Early patterning of the chorion leads to the trilaminar trophoblast cell structure in the placental labyrinth

Development

Volumn 135, Issue 12, 2008, Pages 2083-2091

  Simmons, David G ^a   Natale, David R C ^a   Begay, Valerie ^b   Hughes, Martha ^a   Leutz, Achim ^b   Cross, James C ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

Chorion; Gcm1; Labyrinth; Mouse; Placenta; Syncytin; Syncytiotrophoblast; Trophoblast

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN ALPHA; ENVELOPE PROTEIN; GLIAL CELLS MISSING 1 PROTEIN; HAND1 PROTEIN; SYNCYTIN B; TRANSCRIPTION FACTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL SPECIFICITY; CELL STRUCTURE; CELLULAR DISTRIBUTION; CHORION; CONTROLLED STUDY; EMBRYO; EMBRYO PATTERN FORMATION; FETUS MEMBRANE; GENE EXPRESSION; INNER EAR; MATERNAL BLOOD; MORPHOGENESIS; MOUSE; MUTANT; NONHUMAN; PLACENTA; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SYNCYTIOTROPHOBLAST; TROPHOBLAST;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CCAAT-ENHANCER-BINDING PROTEINS; CELL DIFFERENTIATION; CELLS, CULTURED; CELLULAR STRUCTURES; CHORION; CROSSES, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HETEROZYGOTE; MICE; MICE, INBRED STRAINS; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUTATION; NEUROPEPTIDES; PLACENTA; PREGNANCY; PREGNANCY PROTEINS; STEM CELLS; TROPHOBLASTS;

RODENTIA;

EID: 47649126492     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.020099     Document Type: Article

References (45)

