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Vertebrate reproductive science and technology
RESEARCH ARTICLE

Prostaglandin F–PTGFR signalling activation, growth factor expression and cell proliferation in bovine endometrial explants

Shuangyi Zhang A B , Bo Liu A B , Long Gao A B , Wei Mao A B , Changqi Fu A B , Duritahala A B , Nan Zhang A B , Ying Zhang A B , Yuan Shen A B and Jinshan Cao A B C
+ Author Affiliations
- Author Affiliations

A Laboratory of Veterinary Pharmacology, College of Veterinary Medicine, Inner Mongolia Agricultural University, No. 306, Zhaowuda Road, Saihan District, 010018, Hohhot, China.

B Key Laboratory of Clinical Diagnosis and Treatment Techniques for Animal Disease, Ministry of Agriculture, Inner Mongolia Agricultural University, No. 306, Zhaowuda Road, Saihan District, 010018, Hohhot, China.

C Corresponding author. Email: jinshancao@imau.edu.cn

Reproduction, Fertility and Development 29(11) 2195-2205 https://doi.org/10.1071/RD16144
Submitted: 8 April 2016  Accepted: 11 February 2017   Published: 16 March 2017

Abstract

The endometrium of domestic animals undergoes regular periods of regeneration and degeneration and exhibits a remarkable capacity for self-repair during the oestrous cycle. The endometrial growth pattern is also observed during in the implantation period and early pregnancy, but the mechanism underlying endometrial growth in these processes remains unclear. A positive correlation between endometrial growth in these processes and prostaglandin (PG) F secretion has been reported, but the roles that PGF plays in endometrial growth is less studied. In the present study, cell proliferation and the responses of a series of growth factors essential for endometrial growth to PGF receptor (PTGFR) activation were investigated in bovine endometrial explants in vitro. Using real-time reverse transcription–polymerase chain reaction and western blotting, mRNA and protein expression of connective tissue growth factor, fibroblast growth factor2, interleukin8, matrix metalloproteinase2, transforming growth factor β1 and vascular endothelial growth factor A was increased (P < 0.05) and cell proliferation, including epithelial and fibroblast proliferation, was induced in response to increased levels of proliferating cell nuclear antigen, cytokeratin-18 and fibroblast-specific protein-1 (P < 0.05) following PTGFR activation by adding fluprostenol (10−9–10−5 M) into culture medium of bovine endometrial explants. However, caspase-3 protein expression was reduced following treatment of explants with fluprostenol (10−9–10−5 M, P < 0.05). These results may help define the possible roles the PGF–PTGFR signalling pathway plays in endometrial growth.

Additional keywords: bovine endometrial growth, fluprostenol.


References

Arosh, J. A., Banu, S. K., Kimmins, S., Chapdelaine, P., MacLaren, L. A., and Fortier, M. A. (2004). Effect of interferon-pi on prostaglandin biosynthesis, transport, and signaling at the time of maternal recognition of pregnancy in cattle: evidence of polycrine actions of prostaglandin E2. Endocrinology 145, 5280–5293.
Effect of interferon-pi on prostaglandin biosynthesis, transport, and signaling at the time of maternal recognition of pregnancy in cattle: evidence of polycrine actions of prostaglandin E2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptVygsrg%3D&md5=85ef17cdfd5347da9fbf9a2fd9c5f5ceCAS |

Basu, S. (2007). Novel cyclooxygenase-catalyzed bioactive prostaglandin F2 alpha from physiology to new principles in inflammation. Med. Res. Rev. 27, 435–468.
Novel cyclooxygenase-catalyzed bioactive prostaglandin F2 alpha from physiology to new principles in inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1GjsL4%3D&md5=7b1c41f18e83265f56fe6a67394e7884CAS |

Binelli, M., Bertan, C. M., and da Cunha, P. M. (2004). Estradiol-17 beta potentiates calcium-stimulated prostaglandin F-2 alpha release from bovine endometrium. Biol. Reprod. 71, 169–170.

