Human S100B Protein Interacts with the Escherichia coli Division Protein FtsZ in a Calcium-sensitive Manner

S100B is a small, dimeric EF-hand calcium-binding protein abundant in vertebrates. Upon calcium binding, S100B undergoes a conformational change allowing it to interact with a variety of target proteins, including the cytoskeletal proteins tubulin and glial fibrillary acidic protein. In both cases, S100B promotes the in vitro disassembly of these proteins in a calcium-sensitive manner. Despite this, there is little in vivo evidence for the interaction of proteins such as tubulin with S100B. To probe these interactions, we studied the expression of human S100B in Escherichia coli and its interaction with the prokaryotic ancestor of tubulin, FtsZ, the major protein involved in bacterial division. Expression of S100B protein in E. coli results in little change in FtsZ protein levels, causes a filamenting bacterial phenotype characteristic of FtsZ inhibition, and leads to missed rounds of cell division. Further, S100B localizes to positions similar to those of FtsZ in bacterial filaments: the small foci at the poles, the mid-cell positions, and between the nucleoids at regular intervals. Calcium-dependent physical interaction between S100B and FtsZ was demonstrated in vitro by affinity chromatography, and this interaction was severely inhibited by the competitor peptide TRTK-12. Together these results indicate that S100B interacts with the tubulin homologue FtsZ in vivo, modulating its activity in bacterial cell division. This approach will present an important step for the study of S100 protein interactions in vivo. S100B is a small, dimeric EF-hand calcium-binding protein abundant in vertebrates. Upon calcium binding, S100B undergoes a conformational change allowing it to interact with a variety of target proteins, including the cytoskeletal proteins tubulin and glial fibrillary acidic protein. In both cases, S100B promotes the in vitro disassembly of these proteins in a calcium-sensitive manner. Despite this, there is little in vivo evidence for the interaction of proteins such as tubulin with S100B. To probe these interactions, we studied the expression of human S100B in Escherichia coli and its interaction with the prokaryotic ancestor of tubulin, FtsZ, the major protein involved in bacterial division. Expression of S100B protein in E. coli results in little change in FtsZ protein levels, causes a filamenting bacterial phenotype characteristic of FtsZ inhibition, and leads to missed rounds of cell division. Further, S100B localizes to positions similar to those of FtsZ in bacterial filaments: the small foci at the poles, the mid-cell positions, and between the nucleoids at regular intervals. Calcium-dependent physical interaction between S100B and FtsZ was demonstrated in vitro by affinity chromatography, and this interaction was severely inhibited by the competitor peptide TRTK-12. Together these results indicate that S100B interacts with the tubulin homologue FtsZ in vivo, modulating its activity in bacterial cell division. This approach will present an important step for the study of S100 protein interactions in vivo. S100B is one of more than 20 known members of the small (9–12 kDa), acidic S100 family of EF-hand calcium-binding proteins, which are expressed in vertebrates, generally in a tissue-specific manner (reviewed in Ref. 1Donato R. Int. J. Biochem. Cell Biol. 2001; 33: 637-668Google Scholar). Most of these proteins form homo- and heterodimers that respond to signal-induced increases in intracellular calcium levels. Upon binding calcium, these proteins undergo conformational changes that allow them to bind to target proteins and modulate their activity. S100B is abundantly expressed in glial cells, where its best characterized roles involve modulating protein-protein interactions of all three classes of cytoskeletal structures. The assembly/disassembly of microtubules can be controlled by S100B through its interactions with tubulin (2Reeves R.H. Yao J. Crowley M.R. Buck S. Zhang X. Yarowsky P. Gearhart J.D. Hilt D.C. Proc. Natl. Acad. Sci. U. S. A. 1994; 91: 5359-5363Google Scholar, 3Sorci G. Agneletti A.L. Bianchi R. Donato R. Biochim. Biophys. Acta. 1998; 1448: 277-289Google Scholar, 4Sorci G. Agneletti A.L. Donato R. Neuroscience. 