Abstract
The transcription factor serum response factor (SRF), a phylogenetically conserved nuclear protein, mediates the rapid transcriptional response to extracellular stimuli, e.g. growth and differentiation signals. DNA- protein complexes containing SRF or its homologues function as nuclear targets of the Ras/MAPK signalling network, thereby directing gene activities associated with processes as diverse as pheromone signalling, cell-cycle progression (transitions G0-G1 and G2-M), neuronal synaptic transmission and muscle cell differentiation. So far, the activity of mammalian SRF has been studied exclusively in cultured cells. To study SRF function in a multicellular organism we generated an Srf null allele in mice. SRF-deficient embryos (Srf -/-) have a severe gastrulation defect and do not develop to term. They consist of misfolded ectodermal and endodermal cell layers, do not form a primitive streak or any detectable mesodermal cells and fail to express the developmental marker genes Bra (T), Bmp-2/4 and Shh. Activation of the SRF-regulated immediate early genes Egr-1 and c-fos, as well as the alpha-Actin gene, is severely impaired. Our study identifies SRF as a new and essential regulator of mammalian mesoderm formation. We therefore suggest that in mammals Ras/MAPK signalling contributes to mesoderm induction, as is the case in amphibia.
Full Text
The Full Text of this article is available as a PDF (812.1 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Affolter M., Montagne J., Walldorf U., Groppe J., Kloter U., LaRosa M., Gehring W. J. The Drosophila SRF homolog is expressed in a subset of tracheal cells and maps within a genomic region required for tracheal development. Development. 1994 Apr;120(4):743–753. doi: 10.1242/dev.120.4.743. [DOI] [PubMed] [Google Scholar]
- Althoefer H., Schleiffer A., Wassmann K., Nordheim A., Ammerer G. Mcm1 is required to coordinate G2-specific transcription in Saccharomyces cerevisiae. Mol Cell Biol. 1995 Nov;15(11):5917–5928. doi: 10.1128/mcb.15.11.5917. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beddington R. S., Smith J. C. Control of vertebrate gastrulation: inducing signals and responding genes. Curr Opin Genet Dev. 1993 Aug;3(4):655–661. doi: 10.1016/0959-437x(93)90103-v. [DOI] [PubMed] [Google Scholar]
- Behrens J., von Kries J. P., Kühl M., Bruhn L., Wedlich D., Grosschedl R., Birchmeier W. Functional interaction of beta-catenin with the transcription factor LEF-1. Nature. 1996 Aug 15;382(6592):638–642. doi: 10.1038/382638a0. [DOI] [PubMed] [Google Scholar]
- Belaguli N. S., Schildmeyer L. A., Schwartz R. J. Organization and myogenic restricted expression of the murine serum response factor gene. A role for autoregulation. J Biol Chem. 1997 Jul 18;272(29):18222–18231. doi: 10.1074/jbc.272.29.18222. [DOI] [PubMed] [Google Scholar]
- Buckingham M. Molecular biology of muscle development. Cell. 1994 Jul 15;78(1):15–21. doi: 10.1016/0092-8674(94)90568-1. [DOI] [PubMed] [Google Scholar]
- Cahill M. A., Janknecht R., Nordheim A. Signalling pathways: jack of all cascades. Curr Biol. 1996 Jan 1;6(1):16–19. doi: 10.1016/s0960-9822(02)00410-4. [DOI] [PubMed] [Google Scholar]
- Chen C. Y., Schwartz R. J. Recruitment of the tinman homolog Nkx-2.5 by serum response factor activates cardiac alpha-actin gene transcription. Mol Cell Biol. 1996 Nov;16(11):6372–6384. doi: 10.1128/mcb.16.11.6372. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chiang C., Litingtung Y., Lee E., Young K. E., Corden J. L., Westphal H., Beachy P. A. Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature. 1996 Oct 3;383(6599):407–413. doi: 10.1038/383407a0. [DOI] [PubMed] [Google Scholar]
- Croissant J. D., Kim J. H., Eichele G., Goering L., Lough J., Prywes R., Schwartz R. J. Avian serum response factor expression restricted primarily to muscle cell lineages is required for alpha-actin gene transcription. Dev Biol. 1996 Jul 10;177(1):250–264. doi: 10.1006/dbio.1996.0160. [DOI] [PubMed] [Google Scholar]
- Dalton S., Treisman R. Characterization of SAP-1, a protein recruited by serum response factor to the c-fos serum response element. Cell. 1992 Feb 7;68(3):597–612. doi: 10.1016/0092-8674(92)90194-h. [DOI] [PubMed] [Google Scholar]
- Field S. J., Johnson R. S., Mortensen R. M., Papaioannou V. E., Spiegelman B. M., Greenberg M. E. Growth and differentiation of embryonic stem cells that lack an intact c-fos gene. Proc Natl Acad Sci U S A. 1992 Oct 1;89(19):9306–9310. doi: 10.1073/pnas.89.19.9306. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Firulli A. B., Olson E. N. Modular regulation of muscle gene transcription: a mechanism for muscle cell diversity. Trends Genet. 1997 Sep;13(9):364–369. doi: 10.1016/s0168-9525(97)01171-2. [DOI] [PubMed] [Google Scholar]
- Franzoso G., Carlson L., Brown K., Daucher M. B., Bressler P., Siebenlist U. Activation of the serum response factor by p65/NF-kappaB. EMBO J. 1996 Jul 1;15(13):3403–3412. [PMC free article] [PubMed] [Google Scholar]
- Fujii M., Tsuchiya H., Chuhjo T., Akizawa T., Seiki M. Interaction of HTLV-1 Tax1 with p67SRF causes the aberrant induction of cellular immediate early genes through CArG boxes. Genes Dev. 1992 Nov;6(11):2066–2076. doi: 10.1101/gad.6.11.2066. [DOI] [PubMed] [Google Scholar]
- Gauthier-Rouvière C., Basset M., Blanchard J. M., Cavadore J. C., Fernandez A., Lamb N. J. Casein kinase II induces c-fos expression via the serum response element pathway and p67SRF phosphorylation in living fibroblasts. EMBO J. 1991 Oct;10(10):2921–2930. doi: 10.1002/j.1460-2075.1991.tb07842.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gauthier-Rouvière C., Cavadore J. C., Blanchard J. M., Lamb N. J., Fernandez A. p67SRF is a constitutive nuclear protein implicated in the modulation of genes required throughout the G1 period. Cell Regul. 1991 Jul;2(7):575–588. doi: 10.1091/mbc.2.7.575. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ghosh A., Greenberg M. E. Calcium signaling in neurons: molecular mechanisms and cellular consequences. Science. 1995 Apr 14;268(5208):239–247. doi: 10.1126/science.7716515. [DOI] [PubMed] [Google Scholar]
- Gille H., Sharrocks A. D., Shaw P. E. Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature. 1992 Jul 30;358(6385):414–417. doi: 10.1038/358414a0. [DOI] [PubMed] [Google Scholar]
- Gille H., Strahl T., Shaw P. E. Activation of ternary complex factor Elk-1 by stress-activated protein kinases. Curr Biol. 1995 Oct 1;5(10):1191–1200. doi: 10.1016/s0960-9822(95)00235-1. [DOI] [PubMed] [Google Scholar]
- Giovane A., Pintzas A., Maira S. M., Sobieszczuk P., Wasylyk B. Net, a new ets transcription factor that is activated by Ras. Genes Dev. 1994 Jul 1;8(13):1502–1513. doi: 10.1101/gad.8.13.1502. [DOI] [PubMed] [Google Scholar]
- Groisman R., Masutani H., Leibovitch M. P., Robin P., Soudant I., Trouche D., Harel-Bellan A. Physical interaction between the mitogen-responsive serum response factor and myogenic basic-helix-loop-helix proteins. J Biol Chem. 1996 Mar 1;271(9):5258–5264. doi: 10.1074/jbc.271.9.5258. [DOI] [PubMed] [Google Scholar]
