A membrane protein complex mediates retro-translocation from the ER lumen into the cytosol

Nature

Volumn 429, Issue 6994, 2004, Pages 841-847

  Ye, Yihong ^a   Shibata, Yoko ^a   Yun, Chi ^b   Ron, David ^b   Rapoport, Tom A ^a  

^a HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MEMBRANES; BIOSYNTHESIS; SUBSTRATES;

ENDOPLASMIC RETICULUM (ER); MEMBRANE PROTEINS; RETRO-TRANSLOCATION;

ADENOSINETRIPHOSPHATE;

ADENOSINE TRIPHOSPHATASE; CELL PROTEIN; DERLIN 1; FUNGAL PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MEMBRANE PROTEIN; PROTEIN DER1P; PROTEIN P97; PROTEIN US11; PROTEIN VIMP; UNCLASSIFIED DRUG;

PROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; CYTOSOL; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN TRANSPORT; STRESS;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; CYTOSOL; DOGS; ENDOPLASMIC RETICULUM; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; MACROMOLECULAR SUBSTANCES; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; PROTEIN FOLDING; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; RNA-BINDING PROTEINS; SELENOPROTEINS; VIRAL PROTEINS;

ANIMALIA; MAMMALIA;

EID: 3042677637     PISSN: 00280836     EISSN: None     Source Type: Journal    
DOI: 10.1038/nature02656     Document Type: Article

References (40)