2000; 99: 773-783Google Scholar) and the microtubule-associated protein, tau (5Baudier J. Cole R.D. J. Biol. Chem. 1988; 263: 5876-5883Google Scholar). In addition, S100B can regulate the dynamics of intermediate filaments through its interactions with the glial fibrillary acidic protein, vimentin (3Sorci G. Agneletti A.L. Bianchi R. Donato R. Biochim. Biophys. Acta. 1998; 1448: 277-289Google Scholar, 6Ziegler D.R. Innocente C.E. Leal R.B. Rodnight R. Goncalves C.A. Neurochem. Res. 1998; 23: 1259-1263Google Scholar), and annexin VI (7Garbuglia M. Verzini M. Donato R. Cell Calcium. 1998; 24: 177-191Google Scholar, 8Garbuglia M. Verzini M. Hofmann A. Huber R. Donato R. Biochim. Biophys. Acta. 2000; 1498: 192-206Google Scholar). The S100B-mediated regulation of microfilaments has been suggested based on calcium-dependent in vitro interactions with the actin capping protein, CapZα (9Kilby P.M. Van Eldik L.J. Roberts G.C. Protein Sci. 1997; 6: 2494-2503Google Scholar), and by disruption of the interactions of F-actin with caldesmon (10Fujii T. Machino K. Andoh H. Satoh T. Kondo Y. J. Biochem. (Tokyo). 1990; 107: 133-137Google Scholar) and calponin (11Fujii T. Oomatsuzawa A. Kuzumaki N. Kondo Y. J. Biochem. (Tokyo). 1994; 116: 121-127Google Scholar). S100B has been implicated in the calcium-dependent binding of at least 20 target proteins in mammals (1Donato R. Int. J. Biochem. Cell Biol. 2001; 33: 637-668Google Scholar). However, because many of these target proteins have been identified only by in vitro methods, they require identification in vivo and a rationale for physiological relevance. In many cases, the S100B recognition site on putative targets has been characterized by the peptide chemical pattern +OXO*XOO (+ = basic, O = hydrophobic, * = hydrophilic, X = variable) which is found in the strong competitor peptide TRTKIDWNKILS (TRTK-12) (12Ivanenkov V.V. Jamieson Jr., G.A. Gruenstein E. Dimlich R.V. J. Biol. Chem. 1995; 270: 14651-14658Google Scholar, 13McClintock K.A. Shaw G.S. Protein Sci. 2000; 9: 2043-2046Google Scholar). During our study of the mechanism(s) by which S100B recognizes its target proteins, we observed that human S100B expressed in bacteria causes a filamentation phenotype, which is likely the result of a specific interaction with one or more bacterial proteins. Our initial candidate was the protein FtsZ, the evolutionary precursor to tubulin. FtsZ is required for the division of bacteria, archaea, chloroplasts, and the mitochondria of some algae (14Beech P.L. Nheu T. Schultz T. Herbert S. Lithgow T. Gilson P.R. McFadden G.I. Science. 2000; 287: 1276-1279Google Scholar, 15Erickson H.P. J. Cell Biol. 2000; 148: 1103-1105Google Scholar, 16Kiessling J. Kruse S. Rensing S.A. Harter K. Decker E.L. Reski R. J. Cell Biol. 2000; 151: 945-950Google Scholar, 17Lutkenhaus J. Curr. Biol. 1998; 8: R619-R621Google Scholar, 18Margolin W. Curr. Biol. 2000; 10: R328-R330Google Scholar, 19Margolin W. Wang R. Kumar M. J. Bacteriol. 1996; 178: 1320-1327Google Scholar, 20Martin W. Science. 2000; 2871219Google Scholar, 21Takahara M. Takahashi H. Matsunaga S. Miyagishima S. Takano H. Sakai A. Kawano S. Kuroiwa T. Mol. Gen. Genet. 2000; 264: 452-460Google Scholar, 22van den Ent F. Amos L.A. Lowe J. Nature. 2001; 413: 39-44Google Scholar, 23Vitha S. McAndrew R.S. Osteryoung K.W. J. Cell Biol. 2001; 153: 111-119Google Scholar). When FtsZ is nonfunctional or under-expressed, bacteria form long filaments lacking signs of invagination at the division sites (24Begg K.J. Donachie W.D. J. Bacteriol. 1985; 163: 615-622Google Scholar, 25Dai K. Lutkenhaus J. J. Bacteriol. 1991; 173: 3500-3506Google Scholar, 26Ma X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar). Multinuclear filaments can also be formed when FtsZ is over-expressed (27Ward Jr., J.E. Lutkenhaus J. Cell. 1985; 42: 941-949Google Scholar) or misdirected to secondary division sites by defects in the proteins of the minB locus (28de Boer P.A.J. Crossley R.E. Rothfield L.I. Cell. 1989; 56: 641-649Google Scholar). However, this phenotype is characterized by the additional presence of anucleate mini-cells, which are not observed when FtsZ is dysfunctional or under-expressed. Evidence that FtsZ is the evolutionary precursor to tubulin (reviewed in Ref. 29Addinall S.G. Holland B. J. Mol. Biol. 2002; 318: 219-236Google Scholar) includes their similar GTPase sequence motifs, enzymatic activities (30de Boer P. Crossley R. Rothfield L. Nature. 1992; 359: 254-256Google Scholar, 31Raychaudhuri D. Park J.T. Nature. 1992; 359: 251-254Google Scholar, 32Nogales E. Downing K.H. Amos L.A. Lowe J. Nat. Struct. Biol. 1998; 5: 451-458Google Scholar), and three-dimensional structures (32Nogales E. Downing K.H. Amos L.A. Lowe J. Nat. Struct. Biol. 1998; 5: 451-458Google Scholar, 33Lowe J. Amos L.A. Nature. 1998; 391: 203-206Google Scholar, 34Lowe J. J. Struct. Biol. 1998; 124: 235-243Google Scholar). As well, bacterial FtsZ in vitro can form structures resembling protofilaments, rings, and tubes, similar to those formed by tubulin (35Lowe J. Amos L.A. EMBO J. 1999; 18: 2364-2371Google Scholar, 36Lowe J. Amos L.A. J. Biol. Chem. 2000; 381: 993-999Google Scholar, 37Lu M. H.P. J. Bacteriol. 2000; Scholar, A. Lutkenhaus J. J. Bacteriol. 1994; Scholar). is a of FtsZ that the as the step in bacterial J. H.P. Cell 1998; Scholar, H.P. 1998; Scholar). This FtsZ the which at least proteins and to form the division J. Mol. 2001; 42: Scholar, C.A. Boer J. Bacteriol. 2002; Scholar, N. N. D. J. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: Scholar, S. Lutkenhaus J. EMBO J. 2002; Scholar). FtsZ the that causes and of the cells, or it the which the will be M. H.P. J. Bacteriol. 2000; Scholar). The proteins and which bind to FtsZ of are not required for of the FtsZ they the and proteins to the division site S. Lutkenhaus J. EMBO J. 2002; Scholar, C.A. Boer J. Bacteriol. 2000; Scholar). In a to tubulin is the bacterial homologue of the microtubule-associated protein, C.A. Boer J. Bacteriol. 2000; Scholar, D. EMBO J. 1999; 18: Scholar, H.P. Curr. Cell Biol. 2001; Scholar), with the protein is a homologue of actin den Ent F. Amos L.A. Lowe J. Nature. 2001; 413: 39-44Google Scholar, den Ent F. Lowe J. EMBO J. 2000; Scholar, J. P. M. J. Struct. Biol. 2001; Scholar). the between the bacterial cytoskeletal proteins to those of have more the of The identification of in vivo protein interactions with the calcium-binding protein and many of the S100 proteins, has the interactions are and by calcium, such as have to target proteins J. Res. Scholar). The is which not bind calcium and undergoes a interaction with the protein annexin M. 2000; Scholar). Further, the sequence of the In addition, of the S100 proteins, including and have the to form S100 in vivo, protein interaction because interactions can in with homo- or S100 the S100 proteins are to vertebrates, one of protein interactions and of these proteins is through the of a In this Escherichia coli is because the of many of the S100B proteins, those involved in cytoskeletal all S100 protein protein interactions and their on in E. coli can be studied for S100B S100 proteins. In this we present in vivo and in vitro evidence the physical interaction between the calcium-binding protein S100B and the cytoskeletal tubulin homologue FtsZ found in E. This interaction with bacterial a phenotype as a result of missed rounds of cell division. and S100B protein with a and FtsZ proteins expressed in E. coli a of H. T. Res. Scholar). S100B a of was by the of site a of expression Shaw G.S. 1996; Scholar) to have a site the S100B The protein has a between the S100B and was by the with and the Most of the S100B protein is for the of to the of by the The E. coli FtsZ was by as based on the FtsZ sequence in G. C.A. M. J. J.D. J. A. B. Y. Science. 