Expression of macrophage migration inhibitory factor (MIF) in bovine oviducts is higher in the postovulatory phase than during the oestrus and luteal phase
Asrafun Nahar A and Hiroya Kadokawa A B
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary Medicine, Yamaguchi University, Yoshida 1677-1, Yamaguchi-shi, Yamaguchi-ken, 753-8515, Japan.
B Corresponding author. Email: hiroya@yamaguchi-u.ac.jp
Reproduction, Fertility and Development 29(8) 1521-1529 https://doi.org/10.1071/RD15546
Submitted: 24 December 2015 Accepted: 21 June 2016 Published: 28 July 2016
Abstract
Whether macrophage migration inhibitory factor (MIF) in the bovine oviduct is important for early embryogenesis has not been well substantiated. The aim of the present study was to test the hypothesis that bovine oviduct expresses higher levels of MIF during the post-ovulation phase. Both ampullary and isthmic samples were collected from Japanese black heifers during oestrus (Day 0; n = 5), postovulation (Day 3; n = 6) and luteal phase (Days 9–12; n = 5). MIF mRNA and protein were extracted from the ampullary and isthmic samples and their levels measured by real-time polymerase chain reaction and western blot analysis respectively. Fluorescent immunohistochemistry was performed on frozen ampullary and isthmic sections using antibodies against MIF. MIF mRNA and protein expression was higher in the postovulatory phase than during oestrus and the luteal phase (P < 0.05). Fluorescent immunohistochemistry confirmed that in all phases of the oestrous cycle evaluated, the primary site of MIF expression in the ampulla and isthmus was the tunica mucosa. In conclusion, the bovine ampulla and isthmus have higher MIF expression during the postovulatory phase. Further studies are needed to clarify the role of MIF in bovine oviducts.
Additional keywords: cytokine, growth factor, ruminant, tunica mucosa.
References
Aloisi, A. M., Pari, G., Ceccarelli, I., Vecchi, I., Ietta, F., Lodi, L., and Paulesu, L. (2005). Gender-related effects of chronic non-malignant pain and opioid therapy on plasma levels of macrophage migration inhibitory factor (MIF). Pain 115, 142–151.| Gender-related effects of chronic non-malignant pain and opioid therapy on plasma levels of macrophage migration inhibitory factor (MIF).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjt1Sqtbs%3D&md5=45ea9739f7d11ce7067b8d43dc3b9fc9CAS | 15836977PubMed |
Ashcroft, G. S., Mills, S. J., and Lei, K. (2003). Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor. J. Clin. Invest. 111, 1309–1318.
| Estrogen modulates cutaneous wound healing by downregulating macrophage migration inhibitory factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsFCrsrw%3D&md5=2a27b5589bb8791ab44c5aca8c2c477eCAS | 12727922PubMed |
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=27b24b2d9f61e0d14cc86714d9a5579cCAS | 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=3abca3aee423690bed28fb5101a901f4CAS | 11086030PubMed |
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=cc5b28f8a718570f3caefdbb77ae6f60CAS | 24215782PubMed |
Bondza, P. K., Metz, C. N., and Akoum, A. (2008). Postgestational effects of macrophage migration inhibitory factor on embryonic implantation in mice. Fertil. Steril. 90, 1433–1443.
| Postgestational effects of macrophage migration inhibitory factor on embryonic implantation in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlSru7%2FM&md5=6282bfb910759c45197fbe4900826bd7CAS | 18022162PubMed |
Bove, S. E., Petroff, M. G., Nishibori, M., and Pate, J. L. (2000). Macrophage migration inhibitory factor in the bovine corpus luteum: characterization of steady-state messenger ribonucleic acid and immunohistochemical localization. Biol. Reprod. 62, 879–885.
| Macrophage migration inhibitory factor in the bovine corpus luteum: characterization of steady-state messenger ribonucleic acid and immunohistochemical localization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitFajt70%3D&md5=89fa799bceeed0ba49f80fc9132d2e22CAS | 10727256PubMed |
Bucala, R., and Shachar, I. (2014). The integral role of CD74 in antigen presentation, MIF signal transduction, and B cell survival and homeostasis. Mini Rev. Med. Chem. 14, 1132–1138.
