Hostname: page-component-78c5997874-m6dg7 Total loading time: 0 Render date: 2024-11-11T04:29:56.223Z Has data issue: false hasContentIssue false
  • English
  • Français

Maternal-embryo interaction leading up to the initiation of implantation of pregnancy in cattle

Published online by Cambridge University Press:  28 March 2014

P. Lonergan  and
N. Forde
P. Lonergan*
Affiliation:
School of Agriculture and Food Science, Belfield, Dublin 4, Ireland
N. Forde
Affiliation:
School of Agriculture and Food Science, Belfield, Dublin 4, Ireland
*
†E-mail: pat.lonergan@ucd.ie
Get access

Abstract

Early embryo development following fertilization occurs in the oviduct. However, despite being the site of fertilization in cattle, it is possible to by-pass the oviduct by producing embryos in vitro and/or by transferring blastocysts recovered from one female into the uterus of another. While there is substantial evidence for the oviduct having an influence on the quality of the developing embryo, manifested in altered morphology, gene expression and cryotolerance, evidence for a two-way dialogue is weak. In contrast, successful growth and development of the post-hatching blastocyst and pregnancy establishment are a result of the two-way interaction between a competent embryo and a receptive uterine environment. Progesterone (P4) plays a key role in reproductive events associated with establishment and maintenance of pregnancy through its action on the uterine endometrium. Elevated concentrations of circulating P4 in the immediate post-conception period have been associated with an advancement of conceptus elongation, an increase in interferon-tau production and, in some studies, higher pregnancy rates in cattle. This review summarizes current knowledge on the communication between the developing embryo and the maternal reproductive tract.

Keywords

embryo mortalityendometriumconceptuspregnancybovine
Type
Full Paper
Information
animal , Volume 8 , Supplement s1: New Science ‐ New Practices International Cow Fertility Conference 18‐21 May 2014, Westport, Ireland , May 2014 , pp. 64 - 69
Copyright
© The Animal Consortium 2014 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alexopoulos, NI, Vajta, G, Maddox-Hyttel, P, French, AJ and Trounson, AO 2005. Stereomicroscopic and histological examination of bovine embryos following extended in vitro culture. Reproduction Fertility and Development 17, 799–808.CrossRefGoogle ScholarPubMed
Alminana, C, Heath, PR, Wilkinson, S, Sanchez-Osorio, J, Cuello, C, Parrilla, I, Gil, MA, Vazquez, JL, Vazquez, JM, Roca, J, Martinez, EA and Fazeli, A 2012. Early developing pig embryos mediate their own environment in the maternal tract. PLoS One 7, e33625.CrossRefGoogle ScholarPubMed
Bauersachs, S, Mitko, K, Ulbrich, SE, Blum, H and Wolf, E 2008. Transcriptome studies of bovine endometrium reveal molecular profiles characteristic for specific stages of estrous cycle and early pregnancy. Experimental and Clinical Endocrinology & Diabetes 116, 371–384.Google ScholarPubMed
Bauersachs, S, Rehfeld, S, Ulbrich, SE, Mallok, S, Prelle, K, Wenigerkind, H, Einspanier, R, Blum, H and Wolf, E 2004. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. Journal of Molecular Endocrinology 32, 449–466.CrossRefGoogle ScholarPubMed
Bauersachs, S, Ulbrich, SE, Zakhartchenko, V, Minten, M, Reichenbach, M, Reichenbach, HD, Blum, H, Spencer, TE and Wolf, E 2009. The endometrium responds differently to cloned versus fertilized embryos. Proceedings of the National Academy of Sciences USA 106, 5681–5686.CrossRefGoogle ScholarPubMed
Bauersachs, S, Ulbrich, SE, Gross, K, Schmidt, SE, Meyer, HH, Wenigerkind, H, Vermehren, M, Sinowatz, F, Blum, H and Wolf, E 2006. Embryo-induced transcriptome changes in bovine endometrium reveal species-specific and common molecular markers of uterine receptivity. Reproduction 132, 319–331.CrossRefGoogle ScholarPubMed
Bauersachs, S, Ulbrich, SE, Gross, K, Schmidt, SE, Meyer, HH, Einspanier, R, Wenigerkind, H, Vermehren, M, Blum, H, Sinowatz, F and Wolf, E 2005. Gene expression profiling of bovine endometrium during the oestrous cycle: detection of molecular pathways involved in functional changes. Journal of Molecular Endocrinology 34, 889–908.CrossRefGoogle ScholarPubMed
Bauersachs, S, Ulbrich, SE, Reichenbach, HD, Reichenbach, M, Buttner, M, Meyer, HH, Spencer, TE, Minten, M, Sax, G, Winter, G and Wolf, E 2012. Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium. Biology of Reproduction 86 (46), 1–15.CrossRefGoogle ScholarPubMed
Betteridge, KJ, Eaglesome, MD, Randall, GC and Mitchell, D 1980. Collection, description and transfer of embryos from cattle 10–16 days after oestrus. Journal of Reproduction and Fertility 59, 205–216.CrossRefGoogle ScholarPubMed
Brandao, DO, Maddox-Hyttel, P, Lovendahl, P, Rumpf, R, Stringfellow, D and Callesen, H 2004. Post hatching development: a novel system for extended in vitro culture of bovine embryos. Biology of Reproduction 71, 2048–2055.CrossRefGoogle ScholarPubMed
Carter, F, Forde, N, Duffy, P, Wade, M, Fair, T, Crowe, MA, Evans, AC, Kenny, DA, Roche, JF and Lonergan, P 2008. Effect of increasing progesterone concentration from day 3 of pregnancy on subsequent embryo survival and development in beef heifers. Reproduction Fertility and Development 20, 368–375.CrossRefGoogle ScholarPubMed
Clemente, M, de La Fuente, J, Fair, T, Al Naib, A, Gutierrez-Adan, A, Roche, JF, Rizos, D and 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.CrossRefGoogle ScholarPubMed
Clemente, M, Lopez-Vidriero, I, O'Gaora, P, Mehta, JP, Forde, N, Gutierrez-Adan, A, Lonergan, P and Rizos, D 2011. Transcriptome changes at the initiation of elongation in the bovine conceptus. Biology of Reproduction 85, 285–295.CrossRefGoogle ScholarPubMed
Costello, LM, O'Boyle, P, Godkin, JD, Diskin, MG, Hynes, AC and Morris, DG 2010. Retinol-binding protein (RBP), retinol and beta-carotene in the bovine uterus and plasma during the oestrous cycle and the relationship between systemic progesterone and RBP on day 7. Reproduction Fertility and Development 22, 1198–1205.CrossRefGoogle ScholarPubMed
Degrelle, SA, Campion, E, Cabau, C, Piumi, F, Reinaud, P, Richard, C, Renard, JP and Hue, I 2005. Molecular evidence for a critical period in mural trophoblast development in bovine blastocysts. Developmental Biology 288, 448–460.CrossRefGoogle ScholarPubMed
Degrelle, SA, Le Cao, KA, Heyman, Y, Everts, RE, Campion, E, Richard, C, Ducroix-Crepy, C, Tian, XC, Lewin, HA, Renard, JP, Robert-Granie, C and Hue, I 2011. A small set of extra-embryonic genes defines a new landmark for bovine embryo staging. Reproduction 141, 79–89.CrossRefGoogle ScholarPubMed
Diskin, MG and Morris, DG 2008. Embryonic and early foetal losses in cattle and other ruminants. Reproduction in Domestic Animals 43 (suppl. 2), 260–267.CrossRefGoogle ScholarPubMed
Dorniak, P, Bazer, FW, Wu, G and Spencer, TE 2012. Conceptus-derived prostaglandins regulate endometrial function in sheep. Biology of Reproduction 87 (9), 1–7.Google ScholarPubMed
Dorniak, P, Welsh, TH Jr, Bazer, FW and Spencer, TE 2013. Cortisol and interferon tau regulation of endometrial function and conceptus development in female sheep. Endocrinology 154, 931–941.CrossRefGoogle ScholarPubMed
Enright, BP, Lonergan, P, Dinnyes, A, Fair, T, Ward, FA, Yang, X and Boland, MP 2000. Culture of in vitro produced bovine zygotes in vitro v. in vivo: implications for early embryo development and quality. Theriogenology 54, 659–673.CrossRefGoogle Scholar
Faulkner, S, Elia, G, Mullen, MP, O'Boyle, P, Dunn, MJ and Morris, D 2012. A comparison of the bovine uterine and plasma proteome using iTRAQ proteomics. Proteomics 12, 2014–2023.CrossRefGoogle ScholarPubMed
Fazeli, A, Affara, NA, Hubank, M and Holt, WV 2004. Sperm-induced modification of the oviductal gene expression profile after natural insemination in mice. Biology of Reproduction 71, 60–65.CrossRefGoogle ScholarPubMed
Forde, N, Spencer, TE, Bazer, FW, Song, G, Roche, JF and Lonergan, P 2010. Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiological Genomics 41, 53–62.CrossRefGoogle ScholarPubMed
Forde, N, Mehta, JP, Minten, M, Crowe, MA, Roche, JF, Spencer, TE and Lonergan, P 2012a. Effects of low progesterone on the endometrial transcriptome in cattle. Biology of Reproduction 87 (124), 1–11.CrossRefGoogle ScholarPubMed
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 and Evans, AC 2012b. Evidence for an early endometrial response to pregnancy in cattle: both dependent upon and independent of interferon tau. Physiological Genomics 44, 799–810.CrossRefGoogle ScholarPubMed
Forde, N, Mehta, JP, McGettigan, PA, Mamo, S, Bazer, FW, Spencer, TE and Lonergan, P 2013. Alterations in expression of endometrial genes coding for proteins secreted into the uterine lumen during conceptus elongation in cattle. BMC Genomics 14 (321), 1–13.CrossRefGoogle ScholarPubMed
Forde, N, Beltman, ME, Duffy, GB, Duffy, P, Mehta, JP, O’Gaora, P, Roche, JF, Lonergan, P and Crowe, MA 2011a. Changes in the endometrial transcriptome during the bovine estrous cycle: effect of low circulating progesterone and consequences for conceptus elongation. Biology of Reproduction 84, 266–278.CrossRefGoogle ScholarPubMed
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 and Lonergan, P 2011b. Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biology of Reproduction 85, 144–156.CrossRefGoogle Scholar
Forde, N, Carter, F, Fair, T, Crowe, MA, Evans, AC, Spencer, TE, Bazer, FW, McBride, R, Boland, MP, O’Gaora, P, Lonergan, P and Roche, JF 2009. Progesterone-regulated changes in endometrial gene expression contribute to advanced conceptus development in cattle. Biology of Reproduction 81, 784–794.CrossRefGoogle ScholarPubMed
Gordon, I 2003. Laboratory production of cattle embryos. CABI Publishing, Wallingford, Oxon, UK (H ISBN 9780851996660).CrossRefGoogle Scholar
Gray, CA, Burghardt, RC, Johnson, GA, Bazer, FW and Spencer, TE 2002. Evidence that absence of endometrial gland secretions in uterine gland knockout ewes compromises conceptus survival and elongation. Reproduction 124, 289–300.CrossRefGoogle ScholarPubMed
Guillomot, M, Flechon, JE and Wintenberger-Torres, S 1981. Conceptus attachment in the ewe: an ultrastructural study. Placenta 2, 169–182.CrossRefGoogle ScholarPubMed
Hicks, BA, Etter, SJ, Carnahan, KG, Joyce, MM, Assiri, AA, Carling, SJ, Kodali, K, Johnson, GA, Hansen, TR, Mirando, MA, Woods, GL, Vanderwall, DK and Ott, TL 2003. Expression of the uterine Mx protein in cyclic and pregnant cows, gilts, and mares. Journal of Animal Science 81, 1552–1561.CrossRefGoogle ScholarPubMed
Hue, I, Degrelle, SA, Campion, E and Renard, JP 2007. Gene expression in elongating and gastrulating embryos from ruminants. Society of Reproduction and Fertility 64 (suppl.), 365–377.Google ScholarPubMed
Hugentobler, SA, Morris, DG, Sreenan, JM and Diskin, MG 2007. Ion concentrations in oviduct and uterine fluid and blood serum during the estrous cycle in the bovine. Theriogenology 68, 538–548.CrossRefGoogle ScholarPubMed
Hugentobler, SA, Humpherson, PG, Leese, HJ, Sreenan, JM and Morris, DG 2008. Energy substrates in bovine oviduct and uterine fluid and blood plasma during the oestrous cycle. Molecular Reproduction and Development 75, 496–503.CrossRefGoogle ScholarPubMed
Hugentobler, SA, Sreenan, JM, Humpherson, PG, Leese, HJ, Diskin, MG and Morris, DG 2010. Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood. Reproduction Fertility and Development 22, 684–694.CrossRefGoogle Scholar
Johnson, GA, Austin, KJ, Van Kirk, EA and Hansen, TR 1998. Pregnancy and interferon-tau induce conjugation of bovine ubiquitin cross-reactive protein to cytosolic uterine proteins. Biology of Reproduction 58, 898–904.CrossRefGoogle ScholarPubMed
Larson, JE, Krisher, RL and Lamb, GC 2011. Effects of supplemental progesterone on the development, metabolism and blastocyst cell number of bovine embryos produced in vitro. Reproduction Fertility and Development 23, 311–318.CrossRefGoogle ScholarPubMed
Ledgard, AM, Lee, RS and Peterson, AJ 2009. Bovine endometrial legumain and TIMP-2 regulation in response to presence of a conceptus. Molecular Reproduction and Development 76, 65–74.CrossRefGoogle ScholarPubMed
Lee, KF, Yao, YQ, Kwok, KL, Xu, JS and Yeung, WS 2002. Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochemical and Biophysical Research Communications 292, 564–570.CrossRefGoogle ScholarPubMed
Maillo, V, O'Gaora, P, Mehta, JP, De Frutos, C, Forde, N, Spencer, TE, Lonergan, P and Rizos, D 2014. Oviduct-embryo interactions: two way traffic or a one-way street? Transcriptomic response of the bovine oviduct to the presence of an embryo. Reproduction Fertility and Development 26, 152–153.CrossRefGoogle Scholar
Mamo, S, Mehta, JP, McGettigan, P, Fair, T, Spencer, TE, Bazer, FW and Lonergan, P 2011. RNA sequencing reveals novel gene clusters in bovine conceptuses associated with maternal recognition of pregnancy and implantation. Biology of Reproduction 85, 1143–1151.CrossRefGoogle ScholarPubMed
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 and Renard, JP 2009. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proceedings of the National Academy of Sciences USA 106, 5687–5692.CrossRefGoogle ScholarPubMed
Mitko, K, Ulbrich, SE, Wenigerkind, H, Sinowatz, F, Blum, H, Wolf, E and Bauersachs, S 2008. Dynamic changes in messenger RNA profiles of bovine endometrium during the oestrous cycle. Reproduction 135, 225–240.CrossRefGoogle ScholarPubMed
Mullen, MP, Elia, G, Hilliard, M, Parr, MH, Diskin, MG, Evans, AC and Crowe, MA 2012. Proteomic characterization of histotroph during the preimplantation phase of the estrous cycle in cattle. Journal of Proteome Research 11, 3004–3018.CrossRefGoogle ScholarPubMed
O’Hara, L, Forde, N, Carter, F, Rizos, D, Maillo, V, Ealy, AD, Kelly, AK, Rodriguez, P, Isaka, N, Evans, AC and Lonergan, P 2014. Paradoxical effect of supplementary progesterone between Day 3 and Day 7 on corpus luteum function and conceptus development in cattle. Reproduction Fertility and Development 26, 328–336.CrossRefGoogle Scholar
Okumu, LA, Forde, N, Fahey, AG, Fitzpatrick, E, Roche, JF, Crowe, MA and 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, 143–153.CrossRefGoogle ScholarPubMed
Rizos, D, Ward, F, Duffy, P, Boland, MP and Lonergan, P 2002. Consequences of bovine oocyte maturation, fertilization or early embryo development in vitro versus in vivo: implications for blastocyst yield and blastocyst quality. Molecular Reproduction and Development 61, 234–248.CrossRefGoogle ScholarPubMed
Rizos, D, Pintado, B, de la Fuente, J, Lonergan, P and Gutierrez-Adan, A 2007. Development and pattern of mRNA relative abundance of bovine embryos cultured in the isolated mouse oviduct in organ culture. Molecular Reproduction and Development 74, 716–723.CrossRefGoogle ScholarPubMed
Rizos, D, Ramirez, MA, Pintado, B, Lonergan, P and Gutierrez-Adan, A 2010. Culture of bovine embryos in intermediate host oviducts with emphasis on the isolated mouse oviduct. Theriogenology 73, 777–785.CrossRefGoogle ScholarPubMed
Sandra, O, Mansouri-Attia, N and Lea, RG 2011. Novel aspects of endometrial function: a biological sensor of embryo quality and driver of pregnancy success. Reproduction Fertility and Development 24, 68–79.CrossRefGoogle ScholarPubMed
Simmons, RM, Erikson, DW, Kim, J, Burghardt, RC, Bazer, FW, Johnson, GA and Spencer, TE 2009. Insulin-like growth factor binding protein-1 in the ruminant uterus: potential endometrial marker and regulator of conceptus elongation. Endocrinology 150, 4295–4305.CrossRefGoogle ScholarPubMed
Spencer, TE and Gray, CA 2006. Sheep uterine gland knockout (UGKO) model. Methods in Molecular Medicine 121, 85–94.Google ScholarPubMed
Spencer, TE, Forde, N, Dorniak, P, Hansen, TR, Romero, JJ and Lonergan, P 2013. Conceptus-derived prostaglandins regulate gene expression in the endometrium prior to pregnancy recognition in ruminants. Reproduction 146, 377–387.CrossRefGoogle ScholarPubMed
Tesfaye, D, Lonergan, P, Hoelker, M, Rings, F, Nganvongpanit, K, Havlicek, V, Besenfelder, U, Jennen, D, Tholen, E and Schellander, K 2007. Suppression of connexin 43 and E-cadherin transcripts in in vitro derived bovine embryos following culture in vitro or in vivo in the homologous bovine oviduct. Molecular Reproduction and Development 74, 978–988.CrossRefGoogle ScholarPubMed
Ushizawa, K, Herath, CB, Kaneyama, K, Shiojima, S, Hirasawa, A, Takahashi, T, Imai, K, Ochiai, K, Tokunaga, T, Tsunoda, Y, Tsujimoto, G and Hashizume, K 2004. cDNA microarray analysis of bovine embryo gene expression profiles during the pre-implantation period. Reproductive Biology and Endocrinology 2, 77.CrossRefGoogle ScholarPubMed