Membrane Protein Integration and Topogenesis at the ER
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Kyte J, Doolittle RF (1982) A simple method for displaying the hydropathic character of a protein. J Mol Biol 157:105–132. https://doi.org/10.1016/0022-2836(82)90515-0
Wimley WC (2002) Toward genomic identification of beta-barrel membrane proteins: composition and architecture of known structures. Protein Sci 11:301–312. https://doi.org/10.1110/ps.29402
Schiffrin B, Brockwell DJ, Radford SE (2017) Outer membrane protein folding from an energy landscape perspective. BMC Biol 15:123. https://doi.org/10.1186/s12915-017-0464-5
Gruss F, Zähringer F, Jakob RP et al (2013) The structural basis of autotransporter translocation by TamA. Nat Struct Mol Biol 20:1318–1320. https://doi.org/10.1038/nsmb.2689
Höhr AIC, Lindau C, Wirth C et al (2018) Membrane protein insertion through a mitochondrial β-barrel gate. Science 359:eaah6834. https://doi.org/10.1126/science.aah6834
Park E, Ménétret J-F, Gumbart JC et al (2014) Structure of the SecY channel during initiation of protein translocation. Nature 506:102–106. https://doi.org/10.1038/nature12720
Gogala M, Becker T, Beatrix B et al (2014) Structures of the Sec61 complex engaged in nascent peptide translocation or membrane insertion. Nature 506:107–110. https://doi.org/10.1038/nature12950
Voorhees RM, Hegde RS (2016) Structure of the Sec61 channel opened by a signal sequence. Science 351:88–91. https://doi.org/10.1126/science.aad4992
MacKinnon AL, Paavilainen VO, Sharma A et al (2014) An allosteric Sec61 inhibitor traps nascent transmembrane helices at the lateral gate. Elife 3:e01483. https://doi.org/10.7554/eLife.01483
Junne T, Wong J, Studer C et al (2015) Decatransin, a novel natural product inhibiting protein translocation at the Sec61/SecY translocon. J Cell Sci 128:1217–1229. https://doi.org/10.1242/jcs.165746
Paatero AO, Kellosalo J, Dunyak BM et al (2016) Apratoxin kills cells by direct blockade of the Sec61 protein translocation channel. Cell Chem Biol 23:561–566. https://doi.org/10.1016/j.chembiol.2016.04.008
Blobel G, Dobberstein B (1975) Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J Cell Biol 67:835–851. https://doi.org/10.1083/jcb.67.3.835
Heijne G (1986) The distribution of positively charged residues in bacterial inner membrane proteins correlates with the trans-membrane topology. EMBO J 5:3021–3027
Nilsson J, Persson B, von Heijne G (2005) Comparative analysis of amino acid distributions in integral membrane proteins from 107 genomes. Proteins 60:606–616. https://doi.org/10.1002/prot.20583
Hartmann E, Rapoport TA, Lodish HF (1989) Predicting the orientation of eukaryotic membrane-spanning proteins. Proc Natl Acad Sci USA 86:5786–5790
Szczesna-Skorupa E, Kemper B (1989) NH2-terminal substitutions of basic amino acids induce translocation across the microsomal membrane and glycosylation of rabbit cytochrome P450IIC2. J Cell Biol 108:1237–1243
Beltzer JP, Fiedler K, Fuhrer C et al (1991) Charged residues are major determinants of the transmembrane orientation of a signal-anchor sequence. J Biol Chem 266:973–978
Parks GD, Lamb RA (1991) Topology of eukaryotic type II membrane proteins: importance of N-terminal positively charged residues flanking the hydrophobic domain. Cell 64:777–787. https://doi.org/10.1016/0092-8674(91)90507-U
Denzer AJ, Nabholz CE, Spiess M (1995) Transmembrane orientation of signal-anchor proteins is affected by the folding state but not the size of the N-terminal domain. EMBO J 14:6311–6317
Sakaguchi M, Tomiyoshi R, Kuroiwa T et al (1992) Functions of signal and signal-anchor sequences are determined by the balance between the hydrophobic segment and the N-terminal charge. Proc Natl Acad Sci USA 89:16–19. https://doi.org/10.1073/pnas.89.1.16
Wahlberg JM, Spiess M (1997) Multiple determinants direct the orientation of signal-anchor proteins: the topogenic role of the hydrophobic signal domain. 137:555–562
Rösch K, Naeher D, Laird V et al (2000) The topogenic contribution of uncharged amino acids on signal sequence orientation in the endoplasmic reticulum. J Biol Chem 275:14916–14922. https://doi.org/10.1074/jbc.M000456200
Goder V, Spiess M (2003) Molecular mechanism of signal sequence orientation in the endoplasmic reticulum. EMBO J 22:3645–3653. https://doi.org/10.1093/emboj/cdg361