1997; Scholar) to and sites for for This was also to an site of the site for of the FtsZ expression by of the S100B in with the FtsZ by proteins by Protein was as Shaw G.S. 1996; Scholar, P.L. Shaw G.S. 2002; Scholar). required a in the in which a of was for FtsZ was as by and Lutkenhaus A. Lutkenhaus J. 1998; Scholar). E. coli in of with to an of and with for and at by and the FtsZ protein was in and FtsZ protein was based on presence of was by a of a E. coli Expression Scholar). or FtsZ expression in 20 of with to an of with for in of and at in the presence of 20 and by The was as a cell The was at for at and of the was to a the was and the was in of the of was with for the S100B in this, bacteria to and to an = Protein expression was by to of 20 and In of bacteria at to in bacteria at and at for that or for to with change in or also by in and at The bacteria in and at with to the bacterial on with a of on as by and Lutkenhaus A. Lutkenhaus J. 1998; Scholar). as the secondary a on a with a and S100B was to a to the The was with to the FtsZ protein. with of the in which of for protein was with the peptide binding peptide was at in and the and with to proteins the S100B affinity with and for and as P.L. 1997; 18: Scholar). To FtsZ expression to of of bacterial in a and in of for and The proteins with by W. and by of E. coli in this study is of the in of its When in the bacteria have a of and in between and on their in the division human S100B expression by causes a filamenting phenotype in the bacteria which is also observed at of for expression of S100B and and The protein, which of S100B to not the filamenting phenotype at and the is in the the is a This result is with of the bacterial X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar). of the signs of with However, the there are bacteria of the that some or some bacteria have been of the because of its The filamentation by S100B and is similar to that observed when FtsZ is dysfunctional or (24Begg K.J. Donachie W.D. J. Bacteriol. 1985; 163: 615-622Google Scholar, 25Dai K. Lutkenhaus J. J. Bacteriol. 1991; 173: 3500-3506Google Scholar, 26Ma X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar), including the presence of some This that S100B the tubulin FtsZ, and with its the in vivo interaction between S100B and FtsZ, the intracellular of S100B was by the protein. the of to is the expression of the protein Margolin W. J. Bacteriol. 1998; Scholar). this in and because we to the of the for with of there is a between expression and the of the filamenting phenotype with a of with a of to and than In the the foci of at the and the with a of and nucleoids The the protein foci to the and that the cell This pattern filaments is similar to that observed by of FtsZ dynamics and Margolin W. J. Bacteriol. 1998; Scholar, S.G. Lutkenhaus J. J. Bacteriol. 1997; Scholar, Margolin W. J. Bacteriol. 2001; Scholar, J. Bacteriol. 2001; Scholar) and in the protein in Ref. 26Ma X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar). The of is with FtsZ to bacterial X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar, Jr., J.E. Lutkenhaus J. Cell. 1985; 42: 941-949Google Scholar). The pattern of expression at an because in a small of the bacteria, expression of the protein the strong results in small, foci at one or both of the cells, with mid-cell in that are long to be of at all of between the foci not foci more and the bacterial Further, protein structures bacteria can be observed by of and The foci of the in are by and the pattern is that formed by FtsZ over-expressed in the expression of S100B with 20 results in bacteria with mid-cell by S100B to mid-cell to a cell with a the between bacteria in a division is also with of the of evidence of and FtsZ is the that in some bacteria structures are because of the of the structures are similar to those FtsZ that are formed in E. coli X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar, Margolin W. J. Bacteriol. 1998; Scholar, S.G. Lutkenhaus J. Mol. 1996; Scholar, J. P. H.P. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: Scholar, S. H.P. J. Bacteriol. Scholar) and S. R. Cell. 2002; Scholar), S100B and FtsZ similar in the S100B in the bacteria was by bacteria with and a secondary The bacteria by of to allow for bacterial division to and to have a of bacterial The structures observed in bacteria are not the result of the because similar are by the of bacteria S100B a of bacteria a mid-cell with S100B at the In some of cell is observed in the between the of of FtsZ in E. coli have been to be between J. M. P. M. M. Mol. 1991; 5: Scholar) and H.P. 1998; Scholar), with little the division S.G. Holland B. J. Mol. Biol. 2002; 318: 219-236Google Scholar, M. T. J. M. EMBO J. 1990; 9: Scholar, T. M. P. M. M. EMBO J. Scholar). of FtsZ causes A. Lutkenhaus J. 1998; Scholar) or the phenotype of and filamentation (27Ward Jr., J.E. Lutkenhaus J. Cell. 1985; 42: 941-949Google Scholar), of FtsZ results in filamentation only K. Lutkenhaus J. J. 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Scholar). we for the presence of of with evidence for S100B and was found in the and cell of S100B and found in the and of FtsZ and binding of S100B to a target protein such as tubulin is of calcium to S100B a conformational change in required for protein interactions Shaw G.S. 1998; 6: Scholar). The interaction between FtsZ and S100B was characterized by an affinity to which S100B been of FtsZ protein in calcium was the S100B affinity and with calcium The FtsZ on the in the and there was FtsZ by The FtsZ by the was in the of FtsZ is in of When the S100B affinity was with which and the S100B target recognition all of the FtsZ in the and and protein to be by This result FtsZ binding is calcium-dependent and specific to the site on S100B. The expression of human S100B in E. coli causes a filamenting phenotype lacking at division sites in the This phenotype that observed when FtsZ is dysfunctional or not expressed (24Begg K.J. Donachie W.D. J. Bacteriol. 1985; 163: 615-622Google Scholar, 25Dai K. Lutkenhaus J. J. Bacteriol. 1991; 173: 3500-3506Google Scholar, 26Ma X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar). with this, S100B has little on the FtsZ expression and is to bind in a calcium-sensitive manner to indicate the interaction between S100B and FtsZ the filamentation phenotype, likely because of an of FtsZ of S100B with FtsZ is by its intracellular of bacteria of S100B a at mid-cell that the pattern of FtsZ in bacteria X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar, S.G. Lutkenhaus J. J. Bacteriol. 1997; Scholar), including in cells, as observed S.G. Lutkenhaus J. J. Bacteriol. 1997; Scholar). that at levels, filamentation because S100B with FtsZ the of in FtsZ at the of the and to the cell as a S.G. Lutkenhaus J. Mol. 1996; Scholar). When FtsZ is the FtsZ in the can the protein and sites at the cell and at an to for on X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar). The of FtsZ and is with that FtsZ has an affinity for a that the of proteins is for (28de Boer P.A.J. Crossley R.E. Rothfield L.I. Cell. 1989; 56: 641-649Google Scholar). be at the a the of some of the FtsZ The of S100B and to FtsZ is by the of structures in a small of are known to FtsZ because they have been observed for of FtsZ S.G. Lutkenhaus J. Mol. 1996; Scholar, S. H.P. J. Bacteriol. Scholar), with to FtsZ and proteins X. Ehrhardt D.W. Margolin W. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 12998-13003Google Scholar, J. P. H.P. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: Scholar), in E. coli FtsZ S. Lutkenhaus J. EMBO J. 2002; Scholar) and in E. coli with E. Margolin W. W. J. Bacteriol. 