Endogenous lysophosphatidic acid participates in vascularisation and decidualisation at the maternal–fetal interface in the rat
Micaela S. Sordelli A H , Jimena S. Beltrame A , Elsa Zotta B , Natalia Gomez C , Ganna Dmytrenko D , María Elena Sales D , Sandra M. Blois E , Carlos Davio C , Silvina Perez Martinez F , Ana M. Franchi G and María L. Ribeiro A
+ Author Affiliations
- Author Affiliations
A Laboratorio de Fisiología y Farmacología de la Reproducción, Centre for Pharmacological and Botanicals Studies (CONICET – Facultad de Medicina, University of Buenos Aires), Paraguay 2155, 16th floor, Buenos Aires, Argentina.
B Laboratorio de Fisiopatología Molecular, Cátedra de Fisiopatología, Departamento de Ciencias Biológicas, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina.
C Laboratorio de Farmacología de Receptores, Departamento de Farmacología, Facultad de Farmacia y Bioquímica, Universidad de Buenos Aires, Buenos Aires, Argentina.
D Laboratorio de Inmunofarmacología Tumoral, CEFYBO (CONICET – Facultad de Medicina, UBA).
E Charité Centrum 12 für Innere Medizin und Dermatologie, Reproductive Medicine Research Group, University Medicine of Berlin, Berlin, Germany.
F Laboratorio de Biología de la Reproducción en Mamíferos, CEFYBO (CONICET – Facultad de Medicina, UBA), Buenos Aires, Argentina.
G Laboratorio de Fisiopatología de la Preñez y al Parto, CEFYBO (CONICET – Facultad de Medicina, UBA), Buenos Aires, Argentina.
H Corresponding author. Email: micaelasordelli@yahoo.com.ar
Reproduction, Fertility and Development 29(11) 2112-2126 https://doi.org/10.1071/RD16235
Submitted: 7 June 2016 Accepted: 12 January 2017 Published: 5 April 2017
Abstract
Lysophosphatidic acid (LPA) affects several female reproductive functions through G-protein-coupled receptors. LPA contributes to embryo implantation via the lysophospholipid LPA3 receptor. In the present study we investigated the participation of endogenous LPA signalling through the LPA3 receptor in vascularisation and decidualisation, two crucial events at the maternal–fetal interface. Pregnant rats were treated with diacylglycerol pyrophosphate (DGPP), a highly selective antagonist of LPA3 receptors, on Day 5 of gestation. Pregnant rats received intrauterine (i.u.) injections of single doses of DGPP (0.1 mg kg−1) in a total volume of 2 μL in the left horn (treated horn) in the morning of GD5. DGPP treatment produced aberrant embryo spacing and increased embryo resorption. The LPA3 receptor antagonist decreased the cross-sectional length of the uterine and arcuate arteries and induced histological anomalies in the decidua and placentas. Marked haemorrhagic processes, infiltration of immune cells and tissue disorganisation were observed in decidual and placental tissues from sites of resorption. The mRNA expression of three vascularisation markers, namely interleukin 10 (Il10), vascular endothelial growth factor (Vegfa) and vascular endothelial growth factor receptor 1 (Vegfr1), was reduced at sites of resorption from Day 8. The results show that the disruption of endogenous LPA signalling by blocking the LPA3 receptor modified the development of uterine vessels with consequences in the formation of the decidua and placenta and in the growth of embryos.
Additional keywords: decidua development, implantation, lysophospholipids, vascular response.
