Altered endometrial immune gene expression in beef heifers with retarded embryos
M. E. Beltman A D , N. Forde B , P. Lonergan B C and M. A. Crowe A C
+ Author Affiliations
- Author Affiliations
A School of Veterinary Medicine, University College Dublin, Belfield, Dublin 4, Ireland.
B School of Agriculture and Food Science, University College Dublin, Belfield, Dublin 4, Ireland.
C Conway Institute, University College Dublin, Belfield, Dublin 4, Ireland.
D Corresponding author. Email: marijke.beltman@ucd.ie
Reproduction, Fertility and Development 25(6) 966-970 https://doi.org/10.1071/RD12232
Submitted: 27 May 2012 Accepted: 28 August 2012 Published: 4 October 2012
Abstract
The aim of the present study was to compare endometrial gene expression profiles in a group of beef heifers yielding viable or retarded embryos on Day 7 after oestrus as a means of potentially explaining differences in embryo survival rates. Heifers were classified as either: (1) viable, when the embryo collected on Day 7 after oestrus was at the correct developmental stage (i.e. morula/early blastocyst); or (2) retarded, when the embryo was arrested at the 2–16-cell stage. The focus of the present study was on genes that were associated with either the pro- or anti-inflammatory immune response. Endometrial gene expression was determined using quantitative real-time polymerase chain reaction analysis. Expression of the β-defensin (DEFB1), interferon (IFN)-α (IFNA), IFN-γ (IFNG), interleukin (IL)-6 (IL6), IL-10 (IL10), forkhead box P3 (FOXP3) and natural cytotoxicity triggering receptor 1 (NCR1) genes was lower in endometria from viable than retarded heifers. Expression of the nuclear factor of kappa light polypeptide gene enhancer in B cells 1 (NKFB1), transforming growth factor (TGF)-β (TGFB), IFN-γ-inducible protein 16 (IFI16) and IL-21 (IL21) genes was higher in viable than retarded heifers. We propose that small disturbances in the expression of immune genes in the endometrium on Day 7 after oestrus can have detrimental effects on embryo survival.
Additional keywords : anti-inflammatory, embryo development, pre-implantation, pro-inflammatory, uterus.
References
Bauersachs, S., Ulbrich, S. E., Zakhartchenko, V., Minten, M., Reichenbach, M., Reichenbach, H.-D., Blum, H., Spencer, T. E., and Wolf, E. (2009). The endometrium responds differently to cloned versus fertilized embryos. Proc. Natl. Acad. Sci. USA 106, 5681–5686.| The endometrium responds differently to cloned versus fertilized embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXkvFGhurk%3D&md5=051e04fdc18c3748867ca4da6a783b7bCAS | 19307558PubMed |
Bauersachs, S., Ulbrich, S. E., Reichenbach, H.-D., Reichenbach, M., Büttner, M., Meyer, H. H. D., Spencer, T. E., 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. Biol. Reprod. 86, 1–15.
| Comparison of the effects of early pregnancy with human interferon, alpha 2 (IFNA2), on gene expression in bovine endometrium.Crossref | GoogleScholarGoogle Scholar |
Beltman, M. E., Forde, N., Furney, P., Carter, F., Roche, J. F., Lonergan, P., and Crowe, M. A. (2010). Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on Day 7 after insemination. Reprod. Fertil. Dev. 22, 987–999.
| Characterisation of endometrial gene expression and metabolic parameters in beef heifers yielding viable or non-viable embryos on Day 7 after insemination.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3cnjvFOksA%3D%3D&md5=df86a9a8bef3c03c85a262ffdec72be5CAS | 20591333PubMed |
Chapwanya, A., Meade, K. G., Doherty, M. L., Callanan, J. J., Mee, J. F., and O’Farrelly, C. (2009). Histopathological and molecular evaluation of Holstein–Friesian cows postpartum: toward an improved understanding of uterine innate immunity. Theriogenology 71, 1396–1407.
| Histopathological and molecular evaluation of Holstein–Friesian cows postpartum: toward an improved understanding of uterine innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltl2murw%3D&md5=99cc2e0aeeb7b2fc813ffcac2bd4717eCAS | 19233457PubMed |
Eckersall, P. D., and Bell, R. (2010). Acute phase proteins: biomarkers of infection and inflammation in veterinary medicine. Vet. J. 185, 23–27.
| Acute phase proteins: biomarkers of infection and inflammation in veterinary medicine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVaqs7c%3D&md5=e5a6b28956fc82989b59a36b43c1ac76CAS | 20621712PubMed |
Forde, N., Spencer, T. E., Bazer, F. W., Song, G., Roche, J. F., and Lonergan, P. (2010). Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium. Physiol. Genomics 41, 53–62.
| Effect of pregnancy and progesterone concentration on expression of genes encoding for transporters or secreted proteins in the bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlakt7jN&md5=72dbde56303e12b95050e4ea9f597349CAS | 19996158PubMed |
Forde, N., Carter, F., Spencer, T. E., Bazer, F. W., Sandra, O., Mansouri-Attia, N., Okumu, L. A., McGettigan, P. A., Mehta, J. P., McBride, R., O’Gaora, P., Roche, J. F., and Lonergan, P. (2011). Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant? Biol. Reprod. 85, 144–156.
