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Journal of Bacteriology, October 1999, p. 6419-6424, Vol. 181, No. 20
Department of Molecular Biology and
Microbiology, Case Western Reserve University, School of Medicine,
Cleveland, Ohio 44106-4960
Received 7 July 1999/Accepted 11 August 1999
By inhibiting FtsZ ring formation near the cell ends, the MinC
protein plays a critical role in proper positioning of the division
apparatus in Escherichia coli. MinC activity requires that
of MinD, and the MinE peptide provides topological specificity by
suppressing MinC-MinD-mediated division inhibition specifically at the
middle of the cell. We recently presented evidence that MinE not only
accumulates in an FtsZ-independent ring structure at the cell's middle
but also imposes a unique dynamic localization pattern upon MinD in
which the latter accumulates alternately in either one of the cell
halves in what appears to be a rapidly oscillating membrane
association-dissociation cycle. Here we show that functional green
fluorescent protein-MinC displays a very similar oscillatory behavior
which is dependent on both MinD and MinE and independent of FtsZ. The
results support a model in which MinD recruits MinC to its site of
action and in which FtsZ ring assembly at each of the cell ends is
blocked in an intermittent and alternate fashion.
Cell division in prokaryotes is
initiated by the localization of the tubulin-like GTPase FtsZ to the
future division site. FtsZ assembles into a ring, and other proteins
are then recruited to form the septal ring organelle which mediates
cell envelope invagination (5, 23, 24, 34). Division of
Escherichia coli normally occurs at the middle of the cell,
but potential division sites (PDSs) are also present near each of the
cell poles (1, 37). Restricting division to the cell's
midpoint requires the activity of the protein products of the
min operon, MinC, MinD, and MinE (10). MinC can
inhibit division at all PDSs by preventing formation of the FtsZ ring
but normally requires the activity of the peripheral membrane ATPase
MinD for this function (3, 8-10). How MinD stimulates MinC
function is not clear, but the two proteins interact in two-hybrid
assays, suggesting that they form a complex (18). Mutants
lacking either MinC or MinD frequently divide near the cell ends,
resulting in the production of small, chromosomeless minicells (9,
10, 12). MinE provides topological specificity to the system by
suppressing MinCD division inhibition specifically at midcell, allowing
FtsZ ring assembly at this site (10, 31, 32, 42).
We recently showed that a functional green fluorescent protein
(Gfp)-tagged derivative of MinE accumulates in a ring at or near
midcell. Formation of the MinE ring did not require MinC or FtsZ but
depended on the presence of MinD (32). Conversely, functional Gfp-MinD was found to undergo a unique, dynamic, oscillatory localization cycle which is also independent of MinC and FtsZ but
requires MinE (33). In the absence of MinE, Gfp-MinD
accumulated along the periphery of the entire cell. In
MinE+ cells, however, Gfp-MinD segregated to the periphery
of one of the cell halves, where it dwelled for a short period of time
(~10 s), and then relocated to the opposite cell half, where it
dwelled again, followed by relocation to its original position, and so on. A moderate increase in the Gfp-MinD/MinE ratio in the cell led to
an increase in the average dwell time and the concomitant formation of
polar septa, suggesting that a certain minimum oscillation frequency of
MinD is required to efficiently suppress FtsZ ring formation at both
poles (33).
These results support a model in which MinD stimulates division
inhibition in one cell half at a time while MinE protects the midcell
from MinC-MinD action (20, 33). This model is compatible
with two possible mechanisms of MinC-MinD action, depending on the
relative affinities of MinC for MinD on the one hand and for its
presumed sites of action on the other. Thus, MinC may have a higher
affinity for MinD and follow the latter from one cell half to the
other. Alternatively, MinC may have a higher affinity for fixed
cellular sites, such as cell poles, and become activated whenever the
two proteins colocalize.
Supporting the first possibility, we here describe the dynamic
properties of a functional Gfp-MinC fusion protein in live cells.
Gfp-MinC oscillated from pole to pole in a membrane
association-dissociation cycle that is similar to that of Gfp-MinD
(33). Furthermore, segregation and oscillation of Gfp-MinC
did not require FtsZ ring assembly but were dependent on both MinD and
MinE. The results strongly support the notion that E. coli
prevents polar division events from occurring by rapidly shuttling the
MinC division inhibitor back and forth between the cell ends in a
MinD-driven process, leaving only the middle of the cell competent to
support septum formation.
Strains, plasmids, and phages.
Strains PB103 (dadR
trpE trpA tna) (11) and PB114 (PB103,
0021-9193/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
MinDE-Dependent Pole-to-Pole Oscillation of
Division Inhibitor MinC in Escherichia coli
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
minCDE::aph) (10) have
been described previously.
pR::gfpmut2-minC) is a
pGB2 (pSC101) derivative which encodes a 52.5-kDa fusion protein in
which the complete Gfpmut2 peptide (7) is joined by the
linker peptide ASMTGGQQMGRIP to residues 5 to 232 of MinC. The plasmid
was constructed in several steps. Insertion of the 1,857-bp
BamHI/EcoRI fragment of pDB124 (10)
into the multicloning sequence of pET21c (Novagen) yielded pDB299. The
1,999-bp BglII/EcoRI fragment of pDB299 was next
inserted into the multicloning sequence of pMLB1115 (10). Replacement of the 76-bp XbaI/BamHI fragment of
the resulting plasmid (pCH2) with the 771-bp
XbaI/BamHI fragment of pDR107c (33)
gave rise to pDR115, and replacement of the 2,492-bp
ClaI/NsiI fragment of this plasmid with the
1,495-bp ClaI/NsiI fragment of pDB171
(10) resulted in pDR121. Finally, pDR175 was obtained by
replacement of the 1,096-bp XbaI/SalI fragment of
pDB346 (32) with the 1,614-bp
XbaI/SalI fragment of pDR121.
The phages DB156 (imm21
bla+ lacIq+
Plac::minE), DB175
(imm21 bla+
lacIq+
Plac::minDE), DR122
(imm21 bla+
lacIq+
Plac::gfp-minDE), and
DR144 (imm21 bla+
lacIq+
Plac::sfiA) have been
described previously (10, 32, 33). Phage DR155
(imm21 bla+
lacIq+
Plac::minD) was obtained by
crossing pDR155 with NT5 (10).
Microscopy and other methods.
Cells were grown at either 30 or 37°C in M9 minimal salts medium supplemented with tryptophan (50 µg/ml), Casamino Acids (0.2%), maltose (0.2%), and
isopropyl-
-D-thiogalactopyranoside (IPTG; as indicated)
to an optical density (600 nm) of approximately 0.5. Doubling times
ranged from 175 (30°C) to 90 (37°C) min.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Gfp-MinC is functional.
To study the location of MinC in
living cells, we constructed pDR175
(pR::gfp-minC cI857), a
low-copy-number plasmid encoding a Gfp-MinC fusion in which the first
four amino acids of MinC are replaced by a bright variant of Gfp
(Gfpmut2 [7]). Transcription of gfp-minC
from this plasmid is under control of the pR
promoter and a temperature-sensitive allele of the repressor such
that expression of the fusion increases with increasing temperature (Fig. 1). The functionality of Gfp-MinC
was studied by testing the ability of pDR175 to correct the minicell
phenotype (Min
) of strain PB114(DB175)
[minCDE(Plac::minDE)].
This strain lacks the chromosomal minCDE operon but is
lysogenic for a phage which carries the minD and
minE genes downstream from the lac promoter. When
grown in the absence of IPTG (MinDE), cells of strain
PB114(DB175)/pDR175 showed the Min phenotype
regardless of the temperature (Table 1).
At 30 and 37°C, respectively, 45 and 55% of all septa were misplaced
at a pole.
|
|
DB175)/pDR175 depended on the incubation
temperature. At 30°C, cells were still clearly Min
(Fig. 2F; Table 1), although the percentage of polar septa (15%) was
reduced significantly when compared to that of cells grown in the
absence of IPTG. As judged from immunoblot analyses with MinC-specific
antiserum, Gfp-MinC was expressed at a low but detectable level at this
temperature (Fig. 1, lane 6), providing a likely explanation for the
partial suppression of the Min phenotype under these
conditions. When cells were grown at 37°C, the level of Gfp-MinC
increased to a fewfold that of native MinC in the wild-type (WT)
strain, PB103 (Fig. 1, lanes 2 to 5). Importantly, cells displayed a
normal division phenotype under these conditions (Fig.
2G; Table 1), with less than 1% (2 of
215) of septa being polar. In addition to full-length fusion, cell
extracts also contained some smaller species that reacted with
anti-MinC antiserum (Fig. 1, lanes 3 to 7). Although these likely
represented incomplete translation and/or breakdown products of
Gfp-MinC, it cannot be ruled out that they actively contributed to
suppression of the Min phenotype. With this caveat in
mind, we conclude that the full-length Gfp-MinC fusion retained a level
of biological activity close to that of the native protein.
|
Segregation and oscillation of Gfp-MinC.
Microscopic
inspection of normally dividing cells of PB114(DB175)/pDR175, grown
at 37°C (Gfp-MinC+) in the presence of 50 µM IPTG
(MinDE+), showed a dynamic distribution of Gfp-MinC
fluorescence (Fig. 2A, B, and D) that was remarkably similar to that
observed for Gfp-MinD (33). Compared to Gfp-MinD
(33), the Gfp-MinC fusion produced a significantly weaker
fluorescent signal, resulting in a relatively low signal/background
ratio. Nevertheless, Gfp-MinC could be readily observed to segregate to
one of the cell halves, where it accumulated at the periphery of the
pole and a variable portion of the adjacent cylindrical portion of the
cell. The protein dwelled for a short period of time and then moved to
take up a similar position in the opposite half of the cell, where it
dwelled again before returning to its original position, and so on.
Figure 2D shows a typical cell in which Gfp-MinC relocated four times in a span of 96 s. We observed up to 15 relocation events per cell
within a span of 305 s, before the signal became too weak to be
detected. Segregation and oscillation of Gfp-MinC could be observed in
virtually all cells in the population, including very small (Fig. 2A)
and constricting (Fig. 2B) cells. As previously noticed with Gfp-MinD
(33), the fluorescent signal at the cell's periphery
weakened as it appeared to increase in the cytoplasm during each shift
period (Fig. 2A to C, 8 s), suggesting that a portion or all of
Gfp-MinC dissociated from the membrane before relocation to the
opposite cell half.
pR::gfp-minC)
divided normally at 37°C (Table 1), indicating that expression of
Gfp-MinC at this level did not noticeably interfere with the activities
of the native Min proteins.
The average oscillation cycle of Gfp-MinC, consisting of two dwell plus
two shift periods, was ~43 s in both PB114(DB175)/pDR175 and PB103/pDR175 cells. Significantly, this oscillation rate was virtually identical to that of Gfp-MinD in cells of strain
PB103(DR122) [WT/(Plac::gfp-minDE)]
grown under similar conditions (Table 1).
These results showed that the behavior of Gfp-MinC in normally dividing
cells is remarkably similar to that previously observed for Gfp-MinD
(33) and suggested a role for native MinD in the oscillatory
behavior of Gfp-MinC in the present experiments.
Segregation and oscillation of Gfp-MinC require both MinD and
MinE.
We previously showed that MinE, but not MinC, is required
for segregation and oscillation of Gfp-MinD. However, Gfp-MinD
localized evenly along the entire periphery of both MinE
MinC+ and MinE MinC cells,
indicating that MinD associates with the membrane, even in the absence
of MinE and MinC (33).
DR155)
[minCDE(Plac::minD)] and cells were grown at 37°C (Gfp-MinC+) in the absence
or presence of IPTG. In the presence of 50 µM IPTG (MinD+
MinE), cells formed long nonseptate filaments, confirming
that Gfp-MinC acted as a potent division inhibitor. Furthermore, the
fusion failed to show the typical segregation and oscillation behavior seen in normally dividing cells but, instead, appeared evenly distributed along the periphery of the entire filament (Fig.
3A; Table 1). These results suggested
that MinD was responsible for recruiting Gfp-MinC to the membrane in
these filaments. Support for this idea came from the observation of
PB114(DR155)/pDR175 cells that had been grown in the absence of IPTG
(MinD MinE). As expected, these cells did
not form filaments but showed the Min phenotype. In
addition, Gfp-MinC was present diffusely throughout the cytoplasm, with
no obvious preference for the membrane or any other specific location
(Table 1). The same cytoplasmic distribution of Gfp-MinC was also
observed in strain PB114(DB175)/pDR175 after growth in the absence
of IPTG (Fig. 2E; Table 1) as well in the nonlysogenic strain
PB114/pDR175 (Table 1). Expression of minE had no effect on
the random distribution of Gfp-MinC in MinD cells. Thus,
cells of strain PB114(DB156)/pDR175
[minCDE(Plac::minE)/pR::gfp-minC], which is lysogenic for a phage carrying minE
downstream of the lac promoter, showed a random distribution
of fluorescence both in the absence (MinD
MinE) and presence (MinD MinE+)
of IPTG (Table 1).
|
Segregation and oscillation of Gfp-MinC do not require FtsZ ring
assembly.
SfiA (SulA) is a MinCDE-independent division inhibitor
which is normally not expressed but is induced as part of the SOS
response to DNA damage. The protein binds FtsZ directly (15,
18), inhibits polymer formation in vitro (26, 38), and
prevents FtsZ ring assembly in vivo (3). In contrast, SfiA
does not interfere with MinE ring formation, and SfiA-induced filaments
contain multiple MinE ring structures (32). To examine the
behavior of Gfp-MinC under conditions where FtsZ ring assembly is
prevented, we constructed strain PB103(DR144)/pDR175
[WT(Plac::sfiA)/pR::gfp-minC], in which sfiA is under control of the lac
promoter. When grown in the presence of 50 µM IPTG, cells formed
nonseptate filaments. Similar to what we observed with Gfp-MinD in
FtsZ filaments (33), Gfp-MinC accumulated in
membrane-associated segments throughout the length of these filaments.
A time lapse series of a short filament containing three such segments
is shown in Fig. 3B. At time zero (t = 0), Gfp-MinC is
present in the central segment but absent from both polar segments.
Eight seconds later, the fusion is present throughout the filament,
with some accumulation at the membrane at the two cell poles. At
t = 16 s, the fusion is located exclusively at the
membrane in the two polar segments. Between t = 24 s
and t = 32 s, the fusion is in transition from the
polar segments to the central segment, with decreased accumulation at
the polar segments and increased accumulation in the central segment.
At t = 40 s, the cycle is complete, and the fusion has returned to the membrane of the central segment. Just as observed with
Gfp-MinD in FtsZ filaments (33), longer
filaments contained an increasing number of segments and Gfp-MinC
appeared to move from the membrane of one segment to the membrane
of neighboring segments (data not shown). As in WT cells (see
above), segregation and oscillation of Gfp-MinC in SfiAinduced
filaments were dependent on the presence of MinD and MinE, and the
fusion was evenly distributed throughout the cytoplasm of SfiA-induced
filaments of strain PB114 (DR144)/pDR175 [minCDE(Plac::sfiA)/pR::gfp-minC]
(Fig. 3C).
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Recently, we showed that functional Gfp-MinD rapidly oscillates
between the two cell halves in a membrane association-dissociation cycle which is dependent on MinE but does not require MinC or FtsZ
(33). Here we showed that biologically active Gfp-MinC undergoes a very similar localization cycle in which the protein oscillates between cell ends at about the same rate as that observed for Gfp-MinD. Like Gfp-MinD (33), segregation and
oscillation of Gfp-MinC required the presence of MinE and occurred
independently of FtsZ rings. However, whereas Gfp-MinD localizes
independently of MinC, the localization of Gfp-MinC appeared to be
directly dictated by MinD. Thus, like MinD itself (33),
Gfp-MinC preferentially associated along the entire periphery of
MinE filaments, but the fusion failed to accumulate at
any specific location in the absence of MinD regardless of the presence
of MinE.
Combined with the knowledge that MinC and MinD show a strong
interaction in two-hybrid assays (18), these observations
support a model for MinC action which is summarized in Fig.
4. In the absence of MinD and MinE, MinC
has no intrinsic affinity for any special site and is present
throughout the cell (Fig. 4A). In MinE cells, MinD
associates with the cytoplasmic membrane and recruits MinC. The even
distribution of MinC-MinD along the membrane results in a block of FtsZ
ring assembly at all PDSs and the formation of nonseptate filaments
(Fig. 4B). In WT cells, MinE accumulates in a ring at midcell and
stimulates the dynamic oscillatory behavior of MinD. MinC follows along
with MinD and either remains associated with MinD throughout
oscillation or disengages during disassembly of MinD from the membrane,
only to reengage when MinD assembles at the membrane in the opposite
half. In either case, MinC actively interferes with FtsZ ring assembly
at only one of the cell poles at a time (Fig. 4C).
|
, MinC;
, MinD;
, the
MinE ring. PDSs are represented by either a minus (blocked by
MinC-MinD) or a plus (not blocked, available for FtsZ ring assembly)
sign. (A) In the absence of MinD and MinE, MinC localizes
nonspecifically to the cytoplasm and has no effect on septal or FtsZ
ring formation. (B) In the presence of MinD, and absence of MinE, MinC
associates with MinD along the entire membrane, preventing FtsZ ring
formation at all PDSs. (C) In WT cells, MinC co-oscillates with MinD
from one side of the MinE ring to the other, actively interfering with
FtsZ ring assembly at each cell end in a sequential and rapidly
repeating fashion. (D) In cells lacking FtsZ rings, multiple MinE rings
define three or more cell segments. As in WT cells, MinC co-oscillates
with MinD between the segments flanking each MinE ring. Note that
although the figure suggests the presence of a limited number of
regularly spaced PDSs in each cell, the proposed mechanism of MinCDE
action does not depend on the exact number or nature of the PDSs and is
equally tenable whether potential sites for FtsZ ring assembly are
(co)determined by positioning of the nucleoids (Given the evidence for a direct interaction between MinC and MinD, the formal possibility that the two proteins segregate to opposite cell halves and oscillate out of phase by half a cycle is far less likely. So far, attempts to exclude this possibility by observing cells in which the two proteins are tagged with different color Gfp derivatives have failed, due to insufficient signal intensities of the nongreen varieties. However, in MinE+ cells in which Gfp-MinC and Gfp-MinD are expressed simultaneously, we have observed that fluorescence still clearly segregates to only one cell end at a time, indicating that the two proteins indeed co-oscillate in the same direction (data not shown).
It is also noteworthy that the average oscillation rate of Gfp-MinC measured in WT cells (~40 s/cycle) was very close to that of Gfp-MinD in cells in which gfp-minD was coexpressed with minE to maintain a normal MinD-to-MinE ratio (33). This finding not only further supports the idea that the behavior of Gfp-MinC directly reflects that of native MinD in the present experiments but also suggests that oscillation parameters measured with the Gfp-tagged proteins fairly accurately reflect those of native MinC-MinD.
How MinC prevents FtsZ ring assembly is not known. Two-hybrid studies failed to show an interaction between the two proteins (18), and it is well possible that MinC interferes with the activity of another factor required for FtsZ ring assembly, such as a hypothetical membrane-associated molecule that might nucleate FtsZ polymerization. How MinD stimulates MinC activity is also not clear. The present results suggest one straightforward possibility, however; i.e., by recruiting MinC to the membrane, MinD may simply act to increase the local concentration of MinC to effective levels. Compatible with this idea is the fact that an increase in the cellular concentration of MinC to more than ~30-fold its normal level is sufficient to cause division inhibition, even in the absence of MinD (12). Whether this idea is correct or not, the finding that Gfp-MinC associates with MinD at the cell's periphery indicates that MinC-MinD-mediated division inhibition is a membrane-associated event, arguing against mechanisms whereby MinC directly modifies cytoplasmic FtsZ pools to a polymerization-incompetent state.
This work extends and supports our observations on the remarkable properties of the Min proteins in living E. coli cells (32, 33). One of the surprising implications is that MinC-MinD prevents aberrant FtsZ ring formation intermittently, at only one of the cell poles at a time. This mode of action appears not to have been conserved in the gram-positive rod Bacillus subtilis (14, 20, 25) and begs the question why such an oscillatory mechanism might have developed. MinD and MinE determine each other's localization pattern (32) and, as suggested before (33), one attractive possibility is that oscillation of MinD between the cell segments on either side of a MinE ring is coupled to positioning of the ring. In this view, oscillation of MinD provides cells with a measuring device which allows the positioning of MinE at midcell, in the case of WT cells containing one ring, or at regularly spaced intervals, in the case of filaments containing multiple rings.
The idea that the Min system, in addition to preventing aberrant FtsZ
ring assembly, may also function as a measuring device is supported by
recent work by Yu and Margolin (41) in which they analyzed
the placement of FtsZ rings in Min mutants containing
additional mutations that affect nucleoid partitioning
(Par). Placement of division septa in Min
mutants is typically not random but is restricted to a narrow area near
each cell pole and regular positions between segregated nucleoids
(2, 13, 21, 22, 37). One factor that is likely to contribute
to this nonrandom pattern is a phenomenon called nucleoid occlusion
which is based on the observation that septum formation appears to be
inhibited in the close vicinity of the nucleoid(s) of certain DNA
replication and topoisomerase mutants (19, 27, 28, 30, 36,
41). The mechanism of this inhibitory effect is not understood,
although it is conceivable that the formation of septal rings at
envelope sites directly surrounding a nucleoid would be sterically
hindered by an abundance of membrane-associated transcription and
translation complexes (29). In some models, positioning of
the nucleoid is proposed to be the sole determining factor for
positioning of the division apparatus (2, 39, 40), but this
idea is refuted by a host of experimental data (references 4,
6, 16, 35, and 36 and references therein). For instance, mutants affected in nucleoid replication and segregation typically form filamentous cells which release chromosomeless cells
from their ends. In several such mutants, septal placement is not
random and the size distribution of the DNA-less rods is close to that
of normal newly born cells, suggesting that cells can somehow measure a
certain distance from the cell pole (4, 6, 17, 36).
Compelling evidence that the Min proteins are involved in defining this
distance comes from the observation that the positioning of FtsZ rings
becomes essentially random in the nucleoid-free segments of
minCDE parC double mutants (41). One of
several interesting predictions of this work is that MinC-MinD in WT
cells inhibits FtsZ ring assembly not only at the extreme cell ends but
throughout most of the cell envelope except for a relatively narrow
zone at the cell's center defined by the MinE ring (41). Our observations on the distribution of Gfp-MinC and Gfp-MinD are
compatible with this possibility insofar that, during dwell periods,
the association of the two proteins with the membrane is clearly not
restricted to the polar caps. This was especially obvious in the case
of Gfp-MinD, which was frequently seen to cover the membrane from a
pole to approximately the middle of the cell (33). In
general, Gfp-MinC did not appear to extend as far toward midcell,
although the protein was still observed to cover at least one-quarter
of the membrane in most cells. Whether this was due to low signal
intensities or whether factors, in addition to the location of MinD,
further bias Gfp-MinC localization toward the cell ends is not clear.
In any event, additional analyses of the behavior of the Min proteins
in relation to nucleoid dynamics should prove valuable in testing the
proposal by Yu and Margolin that the combination of MinCDE action and
nucleoid occlusion may be sufficient to explain septal placement in
E. coli (41).
Clearly, the dynamic behavior of MinC and MinD raises many new questions requiring additional experimentation. Further elucidation of the mechanisms underlying membrane assembly-disassembly of MinC-MinD and of the role(s) of the MinE ring is likely to contribute significantly to our understanding of the spatial organization of bacterial cells.
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ACKNOWLEDGMENTS |
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We thank Cynthia Hale for help in plasmid construction, technical advice, and comments on the manuscript.
This work was supported by NIH grant GM-57059, NSF Young Investigator Award MCB94-58197, and generous donations from The Elizabeth M. and William C. Treuhaft Fund, The Frank K. Griesinger Trust, Arline H. Garvin, James S. Blank, Charles E. Spahr, Alfred M. Taylor, and Theodore J. Castele (to P.A.J.D.). D.M.R. was supported by an NRSA Institutional Training Grant (T32GM08056) from the National Institutes of Health.
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ADDENDUM IN PROOF |
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Marston and Errington recently showed that the cellular location of Bacillus subtilis MinC is also directly dictated by that of MinD (A. L. Marston and J. Errington, Mol. Microbiol. 33:84-96, 1999).
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Molecular Biology and Microbiology, Case Western Reserve University, School of Medicine, 10900 Euclid Ave., Cleveland, OH 44106-4960. Phone: (216) 368-1697. Fax: (216) 368-3055. E-mail: pad5{at}po.cwru.edu.
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REFERENCES |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Journal of Bacteriology, October 1999, p. 6419-6424, Vol. 181, No. 20
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