Suppressed expression of macrophage migration inhibitory factor in the oviducts of lean and obese cows
Asrafun Nahar A and Hiroya Kadokawa A BA Faculty of Veterinary Medicine, Yamaguchi University, Yamaguchi-shi, Yamaguchi-ken 1677-1, Japan.
B Corresponding author. Email: [email protected]
Reproduction, Fertility and Development 28(6) 655-662 https://doi.org/10.1071/RD14164
Submitted: 19 May 2014 Accepted: 11 October 2014 Published: 25 November 2014
Abstract
Oviducts synthesise macrophage migration inhibitory factor (MIF) to promote sperm capacitation and embryogenesis. This study aimed to test a hypothesis that the oviducts of obese cows may express MIF at a lower level than those of normal and lean cows. Ampullar and isthmic oviduct sections were collected from lean (n = 5; body condition score (BCS) on a 5-point scale, 2.5), normal (n = 6; BCS, 3.0) and obese (n = 5; BCS, 4.0) Japanese Black cows. MIF mRNA and protein were extracted from ampullae and isthmuses and their levels measured by real-time polymerase chain reaction or western blot. Immunohistochemistry was performed on frozen sections of ampullae and isthmuses by using antibodies to MIF. MIF mRNA and protein expression were lower in the obese and lean groups than in the normal group (P < 0.05). Immunohistochemistry revealed that the primary site of MIF expression in the ampulla and isthmus is the tunica mucosa. In conclusion, obese cows have suppressed MIF expression in the ampullae and isthmuses of their oviducts, as hypothesised, but, unexpectedly, MIF expression was also lower in lean cows.
Additional keywords: body condition score, ruminant, tunica mucosa.
References
Agriculture, Forestry and Fisheries Research Council Secretariat (2008). Nutrition requirement. In ‘Japanese Feeding Standard for Beef Cattle’. (Ed. Ministry of Agriculture, Forestry and Fisheries.) pp. 31–48. (Central Association of Livestock Industry: Tokyo.)Akoum, A., Metz, C. N., and Morin, M. (2005). Marked increase in macrophage migration inhibitory factor synthesis and secretion in human endometrial cells in response to human chorionic gonadotrophin hormone. J. Clin. Endocrinol. Metab. 90, 2904–2910.
| Marked increase in macrophage migration inhibitory factor synthesis and secretion in human endometrial cells in response to human chorionic gonadotrophin hormone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkt1WgtLo%3D&md5=ca041efa3c759578f60fdb7ca19577f4CAS | 15687332PubMed |
Arcuri, F., Ricci, C., Ietta, F., Cintorino, M., Tripodi, S. A., Cetin, I., Garzia, E., Schatz, F., Klemi, P., Santopietro, R., and Paulesu, L. (2001). Macrophage migration inhibitory factor in the human endometrium: expression and localisation during the menstrual cycle and early pregnancy. Biol. Reprod. 64, 1200–1205.
| Macrophage migration inhibitory factor in the human endometrium: expression and localisation during the menstrual cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXit1aru7Y%3D&md5=037d1cce71037af5abd548b35c08b3cbCAS | 11259268PubMed |
Atsumi, T., Cho, Y. R., and Leng, L. (2007). The pro-inflammatory cytokine macrophage migration inhibitory factor regulates glucose metabolism during systemic inflammation. J. Immunol. 179, 5399–5406.
| The pro-inflammatory cytokine macrophage migration inhibitory factor regulates glucose metabolism during systemic inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFWitrbK&md5=6db63174289364af598b1240a276f078CAS | 17911626PubMed |
Benigni, F., Atsumi, T., Calandra, T., Metz, C., Echtenacher, B., Peng, T., and Bucala, R. (2000). The pro-inflammatory mediator macrophage migration inhibitory factor induces glucose catabolism in muscle. J. Clin. Invest. 106, 1291–1300.
| The pro-inflammatory mediator macrophage migration inhibitory factor induces glucose catabolism in muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotlChu7k%3D&md5=4c6f5ab0f5d53e168ecf4fe83076b98cCAS | 11086030PubMed |
Bergman, E. N., Reulein, S. S., and Corlett, R. E. (1989). Effects of obesity on insulin sensitivity and responsiveness in sheep. Am. J. Physiol. 257, E772–E781.
