Faure, Mélanie ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Neuroendocrinology ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques
Sicard, Pierre
Raymond-Letron, Isabelle
Giton, Frank
Vessieres, Emilie
Prévot, Vincent
Henrion, Daniel
Arnal, Jean-François
Cornil, Charlotte ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques ; Université de Liège - ULiège > GIGA > GIGA Neurosciences - Neuroendocrinology
Lenfant, Françoise
Langue du document :
Anglais
Titre :
Loss of function of the maternal membrane oestrogen receptor ERα alters expansion of trophoblast cells and impacts mouse fertility
Date de publication/diffusion :
2022
Titre du périodique :
Development
ISSN :
0950-1991
eISSN :
1477-9129
Maison d'édition :
The Company of Biologists, Cambridge, Royaume-Uni
Volume/Tome :
149
Fascicule/Saison :
19
Pagination :
dev200683
Peer reviewed :
Peer reviewed vérifié par ORBi
Organisme subsidiant :
F.R.S.-FNRS - Fonds de la Recherche Scientifique ULiège - University of Liège ANR - Agence Nationale de la Recherche INSERM - Institut National de la Santé et de la Recherche Médicale
Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C. and Cross, J. C. (2002). Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev. Biol. 250, 358-373. doi:10.1006/ dbio.2002.0773
Adlanmerini, M., Solinhac, R., Abot, A., Fabre, A., Raymond-Letron, I., Guihot, A.-L., Boudou, F., Sautier, L., Vessieres, ̀ E., Kim, S. H. et al. (2014). Mutation of the palmitoylation site of estrogen receptor α in vivo reveals tissue-specific roles for membrane versus nuclear actions. Proc. Natl. Acad. Sci. USA 111, E283-E290. doi:10.1073/pnas.1322057111
Adlanmerini, M., Fébrissy, C., Zahreddine, R., Vessieres, ̀ E., Buscato, M., Solinhac, R., Favre, J., Anquetil, T., Guihot, A.-L., Boudou, F. et al. (2020). Mutation of Arginine 264 on ERα (Estrogen Receptor Alpha) selectively abrogates the rapid signaling of estradiol in the endothelium without altering fertility. Arterioscler. Thromb. Vasc. Biol. 40, 2143-2158. doi:10.1161/ATVBAHA.120. 314159
Albrecht, E. D. and Pepe, G. J. (2010). Estrogen regulation of placental angiogenesis and fetal ovarian development during primate pregnancy. Int. J. Dev. Biol. 54, 397-408. doi:10.1387/ijdb.082758ea
Albrecht, E. D., Robb, V. A. and Pepe, G. J. (2004). Regulation of placental vascular endothelial growth/permeability factor expression and angiogenesis by estrogen during early baboon pregnancy. J. Clin. Endocrinol. Metab. 89, 5803-5809. doi:10.1210/jc.2004-0479
Albrecht, E. D., Bonagura, T. W., Burleigh, D. W., Enders, A. C., Aberdeen, G. W. and Pepe, G. J. (2006). Suppression of extravillous trophoblast invasion of uterine spiral arteries by estrogen during early baboon pregnancy. Placenta 27, 483-490. doi:10.1016/j.placenta.2005.04.005
Antal, M. C., Krust, A., Chambon, P. and Mark, M. (2008). Sterility and absence of histopathological defects in nonreproductive organs of a mouse ERβ-null mutant. Proc. Natl. Acad. Sci. USA 105, 2433-2438. doi:10.1073/pnas.0712029105
Arnal, J. F., Lenfant, F., Metivier, R., Flouriot, G., Henrion, D., Adlanmerini, M., Fontaine, C., Gourdy, P., Chambon, P., Katzenellenbogen, B. et al. (2017). Membrane and nuclear estrogen receptor alpha actions: from tissue specificity to medical implications. Physiol. Rev. 97, 1045-1087. doi:10.1152/physrev.00024. 2016
Berkane, N., Liere, P., Oudinet, J.-P., Hertig, A., Lefevre, ̀ G., Pluchino, N., Schumacher, M. and Chabbert-Buffet, N. (2017). From pregnancy to preeclampsia: a key role for estrogens. Endocr. Rev. 38, 123-144. doi:10.1210/ er.2016-1065
Billon-Galés, A., Fontaine, C., Filipe, C., Douin-Echinard, V., Fouque, M. J., Flouriot, G., Gourdy, P., Lenfant, F., Laurell, H., Krust, A. et al. (2009). The transactivating function 1 of estrogen receptor alpha is dispensable for the vasculoprotective actions of 17beta-estradiol. Proc. Natl. Acad. Sci. USA 106, 2053-2058. doi:10.1073/pnas.0808742106
Billon-Galés, A., Krust, A., Fontaine, C., Abot, A., Flouriot, G., Toutain, C., Berges, H., Gadeau, A.-P., Lenfant, F., Gourdy, P. et al. (2011). Activation function 2 (AF2) of estrogen receptor-alpha is required for the atheroprotective action of estradiol but not to accelerate endothelial healing. Proc. Natl. Acad. Sci. USA 108, 13311-13316. doi:10.1073/pnas.1105632108
Bonagura, T. W., Babischkin, J. S., Aberdeen, G. W., Pepe, G. J. and Albrecht, E. D. (2012). Prematurely elevating estradiol in early baboon pregnancy suppresses uterine artery remodeling and expression of extravillous placental vascular endothelial growth factor and α1β1 and α5β1 integrins. Endocrinology 153, 2897-2906. doi:10.1210/en.2012-1141
Bukovsky, A., Caudle, M. R., Cekanova, M., Fernando, R. I., Wimalasena, J., Foster, J. S., Henley, D. C. and Elder, R. F. (2003). Placental expression of estrogen receptor beta and its hormone binding variant–comparison with estrogen receptor alpha and a role for estrogen receptors in asymmetric division and differentiation of estrogen-dependent cells. Reprod. Biol. Endocrinol. 1, 36. doi:10.1186/1477-7827-1-36
Chang, K. and Zhang, L. (2008). Review article: steroid hormones and uterine vascular adaptation to pregnancy. Reprod. Sci. 15, 336-348. doi:10.1177/ 1933719108317975
Corcoran, J. J., Nicholson, C., Sweeney, M., Charnock, J. C., Robson, S. C., Westwood, M. and Taggart, M. J. (2014). Human uterine and placental arteries exhibit tissue-specific acute responses to 17beta-estradiol and estrogen-receptor-specific agonists. Mol. Hum. Reprod. 20, 433-441. doi:10.1093/molehr/gat095
Cross, J. C., Hemberger, M., Lu, Y., Nozaki, T., Whiteley, K., Masutani, M. and Adamson, S. L. (2002). Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta. Mol. Cell. Endocrinol. 187, 207-212. doi:10.1016/S0303-7207(01)00703-1
Das, A., Mantena, S. R., Kannan, A., Evans, D. B., Bagchi, M. K. and Bagchi, I. C. (2009). De novo synthesis of estrogen in pregnant uterus is critical for stromal decidualization and angiogenesis. Proc. Natl. Acad. Sci. USA 106, 12542-12547. doi:10.1073/pnas.0901647106
David, H., Ughetto, A., Gaudard, P., Plawecki, M., Paiyabhroma, N., Zub, E., Colson, P., Richard, S., Marchi, N. and Sicard, P. (2020). Experimental myocardial infarction elicits time-dependent patterns of vascular hypoxia in peripheral organs and in the brain. Front. Cardiovasc. Med. 7, 615507. doi:10. 3389/fcvm.2020.615507
Dupont, S., Krust, A., Gansmuller, A., Dierich, A., Chambon, P. and Mark, M. (2000). Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes. Development 127, 4277-4291. doi:10.1242/dev.127.19.4277
Edey, L. F., Georgiou, H., O’Dea, K. P., Mesiano, S., Herbert, B. R., Lei, K., Hua, R., Markovic, D., Waddington, S. N., MacIntyre, D. et al. (2018). Progesterone, the maternal immune system and the onset of parturition in the mouse. Biol. Reprod. 98, 376-395. doi:10.1093/biolre/iox146
Gasperowicz, M., Surmann-Schmitt, C., Hamada, Y., Otto, F. and Cross, J. C. (2013). The transcriptional co-repressor TLE3 regulates development of trophoblast giant cells lining maternal blood spaces in the mouse placenta. Dev. Biol. 382, 1-14. doi:10.1016/j.ydbio.2013.08.005
Georgiades, P., Ferguson-Smith, A. C. and Burton, G. J. (2002). Comparative developmental anatomy of the murine and human definitive placentae. Placenta 23, 3-19. doi:10.1053/plac.2001.0738
Geva, E., Ginzinger, D. G., Moore, D. H., II, Ursell, P. C. and Jaffe, R. B. (2005). In utero angiopoietin-2 gene delivery remodels placental blood vessel phenotype: a murine model for studying placental angiogenesis. Mol. Hum. Reprod. 11, 253-260. doi:10.1093/molehr/gah159
Gibson, D. A., Greaves, E., Critchley, H. O. D. and Saunders, P. T. K. (2015). Estrogen-dependent regulation of human uterine natural killer cells promotes vascular remodelling via secretion of CCL2. Hum. Reprod. 30, 1290-1301. doi:10. 1093/humrep/dev067
Giton, F., Sirab, N., Franck, G., Gervais, M., Schmidlin, F., Ali, T., Allory, Y., de la Taille, A., Vacherot, F., Loric, S. et al. (2015). Evidence of estrone-sulfate uptake modification in young and middle-aged rat prostate. J. Steroid Biochem. Mol. Biol. 152, 89-100. doi:10.1016/j.jsbmb.2015.05.002
Goldman-Wohl, D. and Yagel, S. (2002). Regulation of trophoblast invasion: from normal implantation to pre-eclampsia. Mol. Cell. Endocrinol. 187, 233-238. doi:10. 1016/S0303-7207(01)00687-6
Guivarc’h, E., Buscato, M., Guihot, A.-L., Favre, J., Vessieres, ̀ E., Grimaud, L., Wakim, J., Melhem, N.-J., Zahreddine, R., Adlanmerini, M. et al. (2018). Predominant role of nuclear versus membrane estrogen receptor alpha in arterial protection: implications for estrogen receptor alpha modulation in cardiovascular prevention/safety. J. Am. Heart Assoc. 7, e008950. doi:10.1161/JAHA.118. 008950
Gustafsson, K. L., Farman, H., Henning, P., Lionikaite, V., Movérare-Skrtic, S., Wu, J., Ryberg, H., Koskela, A., Gustafsson, J.-A., Tuukkanen, J. et al. (2016). The role of membrane ERα signaling in bone and other major estrogen responsive tissues. Sci. Rep. 6, 29473. doi:10.1038/srep29473
He, Y., Smith, S. K., Day, K. A., Clark, D. E., Licence, D. R. and Charnock-Jones, D. S. (1999). Alternative splicing of vascular endothelial growth factor (VEGF)-R1 (FLT-1) pre-mRNA is important for the regulation of VEGF activity. Mol. Endocrinol. 13, 537-545. doi:10.1210/mend.13.4.0265
He, W.-H., Jin, M.-M., Liu, A.-P., Zhou, Y., Hu, X.-L., Zhu, Y.-M. and Liu, A.-X. (2019). Estradiol promotes trophoblast viability and invasion by activating SGK1. Biomed. Pharmacother. 117, 109092. doi:10.1016/j.biopha.2019.109092
Hemberger, M., Hanna, C. W. and Dean, W. (2020). Mechanisms of early placental development in mouse and humans. Nat. Rev. Genet. 21, 27-43. doi:10.1038/ s41576-019-0169-4
Hewitt, S. C. and Korach, K. S. (2018). Estrogen receptors: new directions in the new millennium. Endocr. Rev. 39, 664-675. doi:10.1210/er.2018-00087
Hu, D. and Cross, J. C. (2011). Ablation of Tpbpa-positive trophoblast precursors leads to defects in maternal spiral artery remodeling in the mouse placenta. Dev. Biol. 358, 231-239. doi:10.1016/j.ydbio.2011.07.036
Hunkapiller, N. M., Gasperowicz, M., Kapidzic, M., Plaks, V., Maltepe, E., Kitajewski, J., Cross, J. C. and Fisher, S. J. (2011). A role for Notch signaling in trophoblast endovascular invasion and in the pathogenesis of pre-eclampsia. Development 138, 2987-2998. doi:10.1242/dev.066589
Ilicic, M., Zakar, T. and Paul, J. W. (2020). The regulation of uterine function during parturition: an update and recent advances. Reprod. Sci. 27, 3-28. doi:10.1007/ s43032-019-00001-y
Kauffenstein, G., Tamareille, S., Prunier, F., Roy, C., Ayer, A., Toutain, B., Billaud, M., Isakson, B. E., Grimaud, L., Loufrani, L. et al. (2016). Central role of P2Y6 UDP receptor in arteriolar myogenic tone. Arterioscler. Thromb. Vasc. Biol. 36, 1598-1606. doi:10.1161/ATVBAHA.116.307739
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. doi:10.1095/biolreprod.102.014977
Kelleher, A. M., DeMayo, F. J. and Spencer, T. E. (2019). Uterine Glands: Developmental Biology and Functional Roles in Pregnancy. Endocr. Rev. 40, 1424-1445. doi:10.1210/er.2018-00281
Kota, S. K., Gayatri, K., Jammula, S., Kota, S. K., Krishna, S. V. S., Meher, L. K. and Modi, K. D. (2013). Endocrinology of parturition. Indian J. Endocrinol. Metab. 17, 50-59. doi:10.4103/2230-8210.107841
Kumar, P., Kamat, A. and Mendelson, C. R. (2009). Estrogen receptor α (ERα) mediates stimulatory effects of estrogen on aromatase (CYP19) gene expression in human placenta. Mol. Endocrinol. 23, 784-793. doi:10.1210/me.2008-0371
Lacko, L. A., Hurtado, R., Hinds, S., Poulos, M. G., Butler, J. M. and Stuhlmann, H. (2017). Altered feto-placental vascularization, feto-placental malperfusion and fetal growth restriction in mice with Egfl7 loss of function. Development 144, 2469-2479. doi:10.1242/dev.147025
Lawrence, D. J., Escott, M. E., Myers, L., Intapad, S., Lindsey, S. H. and Bayer, C. L. (2019). Spectral photoacoustic imaging to estimate in vivo placental oxygenation during preeclampsia. Sci. Rep. 9, 558. doi:10.1038/s41598-018-37310-2
Malassine, A., Frendo, J.-L. and Evain-Brion, D. (2003). A comparison of placental development and endocrine functions between the human and mouse model. Hum. Reprod. Update 9, 531-539. doi:10.1093/humupd/dmg043
Maliqueo, M., Echiburú, B. and Crisosto, N. (2016). Sex steroids modulate uterine-placental vasculature: implications for obstetrics and neonatal outcomes. Front. Physiol. 7, 152. doi:10.3389/fphys.2016.00152
Mandala, M. (2020). Influence of estrogens on uterine vascular adaptation in normal and preeclamptic pregnancies. Int. J. Mol. Sci. 21, 2592. doi:10.3390/ ijms21072592
Mandala, M. and Osol, G. (2012). Physiological remodelling of the maternal uterine circulation during pregnancy. Basic Clin. Pharmacol. Toxicol. 110, 12-18. doi:10. 1111/j.1742-7843.2011.00793.x
