A Case for Sec61 Channel Involvement in ERAD

Trends in Biochemical Sciences

Volumn 42, Issue 3, 2017, Pages 171-179

  Römisch, Karin ^a  

^a SAARLAND UNIVERSITY   (Germany)

Author keywords

antigen cross presentation; Der1; ER associated degradation; Hrd1; proteasome 19S regulatory particle; Sec61 channel

Indexed keywords

CELL PROTEIN; DER1 PROTEIN; HRD1 PROTEIN; PROTEASOME; PROTEIN P97; PROTEINASE; SEC61 CHANNEL; SECRETORY PROTEIN; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; 26S PROTEASOME NON-ATPASE REGULATORY SUBUNIT 13; SEC61A1 PROTEIN, HUMAN; TRANSLOCON;

ALLELE; BIOGENESIS; CYTOSOL; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME ACTIVITY; HUMAN; MAMMAL CELL; MOLECULAR DYNAMICS; MUTANT; NONHUMAN; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN MISFOLDING; PROTEIN TRANSPORT; REVIEW; TEMPERATURE SENSITIVITY; ENDOPLASMIC RETICULUM; GENETICS; METABOLISM; PHYSIOLOGY;

ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; HUMANS; PROTEASOME ENDOPEPTIDASE COMPLEX; SEC TRANSLOCATION CHANNELS;

EID: 85007586487     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2016.10.005     Document Type: Review

References (75)

1. 1 Xie, W., Ng, D.T., ERAD substrate recognition in budding yeast. Semin. Cell Dev. Biol. 21 (2010), 533–539.
2. 2 Schlenstedt, G., et al. A large presecretory protein translocates both cotranslationally, using SRP and ribosome, and posttranslationally, without these ribonucleoparticles, when synthesized in the presence of mammalian microsomes. J. Biol. Chem. 265 (1990), 13960–13968.
3. 3 Wiertz, E.J., et al. Sec61-mediated transfer of a membrane protein from the endoplasmic reticulum to the proteasome for destruction. Nature 384 (1996), 432–438.
4. 4 Pilon, M., et al. Sec61p mediates export of a misfolded secretory protein from the endoplasmic reticulum to the cytosol for degradation. EMBO J. 16 (1997), 4540–4548.
5. 5 Burr, M.L., et al. MHC class I molecules are preferentially ubiquitinated on endoplasmic reticulum lumenal residues during Hrd1 ubiquitin E3 ligase-mediated dislocation. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 14290–14295.
6. 6 Schmitz, A., et al. Cholera toxin is exported from microsomes by the Sec61p complex. J. Cell Biol. 148 (2000), 1203–1212.
7. 7 Pilon, M., et al. Cold-sensitive mutations in SEC61 cause defects in initiation of protein translocation into the yeast endoplasmic reticulum. Mol. Biol. Cell 9 (1998), 3455–3473.
8. 8 Gillece, P., et al. Export of a cysteine-free misfolded secretory protein from the ER for degradation requires interaction with protein disulfide isomerase. J. Cell Biol. 147 (1999), 1443–1456.
9. 9 Ng, D.T., et al. The unfolded protein response regulates multiple aspects of secretory and membrane protein biogenesis and ER quality control. J. Cell Biol. 150 (2000), 77–88.
10. 10 Wahlman, J., et al. Real-time fluorescence detection of ERAD substrate retrotranslocation in a mammalian in vitro system. Cell 129 (2007), 943–955.
11. 11 Gillece, P., et al. The protein translocation channel mediates glycopeptide export across the endoplasmic reticulum membrane. Proc. Natl. Acad. Sci. U.S.A. 97 (2000), 4609–4614.
12. 12 Zattas, D., et al. N-terminal acetylation of the yeast Derlin Der1 is essential for Hrd1 ubiquitin-ligase activity toward luminal ER substrates. Mol. Biol. Cell 24 (2013), 890–900.
13. 13 Mehnert, M., et al. Der1 promotes movement of misfolded proteins through the endoplasmic reticulum membrane. Nat. Cell Biol. 16 (2014), 77–86.
14. 14 Knop, M., et al. Der1, a novel protein specifically required for endoplasmic reticulum degradation in yeast. EMBO J. 15 (1996), 753–763.
15. 15 Delic, M., et al. The secretory pathway: exploring yeast diversity. FEMS Microbiol. Rev. 37 (2013), 872–914.
16. 16 Conti, B.J., et al. Cotranslational stabilization of Sec62/63 within the ER Sec61 translocon is controlled by distinct substrate-driven translocation events. Mol. Cell 58 (2015), 269–283.
17. 17 Hennon, S.W., et al. YidC/Alb3/Oxa1 family of insertases. J. Biol. Chem. 290 (2015), 14866–14874.
18. 18 Bays, N.W., et al. Hrd1p/Der3p is a membrane-anchored ubiquitin ligase required for ER-associated degradation. Nat. Cell Biol. 3 (2001), 24–29.
19. 19 Vashist, S., Ng, D.T., Misfolded proteins are sorted by a sequential checkpoint mechanism of ER quality control. J. Cell Biol. 165 (2004), 41–52.
20. 20 Zattas, D., Hochstrasser, M., Ubiquitin-dependent protein degradation at the yeast endoplasmic reticulum and nuclear envelope. Crit. Rev. Biochem. Mol. Biol. 50 (2015), 1–17.
21. 21 Stein, A., et al. Key steps in ERAD of luminal ER proteins reconstituted with purified components. Cell 158 (2014), 1375–1388.
22. 22 Garza, R.M., et al. In vitro analysis of Hrd1p-mediated retrotranslocation of its multi-spanning membrane substrate HMG-CoA reductase. J. Biol. Chem. 284 (2009), 14710–14722.
23. 23 Baldridge, R.D., Rapoport, T.A., Autoubiquitination fo the Hrd1 ligase triggers protein retrotranslocation and ERAD. Cell 166 (2016), 1–14.
24. 24 Grotzke, J.E., et al. Deglycosylation-dependent fluorescent proteins provide unique tools for the study of ER-associated degradation. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 3393–3398.
