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. 2000 May 1;347(Pt 3):601–612. doi: 10.1042/0264-6021:3470601

Role of lipids in the translocation of proteins across membranes.

F Van Voorst 1, B De Kruijff 1
PMCID: PMC1220995  PMID: 10769162

Abstract

The architecture of cells, with various membrane-bound compartments and with the protein synthesizing machinery confined to one location, dictates that many proteins have to be transported through one or more membranes during their biogenesis. A lot of progress has been made on the identification of protein translocation machineries and their sorting signals in various organelles and organisms. Biochemical characterization has revealed the functions of several individual protein components. Interestingly, lipid components were also found to be essential for the correct functioning of these translocases. This led to the idea that there is a very intimate relationship between the lipid and protein components that enables them to fulfil their intriguing task of transporting large biopolymers through a lipid bilayer without leaking their contents. In this review we focus on the Sec translocases in the endoplasmic reticulum and the bacterial inner membrane. We also highlight the interactions of lipids and proteins during the process of translocation and integrate this into a model that enables us to understand the role of membrane lipid composition in translocase function.

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Selected References

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  1. Adam S. A. Transport pathways of macromolecules between the nucleus and the cytoplasm. Curr Opin Cell Biol. 1999 Jun;11(3):402–406. doi: 10.1016/S0955-0674(99)80056-8. [DOI] [PubMed] [Google Scholar]
  2. Ahn T., Kim H. Effects of nonlamellar-prone lipids on the ATPase activity of SecA bound to model membranes. J Biol Chem. 1998 Aug 21;273(34):21692–21698. doi: 10.1074/jbc.273.34.21692. [DOI] [PubMed] [Google Scholar]
  3. Ahn T., Kim H. SecA of Escherichia coli traverses lipid bilayer of phospholipid vesicles. Biochem Biophys Res Commun. 1994 Aug 30;203(1):326–330. doi: 10.1006/bbrc.1994.2185. [DOI] [PubMed] [Google Scholar]
  4. Batenburg A. M., Demel R. A., Verkleij A. J., de Kruijff B. Penetration of the signal sequence of Escherichia coli PhoE protein into phospholipid model membranes leads to lipid-specific changes in signal peptide structure and alterations of lipid organization. Biochemistry. 1988 Jul 26;27(15):5678–5685. doi: 10.1021/bi00415a043. [DOI] [PubMed] [Google Scholar]
  5. Bogdanov M., Dowhan W. Phosphatidylethanolamine is required for in vivo function of the membrane-associated lactose permease of Escherichia coli. J Biol Chem. 1995 Jan 13;270(2):732–739. doi: 10.1074/jbc.270.2.732. [DOI] [PubMed] [Google Scholar]
  6. Bogdanov M., Dowhan W. Phospholipid-assisted protein folding: phosphatidylethanolamine is required at a late step of the conformational maturation of the polytopic membrane protein lactose permease. EMBO J. 1998 Sep 15;17(18):5255–5264. doi: 10.1093/emboj/17.18.5255. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Bogdanov M., Sun J., Kaback H. R., Dowhan W. A phospholipid acts as a chaperone in assembly of a membrane transport protein. J Biol Chem. 1996 May 17;271(20):11615–11618. doi: 10.1074/jbc.271.20.11615. [DOI] [PubMed] [Google Scholar]
  8. Bogdanov M., Umeda M., Dowhan W. Phospholipid-assisted refolding of an integral membrane protein. Minimum structural features for phosphatidylethanolamine to act as a molecular chaperone. J Biol Chem. 1999 Apr 30;274(18):12339–12345. doi: 10.1074/jbc.274.18.12339. [DOI] [PubMed] [Google Scholar]
  9. Breukink E., Demel R. A., de Korte-Kool G., de Kruijff B. SecA insertion into phospholipids is stimulated by negatively charged lipids and inhibited by ATP: a monolayer study. Biochemistry. 1992 Feb 4;31(4):1119–1124. doi: 10.1021/bi00119a021. [DOI] [PubMed] [Google Scholar]
  10. Cantor R. S. Lipid composition and the lateral pressure profile in bilayers. Biophys J. 1999 May;76(5):2625–2639. doi: 10.1016/S0006-3495(99)77415-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cantor R. S. The lateral pressure profile in membranes: a physical mechanism of general anesthesia. Toxicol Lett. 1998 Nov 23;100-101:451–458. doi: 10.1016/s0378-4274(98)00220-3. [DOI] [PubMed] [Google Scholar]
  12. Chen X., Brown T., Tai P. C. Identification and characterization of protease-resistant SecA fragments: secA has two membrane-integral forms. J Bacteriol. 1998 Feb;180(3):527–537. doi: 10.1128/jb.180.3.527-537.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chupin V., Killian J. A., Breg J., de Jongh H. H., Boelens R., Kaptein R., de Kruijff B. PhoE signal peptide inserts into micelles as a dynamic helix-break-helix structure, which is modulated by the environment. A two-dimensional 1H NMR study. Biochemistry. 1995 Sep 12;34(36):11617–11624. doi: 10.1021/bi00036a038. [DOI] [PubMed] [Google Scholar]
  14. Crookes W. J., Olsen L. J. Peroxin puzzles and folded freight: peroxisomal protein import in review. Naturwissenschaften. 1999 Feb;86(2):51–61. doi: 10.1007/s001140050572. [DOI] [PubMed] [Google Scholar]
  15. Crowley K. S., Liao S., Worrell V. E., Reinhart G. D., Johnson A. E. Secretory proteins move through the endoplasmic reticulum membrane via an aqueous, gated pore. Cell. 1994 Aug 12;78(3):461–471. doi: 10.1016/0092-8674(94)90424-3. [DOI] [PubMed] [Google Scholar]
  16. 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 Jun 18;73(6):1101–1115. doi: 10.1016/0092-8674(93)90640-c. [DOI] [PubMed] [Google Scholar]
  17. Dalbey R. E., Lively M. O., Bron S., van Dijl J. M. The chemistry and enzymology of the type I signal peptidases. Protein Sci. 1997 Jun;6(6):1129–1138. doi: 10.1002/pro.5560060601. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dalbey R. E., Robinson C. Protein translocation into and across the bacterial plasma membrane and the plant thylakoid membrane. Trends Biochem Sci. 1999 Jan;24(1):17–22. doi: 10.1016/s0968-0004(98)01333-4. [DOI] [PubMed] [Google Scholar]
  19. Daum G., Lees N. D., Bard M., Dickson R. Biochemistry, cell biology and molecular biology of lipids of Saccharomyces cerevisiae. Yeast. 1998 Dec;14(16):1471–1510. doi: 10.1002/(SICI)1097-0061(199812)14:16<1471::AID-YEA353>3.0.CO;2-Y. [DOI] [PubMed] [Google Scholar]
  20. DeChavigny A., Heacock P. N., Dowhan W. Sequence and inactivation of the pss gene of Escherichia coli. Phosphatidylethanolamine may not be essential for cell viability. J Biol Chem. 1991 Mar 15;266(8):5323–5332. [PubMed] [Google Scholar]
  21. Do H., Falcone D., Lin J., Andrews D. W., Johnson A. E. The cotranslational integration of membrane proteins into the phospholipid bilayer is a multistep process. Cell. 1996 May 3;85(3):369–378. doi: 10.1016/s0092-8674(00)81115-0. [DOI] [PubMed] [Google Scholar]
  22. Dowhan W. Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annu Rev Biochem. 1997;66:199–232. doi: 10.1146/annurev.biochem.66.1.199. [DOI] [PubMed] [Google Scholar]
  23. Duong F., Wickner W. Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme. EMBO J. 1997 May 15;16(10):2756–2768. doi: 10.1093/emboj/16.10.2756. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Duong F., Wickner W. Sec-dependent membrane protein biogenesis: SecYEG, preprotein hydrophobicity and translocation kinetics control the stop-transfer function. EMBO J. 1998 Feb 2;17(3):696–705. doi: 10.1093/emboj/17.3.696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Duong F., Wickner W. The SecDFyajC domain of preprotein translocase controls preprotein movement by regulating SecA membrane cycling. EMBO J. 1997 Aug 15;16(16):4871–4879. doi: 10.1093/emboj/16.16.4871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Economou A., Pogliano J. A., Beckwith J., Oliver D. B., Wickner W. SecA membrane cycling at SecYEG is driven by distinct ATP binding and hydrolysis events and is regulated by SecD and SecF. Cell. 1995 Dec 29;83(7):1171–1181. doi: 10.1016/0092-8674(95)90143-4. [DOI] [PubMed] [Google Scholar]
  27. Economou A., Wickner W. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion. Cell. 1994 Sep 9;78(5):835–843. doi: 10.1016/s0092-8674(94)90582-7. [DOI] [PubMed] [Google Scholar]
  28. Eichler J., Brunner J., Wickner W. The protease-protected 30 kDa domain of SecA is largely inaccessible to the membrane lipid phase. EMBO J. 1997 May 1;16(9):2188–2196. doi: 10.1093/emboj/16.9.2188. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Eichler J., Rinard K., Wickner W. Endogenous SecA catalyzes preprotein translocation at SecYEG. J Biol Chem. 1998 Aug 21;273(34):21675–21681. doi: 10.1074/jbc.273.34.21675. [DOI] [PubMed] [Google Scholar]
  30. Eichler J., Wickner W. Both an N-terminal 65-kDa domain and a C-terminal 30-kDa domain of SecA cycle into the membrane at SecYEG during translocation. Proc Natl Acad Sci U S A. 1997 May 27;94(11):5574–5581. doi: 10.1073/pnas.94.11.5574. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Eichler J., Wickner W. The SecA subunit of Escherichia coli preprotein translocase is exposed to the periplasm. J Bacteriol. 1998 Nov;180(21):5776–5779. doi: 10.1128/jb.180.21.5776-5779.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Engelman D. M., Steitz T. A. The spontaneous insertion of proteins into and across membranes: the helical hairpin hypothesis. Cell. 1981 Feb;23(2):411–422. doi: 10.1016/0092-8674(81)90136-7. [DOI] [PubMed] [Google Scholar]
  33. Görlich D., Hartmann E., Prehn S., Rapoport T. A. A protein of the endoplasmic reticulum involved early in polypeptide translocation. Nature. 1992 May 7;357(6373):47–52. doi: 10.1038/357047a0. [DOI] [PubMed] [Google Scholar]
  34. Hamman B. D., Chen J. C., Johnson E. E., Johnson A. E. The aqueous pore through the translocon has a diameter of 40-60 A during cotranslational protein translocation at the ER membrane. Cell. 1997 May 16;89(4):535–544. doi: 10.1016/s0092-8674(00)80235-4. [DOI] [PubMed] [Google Scholar]
  35. Hamman B. D., Hendershot L. M., Johnson A. E. BiP maintains the permeability barrier of the ER membrane by sealing the lumenal end of the translocon pore before and early in translocation. Cell. 1998 Mar 20;92(6):747–758. doi: 10.1016/s0092-8674(00)81403-8. [DOI] [PubMed] [Google Scholar]
  36. Hanein D., Matlack K. E., 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 Nov 15;87(4):721–732. doi: 10.1016/s0092-8674(00)81391-4. [DOI] [PubMed] [Google Scholar]
  37. Harris C. R., Silhavy T. J. Mapping an interface of SecY (PrlA) and SecE (PrlG) by using synthetic phenotypes and in vivo cross-linking. J Bacteriol. 1999 Jun;181(11):3438–3444. doi: 10.1128/jb.181.11.3438-3444.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Hartl F. U., Lecker S., Schiebel E., Hendrick J. P., Wickner W. The binding cascade of SecB to SecA to SecY/E mediates preprotein targeting to the E. coli plasma membrane. Cell. 1990 Oct 19;63(2):269–279. doi: 10.1016/0092-8674(90)90160-g. [DOI] [PubMed] [Google Scholar]
  39. Heacock P. N., Dowhan W. Alteration of the phospholipid composition of Escherichia coli through genetic manipulation. J Biol Chem. 1989 Sep 5;264(25):14972–14977. [PubMed] [Google Scholar]
  40. Heacock P. N., Dowhan W. Construction of a lethal mutation in the synthesis of the major acidic phospholipids of Escherichia coli. J Biol Chem. 1987 Sep 25;262(27):13044–13049. [PubMed] [Google Scholar]
  41. Hendrick J. P., Wickner W. SecA protein needs both acidic phospholipids and SecY/E protein for functional high-affinity binding to the Escherichia coli plasma membrane. J Biol Chem. 1991 Dec 25;266(36):24596–24600. [PubMed] [Google Scholar]
  42. Hoyt D. W., Gierasch L. M. A peptide corresponding to an export-defective mutant OmpA signal sequence with asparagine in the hydrophobic core is unable to insert into model membranes. J Biol Chem. 1991 Aug 5;266(22):14406–14412. [PubMed] [Google Scholar]
  43. Jordi W., Hergersberg C., de Kruijff B. Bilayer-penetrating properties enable apocytochrome c to follow a special import pathway into mitochondria. Eur J Biochem. 1992 Mar 1;204(2):841–846. doi: 10.1111/j.1432-1033.1992.tb16703.x. [DOI] [PubMed] [Google Scholar]
  44. Kaufmann A., Manting E. H., Veenendaal A. K., Driessen A. J., van der Does C. Cysteine-directed cross-linking demonstrates that helix 3 of SecE is close to helix 2 of SecY and helix 3 of a neighboring SecE. Biochemistry. 1999 Jul 13;38(28):9115–9125. doi: 10.1021/bi990539d. [DOI] [PubMed] [Google Scholar]
  45. Keegstra K., Cline K. Protein import and routing systems of chloroplasts. Plant Cell. 1999 Apr;11(4):557–570. doi: 10.1105/tpc.11.4.557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Keller R. C., Snel M. M., de Kruijff B., Marsh D. SecA restricts, in a nucleotide-dependent manner, acyl chain mobility up to the center of a phospholipid bilayer. FEBS Lett. 1995 Jan 30;358(3):251–254. doi: 10.1016/0014-5793(94)01439-8. [DOI] [PubMed] [Google Scholar]
  47. Keller R. C., ten Berge D., Nouwen N., Snel M. M., Tommassen J., Marsh D., de Kruijff B. Mode of insertion of the signal sequence of a bacterial precursor protein into phospholipid bilayers as revealed by cysteine-based site-directed spectroscopy. Biochemistry. 1996 Mar 5;35(9):3063–3071. doi: 10.1021/bi951870+. [DOI] [PubMed] [Google Scholar]
  48. Killian J. A. Hydrophobic mismatch between proteins and lipids in membranes. Biochim Biophys Acta. 1998 Nov 10;1376(3):401–415. doi: 10.1016/s0304-4157(98)00017-3. [DOI] [PubMed] [Google Scholar]
  49. Killian J. A., de Jong A. M., Bijvelt J., Verkleij A. J., de Kruijff B. Induction of non-bilayer lipid structures by functional signal peptides. EMBO J. 1990 Mar;9(3):815–819. doi: 10.1002/j.1460-2075.1990.tb08178.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Kim Y. J., Rajapandi T., Oliver D. SecA protein is exposed to the periplasmic surface of the E. coli inner membrane in its active state. Cell. 1994 Sep 9;78(5):845–853. doi: 10.1016/s0092-8674(94)90602-5. [DOI] [PubMed] [Google Scholar]
  51. Kusters R., Breukink E., Gallusser A., Kuhn A., de Kruijff B. A dual role for phosphatidylglycerol in protein translocation across the Escherichia coli inner membrane. J Biol Chem. 1994 Jan 14;269(2):1560–1563. [PubMed] [Google Scholar]
  52. Kusters R., Dowhan W., de Kruijff B. Negatively charged phospholipids restore prePhoE translocation across phosphatidylglycerol-depleted Escherichia coli inner membranes. J Biol Chem. 1991 May 15;266(14):8659–8662. [PubMed] [Google Scholar]
  53. Káldi K., Neupert W. Protein translocation into mitochondria. Biofactors. 1998;8(3-4):221–224. doi: 10.1002/biof.5520080308. [DOI] [PubMed] [Google Scholar]
  54. Laird V., High S. Discrete cross-linking products identified during membrane protein biosynthesis. J Biol Chem. 1997 Jan 17;272(3):1983–1989. doi: 10.1074/jbc.272.3.1983. [DOI] [PubMed] [Google Scholar]
  55. Lazdunski C., Baty D., Pagès J. M. Procaine, a local anesthetic interacting with the cell membrane, inhibits the processing of precursor forms of periplasmic proteins in Escherichia coli. Eur J Biochem. 1979 May 2;96(1):49–57. doi: 10.1111/j.1432-1033.1979.tb13012.x. [DOI] [PubMed] [Google Scholar]
  56. Leenhouts J. M., van den Wijngaard P. W., de Kroon A. I., de Kruijff B. Anionic phospholipids can mediate membrane insertion of the anionic part of a bound peptide. FEBS Lett. 1995 Aug 21;370(3):189–192. doi: 10.1016/0014-5793(95)00823-r. [DOI] [PubMed] [Google Scholar]
  57. Lill R., Cunningham K., Brundage L. A., Ito K., Oliver D., Wickner W. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli. EMBO J. 1989 Mar;8(3):961–966. doi: 10.1002/j.1460-2075.1989.tb03458.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Lill R., Dowhan W., Wickner W. The ATPase activity of SecA is regulated by acidic phospholipids, SecY, and the leader and mature domains of precursor proteins. Cell. 1990 Jan 26;60(2):271–280. doi: 10.1016/0092-8674(90)90742-w. [DOI] [PubMed] [Google Scholar]
  59. Lopez C. D., Yost C. S., Prusiner S. B., Myers R. M., Lingappa V. R. Unusual topogenic sequence directs prion protein biogenesis. Science. 1990 Apr 13;248(4952):226–229. doi: 10.1126/science.1970195. [DOI] [PubMed] [Google Scholar]
  60. Martoglio B., Hofmann M. W., Brunner J., Dobberstein B. The protein-conducting channel in the membrane of the endoplasmic reticulum is open laterally toward the lipid bilayer. Cell. 1995 Apr 21;81(2):207–214. doi: 10.1016/0092-8674(95)90330-5. [DOI] [PubMed] [Google Scholar]
  61. Matlack K. E., Mothes W., Rapoport T. A. Protein translocation: tunnel vision. Cell. 1998 Feb 6;92(3):381–390. doi: 10.1016/s0092-8674(00)80930-7. [DOI] [PubMed] [Google Scholar]
  62. Meyer T. H., Ménétret J. F., Breitling R., Miller K. R., Akey C. W., Rapoport T. A. The bacterial SecY/E translocation complex forms channel-like structures similar to those of the eukaryotic Sec61p complex. J Mol Biol. 1999 Jan 29;285(4):1789–1800. doi: 10.1006/jmbi.1998.2413. [DOI] [PubMed] [Google Scholar]
  63. Morein S., Andersson A., Rilfors L., Lindblom G. Wild-type Escherichia coli cells regulate the membrane lipid composition in a "window" between gel and non-lamellar structures. J Biol Chem. 1996 Mar 22;271(12):6801–6809. doi: 10.1074/jbc.271.12.6801. [DOI] [PubMed] [Google Scholar]
  64. Munro S. An investigation of the role of transmembrane domains in Golgi protein retention. EMBO J. 1995 Oct 2;14(19):4695–4704. doi: 10.1002/j.1460-2075.1995.tb00151.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Nishiyama K., Fukuda A., Morita K., Tokuda H. Membrane deinsertion of SecA underlying proton motive force-dependent stimulation of protein translocation. EMBO J. 1999 Feb 15;18(4):1049–1058. doi: 10.1093/emboj/18.4.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Nishiyama K., Mizushima S., Tokuda H. A novel membrane protein involved in protein translocation across the cytoplasmic membrane of Escherichia coli. EMBO J. 1993 Sep;12(9):3409–3415. doi: 10.1002/j.1460-2075.1993.tb06015.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Nishiyama K., Suzuki T., Tokuda H. Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation. Cell. 1996 Apr 5;85(1):71–81. doi: 10.1016/s0092-8674(00)81083-1. [DOI] [PubMed] [Google Scholar]
