A comparison of placental development and endocrine functions between the human and mouse model
Abstract
The placenta plays a key role in pregnancy, mediating exchanges between mother and fetus and maternal tolerance of fetopaternal antigens. In some species, it also produces hormones that ensure the maintenance of gestation and fetal well-being. This unique organ also has considerable potential for use as a model for various aspects of biology. Indeed, the use of transgenic mouse models has greatly improved our understanding of the genetic control of placental development in this species and has opened up new fields of investigation in developmental biology. Analogous cell types have been identified among human and murine trophoblasts: proliferative trophoblastic cells, invasive trophoblastic cells and cells differentiating into syncytium, but human and mouse placentas differ in both morphogenesis and endocrine function. Herein, the similarities and differences between the human and mouse models are reviewed, with a view to encouraging caution in the extrapolation of results from one model to the other.
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Unlike the human, the murine syncytiotrophoblast has no endocrine function.
“Unlike the human, the murine syncytiotrophoblast has no endocrine function (355).”
From Placental Origins of Chronic Disease (2016) · cites this paper as [355]
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Cites
The Pathology of the Human Placenta
Benirschke, K., & Driscoll, S. G. (1967) · Springer eBooks · doi:10.1007/978-1-4612-9809-0 · Cited by 2,123 · see citing works
Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis
Mi, S., Lee, X., Li, X., Veldman, G. M., Finnerty, H. F., Collins‐Racie, L. A., LaVallie, E. R., Tang, X.-Y., Edouard, P., Howes, S., et al. (2000) · Nature · doi:10.1038/35001608 · Cited by 1,660 · see citing works
Kliman, H. J., Nestler, J. E., SERMASI, E., Sanger, J. M., & Strauss, J. F. (1986) · Endocrinology · doi:10.1210/endo-118-4-1567 · Cited by 1,572 · see citing works
Placental development: Lessons from mouse mutants
Rossant, J., & Cross, J. C. (2001) · Nature Reviews Genetics · doi:10.1038/35080570 · Cited by 1,273 · see citing works
BMP4 initiates human embryonic stem cell differentiation to trophoblast
Xu, R., Chen, X., Li, D. S., Li, R., Addicks, G. C., Glennon, C., Zwaka, T. P., & Thomson, J. A. (2002) · Nature Biotechnology · doi:10.1038/nbt761 · Cited by 1,118 · see citing works
Establishment and Characterization of First Trimester Human Trophoblast Cells with Extended Lifespan
Graham, C. H., Hawley, T. S., Hawley, R. G., MacDougall, J. R., Kerbel, R. S., Khoo, N. K. S., & Lala, P. K. (1993) · Experimental Cell Research · doi:10.1006/excr.1993.1139 · Cited by 1,056 · see citing works
Regulation of Human Placental Development by Oxygen Tension
Genbačev, O., Zhou, Y., Ludlow, J. W., & Fisher, S. J. (1997) · Science · doi:10.1126/science.277.5332.1669 · Cited by 914 · see citing works
Blond, J.-L., Lavillette, D., Cheynet, V., Bouton, O., Oriol, G., Chapel‐Fernandes, S., Mandrand, B., Mallet, F., & Cosset, F. (2000) · Journal of Virology · doi:10.1128/jvi.74.7.3321-3329.2000 · Cited by 714 · see citing works
Pathology of the Human Placenta
Benirschke, K., & Kaufmann, P. (1990) · Springer eBooks · doi:10.1007/978-1-4757-4193-3 · Cited by 689 · see citing works
Caniggia, I., Mostachfi, H., Winter, J., Gassmann, M., Lye, S. J., Kuliszewski, M., & Post, M. (2000) · Journal of Clinical Investigation · doi:10.1172/jci8316 · Cited by 644 · see citing works
Comparative Developmental Anatomy of the Murine and Human Definitive Placentae
Georgiades, P., Ferguson-Smith, A. C., & Burton, G. J. (2002) · Placenta · doi:10.1053/plac.2001.0738 · Cited by 641 · see citing works
Interactions between Trophoblast Cells and the Maternal and Fetal Circulation in the Mouse Placenta
Adamson, S. L., Lu, Y., Whiteley, K. J., Holmyard, D., Hemberger, M., Pfarrer, C., & Cross, J. C. (2002) · Developmental Biology · doi:10.1006/dbio.2002.0773 · Cited by 617 · see citing works
The establishment of a cell line of human hormone-synthesizing trophoblastic cells in vitro.
