JunB is essential for mammalian placentation

EMBO Journal

Volumn 18, Issue 4, 1999, Pages 934-948

  Schorpp Kistner, Marina ^a   Wang, Zhao Qi ^b,c   Angel, Peter ^a   Wagner, Erwin F ^b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^c INTERNATIONAL AGENCY FOR RESEARCH ON CANCER   (France)

Author keywords

AP 1 transcription factor; Embryonic lethality; Gene targeting; junB; Placental development

Indexed keywords

GELATINASE B; PROLIFERIN; TRANSCRIPTION FACTOR AP 1; UROKINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLASTOCYST; CONTROLLED STUDY; DECIDUA; EMBRYO; EMBRYO DEATH; EMBRYO DEVELOPMENT; FEMALE; GENE EXPRESSION; GROWTH RETARDATION; MALE; MESODERM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); NONHUMAN; ONCOGENE C JUN; PHENOTYPE; PLACENTA DEVELOPMENT; PRIORITY JOURNAL; REPRODUCTION; STEM CELL; TETRAPLOIDY; TROPHOBLAST; VASODILATATION; YOLK SAC;

ANIMALS; CELL DIVISION; EMBRYONIC AND FETAL DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE TARGETING; GENOTYPE; IN SITU HYBRIDIZATION; MICE; MICE, KNOCKOUT; MUTATION; PHENOTYPE; PLACENTA; PLOIDIES; PROTO-ONCOGENE PROTEINS C-JUN; STEM CELLS; TRANSCRIPTION FACTOR AP-1; YOLK SAC;

ANIMALIA; MAMMALIA;

EID: 0033557740     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.4.934     Document Type: Article

References (69)

1. Alexander, C.M., Hansell, E.J., Behrendtsen, O., Flannery, M.L., Kishnani, N.S., Haukes, S.P. and Werb, Z. (1996) Expression and function of matrix metalloproteinases and their inhibitors at the maternal boundary during mouse implantation. Development. 122, 1723-1736.
2. Angel, P. and Karin, M. (1991) The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochem. Biophys. Acta, 1072, 129-157.
3. Angel, P. and Herrlich, P. (1994) The Fos and Jun Families of Transcripion Factors. CRC Press, Boca Raton, FL.
4. Baldwin, H. et al. (1994) Platelet endothelial cell adhesion molecule-1 (PECAM/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development, 120, 2539-2553.
5. Baumhueter, S., Singer, M.S., Henzel, W., Hemmerich, S., Renz, M., Rosen, S.D. and Laskey, L.A. (1993) Binding of L-selectin in the vascular sialomucin CD34. Science, 262, 436-438.
6. Belin, D., Vasalli, J.D., Combepine, C., Godeau, F., Nagamine, Y., Reich, E., Kocher, H.P. and Duvoisin, R.M. (1985) Cloning, nucleotide sequence and expression of cDNAs encoding mouse urokinase-type plasminogen activator. Eur. J. Biochem., 148, 225-232.
7. Birkedal-Hansen, H., Moore, W.G.I., Bodden, M.K., Windsor, L.J., Birkedal-Hansen, B., DeCarlo, A. and Engler, J.A. (1993) Matrix metalloproteinases: a review. Crit. Rev. Oral Biol. Med., 4, 197-250.
8. Borden, P. and Heller, R.A. (1997) Transcriptional control of matrix metalloproteinases and the tissue inhibitors of matrix metalloproteinases. Crit. Rev. Eukaryot. Gene Expr., 7, 159-178.
9. Breier, G., Clauss, M. and Risau, W. (1995) Coordinate expression of vascular endothelial growth factor receptor (flt-1) and its ligand suggests a paracrine regulation of murine vascular development. Dev. Dyn., 204, 228-239.
10. Brown, J.R., Ye, H., Bronson, R.T., Dikkes, P. and Greenberg, M. (1996) A defect in nurturing in mice lacking the immediate early gene fosB. Cell, 86, 297-309.
11. Butterwith, S.C. (1994) Molecular events in adipocyte development. Pharmacol. Ther., 61, 399-411.
12. Carmeliet, P. et al. (1996) Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature, 380, 435-439.
13. Carney, E.W., Prideaux, V., Lye, S.J. and Rossant, J. (1993) Progressive expression of trophoblast-specific genes during formation of mouse trophoblast giant cells in vitro. Mol. Reprod. Dev., 34, 357-368.
14. Chiu, R., Angel, P. and Karin, M. (1989) Jun-B differs in its biological properties from and is a negative regulator of c-Jun. Cell, 59, 979-986.
15. Chung, K.Y., Agarwal, A. Uitto, J. and Mauviel, A. (1996) An AP-1 binding sequence is essential for regulation of the human α a(I) collagen (COL1A2) promoter activity by transforming growth factor-β. J. Biol. Chem., 271, 3272-3278.
16. Church, G.M. and Gilbert, W. (1984) Genomic sequencing. Proc. Natl Acad. Sci. USA, 81, 1991-1995.
17. Colosi, P.F. Talamantes, F. and Linzer, D.I. (1987) Molecular cloning and expression of mouse placental lactogen I complementary deoxyribonucleic acid. Mol. Endocrinol., 1, 767-776.
18. Conlan, R.A. and Herrmann, B.G. (1993) Detection of messenger RNA by in situ hybridization to postimplantation embryo whole mounts. Methods Enzymol., 225, 373-383.
19. Cross, J.C., Werb, Z. and Fisher, S.J. (1994) Implantation and the placenta: Key pieces of the development puzzle. Science, 266, 1508-1518.
20. Damsky, C.H., Fitzgerald, M.L. and Fisher, S.J. (1992) Distribution patterns of extracellular matrix components and adhesion receptors are intricately modulated during first trimester cytotrophoblast differentiation along the invasive pathway, in vivo. J. Clin. Invest., 89, 210-222.
21. De Cesare, D., Vallone, D., Carraciolo, A., Sassone-Corsi, P., Nerlov, C. and Verde, P. (1995) Heterodimerization of c-Jun with ATF-2 and c-Fos is required tor positive and negative regulation of the human urokinase promoter. Oncogene, 11, 365-376.
22. Deng, T. and Karin, M. (1993) JunB differs from c-Jun in its DNA-binding and dimerization domains and represses c-Jun by formation of inactive heterodimers. Genes Dev., 7, 479-490.
23. Dickson, M.C., Martin, J.S., Cousins, F.M. Kulkarni, A.B., Karlsson, S. and Akhurst, R.J. (1995) Defective haematopoiesis and vasculogenesis in transforming growth factor-β1 knock out mice. Development, 121, 1845-1854.
24. Dumont, D.J., Gradwohl, G., Fong, G.H., Puri, M.C., Gertsenstein, M., Auerbach, A. and Breitman, M.L. (1994) Dominant-negative and targeted null mutations in the endothelial receptor tyrosine kinase, tek, reveal a critical role in vasculogenesis of the embryo. Genes Dev., 8, 1897-1909.
25. Dungy, L.J., Siddiqi, T.A. and Khan, S. (1991) c-jun and junB oncogene expression during placental development. Am. J. Obstet. Gynecol., 165, 1853-1856.
26. Ferrara, N., Carver-Moore, K., Chen, H., Dowd, M., Lu, L., O'Shea, K.S., Powell-Braxton, L., Hillan, K.J. and Moore, M.W. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature, 380, 439-442.
27. Fong, G.-H., Rossant, J., Gertsenstein, M. and Breitman, M.L. (1995) Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature, 376, 66-70.
28. Groskopf, J.C. and Linzer, D.I. (1994) Characterization of a delayed early serum response region. Mol. Cell. Biol., 14, 6013-6020.
29. Guillemot, F., Nagy, A., Auerbach, A., Rossant, J. and Joyner, A.L. (1994) Essential role of Mash-2 in extraembryonic development. Nature, 371, 333-336.
30. Hilberg, F. and Wagner, E.F. (1992) Embryonic stem (ES) cells lacking functional c-jun: consequences for growth and differentiation. AP-1 activity and tumorigenesis. Oncogene, 7, 2371-2380.
31. Hilberg, F. Aguzzi, A., Howells, N. and Wagner, E.F. (1993) c-Jun is essential for normal mouse development and hepatogenesis. Nature, 365, 179-181.
32. Iwama, A., Hamaguchi, I., Hashiyama, M., Murayama, Y., Yasunaga, K. and Suda, T. (1993) Molecular cloning and characterization of the mouse TIE and TEK receptor tyrosine kinase genes and their expression in hematopoietic stem cells. Biochem. Biophys. Res. Commun., 195, 301-309.
33. Jackson, D., Volpert, O.V. Bouck, N. and Linzer, D.I. (1994) Stimulation and inhibition of angiogenesis by placental proliferin and proliferin-related protein. Science, 266, 1581-1584.
34. Johnson, R.S., Spiegelman, B.M. and Papaioannou, V.E. (1992) Pleiotropic effects of a null mutation in the c-fos proto-oncogene. Cell, 71, 577-586.
35. Johnson, R.S., van Lingen, B., Papaioanou, V.E. and Spiegelman, B.M. (1993) A null mutalion at the c-jun locus causes embryonic lethality and retarded cell growth in culture. Genes Dev., 7, 1309-1317.
36. 33P-labelled riboprobes for in situ hybridizations: localization of myosin alkali light-chain mRNAs in adult human skeletal muscle. Histochem. J., 26, 32-40.
37. Leco, K.J., Edwards, D.R. and Schultz, G.A. (1996) Tissue inhibitor of metalloproteinases-3 is the major metalloproteinase inhibitor in the decidualizing murine uterus. Mol. Reprod. Dev., 45, 458-165.
38. Lescisin, K.R., Varmuza, S. and Rossant, J. (1989) Isolation and characterization of a novel trophoblast-specific cDNA in the mouse. Genes Dev., 2, 1639-1649.
39. Ma, G.T. Roth, M.E., Groskopf, J.C., Tsai, F.-Y., Orkin, S.H., Grosveld, F., Engel, J.D. and Linzer, D.I. (1997) GATA-2 and GATA-3 regulate trophoblast-specitic gene expression in vivo. Development, 124, 907-914.
40. Macleod, K., Leprince, D. and Stehelin, D. (1992) The ets gene family. Trends Biochem. Sci., 17, 251-256.
41. Mauviel, A., Chung, K.Y., Agarwal, A., Tamai, K. and Uitto, J. (1996) Cell-specific induction of distinct oncogenes of the Jun family is responsible for differential regulation of collagenase gene expression by transforming growth factor-β in fibroblasts and keratinocytes. J. Biol. Chem., 271, 10917-10923.
42. Nakabeppu, Y., Ryder, K. and Nathans, D. (1988) DNA-binding activities of the three murine jun proteins: Stimulation by fos. Cell, 55, 907-915.
43. Nerlov, C., DeCesare, D., Pergola, F., Carracciolo, A., Balsi, F., Johnson, M. and Verde, P. (1992) A regulatory element that mediates co-operation between a PEA-3-AP-1 element and an AP-1 site is required for phorbol ester induction of urokinase enhancer activity in HepG2 hepatoma cells. EMBO J., 11, 4573-1582.
44. Reimold, A.M. et al. (1996) Chondrodysplasia and neurological abnormalities in ATF-2-deficient mice. Nature, 379, 262-265.
45. Reponen, R., Leivo, I., Sahlberg, C., Apte, S.S., Olsen, B.R., Thesleff, I. and Tryggvason, K. (1995) 92-kDa type IV collagenase and TIMP-3, but not 72-kDa type IV collagenase or TIPM-1 or TIMP-2, are highly expressed during mouse embryo implantation. Dev. Dyn., 202, 388-396.
46. Rinkenberger, J.L., Cross, J.C. and Werb, Z. (1997) Molecular genetics of implantation in the mouse. Dev. Genet., 21, 6-20.
47. Rohwedel, J., Horák, V., Hebrok, M., Füchtbauer, E.-M. and Wobus, A.M. (1995) M-twist expression inhibits mouse embryonic stem cell-derived myogenic differentiation in vitro. Exp. Cell Res., 220, 92-100.
48. Ryder, K., Lau, L.F. and Nathans, D. (1988) A gene activated by growth factors is related to the oncogene v-jun. Proc. Natl Acad. Sci. USA, 85, 1487-1491.
49. Ryseck, R.F. and Bravo, R. (1991) c-JUN, JUNB and JUND differ in their binding affinities to AP-1 and CRE consensus sequences: Effect of Fos proteins. Oncogene, 6, 533-542.
50. Sato, T.N. et al. (1995) Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature, 376, 70-74.
51. Schlüter, C., Duchrow, M., Wohlenberg, C., Becker, M.H., Key, G., Flad, H.D. and Gerdes, J. (1993) The cell proliferation-associated antigen of antibody Ki-67: a very large, ubiquitous nuclear protein with numerous repeated elements, representing a new kind of cell cycle-maintaining proteins. J. Cell Biol., 123, 513-522.
52. 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.
53. Schnürch, H. and Risau, W. (1993) Expression of tie-2, a member of a novel family of receptor tyrosine kinases, in the endothelial cell lineage. Development, 119, 957-968.
54. Schorpp, M., Jäger, R., Schellander, K., Schenkel, J., Wagner, E.F., Weiher, H. and Angel, P. (1996) The human ubiquitin C promoter directs high ubiquitous expression of transgenes in mice. Nucleic Acids Res., 24, 1787-1788.
55. Schreiber, M., Baumann, B., Cotten, M., Angel, P. and Wagner, E.F. (1995) Fos is an essential component of the mammalian UV response. EMBO J., 14, 5338-5349.
56. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.-F., Breitman, M.L. and Schuh, A. (1995) Failure of blood-island formation and vasculogenesis in Flk-1 deficient mice. Nature, 376, 62-66.
57. Shida, M.M., Ng, Y.K., Soares, M.J. and Linzer, D.I. (1993) Trophoblast-specific transcription from the mouse placental lactogen-I gene promoter. Mol. Endocrinol., 7, 181-188.
58. Shweiki, D., Itin, A., Neufeld, G., Gitay-Goren, H. and Keshet, E. (1993) Patterns of expression of vascular endothelial growth factor (VEGF) and VEGF receptors in mice suggest a role in hormonally regulated angiogenesis. J. Clin. Invest., 91, 2235-2243.
59. Suri, C., Jones, P.F., Patan, S., Bartunkova, S., Maisonpierre, P.C., Davies, S., Sato, T.N. and Yancopoulos, G.D. (1996) Requisite role of angiopoietin-I. a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell, 87, 1171-1180.
60. Suzuki, A. et al. (1997) Brca2 is required for embryonic cellular proliferation in the mouse. Genes Dev., 11, 1242-1252.
61. te Riele, H., Maandag, E.R., Clarke, A., Hooper, M. and Berns, A. (1990) Consecutive inactivation of both alleles of the pim-1 proto-oncogene by homologous recombination in embryonic stem cells. Nature, 348, 649-651.
62. Vogt, P.K. and Bos, T.J. (1990) Jun: oncogene and transcription factor. Adv. Cancer Res., 55, 1-35.
63. Wang, Z.-Q., Ovitt, C., Grigoriadis, A.E., Möhle-Steinlein, U., Rüther, U. and Wagner, E.F. (1992) Bone and haematopoetic defects in mice lacking c-fos. Nature, 360, 741-745.
64. Wang, Z.-Q., Kiefer, F., Urbanek, P. and Wagner, E.F. (1997) Generation of completely embryonic stem cell-derived mutant mice using tetraploid blastocyst injection. Mech. Dev., 62, 137-145.
65. Welter, J.F. and Eckert, R.L. (1995) Differential expression of the fos and jun family members c-fos, fosB, Fra-1, Fra-2, c-jun, junB and junD during human epidermal keratinocyte differentiation. Oncogene, 11, 2681-2687.
66. Wilkinson, D.G. and Green, J. (1990) In situ hybridization and the three-dimensional reconstruction of serial sections. In Copp, A.J. and Cockroft, D.L. (eds), Postimplantation Mammalian Embryos. A Practical Approach. IRL Press, Oxford University Press, Oxford, UK, pp. 155-171.
67. Xavier, F., Guillomot, M., Charlier, M., Martal, J. and Gaye, P. (1991) Coexpression of the proto-oncogene FOS (c-fos) and an embryonic interferon (ovine trophoblastin) by sheep conceptuses during implantation. Biol. Cell, 73, 27-33.
68. Yamamoto, H., Flannery, M.L., Kupriyanov, S., Pearce, J., McKercher, S.R., Henkel, G.W., Werb, Z. and Oshima, R.G. (1997) Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev., 12, 1315-1326.
69. Zhou, Y., Damsky, C.H. and Fisher, S.J. (1997) Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. J. Clin. Invest., 99, 2152-2164.