Apolar surface area determines the efficiency of translocon-mediated membrane-protein integration into the endoplasmic reticulum

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 31, 2011, Pages

  Öjemalm, Karin ^a   Higuchi, Takashi ^b   Jiang, Yang ^a   Langel, Ülo ^a   Nilsson, IngMarie ^a   White, Stephen H ^c   Suga, Hiroaki ^b   Von Heijne, Gunnar ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Flexizyme; Hydrophobicity; Nonproteinogenic amino acid; Transmembrane helix

Indexed keywords

ALIPHATIC COMPOUND; AROMATIC AMINO ACID; TRANSLOCON;

AQUEOUS SOLUTION; ARTICLE; ENDOPLASMIC RETICULUM; HYDROPHOBICITY; NONHUMAN; PHASE PARTITIONING; PRIORITY JOURNAL; SOLVATION; THERMODYNAMICS;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; DOGS; ENDOPLASMIC RETICULUM; ESCHERICHIA COLI PROTEINS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN STRUCTURE, SECONDARY; PROTEIN TRANSPORT; SERINE ENDOPEPTIDASES; STATIC ELECTRICITY; THERMODYNAMICS;

EGEA;

EID: 79961238544     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1100120108     Document Type: Article

References (35)

1. Rapoport TA (2007) Protein translocation across the eukaryotic endoplasmic reticulum and bacterial plasma membranes. Nature 450:663-669.
2. White SH, von Heijne G (2008) How translocons select transmembrane helices. Annu Rev Biophys 37:23-42.
3. Hessa T, et al. (2007) Molecular code for transmembrane-helix recognition by the Sec61 translocon. Nature 450:1026-1030. (Pubitemid 350273612)
4. van den Berg B, et al. (2004) X-ray structure of a protein-conducting channel. Nature 427:36-44.
5. Egea PF, Stroud RM (2010) Lateral opening of a translocon upon entry of protein suggests the mechanism of insertion into membranes. Proc Natl Acad Sci USA 107:17182-17187.
6. Hessa T, et al. (2005) Recognition of transmembrane helices by the endoplasmic reticulum translocon. Nature 433:377-381. (Pubitemid 40203311)
7. Schow EV, et al. (2011) Arginine in membranes: The connection between molecular dynamics simulations and translocon-mediated insertion experiments. J Membr Biol 239:35-48.
8. Murakami H, Ohta A, Ashigai H, Suga H (2006) A highly flexible tRNA acylation method for non-natural polypeptide synthesis. Nat Methods 3:357-359.
9. Xiao H, Murakami H, Suga H, Ferre-D'Amare AR (2008) Structural basis of specific tRNA aminoacylation by a small in vitro selected ribozyme. Nature 454:358-361.
10. Johansson M, Nilsson I, von Heijne G (1993) Positively charged amino acids placed next to a signal sequence block protein translocation more efficiently in Escherichia coli than in mammalian microsomes. Mol Gen Genet 239:251-256. (Pubitemid 23167505)
11. Sääf A, Wallin E, von Heijne G (1998) Stop-transfer function of pseudo-random amino acid segments during translocation across prokaryotic and eukaryotic membranes. Eur J Biochem 251:821-829. (Pubitemid 28108978)
12. Wimley WC, Creamer TP, White SH (1996) Solvation energies of amino acid sidechains and backbone in a family of host-guest pentapeptides. Biochemistry 35:5109-5124.
13. Karplus PA (1997) Hydrophobicity regained. Protein Sci 6:1302-1307.
14. Marqusee JA, Dill KA (1986) Solute partitioning into chain molecule interphases: Monolayers, bilayer membranes, and micelles. J Chem Phys 85:434-444.
15. White SH, King GI, Cain JE (1981) Location of hexane in lipid bilayers determined by neutron diffraction. Nature 290:161-163. (Pubitemid 11149697)
16. Yau WM, Wimley WC, Gawrisch K, White SH (1998) The preference of tryptophan for membrane interfaces. Biochemistry 37:14713-14718. (Pubitemid 28487579)
17. Buton X, Morrot G, Fellmann P, Seigneuret M (1996) Ultrafast glycerophospholipidselective transbilayer motion mediated by a protein in the endoplasmic reticulum membrane. J Biol Chem 271:6651-6657. (Pubitemid 26104093)
18. van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: Where they are and how they behave. Nat Rev Mol Cell Biol 9:112-124. (Pubitemid 351158912)
19. Heinrich S, Mothes W, Brunner J, Rapoport T (2000) The Sec61p complex mediates the integration of a membrane protein by allowing lipid partitioning of the transmembrane domain. Cell 102:233-244.
20. Gumbart J, Chipot C, Schulten K (2011) Free-energy cost for translocon-assisted insertion of membrane proteins. Proc Natl Acad Sci USA 108:3596-3601.
21. Rychkova A, Vicatos S, Warshel A (2010) On the energetics of translocon-assisted insertion of charged transmembrane helices into membranes. Proc Natl Acad Sci USA 107:17598-17603.
22. Zimmer J, Nam Y, Rapoport TA (2008) Structure of a complex of the ATPase SecA and the protein-translocation channel. Nature 455:936-943.
23. Tsukazaki T, et al. (2008) Conformational transition of Sec machinery inferred from bacterial SecYE structures. Nature 455:988-991.
24. Johansson AC, Lindahl E (2009) The role of lipid composition for insertion and stabilization of amino acids in membranes. J Chem Phys 130:185101.
25. Chothia C (1976) The nature of the accessible and buried surfaces in proteins. J Mol Biol 105:1-12.
26. Eisenberg D, McLachlan AD (1986) Solvation energy in protein folding. Nature 319:199-203.
27. Hermann RB (1977) Use of solvent cavity area and number of packed solvent molecules around a solute in regard to hydrocarbon solubilities and hydrophobic interactions. Proc Natl Acad Sci USA 74:4144-4145.
28. Reynolds JA, Gilbert DB, Tanford C (1974) Empirical correlation between hydrophobic free energy and aqueous cavity surface area. Proc Natl Acad Sci USA 71:2925-2927.
29. Junne T, Kocik L, SpiessM(2010) The hydrophobic core of the Sec61 translocon defines the hydrophobicity threshold for membrane integration. Mol Biol Cell 21:1662-1670.
30. Simon SM, Peskin CS, Oster GF (1992) What drives the translocation of proteins? Proc Natl Acad Sci USA 89:3770-3774.
31. Liebermeister W, Rapoport TA, Heinrich R (2001) Ratcheting in post-translational protein translocation: A mathematical model. J Mol Biol 305:643-656. (Pubitemid 33032868)
32. Ohta A, Murakami H, Higashimura E, Suga H (2007) Synthesis of polyester by means of genetic code reprogramming. Chem Biol 14:1315-1322. (Pubitemid 350257006)
33. Saito H, Kourouklis D, Suga H (2001) An in vitro evolved precursor tRNA with aminoacylation activity. EMBO J 20:1797-1806. (Pubitemid 32299415)
34. Nilsson I, Johnson AE, von Heijne G (2003) How hydrophobic is alanine? J Biol Chem 278:29389-29393. (Pubitemid 36962317)
35. Hedin LE, et al. (2010) Membrane insertion of marginally hydrophobic transmembrane helices depends on sequence context. J Mol Biol 396:221-229.