Implication of a multisubunit Ets-related transcription factor in synaptic expression of the nicotinic acetylcholine receptor

EMBO Journal

Volumn 17, Issue 11, 1998, Pages 3078-3090

  Schaeffer, Laurent ^a   Duclert, Nathalie ^a   Huchet Dymanus, Monique ^a   Changeux, Jean Pierre ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Ets transcription factors; Neuregulins; Neuromuscular junction; Nicotinic acetylcholine receptor; Synaptic expression

Indexed keywords

BINDING PROTEIN; MESSENGER RNA; NICOTINIC RECEPTOR; TRANSCRIPTION FACTOR;

ARTICLE; DROSOPHILA; IN SITU HYBRIDIZATION; MYOTUBE; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE HOMOLOGY; TRANSCRIPTION REGULATION;

ANIMALS; CELLS, CULTURED; CHICKENS; DNA-BINDING PROTEINS; GA-BINDING PROTEIN TRANSCRIPTION FACTOR; GLYCOPROTEINS; MICE; MOLECULAR WEIGHT; MUSCLES; MUTAGENESIS, SITE-DIRECTED; NEUREGULINS; NICOTINIC ANTAGONISTS; OLIGONUCLEOTIDES, ANTISENSE; PEPTIDES; PHOSPHORYLATION; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-ETS; RECEPTORS, CHOLINERGIC; RECEPTORS, NICOTINIC; SYNAPSES; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

ARACHNIDA; HEXAPODA;

EID: 0032101544     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.11.3078     Document Type: Article

References (70)