References
Achache, H., Tsafrir, A., Prus, D., Reich, R., and Revel, A. (2010). Defective endometrial prostaglandin synthesis identified in patients with repeated implantation failure undergoing in vitro fertilization. Fertil. Steril. 94, 1271–1278.| Defective endometrial prostaglandin synthesis identified in patients with repeated implantation failure undergoing in vitro fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVyrtLjL&md5=b4ac5e8ab796b716054c831c57288685CAS |
Aikawa, S., Hashimoto, T., Kano, K., and Aoki, J. (2015). Lysophosphatidic acid as a lipid mediator with multiple biological actions. J. Biochem. 157, 81–89.
| Lysophosphatidic acid as a lipid mediator with multiple biological actions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XntVSksLc%3D&md5=aeb4f75d6879a3121dc4658026e667a1CAS |
Aisemberg, J., Vercelli, C., Billi, S., Ribeiro, M. L., Ogando, D., Meiss, R., McCann, S. M., Rettori, V., and Franchi, A. M. (2007). Nitric oxide mediates prostaglandins’ deleterious effect on lipopolysaccharide-triggered murine fetal resorption Proc. Natl Acad. Sci. USA 104, 7534–7539.
| Nitric oxide mediates prostaglandins’ deleterious effect on lipopolysaccharide-triggered murine fetal resorptionCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlslWqt7k%3D&md5=e55b60c80adb6aac70d58fdc0e99902eCAS |
Beltrame, J. S., Sordelli, M. S., Cella, M., Perez Martinez, S., Franchi, A. M., and Ribeiro, M. L. (2013). Lysophosphatidic acid increases the production of pivotal mediators of decidualization and vascularization in the rat uterus. Placenta 34, 751–756.
| Lysophosphatidic acid increases the production of pivotal mediators of decidualization and vascularization in the rat uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvVynur0%3D&md5=cce0558a4b70d27736fb81976657a935CAS |
Blois, S. M., Klapp, B. F., and Barrientos, G. (2011). Decidualization and angiogenesis in early pregnancy: unravelling the functions of DC and NK cells. J. Reprod. Immunol. 88, 86–92.
| Decidualization and angiogenesis in early pregnancy: unravelling the functions of DC and NK cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjs12jtr8%3D&md5=ebef91e148bbfea8f3a13ccf863b42fbCAS |
Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248–254.
| A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=d166069944bf0e551b4658d7addafd30CAS |
Burdet, J., Zotta, E., Franchi, A. M., and Ibarra, C. (2009). Intraperitoneal administration of shiga toxin type 2 in rats in the late stage of pregnancy produces premature delivery of dead fetuses. Placenta 30, 491–496.
| Intraperitoneal administration of shiga toxin type 2 in rats in the late stage of pregnancy produces premature delivery of dead fetuses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXms12ntr8%3D&md5=baa9802004c42e47f73cb606630468b9CAS |
Chen, S. U., Lee, H., Chang, D. Y., Chou, C. H., Chang, C. Y., Chao, K. H., Lin, C. W., and Yang, Y. S. (2008). Lysophosphatidic acid mediates interleukin-8 expression in human endometrial stromal cells through its receptor and nuclear factor-kappaB-dependent pathway: a possible role in angiogenesis of endometrium and placenta. Endocrinology 149, 5888–5896.
| Lysophosphatidic acid mediates interleukin-8 expression in human endometrial stromal cells through its receptor and nuclear factor-kappaB-dependent pathway: a possible role in angiogenesis of endometrium and placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWnsrfJ&md5=45064b5fc434650e204382456a99a8b1CAS |
Chen, S. U., Chou, C. H., Chao, K. H., Lee, H., Lin, C. W., Lu, H. F., and Yang, Y. S. (2010). Lysophosphatidic acid up-regulates expression of growth-regulated oncogene-alpha, interleukin-8, and monocyte chemoattractant protein-1 in human first-trimester trophoblasts: possible roles in angiogenesis and immune regulation. Endocrinology 151, 369–379.
| Lysophosphatidic acid up-regulates expression of growth-regulated oncogene-alpha, interleukin-8, and monocyte chemoattractant protein-1 in human first-trimester trophoblasts: possible roles in angiogenesis and immune regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXls1Gitg%3D%3D&md5=8dafb86014b2f2a24e852a52b2b840d7CAS |
Chou, C. H., Wei, L. H., Kuo, M. L., Huang, Y. L., Lai, K. P., Chen, C. A., and Hsieh, C. Y. (2005). Up-regulation of interleukin-6 in human ovarian cancer cell via a Gi/PI3K–Akt/NF-kB pathway by lysophosphatidic acid, an ovarian cancer-activating factor. Carcinogenesis 26, 45–52.
