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Reproduction (Cambridge, England)2021; 161(6); R139-R155; doi: 10.1530/REP-20-0437

Maternal recognition of pregnancy in the mare: does it exist and why do we care?

Abstract: Maternal recognition of pregnancy (MRP) is a process by which an early conceptus signals its presence to the maternal system and prevents the lysis of the corpus luteum, thus ensuring a maternal milieu supportive of pregnancy continuation. It is a fundamental aspect of reproductive biology, yet in the horse, the mechanism underlying MRP remains unknown. This review seeks to address some of the controversies surrounding the evidence and theories of MRP in the equine species, such as the idea that the horse does not conform to the MRP paradigm established in other species or that equine MRP involves a mechanical, rather than chemical, signal. The review examines the challenges of studying this particularly clandestine phenomenon along with the new tools in scientific research that will drive this quest forward in coming years, and discuss the value of knowledge gleaned along this path in the context of clinical applications for improving breeding outcomes in the horse industry.
Publication Date: 2021-05-05 PubMed ID: 33957605PubMed Central: PMC8183633DOI: 10.1530/REP-20-0437Google Scholar: Lookup
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  • Journal Article
  • Review

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.

This research article focusses on the concept of Maternal Recognition of Pregnancy (MRP) in horses, exploring theories and controversies, challenges in studying this phenomenon, and its potential application in the horse breeding industry.

Understanding Maternal Recognition of Pregnancy (MRP) in horses

In the body of the report, the authors delve into the process of MRP, which acts as a communication tool between the early embryo and the mother’s system. This interaction signals that pregnancy has begun and prevents the breakdown of the corpus luteum, a structure necessary during early pregnancy. It is crucial because it creates a favorable environment in the mother’s body to support the continuation of the pregnancy.

  • The authors highlight that while this is a fundamental aspect of reproductive biology, its functioning is not fully understood in horses.
  • The discussion sheds light on various controversies about MRP in horses. One of the controversies argues that horses do not follow the same MRP pattern observed in other species. Another theory suggests that the MRP in horses involves a physical signal rather than a chemical one.

Research Challenges and Future Directions

This part of the research paper examines the challenges of studying this relatively secretive phenomenon.

  • The clandestine nature of this process leads to difficulties in its research. However, the authors remain positive about the future of the field as new tools and methodologies in scientific research will aid in advancing our understanding of MRP in the coming years.
  • The research also implies that unlocking the mystery behind MRP could have significant therapeutic implications, particularly in improving the outcomes of horse breeding. This could potentially lead to a greater understanding of fertility and reproductive efficiency not only in horses but also other species.

Cite This Article

APA
Swegen A. (2021). Maternal recognition of pregnancy in the mare: does it exist and why do we care? Reproduction, 161(6), R139-R155. https://doi.org/10.1530/REP-20-0437

Publication

ISSN: 1741-7899
NlmUniqueID: 100966036
Country: England
Language: English
Volume: 161
Issue: 6
Pages: R139-R155
PII: REP-20-0437

Researcher Affiliations

Swegen, Aleona
  • Nuffield Department of Women's and Reproductive Health, University of Oxford, Oxford, UK.
  • Priority Research Centre for Reproductive Science, University of Newcastle, Callaghan, New South Wales, Australia.

MeSH Terms

  • Animals
  • Corpus Luteum Maintenance
  • Embryonic Development
  • Female
  • Horses
  • Pregnancy
  • Pregnancy, Animal