1998; Scholar). In our the structures are because of the S100B is with the the interaction between S100B and FtsZ is specific and This is with the S100B calcium-dependent target recognition because the interaction is inhibited by the characterized target peptide TRTK-12. This which has the affinity for S100B of known target K.A. Van Eldik L.J. Shaw G.S. 2002; Scholar), a for that is in cytoskeletal proteins including tubulin, glial fibrillary acidic protein, and vimentin K.A. Shaw G.S. Protein Sci. 2000; 9: 2043-2046Google Scholar). Further, S100B and both the filamenting phenotype and similar that the not with the in S100B at its and K.A. Van Eldik L.J. Shaw G.S. 2002; Scholar). have that the with S100B causes or of L. and G. S. The of in E. coli S100B calcium and undergoes a conformational change in to increases in intracellular calcium the of to In this the calcium-dependent binding of FtsZ to S100B is with the known of S100B In bacteria, the of S100B with FtsZ and the filamentation that S100B is at least a because the of E. coli increases in calcium the P. Biol. Res. 1988; Scholar). calcium has been suggested to of the cell in a manner similar to that observed in S. Holland J. Biol. 1988; Scholar, Cell Calcium. 1989; 10: Scholar, A. 1999; Scholar). This is by in calcium FtsZ (35Lowe J. Amos L.A. EMBO J. 1999; 18: 2364-2371Google Scholar) and the of structures M. H.P. J. Bacteriol. 2000; Scholar, Margolin W. EMBO J. 1997; Scholar, A. Lutkenhaus J. J. Bacteriol. 1999; Scholar), and its GTPase activity Margolin W. EMBO J. 1997; Scholar). In addition, the of calcium-binding proteins in (reviewed in Ref. J. J. J. 2002; 10: Scholar), including EF-hand proteins, that calcium in bacteria be an important of modulating protein including cytoskeletal and S100B be a probe to our of calcium in between FtsZ and tubulin has the to form microtubules and interact with proteins. In vitro that the of tubulin is inhibited by the protein a protein that is to (1Donato R. Int. J. Biochem. Cell Biol. 2001; 33: 637-668Google Scholar). The of FtsZ and its interactions with proteins is The of tubulin FtsZ is by their and of proteins have the site in E. coli FtsZ, in human in the between and (32Nogales E. Downing K.H. Amos L.A. Lowe J. Nat. Struct. Biol. 1998; 5: 451-458Google Scholar, 33Lowe J. Amos L.A. Nature. 1998; 391: 203-206Google Scholar, H.P. Cell. 1995; Scholar) and a of GTPase activity E. S.G. Downing K.H. Nature. 1998; 391: Scholar) that a the between and in both FtsZ and tubulin. The interacts with the in the the and the GTPase activity M.R. P. K.H. 1999; Scholar, den T. 2002; Scholar). the between FtsZ are to of the FtsZ of the of FtsZ and tubulin has the sequence in the as as the of that be at the FtsZ or tubulin (32Nogales E. Downing K.H. Amos L.A. Lowe J. Nat. Struct. Biol. 1998; 5: 451-458Google Scholar). be that S100B interaction with tubulin, and by FtsZ, this site and to an of The that the target peptide can with FtsZ for S100B binding in a calcium-sensitive manner. is to with the of S100B for the of microtubules and intermediate filaments G. Agneletti A.L. Donato R. Neuroscience. 2000; 99: 773-783Google Scholar). these results that FtsZ, tubulin, interact with S100B a a of the recognition the in both FtsZ and tubulin is to of protofilaments, it that the recognition sequence in or this In tubulin, one candidate sequence K.A. Shaw G.S. Protein Sci. 2000; 9: 2043-2046Google Scholar), the similar sequence in FtsZ is found at the of to the indicate in S100B be with a the and that with is to this that of FtsZ have be to of the mid-cell as the step for cell division J. H.P. Cell 1998; Scholar, H.P. 1998; Scholar). S100B be with FtsZ on a for the between FtsZ to form the or for of protein. has been that there is to proteins involved in site or N. N. D. J. Proc. Natl. Acad. Sci. U. S. A. 2002; 99: Scholar). a protein such as S100B to FtsZ has an in that it can be with FtsZ in vivo and the of S100B can be to the on have expressed S100B at to filamentation and to the mid-cell to FtsZ and proteins of the as have been in have some such as or in protein-protein and Margolin Margolin W. J. Bacteriol. 1998; Scholar) found to be in vivo only when expressed at levels, where it form with S100B protein as a to study bacterial division the of proteins. of and of for the of and Margolin of and of for of are also to of for with

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