Previous Article | Next Article 
Journal of Bacteriology, April 2001, p. 2187-2197, Vol. 183, No. 7
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.7.2187-2197.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Physiological Basis for Conservation of the Signal
Recognition Particle Targeting Pathway in Escherichia
coli
Harris D.
Bernstein* and
Janine B.
Hyndman
Genetics and Biochemistry Branch, National
Institute of Diabetes and Digestive and Kidney Diseases, National
Institutes of Health, Bethesda, Maryland 20892-1810
Received 2 November 2000/Accepted 5 January 2001
The Escherichia coli signal recognition particle (SRP)
is a ribonucleoprotein complex that targets nascent inner membrane proteins (IMPs) to transport sites in the inner membrane (IM). Since
SRP depletion only partially inhibits IMP insertion under some growth
conditions, however, it is not clear why the particle is absolutely
essential for viability. Insights into this question emerged from
experiments in which we analyzed the physiological consequences of
reducing the intracellular concentration of SRP below the wild-type
level. We found that even moderate SRP deficiencies that have little
effect on cell growth led to the induction of a heat shock response.
Genetic manipulations that suppress the heat shock response were lethal
in SRP-deficient cells, indicating that the elevated synthesis of heat
shock proteins plays an important role in maintaining cell viability.
Although it is conceivable that the heat shock response serves to
increase the capacity of cells to target IMPs via chaperone-based
mechanisms, SRP-deficient cells did not show an increased dependence on
either GroEL or DnaK. By contrast, the heat shock-regulated proteases
Lon and ClpQ became essential for viability when SRP levels were
reduced. These results suggest that the heat shock response protects
SRP-deficient cells by increasing their capacity to degrade
mislocalized IMPs. Consistent with this notion, a model IMP that was
mislocalized in the cytoplasm as the result of SRP depletion appeared
to be more stable in a
lon
clpQ strain than in
control cells. Taken together, the data provide direct evidence that
SRP is essential in E. coli and possibly conserved
throughout prokaryotic evolution as well partly because efficient IMP
targeting prevents a toxic accumulation of aggregated proteins in the cytoplasm.
*
Corresponding author. Mailing address: National
Institutes of Health, Building 10, Room 9D-20, Bethesda, MD 20892-1810. Phone: (301) 402-4770. Fax: (301) 402-0387. E-mail:
harris_bernstein{at}nih.gov.
Journal of Bacteriology, April 2001, p. 2187-2197, Vol. 183, No. 7
0021-9193/01/$04.00+0 DOI: 10.1128/JB.183.7.2187-2197.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Burk, J., Weiche, B., Wenk, M., Boy, D., Nestel, S., Heimrich, B., Koch, H.-G.
(2009). Depletion of the Signal Recognition Particle Receptor Inactivates Ribosomes in Escherichia coli. J. Bacteriol.
191: 7017-7026
[Abstract]
[Full Text]
-
Akiyama, Y.
(2009). Quality Control of Cytoplasmic Membrane Proteins in Escherichia coli. J Biochem
146: 449-454
[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]
-
Bradshaw, N., Walter, P.
(2007). The Signal Recognition Particle (SRP) RNA Links Conformational Changes in the SRP to Protein Targeting. Mol. Biol. Cell
18: 2728-2734
[Abstract]
[Full Text]
-
Shimohata, N., Nagamori, S., Akiyama, Y., Kaback, H. R., Ito, K.
(2007). SecY alterations that impair membrane protein folding and generate a membrane stress. JCB
176: 307-317
[Abstract]
[Full Text]
-
Ullers, R. S., Houben, E. N. G., Brunner, J., Oudega, B., Harms, N., Luirink, J.
(2006). Sequence-specific Interactions of Nascent Escherichia coli Polypeptides with Trigger Factor and Signal Recognition Particle. J. Biol. Chem.
281: 13999-14005
[Abstract]
[Full Text]
-
Su, S., Stephens, B. B., Alexandre, G., Farrand, S. K.
(2006). Lon protease of the {alpha}-proteobacterium Agrobacterium tumefaciens is required for normal growth, cellular morphology and full virulence.. Microbiology
152: 1197-1207
[Abstract]
[Full Text]
-
Houben, E. N.G., Zarivach, R., Oudega, B., Luirink, J.
(2005). Early encounters of a nascent membrane protein: specificity and timing of contacts inside and outside the ribosome. JCB
170: 27-35
[Abstract]
[Full Text]
-
Henrichs, T., Mikhaleva, N., Conz, C., Deuerling, E., Boyd, D., Zelazny, A., Bibi, E., Ban, N., Ehrmann, M.
(2005). Target-directed proteolysis at the ribosome. Proc. Natl. Acad. Sci. USA
102: 4246-4251
[Abstract]
[Full Text]
-
Froderberg, L., Houben, E. N. G., Baars, L., Luirink, J., de Gier, J.-W.
(2004). Targeting and Translocation of Two Lipoproteins in Escherichia coli via the SRP/Sec/YidC Pathway. J. Biol. Chem.
279: 31026-31032
[Abstract]
[Full Text]
-
Jones, S. E., Lloyd, L. J., Tan, K. K., Buck, M.
(2003). Secretion Defects That Activate the Phage Shock Response of Escherichia coli. J. Bacteriol.
185: 6707-6711
[Abstract]
[Full Text]
-
Qi, H.-Y., Hyndman, J. B., Bernstein, H. D.
(2002). DnaK Promotes the Selective Export of Outer Membrane Protein Precursors in SecA-deficient Escherichia coli. J. Biol. Chem.
277: 51077-51083
[Abstract]
[Full Text]
-
Park, S.-K., Jiang, F., Dalbey, R. E., Phillips, G. J.
(2002). Functional Analysis of the Signal Recognition Particle in Escherichia coli by Characterization of a Temperature-Sensitive ffh Mutant. J. Bacteriol.
184: 2642-2653
[Abstract]
[Full Text]