References

This article includes 108 references
  1. Ababneh MM, Troedsson MH, Michelson JR, Seguin BE. Partial characterization of an equine conceptus prostaglandin inhibitory factor.. J Reprod Fertil Suppl 2000;(56):607-13.
    pubmed: 20681176
  2. Aggarwal BB, Farmer SW, Papkoff H, Stewart F, Allen WR. Purification and characterization of the gonadotropin secreted by cultured horse trophoblast cells.. Endocrinology 1980 Jun;106(6):1755-9.
    doi: 10.1210/endo-106-6-1755pubmed: 6768542google scholar: lookup
  3. Albihn A, Waelchli RO, Samper J, Oriol JG, Croy BA, Betteridge KJ. Production of capsular material by equine trophoblast transplanted into immunodeficient mice.. Reproduction 2003 Jun;125(6):855-63.
    doi: 10.1530/rep.0.1250855pubmed: 12773108google scholar: lookup
  4. Ball BA, Altschul M, Freeman KP, Hillman RB. Culture of equine trophoblastic vesicles in vitro.. Theriogenology 1989 Sep;32(3):401-12.
    doi: 10.1016/0093-691x(89pubmed: 16726686google scholar: lookup
  5. Ball BA, Altschul M, McDowell KJ, Ignotz G, Currie WB. Trophoblastic vesicles and maternal recognition of pregnancy in mares.. J Reprod Fertil Suppl 1991;44:445-54.
    pubmed: 1795288
  6. Bauersachs S, Wolf E. Transcriptome analyses of bovine, porcine and equine endometrium during the pre-implantation phase.. Anim Reprod Sci 2012 Sep;134(1-2):84-94.
  7. Bazer FW. History of Maternal Recognition of Pregnancy.. Adv Anat Embryol Cell Biol 2015;216:5-25.
    doi: 10.1007/978-3-319-15856-3_2pubmed: 26450492google scholar: lookup
  8. Bazer FW, Spencer TE, Johnson GA, Burghardt RC. Uterine receptivity to implantation of blastocysts in mammals.. Front Biosci (Schol Ed) 2011 Jan 1;3(2):745-67.
    doi: 10.2741/s184pubmed: 21196409google scholar: lookup
  9. Beckelmann J, Budik S, Helmreich M, Palm F, Walter I, Aurich C. Sex-dependent insulin like growth factor-1 expression in preattachment equine embryos.. Theriogenology 2013 Jan 1;79(1):193-9.
  10. Bemis LT, McCue PM, Hatzel JN, Bemis J, Ferris RA. Evidence for production of early pregnancy factor (Hsp10), microRNAs and exosomes by day 8 equine embryos. Journal of Equine Veterinary Science 32 398.
  11. Berglund LA, Sharp DC, Vernon MW, Thatcher WW. Effect of pregnancy and collection technique on prostaglandin F in the uterine lumen of Pony mares.. J Reprod Fertil Suppl 1982;32:335-41.
    pubmed: 6962869
  12. Betteridge KJ, Mitchell D. Retention of ova by the Fallopian tube in mares.. J Reprod Fertil 1972 Dec;31(3):515.
    doi: 10.1530/jrf.0.0310515pubmed: 4675923google scholar: lookup
  13. Betteridge KJ, Mitchell D. Direct evidence of retention of unfertilized ova in the oviduct of the mare.. J Reprod Fertil 1974 Jul;39(1):145-8.
    doi: 10.1530/jrf.0.0390145pubmed: 4604330google scholar: lookup
  14. Betteridge KJ, Eaglesome MD, Flood PF. Embryo transport through the mare's oviduct depends upon cleavage and is independent of the ipsilateral corpus luteum.. J Reprod Fertil Suppl 1979;(27):387-94.
    pubmed: 289814
  15. Betteridge KJ, Eaglesome MD, Randall GC, Mitchell D. Collection, description and transfer of embryos from cattle 10--16 days after oestrus.. J Reprod Fertil 1980 May;59(1):205-16.
    doi: 10.1530/jrf.0.0590205pubmed: 7401037google scholar: lookup
  16. Binelli M, Subramaniam P, Diaz T, Johnson GA, Hansen TR, Badinga L, Thatcher WW. Bovine interferon-tau stimulates the Janus kinase-signal transducer and activator of transcription pathway in bovine endometrial epithelial cells.. Biol Reprod 2001 Feb;64(2):654-65.
    doi: 10.1095/biolreprod64.2.654pubmed: 11159370google scholar: lookup
  17. Boerboom D, Brown KA, Vaillancourt D, Poitras P, Goff AK, Watanabe K, Doré M, Sirois J. Expression of key prostaglandin synthases in equine endometrium during late diestrus and early pregnancy.. Biol Reprod 2004 Feb;70(2):391-9.
    doi: 10.1095/biolreprod.103.020800pubmed: 14561653google scholar: lookup
  18. Budik S, Nöbauer K, Razzazi-Fazeli E, Aurich C. Analysis of the proteins and peptides isolated from incubation medium of early equine conceptuses - preliminary results. Journal of Equine Veterinary Science 32 400.
  19. Cameron EZ, Linklater WL. Extreme sex ratio variation in relation to change in condition around conception.. Biol Lett 2007 Aug 22;3(4):395-7.
    doi: 10.1098/rsbl.2007.0089pmc: PMC2390657pubmed: 17439844google scholar: lookup
  20. Cameron EZ, Linklater WL, Stafford KJ, Veltman CJ. Birth sex ratios relate to mare condition at conception in Kaimanawa horses. Behavioral Ecology 10 472–475.
    doi: 10.1093/beheco/10.5.472google scholar: lookup
  21. Camozzato GC, Martinez MN, Bastos HBA, Fiala-Rechsteiner S, Meikle A, Jobim MIM, Gregory RM, Mattos RC. Ultrastructural and histological characteristics of the endometrium during early embryo development in mares.. Theriogenology 2019 Jan 1;123:1-10.
  22. Carnevale EM, Catandi GD, Fresa K. Equine Aging and the Oocyte: A Potential Model for Reproductive Aging in Women.. J Equine Vet Sci 2020 Jun;89:103022.
    doi: 10.1016/j.jevs.2020.103022pubmed: 32563447google scholar: lookup
  23. Casper RF, Wilson E, Collins JA, Brown SF, Parker JA. Enhancement of human implantation by exogenous chorionic gonadotropin.. Lancet 1983 Nov 19;2(8360):1191.
    doi: 10.1016/s0140-6736(83pubmed: 6139540google scholar: lookup
  24. Chen Y, Antoniou E, Liu Z, Hearne LB, Roberts RM. A microarray analysis for genes regulated by interferon-tau in ovine luminal epithelial cells.. Reproduction 2007 Jul;134(1):123-35.
    doi: 10.1530/REP-07-0387pubmed: 17641094google scholar: lookup
  25. Chen HY, Li OY, Pang LH, Xu H, Fan XJ, Liang HF, Chen XF, Qing JZ, Huang RD, Deng BY. Expression of FK506-binding protein 52 (FKBP52) in chorionic villi with early recurrent spontaneous abortion.. J Matern Fetal Neonatal Med 2015 Jul;28(10):1165-9.
    doi: 10.3109/14767058.2014.947572pubmed: 25053194google scholar: lookup
  26. de Ruijter-Villani M, van Tol HT, Stout TA. Effect of pregnancy on endometrial expression of luteolytic pathway components in the mare.. Reprod Fertil Dev 2015 Jun;27(5):834-45.
    doi: 10.1071/RD13381pubmed: 24679480google scholar: lookup
  27. Duranthon V, Chavatte-Palmer P. Long term effects of ART: What do animals tell us?. Mol Reprod Dev 2018 Apr;85(4):348-368.
    doi: 10.1002/mrd.22970pubmed: 29457303google scholar: lookup
  28. Ealy AD, Eroh ML, Sharp DC 3rd. Prostaglandin H synthase Type 2 is differentially expressed in endometrium based on pregnancy status in pony mares and responds to oxytocin and conceptus secretions in explant culture.. Anim Reprod Sci 2010 Jan;117(1-2):99-105.
  29. Ferraz MAMM, Rho HS, Hemerich D, Henning HHW, van Tol HTA, Hölker M, Besenfelder U, Mokry M, Vos PLAM, Stout TAE, Le Gac S, Gadella BM. An oviduct-on-a-chip provides an enhanced in vitro environment for zygote genome reprogramming.. Nat Commun 2018 Nov 22;9(1):4934.
    doi: 10.1038/s41467-018-07119-8pmc: PMC6250703pubmed: 30467383google scholar: lookup
  30. Fishel SB, Edwards RG, Evans CJ. Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro.. Science 1984 Feb 24;223(4638):816-8.
    doi: 10.1126/science.6546453pubmed: 6546453google scholar: lookup
  31. Fleming TP, Watkins AJ, Sun C, Velazquez MA, Smyth NR, Eckert JJ. Do little embryos make big decisions? How maternal dietary protein restriction can permanently change an embryo's potential, affecting adult health.. Reprod Fertil Dev 2015 May;27(4):684-92.
    doi: 10.1071/RD14455pubmed: 25730413google scholar: lookup
  32. Fournier T, Guibourdenche J, Evain-Brion D. Review: hCGs: different sources of production, different glycoforms and functions.. Placenta 2015 Apr;36 Suppl 1:S60-5.
  33. Gebhardt S, Merkl M, Herbach N, Wanke R, Handler J, Bauersachs S. Exploration of global gene expression changes during the estrous cycle in equine endometrium.. Biol Reprod 2012 Jun;87(6):136.
    doi: 10.1095/biolreprod.112.103226pubmed: 23077167google scholar: lookup
  34. Gnecco JS, Ding T, Smith C, Lu J, Bruner-Tran KL, Osteen KG. Hemodynamic forces enhance decidualization via endothelial-derived prostaglandin E2 and prostacyclin in a microfluidic model of the human endometrium.. Hum Reprod 2019 Apr 1;34(4):702-714.
    doi: 10.1093/humrep/dez003pmc: PMC6443116pubmed: 30789661google scholar: lookup
  35. Goff AK, Pontbriand D, Sirois J. Oxytocin stimulation of plasma 15-keto-13,14-dihydro prostaglandin F-2 alpha during the oestrous cycle and early pregnancy in the mare.. J Reprod Fertil Suppl 1987;35:253-60.
    pubmed: 3479581