1. Altiok, N., Altiok, S. and Changeux, J.P. (1997) Heregulin-stimulated acetylcholine receptor gene expression in muscle - requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity. EMBO J., 16, 717-725.
2. Baldwin, T.J. and Burden, S.J. (1988) Isolation and characterization of the mouse acetylcholine receptor delta subunit gene: identification of a 148-bp cis-acting region that confers myotube-specific expression. J. Cell Biol., 107, 2271-2279.
3. Beall, J.A. and Mitchell, G.F. (1986) Identification of a particular antigen from a parasite cDNA library using antibodies affinity purified from selected portions of Western blots. J. Immunol. Methods, 86, 217-223.
4. Bessereau, J.L., Mendelzon, D., Le Poupon, C., Fiszman, M., Changeux, J.P. and Piette, J. (1993) Muscle specific expression of the acetylcholine receptor alpha subunit gene requires both positive and negative interaction between myogenic factors Sp1 and GBF factors. EMBO J., 12, 443-449.
5. Bessereau, J.L., Stratford-Perricaudet, L.D., Piette, J., Le Poupon, C. and Changeux, J.P. (1994) In vivo and in vitro analysis of electrical activity-dependent expression of muscle acetylcholine receptor genes using adenovirus. Proc. Natl Acad. Sci. USA, 91, 1304-1308.
6. Blank, V., Kourilsky, P. and Israel, A. (1992) NF-kappa B and related proteins: Rel/dorsal homologies meet ankyrin-like repeats. Trends Biochem. Sci., 17, 135-140.
7. Brenner, H.R., Witzemann, V. and Sakmann, B. (1990) Imprinting of acetylcholine receptor messenger RNA accumulation in mammalian neuromuscular synapses. Nature, 344, 544-547.
8. Brown, T.A. and McKnight, S.L. (1992) Specificities of protein-protein and protein-DNA interaction of GABP alpha and two newly defined ets-related proteins. Genes Dev., 6, 2502-2512.
9. Burden, S. and Yarden, Y. (1997) Neuregulins and their receptors: a versatile signaling module in organogenesis and ontogenesis. Neuron, 18, 847-855.
10. Changeux, J.P. et al. (1990) Compartmentalization of acetylcholine receptor genes expression during development of the neuromuscular junction. Cold Spring Harbor Symp. Quant. Biol., 55, 381-396.
11. Chomczynski, P. and Sacchi, N. (1987) Single step method for RNA isolation by acid guanidium thiocyanate-phenol-chloroform extraction. Anal. Biochem., 162, 156-159.
12. Crepieux, P., Coll, J. and Stehelin, D. (1994) The Ets family of proteins: weak modulators of gene expression in quest for transcriptional partners. Crit. Rev. Oncogen., 5, 615-638.
13. de la Brousse, F. Birkenmeier, E.H., King, D.S., Rowe, L.B. and McKnight, S.L. (1994) Molecular and genetic characterization of GABP beta. Genes Dev., 8, 1853-1865.
14. Dennis, C.L., Tinsley, J.M., Deconinck, A.E. and Davies, K.E. (1996) Molecular and functional analysis of the utrophin promoter. Nucleic Acids Res., 24, 1646-1652.
15. Duclert, A. and Changeux, J.P. (1995) Acetylcholine receptor genes expression at the developing neuromuscular junction. Physiol. Rev., 75, 339-367.
16. Duclert, A., Piette, J. and Changeux, J.P. (1991) Influence of innervation on myogenic factors and acetylcholine receptor α-subunit mRNAs. NeuroReport, 2, 25-28.
17. Duclert, A., Savatier, N. and Changeux, J.P. (1993) An 83 nucleotide promoter of the acetylcholine receptor epsilon-subunit gene confers preferential synaptic expression in mouse muscle. Proc. Natl Acad. Sci. USA, 90, 3043-3047.
18. Duclert, A., Savatier, N., Schaeffer, L. and Changeux, J.P. (1996) Identification of an element crucial for the sub-synaptic expression of the acetylcholine receptor epsilon-subunit gene. J. Biol Chem., 271, 17433-17438.
19. Falls, D.L., Rosen, K.M., Corfas, G., Lane, W.S. and Fischbach, G.D. (1993) ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the Neu ligand family. Cell, 72, 801-815.
20. Flory, E., Hoffmeyer, A., Smola, U., Rapp, U.R. and Bruder, J.T. (1996) Raf-1 kinase targets GA-binding protein in transcriptional regulation of the human immunodeficiency virus type 1 promoter. J. Virol., 70, 2260-2268.
21. Fontaine, B. and Changeux, J.P. (1989) Localization of nicotinic acetylcholine receptor alpha-subunit transcripts during myogenesis and motor endplate development in the chick. J. Cell Biol., 108, 1025-1037.
22. Fontaine, B., Klarsfeld, A., Hökfelt, T. and Changeux, J.P. (1986) Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes. Neurosci. Lett., 71, 59-65.
23. Fontaine, B., Sassoon, D., Buckingham, M. and Changeux, J.P. (1988) Detection of the nicotinic acetylcholine receptor alpha-subunit mRNA by in situ hybridization at neuromuscular junctions of 15-day-old chick striated muscles. EMBO J., 7, 603-609.