| 1:CAS:528:DyaK3cXhvFKisQ%3D%3D&md5=89dc8afcf5c1f675aa408f98bf5c2199CAS | 2688439PubMed |
Besenfelder, U., Havlicek, V., and Brem, G. (2012). Role of the oviduct in early embryo development. Reprod. Domest. Anim. 47, 156–163.
| Role of the oviduct in early embryo development.Crossref | GoogleScholarGoogle Scholar | 22827365PubMed |
Bevilacqua, E., Paulesu, L., Ferro, E. A. V., Ietta, F., Faria, M. R., Lorenzon, A. R., Costa, A. F., and Martucci, M. (2014). Review: putative roles for the macrophage migratory inhibitory factor at the maternal–fetal interface. Placenta 35, S51–S56.
| Review: putative roles for the macrophage migratory inhibitory factor at the maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslGlsb%2FI&md5=772c011562e4166d9f04eca4acd0d343CAS | 24215782PubMed |
Bondza, P. K., Metz, C. N., and Akoum, A. (2008). Post-gestational effects of macrophage migration inhibitory factor on embryonic implantation in mice. Fertil. Steril. 90, 1433–1443.
| Post-gestational effects of macrophage migration inhibitory factor on embryonic implantation in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlSru7%2FM&md5=9f828e5165cae26b89293b482bfff41aCAS | 18022162PubMed |
Carli, C., Leclerc, P., Metz, C. N., and Akoum, A. (2007). Direct effect of macrophage migration inhibitory factor on sperm function: possible involvement in endometriosis-associated infertility. Fertil. Steril. 88, 1240–1247.
| Direct effect of macrophage migration inhibitory factor on sperm function: possible involvement in endometriosis-associated infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlShsLnF&md5=7499e16de2dc218376de691429aef419CAS | 17658526PubMed |
Cebrian-Serrano, A., Salvador, I., Garcia-Rosello, E., Pericuesta, E., Perez-Cerezales, S., Gutierrez-Adan, A., Coy, P., and Silvestre, M. A. (2013). Effect of the bovine oviductal fluid on in vitro fertilisation, development and gene expression of in vitro-produced bovine blastocysts. Reprod. Domest. Anim. 48, 331–338.
| Effect of the bovine oviductal fluid on in vitro fertilisation, development and gene expression of in vitro-produced bovine blastocysts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlWqu7c%3D&md5=1957a94cbdb9028adefde6f3bbff75b1CAS | 22908847PubMed |
Downs, S. M., Humpherson, P. G., and Leese, H. J. (1998). Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway. Biol. Reprod. 58, 1084–1094.
| Meiotic induction in cumulus cell-enclosed mouse oocytes: involvement of the pentose phosphate pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1KhtL0%3D&md5=2719f3aa4b176a69e273830db2296c3cCAS | 9546744PubMed |
el-Banna, A. A., and Hafez, E. S. (1970). Egg transport in beef cattle. J. Anim. Sci. 30, 430–432.
| 1:STN:280:DyaE3c7lt1Slsw%3D%3D&md5=a999ca39fdf129ea91ed20e7f482064dCAS | 5461745PubMed |
Ferguson, J. D., Galligan, D. T., and Thomsen, N. (1994). Principal descriptors of body condition score in Holstein cows. J. Dairy Sci. 77, 2695–2703.
| Principal descriptors of body condition score in Holstein cows.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7hsVantw%3D%3D&md5=2fa155b2a068e21c93af8c1e7564f2b7CAS | 7814740PubMed |
Hamilton, J. A., Davis, J., Pobjoy, J., and Cook, A. D. (2012). GM-CSF is not essential for optimal fertility or for weight control. Cytokine 57, 30–31.
| GM-CSF is not essential for optimal fertility or for weight control.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yrs77P&md5=c7db5b118c7139f517b0ae139e15f560CAS | 22129623PubMed |
Haney, A. F., Misukonis, M. A., and Weinberg, J. B. (1983). Macrophages and infertility: oviductal macrophages as potential mediators of infertility. Fertil. Steril. 39, 310–315.
| 1:STN:280:DyaL3s7jt1Crsg%3D%3D&md5=b195653b19e2dd5664b7acca608c91f7CAS | 6681781PubMed |
Hashimoto, S., Minami, N., Yamada, M., and Imai, H. (2000). An excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilisation: relevance to intracellular reactive oxygen species and glutathione contents. Mol. Reprod. Dev. 56, 520–526.