- Grueneberg D. A., Henry R. W., Brauer A., Novina C. D., Cheriyath V., Roy A. L., Gilman M. A multifunctional DNA-binding protein that promotes the formation of serum response factor/homeodomain complexes: identity to TFII-I. Genes Dev. 1997 Oct 1;11(19):2482–2493. doi: 10.1101/gad.11.19.2482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grueneberg D. A., Natesan S., Alexandre C., Gilman M. Z. Human and Drosophila homeodomain proteins that enhance the DNA-binding activity of serum response factor. Science. 1992 Aug 21;257(5073):1089–1095. doi: 10.1126/science.257.5073.1089. [DOI] [PubMed] [Google Scholar]
- Guillemin K., Groppe J., Ducker K., Treisman R., Hafen E., Affolter M., Krasnow M. A. The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development. 1996 May;122(5):1353–1362. doi: 10.1242/dev.122.5.1353. [DOI] [PubMed] [Google Scholar]
- Herdegen T., Blume A., Buschmann T., Georgakopoulos E., Winter C., Schmid W., Hsieh T. F., Zimmermann M., Gass P. Expression of activating transcription factor-2, serum response factor and cAMP/Ca response element binding protein in the adult rat brain following generalized seizures, nerve fibre lesion and ultraviolet irradiation. Neuroscience. 1997 Nov;81(1):199–212. doi: 10.1016/s0306-4522(97)00170-x. [DOI] [PubMed] [Google Scholar]
- Herrera R. E., Shaw P. E., Nordheim A. Occupation of the c-fos serum response element in vivo by a multi-protein complex is unaltered by growth factor induction. Nature. 1989 Jul 6;340(6228):68–70. doi: 10.1038/340068a0. [DOI] [PubMed] [Google Scholar]
- Herschman H. R. Primary response genes induced by growth factors and tumor promoters. Annu Rev Biochem. 1991;60:281–319. doi: 10.1146/annurev.bi.60.070191.001433. [DOI] [PubMed] [Google Scholar]
- Hill C. S., Treisman R. Differential activation of c-fos promoter elements by serum, lysophosphatidic acid, G proteins and polypeptide growth factors. EMBO J. 1995 Oct 16;14(20):5037–5047. doi: 10.1002/j.1460-2075.1995.tb00186.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hill C. S., Wynne J., Treisman R. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell. 1995 Jun 30;81(7):1159–1170. doi: 10.1016/s0092-8674(05)80020-0. [DOI] [PubMed] [Google Scholar]
- Hipskind R. A., Büscher D., Nordheim A., Baccarini M. Ras/MAP kinase-dependent and -independent signaling pathways target distinct ternary complex factors. Genes Dev. 1994 Aug 1;8(15):1803–1816. doi: 10.1101/gad.8.15.1803. [DOI] [PubMed] [Google Scholar]
- Hipskind R. A., Rao V. N., Mueller C. G., Reddy E. S., Nordheim A. Ets-related protein Elk-1 is homologous to the c-fos regulatory factor p62TCF. Nature. 1991 Dec 19;354(6354):531–534. doi: 10.1038/354531a0. [DOI] [PubMed] [Google Scholar]
- Huber O., Korn R., McLaughlin J., Ohsugi M., Herrmann B. G., Kemler R. Nuclear localization of beta-catenin by interaction with transcription factor LEF-1. Mech Dev. 1996 Sep;59(1):3–10. doi: 10.1016/0925-4773(96)00597-7. [DOI] [PubMed] [Google Scholar]
- Imamoto A., Soriano P. Disruption of the csk gene, encoding a negative regulator of Src family tyrosine kinases, leads to neural tube defects and embryonic lethality in mice. Cell. 1993 Jun 18;73(6):1117–1124. doi: 10.1016/0092-8674(93)90641-3. [DOI] [PubMed] [Google Scholar]
- Janknecht R., Ernst W. H., Pingoud V., Nordheim A. Activation of ternary complex factor Elk-1 by MAP kinases. EMBO J. 1993 Dec 15;12(13):5097–5104. doi: 10.1002/j.1460-2075.1993.tb06204.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Janknecht R., Hipskind R. A., Houthaeve T., Nordheim A., Stunnenberg H. G. Identification of multiple SRF N-terminal phosphorylation sites affecting DNA binding properties. EMBO J. 1992 Mar;11(3):1045–1054. doi: 10.1002/j.1460-2075.1992.tb05143.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johansen F. E., Prywes R. Identification of transcriptional activation and inhibitory domains in serum response factor (SRF) by using GAL4-SRF constructs. Mol Cell Biol. 1993 Aug;13(8):4640–4647. doi: 10.1128/mcb.13.8.4640. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Johansen F. E., Prywes R. Serum response factor: transcriptional regulation of genes induced by growth factors and differentiation. Biochim Biophys Acta. 1995 Jul 28;1242(1):1–10. doi: 10.1016/0304-419x(94)00014-s. [DOI] [PubMed] [Google Scholar]
- Kispert A., Koschorz B., Herrmann B. G. The T protein encoded by Brachyury is a tissue-specific transcription factor. EMBO J. 1995 Oct 2;14(19):4763–4772. doi: 10.1002/j.1460-2075.1995.tb00158.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- LaBonne C., Whitman M. Mesoderm induction by activin requires FGF-mediated intracellular signals. Development. 1994 Feb;120(2):463–472. doi: 10.1242/dev.120.2.463. [DOI] [PubMed] [Google Scholar]
- Lee S. L., Sadovsky Y., Swirnoff A. H., Polish J. A., Goda P., Gavrilina G., Milbrandt J. Luteinizing hormone deficiency and female infertility in mice lacking the transcription factor NGFI-A (Egr-1). Science. 1996 Aug 30;273(5279):1219–1221. doi: 10.1126/science.273.5279.1219. [DOI] [PubMed] [Google Scholar]
- Lemaire P., Kodjabachian L. The vertebrate organizer: structure and molecules. Trends Genet. 1996 Dec;12(12):525–531. doi: 10.1016/s0168-9525(97)81401-1. [DOI] [PubMed] [Google Scholar]
- Liu S. H., Lee H. H., Chen J. J., Chuang C. F., Ng S. Y. Serum response element-regulated transcription in the cell cycle: possible correlation with microtubule reorganization. Cell Growth Differ. 1994 Apr;5(4):447–455. [PubMed] [Google Scholar]
- Lopez M., Oettgen P., Akbarali Y., Dendorfer U., Libermann T. A. ERP, a new member of the ets transcription factor/oncoprotein family: cloning, characterization, and differential expression during B-lymphocyte development. Mol Cell Biol. 1994 May;14(5):3292–3309. doi: 10.1128/mcb.14.5.3292. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Magnaghi-Jaulin L., Masutani H., Robin P., Lipinski M., Harel-Bellan A. SRE elements are binding sites for the fusion protein EWS-FLI-1. Nucleic Acids Res. 1996 Mar 15;24(6):1052–1058. doi: 10.1093/nar/24.6.1052. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Maher M., Cong F., Kindelberger D., Nasmyth K., Dalton S. Cell cycle-regulated transcription of the CLB2 gene is dependent on Mcm1 and a ternary complex factor. Mol Cell Biol. 1995 Jun;15(6):3129–3137. doi: 10.1128/mcb.15.6.3129. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mansour S. L., Thomas K. R., Capecchi M. R. Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature. 1988 Nov 24;336(6197):348–352. doi: 10.1038/336348a0. [DOI] [PubMed] [Google Scholar]
- Marais R. M., Hsuan J. J., McGuigan C., Wynne J., Treisman R. Casein kinase II phosphorylation increases the rate of serum response factor-binding site exchange. EMBO J. 1992 Jan;11(1):97–105. doi: 10.1002/j.1460-2075.1992.tb05032.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marais R., Wynne J., Treisman R. The SRF accessory protein Elk-1 contains a growth factor-regulated transcriptional activation domain. Cell. 1993 Apr 23;73(2):381–393. doi: 10.1016/0092-8674(93)90237-k. [DOI] [PubMed] [Google Scholar]
