Spatiotemporal expression profile of proteases and immunological, angiogenic, hormonal and apoptotic mediators in rat placenta before and during intrauterine trophoblast migration
Juneo F. Silva A , Natália M. Ocarino B and Rogéria Serakides B C
+ Author Affiliations
- Author Affiliations
A Laboratório de Histologia Animal, Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Campus Soane Nazaré de Andrade, Rodovia Jorge Amado, Km 16, 45662-900, Ilhéus, Bahia, Brazil.
B Laboratório de Patologia, Departamento de Clínica e Cirurgia Veterinárias, Escola de Veterinária, Universidade Federal de Minas Gerais, Campus Pampulha, Avenida Antônio Carlos, 31270-901, Belo Horizonte, Minas Gerais, Brazil.
C Corresponding author. Email: serakidesufmg@gmail.com
Reproduction, Fertility and Development 29(9) 1774-1786 https://doi.org/10.1071/RD16280
Submitted: 14 July 2016 Accepted: 19 September 2016 Published: 14 October 2016
Abstract
The gene and/or protein expression of proteases and immunological, angiogenic, hormonal and apoptotic mediators was evaluated in rat placenta before and during intrauterine trophoblast migration. The depth of interstitial and endovascular intrauterine trophoblast invasion and the immunohistochemical expression of vascular endothelial growth factor (VEGF), fetal liver kinase 1 (Flk1), interferon (IFN)-γ, migration inhibitory factor (MIF), and inducible nitric oxide synthase (iNOS; also known as nitric oxide synthase (NOS) 2) were evaluated. In addition, the expression of the Vegf, Flk1, placental growth factor (Pigf), soluble fms-like tyrosine kinase 1 (sFlt1), placental lactogen 1 (Pl1), proliferin-related protein (rPlf), placental leptin (Lep), Toll-like receptor 2 (Tlr2), Toll-like receptor 4 (Tlr4), Infg, Mif, tumour necrosis factor-α (Tnf), interleukin-10 (Il10), Nos2, caspase 3 (Casp3), Bax, Bcl2, matrix metalloproteinase 2 (Mmp2) and matrix metalloproteinase 9 (Mmp9) genes was determined by real-time reverse transcription–polymerase chain reaction. At 10 days gestation, gene expression of Tlr2, Tlr4, Tnf, Infg, Il10, Casp3, Pigf, sFlt1 and Lep (P < 0.05) were higher than at 14 and/or 19 days of gestation. The beginning of intrauterine trophoblast invasion, i.e., at 14 days of gestation, coincided with higher gene and/or protein expression of MMP9, VEGF, Flk1, NOS2, MIF, BAX and rPlf compared to days 10 and 19 (P < 0.05). In contrast, gene expression of Mmp2 and Pl1 was higher at the end of trophoblast invasion compared to 10 and 14 days of gestation (P < 0.05). In conclusion, before intrauterine trophoblast migration, expression of TLRs and immunological and pro-apoptotic mediators is higher, whereas the beginning of trophoblast migration is characterised by higher expression of the pro-angiogenic factors NOS2 and MMP9. In contrast, MMP2 and PL1 expression is higher at the end of intrauterine trophoblast migration.
Additional keywords: cytokines, factors, lactogenic, rodent, trophoblastic invasion, vascular.
References
Ahmed, A., Dunk, C., Ahmad, S., and Khaliq, A. (2000). Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen: a review. Placenta 21, S16–S24.| Regulation of placental vascular endothelial growth factor (VEGF) and placenta growth factor (PIGF) and soluble Flt-1 by oxygen: a review.Crossref | GoogleScholarGoogle Scholar | 10831117PubMed |
Amin, M. A., Volpert, O. V., Woods, J. M., Kumar, P., Harlow, L. A., and Koch, A. E. (2003). Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase. Circ. Res. 93, 321–329.
| Migration inhibitory factor mediates angiogenesis via mitogen-activated protein kinase and phosphatidylinositol kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1Ohs7w%3D&md5=70f7930cdb165eadfa2595fc269d60d9CAS | 12881477PubMed |
Andraweera, P. H., Dekker, G. A., and Roberts, C. T. (2012). The vascular endothelial growth factor family in adverse pregnancy outcomes. Hum. Reprod. Update 18, 436–457.