| Up-regulation of interleukin-6 in human ovarian cancer cell via a Gi/PI3K–Akt/NF-kB pathway by lysophosphatidic acid, an ovarian cancer-activating factor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVSmuw%3D%3D&md5=5b332d55da0e3c8b0fc30b0bed5e4353CAS |
de la Torre, E., Hovsepian, E., Penas, F. N., Dmytrenko, G., Castro, M. E., Goren, N. B., and Sales, M. E. (2013). Macrophages derived from septic mice modulate nitric oxide synthase and angiogenic mediators in the heart. J. Cell. Physiol. 228, 1584–1593.
| Macrophages derived from septic mice modulate nitric oxide synthase and angiogenic mediators in the heart.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktleqs7Y%3D&md5=792664b470028ca71594bc8b2a8f656aCAS |
Demir, R., Yaba, A., and Huppertz, B. (2010). Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation. Acta Histochem. 112, 203–214.
| Vasculogenesis and angiogenesis in the endometrium during menstrual cycle and implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVehtLo%3D&md5=9d1a36daf5f2df7fd0bb8c6b3340066fCAS |
Dey, S. K., Lim, H., Das, S. K., Reese, J., Paria, B. C., Daikoku, T., and Wang, H. (2004). Molecular cues to implantation. Endocr. Rev. 25, 341–373.
| Molecular cues to implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvVeltL8%3D&md5=de9713be8ad70e7bc8e0418727b0898cCAS |
Diao, H., Li, R., El Zowalaty, A. E., Xiao, S., Zhao, F., Dudley, E. A., and Ye, X. (2015). Deletion of lysophosphatidic acid receptor 3 (Lpar3) disrupts fine local balance of progesterone and estrogen signaling in mouse uterus during implantation. Biol. Reprod. 93, 123.
| Deletion of lysophosphatidic acid receptor 3 (Lpar3) disrupts fine local balance of progesterone and estrogen signaling in mouse uterus during implantation.Crossref | GoogleScholarGoogle Scholar |
Fonseca, B. M., Correia-da-Silva, G., and Teixeira, N. A. (2012). The rat as an animal model for fetoplacental development: a reappraisal of the post-implantation period. Reprod. Biol. 12, 97–118.
| The rat as an animal model for fetoplacental development: a reappraisal of the post-implantation period.Crossref | GoogleScholarGoogle Scholar |
Fonseca, B. M., Almada, M., Costa, M. A., Teixeira, N. A., and Correia-da-Silva, G. (2014). Rat spontaneous foetal resorption: altered α2-macroglobulin levels and uNK cell number. Histochem. Cell. Biol. 142, 693–701.
| Rat spontaneous foetal resorption: altered α2-macroglobulin levels and uNK cell number.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1OqtLjO&md5=7970d14880267714f71ffe83a1420543CAS |
Freitag, N., Tirado-González, I., Barrientos, G., Herse, F., Thijssen, V. L., Weedon-Fekjær, S. M., Schulz, H., Wallukat, G., Klapp, B. F., Nevers, T., Sharma, S., Staff, A. C., Dechend, R., and Blois, S. M. (2013). Interfering with Gal-1-mediated angiogenesis contributes to the pathogenesis of preeclampsia. Proc. Natl. Acad. Sci. USA 110, 11451–11456.
| Interfering with Gal-1-mediated angiogenesis contributes to the pathogenesis of preeclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1Gntr%2FM&md5=a92161ce3612199dda1bd38bff7ebebfCAS |
Fukushima, N., Ishii, S., Tsujiuchi, T., Kagawa, N., and Katoh, K. (2015). Comparative analyses of lysophosphatidic acid receptor-mediated signaling. Cell. Mol. Life Sci. 72, 2377–2394.