Blitek, A., and Ziecik, A. J. (2004). Prostaglandins F2 alpha and E2 secretion by porcine epithelial and stromal endometrial cells on different days of the oestrous cycle. Reprod. Domest. Anim. 39, 340–346.
Prostaglandins F2 alpha and E2 secretion by porcine epithelial and stromal endometrial cells on different days of the oestrous cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXpvF2qu70%3D&md5=94d2457dfb34d35ce51bc71624abb984CAS |

Boone, D. L., and Tsang, B. K. (1998). Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression. Biol. Reprod. 58, 1533–1539.
Caspase-3 in the rat ovary: localization and possible role in follicular atresia and luteal regression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXjsFShur8%3D&md5=886ffda7ab2e3eddaf3d958c8f0e4ff8CAS |

Bukowska, D., Kempisty, B., Jackowska, M., Woźna, M., Antosik, P., Piotrowska, H., and Jaśkowski, J. (2011). Differential expression of epidermal growth factor and transforming growth factor beta isoforms in dog endometrium during different periods of the estrus cycle. Pol. J. Vet. Sci. 14, 259–264.
Differential expression of epidermal growth factor and transforming growth factor beta isoforms in dog endometrium during different periods of the estrus cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1agurrJ&md5=1f0045486d98ca5e156c719761b7224cCAS |

Caron, P. L., Frechette-Frigon, G., Shooner, C., Leblanc, V., and Asselin, E. (2009). Transforming growth factor beta isoforms regulation of Akt activity and XIAP levels in rat endometrium during estrous cycle, in a model of pseudopregnancy and in cultured decidual cells. Reprod. Biol. Endocrinol. 7, 80.
Transforming growth factor beta isoforms regulation of Akt activity and XIAP levels in rat endometrium during estrous cycle, in a model of pseudopregnancy and in cultured decidual cells.Crossref | GoogleScholarGoogle Scholar |

Chan, R. W. S., and Gargett, C. E. (2006). Identification of label-retaining cells in mouse endometrium. Stem Cells 24, 1529–1538.
Identification of label-retaining cells in mouse endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFKlsbfO&md5=4e544ef4d81dc530e069cd4a764014cdCAS |

Chan, R. W. S., Schwab, K. E., and Gargett, C. E. (2004). Clonogenicity of human endometrial epithelial and stromal cellss. Biol. Reprod. 70, 1738–1750.
Clonogenicity of human endometrial epithelial and stromal cellss.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXktlOmt7o%3D&md5=3fa7b335a012c41db942149de9373286CAS |

Chang, M. C., Chang, H. H., Lee, M. Y., Lin, C. C., Yeh, H. W., Yang, T. T., Lin, P. S., Tseng, W. Y., and Jeng, J. H. (2009). Prostaglandin F2 alpha-induced interleukin-8 production in human dental pulp cells is associated with MEK/ERK signaling. J. Endod. 35, 508–512.
Prostaglandin F2 alpha-induced interleukin-8 production in human dental pulp cells is associated with MEK/ERK signaling.Crossref | GoogleScholarGoogle Scholar |

Cobellis, L., Razzi, S., De Simone, S., Sartini, A., Fava, A., Danero, S., Gioffre, W., Mazzini, M., and Petraglia, F. (2004). The treatment with a COX-2 specific inhibitor is effective in the management of pain related to endometriosis. Eur. J. Obstet. Gynecol. Reprod. Biol. 116, 100–102.
The treatment with a COX-2 specific inhibitor is effective in the management of pain related to endometriosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmt1Wlt7c%3D&md5=ea43f9d491634c3012490811ca5736d3CAS |

Demers, L. M., Yoshinaga, K., and Greep, R. O. (1974). Prostaglandin F in monkey uterine fluid during the menstrual cycle and following steroid treatment. Prostaglandins 5, 513–519.
Prostaglandin F in monkey uterine fluid during the menstrual cycle and following steroid treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXktlektbY%3D&md5=5bd3bc177cf7cd57f2a03c668e982e51CAS |

Dong, Z., Zhang, N., Mao, W., Liu, B., Huang, N., Li, P., Li, C., and Cao, J. (2015). Kinetic effect of oestrogen on secretion of prostaglandins E2 and F2α in bovine oviduct epithelial cells. Reprod. Fertil. Dev. , .
Kinetic effect of oestrogen on secretion of prostaglandins E2 and F in bovine oviduct epithelial cells.Crossref | GoogleScholarGoogle Scholar |

Fagotti, A., Ferrandina, G., Fanfani, F., Legge, F., Lauriola, L., Gessi, M., Castelli, P., Barbieri, F., Minelli, L., and Scambia, G. (2004). Analysis of cyclooxygenase‐2 (COX‐2) expression in different sites of endometriosis and correlation with clinico‐pathological parameters. Hum. Reprod. 19, 393–397.
Analysis of cyclooxygenase‐2 (COX‐2) expression in different sites of endometriosis and correlation with clinico‐pathological parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXos1ensw%3D%3D&md5=a7bdc6e87d1be2e927453229ae3f6d80CAS |

Ferrara, N. (2004). Vascular endothelial growth factor: basic science and clinical progress. Endocr. Rev. 25, 581–611.
Vascular endothelial growth factor: basic science and clinical progress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Ght74%3D&md5=ec34cfef979abba25b32e3764592bdf4CAS |

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=23453c686531ddf8ce582b3a5372adb3CAS |

Fowler, J. M., Ramirez, N., Cohn, D. E., Kelbick, N., Pavelka, J., Ben-Shachar, I., and Morrison, C. (2005). Correlation of cyclooxygenase-2 (COX-2) and aromatase expression in human endometrial cancer: tissue microarray analysis. Am. J. Obstet. Gynecol. 192, 1262–1271.
Correlation of cyclooxygenase-2 (COX-2) and aromatase expression in human endometrial cancer: tissue microarray analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtVyltb8%3D&md5=1f6dffd7ba8dcfc115911747e156b8bfCAS |

Gao, J., Niwa, K., Takemura, M., Sun, W., Onogi, K., Wu, Y., Seishima, M., Mori, H., and Tamaya, T. (2005). Significant anti-proliferation of human endometrial cancer cells by combined treatment with a selective COX-2 inhibitor NS398 and specific MEK inhibitor U0126. Int. J. Oncol. 26, 737–744.
| 1:CAS:528:DC%2BD2MXisVeqtr0%3D&md5=08901d57f79c2287492201e7396099edCAS |

Hertrampf, T., Schmidt, S., Laudenbach-Leschowsky, U., Seibel, J., and Diel, P. (2005). Tissue-specific modulation of cyclooxygenase-2 (Cox-2) expression in the uterus and the v. cava by estrogens and phytoestrogens. Mol. Cell. Endocrinol. 243, 51–57.
Tissue-specific modulation of cyclooxygenase-2 (Cox-2) expression in the uterus and the v. cava by estrogens and phytoestrogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1SqsbbK&md5=30dde51295a2379af6800efcaef62cf4CAS |

Horsley, V., and Pavlath, G. K. (2003). Prostaglandin F2 alpha stimulates growth of skeletal muscle cells via an NFATC2-dependent pathway. J. Cell Biol. 161, 111–118.
Prostaglandin F2 alpha stimulates growth of skeletal muscle cells via an NFATC2-dependent pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtVait7o%3D&md5=77ff0f60fae738957dcb27eda06e2809CAS |

Hsu, J.-Y. C., McKeon, R., Goussev, S., Werb, Z., Lee, J.-U., Trivedi, A., and Noble-Haeusslein, L. J. (2006). Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury. J. Neurosci. 26, 9841–9850.
Matrix metalloproteinase-2 facilitates wound healing events that promote functional recovery after spinal cord injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtVOmtLjE&md5=da896f445be0edb198ca4d1c3f10a90dCAS |

Huang, N., Liu, B., Dong, Z. H., Mao, W., Zhang, N., Li, C. Y., and Cao, J. S. (2015). Prostanoid receptors EP2, EP4, and FP are regulated by estradiol in bovine oviductal smooth muscle. Prostaglandins Other Lipid Mediat. 121, 170–175.
Prostanoid receptors EP2, EP4, and FP are regulated by estradiol in bovine oviductal smooth muscle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVGnsLjL&md5=a622b37d66eeaa072eaa752e4d23a9c6CAS |

Husain, S., Jafri, F., and Crosson, C. E. (2005). Acute effects of PGF(2 alpha) on MMP-2 secretion from human ciliary muscle cells: a PKC- and ERK-dependent process. Invest. Ophthalmol. Vis. Sci. 46, 1706–1713.
Acute effects of PGF(2 alpha) on MMP-2 secretion from human ciliary muscle cells: a PKC- and ERK-dependent process.Crossref | GoogleScholarGoogle Scholar |

Ireland, J. J., Murphee, R. L., and Coulson, P. B. (1980). Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum. J. Dairy Sci. 63, 155–160.
Accuracy of predicting stages of bovine estrous cycle by gross appearance of the corpus luteum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3c7ot1yjsg%3D%3D&md5=10dd5fac037a21ad9544584cb52e103dCAS |

Jones, R. L., Stoikos, C., Findlay, J. K., and Salamonsen, L. A. (2006). TGF-beta superfamily expression and actions in the endometrium and placenta. Reproduction 132, 217–232.
TGF-beta superfamily expression and actions in the endometrium and placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xpt1Wjsrs%3D&md5=8ee2e422e2c5b24a6bcc42c2f6a99690CAS |

Kaczynski, P., and Waclawik, A. (2013). Effect of conceptus on expression of prostaglandin F2 alpha receptor in the porcine endometrium. Theriogenology 79, 784–790.
Effect of conceptus on expression of prostaglandin F2 alpha receptor in the porcine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXovFGgsQ%3D%3D&md5=625f5e8d6fdd89659e90b1ee115dacedCAS |

Kaczynski, P., Kowalewski, M. P., and Waclawik, A. (2016). Prostaglandin F2 alpha promotes angiogenesis and embryo–maternal interactions during implantation. Reproduction 151, 539–552.
Prostaglandin F2 alpha promotes angiogenesis and embryo–maternal interactions during implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVOgs73J&md5=97d7d5e007c013f3d04b6c387f5726e0CAS |

Kizaki, K., Ushizawa, K., Takahashi, T., Yamada, O., Todoroki, J., Sato, T., Ito, A., and Hashizume, K. (2008). Gelatinase (MMP-2 and-9) expression profiles during gestation in the bovine endometrium. Reprod. Biol. Endocrinol. 6, 66.
Gelatinase (MMP-2 and-9) expression profiles during gestation in the bovine endometrium.Crossref | GoogleScholarGoogle Scholar |

Kurihara, Y., Hatori, M., Ando, Y., Ito, D., Toyoshima, T., Tanaka, M., and Shintani, S. (2009). Inhibition of cyclooxygenase-2 suppresses the invasiveness of oral squamous cell carcinoma cell lines via down-regulation of matrix metalloproteinase-2 production and activation. Clin. Exp. Metastasis 26, 425–432.
Inhibition of cyclooxygenase-2 suppresses the invasiveness of oral squamous cell carcinoma cell lines via down-regulation of matrix metalloproteinase-2 production and activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmtVKgsLg%3D&md5=232177ca51b7d908ca9419012e98ededCAS |

Lash, G. E., Innes, B. A., Drury, J. A., Robson, S. C., Quenby, S., and Bulmer, J. N. (2012). Localization of angiogenic growth factors and their receptors in the human endometrium throughout the menstrual cycle and in recurrent miscarriage. Hum. Reprod. 27, 183–195.
Localization of angiogenic growth factors and their receptors in the human endometrium throughout the menstrual cycle and in recurrent miscarriage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Cqtr3E&md5=0dd9f97c1f2ec9e34be4cd874829577dCAS |

Liang, Y., Li, C., Guzman, V. M., Evinger, A. J., Protzman, C. E., Krauss, A. H. P., and Woodward, D. F. (2003). Comparison of prostaglandin F2 alpha, bimatoprost (prostamide), and butaprost (EP2 agonist) on Cyr61 and connective tissue growth factor gene expression. J. Biol. Chem. 278, 27267–27277.
Comparison of prostaglandin F2 alpha, bimatoprost (prostamide), and butaprost (EP2 agonist) on Cyr61 and connective tissue growth factor gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlOjsrs%3D&md5=2b49804a7a4caf9efc2e77e5a194e550CAS |

Lin, H. Y., Qian, D., Zhang, X., Liu, G. Y., Wang, H. M., and Zhu, C. (2006). Gene expression of transforming growth factor-beta receptors types I and II in rat endometrium during the estrous cycle and early pregnancy. Life Sci. 78, 2669–2675.
Gene expression of transforming growth factor-beta receptors types I and II in rat endometrium during the estrous cycle and early pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjvValtrw%3D&md5=c05ff04e3a88e23ee2a39d3e19e3a83dCAS |

Machado, D. E., Berardo, P. T., Landgraf, R. G., Fernandes, P. D., Palmero, C., Alves, L. M., Abrao, M. S., and Nasciutti, L. E. (2010). A selective cyclooxygenase-2 inhibitor suppresses the growth of endometriosis with an antiangiogenic effect in a rat model. Fertil. Steril. 93, 2674–2679.
A selective cyclooxygenase-2 inhibitor suppresses the growth of endometriosis with an antiangiogenic effect in a rat model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1aru70%3D&md5=24994aadcd7122bb3a1c57f26b3daa51CAS |

Maybin, J. A., Hirani, N., Brown, P., Jabbour, H. N., and Critchley, H. O. D. (2011a). The regulation of vascular endothelial growth factor by hypoxia and prostaglandin F2 alpha during human endometrial repair. J. Clin. Endocrinol. Metab. 96, 2475–2483.
The regulation of vascular endothelial growth factor by hypoxia and prostaglandin F2 alpha during human endometrial repair.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVKhsb7N&md5=1239fd0ad1fa220aac9c395490501181CAS |

Maybin, J. A., Hirani, N., Jabbour, H. N., and Critchley, H. O. D. (2011b). Novel roles for hypoxia and prostaglandin E2 in the regulation of IL-8 during endometrial repair. Am. J. Pathol. 178, 1245–1256.
Novel roles for hypoxia and prostaglandin E2 in the regulation of IL-8 during endometrial repair.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXktFansbg%3D&md5=c127eda3f569fb20645c4f0ff76f628fCAS |

Maybin, J. A., Barcroft, J., Thiruchelvam, U., Hirani, N., Jabbour, H. N., and Critchley, H. O. D. (2012). The presence and regulation of connective tissue growth factor in the human endometrium. Hum. Reprod. 27, 1112–1121.
The presence and regulation of connective tissue growth factor in the human endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XksVarsLg%3D&md5=b22a5ceba3dbb6ba9ce22d0497102259CAS |

Meinel, A., Leo, C., Zimmermann, G., Alexander, H., and Horn, L. (2008). COX-2 is overexpressed in ovarian endometriosis and might represent a therapeutic target. Geburtshilfe Frauenheilkd 68, FV_Endo_01_03.

