MuSK is required for anchoring acetylcholinesterase at the neuromuscular junction

Journal of Cell Biology

Volumn 165, Issue 4, 2004, Pages 505-515

  Cartaud, Annie ^a   Strochlic, Laure ^a   Guerra, Manuel ^b   Blanchard, Benoît ^a   Lambergeon, Monique ^b   Krejci, Eric ^b   Cartaud, Jean ^a   Legay, Claire ^b,c  

^a INSTITUT JACQUES MONOD   (France)

^b ECOLE NORMALE SUPÉRIEURE   (France)

^c Laboratoire de Neurobiologie Mol   (France)

Author keywords

Cholinergic transmission; ColQ; Heparin binding sites; Perlecan; Synapse

Indexed keywords

ACETYLCHOLINESTERASE; COLLAGEN; COLLAGEN Q; DYSTROGLYCAN; HEPARIN; MUSCLE SPECIFIC KINASE; PERLECAN; PROTEIN; TETRAMER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BASEMENT MEMBRANE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL LINE; CELL STRAIN COS7; CONTROLLED STUDY; CROSS LINKING; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; MOUSE; MYOTUBE; NEUROMUSCULAR SYNAPSE; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SYNAPTIC MEMBRANE; TORPEDO;

ACETYLCHOLINESTERASE; ANIMALS; BINDING SITES; COLLAGEN; COS CELLS; HEPARAN SULFATE PROTEOGLYCANS; MACROMOLECULAR SUBSTANCES; MICE; MICE, KNOCKOUT; MUSCLE FIBERS; MUSCLE PROTEINS; MUTATION; NEUROMUSCULAR JUNCTION; PROTEIN BINDING; RECEPTOR AGGREGATION; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, CHOLINERGIC; SYNAPTIC MEMBRANES; SYNAPTIC TRANSMISSION; TRANSFECTION;

ANIMALIA; TORPEDO;

EID: 2542487390     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200307164     Document Type: Article

References (46)

1. 125I-labeled fasciculin 2: a new tool for quantitation of acetylcholinesterase densities at synaptic sites by EM-autoradiography. J. Neurosci. Methods. 81:63-71.
2. Arikawa-Hirasawa, E., S.G. Rossi, R.L. Rotundo, and Y. Yamada. 2002. Absence of acetylcholinesterase at the neuromuscular junctions of perlecan-null mice. Nat. Neurosci. 5:119-123.
3. Bon, S., F. Coussen, and J. Massoulié. 1997. Quaternary associations of acetylcholinesterase. II. The polyproline attachment domain of the collagen tail. J. Biol. Chem. 272:3016-3021.
4. Brandan, E., M. Maldonado, J. Garrido, and N.C. Inestrosa. 1985. Anchorage of collagen-tailed acetylcholinesterase to the extracellular matrix is mediated by heparan sulfate proteoglycans. J. Cell Biol. 101:985-992.
5. Burden, S.J., R.L. DePalma, and G.S. Gottesman. 1983. Crosslinking of proteins in acetylcholine receptor-rich membranes: association between the beta-subunit and the 43 kd subsynaptic protein. Cell. 35:687-692.
6. Burden, S.J. 2002. Building the vertebrate neuromuscular synapse. J. Neurobiol. 53:501-511.
7. Cartaud, A., S. Coutant, T.C. Petrucci, and J. Cartaud. 1998. Evidence for in situ and in vitro association between beta-dystroglycan and the subsynaptic 43K rapsyn protein. Consequence for acetylcholine receptor clustering at the synapse. J. Biol. Chem. 273:11321-11326.
8. Chakkalakal, J.V., and B.J. Jasmin. 2003. Localizing synaptic mRNAs at the neuromuscular junction: it takes more than transcription. Bioessays. 25:25-31.
9. 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.
10. Deprez, P.N., and N.C. Inestrosa. 1995. Two heparin-binding domains are present on the collagenic tail of asymmetric acetylcholinesterase. J. Biol. Chem. 270:11043-11046.
11. Deprez, P.N., N.C. Inestrosa, and E. Krejci. 2003. Two heparin-binding domains in the triple-helical domain of ColQ, the collagen tail subunit of synaptic acetylcholinesterase. J. Biol. Chem. 278:23233-23242.
12. Donger, C., E. Krejci, A.P. Serradell, B. Eymard, S. Bon, S. Nicole, D. Chateau, F. Gary, M. Fardeau, J. Massoulie, and P. Guicheney. 1998. Mutation in the human acetylcholinesterase-associated collagen gene, COLQ, is responsible for congenital myasthenic syndrome with end-plate acetylcholinesterase deficiency (Type Ic). Am. J. Hum. Genet. 63:967-975.
13. Engel, A.G., K. Ohno, and S.M. Sine. 2003. Sleuthing molecular targets for neurological diseases at the neuromuscular junction. Nat. Rev. Neurosci. 4:339-352.
14. Feng, G., E. Krejci, J. Molgo, J.M. Cunningham, J. Massoulie, and J.R. Sanes. 1999. Genetic analysis of collagen Q: roles in acetylcholinesterase and butyrylcholinesterase assembly and in synaptic structure and function. J. Cell Biol. 144:1349-1360.
15. Hall, Z.W., and R.B. Kelly. 1971. Enzymatic detachment of endplate acetylcholinesterase from muscle. Nat. New Biol. 232:62-63.
16. Herbst, R., and S.J. Burden. 2000. The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J. 19:67-77 (published erratum in EMBO J. 2000. 19:1167).
17. Herbst, R., and S.J. Burden. 2000. The juxtamembrane region of MuSK has a critical role in agrin-mediated signaling. EMBO J. 19:67-77 (published erratum in EMBO J. 2000. 19:1167).
18. Hopf, C., and W. Hoch. 1997. Heparin inhibits acetylcholine receptor aggregation at two distinct steps in the agrin-induced pathway. Eur. J. Neurosci. 9:1170-1177.
19. Hopf, C., and W. Hoch. 1998. Dimerization of the muscle-specific kinase induces tyrosine phosphorylation of acetylcholine receptors and their aggregation on the surface of myotubes. J. Biol. Chem. 273:6467-6473.
20. Jacobson, C., P.D. Cote, S.G. Rossi, R.L. Rotundo, and S. Carbonetto. 2001. The dystroglycan complex is necessary for stabilization of acetylcholine receptor clusters at neuromuscular junctions and formation of the synaptic basement membrane. J. Cell Biol. 152:435-450.
21. Jasmin, B.J., R.K. Lee, and R.L. Rotundo. 1993. Compartmentalization of acetylcholinesterase mRNA and enzyme at the vertebrate neuromuscular junction. Neuron. 11:467-477.
22. Jat, P.S., M.D. Noble, P. Ataliotis, Y. Tanaka, N. Yannoutsos, L. Larsen, and D. Kioussis. 1991. Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc. Natl. Acad. Sci. USA. 88:5096-5100.
23. Krejci, E., F. Coussen, N. Duval, J.M. Chatel, C. Legay, M. Puype, J. Vandekerckhove, J. Cartaud, S. Bon, and J. Massoulié. 1991. Primary structure of a collagenic tail peptide of Torpedo acetylcholinesterase: co-expression with catalytic subunit induces the production of collagen-tailed forms in transfected cells. EMBO J. 10:1285-1293.
