Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2024-0041
Animal Reproduction (AR)
Thematic Section: 37th Annual Meeting of the Brazilian Embryo Technology Society (SBTE)

Solutions to the fertility equation in beef embryo recipients

Mario Binelli; Cecilia Constantino Rocha; Alexandra Bennett; Abdul Waheed; Halima Sultana; Mariângela Bueno Cordeiro Maldonado; Fernando Silveira Mesquita

Downloads: 0
Views: 145

Abstract

In beef cattle operations that conduct embryo transfer, the overall success depends on the pregnancy outcome that results from every pregnancy opportunity. In this review, we dissected the main components that determine if a recipient will sustain the pregnancy after embryo transfer up to calving. Specifically, we describe the effect of the uterus on its ability to provide a receptive environment for embryo development. We then discuss the capacity of the embryo to thrive after transfer, and especially the contribution of the sire to embryo fitness. Finally, we review the interaction between the uterus and the embryo as an integrated unit that defines the pregnancy.

Keywords

cattle, embryo transfer, uterus, pregnancy

References

Batista EOS, Cardoso BO, Oliveira ML, Cuadros FDC, Mello BP, Sponchiado M, Monteiro BM, Pugliesi G, Binelli M. Supplemental progesterone induces temporal changes in luteal development and endometrial transcription in beef cattle. Domest Anim Endocrinol. 2019;68:126-34. http://doi.org/10.1016/j.domaniend.2019.02.001. PMid:31082784.

Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, Reichenbach HD, Blum H, Spencer TE, Wolf E. The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci USA. 2009;106(14):5681-6. http://doi.org/10.1073/pnas.0811841106. PMid:19307558.

Bazer FW, Burghardt RC, Johnson GA, Spencer TE, Wu G. Interferons and progesterone for establishment and maintenance of pregnancy: interactions among novel cell signaling pathways. Reprod Biol. 2008;8(3):179-211. http://doi.org/10.1016/S1642-431X(12)60012-6. PMid:19092983.

Binelli M, Scolari SC, Pugliesi G, Van Hoeck V, Gonella-Diaza AM, Andrade SC, Gasparin GR, Coutinho LL. The transcriptome signature of the receptive bovine uterus determined at early gestation. PLoS One. 2015;10(4):e0122874. http://doi.org/10.1371/journal.pone.0122874. PMid:25849079.

Binelli M, Silva FACC, Rocha CC, Martins T, Sponchiado M, van Hoeck V, Cordeiro A, Campbell M, Leroy JLMR, Peñagaricano F, Pugliesi G. Endometrial receptivity in cattle: the mutual reprogramming paradigm. Anim Reprod. 2022;19(4):e20220097. http://doi.org/10.1590/1984-3143-ar2022-0097. PMid:36570681.

Clemente M, de La Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, Roche JF, Rizos D, Lonergan P. Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction. 2009;138(3):507-17. http://doi.org/10.1530/REP-09-0152. PMid:19556439.

De Bem THC, Tinning H, Vasconcelos EJR, Wang D, Forde N. Endometrium on-a-chip reveals insulin- and glucose-induced alterations in the transcriptome and proteomic secretome. Endocrinology. 2021;162(6):bqab054. http://doi.org/10.1210/endocr/bqab054. PMid:33693651.

DeJarnette JM, Saacke RG, Bame J, Vogler CJ. Accessory sperm: their importance to fertility and embryo quality, and attempts to alter their numbers in artificially inseminated cattle. J Anim Sci. 1992;70(2):484-91. http://doi.org/10.2527/1992.702484x. PMid:1548211.

Eyestone WH, First NL. Variation in bovine embryo development in vitro due to bulls. Theriogenology. 1989;31(1):191. http://doi.org/10.1016/0093-691X(89)90599-2.

Fair S, Lonergan P. Review: understanding the causes of variation in reproductive wastage among bulls. Animal. 2018;12(s1):s53-62. http://doi.org/10.1017/S1751731118000964. PMid:29779500.

Fitzpatrick JL, Lüpold S. Sexual selection and the evolution of sperm quality. Mol Hum Reprod. 2014;20(12):1180-9. http://doi.org/10.1093/molehr/gau067. PMid:25323970.

Fitzpatrick JL, Willis C, Devigili A, Young A, Carroll M, Hunter HR, Brison DR. Chemical signals from eggs facilitate cryptic female choice in humans. Proc Biol Sci. 2020;287(1928):20200805. http://doi.org/10.1098/rspb.2020.0805. PMid:32517615.

Forde N, Carter F, Fair T, Crowe MA, Evans AC, Spencer TE, Bazer FW, McBride R, Boland MP, O’Gaora P, Lonergan P, Roche JF. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod. 2009;81(4):784-94. http://doi.org/10.1095/biolreprod.108.074336. PMid:19553605.

Forde N, Carter F, Spencer TE, Bazer FW, Sandra O, Mansouri-Attia N, Okumu LA, McGettigan PA, Mehta JP, McBride R, O’Gaora P, Roche JF, Lonergan P. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol Reprod. 2011;85(1):144-56. http://doi.org/10.1095/biolreprod.110.090019. PMid:21349821.

Forde N, Duffy GB, McGettigan PA, Browne JA, Mehta JP, Kelly AK, Mansouri-Attia N, Sandra O, Loftus BJ, Crowe MA, Fair T, Roche JF, Lonergan P, Evans AC. Evidence for an early endometrial response to pregnancy in cattle: both dependent upon and independent of interferon tau. Physiol Genomics. 2012;44(16):799-810. http://doi.org/10.1152/physiolgenomics.00067.2012. PMid:22759920.

Forde N, Simintiras CA, Sturmey R, Mamo S, Kelly AK, Spencer TE, Bazer FW, Lonergan P. Amino acids in the uterine luminal fluid reflects the temporal changes in transporter expression in the endometrium and conceptus during early pregnancy in cattle. PLoS One. 2014;9(6):e100010. http://doi.org/10.1371/journal.pone.0100010. PMid:24960174.

Franco G, Reese S, Poole R, Rhinehart J, Thompson K, Cooke R, Pohler K. Sire contribution to pregnancy loss in different periods of embryonic and fetal development of beef cows. Theriogenology. 2020;154:84-91. http://doi.org/10.1016/j.theriogenology.2020.05.021. PMid:32535394.

Franco GA. Sire contribution to pregnancy establishment and sire contribution to pregnancy establishment and maintenance in beef cows maintenance [dissertation]. Knoxville: University of Tennessee; 2018 [cited 2024 Mar 29]. Available from: https://trace.tennessee.edu/utk_gradthes.

Gray CA, Bartol FF, Tarleton BJ, Wiley AA, Johnson GA, Bazer FW, Spencer TE. Developmental biology of uterine glands. Biol Reprod. 2001;65(5):1311-23. http://doi.org/10.1095/biolreprod65.5.1311. PMid:11673245.

Greenstein JS, Murray RW, Foley RC. Observations on the morphogenesis and histochemistry of the bovine preattachment placenta between 16 and 33 days of gestation. Anat Rec. 1958;132(3):321-41. http://doi.org/10.1002/ar.1091320308. PMid:13637407.

Jokiniemi A, Magris M, Ritari J, Kuusipalo L, Lundgren T, Partanen J, Kekäläinen J. Post-copulatory genetic matchmaking: HLA-dependent effects of cervical mucus on human sperm function. Proc Biol Sci. 2020;287(1933):20201682. http://doi.org/10.1098/rspb.2020.1682. PMid:32811307.

Kekäläinen J, Evans JP. Gamete-mediated mate choice: towards a more inclusive view of sexual selection. Proc Biol Sci. 2018;285(1883):20180836. http://doi.org/10.1098/rspb.2018.0836. PMid:30051836.

Kekäläinen J. Genetic incompatibility of the reproductive partners: an evolutionary perspective on infertility. Hum Reprod. 2021;36(12):3028-35. http://doi.org/10.1093/humrep/deab221. PMid:34580729.

Ketchum JN, Perry GA, Quail LK, Epperson KM, Ogg MA, Zezeski AL, Rich JJJ, Zoca SM, Kline AC, Andrews TN, Ortega MS, Smith MF, Geary TW. Influence of preovulatory estradiol treatment on the maintenance of pregnancy in beef cattle receiving in vivo produced embryos. Anim Reprod Sci. 2023;255:107274. http://doi.org/10.1016/j.anireprosci.2023.107274. PMid:37320862.

Lacerda IP, Dode MA, Lima MM, Guerra BF, Costa ES, Moreira GR, de Oliveira Carvalho J. Cattle breed affects in vitro embryo production in a large-scale commercial program on dairy farms. Livest Sci. 2020;240:104135. http://doi.org/10.1016/j.livsci.2020.104135.

Madureira AML, Burnett TA, Marques JCS, Moore AL, Borchardt S, Heuwieser W, Guida TG, Vasconcelos JLM, Baes CF, Cerri RLA. Occurrence and greater intensity of estrus in recipient lactating dairy cows improve pregnancy per embryo transfer. J Dairy Sci. 2022;105(1):877-88. http://doi.org/10.3168/jds.2021-20437. PMid:34656349.

Mansouri-Attia N, Sandra O, Aubert J, Degrelle S, Everts RE, Giraud-Delville C, Heyman Y, Galio L, Hue I, Yang X, Tian XC, Lewin HA, Renard JP. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci USA. 2009;106(14):5687-92. http://doi.org/10.1073/pnas.0812722106. PMid:19297625.

Martins T, Sponchiado M, Ojeda-Rojas OA, Gonella-Diaza AM, Batista EOS, Cardoso BO, Rocha CC, Basso AC, Binelli M. Exacerbated conceptus signaling does not favor establishment of pregnancy in beef cattle. J Anim Sci Biotechnol. 2018;9(1):87. http://doi.org/10.1186/s40104-018-0302-9. PMid:30555692.

Martins T, Sponchiado M, Silva FACC, Estrada-Cortés E, Hansen PJ, Peñagaricano F, Binelli M. Progesterone-dependent and progesterone-independent modulation of luminal epithelial transcription to support pregnancy in cattle. Physiol Genomics. 2022;54(2):71-85. http://doi.org/10.1152/physiolgenomics.00108.2021. PMid:34890509.

Mathew DJ, Sánchez JM, Passaro C, Charpigny G, Behura SK, Spencer TE, Lonergan P. Interferon tau-dependent and independent effects of the bovine conceptus on the endometrial transcriptome†. Biol Reprod. 2019;100(2):365-80. http://doi.org/10.1093/biolre/ioy199. PMid:30203055.

Melo GD, Franco G, Ortega MS, Oliveira RV Fo, Bega A, Vasconcelos JLM, Cerri R, Pohler KG. PSIII-A-15 pregnancy associated glycoproteins effects on placenta function, uterine remodeling and attachment of bovine conceptuses. J Anim Sci. 2022;100(Suppl 3):297-8. http://doi.org/10.1093/jas/skac247.541.

Mesquita FS, Ramos RS, Pugliesi G, Andrade SC, Van Hoeck V, Langbeen A, Oliveira ML, Gonella-Diaza AM, Gasparin G, Fukumasu H, Pulz LH, Membrive CM, Coutinho LL, Binelli M. The Receptive Endometrial Transcriptomic Signature Indicates an Earlier Shift from Proliferation to Metabolism at Early Diestrus in the Cow. Biol Reprod. 2015;93(2):52. http://doi.org/10.1095/biolreprod.115.129031. PMid:26178716.

Moraes JGN, Behura SK, Geary TW, Hansen PJ, Neibergs HL, Spencer TE. Uterine influences on conceptus development in fertility-classified animals. Proc Natl Acad Sci USA. 2018;115(8):E1749-58. http://doi.org/10.1073/pnas.1721191115. PMid:29432175.

Morotti F, Sanches BV, Pontes JH, Basso AC, Siqueira ER, Lisboa LA, Seneda MM. Pregnancy rate and birth rate of calves from a large-scale IVF program using reverse-sorted semen in Bos indicus, Bos indicus-taurus, and Bos taurus cattle. Theriogenology. 2014;81(5):696-701. http://doi.org/10.1016/j.theriogenology.2013.12.002. PMid:24412681.

Northrop EJ, Rich JJJ, Cushman RA, McNeel AK, Soares ÉM, Brooks K, Spencer TE, Perry GA. Effects of preovulatory estradiol on uterine environment and conceptus survival from fertilization to maternal recognition of pregnancy. Biol Reprod. 2018;99(3):629-38. http://doi.org/10.1093/biolre/ioy086. PMid:29672673.

O’Callaghan E, Sánchez JM, McDonald M, Kelly AK, Hamdi M, Maicas C, Fair S, Kenny DA, Lonergan P. Sire contribution to fertilization failure and early embryo survival in cattle. J Dairy Sci. 2021;104(6):7262-71. http://doi.org/10.3168/jds.2020-19900. PMid:33714587.

Ortega MS, Moraes JGN, Patterson DJ, Smith MF, Behura SK, Poock S, Spencer TE. Influences of sire conception rate on pregnancy establishment in dairy cattle. Biol Reprod. 2018;99(6):1244-54. http://doi.org/10.1093/biolre/ioy141. PMid:29931362.

Passaro C, Tutt D, Mathew DJ, Sanchez JM, Browne JA, Boe-Hansen GB, Fair T, Lonergan P. Blastocyst-induced changes in the bovine endometrial transcriptome. Reproduction. 2018;156(3):219-29. http://doi.org/10.1530/REP-18-0188. PMid:30021913.

Penn DJ, Potts WK. The evolution of mating preferences and major histocompatibility complex genes. Am Nat. 1999;153(2):145-64. http://doi.org/10.1086/303166. PMid:29578757.

Pereira G, Guo Y, Silva E, Bevilacqua C, Charpigny G, Lopes-da-Costa L, Humblot P. Progesterone differentially affects the transcriptomic profiles of cow endometrial cell types. BMC Genomics. 2022;23(1):82. http://doi.org/10.1186/s12864-022-08323-z. PMid:35086476.

Pereira MHC, Wiltbank MC, Vasconcelos JLM. Expression of estrus improves fertility and decreases pregnancy losses in lactating dairy cows that receive artificial insemination or embryo transfer. J Dairy Sci. 2016;99(3):2237-47. http://doi.org/10.3168/jds.2015-9903. PMid:26723130.

Perry GA, Smith MF, Lucy MC, Green JA, Parks TE, MacNeil MD, Roberts AJ, Geary TW. Relationship between follicle size at insemination and pregnancy success. Proc Natl Acad Sci USA. 2005;102(14):5268-73. http://doi.org/10.1073/pnas.0501700102. PMid:15795381.

Perry GA, Smith MF, Roberts AJ, MacNeil MD, Geary TW. Relationship between size of the ovulatory follicle and pregnancy success in beef heifers. J Anim Sci. 2007;85(3):684-9. http://doi.org/10.2527/jas.2006-519. PMid:17060416.

Pohler KG, Geary TW, Johnson CL, Atkins JA, Jinks EM, Busch DC, Green JA, MacNeil MD, Smith MF. Circulating bovine pregnancy associated glycoproteins are associated with late embryonic/fetal survival but not ovulatory follicle size in suckled beef cows. J Anim Sci. 2013;91(9):4158-67. PMid:23825331.

Pugliesi G, Dalmaso de Melo G, Silva JB, Carvalhêdo AS, Lopes E, Siqueira E Fo, Silva LA, Binelli M. Use of color-Doppler ultrasonography for selection of recipients in timed-embryo transfer programs in beef cattle. Theriogenology. 2019;135:73-9. http://doi.org/10.1016/j.theriogenology.2019.06.006. PMid:31203090.

Pugliesi G, Melo GD, Ataíde GA Jr, Pellegrino CAG, Silva JB, Rocha CC, Motta IG, Vasconcelos JLM, Binelli M. Use of Doppler ultrasonography in embryo transfer programs: feasibility and field results. Anim Reprod. 2018;15(3):239-46. http://doi.org/10.21451/1984-3143-AR2018-0059. PMid:34178147.

Rabaglino MB, Kadarmideen HN. Machine learning approach to integrated endometrial transcriptomic datasets reveals biomarkers predicting uterine receptivity in cattle at seven days after estrous. Sci Rep. 2020;10(1):16981. http://doi.org/10.1038/s41598-020-72988-3. PMid:33046742.

Reese ST, Franco GA, Poole RK, Hood R, Fernadez Montero L, Oliveira RV Fo, Cooke RF, Pohler KG. Pregnancy loss in beef cattle: a meta-analysis. Anim Reprod Sci. 2020;212:106251. http://doi.org/10.1016/j.anireprosci.2019.106251. PMid:31864492.

Rizzo R, Fuzzi B, Stignani M, Criscuoli L, Melchiorri L, Dabizzi S, Campioni D, Lanza F, Marzola A, Branconi F, Noci I, Baricordi OR. Soluble HLA-G molecules in follicular fluid: a tool for oocyte selection in IVF? J Reprod Immunol. 2007;74(1-2):133-42. http://doi.org/10.1016/j.jri.2007.02.005. PMid:17399800.

Rocha CC, Martins T, Cardoso BO, Silva LA, Binelli M, Pugliesi G. Ultrasonography-accessed luteal size endpoint that most closely associates with circulating progesterone during the estrous cycle and early pregnancy in beef cows. Anim Reprod Sci. 2019;201:12-21. http://doi.org/10.1016/j.anireprosci.2018.12.003. PMid:30583812.

Rocha CC, Martins T, Silva FACC, Sponchiado M, Pohler KG, Binelli M. Viperin (RSAD2) gene expression in peripheral blood mononuclear cells of pregnant crossbred beef cows is altered by Bos indicus genetics. Theriogenology. 2023;209:226-33. http://doi.org/10.1016/j.theriogenology.2023.07.003. PMid:37437340.

Rocha CC, Silva FAC, Martins T, Marrero MG, Bromfield JJ, Driver J, Hansen T, Oliveira L, Binelli M. Culture of endometrial epithelial cells collected by a cytological brush in vivo. JDS Commun. 2022;3(3):217-21. http://doi.org/10.3168/jdsc.2021-0189. PMid:36338819.

Scott IC, Anson-Cartwright L, Riley P, Reda D, Cross JC. The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol Cell Biol. 2000;20(2):530-41. http://doi.org/10.1128/MCB.20.2.530-541.2000. PMid:10611232.

Selvaraju S, Ghosh J, Ravindra JP. Prognostic value of various spermatological attributes as predictors of zona binding and zona penetration of buffalo (Bubalus bubalis) semen. Reprod Domest Anim. 2009;44(1):6-11. http://doi.org/10.1111/j.1439-0531.2007.00979.x. PMid:18673329.

Sereshki N, Andalib A, Ghahiri A, Mehrabian F, Sherkat R, Rezaei A, Wilkinson D. The expression of human leukocyte antigen by human ejaculated spermatozoa. Mol Genet Genomic Med. 2019;7(12):e1005. http://doi.org/10.1002/mgg3.1005. PMid:31625276.

Silva FACC, Martins T, Sponchiado M, Rocha CC, Ashrafi N, Graham SF, Pohler KG, Peñagaricano F, Gonella-Diaza AM, Binelli M. Pre-estrus progesterone does not affect post-estrus luminal metabolome in cross-bred beef cows. Reproduction. 2023a;166(2):99-116. http://doi.org/10.1530/REP-22-0372. PMid:37224090.

Silva FACC, Martins T, Sponchiado M, Rocha CC, Pohler KG, Peñagaricano F, Binelli M. Hormonal profile prior to luteolysis modulates the uterine luminal transcriptome in the subsequent cycle in beef cross-bred cows†. Biol Reprod. 2023b;108(6):922-35. http://doi.org/10.1093/biolre/ioad035. PMid:36930057.

Silva FACC, Silva GF, Vieira BS, Laurindo A No, Rocha CC, Lo Turco EG, Nogueira GP, Pugliesi G, Binelli M. Peri-estrus ovarian, uterine, and hormonal variables determine the uterine luminal fluid metabolome in beef heifers. Biol Reprod. 2021;105(5):1140-53. http://doi.org/10.1093/biolre/ioab149. PMid:34350935.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. The influence of progesterone on bovine uterine fluid energy, nucleotide, vitamin, cofactor, peptide, and xenobiotic composition during the conceptus elongation-initiation window. Sci Rep. 2019a;9(1):7716. http://doi.org/10.1038/s41598-019-44040-6. PMid:31118434.

Simintiras CA, Sánchez JM, McDonald M, Martins T, Binelli M, Lonergan P. Biochemical characterization of progesterone-induced alterations in bovine uterine fluid amino acid and carbohydrate composition during the conceptus elongation window†. Biol Reprod. 2019b;100(3):672-85. PMid:30388203.

Siqueira AFP, de Castro LS, de Assis PM, Bicudo LC, Mendes CM, Nichi M, Visintin JA, Assumpção MEOD. Sperm traits on in vitro production (IVP) of bovine embryos: too much of anything is good for nothing. PLoS One. 2018;13(7):e0200273. http://doi.org/10.1371/journal.pone.0200273. PMid:29990330.

Song G, Bazer FW, Spencer TE. Pregnancy and interferon tau regulate RSAD2 and IFIH1 expression in the ovine uterus. Reproduction. 2007;133(1):285-95. http://doi.org/10.1530/REP-06-0092. PMid:17244754.

Souza AH, Silva EP, Cunha AP, Gümen A, Ayres H, Brusveen DJ, Guenther JN, Wiltbank MC. Ultrasonographic evaluation of endometrial thickness near timed AI as a predictor of fertility in high-producing dairy cows. Theriogenology. 2011;75(4):722-33. http://doi.org/10.1016/j.theriogenology.2010.10.013. PMid:21196031.

Spencer TE, Johnson GA, Burghardt RC, Bazer FW. Progesterone and placental hormone actions on the uterus: insights from domestic animals. Biol Reprod. 2004;71(1):2-10. http://doi.org/10.1095/biolreprod.103.024133. PMid:14973264.

Sponchiado M, Gomes NS, Fontes PK, Martins T, Del Collado M, Pastore AA, Pugliesi G, Nogueira MFG, Binelli M. Pre-hatching embryo-dependent and -independent programming of endometrial function in cattle. PLoS One. 2017;12(4):e0175954. http://doi.org/10.1371/journal.pone.0175954. PMid:28423001.

Sponchiado M, Gonella-Diaza AM, Rocha CC, Turco EGL, Pugliesi G, Leroy JLMR, Binelli M. The pre-hatching bovine embryo transforms the uterine luminal metabolite composition in vivo. Sci Rep. 2019;9(1):8354. http://doi.org/10.1038/s41598-019-44590-9. PMid:31175317.

Sponchiado M, Marei WFA, Beemster GTS, Bols PEJ, Binelli M, Leroy JLMR. Molecular interactions at the bovine embryo-endometrial epithelium interface. Reproduction. 2020;160(6):887-903. http://doi.org/10.1530/REP-20-0344. PMid:33112768.

Ward F, Rizos D, Corridan D, Quinn K, Boland M, Lonergan P. Paternal influence on the time of first embryonic cleavage post insemination and the implications for subsequent bovine embryo development in vitro and fertility in vivo. Mol Reprod Dev. 2001;60(1):47-55. http://doi.org/10.1002/mrd.1060. PMid:11550267.

Wooding FB. The synepitheliochorial placenta of ruminants: binucleate cell fusions and hormone production. Placenta. 1992;13(2):101-13. http://doi.org/10.1016/0143-4004(92)90025-O. PMid:1631024.

Zoca SM, Geary TW, Zezeski AL, Kerns KC, Dalton JC, Harstine BR, Utt MD, Cushman RA, Walker JA, Perry GA. Bull field fertility differences can be estimated with in vitro sperm capacitation and flow cytometry. Frontiers in Animal Science. 2023;4:1180975. http://doi.org/10.3389/fanim.2023.1180975.
 


Submitted date:
03/29/2024

Accepted date:
06/07/2024

66b4b27da95395065a4d4ea2 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections