Metabolic stabilization of muscle nicotinic acetylcholine receptor by rapsyn

Journal of Neuroscience

Volumn 19, Issue 6, 1999, Pages 1998-2007

  Wang, Zuo Zhong ^a,c   Mathias, Askale ^a   Gautam, Medha ^b   Hall, Zach W ^a,d  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

43 kDa protein; Acetylcholine; Endplate; Myotubes; Neuromuscular junction; Nicotinic receptors; Rapsyn; Receptor turnover

Indexed keywords

CHOLINERGIC RECEPTOR; COLCHICINE; CYTOCHALASIN D; MUTANT PROTEIN; NICOTINIC RECEPTOR; RAPSYN;

ANIMAL CELL; ARTICLE; DRUG EFFECT; DRUG MECHANISM; EMBRYO; GENETIC TRANSFECTION; METABOLIC REGULATION; MORPHOGENESIS; MOUSE; MUSCLE CELL; MUSCLE FIBRIL; MYRISTYLATION; NERVE ENDING; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RECEPTOR DENSITY; RECEPTOR INTRINSIC ACTIVITY; TISSUE DEGENERATION;

EID: 0033559789     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-06-01998.1999     Document Type: Article

References (74)

1. Adams M E, Butler M H, Dvvyer TM, Peters M F, Murnane AA, Froehner SC (1943) Two forms of mouse syntrophin, a 58 kd dystrophinassociated protein, differ in primary structure and tissue distribution. Neuron 11:531-540.
2. Andreose JS. Xu R. Lomo T. Salpeter MM, Fumagalli G (1993) Degradation of two AChR populations at rat ncuromuscular junetions: regulation in vivo by electrical stimulation. J Neurosci 13:3433-3438.
3. Apel ED, Merlie JP (1995) Assembly of the postsynaptic apparatus. Curr Opin Ncurobiol 5:62-67.
4. Apel ED, Roberds SL, Campbell KP, Merlie JP (1995) Rapsyn may function as a link between the acetylcholine receptor and the agrinbinding dystrophin-associatcd glycoprotein complex. Neuron 15:115-126.
5. Berg DK. Hall ZW (1974) Fate of a-bungarotoxin bound to acetylcholine receptor in normal and dcnervated muscle. Science 184:473-475.
6. 2+ and effects of drugs which depolymcrize microtubules. J Neurosci 3:2670-2680.
7. Blount P, Smith MM, Merlie JP (1990) Assembly intermediates of the mouse muscle nicotinic acetylcholine receptor in stably transfected fibroblasts. J Cell Biol 111:2601-2611.
8. Brennan C.Scotland PB, Froehner SC. Hendcrson LP (1992) Functional properties of acetylcholine rcceptur coexpressed with the 43K protein in heterologous cell systems. Dev Biol 149:100-111.
9. Brodsky MH, Warton M. Myers RM, Littman DR (1990) Analysis of the site in CD4 that binds to the HIV envelope glycoprotein. J Immunol 144:3078-3086.
10. Buonanno A, Mudd J, Shah V. Merlie JP (1986) A universal oligonucleotide probe for acetylcholine receptor genes: selection and sequencing of cDNA clones for the mouse β subunit. J Biol Chem 261:16451-16458.
11. Burden S (1977) Acetylcholine receptors at the neuromuscular junction: developmental change in receptor turnover. Dev Biol 61:79-85.
12. Burden SJ (1985) The subsynaptic 43-kDa protein is concentrated at developing nerve-muscle svnapscs in vitro. Proc Natl Acad Sci USA 82:8270-8273.
13. Burden SJ, DePalma RL, Gottesman GS (1983) Crosslinking of proteins in acetylcholine receptor-rich membranes: association between the beta-subunit and the 43 KD subsynaptic protein. Cell 35:687-692.
14. Chang CC. Huang MC (1975) Turnover of junctional and extrajunctional acetylcholine receptors of the rat diaphragm. Nature 253:643-644.
15. Colledge M, Froehner SC (1998) To muster a cluster: anchoring neurotransmitter receptors at synapses. Proc Natl Acad Sci USA 95:3341-3343.
16. Connolly JA (1984) Role of the cytoskeleton in the formation, stabilization, and removal of acetylcholine receptor clusters in cultured muscle cells. J Cell Biol 99:148-154.
17. Cooper ST. Millar NS (1997) Host cell-specific folding and assembly of the neuronal nicotinic acetylcholine receptor alpha? subunit. J Neurochcm 68:2140-2151.
18. Dineley KT, Patrick JW (1998) Surface receptor expression determinants: mechanism. Soc Neurosci Abstr 24:838.
19. Fisele J-L, Bertrand S, Galzi J-L, Devillers-Thiery A, Changeux J-P, Bertrand D (1993) Chimaeric nicotinic-serotonergic receptor combines distinct ligand binding and channel specificities. Nature 366:479-483.
20. Fallon JR. Hall ZW (1994) Building synapses: agrin and dystroglycan stick together. Trends Neurosci 17:469-473.
21. Fambrough DM (1979) Control of acetylcholine receptors in skeletal muscle. Physiol Rev 59:165-227.
22. Ferns M, Deiner M, Hall ZW (1996) Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation. J Cell Biol 132:937-944.
23. Forsayeth JR. Garcia PD (1994) Adenovirus-mediated transfection of cultured cells. Biotechniqucs 17:354-358.
24. Frail DE. Musil LS. Buonanno A, Merlie JP (1989) Expression of R APsyn (43K protein) and nicotinic acetylcholine receptor genes is not coordinately regulated in mouse muscle. Neuron 2:1077-1086.
25. Froehner SC (1989) Expression of RNA transcript for the postsynaptic 43 kDa protein in innervated and denervated rat skeletal muscle. FEBS Lett 249:229-233.
26. Froehner SC (1991) The submembrane machinery for nicotinic acetylcholine receptor clustering. J Cell Biol 114:1-7.
27. Froehner SC, Luetje CW, Scotland PB. Patrick J (1990) The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron 5:403-410.
28. Froehner SC, Adams ME, Peters MF. Gee SH (1997) Syntrophins: modular adapter proteins at the neuromuscular junction and the sarcolemma. Soc Gen Physiol Ser 52:197-207.
29. Gardner PD (1990) Nucleotide sequence of the epsilon-subunit of the mouse muscle nicotinic acetylcholine receptor. Nucleic Acids Res 18:6714.
30. Gautam M, Noakes PG, Mudd J, Nichol M, Chu GC, Sanes JR, Merlie JP (1995) Failure of postsynaptic specialization to develop at ncuromuscular junctions of rapsyn-deficient mice. Nature 377:232-236.
31. Gee SH, Madhavan R, Levinson SR. Caldwcll JH. Sealock R, Froehner SC (1998) Interaction of muscle and hrain sodium channels with multiple members of the syntrophin family of dystrophin-associated proteins. J Neurosci 18:128-137.
32. Glass DJ, Yancopoulos GD (1997) Sequential roles of agrin, MuSK and rapsyn during neuromuscular junction formation. Curr Opin Ncurobiol 7:379-384.
33. Gu Y, Franco A, Gardner PD, Lansman JB, Hall ZW (1990) Properties of embryonic and adult muscle acetylcholine receptors transiently expressed in COS cells. Neuron 5:147-157.
34. Huganir RL, Miles K (1989) Protein phosphorylation of nicotinic acetylcholine receptors. Crit Rev Biochcm Mol Biol 24:183-215.
35. Ibraghimov-Beskrovnaya O, Ervasti JM, Lcveille CJ. Slaughter CA, Sernett SW, Campbell KP (1992) Primary structure of dystrophinassociated glycoproteins linking dystrophin to the extracellular matrix. Nature 355:696-702.
36. Isenberg KE, Mudd J, Shah V, Merlie JP (1986) Nuclcotide sequence of the mouse muscle acetylcholine receptor a subunit. Nucleic Acids Res 14:5111.
37. b-tsA58 transgenic mouse. Proc Natl Acad Sci USA 88:5096-5100.