- Miranti C. K., Ginty D. D., Huang G., Chatila T., Greenberg M. E. Calcium activates serum response factor-dependent transcription by a Ras- and Elk-1-independent mechanism that involves a Ca2+/calmodulin-dependent kinase. Mol Cell Biol. 1995 Jul;15(7):3672–3684. doi: 10.1128/mcb.15.7.3672. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mishina Y., Suzuki A., Ueno N., Behringer R. R. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev. 1995 Dec 15;9(24):3027–3037. doi: 10.1101/gad.9.24.3027. [DOI] [PubMed] [Google Scholar]
- Mohun T. J., Taylor M. V., Garrett N., Gurdon J. B. The CArG promoter sequence is necessary for muscle-specific transcription of the cardiac actin gene in Xenopus embryos. EMBO J. 1989 Apr;8(4):1153–1161. doi: 10.1002/j.1460-2075.1989.tb03486.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Montagne J., Groppe J., Guillemin K., Krasnow M. A., Gehring W. J., Affolter M. The Drosophila Serum Response Factor gene is required for the formation of intervein tissue of the wing and is allelic to blistered. Development. 1996 Sep;122(9):2589–2597. doi: 10.1242/dev.122.9.2589. [DOI] [PubMed] [Google Scholar]
- Moss J. B., McQuinn T. C., Schwartz R. J. The avian cardiac alpha-actin promoter is regulated through a pair of complex elements composed of E boxes and serum response elements that bind both positive- and negative-acting factors. J Biol Chem. 1994 Apr 29;269(17):12731–12740. [PubMed] [Google Scholar]
- Muscat G. E., Gustafson T. A., Kedes L. A common factor regulates skeletal and cardiac alpha-actin gene transcription in muscle. Mol Cell Biol. 1988 Oct;8(10):4120–4133. doi: 10.1128/mcb.8.10.4120. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Norman C., Runswick M., Pollock R., Treisman R. Isolation and properties of cDNA clones encoding SRF, a transcription factor that binds to the c-fos serum response element. Cell. 1988 Dec 23;55(6):989–1003. doi: 10.1016/0092-8674(88)90244-9. [DOI] [PubMed] [Google Scholar]
- Panitz F., Krain B., Hollemann T., Nordheim A., Pieler T. The Spemann organizer-expressed zinc finger gene Xegr-1 responds to the MAP kinase/Ets-SRF signal transduction pathway. EMBO J. 1998 Aug 3;17(15):4414–4425. doi: 10.1093/emboj/17.15.4414. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pellegrini L., Tan S., Richmond T. J. Structure of serum response factor core bound to DNA. Nature. 1995 Aug 10;376(6540):490–498. doi: 10.1038/376490a0. [DOI] [PubMed] [Google Scholar]
- Price M. A., Cruzalegui F. H., Treisman R. The p38 and ERK MAP kinase pathways cooperate to activate Ternary Complex Factors and c-fos transcription in response to UV light. EMBO J. 1996 Dec 2;15(23):6552–6563. [PMC free article] [PubMed] [Google Scholar]
- Price M. A., Rogers A. E., Treisman R. Comparative analysis of the ternary complex factors Elk-1, SAP-1a and SAP-2 (ERP/NET). EMBO J. 1995 Jun 1;14(11):2589–2601. doi: 10.1002/j.1460-2075.1995.tb07257.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Prywes R., Roeder R. G. Purification of the c-fos enhancer-binding protein. Mol Cell Biol. 1987 Oct;7(10):3482–3489. doi: 10.1128/mcb.7.10.3482. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raingeaud J., Whitmarsh A. J., Barrett T., Dérijard B., Davis R. J. MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol Cell Biol. 1996 Mar;16(3):1247–1255. doi: 10.1128/mcb.16.3.1247. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rivera V. M., Miranti C. K., Misra R. P., Ginty D. D., Chen R. H., Blenis J., Greenberg M. E. A growth factor-induced kinase phosphorylates the serum response factor at a site that regulates its DNA-binding activity. Mol Cell Biol. 1993 Oct;13(10):6260–6273. doi: 10.1128/mcb.13.10.6260. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Roch F., Baonza A., Martín-Blanco E., García-Bellido A. Genetic interactions and cell behaviour in blistered mutants during proliferation and differentiation of the Drosophila wing. Development. 1998 May;125(10):1823–1832. doi: 10.1242/dev.125.10.1823. [DOI] [PubMed] [Google Scholar]
- Sartorelli V., Webster K. A., Kedes L. Muscle-specific expression of the cardiac alpha-actin gene requires MyoD1, CArG-box binding factor, and Sp1. Genes Dev. 1990 Oct;4(10):1811–1822. doi: 10.1101/gad.4.10.1811. [DOI] [PubMed] [Google Scholar]
- Sasaki H., Hogan B. L. HNF-3 beta as a regulator of floor plate development. Cell. 1994 Jan 14;76(1):103–115. doi: 10.1016/0092-8674(94)90176-7. [DOI] [PubMed] [Google Scholar]
- Schröter H., Shaw P. E., Nordheim A. Purification of intercalator-released p67, a polypeptide that interacts specifically with the c-fos serum response element. Nucleic Acids Res. 1987 Dec 23;15(24):10145–10158. doi: 10.1093/nar/15.24.10145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Schwarz-Sommer Z., Huijser P., Nacken W., Saedler H., Sommer H. Genetic Control of Flower Development by Homeotic Genes in Antirrhinum majus. Science. 1990 Nov 16;250(4983):931–936. doi: 10.1126/science.250.4983.931. [DOI] [PubMed] [Google Scholar]
- Sepulveda J. L., Belaguli N., Nigam V., Chen C. Y., Nemer M., Schwartz R. J. GATA-4 and Nkx-2.5 coactivate Nkx-2 DNA binding targets: role for regulating early cardiac gene expression. Mol Cell Biol. 1998 Jun;18(6):3405–3415. doi: 10.1128/mcb.18.6.3405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sharrocks A. D., Gille H., Shaw P. E. Identification of amino acids essential for DNA binding and dimerization in p67SRF: implications for a novel DNA-binding motif. Mol Cell Biol. 1993 Jan;13(1):123–132. doi: 10.1128/mcb.13.1.123. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw P. E., Frasch S., Nordheim A. Repression of c-fos transcription is mediated through p67SRF bound to the SRE. EMBO J. 1989 Sep;8(9):2567–2574. doi: 10.1002/j.1460-2075.1989.tb08395.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shaw P. E., Schröter H., Nordheim A. The ability of a ternary complex to form over the serum response element correlates with serum inducibility of the human c-fos promoter. Cell. 1989 Feb 24;56(4):563–572. doi: 10.1016/0092-8674(89)90579-5. [DOI] [PubMed] [Google Scholar]
- Shore P., Sharrocks A. D. The MADS-box family of transcription factors. Eur J Biochem. 1995 Apr 1;229(1):1–13. doi: 10.1111/j.1432-1033.1995.tb20430.x. [DOI] [PubMed] [Google Scholar]
- Smith J. C. Mesoderm-inducing factors and mesodermal patterning. Curr Opin Cell Biol. 1995 Dec;7(6):856–861. doi: 10.1016/0955-0674(95)80070-0. [DOI] [PubMed] [Google Scholar]
- Soriano P., Montgomery C., Geske R., Bradley A. Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice. Cell. 1991 Feb 22;64(4):693–702. doi: 10.1016/0092-8674(91)90499-o. [DOI] [PubMed] [Google Scholar]
- Soulez M., Rouviere C. G., Chafey P., Hentzen D., Vandromme M., Lautredou N., Lamb N., Kahn A., Tuil D. Growth and differentiation of C2 myogenic cells are dependent on serum response factor. Mol Cell Biol. 1996 Nov;16(11):6065–6074. doi: 10.1128/mcb.16.11.6065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- St-Jacques B., McMahon A. P. Early mouse development: lessons from gene targeting. Curr Opin Genet Dev. 1996 Aug;6(4):439–444. doi: 10.1016/s0959-437x(96)80065-7. [DOI] [PubMed] [Google Scholar]
- Sutherland D., Samakovlis C., Krasnow M. A. branchless encodes a Drosophila FGF homolog that controls tracheal cell migration and the pattern of branching. Cell. 1996 Dec 13;87(6):1091–1101. doi: 10.1016/s0092-8674(00)81803-6. [DOI] [PubMed] [Google Scholar]
