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PMID: 2277074 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Assembly intermediates of the mouse muscle nicotinic acetylcholine receptor in stably transfected fibroblasts.

The Journal of cell biology ·Vol. 111 ·No. 6 Pt 1 ·1990-12-00 ·Pages 2601-11

Blount P, Smith MM, Merlie JP

Abstract

We have used fibroblast clones expressing muscle nicotinic acetylcholine receptor alpha and gamma, and alpha and delta subunits to measure the kinetics of subunit assembly, and to study the properties of the partially assembled products that are formed. We demonstrate by coimmunoprecipitation that assembly intermediates in fibroblasts coexpressing alpha and delta subunits are formed in a time-dependent manner. The alpha and gamma- and the alpha and delta-producing transfected cells form complexes that, when labeled with 125I-alpha-bungarotoxin, migrate in sucrose gradients at 6.3S, a value consistent with a hetero-dimer structure. An additional peak at 8.5S is formed from the alpha and gamma subunits expressed in fibroblasts suggesting that gamma may have more than one binding site for alpha subunit. The stability and specificity of formation of these partially assembled complexes suggests that they are normal intermediates in the assembly of acetylcholine receptor. Comparison of the binding of 125I-alpha-bungarotoxin to intact and detergent-extracted fibroblasts indicate that essentially all of the binding sites are retained in an intracellular pool. The fibroblast delta subunit has the electrophoretic mobility in SDS-PAGE of a precursor that does not contain complex carbohydrates. In addition, alpha gamma and alpha delta complexes had lectin binding properties expected of subunits lacking complex oligosaccharides. Therefore, fibroblasts coexpressing alpha and gamma or alpha and delta subunits produce discrete assembly intermediates that are retained in an intracellular compartment and are not processed by Golgi enzymes.

MeSH Terms
Animals Bungarotoxins/metabolism Cell Line Fibroblasts/metabolism Kinetics Macromolecular Substances Molecular Weight Muscles/metabolism Protein Processing, Post-Translational Receptors, Nicotinic/genetics,isolation & purification,metabolism Transfection
Chemicals
Bungarotoxins Macromolecular Substances Receptors, Nicotinic
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Blount P
Department of Pharmacology, Washington University School of Medicine, St. Louis, Missouri 63110.
Smith M M
Merlie J P
References (49)
49 references, click to expand
  1. Cleavage of structural proteins during the assembly of the head of bacteriophage T4.
    Nature. 1970 Aug 15;227(5259):680-5 PMID: 5432063
  2. Purification of an acetylcholine receptor from a nonfusing muscle cell line.
    Biochemistry. 1977 Nov 1;16(22):4900-8 PMID: 911800
  3. Acetylcholine receptor subunits transit a precursor pool before acquiring alpha-bungarotoxin binding activity.
    J Biol Chem. 1981 Apr 25;256(8):3605-8 PMID: 7217046
  4. Restoration of 125I-alpha-bungarotoxin binding activity to the alpha subunit of Torpedo acetylcholine receptor isolated by gel electrophoresis in sodium dodecyl sulfate.
    J Biol Chem. 1981 Aug 25;256(16):8294-7 PMID: 7263653
  5. Mapping of surface structures of electrophorus acetylcholine receptor using monoclonal antibodies.
    J Biol Chem. 1981 Aug 25;256(16):8635-45 PMID: 6167581
  6. Relative locations of the beta and delta chains of the acetylcholine receptor determined by electron microscopy of isolated receptor trimer.
    J Biol Chem. 1981 Dec 25;256(24):12624-7 PMID: 7309725
  7. Structure and function of an acetylcholine receptor.
    Biophys J. 1982 Jan;37(1):371-83 PMID: 7055628
  8. Inhibition of glycosylation with tunicamycin blocks assembly of newly synthesized acetylcholine receptor subunits in muscle cells.
    J Biol Chem. 1982 Mar 10;257(5):2694-701 PMID: 7061443
  9. Swainsonine inhibits the biosynthesis of complex glycoproteins by inhibition of Golgi mannosidase II.
    J Biol Chem. 1982 Jul 25;257(14):7936-9 PMID: 6806288
  10. Direct structural localization of two toxin-recognition sites on an ACh receptor protein.
    Nature. 1982 Sep 2;299(5878):81-4 PMID: 7110329
  11. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins.
    J Biol Chem. 1982 Oct 10;257(19):11230-4 PMID: 7118880
  12. Structural homology of Torpedo californica acetylcholine receptor subunits.
    Nature. 1983 Apr 7;302(5908):528-32 PMID: 6188060
  13. The arrangement of the subunits of the acetylcholine receptor of Torpedo californica.
    J Biol Chem. 1983 Jun 10;258(11):6678-81 PMID: 6853498
  14. Monoclonal antibodies to cytoplasmic domains of the acetylcholine receptor.
    J Biol Chem. 1983 Jun 10;258(11):7112-20 PMID: 6189834
  15. Identification of homo-oligomers as potential intermediates in acetylcholine receptor subunit assembly.
    Proc Natl Acad Sci U S A. 1983 Jul;80(14):4359-63 PMID: 6224218
  16. Mapping the binding of monoclonal antibodies to the acetylcholine receptor from Torpedo californica.
    Biochemistry. 1983 Jul 5;22(14):3312-20 PMID: 6615777
  17. Assembly in vivo of mouse muscle acetylcholine receptor: identification of an alpha subunit species that may be an assembly intermediate.
    Cell. 1983 Oct;34(3):747-57 PMID: 6627392
  18. Expression of functional acetylcholine receptor from cloned cDNAs.
    Nature. 1984 Feb 16-22;307(5952):604-8 PMID: 6320016
  19. Image analysis of the heavy form of the acetylcholine receptor from Torpedo marmorata.
    J Mol Biol. 1984 Jun 25;176(2):205-37 PMID: 6748076
  20. Identification of the alpha subunit half-cystine specifically labeled by an affinity reagent for the acetylcholine receptor binding site.
    J Biol Chem. 1984 Oct 10;259(19):11662-5 PMID: 6480577
  21. An acetylcholine receptor precursor alpha subunit that binds alpha-bungarotoxin but not d-tubocurare.
    Proc Natl Acad Sci U S A. 1986 Jan;83(2):498-502 PMID: 3455784
  22. Isolation of a cDNA clone coding for a possible neural nicotinic acetylcholine receptor alpha-subunit.
    Nature. 1986 Jan 30-Feb 5;319(6052):368-74 PMID: 3753746
  23. Carbohydrate structures of acetylcholine receptor from Torpedo californica and distribution of oligosaccharides among the subunits.
    Eur J Biochem. 1986 Jun 2;157(2):233-42 PMID: 3709535
  24. Molecular distinction between fetal and adult forms of muscle acetylcholine receptor.
