Skip to main content
NCBI home page
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1991 Dec 2;115(6):1713–1723. doi: 10.1083/jcb.115.6.1713

Mutagenesis of the 43-kD postsynaptic protein defines domains involved in plasma membrane targeting and AChR clustering

PMCID: PMC2289204  PMID: 1757470

Abstract

The postsynaptic membrane of the neuromuscular junction contains a myristoylated 43-kD protein (43k) that is closely associated with the cytoplasmic face of the nicotinic acetylcholine receptor (AChR)-rich plasma membrane. Previously, we described fibroblast cell lines expressing recombinant AChRs. Transfection of these cell lines with 43k was necessary and sufficient for reorganization of AChR into discrete 43k-rich plasma membrane domains (Phillips, W. D., C. Kopta, P. Blount, P. D. Gardner, J. H. Steinbach, and J. P. Merlie. 1991. Science (Wash. DC). 251:568-570). Here we demonstrate the utility of this expression system for the study of 43k function by site-directed mutagenesis. Substitution of a termination codon for Asp254 produced a truncated (28- kD) protein that associated poorly with the cell membrane. The conversion of Gly2 to Ala2, to preclude NH2-terminal myristoylation, reduced the frequency with which 43k formed plasma membrane domains by threefold, but did not eliminate the aggregation of AChRs at these domains. Since both NH2 and COOH-termini seemed important for association of 43k with the plasma membrane, a deletion mutant was constructed in which the codon Gln15 was fused in-frame to Ile255 to create a 19-kD protein. This mutated protein formed 43k-rich plasma membrane domains at wild-type frequency, but the domains failed to aggregate AChRs, suggesting that the central part of the 43k polypeptide may be involved in AChR aggregation. Our results suggest that membrane association and AChR interactions are separable functions of the 43k molecule.

Full Text

The Full Text of this article is available as a PDF (1.5 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baldwin T. J., Theriot J. A., Yoshihara C. M., Burden S. J. Regulation of transcript encoding the 43K subsynaptic protein during development and after denervation. Development. 1988 Dec;104(4):557–564. doi: 10.1242/dev.104.4.557. [DOI] [PubMed] [Google Scholar]
  2. Barrantes F. J., Neugebauer D. C., Zingsheim H. P. Peptide extraction by alkaline treatment is accompanied by rearrangement of the membrane-bound acetylcholine receptor from Torpedo marmorata. FEBS Lett. 1980 Mar 24;112(1):73–78. doi: 10.1016/0014-5793(80)80131-1. [DOI] [PubMed] [Google Scholar]
  3. Berg J. M. Zinc fingers and other metal-binding domains. Elements for interactions between macromolecules. J Biol Chem. 1990 Apr 25;265(12):6513–6516. [PubMed] [Google Scholar]
  4. Bloch R. J., Morrow J. S. An unusual beta-spectrin associated with clustered acetylcholine receptors. J Cell Biol. 1989 Feb;108(2):481–493. doi: 10.1083/jcb.108.2.481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Blount P., Merlie J. P. Native folding of an acetylcholine receptor alpha subunit expressed in the absence of other receptor subunits. J Biol Chem. 1988 Jan 15;263(2):1072–1080. [PubMed] [Google Scholar]
  6. Burden S. J., DePalma R. L., Gottesman G. S. Crosslinking of proteins in acetylcholine receptor-rich membranes: association between the beta-subunit and the 43 kd subsynaptic protein. Cell. 1983 Dec;35(3 Pt 2):687–692. doi: 10.1016/0092-8674(83)90101-0. [DOI] [PubMed] [Google Scholar]
  7. Burden S. J. The subsynaptic 43-kDa protein is concentrated at developing nerve-muscle synapses in vitro. Proc Natl Acad Sci U S A. 1985 Dec;82(23):8270–8273. doi: 10.1073/pnas.82.23.8270. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Capetanaki Y., Kuisk I., Rothblum K., Starnes S. Mouse vimentin: structural relationship to fos, jun, CREB and tpr. Oncogene. 1990 May;5(5):645–655. [PubMed] [Google Scholar]