24. Krejci, E., S. Thomine, N. Boschetti, C. Legay, J. Sketelj, and J. Massoulié. 1997. The mammalian gene of acetylcholinesterase-associated collagen. J. Biol. Chem. 272:22840-22847.
25. Krejci, E., C. Legay, S. Thomine, J. Sketelj, and J. Massoulié. 1999. Differences in expression of acetylcholinesterase and collagen Q control the distribution and oligomerization of the collagen-tailed forms in fast and slow muscles. J. Neurosci. 19:10672-10679.
26. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
27. Legay, C., S. Bon, P. Vernier, F. Coussen, and J. Massoulié. 1993. Cloning and expression of a rat acetylcholinesterase subunit: generation of multiple moleculax forms and complementarity with a Torpedo collagenic subunit. J. Neurochem. 60:337-346.
28. Legay, C., M. Huchet, J. Massoulié, and J.P. Changeux. 1995. Developmental regulation of acetylcholinesterase transcripts in the mouse diaphragm: alternative splicing and focalization. Eur. J. Neurosci. 7:1803-1809.
29. Legay, C., F.A. Mankal, J. Massoulié, and B.J. Jasmin. 1999. Stability and secretion of acetylcholinesterase forms in skeletal muscle cells. J. Neurosci. 19:8252-8259.
30. Legay, C. 2000. Why so many forms of acetylcholinesterase? Microsc. Res. Tech. 49:56-72.
31. Luo, Z., M.E. Fuentes, and P. Taylor. 1994. Regulation of acetylcholinesterase mRNA stability by calcium during differentiation from myoblasts to myotubes. J. Biol. Chem. 269:27216-27223.
32. Marsh, D., J. Grassi, M. Vigny, and J. Massoulié. 1984. An immunological study of rat acetylcholinesterase: comparison with acetylcholinesterases from other vertebrates. J. Neurochem. 43:204-213.
33. McMahan, U.J., J.R. Sanes, and L.M. Marshall. 1978. Cholinesterase is associated with the basal lamina at the neuromuscular junction. Nature. 271:172-174.
34. Ohno, K., J. Brengman, A. Tsujino, and A.G. Engel. 1998. Human endplate acetylcholinesterase deficiency caused by mutations in the collagen-like tail subunit (ColQ) of the asymmetric enzyme. Proc. Natl. Acad. Sci. USA. 95:9654-9659.
35. Ohno, K., A.G. Engel, J.M. Brengman, X.M. Shen, F. Heidenreich, A. Vincent, M. Milone, E. Tan, M. Demirci, P. Walsh, et al. 2000. The spectrum of mutations causing end-plate acetylcholinesterase deficiency. Ann. Neurol. 47:162-170 (published erratum in Ann. Neurol. 2000. 47:554).
36. Ohno, K., A.G. Engel, J.M. Brengman, X.M. Shen, F. Heidenreich, A. Vincent, M. Milone, E. Tan, M. Demirci, P. Walsh, et al. 2000. The spectrum of mutations causing end-plate acetylcholinesterase deficiency. Ann. Neurol. 47:162-170 (published erratum in Ann. Neurol. 2000. 47:554).
37. Peng, H.B., H. Xie, S.G. Rossi, and R.L. Rotundo. 1999. Acetylcholinesterase clustering at the neuromuscular junction involves perlecan and dystroglycan. J. Cell Biol. 145:911-921.
38. Rossi, S.G., and R.L. Rotundo. 1996. Transient interactions between collagen-tailed acetylcholinesterase and sulfated proteoglycans prior to immobilization on the extracellular matrix. J. Biol. Chem. 271:1979-1987.
39. Rotundo, R.L., S.G. Rossi, and L. Anglister. 1997. Transplantation of quail collagen-tailed acetylcholinesterase molecules onto the frog neuromuscular synapse. J. Cell Biol. 136:367-374.
40. 2+ mediate changes in acetylcholinesterase and acetylcholine receptors caused by muscle contraction. Proc. Natl. Acad. Sci. USA. 82:7121-7125.
41. Sander, A., B.A. Hesser, and V. Witzemann. 2001. MuSK induces in vivo acetylcholine receptor clusters in a ligand-independent manner. J. Cell Biol. 155:1287-1296.
42. Sanes, J.R., and J.W. Lichtman. 2001. Induction, assembly, maturation and maintenance of a postsynaptic apparatus. Nat. Rev. Neurosci. 2:791-805.
43. Simon, S., E. Krejci, and J. Massoulié. 1998. A four to one association between peptide motifs: four C-terminal domains from cholinesterase assemble with one proline-rich attachment domain (PRAD) in the secretory pathway. EMBO J. 17:6178-6187.
44. Strochlic, L., A. Cartaud, V. Labas, W. Hoch, J. Rossier, and J. Cartaud. 2001. MAGI-1c: a synaptic MAGUK interacting with MuSK at the vertebrate neuromuscular junction. J. Cell Biol. 153:1127-1132.
45. Trinidad, J.C., G.D. Fischbach, and J.B. Cohen. 2000. The Agrin/MuSK signaling pathway is spatially segregated from the neuregulin/ErbB receptor signaling pathway at the neuromuscular junction. J. Neurosci. 20:8762-8770.
46. Watty, A., G. Neubauer, M. Dreger, M. Zimmer, M. Wilm, and S.J. Burden. 2000. The in vivo and in vitro phosphotyrosine map of activated MuSK. Proc. Natl. Acad. Sci. USA. 97:4585-4590.