Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2020-0006
Animal Reproduction (AR)
Original Article

Histomorphometric and vascular changes in equine endometrium after the infusion of conceptus fragments

Cesar Augusto Camacho; Maria José Estradé; Nicolás Cazales; Jorge Emilio Caballeros; Sandra Mara Fiala-Rechsteiner; Adriana Pires Neves; Rodrigo Costa Mattos

Downloads: 0
Views: 790

Abstract

Abstract: This experiment aimed to verify if the proteins present in a 13th day conceptus induce changes in the equine endometrial ultra-structure, histology, and vascularization, two days after its infusion. Ten healthy cyclic mares were used. Once estrus was confirmed, mares were examined daily to detect ovulation (day 0). After ovulation, mares were examined daily until day seven by transrectal palpation and B-mode and Doppler ultrasonography. In this first cycle, intrauterine biopsies were collected at day seven after ovulation, constituting the Cyclic group (n = 10). In the second cycle, the same mares daily were examined until ovulation was detected. After ovulation, mares were examined daily by transrectal palpation and B-mode and Doppler ultrasonography until day 7. On day 5, after ovulation, fragments from previously collected 13-day-old concepti were infused into the uterus of each mare. Intrauterine biopsies were collected at day 7 in all mares (n = 10), constituting the Fragment group. The percentage of ciliated and flattened cells decreased in the Fragment group. Protruded cells, superficial and intraglandular secretion, glandular lumen and diameter, blood vessel diameter, endometrial vascularization, and immune cells were higher in the Fragment group than in the Cyclic group. In summary, proteins of 13th day equine conceptus fragments infused at day five after ovulation signaled histological and vascular changes in the endometrium at the 7th day after ovulation.

Keywords

ultrastructure, histological, vascularization, uterus

References

Aurich C, Budik S. Early pregnancy in the horse revisited: does exception prove the rule? J Anim Sci Biotechnol. 2015;6(1):50. http://dx.doi.org/10.1186/s40104-015-0048-6. PMid:26635959.

Ball B, Altschul M, Hillman R. Luteal maintenance in mares after transfer of equine trophoblastic vesicles. Equine Vet J. 1989;21(S8):21-4. http://dx.doi.org/10.1111/j.2042-3306.1989.tb04667.x.

Bastos HBA, Martinez MN, Camozzato GC, Estradé MJ, Barros E, Vital CE, Vidigal PMP, Meikle A, Jobim MIM, Gregory RM, Mattos RC. Proteomic profile of histotroph during early embryo development in mares. Theriogenology. 2019;125:224-35. http://dx.doi.org/10.1016/j.theriogenology.2018.11.002. PMid:30472502.

Bazer FW, Roberts RM, Thatcher WW. Actions of hormones on the uterus and effect on conceptus development. J Anim Sci. 1979;49(Suppl 2):35-45. http://dx.doi.org/10.1093/ansci/49.Supplement_II.35. PMid:400776.

Bazer FW, Vallet JL, Roberts RM, Sharp DC, Thatcher WW. Role of conceptus secretory products in establishment of pregnancy. J Reprod Fertil. 1986;76(2):841-50. http://dx.doi.org/10.1530/jrf.0.0760841. PMid:3517318.

Bollwein H, Maierl J, Mayer R, Stolla R. Transrectal color doppler sonography of the A. uterina in cyclic mares. Theriogenology. 1998;49(8):1483-8. http://dx.doi.org/10.1016/S0093-691X(98)00094-6. PMid:10732012.

Bollwein H, Mayer R, Stolla R. Transrectal Doppler sonography of uterine blood flow during early pregnancy in mares. Theriogenology. 2003;60(4):597-605. http://dx.doi.org/10.1016/S0093-691X(03)00080-3. PMid:12832010.

Brady HA, Burghardt RC, Evans JW, Blanchard TL, Vamer DD, Bruemmer JE. Model system for the study of uterine/trophoblast interactions in the mare. J Equine Vet Sci. 1993;13(9):506-11. http://dx.doi.org/10.1016/S0737-0806(07)80265-6.

Caballeros JE, Camacho C, Cazales N, Estradé MJ, Fiala-Rechsteiner S, Jobim MIM, Mattos RC. Ultrastructural and histological characteristics of the equine endometrium at day 5 post ovulation. Theriogenology. 2019;132:106-12. http://dx.doi.org/10.1016/j.theriogenology.2019.04.006. PMid:31004876.

Camous S, Heyman Y, Méziou W, Ménézo Y. Cleavage beyond the block stage and survival after transfer of early bovine embryos cultured with trophoblastic vesicles. J Reprod Fertil. 1984;72(2):479-85. http://dx.doi.org/10.1530/jrf.0.0720479. PMid:6512770.

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;123:1-10. http://dx.doi.org/10.1016/j.theriogenology.2018.09.018. PMid:30253251.

Cuervo-Arango J, Claes AN, Stout TA. Effect of embryo transfer technique on the likelihood of pregnancy in the mare: a comparison of conventional and Wilsher’s forceps-assisted transfer. Vet Rec. 2018;183(10):323. http://dx.doi.org/10.1136/vr.104808. PMid:29798842.

Das SK. Cell cycle regulatory control for uterine stromal cell decidualization in implantation. Reproduction. 2009;137(6):889-99. http://dx.doi.org/10.1530/REP-08-0539. PMid:19307426.

Fahy GM, Wowk B. Cryopreservation and freeze-drying protocols. New York: Springer; 2015; p. 21-82. Chapter 2, Principles of cryopreservation by vitrification. http://dx.doi.org/10.1007/978-1-4939-2193-5_2.

Garber Cohen IP, Castello PR, Flecha FLG. Ice-induced partial unfolding and aggregation of an integral membrane protein. Biochim Biophys Acta. 2010;1798(11):2040-7. http://dx.doi.org/10.1016/j.bbamem.2010.07.035. PMid:20691147.

Ginther OJ. Ultrasonic imaging and animal reproduction: book 4, color-Doppler ultrasonography. Cross Plains, WI: Equiservices Publishing; 2007. 258 p.

Heyman Y, Chesné P, Chupin D, Ménézo Y. Improvement of survival rate of frozen cattle blastocysts after transfer with trophoblastic vesicles. Theriogenology. 1987;27(3):477-84. http://dx.doi.org/10.1016/0093-691X(87)90235-4. PMid:16726252.

Keenan LR, Forde D, McGeady T, Wade J, Roche JF. Endometrial histology of early pregnant and non-pregnant mares. J Reprod Fertil Suppl. 1987;35:499-504. http://dx.doi.org/10.1063/1.857816. PMid:3479603.

Kenney RM, Doig PA. Equine endometrial biopsy. In: Morrow DA, editor. Current therapy in theriogenology. Philadelphia: W.B. Saunders; 1986. p. 723-9.

Klein C, Troedsson MHT. Maternal recognition of pregnancy in the horse: a mystery still to be solved. Reprod Fertil Dev. 2011a;23(8):952-63. http://dx.doi.org/10.1071/RD10294. PMid:22127001.

Klein C, Troedsson MHT. Transcriptional profiling of equine conceptuses reveals new aspects of embryo-maternal communication in the horse. Biol Reprod. 2011b;84(5):872-85. http://dx.doi.org/10.1095/biolreprod.110.088732. PMid:21209420.

Klein C. Early pregnancy in the mare: old concepts revisited. Domest Anim Endocrinol. 2016;56(Suppl):S212-7. http://dx.doi.org/10.1016/j.domaniend.2016.03.006. PMid:27345319.

Malschitzky E, Schilela A, Meirelles LS, Gelpi Mattos AL, Gregory RM, Mattos RC. Artificial photoperiod in pregnant mares and its effect on pregnancy length and postpartum reproductive performance. Pferdeheilkunde. 2001;17(6):565-9. http://dx.doi.org/10.21836/PEM20010605.

Martínez Pereira MN. Preñez temprana en la yegua: cambios histomorfológicos e inflamatorios endometriales y de hormonas circulantes desde la ovulación hasta los 13 días [thesis]. Montevideo: Universidad de la República; 2016.

McDowell KJ, Sharp DC, Fazleabas AT, Roberts RM. Two-dimensional polyacrylamide gel electrophoresis of proteins synthesized and released by conceptuses and endometria from pony mares. J Reprod Fertil. 1990;89(1):107-15. http://dx.doi.org/10.1530/jrf.0.0890107. PMid:2374112.

Merkl M, Ulbrich SE, Otzdorff C, Herbach N, Wanke R, Wolf E, Handler J, Bauersachs S. Microarray analysis of equine endometrium at days 8 and 12 of pregnancy. Biol Reprod. 2010;83(5):874-86. http://dx.doi.org/10.1095/biolreprod.110.085233. PMid:20631402.

Nadkarni S, Smith J, Sferruzzi-Perri AN, Ledwozyw A, Kishore M, Haas R, Mauro C, Williams DJ, Farsky SH, Marelli-Berg FM, Perretti M. Neutrophils induce proangiogenic T cells with a regulatory phenotype in pregnancy. Proc Natl Acad Sci USA. 2016;113(52):E8415-24. http://dx.doi.org/10.1073/pnas.1611944114. PMid:27956610.

Nie GJ, Johnson KE, Braden TD, Wenzel JGW. Use of an intra-uterine glass ball protocol to extend luteal function in mares. J Equine Vet Sci. 2003;23(6):266-73. http://dx.doi.org/10.1053/jevs.2003.75.

Nieto-Olmedo P, Tapia JA, Peña FJ, Ferrusola CO. The use of power mode doppler ultrasonography as a predictive tool of early pregnancy in the mare. J Equine Vet Sci. 2018;66:218-9. http://dx.doi.org/10.1016/j.jevs.2018.05.106.

Pearson H. Reproductive immunology: immunity’s pregnant pause. Nature. 2002;420(6913):265-6. http://dx.doi.org/10.1038/420265a. PMid:12447413.

Ricketts SW, Rossdale PD, Samuel CA. Endometrial Biopsy Studies of Mares with Contagious Equine Metritis. Equine Vet J. 1978;10(3):160-6. http://dx.doi.org/10.1111/j.2042-3306.1978.tb02247.x. PMid:688997.

Rivera del Alamo MM, Reilas T, Kindahl H, Katila T. Mechanisms behind intrauterine device-induced luteal persistence in mares. Anim Reprod Sci. 2008;107(1-2):94-106. http://dx.doi.org/10.1016/j.anireprosci.2007.06.010. PMid:17643876.

Rowson LE, Moor RM. The influence of embryonic tissue homogenate infused into the uterus, on the life-span of the corpus luteum in the sheep. J Reprod Fertil. 1967;13(3):511-6. http://dx.doi.org/10.1530/jrf.0.0130511. PMid:6067575.

Samuel CA, Ricketts SW, Rossdale PD, Steven DH, Thurley KW. Scanning electron microscope studies of the endometrium of cyclic mare. J Reprod Fertil Suppl. 1979;27(27):287-92. PMid:289802.

Sharp D, McDowell K, Weithenauer J, Thatcher W. The continuum of events leading to maternal recognition of pregnancy in mares. J Reprod Fertil Suppl. 1989;37(37):101-7. PMid:2810225.

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;72(3):755-61. http://dx.doi.org/10.1095/biolreprod.104.036384. PMid:15576822.

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;142(4):593-603. http://dx.doi.org/10.1530/REP-11-0149. PMid:21757474.

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;8(1):5249. http://dx.doi.org/10.1038/s41598-018-23537-6. PMid:29588480.

Tayade C, Fang Y, Hilchie D, Croy BA. Lymphocyte contributions to altered endometrial angiogenesis during early and midgestation fetal loss. J Leukoc Biol. 2007;82(4):877-86. http://dx.doi.org/10.1189/jlb.0507330. PMid:17634279.

Tolosa E, Rodrigues C, Brehmer A, Freitas-Neto A. Manual de técnicas para histologia normal e patológica. São Paulo: Manole; 2003.

Waclawik A, Kaczmarek MM, Blitek A, Kaczynski P, Ziecik AJ. Embryo-maternal dialogue during pregnancy establishment and implantation in the pig. Mol Reprod Dev. 2017;84(9):842-55. http://dx.doi.org/10.1002/mrd.22835. PMid:28628266.

Waclawik A. Novel insights into the mechanisms of pregnancy establishment: regulation of prostaglandin synthesis and signaling in the pig. Reproduction. 2011;142(3):389-99. http://dx.doi.org/10.1530/REP-11-0033. PMid:21677026.

Wilsher S, Gower S, Allen WRT. Immunohistochemical localisation of progesterone and oestrogen receptors at the placental interface in mares during early pregnancy. Anim Reprod Sci. 2011;129(3-4):200-8. http://dx.doi.org/10.1016/j.anireprosci.2011.11.004. PMid:22176887.
 

5f04746b0e88256c1ebb8295 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections