Co-translational targeting and translocation of proteins to the endoplasmic reticulum

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1833, Issue 11, 2013, Pages 2392-2402

  Nyathi, Yvonne ^a   Wilkinson, Barrie M ^a   Pool, Martin R ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Protein biogenesis; Protein targeting; Protein translocation; Ribosome; Signal recognition particle; Translocon

Indexed keywords

GUANOSINE TRIPHOSPHATASE; SECRETORY PROTEIN; SIGNAL PEPTIDE; SIGNAL RECOGNITION PARTICLE; TRANSLOCON;

AMINO ACID COMPOSITION; CELL MEMBRANE; ENDOPLASMIC RETICULUM; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; PROTEIN TARGETING; REVIEW; RIBOSOME; SIGNAL TRANSDUCTION;

5′-GUANYLYL IMIDODIPHOSPHATE; BINDING IMMUNOGLOBULIN PROTEIN; BIP; ENDOPLASMIC RETICULUM; ER; GPPNHP; OLIGOSACCHARYL TRANSFERASE; OST; PROTEIN BIOGENESIS; PROTEIN TARGETING; PROTEIN TRANSLOCATION; RAMP4; RIBOSOMAL RNA; RIBOSOME; RIBOSOME NASCENT CHAIN COMPLEX; RIBOSOME-ASSOCIATED MEMBRANE PROTEIN 4; RIBOSOME-NASCENT CHAIN COMPLEX; RNC; RRNA; SIGNAL PEPTIDASE; SIGNAL RECOGNITION PARTICLE; SIGNAL RECOGNITION PARTICLE RECEPTOR; SPASE; SR; SRP; TM; TRAM; TRANSFER RNA; TRANSLOCATING CHAIN-ASSOCIATED MEMBRANE PROTEIN; TRANSLOCON; TRANSLOCON-ASSOCIATED PROTEIN COMPLEX; TRANSMEMBRANE HELIX; TRAP; TRNA;

ANIMALS; ENDOPLASMIC RETICULUM; HUMANS; PROTEIN BIOSYNTHESIS; PROTEIN TRANSPORT; PROTEINS; SIGNAL RECOGNITION PARTICLE;

BACTERIA (MICROORGANISMS);

EID: 84880641715     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2013.02.021     Document Type: Review

References (137)

1. Saraogi I., Shan S.O. Molecular mechanism of co-translational protein targeting by the signal recognition particle. Traffic 2011, 12:535-542.
2. Pool M.R. Signal recognition particles in chloroplasts, bacteria, yeast and mammals (review). Mol. Membr. Biol. 2005, 22:3-15.
3. Bibi E. Early targeting events during membrane protein biogenesis in Escherichia coli. Biochim. Biophys. Acta 2011, 1808:841-850.
4. Eichler J., Moll R. The signal recognition particle of Archaea. Trends Microbiol. 2001, 9:130-136.
5. Walter P., Blobel G. Disassembly and reconstitution of signal recognition particle. Cell 1983, 34:525-533.
6. Gundelfinger E.D., Krause E., Melli M., Dobberstein B. The organization of the 7SL RNA in the signal recognition particle. Nucleic Acids Res. 1983, 11:7363-7374.
7. Mason N., Ciufo L.F., Brown J.D. Elongation arrest is a physiologically important function of the signal recognition particle. EMBO J. 2000, 19:4164-4174.
8. Strub K., Fornallaz M., Bui N. The Alu domain homolog of the yeast signal recognition particle consists of an Srp14p homodimer and a yeast-specific RNA structure. RNA 1999, 5:1333-1347.
9. Hann B.C., Walter P. The signal recognition particle in S. cerevisiae. Cell 1991, 67:131-144.
10. Keenan R.J., Freymann D.M., Stroud R.M., Walter P. The signal recognition particle. Ann. Rev. Biochem. 2001, 70:755-775.
11. Powers T., Walter P. Co-translational protein targeting catalyzed by the Escherichia coli signal recognition particle and its receptor. EMBO J. 1997, 16:4880-4886.
12. Kurzchalia T.V., Wiedmann M., Girshovich A.S., Bochkareva E.S., Bielka H., Rapoport T.A. The signal sequence of nascent preprolactin interacts with the 54K polypeptide of signal recognition particle. Nature 1986, 320:634-636.
13. Krieg U.C., Walter P., Johnson A.E. Photocrosslinking of the signal sequence of nascent preprolactin to the 54-kilodalton polypeptide of the signal recognition particle. Proc. Natl. Acad. Sci. U. S. A. 1986, 83:8604-8608.
14. Connolly T., Gilmore R. The signal recognition particle receptor mediates the GTP-dependent displacement of SRP from the signal sequence of the nascent polypeptide. Cell 1989, 57:599-610.
15. Freymann D.M., Keenan R.J., Stroud R.N., Walter P. Structure of the conserved GTPase domain of the signal recognition particle. Nature 1997, 385:361-364.
16. Montoya G., Svensson C., Luirink J., Sinning I. Crystal structure of the NG domain from the signal recognition particle receptor FtsY. Nature 1997, 385:365-368.
17. Janda C.Y., Li J., Oubridge C., Hernandez H., Robinson C.V., Nagai K. Recognition of a signal peptide by the signal recognition particle. Nature 2010, 465:507-510.
18. Hainzl T., Huang S., Merilainen G., Brannstrom K., Sauer-Eriksson A.E. Structural basis of signal-sequence recognition by the signal recognition particle. Nat. Struct. Mol. Biol. 2011, 18:389-391.
19. Keenan R.J., Freymann D.M., Walter P., Stroud R.M. Crystal structure of the signal sequence binding protein of the signal recognition particle. Cell 1998, 94:181-191.
20. Batey R.T., Rambo R.P., Lucast L., Rha B., Doudna J.A. Crystal structure of the ribonucleoprotein core of the signal recognition particle. Science 2000, 287:1232-1239.
21. Sauer-Eriksson A.E., Hainzl T. S-domain assembly of the signal recognition particle. Curr. Opin. Struct. Biol. 2003, 13:64-70.
22. Römisch K., Webb J., Herz J., Prehn S., Frank R., Vingron M., Dobberstein B. Homology of 54K protein of signal-recognition particle, docking protein and two E. coli proteins with putative GTP-binding domains. Nature 1989, 340:478-482.
23. Lütcke H., High S., Römisch K., Ashford A.J., Dobberstein B. The methionine-rich domain of the 54kDa subunit of signal recognition particle is sufficient for the interaction with signal sequences. EMBO J. 1992, 11:1543-1551.
24. Gierasch L.M. Signal sequences. Biochemistry 1989, 28:923-930.
25. von Heijne G. Signal sequences. The limits of variation. J. Mol. Biol. 1985, 184:99-105.
26. Zheng N., Gierasch L.M. Signal sequences: the same yet different. Cell 1996, 86:849-852.
27. Hatsuzawa K., Tagaya M., Mizushima S. The hydrophobic region of signal peptides is a determinant for SRP recognition and protein translocation across the ER membrane. J. Biochem. 1997, 121:270-277.
28. Ng D.T., Brown J.D., Walter P. Signal sequences specify the targeting route to the endoplasmic reticulum membrane. J. Cell Biol. 1996, 134:269-278.
29. Huber D., Boyd D., Xia Y., Olma M.H., Gerstein M., Beckwith J. Use of thioredoxin as a reporter to identify a subset of Escherichia coli signal sequences that promote signal recognition particle-dependent translocation. J. Bacteriol. 2005, 187:2983-2991.
30. Matoba S., Morano K.A., Klionsky D.J., Kim K., Ogrydziak D.M. Dipeptidyl aminopeptidase processing and biosynthesis of alkaline extracellular protease from Yarrowia lipolytica. Microbiology 1997, 143(Pt 10):3263-3272.
31. Peterson J.H., Woolhead C.A., Bernstein H.D. Basic amino acids in a distinct subset of signal peptides promote interaction with the signal recognition particle. J. Biol. Chem. 2003, 278:46155-46162.
32. Lakkaraju A.K., Thankappan R., Mary C., Garrison J.L., Taunton J., Strub K. Efficient secretion of small proteins in mammalian cells relies on Sec62-dependent posttranslational translocation. Mol. Biol. Cell 2012, 23:2712-2722.
33. Peterson J.H., Szabady R.L., Bernstein H.D. An unusual signal peptide extension inhibits the binding of bacterial presecretory proteins to the signal recognition particle, trigger factor, and the SecYEG complex. J. Biol. Chem. 2006, 281:9038-9048.
34. Flanagan J.J., Chen J.C., Miao Y., Shao Y., Lin J., Bock P.E., Johnson A.E. SRP binds to ribosome-bound signal sequences with fluorescence-detected subnanomolar affinity that does not diminish as the nascent chain lengthens. J. Biol. Chem. 2003, 278:18628-18637.
35. Bornemann T., Jockel J., Rodnina M.V., Wintermeyer W. Signal sequence-independent membrane targeting of ribosomes containing short nascent peptides within the exit tunnel. Nat. Struct. Mol. Biol. 2008, 15:494-499.
36. Holtkamp W., Lee S., Bornemann T., Senyushkina T., Rodnina M.V., Wintermeyer W. Dynamic switch of the signal recognition particle from scanning to targeting. Nat. Struct. Mol. Biol. 2012.
37. Ogg S.C., Walter P. SRP samples nascent chains for the presence of signal sequences by interacting with the ribosome at a discrete step during translation elongation. Cell 1995, 81:1075-1084.
38. Pool M.R., Stumm J., Fulga T.A., Sinning I., Dobberstein B. Distinct modes of signal recognition particle interaction with the ribosome. Science 2002, 297:1345-1348.
39. Halic M., Becker T., Pool M.R., Spahn C.M., Grassucci R.A., Frank J., Beckmann R. Structure of the signal recognition particle interacting with the elongation-arrested ribosome. Nature 2004, 427:808-814.
40. Halic M., Blau M., Becker T., Mielke T., Pool M.R., Wild K., Sinning I., Beckmann R. Following the signal sequence from ribosomal tunnel exit to signal recognition particle. Nature 2006, 444:507-511.
41. Gu S.Q., Peske F., Wieden H.J., Rodnina M.V., Wintermeyer W. The signal recognition particle binds to protein L23 at the peptide exit of the Escherichia coli ribosome. RNA 2003, 9:566-573.
42. Kramer G., Boehringer D., Ban N., Bukau B. The ribosome as a platform for co-translational processing, folding and targeting of newly synthesized proteins. Nat. Struct. Mol. Biol. 2009, 16:589-597.
43. Bradshaw N., Neher S.B., Booth D.S., Walter P. Signal sequences activate the catalytic switch of SRP RNA. Science 2009, 323:127-130.
44. Wild K., Rosendal K.R., Sinning I. A structural step into the SRP cycle. Mol. Microbiol. 2004, 53:357-363.
45. Berndt U., Oellerer S., Zhang Y., Johnson A.E., Rospert S. A signal-anchor sequence stimulates signal recognition particle binding to ribosomes from inside the exit tunnel. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1398-1403.
46. Lin K.F., Sun C.S., Huang Y.C., Chan S.I., Koubek J., Wu T.H., Huang J.J. Cotranslational protein folding within the ribosome tunnel influences trigger-factor recruitment. Biophys. J. 2012, 102:2818-2827.
47. Pool M.R. A trans-membrane domain segment inside the ribosome exit tunnel triggers RAMP4 recruitment to the Sec61p translocase. J. Cell Biol. 2009, 185:889-902.
48. Liao S., Lin J., Do H., Johnson A.E. Both lumenal and cytosolic gating of the aqueous ER translocon pore is regulated from within the ribosome during membrane protein integration. Cell 1997, 90:31-41.
49. High S., Dobberstein B. The signal sequence interacts with the methionine-rich domain of the 54-kD protein of signal recognition particle. J. Cell Biol. 1991, 113:229-233.
50. Zopf D., Bernstein H.D., Johnson A.E., Walter P. The methionine-rich domain of the 54kD protein subunit of the signal recognition particle contains an RNA binding site and can be crosslinked to a signal sequence. EMBO J. 1990, 9:4511-4517.
51. Bernstein H.D., Poritz M.A., Strub K., Hoben P.J., Brenner S., Walter P. Model for signal sequence recognition from amino-acid sequence of 54K subunit of signal recognition particle. Nature 1989, 340:482-486.
52. Schwartz T., Blobel G. Structural basis for the function of the beta subunit of the eukaryotic signal recognition particle receptor. Cell 2003, 112:793-803.
53. Schlenker O., Hendricks A., Sinning I., Wild K. The structure of the mammalian signal recognition particle (SRP) receptor as prototype for the interaction of small GTPases with Longin domains. J. Biol. Chem. 2006, 281:8898-8906.
54. Miller J.D., Tajima S., Lauffer L., Walter P. The b subunit of the signal recognition particle receptor is a transmembrane GTPase that anchors the a subunit, a peripheral membrane GTPase, to the endoplasmic reticulum membrane. J. Cell Biol. 1995, 128:273-282.
55. Legate K., Falcone D., Andrews D. Nucleotide-dependent binding of the GTPase domain of the signal recognition particle receptor b-subunit to the a-subunit. J. Biol. Chem. 2000, 275:27439-27446.
56. Egea P.F., Shan S.O., Napetschnig J., Savage D.F., Walter P., Stroud R.M. Substrate twinning activates the signal recognition particle and its receptor. Nature 2004, 427:215-221.
57. Focia P.J., Shepotinovskaya I.V., Seidler J.A., Freymann D.M. Heterodimeric GTPase core of the SRP targeting complex. Science 2004, 303:373-377.
58. Moser C., Mol O., Goody R.S., Sinning I. The signal recognition particle receptor of Escherichia coli (FtsY) has a nucleotide exchange factor built into the GTPase domain. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11339-11344.
59. Rapiejko P.J., Gilmore R. Empty site forms of SRP54 and SRalpha GTPases mediate targeting of ribosome-nascent chain complexes to the endoplasmic reticulum. Cell 1997, 89:703-713.
60. Powers T., Walter P. Reciprocal stimulation of GTP hydrolysis by two directly interacting GTPases. Science 1995, 269:1422-1424.
61. Zhang X., Kung S., Shan S.O. Demonstration of a multistep mechanism for assembly of the SRP x SRP receptor complex: implications for the catalytic role of SRP RNA. J. Mol. Biol. 2008, 381:581-593.
62. Shen K., Zhang X., Shan S.O. Synergistic actions between the SRP RNA and translating ribosome allow efficient delivery of the correct cargos during cotranslational protein targeting. RNA 2011, 17:892-902.
63. Shan S.O., Stroud R.M., Walter P. Mechanism of association and reciprocal activation of two GTPases. PLoS Biol. 2004, 2:e320.
64. Zhang X., Schaffitzel C., Ban N., Shan S.O. Multiple conformational switches in a GTPase complex control co-translational protein targeting. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:1754-1759.
65. Zhang X., Rashid R., Wang K., Shan S.O. Sequential checkpoints govern substrate selection during cotranslational protein targeting. Science 2010, 328:757-760.
66. Peluso P., Herschlag D., Nock S., Freymann D., Johnson A.E., Walter P. Role of the 4.5S RNA in assembly of the bacterial signal recognition particle with its receptor. Science 2000, 288.