| The integral role of CD74 in antigen presentation, MIF signal transduction, and B cell survival and homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjslyhsLY%3D&md5=c413df5c5f666c167cbc515bcd741de2CAS | 25643611PubMed |
Buhi, W. C. (2002). Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein. Reproduction 123, 355–362.
| Characterization and biological roles of oviduct-specific, oestrogen-dependent glycoprotein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xit1Clsr0%3D&md5=1d68456fdb6977b6b0095f71e7a6b8aaCAS | 11882012PubMed |
Buhi, W. C., Alvarez, I. M., and Kouba, A. J. (2000). Secreted proteins of the oviduct. Cells Tissues Organs 166, 165–179.
| Secreted proteins of the oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtVyru74%3D&md5=845d813fbb90353ab809ae1328e08e83CAS | 10729726PubMed |
Calandra, T., Spiegel, L. A., Metz, C. N., and Bucala, R. (1998). Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria. Proc. Natl Acad. Sci. USA 95, 11 383–11 388.
| Macrophage migration inhibitory factor is a critical mediator of the activation of immune cells by exotoxins of Gram-positive bacteria.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmt1anu7c%3D&md5=f590b108069c3753fc788d6957297040CAS |
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=abe1798ef106d8fc95bfa12ab9e42d4dCAS | 17658526PubMed |
Croxatto, H. B. (2002). Physiology of gamete and embryo transport through the fallopian tube. Reprod. Biomed. Online 4, 160–169.
| Physiology of gamete and embryo transport through the fallopian tube.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjtlyktbg%3D&md5=c08fce6e50a2e64f46677ce903191641CAS | 12470580PubMed |
de Jonge, M. I., Keizer, S. A. S., El Moussaoui, H. M., van Dorsten, L., Azzawi, R., van Zuilekom, H. I., Peters, P. P. W., van Opzeeland, F. J. H., van Dijk, L., Nieuwland, R., Roosenboom-Theunissen, H. W. M., Vrijenhoek, M. P., Debyser, I., Verweij, P. J. M., van Duijnhoven, W. G. F., van den Bosch, J. F., and Nuijten, P. J. M. (2011). A novel guinea pig model of Chlamydia trachomatis genital tract infection. Vaccine 29, 5994–6001.
| A novel guinea pig model of Chlamydia trachomatis genital tract infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXpsFKisLY%3D&md5=1f2bbfcf8437ec1998f18d518618808bCAS | 21718744PubMed |
de Oliveira Gomes, A., de Oliveira Silva, D. A., Silva, N. M., de Freitas Barbosa, B., Franco, P. S., Angeloni, M. B., Fermino, M. L., Roque-Barreira, M. C., Bechi, N., Paulesu, L. R., Dos Santos, M. C., Mineo, J. R., and Ferro, E. A. (2011). Effect of macrophage migration inhibitory factor (MIF) in human placental explants infected with Toxoplasma gondii depends on gestational age. Am. J. Pathol. 178, 2792–2801.
| Effect of macrophage migration inhibitory factor (MIF) in human placental explants infected with Toxoplasma gondii depends on gestational age.Crossref | GoogleScholarGoogle Scholar | 21641401PubMed |
Donati, M., Di Paolo, M., Favaroni, A., Aldini, R., Di Francesco, A., Ostanello, F., Biondi, R., Cremonini, E., Ginocchietti, L., and Cevenini, R. (2015). A mouse model for Chlamydia suis genital infection. Pathog. Dis. 73, 1–3.
| A mouse model for Chlamydia suis genital infection.Crossref | GoogleScholarGoogle Scholar | 25854004PubMed |
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=051c91ba5dae23822ff0a68ef3e0332dCAS | 5461745PubMed |
Faria, M. R., Hoshida, M. S., Ferro, E. A., Ietta, F., Paulesu, L., and Bevilacqua, E. (2010). Spatiotemporal patterns of macrophage migration inhibitory factor (Mif) expression in the mouse placenta. Reprod. Biol. Endocrinol. 8, 95.
| Spatiotemporal patterns of macrophage migration inhibitory factor (Mif) expression in the mouse placenta.Crossref | GoogleScholarGoogle Scholar | 20684790PubMed |
Gabler, C., Killian, G. J., and Einspanier, R. (2001). Differential expression of extracellular matrix components in the bovine oviduct during the oestrous cycle. Reproduction 122, 121–130.
| Differential expression of extracellular matrix components in the bovine oviduct during the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsVGis7w%3D&md5=6511f8f579779625d3055e34121f44ffCAS | 11425336PubMed |
Gawronska, B., Paukku, T., Huhtaniemi, I., Wasowicz, G., and Ziecik, A. J. (1999). Oestrogen-dependent expression of LH/hCG receptors in pig fallopian tube and their role in relaxation of the oviduct. J. Reprod. Fertil. 115, 293–301.
| Oestrogen-dependent expression of LH/hCG receptors in pig fallopian tube and their role in relaxation of the oviduct.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXisFWkurc%3D&md5=b7b3686120a298a839a3aa23b22d3c5aCAS | 10434935PubMed |
Hafner, L. M. (2015). Pathogenesis of fallopian tube damage caused by Chlamydia trachomatis infections. Contraception 92, 108–115.
| Pathogenesis of fallopian tube damage caused by Chlamydia trachomatis infections.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtlGjs78%3D&md5=01a017a18ac799a6931f913442598ed3CAS | 25592078PubMed |
Hardman, M. J., Waite, A., Zeef, L., Burow, M., Nakayama, T., and Ashcroft, G. S. (2005). Macrophage migration inhibitory factor: a central regulator of wound healing. Am. J. Pathol. 167, 1561–1574.
| Macrophage migration inhibitory factor: a central regulator of wound healing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xkt1aktQ%3D%3D&md5=1fe59cb023bc542f0a20b27fcfebe7adCAS | 16314470PubMed |
Herath, S., Williams, E. J., Lilly, S. T., Gilbert, R. O., Dobson, H., Bryant, C. E., and Sheldon, I. M. (2007). Ovarian follicular cells have innate immune capabilities that modulate their endocrine function. Reproduction 134, 683–693.
| Ovarian follicular cells have innate immune capabilities that modulate their endocrine function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXovVCitA%3D%3D&md5=038ab762673822e0e4e1cab368d6812eCAS | 17965259PubMed |
Hoof, K. (2007). Pelvic inflammatory disease. Ther. Umsch. 64, 365–368.
| Pelvic inflammatory disease.Crossref | GoogleScholarGoogle Scholar | 17948752PubMed |
Houdeau, E., Moriez, R., Leveque, M., Salvador-Cartier, C., Waget, A., Leng, L., Bueno, L., Bucala, R., and Fioramonti, J. (2007). Sex steroid regulation of macrophage migration inhibitory factor in normal and inflamed colon in the female rat. Gastroenterology 132, 982–993.
| Sex steroid regulation of macrophage migration inhibitory factor in normal and inflamed colon in the female rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkslCju7k%3D&md5=b195d0e98c1b4f8abb3d39ba01b4e6b8CAS | 17324399PubMed |
Hristoskova, S., Holzgreve, W., Zhong, X. Y., and Hahn, S. (2006). Macrophage migration inhibition factor is elevated in pregnancy, but not to a greater extent in preeclampsia. Arch. Gynecol. Obstet. 274, 25–28.
| Macrophage migration inhibition factor is elevated in pregnancy, but not to a greater extent in preeclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Olurw%3D&md5=6065c2ce74b22384fbb71a780b5dd0a8CAS | 16369812PubMed |
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=cdcfa150e7bfea36b02dd8ddd103f549CAS | 20353728PubMed |
Hunter, R. H. (2005). The Fallopian tubes in domestic mammals: how vital is their physiological activity? Reprod. Nutr. Dev. 45, 281–290.
| The Fallopian tubes in domestic mammals: how vital is their physiological activity?Crossref | GoogleScholarGoogle Scholar | 15982454PubMed |
Ietta, F., Bechi, N., Romagnoli, R., Bhattacharjee, J., Realacci, M., Di Vito, M., Ferretti, C., and Paulesu, L. (2010). 17 beta-Estradiol modulates the macrophage migration inhibitory factor secretory pathway by regulating ABCA1 expression in human first-trimester placenta. Am. J. Physiol. Endocrinol. Metab. 298, E411–E418.
| 17 beta-Estradiol modulates the macrophage migration inhibitory factor secretory pathway by regulating ABCA1 expression in human first-trimester placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjsFGgs7s%3D&md5=ffeebcb058da8aa9a20a5c6e35d77a56CAS | 20173014PubMed |
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=f768022d8ee8849841d4ea2e7d3aabd6CAS | 21819986PubMed |
Kadokawa, H., and Yamada, Y. (1999). Enhancing effect of acute fasting on ethanol suppression of pulsatile luteinizing hormone release via an estrogen-dependent mechanism in Holstein heifers. Theriogenology 51, 673–680.
| Enhancing effect of acute fasting on ethanol suppression of pulsatile luteinizing hormone release via an estrogen-dependent mechanism in Holstein heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsFegtb0%3D&md5=396cfc9fc1ab6f8174d24552641f080eCAS | 10728992PubMed |
Kats, R., Al-Akoum, M., Guay, S., Metz, C., and Akoum, A. (2005). Cycle-dependent expression of macrophage migration inhibitory factor in the human endometrium. Hum. Reprod. 20, 3518–3525.
| Cycle-dependent expression of macrophage migration inhibitory factor in the human endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Gltr3L&md5=e8bfbc85f85b4a94022ad23898bb120bCAS | 16085663PubMed |
Kelly, R. W., Carr, G. G., and Critchley, H. O. (1997). A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease. Hum. Reprod. 12, 677–681.
| A cytokine switch induced by human seminal plasma: an immune modulation with implications for sexually transmitted disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjsF2hurw%3D&md5=6f8e39d64f7191ee93d288019872cf78CAS | 9159423PubMed |
Koizumi, M., Nahar, A., Yamabe, R., and Kadokawa, H. (2016). Positive correlations of age and parity with plasma concentration of macrophage migration inhibitory factor in Japanese black cows. J. Reprod. Dev. 62, 257–263.
| Positive correlations of age and parity with plasma concentration of macrophage migration inhibitory factor in Japanese black cows.Crossref | GoogleScholarGoogle Scholar | 26853787PubMed |
Lam, P. M., Po, L. S., Cheung, L. P., and Haines, C. (2005). The effect of exogenous estradiol treatment on the mRNA expression of vascular endothelial growth factor and its receptors in cultured human oviduct mucosal cells. J. Assist. Reprod. Genet. 22, 251–255.
| The effect of exogenous estradiol treatment on the mRNA expression of vascular endothelial growth factor and its receptors in cultured human oviduct mucosal cells.Crossref | GoogleScholarGoogle Scholar | 16021854PubMed |
Leese, H. J. (1995). Metabolic control during preimplantation mammalian development. Hum. Reprod. Update 1, 63–72.
| Metabolic control during preimplantation mammalian development.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2s3jsFSmuw%3D%3D&md5=7dbb54338e469c244f146e7aeb1854a8CAS | 9080207PubMed |
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, characterization, 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, characterization, tissue distribution, and expression in the ewe reproductive tract and in the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsFamsL8%3D&md5=447dee5b4f4d27fc73797d5ed29fca94CAS | 21419644PubMed |
Maillo, V., Gaora, P. Ó., Forde, N., Besenfelder, U., Havlicek, V., Burns, G. W., Spencer, T. E., Gutierrez-Adan, A., Lonergan, P., and Rizos, D. (2015). Oviduct–embryo interactions in cattle: two-way traffic or a one-way street? Biol. Reprod. 92, 144.
