Placental development: Lessons from mouse mutants

Nature Reviews Genetics

Volumn 2, Issue 7, 2001, Pages 538-548

  Rossant, Janet ^a   Cross, James C ^b  

^a MOUNT SINAI HOSPITAL   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MAMMALIA;

ANIMAL; CELL DIFFERENTIATION; COMPARATIVE STUDY; FEMALE; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; MOUSE; MOUSE MUTANT; PHYSIOLOGY; PLACENTA; PREGNANCY; PRENATAL DEVELOPMENT; REVIEW; SPECIES DIFFERENCE; TROPHOBLAST;

ANIMALS; CELL DIFFERENTIATION; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE; MICE, KNOCKOUT; PLACENTA; PREGNANCY; SPECIES SPECIFICITY; TROPHOBLASTS;

EID: 0035406530     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/35080570     Document Type: Review

References (115)

1. Cross, J. C. Genetic insights into trophoblast differentiation and placental morphogenesis. Semin. Cell Dev. Biol. 11, 105-113 (2000).
2. Barak, Y. et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol. Cell 4, 585-595 (1999).
3. Cross, J. C. et al. Trophoblast functions, angiogenesis and remodeling of the maternal vasculature in the placenta. Mol. Cell Endocrinol. (in the press).
4. Damsky, C. H. & Fisher, S. J. Trophoblast pseudovasculogenesis: faking it with endothelial adhesion receptors. Curr. Opin Cell Biol. 10, 660-666 (1998).
5. Copp, A. J. Interaction between inner cell mass and trophectoderm of the mouse blastocyst. II. The fate of the polar trophectoderm. J. Embryol. Exp. Morphol. 51, 109-120 (1979).
6. Scares, M. J. et al. Differentiation of trophoblast endocrine cells. Placenta 17, 277-289 (1996).
7. Groskopf, J. C., Syu, L. J., Saltiel, A. R. & Linzer, D. I. Proliferin induces endothelial cell chemotaxis through a G protein-coupled, mitogen-activated protein kinase-dependent pathway. Endocrinology 138, 2835-2840 (1997).
8. Vuorela, P. et al. Expression of vascular endothelial growth factor and placenta growth factor in human placenta. Biol. Reprod. 56, 489-494 (1997).
9. Achen, M. G., Gad, J. M., Stacker, S. A. & Wilks, A. F. Placenta growth factor and vascular endothelial growth factor are co-expressed during early embryonic development. Growth Factors 15, 69-80 (1997).
10. Teesalu, T., Masson, R., Basset, P., Blasi, F. & Talarico, D. Expression of matrix metalloproteinases during murine chorioallantoic placenta maturation. Dev. Dyn. 214, 248-258 (1999).
11. Teesalu, T., Blasi, F. & Talarico, D. Expression and function of the urokinase type plasminogen activator during mouse hemochorial placental development. Dev. Dyn. 213, 27-38 (1998).
12. Gardner, R. L., Papaioannou, V. E. & Barton, S. C. Origin of the ectoplacental cone and secondary giant cells in mouse blastocysts reconstituted from isolated trophectoderm and inner cell mass. J. Embryol. Exp. Morphol. 30, 561-572 (1973).
13. Hunt, C. V. & Avery, G. B. The development and proliferation of the trophoblast from ectopic mouse embryo allografts of increasing gestational age. J. Reprod. Fertil. 46, 305-311 (1976).
14. Jenkinson, E. J. & Billington, W. D. Differential susceptibility of mouse trophoblast and embryonic tissue to immune cell lysis. Transplantation 18, 286-289 (1974).
15. Rossant, J. & Ofer, L. Properties of extra-embryonic ectoderm isolated from postimplantation mouse embryos. J. Embryol. Exp. Morphol. 39, 183-194 (1977).
16. Rossant, J. & Tamara-Lis, W. Effect of culture conditions in diploid to giant-cell transformation in postimplantation mouse trophoblast. J. Embryol. Exp. Morphol. 62, 217-227 (1981).
17. Ilgren, E. B. On the control of the trophoblastic giant-cell transformation in the mouse: homotypic cellular interactions and polyploidy. J. Embryol. Exp. Morphol. 62, 183-202 (1981).
18. Johnson, M. H. & Rossant, J. Molecular studies on cells of the trophectoderm lineage of the postimplantation mouse embryo. J. Embryol. Exp. Morphol. 61, 103-116 (1981).