67. Lam V.Q., Akopian D., Rome M., Henningsen D., Shan S.O. Lipid activation of the signal recognition particle receptor provides spatial coordination of protein targeting. J. Cell Biol. 2010, 190:623-635.
68. Shan S.O., Chandrasekar S., Walter P. Conformational changes in the GTPase modules of the signal reception particle and its receptor drive initiation of protein translocation. J. Cell Biol. 2007, 178:611-620.
69. Rapiejko P.J., Gilmore R. Protein translocation across the ER requires a functional GTP binding site in the a subunit of the signal recognition particle receptor. J. Cell Biol. 1992, 117:493-503.
70. Connolly T., Rapiejko P.J., Gilmore R. Requirement of GTP hydrolysis for release of signal recognition particle from its receptor. Science 1991, 252:1171-1173.
71. Ataide S.F., Schmitz N., Shen K., Ke A., Shan S.O., Doudna J.A., Ban N. The crystal structure of the signal recognition particle in complex with its receptor. Science 2011, 331:881-886.
72. Shen K., Arslan S., Akopian D., Ha T., Shan S.O. Activated GTPase movement on an RNA scaffold drives co-translational protein targeting. Nature 2012, 492:271-275.
73. Rodnina M.V., Wintermeyer W. Ribosome fidelity: tRNA discrimination, proofreading and induced fit. Trends Biochem. Sci. 2001, 26:124-130.
74. Mary C., Scherrer A., Huck L., Lakkaraju A.K., Thomas Y., Johnson A.E., Strub K. Residues in SRP9/14 essential for elongation arrest activity of the signal recognition particle define a positively charged functional domain on one side of the protein. RNA 2010, 16:969-979.
75. Walter P., Blobel G. Translocation of proteins across the endoplasmic reticulum III. Signal recognition protein (SRP) causes signal sequence-dependent and site-specific arrest of chain elongation that is released by microsomal membranes. J. Cell Biol. 1981, 91:557-561.
76. Siegel V., Walter P. Elongation arrest is not a prerequisite for secretory protein translocation across the microsomal membrane. J. Cell Biol. 1985, 100:1913-1921.
77. Thomas Y., Bui N., Strub K. A truncation in the 14kDa protein of the signal recognition particle leads to tertiary structure changes in the RNA and abolishes the elongation arrest activity of the particle. Nucleic Acids Res. 1997, 25:1920-1929.
78. Lakkaraju A.K., Mary C., Scherrer A., Johnson A.E., Strub K. SRP keeps polypeptides translocation-competent by slowing translation to match limiting ER-targeting sites. Cell 2008, 133:440-451.
79. Terzi L., Pool M.R., Dobberstein B., Strub K. Signal recognition particle Alu domain occupies a defined site at the ribosomal subunit interface upon signal sequence recognition. Biochemistry 2004, 43:107-117.
80. Siegel V., Walter P. Each of the activities of signal recognition particle (SRP) is contained within a distinct domain: analysis of biochemical mutants of SRP. Cell 1988, 52:39-49.
81. Rapoport T.A. Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 2007, 450:663-669.
82. Mothes W., Prehn S., Rapoport T.A. Systematic probing of the environment of a translocating secretory protein during translocation through the ER membrane. EMBO J. 1994, 13:3973-3982.
83. Brunner J. Labelling the hydrophobic core of membranes. Trends Biochem. Sci. 1981, 6:44-46.
84. Görlich D., Rapoport T.A. Protein translocation into proteoliposomes reconstituted from purified components of the endoplasmic reticulum membrane. Cell 1993, 75:615-630.
85. Simon S.M., Blobel G. Signal peptides open protein-conducting channels in E. coli. Cell 1992, 69:677-684.
86. Crowley K.S., Reinhart G.D., Johnson A.E. The signal sequence moves through a ribosomal tunnel into a noncytoplasmic aqueous environment at the ER membrane early in translocation. Cell 1993, 73:1101-1115.
87. Van den Berg B., Clemons W.M., Collinson I., Modis Y., Hartmann E., Harrison S.C., Rapoport T.A. X-ray structure of a protein-conducting channel. Nature 2004, 427:36-44.
88. Tsukazaki T., Mori H., Fukai S., Ishitani R., Mori T., Dohmae N., Perederina A., Sugita Y., Vassylyev D.G., Ito K., Nureki O. Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 2008, 455:988-991.
89. Zimmer J., Nam Y., Rapoport T.A. Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 2008, 455:936-943.
90. Becker T., Bhushan S., Jarasch A., Armache J.P., Funes S., Jossinet F., Gumbart J., Mielke T., Berninghausen O., Schulten K., Westhof E., Gilmore R., Mandon E.C., Beckmann R. Structure of monomeric yeast and mammalian Sec61 complexes interacting with the translating ribosome. Science 2009, 326:1369-1373.
91. Menetret J.F., Hegde R.S., Aguiar M., Gygi S.P., Park E., Rapoport T.A., Akey C.W. Single copies of Sec61 and TRAP associate with a nontranslating mammalian ribosome. Structure 2008, 16:1126-1137.
92. Cannon K.S., Or E., Clemons W.M., Shibata Y., Rapoport T.A. Disulfide bridge formation between SecY and a translocating polypeptide localizes the translocation pore to the center of SecY. J. Cell Biol. 2005, 169:219-225.
93. Gumbart J., Schulten K. Molecular dynamics studies of the archaeal translocon. Biophys. J. 2006, 90:2356-2367.
94. Saparov S.M., Erlandson K., Cannon K., Schaletzky J., Schulman S., Rapoport T.A., Pohl P. Determining the conductance of the SecY protein translocation channel for small molecules. Mol. Cell 2007, 26:501-509.
95. Shaw A.E., Rottier P.J.M., Rose J.K. Evidence for the loop model of signal sequence insertion into the endoplasmic reticulum. Proc. Natl. Acad. Sci. U. S. A. 1988, 85:7592-7596.
96. Plath K., Mothes W., Wilkinson B.M., Stirling C.J., Rapoport T.A. Signal sequence recognition in posttranslational protein transport across the yeast ER membrane. Cell 1998, 94:795-807.
97. Wilkinson B.M., Brownsword J.K., Mousley C.J., Stirling C.J. Sss1p is required to complete protein translocon activation. J. Biol. Chem. 2010, 285:32671-32677.
98. Maillard A.P., Lalani S., Silva F., Belin D., Duong F. Deregulation of the SecYEG translocation channel upon removal of the plug domain. J. Biol. Chem. 2007, 282:1281-1287.
99. Junne T., Kocik L., Spiess M. The hydrophobic core of the Sec61 translocon defines the hydrophobicity threshold for membrane integration. Mol. Biol. Cell 2010, 21:1662-1670.
100. Smith M.A., Clemons W.M., DeMars C.J., Flower A.M. Modeling the effects of prl mutations on the Escherichia coli SecY complex. J. Bacteriol. 2005, 187:6454-6465.
101. Tam P.C., Maillard A.P., Chan K.K., Duong F. Investigating the SecY plug movement at the SecYEG translocation channel. EMBO J. 2005, 24:3380-3388.
102. Trueman S.F., Mandon E.C., Gilmore R. Translocation channel gating kinetics balances protein translocation efficiency with signal sequence recognition fidelity. Mol. Biol. Cell 2011, 22:2983-2993.
103. Weihofen A., Binns K., Lemberg M.K., Ashman K., Martoglio B. Identification of signal peptide peptidase, a presenilin-type aspartic protease. Science 2002, 296:2215-2218.
104. Devaraneni P.K., Conti B., Matsumura Y., Yang Z., Johnson A.E., Skach W.R. Stepwise insertion and inversion of a type II signal anchor sequence in the ribosome-Sec61 translocon complex. Cell 2011, 146:134-147.