| Oviduct–embryo interactions in cattle: two-way traffic or a one-way street?Crossref | GoogleScholarGoogle Scholar | 25926440PubMed |
Mårdh, P. A., Møller, B. R., Ingerselv, H. J., Nüssler, E., Weström, L., and Wølner-Hanssen, P. (1981). Endometritis caused by Chlamydia trachomatis. Br. J. Vener. Dis. 57, 191–195.
| 7237083PubMed |
Murray, M. K. (1995). Epithelial lining of the sheep ampulla oviduct undergoes pregnancy-associated morphological changes in secretory status and cell height. Biol. Reprod. 53, 653–663.
| Epithelial lining of the sheep ampulla oviduct undergoes pregnancy-associated morphological changes in secretory status and cell height.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXns1ylsLY%3D&md5=9f8c05cc110ab608ae19a38db0ddd16aCAS | 7578690PubMed |
Murray, M. K., De Souza, M. M., and Messinger, S. M. (1995). Oviduct during early pregnancy: hormonal regulation and interactions with the fertilized ovum. Microsc. Res. Tech. 31, 497–506.
| Oviduct during early pregnancy: hormonal regulation and interactions with the fertilized ovum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotVWqt70%3D&md5=914f303d2fc8827d6eb2a904eb0c2d7bCAS | 8527850PubMed |
Nahar, A., and Kadokawa, H. (2016). Suppressed expression of macrophage migration inhibitory factor in the oviducts of lean and obese cows. Reprod. Fertil. Dev. 31, 497–506.
| Suppressed expression of macrophage migration inhibitory factor in the oviducts of lean and obese cows.Crossref | GoogleScholarGoogle Scholar |
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=f38aa7c44f547ae9fe11ad9a8b008b7cCAS | 22200576PubMed |
Profet, M. (1993). Menstruation as a defense against pathogens transported by sperm. Q. Rev. Biol. 68, 335–386.
| Menstruation as a defense against pathogens transported by sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2Fit12jsg%3D%3D&md5=31da958d0c6625436f840eb41e179e9fCAS | 8210311PubMed |
Quayle, A. J. (2002). The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells. J. Reprod. Immunol. 57, 61–79.
| The innate and early immune response to pathogen challenge in the female genital tract and the pivotal role of epithelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XnvVOnu7o%3D&md5=27035ee394e8ff58902fd2657a596657CAS | 12385834PubMed |
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 |
Ruijter, J. M., Ramakers, C., Hoogaars, W. M. H., Karlen, Y., Bakker, O., van den Hoff, M. J. B., and Moorman, A. F. M. (2009). Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37, e45.
| Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3lslGhtA%3D%3D&md5=722fbca3047f60d9b1fbd130f682f9c5CAS | 19237396PubMed |
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=ce42a8b40742469cafb359146752deedCAS | 10415161PubMed |
Schmaltz-Panneau, B., Cordova, A., Dhorne-Pollet, S., Hennequet-Antier, C., Uzbekova, S., Martinot, E., Doret, S., Martin, P., Mermillod, P., and Locatelli, Y. (2014). Early bovine embryos regulate oviduct epithelial cell gene expression during in vitro co-culture. Anim. Reprod. Sci. 149, 103–116.
| Early bovine embryos regulate oviduct epithelial cell gene expression during in vitro co-culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtlartbrI&md5=4c5575cc1d148a7475fdbd52e9fb01f0CAS | 25113901PubMed |
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=4ba4f8714677404c788330307344b509CAS | 14511905PubMed |
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=a06c674ee2892a5f1ecaa9308b44c859CAS | 8832282PubMed |
Tadokoro, C., Yoshimoto, Y., Sakata, M., Imai, T., Yamaguchi, M., Kurachi, H., Oka, Y., Maeda, T., and Miyake, A. (1995). Expression and localization of glucose transporter 1 (GLUT1) in the rat oviduct: a possible supplier of glucose to embryo during early embryonic development. Biochem. Biophys. Res. Commun. 214, 1211–1218.