Pattillo, R. A., & Gey, G. O. (1968) · PubMed · Cited by 572 · see citing works
Actions of Placental and Fetal Adrenal Steroid Hormones in Primate Pregnancy*
Pepe, G. J., & Albrecht, E. D. (1995) · Endocrine Reviews · doi:10.1210/edrv-16-5-608 · Cited by 491 · see citing works
Adhesive and degradative properties of human placental cytotrophoblast cells in vitro.
Fisher, S. J., Cui, T. Y., Zhang, L., Hartman, L., Grahl, K., Zhang, G. Y., Tarpey, J., & Damsky, C. H. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.2.891 · Cited by 465 · see citing works
Burton, G. J., Jauniaux, E. R. M., & Watson, A. L. (1999) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(99)70518-1 · Cited by 453 · see citing works
Placental structure: in a comparative aspect
Leiser, R., & Kaufmann, P. (2009) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-0029-1211275 · Cited by 452 · see citing works
A comparative study of the fine structure of the trophoblast in several hemochorial placentas
Enders, A. C. (1965) · American Journal of Anatomy · doi:10.1002/aja.1001160103 · Cited by 443 · see citing works
Direct Involvement of HERV-W Env Glycoprotein in Human Trophoblast Cell Fusion and Differentiation
Frendo, J., Olivier, D., Cheynet, V., Blond, J.-L., Bouton, O., Vidaud, M., Rabreau, M., Evain‐Brion, D., & Mallet, F. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.10.3566-3574.2003 · Cited by 439 · see citing works
Self-citationPijnenborg, R., Robertson, W. B., Brosens, I. A., & Dixon, G. (1981) · Placenta · doi:10.1016/s0143-4004(81)80042-2 · Cited by 435 · see citing works
Human cytotrophoblast differentiation/invasion is abnormal in pre-eclampsia.
Lim, K.-H., Zhou, Y., Janatpour, M. J., McMaster, M., Bass, K. E., Chun, S. H., & Fisher, S. J. (1997) · Europe PMC (PubMed Central) · Cited by 393 · see citing works
Handwerger, S., & Freemark, M. (2000) · Journal of Pediatric Endocrinology and Metabolism · doi:10.1515/jpem.2000.13.4.343 · Cited by 351 · see citing works
Genes, Development and Evolution of the Placenta
Cross, J. C., Baczyk, D., Dobric, N., Hemberger, M., Hughes, M., Simmons, D. G., Yamamoto, H., & Kingdom, J. C. (2003) · Placenta · doi:10.1053/plac.2002.0887 · Cited by 348 · see citing works
Hustin, J., & Schaaps, J. (1987) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(87)80371-x · Cited by 343 · see citing works
Characterization of Human Chorionic Gonadotropin as a Novel Angiogenic Factor
Zygmunt, M., Herr, F., Keller-Schoenwetter, S., Kunzi‐Rapp, K., Münstedt, K., Rao, C. V., Lang, U., & Preissner, K. T. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020642 · Cited by 340 · see citing works
Brown, R. W., Diaz, R., Robson, A. C., Kotelevtsev, Y. V., Mullins, J. J., Kaufman, M. H., & Seckl, J. R. (1996) · Endocrinology · doi:10.1210/endo.137.2.8593833 · Cited by 307 · see citing works
Placental Steroid Hormone Biosynthesis in Primate Pregnancy*
Albrecht, E. D., & Pepe, G. J. (1990) · Endocrine Reviews · doi:10.1210/edrv-11-1-124 · Cited by 305 · see citing works
Histological study of the materno-embryonic interface in spontaneous abortion
Hustin, J., Jauniaux, E. R. M., & Schaaps, J. P. (1990) · Placenta · doi:10.1016/s0143-4004(05)80193-6 · Cited by 299 · see citing works
Novel role of human chorionic gonadotropin in differentiation of human cytotrophoblasts
Shi, Q. J., Lei, Z. M., Rao, C. V., & Lin, J. (1993) · Endocrinology · doi:10.1210/endo.132.3.7679981 · Cited by 298 · see citing works
Human implantation : cell biology and immunology
Loke, Y. W., & King, A. (1995) · Cambridge University Press eBooks · Cited by 294 · see citing works
A New Cause of Female Pseudohermaphroditism: Placental Aromatase Deficiency
Shozu, M., Akasofu, K., HARADA, T., & Kubota, Y. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-72-3-560 · Cited by 287 · see citing works
Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts
Craven, C., Morgan, T. K., & Ward, K. R. (1998) · Placenta · doi:10.1016/s0143-4004(98)90055-8 · Cited by 283 · see citing works
McTernan, C. L., Draper, N. R., Nicholson, H. O., Chalder, S. M., Driver, P., Hewison, M., Kilby, M. D., & Stewart, P. M. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.10.7893 · Cited by 282 · see citing works
Couturier‐Tarrade, A., Lai–Kuen, R., Malassiné, A., Tricottet, V., Blain, P. L., Vidaud, M., & Evain‐Brion, D. (2001) · Laboratory Investigation · doi:10.1038/labinvest.3780334 · Cited by 259 · see citing works
Self-citationTrophoblast pseudo-vasculogenesis: faking it with endothelial adhesion receptors
Damsky, C. H., & Fisher, S. J. (1998) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(98)80043-4 · Cited by 248 · see citing works
Elliott, M. M., Kardana, A., Lustbader, J. W., & Cole, L. A. (1997) · Endocrine · doi:10.1007/bf02778058 · Cited by 228 · see citing works
Expression analysis of a Notch homologue in the mouse embryo
Reaume, A. G., Conlon, R. A., Zirngibl, R. A., Yamaguchi, T. P., & Rossant, J. (1992) · Developmental Biology · doi:10.1016/0012-1606(92)90076-s · Cited by 228 · see citing works
Chorionic Gonadotropin Has a Recent Origin Within Primates and an Evolutionary History of Selection
Maston, G. A., & Ruvolo, M. (2002) · Molecular Biology and Evolution · doi:10.1093/oxfordjournals.molbev.a004085 · Cited by 225 · see citing works
Activin Is a Local Regulator of Human Cytotrophoblast Cell Differentiation1
Caniggia, I., Lye, S. J., & Cross, J. C. (1997) · Endocrinology · doi:10.1210/endo.138.9.5403 · Cited by 225 · see citing works
Kliman, H. J. (2000) · American Journal Of Pathology · doi:10.1016/s0002-9440(10)64813-4 · Cited by 219 · see citing works
Licht, P., Russu, V., & Wildt, L. (2001) · Seminars in Reproductive Medicine · doi:10.1055/s-2001-13909 · Cited by 215 · see citing works
Genbačev, O., Schubach, S. A., & Miller, R. K. (1992) · Placenta · doi:10.1016/0143-4004(92)90051-t · Cited by 198 · see citing works
Interactions between Trophoblast Cells and the Maternal and Fetal Circulation in the Mouse Placenta
Adamson, S. L. (2002) · Developmental Biology · doi:10.1016/s0012-1606(02)90773-6 · Cited by 197 · see citing works
Schaiff, W. T., Carlson, M. G., Smith, S. D., Levy, R., Nelson, D. M., & Sadovsky, Y. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.10.6885 · Cited by 189 · see citing works
Placental Steroid Hormone Synthesis: Unique Features and Unanswered Questions1
Strauss, J. F., Martı́nez, F., & Kiriakidou, M. (1996) · Biology of Reproduction · doi:10.1095/biolreprod54.2.303 · Cited by 187 · see citing works
Regulation of Chorionic Gonadotropin Gene Expression*
Jameson, J. L., & Hollenberg, A. N. (1993) · Endocrine Reviews · doi:10.1210/edrv-14-2-203 · Cited by 182 · see citing works
Cell Culture Models of Human Trophoblast II: Trophoblast Cell Lines—A Workshop Report
Shiverick, K. T., King, A., Frank, H., Whitley, G. S. J., Cartwright, J. E., & Schneider, H. (2001) · Placenta · doi:10.1053/plac.2001.0647 · Cited by 179 · see citing works
Functional regulation of human trophoblast differentiation