24. Galzi, J.L. and Changeux, J.P. (1994) Neurotransmitter-gated ion channels as unconventional allosteric proteins. Curr. Opin. Struct. Biol., 4, 554-565.
25. Genuario, R.R. and Perry, R.P. (1996) The GA-binding protein can serve as both an activator and repressor of ribosomal protein gene transcription. J. Biol. Chem., 271, 4388-4395.
26. Giovane, A., Pintzas, A., Maira, S.M., Sobieszczuk, P. and Wasylyk, B. (1994) Net, a new ets transcription factor that is activated by Ras. Genes Dev., 8, 1502-1513.
27. Goldman, D. and Staple, J. (1989) Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle. Neuron, 3, 219-228.
28. Goldman, D., Brenner, H.R. and Heinemann, S. (1988) Acetylcholine receptor alpha-, beta-, gamma-, and delta-subunit mRNA levels are regulated by muscle activity. Neuron, 1, 329-335.
29. Hall, Z.W. and Sanes, J.R. (1993) Synaptic structure and development: the neuromuscular junction. Cell/Neuron, 72, 99-121.
30. Jia, H.T., Tsay, H.J. and Schmidt, J. (1992) Analysis of binding and activating functions of the chick muscle acetylcholine receptor gamma-subunit upstream sequence. Cell. Mol. Neurobiol., 12, 241-258.
31. Jo, S.A., Zhu, X., Marchionni, M.A. and Burden, S.J. (1995) Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature, 373, 158-161.
32. Jousset, C. et al. (1997) A domain of tel conserved in a subset of ets proteins defines a specific oligomerization interface essential to the mitogenic properties of the tel-pdgfr-beta oncoprotein. EMBO J., 16, 69-82.
33. Karlin, A. and Akabas, M.H. (1995) Toward a structural basis for the function of nicotinic acetylcholine receptors and their cousins. Neuron, 15, 1231-1244.
34. Klarsfeld, A. and Changeux, J.P. (1985) Activity regulates the levels of acetylcholine receptor α-subunit mRNA in cultured chicken myotubes. Proc. Natl Acad. Sci. USA, 82, 4558-4562.
35. Klarsfeld, A., Bessereau, J.L., Salmon, A.M., Triller, A., Babinet, C. and Changeux, J.P. (1991) An acetylcholine receptor alpha-subunit promoter conferring preferential synaptic expression in muscle of transgenic mice. EMBO J., 10, 625-632.
36. Koelle, G.B. and Fiedenwald, J.S. (1949) A histological method for localizing cholinesterase activity. Proc. Soc. Biol. Med., 70, 617-622.
37. Koike, S., Schaeffer, L. and Changeux, J.P. (1995) Identification of a DNA element determining synaptic expression of the mouse acetylcholine receptor delta-subunit gene. Proc. Natl Acad. Sci. USA, 92, 10624-10628.
38. Kues, W.A., Sakmann, B. and Witzemann, V. (1995) Differential expression patterns of five acetylcholine receptor subunit genes in rat muscle during development. Eur. J. Neurosci., 7, 1376-1385.
39. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
40. LaMarco, K., Thompson, C.C., Byers, B.P., Walton, E.M. and McKnight, S.L. (1991) Identification of Ets-and notch-related subunits in GA binding protein. Science, 253, 789-792.
41. Laufer, R. and Changeux, J.P. (1989) Activity dependent regulation of gene expression in muscle and neuronal cells. Mol. Neurobiol., 3, 1-54.
42. Lopez, M., Oettgen, P., Akbarali, Y., Dendorfer, U. and Libermann, T.A. (1994) ERP, a new member of the ets transcription factor/oncoprotein family: cloning, characterization, and differential expression during B-lymphocyte development. Mol. Cell. Biol., 14, 3292-3309.
43. Macleod, K., Leprince, D. and Stehelin, D. (1992) The ets gene family. Trends Biochem. Sci., 17, 251-256.
44. Mendelzon, D., Changeux, J.P. and Nghiêm, H.O. (1994) Phosphorylation of myogenin in chick myotubes: regulation by electrical activity and by protein kinase C. Implications for acetylcholine receptor gene expression. Biochemistry, 33, 2568-2575.
45. Merlie, J.P. and Kornhauser, J.M. (1989) Neural regulation of gene expression by an acetylcholine receptor promoter in muscle of transgenic mice. Neuron, 2, 1295-1300.
46. Merlie, J. and Sanes, J.R. (1985) Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibers. Nature, 317, 66-68.
47. Moscoso, L.M., Chu, G.C., Gautam, M., Noakes, P.G., Merlie, J.P. and Sanes, J.R. (1995) Synapse-associated expression of an acetylcholine receptor-inducing protein, ARIA/heregulin, and its putative receptors, ErbB2 and ErbB3, in developing mammalian muscle. Dev. Biol., 172, 158-169.
48. Nef, P., Mauron, A., Stalder, R., Alloid, C. and Ballivet, M. (1984) Structure linkage, and sequence of the two genes encoding the delta and gamma subunits of the nicotinic acetylcholine receptor. Proc. Natl Acad. Sci. USA, 81, 7975-7979.
49. New, H.V. and Mudge, A.W. (1986) Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis. Nature, 323, 809-811.
50. Ouyang, L., Jacob, K.K. and Stanley, F.M. (1996) GABP mediates insulin-increased prolactin gene transcription. J. Biol. Chem., 271, 10425-10428.
51. Piette, J., Bessereau, J.L., Huchet, M. and Changeux, J.P. (1990) Two adjacent MyoD1-binding sites regulate the expression of the acetylcholine receptor α-subunit gene. Nature, 345, 353-355.
52. Piette, J., Huchet, M., Houzelstein, D. and Changeux, J.P. (1993) Compartmentalized expression of the α and γ-subunits of the acetylcholine receptor in recently fused myotubes. Dev. Biol., 157, 205-213.
53. Prody, C.A. and Merlie, J.P. (1992) The 5′-flanking region of the mouse muscle nicotinic acetylcholine receptor beta-subunit gene promotes expression in cultured muscle cells and is activated by MRF4, myogenin and MyoD. Nucleic Acids Res., 20, 2367-2372.
54. Rivera, R.R., Stuiver, M.H., Steenbergen, R. and Murre, C. (1993) Ets proteins: new factors that regulate immunoglobulin heavy-chain gene expression. Mol. Cell. Biol., 13, 7163-7169.
55. Sandrock, A.J., Dryer, S.E., Rosen, K.M., Gozani, S.N., Kramer, R., Theill, L.E. and Fischbach, G.D. (1997) Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction in vivo. Science, 276, 599-603.
56. Sanes, J.R., Johnson, Y.R., Kotzbauer, P.T., Mudd, J., Hanley, T., Martinou, J.C. and Merlie, J.P. (1991) Selective expression of an acetylcholine receptor-LacZ transgene in synaptic nuclei of adult muscle fibers. Development, 113, 1181-1191.
57. Sapru, M.K., Florance, S.K., Kirk, C. and Glodman, D. (1998) Identification of a neuregulin and protein-tyrosine phosphatase response element in the nicotinic acetylcholine receptor ε subunit gene: regulatory role of an Ets transcription factor. Proc. Natl Acad. Sci. USA, 95, 1289-1294.
58. Sawa, C., Goto, M., Suzuki, F., Watanabe, H., Sawada, J.I. and Handa, H. (1996) Functional domains of transcription factor hgabp-beta-1/e4tf1-53 required for nuclear localization and transcription activation. Nucleic Acids Res., 24, 4954-4961.
59. Seth, A. and Papas, T.S. (1990) The c-ets-1 proto-oncogene has oncogenic activity and is positively autoregulated. Oncogene, 5, 1761-1767.
60. Sgouras, D.N., Athanasiou, M.A., Beal, G.J., Jr. Fisher, R.J., Blair, D.G. and Mavrothalassitis, G.J. (1995) ERF: an Ets domain protein with strong transcriptional repressor activity, can suppress ets-associated tumorigenesis and is regulated by phosphorylation during cell cycle and mitogenic stimulation. EMBO J., 14, 4781-4793.
61. Simon, A.M. and Burden, S.J. (1993) An E box mediates activation and repression of the acetylcholine receptor δ-subunit gene during myogenesis. Mol. Cell. Biol., 13, 5133-5140.
62. Simon, A.M., Hoppe, P. and Burden, S.J. (1992) Spatial restriction of AChR gene expression to subsynaptic nuclei. Development, 114, 545-553.
63. Skolnik, E.Y., Batzer, A., Li, N., Lee, C.H., Lowenstein, E., Mohammadi, M., Margolis, B. and Schlessinger, J. (1993) The function of GRB2 in linking the insulin receptor to Ras signaling pathways. Science, 260, 1953-1955.
64. Tang, J., Jo, S.A. and Burden, S.J. (1994) Separate pathways for synapse-specific and electrical activity-dependent gene expression in skeletal muscle. Development, 120, 1799-1804.
65. Tansey, M.G., Chu, G.C. and Merlie, J.P. (1996) Aria/hg regulates Achr epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and ras/mapk pathway. J. Cell Biol., 134, 465-476.
66. Thompson, C.C., Brown, T.A. and McKnight, S.L. (1991) Convergence of Ets-and notch-related structural motifs in a heteromeric DNA binding complex. Science, 253, 762-768.
67. Tsay, H.J. and Schmidt, J. (1989) Skeletal muscle denervation activates acetylcholine receptor genes. J. Cell Biol., 108, 1523-1526.
68. van Beveren, C.P., Rands, E., Chattopadhyay, S.K., Lowy, D.R. and Verma, I.M. (1982) Long terminal repeats of murine retroviral dans: sequence analysis, host-proviral junctions, and integration sites. J. Virol., 41, 542-556.
69. Wang, C.Y., Petryniak, B., Ho, I.C., Thompson, C.B. and Leiden, J.M. (1992) Evolutionarily conserved Ets family members display distinct DNA binding specificities. J. Exp. Med., 175, 1391-1399.
70. Watanabe, H., Wada, T. and Handa, H. (1990) Transcription factor E4TF1 contains two subunits with different functions. EMBO J., 9, 841-847.