Applied Microbiology and Biotechnology

, Volume 73, Issue 1, pp 37–47 | Cite as

The prokaryotic cytoskeleton: a putative target for inhibitors and antibiotics?

  • Waldemar VollmerEmail author


In the recent decade, our view on the organization of the bacterial cell has been revolutionized by the identification of cytoskeletal elements. Most bacterial species have structural homologs of actin and tubulin that assemble into dynamic, filamentous structures at precisely defined sub-cellular locations. The essential cell division protein FtsZ forms a dynamic ring at mid-cell and is similar in its structure to tubulin. Proteins of the MreB family, which are structural homologs of actin, assemble into helical or straight filaments in the bacterial cytoplasm. As in eukaryotic cells, the bacterial cytoskeleton drives essential cellular processes such as cell division, cell wall growth, DNA movement, protein targeting, and alignment of organelles. Different high-throughput assays have been developed to search for inhibitors of components of the bacterial cytoskeleton. Cell-based assays for the detection of cell division inhibitors as well as FtsZ GTPase assays led to the identification of several compounds that inhibit the polymerization of FtsZ, by this blocking bacterial cell division. Such inhibitors might not only be valuable tools for basic research, but might also lead to novel therapeutic agents against pathogenic bacteria. For example, the polyphenol dichamanetin, the 2-alkoxycarbonylaminopyridine SRI-3072, and the benzophenanthridine alkaloid sanguinarine inhibit the GTPase activity of FtsZ and exhibit antimicrobial activity.


cytoskeleton cell division cell wall DNA segregation 



I thank Petra Born for her critical reading of the manuscript, and the European Commission (LSHM-CT-2004-512138) and the 'Deutsche Forschungsgemeinschaft' (FOR 449) for their support.


  1. Addinall SG, Holland B (2002) The tubulin ancestor, FtsZ, draughtsman, designer and driving force for bacterial cytokinesis. J Mol Biol 318:219–236PubMedGoogle Scholar
  2. Anderson DE, Gueiros-Filho FJ, Erickson HP (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J Bacteriol 186:5775–5781PubMedPubMedCentralGoogle Scholar
  3. Ausmees N, Kuhn JR, Jacobs-Wagner C (2003) The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115:705–713PubMedGoogle Scholar
  4. Beck BD, Arscott PG, Jacobson A (1978) Novel properties of bacterial elongation factor Tu. Proc Natl Acad Sci USA 75:1250–1254PubMedGoogle Scholar
  5. Bermudes D, Hinkle G, Margulis L (1994) Do prokaryotes contain microtubules? Microbiol Rev 58:387–400PubMedPubMedCentralGoogle Scholar
  6. Bernhardt TG, de Boer PA (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18:555–564PubMedPubMedCentralGoogle Scholar
  7. Beuria TK, Santra MK, Panda D (2005) Sanguinarine blocks cytokinesis in bacteria by inhibiting FtsZ assembly and bundling. Biochemistry 44:16584–16593PubMedGoogle Scholar
  8. Bhavsar AP, Brown ED (2006) Cell wall assembly in Bacillus subtilis: how spirals and spaces challenge paradigms. Mol Microbiol 60:1077–1090PubMedGoogle Scholar
  9. Bi E, Lutkenhaus J (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354:161–164PubMedPubMedCentralGoogle Scholar
  10. Bork P, Sander C, Valencia A (1992) An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc Natl Acad Sci USA 89:7290–7294PubMedGoogle Scholar
  11. Brown ED, Wright GD (2005) New targets and screening approaches in antimicrobial drug discovery. Chem Rev 105:759–774PubMedGoogle Scholar
  12. Carballido-Lopez R, Errington J (2003) The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev Cell 4:19–28PubMedGoogle Scholar
  13. Carettoni D, Gomez-Puertas P, Yim L, Mingorance J, Massidda O, Vicente M, Valencia A, Domenici E, Anderluzzi D (2003) Phage-display and correlated mutations identify an essential region of subdomain 1C involved in homodimerization of Escherichia coli FtsA. Proteins 50:192–206PubMedGoogle Scholar
  14. Cordell SC, Robinson EJ, Löwe J (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci USA 100:7889–7894PubMedGoogle Scholar
  15. Daniel RA, Errington J (2003) Control of cell morphogenesis in bacteria: two distinct ways to make a rod-shaped cell. