What has embryo recovery and transfer taught us about equine reproductive physiology?
Keywords:
Fetomaternal interactions, nonsurgical embryo transfer, surgical embryo transfer
Abstract
Equine embryo transfer has been the foundation stone on which modern reproductive technologies and novel research in this species has been built. Nonsurgical embryo recovery and transfer methods developed from the original surgical methods, and the ease with which these procedures can be undertaken has enabled these techniques to play a continuing role in original research. We document how embryo recovery and/or transfer have increased our knowledge about many of the events involved in equine reproductive physiology. These include, when the equine embryo enters the uterus, the importance and development of the blastocyst capsule, secretory products of early embryos, early maternal-embryo interactions, effects of uterine asynchrony on early embryo development, the role of endometrial cups and maternal immunological tolerance of extraspecies embryo transfers, and the influence of uterine environmental on fetal growth and development.
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References
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2. Kraemer DC: A history of equine embryo transfer and related technologies. J Equine Vet Sci 2013;33:305-308. doi: 10.1016/j.jevs.2013.03.007
3. Allen WR, Wilsher S: Historic aspect of equine embryo transfer. J Equine Vet Sci 2020;89:10298. doi: 10.1016/j.jevs.2020.102987
4. Stout TAE, Griffiths H: Clinical insights: assisted reproductive techniques: more than a solution to subfertility. Equine Vet J 2021;53:1084-1087. doi: 10.1111/evj.13510
5. Oguri N, Tsutsumi Y: Non-surgical recovery of equine eggs and an attempt at non-surgical egg transfer in horses. J Reprod Fertil 1972;31:187-198. doi: 10.1530/jrf.0.0310187
6. Betteridge KJ, Eaglesome MD, Mitchell D, et al: Development of horse embryos up to twenty-two days after ovulation: observations on fresh specimens. J Anat 1982;135:191-209.
7. Chevalier F, Palmer E: Ultrasonic echography in the mare. J Reprod Fertil 1982;32:423-430.
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9. Battut I, Colchen S, Fieni F, et al: Success rate when attempting to non-surgically collect equine embryos at 144, 156 and 168 hours after ovulation. Equine Vet J 1997;25:60-62. doi: 10.1111/j.2042-3306.1997.tb05102.x
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11. Battut I, Grandchamp des Raux A, Nicaise JL, et al: When do equine embryos enter the uterine cavity: an attempt to answer? Havemeyer Monograph 3: Proc 5th Int Symp Equine Embryo Transfer 2000;66-68.
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16. Stout TAE, Meadows S, Allen WR: Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo. Anim Reprod Sci 2005;87:269-281. doi: 10.1016/j.anireprosci.2004.11.009
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32. Stout TAE, Allen WR: Role of prostaglandins in intrauterine migration of the equine conceptus. Reproduction 2001;121:771-775. doi: 10.1530/rep.0.1210771
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36. Budik S, Nöbauer K, Razzazi-Fazeli E, et al: 2012 Analysis of the proteins and peptides isolated from incubation medium of early equine conceptuses - preliminary results. J Equine Vet Sci 2012;32:400. doi: 10.1016/j.jevs.2012.05.014
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41. Swegen A, Grupen CG, Gibb Z, et al: From peptide masses to pregnancy maintenance: a comprehensive proteomic analysis of the early equine embryo secretome, blastocoel fluid and capsule. Proteomics 2017;17:1600433. doi: 10.1002/pmic.201600433
42. Gibson C, de Ruijter-Villani M, Rietveld J, et al: Expression of glucose transporters in the endometrium and early conceptus membranes of the horse. Placenta 2018;68:23-32. doi: 10.1016/j.placenta.2018.06.308
43. Gibson C, de Ruijter-Villani M, Rietveld J, et al: Amino acid transporter expression in the endometrium and conceptus membranes during early equine pregnancy. Reprod Fertil Dev 2018;30:1675-1688. doi: 10.1071/RD17352
44. Smits K, Willems S, van Steendam K, et al: Proteins involved in embryo-maternal interaction around the signalling of maternal recognition of pregnancy in the horse. Sci Rep 2018;8:5249.
45. Derisoud E, Jouneau L, Dubois C, et al: Maternal age affects equine day 8 embryo gene expression both in trophoblast and inner cell mass. BMC Genomics 2022;23:443. doi: 10.1186/s12864-022-08593-7
46. Vegas AR, Podico G, Canisso IF, et al: Dynamic regulation of the transcriptome and proteome of the equine embryo during maternal recognition of pregnancy. FASEB Bioadv 2022;4:775-797. doi: 10.1096/fba.2022-00063
47. Allen WR, Rowson LEA: Surgical and non-surgical egg transfer in horses. J Reprod Fertil 1975;23:525-532.
48. Ball BA, Little TV, Weber JA, et al: Survival of day-4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J Reprod Fertil 1989;85:187-194.
49. Wilsher S, Allen WR: Uterine influences on embryogenesis and early placentation in the horse revealed by transfer of day-10 embryos to day-3 recipient mares. Reproduction 2009;137:583-593. doi: 10.1530/REP-08-0328
50. Wilsher S, Clutton-Brock A, Allen WR: Successful transfer of day-10 equine embryos: influence of donor-recipient asynchrony on embryo development. Reproduction 2010;139:575-585. doi: 10.1530/REP-09-0306
51. Gibson C, de Ruijter-Villani M, Bauersachs S, et al: Asynchronous embryo transfer followed by comparative analysis of conceptus membranes and endometrium identifies processes important to the establishment of equine pregnancy. Int J Mol Sci 2020;21:2562. doi: 10.3390/ijms21072562
52. Gibson C, de Ruijter-Villani M, Stout TAE: Negative asynchrony retards early conceptus development and upregulation of placental imprinted genes. Placenta 2017;57:175-182. doi: 10.1016/j.placenta.2017.07.007
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2. Kraemer DC: A history of equine embryo transfer and related technologies. J Equine Vet Sci 2013;33:305-308. doi: 10.1016/j.jevs.2013.03.007
3. Allen WR, Wilsher S: Historic aspect of equine embryo transfer. J Equine Vet Sci 2020;89:10298. doi: 10.1016/j.jevs.2020.102987
4. Stout TAE, Griffiths H: Clinical insights: assisted reproductive techniques: more than a solution to subfertility. Equine Vet J 2021;53:1084-1087. doi: 10.1111/evj.13510
5. Oguri N, Tsutsumi Y: Non-surgical recovery of equine eggs and an attempt at non-surgical egg transfer in horses. J Reprod Fertil 1972;31:187-198. doi: 10.1530/jrf.0.0310187
6. Betteridge KJ, Eaglesome MD, Mitchell D, et al: Development of horse embryos up to twenty-two days after ovulation: observations on fresh specimens. J Anat 1982;135:191-209.
7. Chevalier F, Palmer E: Ultrasonic echography in the mare. J Reprod Fertil 1982;32:423-430.
8. Simpson DJ, Greenwood RES, Ricketts SW, et al: Use of ultrasound echography for early diagnosis of single and twin pregnancy in the mare. J Reprod Fertil 1982;32:431-439.
9. Battut I, Colchen S, Fieni F, et al: Success rate when attempting to non-surgically collect equine embryos at 144, 156 and 168 hours after ovulation. Equine Vet J 1997;25:60-62. doi: 10.1111/j.2042-3306.1997.tb05102.x
10. Colchen S, Battut I, Fieni F, et al: Quantitative histological analysis of equine embryos at exactly 156 and 168 h after ovulation. J Reprod Fertil 2000;56:527-537.
11. Battut I, Grandchamp des Raux A, Nicaise JL, et al: When do equine embryos enter the uterine cavity: an attempt to answer? Havemeyer Monograph 3: Proc 5th Int Symp Equine Embryo Transfer 2000;66-68.
12. Couto GR, Vigano DWA, dos Santos GD, et al: Embryo recovery on consecutive days from Day 6.5 to obtain small embryos for vitrification: is it effective? J Equine Vet Sci 2023;125:104643. doi: 10.1016/j.jevs.2023.104643
13. Lascombes FA, Pashen RL: Results from embryo freezing and post ovulation breeding in a commercial embryo transfer programme. Proc 5th Int Symp Equine Embryo Transfer Havemeyer Foundation Monograph Series No. 3;2000:95-96.
14. Eldridge-Panuska WD, di Brienza VC, Seidel GE Jr, et al: Establishment of pregnancies after serial dilution or direct transfer by vitrified equine embryos. Theriogenology 2005;63:1308-1319. doi: 10.1016/j.theriogenology.2004.06.015
15. Betteridge KJ: Comparative aspects of equine embryonic development. Anim Reprod Sci 2000;60-61:691-702. doi: 10.1016/S0378-4320(00)00075-0
16. Stout TAE, Meadows S, Allen WR: Stage-specific formation of the equine blastocyst capsule is instrumental to hatching and to embryonic survival in vivo. Anim Reprod Sci 2005;87:269-281. doi: 10.1016/j.anireprosci.2004.11.009
17. Oriol JG, Betteridge KJ, Clarke AJ, et al: Mucin-like glycoproteins in the equine embryonic capsule. Mol Reprod Dev 1993;34:255-265. doi: 10.1002/mrd.1080340305
18. Oriol JG, Sharom FJ, Betteridge KJ: Developmentally regulated changes of the equine embryonic capsule. J Reprod Fertil 1993;99:653-664. doi: 10.1530/jrf.0.0990653
19. Tremoleda JL, Stout TAE, Lagutina I, et al: Effects of in vitro production on horse embryo morphology, cytoskeletal characteristics, and blastocyst capsule formation. Biol Reprod 2003;69:1895-1906. doi: 10.1095/biolreprod.103.018515
20. Kovascy S, Allen WR, Wilsher S: The mystery of the capsular vesicles: preliminary studies. 10th Int Symp Equine Embryo Transfer. J Equine Vet Sci 2022;113:103978. doi: 10.1016/j.jevs.2022.103978
21. Wilsher S, Kovacsy S, A Ismer A, et al: The mystery of the capsular vesicles: preliminary studies. Proc 13th Int Symp Equine Reprod J Equine Vet Sci 2023;125:226. doi: 10.1016/j.jevs.2023.104796
22. Albihn A, Waelchli RO, Samper J, et al: Production of capsular material by equine trophoblast transplanted into immunodeficient mice. Reproduction 2003;125:855-863. doi: 10.1530/rep.0.1250855
23. Flood PF, Betteridge KJ, lrvine DS: Oestrogens and androgens in blastocoelic fluid and cultures of cells from equine conceptuses of 10-22 days gestation. J Reprod Fertil 1979;27:414-420.
24. Heap RB, Hamon MH, Allen WR: Oestrogen production by the preimplantation donkey conceptus compared with that of the horse and the effect of between-species embryo transfer. J Reprod Fertil 1991;93:141-147. doi: 10.1530/jrf.0.0930141
25. Goff AK, Leduc S, Poitras P, et al: Steroid synthesis by equine conceptuses between days 7 and 14 and endometrial steroid metabolism. Dom Anim Endocrin 1993;10:229-236. doi: 10.1016/0739-7240(93)90027-9
26. Marsan C, Goff AK, Sirois J, et al: Steroid secretion by different cell types of the horse conceptus. J Reprod Fertil 1987;35:363-369.
27. Rambags BPB, van Tol HTA, van den Eng MM, et al: Expression of progesterone and oestrogen receptors by early intrauterine equine conceptuses. Theriogenology 2008;69:366-375. doi: 10.1016/j.theriogenology.2007.10.011
28. Watson ED, Sertich PL: Prostaglandin production by horse embryos and the effect of co-culture of embryos with endometrium from pregnant mares J Reprod Fertil 1989;87:331-336.
29. Weber JA, Woods GL, Freeman DA, et al: Prostaglandin E2 secretion by day 6 to day 9 equine embryos. Prostaglandins 1992;43:55-59. doi: 10.1016/0090-6980(92)90064-Z
30. Vanderwall DJ, Woods GL, Weber JA, et al: PGE2 secretion by the conceptus and binding by non-pregnant endometrium in the horse. Equine Vet J 1993;15:24-27. doi: 10.1111/j.2042-3306.1993.tb04818.x
31. Stout TAE, Allen WR: Prostaglandin E2 and F2a production by equine conceptuses and concentrations in conceptus fluids and uterine flushings recovered from early pregnant and dioestrous mares. Reproduction 2002;123:261-268. doi: 10.1530/rep.0.1230261
32. Stout TAE, Allen WR: Role of prostaglandins in intrauterine migration of the equine conceptus. Reproduction 2001;121:771-775. doi: 10.1530/rep.0.1210771
33. McDowell KJ, Sharp DC, Fazleabas AT, et al: Two-dimensional polyacrylamide gel electrophoresis of proteins synthesized and released by conceptuses and endometria from pony mares. J Reprod Fertil 1990;89:107-115. doi: 10.1530/jrf.0.0890107
34. Stewart F, Charleston B, Crossett B, et al: A novel uterine protein associated with the embryonic capsule in equids. J Reprod Fertil 1995;105:65-70. doi: 10.1530/jrf.0.1050065
35. Herrler A, Pell JM, Allen WR, et al: Horse conceptuses secrete insulin-like growth factor-binding protein 3. Biol Reprod 2000;62:1804-1811. doi: 10.1095/biolreprod62.6.1804
36. Budik S, Nöbauer K, Razzazi-Fazeli E, et al: 2012 Analysis of the proteins and peptides isolated from incubation medium of early equine conceptuses - preliminary results. J Equine Vet Sci 2012;32:400. doi: 10.1016/j.jevs.2012.05.014
37. Klein C, Troedsson MHT: Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse. Biol Reprod 2011;84:872-885. doi: 10.1095/biolreprod.110.088732
38. Beckelmann J, Budik S, Bartel C, et al: Evaluation of Xist expression in preattachment equine embryos. Theriogenology 2012;78:1429-1436.
39. de Ruijter-Villani M, van Boxtel PR, Stout TA: Fibroblast growth factor-2 expression in the preimplantation equine conceptus and endometrium of pregnant and cyclic mares. Theriogenology 2013;80:979-989. doi: 10.1016/j.theriogenology.2013.07.024
40. de Ruijter-Villani M, Deelen C, Stout TA: Expression of leukaemia inhibitory factor at the conceptus-maternal interface during preimplantation development and in the endometrium during the oestrous cycle in the mare. Reprod Fertil Dev 2015;28:1642-1651. doi: 10.1071/RD14334
41. Swegen A, Grupen CG, Gibb Z, et al: From peptide masses to pregnancy maintenance: a comprehensive proteomic analysis of the early equine embryo secretome, blastocoel fluid and capsule. Proteomics 2017;17:1600433. doi: 10.1002/pmic.201600433
42. Gibson C, de Ruijter-Villani M, Rietveld J, et al: Expression of glucose transporters in the endometrium and early conceptus membranes of the horse. Placenta 2018;68:23-32. doi: 10.1016/j.placenta.2018.06.308
43. Gibson C, de Ruijter-Villani M, Rietveld J, et al: Amino acid transporter expression in the endometrium and conceptus membranes during early equine pregnancy. Reprod Fertil Dev 2018;30:1675-1688. doi: 10.1071/RD17352
44. Smits K, Willems S, van Steendam K, et al: Proteins involved in embryo-maternal interaction around the signalling of maternal recognition of pregnancy in the horse. Sci Rep 2018;8:5249.
45. Derisoud E, Jouneau L, Dubois C, et al: Maternal age affects equine day 8 embryo gene expression both in trophoblast and inner cell mass. BMC Genomics 2022;23:443. doi: 10.1186/s12864-022-08593-7
46. Vegas AR, Podico G, Canisso IF, et al: Dynamic regulation of the transcriptome and proteome of the equine embryo during maternal recognition of pregnancy. FASEB Bioadv 2022;4:775-797. doi: 10.1096/fba.2022-00063
47. Allen WR, Rowson LEA: Surgical and non-surgical egg transfer in horses. J Reprod Fertil 1975;23:525-532.
48. Ball BA, Little TV, Weber JA, et al: Survival of day-4 embryos from young, normal mares and aged, subfertile mares after transfer to normal recipient mares. J Reprod Fertil 1989;85:187-194.
49. Wilsher S, Allen WR: Uterine influences on embryogenesis and early placentation in the horse revealed by transfer of day-10 embryos to day-3 recipient mares. Reproduction 2009;137:583-593. doi: 10.1530/REP-08-0328
50. Wilsher S, Clutton-Brock A, Allen WR: Successful transfer of day-10 equine embryos: influence of donor-recipient asynchrony on embryo development. Reproduction 2010;139:575-585. doi: 10.1530/REP-09-0306
51. Gibson C, de Ruijter-Villani M, Bauersachs S, et al: Asynchronous embryo transfer followed by comparative analysis of conceptus membranes and endometrium identifies processes important to the establishment of equine pregnancy. Int J Mol Sci 2020;21:2562. doi: 10.3390/ijms21072562
52. Gibson C, de Ruijter-Villani M, Stout TAE: Negative asynchrony retards early conceptus development and upregulation of placental imprinted genes. Placenta 2017;57:175-182. doi: 10.1016/j.placenta.2017.07.007
53. Ginther OJ: Fixation and orientation of the early equine conceptus. Theriogenology 1983;19:613-623.
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Published
2024-07-22
How to Cite
Wilsher S., & Hoogewijs M. (2024). What has embryo recovery and transfer taught us about equine reproductive physiology?. Clinical Theriogenology, 16. https://doi.org/10.58292/CT.v16.10602
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Review Reports
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