  36. Guy NC, Garcia YA, Cox MB. Therapeutic Targeting of the FKBP52 Co-Chaperone in Steroid Hormone Receptor-Regulated Physiology and Disease.. Curr Mol Pharmacol 2015;9(2):109-25.
  37. Hall SE, Upton RMO, McLaughlin EA, Sutherland JM. Phosphoinositide 3-kinase/protein kinase B (PI3K/AKT) and Janus kinase/signal transducer and activator of transcription (JAK/STAT) follicular signalling is conserved in the mare ovary.. Reprod Fertil Dev 2018 Mar;30(4):624-633.
    doi: 10.1071/RD17024pubmed: 28945982google scholar: lookup
  38. Hansen TR, Pru JK. ISGylation: a conserved pathway in mammalian pregnancy.. Adv Exp Med Biol 2014;759:13-31.
    doi: 10.1007/978-1-4939-0817-2_2pubmed: 25030758google scholar: lookup
  39. Hansen TR, Sinedino LDP, Spencer TE. Paracrine and endocrine actions of interferon tau (IFNT).. Reproduction 2017 Nov;154(5):F45-F59.
    doi: 10.1530/REP-17-0315pubmed: 28982937google scholar: lookup
  40. Hennes A, Held K, Boretto M, De Clercq K, Van den Eynde C, Vanhie A, Van Ranst N, Benoit M, Luyten C, Peeraer K, Tomassetti C, Meuleman C, Voets T, Vankelecom H, Vriens J. Functional expression of the mechanosensitive PIEZO1 channel in primary endometrial epithelial cells and endometrial organoids.. Sci Rep 2019 Feb 11;9(1):1779.
    doi: 10.1038/s41598-018-38376-8pmc: PMC6370865pubmed: 30741991google scholar: lookup
  41. Herrler A, Pell JM, Allen WR, Beier HM, Stewart F. Horse conceptuses secrete insulin-like growth factor-binding protein 3.. Biol Reprod 2000 Jun;62(6):1804-11.
    doi: 10.1095/biolreprod62.6.1804pubmed: 10819785google scholar: lookup
  42. Hughes-Fulford M. Signal transduction and mechanical stress.. Sci STKE 2004 Aug 31;2004(249):RE12.
    doi: 10.1126/stke.2492004re12pubmed: 15353762google scholar: lookup
  43. Jarvis GE. Early embryo mortality in natural human reproduction: What the data say.. F1000Res 2016;5:2765.
  44. Jenkins TG, Aston KI, Meyer T, Carrell DT. The Sperm Epigenome, Male Aging, and Potential Effects on the Embryo.. Adv Exp Med Biol 2015;868:81-93.
    doi: 10.1007/978-3-319-18881-2_4pubmed: 26178846google scholar: lookup
  45. Kimura K, Spate LD, Green MP, Roberts RM. Effects of oxidative stress and inhibitors of the pentose phosphate pathway on sexually dimorphic production of IFN-tau by bovine blastocysts.. Mol Reprod Dev 2004 May;68(1):88-95.
    doi: 10.1002/mrd.20053pubmed: 15039952google scholar: lookup
  46. Klein C. Pregnancy Recognition and Implantation of the Conceptus in the Mare.. Adv Anat Embryol Cell Biol 2015;216:165-88.
    doi: 10.1007/978-3-319-15856-3_9pubmed: 26450499google scholar: lookup
  47. Klein C. Novel equine conceptus?endometrial interactions on Day 16 of pregnancy based on RNA sequencing.. Reprod Fertil Dev 2015 May 5;.
    doi: 10.1071/RD14489pubmed: 25940503google scholar: lookup
  48. Klein C. Early pregnancy in the mare: old concepts revisited.. Domest Anim Endocrinol 2016 Jul;56 Suppl:S212-7.
  49. Klein C, Troedsson MH. Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse.. Biol Reprod 2011 May;84(5):872-85.
    doi: 10.1095/biolreprod.110.088732pubmed: 21209420google scholar: lookup
  50. 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
  51. Klein C, Scoggin KE, Troedsson MH. The expression of interferon-stimulated gene 15 in equine endometrium.. Reprod Domest Anim 2011 Aug;46(4):692-8.
  52. 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
  53. 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
  54. 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.
  55. Larson MA, Kimura K, Kubisch HM, Roberts RM. Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signaling molecule IFN-tau.. Proc Natl Acad Sci U S A 2001 Aug 14;98(17):9677-82.
    doi: 10.1073/pnas.171305398pmc: PMC55511pubmed: 11481449google scholar: lookup
  56. Lawson EF, Gibb Z, de Ruijter-Villani M, Smith ND, Stout TA, Clutton-Brock A, Aitken JR, Swegen A. Proteomic analysis of pregnant mare uterine fluid. Journal of Equine Veterinary Science 66 171–172.
  57. Lee J, Stanley JA, McCracken JA, Banu SK, Arosh JA. Intrauterine coadministration of ERK1/2 inhibitor U0126 inhibits interferon TAU action in the endometrium and restores luteolytic PGF2alpha pulses in sheep.. Biol Reprod 2014 Aug;91(2):46.
    doi: 10.1095/biolreprod.113.111872pubmed: 24876409google scholar: lookup
  58. 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(84pubmed: 16725972google scholar: lookup
  59. Lennard SN, Stewart F, Allen WR. Transforming growth factor beta 1 expression in the endometrium of the mare during placentation.. Mol Reprod Dev 1995 Oct;42(2):131-40.
    doi: 10.1002/mrd.1080420202pubmed: 8562058google scholar: lookup
  60. Maj T, Chelmonska-Soyta A. Pleiotropy and redundancy of STAT proteins in early pregnancy.. Reprod Domest Anim 2007 Aug;42(4):343-53.
  61. Mauffré V, Grimard B, Eozenou C, Inghels S, Silva L, Giraud-Delville C, Capo D, Sandra O, Constant F. Interferon stimulated genes as peripheral diagnostic markers of early pregnancy in sheep: a critical assessment.. Animal 2016 Nov;10(11):1856-1863.
    doi: 10.1017/S175173111600077Xpubmed: 27150201google scholar: lookup
  62. 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
  63. Mikuni-Takagaki Y. Mechanical responses and signal transduction pathways in stretched osteocytes.. J Bone Miner Metab 1999;17(1):57-60.
    doi: 10.1007/s007740050065pubmed: 10084403google scholar: lookup
  64. Monard A-M, Duncan P, Fritz H, Feh C. Variations in the birth sex ratio and neonatal mortality in a natural herd of horses. Behavioral Ecology and Sociobiology 41 243–249.
    doi: 10.1007/s002650050385google scholar: lookup
  65. Moor RM, Rowson LE. The corpus luteum of the sheep: functional relationship between the embryo and the corpus luteum.. J Endocrinol 1966 Feb;34(2):233-9.
    doi: 10.1677/joe.0.0340233pubmed: 5901838google scholar: lookup
  66. Nguyen HPT, Xiao L, Deane JA, Tan KS, Cousins FL, Masuda H, Sprung CN, Rosamilia A, Gargett CE. N-cadherin identifies human endometrial epithelial progenitor cells by in vitro stem cell assays.. Hum Reprod 2017 Nov 1;32(11):2254-2268.
    doi: 10.1093/humrep/dex289pubmed: 29040564google scholar: lookup
  67. Northey DL, French LR. Effect of embryo removal and intrauterine infusion of embryonic homogenates on the lifespan of the bovine corpus luteum.. J Anim Sci 1980 Feb;50(2):298-302.
    doi: 10.2527/jas1980.502298xpubmed: 7358600google scholar: lookup
  68. Nyalwidhe J, Burch T, Bocca S, Cazares L, Green-Mitchell S, Cooke M, Birdsall P, Basu G, Semmes OJ, Oehninger S. The search for biomarkers of human embryo developmental potential in IVF: a comprehensive proteomic approach.. Mol Hum Reprod 2013 Apr;19(4):250-63.
    doi: 10.1093/molehr/gas063pubmed: 23247814google scholar: lookup
  69. Ohnuma K, Yokoo M, Ito K, Nambo Y, Miyake YI, Komatsu M, Takahashi J. Study of early pregnancy factor (EPF) in equine (Equus caballus).. Am J Reprod Immunol 2000 Mar;43(3):174-9.
  70. Rivera Del Alamo MM, Reilas T, Kindahl H, Katila T. Mechanisms behind intrauterine device-induced luteal persistence in mares.. Anim Reprod Sci 2008 Aug;107(1-2):94-106.
  71. Rivera Del Alamo MM, Reilas T, Galvão A, Yeste M, Katila T. Cyclooxygenase-2 is inhibited in prolonged luteal maintenance induced by intrauterine devices in mares.. Anim Reprod Sci 2018 Dec;199:93-103.
  72. Roberts RM, Chen Y, Ezashi T, Walker AM. Interferons and the maternal-conceptus dialog in mammals.. Semin Cell Dev Biol 2008 Apr;19(2):170-7.
  73. Ross GT. Human chorionic gonadotropin and maternal recognition of pregnancy.. Ciba Found Symp 1978;(64):191-208.
    pubmed: 259039doi: 10.1002/9780470720479.ch9google scholar: lookup
  74. Ryan JP, O'Neill C, Ammit AJ, Roberts CG. Metabolic and developmental responses of preimplantation embryos to platelet activating factor (PAF).. Reprod Fertil Dev 1992;4(4):387-98.
    doi: 10.1071/rd9920387pubmed: 1461990google scholar: lookup
  75. Schwinghamer R, Massolo A, Knight C, Klein C. Equine Endometrial Explants Undergo Significant Degenerative Changes in Culture.. Anat Rec (Hoboken) 2018 Jan;301(1):148-153.
    doi: 10.1002/ar.23701pubmed: 29024547google scholar: lookup
  76. Scigelova M, Makarov A. Advances in bioanalytical LC-MS using the Orbitrap™ mass analyzer.. Bioanalysis 2009 Jul;1(4):741-54.
    doi: 10.4155/bio.09.65pubmed: 21083136google scholar: lookup
  77. Sharp DC, Zavy MT, Vernon MW, Bazer FW, Thatcher WW, Berglund LA. The role of prostaglandins in the maternal recognition of pregnancy in mares. Animal Reproduction Science 7 269–282.
    doi: 10.1016/0378-4320(84google scholar: lookup
  78. Sharp DC, McDowell KJ, Weithenauer J, Thatcher WW. The continuum of events leading to maternal recognition of pregnancy in mares.. J Reprod Fertil Suppl 1989;37:101-7.
    pubmed: 2810225
  79. Short RV. Implantation and the maternal recognition of pregnancy. Ciba Foundation Symposium ‐ Foetal Autonomy 2 pp. 31.
  80. Silva LA, Gastal EL, Beg MA, Ginther OJ. Changes in vascular perfusion of the endometrium in association with changes in location of the embryonic vesicle in mares.. Biol Reprod 2005 Mar;72(3):755-61.
    doi: 10.1095/biolreprod.104.036384pubmed: 15576822google scholar: lookup
  81. Silva LA, Klein C, Ealy AD, Sharp DC. Conceptus-mediated endometrial vascular changes during early pregnancy in mares: an anatomic, histomorphometric, and vascular endothelial growth factor receptor system immunolocalization and gene expression study.. Reproduction 2011 Oct;142(4):593-603.
    doi: 10.1530/REP-11-0149pubmed: 21757474google scholar: lookup
  82. Sissener TR, Squires EL, Clay CM. Differential suppression of endometrial prostaglandin F2alpha by the equine conceptus.. Theriogenology 1996 Feb;45(3):541-6.
    doi: 10.1016/0093-691x(95pubmed: 16727817google scholar: lookup
  83. Sivils JC, Storer CL, Galigniana MD, Cox MB. Regulation of steroid hormone receptor function by the 52-kDa FK506-binding protein (FKBP52).. Curr Opin Pharmacol 2011 Aug;11(4):314-9.
    doi: 10.1016/j.coph.2011.03.010pmc: PMC3156321pubmed: 21511531google scholar: lookup
  84. 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/s41598-018-23537-6pmc: PMC5869742pubmed: 29588480google scholar: lookup
  85. 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/ijms21020419pmc: PMC7014256pubmed: 31936511google scholar: lookup
  86. Starbuck GR, Stout TA, Lamming GE, Allen WR, Flint AP. Endometrial oxytocin receptor and uterine prostaglandin secretion in mares during the oestrous cycle and early pregnancy.. J Reprod Fertil 1998 Jul;113(2):173-9.
    doi: 10.1530/jrf.0.1130173pubmed: 9861156google scholar: lookup
  87. Stout TA. Embryo-maternal communication during the first 4 weeks of equine pregnancy.. Theriogenology 2016 Jul 1;86(1):349-54.
  88. Stout TA, Allen WR. Prostaglandin E(2) and F(2 alpha) production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares.. Reproduction 2002 Feb;123(2):261-8.
    doi: 10.1530/rep.0.1230261pubmed: 11866693google scholar: lookup
  89. Stout TA, Lamming GE, Allen WR. Oxytocin administration prolongs luteal function in cyclic mares.. J Reprod Fertil 1999 Jul;116(2):315-20.
    doi: 10.1530/jrf.0.1160315pubmed: 10615256google scholar: lookup
  90. Sutherland JM, Frost ER, Ford EA, Peters AE, Reed NL, Seldon AN, Mihalas BP, Russel DL, Dunning KR, McLaughlin EA. Janus kinase JAK1 maintains the ovarian reserve of primordial follicles in the mouse ovary.. Mol Hum Reprod 2018 Nov 1;24(11):533-542.
    doi: 10.1093/molehr/gay041pubmed: 30247637google scholar: lookup
  91. Swegen A, Grupen CG, Gibb Z, Baker MA, de Ruijter-Villani M, Smith ND, Stout TAE, Aitken RJ. From Peptide Masses to Pregnancy Maintenance: A Comprehensive Proteomic Analysis of The Early Equine Embryo Secretome, Blastocoel Fluid, and Capsule.. Proteomics 2017 Sep;17(17-18).
    doi: 10.1002/pmic.201600433pubmed: 28782881google scholar: lookup
  92. Thatcher WW, Guzeloglu A, Mattos R, Binelli M, Hansen TR, Pru JK. Uterine-conceptus interactions and reproductive failure in cattle.. Theriogenology 2001 Dec 1;56(9):1435-50.
    doi: 10.1016/s0093-691x(01pubmed: 11768809google scholar: lookup
  93. Thompson RE, Johnson AK, Dini P, Turco MY, Prado TM, Premanandan C, Burton GJ, Ball BA, Whitlock BK, Pukazhenthi BS. Hormone-responsive organoids from domestic mare and endangered Przewalski's horse endometrium.. Reproduction 2020 Dec;160(6):819-831.
    doi: 10.1530/REP-20-0266pubmed: 33112764google scholar: lookup
  94. Tranguch S, Cheung-Flynn J, Daikoku T, Prapapanich V, Cox MB, Xie H, Wang H, Das SK, Smith DF, Dey SK. Cochaperone immunophilin FKBP52 is critical to uterine receptivity for embryo implantation.. Proc Natl Acad Sci U S A 2005 Oct 4;102(40):14326-31.
    doi: 10.1073/pnas.0505775102pmc: PMC1242310pubmed: 16176985google scholar: lookup
  95. Tranguch S, Smith DF, Dey SK. Progesterone receptor requires a co-chaperone for signalling in uterine biology and implantation.. Reprod Biomed Online 2006 Nov;13(5):651-60.
    doi: 10.1016/s1472-6483(10pubmed: 17169175google scholar: lookup
  96. Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, Hollinshead M, Marsh SGE, Brosens JJ, Critchley HO, Simons BD, Hemberger M, Koo BK, Moffett A, Burton GJ. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium.. Nat Cell Biol 2017 May;19(5):568-577.
    doi: 10.1038/ncb3516pmc: PMC5410172pubmed: 28394884google scholar: lookup
  97. Turco MY, Gardner L, Kay RG, Hamilton RS, Prater M, Hollinshead MS, McWhinnie A, Esposito L, Fernando R, Skelton H, Reimann F, Gribble FM, Sharkey A, Marsh SGE, O'Rahilly S, Hemberger M, Burton GJ, Moffett A. Trophoblast organoids as a model for maternal-fetal interactions during human placentation.. Nature 2018 Dec;564(7735):263-267.
    doi: 10.1038/s41586-018-0753-3pmc: PMC7220805pubmed: 30487605google scholar: lookup
  98. Vernon MW, Zavy MT, Asquith RL, Sharp DC. Prostaglandin F2alpha in the equine endometrium: steroid modulation and production capacities during the estrous cycle and early pregnancy.. Biol Reprod 1981 Oct;25(3):581-9.
    doi: 10.1095/biolreprod25.3.581pubmed: 6946841google scholar: lookup
  99. Vilella F, Ramirez LB, Simón C. Lipidomics as an emerging tool to predict endometrial receptivity.. Fertil Steril 2013 Mar 15;99(4):1100-6.
  100. Wade CM, Giulotto E, Sigurdsson S, Zoli M, Gnerre S, Imsland F, Lear TL, Adelson DL, Bailey E, Bellone RR, Blöcker H, Distl O, Edgar RC, Garber M, Leeb T, Mauceli E, MacLeod JN, Penedo MC, Raison JM, Sharpe T, Vogel J, Andersson L, Antczak DF, Biagi T, Binns MM, Chowdhary BP, Coleman SJ, Della Valle G, Fryc S, Guérin G, Hasegawa T, Hill EW, Jurka J, Kiialainen A, Lindgren G, Liu J, Magnani E, Mickelson JR, Murray J, Nergadze SG, Onofrio R, Pedroni S, Piras MF, Raudsepp T, Rocchi M, Røed KH, Ryder OA, Searle S, Skow L, Swinburne JE, Syvänen AC, Tozaki T, Valberg SJ, Vaudin M, White JR, Zody MC, Lander ES, Lindblad-Toh K. Genome sequence, comparative analysis, and population genetics of the domestic horse.. Science 2009 Nov 6;326(5954):865-7.
    doi: 10.1126/science.1178158pmc: PMC3785132pubmed: 19892987google scholar: lookup
  101. Walters KW, Roser JF, Anderson GB. Maternal-conceptus signalling during early pregnancy in mares: oestrogen and insulin-like growth factor I.. Reproduction 2001 Feb;121(2):331-8.
    doi: 10.1530/rep.0.1210331pubmed: 11226058google scholar: lookup
  102. Watson ED, Aubrey ES, Zanecosky HG, Sertich PL. Isolation and culture of glandular epithelial and stromal cells from the endometrium of mares.. J Reprod Fertil 1992 May;95(1):269-75.
    doi: 10.1530/jrf.0.0950269pubmed: 1625242google scholar: lookup
  103. Wilsher S, Allen WR. Intrauterine administration of plant oils inhibits luteolysis in the mare.. Equine Vet J 2011 Jan;43(1):99-105.
  104. Wilsher S, Clutton-Brock A, Allen WR. Successful transfer of day 10 horse embryos: influence of donor-recipient asynchrony on embryo development.. Reproduction 2010 Mar;139(3):575-85.
    doi: 10.1530/REP-09-0306pubmed: 19948839google scholar: lookup
  105. Wood PL, Ball BA, Scoggin K, Troedsson MH, Squires EL. Lipidomics of equine amniotic fluid: Identification of amphiphilic (O-acyl)-ω-hydroxy-fatty acids.. Theriogenology 2018 Jan 1;105:120-125.
  106. Woods DC, Khrapko K, Tilly JL. Influence of Maternal Aging on Mitochondrial Heterogeneity, Inheritance, and Function in Oocytes and Preimplantation Embryos.. Genes (Basel) 2018 May 21;9(5).
    doi: 10.3390/genes9050265pmc: PMC5977205pubmed: 29883421google scholar: lookup
  107. Xiao CW, Murphy BD, Sirois J, Goff AK. Down-regulation of oxytocin-induced cyclooxygenase-2 and prostaglandin F synthase expression by interferon-tau in bovine endometrial cells.. Biol Reprod 1999 Mar;60(3):656-63.
    doi: 10.1095/biolreprod60.3.656pubmed: 10026113google scholar: lookup
  108. Yoshizaki K, Kimura R, Kobayashi H, Oki S, Kikkawa T, Mai L, Koike K, Mochizuki K, Inada H, Matsui Y, Kono T, Osumi N. Paternal age affects offspring via an epigenetic mechanism involving REST/NRSF.. EMBO Rep 2021 Feb 3;22(2):e51524.
    doi: 10.15252/embr.202051524pmc: PMC7857438pubmed: 33399271google scholar: lookup

Citations

This article has been cited 8 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. Hallman I, Karikoski N, Kareskoski M. The effects of obesity and insulin dysregulation on mare reproduction, pregnancy, and foal health: a review.. Front Vet Sci 2023;10:1180622.
    doi: 10.3389/fvets.2023.1180622pubmed: 37152686google scholar: lookup
  3. 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
  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. Perera TRW, Skerrett-Byrne DA, Gibb Z, Nixon B, Swegen A. The Future of Biomarkers in Veterinary Medicine: Emerging Approaches and Associated Challenges.. Animals (Basel) 2022 Aug 26;12(17).
    doi: 10.3390/ani12172194pubmed: 36077913google 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. Morrell JM, Rocha A. A Novel Approach to Minimising Acute Equine Endometritis That May Help to Prevent the Development of the Chronic State.. Front Vet Sci 2021;8:799619.
    doi: 10.3389/fvets.2021.799619pubmed: 35071389google scholar: lookup
  8. Benammar A, Derisoud E, Vialard F, Palmer E, Ayoubi JM, Poulain M, Chavatte-Palmer P. The Mare: A Pertinent Model for Human Assisted Reproductive Technologies?. Animals (Basel) 2021 Aug 4;11(8).
    doi: 10.3390/ani11082304pubmed: 34438761google scholar: lookup