25. 25 Biederer, T., et al. Degradation of subunits of the Sec61p complex, an integral component of the ER membrane, by the ubiquitin-proteasome pathway. EMBO J. 15 (1996), 2069–2076.
26. 26 Voorhees, R.M., et al. Structure of the mammalian ribosome-Sec61 complex to 3.4 Å resolution. Cell 157 (2014), 1632–1643.
27. 27 Park, E., et al. Structure of the SecY channel during initiation of protein translocation. Nature 506 (2014), 102–106.
28. 28 Voorhees, R.M., Hegde, R.S., Toward a structural understanding of co-translational protein translocation. Curr. Opin. Cell Biol. 41 (2016), 91–99.
29. 29 Wilkinson, B.M., et al. Distinct domains within yeast Sec61p involved in post-translational translocation and protein dislocation. J. Biol. Chem. 275 (2000), 521–529.
30. 30 Junne, T., et al. The plug domain of yeast Sec61p is important for efficient protein translocation, but not essential for cell viability. Mol. Biol. Cell 17 (2006), 4063–4068.
31. 31 Junne, T., et al. The hydrophobic core of the Sec61 translocon defines the hydrophobicity threshold for membrane integration. Mol. Biol. Cell 21 (2010), 1662–1670.
32. 32 Trueman, S.F., et al. A gating motif in the translocation channel sets the hydrophobicity threshold for signal sequence function. J. Cell Biol. 199 (2012), 907–918.
33. 33 Lloyd, D.J., et al. A point mutation in Sec61alpha1 leads to diabetes and hepatosteatosis in mice. Diabetes 59 (2010), 460–470.
34. 34 Schäuble, N., et al. BiP-mediated closing of the Sec61 channel limits Ca2+ leakage from the ER. EMBO J. 31 (2012), 3282–3296.
35. 35 Wheeler, M.C., Gekakis, N., Defective ER associated degradation of a model luminal substrate in yeast carrying a mutation in the 4th ER luminal loop of Sec61p. Biochem. Biophys. Res. Commun. 427 (2012), 768–773.
36. 36 Tretter, T., et al. ERAD and translocation defects in a sec61 mutant lacking ER-lumenal loop 7. BMC Cell Biol., 14, 2013, 56.
37. 37 Kaiser, M., Römisch, K., Proteasome 19S RP binding to the Sec61 channel plays a key role in ERAD. PLoS One, 10, 2015, e0117260.
38. 38 Lee, R.J., et al. The 19S (PA700) cap of the 26S proteasome is sufficient to retro-translocate and deliver a soluble polypeptide for ER-associated degradation (ERAD). EMBO J. 23 (2004), 2206–2215.
39. 39 Morris, L.L., et al. Sequential actions of the AAA-ATPase p97 and the proteasome 19S RP in sterol-accelerated ERAD of HMG CoA reductase. J. Biol. Chem. 289 (2014), 19053–19066.
40. 40 Corey, R.A., et al. Unlocking the bacterial SecY translocon. Structure 24 (2016), 518–527.
41. 41 Kalies, K.U., et al. The protein translocation channel binds proteasomes to the endoplasmic reticulum. EMBO J. 24 (2005), 2284–2293.
42. 42 Sasset, L., et al. The VCP/p97 and YOD1 proteins have different substrate-dependent activities in ERAD. J. Biol. Chem. 290 (2015), 28175–28188.
43. 43 Li, S., et al. Cytosolic entry of shiga-like toxin A chain from the yeast ER requires catalytically active Hrd1p. PLoS One, 7, 2012, e41119.
44. 44 Ng, W., et al. Characterization of the proteasome interaction with the Sec61 channel in the endoplasmic reticulum. J. Cell Sci. 120 (2007), 682–691.
45. 45 Schäfer, A., Wolf, D.H., Sec61p is part of the endoplasmic reticulum-associated degradation machinery. EMBO J. 28 (2009), 2874–2884.
46. 46 Denic, V., et al. A luminal surveillance complex that selects misfolded glycoproteins for ER-associated degradation. Cell 126 (2006), 349–359.
47. 47 Carvalho, P., et al. Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126 (2006), 361–373.
48. 48 Eshragi, A., et al. Cytolethal distending toxins require components of the ERAD pathway for host cell entry. PLoS Pathog., 10, 2014, e1004295.
49. 49 Moreau, D., et al. Genome-wide RNAi screens identify genes required for ricin and PE intoxications. Dev. Cell 21 (2011), 231–244.
50. 50 Kalies, K.U., Römisch, K., Inhibitors of protein translocation across the ER membrane. Traffic 16 (2015), 1027–1038.
51. 51 Spooner, R.A., Lord, M.J., How ricin and shiga toxin reach the cytosol of target cells: retrotranslocation from the endoplasmic reticulum. Curr. Topics Microbiol. Immunol. 357 (2012), 19–40.
52. 52 Simpson, J.C., et al. Ricin A chain utilises the ERAD pathway to enter the cytosol of yeast. FEBS Lett. 459 (1999), 80–84.
53. 53 Ye, Y., et al. Function of the p97-Ufd1-Npl4 complex in retrotranslocation from the ER to the cytosol: dual recognition of nonubiquitinated polypeptide segments and polyubiquitin chains. J. Cell Biol. 162 (2003), 71–84.
54. 54 Braunstein, I., et al. Proteasomal degradation of preemptive quality control (pQC) substrates is mediated by an AIRAPL-p97 complex. Mol. Biol. Cell 26 (2015), 3719–3727.
55. 55 Isakov, E., Stanhill, A., Stalled proteasomes are directly relieved by p97 recruitment. J. Biol. Chem. 286 (2011), 30274–30283.
56. 56 Grotzke, J.E., Cresswell, P., Are ERAD components involved in cross-presentation?. Mol. Immunol. 68 (2015), 112–115.
57. 57 Ackerman, A.L., et al. A role for endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 25 (2006), 607–617.
58. 58 Imai, J., et al. Exogenous antigens are processed through the endoplasmic reticulum-associated degradation (ERAD) in cross-presentation by dendritic cells. Int. Immunol. 17 (2005), 45–53.
59. 59 Zehner, M., et al. The translocon protein Sec61 mediates antigen transport from endosomes in the cytosol for cross-presentation to CD8(+) cells. Immunity 42 (2015), 850–863.
60. 60 Schäuble, N., et al. Interaction of Pseudomonas aeruginosa Exotoxin A with the human Sec61 complex suppresses passive calcium efflux from the endoplasmic reticulum. Channels 8 (2014), 76–83.
61. 61 Plemper, R.K., et al. Mutant analysis links the translocon and BiP to retrograde protein transport for ER degradation. Nature 388 (1997), 891–895.
62. 62 Bordallo, J., et al. Der3p/Hrd1p is required for ERAD of misfolded lumenal and integral membrane proteins. Mol. Biol. Cell 9 (1998), 209–222.
63. 63 Huyer, G., et al. Distinct machinery is required in Saccharomyces cerevisiae for the ERAD of a multispanning membrane protein and a soluble lumenal protein. J. Biol. Chem. 279 (2004), 38369–38378.
64. 64 Scott, D.C., Schekman, R., Role of Sec61p in the ER-associated degradation of short-lived transmembrane proteins. J. Cell Biol. 181 (2008), 1095–1105.
65. 65 Willer, M., et al. Sec61p is required for ERAD-L: genetic dissection of the translocation and ERAD-L functions of Sec61p using novel derivatives of CPY*. J. Biol. Chem. 283 (2008), 33883–33888.
66. 66 Kiser, G.L., et al. Expression and degradation of the Cystic Fibrosis Transmembrane Conductance Regulator in Saccharomyces cerevisiae. Arch. Biochem. Biophys. 390 (2001), 195–205.
67. 67 Zhang, Y., et al. Hsp70 molecular chaperone facilitates ERAD of CFTR in yeast. Mol. Biol. Cell 12 (2001), 1303–1314.
68. 68 Gnann, A., et al. CFTR degradation depends on the lectins Htm1p/EDEM and the Cdc48 protein complex in yeast. Mol. Biol. Cell 15 (2004), 4125–4135.
69. 69 Stolz, A., et al. Dfm1 forms distinct complexes with Cdc48 and the ER ubiquitin ligases and is required for ERAD. Traffic 11 (2010), 1363–1369.
70. 70 Horn, S.C., et al. Usa1 functionas as a scaffold of the Hrd-Ubiquitin ligase. Mol. Cell 36 (2009), 782–793.
71. 71 Sato, B.K., et al. Misfolded membrane proteins are specifically recognized by the transmembrane domain of the Hrd1p ubiquitin ligase. Mol. Cell 34 (2009), 212–222.
72. 72 Plemper, R.K., et al. Endoplasmic reticulum degradation of a mutated ATP-binding cassette transporter Pdr5 proceeds in a concerted action of Sec61 and the proteasome. J. Biol. Chem. 273 (1998), 32848–32856.
73. 73 Plemper, R.K., et al. Genetic interactions of Hrd3p and Der3p/Hrd1p with Sec61p suggest a retrotranslocation complex mediating protein transport for ERAD. J. Cell Sci. 112 (1999), 4123–4134.
74. 74 Rubenstein, E.M., et al. Aberrant substrate engagement of the ER translocon triggers degradationby the Hrd1 ubiquitin ligase. J. Cell Biol. 197 (2012), 761–773.
75. 75 Kothe, M., et al. Role of p97 AAA-ATPase in the retrotranslocation of the cholera toxin A1 chain, a non-ubiquitinated substrate. J. Biol. Chem. 280 (2005), 28127–28132.