38. Kopta C, Steinbach JH (1994) Comparison of mammalian adult and fetal nicotinic acetylcholine receptors stably expressed in fibroblasts. J Neurosci 14:3922-3933.
39. Kornilova E, Sorkina T, Beguinot L, Sorkin A (1996) Lysosomal targeting of epidermal growth factor receptors via a kinase-dcpendent pathway is mediated by the receptor carboxyl-terminal residues 1022-1123. J Biol Chem 271:30340-30346.
40. Krikorian JG, Bloch RJ (1992) Treatments that extract the 43K protein from acetylcholine receptor clusters modify the conformation of cytoplasmic domains of all subunits of the receptor. J Biol Chem 267:9118-9128.
41. Kurten RC, Cadena DL, Gill ON (1996) Enhanced degradation of EGF receptors by a sorting nexin, SNX1. Science 272:1008-1010.
42. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
43. Lapolla RJ, Mayne KM, Davidson N (1984) Isolation and characterization of a cDNA clone for the complete protein coding region of the S subunit of the mouse acetylcholine receptor. Proc Natl Acad Sci USA 81:7970-7974.
44. LaRochelle WJ. Froehner SC (1986) Determination of the tissue distributions and relative concentrations of the postsynaptic 43-kDa protein and the acetylcholine receptor in Torpedo. J Biol Chem 261:5270-5274.
45. LaRochelle WJ, Froehner SC (1987) Comparison of the postsynaptic 43-kDa protein from muscle cells that differ in acetylcholine receptor clustering activity. J Biol Chem 262:8190-8195.
46. LaRochelle WJ, Witzemann V, Fiedler W Froehner SC (1990) Developmental expression of the 43K and 58K postsynaptic membrane proteins and nicotinic acetylcholine receptors in Torpedo electrocytes. J Neurosci 10:3460-3467.
47. Littman DR (1987) The structure of the CD4 and CD8 genes. Annu Rev Immunol 5:561-584.
48. Liu E, Hamill OP. Salpeter MM (1994) Mouse muscle ε- and γ-containing acetylcholine receptors expressed in Xenopus laevis oocytes do not differ in their degradation half-lives. Neurosci Lett 174:77-80.
49. Maimone MM, Merlie JP (1993) Interaction of the 43 kd postsynaptic protein with all subunits of the muscle nicotinic acetylcholine receptor. Neuron 11:53-66.
50. Mitra AAK, McCarthy MF. Stroud RM (1989) Three dimensional structure of the nicotinic acetvlcholine receptor, and location of the major associated 43-kD cytoskeletal protein, determined at 22 Å by low dose electron microscopy and x-ray diffraction to 12.5 Å. J Cell Biol 109:755-774.
51. Noakes PG, Phillips WD, Hanley TA, Sanes JR, Merlie JP (1993) 43K protein and acetylcholine receptors colocalize during the initial stages of neuromuscular synapse formation in vivo. Dev Biol 155:275-280.
52. O'Malley JP, Ruhin LL. Salpeter MM (1993) Two populations of AChR in rat myotuhes have different degradation rates and responses to cAMP. Exp Cell Res 208:44-47.
53. Pcng HB, Froehner SC (1985) Association of the postsynaptic 43K protein with newly formed acetylcholinc receptor clusters in cultured muscle cells. J Cell Biol 100:1698-1705.
54. Phillips WD, Kopta C, Blount P, Gardner PD, Steinbach JH, Merlic JP (1991a) ACh receptor-rich domains organized in fihrohlasts by rccomhinant 43-kilodalton protein. Science 251:568-570.
55. Phillips WD, Maimone MM, Merlie JP (1991b) Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering. J Cell Biol 115:1713-1723.
56. Phillips WD, Noakcs PG, Robcrds SL. Campbell KP, Merlic JP (1993) Clustering and immobilization of acetylcholinc receptors by the 43-kD protein: a possible role for dystrophin-relatcd protein. J Cell Biol 123:729-740.
57. Phillips WD. Vladeta D. Han H, Noakes PG (1997) Rapsyn and agrin slow the metabolic degradation of the acetylcholinc receptor. Mol Cell Neurosci 10:16-26.
58. Ramarao MK, Cohen JB (1998) Mechanism of nicotinic acetylcholinc receptor cluster formation by rapsyn. Proc Nail Acad Sci USA 95:4007-4012.
59. Salpeter MM (1987) Development and neural control of the ncuromuscular junction and of the junctional acetylcholinc receptor. In: The vertebrate neuromuscular junction (Salpeter MM, cd), pp 55-115. New York: Alan R. Liss.
60. Salpeter MM. Spanton S, Holly K, Podleski TR (1982) Brain extract causes acetylcholinc receptor redistribution which mimics some early events at developing neuromuscular junctions. J Cell Biol 93:417-425.
61. Sala C. O'Malley J. Xu R, Fumagalli G, Salpeter MM (1997) Epsilon suhunit-containing acctylcholine receptors in myotubes belong to the slowly degrading population. J Neurosci 17:8937-8944.
62. Scotland PB, Colledge M, Mclnikova I. Dai Z, Froehner SC (1993) Clustering of the acctylcholine receptor by the 43-kD protein: involvement of the zinc finger domain. J Cell Biol 123:719-728.
63. Sealock R. Wray BE, Froehner SC (1984) Ultrastructural localization of the Mr 43,000 prolein and acctylcholinc receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J Cell Biol 98:2239-2244.
64. Shcng M. Kim E (1996) Ion channel associated proteins. Curr Opin Neurobiol. 6:602-608.
65. Steinbach JH, Merlic J, Hcinemann S, Bloch R (1979) Degradation of junctional and cxtrajunctional acctylcholine receptors by developing rat skeletal muscle. Proc Natl Acad Sci USA 76:3547-3551.
66. Wagner K. Edson K, Heginbotham L, Post M, Huganir RL, Czcrnik AJ (1991) Determination of the tyrosine phosphorylation sites of the nicotinic acctylcholine receptor. J Biol Chem 266:23784-23789.
67. Walker JH, Boustcad CM, Witzemann V (1984) The 43-K protein, vl, associated with acetylcholine receptor containing membrane fragments is an actin-binding protein. EMBO J 3:2287-2290.
68. Wang ZZ, Hall ZW (1996) Cocxpression of rapsyn (43 kDa protein) slows the turnover of the nicotinic acetylcholine receptor in COS cells. Soc Neurosci Abstr 22:1034.
69. Wang ZZ, Hardy SF, Hall ZW (1996a) Assembly of the nicotinic acclylcholine receptor: the first transmcmbranc domains of truncated a and δ subunits are required for hetcrodimer formation in vivo. J Biol Chcm 271:27575-27584.
70. Wang ZZ, Hardy SF, Hall ZW (1996b) Membrane tethering enables an extracellular domain of the acetylcholine receptor a subunit to form a hetcrodimeric ligand-binding site. J Cell Biol 135:809-817.
71. Xu R, Salpeter MM (1995) Protein kinasc A regulates the degradation rate of Rs acctylcholinc receptors. J Cell Physiol 165:30-39.
72. Xu R, Salpeter MM (1997) Acetylcholine receptors in innervated muscles of dystrophic max mice degrade as after denervation. J Neurosci 17:8194-8200.
73. Yu L, LaPolla RJ. Davidson N (1986) Mouse muscle nicotinic acetylcholine receptor γ subunit: cDNA sequence and gene expression. Nucleic Acids Res 14:3539-3555.
74. Yu X-M, Hall ZW (1994) The role of the cytoplasmic domains of individual subunits of the acetylcholine receptor in 43 kDa protein-induced clustering in COS cells. J Neurosci 14:785-795.