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Genes to Cells (2004) 9, 765-771. doi:10.1111/j.1365-2443.2004.00770.x
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FtsZ-dependent localization of GroEL protein at possible division sites

Hidetaka Ogino1, Masaaki Wachi1,*, Akihiro Ishii1, Noritaka Iwai1, Tetsuya Nishida2, Sakuo Yamada3, Kazuo Nagai4 and Motoyuki Sugai2

1 Department of Bioengineering, Tokyo Institute of Technology, 4259-B-38 Nagatsuta, Midori-ku, Yokohama 226-8501, Japan
2 Department of Bacteriology, Hiroshima University Graduate School of Biomedical Sciences, Kasumi 1-2-3, Minami-ku, Hiroshima 734-8553, Japan
3 Department of Microbiology, Kawasaki Medical School, 577 Matsushima, Kurashiki, Okayama 701-0192, Japan
4 Department of Biological Chemistry, Chubu University, 1200 Matsumoto-cho, Kasugai, Aichi 487-8501, Japan


   Abstract
Top
 Abstract
Introduction
 Results
 Discussion
 Experimental procedures
 References
 
When Escherichia coli is treated with penicillin, the envelopes bulge at the centre of the cells and the cells then lyse. The bulges expand into vesicle-like structures termed penicillin-induced vesicles. We have developed a method to isolate these structures and have shown that they contain mainly membrane proteins plus a high concentration of a 60 kDa protein. The N-terminal amino acid sequence of the protein is identical to that of GroEL protein. Western blotting analysis using anti-GroEL antibody showed that GroEL is indeed concentrated in the vesicles. Indirect immuno-fluorescence microscopy showed that GroEL protein is localized at the centre of the cells at the site of formation of FtsZ-rings. Localization of GroEL is dependent on FtsZ but not other Fts proteins. GroEL mutants formed elongated cells having no or asymmetrically localized FtsZ-rings at the restrictive temperature. These findings suggest a possible role of the GroEL protein in cell division.


   Introduction
Top
 Abstract
 Introduction
Results
 Discussion
 Experimental procedures
 References
 
The groE operon consists of two genes groES and groEL (Tilly et al. 1981). These genes were first shown to be required for morphogenesis of {lambda} phage (Georgopoulos et al. 1973) and then to constitute GroE chaperone system. Most of the studies to date have focused on the chaperone role of GroEL in protein folding (for a review, Grantcharova et al. 2001). GroE chaperone is required for many cellular processes, such as cytoplasmic protein folding (Horwich et al. 1993), protein degradation (Kandror et al. 1994), and protein export (Kusukawa et al. 1989). The precise in vivo role of these proteins remains to be fully defined. Expression of the groE operon is strongly induced by heat shock (Herendeen et al. 1979) but these genes are essential at all temperatures (Fayet et al. 1989). In vivo experiments showed that almost half of E. coli proteins are able to bind to GroEL (Viitanen et al. 1992) and an experiment identified in vivo substrates of GroEL (Houry et al. 1999). It is also been shown that diaminopimelate (DAP), a component of the cell wall peptidoglycan, suppresses lysis of the cells caused by depletion of GroES and GroEL (McLennan & Masters 1998). However, DAP alone does not restore colony-forming ability. Observations that seem not to be related to the protein folding function of GroEL have also been reported. GroEL proteins were found as cell surface antigens of several bacteria, such as Helicobactor pylori and Mycobacterium tuberculosis (Shinnick et al. 1988; Yamaguchi et al. 1997). Monoclonal antibody against H. pylori GroEL inhibits cell growth (Yamaguchi et al. 1997).

In the course of analysing the action mechanism of penicillin, we found that the GroEL protein was accumulated in the vesicle-like structures formed at the centre of cells upon penicillin-treatment. In addition, indirect immuno-fluorescence microscopy showed that GroEL was localized at possible division sites in an FtsZ-ring dependent manner. These findings suggest a possible role of the GroEL protein in cell division.


   Results
Top
 Abstract
 Introduction
 Results
Discussion
 Experimental procedures
 References
 
Penicillin inhibits peptidoglycan synthesis by covalently binding to the active site of transpeptidase domain of penicillin-binding proteins. When E. coli is treated with penicillin, the envelopes bulge at the centre of the cells and the cells then lyse. It has been reported that peptidoglycan synthesis is carried out all over the cell surface (Burman et al. 1983). It is not obvious then why bulges are formed preferentially at the centre of the cells. Electron microscopic observation of penicillin-treated E. coli cells showed that vesicle-like structures termed penicillin-induced vesicles (PIVs) were formed at the centre of the cells (Fig. 1 A,B). PIVs appeared to be released from the cells upon cell lysis and were found outside of the cells (Fig. 1C,D). Similar vesicle-like structures have been also observed in penicillin-treated Staphylococcus aureus. A lytic enzyme, autolysin, is concentrated in these structures (Sugai et al. 1997 and our unpublished data). We succeeded in isolating E. coli PIVs using a method developed for isolation of S. aureus vesicles. Vesicles with diameters of 10-200 nm were observed by electron microscopy of the isolated PIV fraction (Fig. 1E). Without penicillin-treatment, such vesicles were not recovered (data not shown). SDS-polyacrylamide gel electrophoresis of the preparation showed that the vesicles contain proteins similar to those of E. coli outer-membrane fractions and in addition a relatively high concentration of a protein with Mr of 60 kDa (Fig. 2A). The N-terminal amino acid sequence of the 60 kDa protein was AAKDVKFGND, which is identical with that of GroEL. Western blotting analysis using anti-GroEL antibody showed that this protein is found mainly in the soluble fraction rather than the membrane fraction of untreated wild-type E. coli cells but that it indeed accumulates in the PIVs (Fig. 2B). Since GroEL is a stress-induced protein, it is possible that synthesis of GroEL protein was enhanced by penicillin-treatment and that the overproduced protein was recovered in PIVs. To check this possibility, the total amount of GroEL protein was examined by Western blotting and it was found that penicillin-treatment did not enhance GroEL synthesis (Fig. 2D)



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  		Figure 1  Ultra-thin sections of penicillin-treated E. coli cells and the isolated PIVs. Exponentially growing E. coli cells at 30 °C were treated with 64 µg/mL penicillin G (2 x MIC) and 0.51 M NaCl for 3 h. PIVs were isolated as described in the Experimental procedures. Electron micrographs of penicillin-treated E. coli cells (A–D), and the isolated PIVs (E) are shown. The bar represents 200 nm.

 


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  		Figure 2  Accumulation of GroEL protein in the isolated PIVs. (A) Protein profiles of soluble fractions (lane 1) and membrane fractions (lane 2) of untreated wild-type E. coli cells, the isolated PIVs (lane 3), and purified GroEL (lane 4). A Coommassie-Brilliant Blue stained polyacrylamide gel (12.5%) is shown. (B) Western blot analysis of (A) with anti-GroEL antibody. (C) Western blot analysis with anti-GroES antibody. A 15% polyacrylamide gel was used. Lanes 1–3 are the same as in (A), and lane 4 is purified GroES protein. (D) Effect of penicillin-treatment on GroEL synthesis. Total cellular proteins were examined by Western blotting using anti-GroEL antibody. Cell lysates from untreated cells (lane 1), treated with 64 µg/mL penicillin G (2 x MIC) and 0.51 M NaCl for 3 h (lane 2), or with 0.51 M NaCl for 3 h (lane 3), or treated at 50 °C for 10 min (lane 4).

 
We surmise that GroEL originally localizes in the centre of the cells and that it becomes enclosed in vesicles during their formation by penicillin-treatment. We examined the intracellular localization of GroEL by indirect immuno-fluorescence microscopy using anti-GroEL antibody. In the wild-type E. coli cells, GroEL preferentially localizes at the centre of the cells, and occasionally at the cell poles. Double staining with anti-FtsZ antibody revealed that centrally located GroEL overlaps with the FtsZ-ring. In shorter cells, GroEL was not localized at the cell centre but was found at the poles only (Fig. 3). It could be argued that central and polar localization of GroEL represent protein molecules that were thrust aside by nucleoids (‘nucleoid exclusion’). To examine this possibility, we looked at anucleate cells (chromosome-less cells) in a parC mutant (temperature-sensitive in TopoIV) (Kato et al. 1988). As shown in Fig. 4(A–E), the central localization of GroEL was still seen in anucleate cells co-localized with FtsZ-ring. The polar localization of GroEL disappeared in anucleate cells, which is compatible with nucleoid exclusion. ß-Galactosidase was used as a reference for soluble cytoplasmic proteins and did not show any specific localization in anucleate cells (Fig. 4F–H). Fractions of cells having an FtsZ-ring and/or centrally localized GroEL in exponentially growing wild-type cells were counted (Table 1). About 75% of cells had FtsZ-rings co-localized with GroEL and about 14% cells had FtsZ-rings only. 7% of cells had neither an FtsZ-ring nor a GroEL ring. About 4% had GroEL rings only. These results suggest that FtsZ-ring formation occurs prior to the central localization of GroEL.



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  		Figure 3  Intracellular localization of GroEL protein in wild-type E. coli cells. Images of differential interference contrast (DIC) microscopy (A, D) and of fluorescence microscopy stained with anti-FtsZ (B, E) or anti-GroEL (C, F) are shown. The bar represents 2 µm.

 


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  		Figure 4  Localization of GroEL in anucleate cells. parC1215 mutant cells (EJ812) were grown at 42 °C for 3 h. Boxed regions in (A, B), in which three anucleate cells were found, are magnified in (C–E). (A, C, F) Images of DIC. (B) Image of DAPI. (D, G) Images of anti-FtsZ. (E) Images of anti-GroEL. (H) Image of anti-ß-galactosidase. Two cells seen in (F–H) were anucleate cells (image of DAPI staining is not shown). The bar represents 6 µm for (A, B) and 2 µm for (C–H).

 

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  		Table 1  Co-localization of FtsZ-ring and centrally localized GroEL
 
It is known that assembly of the cell division machinery, the so-called divisome, is a sequential process initiated by FtsZ-ring formation at the future division site, the centre of the cell. Recruitment of a given protein to the division site depends on the local presence of a former one (for reviews, Rothfield et al. 1999; Margolin 2000). We examined the dependency of GroEL localization on various components of the divisome. Specific localization of GroEL was not observed in ftsZ84 mutant cells defective in FtsZ-ring formation (Fig. 5A). On the other hand, GroEL co-localized with FtsZ-rings in elongated cells of ftsA, ftsQ, ftsL, ftsW, or ftsI mutant strains (Fig. 5B–F). This indicates that localization of GroEL at the possible division site is dependent on FtsZ-ring formation but not on the subsequent assembly of other cell division proteins. This also confirms that localization of GroEL is not due to nucleoid exclusion. A band of GroEL was also seen at the centre of some filaments and between the two main FtsZ-rings (Fig. 5C–F). This position may be the site of formation of the old FtsZ-ring since a faint, probably disassembling, FtsZ-ring could be found occasionally at the centre of filaments (see Fig. 5C,D).



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  		Figure 5  FtsZ-dependent localization of GroEL protein at possible division sites and abnormal FtsZ-ring formation in groEL mutant cells. Images of DIC microscopy and fluorescence microscopy (anti-FtsZ and anti-GroEL) are shown. fts mutant strains were grown at 42 °C for 2 h (A) ftsZ84 (JEFZ1). (B) ftsA (JEFA1). (C) ftsQ1 (JEFQ1). (D) mraR36/ftsL36 (JLB36). (E) ftsW17 (JLB17). (F) ftsI (JLB1). (G, H) Temperature sensitive groEL44 mutant cells (CG2241) were grown at 42 °C for 2 h. The bar represents 5 µm.

 
We further examined if GroEL plays a role in cell division process. Temperature-sensitive groEL mutant (Zeilstra-Ryalls et al. 1994) formed elongated cells at the restrictive temperature, indicating that cell division was affected. Some of elongated groEL cells had one FtsZ-ring asymmetrically localized (Fig. 5G,H). On the other hand, most of the elongated cells of typical fts mutants had two intact FtsZ-rings that were symmetrically localized (see Fig. 5B–F). As shown in Table 2, most of the ftsA filaments (more than 98%) had symmetrically localized FtsZ-rings. On the other hand, 30% of groEL filaments had no FtsZ-ring and about 12% had one FtsZ-ring asymmetrically localized. It appears that formation of FtsZ-ring itself is not dependent on GroEL but that FtsZ-rings are unstable in the absence of active GroEL protein.


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  		Table 2  FtsZ-ring formation in groEL and ftsA filaments
 
Since GroEL functions as a molecular chaperone with GroES, we determined whether GroES is also concentrated in the PIVs. Unexpectedly, GroES was not found in the PIVs (Fig. 2C) nor was it detected at the centre of the cells (data not shown).


   Discussion
Top
 Abstract
 Introduction
 Results
 Discussion
Experimental procedures
 References
 
In the course of analysing the action mechanism of penicillin, we found that the GroEL protein was accumulated in the vesicle-like structures formed at the centre of cells upon penicillin-treatment (Figs 1 and 2). Although the origin and the mechanism of formation of these vesicles are unknown, we surmised that the GroEL protein is originally localized at the centre of cells. Indirect immuno-fluorescence microscopy using anti-GroEL antibody showed that GroEL protein localized at possible division sites where FtsZ-rings formed, and also at cell poles (Fig. 3). Analysis with anucleate cells revealed that polar localization of GroEL was due to nucleoid exclusion (Fig. 4). Analysis with fts mutants revealed that specific central localization of GroEL is dependent on FtsZ-ring formation but not on assembly of other components of divisome (Fig. 5A–F). This is the first evidence demonstrating the involvement of GroEL protein in the cell division process of E. coli. Since GroEL is a molecular chaperone, it seems likely that GroEL is required for recruitment of cell division proteins on to FtsZ-rings or the maintenance of the assembled divisome. It is also possible that GroEL works simply to stabilize the FtsZ-ring. GroEL may be required for efficient polymerization of FtsZ itself. Lack of a complete FtsZ-ring would result in failure to recruit other Fts proteins. This notion is supported by the abnormal FtsZ-ring formation in the absence of active GroEL (Fig. 5G,H). A defect of GroEL leads eventually to cell lysis, which is suppressed by addition of DAP (McLennan & Masters 1998). It could be argued that loss of FtsZ-rings in the groEL filaments is related to deficiency in murein synthesis due to DAP depletion. However, this notion may not be relevant since a DAP auxotroph does not form filaments but lyses by depletion of DAP.

The eukaryotic counterpart of GroEL, TRiC (also called CCT), is bound to tubulin, a eukaryotic homologue of FtsZ (Dunn et al. 2001; Llorca et al. 2001). FtsZ-dependent specific localization was observed only for GroEL but not for GroES. The mutant GroEL44 protein no longer co-localized with FtsZ-rings (Fig. 5G,H). The mutation of GroEL44, E191G, which is located in the hinge region between intermediate and apical domains, affects its interaction with GroES (Chatellier et al. 2000). It is likely that recruitment of GroEL to possible division sites is also mediated by this region. Therefore, direct interaction of GroEL with the FtsZ-ring, or some FtsZ-ring associated protein, may compete with GroES binding to GroEL. GroEL, but not GroES, has been shown to function in the stabilization of RNA polymerase under certain conditions (Mukherjee et al. 1999). It has also been reported that GroEL alone promotes protein folding without GroES, at least, in vitro (Martin et al. 1991). A eukaryotic counterpart of GroES has not yet been identified. Therefore, it is possible that GroEL alone plays its role at the possible division sites as a component of the divisome. This may be one of the essential roles of this protein in bacterial cells. It has also been reported that penicillin-induced cell lysis was suppressed by over-expression of heat shock proteins including GroEL (Powell & Young 1991), suggesting a possible role of PIVs containing GroEL in penicillin-induced cell lysis.


   Experimental procedures
Top
 Abstract
 Introduction
 Results
 Discussion
 Experimental procedures
References
 
Bacterial strains and media

E. coli K-12 strain W3110 (wild-type), CG2241 (groEL44) (Zeilstra-Ryalls et al. 1994), AI90/pBAD-EL ({Delta}groEL/para-groEL) (Ivic et al. 1997), EJ812 (parC1215) (Kato et al. 1988), JLB17 (ftsW17), JLB36 (mraR36/ftsL36) (Ishino et al. 1989), JLB1 (ftsI), JEFA1 (ftsA), JEFQ1 (ftsQ1), and JEFZ1 (ftsZ84) (Jung et al. 1989) were grown in Lennox broth containing 1% Bactopeptone, 0.5% yeast extract, 0.5% NaCl, and 0.1% glucose (pH 7.0), supplemented with 20 mg/L of thymine.

Isolation of PIVs

E. coli PIVs were isolated by essentially following the method developed for isolation of S. aureus PIVs (Sugai et al. 1997 and our unpublished data). Exponentially growing E. coli cells at 30 °C were treated with 64 µg/mL penicillin G (2 x MIC) and 0.51 M NaCl for 3 h. Cells were removed by centrifugation (10 000 g, 30 min) and the supernatant was filtrated with membrane filter (0.2 µm) to remove debris. Then the filtrate was centrifuged at 4 °C for 1 h at 120 000 g. The precipitate was suspended in 0.1 M sodium phosphate buffer (pH 7.0) and collected as PIV fractions.

Electron microscopy

Thin-section electron microscopy was performed as previously described (Sugai et al. 1997; Yamada et al. 1996). Penicillin G-treated E. coli cells were washed with phosphate-buffered saline, and then the cells were doubly fixed with 2.5% glutaraldehyde and 1% OsO4. The samples were dehydrated in a series of ethanol concentrations and then embedded in Spurr's Epon. Thin sections were cut on an ultramicrotome with a diamond knife and were examined in an electron microscope (JEM-2000 EX II, JEOL Ltd, Tokyo, Japan) at 80 kV.

Indirect immuno-fluorescence microscopy

Indirect immuno-fluorescence microscopy was carried out by essentially following the method of Hiraga et al. (1998). One hundred µL of cultures were added to 900 µL of ice-cold methanol and incubated for 5 min on ice. Cells were harvested by centrifugation and suspended in 100 µL 90% methanol. Cell suspension was spread on poly L-lysine coated slide glass. After drying, cells were treated with lysozyme solution (0.2 mg/mL lysozyme, 25 mM Tris-HCl pH 8.0, 50 mM glucose, 10 mM EDTA) for 5 min and then rinsed with PBSTS (140 mM NaCl, 2 mM KCl, 8 mM Na2HPO4, 0.05% Tween 20, 20% sucrose). Then, cells were treated with methanol for 1 min and acetone for 1 min and dried. Fixed cells were treated with 2% bovine serum albumin in PBSTS for 15 min. After rinse with PBSTS, cells were stained with first antibody for 1 h and then with fluorescence-labelled second antibody for 1 h. The immuno-stained samples were observed by a microscope (Axioskop 2, Carl Zeiss Co. Ltd, Oberkochen, Germany) with a chilled 3CCD camera (MicroMax, Roper Industries Inc., Bogart, GA, USA). Anti-GroEL rabbit antiserum was raised against GroEL protein purchased from Takara Shuzo (Kyoto, Japan) and used after nonspecific antibodies were absorbed with cell lysate prepared from GroEL-depleted cells (AI90/pBAD-EL grown in the presence of glucose). Anti-FtsZ mouse antiserum and anti-FtsZ rabbit antiserum were raised against His-tagged FtsZ protein purified chromatographically. Anti-GroES rabbit antiserum was purchased from StressGen (Victoria, B.C., Canada). Anti-ß-galactosidase monoclonal mouse IgG was purchased from Monosan (Uden, Netherlands). Alexa488-labelled goat anti-rabbit IgG was purchased from Molecular Probes (Eugene, OR, USA) and Cy3-labelled goat anti-mouse IgG from Amersham Pharmacia Biotech (Foster City, CA, USA).


   Acknowledgements
 
Authors thank M. Schaechter for critical reading of the manuscript and M. Yoshida, J. Kato and P. A. Lund for providing bacterial strains, CG2241, EJ812 and AI90/pBAD-EL, respectively. This work was supported in part by the Grant-in-Aid for Scientific Research (B) (15380059 to M. W.) from Japan Society for the Promotion of Science and the Grant of the 21st Century COE Program from the Ministry of Education, Culture, Sports, Science and Technology of Japan.


   Footnotes
 
Communicated by: Hiroji Aiba

* Correspondence: E-mail: mwachi{at}bio.titech.ac.jp


   References
Top
 Abstract
 Introduction
 Results
 Discussion
 Experimental procedures
 References
 
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Received: 2 June 2004
Accepted: 28 June 2004




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V. Norris, T. den Blaauwen, A. Cabin-Flaman, R. H. Doi, R. Harshey, L. Janniere, A. Jimenez-Sanchez, D. J. Jin, P. A. Levin, E. Mileykovskaya, et al.
Functional Taxonomy of Bacterial Hyperstructures
Microbiol. Mol. Biol. Rev., March 1, 2007; 71(1): 230 - 253.
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 J. Bacteriol.Home page
T. J. Radosevich, T. A. Reinhardt, J. D. Lippolis, J. P. Bannantine, and J. R. Stabel
Proteome and Differential Expression Analysis of Membrane and Cytosolic Proteins from Mycobacterium avium subsp. paratuberculosis Strains K-10 and 187
J. Bacteriol., February 1, 2007; 189(3): 1109 - 1117.
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M. Vicente, A. I. Rico, R. Martinez-Arteaga, and J. Mingorance
Septum Enlightenment: Assembly of Bacterial Division Proteins
J. Bacteriol., January 1, 2006; 188(1): 19 - 27.
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