Animal Reproduction (AR)
https://www.animal-reproduction.org/article/doi/10.21451/1984-3143-AR2019-0075
Animal Reproduction (AR)
Congress Paper

Aspects of embryo-maternal communication in establishment of pregnancy in cattle

José M. Sánchez, Constantine A. Simintiras, Patrick Lonergan

Downloads: 0
Views: 20

Abstract

Establishment of pregnancy in mammals requires reciprocal molecular communication between the conceptus and endometrium that modifies the endometrial transcriptome and uterine luminal milieu to support pregnancy. Due to the small size of the early embryo and elongating conceptus relative to the volume of the uterine lumen, collection of endometrium adjacent to the developing conceptus is difficult following conventional uterine flushing methods in cattle. Use of endometrial explants in culture can overcome this challenge and reveal information about the dialogue between the developing embryo and the uterus. The aim of this short review is to summarize some of our recent findings in relation to embryo maternal interaction during bovine pregnancy establishment and to put them in the wider context of fertility in cattle.

Keywords

conceptus, fertility, bovine, uterus, progesterone.

References

Ashworth CJ, Sales DI, Wilmut I. 1989. Evidence of an association between the survival of embryos and the periovulatory plasma progesterone concentration in the ewe. J Reprod Fertil, 87:23-32.

Barnwell CV, Farin PW, Ashwell CM, Farmer WT, Galphin SP, Farin CE. 2016. Differences in mRNA populations of short and long bovine conceptuses on Day 15 of gestation. Mol Reprod Dev, 83:424-441.

Bartol FF, Roberts RM, Bazer FW, Lewis GS, Godkin JD, Thatcher WW. 1985. Characterization of proteins produced in vitro by periattachment bovine conceptuses. Biol Reprod, 32:681-693.

Bauersachs S, Ulbrich SE, Zakhartchenko V, Minten M, Reichenbach M, Reichenbach H-D, Blum H, Spencer TE, Wolf E. 2009. The endometrium responds differently to cloned versus fertilized embryos. Proc Natl Acad Sci USA, 106:5681-5686.

Bauersachs S, Ulbrich SE, Reichenbach HD, Reichenbach M, Büttner M, Meyer HH, Spencer TE, Minten M, Sax G, Winter G, Wolf E. 2012. Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. Biol Reprod, 29:86(2):46. Doi: 10.1095/biolreprod.111.094771.

Bagés-Arnal S, Sánchez JM, Fernández-Fuertes B, McDonald M, Behura SK, Spencer TE, Fair T, Lonergan P. 2019. Differential response of bovine endometrium ipsilateral and contralateral to the corpus luteum to a Day 14 conceptus. Annual Meeting of the Society for the Study of Reproduction, San Jose, CA, USA, July 2019.

Bazer FW, Wang X, Johnson GA, Wu G. 2015. Select nutrients and their effects on conceptus development in mammals. Anim Nutr, 1(3):85-95. Doi: 10.1016/j.aninu.2015.07.005.

Bazer FW, Thatcher WW. 2017. Chronicling the discovery of interferon tau. Reproduction, 154:F11-F20.

Brandão DO, Maddox-Hyttel P, Løvendahl P, Rumpf R, Stringfellow D, Callesen H. 2004. Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biol Reprod, 71:2048-2055.

Betteridge K, Eaglesome M, Randall GCB, Mitchell D. 1980. Collection, description and transfer of embryos from cattle 10-16 days after oestrus. J Reprod Fertil, 59:205-216.

Borges AM, Healey GD, Sheldon IM. 2012. Explants of intact endometrium to model bovine innate immunity and inflammation ex vivo. Am J Reprod Immunol, 67:526-539.

Brooks K, Burns G, Spencer TE. 2014. Conceptus elongation in ruminants: Roles of progesterone, prostaglandin, interferon tau and cortisol. J Anim Sci Biotechnol, 5:1-12.

Carter F, Forde N, Duffy P, Wade M, Fair T, Crowe MA, Evans ACO, Kenny DA, Roche JF, Lonergan P. 2008. Effect of increasing progesterone concentration from Day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reprod Fertil Dev, 20:368-375.

Christie WB, Newcomb R, Rowson LE. 1979. Embryo survival in heifers after transfer of an egg to the uterine horn contralateral to the corpus luteum and the effect of treatments with progesterone or hCG on pregnancy rates. J Reprod Fertil, 56:701-706.

Clemente M, de La Fuente J, Fair T, Al Naib A, Gutierrez-Adan A, Roche JF, Rizos D, Lonergan P. 2009. Progesterone and conceptus elongation in cattle: a direct effect on the embryo or an indirect effect via the endometrium? Reproduction, 138:507-517.

Faulkner S, Elia G, O' Boyle P, Dunn M, Morris D. 2013. Composition of the bovine uterine proteome is associated with stage of cycle and concentration of systemic progesterone. Proteomics, 13:3333-3353.

Forde N, Carter F, Fair T, Crowe MA, Evans ACO, Spencer TE, Bazer FW, McBride R, Boland MP, O’Gaora P, Lonergan P, Roche JF. 2009. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biol Reprod, 81:784-794.

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. 2011. Conceptus-Induced Changes in the Endometrial Transcriptome: How Soon Does the Cow Know She Is Pregnant? Biol Reprod, 85:144-156.

Forde N, Lonergan P. 2012. Transcriptomic analysis of the bovine endometrium: What is required to establish uterine receptivity to implantation in cattle? J Reprod Dev, 58(2):189-95.

Forde N, Mehta JP, Minten M, Crowe MA, Roche JF, Spencer TE, Lonergan P. 2012. Effects of low progesterone on the endometrial transcriptome in cattle. Biol Reprod, 87:124.

Forde N, McGettigan PA, Mehta JP, O’Hara L, Mamo S, Bazer FW, Spencer TE, Lonergan P. 2014. Proteomic analysis of uterine fluid during the pre-implantation period of pregnancy in cattle. Reproduction, 147:575-587.

Forde N, Bazer FW, Spencer TE, Lonergan P. 2015. 'Conceptualizing' the endometrium: identification of conceptus-derived proteins during early pregnancy in cattle. Biol Reprod, 92:156.

Forde N, Lonergan P. 2017. Interferon-tau and fertility in ruminants. Reproduction, 154:F33-F43.

Gad A, Hoelker M, Besenfelder U, Havlicek V, Cinar U, Rings F, Held E, Dufort I, Sirard MA, Schellander K, Tesfaye D. 2012. Molecular mechanisms and pathways involved in bovine embryonic genome activation and their regulation by alternative in vivo and in vitro culture conditions. Biol Reprod, 87:100.

Geary TW, Burns GW, Moraes JG, Moss JI, Denicol AC, Dobbs KB, Ortega MS, Hansen PJ, Wehrman ME, Neibergs H, O'Neil E, Behura S, Spencer TE. 2016. Identification of Beef Heifers with Superior Uterine Capacity for Pregnancy. Biol Reprod, 95(2):47. Doi: 10.1095/biolreprod.116.141390.

Gómez E, Sánchez-Calabuig MJ, Martin D, Carrocera S, Murillo A, Correia-Alvarez E, Herrero P, Canela N, Gutiérrez-Adán A, Ulbrich S, Muñoz M. 2018. In vitro cultured bovine endometrial cells recognize embryonic sex. Theriogenology, 108:176-184.

Gray CA, Burghardt RC, Johnson GA, Bazer FW, Spencer TE. 2002. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction, 124:289-300.

Hasler JF, Henderson WB, Hurtgen PJ, Jin ZQ, McCauley AD, Mower SA, Neely B, Shuey LS, Stokes JE, Trimmer SA. 1995. Production, freezing and transfer of bovine IVF embryos and subsequent calving results. Theriogenology, 43:141-152.

Kimura K, Matsuyama S. 2014. Successful Nonsurgical Transfer of Bovine Elongating Conceptuses and Its Application to Sexing. J Reprod Dev, 60:210-215.

Lonergan P, Rizos D, Kanka J, Nemcova L, Mbaye AM, Kingston M, Wade M, Duffy P, Boland MP. 2003a. Temporal sensitivity of bovine embryos to culture environment after fertilization and the implications for blastocyst quality. Reproduction, 126:337-346

Lonergan P, Rizos D, Gutierrez-Adan A, Moreira PM, Pintado B, de la Fuente J, Boland MP. 2003b. Temporal divergence in the pattern of messenger RNA expression in bovine embryos cultured from the zygote to blastocyst stage in vitro or in vivo. Biol Reprod, 69:1424-1431.

Lonergan P, Forde N, Spencer T. 2016. The role of progesterone in embryo development in cattle. Reprod Fertil Dev, 28:66-74.

Mann GE, Lamming GE. 2001. Relationship between maternal endocrine environment, early embryo development and inhibition of the luteolytic mechanism in cows. Reproduction, 121:175-180.

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. 2009. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci USA, 106:5687-5692.

Mathew DJ, Sánchez JM, Passaro, Charpigny G, Behura S, Spencer TE, Lonergan P. 2019. Interferon tau (IFNT)-dependent and -independent effects of the bovine conceptus on the endometrium during early pregnancy. Biol Reprod, 100:365-380.

McMillan WH, Donnison MJ. 1999. Understanding maternal contributions to fertility in recipient cattle: development of herds with contrasting pregnancy rates. Anim Reprod Sci, 57:127-140

McNeill RE, Diskin MG, Sreenan JM, Morris DG. 2006. Associations between milk progesterone concentration on different days and with embryo survival during the early luteal phase in dairy cows. Theriogenology, 65:1435-1441.

Moraes JGN, Behura SK, Geary TW, Hansen PJ, Neibergs HL, Spencer TE. 2018. Uterine influences on conceptus development in fertility-classified animals. Proc Natl Acad Sci USA, 115:E1749-E1758.

Mullen MP, Elia G, Hilliard M, Parr MH, Diskin MG, Evans AC, Crowe MA. 2012. Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle. J Proteome Res, 11:3004-3018.

Muñoz M, Corrales FJ, Caamaño JN, Díez C, Trigal B, Mora MI, Martín D, Carrocera S, Gómez E. 2012. Proteome of the early embryo-maternal dialogue in the cattle uterus. J Proteome Res, 11:751-766.

O’Hara L, Forde N, Kelly AK, Lonergan P. 2014. Effect of bovine blastocyst size at embryo transfer on day 7 on conceptus length on day 14: Can supplementary progesterone rescue small embryos? Theriogenology, 81:1123-1128.

Okumu LA, Forde N, Fahey AG, Fitzpatrick E, Roche JF, Crowe MA, Lonergan P. 2010. The effect of elevated progesterone and pregnancy status on mRNA expression and localisation of progesterone and oestrogen receptors in the bovine uterus. Reproduction, 140:143-53.

Ortega MS, Moraes JGN, Patterson DJ, Smith MF, Behura SK, Poock S, Spencer TE. 2018. Influences of sire conception rate on pregnancy establishment in dairy cattle. Biol Reprod, 99:1244-1254.

Passaro C, Tutt D, Mathew DJ, Sánchez JM, Browne JA, Boe-Hansen GB, Fair T, Lonergan P. 2018. Blastocyst-induced changes in the bovine endometrial transcriptome. Reproduction, 156:219-229.

Passaro C, Tutt D, Bages-Arnal S, Maicas C, Laguna-Barraza R, Gutierrez-Adan A, Browne JA, Rath D, Behura SK, Spencer TE, Fair T, Lonergan P. 2019. Global transcriptomic response of bovine endometrium to blastocyst stage embryos. Reproduction. In press.

Rizos D, Fair T, Papadopoulos S, Boland MP, Lonergan P. 2002a. Developmental, qualitative, and ultrastructural differences between ovine and bovine embryos produced in vivo or in vitro. Mol Reprod Dev, 62:320-327.

Rizos D, Ward F, Duffy P, Boland MP, Lonergan P. 2002b. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Mol Reprod Dev, 61:234-248.

Rizos D, Scully S, Kelly AK, Ealy AD, Moros R, Duffy P, Al Naib A, Forde N, Lonergan P. 2012. Effects of human chorionic gonadotrophin administration on day 5 after oestrus on corpus luteum characteristics, circulating progesterone and conceptus elongation in cattle. Reprod Fertil Dev, 24:472-481.

Sánchez JM, Passaro C, Forde N, Browne JA, Behura SK, Fernández-Fuertes B, Mathew DJ, Kelly AK, Butler ST, Spencer TE, Lonergan P. 2019a. Do differences in the endometrial transcriptome between uterine horns ipsilateral and contralateral to the corpus luteum influence conceptus development to Day 14 in cattle? Biol Reprod, 100:86-100.

Sánchez JM, Mathew DJ, Behura SK, Passaro C, Charpigny G, Butler ST, Spencer TE, Lonergan P. 2019b. Bovine endometrium responds differentially to age-matched short and long conceptuses†. Biol Reprod, 101(1):26-39. Doi: 10.1093/biolre/ioz060.

Sartori R, Bastos MR, Wiltbank MC. 2010. Factors affecting fertilisation and early embryo quality in single- and superovulated dairy cattle. Reprod Fertil Dev, 22:151-158.

Satterfield MC, Bazer FW, Spencer TE. 2006. Progesterone regulation of preimplantation conceptus growth and galectin 15 (LGALS15) in the ovine uterus. Biol Reprod, 75:289-96.

Simintiras CA, Sánchez JM, McDonald M, Martins T, Binelli M, Lonergan P. 2019a. Biochemical characterization of progesterone-induced alterations in bovine uterine fluid amino acid and carbohydrate composition during the conceptus elongation window. Biol Reprod, 100:672-685.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. 2019b. Progesterone alters the bovine uterine fluid lipidome during the period of elongation. Reproduction, 157:399-411.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. 2019c. The influence of progesterone on bovine uterine fluid energy, nucleotide, vitamin, cofactor, and xenobiotic composition during the conceptus elongation-initiation window. Sci Rep. In press.

Simintiras CA, Sánchez JM, McDonald M, Lonergan P. 2019d. The biochemistry surrounding conceptus elongation. Biol Reprod. In press.

Spencer TE, Forde N, Dorniak P, Hansen TR, Romero JJ, Lonergan P. 2013. Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction, 146:377-387.

Spencer TE, Forde N, Lonergan P. 2016. The role of progesterone and conceptus-derived factors in uterine biology during early pregnancy in ruminants. J Dairy Sci, 99:5941-5950.

Spencer TE, Forde N, Lonergan P. 2017. Insights into conceptus elongation and establishment of pregnancy in ruminants. Reprod Fertil Dev, 29:84-100.

Sponchiado M, Gomes NS, Fontes PK, Martins T, Del Collado M, Pastore A de A, Pugliesi G, Nogueira MFG and Binelli M, Lonergan P. 2017. Pre-hatching embryo-dependent and -independent programming of endometrial function in cattle. PloS One, 12:e0175954.

Stronge AJH, Sreenan JM, Diskin MG, Mee JF, Kenny DA, Morris DG. 2005. Post-insemination milk progesterone concentration and embryo survival in dairy cows. Theriogenology, 64:1212-1224.

Takahashi H, Haneda S, Kayano M, Matsui M. 2016. Differences in progesterone concentrations and mRNA expressions of progesterone receptors in bovine endometrial tissue between the uterine horns ipsilateral and contralateral to the corpus luteum. J Vet Med Sci, 78:613-618.

Talukder AK, Yousef MS, Rashid MB, Awai K, Acosta TJ, Shimizu T, Okuda K, Shimada M, Imakawa K, Miyamoto A. 2017. Bovine embryo induces an anti-inflammatory response in uterine epithelial cells and immune cells in vitro: possible involvement of interferon tau as an intermediator. J Reprod Dev, 63:425-434.

Viana J. 2018. 2017 Statistics of embryo production and transfer in domestic farm animals. Embryo Technology Newsletter 36:8-25.

Wiltbank MC, Baez GM, Garcia-Guerra A, Toledo MZ, Monteiro PLJ, Melo LF, Ochoa JC, Santos JEP, Sartori R. 2016. Pivotal periods for pregnancy loss during the first trimester of gestation in lactating dairy cows. Theriogenology, 86:239-253.

Wydooghe E, Vandaele L, Heras S, De Sutter P, Deforce D, Peelman L, De Schauwer C and Van Soom A. 2015. Autocrine embryotropins revisited: how do embryos communicate with each other in vitro when cultured in groups? Biol Rev Camb Philos Soc, 92:505-520.

5d52b2720e88252839daee82 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections