Regulation of nicotinic receptor expression by the ubiquitin-proteasome system

EMBO Journal

Volumn 23, Issue 21, 2004, Pages 4156-4165

  Christianson, John C ^a,b   Green, William N ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

Acetylcholine receptor; Endoplasmic reticulum associated degradation; Ubiquitin proteasome system

Indexed keywords

ION CHANNEL; NICOTINIC RECEPTOR; PROTEASOME; PROTEASOME INHIBITOR; UBIQUITIN;

ANIMAL CELL; ARTICLE; AUTORADIOGRAPHY; BIOGENESIS; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; MOUSE; MYOTUBE; NERVE CELL PLASTICITY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN PROCESSING; SOLUBILIZATION; UBIQUITINATION; WESTERN BLOTTING;

ACETYLCYSTEINE; ANIMALS; BUNGAROTOXINS; CELL LINE; CYSTEINE PROTEINASE INHIBITORS; ENDOPLASMIC RETICULUM; MICE; MUSCLE FIBERS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SUBUNITS; PROTEIN TRANSPORT; RADIOLIGAND ASSAY; RECEPTORS, NICOTINIC; UBIQUITIN;

ANIMALIA;

EID: 9144229330     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600436     Document Type: Article

References (73)

1. Beattie EC, Carroll RC, Yu X, Morishita W, Yasuda H, von Zastrow M, Malenka RC (2000) Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nat Neurosci 3: 1291-1300
2. Bèuttner C, Sadtler S, Leyendecker A, Laube B, Griffon N, Betz H, Schmalzing G (2001) Ubiquitination precedes internalization and proteolytic cleavage of plasma membrane-bound glycine receptors. J Biol Chem 276: 42978-42985
3. Blount P, Merlie JP (1988) Native folding of an acetylcholine receptor alpha subunit expressed in the absence of other receptor subunits. J Biol Chem 263: 1072-1080
4. Blount P, Merlie JP (1990) Mutational analysis of muscle nicotinic acetylcholine receptor subunit assembly. J Cell Biol 111: 2613-2622
5. Bonifacino JS, Cosson P, Shah N, Klausner RD (1991) Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum. EMBO J 10: 2783-2793
6. Bonifacino JS, Weissman AM (1998) Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev Cell Dev Biol 14: 19-57
7. Brodsky JL, McCracken AA (1999) ER protein quality control and proteasome-mediated protein degradation. Semin Cell Dev Biol 10: 507-513
8. Burbea M, Dreier L, Dittman JS, Grunwald ME, Kaplan JM (2002) Ubiquitin and AP180 regulate the abundance of GLR-1 glutamate receptors at postsynaptic elements in C. elegans. Neuron 35: 107-120
9. Cheng SH, Gregory RJ, Marshall J, Paul S, Souza DW, White GA, O'Riordan CR, Smith AE (1990) Defective intracellular transport and processing of CFTR is the molecular basis of most cystic fibrosis. Cell 63: 827-834
10. Ciechanover A, Schwartz AL (1998) The ubiquitin-proteasome pathway: the complexity and myriad functions of proteins death. Proc Natl Acad Sci USA 95: 2727-2730
11. Claudio T, Paulson HL, Green WN, Ross AF, Hartman DS, Hayden D (1989) Fibroblasts transfected with Torpedo acetylcholine receptor beta-, gamma-, and delta-subunit cDNAs express functional receptors when infected with a retroviral alpha recombinant. J Cell Biol 108: 2277-2290
12. de Virgilio M, Weninger H, Ivessa NE (1998) Ubiquitination is required for the retro-translocation of a short-lived luminal endoplasmic reticulum glycoprotein to the cytosol for degradation by the proteasome. J Biol Chem 273: 9734-9743
13. Denning GM, Anderson MP, Amara JF, Marshall J, Smith AE, Welsh MJ (1992) Processing of mutant cystic fibrosis transmembrane conductance regulator is temperature-sensitive. Nature 358: 761-764
14. Devreotes PN, Fambrough DM (1975) Acetylcholine receptor turnover in membranes of developing muscle fibers. J Cell Biol 65: 335-358
15. Eertmoed AL, Vallejo YF, Green WN (1998) Transient expression of heteromeric ion channels. Methods Enzymol 293: 564-585
16. Ehlers MD (2003) Activity level controls postsynaptic composition and signaling via the ubiquitin-proteasome system. Nat Neurosci 6: 231-242
17. Gardner RG, Hampton RY (1999) A 'distributed degron' allows regulated entry into the ER degradation pathway. EMBO J 18: 5994-6004
18. Gilon T, Chomsky O, Kulka RG (2000) Degradation signals recognized by the Ubc6p-Ubc7p ubiquitin-conjugating enzyme pair. Mol Cell Biol 20: 7214-7219
19. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 82: 373-428
20. A receptors composed of alpha1 and beta2 subunits in both cultured neurons and fibroblasts. J Neurosci 17: 6587-6596
21. Green WN (1999) Ion channel assembly: creating structures that function. J Gen Physiol 113: 163-170
22. Green WN, Claudio T (1993) Acetylcholine receptor assembly: subunit folding and oligomerization occur sequentially. Cell 74: 57-69
23. Green WN, Millar NS (1995) Ion-channel assembly. Trends Neurosci 18: 280-287
24. Green WN, Wanamaker CP (1998) Formation of the nicotinic acetylcholine receptor binding sites. J Neurosci 18: 5555-5564
25. Gu Y, Forsayeth JR, Verrall S, Yu XM, Hall ZW (1991) Assembly of the mammalian muscle acetylcholine receptor in transfected COS cells. J Cell Biol 114: 799-807
26. Hicke L (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2: 195-201
27. Horton AC, Ehlers MD (2003) Dual modes of endoplasmic reticulum-to-Golgi transport in dendrites revealed by live-cell imaging. J Neurosci 23: 6188-6199
28. Hyman C, Froehner SC (1983) Degradation of acetylcholine receptors in muscle cells: effect of leupeptin on turnover rate, intracellular pool sizes, and receptor properties. J Cell Biol 96: 1316-1324
29. Jensen TJ, Loo MA, Find S, Williams DB, Goldberg AL, Riordan JR (1995) Multiple proteolytic systems, including the proteasome, contribute to CFTR processing. Cell 83: 129-135
30. Johnson PR, Swanson R, Rakhilina L, Hochstrasser M (1998) Degradation signal masking by heterodimerization of MATalpha2 and MATa1 blocks their mutual destruction by the ubiquitin-proteasome pathway. Cell 94: 217-227
31. Johnston JA, Ward CL, Kopito RR (1998) Aggresomes: a cellular response to misfolded proteins. J Cell Biol 143: 1883-1898
32. Keller SH, Lindstrom J, Ellisman M, Taylor P (2001) Adjacent basic amino acid residues recognized by the COP I complex and ubiquitination govern endoplasmic reticulum to cell surface trafficking of the nicotinic acetylcholine receptor alpha-subunit. J Biol Chem 276: 18384-18391
33. Keller SH, Lindstrom J, Taylor P (1998) Inhibition of glucose trimming with castanospermine reduces calnexin association and promotes proteasome degradation of the alpha-subunit of the nicotinic acetylcholine receptor. J Biol Chem 273: 17064-17072
34. Keller SH, Taylor P (1999) Determinants responsible for assembly of the nicotinic acetylcholine receptor. J Gen Physiol 113: 171-176
35. Libby P, Bursztajn S, Goldberg AL (1980) Degradation of the acetylcholine receptor in cultured muscle cells: selective inhibitors and the fate of undegraded receptors. Cell 19: 481-491
36. Lindstrom JM (2000) Acetylcholine receptors and myasthenia. Muscle Nerve 23: 453-477
37. Malik B, Schlanger L, Al-Khalili O, Bao HF, Yue G, Price SR, Mitch WE, Eaton DC (2001) ENaC degradation in A6 cells by the ubiquitin-proteasome proteolytic pathway. J Biol Chem 276: 12903-12910
38. Malinow R, Malenka R (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126
39. Man HY, Lin JW, Ju WH, Ahmadian G, Liu L, Becker LE, Sheng M, Wang YT (2000) Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron 25: 649-662
40. Melman L, Geuze HJ, Li Y, McCormick LM, Van Kerkhof P, Strous GJ, Schwartz AL, Bu G (2002) Proteasome regulates the delivery of LDL receptor-related protein into the degradation pathway. Mol Biol Cell 13: 3325-3335
41. Merlie JP, Lindstrom J (1983) Assembly in vivo of mouse muscle acetylcholine receptor: identification of an alpha subunit species that may be an assembly intermediate. Cell 34: 747-757
42. Molinari M, Calanca V, Galli C, Lucca P, Paganetti P (2003) Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299: 1397-1400
43. Musil LS, Le AC, VanSlyke JK, Roberts LM (2000) Regulation of connexin degradation as a mechanism to increase, gap junction assembly and function. J Biol Chem 275: 25207-25215
44. Oda Y, Hosokawa N, Wada I, Nagata K (2003) EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299: 1394-1397
45. Petaja-Repo UE, Hogue M, Laperriere A, Bhalla S, Walker P, Bouvier M (2001) Newly synthesized human delta opioid receptors retained in the endoplasmic reticulum are retrotranslocated to the cytosol, deglycosylated, ubiquitinated, and degraded by the proteasome. J Biol Chem 276: 4416-4423
46. Plemper RK, Egner R, Kuchler K, Wolf DH (1998) Endoplasmic reticulum degradation of a mutated ATP-binding cassette transporter Pdr5 proceeds in a concerted action of Sec61 and the proteasome. J Biol Chem 273: 32848-32856
47. Rabinovich E (2001) AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Nature 414: 652-656
48. Rechsteiner M, Rogers SW (1996) PEST sequences and regulation by proteolysis. Trends Biochem Sci 21: 267-271
49. Ross AF, Green WN, Hartman DS, Claudio T (1991) Efficiency of acetylcholine receptor subunit assembly and its regulation by cAMP. J Cell Biol 113: 623-636
50. Sanes JR, Lichtman JW (2001) Induction, assembly, maturation and maintenance of a post-synaptic apparatus. Nat Rev Neurosci 2: 791-805
51. Schmidt JW, Catterall WA (1986) Biosynthesis and processing of the alpha subunit of the voltage-sensitive sodium channel in rat brain neurons. Cell 46: 437-444
52. Shamu CE, Story CM, Rapoport TA, Ploegh HL (1999) The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate. J Cell Biol 147: 45-58
53. Shenoy SK, McDonald PH, Kohout TA, Lefkowitz RJ (2001) Regulation of receptor fate by ubiquitination of activated beta 2-adrenergic receptor and beta-arrestin. Science 294: 1307-1313
54. Sine SM (1993) Molecular dissection of subunit interfaces in the acetylcholine receptor: identification of residues that determine curare selectivity. Proc Natl Acad Sci USA 90: 9436-9440
55. Speese SD, Trotta N, Rodesch CK, Aravamudan B, Broadie K (2003) The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr Biol 13: 899-910
56. + channel (ENaC) by ubiquitination. EMBO J 16: 6325-6336
57. Steinbach JH, Chen Q (1995) Antagonist and partial agonist actions of d-tubocurarine at mammalian muscle acetylcholine receptors. J Neurosci 15 (Part 1): 230-240
58. Sumikawa K, Miledi R (1989) Assembly and n-glycosylation of all ACh receptor subunits are required for their efficient insertion into plasma membranes. Mol Brain Res 5: 183-192
59. Tiwari S (2001) Endoplasmic reticulum (ER)-associated degradation of T cell receptor subunits. Involvement of ER-associated ubiquitin-conjugating enzymes (E2s). J Biol Chem 276: 16193-16200
60. Valentijn JA, Fyfe GK, Canessa CM (1998) Biosynthesis and processing of epithelial sodium channels in Xenopus oocytes. J Biol Chem 273: 30344-30351
61. van Kerkhof P, Govers R, Alves dos Santos CM, Strous GJ (2000) Endocytosis and degradation of the growth hormone receptor are proteasome-dependent. J Biol Chem 275: 1575-1580
62. VanSlyke JK, Deschenes SM, Musil LS (2000) Intracellular transport, assembly, and degradation of wild-type and disease-linked mutant gap junction proteins. Mol Biol Cell 11: 1933-1946
63. Wang JM, Zhang L, Yao Y, Viroonchatapan N, Rothe E, Wang ZZ (2002) A transmembrane motif governs the surface trafficking of nicotinic acetylcholine receptors. Nat Neurosci 5: 963-970
64. Wang YT, Linden DJ (2000) Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron 25: 635-647
65. Ward CL, Kopito RR (1994) Intracellular turnover of cystic fibrosis transmembrane conductance regulator. Inefficient processing and rapid degradation of wild-type and mutant proteins. J Biol Chem 269: 25710-25718
66. Ward CL, Omura S, Kopito RR (1995) Degradation of CFTR by the ubiquitin-proteasome pathway. Cell 83: 121-127
67. Wiertz EJ, Tortorella D, Bogyo M, Yu J, Mothes W, Jones TR, Rapoport TA, Ploegh HL (1996) Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384: 432-438
68. Xiong X, Chong E, Skach WR (1999) Evidence that endoplasmic reticulum (ER)-associated degradation of cystic flbrosis transmembrane conductance regulator is linked to retrograde translocation from the ER membrane. J Biol Chem 274: 2616-2624
69. Yang M, Omura S, Bonifacino JS, Weissman AM (1998) Novel aspects of degradation of T cell receptor subunits from the endoplasmic reticulum (ER) in T cells: importance of oligosaccharide processing, ubiquitination, and proteasome-dependent removal from ER membranes. J Exp Med 187: 835-846
70. Ye Y, Meyer HH, Rapoport TA (2003) Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J Cell Biol 162: 71-84
71. Yu A, Malek TR (2001) The proteasome regulates receptor-mediated endocytosis of interleukin-2. J Biol Chem 276: 381-385
72. Yu H, Kaung G, Kobayashi S, Kopito RR (1997) Cytosolic degradation of T-cell receptor alpha chains by the proteasome. J Biol Chem 272: 20800-20804
73. Zhao Y, Hegde AN, Martin KC (2003) The ubiquitin proteasome system functions as an inhibitory constraint on synaptic strengthening. Can Biol 13: 887-898