Winged-Helix, Hedgehog and Bmp genes are differentially expressed in distinct cell layers of the murine yolk sac

Mechanisms of Development

Volumn 62, Issue 2, 1997, Pages 197-211

  Farrington, Sarah M ^a   Belaoussoff, Maria ^a   Baron, Margaret H ^a  

^a HARVARD UNIVERSITY   (United States)

Author keywords

bone morphogenetic protein; extraembryonic mesoderm; hedgehog; visceral endoderm; winged helix; yolk sac

Indexed keywords

BONE MORPHOGENETIC PROTEIN; COMPLEMENTARY DNA;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ENDODERM; GENE EXPRESSION; HEDGEHOG; IN SITU HYBRIDIZATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; YOLK SAC;

AMINO ACID SEQUENCE; ANIMALS; BONE MORPHOGENETIC PROTEINS; DNA-BINDING PROTEINS; DROSOPHILA PROTEINS; HEPATOCYTE NUCLEAR FACTOR 3-ALPHA; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HEPATOCYTE NUCLEAR FACTOR 3-GAMMA; INSECT PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; TIME FACTORS; TRANSCRIPTION FACTORS; YOLK SAC;

EID: 0030913168     PISSN: 09254773     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0925-4773(97)00664-3     Document Type: Article

References (82)

1. Adamson, E.D. (1982) The location and synthesis of transferrin in mouse embryos and teratocarcinoma cells. Dev. Biol. 91, 227-234.
2. Ang, S.-L. and Rossant, J. (1994) HNF-3β is essential for node and notochord formation in mouse development. Cell 78, 561-574.
3. Ang, S.-L., Wierda, A., Wong, D., Stevens, K.A., Cascio, S., Rossant, J. and Zaret, K.S. (1993) The formation and maintenance of the definitive endoderm lineage in the mouse: involvement of HNF3/forkhead proteins. Development 119, 1301-1315.
4. Ang, S.-L., Jin, O., Rhinn, M., Daigle, N., Stevenson, L. and Rossant, J. (1996) A targeted mouse Otx2 mutation leads to severe defects in gastrulation and formation of axial mesoderm and to deletion of rostral brain. Development 122, 243-252.
5. Augé-Gouillou, C., Petropoulos, I. and Zakin, M.M. (1993) Liver-enriched HNF-3 alpha and ubiquitous factors interact with the human transferrin gene enhancer. FEBS Lett. 323, 4-10.
6. Baron, M.H. and Maniatis, T. (1986) Rapid reprogramming of globin gene expression in transient heterokaryons. Cell 46, 591-602.
7. Bassel-Duby, R., Hernandez, M., Yang, Q., Rochelle, J., Seldin, M. and Williams, R. (1994) Myocyte nuclear factor, a novel winged-helix transcription factor under both developmental and neural regulation in striated myocytes. Mol. Cell. Biol. 14, 4596-4605.
8. Bitgood, M.J. and McMahon, A.P. (1995) Hedgehog and Bmp genes are coexpressed at many diverse sites of cell-cell interaction in the mouse embryo. Dev. Biol. 172, 126-138.
9. Bitgood, M.J., Shen, L. and McMahon, A.P. (1996) Sertoli cell signaling by Desert hedgehog regulates the male germline. Curr. Biol. 6, 298-304.
10. Chen, W.S., Manova, K., Weinstein, D.C., Duncan, S.A., Plump, A.S., Prezioso, V.R., Bachvarova, R.F. and Darnell, J.E.J. (1994) Disruption of the HNF-4 gene, expressed in visceral endoderm, leads to cell death in embryonic ectoderm and impaired gastrulation of mouse embryos. Genes Dev. 8, 2466-2477.
11. Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
12. Clark, K.L., Halay, E.D., Lai, E. and Burley, S.K. (1993) Co-crystal structure of the HNF-3/fork head DNA-recognition motif resembles histone H5. Nature 364, 412-420.
13. Clevidence, D.E., Overdier, D.G., Tao, W., Qian, X., Pani, L., Lai, E. and Costa, R.H. (1993) Identification of nine tissue-specific transcription factors of the hepatocyte nuclear factor 3/forkhead DNA-binding-domain family. Proc. Natl. Acad. Sci. USA 90, 3948-3952.
14. Concordet, J.P. and Ingham, P. (1995) Patterning goes sonic. Nature 375, 279-280.
15. Copp, A.J. (1995) Death before birth: clues from gene knockouts and mutations. Trends Genet. 11, 87-93.
16. Costa, R.H. (1994) Hepatocyte nuclear factor 3/forkhead protein family: mammalian transcription factors that possess divergent cellular expression patterns and binding specificities. In Tronche, F. and Yaniv, M. (eds.), Liver Gene Expression, Landes, Austin, TX, pp. 183-205.
17. Costa, R.H., Dyke, T.A.V., Yan, C., Kuo, F. and Darnell, J.E. (1990) Similarities in transthyretin gene expression and differences in transcription factors: liver and yolk sac compared to choroid plexus. Proc. Natl. Acad. Sci. USA 87, 6589-6593.
18. Costa, M., Sweeton, D. and Wieschaus, E. (1993) Gastrulation in Drosophila: cellular mechanisms of morphogenetic movements. In Bate, M. and Martinez-Arias, A. (eds.), Development of Drosophila melanogaster, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 425-465.
19. Coucouvanis, E. and Martin, G.R. (1995) Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell 83, 279-287.
20. Cross, J.C., Werb, Z. and Fisher, S.J. (1994) Implantation and the placenta: key pieces of the development puzzle. Science 2664, 1508-1518.
21. Duncan, S.A., Manova, K., Chen, W.S., Hoodless, P., Weinstein, D.C., Bachvarova, R.F. and Darnell, J.E.J. (1994) Expression of transcription factor HNF-4 in the extraembryonic endoderm, gut, and nephrogenic tissue of the developing mouse embryo: HNF-4 is a marker for primary endoderm in the implanting blastocyst. Proc. Natl. Acad. Sci. USA 91, 7598-7602.
22. Dziadek, M.A. and Andrews, G.K. (1983) Tissue specificity of alpha-fetoprotein messenger RNA expression during mouse embryogenesis. EMBO J. 2, 549-554.
23. Echelard, Y., Epstein, D.J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J.A. and McMahon, A.P. (1993) Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
24. Fan, C.-M. and Tessier-Lavigne, M. (1994) Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homolog. Cell 79, 1175-1186.
25. Farrington, S.M. (1996) Winged-Helix Transcription Factors and Yolk Sac Function in the Developing Mouse Embryo. Harvard University, Cambridge, MA.
26. Gardner, R.L. (1983) Origin and differentiation of extraembryonic tissues in the mouse. Int. Rev. Exp. Pathol. 24, 63-133.
27. Gordon-Thomson, C. and Fabian, B.C. (1994) Hypoblastic tissue and fibroblast growth factor induce blood tissue (haemoglobin) in the early chick embryo. Development 120, 3571-3579.
28. Gorin, M.B., Cooper, D.L., Eiferman, F., van de Rijn, P. and Tilghman, S.M. (1981) The evolution of α-fetoprotein and albumin I. A comparison of the primary amino acid sequences of mammalian α-fetoprotein and albumin. J. Biol. Chem. 256, 1954-1959.
29. Haar, J.L. and Ackerman, G.A. (1971) A phase and electron microscopic study of vasculogenesis and erythropoiesis in the yolk sac of the mouse. Anat. Rec. 170, 199-224.
30. Hatini, V., Huh, S.O., Herzlinger, D., Soares, V.C. and Lai, E. (1996) Essential role of stromal mesenchyme in kidney morphogenesis revealed by targeted disruption of Winged Helix transcription factor BF-2. Genes Dev. 10, 1467-1478.
31. Hogan, B. (1996) Bone morphogenetic proteins: multifunctional regulators of vertebrate development. Genes Dev. 10, 1580-1594.
32. Hogan, B., Beddington, R., Costantini, F. and Lacy, E. (1994) Manipulating the Mouse Embryo: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
33. Ingham, P.W. (1995) Signalling by hedgehog family proteins in Drosophila and vertebrate development. Curr. Opin. Genet. Dev. 5, 492-498.
34. Jacob, A., Budhiraja, S., Xian, X., Clevidence, D., Costa, R.H. and Reichel, R.R. (1994) Retinoic acid-mediated activation of HNF-3 alpha during EC stem cell differentiation. Nucleic Acids Res. 22, 2126-2133.
35. Johansson, B.M. and Wiles, M.V. (1995) Evidence for involvement of activin A and bone morphogenetic protein 4 in mammalian mesoderm and hematopoietic development. Mol. Cell. Biol. 15, 141-151.
36. Jollie, W.P. (1990) Development, morphology, and function of the yolk-sac placenta of laboratory rodents. Teratology 41, 361-381.
37. Kaestner, K.H., Lee, K.H., Schlöndorff, J., Hiemisch, H., Monaghan, A.P. and Schütz, G. (1993) Six members of the mouse forkhead gene family are developmentally regulated. Proc. Natl. Acad. Sci. USA 90, 7628-7631.
38. Kaestner, K.H., Hiemisch, H., Luckow, B. and Schütz, G. (1994) The HNF-3 gene family of transcription factors in mice: gene structure, cDNA sequence, and mRNA distribution. Genomics 20, 377-385.
39. Kaufman, M.H. (1992) The Atlas of Mouse Development, Academic Press, London.
40. Lai, E., Prezioso, V.R., Smith, E., Litvin, O., Costa, R.H. and Darnell, J.E. (1990) HNF-3A, a hepatocyte-enriched transcription factor of novel structure is regulated transcriptionally. Genes Dev. 4, 1427-1436.
41. Lai, E., Prezioso, V.R., Tao, W., Chen, W.S. and Darnell, J.E. (1991) Hepatocyte nuclear factor 3α belongs to a gene family in mammals that is homologous to the Drosophila homeotic gene fork head. Genes Dev. 5, 416-427.
42. Laufer, E., Nelson, C.E., Johnson, R.L., Morgan, B.A. and Tabin, C. (1994) Sonic hedgehog and Fgf-4 act through a signaling cascade and feedback loop to integrate growth and patterning of the developing limb bud. Cell 79, 993-1003.
43. Lawson, K.A. and Pedersen, R.A. (1987) Cell fate, morphogenetic movement and population kinetics of embryonic endoderm at the time of germ layer formation in the mouse. Development 101, 627-652.
44. Lawson, K.A., Meneses, J.J. and Pedersen, R.A. (1991) Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891-911.
45. Levak-Svajger, B., Svajger, A. and Skreb, N. (1969) Separation of germ layers in presomite rat embryos. Experientia 25, 1311-1312.
46. Li, C., Lai, C., Sigman, D.S. and Gaynor, R.B. (1991) Cloning of a cellular factor, interleukin binding factor, that binds to NFAT-like motifs in the human immunodeficiency virus long terminal repeat. Proc. Natl. Acad. Sci. USA 88, 7739-7743.
47. Martí, E., Bumcrot, D.A., Takada, R. and McMahon, A.P. (1995) Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375, 322-325.
48. Meehan, R.R., Barlow, D.P., Hill, R.E., Hogan, B.L. and Hastie, N.D. (1984) Pattern of serum protein gene expression in mouse visceral yolk sac and foetal liver. EMBO J. 3, 1881-1885.
49. Millonig, J.H., Emerson, J.A., Levorse, J.M. and Tilghman, S.M. (1995) Molecular analysis of the distal enhancer of the mouse alpha-fetoprotein gene. Mol. Cell. Biol. 15, 3848-3856.
50. Miura, Y. and Wilt, F.H. (1969) Tissue interaction and the formation of the first erythroblasts of the chick embryo. Dev. Biol. 19, 201-211.
51. Monaghan, A.P., Kaestner, K.H., Grau, E. and Schütz, G. (1993) Post-implantation expression patterns indicate a role for the mouse fork-head/HNF-3α, β and γ genes in determination of the definitive endoderm, chordamesoderm and neuroectoderm. Development 119, 567-578.
52. Niswander, L. and Martin, G.R. (1992) Fgf-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755-768.
53. O'Reilly, M.-A.J., Smith, J.C. and Cunliffe, V. (1995) Patterning of the mesoderm in Xenopus: dose-dependent and synergistic effects of Brachyury and Pintallavis. Development 121, 1351-1359.
54. Palis, J., McGrath, K.E. and Kingsley, P.D. (1995) Initiation of hematopoiesis and vasculogenesis in murine yolk sac explants. Blood 86, 156-163.
55. Peters, G., Brookes, S., Smith, R., Placzek, M. and Dickson, C. (1989) The mouse homolog of the hst/k-fgf gene is adjacent to int-2 and is activated by proviral insertion of some virally induced mammary tumors. Proc. Natl. Acad. Sci. USA 86, 5678-5682.
56. Reichel, R.R., Budhiraja, S. and Jacob, A. (1994) Delayed activation of HNF-3 beta upon retinoic acid-induced teratocarcinoma cell differentiation. Exp. Cell Res. 214, 634-641.
57. Riddle, R.D., Johnson, R.L., Laufer, E. and Tabin, C. (1993) Sonic hedgehog mediates the polarizing activity of the ZPA. Cell 75, 1401-1416.
58. Roach, S., Schmid, W. and Pera, M.F. (1994) Hepatocytic transcription factor expression in human embryonal carcinoma and yolk sac carcinoma cell lines: expression of HNF-3 alpha in models of early endodermal cell differentiation. Exp. Cell Res. 2154, 189-198.
59. Roberts, D.J., Johnson, R.L., Burke, A.C., Nelson, C.E., Morgan, B.A. and Tabin, C. (1995) Sonic hedgehog is an endodermal signal inducing Bmp-4 and Hox genes during induction and regionalization of the chick hindgut. Development 121, 3163-3174.
60. Roelink, H., Augsburger, A., Heemskerk, J., Korzh, V., Norlin, S., Ruiz i Altaba, A., Tanabe, Y., Placzek, M., Edlund, T., Jessell, T.M., et al. (1994) Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76, 761-775.
61. Ruiz i Altaba, A., Cox, C., Jessel, T.M. and Klar, A. (1993a) Ectopic neural expression of a floor plate marker in frog embryos injected with the midline transcription factor Pintallavis. Proc. Natl. Acad. Sci. USA 90, 8268-8272.
62. Ruiz i Altaba, A., Prezioso, V.R., Darnell, J.E. and Jessell, T.M. (1993b) Sequential expression of HNF-3β and HNF-3α by embryonic organizing centers: the dorsal lip/node, notochord and floor plate. Mech. Dev. 44, 91-108.
63. Sambrook, J., Fritsch, E.F. and Maniatis, T. (1989) Molecular Cloning: a Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
64. Sasaki, H. and Hogan, B.L.M. (1993) Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118, 47-59.
65. Sasaki, H. and Hogan, B. (1994) HNF-3β as a regulator of floor plate development. Cell 76, 103-115.
66. Schmitt, R.M., Bruyns, E. and Snodgrass, H.R. (1991) Hematopoietic development of embryonic stem cells in vitro: cytokine and receptor gene expression. Genes Dev. 5, 728-740.
67. Shawlot, W. and Behringer, R.R. (1995) Requirement for Lim1 in head-organizer function. Nature 374, 425-430.
68. Soprano, D.R., Soprano, K.J. and Goodman, D.S. (1986) Retinol-binding protein and transthyretin mRNA levels in visceral yolk sac and liver during fetal development in the rat. Proc. Natl. Acad. Sci. USA 83, 7330-7334.
69. Soudais, C., Bielinska, M., Heikinheimo, M., MacArthur, C.A., Narita, N., Saffitz, J.E., Simon, M.C., Leiden, J.M. and Wilson, D.B. (1995) Targeted mutagenesis of the transcription factor GATA-4 gene in mouse embryonic stem cells disrupts visceral endoderm differentiation in vitro. Development 121, 3877-3888.
70. Spyropoulos, D.D. and Capecchi, M.R. (1994) Targeted disruption of the even-skipped gene, evx-1, causes early postimplantation lethality of the mouse conceptus. Genes Dev. 8, 1949-1961.
71. Thomas, T., Southwell, B.R., Schreiber, G. and Jaworowski, A. (1990) Plasma protein synthesis and secretion in the visceral yolk sac of the fetal rat: gene expression, protein synthesis and secretion. Placenta 11, 413-430.
72. Tronche, F. and Yaniv, M. (1994) Liver Gene Expression, Landes, Austin, TX, p. 350.
73. Vainio, S., Karavanova, I., Jowett, A. and Thesleff, I. (1993) Identification of BMP-4 as a signal mediating secondary induction between epithelial and mesenchymal tissues during early tooth development. Cell 75, 45-58.
74. Vortkamp, A., Lee, K., Lanske, B., Segre, G.V., Kronenberg, H.M. and Tabin, C.J. (1996) Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science 273, 613-622.
75. Weigel, D., Bellen, H.J., Jürgens, G. and Jäckle, H. (1989a) Primordium specific requirement of the homeotic gene fork head in the developing gut of the Drosophila embryo. Roux's Arch. Dev. Biol. 198, 201-210.
76. Weigel, D., Jürgens, G., Küttner, F., Seifert, E. and Jäckle, H. (1989b) The homeotic gene fork head encodes a nuclear protein and is expressed in the terminal regions of the Drosophila embryo. Cell 57, 645-658.
77. Weinstein, D.C., Ruiz i Altaba, A., Chen, W.S., Hoodless, P., Prezioso, V.R., Jessell, T.M. and Darnell, J.E. (1994) The winged-helix transcription factor HNF-3β is required for notochord development in the mouse embryo. Cell 78, 575-588.
78. Wilkinson, D.G. and Nieto, M.A. (1993) Detection of messenger RNA by in situ hybridization to tissue sections and whole mounts. In Wassarman, P.M. and DePamphilis, M.L. (eds.), Guide to Techniques in Mouse Development, Academic Press, San Diego, Vol. 225, pp. 361-373.
79. Wilt, F.H. (1965) Erythropoiesis in the chick embryo: the role of the endoderm. Science 147, 1588-1590.
80. Winnier, G., Blessing, M., Labosky, P.A. and Hogan, B.L. (1995) Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9, 2105-2116.
81. Xuan, S., Baptista, C.A., Balas, G., Tao, W., Soares, V.C. and Lai, E. (1995) Winged helix transcription factor BF-1 is essential for the development of the cerebral hemispheres. Neuron 14, 1141-1152.
82. Zakin, M.M., Bovard-Houppermans, S. and Ochoa, A. (1994) Liver-specific expression of plasma protein genes. In Tronche, F. and Yaniv, M. (eds.), Liver Gene Expression, Landes, Austin, TX, pp. 53-61.