Devaraneni PK, Conti B, Matsumura Y et al (2011) Stepwise insertion and inversion of a type II signal anchor sequence in the ribosome-Sec61 translocon complex. Cell 146:134–147. https://doi.org/10.1016/j.cell.2011.06.004
Kocik L, Junne T, Spiess M (2012) Orientation of internal signal-anchor sequences at the Sec61 translocon. J Mol Biol 424:368–378. https://doi.org/10.1016/j.jmb.2012.10.010
McKenna M, Simmonds RE, High S (2017) Mycolactone reveals the substrate-driven complexity of Sec61-dependent transmembrane protein biogenesis. J Cell Sci 130:1307–1320. https://doi.org/10.1242/jcs.198655
Goder V, Junne T, Spiess M (2004) Sec61p contributes to signal sequence orientation according to the positive-inside rule. Mol Biol Cell 15:1470–1478. https://doi.org/10.1091/mbc.E03-08-0599
Junne T, Schwede T, Goder V, Spiess M (2007) Mutations in the Sec61p channel affecting signal sequence recognition and membrane protein topology. J Biol Chem 282:33201–33209. https://doi.org/10.1074/jbc.M707219200
Emr SD, Hanley-Way S, Silhavy TJ (1981) Suppressor mutations that restore export of a protein with a defective signal sequence. Cell 23:79–88
Tam PCK, Maillard AP, Chan KKY, Duong F (2005) Investigating the SecY plug movement at the SecYEG translocation channel. EMBO J 24:3380–3388. https://doi.org/10.1038/sj.emboj.7600804
Saparov SM, Erlandson K, Cannon K et al (2007) Determining the conductance of the SecY protein translocation channel for small molecules. Mol Cell 26:501–509. https://doi.org/10.1016/j.molcel.2007.03.022
Flower AM (2007) The SecY translocation complex: convergence of genetics and structure. Trends Microbiol. https://doi.org/10.1016/j.tim.2007.03.001
Audigier Y, Friedlander M, Blobel G (1987) Multiple topogenic sequences in bovine opsin. Proc Natl Acad Sci USA 84:5783–5787. https://doi.org/10.1073/pnas.84.16.5783
Wessels HP, Spiess M (1988) Insertion of a multispanning membrane protein occurs sequentially and requires only one signal sequence. Cell 55:61–70
Lipp J, Flint N, Haeuptle MT, Dobberstein B (1989) Structural requirements for membrane assembly of proteins spanning the membrane several times. J Cell Biol 109:2013–2022. https://doi.org/10.1083/jcb.109.5.2013
Sato M, Hresko R, Mueckler M (1998) Testing the charge difference hypothesis for the assembly of a eucaryotic multispanning membrane protein. J Biol Chem 273:25203–25208. https://doi.org/10.1074/jbc.273.39.25203
Sato M, Mueckler M (1999) A conserved amino acid motif (R-X-G-R-R) in the Glut1 glucose transporter is an important determinant of membrane topology. J Biol Chem 274:24721–24725. https://doi.org/10.1074/jbc.274.35.24721
Gafvelin G, von Heijne G (1994) Topological “frustration” in multispanning E. coli inner membrane proteins. Cell 77:401–412. https://doi.org/10.1016/0092-8674(94)90155-4
Goder V, Bieri C, Spiess M (1999) Glycosylation can influence topogenesis of membrane proteins and reveals dynamic reorientation of nascent polypeptides within the translocon. J Cell Biol 147:257–266
Tu L, Khanna P, Deutsch C (2014) Transmembrane segments form tertiary hairpins in the folding vestibule of the ribosome. J Mol Biol 426:185–198. https://doi.org/10.1016/j.jmb.2013.09.013
Hessa T, Kim H, Bihlmaier K et al (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377–381. https://doi.org/10.1038/nature03216
Hessa T, Meindl-Beinker NM, Bernsel A et al (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450:1026–1030. https://doi.org/10.1038/nature06387
Hedin LE, Ojemalm K, Bernsel A et al (2010) Membrane insertion of marginally hydrophobic transmembrane helices depends on sequence context. J Mol Biol 396:221–229. https://doi.org/10.1016/j.jmb.2009.11.036
MacCallum JL, Tieleman DP (2011) Hydrophobicity scales: a thermodynamic looking glass into lipid-protein interactions. Trends Biochem Sci 36:653–662. https://doi.org/10.1016/j.tibs.2011.08.003
Schow EV, Freites JA, Cheng P et al (2011) Arginine in membranes: the connection between molecular dynamics simulations and translocon-mediated insertion experiments. J Membr Biol 239:35–48. https://doi.org/10.1007/s00232-010-9330-x
Gumbart JC, Teo I, Roux B, Schulten K (2013) Reconciling the roles of kinetic and thermodynamic factors in membrane-protein insertion. J Am Chem Soc 135:2291–2297. https://doi.org/10.1021/ja310777k
Junne T, Kocik L, Spiess M (2010) The hydrophobic core of the Sec61 translocon defines the hydrophobicity threshold for membrane integration. Mol Biol Cell 21:1662–1670. https://doi.org/10.1091/mbc.E10-01-0060
Demirci E, Junne T, Baday S et al (2013) Functional asymmetry within the Sec61p translocon. Proc Natl Acad Sci USA 110:18856–18861. https://doi.org/10.1073/pnas.1318432110
Ismail N, Hedman R, Schiller N, von Heijne G (2012) A biphasic pulling force acts on transmembrane helices during translocon-mediated membrane integration. Nat Struct Mol Biol 19:1018–1022. https://doi.org/10.1038/nsmb.2376
Junne T, Spiess M (2017) Integration of transmembrane domains is regulated by their downstream sequences. J Cell Sci 130:372–381. https://doi.org/10.1242/jcs.194472
Lundin C, Kim H, Nilsson I et al (2008) 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 USA 105:15702–15707. https://doi.org/10.1073/pnas.0804842105
Cymer F, Ismail N, von Heijne G (2014) Weak pulling forces exerted on Nin-orientated transmembrane segments during co-translational insertion into the inner membrane of Escherichia coli. FEBS Lett 588:1930–1934. https://doi.org/10.1016/j.febslet.2014.03.050
Deshaies RJ, Sanders SL, Feldheim DA, Schekman R (1991) Assembly of yeast Sec proteins involved in translocation into the endoplasmic reticulum into a membrane-bound multisubunit complex. Nature 349:806–808. https://doi.org/10.1038/349806a0
Panzner S, Dreier L, Hartmann E et al (1995) Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p. Cell 81:561–570
Itskanov S, Park E (2019) Structure of the posttranslational Sec protein-translocation channel complex from yeast. Science 363:84–87. https://doi.org/10.1126/science.aav6740
Wu X, Cabanos C, Rapoport TA (2019) Structure of the post-translational protein translocation machinery of the ER membrane. Nature 566:136–139. https://doi.org/10.1038/s41586-018-0856-x
Brodsky JL, Goeckeler J, Schekman R (1995) BiP and Sec63p are required for both co- and posttranslational protein translocation into the yeast endoplasmic reticulum. Proc Natl Acad Sci USA 92:9643–9646
Young BP, Craven RA, Reid PJ et al (2001) Sec63p and Kar2p are required for the translocation of SRP-dependent precursors into the yeast endoplasmic reticulum in vivo. EMBO J 20:262–271. https://doi.org/10.1093/emboj/20.1.262
Lang S, Benedix J, Fedeles SV et al (2012) Different effects of Sec61α, Sec62 and Sec63 depletion on transport of polypeptides into the endoplasmic reticulum of mammalian cells. J Cell Sci 125:1958–1969. https://doi.org/10.1242/jcs.096727
Voigt S, Jungnickel B, Hartmann E, Rapoport TA (1996) Signal sequence-dependent function of the TRAM protein during early phases of protein transport across the endoplasmic reticulum membrane. J Cell Biol 134:25–35
Chen Q, Denard B, Lee C-E et al (2016) Inverting the topology of a transmembrane protein by regulating the translocation of the first transmembrane helix. Mol Cell 63:567–578. https://doi.org/10.1016/j.molcel.2016.06.032
Jonikas MC, Collins SR, Denic V et al (2009) Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 323:1693–1697. https://doi.org/10.1126/science.1167983
Chitwood PJ, Juszkiewicz S, Guna A et al (2018) EMC is required to initiate accurate membrane protein topogenesis. Cell 175:1507–1519.e16. https://doi.org/10.1016/j.cell.2018.10.009
Shurtleff MJ, Itzhak DN, Hussmann JA et al (2018) The ER membrane protein complex interacts cotranslationally to enable biogenesis of multipass membrane proteins. Elife 7:382. https://doi.org/10.7554/eLife.37018
van den Berg B, Clemons WM, Collinson I et al (2004) X-ray structure of a protein-conducting channel. Nature 427:36–44. https://doi.org/10.1038/nature02218
Sommer N, Junne T, Kalies K-U et al (2013) TRAP assists membrane protein topogenesis at the mammalian ER membrane. Biochim Biophys Acta 1833:3104–3111. https://doi.org/10.1016/j.bbamcr.2013.08.018
Hessa T, Reithinger JH, von Heijne G, Kim H (2009) Analysis of transmembrane helix integration in the endoplasmic reticulum in S. cerevisiae. J Mol Biol 386:1222–1228
Xie K, Hessa T, Seppälä S et al (2007) Features of transmembrane segments that promote the lateral release from the translocase into the lipid phase. Biochemistry 46:15153–15161. https://doi.org/10.1021/bi701398y