McLaren, A. (1965). Genetic and environmental effects on foetal and placental growth in mice. J. Reprod. Fertil. 9, 79-98. doi:10.1530/jrf.0.0090079
Mesiano, S. (2019). The endocrinology of human pregnancy and fetal-placental neuroendocrine development. In Yen & Jaffe’s Reproductive Endocrinology (J. F. Strauss, III, R. L. Barbieri and A. R. Gargiulo, eds), 8th edn, Chapter 11, 256-284.e9. doi:10.1016/B978-1-4557-2758-2.00012-3
Moffett, A. and Loke, C. (2006). Immunology of placentation in eutherian mammals. Nat. Rev. Immunol. 6, 584-594. doi:10.1038/nri1897
Nelson, A. C., Mould, A. W., Bikoff, E. K. and Robertson, E. J. (2016). Single-cell RNA-seq reveals cell type-specific transcriptional signatures at the maternal-foetal interface during pregnancy. Nat. Commun. 7, 11414. doi:10.1038/ncomms11414
Pedram, A., Razandi, M., Lewis, M., Hammes, S. and Levin, E. R. (2014). Membrane-localized estrogen receptor α is required for normal organ development and function. Dev. Cell 29, 482-490. doi:10.1016/j.devcel.2014.04.016
Pijnenborg, R., Vercruysse, L. and Hanssens, M. (2006). The uterine spiral arteries in human pregnancy: facts and controversies. Placenta 27, 939-958. doi:10.1016/j.placenta.2005.12.006
Rai, A. and Cross, J. C. (2014). Development of the hemochorial maternal vascular spaces in the placenta through endothelial and vasculogenic mimicry. Dev. Biol. 387, 131-141. doi:10.1016/j.ydbio.2014.01.015
Roca, C. and Adams, R. H. (2007). Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21, 2511-2524. doi:10.1101/gad.1589207
Silva, J. F. and Serakides, R. (2016). Intrauterine trophoblast migration: a comparative view of humans and rodents. Cell Adh. Migr. 10, 88-110. doi:10. 1080/19336918.2015.1120397
Simmons, D. G., Rawn, S., Davies, A., Hughes, M. and Cross, J. C. (2008). Spatial and temporal expression of the 23 murine Prolactin/Placental Lactogenrelated genes is not associated with their position in the locus. BMC Genomics 9, 352. doi:10.1186/1471-2164-9-352
Soares, R., Balogh, G., Guo, S., Gärtner, F., Russo, J. and Schmitt, F. (2004). Evidence for the notch signaling pathway on the role of estrogen in angiogenesis. Mol. Endocrinol. 18, 2333-2343. doi:10.1210/me. 2003-0362
Stewart, C. L., Kaspar, P., Brunet, L. J., Bhatt, H., Gadi, I., Köntgen, F. and Abbondanzo, S. J. (1992). Blastocyst implantation depends on maternal expression of leukaemia inhibitory factor. Nature 359, 76-79. doi:10.1038/ 359076a0
Szego, C. M. and Davis, J. S. (1967). Adenosine 3′,5′-monophosphate in rat uterus: acute elevation by estrogen. Proc. Natl. Acad. Sci. USA 58, 1711-1718. doi:10. 1073/pnas.58.4.1711
Wang, S., Lin, J., Wang, T., Chen, X. and Huang, P. (2016). Recent advances in photoacoustic imaging for deep-tissue biomedical applications. Theranostics 6, 2394-2413. doi:10.7150/thno.16715
Woods, L., Perez-Garcia, V. and Hemberger, M. (2018). Regulation of placental development and its impact on fetal growth-new insights from mouse models. Front. Endocrinol. (Lausanne) 9, 570. doi:10.3389/fendo.2018. 00570
Young, B. C., Levine, R. J. and Karumanchi, S. A. (2010). Pathogenesis of preeclampsia. Annu. Rev. Pathol. 5, 173-192. doi:10.1146/annurev-pathol-121808-102149