| An excessive concentration of glucose during in vitro maturation impairs the developmental competence of bovine oocytes after in vitro fertilisation: relevance to intracellular reactive oxygen species and glutathione contents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkslKlur8%3D&md5=77f560d8bcb324702a827ab4d72a8ab9CAS | 10911402PubMed |
Herrick, J. R., Brad, A. M., and Krisher, R. L. (2006). Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro. Reproduction 131, 289–298.
| Chemical manipulation of glucose metabolism in porcine oocytes: effects on nuclear and cytoplasmic maturation in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFalsLs%3D&md5=93facacae47dd0864810313619f0022cCAS | 16452722PubMed |
Hugentobler, S. A., Sreenan, J. M., Humpherson, P. G., Leese, H. J., Diskin, M. G., and Morris, D. G. (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. Reprod. Fertil. Dev. 22, 684–694.
| Effects of changes in the concentration of systemic progesterone on ions, amino acids and energy substrates in cattle oviduct and uterine fluid and blood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvF2isLY%3D&md5=54d1dd379f3ec2e83aa1d574c3d46ef1CAS | 20353728PubMed |
Jantra, S., Paulesu, L., Lo Valvo, M., Lillo, F., Ietta, F., Avanzati, A. M., Romagnoli, R., Bechi, N., and Brizzi, R. (2011). Cytokine components and mucosal immunity in the oviduct of Xenopus laevis (Amphibia, Pipidae). Gen. Comp. Endocrinol. 173, 454–460.
| Cytokine components and mucosal immunity in the oviduct of Xenopus laevis (Amphibia, Pipidae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFKjs7bO&md5=4eebe89414c689baac26e432d3e28a9eCAS | 21819986PubMed |
Kakar, M. A., Maddocks, S., Lorimer, M. F., Kleemann, D. O., Rudiger, S. R., Hartwich, K. M., and Walker, S. K. (2005). The effect of peri-conception nutrition on embryo quality in superovulated ewes. Theriogenology 64, 1090–1103.
| The effect of peri-conception nutrition on embryo quality in superovulated ewes.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2MvlvF2muw%3D%3D&md5=2d1d5eea9637eeb0acde186ab61636e8CAS | 16125553PubMed |
Kim, J. H., Funahashi, H., Niwa, K., and Okuda, K. (1993). Glucose requirement at different developmental stages of in vitro-fertilised bovine embryos cultured in semi-defined medium. Theriogenology 39, 875–886.
| Glucose requirement at different developmental stages of in vitro-fertilised bovine embryos cultured in semi-defined medium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXktVGlsbw%3D&md5=47e18518e2da7a36a45b10fa15535950CAS | 16727260PubMed |
Kölle, S., Dubielzig, S., Reese, S., Wehrend, A., König, P., and Kummer, W. (2009). Ciliary transport, gamete interaction and effects of the early embryo in the oviduct: ex vivo analyses using a new digital video-microscopic system in the cow. Biol. Reprod. 81, 267–274.
| Ciliary transport, gamete interaction and effects of the early embryo in the oviduct: ex vivo analyses using a new digital video-microscopic system in the cow.Crossref | GoogleScholarGoogle Scholar | 19299315PubMed |
Kumar, P., Verma, A., Roy, B., Rajput, S., Ojha, S., Anand, S., Yadav, P., Arora, J., De, S., Goswami, S. I., and Datta, T. K. (2012). Effect of varying glucose concentrations during in vitro maturation and embryo culture on efficiency of in vitro embryo production in buffalo. Reprod. Domest. Anim. 47, 269–273.
| Effect of varying glucose concentrations during in vitro maturation and embryo culture on efficiency of in vitro embryo production in buffalo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XmtlOkt7s%3D&md5=1718ce6d44b3eed8e0d6b413a061c090CAS | 21762215PubMed |
Larson, M. A., Kimura, K., Kubisch, H. M., and Roberts, R. M. (2001). Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signalling molecule IFN-tau. Proc. Natl. Acad. Sci. USA 98, 9677–9682.