  9. Carr C., Fischbach G. D., Cohen J. B. A novel 87,000-Mr protein associated with acetylcholine receptors in Torpedo electric organ and vertebrate skeletal muscle. J Cell Biol. 1989 Oct;109(4 Pt 1):1753–1764. doi: 10.1083/jcb.109.4.1753. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carr C., McCourt D., Cohen J. B. The 43-kilodalton protein of Torpedo nicotinic postsynaptic membranes: purification and determination of primary structure. Biochemistry. 1987 Nov 3;26(22):7090–7102. doi: 10.1021/bi00396a034. [DOI] [PubMed] [Google Scholar]
  11. Carr C., Tyler A. N., Cohen J. B. Myristic acid is the NH2-terminal blocking group of the 43-kDa protein of Torpedo nicotinic post-synaptic membranes. FEBS Lett. 1989 Jan 16;243(1):65–69. doi: 10.1016/0014-5793(89)81219-0. [DOI] [PubMed] [Google Scholar]
  12. Cartaud J., Sobel A., Rousselet A., Devaux P. F., Changeux J. P. Consequences of alkaline treatment for the ultrastructure of the acetylcholine-receptor-rich membranes from Torpedo marmorata electric organ. J Cell Biol. 1981 Aug;90(2):418–426. doi: 10.1083/jcb.90.2.418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Changeux J. P. Compartmentalized transcription of acetylcholine receptor genes during motor endplate epigenesis. New Biol. 1991 May;3(5):413–429. [PubMed] [Google Scholar]
  14. Chen C., Okayama H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol Cell Biol. 1987 Aug;7(8):2745–2752. doi: 10.1128/mcb.7.8.2745. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dingwall C., Laskey R. A. Protein import into the cell nucleus. Annu Rev Cell Biol. 1986;2:367–390. doi: 10.1146/annurev.cb.02.110186.002055. [DOI] [PubMed] [Google Scholar]
  16. Elliott J., Blanchard S. G., Wu W., Miller J., Strader C. D., Hartig P., Moore H. P., Racs J., Raftery M. A. Purification of Torpedo californica post-synaptic membranes and fractionation of their constituent proteins. Biochem J. 1980 Mar 1;185(3):667–677. doi: 10.1042/bj1850667. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Frail D. E., McLaughlin L. L., Mudd J., Merlie J. P. Identification of the mouse muscle 43,000-dalton acetylcholine receptor-associated protein (RAPsyn) by cDNA cloning. J Biol Chem. 1988 Oct 25;263(30):15602–15607. [PubMed] [Google Scholar]
  18. Frail D. E., Mudd J., Shah V., Carr C., Cohen J. B., Merlie J. P. cDNAs for the postsynaptic 43-kDa protein of Torpedo electric organ encode two proteins with different carboxyl termini. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6302–6306. doi: 10.1073/pnas.84.17.6302. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Frail D. E., Musil L. S., Buonanno A., Merlie J. P. Expression of RAPsyn (43K protein) and nicotinic acetylcholine receptor genes is not coordinately regulated in mouse muscle. Neuron. 1989 Jan;2(1):1077–1086. doi: 10.1016/0896-6273(89)90232-8. [DOI] [PubMed] [Google Scholar]
  20. Freemont P. S., Hanson I. M., Trowsdale J. A novel cysteine-rich sequence motif. Cell. 1991 Feb 8;64(3):483–484. doi: 10.1016/0092-8674(91)90229-r. [DOI] [PubMed] [Google Scholar]
  21. Froehner S. C. Expression of RNA transcripts for the postsynaptic 43 kDa protein in innervated and denervated rat skeletal muscle. FEBS Lett. 1989 Jun 5;249(2):229–233. doi: 10.1016/0014-5793(89)80629-5. [DOI] [PubMed] [Google Scholar]
  22. Froehner S. C., Gulbrandsen V., Hyman C., Jeng A. Y., Neubig R. R., Cohen J. B. Immunofluorescence localization at the mammalian neuromuscular junction of the Mr 43,000 protein of Torpedo postsynaptic membranes. Proc Natl Acad Sci U S A. 1981 Aug;78(8):5230–5234. doi: 10.1073/pnas.78.8.5230. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Froehner S. C., Luetje C. W., Scotland P. B., Patrick J. The postsynaptic 43K protein clusters muscle nicotinic acetylcholine receptors in Xenopus oocytes. Neuron. 1990 Oct;5(4):403–410. doi: 10.1016/0896-6273(90)90079-u. [DOI] [PubMed] [Google Scholar]
  24. Froehner S. C., Murnane A. A., Tobler M., Peng H. B., Sealock R. A postsynaptic Mr 58,000 (58K) protein concentrated at acetylcholine receptor-rich sites in Torpedo electroplaques and skeletal muscle. J Cell Biol. 1987 Jun;104(6):1633–1646. doi: 10.1083/jcb.104.6.1633. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Froehner S. C. Peripheral proteins of postsynaptic membranes from Torpedo electric organ identified with monoclonal antibodies. J Cell Biol. 1984 Jul;99(1 Pt 1):88–96. doi: 10.1083/jcb.99.1.88. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Froehner S. C. The submembrane machinery for nicotinic acetylcholine receptor clustering. J Cell Biol. 1991 Jul;114(1):1–7. doi: 10.1083/jcb.114.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Ghosh S., Baltimore D. Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 1990 Apr 12;344(6267):678–682. doi: 10.1038/344678a0. [DOI] [PubMed] [Google Scholar]
  28. Gysin R., Yost B., Flanagan S. D. Immunochemical and molecular differentiation of 43 000 molecular weight proteins associated with Torpedo neuroelectrocyte synapses. Biochemistry. 1983 Dec 6;22(25):5781–5789. doi: 10.1021/bi00294a016. [DOI] [PubMed] [Google Scholar]
  29. Hunt T. Cytoplasmic anchoring proteins and the control of nuclear localization. Cell. 1989 Dec 22;59(6):949–951. doi: 10.1016/0092-8674(89)90747-2. [DOI] [PubMed] [Google Scholar]
  30. Johnson G. D., Nogueira Araujo G. M. A simple method of reducing the fading of immunofluorescence during microscopy. J Immunol Methods. 1981;43(3):349–350. doi: 10.1016/0022-1759(81)90183-6. [DOI] [PubMed] [Google Scholar]
  31. Kaplan J. M., Mardon G., Bishop J. M., Varmus H. E. The first seven amino acids encoded by the v-src oncogene act as a myristylation signal: lysine 7 is a critical determinant. Mol Cell Biol. 1988 Jun;8(6):2435–2441. doi: 10.1128/mcb.8.6.2435. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Kaplan J. M., Varmus H. E., Bishop J. M. The src protein contains multiple domains for specific attachment to membranes. Mol Cell Biol. 1990 Mar;10(3):1000–1009. doi: 10.1128/mcb.10.3.1000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Klarsfeld A., Bessereau J. L., Salmon A. M., Triller A., Babinet C., Changeux J. P. An acetylcholine receptor alpha-subunit promoter conferring preferential synaptic expression in muscle of transgenic mice. EMBO J. 1991 Mar;10(3):625–632. doi: 10.1002/j.1460-2075.1991.tb07990.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Kouzarides T., Ziff E. The role of the leucine zipper in the fos-jun interaction. Nature. 1988 Dec 15;336(6200):646–651. doi: 10.1038/336646a0. [DOI] [PubMed] [Google Scholar]
  35. LaRochelle W. J., Froehner S. C. Comparison of the postsynaptic 43-kDa protein from muscle cells that differ in acetylcholine receptor clustering activity. J Biol Chem. 1987 Jun 15;262(17):8190–8195. [PubMed] [Google Scholar]
  36. LaRochelle W. J., Ralston E., Forsayeth J. R., Froehner S. C., Hall Z. W. Clusters of 43-kDa protein are absent from genetic variants of C2 muscle cells with reduced acetylcholine receptor expression. Dev Biol. 1989 Mar;132(1):130–138. doi: 10.1016/0012-1606(89)90211-x. [DOI] [PubMed] [Google Scholar]
  37. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  38. Landschulz W. H., Johnson P. F., McKnight S. L. The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science. 1988 Jun 24;240(4860):1759–1764. doi: 10.1126/science.3289117. [DOI] [PubMed] [Google Scholar]
  39. Lo M. M., Garland P. B., Lamprecht J., Barnard E. A. Rotational mobility of the membrane-bound acetylcholine receptor of Torpedo electric organ measured by phosphorescence depolarisation. FEBS Lett. 1980 Mar 10;111(2):407–412. doi: 10.1016/0014-5793(80)80838-6. [DOI] [PubMed] [Google Scholar]
  40. Moscovici C., Moscovici M. G., Jimenez H., Lai M. M., Hayman M. J., Vogt P. K. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail. Cell. 1977 May;11(1):95–103. doi: 10.1016/0092-8674(77)90320-8. [DOI] [PubMed] [Google Scholar]
