Protein quality control at the plasma membrane

Current Opinion in Cell Biology

Volumn 23, Issue 4, 2011, Pages 483-491

  Okiyoneda, Tsukasa ^a   Apaja, Pirjo M ^a   Lukacs, Gergely L ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN;

CELL MEMBRANE; CELL SURFACE; ENDOPLASMIC RETICULUM; LYSOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN HOMEOSTASIS; REVIEW; UBIQUITINATION;

ANIMALS; CELL MEMBRANE; ENDOPLASMIC RETICULUM; HUMANS; LYSOSOMES; MAMMALS; MEMBRANE PROTEINS; PROTEIN TRANSPORT; UBIQUITINATION; YEASTS;

EID: 79960709233     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2011.04.012     Document Type: Review

References (73)

1. Ellgaard L., Helenius A. Quality control in the endoplasmic reticulum. Nat Rev Mol Cell Biol 2003, 4:181-191.
2. Arvan P., Zhao X., Ramos-Castaneda J., Chang A. Secretory pathway quality control operating in Golgi, plasmalemmal, and endosomal systems. Traffic 2002, 3:771-780.
3. Powers E.T., Morimoto R.I., Dillin A., Kelly J.W., Balch W.E. Biological and chemical approaches to diseases of proteostasis deficiency. Annu Rev Biochem 2009, 78:959-991.
4. Young J.C., Agashe V.R., Siegers K., Hartl F.U. Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 2004, 5:781-791.
5. Vembar S.S., Brodsky J.L. One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 2008, 9:944-957.
6. Raiborg C., Stenmark H. The ESCRT machinery in endosomal sorting of ubiquitylated membrane proteins. Nature 2009, 458:445-452.
7. Gong X., Chang A. A mutant plasma membrane ATPase, Pma1-10, is defective in stability at the yeast cell surface. Proc Natl Acad Sci USA 2001, 98:9104-9109.
8. Li Y., Kane T., Tipper C., Spatrick P., Jenness D.D. Yeast mutants affecting possible quality control of plasma membrane proteins. Mol Cell Biol 1999, 19:3588-3599.
9. Lauwers E., Grossmann G., Andre B. Evidence for coupled biogenesis of yeast Gap1 permease and sphingolipids: essential role in transport activity and normal control by ubiquitination. Mol Biol Cell 2007, 18:3068-3080.
10. Benharouga M., Haardt M., Kartner N., Lukacs G.L. COOH-terminal truncations promote proteasome-dependent degradation of mature cystic fibrosis transmembrane conductance regulator from post-Golgi compartments. J Cell Biol 2001, 153:957-970.
11. Fayadat L., Kopito R.R. Recognition of a single transmembrane degron by sequential quality control checkpoints. Mol Biol Cell 2003, 14:1268-1278.
12. Ljunggren H.G., Stam N.J., Ohlen C., Neefjes J.J., Hoglund P., Heemels M.T., Bastin J., Schumacher T.N., Townsend A., Karre K., et al. Empty MHC class I molecules come out in the cold. Nature 1990, 346:476-480.
13. Sharma M., Benharouga M., Hu W., Lukacs G.L. Conformational and temperature-sensitive stability defects of the delta F508 cystic fibrosis transmembrane conductance regulator in post-endoplasmic reticulum compartments. J Biol Chem 2001, 276:8942-8950.
14. Wilson M.H., Highfield H.A., Limbird L.E. The role of a conserved inter-transmembrane domain interface in regulating alpha(2a)-adrenergic receptor conformational stability and cell-surface turnover. Mol Pharmacol 2001, 59:929-938.
15. Zaliauskiene L., Kang S., Brouillette C.G., Lebowitz J., Arani R.B., Collawn J.F. Down-regulation of cell surface receptors is modulated by polar residues within the transmembrane domain. Mol Biol Cell 2000, 11:2643-2655.
16. Schaheen B., Dang H., Fares H. Derlin-dependent accumulation of integral membrane proteins at cell surfaces. J Cell Sci 2009, 122(Pt 13):2228-2239.
17. Lukacs G.L., Chang X.B., Bear C., Kartner N., Mohamed A., Riordan J.R., Grinstein S. The delta F508 mutation decreases the stability of cystic fibrosis transmembrane conductance regulator in the plasma membrane. Determination of functional half-lives on transfected cells. J Biol Chem 1993, 268:21592-21598.
18. Vagin O., Turdikulova S., Sachs G. The H,K-ATPase beta subunit as a model to study the role of N-glycosylation in membrane trafficking and apical sorting. J Biol Chem 2004, 279:39026-39034.
19. Li J.-G., Chen C., Liu-Chen L.-Y. N-glycosylation of the human κ opioid receptor enhances its stability but slows its trafficking along the biosynthesis pathway†. Biochemistry 2007, 46:10960-10970.
20. Markkanen P.M.H., Petäjä-Repo U.E. N-glycan-mediated quality control in the endoplasmic reticulum is required for the expression of correctly folded δ-opioid receptors at the cell surface. J Biol Chem 2008, 283:29086-29098.
21. Watanabe I., Zhu J., Recio-Pinto E., Thornhill W.B. Glycosylation affects the protein stability and cell surface expression of Kv1.4 but not Kv1.1 potassium channels. J Biol Chem 2004, 279:8879-8885.
22. Glozman R., Okiyoneda T., Mulvihill C.M., Rini J.M., Barriere H., Lukacs G.L. N-glycans are direct determinants of CFTR folding and stability in secretory and endocytic membrane traffic. J Cell Biol 2009, 184:847-862.
23. Lederkremer G.Z. Glycoprotein folding, quality control and ER-associated degradation. Curr Opin Struct Biol 2009, 19:515-523.
24. Hanson S.R., Culyba E.K., Hsu T.L., Wong C.H., Kelly J.W., Powers E.T. The core trisaccharide of an N-linked glycoprotein intrinsically accelerates folding and enhances stability. Proc Natl Acad Sci USA 2009, 106:3131-3136.
25. Rotin D., Staub O. Role of the ubiquitin system in regulating ion transport. Pflugers Arch 2010, 461:1-21.
26. Lin C.H., MacGurn J.A., Chu T., Stefan C.J., Emr S.D. Arrestin-related ubiquitin-ligase adaptors regulate endocytosis and protein turnover at the cell surface. Cell 2008, 135:714-725.
27. Sharma M., Pampinella F., Nemes C., Benharouga M., So J., Du K., Bache K.G., Papsin B., Zerangue N., Stenmark H., Lukacs G.L. Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J Cell Biol 2004, 164:923-933.
28. Apaja P.M., Xu H., Lukacs G.L. Quality control for unfolded proteins at the plasma membrane. J Cell Biol 2010, 191:553-570.
29. Wang Q., Chang A. Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1. Proc Natl Acad Sci USA 2002, 99:12853-12858.
30. Shearer A.G., Hampton R.Y. Lipid-mediated, reversible misfolding of a sterol-sensing domain protein. EMBO J 2005, 24:149-159.
31. Traub L.M., Lukacs G.L. Decoding ubiquitin sorting signals for clathrin-dependent endocytosis by CLASPs. J Cell Sci 2007, 120(Pt 4):543-553.
32. Ehrlich E.S., Wang T., Luo K., Xiao Z., Niewiadomska A.M., Martinez T., Xu W., Neckers L., Yu X.F. Regulation of Hsp90 client proteins by a Cullin5-RING E3 ubiquitin ligase. Proc Natl Acad Sci USA 2009, 106:20330-20335.
33. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat Rev Mol Cell Biol 2010, 11:515-528.
34. Trepel J., Mollapour M., Giaccone G., Neckers L. Targeting the dynamic HSP90 complex in cancer. Nat Rev Cancer 2010, 10:537-549.
35. Roxrud I., Raiborg C., Gilfillan G.D., Stromme P., Stenmark H. Dual degradation mechanisms ensure disposal of NHE6 mutant protein associated with neurological disease. Exp Cell Res 2009, 315:3014-3027.
36. Hayashi H., Sugiyama Y. Short-chain ubiquitination is associated with the degradation rate of a cell-surface-resident bile salt export pump (BSEP/ABCB11). Mol Pharmacol 2009, 75:143-150.
37. Guo J., Massaeli H., Xu J., Jia Z., Wigle J.T., Mesaeli N., Zhang S. Extracellular K+ concentration controls cell surface density of IKr in rabbit hearts and of the HERG channel in human cell lines. J Clin Invest 2009, 119:2745-2757.
38. Xu P., Duong D.M., Seyfried N.T., Cheng D., Xie Y., Robert J., Rush J., Hochstrasser M., Finley D., Peng J. Quantitative proteomics reveals the function of unconventional ubiquitin chains in proteasomal degradation. Cell 2009, 137:133-145.
39. Boname J.M., Thomas M., Stagg H.R., Xu P., Peng J., Lehner P.J. Efficient internalization of MHC I requires lysine-11 and lysine-63 mixed linkage polyubiquitin chains. Traffic 2009.
40. Zhang M., Windheim M., Roe S.M., Peggie M., Cohen P., Prodromou C., Pearl L.H. Chaperoned ubiquitylation - crystal structures of the CHIP U box E3 ubiquitin ligase and a CHIP-Ubc13-Uev1a complex. Mol Cell 2005, 20:525-538.
41. Meacham G.C., Patterson C., Zhang W., Younger J.M., Cyr D.M. The Hsc70 co-chaperone CHIP targets immature CFTR for proteasomal degradation. Nat Cell Biol 2001, 3:100-105.
42. Heck J.W., Cheung S.K., Hampton R.Y. Cytoplasmic protein quality control degradation mediated by parallel actions of the E3 ubiquitin ligases Ubr1 and San1. Proc Natl Acad Sci USA 2010, 107:1106-1111.
43. Rosser M.F., Washburn E., Muchowski P.J., Patterson C., Cyr D.M. Chaperone functions of the E3 ubiquitin ligase CHIP. J Biol Chem 2007, 282:22267-22277.
44. Okiyoneda T., Barriere H., Bagdany M., Rabeh W.M., Du K., Hohfeld J., Young J.C., Lukacs G.L. Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 2010, 329:805-810.
45. Kundrat L., Regan L. Balance between folding and degradation for Hsp90-dependent client proteins: a key role for CHIP. Biochemistry 2010, 49:7428-7438.
46. Stankiewicz M., Nikolay R., Rybin V., Mayer M.P. CHIP participates in protein triage decisions by preferentially ubiquitinating Hsp70-bound substrates. FEBS J 2010, 277:3353-3367.
47. Younger J.M., Ren H.Y., Chen L., Fan C.Y., Fields A., Patterson C., Cyr D.M. A foldable CFTR{Delta}F508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase. J Cell Biol 2004, 167:1075-1085.
48. Koulov A.V., Lapointe P., Lu B., Razvi A., Coppinger J., Dong M.Q., Matteson J., Laister R., Arrowsmith C., Yates J.R., Balch W.E. Biological and structural basis for Aha1 regulation of Hsp90 ATPase activity in maintaining proteostasis in the human disease cystic fibrosis. Mol Biol Cell 2010, 21:871-884.
49. Wang X., Venable J., LaPointe P., Hutt D.M., Koulov A.V., Coppinger J., Gurkan C., Kellner W., Matteson J., Plutner H., et al. Hsp90 cochaperone Aha1 downregulation rescues misfolding of CFTR in cystic fibrosis. Cell 2006, 127:803-815.
50. Marozkina N.V., Yemen S., Borowitz M., Liu L., Plapp M., Sun F., Islam R., Erdmann-Gilmore P., Townsend R.R., Lichti C.F., et al. Hsp 70/Hsp 90 organizing protein as a nitrosylation target in cystic fibrosis therapy. Proc Natl Acad Sci USA 2010, 107:11393-11398.
51. Westhoff B., Chapple J.P., van der Spuy J., Hohfeld J., Cheetham M.E. HSJ1 is a neuronal shuttling factor for the sorting of chaperone clients to the proteasome. Curr Biol 2005, 15:1058-1064.
52. Liu Y., Chang A. Quality control of a mutant plasma membrane ATPase: ubiquitylation prevents cell-surface stability. J Cell Sci 2006, 119(Pt 2):360-369.
53. Bomberger J.M., Barnaby R.L., Stanton B.A. The deubiquitinating enzyme USP10 regulates the post-endocytic sorting of cystic fibrosis transmembrane conductance regulator in airway epithelial cells. J Biol Chem 2009, 284:18778-18789.
54. Mishra A., Godavarthi S.K., Maheshwari M., Goswami A., Jana N.R. The ubiquitin ligase E6-AP is induced and recruited to aggresomes in response to proteasome inhibition and may be involved in the ubiquitination of Hsp70-bound misfolded proteins. J Biol Chem 2009, 284:10537-10545.
55. Sato B.K., Schulz D., Do P.H., Hampton R.Y. Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol Cell 2009, 34:212-222.
56. Rosenbaum J.C., Fredrickson E.K., Oeser M.L., Garrett-Engele C.M., Locke M.N., Richardson L.A., Nelson Z.W., Hetrick E.D., Milac T.I., Gottschling D.E., Gardner R.G. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol Cell 2011, 41:93-106.
57. Hirsch C., Gauss R., Horn S.C., Neuber O., Sommer T. The ubiquitylation machinery of the endoplasmic reticulum. Nature 2009, 458:453-460.
58. Luders J., Demand J., Hohfeld J. The ubiquitin-related BAG-1 provides a link between the molecular chaperones Hsc70/Hsp70 and the proteasome. J Biol Chem 2000, 275:4613-4617.
59. Gurusamy N., Lekli I., Gherghiceanu M., Popescu L.M., Das D.K. BAG-1 induces autophagy for cardiac cell survival. Autophagy 2009, 5:120-121.
60. Orenstein S.J., Cuervo A.M. Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin Cell Dev Biol 2010, 21:719-726.
61. Finley D. Recognition and processing of ubiquitin-protein conjugates by the proteasome. Annu Rev Biochem 2009, 78:477-513.
62. Younger J.M., Chen L., Ren H.Y., Rosser M.F., Turnbull E.L., Fan C.Y., Patterson C., Cyr D.M. Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 2006, 126:571-582.
63. Morito D., Hirao K., Oda Y., Hosokawa N., Tokunaga F., Cyr D.M., Tanaka K., Iwai K., Nagata A.K. Gp78 cooperates with RMA1 in endoplasmic reticulum-associated degradation of CFTRDeltaF508. Mol Biol Cell 2008, 19:1328-1336.
64. Barriere H., Nemes C., Lechardeur D., Khan-Mohammad M., Fruh K., Lukacs G.L. Molecular basis of oligoubiquitin-dependent internalization of membrane proteins in mammalian cells. Traffic 2006, 7:282-297.
65. Lam P., Pearson C.L., Soroka C.J., Xu S., Mennone A., Boyer J.L. Levels of plasma membrane expression in progressive and benign mutations of the bile salt export pump (Bsep/Abcb11) correlate with severity of cholestatic diseases. Am J Physiol Cell Physiol 2007, 293:C1709-C1716.
66. Duarri A., Teijido O., Lopez-Hernandez T., Scheper G.C., Barriere H., Boor I., Aguado F., Zorzano A., Palacin M., Martinez A., et al. Molecular pathogenesis of megalencephalic leukoencephalopathy with subcortical cysts: mutations in MLC1 cause folding defects. Hum Mol Genet 2008, 17:3728-3739.
67. Robben J.H., Knoers N.V., Deen P.M. Characterization of vasopressin V2 receptor mutants in nephrogenic diabetes insipidus in a polarized cell model. Am J Physiol Renal Physiol 2005, 289:F265-272.
68. Fairbank M., St-Pierre P., Nabi I.R. The complex biology of autocrine motility factor/phosphoglucose isomerase (AMF/PGI) and its receptor, the gp78/AMFR E3 ubiquitin ligase. Mol Biosyst 2009, 5:793-801.
69. Edwards S.W., Limbird L.E. Role for the third intracellular loop in cell surface stabilization of the α2A-adrenergic receptor. J Biol Chem 1999, 274:16331-16336.
70. Asano T., Takata K., Katagiri H., Ishihara H., Inukai K., Anai M., Hirano H., Yazaki Y., Oka Y. The role of N-glycosylation in the targeting and stability of GLUT1 glucose transporter. FEBS Lett 1993, 324:258-261.
71. Shimamura T., Lowell A.M., Engelman J.A., Shapiro G.I. Epidermal growth factor receptors harboring kinase domain mutations associate with the heat shock protein 90 chaperone and are destabilized following exposure to geldanamycins. Cancer Res 2005, 65:6401-6408.
72. Marx C., Held J.M., Gibson B.W., Benz C.C. ErbB2 trafficking and degradation associated with K48 and K63 polyubiquitination. Cancer Res 2010, 70:3709-3717.
73. Wrighton K.H., Lin X., Feng X.H. Critical regulation of TGFbeta signaling by Hsp90. Proc Natl Acad Sci USA 2008, 105:9244-9249.