| Sexual dimorphism among bovine embryos in their ability to make the transition to expanded blastocyst and in the expression of the signalling molecule IFN-tau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmtlCnu7g%3D&md5=ddc65338418684b7dd761b78ae52f2d5CAS | 11481449PubMed |
Leese, H. J., Tay, J. I., Reischl, J., and Downing, S. J. (2001). Formation of fallopian tubal fluid: role of a neglected epithelium. Reproduction 121, 339–346.
| Formation of fallopian tubal fluid: role of a neglected epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisFSquro%3D&md5=a0485d6efaa5ed881b49a1b92af0cb25CAS | 11226059PubMed |
Leng, L., Metz, C. N., Fang, Y., Xu, J., Donnelly, S., Baugh, J., Delohery, T., Chen, Y., Mitchell, R. A., and Bucala, R. (2003). MIF signal transduction initiated by binding to CD74. J. Exp. Med. 197, 1467–1476.
| MIF signal transduction initiated by binding to CD74.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksVOit7o%3D&md5=c0fc7bb78284f5e263445ca37c52951dCAS | 12782713PubMed |
Lopes, F., Vannoni, A., Sestini, S., Casciaro, A., Carducci, A., Bartolommei, S., Toschi, P., Ptak, G., Cintorino, M., and Arcuri, F. (2011). Sheep (Ovis aries) macrophage migration inhibitory factor: molecular cloning, characterisation, tissue distribution and expression in the ewe reproductive tract and in the placenta. Cytokine 54, 315–323.
| Sheep (Ovis aries) macrophage migration inhibitory factor: molecular cloning, characterisation, tissue distribution and expression in the ewe reproductive tract and in the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFamsL8%3D&md5=095015f9abef19cd60555b109396fddfCAS | 21419644PubMed |
Lozano, J. M., Lonergan, P., Boland, M. P., and O’Callaghan, D. (2003). Influence of nutrition on the effectiveness of superovulation programmes in ewes: effect on oocyte quality and post-fertilisation development. Reproduction 125, 543–553.
| Influence of nutrition on the effectiveness of superovulation programmes in ewes: effect on oocyte quality and post-fertilisation development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjvFOqtL0%3D&md5=b60340fdb0f76c9d3f1b393ef83fbf4aCAS | 12683925PubMed |
Matsuura, T., Sugimura, M., Iwaki, T., Ohashi, R., Kanayama, N., and Nishihira, J. (2002). Anti-macrophage inhibitory factor antibody inhibits PMSG-hCG-induced follicular growth and ovulation in mice. J. Assist. Reprod. Genet. 19, 591–595.
| Anti-macrophage inhibitory factor antibody inhibits PMSG-hCG-induced follicular growth and ovulation in mice.Crossref | GoogleScholarGoogle Scholar | 12503892PubMed |
Mburu, J. N., Einarsson, S., Kindahl, H., Madej, A., and Rodriguez-Martinez, H. (1998). Effects of post-ovulatory food deprivation on oviductal sperm concentration, embryo development and hormonal profiles in the pig. Anim. Reprod. Sci. 52, 221–234.
| Effects of post-ovulatory food deprivation on oviductal sperm concentration, embryo development and hormonal profiles in the pig.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsl2ksrs%3D&md5=b6117bcc4c46f2cc8b83f1a8e8a8edb4CAS | 9783995PubMed |
McCann, J. P., and Reimers, T. J. (1985). Insulin response to glucose in oestrous and diestrous obese and lean heifers. J. Anim. Sci. 61, 619–623.
| 1:CAS:528:DyaL2MXlvFSgsro%3D&md5=29d919f2d3141c75c8124fe5efb75832CAS | 3905736PubMed |
McCann, J. P., Ullmann, M. B., Temple, M. R., Reimers, T. J., and Bergman, E. N. (1986). Insulin and glucose responses to glucose injection in fed and fasted obese and lean sheep. J. Nutr. 116, 1287–1297.
| 1:CAS:528:DyaL28XlsFWqurs%3D&md5=148c1bc379d3571b2e965a10e875b311CAS | 3528428PubMed |
Meinhardt, A., Bacher, M., Metz, C., Bucala, R., Wreford, N., Lan, H., Atkins, R., and Hedger, M. (1998). Local regulation of macrophage subsets in the adult rat testis: examination of the roles of the seminiferous tubules, testosterone and macrophage-migration inhibitory factor. Biol. Reprod. 59, 371–378.