105. Alder N.N., Shen Y., Brodsky J.L., Hendershot L.M., Johnson A.E. The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum. J. Cell Biol. 2005, 168:389-399.
106. Schauble N., Lang S., Jung M., Cappel S., Schorr S., Ulucan O., Linxweiler J., Dudek J., Blum R., Helms V., Paton A.W., Paton J.C., Cavalie A., Zimmermann R. BiP-mediated closing of the Sec61 channel limits Ca2+ leakage from the ER. EMBO J. 2012, 31:3282-3296.
107. Panzner S., Dreier L., Hartmann E., Kostka S., Rapoport T.A. Posttranslational protein translocation in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 1995, 81:561-570.
108. Meyer H.A., Grau H., Kraft R., Kostka S., Prehn S., Kalies K.U., Hartmann E. Mammalian Sec61 is associated with Sec62 and Sec63. J. Biol. Chem. 2000, 275:14550-14557.
109. Tyedmers J., Lerner M., Bies C., Dudek J., Skowronek M.H., Haas I.G., Heim N., Nastainczyk W., Volkmer J., Zimmermann R. Homologs of the yeast Sec complex subunits Sec62p and Sec63p are abundant proteins in dog pancreas microsomes. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7214-7219.
110. Young B.P., Craven R., Reid P.J., Willer M., Stirling C.J. Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo. EMBO J. 2001, 20:262-271.
111. Lang S., Benedix J., Fedeles S.V., Schorr S., Schirra C., Schauble N., Jalal C., Greiner M., Hassdenteufel S., Tatzelt J., Kreutzer B., Edelmann L., Krause E., Rettig J., Somlo S., Zimmermann R., Dudek J. Different effects of Sec61alpha, Sec62 and Sec63 depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J. Cell Sci. 2012, 125:1958-1969.
112. Blau M., Mullapudi S., Becker T., Dudek J., Zimmermann R., Penczek P.A., Beckmann R. ERj1p uses a universal ribosomal adaptor site to coordinate the 80S ribosome at the membrane. Nat. Struct. Mol. Biol. 2005, 12:1015-1016.
113. Benedix J., Lajoie P., Jaiswal H., Burgard C., Greiner M., Zimmermann R., Rospert S., Snapp E.L., Dudek J. BiP modulates the affinity of its co-chaperone ERj1 for ribosomes. J. Biol. Chem. 2010, 285:36427-36433.
114. Erdmann F., Schauble N., Lang S., Jung M., Honigmann A., Ahmad M., Dudek J., Benedix J., Harsman A., Kopp A., Helms V., Cavalie A., Wagner R., Zimmermann R. Interaction of calmodulin with Sec61alpha limits Ca2+ leakage from the endoplasmic reticulum. EMBO J. 2011, 30:17-31.
115. Frauenfeld J., Gumbart J., Sluis E.O., Funes S., Gartmann M., Beatrix B., Mielke T., Berninghausen O., Becker T., Schulten K., Beckmann R. Cryo-EM structure of the ribosome-SecYE complex in the membrane environment. Nat. Struct. Mol. Biol. 2011, 18:614-621.
116. Kedrov A., Kusters I., Krasnikov V.V., Driessen A.J. A single copy of SecYEG is sufficient for preprotein translocation. EMBO J. 2011, 30:4387-4397.
117. Park E., Rapoport T.A. Bacterial protein translocation requires only one copy of the SecY complex in vivo. J. Cell Biol. 2012, 198:881-893.
118. Hanein D., Matlack K.E.S., Jungnickel B., Plath K., Kalies K.-U., Miller K.R., Rapoport T.A., Akey C.W. Oligomeric rings of the Sec61p complex induced by ligands required for protein translocation. Cell 1996, 87:721-732.
119. Snapp E.L., Reinhart G.A., Bogert B.A., Lippincott-Schwartz J., Hegde R.S. The organization of engaged and quiescent translocons in the endoplasmic reticulum of mammalian cells. J. Cell Biol. 2004, 164:997-1007.
120. Deville K., Gold V.A., Robson A., Whitehouse S., Sessions R.B., Baldwin S.A., Radford S.E., Collinson I. The oligomeric state and arrangement of the active bacterial translocon. J. Biol. Chem. 2011, 286:4659-4669.
121. Jermy A.J., Willer M., Davis E., Wilkinson B.M., Stirling C.J. The Brl domain in Sec63p is required for assembly of functional endoplasmic reticulum translocons. J. Biol. Chem. 2006, 281:7899-7906.
122. Dalal K., Chan C.S., Sligar S.G., Duong F. Two copies of the SecY channel and acidic lipids are necessary to activate the SecA translocation ATPase. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:4104-4109.
123. Osborne A.R., Rapoport T.A. Protein translocation is mediated by oligomers of the SecY complex with one SecY copy forming the channel. Cell 2007, 129:97-110.
124. Voigt S., Jungnickel B., Hartmann E., Rapoport T.A. Signal sequence-dependent function of the TRAM protein during early phases of translocation across the endoplasmic reticulum membrane. EMBO J. 1996, 134:25-35.
125. Fons R.D., Bogert B.A., Hegde R.S. Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane. J. Cell Biol. 2003, 160:529-539.
126. Shao S., Hegde R.S. Membrane protein insertion at the endoplasmic reticulum. Ann. Rev. Cell Dev. Biol. 2011, 27:25-56.
127. Woolhead C.A., McCormick P.J., Johnson A.E. Nascent membrane and secretory proteins differ in FRET-detected folding far inside the ribosome and in their exposure to ribosomal proteins. Cell 2004, 116:725-736.
128. Mothes W., Heinrich S.U., Graf R., Nilsson I., von Heijne G., Brunner J., Rapoport T.A. Molecular mechanism of membrane protein integration into the endoplasmic reticulum. Cell 1997, 89:523-533.
129. Hessa T., Kim H., Bihlmaier K., Lundin C., Boekel J., Andersson H., Nilsson I., White S.H., von Heijne G. Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 2005, 433:377-381.
130. Lundin C., Kim H., Nilsson I., White S.H., von Heijne G. Molecular code for protein insertion in the endoplasmic reticulum membrane is similar for N(in)-C(out) and N(out)-C(in) transmembrane helices. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:15702-15707.
131. Ismail N., Hedman R., Schiller N., von Heijne G. A biphasic pulling force acts on transmembrane helices during translocon-mediated membrane integration. Nat. Struct. Mol. Biol. 2012, 19:1018-1022.
132. Lin P.J., Jongsma C.G., Pool M.R., Johnson A.E. Polytopic membrane protein folding at L17 in the ribosome tunnel initiates cyclical changes at the translocon. J. Cell Biol. 2011, 195:55-70.
133. Sadlish H., Pitonzo D., Johnson A.E., Skach W.R. Sequential triage of transmembrane segments by Sec61alpha during biogenesis of a native multispanning membrane protein. Nat. Struct. Mol. Biol. 2005, 12:870-878.
134. Ismail N., Crawshaw S.G., Cross B.C., Haagsma A.C., High S. Specific transmembrane segments are selectively delayed at the ER translocon during opsin biogenesis. Biochem. J. 2008, 411:495-506.
135. Hou B., Lin P.J., Johnson A.E. Membrane protein TM segments are retained at the translocon during integration until the nascent chain cues FRET-detected release into bulk lipid. Mol. Cell 2012, 48:398-408.
136. Ojemalm K., Halling K.K., Nilsson I., von Heijne G. Orientational preferences of neighboring helices can drive ER insertion of a marginally hydrophobic transmembrane helix. Mol. Cell 2012, 45:529-540.
137. Larsen N., Zwieb C. SRP-RNA sequence alignment and secondary structure. Nucl. Acids Res. 1991, 19:209-215.