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PMID: 9184221 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Distinct catalytic roles of the SecYE, SecG and SecDFyajC subunits of preprotein translocase holoenzyme.

The EMBO journal ·Vol. 16 ·No. 10 ·1997-05-15 ·Pages 2756-68

Duong F, Wickner W

Abstract

Escherichia coli preprotein translocase contains a membrane-embedded trimeric complex of SecY, SecE and SecG (SecYEG) and the peripheral SecA protein. SecYE is the conserved functional 'core' of the SecYEG complex. Although sufficient to provide sites for high-affinity binding and membrane insertion of SecA, and for its activation as a preprotein-dependent ATPase, SecYE has only very low capacity to support translocation. The proteins encoded by the secD operon--SecD, SecF and YajC--also form an integral membrane heterotrimeric complex (SecDFyajC). Physical and functional studies show that these two trimeric complexes are associated to form SecYEGDFyajC, the hexameric integral membrane domain of the preprotein translocase 'holoenzyme'. Either SecG or SecDFyajC can support the translocation activity of SecYE by facilitating the ATP-driven cycle of SecA membrane insertion and de-insertion at different stages of the translocation reaction. Our findings show that each of the prokaryote-specific subunits (SecA, SecG and SecDFyajC) function together to promote preprotein movement at the SecYE core of the translocase.

MeSH Terms
Adenosine Triphosphatases/genetics,metabolism Adenosine Triphosphate/metabolism Bacterial Proteins/genetics,metabolism Biological Transport Coenzymes/genetics,metabolism Escherichia coli/enzymology,genetics,metabolism Escherichia coli Proteins Hydrolysis Macromolecular Substances Membrane Proteins Membrane Transport Proteins Precipitin Tests Protein Binding Protein Precursors/metabolism SEC Translocation Channels SecA Proteins
Chemicals
Bacterial Proteins Coenzymes Escherichia coli Proteins Macromolecular Substances Membrane Proteins Membrane Transport Proteins Protein Precursors SEC Translocation Channels SecD protein, E coli SecE protein, E coli SecF protein, E coli SecG protein, E coli SecY protein, E coli secD protein, Bacteria secF protein, Bacteria Adenosine Triphosphate Adenosine Triphosphatases SecA Proteins
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Duong F
Dartmouth Medical School, Department of Biochemistry, Hanover, NH 03755, USA.
Wickner W
References (45)
45 references, click to expand
  1. Ligand: a versatile computerized approach for characterization of ligand-binding systems.
    Anal Biochem. 1980 Sep 1;107(1):220-39 PMID: 6254391
  2. The major pathways of protein translocation across membranes.
    Genes Cells. 1996 Apr;1(4):337-46 PMID: 9135078
  3. ProOmpA spontaneously folds in a membrane assembly competent state which trigger factor stabilizes.
    EMBO J. 1988 Jun;7(6):1831-5 PMID: 3049077
  4. Purified secB protein of Escherichia coli retards folding and promotes membrane translocation of the maltose-binding protein in vitro.
    Proc Natl Acad Sci U S A. 1988 Dec;85(23):8978-82 PMID: 2848249
  5. SecA protein, a peripheral protein of the Escherichia coli plasma membrane, is essential for the functional binding and translocation of proOmpA.
    EMBO J. 1989 Mar;8(3):955-9 PMID: 2542028
  6. SecA protein hydrolyzes ATP and is an essential component of the protein translocation ATPase of Escherichia coli.
    EMBO J. 1989 Mar;8(3):961-6 PMID: 2542029
  7. The purified E. coli integral membrane protein SecY/E is sufficient for reconstitution of SecA-dependent precursor protein translocation.
    Cell. 1990 Aug 24;62(4):649-57 PMID: 2167176
  8. The sec and prl genes of Escherichia coli.
    J Bioenerg Biomembr. 1990 Jun;22(3):291-310 PMID: 2202721
  9. 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):269-79 PMID: 2170023
  10. The secD locus of E.coli codes for two membrane proteins required for protein export.
    EMBO J. 1990 Oct;9(10):3209-16 PMID: 2170107
  11. Delta mu H+ and ATP function at different steps of the catalytic cycle of preprotein translocase.
    Cell. 1991 Mar 8;64(5):927-39 PMID: 1825804
  12. Reconstitution of a protein translocation system containing purified SecY, SecE, and SecA from Escherichia coli.
    Proc Natl Acad Sci U S A. 1991 Aug 1;88(15):6545-9 PMID: 1830665
  13. SecY, SecE, and band 1 form the membrane-embedded domain of Escherichia coli preprotein translocase.
    J Biol Chem. 1992 Feb 25;267(6):4166-70 PMID: 1531482
  14. Sec61p and BiP directly facilitate polypeptide translocation into the ER.
    Cell. 1992 Apr 17;69(2):353-65 PMID: 1568250
  15. Overproduction, purification and characterization of SecD and SecF, integral membrane components of the protein translocation machinery of Escherichia coli.
    Biochim Biophys Acta. 1992 Jul 13;1122(1):77-84 PMID: 1633199
  16. Suppressor analysis suggests a multistep, cyclic mechanism for protein secretion in Escherichia coli.
    EMBO J. 1992 Sep;11(9):3165-74 PMID: 1387081
  17. SecD is involved in the release of translocated secretory proteins from the cytoplasmic membrane of Escherichia coli.
    EMBO J. 1993 Jan;12(1):265-70 PMID: 8428584
  18. Purified Escherichia coli preprotein translocase catalyzes multiple cycles of precursor protein translocation.
    Biochemistry. 1993 Mar 16;32(10):2626-30 PMID: 8448119
  19. The Cs sec mutants of Escherichia coli reflect the cold sensitivity of protein export itself.
    Genetics. 1993 Apr;133(4):763-73 PMID: 8462840
  20. A tetrameric complex of membrane proteins in the endoplasmic reticulum.
    Eur J Biochem. 1993 Jun 1;214(2):375-81 PMID: 7916687
  21. Genetic and molecular characterization of the Escherichia coli secD operon and its products.
    J Bacteriol. 1994 Feb;176(3):804-14 PMID: 7507921
  22. SecD and SecF facilitate protein export in Escherichia coli.
    EMBO J. 1994 Feb 1;13(3):554-61 PMID: 8313900
  23. Evolutionary conservation of components of the protein translocation complex.
    Nature. 1994 Feb 17;367(6464):654-7 PMID: 8107851
  24. SecD and SecF are required for the proton electrochemical gradient stimulation of preprotein translocation.
    EMBO J. 1994 Feb 15;13(4):954-63 PMID: 8112309
  25. Genetic analysis of SecY: additional export-defective mutations and factors affecting their phenotypes.
    Mol Gen Genet. 1994 May 10;243(3):261-9 PMID: 8190079
  26. Subunit dynamics in Escherichia coli preprotein translocase.
    Proc Natl Acad Sci U S A. 1994 May 24;91(11):4703-7 PMID: 8197122
  27. SecF stabilizes SecD and SecY, components of the protein translocation machinery of the Escherichia coli cytoplasmic membrane.
    J Bacteriol. 1994 Jul;176(13):4111-6 PMID: 8021192
  28. Disruption of the gene encoding p12 (SecG) reveals the direct involvement and important function of SecG in the protein translocation of Escherichia coli at low temperature.
    EMBO J. 1994 Jul 15;13(14):3272-7 PMID: 8045257
  29. Sec72p contributes to the selective recognition of signal peptides by the secretory polypeptide translocation complex.
    J Cell Biol. 1994 Aug;126(4):935-43 PMID: 8051213
  30. SecA promotes preprotein translocation by undergoing ATP-driven cycles of membrane insertion and deinsertion.
    Cell. 1994 Sep 9;78(5):835-43 PMID: 8087850
  31. SecA protein is exposed to the periplasmic surface of the E. coli inner membrane in its active state.
    Cell. 1994 Sep 9;78(5):845-53 PMID: 8087851
  32. Reconstitution of an efficient protein translocation machinery comprising SecA and the three membrane proteins, SecY, SecE, and SecG (p12).
    J Biol Chem. 1994 Sep 23;269(38):23625-31 PMID: 8089132
  33. A double counter-selection system for the study of null alleles of essential genes in Escherichia coli.
    Gene. 1995 Mar 21;155(1):1-7 PMID: 7698651
  34. High selectivity with low specificity: how SecB has solved the paradox of chaperone binding.
    Trends Biochem Sci. 1995 Feb;20(2):65-9 PMID: 7701564
  35. Posttranslational protein transport in yeast reconstituted with a purified complex of Sec proteins and Kar2p.
    Cell. 1995 May 19;81(4):561-70 PMID: 7758110
  36. The MIM complex mediates preprotein translocation across the mitochondrial inner membrane and couples it to the mt-Hsp70/ATP driving system.
    Cell. 1995 Jun 30;81(7):1085-93 PMID: 7600576
  37. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
    J Bacteriol. 1995 Jul;177(14):4121-30 PMID: 7608087
  38. SecYEG and SecA are the stoichiometric components of preprotein translocase.
    J Biol Chem. 1995 Aug 25;270(34):20106-11 PMID: 7650029
  39. A new genetic selection identifies essential residues in SecG, a component of the Escherichia coli protein export machinery.
    EMBO J. 1995 Sep 15;14(18):4412-21 PMID: 7556084
  40. 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):1171-81 PMID: 8548804
  41. Inversion of the membrane topology of SecG coupled with SecA-dependent preprotein translocation.
    Cell. 1996 Apr 5;85(1):71-81 PMID: 8620539
  42. SecG plays a critical role in protein translocation in the absence of the proton motive force as well as at low temperature.
    FEBS Lett. 1996 Feb 26;381(1-2):25-8 PMID: 8641431
  43. In vivo analyses of interactions between SecE and SecY, core components of the Escherichia coli protein translocation machinery.
    J Biol Chem. 1996 Aug 16;271(33):19908-14 PMID: 8702704
  44. Separable ATPase and membrane insertion domains of the SecA subunit of preprotein translocase.
    J Biol Chem. 1996 Dec 6;271(49):31580-4 PMID: 8940175
  45. Regulation of a membrane component required for protein secretion in Escherichia coli.
    Cell. 1982 Aug;30(1):311-9 PMID: 6751561
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1997-05-15
Pages
2756-68
Language
English
Region
England
NLM ID
8208664
PMCID
PMC1169885
Subset
IM
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