Agrin can mediate acetylcholine receptor gene expression in muscle by aggregation of muscle-derived neuregulins

Journal of Cell Biology

Volumn 141, Issue 3, 1998, Pages 715-726

  Meier, Thomas ^a   Masciulli, Fabrizio ^a   Moore, Chris ^a   Schoumacher, Fabrice ^b   Eppenberger, Urs ^b   Denzer, Alain J ^c   Jones, Graham ^a   Brenner, Hans Rudolf ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY WOMEN S HOSPITAL   (Switzerland)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

AGRIN; CHOLINERGIC RECEPTOR; NEU DIFFERENTIATION FACTOR; PROTEOHEPARAN SULFATE;

ACETYLCHOLINE RELEASE; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; LIGAND BINDING; MUSCLE FIBER MEMBRANE; MYOTUBE; NEUROMUSCULAR SYNAPSE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION;

AGRIN; ANIMALS; CELL LINE; EPIDERMAL GROWTH FACTOR; GENE EXPRESSION REGULATION; GLYCOPROTEINS; GLYCOSAMINOGLYCANS; HEPARAN SULFATE PROTEOGLYCANS; HUMANS; IMMUNOGLOBULINS; MICE; MUSCLES; NEUREGULINS; PROTEIN BINDING; RECEPTOR, ERBB-2; RECEPTORS, CHOLINERGIC; SYNAPTIC MEMBRANES; TRANSCRIPTION, GENETIC;

EID: 0032482197     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.3.715     Document Type: Article

References (70)