| The vascular endothelial growth factor family in adverse pregnancy outcomes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XptVGktLw%3D&md5=520818f6a5c7e30ba30a2675d4d42e57CAS | 22495259PubMed |
Ashkar, A. A., Di Santo, J. P., and Croy, B. A. (2000). Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy. J. Exp. Med. 192, 259–270.
| Interferon gamma contributes to initiation of uterine vascular modification, decidual integrity, and uterine natural killer cell maturation during normal murine pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXkvFGiu7o%3D&md5=f8ab4c6af64fb787e40656db2add4e70CAS | 10899912PubMed |
Bevilacqua, E., and Abrahamsohn, P. A. (1994). Invasiveness of mouse trophoblastic cells in connective tissue. Acta Anat. (Basel) 150, 246–252.
| Invasiveness of mouse trophoblastic cells in connective tissue.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7ktFOmsg%3D%3D&md5=aa02c9b32c900fe9a7d9575885bf2e13CAS | 7839792PubMed |
Burton, G. J., and Jaunaiux, E. (2001). Maternal vascularisation of the human placenta: does the embryo develop in a hypoxic environment? Gynecol. Obstet. Fertil. 29, 503–508.
| Maternal vascularisation of the human placenta: does the embryo develop in a hypoxic environment?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MrivFeqsA%3D%3D&md5=a08fa828cfe6f4665e6294c2f25fbe0bCAS | 11575145PubMed |
Caluwaerts, S., Vercruysse, L., Luyten, C., and Pijnenborg, R. (2005). Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat. Placenta 26, 574–584.
| Endovascular trophoblast invasion and associated structural changes in uterine spiral arteries of the pregnant rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlvFKls7o%3D&md5=9f71cd4821bc5aee6b88bcd92d258eaaCAS | 15993707PubMed |
Cardaropoli, S., Paulesu, L., Romagnoli, R., Ietta, F., Marzioni, D., Castellucci, M., Rolfo, A., Vasario, E., Piccoli, E., and Todros, T. (2012). Macrophage migration inhibitory factor in fetoplacental tissues from preeclamptic pregnancies with or without fetal growth restriction. Clin. Dev. Immunol. 2012, 639342.
| Macrophage migration inhibitory factor in fetoplacental tissues from preeclamptic pregnancies with or without fetal growth restriction.Crossref | GoogleScholarGoogle Scholar | 22007254PubMed |
Cartwright, J. E., Holden, D. P., and Whitley, G. S. (1999). Hepatocyte growth factor regulates human trophoblast motility and invasion: a role for nitric oxide. Br. J. Pharmacol. 128, 181–189.
| Hepatocyte growth factor regulates human trophoblast motility and invasion: a role for nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmt1Wjsrk%3D&md5=2422d73a1a69663ce7ac08994a9677adCAS | 10498850PubMed |
Chakraborty, D., Rumi, M. A., Konno, T., and Soares, M. J. (2011). Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions. Proc. Natl Acad. Sci. USA 108, 16 295–16 300.
| Natural killer cells direct hemochorial placentation by regulating hypoxia-inducible factor dependent trophoblast lineage decisions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Kmtb%2FF&md5=09c265b1de857795f0ac563e3f7d52eeCAS |
Corbacho, A. M., Martinez De La Escalera, G., and Clapp, C. (2002). Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J. Endocrinol. 173, 219–238.
| Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xkt1SlsLw%3D&md5=0732f0152c8b7cd5fd3dcc985d4b26c7CAS | 12010630PubMed |
Coulam, C. B. (2000). Understanding the immunobiology of pregnancy and applying it to treatment of recurrent pregnancy loss. Early Pregnancy 4, 19–29.
| 1:CAS:528:DC%2BD3MXntlegt7w%3D&md5=195452c13845e0c78a528d0ade515b76CAS | 11719819PubMed |
Cross, J. C. (2005). How to make a placenta: mechanisms of trophoblast cell differentiation in mice: a review. Placenta 26, S3–S9.
| How to make a placenta: mechanisms of trophoblast cell differentiation in mice: a review.Crossref | GoogleScholarGoogle Scholar | 15837063PubMed |
Cross, J. C., Anson-Cartwright, L., and Scott, I. C. (2002a). Transcription factors underlying the development and endocrine functions of the placenta. Recent Prog. Horm. Res. 57, 221–234.
| Transcription factors underlying the development and endocrine functions of the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1WqtL8%3D&md5=ef1994a9b8563f444aa5bd1e77ee0b14CAS | 12017545PubMed |
Cross, J. C., Hemberger, M., Lu, Y., Nozaki, T., Whiteley, K., Masutani, M., and Adamson, S. L. (2002b). Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta. Mol. Cell. Endocrinol. 187, 207–212.
| Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Sqt78%3D&md5=b69c42339f537667754bf2af34046da3CAS | 11988329PubMed |
Erboga, M., and Kanter, M. (2015). Trophoblast cell proliferation and apoptosis in placental development during early gestation period in rats. Anal. Quant. Cytopathol. Histpathol. 37, 286–294.
| 26856113PubMed |
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 |
Flo, T. H., Ryan, L., Latz, E., Takeuchi, O., Monks, B. G., Lien, E., Halaas, O., Akira, S., Skjak-Braek, G., Golenbock, D. T., and Espevik, T. (2002). Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers. J. Biol. Chem. 277, 35 489–35 495.
| Involvement of toll-like receptor (TLR) 2 and TLR4 in cell activation by mannuronic acid polymers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xnt1Wmtbw%3D&md5=b03bfc7d388bbdc485ea81607f26c63fCAS |
Gambino, Y. P., Maymo, J. L., Perez-Perez, A., Duenas, J. L., Sanchez-Margalet, V., Calvo, J. C., and Varone, C. L. (2010). 17Beta-estradiol enhances leptin expression in human placental cells through genomic and nongenomic actions. Biol. Reprod. 83, 42–51.
| 17Beta-estradiol enhances leptin expression in human placental cells through genomic and nongenomic actions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXotlWqtL0%3D&md5=3cfeb9378f71c3928c080ae3c8fb8ad3CAS | 20237333PubMed |
Gambino, Y. P., Maymo, J. L., Perez Perez, A., Calvo, J. C., Sanchez-Margalet, V., and Varone, C. L. (2012). Elsevier Trophoblast Research Award Lecture: molecular mechanisms underlying estrogen functions in trophoblastic cells–focus on leptin expression. Placenta 33, S63–S70.
| Elsevier Trophoblast Research Award Lecture: molecular mechanisms underlying estrogen functions in trophoblastic cells–focus on leptin expression.Crossref | GoogleScholarGoogle Scholar | 22197627PubMed |
Giannice, R., Erreni, M., Allavena, P., Buscaglia, M., and Tozzi, R. (2013). Chemokines mRNA expression in relation to the macrophage migration inhibitory factor (MIF) mRNA and vascular endothelial growth factor (VEGF) mRNA expression in the microenvironment of endometrial cancer tissue and normal endometrium: a pilot study. Cytokine 64, 509–515.
| Chemokines mRNA expression in relation to the macrophage migration inhibitory factor (MIF) mRNA and vascular endothelial growth factor (VEGF) mRNA expression in the microenvironment of endometrial cancer tissue and normal endometrium: a pilot study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlCgt7zI&md5=ed8e640b90670bb8d27b4e326454160eCAS | 23985752PubMed |
Goedbloed, J. F. (1976). Embryonic and postnatal growth of rat and mouse. IV. Prenatal growth of organs and tissues: age determination, and general growth pattern. Acta Anat. (Basel) 95, 8–33.
| Embryonic and postnatal growth of rat and mouse. IV. Prenatal growth of organs and tissues: age determination, and general growth pattern.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE283kvFCjtQ%3D%3D&md5=57af544f9b955dce10a3c69e35457f98CAS | 952201PubMed |
Hammer, A. (2011). Immunological regulation of trophoblast invasion. J. Reprod. Immunol. 90, 21–28.
| Immunological regulation of trophoblast invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1ygsLc%3D&md5=1c8dd479d7f9f73ee7116b7d20f3a45bCAS | 21641660PubMed |
He, H., Venema, V. J., Gu, X., Venema, R. C., Marrero, M. B., and Caldwell, R. B. (1999). Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src. J. Biol. Chem. 274, 25 130–25 135.
| Vascular endothelial growth factor signals endothelial cell production of nitric oxide and prostacyclin through flk-1/KDR activation of c-Src.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXls1ymu70%3D&md5=d6da80ef46d69da4433724bd90ef0944CAS |
Hemberger, M., Nozaki, T., Masutani, M., and Cross, J. C. (2003). Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion. Dev. Dyn. 227, 185–191.
