Garbage on, garbage off: New insights into plasma membrane protein quality control

Current Opinion in Cell Biology

Volumn 29, Issue 1, 2014, Pages 92-98

  MacGurn, Jason A ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANE PROTEIN; CHAPERONE;

CELL MEMBRANE; CELL SURFACE; CONTROL STRATEGY; ENDOCYTOSIS; HUMAN; NONHUMAN; PLASMA MEMBRANE PROTEIN QUALITY CONTROL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN QUALITY; PROTEIN TARGETING; QUALITY CONTROL; REVIEW; SIGNAL TRANSDUCTION; UBIQUITINATION; YEAST CELL;

ANIMALS; CELL MEMBRANE; HUMANS; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN TRANSPORT;

EID: 84901684419     PISSN: 09550674     EISSN: 18790410     Source Type: Journal    
DOI: 10.1016/j.ceb.2014.05.001     Document Type: Review

References (57)

1. Theodoraki M.A., Nillegoda N.B., Saini J., Caplan A.J. A network of ubiquitin ligases is important for the dynamics of misfolded protein aggregates in yeast. J Biol Chem 2012, 287:23911-23922.
2. Nillegoda N.B., Theodoraki M.A., Mandal A.K., Mayo K.J., Ren H.Y., Sultana R., Wu K., Johnson J., Cyr D.M., Caplan A.J. Ubr1 and Ubr2 function in a quality control pathway for degradation of unfolded cytosolic proteins. Mol Biol Cell 2010, 21:2102-2116.
3. Walter P., Ron D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 2011, 334:1081-1086.
4. Gardner B.M., Pincus D., Gotthardt K., Gallagher C.M., Walter P. Endoplasmic reticulum stress sensing in the unfolded protein response. Cold Spring Harb Perspect Biol 2013, 5:a013169.
5. Brodsky J.L. Cleaning up: ER-associated degradation to the rescue. Cell 2012, 151:1163-1167.
6. Thibault G., Ng D.T. The endoplasmic reticulum-associated degradation pathways of budding yeast. Cold Spring Harb Perspect Biol 2012, 4.
7. Hampton R.Y., Sommer T. Finding the will and the way of ERAD substrate retrotranslocation. Curr Opin Cell Biol 2012, 24:460-466.
8. Gardner R.G., Nelson Z.W., Gottschling D.E. Degradation-mediated protein quality control in the nucleus. Cell 2005, 120:803-815.
9. Rosenbaum J.C., Gardner R.G. How a disordered ubiquitin ligase maintains order in nuclear protein homeostasis. Nucleus 2011, 2:264-270.
10. Baker B.M., Haynes C.M. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem Sci 2011, 36:254-261.
11. Haynes C.M., Ron D. The mitochondrial UPR - protecting organelle protein homeostasis. J Cell Sci 2010, 123:3849-3855.
12. Macgurn J.A., Hsu P.C., Emr S.D. Ubiquitin and membrane protein turnover: from cradle to grave. Annu Rev Biochem 2012, 81:231-259.
13. Henne W.M., Buchkovich N.J., Emr S.D. The ESCRT pathway. Dev Cell 2011, 21:77-91.
14. Carvalho P., Goder V., Rapoport T.A. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 2006, 126:361-373.
15. Sharma M., Pampinella F., Nemes C., Benharouga M., So J., Du K., Bache K.G., Papsin B., Zerangue N., Stenmark H., et al. Misfolding diverts CFTR from recycling to degradation: quality control at early endosomes. J Cell Biol 2004, 164:923-933.
16. Jenness D.D., Li Y., Tipper C., Spatrick P. Elimination of defective alpha-factor pheromone receptors. Mol Cell Biol 1997, 17:6236-6245.
17. 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.
18. Okiyoneda T., Barrière H., Bagdány M., Rabeh W., Du K., Höhfeld J., Young J., Lukacs G. Peripheral protein quality control removes unfolded CFTR from the plasma membrane. Science 2010, 329:805-810.
19. Apaja P.M., Xu H., Lukacs G.L. Quality control for unfolded proteins at the plasma membrane. J Cell Biol 2010, 191:553-570.
