Protein quality control at the inner nuclear membrane

Nature

Volumn 516, Issue 7531, 2014, Pages 410-413

  Khmelinskii, Anton ^a   Blaszczak, Ewa ^b,c   Pantazopoulou, Marina ^d   Fischer, Bernd ^e,f   Omnus, Deike J ^d   Dez, Gaëlle Le ^b,c   Brossard, Audrey ^b,c   Gunnarsson, Alexander ^d   Barry, Joseph D ^e   Meurer, Matthias ^a   Kirrmaier, Daniel ^a   Boone, Charles ^g   Huber, Wolfgang ^e   Rabut, Gwenaël ^b,c   Ljungdahl, Per O ^d   Knop, Michael ^a,f  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b CNRS   (France)

^c UNIVERSITÉ DE RENNES 1   (France)

^d STOCKHOLM UNIVERSITY   (Sweden)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; RING FINGER PROTEIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; ASI1 PROTEIN, S CEREVISIAE; ASI3 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; UBC6 PROTEIN, S CEREVISIAE; UBC7 PROTEIN, S CEREVISIAE;

CYTOPLASM; GENE EXPRESSION; GENOME; MEMBRANE; PROTEIN; QUALITY CONTROL; YEAST;

ARTICLE; CELL NUCLEUS MEMBRANE; DELETION MUTANT; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM MEMBRANE; GENE EXPRESSION; GENE INTERACTION; NONHUMAN; NUCLEAR PORE COMPLEX; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN QUALITY; QUALITY CONTROL; SACCHAROMYCES CEREVISIAE; UNFOLDED PROTEIN RESPONSE; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN TRANSPORT;

SACCHAROMYCES CEREVISIAE;

ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; MEMBRANE PROTEINS; NUCLEAR ENVELOPE; PROTEIN TRANSPORT; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84922218720     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature14096     Document Type: Article

References (43)

1. Mekhail, K.Moazed, D.The nuclear envelopein genomeorganization, expression and stability. Nature Rev. Mol. Cell Biol. 11, 317-328 (2010).
2. Zattas, D. & Hochstrasser, M. Ubiquitin-dependent protein degradation at the yeast endoplasmic reticulum and nuclear envelope. Crit. Rev. Biochem. Mol. Biol. http://dx.doi.org/10.3109/10409238.2014.959889 (2014).
3. Ruggiano, A., Foresti, O.& Carvalho, P. Quality control: ER-associated degradation: protein quality control and beyond. J. Cell Biol. 204, 869-879 (2014).
4. Zargari, A. et al. Inner nuclear membrane proteins Asi1, Asi2, and Asi3 function in concert to maintain the latent properties of transcription factors Stp1 and Stp2. J. Biol. Chem. 282, 594-605 (2007).
5. Khmelinskii, A. et al. Tandem fluorescent protein timers for in vivo analysis of protein dynamics. Nature Biotechnol. 30, 708-714 (2012).
6. Deng, M. & Hochstrasser, M. Spatially regulated ubiquitin ligation by an ER/nuclear membrane ligase. Nature 443, 827-831 (2006).
7. Boban, M., Pantazopoulou, M., Schick, A., Ljungdahl, P. O. & Foisner, R. A nuclear ubiquitin-proteasome pathway targets the inner nuclear membrane protein Asi2 for degradation. J. Cell Sci. 127, 3603-3613 (2014).
8. Hu, C.-D., Chinenov, Y. & Kerppola, T. K. Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798 (2002).
9. Forsberg, H., Hammar, M., Andreásson, C., Molinér, A. & Ljungdahl, P. O. Suppressors of ssy1 and ptr3 null mutations define novel amino acid sensorindependent genes in Saccharomyces cerevisiae. Genetics 158, 973-988 (2001).
10. Boban, M. et al. Asi1 is an inner nuclear membrane protein that restricts promoter access of two latent transcription factors. J. Cell Biol. 173, 695-707 (2006).
11. Omnus, D. J. & Ljungdahl, P. O. Latency of transcription factor Stp1 depends on a modular regulatorymotif that functions as cytoplasmic retention determinant and nuclear degron. Mol. Biol. Cell 25, 3823-3833 (2014).
12. Wienken, C. J., Baaske, P., Rothbauer, U., Braun, D. & Duhr, S. Protein-binding assays in biological liquids using microscale thermophoresis. Nature Commun. 1, 100 (2010).
13. Kostova, Z., Mariano, J., Scholz, S., Koenig, C. & Weissman, A. M. A. Ubc7p-binding domain in Cue1p activates ER-associated protein degradation. J. Cell Sci. 122, 1374-1381 (2009).
14. Biederer, T., Volkwein, C. & Sommer, T. Role of Cue1p in ubiquitination and degradation at the ER surface. Science 278, 1806-1809 (1997).
15. Costanzo, M., Baryshnikova, A., Myers, C. L., Andrews, B. & Boone, C. Charting the genetic interaction map of a cell. Curr. Opin. Biotechnol. 22, 66-74 (2011).
16. Costanzo, M. et al. The genetic landscape of a cell. Science 327, 425-431 (2010).
17. Friedlander, R., Jarosch, E., Urban, J., Volkwein, C. & Sommer, T. A regulatory link between ER-associated protein degradation and the unfolded-protein response. Nature Cell Biol. 2, 379-384 (2000).
18. Foresti, O., Rodriguez-Vaello, V., Funaya, C. & Carvalho, P. Quality control of inner nuclear membrane proteins by the Asi complex. Science 346, 751-755 (2014).
19. Khmelinskii, A.,Meurer, M.,Duishoev, N., Delhomme, N.& Knop, M. Seamless gene tagging by endonuclease-driven homologous recombination. PLoS ONE 6, e23794 (2011).
20. Baryshnikova, A. et al. Synthetic genetic array (SGA) analysis in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Methods Enzymol. 470, 145-179 (2010).
21. Zattas, D., Adle, D. J., Rubenstein, E. M.Hochstrasser, M. N-terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Mol. Biol. Cell 24, 890-900 (2013).
22. Uttenweiler, A., Schwarz, H., Neumann, H. & Mayer, A. The vacuolar transporter chaperone (VTC) complex is required for microautophagy. Mol. Biol. Cell 18, 166-175 (2007).
23. Sharpe, H. J., Stevens, T. J. & Munro, S. A comprehensive comparison of transmembrane domains reveals organelle-specific properties. Cell 142, 158-169 (2010).
24. Meinema, A. C., Poolman, B. & Veenhoff, L. M. The transport of integralmembrane proteins across the nuclear pore complex. Nucleus 3, 322-329 (2012).
25. Ellenberg, J. et al. Nuclear membrane dynamics and reassembly in living cells: targeting of an inner nuclear membrane protein in interphase and mitosis. J. Cell Biol. 138, 1193-1206 (1997).
26. Soullam, B.Worman, H. J. Theamino-terminal domain of the laminB receptor is a nuclear envelope targeting signal. J. Cell Biol. 120, 1093-1100 (1993).
27. Hinshaw, J. E., Carragher, B. O. & Milligan, R. A. Architecture and design of the nuclear pore complex. Cell 69, 1133-1141 (1992).
28. Beck, M., Lucić, V., Fö rster, F., Baumeister, W. & Medalia, O. Snapshots of nuclear pore complexes in action captured by cryo-electron tomography. Nature 449, 611-615 (2007).
29. Nakamura, N. The Role of the transmembrane RINGfinger proteins in cellular and organelle function. Membranes 1, 354-393 (2011).
30. Janke, C. et al. A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins,moremarkers and promoter substitution cassettes. Yeast 21, 947-962 (2004).
31. Andreásson, C. & Ljungdahl, P. O. The N-terminal regulatory domain of Stp1p is modular and, fused to an artificial transcription factor, confers full Ssy1p-Ptr3p-Ssy5p sensor control. Mol. Cell. Biol. 24, 7503-7513 (2004).
32. Becuwe, M. et al. A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J. Cell Biol. 196, 247-259 (2012).
33. León, S., Erpapazoglou, Z. & Haguenauer-Tsapis, R. Ear1p and Ssh4p are new adaptors of the ubiquitin ligase Rsp5p for cargo ubiquitylation and sorting at multivesicular bodies. Mol. Biol. Cell 19, 2379-2388 (2008).
34. Shyu, Y. J., Liu, H., Deng, X. & Hu, C. Identification of new fluorescent protein fragments for biomolecular fluorescence complementation analysis under physiological conditions. Biotechniques 40, 61 (2006).
35. Sommer, T. & Jentsch, S. A protein translocation defect linked to ubiquitin conjugation at the endoplasmic reticulum. Nature 365, 176-179 (1993).
36. Metzger, M. B. et al. A structurally unique E2-binding domain activates ubiquitination by the ERAD E2, Ubc7p, through multiple mechanisms. Mol. Cell 50, 516-527 (2013).
37. Sheff, M. A. & Thorn, K. S. Optimized cassettes for fluorescent protein tagging in Saccharomyces cerevisiae. Yeast 21, 661-670 (2004).
38. Laporte, D., Salin, B., Daignan-Fornier, B. & Sagot, I. Reversible cytoplasmic localization of the proteasome in quiescent yeast cells. J. Cell Biol. 181, 737-745 (2008).
39. Schneider, C. A., Rasband, W. S. & Eliceiri, K. W. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9, 671-675 (2012).
40. Knop, M. et al. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 15, 963-972 (1999).
41. Winzeler, E. A. et al. Functional characterization of the S. cerevisiae genome by gene deletion and parallel analysis. Science 285, 901-906 (1999).
42. Smyth, G. K. in Bioinformatics and Computational Biology Solutions Using R and Bioconductor (eds Gentleman, R., Carey, V., Dudoit, S., Irizarry, R. & Huber, W.) 397-420 (Springer, 2005).
43. Khmelinskii, A. & Knop, M. Analysis of protein dynamics with tandem fluorescent protein timers. Methods Mol. Biol. 1174, 195-210 (2014).