The Spemann organizer-expressed zinc finger gene Xegr-1 responds to the MAP kinase/Ets-SRF signal transduction pathway

EMBO Journal

Volumn 17, Issue 15, 1998, Pages 4414-4425

  Panitz, Frank ^a   Krain, Bernhard ^a   Hollemann, Thomas ^a   Nordheim, Alfred ^a   Pieler, Tomas ^a  

^a NONE

Author keywords

egr 1; FGF; MAP kinase signalling; Serum response element; Xenopus laevis

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; ZINC FINGER PROTEIN;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GENETIC ORGANIZATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; XENOPUS LAEVIS;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BINDING SITES; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; DNA, COMPLEMENTARY; DNA-BINDING PROTEINS; EARLY GROWTH RESPONSE PROTEIN 1; FETAL PROTEINS; FIBROBLAST GROWTH FACTORS; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IMMEDIATE-EARLY PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PEPTIDES; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ETS; SERUM RESPONSE FACTOR; SIGNAL TRANSDUCTION; T-BOX DOMAIN PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA; XENOPUS LAEVIS; XENOPUS PROTEINS; ZINC FINGERS;

ANIMALIA; XENOPUS LAEVIS;

EID: 0032479982     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.15.4414     Document Type: Article

References (88)

1. Amaya, E., Musci, T.J. and Kirschner, M.W. (1991) Expression of a dominant negative mutant of the FGF receptor disrupts mesoderm formation in Xenopus embryos. Cell, 66, 257-270.
2. Artinger, M., Blitz, I., Inoue, K., Tran, U. and Cho, K.W.Y. (1997) Interaction of goosecoid and brachyury in Xenopus mesoderm patterning. Mech. Dev., 65, 187-196.
3. Baker, J.C. and Harland, R.M. (1996) A novel mesoderm inducer, Madr2, functions in the activin signal transduction pathway. Genes Der., 10, 1880-1889.
4. Blumberg, B., Wright, C.V.E., De Robertis, E.M. and Cho, K.W.Y. (1991) Organizer-specific homeobox genes in Xenopus laevis embryos. Science, 253, 194-196.
5. Carman, J.A. and Monroe, J.G. (1995) The EGRI protein contains a discrete transcriptional regulatory domain whose deletion results in a truncated protein that blocks EGR1-induced transcription. DNA Cell Biol., 114, 581-589.
6. Changelian, P.S., Feng, P., King, T.C. and Milbrandt, J. (1989) Structure of the NGFI-A gene and detection of upstream sequences responsible for its transcriptional induction by nerve growth factor. Proc. Natl Acad. Sci. USA, 86, 377-381.
7. Charles, C.H., Abler, A.S. and Lau, L.F. (1992) cDNA sequence of a growth factor-inducible immediate early gene and characterization of its encoded protein. Oncogene, 7, 187-190.
8. Chen, X., Rubock, M.J. and Whitman, M. (1996) A transcriptional partner for MAD proteins in TGF-β signalling. Nature, 383, 691-696.
9. Chen, X., Weisberg, E., Fridmacher, V., Watanabe, M., Naco, G. and Whitman, M. (1997) Smad4 and Fast-1 in the assembly of activin-responsive factor. Nature, 389, 85-89.
10. Cho, K.W.Y., Blumberg, B., Steinbeisser, H. and De Robertis, E.M. (1991) Molecular nature of Spemann's organizer: the role of the Xenopus homeobox gene goosecoid. Cell, 67, 1111-1120.
11. Christy, B. and Nathans, D. (1989) Functional serum response elements upstream of the growth factor-inducible gene zif268. Mol. Cell. Biol., 9, 4889-4895.
12. Christy, B.A., Lau, L.F. and Nathans, D. (1988) A gene activated in mouse 3T3 cells by serum growth factors encodes a protein with 'zinc finger' sequences. Proc. Natl Acad. Sci. USA, 85, 7857-7861.
13. Cunliffe, V. and Smith, J.C. (1992) Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature, 358, 427-430.
14. Dalton, S. and Treisman, R. (1992) Characterization of SAP-1, a protein recruited by the serum response factor to the c-fos serum response element. Cell, 68, 597-612.
15. De Block, M. and Debrouwer, D. (1993) RNA-RNA in situ hybridization using digoxigenin-labeled probes: the use of high molecular weight polyvinyl alcohol in the alkaline phosphatase indoxyl-nitro-blue tetrazolium reaction. Anal. Biochem., 215, 86-89.
16. De Franco, C., Ro, M., Grossel, M., English, M.A., Hansen, U.M., Wagner, J.A. and Light, J.D. (1993) NGFIA (EGR1) contains transcription activating domains in both the amino terminal and carboxy terminal regions of the protein. Biochem. Biophys. Res. Commun., 194, 425-431.
17. Drummond, I.A., Rohwer-Nutter, P. and Sukhatme, V.P. (1994) The zebrafish egr1 gene encodes a highly conserved, zinc-finger transcriptional regulator. DNA Cell Biol., 13, 953-961.
18. Gashler, A. and Sukhatme, V.P. (1995) Early growth response protein 1 (Egr-1): prototype of a zinc finger family of transcription factors. Progr. Nucleic Acid Res. Mol. Biol., 50, 191-224.
19. Gashler, A.L., Swaminathan, S. and Sukhatme, V.P. (1993) A novel repression module, an extensive activation domain and a bipartite nuclear localization signal defined in the immediate-early transcription factor Egr-1. Mol. Cell. Biol., 13, 4556-4571.
20. Gawantka, V., Delius, H., Hirschfeld, K., Blumenstock, C. and Niehrs, C. (1995) Antagonizing the Spemann organizer: role of the homeobox gene Xvent-1. EMBO J., 14, 6268-6279.
21. Gotoh, Y., Masuyama, N., Suzuki, A., Ueno, N. and Nishida, E. (1995) Involvement of the MAP kinase cascade in Xenopus mesoderm induction. EMBO J., 14, 2491-2498.
22. Graff, J.M., Bansal, A. and Melton, D.A. (1996) Xenopus Mad proteins transduce distinct subsets of signals for the TGFβ superfamily. Cell, 85, 479-487.
23. Gurdon, J.B. (1992) The generation of diversity and pattern in animal development. Cell, 68, 185-199.
24. Harland, R. (1991) In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell. Biol., 36, 685-695.
25. Harland, R. and Gerhart, J. (1997) Formation and function of Spemann's organizer. Annu. Rev. Cell Dev. Biol., 13, 611-667.
26. Hartrey, R.S., Lewellyn, A.L. and Maller, J.L. (1994) MAP kinase is activated during mesoderm induction in Xenopus laevis. Dev. Biol., 163, 521-524.
27. Hemmati-Brivanlou, A. and Melton, D.A. (1992) A truncated activin receptor inhibits mesoderm induction and formation of axial structures in Xenopus embryos. Nature, 359, 609-614.
28. Herschman, H.R. (1991) Primary response genes induced by growth factors and tumor promoters. Annu. Rev. Biochem., 60, 281-319.
29. Huang, H.C., Murtaugh, L.C., Vize, P.D. and Whitman, M. (1995) Identification of a potential regulator of early transcriptional responses to mesoderm inducers in the frog embryo. EMBO J., 14, 5965-5973.
30. Isaacs, H.V., Tannahill, D. and Slack, J.M.W. (1992) Expression of a novel FGF in the Xenopus embryo. A new candidate inducing factor for mesoderm formation and anteroposterior specification. Development, 114, 711-720.
31. Isaacs, H.V., Pownall, M.E. and Slack, J.M. (1994) eFGF regulates Xbra expression during Xenopus gastrulation. EMBO J., 13, 4469-4481.
32. Janknecht, R. and Nordheim, A. (1991) Affinity purification of histidine-tagged proteins transiently produced in HeLa cells. Gene, 121, 321-324.
33. Janknecht, R. and Nordheim, A. (1992) Elk-1 protein domains are required for direct and SRF-assisted DNA-binding. Nucleic Acids Res., 20, 3317-3324.
34. Janknecht, R., De Martynoff, G., Lou, J., Hipskind, R.A., Nordheim, A. and Stunnenberg, H.G. (1991) Rapid and efficient purification of native histidine-tagged protein expressed by recombinant vaccinia virus. Proc. Natl Acad Sci. USA, 88, 8972-8976.
35. Janknecht, R., Ernst, W.H., Pingoud, V. and Nordheim, A. (1993) Activation of ternary complex factor Elk-1 by MAP kinases. EMBO J., 12, 5097-5104.
36. Janssen-Timmen, U., Lemaire, P., Mattéi, M.-G., Revelant, O. and Charnay, P. (1989) Structure, chromosome mapping and regulation of the mouse zinc finger gene Krox-24; evidence for a common regulatory pathway for immediate-early serum-response genes. Gene, 80, 325-336.
37. Kaufmann, E., Paul, H., Friedle, H., Metz, A., Scheucher, M., Clement, J.H. and Knöchel, W. (1996) Antagonistic actions of activin A and BMP-2/4 control dorsal lip-specific activation of the early response gene XFD-1' in Xenopus laevis embryos. EMBO J., 15, 6739-6749.
38. Köster, M., Plessow, S., Clement, J.H., Lorenz, A., Tiedemann, H. and Knöchel, W. (1991) Bone morphogenetic protein 4 (BMP-4), a member of the TGF-β family, in early embryos of Xenopus laevis: analysis of mesoderm inducing activity. Mech. Dev., 33, 191-200.
39. Krieg, D.A. and Melton, D.A. (1984) Functional messenger RNAs are produced by SP6 in vitro transcription of cloned cDNAs. Nucleic Acids Res., 12, 7057-7071.
40. La Bonne, C. and Whitman, M. (1997) Localization of MAP kinase activity in early Xenopus embryos: implications for endogenous FGF signaling. Dev. Biol., 183, 9-20.
41. La Bonne, C., Burke, B. and Whitman, M. (1995) Role of MAP kinase in mesoderm induction and axial patterning during Xenopus development. Development, 121, 1475-1486.
42. Latinkic, B.V., Umbhauer, M., Neal, K.A., Lerchner, W., Smith, J.C. and Cunliffe, V. (1997) The Xenopus Brachyury promoter is activated by FGF and low concentrations of activin and suppressed by high concentrations of activin and by paired-type homeodomain proteins. Genes Dev., 11, 3265-3276.
43. Lee, S.L., Sadovsky, Y., Swirnoff, A.H., Polish, J.A., Goda, P., Gavrilina, G. and Milbrandt, J. (1996) Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science, 273, 1219-1221.
44. Lemaire, P. and Gurdon, J.B. (1994) A role for cytoplasmic determinants in mesoderm patterning: cell-autonomous activation of the goosecoid and Xwnt-8 genes along the dorsoventral axis of early Xenopus embryos. Development, 120, 1191-1199.
45. Lemaire, P., Vesque, C., Schmitt, J., Stunnenberg, H., Frank, R. and Charnay, P. (1990) The serum-inducible mouse gene Krox-24 encodes a sequence-specific transcriptional activator. Mol. Cell. Biol., 10, 3456-3467.
46. MacNicol, A.M., Muslin, A.J. and Williams, L.T. (1993) Raf-1 kinase is essential for early Xenopus development and mediates the induction of mesoderm by FGF. Cell, 73, 571-583.
47. Marais, R., Wynne, J. and Treisman, R. (1993) The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell, 73, 381-393.
48. Matheny, C., Day, M.L. and Milbrandt, J. (1994) The nuclear localization signal of NGFI-A is located within the zinc finger DNA binding domain. J. Biol. Chem., 269, 8176-8181.
49. McMahon, S.B. and Monroe, J.G. (1995) A ternary complex factor-dependent mechanism mediates induction of egr-1 through selective serum response elements following antigen receptor cross-linking in B lymphocytes. Mol. Cell. Biol., 15, 1086-1093.
50. Melton, D.A., Krieg, P.A., Rebagliati, M.R., Maniatis, T., Zinn, K. and Green, M.R. (1984) Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res., 12, 7035-7056.
51. Milbrandt, J. (1987) A nerve growth factor-induced gene encodes a possible transcriptional regulatory factor. Science, 238, 797-799.
52. Mohun, T.J., Taylor, M.V., Garrett, N. and Gurdon, J.B. (1989) The CArG promoter sequence is necessary for muscle-specific transcription of the cardiac actin gene in Xenopus embryos. EMBO J., 8, 1153-1161.
53. Mohun, T.J., Chambers, A.E., Towers, N. and Taylor, M.V. (1991) Expression of genes encoding the transcription factor SRF during early development of Xenopus laevis: identification of CArG box-binding activity as SRF. EMBO J., 10, 933-940.
54. Niehrs, C., Steinbeisser, H. and De Robertis, E.M. (1994) Mesodermal patterning by a gradient of the vertebrate homeobox gene goosecoid. Science, 263, 817-820.
55. Nieuwkoop, P.D. (1969) The formation of mesoderm in urodelean amhibians I. Induction by the endoderm. Roux's Arch. Dev. Biol., 162, 341-373.
56. Nieuwkoop, P.D. (1977) Origin and establishment of embryonic polar axes in amphibian development. Curr. Top. Dev. Biol., 11, 115-132.
57. Nieuwkoop, P.D. and Faber, J. (1967) A Normal Table of Xenopus laevis (Daudin). North Holland Publishing Co., Amsterdam, The Netherlands.
58. Northrop, J., Woods, A., Seger, R., Suzuki, A., Ueno, N., Krebs, E. and Kimelman, D. (1995) BMP-4 regulates the dorsal-ventral differences in FGF/MAPKK-mediated mesoderm induction in Xenopus. Dev. Biol., 172, 242-252.
59. Ptashne, M. (1988) How eukaryotic transcriptional activators work. Nature, 335, 683-689.
60. Rao, V.N., Huebner, K., Isobe, M., Ar-Rushdi, A., Croce, C.M. and Reddy, E.S.P. (1989) elk, tissue-specific ets-related genes on chromosomes X and 14 near translocation breakpoints. Science, 244, 66-70.
61. Robinson, L., Panayiotakis, A., Papas, T.S., Kola, I. and Seth, A. (1997) ETS target genes: identification of Egr1 as a target by RNA differential display and whole genome PCR techniques. Proc. Natl Acad. Sci. USA, 94, 7170-7175.
62. Rodolpho, M.,A., Groome, N. and Smith, J.C. (1993) Activins are expressed in preimplantation mouse embryos and in ES and EC cells and are regulated on their differentiation. Development, 117, 711-723.
63. Rupp, R.A.W. and Weintraub, H. (1991) Ubiquitous myoD transcription at the midblastula transition precedes induction-dependent myoD expression in presumptive mesoderm of X.laevis. Cell, 65, 927-937.
64. Rupp, R.A.W., Snider, L. and Weintraub, H. (1994) Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev., 8, 1311-1323.
65. Russo, M.W., Sevetson, B.R. and Milbrandt, J. (1995) Identification of NAB1, a repressor of NGFI-A-and Krox20-mediated transcription. Proc. Natl Acad. Sci. USA, 92, 6873-6877.
66. Ryan, K., Garrett, N., Mitchell, A. and Gurdon, J.B. (1996) Fomesodermin, a key early gene in Xenopus mesoderm differentiation. Cell, 87, 989-1000.
67. Sakamoto, K.M., Bardeleben, C., Yates, K.E., Raines, M.A., Golde, D.W. and Gasson, J.C. (1991) 5′ Upstream sequence and genomic structure of the human primary response gene. EGR-1/TIS8. Oncogene, 6, 867-871.
68. Sasai, Y., Lu, B., Steinbeisser, H., Geissert, D., Gont, L.K. and De Robertis, E.M. (1994) Xenopus chordin: a novel dorsalizing factor activated by organizer-specific homeobox genes. Cell, 79, 779-790.
69. Schulte-Merker, S. and Smith, J.C. (1995) Mesoderm formation in response to brachyury requires FGF signalling. Curr. Biol., 5, 62-67.
70. Shore, P. and Sharrocks, A.D. (1994) The transcription factors Elk-1 and serum response factor interact by direct protein-protein contacts mediated by a short region of Elk-1. Mol. Cell. Biol., 14, 3283-3291.
71. Smith, J.C., Price, B.M.J., Green, J.B.A., Weigel, D. and Herrmann, B.G. (1991) Expression of a Xenopus homolog of Brachyury (T) is an immediate-early response to mesoderm induction. Cell, 67, 79-87.
72. Smith, W.C. and Harland, R.M. (1992) Expression cloning of noggin, a new dorsalizing factor localized to the Spemann organizer in Xenopus embryos. Cell, 70, 829-840.
73. Smith, W.C., McKendry, R.M. and Harland, R.M. (1995) A nodal-related gene defines a physical and functional domain within the Spemann organizer. Cell, 82, 37-46.
74. Spemann, H. and Mangold, H. (1924) Über Induktion von Embryonalanlagen durch Implantation artfremder Organisatoren. Arch. Mikr. Anat. Entw. Mech., 100, 599-638.
75. Susgs, S.V., Katzowitz, J.L., Tsai-Morris, C. and Sukhatme, V.P. (1990) cDNA sequence of the human cellular early growth response gene Egr-1. Nucleic Acids Res., 18, 4283.
76. Svaren, J., Sevetson, B.R., Apel, E.D., Zimonjic, D.B., Popescu, N.C. and Milbrandt, J. (1996) NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol. Cell. Biol., 16, 3545-3553.
77. Tada, M., O'Reilly, M.-A.J. and Smith, J. (1997) Analysis of competence and of Brachyury autoinduction by use of hormone-inducible Xbra. Development, 124, 2225-2234.
78. Tang, T.L., Freeman, R.M., O'Reilly, A.M., Neel, B.G. and Sokol, S.Y. (1995) The SH2-containing protein-tyrosine phosphatase SH-PTP2 is required upstream of MAP kinase for early Xenopus development. Cell, 80, 473-483.
79. Thomsen, G.H. (1996) Xenopus mothers against decapentaplegic is an embryonic ventralizing agent that acts downstream of the BMP-2/4 receptor. Development, 122, 2359-2366.
80. Topilko, P. Schneider-Maunoury, S., Levi, G., Trembleau, A., Gourdji, D., Driancourt, M.A., Rao, C.V. and Charnay, P. (1998) Multiple pituitary and ovarian defects in Krox-24 (NGFI-A, Egr-1)-targeted mice. Mol. Endocrinol., 12, 107-122.
81. Treisman, R. (1996) Identification of a protein binding-site that mediates transcriptional response of the c-fos gene to serum response factors. Cell, 46, 567-574.
82. Umbhauer, M., Marshall, C.J., Mason, C.S., Old, R.W. and Smith, J.C. (1995) Mesoderm induction in Xenopus caused by activation of MAP kinase. Nature, 376, 58-62.
83. Van Straaten, F., Muller, R., Curran, T., Van Beveren, C. and Verma, I.M. (1983) Complete nucleotide sequence of a human c-onc gene: deduced amino acid sequence of the human c-fos protein. Proc. Natl Acad. Sci. USA, 80, 3183-3187.
84. Vize, P.D. (1996) DNA sequences mediating the transcriptional response of the Mix.2 homeobox gene to mesoderm induction. Dev. Biol., 177, 226-231.
85. Vodicka, M.A. and Gerhart, J.C. (1995) Blastomere derivation and domains of gene expression in the Spemann organizer of Xenopus laevis. Development, 121, 3505-3518.
86. Wasylyk, B. and Nordheim, A. (1997) Ets transcription factors: partners in the integration of signal responses. In Papavassiliou, A.G. (ed.), Transcription Factors in Eucaryotes. R.G. Landes Co., Georgetown, TX, pp 251-284.
87. Watabe, T., Kim, S., Candia, A., Rothbacher, U., Hashimoto, C., Inoue, K. and Cho, K.W. (1995) Molecular mechanisms of Spemann's organizer formation: conserved growth factor synergy between Xenopus and mouse. Genes Dev., 15, 3038-3050.
88. Whitman, M. and Melton, D.A. (1992) Involvement of p21ras in Xenopus mesoderm induction. Nature, 357, 252-254.