19. Niswander, L. & Martin, G. R. Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755-768 (1992).
20. Rappolee, D. A., Basilico, C., Patel, Y. & Werb, Z. Expression and function of FGF-4 in peri-implantation development in mouse embryos. Development 120, 2259-2269 (1994).
21. Feldman, B., Poueymirou, W., Papaioannou, V. E., DeChiara, T. M. & Goldfarb, M. Requirement of FGF-4 for postimplantation mouse development. Science 267, 246-249 (1995).
22. Wilder, P. J. et al. Inactivation of the FGF-4 gene in embryonic stem cells alters the growth and/or the survival of their early differentiated progeny. Dev. Biol. 192, 614-629 (1997).
23. Chai, N. et al. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev. Biol. 198, 105-115 (1998).
24. Nichols, J. et al. Formation of pluripotent stem cells in the mammalian embryo depends on the POU transcription factor Oct4. Cell 95, 379-391 (1998).
25. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. & Rossant, J. Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075 (1998).
26. Rappolee, D. A., Patel, Y. & Jacobson, K. Expression of fibroblast growth factor receptors in peri-implantation mouse embryos. Mo,. Reprod. Dev. 51, 254-264 (1998).
27. Haffner-Krausz, R., Gorivodsky, M., Chen, Y. & Lonai, P. Expression of Fgfr2 in the early mouse embryo indicates its involvement in preimplantation development. Mech. Dev. 85, 167-172 (1999).
28. Arman, E., Haffner-Krausz, R., Chen, Y., Heath, J. K. & Lonai, P. Targeted disruption of fibroblast growth factor (FGF) receptor 2 suggests a role for FGF signaling in pregastrulation mammalian development. Proc. Natl Acad. Sci. USA 95, 5082-5087 (1998).
29. Xu, X. et al. Fibroblast growth factor receptor 2 (FGFR2)-mediated reciprocal regulation loop between FGF8 and FGF10 is essential for limb induction. Development 125, 753-765 (1998).
30. Isaacs, H. V., Pownall, M. E. & Slack, J. M. Regulation of Hox gene expression and posterior development by the Xenopus caudal homologue Xcad3. EMBO J. 17, 3413-3427 (1998).
31. Smith, J. C., Price, B. M. J., Green, J. B. A., Weigel, D. & Hermann, B. G. Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell 67, 79-87 (1991).
32. Griffin, K. J., Amacher, S. L., Kimmel, C. B. & Kimelman, D. Molecular identification of spadetail: regulation of zebrafish trunk and tail mesoderm formation by T-box genes. Development 125, 3379-3388 (1998).
33. Beck, F., Chawengsaksophak, K., Waring, P., Playford, R. J. & Furness, J. B. Reprogramming of intestinal differentiation and intercalary regeneration in Cdx2 mutant mice. Proc. NatlAcad. Sci. USA 96, 7318-7323 (1999).
34. Russ, A. P. et al. Eomesodermin is required for mouse trophoblast development and mesoderm formation. Nature 404, 95-99 (2000).
35. Ciruna, B. G. & Rossant, J. Expression of the T-box gene Eomesodermin during early mouse development. Mech. Dev. 81, 199-203 (1999).
36. Chawengsaksophak, K., James, R., Hammond, V. E., Kontgen, F. & Beck, F. Homeosis and intestinal tumours in Cdx2 mutant mice. Nature 386, 84-87 (1997).
37. Pettersson, K. et al. Expression of a novel member of estrogen response element-binding nuclear receptors is restricted to the early stages of chorion formation during mouse embryogenesis. Mech. Dev. 54, 211-223 (1996).
38. Luo, J. et al. Placental abnormalities in mouse embryos lacking the orphan nuclear receptor ERR-beta. Nature 388, 778-782 (1997).
39. Tremblay, G. B. et al. Diethylstilbestrol regulates trophoblast stem cell differentiation as a ligand of orphan nuclear receptor ERRbeta. Genes Dev. 15, 833-838(2001).
40. Van, J. et al. Retinoic acid promotes differentiation of trophoblast stem cells to a giant cell fate. Dev. Biol. (in the press).
41. Gurtner, G. C. et al. Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev. 9, 1-14 (1995).
42. Kwee, L. et al. Defective development of the embryonic and extraembryonic circulatory systems in vascular cell adhesion molecule (VCAM-1) deficient mice. Development 121, 489-503 (1995).
