomes of pregnant and non-pregnant ewes during the peri-implantation period.. J Anim Sci Biotechnol 2015;6(1):18.
          doi: 10.1186/s40104-015-0017-0pubmed: 26023329google scholar: lookup
        26. Shen J, Zhou C, Zhu S, Shi W, Hu M, Fu X, Wang C, Wang Y, Zhang Q, Yu Y. Comparative transcriptome analysis reveals early pregnancy-specific genes expressed in peripheral blood of pregnant sows.. PLoS One 2014;9(12):e114036.
          doi: 10.1371/journal.pone.0114036pubmed: 25479131google scholar: lookup
        27. Zhou C, Dobrinsky J, Tsoi S, Foxcroft GR, Dixon WT, Stothard P, Verstegen J, Dyck MK. Characterization of the altered gene expression profile in early porcine embryos generated from parthenogenesis and somatic cell chromatin transfer.. PLoS One 2014;9(3):e91728.
          doi: 10.1371/journal.pone.0091728pubmed: 24633136google scholar: lookup
        28. Almiñana C, Heath PR, Wilkinson S, Sanchez-Osorio J, Cuello C, Parrilla I, Gil MA, Vazquez JL, Vazquez JM, Roca J, Martinez EA, Fazeli A. Early developing pig embryos mediate their own environment in the maternal tract.. PLoS One 2012;7(3):e33625.
          doi: 10.1371/journal.pone.0033625pubmed: 22470458google scholar: lookup
        29. Tang H, Liao Y, Chen G, Xu L, Zhang C, Ju S, Zhou S. Estrogen upregulates the IGF-1 signaling pathway in lung cancer through estrogen receptor-β.. Med Oncol 2012 Dec;29(4):2640-8.
          doi: 10.1007/s12032-012-0198-8pubmed: 22427208google scholar: lookup
        30. Thwaites DT, Anderson CM. The SLC36 family of proton-coupled amino acid transporters and their potential role in drug transport.. Br J Pharmacol 2011 Dec;164(7):1802-16.
        31. Klein C, Rutllant J, Troedsson MH. Expression stability of putative reference genes in equine endometrial, testicular, and conceptus tissues.. BMC Res Notes 2011 Apr 12;4:120.
          doi: 10.1186/1756-0500-4-120pubmed: 21486450google scholar: lookup
        32. Brosnahan MM, Brooks SA, Antczak DF. Equine clinical genomics: A clinician's primer.. Equine Vet J 2010 Oct;42(7):658-70.
        33. Edwards N, Anderson CM, Gatfield KM, Jevons MP, Ganapathy V, Thwaites DT. Amino acid derivatives are substrates or non-transported inhibitors of the amino acid transporter PAT2 (slc36a2).. Biochim Biophys Acta 2011 Jan;1808(1):260-70.
          doi: 10.1016/j.bbamem.2010.07.032pubmed: 20691150google scholar: lookup