Escherichia coli membranes depleted of secyeg elicit seca-dependent ion-channel activity but lose signal peptide specificity

Journal of Membrane Biology

Volumn 245, Issue 11, 2012, Pages 747-757

  Lin, Bor Ruei ^a   Hsieh, Ying Hsin ^a   Jiang, Chun ^a   Tai, Phang C ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Biochemistry Molec. Biology; Electrophysiology; Ion channel; Mechanism of transport protein

Indexed keywords

ION CHANNEL; LIPOSOME; PROTEIN; PROTEIN SECA; PROTEIN SECYEG COMPLEX; PROTEOLIPOSOME; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; ESCHERICHIA COLI; ION CURRENT; MEMBRANE ELECTROPHYSIOLOGY; MEMBRANE VESICLE; NONHUMAN; OOCYTE;

ADENOSINE TRIPHOSPHATASES; ANIMALS; BACTERIAL PROTEINS; CATIONS, MONOVALENT; CELL MEMBRANE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; ION CHANNELS; ION TRANSPORT; MEMBRANE TRANSPORT PROTEINS; OOCYTES; PROTEIN SORTING SIGNALS;

ESCHERICHIA COLI;

EID: 84871310049     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-012-9477-8     Document Type: Article

References (44)

1. Bostina M, Mohsin B, Kuhlbrandt W, Collinson I (2005) Atomic model of the E. coli membrane-bound protein translocation complex SecYEG. J Mol Biol 352:1035-1043
2. Cabelli RJ, Chen L, Tai PC, Oliver DB (1988) SecA protein is required for secretory protein translocation into E. coli membrane vesicles. Cell 55:683-692
3. Chen L, Tai PC, Briggs MS, Gierasch LM (1987) Protein translocation into Escherichia coli membrane vesicles is inhibited by functional synthetic signal peptides. J Biol Chem 262:1427- 1429
4. Chen X, Xu H, Tai PC (1996) A significant fraction of functional SecA is permanently embedded in the membrane. SecA cycling on and off the membrane is not essential during protein translocation. J Biol Chem 271:29698-29706
5. Chen Y, Tai PC, Sui SF (2007) The active ring-like structure of SecA revealed by electron crystallography: conformational change upon interaction with SecB. J Struct Biol 159:149-153
6. Dalal K, Duong F (2009) The SecY complex forms a channel capable of ionic discrimination. EMBO Rep 10:762-768
7. Dalal K, Bao H, Duong F (2010) Modulation of the SecY channel permeability by pore mutations and trivalent cations. Channels (Austin) 4:83-86
8. 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
9. Fandl JP, Tai PC (1987) Biochemical evidence for the secY24 defect in Escherichia coli protein translocation and its suppression by soluble cytoplasmic factors. Proc Natl Acad Sci USA 84:7448- 7452
10. Fandl JP, Cabelli R, Oliver D, Tai PC (1988) SecA suppresses the temperature-sensitive SecY24 defect in protein translocation in Escherichia coli membrane vesicles. Proc Natl Acad Sci USA 85:8953-8957
11. Hsieh Y-h, Zhang H, Lin B-r, Cui N, Na B, Yang H, Jiang C, Sui S-f, Tai PC (2011) SecA alone can promote protein translocation and ion channel activity. J Biol Chem 286:44702-44709
12. Jilaveanu LB, Oliver D (2006) SecA dimer cross-linked at its subunit interface is functional for protein translocation. J Bacteriol 188: 335-338
13. Jilaveanu LB, Oliver DB (2007) In vivo membrane topology of Escherichia coli SecA ATPase reveals extensive periplasmic exposure of multiple functionally important domains clustering on one face of SecA. J Biol Chem 282:4661-4668
14. Jilaveanu LB, Zito CR, Oliver D (2005) Dimeric SecA is essential for protein translocation. Proc Natl Acad Sci USA 102:7511-7516
15. Junne T, Schwede T, Goder V, Spiess M (2006) The plug domain of yeast Sec61p is important for efficient protein translocation, but is not essential for cell viability. Mol Biol Cell 17:4063-4068
16. Kim YJ, Rajapandi T, Oliver D (1994) SecA protein is exposed to the periplasmic surface of the E. coli inner membrane in its active state. Cell 78:845-853
17. Kusters R, Huijbregts R, de Kruijff B (1992) Elevated cytosolic concentrations of SecA compensate for a protein translocation defect in Escherichia coli cells with reduced levels of negatively charged phospholipids. FEBS Lett 308:97-100
18. Li W, Schulman S, Boyd D, Erlandson K, Beckwith J, Rapoport TA (2007) The plug domain of the SecY protein stabilizes the closed state of the translocation channel and maintains a membrane seal. Mol Cell 26:511-521
19. Lin BR, Gierasch LM, Jiang C, Tai PC (2006) Electrophysiological studies in Xenopus oocytes for the opening of Escherichia coli SecA-dependent protein-conducting channels. J Membr Biol 214:103-113
20. Maillard AP, Lalani S, Silva F, Belin D, Duong F (2007) Deregulation of the SecYEG translocation channel upon removal of the plug domain. J Biol Chem 282:1281-1287
21. Manting EH, Driessen AJ (2000) Escherichia coli translocase: the unravelling of a molecular machine. Mol Microbiol 37:226- 238
22. + channels by protein kinase C. Proc Natl Acad Sci USA 101:1087-1092
23. Mori H, Ito K (2001) An essential amino acid residue in the protein translocation channel revealed by targeted random mutagenesis of SecY. Proc Natl Acad Sci USA 98:5128-5133
24. Nicchitta CV, Blobel G (1990) Assembly of translocation-competent proteoliposomes from detergent-solubilized rough microsomes. Cell 60:259-269
25. Oliver DB, Beckwith J (1982a) Identification of a new gene (secA) and gene product involved in the secretion of envelope proteins in Escherichia coli. J Bacteriol 150:686-691
26. Oliver DB, Beckwith J (1982b) Regulation of a membrane component required for protein secretion in Escherichia coli. Cell 30: 311-319
27. Osborne RS, Silhavy TJ (1993) PrlA suppressor mutations cluster in regions corresponding to three distinct topological domains. EMBO J 12:3391-3398
28. Park E, Rapoport TA (2011) Preserving the membrane barrier for small molecules during bacterial protein translocation. Nature 473:239-242
29. Ruiz N, Silhavy TJ (2005) Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr Opin Microbiol 8:122-126
30. Saparov SM, Erlandson K, Cannon K, Schaletzky J, Schulman S, Rapoport TA, Pohl P (2007) Determining the conductance of the SecY protein translocation channel for small molecules. Mol Cell 26:501-509
31. Schiebel E, Wickner W (1992) Preprotein translocation creates a halide anion permeability in the Escherichia coli plasma membrane. J Biol Chem 267:7505-7510
32. Silhavy TJ, Beckwith J (1983) Isolation and characterization of mutants of Escherichia coli K12 affected in protein localization. Methods Enzymol 97:11-40
33. Tai PC, Tian G, Xu H, Lian JP, Yu JN (1991) In vitro protein translocation into Escherichia coli inverted membrane vesicles. Methods Cell Biol 34:167-187
34. Tam PC, Maillard AP, Chan KK, Duong F (2005) Investigating the SecY plug movement at the SecYEG translocation channel. EMBO J 24:3380-3388
35. Van den Berg B, Clemons WM Jr, Collinson I, Modis Y, Hartmann E, Harrison SC, Rapoport TA (2004) X-ray structure of a proteinconducting channel. Nature 427:36-44
36. Veenendaal AK, van der Does C, Driessen AJ (2004) The proteinconducting channel SecYEG. Biochim Biophys Acta 1694: 81-95
37. Wang HW, Chen Y, Yang H, Chen X, Duan MX, Tai PC, Sui SF (2003) Ring-like pore structures of SecA: implication for bacterial protein-conducting channels. Proc Natl Acad Sci USA 100:4221-4226
38. Wang H, Na B, Yang H, Tai PC (2008) Additional in vitro and in vivo evidence for SecA functioning as dimers in the membrane: dissociation into monomers is not essential for protein translocation in Escherichia coli. J Bacteriol 190:1413-1418
39. Watanabe M, Nicchitta CV, Blobel G (1990) Reconstitution of protein translocation from detergent-solubilized Escherichia coli inverted vesicles: PrlA protein-deficient vesicles efficiently translocate precursor proteins. Proc Natl Acad Sci USA 87: 1960-1964
40. Xu H, Cui N, Yang Z, Wu J, Giwa LR, Abdulkadir L, Sharma P, Jiang C (2001) Direct activation of cloned KATP channels by intracellular acidosis. J Biol Chem 276:12898-12902
41. Yang YB, Lian J, Tai PC (1997a) Differential translocation of protein precursors across SecY-deficient membranes of Escherichia coli: SecY is not obligatorily required for translocation of certain secretory proteins in vitro. J Bacteriol 179:7386-7393
42. Yang YB, Yu N, Tai PC (1997b) SecE-depleted membranes of Escherichia coli are active. SecE is not obligatorily required for the in vitro translocation of certain protein precursors. J Biol Chem 272:13660-13665
43. Yi L, Jiang F, Chen M, Cain B, Bolhuis A, Dalbey RE (2003) YidC is strictly required for membrane insertion of subunits a and c of the F1F0ATP synthase and SecE of the SecYEG translocase. Biochemistry 42:10537-10544
44. Zhong X, Kolter R, Tai PC (1996) Processing of colicin V-1, a secretable marker protein of a bacterial ATP binding cassette export system, requires membrane integrity, energy, and cytosolic factors. J Biol Chem 271:28057-28063