1. Akiyama, Y., Hosoya, T., Poole, A. M. and Hotta, Y. (11996). The gcm-motif: a novel DNA-binding motif conserved in Drosophila and mammals. Proc. Natl. Acad. Sci. USA 93, 14912-14916.
2. Anson-Cartwright, L., Dawson, K., Holmyard, D., Fisher, S. J., Lazzarini, R. A. and Cross, J. C. (2000). The glial cells missing-1 protein is essential for branching morphogenesis in the chorioallantoic placenta. Nat. Genet. 25, 311-314.
3. Basyuk, E., Cross, J. C., Corbin, J., Nakayama, H., Hunter, P., Nait-Oumesmar, B. and Lazzarini, R. A. (1999). Murine Gcm1 gene is expressed in a subset of placental trophoblast cells. Dev. Dyn. 214, 303-311.
4. Beck, F., Erler, T., Russell, A. and James, R. (1995). Expression of Cdx-2 in the mouse embryo and placenta: possible role in patterning of the extra-embryonic membranes. Dev. Dyn. 204, 219-227.
5. Begay, V., Smink, J. and Leutz, A. (2004). Essential requirement of CCAAT/enhancer binding proteins in embryogeresis. Mol. Cell. Biol. 24, 9744-9751.
6. Berghorn, K. A., Clark, P. A., Encarnacion, B., Deregis, C. J., Folger, J. K., Morasso, M. I., Soares, M. J., Wolfe, M. W. and Roberson, M. S. (2005). Developmental expression of the homeobox protein Distal-less 3 and its relationship to progesterone production in mouse placenta. J. Endocrinol. 186, 315-323.
7. Campbell, W. J., Deb, S., Kwok, S. C., Joslin, J. A. and Soares, M. J. (1989). Differential expression of placental lactogen-II and prolactin-like protein-A in the rat chorioallantoic placenta. Endocrinology 125, 1565-1574.
8. Chang, C. W., Chuang, H. C., Yu, C., Yao, T. P. and Chen, H. (2005). Stimulation of GCMa transcriptional activity by cyclic AMP/ protein kinase A signaling is attributed to CBP-mediated acetylation of GCMa. Mol. Cell. Biol. 25, 8401-8414.
9. Church, G. M. and Gilbert, W. (1984). Genomic sequencing. Proc. Natl. Acad. Sci. USA 81, 1991-1995.
10. Coan, P. M., Ferguson-Smith, A. C. and Burton, G. J. (2005). Ultrastructural changes in the interhaemal membrane and junctional zone of the murine chorioallantoic placenta across gestation. J. Anat. 207, 783-796.
11. Cross, J. C. (2000). Genetic insights into trophoblast differentiation and placental morphogenesis. Semin. Cell Dev. Biol. 11, 105-113.
12. Cross, J. C., Nakano, H., Natale, D. R., Simmons, D. G. and Watson, E. D. (2006). Branching morphogenesis during development of placental villi. Differentiation 74, 393-401.
13. Dai, G., Wang, D., Liu, B., Kasik, J. W., Muller, H., White, R. A., Hummel, G. S. and Soares, M. J. (2000). Three novel paralogs of the rodent prolactin gene family. J. Endocrinol. 166, 63-75.
14. Davies, J. and Glasser, S. R. (1968). Histological and fine structural observations on the placenta of the rat. Acta Anat. Basel 69, 542-608.
15. Deb, S., Faria, T. N., Roby, K. F., Larsen, D., Kwok, S. C., Talamantes, F. and Soares, M. J. (1991). Identification and characterization of a new member of the prolactin family, placental lactogen-I variant. J. Biol. Chem. 266, 1605-1610.
16. Dupressoir, A., Marceau, G., Vernochet C., Benit L., Kanellopoulos, C., Sapin, V. and Heidmann, T. (2005). Syncytin-A and syncytin-B, two fusogenic placenta-specific murine envelope genes of retroviral origin conserved in Muridae. Proc. Natl. Acad Sci. USA 102, 725-730.
17. Enders, A. C. (1965). A comparative study of the fine structure of the trophoblast in several hemochorial placentas. Am. J. Anat. 116, 29-67.
18. Hancock, S. N., Agulnik, S. I., Silver, L. M. and Papaioannou, V. E. (1999). Mapping and expression analysis of the mouse ortholog of Xenopus Eomesodermin. Mech. Dev. 81, 205-208.
19. Hemberger, M. and Cross, J. C. (2001). Genes governing placental development. Trends Endocrinol. Metab. 12, 162-168.
20. Hernandez-Verdun, D. (1974). Morphogenesis of the syncytium in the mouse placenta. Ultrastructural study. Cell Tissue Res. 148, 381-396.
21. Hughes, M., Dobric, N., Scott, I. C., Su, L., Starovic, M., St-Pierre, B., Egan, S. E., Kingdom, J. C. and Cross, J. C. (2004). The Hand1, Stra13 and Gcm1 transcription factors override FGF signaling to promote terminal differentiation of trophoblast stem cells. Dev. Biol. 271, 362-371.
22. Ishida, M., Ono, K., Taguchi, S., Ohashi, S., Naito, J., Horiguchi, K. and Harigaya, T. (2004). Cathepsin gene expression in Mouse placenta during the latter half of pregnancy. J. Reprod. Dev. 50, 515-523.
23. Jacquemin, P., Sapin, V., Alsat, E., Evain-Brion, D., Polle, P. and Davidson, I. (1998). Differential expression of the TEF family of transcription factors in the munne placenta and during differentiation of primary human trophoblasts in vitro. Dev. Dyn. 212, 423-436.
24. Jollie, W. P. (1964). Fine structural changes in placental labyrinth of the rat with increasing gestational age. J. Ultrastruct. Res. 10, 27-47.
25. Lee, C. K., Moon, D. H., Shin, C. S., Kim, H., Yoon, Y. D., Kang, H. S., Lee, B. J. and Kang, S. G. (2003). Circadian expression of Mel1a and PL-II genes in placenta: effects of melatonin on the PL-II gene expression in the rat placenta. Mol. Cell. Endocrinol. 200, 57-66.
26. Li, Y., Lemaire, P. and Behringer, R. R. (1997). Esx1, a novel X chromosome-linked homeobox gene expressed in mouse extraembryonic tissues and male germ cells. Dev. Biol. 188, 85-95.
27. Mo, F., Muntean, A. G., Chen, C., Stolz, D. B., Watkins, S. C. and Lau, L. F. (2002). CYR61 (CCN1) is essential for placental development and vascular integrity. Mol. Cell. Biol. 22, 8709-8720.
28. Morasso, M. I., Grinberg, A., Robinson, G., Sargent T. D. and Mahon, K. A. (1999). Placental failure in mice lacking the homeobox gene Dlx3. Proc. Natl. Acad. Sci. USA 96, 162-167.
29. Pettersson, K., Svensson, K., Mattsson, R., Carlsson, B., Ohlsson, R. and Berkenstam, A. (1996). Expression of a novel mernber of estrogen response element-binding nuclear receptors is restricted to the early stages of chorion formation during mouse embryogenesis. Mech. Dev. 54, 211-223.
30. Rossant, J. and Cross, J. C. (2001). Placental development: lessons from mouse mutants. Nat. Rev. Genet. 2, 538-548.
31. Sahgal, N., Knipp, G. T, Liu, B., Chapman, B. M., Dai, G. and Soares, M. J. (2000). Identification of two new nonclassical members of the rat prolactin family, J. Mol. Endocrinol. 24, 95-108.
32. Schreiber, J., Sock, E. and Wegner, M. (1997). The regulator of early gliogenesis glial cells missing is a transcription factor with a novel type of DNA-binding domain. Proc. Natl. Acad Sci. USA 94, 4739-4744.
33. Schreiber, J, Riethmacher-Sonnenberg, E., Riethmacher, D., Tuerk, E. E., Enderich, J., Bosl, M. R. and Wegner, M. (2000). Placental failure in mice lacking the mammalian homolog of glial cells missing, GCMa. Mol. Cell. Biol. 20, 2466-2474.
34. Schubert, S. W., Kardash, E., Khan, M. A., Cheusova, T. Killan, K., Wegner, M. and Hashemolhosseini, S. (2004). Interaction, cooperative promoter modulation, and renal colocalization of GCMa and Pitx2. J. Biol. Chem. 279, 50358-50365.
35. Scott, I. C., Anson-Cartwright L., Riley, P., Reda, D. and Cross, J. C. (2000). The HAND1 basic helix-loop-helix transcription factor regulates trophoblast differentiation via multiple mechanisms. Mol. Cell. Biol. 20, 530-541.
36. Simmons, D. G. and Cross, J. C. (2005). Determinants of trophoblast lineage and cell subtype specification in the mouse placenta. Dev. Biol. 284, 12-24.
37. Simmons, D. G, Fortier, A. L. and Cross, J. C. (2007). Diverse subtypes and developmental origins of trophoblast giant cells in the mouse placenta. Dev. Biol. 304, 567-578.
38. Snell, G. D. and Stevens, L. C. (1966). Early embryology. In Biology of the Laboratory Mouse (ed. E. L. Green), pp. 205-245. New York: McGraw-Hill.
39. Steingrimsson, E., Tessarollo, L., Reid, S. W., Jenkins, N. A. and Copeland, N. G. (1998). The bHLH-Zip transcription factor Tfeb is essential for placental vascularization. Development 125, 4607-4616.
40. Susens, U., Aguiluz, J. B., Evans, R. M. and Borgmeyer, U. (1997). The germ cell nuclear factor mGCNF is expressed in the developing nervous system. Dev. Neurosci. 19, 410-420.
41. Tanaka, S., Kunath, T., Hadjantonakis, A. K., Nagy, A. and Rossant, J. (1998). Promotion of trophoblast stem cell proliferation by FGF4. Science 282, 2072-2075.
42. Tompers, D. M., Foreman, R. K., Wang, Q., Kumanova, M. and Labosky, P. A. (2005). Foxd3 is required in the trophoblast progenitor cell lineage of the mouse embryo. Dev. Biol. 285, 126-137.
43. Uy, G. D., Downs, K. M. and Gardner, R. L. (2002). inhibition of trophoblast stem cell potential in chorionic ectoderm coincides with occlusion of the ectoplacental cavity in the mouse. Development 129, 3913-3924.
44. Voss, A. K., Thomas, T. and Gruss, P. (2000). Mice lacking HSP90beta fail to develop a placental labyrinth. Development 127, 1-11.
45. Watson, E. D. and Cross, J. C. (2005), Development of structures and transport functions in the mouse placenta. Physiology Bethesda 20, 180-193.