Distinguishing between retention signals and degrons acting in ERAD

Journal of Cell Science

Volumn 120, Issue 24, 2007, Pages 4377-4387

  Shapira, Ilana ^a   Charuvi, Dana ^a,b   Elkabetz, Yechiel ^a,c   Hirschberg, Koret ^a   Bar Nun, Shoshana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Degrons; ERAD; Proteasome; Retention signals

Indexed keywords

CIS ACTING ELEMENT; CYSTEINE; HYBRID PROTEIN; IMMUNOGLOBULIN MU CHAIN; THYROID PEROXIDASE; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL ACTIVITY; CELL FUNCTION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FUNCTION; PROTEIN GLYCOSYLATION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; UBIQUITINATION;

AMINO ACID MOTIFS; AMINO ACID SUBSTITUTION; CELL LINE; ENDOPLASMIC RETICULUM; GLYCOSYLATION; HELA CELLS; HUMANS; IMMUNOGLOBULIN M; IMMUNOGLOBULIN MU-CHAINS; IODIDE PEROXIDASE; LUMINESCENT PROTEINS; POLYSACCHARIDES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN SORTING SIGNALS; PROTEIN TRANSPORT; PROTEINS; RECOMBINANT FUSION PROTEINS; UBIQUITIN;

EID: 38349008634     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.011247     Document Type: Article

References (58)

1. Allen, M. D., Buchberger, A. and Bycroft, M. (2006). The PUB domain functions as a p97 binding module in human peptide N-glycanase. J. Biol. Chem. 281, 25502-25508.
2. Amitay, R., Bar-Nun, S., Halmovich, J., Rabinovich, E. and Shachar, I. (1991). Post-translational regulation of IgM expression in B lymphocytes. J. Biol. Chem. 266, 12568-12573.
3. Amitay, R., Shachar, I., Rabinovich, E., Haimovich, J. and Bar-Nun, S. (1992). Degradation of secretory IgM in B lymphocytes occurs in a post-endoplasmic reticulum compartment and is mediated by a cysteinc protease. J. Biol. Chem. 267, 20694-20700.
4. Anelli, T., Alessio, M., Mezghrani, A., Simmen, T., Talamo, F., Bachi, A. and Sitia, R. (2002). ERp44, a novel endoplasmic reticulum folding assistant of the thioredoxin family. EMBO J. 21, 835-844.
5. Anelli, T., Alessio, M., Bachi, A., Bergamelli, L., Bertoli, G., Camerini, S., Mezghrani, A., Ruffato, E., Simmen, T. and Sitia, R. (2003). Thiol-mediated protein retention in the endoplasmic reticulum: the role of ERp44. EMBO J. 22, 5015-5022.
6. Arteaga, M. F., Wang, L., Ravid, T., Hochstrasser, M. and Canessa, C. M. (2006). An amphipathic helix targets serum and glucocorticoid-induced kinase 1 to the endoplasmic reticulum-associated ubiquitin-conjugation machinery. Proc. Natl. Acad. Sci. USA 103, 11178-11183.
7. Bar-Nun, S. (2005). The role of p97/Cdc48p in endoplasmic reticulum-associated degradation: from the immune system to yeast, Curr. Top. Microbiol. Immunol. 300, 95-125.
8. Bonifacino, J. S. and Weissman, A. M. (1998). Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Annu. Rev. Cell Dev. Biol. 14, 19-57.
9. Brenckle, R. and Kornfeld, R. (1980). Structure of the oligosaccharides of mouse immunoglobulin M secreted by the MOPC 104E Plasmacytoma. Arch. Biochem. Biophys. 201, 160-173.
10. Cals, M.-M., Guenzi, S., Carelli, S., Simmen, T., Sparvoli, A. and Sitia, R. (1996). IgM polymerization inhibits the Golgi-mediated processing of the mu-chain carboxy-terminal glycans. Mol. Immunol. 33, 15-24.
11. Chen, C. A. and Okayama, H. (1988). Calcium phosphate-mediated gene transfer: a highly efficient transfection system for stably transforming cells with plasmid DNA. Biotechniques 6, 632-638.
12. Dai, R. M. and Li, C. C. (2001). Valosin-containing protein is a multi-ubiquitin chain-targeting factor required in ubiquitin-proteasome degradation. Nat. Cell Biol. 3, 740-744.
13. de Lalla, C., Fagioli, C., Cessi, F. S., Smilovich, D. and Sitla, R. (1998). Biogenesis and function of IgM: the role of the conserved mu-chain tailpiece glycans. Mol. Immumol. 35, 837-845.
14. de Virgilio, M., Kitzmuller, C., Schwaiger, E., Klein, M., Kreibich, G. and Ivessa, N. E. (1999). Degradation of a short-lived glycoprotein from the lumen of the endoplasmic reticulum: the role of N-linked glycans and the unfolded protein response. Mol. Biol. Cell 10, 4059-4073.
15. Doolman, R., Leichner, G. S., Avner, R. and Roitelman, J. (2004). Ubiquitin is conjugated by membrane ubiquitin ligase to three sites, including the N terminus, in transmembrane region of mammalian 3-hydroxy-3-methylglutaryl coenzyme A reductase: implications for sterol-regulated enzyme degradation. J. Biol. Chem. 279, 38184-38193.
16. Doss-Pepe, E. W., Stenroos, E. S., Johnson, W. G. and Madura, K. (2003). Ataxin-3 interactions with rad23 and valosin-containing protein and its associations with ubiquitin chains and the proteasome are consistent with a role in ubiquitin-mediated proteolysis. Mol. Cell. Biol. 23, 6469-6483.
17. Elkabetz, Y., Kerem, A., Tencer, L., Winitz, D., Kopito, R. R. and Bar-Nun, S. (2003). Immunoglobulin light chains dictate vesicular transport-dependent and -independent routes for IgM degradation by the ubiquitin-proteasome pathway. J. Biol. Chem. 278, 18922-18929.
18. Elkabetz, Y., Shapira, I., Rabinovich, E. and Bar-Nun, S. (2004). Distinct steps in dislocation of luminal endoplasmic reticulum-associated degradation substrates: roles of endoplamic reticulum-bound p97/Cdc48p and proteasome. J. Biol. Chem. 279, 3980-3989.
