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Science 2 December 1994:
Vol. 266. no. 5190, pp. 1508 - 1518
DOI: 10.1126/science.7985020
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Articles

Science, Vol 266, Issue 5190, 1508-1518
Copyright © 1994 by American Association for the Advancement of Science

articles

Implantation and the placenta: key pieces of the development puzzle

JC Cross, Z Werb, and SJ Fisher

Samuel Lunenfeld Research Institute, Mount Sinai Hospital, Toronto, Ontario, Canada.

The mammalian embryo cannot develop without the placenta. Its specialized cells (trophoblast, endoderm, and extraembryonic mesoderm) form early in development. They attach the embryo to the uterus (implantation) and form vascular connections necessary for nutrient transport. In addition, the placenta redirects maternal endocrine, immune, and metabolic functions to the embryo's advantage. These complex activities are sensitive to disruption, as shown by the high incidence of early embryonic mortality and pregnancy diseases in humans, as well as the numerous peri-implantation lethal mutations in mice. Integration of molecular and developmental approaches has recently produced insights into the molecules that control these processes.


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Y.-L. Dong, S. Vegiraju, M. Chauhan, P. R. R. Gangula, G. D. V. Hankins, L. Goodrum, and C. Yallampalli (2004)
Am J Physiol Heart Circ Physiol 286, H230-H239
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M. Hirashima, Y. Lu, L. Byers, and J. Rossant (2003)
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Factor XIII A subunit-deficient mice developed severe uterine bleeding events and subsequent spontaneous miscarriages.
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Blood 102, 4410-4412
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Biol Reprod 69, 1515-1524
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A functional overlap of plasminogen and MMPs regulates vascularization during placental development.
H. Solberg, J. Rinkenberger, K. Dano, Z. Werb, and L. R. Lund (2003)
Development 130, 4439-4450
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The Expression of Proprotein Convertase PACE4 Is Highly Regulated by Hash-2 in Placenta: Possible Role of Placenta-Specific Basic Helix-Loop-Helix Transcription Factor, Human Achaete-Scute Homologue-2.
S. Koide, I. Yoshida, A. Tsuji, and Y. Matsuda (2003)
J. Biochem. 134, 433-440
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Complexes of HLA-G Protein on the Cell Surface Are Important for Leukocyte Ig-Like Receptor-1 Function.
T. Gonen-Gross, H. Achdout, R. Gazit, J. Hanna, S.'a. Mizrahi, G. Markel, D. Goldman-Wohl, S. Yagel, V. Horejsi, O. Levy, et al. (2003)
J. Immunol. 171, 1343-1351
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Matrix Metalloproteinase-2 and -9 Involvement in Canine Tumors.
P. Loukopoulos, B. A. Mungall, R. C. Straw, J. R. Thornton, and W. F. Robinson (2003)
Vet. Pathol. 40, 382-394
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Interferon-Stimulated Gene-15 (Isg15) Expression Is Up-Regulated in the Mouse Uterus in Response to the Implanting Conceptus.
K. J. Austin, B. M. Bany, E. L. Belden, L. A. Rempel, J. C. Cross, and T. R. Hansen (2003)
Endocrinology 144, 3107-3113
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Human Protease-Activated Receptor 1 Expression in Malignant Epithelia: A Role in Invasiveness.
Y.-J. Yin, Z. Salah, S. Grisaru-Granovsky, I. Cohen, S. C. Even-Ram, M. Maoz, B. Uziely, T. Peretz, and R. Bar-Shavit (2003)
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Keratin 8 protection of placental barrier function.
D. Jaquemar, S. Kupriyanov, M. Wankell, J. Avis, K. Benirschke, H. Baribault, and R. G. Oshima (2003)
J. Cell Biol. 161, 749-756
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The Human Placenta Remodels the Uterus by Using a Combination of Molecules That Govern Vasculogenesis or Leukocyte Extravasation.
Y. ZHOU, O. GENBACEV, and S. J. FISHER (2003)
Ann. N.Y. Acad. Sci. 995, 73-83
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Chorioallantoic Morphogenesis and Formation of the Placental Villous Tree.
J. C. CROSS, D. G. SIMMONS, and E. D. WATSON (2003)
Ann. N.Y. Acad. Sci. 995, 84-93
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In Situ-Synthesized Novel Microarray Optimized for Mouse Stem Cell and Early Developmental Expression Profiling.
M. G. Carter, T. Hamatani, A. A. Sharov, C. E. Carmack, Y. Qian, K. Aiba, N. T. Ko, D. B. Dudekula, P. M. Brzoska, S. S. Hwang, et al. (2003)
Genome Res. 13, 1011-1021
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Comparison of the genomes of human and mouse lays the foundation of genome zoology.
R. D. Emes, L. Goodstadt, E. E. Winter, and C. P. Ponting (2003)
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Enhanced Expression of Uterine Stathmin during the Process of Implantation and Decidualization in Rats.
K. Tamura, T. Hara, M. Yoshie, S. Irie, A. Sobel, and H. Kogo (2003)
Endocrinology 144, 1464-1473
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Differential Regulation of the Expression of Matrix Metalloproteinases and Tissue Inhibitors of Metalloproteinases by Cytokines and Growth Factors in Bovine Endometrial Stromal Cells and Trophoblast Cell Line BT-1 In Vitro.
M. Hirata, T. Sato, M. Tsumagari, A. Shimada, H. Nakano, K. Hashizume, and A. Ito (2003)
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Hedgehog is required for murine yolk sac angiogenesis.
N. Byrd, S. Becker, P. Maye, R. Narasimhaiah, B. St-Jacques, X. Zhang, J. McMahon, A. McMahon, and L. Grabel (2003)
Development 129, 361-372
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Functional ablation of the mouse Ldb1 gene results in severe patterning defects during gastrulation.
M. Mukhopadhyay, A. Teufel, T. Yamashita, A. D. Agulnick, L. Chen, K. M. Downs, A. Schindler, A. Grinberg, S.-P. Huang, D. Dorward, et al. (2003)
Development 130, 495-505
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Retinoic acid decreases the viability of mouse blastocysts in vitro.
F.-J. Huang, C.-C. Shen, S.-Y. Chang, T.-C. J. Wu, and Y.-D. Hsuuw (2003)
Hum. Reprod. 18, 130-136
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CYR61 (CCN1) Is Essential for Placental Development and Vascular Integrity.
F.-E Mo, A. G. Muntean, C.-C. Chen, D. B. Stolz, S. C. Watkins, and L. F. Lau (2002)
Mol. Cell. Biol. 22, 8709-8720
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Expression of Interleukin-10 and Its Receptor Is Up-Regulated in Early Pregnant Versus Cycling Human Endometrium.
P. Vigano, E. Somigliana, S. Mangioni, M. Vignali, M. Vignali, and A. M. Di Blasio (2002)
J. Clin. Endocrinol. Metab. 87, 5730-5736
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The Mitogenic Potential of Heparin-Binding Epidermal Growth Factor in the Human Endometrium Is Mediated by the Epidermal Growth Factor Receptor and Is Modulated by Tumor Necrosis Factor-{alpha}.
K. Chobotova, M.-E. Muchmore, J. Carver, H.-J Yoo, S. Manek, W. J. Gullick, D. H. Barlow, and H. J. Mardon (2002)
J. Clin. Endocrinol. Metab. 87, 5769-5777
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Diagnosis and Management of Human Cytomegalovirus Infection in the Mother, Fetus, and Newborn Infant.
M. G. Revello and G. Gerna (2002)
Clin. Microbiol. Rev. 15, 680-715
   Abstract »    Full Text »    PDF »
Control of Proliferation, Migration, and Invasiveness of Human Extravillous Trophoblast by Decorin, a Decidual Product.
G. Xu, M.-J. Guimond, C. Chakraborty, and P. K. Lala (2002)
Biol Reprod 67, 681-689
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Localization of heparanase in normal and pathological human placenta.
R. Haimov-Kochman, Y. Friedmann, D. Prus, D. S. Goldman-Wohl, C. Greenfield, E. Y. Anteby, A. Aviv, I. Vlodavsky, and S. Yagel (2002)
Mol. Hum. Reprod. 8, 566-573
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Defective Production of Interleukin-11 by Decidua and Chorionic Villi in Human Anembryonic Pregnancy.
H.-F. Chen, C.-Y. Lin, K.-H. Chao, M.-Y. Wu, Y.-S. Yang, and H.-N. Ho (2002)
J. Clin. Endocrinol. Metab. 87, 2320-2328
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Identification and Regulation of the IGFBP-4 Protease and Its Physiological Inhibitor in Human Trophoblasts and Endometrial Stroma: Evidence for Paracrine Regulation of IGF-II Bioavailability in the Placental Bed during Human Implantation.
L. C. Giudice, C. A. Conover, L. Bale, G. H. Faessen, K. Ilg, I. Sun, B. Imani, L.-F. Suen, J. C. Irwin, M. Christiansen, et al. (2002)
J. Clin. Endocrinol. Metab. 87, 2359-2366
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Why does hydrosalpinx reduce fertility?: The importance of hydrosalpinx fluid.
A. Strandell and A. Lindhard (2002)
Hum. Reprod. 17, 1141-1145
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The Solitary Long Terminal Repeats of ERV-9 Endogenous Retrovirus Are Conserved during Primate Evolution and Possess Enhancer Activities in Embryonic and Hematopoietic Cells.
J. Ling, W. Pi, R. Bollag, S. Zeng, M. Keskintepe, H. Saliman, S. Krantz, B. Whitney, and D. Tuan (2002)
J. Virol. 76, 2410-2423
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Developmental Defects and Male Sterility in Mice Lacking the Ubiquitin-Like DNA Repair Gene mHR23B.
J. M. Y. Ng, H. Vrieling, K. Sugasawa, M. P. Ooms, J. A. Grootegoed, J. T. M. Vreeburg, P. Visser, R. B. Beems, T. G. M. F. Gorgels, F. Hanaoka, et al. (2002)
Mol. Cell. Biol. 22, 1233-1245
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Significant Differences Between Mouse and Human Trophinins Are Revealed by Their Expression Patterns and Targeted Disruption of Mouse Trophinin Gene.
D. Nadano, K. Sugihara, B. C. Paria, S. Saburi, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, J. Nakayama, and M. N. Fukuda (2002)
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H. J. Auman, T. Nottoli, O. Lakiza, Q. Winger, S. Donaldson, and T. Williams (2002)
Development 129, 2733-2747
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Relaxin Increases Secretion of Tissue Inhibitor of Matrix Metalloproteinase-1 and -2 during Uterine and Cervical Growth and Remodeling in the Pig.
J. A. Lenhart, P. L. Ryan, K. M. Ohleth, S. S. Palmer, and C. A. Bagnell (2002)
Endocrinology 143, 91-98
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Expression of vasodilator-stimulated phosphoprotein in human placenta: possible implications in trophoblast invasion.
U. A. Kayisli, B. Selam, R. Demir, and A. Arici (2002)
Mol. Hum. Reprod. 8, 88-94
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Transcription Factors Underlying the Development and Endocrine Functions of the Placenta.
J. C. Cross, L. Anson-Cartwright, and I. C. Scott (2002)
Recent Prog. Horm. Res. 57, 221-234
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UniGene cDNA array-based monitoring of transcriptome changes during mouse placental development.
M. Hemberger, J. C. Cross, H.-H. Ropers, H. Lehrach, R. Fundele, and H. Himmelbauer (2001)
PNAS 98, 13126-13131
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PPAR{gamma}/RXR{alpha} Heterodimers Control Human Trophoblast Invasion.
A. Tarrade, K. Schoonjans, L. Pavan, J. Auwerx, C. Rochette-Egly, D. Evain-Brion, and T. Fournier (2001)
J. Clin. Endocrinol. Metab. 86, 5017-5024
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Colour Doppler analysis of peri-implantation utero-ovarian haemodynamics in women with excessively high oestradiol concentrations after ovarian stimulation.
G. S. Basir, T. P. W. Lam, M. T. Chau, E. H. Y. Ng, W.-s. O, and P. C. Ho (2001)
Hum. Reprod. 16, 2114-2117
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Relaxin Increases Secretion of Matrix Metalloproteinase-2 and Matrix Metalloproteinase-9 during Uterine and Cervical Growth and Remodeling in the Pig.
J. A. Lenhart, P. L. Ryan, K. M. Ohleth, S. S. Palmer, and C. A. Bagnell (2001)
Endocrinology 142, 3941-3949