1. Altiok, N., J.L. Bessereau, and J.P. Changeux. 1995. ErbB3 and erbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the endplate. EMBO (Eur. Mol. Biol. Organ.) J. 14:4258-4266.
2. Altiok, N., S. Altiok, and J.-P. Changeux. 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 (Eur. Mol. Biol. Organ.) J. 16:717-725.
3. Apel, E.D., and J.P. Merlie. 1995. Assembly of the postsynaptic apparatus. Curr. Opin. Neurobiol. 5:62-67.
4. Brenner, H.R., V. Witzemann, and B. Sakmann. 1990. Imprinting of acetylcholine receptor messenger RNA accumulation in mammalian neuromuscular synapses. Nature. 344:544-547.
5. Brenner, H.R., A. Herczeg, and C.R. Slater. 1992. Synapse-specific expression of acetylcholine receptor genes and their products at original synaptic sites in rat soleus muscle fibres regenerating in the absence of innervation. Development (Camb.). 116:41-53.
6. Carbonetto, S., and M. Lindenbaum. 1995. The basement membrane at the neuromuscular junction: a synaptic mediatrix. Curr. Opin. Neurobiol. 5:596-605.
7. Carraway, K.L., J.L. Weber, M.J. Unger, J. Ledesma, Y. Naichen, and M. Gassmann, C. Lai. 1997. Neuregulin-2, a new ligand of ErbB3/ErbB4-receptor tyrosine kinases. Nature. 387:512-516.
8. Chang, H., D.J. Riese, W. Gilbert, D.F. Stern, and U.J. McMahan. 1997. Ligands for ErbB-family receptors encoded by a neuregulin-like gene. Nature. 387:509-512.
9. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
10. Chiquet, M., N. Vrucinic-Fiipi, S. Schenk, K. Beck, and R. Chiquet-Ehrismann. 1991. Isolation of chick tenascin variants and fragments. Eur. J. Biochem. 199:379-388.
11. Chu, G.C., L.M. Moscoso, M.X. Sliwkowski, and J.P. Merlie. 1995. Regulation of the acetylcholine receptor ∈-subunit gene by recombinant ARIA: an in vitro model for transynaptic gene regulation. Neuron. 14:329-339.
12. Cohen, I., M. Rimer, T. Lomo, and U.J. McMahan. 1997. Agrin-induced postsynaptic apparatus in skeletal muscle fibers in vivo. Mol. Cell Neurosci. 9:237-253.
13. Corfas, G., D.L. Falls, and G.D. Fischbach. 1993. ARIA, a protein that stimulates acetylcholine receptor synthesis, also induces tyrosine phosphorylation of a 185-kDa muscle transmembrane protein. Proc. Natl. Acad. Sci. USA. 90: 1624-1628.
14. DeChiara, T.M., D.C. Bowen, D.M. Valenzuela, M.V. Simmons, W.T. Poueymirou, S. Thomas, E. Kinetz, D.L. Compton, E. Rojas, J.S. Park, et al. 1996. The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell. 85:501-512.
15. Denzer, A.J., M. Gesemann, B. Schumacher, and M.A. Ruegg. 1995. An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix. J. Cell Biol. 131:1547-1560.
16. Denzer, A.J., M. Gesemann, and M.A. Ruegg. 1996. Diverse functions of the extracellular matrix molecule agrin. Semin. Neurosci. 8:357-366.
17. Denzer, A.J., R. Brandenberger, M. Gesemann, M. Chiquet, and M.A. Ruegg. 1997. Agrin binds to the nerve-muscle basal lamina via laminin. J. Cell Biol. 137:671-683.
18. Denzer, A.J., T. Schulthess, C. Fauser, B. Schumacher, R.A. Kammerer, J. Engel, and M. A. Ruegg. 1998. Electron microscopic structure of agrin and mapping of its binding site in laminin-1. EMBO (Eur. Mol. Biol. Organ.) J. 17: 335-343.
19. Donnelly, J.J., J.B. Ulmer, J.W. Shiver, and M.A. Liu. 1997. DNA vaccines. Annu. Rev. Immunol. 15:617-648.
20. Eldridge, C.F., J.R. Sanes, A.Y. Chiu, R.P. Bunge, and C.J. Cornbrooks. 1986. Basal lamina-associated heparan sulfate proteoglycan in the rat PNS: characterization and localization using monoclonal antibodies. J. Neurocytol. 15: 37-51.
21. Fallen, J.R., and Z.W. Hall. 1994. Building synapses: agrin and dystroglycan stick together. Trends Neurosci. 17:469-473.
22. Falls, D.L., K.M. Rosen, G. Corfas, W.S. Lane, and G.D. Fischbach. 1993. ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the Neu ligand family. Cell. 72:801-815.
23. Ferns, M.J., W. Hoch, J.T. Campanelli, F. Rupp, Z.W. Hall, and R.H. Scheller. 1992. RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes. Neuron. 8:1079-1086.
24. Ferns, M.J., J.T. Campanelli, W. Hoch, R.H. Scheller, and Z.W. Hall. 1993. The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans. Neuron. 11:491-502.
25. Fischbach, G.D., and K.M. Rosen. 1997. ARIA: a neuromuscular junction neuregulin. Annu. Rev. Neurosci. 20:429-458.
26. Gautam, M., P.G. Noakes, J. Mudd, M. Nichol, G.C. Chu, J.R. Sanes, and J.P. Merlie. 1995. Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature. 377:232-236.
27. Gesemann, M., A.J. Denzer, and M.A. Ruegg. 1995. Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site. J. Cell Biol. 128:625-636.
28. Gesemann, M., V. Cavalli, A.J. Denzer, A. Brancaccio, B. Schumacher, and M.A. Ruegg. 1996. Alternative splicing of agrin alters its binding to heparin, dystroglycan, and the putative agrin receptor. Neuron. 16:755-767.
29. Gesemann, M., A. Brancaccio, B. Schumacher, and M.A. Ruegg. 1997. Agrin is a high-affinity binding protein of dystroglycan in non-muscle tissue. J. Biol. Chem. 273:600-605.
30. Glass, D.J., D.C. Bowen, T.N. Stitt, C. Radziejewski, J. Bruno, T.E. Ryan, D.R. Gies, S. Shah, K. Mattsson, S.J. Burden, et al. 1996. Agrin acts via a MuSK receptor complex. Cell. 85:1-20.
31. Goodearl, A.D.J., A.G. Yee, A.W. Sandrock, G. Corfas, and G.D. Fishbach. 1995. ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction. J. Cell Biol. 130:1423-1434.
32. Hengerer, B. 1993. A rapid procedure for mRNA extraction from a large number of samples. Biotechniques. 14:522-524.
33. Hoch, W., M. Ferns, J.T. Campanelli, Z.W. Hall, and R.H. Scheller. 1993. Developmental regulation of highly spliced forms of agrin. Neuron. 11:479-490.
34. Hunter, W.M., and F.C. Greenwood. 1962. Preparation of iodine-131 labeled human growth hormone of high specific activity. Nature. 194:495-496.
35. Jeschke, M., W. Wels, W. Dengler, R. Imber, E. Stocklin, and B. Groner. 1995. Target inhibition of tumor-cell growth by recombinant heregulin-toxin fusion proteins. Int. J. Cancer. 60:730-739.
36. Jo, S.A., and S.J. Burden. 1992. Synaptic basal lamina contains a signal for synapse-specific transcription. Development (Camb.). 115:673-680.
37. Jo, S.A., X. Zhu, M.A. Marchionni, and S.J. Burden. 1995. Neuregulins are concentrated at nerve-muscle synapses and activate ACh-receptor gene expression. Nature. 373:158-161.
38. Jones, G., A. Herczeg, M.A. Ruegg, M. Lichsteiner, S. Kröger, and H.R. Brenner. 1996. Substrate-bound agrin induces expression of acetylcholine receptor ∈-subunit in cultured mammalian muscle cells. Proc. Natl. Acad. Sci. USA. 93:5985-5990.
39. Jones, G., T. Meier, M. Lichtsteiner, V. Witzemann, B. Sakmann, and H.R. Brenner. 1997. Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle. Proc. Natl. Acad. Sci. USA. 94:2654-2659.
40. Kleinman, H.K., M.L. McGarvey, L.A. Livatta, P.G. Robey, K. Tryggvason, and G.R. Martin. 1982. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from EHS sarcoma. Biochemistry. 21:6188-6193.
41. Lemke, G. 1996. Neuregulins in development. Mol. Cell. Neurosci. 7:247-262.
42. Lieth, E., and J.R. Fallon. 1993. Muscle agrin: neural regulation and localization at nerve-induced acetylcholine receptor clusters. J. Neurosci. 13:2509-2514.
43. Loeb, J.A., and G.D. Fishbach. 1995. ARIA can be released from extracellular matrix through cleavage of a heparin-binding domain. J. Cell Biol. 130:127-135.
44. Martinou, J.C., D.L. Falls, G.D. Fischbach, and J.P. Merlie. 1991. Acetylcholine receptor-inducing activity stimulates expression of the ∈-subunit gene of the muscle acetylcholine receptor. Proc. Natl. Acad. Sci. USA. 88:7669-7673.
45. McMahan, U.J. 1990. The agrin hypothesis. Cold Spring Harbor Symp. Quant. Biol. 55:407-418.
46. Meier, T., D.M. Hauser, M. Chiquet, L. Landmann, M.A. Ruegg, and H.R. Brenner. 1997. Neural agrin induces ectopic postsynaptic specializations in innervated muscle fibers. J. Neurosci. 17:6534-6544.
47. Moscoso, L.M., G.C. Chu, M. Gautam, P.G. Noakes, J.P. Merlie, and J.R. Sanes. 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. Ng, Y.P., S. Pun, J.F. Yang, N.Y. Ip, and K.W.K. Tsim. 1997. Chick muscle expresses various ARIA isoforms: regulation during development, denervation and regeneration. Mol. Cell Neurosci. 9:132-143.
49. Pinset, C., C. Mulle, P. Benoit, J.-P. Changeux, J. Chelly, F. Gros, and D. Montarras. 1991. Functional adult acetylcholine receptor develops independently of motor innervation in Sol8 mouse skeletal muscle cell line. EMBO (Ear. Mol. Biol. Organ.) J. 10:2411-2518.
50. Reist, N.E., C. Magill, and U.J. McMahan. 1987. Agrin-like molecules at synaptic sites in normal, denervated, and damaged skeletal muscles. J. Cell Biol. 105:2457-2469.
51. Rimer, M., I. Mathiesen, T. Lømo, and U.J. McMahan. 1997. γ-AChR/∈-AChR switch at agrin-induced postsynaptic-like apparatus in skeletal muscle. Mol. Cell. Neurosci. 9:254-263.
52. Ruegg, M.A., K.W.K. Tsim, S.E. Horton, S. Kröger, G. Escher, E.M. Gensch, and U.J. McMahan. 1992. The agrin gene codes for a family of basal lamina proteins that differ in function and distribution. Neuron. 8:691-699.
53. Sandrock, A.W., A.D.J. Goodearl, Q.-W. Yin, D. Chang, and G.D. Fischbach. 1995. ARIA is concentrated in nerve terminals at neuromuscular junctions and at other synapses. J. Neurosci. 15:6124-6136.
54. Sandrock, A.W., S.E. Dryer, K.M. Rosen, S.N. Gozani, R. Kramer, L.E. Theill, and G.D. Fischbach. 1997. Maintenance of acetylcholine receptor number by neuregulins at the neuromuscular junction. Science. 276:599-603.
55. Sanes, J.R. 1997. Genetic analysis of postsynaptic differentiation at the vertebrate neuromuscular junction. Curr. Opin. Neurobiol. 7:93-100.
56. Sanes, J.R., Y.R. Johnson, P.T. Kotzbauer, J. Mudd, T. Hanley, J.-C. Martinou, and J.P. Merie. 1991. Selective expression of an acetylcholine receptor-lacZ transgene in synaptic nuclei of adult muscle fibers. Development (Camb.). 113:1181-1191.
57. Shepherd, D., and P. Brehm. 1994. Adult forms of nicotinic acetylcholine receptors are expressed in the absence of nerve during differentiation of a mouse skeletal muscle cell line. Dev. Biol. 162:549-557.
58. Si, J., Z. Luo, and L. Mei. 1996. Induction of acetylcholine receptor gene expression by ARIA requires activation of mitogen-activated protein kinase. J. Biol. Chem. 271:19752-19759.
59. Tansey, M.G., G.C. Chu, and J.P. Merlie. 1996. ARIA/HRG regulates AChR ∈-subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway. J. Cell Biol. 134: 465-476.
60. Timpl, R. 1993. Proteoglycans of basement membranes. Experientia (Basel). 49: 417-428.
61. Timpl, R., and J.C. Brown. 1995. Supramolecular assembly of basement membranes. Bioessays. 18:123-132.
62. Timpl, R., H. Rhode, P.G. Robey, S.I. Rennard, J.M. Foidart, and G.R. Martin. 1979. Laminin-a glycoprotein from basement membranes. J. Biol. Chem. 254:9933-9937.
63. Tsen, G., W. Halfter, S. Kröger, and G.J. Cole. 1995. Agrin is a heparan sulfate proteoglycan. J. Biol. Chem. 270:3392-3399.
64. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
65. Valenzuela, D.M., T.M. Stitt, P.S. DiStefano, E. Rojas, K. Mattsson, D.L. Compton, L. Nunez, J.S. Park, J.L. Stark, D.R. Gies, et al. 1995. Receptor tyrosine kinase specific for the skeletal muscle lineage: expression in embryonic muscle, at the neuromuscular junction, and after injury. Neuron. 15: 573-584.
66. Wallace, B.G. 1989. Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus. J. Neurosci. 9:1294-1302.
67. Wallasch, C., F.U. Weiss, G. Niederfellner, B. Jallal, W. Issing, and A. Ullrich. 1995. Heregulin-dependent regulation of HER2/neu oncogenic signaling by heterodimerization with HER3. EMBO (Eur. Mol. Biol Organ.) J. 14:4267-4275.
68. Wen, D., E. Peles, R. Cupples, S.V. Suggs, S.S. Bacus, Y. Lou, G. Trail, S. Hu, S.M. Silbiger, R. Ben Levy, et al. 1992. Neu differentiation factor: a transmembrane glycoprotein containing an EGF domain and an immunoglobulin homology unit. Cell. 69:559-572.
69. Wen, D., S.V. Suggs, D. Karunagaran, N. Liu, R.L. Cupples, Y. Luo, A.M. Janssen, N. Ben-Baruch, D.B. Trollinger, V.L. Jacobsen, et al. 1994. Structural and functional aspects of the multiplicity of Neu differentiation factors. Mol. Cell. Biol. 14:1909-1919.
70. Yamada, H., A.J. Denzer, H. Hori, T. Tanaka, L.V.B. Anderson, S. Fujita, H. Fukuta-Ohi, T. Shimizu, M.A. Ruegg, and K. Matsumura. 1996. Dystroglycan is a dual receptor for agrin and laminin-2 in Schwann cell membrane. J. Biol. Chem. 271:23418-23423.