| Comparative analyses of lysophosphatidic acid receptor-mediated signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjs1Kmsbs%3D&md5=d37bb910514c0cca49368b28d3b95566CAS |
Gellersen, B., and Brosens, J. J. (2014). Cyclic decidualization of the human endometrium in reproductive health and failure. Endocr. Rev. 35, 851–905.
| Cyclic decidualization of the human endometrium in reproductive health and failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXnslaisg%3D%3D&md5=663e7014c16afa12cfffad6c003d4ba7CAS |
Hama, K., Aoki, J., Inoue, A., Endo, T., Amano, T., Motoki, R., Kanai, M., Ye, X., Chun, J., Matsuki, N., Shibasaki, M., and Arai, H. (2007). Embryo spacing and implantation timing are differentially regulated by LPA3-mediated lysophosphatidic acid signaling in mice. Biol. Reprod. 77, 954–959.
| Embryo spacing and implantation timing are differentially regulated by LPA3-mediated lysophosphatidic acid signaling in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVSgtLnJ&md5=cce84a3fbb887ef411466f285fc2a5b8CAS |
Hu, Y. L., Tee, M. K., Goetzl, E. J., Auersperg, N., Mills, G. B., Ferrara, N., and Jaffe, R. B. (2001). Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells. J. Natl. Cancer Inst. 93, 762–767.
| Lysophosphatidic acid induction of vascular endothelial growth factor expression in human ovarian cancer cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkt1OktLw%3D&md5=d29ad7b9c8d9fc195bc778a7dca158a9CAS |
Ishii, I., Fukushima, N., Ye, X., and Chun, J. (2004). Lysophosphatidic receptors: signaling and biology. Annu. Rev. Biochem. 73, 321–354.
| Lysophosphatidic receptors: signaling and biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmslags7g%3D&md5=995f183bd5ff92d9bdd4b9fee393e224CAS |
Kano, K., Arima, N., Ohgami, M., and Aoki, J. (2008). LPA and its analogs – attractive tools for elucidation of LPA biology and drug development. Curr. Med. Chem. 15, 2122–2131.
| LPA and its analogs – attractive tools for elucidation of LPA biology and drug development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSrs7fJ&md5=5597a9eb4a869b2bdda6c54dce67a8a6CAS |
Kobayashi, T., Yamano, S., Tokumura, A., and Aono, T. (1994). Effect of lysophosphatidic acid on the preimplantation development of mouse embryos. FEBS Lett. 351, 38–40.
| Effect of lysophosphatidic acid on the preimplantation development of mouse embryos.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXlslGqt7Y%3D&md5=7f1064de552da74a12e627f8dcb006c8CAS |
Kunikata, K., Yamano, S., Tokumura, A., and Aono, T. (1999). Effect of lysophosphatidic acid on the ovum transport in mouse oviducts. Life Sci. 65, 833–840.
| Effect of lysophosphatidic acid on the ovum transport in mouse oviducts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkvV2hsLk%3D&md5=1d2aac7a0a1a3f42c86f38cf1da9fad4CAS |
Lim, H. J., and Wang, H. (2010). Uterine disorders and pregnancy complications: insights from mouse models. J. Clin. Invest. 120, 1004–1015.
| Uterine disorders and pregnancy complications: insights from mouse models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXksVChs78%3D&md5=80c76ceae420ca09ceb498bd84a2f750CAS |
Lin, C. I., Chen, C. N., Huang, M. T., Lee, S. J., Lin, C. H., Chang, C. C., and Lee, H. (2008). Lysophosphatidic acid upregulates vascular endothelial growth factor-C and tube formation in human endothelial cells through LPA1/3, COX-2, and NF-κB activation- and EGFR transactivation-dependent mechanisms. Cell. Signal. 20, 1804–1814.
| Lysophosphatidic acid upregulates vascular endothelial growth factor-C and tube formation in human endothelial cells through LPA1/3, COX-2, and NF-κB activation- and EGFR transactivation-dependent mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVejt7rM&md5=3b798586a5654022c8efe8a542d69c83CAS |
Ogando, D. G., Paz, D., Cella, M., and Franchi, A. M. (2003). The fundamental role of increased production of nitric oxide in lipopolysaccharide-induced embryonic resorption in mice. Reproduction 125, 95–110.