  68. Nouwen N., Tommassen J., de Kruijff B. Requirement for conformational flexibility in the signal sequence of precursor protein. J Biol Chem. 1994 Jun 10;269(23):16029–16033. [PubMed] [Google Scholar]
  69. Nouwen N., de Kruijff B., Tommassen J. Delta mu H+ dependency of in vitro protein translocation into Escherichia coli inner-membrane vesicles varies with the signal-sequence core-region composition. Mol Microbiol. 1996 Mar;19(6):1205–1214. doi: 10.1111/j.1365-2958.1996.tb02466.x. [DOI] [PubMed] [Google Scholar]
  70. Paetzel M., Dalbey R. E., Strynadka N. C. Crystal structure of a bacterial signal peptidase in complex with a beta-lactam inhibitor. Nature. 1998 Nov 12;396(6707):186–190. doi: 10.1038/24196. [DOI] [PubMed] [Google Scholar]
  71. Pilon M., Schekman R. Protein translocation: how Hsp70 pulls it off. Cell. 1999 Jun 11;97(6):679–682. doi: 10.1016/s0092-8674(00)80780-1. [DOI] [PubMed] [Google Scholar]
  72. 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 Sep 18;94(6):795–807. doi: 10.1016/s0092-8674(00)81738-9. [DOI] [PubMed] [Google Scholar]
  73. Pugsley A. P., Francetic O., Hardie K., Possot O. M., Sauvonnet N., Seydel A. Pullulanase: model protein substrate for the general secretory pathway of gram-negative bacteria. Folia Microbiol (Praha) 1997;42(3):184–192. doi: 10.1007/BF02818976. [DOI] [PubMed] [Google Scholar]
  74. Raetz C. R. Enzymology, genetics, and regulation of membrane phospholipid synthesis in Escherichia coli. Microbiol Rev. 1978 Sep;42(3):614–659. doi: 10.1128/mr.42.3.614-659.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Rapoport T. A., Jungnickel B., Kutay U. Protein transport across the eukaryotic endoplasmic reticulum and bacterial inner membranes. Annu Rev Biochem. 1996;65:271–303. doi: 10.1146/annurev.bi.65.070196.001415. [DOI] [PubMed] [Google Scholar]
  76. Rietveld A. G., Chupin V. V., Koorengevel M. C., Wienk H. L., Dowhan W., de Kruijff B. Regulation of lipid polymorphism is essential for the viability of phosphatidylethanolamine-deficient Escherichia coli cells. J Biol Chem. 1994 Nov 18;269(46):28670–28675. [PubMed] [Google Scholar]
  77. Rietveld A. G., Killian J. A., Dowhan W., de Kruijff B. Polymorphic regulation of membrane phospholipid composition in Escherichia coli. J Biol Chem. 1993 Jun 15;268(17):12427–12433. [PubMed] [Google Scholar]
  78. Rietveld A. G., Koorengevel M. C., de Kruijff B. Non-bilayer lipids are required for efficient protein transport across the plasma membrane of Escherichia coli. EMBO J. 1995 Nov 15;14(22):5506–5513. doi: 10.1002/j.1460-2075.1995.tb00237.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Rusiñol A. E., Hegde R. S., Chuck S. L., Lingappa V. R., Vance J. E. Translocational pausing of apolipoprotein B can be regulated by membrane lipid composition. J Lipid Res. 1998 Jun;39(6):1287–1294. [PubMed] [Google Scholar]
  80. Ryan M. T., Pfanner N. The preprotein translocase of the mitochondrial outer membrane. Biol Chem. 1998 Mar;379(3):289–294. [PubMed] [Google Scholar]
  81. Sato K., Mori H., Yoshida M., Tagaya M., Mizushima S. Short hydrophobic segments in the mature domain of ProOmpA determine its stepwise movement during translocation across the cytoplasmic membrane of Escherichia coli. J Biol Chem. 1997 Feb 28;272(9):5880–5886. doi: 10.1074/jbc.272.9.5880. [DOI] [PubMed] [Google Scholar]