  41. Musil L. S., Carr C., Cohen J. B., Merlie J. P. Acetylcholine receptor-associated 43K protein contains covalently bound myristate. J Cell Biol. 1988 Sep;107(3):1113–1121. doi: 10.1083/jcb.107.3.1113. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Musil L. S., Frail D. E., Merlie J. P. The mammalian 43-kD acetylcholine receptor-associated protein (RAPsyn) is expressed in some nonmuscle cells. J Cell Biol. 1989 May;108(5):1833–1840. doi: 10.1083/jcb.108.5.1833. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Neubig R. R., Krodel E. K., Boyd N. D., Cohen J. B. Acetylcholine and local anesthetic binding to Torpedo nicotinic postsynaptic membranes after removal of nonreceptor peptides. Proc Natl Acad Sci U S A. 1979 Feb;76(2):690–694. doi: 10.1073/pnas.76.2.690. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Nghiêm H. O., Cartaud J., Dubreuil C., Kordeli C., Buttin G., Changeux J. P. Production and characterization of a monoclonal antibody directed against the 43,000-dalton v1 polypeptide from Torpedo marmorata electric organ. Proc Natl Acad Sci U S A. 1983 Oct;80(20):6403–6407. doi: 10.1073/pnas.80.20.6403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Ono Y., Fujii T., Igarashi K., Kuno T., Tanaka C., Kikkawa U., Nishizuka Y. Phorbol ester binding to protein kinase C requires a cysteine-rich zinc-finger-like sequence. Proc Natl Acad Sci U S A. 1989 Jul;86(13):4868–4871. doi: 10.1073/pnas.86.13.4868. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Pan T., Giedroc D. P., Coleman J. E. 1H NMR studies of T4 gene 32 protein: effects of zinc removal and reconstitution. Biochemistry. 1989 Oct 31;28(22):8828–8832. doi: 10.1021/bi00448a022. [DOI] [PubMed] [Google Scholar]
  47. Pellman D., Garber E. A., Cross F. R., Hanafusa H. An N-terminal peptide from p60src can direct myristylation and plasma membrane localization when fused to heterologous proteins. 1985 Mar 28-Apr 3Nature. 314(6009):374–377. doi: 10.1038/314374a0. [DOI] [PubMed] [Google Scholar]
  48. Pellman D., Garber E. A., Cross F. R., Hanafusa H. Fine structural mapping of a critical NH2-terminal region of p60src. Proc Natl Acad Sci U S A. 1985 Mar;82(6):1623–1627. doi: 10.1073/pnas.82.6.1623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Peng H. B., Froehner S. C. Association of the postsynaptic 43K protein with newly formed acetylcholine receptor clusters in cultured muscle cells. J Cell Biol. 1985 May;100(5):1698–1705. doi: 10.1083/jcb.100.5.1698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Phillips W. D., Kopta C., Blount P., Gardner P. D., Steinbach J. H., Merlie J. P. ACh receptor-rich membrane domains organized in fibroblasts by recombinant 43-kildalton protein. Science. 1991 Feb 1;251(4993):568–570. doi: 10.1126/science.1703661. [DOI] [PubMed] [Google Scholar]
  51. Porter S., Froehner S. C. Characterization and localization of the Mr = 43,000 proteins associated with acetylcholine receptor-rich membranes. J Biol Chem. 1983 Aug 25;258(16):10034–10040. [PubMed] [Google Scholar]
  52. Porter S., Froehner S. C. Interaction of the 43K protein with components of Torpedo postsynaptic membranes. Biochemistry. 1985 Jan 15;24(2):425–432. doi: 10.1021/bi00323a028. [DOI] [PubMed] [Google Scholar]
  53. Rasmussen R., Benvegnu D., O'Shea E. K., Kim P. S., Alber T. X-ray scattering indicates that the leucine zipper is a coiled coil. Proc Natl Acad Sci U S A. 1991 Jan 15;88(2):561–564. doi: 10.1073/pnas.88.2.561. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Rein A., McClure M. R., Rice N. R., Luftig R. B., Schultz A. M. Myristylation site in Pr65gag is essential for virus particle formation by Moloney murine leukemia virus. Proc Natl Acad Sci U S A. 1986 Oct;83(19):7246–7250. doi: 10.1073/pnas.83.19.7246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Resh M. D., Erikson R. L. Highly specific antibody to Rous sarcoma virus src gene product recognizes a novel population of pp60v-src and pp60c-src molecules. J Cell Biol. 1985 Feb;100(2):409–417. doi: 10.1083/jcb.100.2.409. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Resh M. D., Ling H. P. Identification of a 32K plasma membrane protein that binds to the myristylated amino-terminal sequence of p60v-src. Nature. 1990 Jul 5;346(6279):84–86. doi: 10.1038/346084a0. [DOI] [PubMed] [Google Scholar]
  57. Resh M. D. Specific and saturable binding of pp60v-src to plasma membranes: evidence for a myristyl-src receptor. Cell. 1989 Jul 28;58(2):281–286. doi: 10.1016/0092-8674(89)90842-8. [DOI] [PubMed] [Google Scholar]
  58. Rhee S. S., Hunter E. Myristylation is required for intracellular transport but not for assembly of D-type retrovirus capsids. J Virol. 1987 Apr;61(4):1045–1053. doi: 10.1128/jvi.61.4.1045-1053.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Rochlin M. W., Peng H. B. Localization of intracellular proteins at acetylcholine receptor clusters induced by electric fields in Xenopus muscle cells. J Cell Sci. 1989 Sep;94(Pt 1):73–83. doi: 10.1242/jcs.94.1.73. [DOI] [PubMed] [Google Scholar]
  60. Rosenberg A. H., Lade B. N., Chui D. S., Lin S. W., Dunn J. J., Studier F. W. Vectors for selective expression of cloned DNAs by T7 RNA polymerase. Gene. 1987;56(1):125–135. doi: 10.1016/0378-1119(87)90165-x. [DOI] [PubMed] [Google Scholar]
  61. Rousselet A., Cartaud J., Devaux P. F., Changeux J. P. The rotational diffusion of the acetylcholine receptor in Torpeda marmorata membrane fragments studied with a spin-labelled alpha-toxin: importance of the 43 000 protein(s). EMBO J. 1982;1(4):439–445. doi: 10.1002/j.1460-2075.1982.tb01188.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Schuermann M., Neuberg M., Hunter J. B., Jenuwein T., Ryseck R. P., Bravo R., Müller R. The leucine repeat motif in Fos protein mediates complex formation with Jun/AP-1 and is required for transformation. Cell. 1989 Feb 10;56(3):507–516. doi: 10.1016/0092-8674(89)90253-5. [DOI] [PubMed] [Google Scholar]
  63. Sealock R., Wray B. E., Froehner S. C. Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies. J Cell Biol. 1984 Jun;98(6):2239–2244. doi: 10.1083/jcb.98.6.2239. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sobel A., Heidmann T., Hofler J., Changeux J. P. Distinct protein components from Torpedo marmorata membranes carry the acetylcholine receptor site and the binding site for local anesthetics and histrionicotoxin. Proc Natl Acad Sci U S A. 1978 Jan;75(1):510–514. doi: 10.1073/pnas.75.1.510. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Spiegel A. M., Simonds W. F., Jones T. L., Goldsmith P. K., Unson C. G. Antibodies as probes of G-protein receptor-effector coupling and of G-protein membrane attachment. Biochem Soc Symp. 1990;56:61–69. [PubMed] [Google Scholar]
  66. St John P. A., Froehner S. C., Goodenough D. A., Cohen J. B. Nicotinic postsynaptic membranes from Torpedo: sidedness, permeability to macromolecules, and topography of major polypeptides. J Cell Biol. 1982 Feb;92(2):333–342. doi: 10.1083/jcb.92.2.333. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Towler D. A., Eubanks S. R., Towery D. S., Adams S. P., Glaser L. Amino-terminal processing of proteins by N-myristoylation. Substrate specificity of N-myristoyl transferase. J Biol Chem. 1987 Jan 25;262(3):1030–1036. [PubMed] [Google Scholar]
  68. Towler D. A., Gordon J. I., Adams S. P., Glaser L. The biology and enzymology of eukaryotic protein acylation. Annu Rev Biochem. 1988;57:69–99. doi: 10.1146/annurev.bi.57.070188.000441. [DOI] [PubMed] [Google Scholar]
  69. Tsui H. C., Cohen J. B., Fischbach G. D. Variation in the ratio of acetylcholine receptors and the Mr 43,000 receptor-associated protein in embryonic chick myotubes and myoblasts. Dev Biol. 1990 Aug;140(2):437–446. doi: 10.1016/0012-1606(90)90092-w. [DOI] [PubMed] [Google Scholar]
  70. Tzartos S. J., Lindstrom J. M. Monoclonal antibodies used to probe acetylcholine receptor structure: localization of the main immunogenic region and detection of similarities between subunits. Proc Natl Acad Sci U S A. 1980 Feb;77(2):755–759. doi: 10.1073/pnas.77.2.755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Wallace B. G. Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus. J Neurosci. 1989 Apr;9(4):1294–1302. doi: 10.1523/JNEUROSCI.09-04-01294.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Wennogle L. P., Changeux J. P. Transmembrane orientation of proteins present in acetylcholine receptor-rich membranes from Torpedo marmorata studied by selective proteolysis. Eur J Biochem. 1980 May;106(2):381–393. doi: 10.1111/j.1432-1033.1980.tb04584.x. [DOI] [PubMed] [Google Scholar]
  73. Woodruff M. L., Theriot J., Burden S. J. 300-kD subsynaptic protein copurifies with acetylcholine receptor-rich membranes and is concentrated at neuromuscular synapses. J Cell Biol. 1987 Apr;104(4):939–946. doi: 10.1083/jcb.104.4.939. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES