Forcible destruction of severely misfolded mammalian glycoproteins by the non-glycoprotein ERAD pathway

Journal of Cell Biology

Volumn 211, Issue 4, 2015, Pages 775-784

  Ninagawa, Satoshi ^a,b,c   Okada, Tetsuya ^a   Sumitomo, Yoshiki ^a   Horimoto, Satoshi ^a   Sugimoto, Takehiro ^a   Ishikawa, Tokiro ^a   Takeda, Shunichi ^a   Yamamoto, Takashi ^d   Suzuki, Tadashi ^e   Kamiya, Yukiko ^b,c,g   Kato, Koichi ^b,c,f   Mori, Kazutoshi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b INSTITUTE FOR MOLECULAR SCIENCE   (Japan)

^c OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

^e RIK EN Global Research Cluster   (Japan)

^f NAGOYA CITY UNIVERSITY   (Japan)

^g NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 6; ACTIVATING TRANSCRIPTION FACTOR 6 ALPHA; CD3 ANTIGEN; GLYCOPROTEIN; UNCLASSIFIED DRUG; ALPHA MANNOSIDASE; ATF6 PROTEIN, HUMAN; CALCIUM BINDING PROTEIN; EDEM1 PROTEIN, HUMAN; EDEM2 PROTEIN, HUMAN; EDEM3 PROTEIN, HUMAN; MANNOSIDASE; MEMBRANE PROTEIN;

ARTICLE; DEGLYCOSYLATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; INDEL MUTATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN GLYCOSYLATION; PROTEIN HOMEOSTASIS; PROTEIN QUALITY; TURNOVER TIME; GENE INACTIVATION; GENETICS; HCT 116 CELL LINE; METABOLISM;

ACTIVATING TRANSCRIPTION FACTOR 6; ALPHA-MANNOSIDASE; CALCIUM-BINDING PROTEINS; ENDOPLASMIC RETICULUM STRESS; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; GENE KNOCKOUT TECHNIQUES; GLYCOPROTEINS; HCT116 CELLS; HUMANS; MANNOSIDASES; MEMBRANE PROTEINS; PROTEIN FOLDING;

EID: 84970979593     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201504109     Document Type: Article

References (31)

1. Aikawa, J., I. Matsuo, and Y. Ito. 2012. In vitro mannose trimming property of human ER α-1,2 mannosidase I. Glycoconj. J. 29:35-45. http://dx.doi.org/10.1007/s10719-011-9362-1
2. Bernasconi, R., C. Galli, V. Calanca, T. Nakajima, and M. Molinari. 2010. Stringent requirement for HRD1, SEL1L, and OS-9/XTP3-B for disposal of ERAD-LS substrates. J. Cell Biol. 188:223-235. http://dx.doi.org/10.1083/jcb.200910042
3. Brodsky, J.L. 2012. Cleaning up: ER-associated degradation to the rescue. Cell. 151:1163-1167. http://dx.doi.org/10.1016/j.cell.2012.11.012
4. Fujimori, T., Y. Kamiya, K. Nagata, K. Kato, and N. Hosokawa. 2013. Endoplasmic reticulum lectin XTP3-B inhibits endoplasmic reticulum-associated degradation of a misfolded a1-antitrypsin variant. FEBS J. 280:1563-1575. http://dx.doi.org/10.1111/febs.12157
5. Haze, K., H. Yoshida, H. Yanagi, T. Yura, and K. Mori. 1999. Mammalian transcription factor ATF6 is synthesized as a transmembrane protein and activated by proteolysis in response to endoplasmic reticulum stress. Mol. Biol. Cell. 10:3787-3799. http://dx.doi.org/10.1091/mbc.10.11.3787
6. Hirao, K., Y. Natsuka, T. Tamura, I. Wada, D. Morito, S. Natsuka, P. Romero, B. Sleno, L.O. Tremblay, A. Herscovics, et al. 2006. EDEM3, a soluble EDEM homolog, enhances glycoprotein endoplasmic reticulum-associated degradation and mannose trimming. J. Biol. Chem. 281:9650-9658. http://dx.doi.org/10.1074/jbc.M512191200
7. Horimoto, S., S. Ninagawa, T. Okada, H. Koba, T. Sugimoto, Y. Kamiya, K. Kato, S. Takeda, and K. Mori. 2013. The unfolded protein response transducer ATF6 represents a novel transmembrane-type endoplasmic reticulum-associated degradation substrate requiring both mannose trimming and SEL1L protein. J. Biol. Chem. 288:31517-31527. http://dx.doi.org/10.1074/jbc.M113.476010
8. Hosokawa, N., I. Wada, K. Hasegawa, T. Yorihuzi, L.O. Tremblay, A. Herscovics, and K. Nagata. 2001. A novel ER α-mannosidase-like protein accelerates ER-associated degradation. EMBO Rep. 2:415-422. http://dx.doi.org/10.1093/embo-reports/kve084
9. Hosokawa, N., I. Wada, K. Nagasawa, T. Moriyama, K. Okawa, and K. Nagata. 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. http://dx.doi.org/10.1074/jbc.M709336200
10. Hosokawa, N., Y. Kamiya, and K. Kato. 2010. The role of MRH domain-containing lectins in ERAD. Glycobiology. 20:651-660. http://dx.doi.org/10.1093/glycob/cwq013
11. Huang, C., Y. Harada, A. Hosomi, Y. Masahara-Negishi, J. Seino, H. Fujihira, Y. Funakoshi, T. Suzuki, N. Dohmae, and T. Suzuki. 2015. Endo-β-N-acetylglucosaminidase forms N-GlcNAc protein aggregates during ER-associated degradation in Ngly1-defective cells. Proc. Natl. Acad. Sci. USA. 112:1398-1403. http://dx.doi.org/10.1073/pnas.1414593112
12. Izawa, T., H. Nagai, T. Endo, and S. Nishikawa. 2012. Yos9p and Hrd1p mediate ER retention of misfolded proteins for ER-associated degradation. Mol. Biol. Cell. 23:1283-1293. http://dx.doi.org/10.1091/mbc.E11-08-0722
13. Jakob, C.A., D. Bodmer, U. Spirig, P. Battig, A. Marcil, D. Dignard, J.J. Bergeron, D.Y. Thomas, and M. Aebi. 2001. Htm1p, a mannosidase-like protein, is involved in glycoprotein degradation in yeast. EMBO Rep. 2:423-430. http://dx.doi.org/10.1093/embo-reports/kve089
14. Jonikas, M.C., S.R. Collins, V. Denic, E. Oh, E.M. Quan, V. Schmid, J. Weibezahn, B. Schwappach, P. Walter, J.S. Weissman, and M. Schuldiner. 2009. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science. 323:1693-1697. http://dx.doi.org/10.1126/science.1167983
15. Kamiya, Y., T. Satoh, and K. Kato. 2012. Molecular and structural basis for N-glycan-dependent determination of glycoprotein fates in cells. Biochim. Biophys. Acta. 1820:1327-1337. http://dx.doi.org/10.1016/j.bbagen.2011.12.017
16. Kopec, K.O., and A.N. Lupas. 2013. β-Propeller blades as ancestral peptides in protein evolution. PLoS One. 8:e77074. (published erratum appears in PLoS One. 2014. 9. http://dx.doi.org/10.1371/annotation/fee01544-ff98-4ed2-9dc9-7aea9c5fe828) http://dx.doi.org/10.1371/journal.pone.0077074
17. Kostova, Z., and D.H. Wolf. 2005. Importance of carbohydrate positioning in the recognition of mutated CPY for ER-associated degradation. J. Cell Sci. 118:1485-1492. http://dx.doi.org/10.1242/jcs.01740
18. Liu, Y., P. Choudhury, C.M. Cabral, and R.N. Sifers. 1999. Oligosaccharide modification in the early secretory pathway directs the selection of a misfolded glycoprotein for degradation by the proteasome. J. Biol. Chem. 274:5861-5867. http://dx.doi.org/10.1074/jbc.274.9.5861
19. Mast, S.W., K. Diekman, K. Karaveg, A. Davis, R.N. Sifers, and K.W. Moremen. 2005. Human EDEM2, a novel homolog of family 47 glycosidases, is involved in ER-associated degradation of glycoproteins. Glycobiology. 15:421-436. http://dx.doi.org/10.1093/glycob/cwi014
20. Misaghi, S., M.E. Pacold, D. Blom, H.L. Ploegh, and G.A. Korbel. 2004. Using a small molecule inhibitor of peptide: N-glycanase to probe its role in glycoprotein turnover. Chem. Biol. 11:1677-1687. http://dx.doi.org/10.1016/j.chembiol.2004.11.010
21. Molinari, M. 2007. N-glycan structure dictates extension of protein folding or onset of disposal. Nat. Chem. Biol. 3:313-320. http://dx.doi.org/10.1038/nchembio880
22. Ninagawa, S., T. Okada, S. Takeda, and K. Mori. 2011. SEL1L is required for endoplasmic reticulum-associated degradation of misfolded luminal proteins but not transmembrane proteins in chicken DT40 cell line. Cell Struct. Funct. 36:187-195. http://dx.doi.org/10.1247/csf.11018
23. Ninagawa, S., T. Okada, Y. Sumitomo, Y. Kamiya, K. Kato, S. Horimoto, T. Ishikawa, S. Takeda, T. Sakuma, T. Yamamoto, and K. Mori. 2014. EDEM2 initiates mammalian glycoprotein ERAD by catalyzing the first mannose trimming step. J. Cell Biol. 206:347-356. http://dx.doi.org/10.1083/jcb.201404075
24. Pan, S., S. Wang, B. Utama, L. Huang, N. Blok, M.K. Estes, K.W. Moremen, and R.N. Sifers. 2011. Golgi localization of ERManI defines spatial separation of the mammalian glycoprotein quality control system. Mol. Biol. Cell. 22:2810-2822. http://dx.doi.org/10.1091/mbc.E11-02-0118
25. Rosenbaum, J.C., E.K. Fredrickson, M.L. Oeser, C.M. Garrett-Engele, M.N. Locke, L.A. Richardson, Z.W. Nelson, E.D. Hetrick, T.I. Milac, D.E. Gottschling, and R.G. Gardner. 2011. Disorder targets misorder in nuclear quality control degradation: a disordered ubiquitin ligase directly recognizes its misfolded substrates. Mol. Cell. 41:93-106. http://dx.doi.org/10.1016/j.molcel.2010.12.004
26. Sambrook, J., E.F. Fritsch, and T. Maniatis. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. 1626 pp
27. Sifers, R.N., S. Brashears-Macatee, V.J. Kidd, H. Muensch, and S.L. Woo. 1988. A frameshift mutation results in a truncated alpha 1-antitrypsin that is retained within the rough endoplasmic reticulum. J. Biol. Chem. 263:7330-7335
28. Smith, M.H., H.L. Ploegh, and J.S. Weissman. 2011. Road to ruin: targeting proteins for degradation in the endoplasmic reticulum. Science. 334:1086-1090. http://dx.doi.org/10.1126/science.1209235
29. Ushioda, R., J. Hoseki, and K. Nagata. 2013. Glycosylation-independent ERAD pathway serves as a backup system under ER stress. Mol. Biol. Cell. 24:3155-3163. http://dx.doi.org/10.1091/mbc.E13-03-0138
30. Xie, W., and D.T. Ng. 2010. ERAD substrate recognition in budding yeast. Semin. Cell Dev. Biol. 21:533-539. http://dx.doi.org/10.1016/j.semcdb.2010.02.007
31. Xu, C., S. Wang, G. Thibault, and D.T. Ng. 2013. Futile protein folding cycles in the ER are terminated by the unfolded protein O-mannosylation pathway. Science. 340:978-981. http://dx.doi.org/10.1126/science.1234055