| Local regulation of macrophage subsets in the adult rat testis: examination of the roles of the seminiferous tubules, testosterone and macrophage-migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltFGnt7o%3D&md5=afe3993ae21e3d4cc76157b0cf1b79f1CAS | 9687310PubMed |
Nahar, A., Maki, S., and Kadokawa, H. (2013). Suppressed expression of granulocyte–macrophage colony-stimulating factor in oviduct ampullae of obese cows. Anim. Reprod. Sci. 139, 1–8.
| Suppressed expression of granulocyte–macrophage colony-stimulating factor in oviduct ampullae of obese cows.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlCqt7s%3D&md5=b8cb93bbe17c06e59a96df97cfcaf3d7CAS | 23611472PubMed |
Novak, S., Treacy, B. K., Almeida, F. R., Mao, J., Buhi, W. C., Dixon, W. T., and Foxcroft, G. R. (2002). Regulation of IGF-1 and porcine oviductal secretory protein secretion into the pig oviduct in the peri-ovulatory period, and effects of previous nutrition. Reprod. Nutr. Dev. 42, 355–372.
| Regulation of IGF-1 and porcine oviductal secretory protein secretion into the pig oviduct in the peri-ovulatory period, and effects of previous nutrition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslWqsA%3D%3D&md5=fd6d68a9496a7e340dfffd1452ea9356CAS | 12510876PubMed |
Oren-Benaroya, R., Kipnis, J., and Eisenbach, M. (2007). Phagocytosis of human post-capacitated spermatozoa by macrophages. Hum. Reprod. 22, 2947–2955.
| Phagocytosis of human post-capacitated spermatozoa by macrophages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1Shu7bI&md5=e5719a47ba795ee00a64559d5c553ed5CAS | 17766922PubMed |
Paulesu, L., Pfarrer, C., Romagnoli, R., Ietta, F., Callesen, H., Hambruch, N., and Dantzer, V. (2012). Variation in macrophage migration inhibitory factor (MIF) immunoreactivity during bovine gestation. Placenta 33, 157–163.
| Variation in macrophage migration inhibitory factor (MIF) immunoreactivity during bovine gestation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1eisL0%3D&md5=90e018ab36ff221628f396a7a96456faCAS | 22200576PubMed |
Rekawiecki, R., Rutkowska, J., and Kotwica, J. (2012). Identification of optimal housekeeping genes for examination of gene expression in bovine corpus luteum. Reprod. Biol. 12, 362–367.
| Identification of optimal housekeeping genes for examination of gene expression in bovine corpus luteum.Crossref | GoogleScholarGoogle Scholar | 23229008PubMed |
Robinson, R. S., Hammond, A. J., Wathes, D. C., Hunter, M. G., and Mann, G. E. (2008). Corpus luteum–endometrium–embryo interactions in the dairy cow: underlying mechanisms and clinical relevance. Reprod. Domest. Anim. 43, 104–112.
| Corpus luteum–endometrium–embryo interactions in the dairy cow: underlying mechanisms and clinical relevance.Crossref | GoogleScholarGoogle Scholar | 18638111PubMed |
Rodriguez Hurtado, I., Stewart, A. J., Wolfe, D. F., Caldwell, F. J., Harrie, M., and Whitley, E. M. (2011). Immunolocalisation of the hyaluronan receptor CD44 in the reproductive tract of the mare. Theriogenology 75, 276–286.
| Immunolocalisation of the hyaluronan receptor CD44 in the reproductive tract of the mare.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2isbnJ&md5=b7a9e390c9f2d34d674006d47e2db325CAS | 20932561PubMed |
Sakaue, S., Nishihira, J., and Hirokawa, J. (1999). Regulation of macrophage migration inhibitory factor (MIF) expression by glucose and insulin in adipocytes in vitro. Mol. Med. 5, 361–371.
| 1:CAS:528:DyaK1MXlslymu74%3D&md5=21769b4f8568293f25c3475f28617b1aCAS | 10415161PubMed |
Schwartz, V., Lue, H., Kraemer, S., Korbiel, J., Krohn, R., Ohl, K., Bucala, R., Weber, C., and Bernhagen, J. (2009). A functional heteromeric MIF receptor formed by CD74 and CXCR4. FEBS Lett. 583, 2749–2757.