43. Yang, J. T., Rayburn, H. & Hynes, R. O. Cell adhesion events mediated by alpha-4 integrins are essential in placental and cardiac development. Development 121, 549-560 (1995).
44. Hunter, P. J., Swanson, B. J., Haendel, M. A., Lyons, G. E. & Cross, J. C. Mrj encodes a DnaJ-related cobnhe4101 chaperone that is essential for murine placental development. Development 126, 1247-1258 (1999).
45. Anson-Cartwright, L. et al. The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nature Genet. 25, 311-314 (2000).
46. Schreiber, J. et al. Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol. Cell. Biol. 20, 2466-2474 (2000).
47. Basyuk, E. et al. The murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev. Dyn. 214, 303-311 (1999).
48. Hernandez-Verdun, D. Morphogenesis of the syncytium in the mouse placenta. Ultrastructural study. Cell Tissue Res. 148, 381-396 (1974).
49. Hemberger, M. & Cross, J. C. Genes governing placental development. Trends Endocrin. Metab. 12, 162-168 (2001).
50. Nogawa, H. & Ito, T. Branching morphogenesis of embryonic mouse lung epithelium in mesenchyme-free culture. Development 121, 1015-1022 (1995).
51. Arman, E., Haffner-Krausz, R., Gorivodsky, M. & Lonai, P. Fgfr2 is required for limb outgrowth and lung-branching morphogenesis. Proc. Natl Acad. Sci. USA 96, 11895-11899 (1999).
52. Dudley, A. T., Godin, R. E. & Robertson, E. J. Interaction between FGF and BMP signaling pathways regulates development of metanephric mesenchyme. Genes Dev. 13, 1601-1613 (1999).
53. Skaer, H. Morphogenesis: FGF branches out. Curr. Biol. 7, R238-R241 (1997).
54. Cheng, A. M. et al. Mammalian Grb2 regulates multiple steps in embryonic development, lineage commitment and malignant transformation. Cell 95, 793-603 (1998).
55. Saxton, T. M. et al. Gene dosage dependent functions for phosphotyrosine-Grb2 signaling during mammalian tissue morphogenesis. Curr. Biol. 11, 662-670 (2001).
56. Itoh, M. et al. Role of Gab1 in heart, placenta, and skin development and growth factor-and cytokine-induced extracellular signal-regulated kinase mitogen-activated protein kinase activation. Mol. Cell. Biol. 20, 3695-3704 (2000).
57. Qian, X. et al. The Sos1 and Sos2 Ras-specific exchange factors: differences in placental expression and signaling properties. EMBOJ. 19, 642-654 (2000).
58. Giroux, S. et al. Embryonic death of Mek1 -deficient mice reveals a role for this kinase in angiogenesis in the labyrinthine region of the placenta. Curr. Biol. 9, 369-372 (1999).
59. Adams, R. H. et al. Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol. Cell 6, 109-116 (2000).
60. Yang, J. et al. Mekk3 is essential for early embryonic cardiovascular development. Nature Genet. 24, 309-313 (2000).
61. Galceran, J., Farinas, I., Depew, M. J., Clevers, H. & Grosschedl, R. Wnt3a-/-like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev. 13, 709-717 (1999).
62. Monkley, S. J., Delaney, S. J., Pennisi, D. J., Christiansen, J. H. & Wainwright, B. J. Targeted disruption of the Wnt2 gene results in placentation defects. Development 122, 3343-3353 (1996).
63. Ishikawa, T. et al. Mouse Wnt receptor gene Fzd5 is essential for yolk sac and placental angiogenesis. Development 128, 25-33 (2001).
64. Castellucc, M., Kosanke, G., Verdenelli, F., Huppertz, B. & Kaufmann, P. Villous sprouting: fundamental mechanisms of human placental development. Hum. Reprod. Update 6, 485-494 (2000).
65. Burrow, C. R. Regulatory molecules in kidney development. Pediatr. Nephrol. 14, 240-253 (2000).
66. Warburton, D. et al. The molecular basis of lung morphogenesis. Mech. Dev. 92, 55-81 (2000).
67. Li, Y., Lemaire, P. & Behringer, R. R. Esx1, a novel X chromosome-linked homeobox gene expressed in mouse extraembryonic tissues and male germ cells. Dev. Biol. 188, 85-95 (1997).
68. Li, Y. & Behringer, R. R. Esx1 is an X-chromosome-imprinted regulator of placental development and fetal growth. Nature Genet. 20, 309-311 (1998).
69. Adelman, D. M., Gertsenstein, M., Nagy, A., Simon, M. C. & Maltepe, E. Placental cell fates are regulated In vivo by HIF-mediated hypoxia responses. Genes Dev 14, 3191-3203 (2000).
70. Kozak, K. R., Abbott, B. & Hankinson, O. ARNT-deficient mice and placental differentiation. Dev. Biol. 191, 297-305 (1997).
71. Maltepe, E. & Simon, M. C. Oxygen, genes, and development: an analysis of the role of hypoxic gene regulation during murine vascular development. J. Mol. Med. 76, 391-401 (1998).
72. Caniggia, I. et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J. Clin. Invest. 105, 577-587 (2000).
73. Genbacev, O., Zhou, Y., Ludlow, J. W. & Fisher, S. J. Regulation of human placental development by oxygen tension. Science 277, 1669-1672 (1997).
74. Zybina, E. V. & Zybina, T. G. Polytene chromosomes in mammalian cells. Int. Rev. Cytol. 165, 53-119 (1996).
75. MacAuley, A., Cross, J. C. & Werb, Z. Reprogramming the cell cycle for endoreduplication in rodent trophoblast cells. Mol. Biol. Cell 9, 795-807 (1998).
76. Berezowsky, J., Zbieranowski, I., Demers, J. & Murray, D. DNA ploidy of hydatidiform moles and nonmolar conceptuses: a study using flow and tissue section image cytometry. Mod. Pathol. 8, 775-781 (1995).
77. Alders, M. et al. The human Achaete-Scute homologue 2 (ASCL2, HASH2) maps to chromosome 11p15. 5, close to ICF2 and is expressed in extravillus trophoblasts. Hum. Mol. Genet. 6, 859-867 (1997).
78. Janatpour, M. J. et al. A repertoire of differentially expressed transcription factors that offers insight into mechanisms of human cytotrophoblast differentiation. Dev Genet. 25, 146-157 (1999).
79. Knofler, M., Meinhardt, G., Vasicek, R., Husslein, P. & Egarter, C. Molecular cloning of the human Hand1 gene/cDNA and its tissue-restricted expression in cytotrophoblastic cells and heart. Gene 224, 77-86 (1995).
80. Nait-Oumesmar, B., Copperman, A. B. & Lazzarini, R. A. Placental expression and chromosomal localization of the human Gcm 1 gene. J. Histochem. Cytochem. 48, 915-922 (2000).
81. Somerset, D. A. et al. Ontogeny of hepatocyte growth factor (HGF) and its receptor (c-met) in human placenta: reduced HGF expression in intrauterine growth restriction. Am. J. Pathol. 153, 1139-1147 (1998).
82. Cross, J. C. Trophoblast function in normal and preeclamptic pregnancy. Fet. Mat. Med. Rev. 8, 57-66 (1996).
83. Meegdes, B. H., Ingenhoes, R., Peeters, L. L. & Exalto, N. Early pregnancy wastage: relationship between chorionic vascularization and embryonic development. Fertil. Steril. 49, 216-220 (1988).
84. Ornoy, A., Salamon-Arnon, J., Ben-Zur, Z. & Kohn, G. Placental findings in spontaneous abortions and stillbirths. Teratology 24, 243-252 (1981).
85. van Lijnschoten, G., Arends, J. W. & Geraedts, J. P. Comparison of histological features in early spontaneous and induced trisomic abortions. Placenta 15, 765-773 (1994).
86. Krebs, C. et al. Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree. Am. J. Obstet. Gynecol. 175, 1534-1542 (1996).
87. Nagy, A. et al. Embryonic stem cells alone are able to support fetal development in the mouse. Development 110, 815-821 (1990).
88. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W. & Roder, J. C. Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl Acad. Sci. USA 90, 8424-8428 (1993).
89. Tanaka, M., Gertsenstein, M., Rossant, J. & Nagy, A. Mash2 acts cell autonomously in mouse spongiotrophoblast development. Dev. Biol. 190, 55-65 (1997).
90. Guillemot, F., Nagy, A., Auerbach, A., Rossant, J. & Joyner, A. L. Essential role of Mash-2 in extraembryonic development. Nature 371, 333-336 (1994).
91. Voss, A. K., Thomas, T. & Gruss, P. Mice lacking HSP90beta fail to develop a placental labyrinth. Development 127, 1-11 (2000).
92. Schreiber, M. et al. Placental vascularisation requires the AP-1 component fra1. Development 127, 4937-4948 (2000).
93. Schorpp-Kistner, M., Wang, Z. Q., Angel, P. & Wagner, E. F. JunB is essential for mammalian placentation. EMBOJ. 18, 934-948 (1999).
94. Kraut, N., Snider, L., Chen, C. M., Tapscott, S. J. & Groudine, M. Requirement of the mouse I-mfa gene for placental development and skeletal patterning. EMBO J. 17, 6276-6288 (1998).
95. Yamamoto, H. et al. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev. 12, 1315-1326 (1998).
96. Threadgill, D. W. et al. Targeted disruption of mouse EGF receptor: effect of genetic background on mutant phenotype. Science 269, 230-234 (1995).
97. Sibilia, M. & Wagner, E. F. Strain-dependent epithelial defects in mice lacking the EGF receptor. Science 269l 234-238 (1995).
98. Xiao, X. et al. HSF1 is required for extra-embryonic development, postnatal growth and protection during inflammatory responses in mice. EMBO J. 18, 5943-5952 (1999).
99. Solloway, M. J. & Robertson, E. J. Early embryonic lethality in Bmp5;Bmp7 double mutant mice suggests functional redundancy within the 60A subgroup. Development 126, 1753-1768 (1999).
100. Li, E., Bestor, T. H. & Jaenisch, R. Targeted mutation of the DNA methyltransferase gene results in embryonic lethality. Cell 69, 915-926 (1992).
101. Shawlot, W. & Behringer, R. R. Requirement for Lim1 in head-organizer function. Nature 374, 425-430 (1995).
102. Rashbass, P., Cooke, L. A., Herrmann, B. G. & Beddington, R. S. P. A cell autonomous function of Brachyury in T/T embryonic stem cell chimaeras. Nature 353, 348-349 (1991).
103. Morasso, M. I., Grinberg, A., Robinson, G., Sargent, T. D. & Mahon, K. A. Placental failure in mice lacking the homeobox gene Dlx3. Proc. Natl Acad. Sci. USA 96, 162-167 (1999).
104. Kruger, O. et al. Defective vascular development in connexin 45-deficient mice. Development 127, 4179-4193 (2000).
105. Uehara, Y. et al. Placental defect and embryonic lethality in mice lacking hepatocyte growth factor/scatter factor. Nature 373, 702-705 (1995).
106. Goh, K. L., Yang. J. T. & Hynes, R. O. Mesodermal defects and cranial neural crest apoptosis in alpha5 integrin-null embryos. Development 124, 4309-4319 (1997).
107. Ware, C. B. et al. Targeted disruption of the low-affinity leukemia inhibitory factor receptor gene causes placental, skeletal, neural and metabolic defects and results in perinatal death. Development 121, 1283-1299 (1995).
108. Bladt, F., Riethmacher, D., Isenmann, S., Aguzzi, A. & Birchmeier, C. Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud. Nature 376, 768-771 (1995).
109. Ohlsson, R. et al. PDGFB regulates the development of the labyrinthine layer of the mouse fetal placenta. Dev. Biol. 212, 124-136 (1999).
110. Wendung, O., Chambon, P. & Mark, M. Retinoid X receptors are essential for early mouse development and placentogenesis. Proc. Natl Acad. Sci. USA 96, 547-551 (1999).
111. Gnarra, J. R. et al. Defective placental vasculogenesis causes embryonic lethality in VHL-deficient mice. Proc. Natl Acad. Sci. USA 94, 9102-9107 (1997).
112. Steingrimsson, E., Tessarollo, L., Reid, S. W., Jenkins, N. A. & Copeland, N. G. The bHLH-Zip transcription factor Tfeb is essential for placental vascularization. Development 125, 4607-4616 (1998).
113. Gabriel, H. D. et al. Transplacental uptake of glucose is decreased in embryonic lethal connexin26-deficient mice. J. Cell Biol. 140, 1453-1461 (1998).
114. Riley, P., Anson-Cartwright, L. & Cross, J. C. The Hand1 bHLH transcription factor is essential for placentation and cardiac morphogenesis. Nature Genet. 18, 271-275 (1998).
115. Ogura, Y., Takakura, N., Yoshida, H. & Nishikawa, S. I. Essential role of platelet-derived growth factor receptor alpha in the development of the intraplacental yolk sac/sinus of Duval in mouse placenta. Biol. Reprod. 58, 65-72 (1998).