| Differential expression of angiogenic and vasodilatory factors by invasive trophoblast giant cells depending on depth of invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltlKjtro%3D&md5=53a898e7b7d2e4583dc90574d54f085cCAS | 12761846PubMed |
Hu, D., and Cross, J. C. (2010). Development and function of trophoblast giant cells in the rodent placenta. Int. J. Dev. Biol. 54, 341–354.
| Development and function of trophoblast giant cells in the rodent placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXltVajtbg%3D&md5=3e023f2ff2d4b4eb222ed771e10a365cCAS | 19876834PubMed |
Huang, Y. Y., Yao, X. B., Lu, X. H., Liu, H. S., and Chen, D. J. (2009). [Relationship between changes of endogenous nitric oxide synthase inhibitor and hydrolase and initiation of pre-eclampsia.] Zhonghua Fu Chan Ke Za Zhi 44, 249–252.
| 1:CAS:528:DC%2BD1MXot1ent7c%3D&md5=cd786673c0d8d220fd977d5048a7f607CAS | 19570459PubMed |
Hunt, J. S., Atherton, R. A., and Pace, J. L. (1990). Differential responses of rat trophoblast cells and embryonic fibroblasts to cytokines that regulate proliferation and class I MHC antigen expression. J. Immunol. 145, 184–189.
| 1:CAS:528:DyaK3cXltlSgtbk%3D&md5=4ac4a7ed9922ca367846479d6cca2cfaCAS | 2113554PubMed |
Hunt, J. S., Chen, H. L., and Miller, L. (1996). Tumor necrosis factors: pivotal components of pregnancy? Biol. Reprod. 54, 554–562.
| Tumor necrosis factors: pivotal components of pregnancy?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhtFCjt70%3D&md5=656a33888a3b2d99d18480001d015ab4CAS | 8835376PubMed |
Jackson, D., Volpert, O. V., Bouck, N., and Linzer, D. I. (1994). Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein. Science 266, 1581–1584.
| Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXisVGlsrc%3D&md5=db6eb5d8e84f86b06e5f6c350a5ce20aCAS | 7527157PubMed |
Jovanović Krivokuća, M., Stefanoska, I., Abu Rabi, T., Al-Abed, Y., Stošić-Grujičić, S., and Vićovac, L. (2015). Pharmacological inhibition of MIF interferes with trophoblast cell migration and invasiveness. Placenta 36, 150–159.
| Pharmacological inhibition of MIF interferes with trophoblast cell migration and invasiveness.Crossref | GoogleScholarGoogle Scholar | 25530499PubMed |
Kaufmann, P., Black, S., and Huppertz, B. (2003). Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia. Biol. Reprod. 69, 1–7.
| Endovascular trophoblast invasion: implications for the pathogenesis of intrauterine growth retardation and preeclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvFCnsbY%3D&md5=c7838723937192a0e3a8e73128783a06CAS | 12620937PubMed |
Khaliq, A., Dunk, C., Jiang, J., Shams, M., Li, X. F., Acevedo, C., Weich, H., Whittle, M., and Ahmed, A. (1999). Hypoxia down-regulates placenta growth factor, whereas fetal growth restriction up-regulates placenta growth factor expression: molecular evidence for ‘placental hyperoxia’ in intrauterine growth restriction. Lab. Invest. 79, 151–170.
| 1:CAS:528:DyaK1MXhsl2juro%3D&md5=81ef0cae4db6496993938a49cc94fbc7CAS | 10068204PubMed |
Kim, S., Lee, D. S., Watanabe, K., Furuoka, H., Suzuki, H., and Watarai, M. (2005). Interferon-gamma promotes abortion due to Brucella infection in pregnant mice. BMC Microbiol. 5, 22.
| Interferon-gamma promotes abortion due to Brucella infection in pregnant mice.Crossref | GoogleScholarGoogle Scholar | 15869716PubMed |
Knöfler, M. (2010). Critical growth factors and signalling pathways controlling human trophoblast invasion. Int. J. Dev. Biol. 54, 269–280.
| Critical growth factors and signalling pathways controlling human trophoblast invasion.Crossref | GoogleScholarGoogle Scholar | 19876833PubMed |
Koga, K., Aldo, P. B., and Mor, G. (2009). Toll-like receptors and pregnancy: trophoblast as modulators of the immune response. J. Obstet. Gynaecol. Res. 35, 191–202.
| Toll-like receptors and pregnancy: trophoblast as modulators of the immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXls1yqs7w%3D&md5=b602bf4b86adac48c6a460c7b173b586CAS | 19335792PubMed |
Lala, P. K., and Chakraborty, C. (2003). Factors regulating trophoblast migration and invasiveness: possible derangements contributing to pre-eclampsia and fetal injury. Placenta 24, 575–587.
| Factors regulating trophoblast migration and invasiveness: possible derangements contributing to pre-eclampsia and fetal injury.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkvVejsbs%3D&md5=183a43bc7035e514d33765733f77af86CAS | 12828917PubMed |
Lash, G. E., Otun, H. A., Innes, B. A., Kirkley, M., De Oliveira, L., Searle, R. F., Robson, S. C., and Bulmer, J. N. (2006). Interferon-gamma inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels. FASEB J. 20, 2512–2518.
| Interferon-gamma inhibits extravillous trophoblast cell invasion by a mechanism that involves both changes in apoptosis and protease levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1OmsLbL&md5=91ba264df230ec67aa154072796bd76dCAS | 17142800PubMed |
Lea, R. G., Riley, S. C., Antipatis, C., Hannah, L., Ashworth, C. J., Clark, D. A., and Critchley, H. O. (1999). Cytokines and the regulation of apoptosis in reproductive tissues: a review. Am. J. Reprod. Immunol. 42, 100–109.
| 1:STN:280:DyaK1MvgsVensA%3D%3D&md5=aae1d0042195cb143527a81f6d07ca95CAS | 10476692PubMed |
Lunghi, L., Ferretti, M. E., Medici, S., Biondi, C., and Vesce, F. (2007). Control of human trophoblast function. Reprod. Biol. Endocrinol. 5, 6.
| Control of human trophoblast function.Crossref | GoogleScholarGoogle Scholar | 17288592PubMed |
Lyall, F., Bulmer, J. N., Kelly, H., Duffie, E., and Robson, S. C. (1999). Human trophoblast invasion and spiral artery transformation: the role of nitric oxide. Am. J. Pathol. 154, 1105–1114.
| Human trophoblast invasion and spiral artery transformation: the role of nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXislKrs7s%3D&md5=8b53837a7539446ad7eeafc8071a962eCAS | 10233849PubMed |
Maynard, S. E., Min, J. Y., Merchan, J., Lim, K. H., Li, J., Mondal, S., Libermann, T. A., Morgan, J. P., Sellke, F. W., Stillman, I. E., Epstein, F. H., Sukhatme, V. P., and Karumanchi, S. A. (2003). Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J. Clin. Invest. 111, 649–658.
| Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhvFentbc%3D&md5=eddd7f8c3636359b1950f4060b23381aCAS | 12618519PubMed |
Nothnick, W. B., Colvin, A., Cheng, K. F., and Al-Abed, Y. (2011). Inhibition of macrophage migration inhibitory factor reduces endometriotic implant size in mice with experimentally induced disease. J. Endometr. 3, 135–142.
| 24790725PubMed |
Pavan, L., Tarrade, A., Hermouet, A., Delouis, C., Titeux, M., Vidaud, M., Therond, P., Evain-Brion, D., and Fournier, T. (2003). Human invasive trophoblasts transformed with simian virus 40 provide a new tool to study the role of PPARgamma in cell invasion process. Carcinogenesis 24, 1325–1336.
| Human invasive trophoblasts transformed with simian virus 40 provide a new tool to study the role of PPARgamma in cell invasion process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmtFKktbs%3D&md5=1307691eb2801df6a8de4abedceef21fCAS | 12807721PubMed |
Pijnenborg, R., Robertson, W. B., Brosens, I., and Dixon, G. (1981). Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta 2, 71–91.
| Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL3M7ltV2isw%3D%3D&md5=29ca54f6d3afc3cfc490f3f29a21a3aeCAS | 7010344PubMed |
Plaisier, M., Rodrigues, S., Willems, F., Koolwijk, P., van Hinsbergh, V. W., and Helmerhorst, F. M. (2007). Different degrees of vascularization and their relationship to the expression of vascular endothelial growth factor, placental growth factor, angiopoietins, and their receptors in first-trimester decidual tissues. Fertil. Steril. 88, 176–187.
| Different degrees of vascularization and their relationship to the expression of vascular endothelial growth factor, placental growth factor, angiopoietins, and their receptors in first-trimester decidual tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFGks7c%3D&md5=bea4a6c8cfffbe75f5c84c4b91aff2a5CAS | 17383647PubMed |
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=702a501304fe7b365c063897201f1e66CAS | 18854409PubMed |
Rosario, G. X., Konno, T., and Soares, M. J. (2008). Maternal hypoxia activates endovascular trophoblast cell invasion. Dev. Biol. 314, 362–375.
| Maternal hypoxia activates endovascular trophoblast cell invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhslKqtLo%3D&md5=2cd372976e5aee7915b8b0c598c3001cCAS | 18199431PubMed |
Roth, I., and Fisher, S. J. (1999). IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion. Dev. Biol. 205, 194–204.
| IL-10 is an autocrine inhibitor of human placental cytotrophoblast MMP-9 production and invasion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmslCitQ%3D%3D&md5=b26fe6061cd1d185576e2f3ab6c546d0CAS | 9882507PubMed |
Silva, J. F., and Serakides, R. (2016). Intrauterine trophoblast migration: a comparative view of humans and rodents. Cell Adh. Migr. 10, 88–110.
| Intrauterine trophoblast migration: a comparative view of humans and rodents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisVCqsbc%3D&md5=898162b86debf97aefe00c332bad6004CAS | 26743330PubMed |
Silva, J. F., Ocarino, N. M., and Serakides, R. (2014). Maternal thyroid dysfunction affects placental profile of inflammatory mediators and the intrauterine trophoblast migration kinetics. Reproduction 147, 803–816.
| Maternal thyroid dysfunction affects placental profile of inflammatory mediators and the intrauterine trophoblast migration kinetics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtVKjurjO&md5=a8e0c1781056a168a573b67ce28ff290CAS | 24534949PubMed |
Silva, J. F., Vidigal, P. N., Galvao, D. D., Boeloni, J. N., Nunes, P. P., Ocarino, N. M., Nascimento, E. F., and Serakides, R. (2012). Fetal growth restriction in hypothyroidism is associated with changes in proliferative activity, apoptosis and vascularisation of the placenta. Reprod. Fertil. Dev. 24, 923–931.
| Fetal growth restriction in hypothyroidism is associated with changes in proliferative activity, apoptosis and vascularisation of the placenta.Crossref | GoogleScholarGoogle Scholar | 22935153PubMed |
Simon, M. C., and Keith, B. (2008). The role of oxygen availability in embryonic development and stem cell function. Nat. Rev. Mol. Cell Biol. 9, 285–296.
| The role of oxygen availability in embryonic development and stem cell function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsFCksbk%3D&md5=613b01b68bb6e8b2ce218f70e6f14c3aCAS | 18285802PubMed |
Siwetz, M., Blaschitz, A., El-Heliebi, A., Hiden, U., Desoye, G., Huppertz, B., and Gauster, M. (2016). TNF-alpha alters the inflammatory secretion profile of human first trimester placenta. Lab. Invest. 96, 428–438.
| TNF-alpha alters the inflammatory secretion profile of human first trimester placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhtV2ru7g%3D&md5=72b5db5d442c80269c615ae94a941d03CAS | 26752743PubMed |
Smith, S. K., He, Y., Clark, D. E., and Charnock-Jones, D. S. (2000). Angiogenic growth factor expression in placenta. Semin. Perinatol. 24, 82–86.
| Angiogenic growth factor expression in placenta.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c7ntlWjsw%3D%3D&md5=8a1b9ab2d197809a92a9726ac2a68823CAS | 10709867PubMed |
Soares, M. J., Chakraborty, D., Karim Rumi, M. A., Konno, T., and Renaud, S. J. (2012). Rat placentation: an experimental model for investigating the hemochorial maternal–fetal interface. Placenta 33, 233–243.
| Rat placentation: an experimental model for investigating the hemochorial maternal–fetal interface.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383lvVOmtg%3D%3D&md5=a99dab489c181483c3980a2a1a06ce5aCAS | 22284666PubMed |
Sorenson, R. L., and Brelje, T. C. (1997). Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones. Horm. Metab. Res. 29, 301–307.
| Adaptation of islets of Langerhans to pregnancy: beta-cell growth, enhanced insulin secretion and the role of lactogenic hormones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltV2ruro%3D&md5=72674293fb774101c2e61b75ccbf27d0CAS | 9230352PubMed |
Takeda, K., and Akira, S. (2001). Regulation of innate immune responses by Toll-like receptors. Jpn. J. Infect. Dis. 54, 209–219.
| 1:CAS:528:DC%2BD38Xjtlyrs78%3D&md5=e1fc740be259543d0acb3a82194b8053CAS | 11862002PubMed |
Tarrade, A., Schoonjans, K., Pavan, L., Auwerx, J., Rochette-Egly, C., Evain-Brion, D., and Fournier, T. (2001). PPARgamma/RXRalpha heterodimers control human trophoblast invasion. J. Clin. Endocrinol. Metab. 86, 5017–5024.
| 1:CAS:528:DC%2BD3MXptVartLw%3D&md5=25699f3dd5897507ae3ff1ef4c6d4ba1CAS | 11600579PubMed |
Thaxton, J. E., and Sharma, S. (2010). Interleukin-10: a multi-faceted agent of pregnancy. Am. J. Reprod. Immunol. 63, 482–491.
| Interleukin-10: a multi-faceted agent of pregnancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXot1KjtL8%3D&md5=5f8be1fed2bb639d8d5d9dae8b86858fCAS | 20163400PubMed |
Toder, V., Fein, A., Carp, H., and Torchinsky, A. (2003). TNF-alpha in pregnancy loss and embryo maldevelopment: a mediator of detrimental stimuli or a protector of the fetoplacental unit? J. Assist. Reprod. Genet. 20, 73–81.
| TNF-alpha in pregnancy loss and embryo maldevelopment: a mediator of detrimental stimuli or a protector of the fetoplacental unit?Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3s7ntVSmtg%3D%3D&md5=45ad2bb105d3b49d3d21e686b7c3f300CAS | 12688591PubMed |
Toft, D. J., and Linzer, D. I. (2000). Identification of three prolactin-related hormones as markers of invasive trophoblasts in the rat. Biol. Reprod. 63, 519–525.
| Identification of three prolactin-related hormones as markers of invasive trophoblasts in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXltl2gtb0%3D&md5=6e8ec2d3e86024e726167c40011257ecCAS | 10906059PubMed |
Varanou, A., Withington, S. L., Lakasing, L., Williamson, C., Burton, G. J., and Hemberger, M. (2006). The importance of cysteine cathepsin proteases for placental development. J. Mol. Med. (Berl) 84, 305–317.
| The importance of cysteine cathepsin proteases for placental development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtVSms7Y%3D&md5=653a5c4a0e57e4d176ddcaf5b83d7054CAS | 16440214PubMed |
Veillat, V., Carli, C., Metz, C. N., Al-Abed, Y., Naccache, P. H., and Akoum, A. (2010). Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors via CD44, CD74, and MAPK signaling pathways. J. Clin. Endocrinol. Metab. 95, E403–E412.
| Macrophage migration inhibitory factor elicits an angiogenic phenotype in human ectopic endometrial cells and triggers the production of major angiogenic factors via CD44, CD74, and MAPK signaling pathways.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1arsLbK&md5=9081c2dfb1635a9b841d8362df2dd6dbCAS | 20829186PubMed |
Vercruysse, L., Caluwaerts, S., Luyten, C., and Pijnenborg, R. (2006). Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta 27, 22–33.
| Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1GhsrjP&md5=1438c958e871b137885c548ededdd0bfCAS | 16310034PubMed |
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 |
Vuorela, P., Hatva, E., Lymboussaki, A., Kaipainen, A., Joukov, V., Persico, M. G., Alitalo, K., and Halmesmaki, E. (1997). Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol. Reprod. 56, 489–494.
| Expression of vascular endothelial growth factor and placenta growth factor in human placenta.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXos1ertQ%3D%3D&md5=4036fa88911f4276ef3a2f5b3e048096CAS | 9116151PubMed |
Yelavarthi, K. K., Chen, H. L., Yang, Y. P., Cowley, B. D., Fishback, J. L., and Hunt, J. S. (1991). Tumor necrosis factor-alpha mRNA and protein in rat uterine and placental cells. J. Immunol. 146, 3840–3848.
| 1:CAS:528:DyaK3MXkt1Ontro%3D&md5=cd08b412ce521568cb74db793e30b021CAS | 2033253PubMed |
Zhang, L. J., Yang, M., and Ding, Y. L. (2007). [Bcl-2, TGFbeta1, and apoptosis in placenta tissues in patients with hypertensive disorder complicating pregnancy.] Zhong Nan Da Xue Xue Bao Yi Xue Ban 32, 883–889.
| 18007089PubMed |