Meola, J., Rosa e Silva, J. C., Dentillo, D. B., da Silva, W. A., Veiga-Castelli, L. C., Bernardes, L. A. S., Ferriani, R. A., de Paz, C. C. P., Giuliatti, S., and Martelli, L. (2010). Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis. Fertil. Steril. 93, 1750–1773.
Differentially expressed genes in eutopic and ectopic endometrium of women with endometriosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsVOis7c%3D&md5=f8a5a55fa96e3fa8d568fba10d9a739bCAS |

Milne, S. A., and Jabbour, H. N. (2003). Prostaglandin (PG) F(2 alpha) receptor expression and signaling in human endometrium: role of PGF(2 alpha) in epithelial cell proliferation. J. Clin. Endocrinol. Metab. 88, 1825–1832.
Prostaglandin (PG) F(2 alpha) receptor expression and signaling in human endometrium: role of PGF(2 alpha) in epithelial cell proliferation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjtFCltL4%3D&md5=d0644eb957de1b036ff7f5cbe3121936CAS |

Möller, B., Rasmussen, C., Lindblom, B., and Olovsson, M. (2001). Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometrium during the menstrual cycle. Mol. Hum. Reprod. 7, 65–72.
Expression of the angiogenic growth factors VEGF, FGF-2, EGF and their receptors in normal human endometrium during the menstrual cycle.Crossref | GoogleScholarGoogle Scholar |

Mustoe, T. A., Pierce, G. F., Thomason, A., Gramates, P., Sporn, M. B., and Deuel, T. F. (1987). Accelerated healing of incisional wounds in rats induced by transforming growth factor-beta. Science 237, 1333–1336.
Accelerated healing of incisional wounds in rats induced by transforming growth factor-beta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2sXls12msr4%3D&md5=cb85d913f502aa745706dce845dd4396CAS |

Nayak, N. R., and Brenner, R. M. (2002). Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium. J. Clin. Endocrinol. Metab. 87, 1845–1855.
Vascular proliferation and vascular endothelial growth factor expression in the rhesus macaque endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFKksr4%3D&md5=dee9b5258cf1974f346e06e05abeee5eCAS |

Nishimura, K., Setoyama, T., Tsumagari, H. o., Miyata, N., Hatano, Y., Xu, L., Jisaka, M., Nagaya, T., and Yokota, K. (2006). Endogenous prostaglandins E2 and F2 alpha serve as an anti-apoptotic factor against apoptosis induced by tumor necrosis factor-alpha in mouse 3T3-L1 preadipocytes. Biosci. Biotechnol. Biochem. 70, 2145–2153.
Endogenous prostaglandins E2 and F2 alpha serve as an anti-apoptotic factor against apoptosis induced by tumor necrosis factor-alpha in mouse 3T3-L1 preadipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFSjtbfI&md5=2aca5395935a11676f73e3019584475dCAS |

Okumu, L. A., Forde, N., Mamo, S., McGettigan, P., Mehta, J. P., Roche, J. F., and Lonergan, P. (2014). Temporal regulation of fibroblast growth factors and their receptors in the endometrium and conceptus during the pre-implantation period of pregnancy in cattle. Reproduction 147, 825–834.
Temporal regulation of fibroblast growth factors and their receptors in the endometrium and conceptus during the pre-implantation period of pregnancy in cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKjurjI&md5=55fdcc55d2e4cecbab35cfe773d1f933CAS |

Omwandho, C. O. A., Konrad, L., Halis, G., Oehmke, F., and Tinneberg, H.-R. (2010). Role of TGF-beta s in normal human endometrium and endometriosis. Hum. Reprod. 25, 101–109.
Role of TGF-beta s in normal human endometrium and endometriosis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFyrsr3I&md5=715eef78f98147032010899d877be12dCAS |

Reynolds, L., Minten, M., Johnson, M., Borowicz, P., Redmer, D., Bilski, J., Kiedrowski, L., Ptak, G., Loi, P., and Grazul-Bilska, A. (2008). Vascularization and expression of fibroblast growth factor (FGF) 2 and FGF receptor (FGFR) 2 IIIc protein in endometrium, during early pregnancy in sheep. Biol. Reprod. 78, 218.

Rueda, B. R., Hendry, I. R., Tilly, J. L., and Hamernik, D. L. (1999). Accumulation of caspase-3 messenger ribonucleic acid and induction of caspase activity in the ovine corpus luteum following prostaglandin F2alpha treatment in vivo. Biol. Reprod. 60, 1087–1092.
Accumulation of caspase-3 messenger ribonucleic acid and induction of caspase activity in the ovine corpus luteum following prostaglandin F2alpha treatment in vivo.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXislegt7g%3D&md5=550e12717277a12db79a2008d2f050d8CAS |

Sales, K. J., Milne, S. A., Williams, A. R. W., Anderson, R. A., and Jabbour, H. N. (2004). Expression, localization, and signaling of prostaglandin F2 alpha receptor in human endometrial adenocarcinoma: regulation of proliferation by activation of the epidermal growth factor receptor and mitogen-activated protein kinase signaling pathways. J. Clin. Endocrinol. Metab. 89, 986–993.
Expression, localization, and signaling of prostaglandin F2 alpha receptor in human endometrial adenocarcinoma: regulation of proliferation by activation of the epidermal growth factor receptor and mitogen-activated protein kinase signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhsFOjtbg%3D&md5=a65b17765def55ecb7ec5eccea1fe4e6CAS |

Sales, K. J., List, T., Boddy, S. C., Williams, A. R. W., Anderson, R. A., Naor, Z., and Jabbour, H. N. (2005). A novel angiogenic role for prostaglandin F2 alpha–FP receptor interaction in human endometrial adenocarcinomas. Cancer Res. 65, 7707–7716.
| 1:CAS:528:DC%2BD2MXpslaiur8%3D&md5=0e562de224df92898a0bd5a51e7a3567CAS |

Shemesh, M., and Hansel, W. (1975). Levels of prostaglandin F (PGF) in bovine endometrium uterine venous, ovarian arterial and jugular plasma during the estrous cycle (38789). Proc. Soc. Exp. Biol. Med. 148, 123–126.
Levels of prostaglandin F (PGF) in bovine endometrium uterine venous, ovarian arterial and jugular plasma during the estrous cycle (38789).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2MXhtV2lsL0%3D&md5=8708256ccf073d3d3c898026545fe655CAS |

Shoda, T., Hatanaka, K., Saito, M., Majima, M., Ogino, M., Harada, Y., Nishijima, M., Katori, M., and Yamamoto, S. (1995). Induction of cyclooxygenase type-2 (COX-2) in rat endometrium at the peak of serum estradiol during the estrus cycle. Jpn. J. Pharmacol. 69, 289–291.
Induction of cyclooxygenase type-2 (COX-2) in rat endometrium at the peak of serum estradiol during the estrus cycle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsFCju7s%3D&md5=95825976582f10334cc8636d9b7645f4CAS |

Smith, S. K. (2001). Regulation of angiogenesis in the endometrium. Trends Endocrinol. Metab. 12, 147–151.
Regulation of angiogenesis in the endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXisF2ks78%3D&md5=383043b98fcc30d0a235d942ed71fcadCAS |

St-Louis, I., Singh, M., Brasseur, K., Leblanc, V., Parent, S., and Asselin, E. (2010). Expression of COX-1 and COX-2 in the endometrium of cyclic, pregnant and in a model of pseudopregnant rats and their regulation by sex steroids. Reprod. Biol. Endocrinol. 8, 103.
Expression of COX-1 and COX-2 in the endometrium of cyclic, pregnant and in a model of pseudopregnant rats and their regulation by sex steroids.Crossref | GoogleScholarGoogle Scholar |

Strutz, F., Okada, H., Lo, C. W., Danoff, T., Carone, R. L., Tomaszewski, J. E., and Neilson, E. G. (1995). Identification and characterization of a fibroblast marker: FSP1. J. Cell Biol. 130, 393–405.
Identification and characterization of a fibroblast marker: FSP1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXmvVGis7g%3D&md5=3c01c9f12d41a199fd69e3def641286aCAS |

Sun, Y., Jin, K., Xie, L., Childs, J., Mao, X., Logvinova, A., and Greenberg, D. A. (2003). VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia. J. Clin. Invest. 111, 1843–1851.
VEGF-induced neuroprotection, neurogenesis, and angiogenesis after focal cerebral ischemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvV2kur4%3D&md5=26e689c3eba7800ef5c80ebecbca4663CAS |

Tamura, M., Deb, S., Sebastian, S., Okamura, K., and Bulun, S. E. (2004). Estrogen up-regulates cyclooxygenase-2 via estrogen receptor in human uterine microvascular endothelial cells. Fertil. Steril. 81, 1351–1356.
Estrogen up-regulates cyclooxygenase-2 via estrogen receptor in human uterine microvascular endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhvFOjsrg%3D&md5=f7358f2669e2f0b372d386c8a1407d4dCAS |

Tsuboi, R., Sato, Y., and Rifkin, D. B. (1990). Correlation of cell migration, cell invasion, receptor number, proteinase production, and basic fibroblast growth factor levels in endothelial cells. J. Cell Biol. 110, 511–517.
Correlation of cell migration, cell invasion, receptor number, proteinase production, and basic fibroblast growth factor levels in endothelial cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpt1Wguw%3D%3D&md5=fdf265e4295f07e258b58a78413884b6CAS |

Ulug, U., Goldman, S., Ben-Shlomo, I., and Shalev, E. (2001). Matrix metalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F(2alpha) and indomethacin. Mol. Hum. Reprod. 7, 1187–1193.
Matrix metalloproteinase (MMP)-2 and MMP-9 and their inhibitor, TIMP-1, in human term decidua and fetal membranes: the effect of prostaglandin F(2alpha) and indomethacin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XisFOitA%3D%3D&md5=54f7feaa790ab2ce5e61e7f359b3e36fCAS |

Waclawik, A., Rivero-Muller, A., Blitek, A., Kaczmarek, M. M., Brokken, L. J. S., Watanabe, K., Rahman, N. A., and Ziecik, A. J. (2006). Molecular cloning and spatiotemporal expression of prostaglandin F synthase and microsomal prostaglandin E synthase-1 in porcine endometrium. Endocrinology 147, 210–221.
Molecular cloning and spatiotemporal expression of prostaglandin F synthase and microsomal prostaglandin E synthase-1 in porcine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptFem&md5=0ec5e9a6dbfead7aecfe66928f1ade3eCAS |

Weems, Y. S., Nett, T. M., Rispoli, L. A., Davis, T. L., Johnson, D. L., Uchima, T., Raney, A., Lennon, E., Harbert, T., Bowers, G., Tsutahara, N., Randel, R. D., and Weems, C. W. (2010). Effects of prostaglandin E and F receptor agonists in vivo on luteal function in ewes. Prostaglandins Other Lipid Mediat. 92, 67–72.
Effects of prostaglandin E and F receptor agonists in vivo on luteal function in ewes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFeqsbc%3D&md5=dd9b618a2039a1cbc553e4cb02a7d44cCAS |

Welter, H., Wollenhaupt, K., and Einspanier, R. (2004). Developmental and hormonal regulated gene expression of fibroblast growth factor 2 (FGF-2) and its receptors in porcine endometrium. J. Steroid Biochem. Mol. Biol. 88, 295–304.
Developmental and hormonal regulated gene expression of fibroblast growth factor 2 (FGF-2) and its receptors in porcine endometrium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjs1eru7c%3D&md5=79cd936bbedb642772bf18bbaafab000CAS |

Yamakoshi, S., Bai, R., Chaen, T., Ideta, A., Aoyagi, Y., Sakurai, T., Konno, T., and Imakawa, K. (2012). Expression of mesenchymal-related genes by the bovine trophectoderm following conceptus attachment to the endometrial epithelium. Reproduction 143, 377–387.
Expression of mesenchymal-related genes by the bovine trophectoderm following conceptus attachment to the endometrial epithelium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XlvFOqsb4%3D&md5=cdc3af7577b908e6d05e780fab065766CAS |