Interactions between intersubunit transmembrane domains regulate the chaperone-dependent degradation of an oligomeric membrane protein

Biochemical Journal

Volumn 474, Issue 3, 2017, Pages 357-376

  Buck, Teresa M ^a   Jordahl, Alexa S ^a   Yates, Megan E ^a   Preston, G Michael ^a   Cook, Emily ^a,c   Kleyman, Thomas R ^b   Brodsky, Jeffrey L ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; CHIMERIC PROTEIN; EPITHELIAL SODIUM CHANNEL; FUNGAL PROTEIN; LHS1 PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; HEAT SHOCK PROTEIN 70; LHS1 PROTEIN, S CEREVISIAE; PROTEASOME; PROTEIN SUBUNIT; SACCHAROMYCES CEREVISIAE PROTEIN;

ALPHA CHAIN; ARTICLE; BETA CHAIN; CONTROLLED STUDY; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENDOPLASMIC RETICULUM MEMBRANE; FUNGAL STRAIN; GAMMA CHAIN; GENE EXPRESSION SYSTEM; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; PROTEIN SUBUNIT; QUALITY CONTROL; YEAST CELL; AMINO ACID SEQUENCE; CELL MEMBRANE; CHEMISTRY; ENDOPLASMIC RETICULUM; GENE EXPRESSION; GENETICS; HUMAN; METABOLISM; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; SACCHAROMYCES CEREVISIAE; UBIQUITINATION;

AMINO ACID SEQUENCE; CELL MEMBRANE; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM-ASSOCIATED DEGRADATION; EPITHELIAL SODIUM CHANNELS; GENE EXPRESSION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MUTANT CHIMERIC PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN DOMAINS; PROTEIN FOLDING; PROTEIN MULTIMERIZATION; PROTEIN SUBUNITS; PROTEOLYSIS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; UBIQUITINATION;

EID: 85014917810     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BCJ20160760     Document Type: Article

References (97)

1. Brodsky, J.L. (2012) Cleaning up: ER-associated degradation to the rescue. Cell 151, 1163-1167 doi:10.1016/j.cell.2012.11.012
2. Amm, I., Sommer, T. and Wolf, D.H. (2014) Protein quality control and elimination of protein waste: the role of the ubiquitin-proteasome system. Biochim. Biophys. Acta 1843, 182-196 doi:10.1016/j.bbamcr.2013.06.031
3. Christianson, J.C. and Ye, Y. (2014) Cleaning up in the endoplasmic reticulum: ubiquitin in charge. Nat. Struct. Mol. Biol. 21, 325-335 doi:10.1038/nsmb.2793
4. Hampton, R.Y. and Garza, R.M. (2009) Protein quality control as a strategy for cellular regulation: lessons from ubiquitin-mediated regulation of the sterol pathway. Chem. Rev. 109, 1561-1574 doi:10.1021/cr800544v
5. Ismail, N. and Ng, D.T.W. (2006) Have you HRD? Understanding ERAD is DOAble! Cell 126, 237-239 doi:10.1016/j.cell.2006.07.001
6. Meusser, B., Hirsch, C., Jarosch, E. and Sommer, T. (2005) ERAD: the long road to destruction. Nat. Cell Biol. 7, 766-772 doi:10.1038/ncb0805-766
7. Vembar, S.S. and Brodsky, J.L. (2008) One step at a time: endoplasmic reticulum-associated degradation. Nat. Rev. Mol. Cell Biol. 9, 944-957 doi:10.1038/nrm2546
8. Hebert, D.N. and Molinari, M. (2012) Flagging and docking: dual roles for N-glycans in protein quality control and cellular proteostasis. Trends Biochem. Sci. 37, 404-410 doi:10.1016/j.tibs.2012.07.005
9. Rutkevich, L.A. and Williams, D.B. (2011) Participation of lectin chaperones and thiol oxidoreductases in protein folding within the endoplasmic reticulum. Curr. Opin. Cell Biol. 23, 157-166 doi:10.1016/j.ceb.2010.10.011
10. Claessen, J.H.L., Kundrat, L. and Ploegh, H.L. (2012) Protein quality control in the ER: balancing the ubiquitin checkbook. Trends Cell Biol. 22, 22-32 doi:10.1016/j.tcb.2011.09.010
11. Bays, N.W., Wilhovsky, S.K., Goradia, A., Hodgkiss-Harlow, K. and Hampton, R.Y. (2001) HRD4/NPL4 is required for the proteasomal processing of ubiquitinated ER proteins. Mol. Biol. Cell 12, 4114-4128 doi:10.1091/mbc.12.12.4114
12. Hitchcock, A.L., Krebber, H., Frietze, S., Lin, A., Latterich, M. and Silver, P.A. (2001) The conserved npl4 protein complex mediates proteasome-dependent membrane-bound transcription factor activation. Mol. Biol. Cell 12, 3226-3241 doi:10.1091/mbc.12.10.3226
13. 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 doi:10.1128/MCB.22.2.626-634.2002
14. 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 doi:10.1038/414652a
15. Raasi, S. and Wolf, D.H. (2007) Ubiquitin receptors and ERAD: a network of pathways to the proteasome. Semin. Cell Dev. Biol. 18, 780-791 doi:10.1016/j.semcdb.2007.09.008
16. Bhalla, V. and Hallows, K.R. (2008) Mechanisms of ENaC regulation and clinical implications. J. Am. Soc. Nephrol. 19, 1845-1854 doi:10.1681/ASN.2008020225
17. Kashlan, O.B. and Kleyman, T.R. (2012) Epithelial Na(+) channel regulation by cytoplasmic and extracellular factors. Exp. Cell Res. 318, 1011-1019 doi:10.1016/j.yexcr.2012.02.024
18. Snyder, P.M. (2005) Minireview: regulation of epithelial Na+ channel trafficking. Endocrinology 146, 5079-5085 doi:10.1210/en.2005-0894
19. Soundararajan, R., Lu, M. and Pearce, D. (2012) Organization of the ENaC-regulatory machinery. Crit. Rev. Biochem. Mol. Biol. 47, 349-359 doi:10.3109/10409238.2012.678285
20. Blazer-Yost, B.L., Liu, X. and Helman, S.I. (1998) Hormonal regulation of ENaCs: insulin and aldosterone. Am. J. Physiol. 274(5 Pt 1):C1373-C13739 PMID:9612225
21. Eaton, D.C., Malik, B., Bao, H.-F., Yu, L. and Jain, L. (2010) Regulation of epithelial sodium channel trafficking by ubiquitination. Proc. Am. Thorac. Soc. 7, 54-64 doi:10.1513/pats.200909-096JS
22. Canessa, C.M., Merillat, A.M. and Rossier, B.C. (1994) Membrane topology of the epithelial sodium channel in intact cells. Am. J. Physiol. 267(6 Pt 1): C1682-C1690 PMID:7810611
23. Weisz, O.A., Wang, J.-M., Edinger, R.S. and Johnson, J.P. (2000) Non-coordinate regulation of endogenous epithelial sodium channel (ENaC) subunit expression at the apical membrane of A6 cells in response to various transporting conditions. J. Biol. Chem. 275, 39886-39893 doi:10.1074/jbc.M003822200
24. Asher, C., Wald, H., Rossier, B.C. and Garty, H. (1996) Aldosterone-induced increase in the abundance of Na+ channel subunits. Am. J. Physiol. 271(2 Pt 1):C605-C611 PMID:8770001
25. Masilamani, S., Kim, G.-H., Mitchell, C., Wade, J.B. and Knepper, M.A. (1999) Aldosterone-mediated regulation of ENaC α, β, and γ subunit proteins in rat kidney. J. Clin. Invest. 104, R19-R23 doi:10.1172/JCI7840
26. Staub, O., Dho, S., Henry, P., Correa, J., Ishikawa, T., McGlade, J. et al. (1996) WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J. 15, 2371-2380 PMID:8665844
27. Grunder, S., Firsov, D., Chang, S.S., Jaeger, N.F., Gautschi, I., Schild, L. et al. (1997) A mutation causing pseudohypoaldosteronism type 1 identifies a conserved glycine that is involved in the gating of the epithelial sodium channel. EMBO J. 16, 899-907 doi:10.1093/emboj/16.5.899
28. Hobbs, C.A., Da Tan, C. and Tarran, R. (2013) Does epithelial sodium channel hyperactivity contribute to cystic fibrosis lung disease?. J. Physiol. 591, 4377-4387 doi:10.1113/jphysiol.2012.240861
29. Mall, M., Grubb, B.R., Harkema, J.R., O'Neal, W.K. and Boucher, R.C. (2004) Increased airway epithelial Na+ absorption produces cystic fibrosis-like lung disease in mice. Nat. Med. 10, 487-493 doi:10.1038/nm1028
30. Gentzsch, M., Dang, H., Dang, Y., Garcia-Caballero, A., Suchindran, H., Boucher, R.C. et al. (2010) The cystic fibrosis transmembrane conductance regulator impedes proteolytic stimulation of the epithelial Na+ channel. J. Biol. Chem. 285, 32227-32232 doi:10.1074/jbc.M110.155259
31. Ismailov, I.I, Awayda, M.S., Jovov, B., Berdiev, B.K., Fuller, C.M., Dedman, J.R. et al. (1996) Regulation of epithelial sodium channels by the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 271, 4725-4732 doi:10.1074/jbc.271.9.4725
32. Yan, W., Samaha, F.F., Ramkumar, M., Kleyman, T.R. and Rubenstein, R.C. (2004) Cystic fibrosis transmembrane conductance regulator differentially regulates human and mouse epithelial sodium channels in Xenopus oocytes. J. Biol. Chem. 279, 23183-23192 doi:10.1074/jbc.M402373200
33. Malik, B., Schlanger, L., Al-Khalili, O., Bao, H.F., Yue, G., Price, S.R. et al. (2001) ENaC degradation in A6 cells by the ubiquitin-proteosome proteolytic pathway. J. Biol. Chem. 276, 12903-12910 doi:10.1074/jbc.M010626200
34. Staub, O., Gautschi, I., Ishikawa, T., Breitschopf, K., Ciechanover, A., Schild, L. et al. (1997) Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J. 16, 6325-6336 doi:10.1093/emboj/16.21.6325
35. Valentijn, J.A., Fyfe, G.K. and Canessa, C.M. (1998) Biosynthesis and processing of epithelial sodium channels in Xenopus oocytes. J. Biol. Chem. 273, 30344-30351 doi:10.1074/jbc.273.46.30344
36. Needham, P.G. and Brodsky, J.L. (2013) How early studies on secreted and membrane protein quality control gave rise to the ER associated degradation (ERAD) pathway: the early history of ERAD. Biochim. Biophys. Acta 1833, 2447-2457 doi:10.1016/j.bbamcr.2013.03.018
37. Kolb, A.R., Buck, T.M. and Brodsky, J.L. (2011) Saccharomyces cerivisiae as a model system for kidney disease: what can yeast tell us about renal function? Am. J. Physiol. Renal. Physiol. 301, F1-11 doi:10.1152/ajprenal.00141.2011
38. Rotin, D. and Staub, O. (2011) Role of the ubiquitin system in regulating ion transport. Pflugers Arch. 461, 1-21 doi:10.1007/s00424-010-0893-2
39. Foresti, O., Ruggiano, A., Hannibal-Bach, H.K., Ejsing, C.S. and Carvalho, P. (2013) Sterol homeostasis requires regulated degradation of squalene monooxygenase by the ubiquitin ligase Doa10/Teb4. eLife 2, e00953 doi:10.7554/eLife.00953
40. Olzmann, J.A., Richter, C.M. and Kopito, R.R. (2013) Spatial regulation of UBXD8 and p97/VCP controls ATGL-mediated lipid droplet turnover. Proc. Natl Acad. Sci. U.S.A. 110, 1345-1350 doi:10.1073/pnas.1213738110
41. Chen, X., Tukachinsky, H., Huang, C.-H., Jao, C., Chu, Y.-R., Tang, H.-Y. et al. (2011) Processing and turnover of the Hedgehog protein in the endoplasmic reticulum. J. Cell Biol. 192, 825-838 doi:10.1083/jcb.201008090
42. Zettl, M., Adrain, C., Strisovsky, K., Lastun, V. and Freeman, M. (2011) Rhomboid family pseudoproteases use the ER quality control machinery to regulate intercellular signaling. Cell 145, 79-91 doi:10.1016/j.cell.2011.02.047
43. Hampton, R.Y. (2002) Proteolysis and sterol regulation. Annu. Rev. Cell Dev. Biol. 18, 345-378 doi:10.1146/annurev.cellbio.18.032002.131219
44. Kashlan, O.B., Mueller, G.M., Qamar, M.Z., Poland, P.A., Ahner, A., Rubenstein, R.C. et al. (2007) Small heat shock protein αA-crystallin regulates epithelial sodium channel expression. J. Biol. Chem. 282, 28149-28156 doi:10.1074/jbc.M703409200
45. Buck, T.M., Kolb, A.R., Boyd, C., Kleyman, T.R. and Brodsky, J.L. (2010) The ER associated degradation of the epithelial sodium channel requires a unique complement of molecular chaperones. Mol. Biol. Cell 21, 1047-1058 doi:10.1091/mbc.E09-11-0944
46. Buck, T.M., Plavchak, L., Roy, A., Donnelly, B.F., Kashlan, O.B., Kleyman, T.R. et al. (2013) The Lhs1/GRP170 chaperones facilitate the endoplasmic reticulum-associated degradation of the epithelial sodium channel. J. Biol. Chem. 288, 18366-18380 doi:10.1074/jbc.M113.469882
47. Baxter, B.K., James, P., Evans, T. and Craig, E.A. (1996) SSI1 encodes a novel Hsp70 of the Saccharomyces cerevisiae endoplasmic reticulum. Mol. Cell Biol. 16, 6444-6456 doi:10.1128/MCB.16.11.6444
48. Craven, R.A., Egerton, M. and Stirling, C.J. (1996) A novel Hsp70 of the yeast ER lumen is required for the efficient translocation of a number of protein precursors. EMBO J. 15, 2640-2650 PMID:8654361
49. Steel, G.J., Fullerton, D.M., Tyson, J.R. and Stirling, C.J. (2004) Coordinated activation of Hsp70 chaperones. Science 303, 98-101 doi:10.1126/science.1092287
50. Tyson, J.R. and Stirling, C.J. (2000) LHS1 and SIL1 provide a lumenal function that is essential for protein translocation into the endoplasmic reticulum. EMBO J. 19, 6440-6452 doi:10.1093/emboj/19.23.6440
51. de Keyzer, J., Steel, G.J., Hale, S.J., Humphries, D. and Stirling, C.J. (2009) Nucleotide binding by Lhs1p is essential for its nucleotide exchange activity and for function in vivo. J. Biol. Chem. 284, 31564-31571 doi:10.1074/jbc.M109.055160
52. Jasti, J., Furukawa, H., Gonzales, E.B. and Gouaux, E. (2007) Structure of acid-sensing ion channel 1 at 1.9 Å resolution and low pH. Nature 449, 316-323 doi:10.1038/nature06163
53. Gonzales, E.B., Kawate, T. and Gouaux, E. (2009) Pore architecture and ion sites in acid-sensing ion channels and P2X receptors. Nature 460, 599-604 doi:10.1038/nature08218
54. Kashlan, O.B. and Kleyman, T.R. (2011) ENaC structure and function in the wake of a resolved structure of a family member. Am. J. Physiol. Renal. Physiol. 301, F684-F696 doi:10.1152/ajprenal.00259.2011
55. Adams, A., Gottschling, D.E., Kaiser, C.A. and Stearns, T. (1997) Methods in Yeast Genetics. A Cold Spring Harbor Laboratory Course Manual, 1997 edn, Cold Spring Harbor Laboratory Press, Plainview, New York
56. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K. and Pease, L.R. (1989) Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59 doi:10.1016/0378-1119(89)90358-2
57. Longtine, M.S., McKenzie, III, A., Demarini, D.J., Shah, N.G., Wach, A., Brachat, A. et al. (1998) Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14, 953-961 <953::AID-YEA293>3.0.CO;2-U
58. Zhang, Y., Nijbroek, G., Sullivan, M.L., McCracken, A.A., Watkins, S.C., Michaelis, S. et al. (2001) Hsp70 molecular chaperone facilitates endoplasmic reticulum-associated protein degradation of cystic fibrosis transmembrane conductance regulator in yeast. Mol. Biol. Cell 12, 1303-1314 doi:10.1091/mbc.12.5.1303
59. Sullivan, M.L., Youker, R.T., Watkins, S.C. and Brodsky, J.L. (2003) Localization of the BiP molecular chaperone with respect to endoplasmic reticulum foci containing the cystic fibrosis transmembrane conductance regulator in yeast. J. Histochem. Cytochem. 51, 545-548 doi:10.1177/002215540305100417
60. Nakatsukasa, K. and Brodsky, J.L. (2010) In vitro reconstitution of the selection, ubiquitination, and membrane extraction of a polytopic ERAD substrate. Methods Mol. Biol. 619, 365-376 doi:10.1007/978-1-60327-412-8-21
61. Prince, L.S. and Welsh, M.J. (1998) Cell surface expression and biosynthesis of epithelial Na+ channels. Biochem. J. 336(Pt 3), 705-710 doi:10.1042/bj3360705
62. Prince, L.S. and Welsh, M.J. (1999) Effect of subunit composition and Liddle's syndrome mutations on biosynthesis of ENaC. Am. J. Physiol. 276(6 Pt 1):C1346-C1351 PMID:10362597
63. Snyder, P.M., Cheng, C., Prince, L.S., Rogers, J.C. and Welsh, M.J. (1998) Electrophysiological and biochemical evidence that DEG/ENaC cation channels are composed of nine subunits. J. Biol. Chem. 273, 681-684 doi:10.1074/jbc.273.2.681
64. Gupta, S.S. and Canessa, C.M. (2000) Heterologous expression of a mammalian epithelial sodium channel in yeast. FEBS Lett. 481, 77-80 doi:10.1016/S0014-5793(00)01977-3
65. Canessa, C.M., Schild, L., Buell, G., Thorens, B., Gautschi, I., Horisberger, J.-D. et al. (1994) Amiloride-sensitive epithelial Na+ channel is made of three homologous subunits. Nature 367, 463-467 doi:10.1038/367463a0
66. Renard, S., Lingueglia, E., Voilley, N., Lazdunski, M. and Barbry, P. (1994) Biochemical analysis of the membrane topology of the amiloride-sensitive Na+ channel. J. Biol. Chem. 269, 12981-12986 PMID:8175716
67. Snyder, P.M., McDonald, F.J., Stokes, J.B. and Welsh, M.J. (1994) Membrane topology of the amiloride-sensitive epithelial sodium channel. J. Biol. Chem. 269, 24379-24383 PMID:7929098
68. Kashlan, O.B., Adelman, J.L., Okumura, S., Blobner, B.M., Zuzek, Z., Hughey, R.P. et al. (2011) Constraint-based, homology model of the extracellular domain of the epithelial Na+ channel α subunit reveals a mechanism of channel activation by proteases. J. Biol. Chem. 286, 649-660 doi:10.1074/jbc.M110.167098
69. Ferris, S.P., Jaber, N.S., Molinari, M., Arvan, P. and Kaufman, R.J. (2013) UDP-glucose:glycoprotein glucosyltransferase (UGGT1) promotes substrate solubility in the endoplasmic reticulum. Mol. Biol. Cell 24, 2597-2608 doi:10.1091/mbc.E13-02-0101
70. Xu, C. and Ng, D.T. (2015) Glycosylation-directed quality control of protein folding. Nat. Rev. Mol. Cell. Biol. 16, 742-752 doi:10.1038/nrm4073
71. Varki, A., Cummings, R.D., Esko, J.D., Freeze, H.H., Stanley, P., Bertozzi, C.R. et al. (2009) Essentials of Glycobiology, 2nd edn. Cold Spring Harbor Laboratory Press
72. Ruggiano, A., Foresti, O. and Carvalho, P. (2014) Quality control: ER-associated degradation: protein quality control and beyond. J. Cell Biol. 204, 869-879 doi:10.1083/jcb.201312042
73. Nakatsukasa, K., Huyer, G., Michaelis, S. and Brodsky, J.L. (2008) Dissecting the ER-associated degradation of a misfolded polytopic membrane protein. Cell 132, 101-112 doi:10.1016/j.cell.2007.11.023
74. Inoue, T. and Tsai, B. (2016) The Grp170 nucleotide exchange factor executes a key role during ERAD of cellular misfolded clients. Mol. Biol. Cell 27, 1650-1662 doi:10.1091/mbc.E16-01-0033
75. Bachmair, A., Finley, D. and Varshavsky, A. (1986) In vivo half-life of a protein is a function of its amino-terminal residue. Science 234, 179-186 doi:10.1126/science.3018930
76. Varshavsky, A. (1991) Naming a targeting signal. Cell 64, 13-15 doi:10.1016/0092-8674(91)90202-A
77. Hessa, T., Meindl-Beinker, N.M., Bernsel, A., Kim, H., Sato, Y., Lerch-Bader, M. et al. (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450, 1026-1030 doi:10.1038/nature06387
78. Lu, Y., Xiong, X., Helm, A., Kimani, K., Bragin, A. and Skach, W.R. (1998) Co-and posttranslational translocation mechanisms direct cystic fibrosis transmembrane conductance regulator N terminus transmembrane assembly. J. Biol. Chem. 273, 568-576 doi:10.1074/jbc.273.1.568
79. Ota, K., Sakaguchi, M., von Heijne, G., Hamasaki, N. and Mihara, K. (1998) Forced transmembrane orientation of hydrophilic polypeptide segments in multispanning membrane proteins. Mol. Cell 2, 495-503 doi:10.1016/S1097-2765(00)80149-5
80. Öjemalm, K., Halling, K.K., Nilsson, I. and von Heijne, G. (2012) Orientational preferences of neighboring helices can drive ER insertion of a marginally hydrophobic transmembrane helix. Mol. Cell 45, 529-540 doi:10.1016/j.molcel.2011.12.024
81. Kida, Y., Ishihara, Y., Fujita, H., Onishi, Y. and Sakaguchi, M. (2016) Stability and flexibility of marginally hydrophobic-segment stalling at the endoplasmic reticulum translocon. Mol. Biol. Cell 27, 930-940 doi:10.1091/mbc.E15-09-0672
82. Beguin, P., Hasler, U., Beggah, A., Horisberger, J.-D. and Geering, K. (1998) Membrane integration of Na,K-ATPase α-subunits and β-subunit assembly. J. Biol. Chem. 273, 24921-24931 doi:10.1074/jbc.273.38.24921
83. Beguin, P., Hasler, U., Staub, O. and Geering, K. (2000) Endoplasmic reticulum quality control of oligomeric membrane proteins: topogenic determinants involved in the degradation of the unassembled Na,K-ATPase α subunit and in its stabilization by β subunit assembly. Mol. Biol. Cell 11, 1657-1672 doi:10.1091/mbc.11.5.1657
84. Beggah, A., Mathews, P., Beguin, P. and Geering, K. (1996) Degradation and endoplasmic reticulum retention of unassembled α-and β-subunits of Na, K-ATPase correlate with interaction of BiP. J. Biol. Chem. 271, 20895-20902 doi:10.1074/jbc.271.34.20895
85. Beggah, A.T., Beguin, P., Bamberg, K., Sachs, G. and Geering, K. (1999) β-subunit assembly is essential for the correct packing and the stable membrane insertion of the, H,K-ATPase α-subunit. J. Biol. Chem. 274, 8217-8223 doi:10.1074/jbc.274.12.8217
86. Bonifacino, J.S., Cosson, P., Shah, N. and Klausner, R.D. (1991) Role of potentially charged transmembrane residues in targeting proteins for retention and degradation within the endoplasmic reticulum. EMBO J. 10, 2783-2793 PMCID:452987
87. Bonifacino, J.S., Suzuki, C.K. and Klausner, R.D. (1990) A peptide sequence confers retention and rapid degradation in the endoplasmic reticulum. Science 247, 79-82 doi:10.1126/science.2294595
88. Bonifacino, J.S., Cosson, P. and Klausner, R.D. (1990) Colocalized transmembrane determinants for ER degradation and subunit assembly explain the intracellular fate of TCR chains. Cell 63, 503-513 doi:10.1016/0092-8674(90)90447-M
89. Feige, M.J., Behnke, J., Mittag, T. and Hendershot, L.M. (2015) Dimerization-dependent folding underlies assembly control of the clonotypic αβT cell receptor chains. J. Biol. Chem. 290, 26821-26831 doi:10.1074/jbc.M115.689471
90. Feige, M.J. and Hendershot, L.M. (2013) Quality control of integral membrane proteins by assembly-dependent membrane integration. Mol. Cell 51, 297-309 doi:10.1016/j.molcel.2013.07.013
91. Shi, S., Carattino, M.D. and Kleyman, T.R. (2012) Role of the wrist domain in the response of the epithelial sodium channel to external stimuli. J. Biol. Chem. 287, 44027-44035 doi:10.1074/jbc.M112.421743
92. Baconguis, I. and Gouaux, E. (2012) Structural plasticity and dynamic selectivity of acid-sensing ion channel-spider toxin complexes. Nature 489, 400-405 doi:10.1038/nature11375
93. Li, T., Yang, Y. and Canessa, C.M. (2009) Interaction of the aromatics Tyr-72/Trp-288 in the interface of the extracellular and transmembrane domains is essential for proton gating of acid-sensing ion channels. J. Biol. Chem. 284, 4689-4694 doi:10.1074/jbc.M805302200
94. Shi, S., Ghosh, D.D., Okumura, S., Carattino, M.D., Kashlan, O.B., Sheng, S. et al. (2011) Base of the thumb domain modulates epithelial sodium channel gating. J. Biol. Chem. 286, 14753-14761 doi:10.1074/jbc.M110.191734
95. Schmidt, B.Z. and Perlmutter, D.H. (2005) Grp78, Grp94, and Grp170 interact with α1-antitrypsin mutants that are retained in the endoplasmic reticulum. Am. J. Physiol. Gastrointest. Liver Physiol. 289, G444-G455 doi:10.1152/ajpgi.00237.2004
96. Kondoh, Y. and Osada, H. (2013) High-throughput screening identifies small molecule inhibitors of molecular chaperones. Curr. Pharm. Des. 19, 473-492 doi:10.2174/138161213804143743
97. Salem, R.M., Pandey, B., Richard, E., Fung, M.M., Garcia, E.P., Brophy, V.H. et al. (2010) The VA hypertension primary care longitudinal cohort: electronic medical records in the post-genomic era. Health Informatics J. 16, 274-286 doi:10.1177/1460458210380527