Posttranscriptional Regulation of Glycoprotein Quality Control in the Endoplasmic Reticulum Is Controlled by the E2 Ub-Conjugating Enzyme UBC6e

Molecular Cell

Volumn 63, Issue 5, 2016, Pages 753-767

  Hagiwara, Masatoshi ^a   Ling, Jingjing ^a   Koenig, Paul Albert ^a   Ploegh, Hidde L ^a,b  

^a WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA MANNOSIDASE; DERLIN 2 PROTEIN; EDEM1 PROTEIN; GLUCOSYLTRANSFERASE; GLYCAN; GLYCOPROTEIN; KIFUNENSINE; OS 9 PROTEIN; PROTEIN; SEL1L PROTEIN; UBIQUITIN CONJUGATING ENZYME E2; UNCLASSIFIED DRUG; DERL2 PROTEIN, HUMAN; EDEM1 PROTEIN, HUMAN; LECTIN; MEMBRANE PROTEIN; OS9 PROTEIN, HUMAN; SEL1L PROTEIN, HUMAN; TUMOR PROTEIN; UBE2J1 PROTEIN, HUMAN; UBIQUITIN CONJUGATING ENZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENHANCER REGION; ENZYME ACTIVITY; ENZYME DEGRADATION; GENETIC TRANSCRIPTION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; POSTTRANSCRIPTIONAL REGULATION; PROTEIN DEGRADATION; QUALITY CONTROL; TISSUE CULTURE; UNFOLDED PROTEIN RESPONSE; UPREGULATION; ANIMAL; CHEMISTRY; CYTOLOGY; DEFICIENCY; FIBROBLAST; GENE VECTOR; GENETICS; GLYCOSYLATION; HEK293 CELL LINE; HUMAN; LENTIVIRINAE; METABOLISM; PROTEIN PROCESSING;

ANIMALS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; FIBROBLASTS; GENETIC VECTORS; GLYCOSYLATION; HEK293 CELLS; HUMANS; LECTINS; LENTIVIRUS; MEMBRANE PROTEINS; MICE; NEOPLASM PROTEINS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEINS; PROTEOLYSIS; UBIQUITIN-CONJUGATING ENZYMES; UNFOLDED PROTEIN RESPONSE;

EID: 84992445790     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2016.07.014     Document Type: Article

References (46)

1. Burr, M.L., Cano, F., Svobodova, S., Boyle, L.H., Boname, J.M., Lehner, P.J., HRD1 and UBE2J1 target misfolded MHC class I heavy chains for endoplasmic reticulum-associated degradation. Proc. Natl. Acad. Sci. USA 108 (2011), 2034–2039.
2. Christianson, J.C., Shaler, T.A., Tyler, R.E., Kopito, R.R., OS-9 and GRP94 deliver mutant α1-antitrypsin to the Hrd1-SEL1L ubiquitin ligase complex for ERAD. Nat. Cell Biol. 10 (2008), 272–282.
3. Claessen, J.H.L., Mueller, B., Spooner, E., Pivorunas, V.L., Ploegh, H.L., The transmembrane segment of a tail-anchored protein determines its degradative fate through dislocation from the endoplasmic reticulum. J. Biol. Chem. 285 (2010), 20732–20739.
4. Cormier, J.H., Tamura, T., Sunryd, J.C., Hebert, D.N., EDEM1 recognition and delivery of misfolded proteins to the SEL1L-containing ERAD complex. Mol. Cell 34 (2009), 627–633.
5. Dougan, S.K., Hu, C.-C.A., Paquet, M.-E., Greenblatt, M.B., Kim, J., Lilley, B.N., Watson, N., Ploegh, H.L., Derlin-2-deficient mice reveal an essential role for protein dislocation in chondrocytes. Mol. Cell. Biol. 31 (2011), 1145–1159.
6. Ellgaard, L., Frickel, E.-M., Calnexin, calreticulin, and ERp57: teammates in glycoprotein folding. Cell Biochem. Biophys. 39 (2003), 223–247.
7. Fagioli, C., Sitia, R., Glycoprotein quality control in the endoplasmic reticulum. Mannose trimming by endoplasmic reticulum mannosidase I times the proteasomal degradation of unassembled immunoglobulin subunits. J. Biol. Chem. 276 (2001), 12885–12892.
8. Guerriero, C.J., Brodsky, J.L., The delicate balance between secreted protein folding and endoplasmic reticulum-associated degradation in human physiology. Physiol. Rev. 92 (2012), 537–576.
9. Hampton, R.Y., Garza, R.M., Protein quality control as a strategy for cellular regulation: lessons from ubiquitin-mediated regulation of the sterol pathway. Chem. Rev. 109 (2009), 1561–1574.
10. Helenius, A., Trombetta, E.S., Hebert, D.N., Simons, J.F., Calnexin, calreticulin and the folding of glycoproteins. Trends Cell Biol. 7 (1997), 193–200.
11. Hetz, C., Chevet, E., Oakes, S.A., Proteostasis control by the unfolded protein response. Nat. Cell Biol. 17 (2015), 829–838.
12. Hirao, K., Natsuka, Y., Tamura, T., Wada, I., Morito, D., Natsuka, S., Romero, P., Sleno, B., Tremblay, L.O., Herscovics, A., et al. EDEM3, a soluble EDEM homolog, enhances glycoprotein endoplasmic reticulum-associated degradation and mannose trimming. J. Biol. Chem. 281 (2006), 9650–9658.
13. Hosokawa, N., Wada, I., Hasegawa, K., Yorihuzi, T., Tremblay, L.O., Herscovics, A., Nagata, K., A novel ER alpha-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep. 2 (2001), 415–422.
14. Iida, Y., Fujimori, T., Okawa, K., Nagata, K., Wada, I., Hosokawa, N., SEL1L protein critically determines the stability of the HRD1-SEL1L endoplasmic reticulum-associated degradation (ERAD) complex to optimize the degradation kinetics of ERAD substrates. J. Biol. Chem. 286 (2011), 16929–16939.
15. Kaneko, M., Koike, H., Saito, R., Kitamura, Y., Okuma, Y., Nomura, Y., Loss of HRD1-mediated protein degradation causes amyloid precursor protein accumulation and amyloid-beta generation. J. Neurosci. 30 (2010), 3924–3932.
16. Koenig, P.-A., Ploegh, H.L., Protein quality control in the endoplasmic reticulum. F1000Prime Rep., 6, 2014, 49.
17. Koenig, P.-A., Nicholls, P.K., Schmidt, F.I., Hagiwara, M., Maruyama, T., Frydman, G.H., Watson, N., Page, D.C., Ploegh, H.L., The E2 ubiquitin-conjugating enzyme UBE2J1 is required for spermiogenesis in mice. J. Biol. Chem. 289 (2014), 34490–34502.
18. Lenk, U., Yu, H., Walter, J., Gelman, M.S., Hartmann, E., Kopito, R.R., Sommer, T., A role for mammalian Ubc6 homologues in ER-associated protein degradation. J. Cell Sci. 115 (2002), 3007–3014.
19. Lilley, B.N., Ploegh, H.L., A membrane protein required for dislocation of misfolded proteins from the ER. Nature 429 (2004), 834–840.
20. Menon, M.B., Tiedje, C., Lafera, J., Ronkina, N., Konen, T., Kotlyarov, A., Gaestel, M., Endoplasmic reticulum-associated ubiquitin-conjugating enzyme Ube2j1 is a novel substrate of MK2 (MAPKAP kinase-2) involved in MK2-mediated TNFα production. Biochem. J. 456 (2013), 163–172.
21. 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 (2003), 1397–1400.
22. Morito, D., Nagata, K., Pathogenic hijacking of ER-associated degradation: Is ERAD flexible?. Mol. Cell 59 (2015), 335–344.
23. Mueller, B., Lilley, B.N., Ploegh, H.L., SEL1L, the homologue of yeast Hrd3p, is involved in protein dislocation from the mammalian ER. J. Cell Biol. 175 (2006), 261–270.
24. Mueller, B., Klemm, E.J., Spooner, E., Claessen, J.H., Ploegh, H.L., SEL1L nucleates a protein complex required for dislocation of misfolded glycoproteins. Proc. Natl. Acad. Sci. USA 105 (2008), 12325–12330.
25. Ninagawa, S., Okada, T., Sumitomo, Y., Kamiya, Y., Kato, K., Horimoto, S., Ishikawa, T., Takeda, S., Sakuma, T., Yamamoto, T., Mori, K., EDEM2 initiates mammalian glycoprotein ERAD by catalyzing the first mannose trimming step. J. Cell Biol. 206 (2014), 347–356.
26. Noack, J., Bernasconi, R., Molinari, M., How viruses hijack the ERAD tuning machinery. J. Virol. 88 (2014), 10272–10275.
27. Oda, Y., Hosokawa, N., Wada, I., Nagata, K., EDEM as an acceptor of terminally misfolded glycoproteins released from Calnexin. Science 299 (2003), 1394–1397.
28. Olivari, S., Galli, C., Alanen, H., Ruddock, L., Molinari, M., A novel stress-induced EDEM variant regulating endoplasmic reticulum-associated glycoprotein degradation. J. Biol. Chem. 280 (2005), 2424–2428.
29. Palade, G., Intracellular aspects of the process of protein synthesis. Science, 189, 1975, 867.
30. Reggiori, F., Monastyrska, I., Verheije, M.H., Calì, T., Ulasli, M., Bianchi, S., Bernasconi, R., de Haan, C.A., Molinari, M., Coronaviruses hijack the LC3-I-positive EDEMosomes, ER-derived vesicles exporting short-lived ERAD regulators, for replication. Cell Host Microbe 7 (2010), 500–508.
31. Satoh, T., Chen, Y., Hu, D., Hanashima, S., Yamamoto, K., Yamaguchi, Y., Structural basis for oligosaccharide recognition of misfolded glycoproteins by OS-9 in ER-associated degradation. Mol. Cell 40 (2010), 905–916.
32. Seth, R.B., Sun, L., Ea, C.-K., Chen, Z.J., Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122 (2005), 669–682.
33. Sifers, R.N., Brashears-Macatee, S., Kidd, V.J., Muensch, H., Woo, S.L.C., A frameshift mutation results in a truncated alpha 1-antitrypsin that is retained within the rough endoplasmic reticulum. J. Biol. Chem. 263 (1988), 7330–7335.
34. Smith, M.H., Ploegh, H.L., Weissman, J.S., Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science 334 (2011), 1086–1090.
35. Stein, A., Ruggiano, A., Carvalho, P., Rapoport, T.A., Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158 (2014), 1375–1388.
36. Sun, S., Shi, G., Han, X., Francisco, A.B., Ji, Y., Mendonça, N., Liu, X., Locasale, J.W., Simpson, K.W., Duhamel, G.E., et al. Sel1L is indispensable for mammalian endoplasmic reticulum-associated degradation, endoplasmic reticulum homeostasis, and survival. Proc. Natl. Acad. Sci. USA 111 (2014), E582–E591.
37. Svedine, S., Wang, T., Halaban, R., Hebert, D.N., Carbohydrates act as sorting determinants in ER-associated degradation of tyrosinase. J. Cell Sci. 117 (2004), 2937–2949.
38. Toyofuku, K., Wada, I., Spritz, R.A., Hearing, V.J., The molecular basis of oculocutaneous albinism type 1 (OCA1): sorting failure and degradation of mutant tyrosinases results in a lack of pigmentation. Biochem. J. 355 (2001), 259–269.
39. Tsao, Y.S., Ivessa, N.E., Adesnik, M., Sabatini, D.D., Kreibich, G., Carboxy terminally truncated forms of ribophorin I are degraded in pre-Golgi compartments by a calcium-dependent process. J. Cell Biol. 116 (1992), 57–67.
40. van Wijk, S.J.L., Timmers, H.T.M., The family of ubiquitin-conjugating enzymes (E2s): deciding between life and death of proteins. FASEB J. 24 (2010), 981–993.
41. Wang, N., Hebert, D.N., Tyrosinase maturation through the mammalian secretory pathway: bringing color to life. Pigment Cell Res. 19 (2006), 3–18.
42. Wiertz, E.J.H.J., Jones, T.R., Sun, L., Bogyo, M., Geuze, H.J., Ploegh, H.L., The human cytomegalovirus US11 gene product dislocates MHC class I heavy chains from the endoplasmic reticulum to the cytosol. Cell 84 (1996), 769–779.
43. Xu, C., Ng, D.T.W., Glycosylation-directed quality control of protein folding. Nat. Rev. Mol. Cell Biol. 16 (2015), 742–752.
44. Yagishita, N., Ohneda, K., Amano, T., Yamasaki, S., Sugiura, A., Tsuchimochi, K., Shin, H., Kawahara, K., Ohneda, O., Ohta, T., et al. Essential role of synoviolin in embryogenesis. J. Biol. Chem. 280 (2005), 7909–7916.
45. Yoshida, H., Matsui, T., Hosokawa, N., Kaufman, R.J., Nagata, K., Mori, K., A time-dependent phase shift in the mammalian unfolded protein response. Dev. Cell 4 (2003), 265–271.
46. Younger, J.M., Chen, L., Ren, H.-Y., Rosser, M.F.N., Turnbull, E.L., Fan, C.-Y., Patterson, C., Cyr, D.M., Sequential quality-control checkpoints triage misfolded cystic fibrosis transmembrane conductance regulator. Cell 126 (2006), 571–582.