Published online 19 April 2004. doi:10.1083/jcb.200402100
The Rockefeller University Press, 0021-9525 $8.00
JCB, Volume 165, Number 2, 213-222
F1F0 ATP synthase subunit c is a substrate of the novel YidC pathway for membrane protein biogenesis
Martin van der Laan,
Philipp Bechtluft,
Stef Kol,
Nico Nouwen, and
Arnold J.M. Driessen
Department of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, 9751 NN Haren, Netherlands
Address correspondence to Arnold J.M. Driessen, Dept. of Microbiology, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Kerklaan 30, 9751 NN Haren, Netherlands. Tel.: 31-50-3632164. Fax: 31-50-3632154. email: a.j.m.driessen{at}biol.rug.nl
The Escherichia coli YidC protein belongs to the Oxa1 family of membrane proteins that have been suggested to facilitate the insertion and assembly of membrane proteins either in cooperation with the Sec translocase or as a separate entity. Recently, we have shown that depletion of YidC causes a specific defect in the functional assembly of F1F0 ATP synthase and cytochrome o oxidase. We now demonstrate that the insertion of in vitrosynthesized F1F0 ATP synthase subunit c (F0c) into inner membrane vesicles requires YidC. Insertion is independent of the proton motive force, and proteoliposomes containing only YidC catalyze the membrane insertion of F0c in its native transmembrane topology whereupon it assembles into large oligomers. Co-reconstituted SecYEG has no significant effect on the insertion efficiency. Remarkably, signal recognition particle and its membrane-bound receptor FtsY are not required for the membrane insertion of F0c. In conclusion, a novel membrane protein insertion pathway in E. coli is described in which YidC plays an exclusive role.
Key Words: YidC; F1F0 ATP synthase; membrane insertion; membrane targeting; complex assembly
Abbreviations used in this paper: AMdiS, 4-acetamido-4'-maleimidylstilbene-2,2'-disulfonic acid; F0a, F0 subunit a; F0c, F0 subunit c; IMV, inner membrane vesicle; PMF, proton motive force; SRP, signal recognition particle.

CiteULike
Complore
Connotea
Del.icio.us
Digg
Facebook
Reddit
Technorati
Twitter What's this?
This article has been cited by other articles:
-
Saller, M. J., Fusetti, F., Driessen, A. J. M.
(2009). Bacillus subtilis SpoIIIJ and YqjG Function in Membrane Protein Biogenesis. J. Bacteriol.
191: 6749-6757
[Abstract]
[Full Text]
-
Funes, S., Hasona, A., Bauerschmitt, H., Grubbauer, C., Kauff, F., Collins, R., Crowley, P. J., Palmer, S. R., Brady, L. J., Herrmann, J. M.
(2009). Independent gene duplications of the YidC/Oxa/Alb3 family enabled a specialized cotranslational function. Proc. Natl. Acad. Sci. USA
106: 6656-6661
[Abstract]
[Full Text]
-
Ballhausen, B., Altendorf, K., Deckers-Hebestreit, G.
(2009). Constant c10 Ring Stoichiometry in the Escherichia coli ATP Synthase Analyzed by Cross-Linking. J. Bacteriol.
191: 2400-2404
[Abstract]
[Full Text]
-
Yu, Z., Koningstein, G., Pop, A., Luirink, J.
(2008). The Conserved Third Transmembrane Segment of YidC Contacts Nascent Escherichia coli Inner Membrane Proteins. J. Biol. Chem.
283: 34635-34642
[Abstract]
[Full Text]
-
Kol, S., Nouwen, N., Driessen, A. J. M.
(2008). Mechanisms of YidC-mediated Insertion and Assembly of Multimeric Membrane Protein Complexes. J. Biol. Chem.
283: 31269-31273
[Abstract]
[Full Text]
-
Price, C. E., Driessen, A. J. M.
(2008). YidC Is Involved in the Biogenesis of Anaerobic Respiratory Complexes in the Inner Membrane of Escherichia coli. J. Biol. Chem.
283: 26921-26927
[Abstract]
[Full Text]
-
Kawashima, Y., Miyazaki, E., Muller, M., Tokuda, H., Nishiyama, K.-i.
(2008). Diacylglycerol Specifically Blocks Spontaneous Integration of Membrane Proteins and Allows Detection of a Factor-assisted Integration. J. Biol. Chem.
283: 24489-24496
[Abstract]
[Full Text]
-
Baars, L., Wagner, S., Wickstrom, D., Klepsch, M., Ytterberg, A. J., van Wijk, K. J., de Gier, J.-W.
(2008). Effects of SecE Depletion on the Inner and Outer Membrane Proteomes of Escherichia coli. J. Bacteriol.
190: 3505-3525
[Abstract]
[Full Text]
-
Kol, S., Nouwen, N., Driessen, A. J. M.
(2008). The Charge Distribution in the Cytoplasmic Loop of Subunit C of the F1F0 ATPase Is a Determinant for YidC Targeting. J. Biol. Chem.
283: 9871-9877
[Abstract]
[Full Text]
-
Ravaud, S., Stjepanovic, G., Wild, K., Sinning, I.
(2008). The Crystal Structure of the Periplasmic Domain of the Escherichia coli Membrane Protein Insertase YidC Contains a Substrate Binding Cleft. J. Biol. Chem.
283: 9350-9358
[Abstract]
[Full Text]
-
Dong, Y., Palmer, S. R., Hasona, A., Nagamori, S., Kaback, H. R., Dalbey, R. E., Brady, L. J.
(2008). Functional Overlap but Lack of Complete Cross-Complementation of Streptococcus mutans and Escherichia coli YidC Orthologs. J. Bacteriol.
190: 2458-2469
[Abstract]
[Full Text]
-
Oliver, D. C., Paetzel, M.
(2008). Crystal Structure of the Major Periplasmic Domain of the Bacterial Membrane Protein Assembly Facilitator YidC. J. Biol. Chem.
283: 5208-5216
[Abstract]
[Full Text]
-
Suzuki, T., Ozaki, Y., Sone, N., Feniouk, B. A., Yoshida, M.
(2007). The product of uncI gene in F1Fo-ATP synthase operon plays a chaperone-like role to assist c-ring assembly. Proc. Natl. Acad. Sci. USA
104: 20776-20781
[Abstract]
[Full Text]
-
Yuan, J., Phillips, G. J., Dalbey, R. E.
(2007). Isolation of Cold-Sensitive yidC Mutants Provides Insights into the Substrate Profile of the YidC Insertase and the Importance of Transmembrane 3 in YidC Function. J. Bacteriol.
189: 8961-8972
[Abstract]
[Full Text]
-
Pogoryelov, D., Reichen, C., Klyszejko, A. L., Brunisholz, R., Muller, D. J., Dimroth, P., Meier, T.
(2007). The Oligomeric State of c Rings from Cyanobacterial F-ATP Synthases Varies from 13 to 15. J. Bacteriol.
189: 5895-5902
[Abstract]
[Full Text]
-
Jia, L., Dienhart, M. K., Stuart, R. A.
(2007). Oxa1 Directly Interacts with Atp9 and Mediates Its Assembly into the Mitochondrial F1Fo-ATP Synthase Complex. Mol. Biol. Cell
18: 1897-1908
[Abstract]
[Full Text]
-
Nishiyama, K.-i., Ikegami, A., Moser, M., Schiltz, E., Tokuda, H., Muller, M.
(2006). A Derivative of Lipid A Is Involved in Signal Recognition Particle/SecYEG-dependent and -independent Membrane Integrations. J. Biol. Chem.
281: 35667-35676
[Abstract]
[Full Text]
-
Kol, S., Turrell, B. R., de Keyzer, J., van der Laan, M., Nouwen, N., Driessen, A. J. M.
(2006). YidC-mediated Membrane Insertion of Assembly Mutants of Subunit c of the F1F0 ATPase. J. Biol. Chem.
281: 29762-29768
[Abstract]
[Full Text]
-
du Plessis, D. J. F., Nouwen, N., Driessen, A. J. M.
(2006). Subunit a of Cytochrome o Oxidase Requires Both YidC and SecYEG for Membrane Insertion. J. Biol. Chem.
281: 12248-12252
[Abstract]
[Full Text]
-
van Bloois, E., Haan, G.-J., de Gier, J.-W., Oudega, B., Luirink, J.
(2006). Distinct Requirements for Translocation of the N-tail and C-tail of the Escherichia coli Inner Membrane Protein CyoA. J. Biol. Chem.
281: 10002-10009
[Abstract]
[Full Text]
-
Karamyshev, A. L., Johnson, A. E.
(2005). Selective SecA Association with Signal Sequences in Ribosome-bound Nascent Chains: A POTENTIAL ROLE FOR SecA IN RIBOSOME TARGETING TO THE BACTERIAL MEMBRANE. J. Biol. Chem.
280: 37930-37940
[Abstract]
[Full Text]
-
van Bloois, E., Nagamori, S., Koningstein, G., Ullers, R. S., Preuss, M., Oudega, B., Harms, N., Kaback, H. R., Herrmann, J. M., Luirink, J.
(2005). The Sec-independent Function of Escherichia coli YidC Is Evolutionary-conserved and Essential. J. Biol. Chem.
280: 12996-13003
[Abstract]
[Full Text]
-
Preuss, M., Ott, M., Funes, S., Luirink, J., Herrmann, J. M.
(2005). Evolution of Mitochondrial Oxa Proteins from Bacterial YidC: INHERITED AND ACQUIRED FUNCTIONS OF A CONSERVED PROTEIN INSERTION MACHINERY. J. Biol. Chem.
280: 13004-13011
[Abstract]
[Full Text]
-
Lemaire, C., Guibet-Grandmougin, F., Angles, D., Dujardin, G., Bonnefoy, N.
(2004). A Yeast Mitochondrial Membrane Methyltransferase-like Protein Can Compensate for oxa1 Mutations. J. Biol. Chem.
279: 47464-47472
[Abstract]
[Full Text]
-
Yi, L., Celebi, N., Chen, M., Dalbey, R. E.
(2004). Sec/SRP Requirements and Energetics of Membrane Insertion of Subunits a, b, and c of the Escherichia coli F1F0 ATP Synthase. J. Biol. Chem.
279: 39260-39267
[Abstract]
[Full Text]
-
Dalbey, R. E., Kuhn, A.
(2004). YidC family members are involved in the membrane insertion, lateral integration, folding, and assembly of membrane proteins. JCB
166: 769-774
[Abstract]
[Full Text]