A shared endoplasmic reticulum-associated degradation pathway involving the EDEM1 protein for glycosylated and nonglycosylated proteins

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2167-2178

  Shenkman, Marina ^a   Groisman, Bella ^a   Ron, Efrat ^a   Avezov, Edward ^a   Hendershot, Linda M ^b   Lederkremer, Gerardo Z ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ASIALOGLYCOPROTEIN RECEPTORS; CYTOSOLIC; ENDOPLASMIC RETICULUM; GLYCOSYLATED; HEAVY CHAIN; LIGHT CHAIN; MACHINERY COMPONENTS; MISFOLDED PROTEINS; PROTEIN-PROTEIN INTERACTIONS; RETICULUM-ASSOCIATED DEGRADATION PATHWAYS; UBIQUITIN LIGASES;

CELL MEMBRANES; GLYCOPROTEINS; MACHINERY; QUALITY CONTROL; SUBSTRATES;

PROTEINS;

ASIALOGLYCOPROTEIN RECEPTOR; CALNEXIN; CARRIER PROTEIN; ENDOPLASMIC RETICULUM DEGRADATION ENHANCING ALPHA MANNOSIDASE LIKE PROTEIN 1; GLUCOSE REGULATED PROTEIN 78; IMMUNOGLOBULIN HEAVY CHAIN; LECTIN; NONSECRETED 1 KAPPA LIGHT CHAIN; PROTEIN OS 9; PROTEIN XTP3 B; REGULATOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION;

ANIMALS; CHAPERONINS; CYTOSOL; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE EXPRESSION REGULATION; GLYCOSYLATION; HEK293 CELLS; HUMANS; IMMUNOGLOBULIN KAPPA-CHAINS; LECTINS; MANNOSIDASES; MEMBRANE PROTEINS; MICE; NIH 3T3 CELLS; POLYSACCHARIDES; PROTEIN DENATURATION; PROTEIN FOLDING;

EID: 84873849329     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.438275     Document Type: Article

References (53)