  82. Schatz G., Dobberstein B. Common principles of protein translocation across membranes. Science. 1996 Mar 15;271(5255):1519–1526. doi: 10.1126/science.271.5255.1519. [DOI] [PubMed] [Google Scholar]
  83. Schatz G. The protein import system of mitochondria. J Biol Chem. 1996 Dec 13;271(50):31763–31766. doi: 10.1074/jbc.271.50.31763. [DOI] [PubMed] [Google Scholar]
  84. Schiebel E., Driessen A. J., Hartl F. U., Wickner W. Delta mu H+ and ATP function at different steps of the catalytic cycle of preprotein translocase. Cell. 1991 Mar 8;64(5):927–939. doi: 10.1016/0092-8674(91)90317-r. [DOI] [PubMed] [Google Scholar]
  85. Schuenemann D., Amin P., Hartmann E., Hoffman N. E. Chloroplast SecY is complexed to SecE and involved in the translocation of the 33-kDa but not the 23-kDa subunit of the oxygen-evolving complex. J Biol Chem. 1999 Apr 23;274(17):12177–12182. doi: 10.1074/jbc.274.17.12177. [DOI] [PubMed] [Google Scholar]
  86. Shilton B., Svergun D. I., Volkov V. V., Koch M. H., Cusack S., Economou A. Escherichia coli SecA shape and dimensions. FEBS Lett. 1998 Oct 2;436(2):277–282. doi: 10.1016/s0014-5793(98)01141-7. [DOI] [PubMed] [Google Scholar]
  87. Uchida K., Mori H., Mizushima S. Stepwise movement of preproteins in the process of translocation across the cytoplasmic membrane of Escherichia coli. J Biol Chem. 1995 Dec 29;270(52):30862–30868. doi: 10.1074/jbc.270.52.30862. [DOI] [PubMed] [Google Scholar]
  88. Ulbrandt N. D., London E., Oliver D. B. Deep penetration of a portion of Escherichia coli SecA protein into model membranes is promoted by anionic phospholipids and by partial unfolding. J Biol Chem. 1992 Jul 25;267(21):15184–15192. [PubMed] [Google Scholar]
  89. Voigt S., Jungnickel B., Hartmann E., Rapoport T. A. Signal sequence-dependent function of the TRAM protein during early phases of protein transport across the endoplasmic reticulum membrane. J Cell Biol. 1996 Jul;134(1):25–35. doi: 10.1083/jcb.134.1.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Wang Z., Jones J. D., Rizo J., Gierasch L. M. Membrane-bound conformation of a signal peptide: a transferred nuclear Overhauser effect analysis. Biochemistry. 1993 Dec 21;32(50):13991–13999. doi: 10.1021/bi00213a032. [DOI] [PubMed] [Google Scholar]
  91. Zheng N., Gierasch L. M. Signal sequences: the same yet different. Cell. 1996 Sep 20;86(6):849–852. doi: 10.1016/s0092-8674(00)80159-2. [DOI] [PubMed] [Google Scholar]
  92. Zinser E., Sperka-Gottlieb C. D., Fasch E. V., Kohlwein S. D., Paltauf F., Daum G. Phospholipid synthesis and lipid composition of subcellular membranes in the unicellular eukaryote Saccharomyces cerevisiae. J Bacteriol. 1991 Mar;173(6):2026–2034. doi: 10.1128/jb.173.6.2026-2034.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  93. de Gier J. W., Scotti P. A., Säf A., Valent Q. A., Kuhn A., Luirink J., von Heijne G. Differential use of the signal recognition particle translocase targeting pathway for inner membrane protein assembly in Escherichia coli. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14646–14651. doi: 10.1073/pnas.95.25.14646. [DOI] [PMC free article] [PubMed] [Google Scholar]
  94. de Vrije G. J., Batenburg A. M., Killian J. A., de Kruijff B. Lipid involvement in protein translocation in Escherichia coli. Mol Microbiol. 1990 Jan;4(1):143–150. doi: 10.1111/j.1365-2958.1990.tb02024.x. [DOI] [PubMed] [Google Scholar]
  95. de Vrije T., de Swart R. L., Dowhan W., Tommassen J., de Kruijff B. Phosphatidylglycerol is involved in protein translocation across Escherichia coli inner membranes. Nature. 1988 Jul 14;334(6178):173–175. doi: 10.1038/334173a0. [DOI] [PubMed] [Google Scholar]
  96. van Dalen A., Killian A., de Kruijff B. Delta psi stimulates membrane translocation of the C-terminal part of a signal sequence. J Biol Chem. 1999 Jul 9;274(28):19913–19918. doi: 10.1074/jbc.274.28.19913. [DOI] [PubMed] [Google Scholar]
  97. van Klompenburg W., Nilsson I., von Heijne G., de Kruijff B. Anionic phospholipids are determinants of membrane protein topology. EMBO J. 1997 Jul 16;16(14):4261–4266. doi: 10.1093/emboj/16.14.4261. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. van Klompenburg W., Paetzel M., de Jong J. M., Dalbey R. E., Demel R. A., von Heijne G., de Kruijff B. Phosphatidylethanolamine mediates insertion of the catalytic domain of leader peptidase in membranes. FEBS Lett. 1998 Jul 10;431(1):75–79. doi: 10.1016/s0014-5793(98)00733-9. [DOI] [PubMed] [Google Scholar]
  99. van Klompenburg W., Ridder A. N., van Raalte A. L., Killian A. J., von Heijne G., de Kruijff B. In vitro membrane integration of leader peptidase depends on the Sec machinery and anionic phospholipids and can occur post-translationally. FEBS Lett. 1997 Aug 11;413(1):109–114. doi: 10.1016/s0014-5793(97)00888-0. [DOI] [PubMed] [Google Scholar]
  100. van Voorst F., van der Does C., Brunner J., Driessen A. J., de Kruijff B. Translocase-bound SecA is largely shielded from the phospholipid acyl chains. Biochemistry. 1998 Sep 1;37(35):12261–12268. doi: 10.1021/bi9809021. [DOI] [PubMed] [Google Scholar]
  101. van der Does C., Manting E. H., Kaufmann A., Lutz M., Driessen A. J. Interaction between SecA and SecYEG in micellar solution and formation of the membrane-inserted state. Biochemistry. 1998 Jan 6;37(1):201–210. doi: 10.1021/bi972105t. [DOI] [PubMed] [Google Scholar]
  102. van der Does C., Swaving J., van Klompenburg W., Driessen A. J. Non-bilayer lipids stimulate the activity of the reconstituted bacterial protein translocase. J Biol Chem. 2000 Jan 28;275(4):2472–2478. doi: 10.1074/jbc.275.4.2472. [DOI] [PubMed] [Google Scholar]
  103. van der Does C., den Blaauwen T., de Wit J. G., Manting E. H., Groot N. A., Fekkes P., Driessen A. J. SecA is an intrinsic subunit of the Escherichia coli preprotein translocase and exposes its carboxyl terminus to the periplasm. Mol Microbiol. 1996 Nov;22(4):619–629. doi: 10.1046/j.1365-2958.1996.d01-1712.x. [DOI] [PubMed] [Google Scholar]
  104. van der Wolk J. P., de Wit J. G., Driessen A. J. The catalytic cycle of the escherichia coli SecA ATPase comprises two distinct preprotein translocation events. EMBO J. 1997 Dec 15;16(24):7297–7304. doi: 10.1093/emboj/16.24.7297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  105. van't Hof R., van Klompenburg W., Pilon M., Kozubek A., de Korte-Kool G., Demel R. A., Weisbeek P. J., de Kruijff B. The transit sequence mediates the specific interaction of the precursor of ferredoxin with chloroplast envelope membrane lipids. J Biol Chem. 1993 Feb 25;268(6):4037–4042. [PubMed] [Google Scholar]
  106. von Heijne G. Control of topology and mode of assembly of a polytopic membrane protein by positively charged residues. Nature. 1989 Oct 5;341(6241):456–458. doi: 10.1038/341456a0. [DOI] [PubMed] [Google Scholar]
  107. von Heijne G., Gavel Y. Topogenic signals in integral membrane proteins. Eur J Biochem. 1988 Jul 1;174(4):671–678. doi: 10.1111/j.1432-1033.1988.tb14150.x. [DOI] [PubMed] [Google Scholar]
  108. von Heijne G. Signal sequences. The limits of variation. J Mol Biol. 1985 Jul 5;184(1):99–105. doi: 10.1016/0022-2836(85)90046-4. [DOI] [PubMed] [Google Scholar]

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