| Expression and localization of glucose transporter 1 (GLUT1) in the rat oviduct: a possible supplier of glucose to embryo during early embryonic development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXot1yhtbw%3D&md5=10614963ddcbf77c4e6ac0e43f48a843CAS | 7575532PubMed |
Tang, L., Zhang, H., Lei, L., Gong, S., Zhou, Z., Baseman, J., and Zhong, G. (2013). Oviduct infection and hydrosalpinx in dba1/j mice is induced by intracervical but not intravaginal inoculation with Chlamydia muridarum. PLoS One 8, e71649.
| Oviduct infection and hydrosalpinx in dba1/j mice is induced by intracervical but not intravaginal inoculation with Chlamydia muridarum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlWgt7%2FI&md5=f574c8df880e3558b7e7b8eb70a0be07CAS | 23940777PubMed |
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=029111e605c948b3cfef7d5fc03d18b5CAS | 18612626PubMed |
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 Biol. 3, research0034.1.
| Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar |
Wada, S., Kudo, T., Kudo, M., Sakuragi, N., Hareyama, H., Nishihira, J., and Fujimoto, S. (1999). Induction of macrophage migration inhibitory factor in human ovary by human chorionic gonadotrophin. Hum. Reprod. 14, 395–399.
| Induction of macrophage migration inhibitory factor in human ovary by human chorionic gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXitVeqsL4%3D&md5=346156694107600ff7a889df82b2628bCAS | 10099986PubMed |
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=259df8fde272a278018fd299b55edda3CAS | 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 |
Wijayagunawardane, M. P., Miyamoto, A., Cerbito, W. A., Acosta, T. J., Takagi, M., and Sato, K. (1998). Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow. Theriogenology 49, 607–618.
| Local distributions of oviductal estradiol, progesterone, prostaglandins, oxytocin and endothelin-1 in the cyclic cow.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtFShu7s%3D&md5=98ad617441ba5f024156c8ef5287d672CAS | 10732039PubMed |
Wildt, L., Kissler, S., Licht, P., and Becker, W. (1998). Sperm transport in the human female genital tract and its modulation by oxytocin as assessed by hysterosalpingoscintigraphy, hysterotonography, electrohysterography and Doppler sonography. Hum. Reprod. Update 4, 655–666.
| Sperm transport in the human female genital tract and its modulation by oxytocin as assessed by hysterosalpingoscintigraphy, hysterotonography, electrohysterography and Doppler sonography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVShtro%3D&md5=2c2cb62c77aede3deda5863ae6f51d34CAS | 10027619PubMed |
Yamada, H., Kato, E. H., Morikawa, M., Shimada, S., Saito, H., Watari, M., Minakami, H., and Nishihira, J. (2003). Decreased serum levels of macrophage migration inhibition factor in miscarriages with normal chromosome karyotype. Hum. Reprod. 18, 616–620.
| Decreased serum levels of macrophage migration inhibition factor in miscarriages with normal chromosome karyotype.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1yrurs%3D&md5=b7f0985bd48b6750a5f4e066b4f49b85CAS | 12615835PubMed |
Yoshimoto, Y., Kobayashi, Y., Woclawek-Potocka, I., Sinderewicz, E., Yamamoto, Y., Kimura, K., and Okuda, K. (2016). Local effect of lysophosphatidic acid on prostaglandin production in the bovine oviduct. Reprod. Fertil. Dev. , .
| Local effect of lysophosphatidic acid on prostaglandin production in the bovine oviduct.Crossref | GoogleScholarGoogle Scholar | 26953625PubMed |
Zhang, B., Luo, Y., Liu, M. L., Wang, J., Xu, D. Q., Dong, M. Q., Liu, Y., Xu, M., Dong, H. Y., Zhao, P. T., Gao, Y. Q., and Li, Z. C. (2012). Macrophage migration inhibitory factor contributes to hypoxic pulmonary vasoconstriction in rats. Microvasc. Res. 83, 205–212.
| Macrophage migration inhibitory factor contributes to hypoxic pulmonary vasoconstriction in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xitlyhtr0%3D&md5=57aa26ab2528bb4a1839dd0cff3dd567CAS | 22005047PubMed |