- Tam P. P., Behringer R. R. Mouse gastrulation: the formation of a mammalian body plan. Mech Dev. 1997 Nov;68(1-2):3–25. doi: 10.1016/s0925-4773(97)00123-8. [DOI] [PubMed] [Google Scholar]
- Tang S. J., Hoodless P. A., Lu Z., Breitman M. L., McInnes R. R., Wrana J. L., Buchwald M. The Tlx-2 homeobox gene is a downstream target of BMP signalling and is required for mouse mesoderm development. Development. 1998 May;125(10):1877–1887. doi: 10.1242/dev.125.10.1877. [DOI] [PubMed] [Google Scholar]
- Taylor M., Treisman R., Garrett N., Mohun T. Muscle-specific (CArG) and serum-responsive (SRE) promoter elements are functionally interchangeable in Xenopus embryos and mouse fibroblasts. Development. 1989 May;106(1):67–78. doi: 10.1242/dev.106.1.67. [DOI] [PubMed] [Google Scholar]
- Treisman R. Identification and purification of a polypeptide that binds to the c-fos serum response element. EMBO J. 1987 Sep;6(9):2711–2717. doi: 10.1002/j.1460-2075.1987.tb02564.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Treisman R. Identification of a protein-binding site that mediates transcriptional response of the c-fos gene to serum factors. Cell. 1986 Aug 15;46(4):567–574. doi: 10.1016/0092-8674(86)90882-2. [DOI] [PubMed] [Google Scholar]
- Treisman R. Journey to the surface of the cell: Fos regulation and the SRE. EMBO J. 1995 Oct 16;14(20):4905–4913. doi: 10.1002/j.1460-2075.1995.tb00173.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Treisman R. Regulation of transcription by MAP kinase cascades. Curr Opin Cell Biol. 1996 Apr;8(2):205–215. doi: 10.1016/s0955-0674(96)80067-6. [DOI] [PubMed] [Google Scholar]
- Treisman R. Ternary complex factors: growth factor regulated transcriptional activators. Curr Opin Genet Dev. 1994 Feb;4(1):96–101. doi: 10.1016/0959-437x(94)90097-3. [DOI] [PubMed] [Google Scholar]
- Treisman R. The serum response element. Trends Biochem Sci. 1992 Oct;17(10):423–426. doi: 10.1016/0968-0004(92)90013-y. [DOI] [PubMed] [Google Scholar]
- Vandromme M., Gauthier-Rouvière C., Carnac G., Lamb N., Fernandez A. Serum response factor p67SRF is expressed and required during myogenic differentiation of both mouse C2 and rat L6 muscle cell lines. J Cell Biol. 1992 Sep;118(6):1489–1500. doi: 10.1083/jcb.118.6.1489. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wang Z. Q., Ovitt C., Grigoriadis A. E., Möhle-Steinlein U., Rüther U., Wagner E. F. Bone and haematopoietic defects in mice lacking c-fos. Nature. 1992 Dec 24;360(6406):741–745. doi: 10.1038/360741a0. [DOI] [PubMed] [Google Scholar]
- Wilkinson D. G., Bhatt S., Herrmann B. G. Expression pattern of the mouse T gene and its role in mesoderm formation. Nature. 1990 Feb 15;343(6259):657–659. doi: 10.1038/343657a0. [DOI] [PubMed] [Google Scholar]
- Zhang H., Bradley A. Mice deficient for BMP2 are nonviable and have defects in amnion/chorion and cardiac development. Development. 1996 Oct;122(10):2977–2986. doi: 10.1242/dev.122.10.2977. [DOI] [PubMed] [Google Scholar]
- Zinck R., Cahill M. A., Kracht M., Sachsenmaier C., Hipskind R. A., Nordheim A. Protein synthesis inhibitors reveal differential regulation of mitogen-activated protein kinase and stress-activated protein kinase pathways that converge on Elk-1. Mol Cell Biol. 1995 Sep;15(9):4930–4938. doi: 10.1128/mcb.15.9.4930. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zwart R., Broos L., Grosveld G., Meijer D. The restricted expression pattern of the POU factor Oct-6 during early development of the mouse nervous system. Mech Dev. 1996 Feb;54(2):185–194. doi: 10.1016/0925-4773(95)00472-6. [DOI] [PubMed] [Google Scholar]