1. Benyair, R., Ron, E., and Lederkremer, G. Z. (2011) Protein quality control, retention, and degradation at the endoplasmic reticulum. Int. Rev. Cell Mol. Biol. 292, 197-280
2. Lederkremer, G. Z. (2009) Glycoprotein folding, quality control, and ERassociated degradation. Curr. Opin. Struct. Biol. 19, 515-523
3. Brodsky, J. L., and Skach, W. R. (2011) Protein folding and quality control in the endoplasmic reticulum. Recent lessons from yeast and mammalian cell systems. Curr. Opin. Cell Biol. 23, 464-475
4. Bernasconi, R., and Molinari, M. (2011) ERAD and ERAD tuning: disposal of cargo and ofERADregulators from the mammalian ER. Curr. Opin. Cell Biol. 23, 176-183
5. Smith, M. H., Ploegh, H. L., and Weissman, J. S. (2011) Road to ruin. Targeting proteins for degradation in the endoplasmic reticulum. Science 334, 1086-1090
6. D'Alessio, C., Caramelo, J. J., and Parodi, A. J. (2010) UDP-Glc:glycoprotein glucosyltransferase-glucosidase II, the ying-yang of the ER quality control. Semin. Cell Dev. Biol. 21, 491-499
7. Määttänen, P., Gehring, K., Bergeron, J. J., and Thomas, D. Y. (2010) Protein quality control in the ER. The recognition of misfolded proteins. Semin. Cell Dev. Biol. 21, 500-511
8. Frenkel, Z., Gregory, W., Kornfeld, S., and Lederkremer, G. Z. (2003) Endoplasmic reticulum-associated degradation of mammalian glycoproteins involves sugar chain trimming to Man6-5GlcNAc2. J. Biol. Chem. 278, 34119-34124
9. Lederkremer, G. Z., and Glickman, M. H. (2005)Awindow of opportunity. Timing protein degradation by trimming of sugars and ubiquitins. Trends Biochem. Sci. 30, 297-303
10. Aebi, M., Bernasconi, R., Clerc, S., and Molinari, M. (2010) N-Glycan structures. Recognition and processing in the ER. Trends Biochem. Sci. 35, 74-82
11. Hebert, D. N., Bernasconi, R., and Molinari, M. (2010) ERAD substrates. Which way out? Semin. Cell Dev. Biol. 21, 526-532
12. Kamhi-Nesher, S., Shenkman, M., Tolchinsky, S., Fromm, S. V., Ehrlich, R., and Lederkremer, G. Z. (2001) A novel quality control compartment derived from the endoplasmic reticulum. Mol. Biol. Cell 12, 1711-1723
13. Groisman, B., Shenkman, M., Ron, E., and Lederkremer, G. Z. (2011) Mannose trimming is required for delivery of a glycoprotein from EDEM1 to XTP3-B and to late endoplasmic reticulum-associated degradation steps. J. Biol. Chem. 286, 1292-1300
14. Yoshida, Y., Adachi, E., Fukiya, K., Iwai, K., and Tanaka, K. (2005) Glycoprotein- specific ubiquitin ligases recognize N-glycans in unfolded substrates. EMBO Rep. 6, 239-244
15. Ma, J., Kearney, J. F., and Hendershot, L. M. (1990) Association of transport- defective light chains with immunoglobulin heavy chain-binding protein. Mol. Immunol. 27, 623-630
16. Skowronek, M. H., Hendershot, L. M., and Haas, I. G. (1998) The variable domain of nonassembled Ig light chains determines both their half-life and binding to the chaperone BiP. Proc. Natl. Acad. Sci. U.S.A. 95, 1574-1578
17. Okuda-Shimizu, Y., and Hendershot, L. M. (2007) Characterization of an ERAD pathway for nonglycosylated BiP substrates, which require Herp. Mol. Cell 28, 544-554
18. Olivari, S., and Molinari, M. (2007) Glycoprotein folding and the role of EDEM1, EDEM2, and EDEM3 in degradation of folding-defective glycoproteins. FEBS Lett. 581, 3658-3664
19. Tamura, T., Cormier, J. H., and Hebert, D. N. (2011) Characterization of early EDEM1 protein maturation events and their functional implications. J. Biol. Chem. 286, 24906-24915
20. Tolchinsky, S., Yuk, M. H., Ayalon, M., Lodish, H. F., and Lederkremer, G. Z. (1996) Membrane-bound versus secreted forms of human asialoglycoprotein receptor subunits. Role of a juxtamembrane pentapeptide. J. Biol. Chem. 271, 14496-14503
21. Shenkman, M., Ayalon, M., and Lederkremer, G. Z. (1997) Endoplasmic reticulum quality control of asialoglycoprotein receptor H2a involves a determinant for retention and not retrieval. Proc. Natl. Acad. Sci. U.S.A. 94, 11363-11368
22. Chillarón, J., and Haas, I. G. (2000) Dissociation from BiP and retrotranslocation of unassembled immunoglobulin light chains are tightly coupled to proteasome activity. Mol. Biol. Cell 11, 217-226
23. Lee, Y. K., Brewer, J. W., Hellman, R., and Hendershot, L. M. (1999) BiP and immunoglobulin light chain cooperate to control the folding of heavy chain and ensure the fidelity of immunoglobulin assembly. Mol. Biol. Cell 10, 2209-2219
24. Groisman, B., Avezov, E., and Lederkremer, G. Z. (2006) The E3 ubiquitin ligases HRD1 and SCFFbs2 recognize the protein moiety and sugar chains, respectively, of an ER-associated degradation substrate. Isr. J. Chem. 46, 189-196
25. Avezov, E., Frenkel, Z., Ehrlich, M., Herscovics, A., and Lederkremer, G. Z. (2008) Endoplasmic reticulum (ER) mannosidase I is compartmentalized and required for N-glycan trimming to Man5-6GlcNAc2 in glycoprotein ER-associated degradation. Mol. Biol. Cell 19, 216-225
26. Ron, E., Shenkman, M., Groisman, B., Izenshtein, Y., Leitman, J., and Lederkremer, G. Z. (2011) Bypass of glycan-dependent glycoprotein delivery to ERAD by up-regulated EDEM1. Mol. Biol. Cell 22, 3945-3954
27. Christianson, J. C., Shaler, T. A., Tyler, R. E., and Kopito, R. R. (2008) OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10, 272-282
28. Kondratyev, M., Avezov, E., Shenkman, M., Groisman, B., and Lederkremer, G. Z. (2007) PERK-dependent compartmentalization of ERAD and unfolded protein response machineries during ER stress. Exp. Cell Res. 313, 3395-3407
29. Shenkman, M., Ehrlich, M., and Lederkremer, G. Z. (2000) Masking of an endoplasmic reticulum retention signal by its presence in the two subunits of the asialoglycoprotein receptor. J. Biol. Chem. 275, 2845-2851
30. Benyair, R., Kondratyev, M., Veselkin, E., Tolchinsky, S., Shenkman, M., Lurie, Y., and Lederkremer, G. Z. (2011) Constant serum levels of secreted asialoglycoprotein receptor sH2a and decrease with cirrhosis. World J. Gastroenterol. 17, 5305-5309
31. Hendershot, L. M., Wei, J. Y., Gaut, J. R., Lawson, B., Freiden, P. J., and Murti, K. G. (1995) In vivo expression of mammalian BiP ATPase mutants causes disruption of the endoplasmic reticulum. Mol. Biol. Cell 6, 283-296
32. Frenkel, Z., Shenkman, M., Kondratyev, M., and Lederkremer, G. Z. (2004) Separate roles and different routing of calnexin and ERp57 in endoplasmic reticulum quality control revealed by interactions with asialoglycoprotein receptor chains. Mol. Biol. Cell 15, 2133-2142
33. Oda, Y., Hosokawa, N., Wada, I., and Nagata, K. (2003) EDEM as an acceptor of terminally misfolded glycoproteins released from calnexin. Science 299, 1394-1397
34. Hagiwara, M., Maegawa, K., Suzuki, M., Ushioda, R., Araki, K., Matsumoto, Y., Hoseki, J., Nagata, K., and Inaba, K. (2011) Structural basis of an ERAD pathway mediated by the ER-resident protein-disulfide reductase ERdj5. Mol. Cell 41, 432-444
35. Yoshida, Y., Tokunaga, F., Chiba, T., Iwai, K., Tanaka, K., and Tai, T. (2003) Fbs2 is a new member of the E3 ubiquitin ligase family that recognizes sugar chains. J. Biol. Chem. 278, 43877-43884
36. Swanton, E., High, S., and Woodman, P. (2003) Role of calnexin in the glycan-independent quality control of proteolipid protein. EMBO J. 22, 2948-2958
37. Leach, M. R., and Williams, D. B. (2004) Lectin-deficient calnexin is capable of binding class I histocompatibility molecules in vivo and preventing their degradation. J. Biol. Chem. 279, 9072-9079
38. Hosokawa, N., Wada, I., Natsuka, Y., and Nagata, K. (2006) EDEM accelerates ERAD by preventing aberrant dimer formation of misfolded α1- antitrypsin. Genes Cells 11, 465-476
39. Olivari, S., Cali, T., Salo, K. E., Paganetti, P., Ruddock, L. W., and Molinari, M. (2006) EDEM1 regulates ER-associated degradation by accelerating de-mannosylation of folding-defective polypeptides and by inhibiting their covalent aggregation. Biochem. Biophys. Res. Commun. 349, 1278-1284
40. Ushioda, R., Hoseki, J., Araki, K., Jansen, G., Thomas, D. Y., and Nagata, K. (2008) ERdj5 is required as a disulfide reductase for degradation of misfolded proteins in the ER. Science 321, 569-572
41. Hosokawa, N., Tremblay, L. O., Sleno, B., Kamiya, Y., Wada, I., Nagata, K., Kato, K., and Herscovics, A. (2010) EDEM1 accelerates the trimming of α1,2-linked mannose on the C branch of N-glycans. Glycobiology 20, 567-575
42. Cormier, J. H., Tamura, T., Sunryd, J. C., and Hebert, D. N. (2009) EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. Mol. Cell 34, 627-633
43. Slominska-Wojewodzka, M., Gregers, T. F., Wälchli, S., and Sandvig, K. (2006) EDEM is involved in retrotranslocation of ricin from the endoplasmic reticulum to the cytosol. Mol. Biol. Cell 17, 1664-1675
44. Marin, M. B., Ghenea, S., Spiridon, L. N., Chiritoiu, G. N., Petrescu, A. J., and Petrescu, S. M. (2012) Tyrosinase degradation is prevented when EDEM1 lacks the intrinsically disordered region. PLoS ONE 7, e42998
45. Nakatsukasa, K., Nishikawa, S., Hosokawa, N., Nagata, K., and Endo, T. (2001) Mnl1p, an α-mannosidase-like protein in yeast Saccharomyces cerevisiae, is required for endoplasmic reticulum-associated degradation of glycoproteins. J. Biol. Chem. 276, 8635-8638
46. Jakob, C. A., Bodmer, D., Spirig, U., Battig, P., Marcil, A., Dignard, D., Bergeron, J. J., Thomas, D. Y., and Aebi, M. (2001) Htm1p, a mannosidaselike protein, is involved in glycoprotein degradation in yeast. EMBO Rep. 2, 423-430
47. 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
48. Bernasconi, R., Pertel, T., Luban, J., and Molinari, M. (2008)Adual task for the Xbp1-responsive OS-9 variants in the mammalian endoplasmic reticulum. Inhibiting secretion of misfolded protein conformers and enhancing their disposal. J. Biol. Chem. 283, 16446-16454
49. Hosokawa, N., Wada, I., Nagasawa, K., Moriyama, T., Okawa, K., and Nagata, K. (2008) Human XTP3-B forms an endoplasmic reticulum quality control scaffold with the HRD1-SEL1L ubiquitin ligase complex and BiP. J. Biol. Chem. 283, 20914-20924
50. Izawa, T., Nagai, H., Endo, T., and Nishikawa, S. (2012) Yos9p and Hrd1p mediate ER retention of misfolded proteins for ER-associated degradation. Mol. Biol. Cell 23, 1283-1293
51. Jaenicke, L. A., Brendebach, H., Selbach, M., and Hirsch, C. (2011) Yos9p assists in the degradation of certain nonglycosylated proteins from the endoplasmic reticulum. Mol. Biol. Cell 22, 2937-2945
52. Yamaguchi, Y., Hirao, T., Sakata, E., Kamiya, Y., Kurimoto, E., Yoshida, Y., Suzuki, T., Tanaka, K., and Kato, K. (2007) Fbs1 protects the malfolded glycoproteins from the attack of peptide:N-glycanase. Biochem. Biophys. Res. Commun. 362, 712-716
53. Claessen, J. H., Kundrat, L., and Ploegh, H. L. (2012) Protein quality control in the ER. Balancing the ubiquitin checkbook. Trends Cell Biol. 22, 22-32