| A functional heteromeric MIF receptor formed by CD74 and CXCR4.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVOisb7O&md5=0c332b3c57106bbfd5e04f34a52186a8CAS | 19665027PubMed |
Skrypina, N. A., Timofeeva, A. V., Khaspekov, G. L., Savochkina, L. P., and Beabealashvilli, R. Sh. (2003). Total RNA suitable for molecular biology analysis. J. Biotechnol. 105, 1–9.
| Total RNA suitable for molecular biology analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsVKmtLg%3D&md5=9a9301b5ef2c596ef3770044ce8336adCAS | 14511905PubMed |
Sutton-McDowall, M. L., Gilchrist, R. B., and Thompson, J. G. (2010). The pivotal role of glucose metabolism in determining oocyte developmental competence. Reproduction 139, 685–695.
| The pivotal role of glucose metabolism in determining oocyte developmental competence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltFajtr0%3D&md5=817fe0a6fea382753399ce968c38d421CAS | 20089664PubMed |
Suzuki, H., Kanagawa, H., and Nishihirab, J. (1996). Evidence for the presence of macrophage migration inhibitory factor in murine reproductive organs and early embryos. Immunol. Lett. 51, 141–147.
| Evidence for the presence of macrophage migration inhibitory factor in murine reproductive organs and early embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XjvFGgt7w%3D&md5=2effbefb1a4c69b5b551429e5b053a34CAS | 8832282PubMed |
Toso, C., Emamaullee, J. A., Merani, S., and Shapiro, A. M. (2008). The role of macrophage migration inhibitory factor on glucose metabolism and diabetes. Diabetologia 51, 1937–1946.
| The role of macrophage migration inhibitory factor on glucose metabolism and diabetes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1amsrfL&md5=30f74fa9f3d6e34a10420bc0518ac975CAS | 18612626PubMed |
Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Accurate normalisation of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034–research0034.11.
| Accurate normalisation of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |
Vecchio, D., Neglia, G., Di Palo, R., Campanile, G., Balestrieri, M. L., Giovane, A., Killian, G., Zicarelli, L., and Gasparrini, B. (2010). Ion, protein, phospholipid and energy substrate content of oviduct fluid during the oestrous cycle of buffalo (Bubalus bubalis). Reprod. Domest. Anim. 45, e32–e39.
| Ion, protein, phospholipid and energy substrate content of oviduct fluid during the oestrous cycle of buffalo (Bubalus bubalis).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlSgtLfE&md5=1ef686527340131745002dd13f8522a6CAS | 19761531PubMed |
Viganò, P., Cintorino, M., Schatz, F., Lockwood, C. J., and Arcuri, F. (2007). The role of macrophage migration inhibitory factor in maintaining the immune privilege at the fetal–maternal interface. Semin. Immunopathol. 29, 135–150.
| The role of macrophage migration inhibitory factor in maintaining the immune privilege at the fetal–maternal interface.Crossref | GoogleScholarGoogle Scholar | 17621699PubMed |
Wadgaonkar, R., Dudek, S. M., Zaiman, A. L., Linz-McGillem, L., Verin, A. D., Nurmukhambetova, S., Romer, L. H., and Garcia, J. G. (2005). Intracellular interaction of myosin light-chain kinase with macrophage migration inhibition factor (MIF) in endothelium. J. Cell. Biochem. 95, 849–858.
| Intracellular interaction of myosin light-chain kinase with macrophage migration inhibition factor (MIF) in endothelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlslajs7s%3D&md5=9a8da949ed80fc4f7a3da6ebeae68316CAS | 15838879PubMed |
Walker, C. G., Meier, S., Mitchell, M. D., Roche, J. R., and Littlejohn, M. (2009). Evaluation of real-time PCR endogenous control genes for analysis of gene expression in bovine endometrium. BMC Mol. Biol. 10, 100.
| Evaluation of real-time PCR endogenous control genes for analysis of gene expression in bovine endometrium.Crossref | GoogleScholarGoogle Scholar | 19878604PubMed |
Zheng, P., Bavister, B. D., and Ji, W. (2001). Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys. Mol. Reprod. Dev. 58, 348–355.
| Energy substrate requirement for in vitro maturation of oocytes from unstimulated adult rhesus monkeys.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtVShsro%3D&md5=1300ddf84f7a3cfe58d59ba732364bafCAS | 11170277PubMed |