20. 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.
21. Slotman J.A., da Silva Almeida A.C., Hassink G.C., van de Ven R.H., van Kerkhof P., Kuiken H.J., Strous G.J. Ubc13 and COOH terminus of Hsp70-interacting protein (CHIP) are required for growth hormone receptor endocytosis. J Biol Chem 2012, 287:15533-15543.
22. Apaja P.M., Foo B., Okiyoneda T., Valinsky W.C., Barriere H., Atanasiu R., Ficker E., Lukacs G.L., Shrier A. Ubiquitination-dependent quality control of hERG K+ channel with acquired and inherited conformational defect at the plasma membrane. Mol Biol Cell 2013, 24:3787-3804.
23. Matsumura Y., Sakai J., Skach W.R. Endoplasmic reticulum protein quality control is determined by cooperative interactions between Hsp/c70 protein and the CHIP E3 ligase. J Biol Chem 2013, 288:31069-31079.
24. Qian S.B., McDonough H., Boellmann F., Cyr D.M., Patterson C. CHIP-mediated stress recovery by sequential ubiquitination of substrates and Hsp70. Nature 2006, 440:551-555.
25. Cyr D.M., Höhfeld J., Patterson C. Protein quality control: U-box-containing E3 ubiquitin ligases join the fold. Trends Biochem Sci 2002, 27:368-375.
26. Shi Y., Wang J., Li J.D., Ren H., Guan W., He M., Yan W., Zhou Y., Hu Z., Zhang J., et al. Identification of CHIP as a novel causative gene for autosomal recessive cerebellar ataxia. PLoS ONE 2013, 8:e81884.
27. 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.
28. Nikko E., Pelham H.R.B. Arrestin-mediated endocytosis of yeast plasma membrane transporters. Traffic 2009, 10:1856-1867.
29. Nikko E., Sullivan J.A., Pelham H.R.B. Arrestin-like proteins mediate ubiquitination and endocytosis of the yeast metal transporter Smf1. EMBO Rep 2008, 9:1216-1221.
30. Zhao Y., MacGurn J.A., Liu M., Emr S. The ART-Rsp5 ubiquitin ligase network comprises a plasma membrane quality control system that protects yeast cells from proteotoxic stress. Elife 2013, 2:e00459.
31. Keener J.M., Babst M. Quality control and substrate-dependent downregulation of the nutrient transporter Fur4. Traffic 2013, 14:412-427.
32. Shimamura T., Weyand S., Beckstein O., Rutherford N.G., Hadden J.M., Sharples D., Sansom M.S., Iwata S., Henderson P.J., Cameron A.D. Molecular basis of alternating access membrane transport by the sodium-hydantoin transporter Mhp1. Science 2010, 328:470-473.
33. Weyand S., Shimamura T., Yajima S., Suzuki S., Mirza O., Krusong K., Carpenter E.P., Rutherford N.G., Hadden J.M., O'Reilly J., et al. Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 2008, 322:709-713.
34. Reyes N., Ginter C., Boudker O. Transport mechanism of a bacterial homologue of glutamate transporters. Nature 2009, 462:880-885.
35. 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., et al. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol Cell 2011, 41:93-106.
36. Fredrickson E.K., Rosenbaum J.C., Locke M.N., Milac T.I., Gardner R.G. Exposed hydrophobicity is a key determinant of nuclear quality control degradation. Mol Biol Cell 2011, 22:2384-2395.
37. Bardwell J.C., Jakob U. Conditional disorder in chaperone action. Trends Biochem Sci 2012, 37:517-525.
38. Reichmann D., Xu Y., Cremers C.M., Ilbert M., Mittelman R., Fitzgerald M.C., Jakob U. Order out of disorder: working cycle of an intrinsically unfolded chaperone. Cell 2012, 148:947-957.
39. Kolb A.R., Needham P.G., Rothenberg C., Guerriero C.J., Welling P.A., Brodsky J.L. ESCRT regulates surface expression of the Kir2.1 potassium channel. Mol Biol Cell 2014, 25:276-289.
40. Zhang Z.R., Bonifacino J.S., Hegde R.S. Deubiquitinases sharpen substrate discrimination during membrane protein degradation from the ER. Cell 2013, 154:609-622.
41. Lam M.H., Urban-Grimal D., Bugnicourt A., Greenblatt J.F., Haguenauer-Tsapis R., Emili A. Interaction of the deubiquitinating enzyme Ubp2 and the e3 ligase Rsp5 is required for transporter/receptor sorting in the multivesicular body pathway. PLoS ONE 2009, 4:e4259.
42. Kee Y., Muñoz W., Lyon N., Huibregtse J.M. The deubiquitinating enzyme Ubp2 modulates Rsp5-dependent Lys63-linked polyubiquitin conjugates in Saccharomyces cerevisiae. J Biol Chem 2006, 281:36724-36731.
43. Kee Y., Lyon N., Huibregtse J.M. The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme. EMBO J 2005, 24:2414-2424.
44. Quan S., Bardwell J.C. Chaperone discovery. Bioessays 2012, 34:973-981.
45. Lauwers E., Grossmann G., André 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.
46. Kandror O., Bretschneider N., Kreydin E., Cavalieri D., Goldberg A.L. Yeast adapt to near-freezing temperatures by STRE/Msn2,4-dependent induction of trehalose synthesis and certain molecular chaperones. Mol Cell 2004, 13:771-781.
47. Benaroudj N., Lee D.H., Goldberg A.L. Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J Biol Chem 2001, 276:24261-24267.
48. Lee D.H., Goldberg A.L. Proteasome inhibitors cause induction of heat shock proteins and trehalose, which together confer thermotolerance in Saccharomyces cerevisiae. Mol Cell Biol 1998, 18:30-38.
49. Yamamoto A., Mizukami Y., Sakurai H. Identification of a novel class of target genes and a novel type of binding sequence of heat shock transcription factor in Saccharomyces cerevisiae. J Biol Chem 2005, 280:11911-11919.
50. Matsumoto R., Akama K., Rakwal R., Iwahashi H. The stress response against denatured proteins in the deletion of cytosolic chaperones SSA1/2 is different from heat-shock response in Saccharomyces cerevisiae. BMC Genomics 2005, 6:141.
51. Causton H.C., Ren B., Koh S.S., Harbison C.T., Kanin E., Jennings E.G., Lee T.I., True H.L., Lander E.S., Young R.A. Remodeling of yeast genome expression in response to environmental changes. Mol Biol Cell 2001, 12:323-337.
52. Berry D.B., Gasch A.P. Stress-activated genomic expression changes serve a preparative role for impending stress in yeast. Mol Biol Cell 2008, 19:4580-4587.
53. Jones D.L., Petty J., Hoyle D.C., Hayes A., Oliver S.G., Riba-Garcia I., Gaskell S.J., Stateva L. Genome-wide analysis of the effects of heat shock on a Saccharomyces cerevisiae mutant with a constitutively activated cAMP-dependent pathway. Comp Funct Genomics 2004, 5:419-431.
54. Tai S.L., Daran-Lapujade P., Walsh M.C., Pronk J.T., Daran J.M. Acclimation of Saccharomyces cerevisiae to low temperature: a chemostat-based transcriptome analysis. Mol Biol Cell 2007, 18:5100-5112.
55. Welker S., Rudolph B., Frenzel E., Hagn F., Liebisch G., Schmitz G., Scheuring J., Kerth A., Blume A., Weinkauf S., et al. Hsp12 is an intrinsically unstructured stress protein that folds upon membrane association and modulates membrane function. Mol Cell 2010, 39:507-520.
56. Kastenmayer J.P., Ni L., Chu A., Kitchen L.E., Au W.C., Yang H., Carter C.D., Wheeler D., Davis R.W., Boeke J.D., et al. Functional genomics of genes with small open reading frames (sORFs) in S. cerevisiae. Genome Res 2006, 16:365-373.
57. Liu Y., Chang A. Quality control of a mutant plasma membrane ATPase: ubiquitylation prevents cell-surface stability. J Cell Sci 2006, 119:360-369.