Morrish, D. W., Dakour, J., & Li, H. (1998) · Journal of Reproductive Immunology · doi:10.1016/s0165-0378(98)00021-7 · Cited by 177 · see citing works
Dave-Sharma, S., Wilson, R. C., Harbison, M. D., Newfield, R. S., Azar, M. R., Krozowski, Z. S., Funder, J. W., Shackleton, C. H. L., Bradlow, H. L., Wei, J., et al. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.83.7.4986 · Cited by 177 · see citing works
Adler, R. R., Ng, A., & Rote, N. S. (1995) · Biology of Reproduction · doi:10.1095/biolreprod53.4.905 · Cited by 176 · see citing works
The pathogenesis of pre-eclampsia
Redman, C. W. G., & Sargent, I. L. (2001) · Gynécologie Obstétrique & Fertilité · doi:10.1016/s1297-9589(01)00180-1 · Cited by 169 · see citing works
Vićovac, L., Jones, C. J. P., & Aplin, J. (1995) · Placenta · doi:10.1016/0143-4004(95)90080-2 · Cited by 157 · see citing works
Hormones and Human Trophoblast Differentiation
Malassiné, A., & Cronier, L. (2002) · Endocrine · doi:10.1385/endo:19:1:3 · Cited by 155 · see citing works
Dave-Sharma, S. (1998) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.83.7.2244 · Cited by 153 · see citing works
The Human Placental Bed Revisited
Lyall, F. (2002) · Placenta · doi:10.1053/plac.2002.0850 · Cited by 143 · see citing works
Involvement of connexin 43 in human trophoblast cell fusion and differentiation
Frendo, J., Cronier, L., Bertin, G. I., Guibourdenche, J., Vidaud, M., Evain‐Brion, D., & Malassiné, A. (2003) · Journal of Cell Science · doi:10.1242/jcs.00648 · Cited by 142 · see citing works
Self-citationActions of placental and fetal adrenal steroid hormones in primate pregnancy
Pepe, G. J. (1995) · Endocrine Reviews · doi:10.1210/er.16.5.608 · Cited by 142 · see citing works
The Central Role of Human Chorionic Gonadotropin in the Formation of Human Placental Syncytium
Yang, M.-F., Lei, Z. M., & Rao, C. V. (2003) · Endocrinology · doi:10.1210/en.2002-220922 · Cited by 140 · see citing works
Cell Culture Models of Trophoblast II: Trophoblast Cell Lines— A Workshop Report
King, A., Thomas, L., & Bischof, P. (2000) · Placenta · doi:10.1053/plac.1999.0526 · Cited by 135 · see citing works
Differentiation of trophoblast endocrine cells
Soares, M. J., Chapman, B. M., Rasmussen, C. A., et al. (1996) · Placenta · doi:10.1016/s0143-4004(96)90051-x · Cited by 132 · see citing works
Cronier, L., Bastide, B., Hervé, J., Délèze, J., & Malassiné, A. (1994) · Endocrinology · doi:10.1210/endo.135.1.8013377 · Cited by 126 · see citing works
PPARγ/RXRα Heterodimers Control Human Trophoblast Invasion
Couturier‐Tarrade, A., Schoonjans, K., Pavan, L., Auwerx, J. H., Rochette‐Egly, C., Evain‐Brion, D., & Fournier, T. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.10.7924 · Cited by 118 · see citing works
Self-citationRao, C. V. (2001) · Seminars in Reproductive Medicine · doi:10.1055/s-2001-13906 · Cited by 116 · see citing works
Functional Proteomics: Examining the Effects of Hypoxia on the Cytotrophoblast Protein Repertoire
Hoang, V. M., Foulk, R. A., Clauser, K. R., Burlingame, A. L., Gibson, B. W., & Fisher, S. J. (2001) · Biochemistry · doi:10.1021/bi0023910 · Cited by 115 · see citing works
Human placental growth hormone
Alsat, E., Guibourdenche, J., Luton, D., Frankenne, F., & Evain-Brion, D. (1997) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(97)70103-0 · Cited by 113 · see citing works
Self-citationTrophoblast Invasion of Spiral Arteries: a Novel In Vitro Model
Cartwright, J. E., Kenny, L. C., Dash, P. R., Crocker, I. P., Aplin, J., Baker, P. N., & Whitley, G. S. J. (2002) · Placenta · doi:10.1053/plac.2001.0760 · Cited by 111 · see citing works
Müntener, M., & Hsu, Y. (1977) · PubMed · Cited by 110 · see citing works
Expression of integrins by human trophoblast and differential adhesion to laminin or fibronectin
Burrows, T. D., King, A., & Loke, Y. W. (1993) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a138075 · Cited by 106 · see citing works
Alfaidy, N., Gupta, S., Demarco, C., Caniggia, I., & Challis, J. R. G. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020310 · Cited by 105 · see citing works
Kemp, B., Kertschanska, S., Kadyrov, M., et al. (2002) · Histochemistry and Cell Biology · doi:10.1007/s00418-002-0396-0 · Cited by 101 · see citing works
Aronow, B. J., Richardson, B. D., & Handwerger, S. (2001) · Physiological Genomics · doi:10.1152/physiolgenomics.2001.6.2.105 · Cited by 101 · see citing works
Expression of Na+/I−Symporter and Pendred Syndrome Genes in Trophoblast Cells1
Bidart, J., Lacroix, L., Evain-Brion, D., Caillou, B., Lazar, V., Frydman, R., Bellet, D. H., Filetti, S., & Schlumberger, M. J. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.11.6969 · Cited by 100 · see citing works
Self-citationPlacenta-Specific INSL4 Expression Is Mediated by a Human Endogenous Retrovirus Element1
Bièche, I., Laurent, A., Laurendeau, I., Duret, L., Giovangrandi, Y., Frendo, J., Olivi, M., Fausser, J., Evain‐Brion, D., & Vidaud, M. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.102.010322 · Cited by 95 · see citing works
Self-citationMultiple novel roles of luteinizing hormone
Rao, C. V. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(01)02863-1 · Cited by 90 · see citing works
Structural interactions of trophoblast and uterus during hemochorial placenta formation
Enders, A. C., & Welsh, A. O. (1993) · Journal of Experimental Zoology · doi:10.1002/jez.1402660608 · Cited by 89 · see citing works
Cadherin-11 modulates the terminal differentiation and fusion of human trophoblastic cells in vitro
Getsios, S., & MacCalman, C. D. (2003) · Developmental Biology · doi:10.1016/s0012-1606(03)00041-1 · Cited by 88 · see citing works
The Role of Chorionic Gonadotropin (CG) in Blastocyst Implantation
Srisuparp, S., Straková, Z., & Fazleabas, A. T. (2001) · Archives of Medical Research · doi:10.1016/s0188-4409(01)00330-7 · Cited by 86 · see citing works
Transcription Factors Underlying the Development and Endocrine Functions of the Placenta
Cross, J. C. (2002) · Recent Progress in Hormone Research · doi:10.1210/rp.57.1.221 · Cited by 85 · see citing works
Al-Lamki, R. S., Skepper, J. N., & Burton, G. J. (1999) · Human Reproduction · doi:10.1093/humrep/14.2.496 · Cited by 81 · see citing works
Expression of Na+/I- Symporter and Pendred Syndrome Genes in Trophoblast Cells
Bidart, J. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.11.4367 · Cited by 77 · see citing works
Bischof, P., Haenggeli, L., & Campana, A. (1995) · Human Reproduction · doi:10.1093/oxfordjournals.humrep.a136024 · Cited by 71 · see citing works
Luteotropic actions of placental lactogens at midpregnancy in the mouse.
Galosy, S. S., & Talamantes, F. J. (1995) · Endocrinology · doi:10.1210/endo.136.9.7649108 · Cited by 70 · see citing works
Cronier, L. (2002) · Molecular Human Reproduction · doi:10.1093/molehr/8.11.1005 · Cited by 69 · see citing works
Novel self-regulation of human chorionic gonadotropin biosynthesis in term pregnancy human placenta.
Licht, P., Cao, H., Lei, Z. M., et al. (1993) · Endocrinology · doi:10.1210/endo.133.6.8243330 · Cited by 67 · see citing works
Alsat, E., Mirlesse, V., Fondacci, C., et al. (1991) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-73-2-288 · Cited by 65 · see citing works
Activin Is a Local Regulator of Human Cytotrophoblast Cell Differentiation
Caniggia, I. (1997) · Endocrinology · doi:10.1210/en.138.9.3976 · Cited by 65 · see citing works
Morphogenesis of the syncytium in the mouse placenta
Hernandez‐Verdun, D. (1974) · Cell and Tissue Research · doi:10.1007/bf00224265 · Cited by 64 · see citing works
Morrish, D. W., Linetsky, E., Bhardwaj, D., Li, H., Dakour, J., Marsha, R. G., Paterson, M. C., & Godbout, R. (1996) · Placenta · doi:10.1016/s0143-4004(96)90025-9 · Cited by 60 · see citing works
Cronier, L., Frendo, J., Defamie, N., Pidoux, G., Bertin, G. I., Guibourdenche, J., Pointis, G., & Malassiné, A. (2003) · Biology of Reproduction · doi:10.1095/biolreprod.103.016360 · Cited by 59 · see citing works
Self-citationUterine and placental expression of steroidogenic genes during rodent pregnancy
Ben‐Zimra, M., Koler, M., Melamed‐Book, N., Arensburg, J., Payne, A. H., & Orly, J. (2002) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00713-4 · Cited by 58 · see citing works
Yamamoto, T., Roby, K. F., Kwok, S. C. M., & Soares, M. J. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)37402-1 · Cited by 54 · see citing works
Regulation of chorionic gonadotropin gene expression
Jameson, J. L. (1993) · Endocrine Reviews · doi:10.1210/er.14.2.203 · Cited by 54 · see citing works
Key Regulatory Transcription Factors Involved in Placental Trophoblast Development—A Review
Knöfler, M., Vasicek, R., & Schreiber, M. (2001) · Placenta · doi:10.1053/plac.2001.0648 · Cited by 53 · see citing works
Frendo, J., Guibourdenche, J., Pidoux, G., et al. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030668 · Cited by 52 · see citing works
Self-citationComparative Morphological Aspects of Placental Vascularization
Dantzer, V., Leiser, R., Kaufmann, P., & Luckhardt, M. (1988) · Springer eBooks · doi:10.1007/978-1-4615-8109-3_17 · Cited by 49 · see citing works
Dynamic Changes in Gene Expression During Human Trophoblast Differentiation
Handwerger, S. (2003) · Recent Progress in Hormone Research · doi:10.1210/rp.58.1.263 · Cited by 47 · see citing works
The murine 3β-hydroxysteroid dehydrogenase (3β-HSD) gene family
Peng, L., Arensburg, J., Orly, J., & Payne, A. H. (2002) · Molecular and Cellular Endocrinology · doi:10.1016/s0303-7207(01)00689-x · Cited by 46 · see citing works
Goffin, F., Munaut, C., Malassiné, A., et al. (2003) · Tissue Antigens · doi:10.1034/j.1399-0039.2003.00085.x · Cited by 43 · see citing works
Peng, L., & Payne, A. H. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m106765200 · Cited by 40 · see citing works
Lacroix, M.-C., Guibourdenche, J., Frendo, J., et al. (2002) · Endocrine · doi:10.1385/endo:19:1:73 · Cited by 39 · see citing works
Self-citationIslami, D. (2001) · Molecular Human Reproduction · doi:10.1093/molehr/7.1.3 · Cited by 35 · see citing works
Jablonka‐Shariff, A., Garcia-Campayo, V., & Boime, I. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.c100402200 · Cited by 34 · see citing works
Luteotropic actions of placental lactogens at midpregnancy in the mouse
Galosy, S. S. (1995) · Endocrinology · doi:10.1210/en.136.9.3993 · Cited by 34 · see citing works
Schiff, R., Arensburg, J., Itin, A., et al. (1993) · Endocrinology · doi:10.1210/endo.133.2.8344198 · Cited by 29 · see citing works
Dı́az-Cueto, L., de Tomasi, J. B., Timossi, C., et al. (1996) · Molecular Human Reproduction · doi:10.1093/molehr/2.9.643 · Cited by 29 · see citing works
Frendo, J., Thérond, P., Guibourdenche, J., Bidart, J., Vidaud, M., & Evain‐Brion, D. (2000) · Placenta · doi:10.1053/plac.2000.0575 · Cited by 29 · see citing works
Self-citationNovel self-regulation of human chorionic gonadotropin biosynthesis in term pregnancy human placenta
Licht, P. (1993) · Endocrinology · doi:10.1210/en.133.6.3014 · Cited by 24 · see citing works
Incidence of Placental Sulfatase Deficiency on the Mode of Termination of Pregnancy
Bedin, M., Fournier, T., CABROL, D., Bréart, G., Kottler, M., & Cedard, L. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000298784 · Cited by 13 · see citing works
Schiff, R. (1993) · Endocrinology · doi:10.1210/en.133.2.529 · Cited by 12 · see citing works
12 Trophoblast Stem CellsPreprint
Kunath, T., Strumpf, D., Rossant, J., et al. (2001) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969673.40.267 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 3
- Kunath, T., Strumpf, D., Rossant, J. and Tanaka, S. (2001) Trophoblast Stem cells in Stem Cell Biology. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp. 267±287.
- Steven, D. and Morris, G. (1975) Development of the Fetal Membranes; Comparative Placentation. Steven, London, pp. 58±86.
- Wynn, R. (1968) Morphology of the Placenta: Biology of Gestation. Academic Press, New York.
Cited by
Sorted by citations
Placental Origins of Chronic Disease
Burton, G. J., Fowden, A. L., & Thornburg, K. L. (2016) · Physiological Reviews · doi:10.1152/physrev.00029.2015 · Cited by 717 · see citing works
A Randomized Trial of Progesterone in Women with Recurrent Miscarriages
Coomarasamy, A., Williams, H., Truchanowicz, E., Seed, P. T., Small, R., Quenby, S., Gupta, P., Dawood, F., Koot, Y. E. M., Bender Atik, R., et al. (2015) · New England Journal of Medicine · doi:10.1056/nejmoa1504927 · Cited by 312 · see citing works
The omniscient placenta: Metabolic and epigenetic regulation of fetal programming
Nugent, B. M., & Bale, T. L. (2015) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2015.09.001 · Cited by 222 · see citing works
A Randomized Trial of Progesterone in Women with Bleeding in Early Pregnancy
Coomarasamy, A., Devall, A. J., Cheed, V., Harb, H., Middleton, L. J., Gallos, I. D., Williams, H., Eapen, A. K., Roberts, T., Ogwulu, C. C., et al. (2019) · New England Journal of Medicine · doi:10.1056/nejmoa1813730 · Cited by 197 · see citing works
Burton, G. J., & Fowden, A. L. (2012) · Placenta · doi:10.1016/j.placenta.2011.11.013 · Cited by 177 · see citing works
Review: Transport across the placenta of mice and women
Dilworth, M. R., & Sibley, C. P. (2013) · Placenta · doi:10.1016/j.placenta.2012.10.011 · Cited by 155 · see citing works
Animal models of human pregnancy and placentation: alternatives to the mouse
Carter, A. M. (2020) · Reproduction · doi:10.1530/rep-20-0354 · Cited by 130 · see citing works
Saccone, G., Schoen, C., Franasiak, J. M., Scott, R. T., & Berghella, V. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2016.10.031 · Cited by 128 · see citing works
Cuffe, J. S. M., Walton, S. L., Singh, R. R., Spiers, J. G., Bielefeldt‐Ohmann, H., Wilkinson, L., Little, M. H., & Moritz, K. M. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2014.272856 · Cited by 128 · see citing works
AMPK Knockdown in Placental Trophoblast Cells Results in Altered Morphology and Function
Carey, E. A. K., Albers, R. E., Doliboa, S. R., Hughes, M., Wyatt, C. N., Natale, D. R. C., & Brown, T. L. (2014) · Stem Cells and Development · doi:10.1089/scd.2014.0092 · Cited by 56 · see citing works
- Authors
- Malassine, A., Frendo, J. L., & Evain-Brion, D.
- Affiliations
- Inserm (FR)
- ORCID
- Frendo, J.- L.
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 2003-11-01
- Volume
- 9
- Issue
- 6
- Pages
- 531-539
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- OpenAlex
- W2117792063
- Cited by
- 476
- References
- 110
- Citations by year
- 2026: 18 · 2025: 20 · 2024: 21 · 2023: 15 · 2022: 22 · 2021: 32 · 2020: 41 · 2019: 30 · 2018: 25 · 2017: 24 · 2016: 35 · 2015: 24 · 2014: 29 · 2013: 32 · 2012: 20
- FWCI
- 9.28
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Institut National de la Santé et de la Recherche Médicale
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Reproductive Biology and Fertility
- Keywords
- placental development, placental endocrine function, transgenic mouse model, trophoblast differentiation, syncytiotrophoblast, invasive trophoblast, placental morphogenesis, gestational hormones, model extrapolation
- MeSH terms
- Animals, Endocrine Glands, Female, Humans, Placentation, Pregnancy, Trophoblasts, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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