19. Ellgaard, L. and Helenius, A. (2003). Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191.
20. Fayadat, L., Siffrol-Fernandez, S., Lanet, J. and Franc, J. L. (2000). Degradation of human thyroperoxidase in the endoplasmic reticulum involves two different pathways depending on the folding state of the protein. J. Biol. Chem. 275, 15948-15954.
21. Fra, A. M., Fagioli, C., Finazzi, D., Sitia, R. and Alberini, C. M. (1993). Quality control of ER synthesized proteins: an exposed thiol group as a three-way switch mediating assembly, retention and degradation. EMBO J. 12, 4755-4761.
22. Gilon, T., Chomsky, O. and Kulka, R. G. (1998). Degradation signals for ubiquitin system proteolysis in Saccharomyces cerevisiae. EMBO J. 17, 2759-2766.
23. Helenius, A. and Aebi, M. (2001). Intracellular functions of N-linked glycans. Science 291, 2364-2369.
24. Helenius, A. and Aebi, M. (2004). Roles of N-linked glycans in the endoplasmic reticulum. Annu. Rev. Biochem. 73, 1019-1049.
25. Isidoro, C., Maggioni, C., Demoz, M., Pizzagalli, A., Fra, A. M. and Sitia, R. (1996). Exposed thiols confer localization in the endoplasmic reticulum by retention rather than retrieval. J. Biol. Chem. 271, 26138-26142.
26. Johnsong P. R., Swanson, R., Rakhilina, L. and Hochstrasser, M. (1998). Degradation signal masking by heterodimenzation of MATalpha2 and MATa1 blocks their mutual destruction by the ubiquitin-proteasome pathway. Cell 94, 217-227.
27. Kostova, Z. and Wolf, D. H. (2003). For whom the bell tolls: protein quality control of the endoplasmic reticulum, and the ubiquitin-proteasome connection. EMBO J. 22, 2309-2317.
28. Kostova, Z. and Wolf, D. H. (2005). Importance of carbohydrate positioning in the recognition of mutated CPY for ER-associated degradation. J. Cell Sci. 118, 1485-1492.
29. Li, G., Zhou, X., Zhao, G., Schindelin, H. and Lennarz, W. J. (2005). Multiple modes of interaction of the deglycosylation enzyme, mouse peptide N-glycanase, with the proteasome. Proc. Natl. Acad. Sci. USA 102, 15809-15814.
30. Lilley, B. N. and Ploegh, H. L. (2005). Multiprotein complexes that link dislocation, ubiquitination, and extraction of misfolded proteins from the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 102, 14296-14301.
31. Magnusson, R. P., Chazenbalk, G. D., Gestautas, J., Seto, P., Filetti, S., DeGroot, L. J. and Rapoport, B. (1987). Molecular cloning of the complementary deoxyribonucleic acid for human thyroid peroxidase. Mol. Endocrinol. 1, 856-861.
32. Mbonye, U. R., Wada, M., Rieke, C. J., Tang, H. Y., DeWitt, D. L. and Smith, W. L. (2006). The 19-amino acid cassette of cyclooxygenase-2 mediates entry of the protein into the endoplasmic reticulum-associated degradation system. J. Biol. Chem. 281, 35770-35778.
33. McCracken, A. A. and Brodsky, J. L. (2003). Evolving questions and paradigm shifts in endoplasmic-reticulam-associated degradation (ERAD). BioEssays 25, 868-877.
34. Molinari, M., Calanca, V., Galli, C., Lucca, P. and Paganetti, P. (2003). Role of EDEM in the release of misfolded glycoproteins from the calnexin cycle. Science 299, 1397-1400.
35. Moremen, K. W. and Molinari, M. (2006). N-linked glycan recognition and processing: the molecular basis of endoplasmic reticulum quality control. Curr. Opin. Struct. Biol. 16, 592-599.
36. Neuber, O., Jarosch, E., Volkwein, C., Walter, J. and Sommer, T. (2005). Ubx2 links the Cdc48 complex to ER-associated protein degradation. Nat. Cell Biol. 7, 993-998.
37. Neuberger, M. S. (1983). Expression and regulation of immunoglobulin heavy chain gene transfected into lymphoid cells. EMBO J. 2, 1373-1378.
38. Olivari, S., Cali, T., Salo, K. E., Paganetti, P., Ruddock, L. W. and Molinari, M. (2006). EDEM1 regulates ER-associated degradation by accelerating demannosylation of folding-defective polypeptides and by inhibiting their covalent aggregation. Biochem. Biophys. Res. Commun. 349, 1278-1284.
39. Rabinovich, E., Kerem, A., Frohlich, K. U., Diamant, N. and Bar-Nun, S. (2002). AAA-ATPase p97/Cdc48p, a cytosolic chaperone required for endoplasmic reticulum-associated protein degradation. Mol. Cell. Biol. 22, 626-634.
40. Rawitch, A. B., Pollock, G., Yang, S. X. and Taurog, A. (1992). Thyroid peroxidase glycosylation: the location and nature of the N-linked oligosaccharide units in porcine thyroid peroxidase. Arch. Biochem. Biophys. 297, 321-327.
41. Rumpf, S. and Jentsch, S. (2006). Functional division of substrate processing cofactors of the ubiquitin-selective Cdc48 chaperone. Mol. Cell 21, 261-269.
42. Sayeed, A. and Ng, D. T. (2005). Search and destroy: ER quality control and ER-associated protein degradation. Crit. Rev. Biochem. Mol. Biol. 40, 75-91.
43. Schuberth, C. and Buchberger, A. (2005). Membrane-bound Ubx2 recruits Cdc48 to ubiquitin ligases and their substrates to ensure efficient ER-associated protein degradation. Nat. Cell Biol. 7, 999-1006.
44. Sever, N., Song, B. L., Yabe, D., Goldstein, J. L., Brown, M. S. and DeBose-Boyd, R. A. (2003). Insig-dependent ubiquitination and degradation of mammalian 3-hydroxy-3-methylglutaryl-CoA reductase stimulated by sterols and geranylgeraniol. J. Biol. Chem. 278, 52479-52490.
45. Shachar, I., Amitay, R., Rabinovich, E., Haímovich, J. and Bar-Nun, S. (1992). Polymerization of secretary IgM in B lymphocytes is prevented by a preceding targeting to a degradation pathway. J. Biol. Chem. 267, 24241-24247.
46. Sidman, C. (1991). Differing requirements for glycosylation in the secretion of related glycoproteins is determined neither by the producing cell nor by the relative number of oligosaccharide units. J. Biol. Chem. 256, 9374-9376.
47. Sidman, C., Potash, M. J. and Kohler, G. (1981). Roles of protein and carbohydrate in glycoprotein processing and secretion. Studies using mutants expressing altered IgM mu chains. J. Biol. Chem. 256, 13180-13187.
48. Sitia, R. and Brankman, I. (2003). Quality control in the endoplasmic reticulum protein factory. Nature 426, 891-894.
49. Sitia, R., Neuberger, M., Alberini, C., Bet, P., Fra, A., Valetti, C., Williams, G. and Milstein, C. (1990). Developmental regulation of IgM secretion: the role of the carboxy-terminal cysteine. Cell 60, 781-790.
50. Spear, E. D. and Ng, D. T. (2005). Single, context-specific glycans can target misfolded glycoproteins for ER-associated degradation. J. Cell Biol. 169, 73-82.
51. Suzuki, T., Park, H., and Lennarz, W. J. (2002). Cytoplasmic peptide:N-glycanase (PNGase) in eukaryotic cells: occurrence, primary structure, and potential functions. FASEB J. 16, 635-641.
52. Trombetta, E. S. and Parodi, A. J. (2003). Quality control and protein folding in the secretory pathway. Annu. Rev. Cell Dev. Biol. 19, 649-676.
53. Varshavsky, A. (1991). Naming a targeting signal. Cell 64, 13-15.
54. Wang, Q., Li, L. and Ye, Y. (2006). Regulation of retrotranslocation by p97-associated deubiquitinating enzyme ataxin-3. J. Cell Biol. 174, 963-971.
55. Ye, Y., Meyer, H. H. and Rapoport, T. A. (2001). The AAA ATPase Cdc48/p97 and its partners transport proteins from the ER into the cytosol. Nature 414, 652-656.
56. Ye, Y., Shibata, Y., Kikkert, M., van Voorden, S., Wiertz, E. and Rapoport, T. A. (2005). Inaugural Article: Recruitment of the p97 ATPase and ubiquitin ligases to the site of retrotranslocation at the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. USA 102, 14132-14138.
57. Zhong, X. and Pittman, R. N. (2006). Ataxin-3 binds VCP/p97 and regulates retrotranslocation of ERAD substrates. Hum. Mol. Genet. 15, 2409-2420.
58. Zhong, X., Shen, Y., Ballar, P., Apostolou, A., Agami, R. and Fang, S. (2004). AAA ATPase p97/valosin-containing protein interacts with gp78, a ubiquitin ligase for endoplasmic reticulum-associated degradation. J. Biol. Chem. 279, 45676-45684.