1. Ellgaard, L. & Helenius, A. ER quality control: towards an understanding at the molecular level. Curr. Opin. Cell Biol. 13, 431-437 (2001).
2. Tsai, B., Ye, Y. & Rapoport, T. A. Retro-translocation of proteins from the endoplasmic reticulum into the cytosol. Nature Rev. Mol. Cell Biol. 3, 246-255 (2002).
3. Wiertz, E. J. H. et al. The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84, 769-779 (1996).
4. Aridor, M. & Balch, W. E. Integration of endoplasmic reticulum signaling in health and disease. Nature Med. 5, 745-751 (1999).
5. Meyer, H. H., Shorter, J. G., Seemann, J., Pappin, D. & Warren, G. A complex of mammalian ufd1 and np14 links the AAA-ATPase, p97, to ubiquitin and nuclear transport pathways. EMBO J. 19, 2181-2192 (2000).
6. Ye, Y., Meyer, H. H. & Rapoport, T. A. Function of the p97-Ufd1-Np14 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 162, 71-84 (2003).
7. Langer, T. AAA proteases: cellular machines for degrading membrane proteins. Trends Biochem. Sci. 25, 247-251 (2000).
8. Bays, N. W., Wilhovsky, S. K., Goradia, A., Hodgkiss-Harlow, K. & Hampton, R. Y. HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol. Biol. Cell 12, 4114-4128 (2001).
9. Ye, Y., Meyer, H. H. & Rapoport, T. A. The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656 (2001).
10. Jarosch, E. et al. Protein dislocation from the ER requires polyubiquitination and the AAA-ATPase Cdc48. Nature Cell Biol. 4, 134-139 (2002).
11. Rabinovich, E., Kerem, A., Frohlich, K. U., Diamant, N. & Bar-Nun, S. AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22, 626-634 (2002).
12. Wang, Q. & Chang, A. Substrate recognition in ER-associated degradation mediated by Eps1, a member of the protein disulfide isomerase family. EMBO J. 22, 3792-3802 (2003).
13. Story, C. M., Furman, M. H. & Ploegh, H. L. The cytosolic tail of class I MHC heavy chain is required for its dislocation by the human cytomegalovirus US2 and US11 gene products. Proc. Natl Acad. Sci. USA 96, 8516-8521 (1999).
14. Gillece, P., Luz, J. M., Lennarz, W. J., de La Cruz, F. J. & Romisch, K. Export of a cysteine-free misfolded secretory protein from the endoplasmic reticulum for degradation requires interaction with protein disulfide isomerase. J. Cell Biol. 147, 1443-1456 (1999).
15. Nishikawa, S. I., Fewell, S. W., Kato, Y., Brodsky, J. L. & Endo, T. Molecular chaperones in the yeast endoplasmic reticulum maintain the solubility of proteins for retrotranslocation and degradation. J. Cell Biol. 153, 1061-1070 (2001).
16. Tsai, B., Rodighiero, C., Lencer, W. I. & Rapoport, T. A. Protein disulfide isomerase acts as a redox-dependent chaperone to unfold cholera toxin. Cell 104, 937-948 (2001).
17. Molinari, M., Calanca, V., Galli, C., Lucca, P. & Paganetti, P. Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299, 1397-1400 (2003).
18. Oda, Y., Hosokawa, N., Wada, I. & Nagata, K. EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299, 1394-1397 (2003).
19. Knop, M., Finger, A., Braun, T., Hellmuth, K. & Wolf, D. H. Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J. 15, 753-763 (1996).
20. Vashist, S. & Ng, D. T. Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 165, 41-52 (2004).
21. Travers, K. J. et al. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell 101, 249-258 (2000).
22. Hitt, R. & Der Wolf, D. H. 1p, a protein required for degradation of malfolded soluble proteins of the endoplasmic reticulum: topology and Der1-like proteins. FEMS Yeast Res. 4, 721-729 (2004).
23. Kryukov, G. V. et al. Characterization of mammalian selenoproteomes. Science 300, 1439-1443 (2003).
24. DeLaBarre, B. & Brunger, A. T. Complete structure of p97/valosin-containing protein reveals communication between nucleotide domains. Nature Struct. Biol. 10, 856-863 (2003).
25. Flierman, D., Ye, Y., Dai, M., Chau, V. & Rapoport, T. A. Polyubiquitin serves as a recognition signal, rather than a ratcheting molecule, during retrotranslocation of proteins across the endoplasmic reticulum membrane. J. Biol. Chem. 278, 34774-34782 (2003).
26. Wiertz, E. J. H. J. et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384, 432-438 (1996).
27. Lilley, B. N., Tortorella, D. & Ploegh, H. L. Dislocation of a type I membrane protein requires interactions between membrane-spanning segments within the lipid bilayer. Mol. Biol. Cell 14, 3690-3698 (2003).
28. Braakman, I., Helenius, J. & Helenius, A. Manipulating disulfide bond formation and protein folding in the endoplasmic reticulum. EMBO J. 11, 1717-1722 (1992).
29. Calfon, M. et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92-96 (2002).
30. Plemper, R. K. et al. Genetic interactions of Hrd3p and Der3p/Hrd1p with Sec61p suggest a retrotranslocation complex mediating protein transport for ER degradation. J. Cell Sci. 112, 4123-4134 (1999).
31. Gardner, R. G. et al. Endoplasmic reticulum degradation requires lumen to cytosol signaling. Transmembrane control of Hrd1p by Hrd3p. J. Cell Biol. 151, 69-82 (2000).
32. Frand, A. R. & Kaiser, C. A. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell 1, 161-170 (1998).
33. Pollard, M. G., Travers, K. J. & Weissman, J. S. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell 1, 171-182 (1998).
34. Gao, Y. et al. Regulation of the selenoprotein SelS by glucose deprivation and endoplasmic reticulum stress-SelS is a novel glucose-regulated protein. FEBS Lett. 563, 185-190 (2004).
35. Akiyama, Y. & Ito, K. Reconstitution of membrane proteolysis by FtsH. J. Biol. Chem. 278, 18146-18153 (2003).
36. Timmons, L., Court, D. L. & Fire, A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112 (2001).
37. Urano, F. et al. A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J. Cell Biol. 158, 639-646 (2002).
38. Harding, H. P. et al. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11, 619-633 (2003).
39. Shamu, C. E., Story, C. M., Rapoport, T. A. & Ploegh, H. L. The pathway of US11-dependent degradation of MHC class I heavy chains involves a ubiquitin-conjugated intermediate. J. Cell Biol. 147, 45-58 (1999).
40. Lilley, B. N. & Ploegh, H. L. A membrane protein required for dislocation of misfolded proteins from the ER. Nature (this issue).