| Conceptus-induced changes in the endometrial transcriptome: how soon does the cow know she is pregnant?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXotFOlsL4%3D&md5=a2cf07cbd83b8718095708fb15073c45CAS | 21349821PubMed |
Hansen, P. J. (1997). Interactions between the immune system and the bovine conceptus. Theriogenology 47, 121–130.
| Interactions between the immune system and the bovine conceptus.Crossref | GoogleScholarGoogle Scholar |
Hansen, P. J. (2011). The immunology of early pregnancy in farm animals. Reprod. Domest. Anim. 46, 18–30.
| 21854458PubMed |
Hansen, P. J., Soto, P., and Natzke, R. P. (2004). Mastitis and fertility in cattle: possible involvement of inflammation or immune activation in embryonic mortality. Am. J. Reprod. Immunol. 51, 294–301.
| Mastitis and fertility in cattle: possible involvement of inflammation or immune activation in embryonic mortality.Crossref | GoogleScholarGoogle Scholar | 15212683PubMed |
Leung, S., Derecka, K., Mann, G., Flint, A., and Wathes, D. (2000). Uterine lymphocyte distribution and interleukin expression during early pregnancy in cows. J. Reprod. Fertil. 119, 25–33.
| 1:CAS:528:DC%2BD3cXjsF2ju74%3D&md5=9927193d6d8c407770f0e870e416aa45CAS | 10864810PubMed |
Lin, H., Mosmann, T., Guilbert, L., Tuntipopipat, S., and Wegmann, T. (1993). Synthesis of T helper 2-type cytokines at the maternal–fetal interface. J. Immunol. 151, 4562–4573.
| 1:CAS:528:DyaK2cXmsFKj&md5=8535a8b96624b9808030bda1e2b1a565CAS | 8409418PubMed |
Low, B. G., Hansen, P. J., Drost, M., and Gogolin-Ewens, K. J. (1990). Expression of major histocompatibility complex antigens on the bovine placenta. J. Reprod. Fertil. 90, 235–243.
| Expression of major histocompatibility complex antigens on the bovine placenta.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK3M%2FjvFSmtA%3D%3D&md5=f0b341b562cefb3fc926c48629c14ef5CAS | 2231545PubMed |
Maley, S. W., Buxton, D., Macaldowie, C. N., Anderson, I. E., Wright, S. E., Bartley, P. M., Esteban-Redondo, I., Hamilton, C. M., Storset, A. K., and Innes, E. A. (2006). Characterization of the immune response in the placenta of cattle experimentally infected with Neospora caninum in early gestation. J. Comp. Pathol. 135, 130–141.
| Characterization of the immune response in the placenta of cattle experimentally infected with Neospora caninum in early gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvFSisb8%3D&md5=fc2bcd722057217acd51f278b5a2bacaCAS | 16997005PubMed |
Mansouri-Attia, N., Aubert, J., Reinaud, P., Giraud-Delville, C., Taghouti, G., Galio, L., Everts, R. E., Richard, C., Hue, I., Yang, X., Tian, X. C., Lewin, H. A., Renard, J.-P., and Sandra, O. (2009). Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantation Physiol. Genomics 39, 14–27.
| Gene expression profiles of bovine caruncular and intercaruncular endometrium at implantationCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlakt7rM&md5=098db221572bb0da85c578e106f8034cCAS | 19622795PubMed |
Snedecor, G. W., and Cochran, W. G. 1989. ‘Statistical Methods.’ (Iwoa State University Press: Ames, IA.)
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology 3, research00034–research0034.11.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |
Walker, C. G., Meier, S., Littlejohn, M. D., Lehnert, K., Roche, J. R., and Mitchell, M. D. (2010). Modulation of the maternal immune system by the pre-implantation embryo. BMC Genomics 11, 474.
| Modulation of the maternal immune system by the pre-implantation embryo.Crossref | GoogleScholarGoogle Scholar | 20707927PubMed |
Zeng, W.-P., Sollars, V. E., and Belalcazar, A. D. P. (2011). Domain requirements for the diverse immune regulatory functions of foxp3. Mol. Immunol. 48, 1932–1939.
| Domain requirements for the diverse immune regulatory functions of foxp3.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVygs7rK&md5=b5e4124a2965889f38199e7d38a997a0CAS | 21737139PubMed |
Zhou, L., Lopes, J. E., Chong, M. M. W., Ivanov, I. I., Min, R., Victora, G. D., Shen, Y., Du, J., Rubtsov, Y. P., Rudensky, A. Y., Ziegler, S. F., and Littman, D. R. (2008). TGF-β-induced Foxp3 inhibits TH17 cell differentiation by antagonizing RORγt function. Nature 453, 236–240.
| TGF-β-induced Foxp3 inhibits TH17 cell differentiation by antagonizing RORγt function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXls12msL4%3D&md5=1344ffc9c9e8a0dac9ba0f9abb836c72CAS | 18368049PubMed |
