Previous Article | Next Article 
Journal of Bacteriology, November 2001, p. 6538-6542, Vol. 183, No. 22
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.22.6538-6542.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Deletion of lolB, Encoding an Outer
Membrane Lipoprotein, Is Lethal for Escherichia
coli and Causes Accumulation of Lipoprotein Localization
Intermediates in the Periplasm
Kimie
Tanaka,
Shin-Ichi
Matsuyama, and
Hajime
Tokuda*
Institute of Molecular and Cellular
Biosciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo
113-0032, Japan
Received 2 July 2001/Accepted 30 August 2001
Outer membrane lipoproteins of Escherichia coli are
released from the inner membrane upon the formation of a complex with a
periplasmic chaperone, LolA, followed by localization to the outer
membrane. In vitro biochemical analyses revealed that the localization
of lipoproteins to the outer membrane generally requires an outer
membrane lipoprotein, LolB, and occurs via transient formation of a
LolB-lipoprotein complex. On the other hand, a mutant carrying the
chromosomal lolB gene under the control of the
lac promoter-operator grew normally in the absence of
LolB induction if the mutant did not possess the major outer membrane lipoprotein Lpp, suggesting that LolB is only important for the localization of Lpp in vivo. To examine the in vivo function of LolB,
we constructed a chromosomal lolB null mutant harboring a temperature-sensitive helper plasmid carrying the lolB
gene. At a nonpermissive temperature, depletion of the LolB protein due
to loss of the lolB gene caused cessation of growth and
a decrease in the number of viable cells irrespective of the presence or absence of Lpp. LolB-depleted cells accumulated the LolA-lipoprotein complex in the periplasm and the mature form of lipoproteins in the
inner membrane. Taken together, these results indicate that LolB is the
first example of an essential lipoprotein for E. coli and that its depletion inhibits the upstream reactions of lipoprotein trafficking.
*
Corresponding author. Mailing address: Institute of
Molecular and Cellular Biosciences, University of Tokyo, 1-1-1 Yayoi, Bunkyo-ku, Tokyo 113-0032, Japan. Phone: 81-3-5841-7830. Fax: 81-3-5841-8464. E-mail: htokuda{at}iam.u-tokyo.ac.jp.
Journal of Bacteriology, November 2001, p. 6538-6542, Vol. 183, No. 22
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.22.6538-6542.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Nakada, S., Sakakura, M., Takahashi, H., Okuda, S., Tokuda, H., Shimada, I.
(2009). Structural Investigation of the Interaction between LolA and LolB Using NMR. J. Biol. Chem.
284: 24634-24643
[Abstract]
[Full Text]
-
Watanabe, S., Oguchi, Y., Takeda, K., Miki, K., Tokuda, H.
(2008). Introduction of a Lethal Redox Switch That Controls the Opening and Closing of the Hydrophobic Cavity in LolA. J. Biol. Chem.
283: 25421-25427
[Abstract]
[Full Text]
-
Ruiz, N., Gronenberg, L. S., Kahne, D., Silhavy, T. J.
(2008). Identification of two inner-membrane proteins required for the transport of lipopolysaccharide to the outer membrane of Escherichia coli. Proc. Natl. Acad. Sci. USA
105: 5537-5542
[Abstract]
[Full Text]
-
Lewenza, S., Vidal-Ingigliardi, D., Pugsley, A. P.
(2006). Direct visualization of red fluorescent lipoproteins indicates conservation of the membrane sorting rules in the family enterobacteriaceae.. J. Bacteriol.
188: 3516-3524
[Abstract]
[Full Text]
-
Babu, M. M., Priya, M. L., Selvan, A. T., Madera, M., Gough, J., Aravind, L., Sankaran, K.
(2006). A Database of Bacterial Lipoproteins (DOLOP) with Functional Assignments to Predicted Lipoproteins.. J. Bacteriol.
188: 2761-2773
[Abstract]
[Full Text]
-
Ito, Y., Matsuzawa, H., Matsuyama, S.-i., Narita, S.-i., Tokuda, H.
(2006). Genetic Analysis of the Mode of Interplay between an ATPase Subunit and Membrane Subunits of the Lipoprotein-Releasing ATP-Binding Cassette Transporter LolCDE.. J. Bacteriol.
188: 2856-2864
[Abstract]
[Full Text]
-
Taniguchi, N., Matsuyama, S.-i., Tokuda, H.
(2005). Mechanisms Underlying Energy-independent Transfer of Lipoproteins from LolA to LolB, Which Have Similar Unclosed {beta}-Barrel Structures. J. Biol. Chem.
280: 34481-34488
[Abstract]
[Full Text]
-
Onufryk, C., Crouch, M.-L., Fang, F. C., Gross, C. A.
(2005). Characterization of Six Lipoproteins in the {sigma}E Regulon. J. Bacteriol.
187: 4552-4561
[Abstract]
[Full Text]
-
Robichon, C., Vidal-Ingigliardi, D., Pugsley, A. P.
(2005). Depletion of Apolipoprotein N-Acyltransferase Causes Mislocalization of Outer Membrane Lipoproteins in Escherichia coli. J. Biol. Chem.
280: 974-983
[Abstract]
[Full Text]
-
Kamalakkannan, S., Murugan, V., Jagannadham, M.V., Nagaraj, R., Sankaran, K.
(2004). Bacterial lipid modification of proteins for novel protein engineering applications. Protein Eng Des Sel
17: 721-729
[Abstract]
[Full Text]
-
Miyadai, H., Tanaka-Masuda, K., Matsuyama, S.-i., Tokuda, H.
(2004). Effects of Lipoprotein Overproduction on the Induction of DegP (HtrA) Involved in Quality Control in the Escherichia coli Periplasm. J. Biol. Chem.
279: 39807-39813
[Abstract]
[Full Text]
-
Hara, T., Matsuyama, S.-i., Tokuda, H.
(2003). Mechanism Underlying the Inner Membrane Retention of Escherichia coli Lipoproteins Caused by Lol Avoidance Signals. J. Biol. Chem.
278: 40408-40414
[Abstract]
[Full Text]
-
Fukuda, A., Matsuyama, S.-i., Hara, T., Nakayama, J., Nagasawa, H., Tokuda, H.
(2002). Aminoacylation of the N-terminal Cysteine Is Essential for Lol-dependent Release of Lipoproteins from Membranes but Does Not Depend on Lipoprotein Sorting Signals. J. Biol. Chem.
277: 43512-43518
[Abstract]
[Full Text]
-
Suzuki, M., Hara, H., Matsumoto, K.
(2002). Envelope Disorder of Escherichia coli Cells Lacking Phosphatidylglycerol. J. Bacteriol.
184: 5418-5425
[Abstract]
[Full Text]
-
Masuda, K., Matsuyama, S.-i., Tokuda, H.
(2002). Elucidation of the function of lipoprotein-sorting signals that determine membrane localization. Proc. Natl. Acad. Sci. USA
99: 7390-7395
[Abstract]
[Full Text]
-
Higgs, P. I., Letain, T. E., Merriam, K. K., Burke, N. S., Park, H., Kang, C., Postle, K.
(2002). TonB Interacts with Nonreceptor Proteins in the Outer Membrane of Escherichia coli. J. Bacteriol.
184: 1640-1648
[Abstract]
[Full Text]
-
Narita, S.-i., Tanaka, K., Matsuyama, S.-i., Tokuda, H.
(2002). Disruption of lolCDE, Encoding an ATP-Binding Cassette Transporter, Is Lethal for Escherichia coli and Prevents Release of Lipoproteins from the Inner Membrane. J. Bacteriol.
184: 1417-1422
[Abstract]
[Full Text]