    Nature. 1986 May 22-28;321(6068):406-11 PMID: 2423878
  25. Location of antigenic determinants on primary sequences of subunits of nicotinic acetylcholine receptor by peptide mapping.
    Biochemistry. 1986 May 6;25(9):2621-32 PMID: 2424498
  26. Members of a nicotinic acetylcholine receptor gene family are expressed in different regions of the mammalian central nervous system.
    Cell. 1987 Mar 27;48(6):965-73 PMID: 3829125
  27. Formation of the alpha-bungarotoxin binding site and assembly of the nicotinic acetylcholine receptor subunits occur in the endoplasmic reticulum.
    J Biol Chem. 1987 Mar 25;262(9):4367-76 PMID: 3549731
  28. Functional properties of nicotinic acetylcholine receptor subunits expressed in various combinations.
    FEBS Lett. 1987 Apr 20;214(2):253-8 PMID: 2436944
  29. The strychnine-binding subunit of the glycine receptor shows homology with nicotinic acetylcholine receptors.
    Nature. 1987 Jul 16-22;328(6127):215-20 PMID: 3037383
  30. Sequence and functional expression of the GABA A receptor shows a ligand-gated receptor super-family.
    Nature. 1987 Jul 16-22;328(6127):221-7 PMID: 3037384
  31. Location of subunits within the acetylcholine receptor by electron image analysis of tubular crystals from Torpedo marmorata.
    J Cell Biol. 1987 Jul;105(1):9-18 PMID: 3611197
  32. Native folding of an acetylcholine receptor alpha subunit expressed in the absence of other receptor subunits.
    J Biol Chem. 1988 Jan 15;263(2):1072-80 PMID: 2826454
  33. Amino acids of the Torpedo marmorata acetylcholine receptor alpha subunit labeled by a photoaffinity ligand for the acetylcholine binding site.
    Biochemistry. 1988 Apr 5;27(7):2346-57 PMID: 3382627
  34. Degradation from the endoplasmic reticulum: disposing of newly synthesized proteins.
    Cell. 1988 Jul 15;54(2):209-20 PMID: 3292055
  35. Site-directed mutagenesis and single-channel currents define the ionic channel of the nicotinic acetylcholine receptor.
    Trends Neurosci. 1989 Apr;12(4):125-8 PMID: 2470168
  36. Assembly and N-glycosylation of all ACh receptor subunits are required for their efficient insertion into plasma membranes.
    Brain Res Mol Brain Res. 1989 May;5(3):183-92 PMID: 2725195
  37. Inhibitors of asparagine-linked oligosaccharide processing alter the kinetics of the nicotinic acetylcholine receptor.
    J Gen Physiol. 1989 May;93(5):765-83 PMID: 2525606
  38. Cloning by functional expression of a member of the glutamate receptor family.
    Nature. 1989 Dec 7;342(6250):643-8 PMID: 2480522
  39. Protein oligomerization in the endoplasmic reticulum.
    Annu Rev Cell Biol. 1989;5:277-307 PMID: 2688707
  40. A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum.
    Science. 1990 Jan 5;247(4938):79-82 PMID: 2294595
  41. Primary structure and expression of beta 2: a novel subunit of neuronal nicotinic acetylcholine receptors.
    Neuron. 1988 Mar;1(1):45-54 PMID: 3272154
  42. d-Tubocurarine binding sites are located at alpha-gamma and alpha-delta subunit interfaces of the nicotinic acetylcholine receptor.
    Proc Natl Acad Sci U S A. 1990 Apr;87(7):2785-9 PMID: 2320589
  43. Molecular basis of the two nonequivalent ligand binding sites of the muscle nicotinic acetylcholine receptor.
    Neuron. 1989 Sep;3(3):349-57 PMID: 2642001
  44. Mutational analysis of muscle nicotinic acetylcholine receptor subunit assembly.
    J Cell Biol. 1990 Dec;111(6 Pt 1):2613-22 PMID: 2277075
  45. Architectural editing: determining the fate of newly synthesized membrane proteins.
    New Biol. 1989 Oct;1(1):3-8 PMID: 2488271
  46. Quantitative film detection of 3H and 14C in polyacrylamide gels by fluorography.
    Eur J Biochem. 1975 Aug 15;56(2):335-41 PMID: 1175627
  47. Acetylcholine receptor metabolism in a nonfusing muscle cell line.
    J Biol Chem. 1977 Mar 25;252(6):2143-53 PMID: 845167
  48. Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail.
    Cell. 1977 May;11(1):95-103 PMID: 194709
  49. The lectins: carbohydrate-binding proteins of plants and animals.
    Adv Carbohydr Chem Biochem. 1978;35:127-340 PMID: 356549
Article Info
Journal
The Journal of cell biology
Abbr.
J Cell Biol
ISSN
0021-9525
Published
1990-12-00
Pages
2601-11
Language
English
Region
United States
NLM ID
0375356
PMCID
PMC2116397
Subset
IM
Grants
NIGMS NIH HHS · 2 T32 GM 07805 · United States
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