| The fundamental role of increased production of nitric oxide in lipopolysaccharide-induced embryonic resorption in mice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFGls7c%3D&md5=a658259ae80b99d455084794aeca8769CAS |
Plaisier, M., Dennert, I., Rost, E., Koolwijk, P., van Hinsbergh, V. W., and Helmerhorst, F. M. (2009). Decidual vascularization and the expression of angiogenic growth factors and proteases in first trimester spontaneous abortions. Hum. Reprod. 24, 185–197.
| Decidual vascularization and the expression of angiogenic growth factors and proteases in first trimester spontaneous abortions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWjtbbK&md5=5a69897f859207feb52e89706a4c3356CAS |
Pontillo, C., Español, A., Chiappini, F., Miret, N., Cocca, C., Alvarez, L., Kleiman de Pisarev, D., Sales, M. E., and Randi, A. S. (2015). Hexachlorobenzene promotes angiogenesis in vivo, in a breast cancer model and neovasculogenesis in vitro, in the human microvascular endothelial cell line HMEC-1. Toxicol. Lett. 239, 53–64.
| Hexachlorobenzene promotes angiogenesis in vivo, in a breast cancer model and neovasculogenesis in vitro, in the human microvascular endothelial cell line HMEC-1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsV2jtbjL&md5=4572a06b2195657c6bb2183f8d92e4eaCAS |
Ribeiro, M. L., Aisemberg, J., Billi, S., Farina, M. G., Meiss, R., McCann, S., Rettori, V., Villalón, M., and Franchi, A. M. (2005). Epidermal growth factor prevents prepartum luteolysis in the rat. Proc. Natl Acad. Sci. USA 102, 8048–8053.
| Epidermal growth factor prevents prepartum luteolysis in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkvF2is78%3D&md5=c7d69fd3830df4ef8af6f78be4abb92eCAS |
Sacerdoti, F., Amaral, M. M., Aisemberg, J., Cymeryng, C. B., Franchi, A. M., and Ibarra, C. (2015). Involvement of hypoxia and inflammation in early pregnancy loss mediated by Shiga toxin type 2. Placenta 36, 674–680.
| Involvement of hypoxia and inflammation in early pregnancy loss mediated by Shiga toxin type 2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXlt1ajsrY%3D&md5=e0f060374b26bc78d0c8fcc65f9cbc66CAS |
Sharkey, A. M., Day, K., McPherson, A., Malik, S., Licence, D., Smith, S. K., and Charnock Jones, D. S. (2000). Vascular endothelial growth factor expression in humane endometrium is regulated by hypoxia. J. Clin. Endocrinol. Metab. 85, 402–409.
| 1:CAS:528:DC%2BD3cXjtl2ksg%3D%3D&md5=fbb1ed8040a710bb193a33b01daee0a5CAS |
Shimizu, T., Hoshino, Y., Miyazaki, H., and Sato, E. (2012). Angiogenesis and microvasculature in the female reproductive organs: physiological and pathological implications. Curr. Pharm. Des. 18, 303–309.
| Angiogenesis and microvasculature in the female reproductive organs: physiological and pathological implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjtV2htL0%3D&md5=26bd01c48970010f775fcddf7e93d34bCAS |
Skoura, A., and Hla, T. (2009). Lysophospholipid receptors in vertebrate development, physiology, and pathology. J. Lipid Res. 50, S293–S298.
| Lysophospholipid receptors in vertebrate development, physiology, and pathology.Crossref | GoogleScholarGoogle Scholar |
So, J., Navari, J., Wang, F. Q., and Fishman, D. A. (2004). Lysophosphatidic acid enhances epithelial ovarian carcinoma invasion through the increased expression of interleukin-8. Gynecol. Oncol. 95, 314–322.
| Lysophosphatidic acid enhances epithelial ovarian carcinoma invasion through the increased expression of interleukin-8.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXos1eitr8%3D&md5=a246e1338c133e6119722409aec5c221CAS |
Sordelli, M. S., Beltrame, J. S., Cella, M., Gervasi, M. G., Perez Martinez, S., Burdet, J., Zotta, E., Franchi, A. M., and Ribeiro, M. L. (2012). Interaction between lysophosphatidic acid, prostaglandins and the endocannabinoid system during the window of implantation in the rat uterus. PLoS One 7, e46059.
| Interaction between lysophosphatidic acid, prostaglandins and the endocannabinoid system during the window of implantation in the rat uterus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsFWgsbzO&md5=382d87544fec555597401e9333982fbeCAS |
Tokumura, A., Yamano, S., Aono, T., and Fukuzawa, K. (2000). Lysophosphatidic acids produced by lysophospholipase D in mammalian serum and body fluid. Ann. N. Y. Acad. Sci. 905, 347–350.
| Lysophosphatidic acids produced by lysophospholipase D in mammalian serum and body fluid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFCgtrs%3D&md5=6b2ce85f6d5e61183c293e743af7ae77CAS |
Tokumura, A., Kanaya, Y., Miyake, M., Yamano, S., Irahara, M., and Fukuzawa, K. (2002). Increased production of bioactive lysophosphatidic acid by serum lysophospholipase D in human pregnancy. Biol. Reprod. 67, 1386–1392.
| Increased production of bioactive lysophosphatidic acid by serum lysophospholipase D in human pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xot1Kjsr8%3D&md5=5170f4866941ed4c08ff2efe802ac4c0CAS |
Torry, D. S., Leavenworth, J., Chang, M., Maheshwari, V., Groesch, K., Ball, E. R., and Torry, R. J. (2007). Angiogenesis in implantation. J. Assist. Reprod. Genet. 24, 303–315.
| Angiogenesis in implantation.Crossref | GoogleScholarGoogle Scholar |
Wei, Q., St Clair, J. B., Fu, T., Stratton, P., and Nieman, L. K. (2009). Reduced expression of biomarkers associated with the implantation window in women with endometriosis. Fertil. Steril. 91, 1686–1691.
| Reduced expression of biomarkers associated with the implantation window in women with endometriosis.Crossref | GoogleScholarGoogle Scholar |
Ye, X. (2008). Lysophospholipid signaling in the function and pathology of the reproductive system. Hum. Reprod. Update 14, 519–536.
| Lysophospholipid signaling in the function and pathology of the reproductive system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtVSitrfK&md5=59a93a34d7d5d5c5048ed64a73950c4aCAS |
Ye, X., Hama, K., Contos, J. J., Anliker, B., Inoue, A., Skinner, M. K., Suzuki, H., Amano, T., Kennedy, G., Arai, H., Aoki, J., and Chun, J. (2005). LPA3-mediated lysophosphatidic acid signalling in implantation and embryo spacing. Nature 435, 104–108.
| LPA3-mediated lysophosphatidic acid signalling in implantation and embryo spacing.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjvVKnur8%3D&md5=992ca4edcf8d6bd8e07c113eebc0720fCAS |
Ye, X., Herr, D. R., Diao, H., Rivera, R., and Chun, J. (2011). Unique uterine localization and regulation may differentiate LPA3 from other lysophospholipid receptors for its role in embryo implantation. Fertil. Steril. 95, 2107–2113.e4.
| Unique uterine localization and regulation may differentiate LPA3 from other lysophospholipid receptors for its role in embryo implantation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXltFymtb0%3D&md5=98e159de09abb772d31442fb26dbe2adCAS |
Zhou, Z., Niu, J., and Zhang, Z. (2010). The role of lysophosphatidic acid receptors in phenotypic modulation of vascular smooth muscle cells. Mol. Biol. Rep. 37, 2675–2686.
| The role of lysophosphatidic acid receptors in phenotypic modulation of vascular smooth muscle cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosFClu7w%3D&md5=b55bddb3b7b797efd3e57ac7c07a79d9CAS |
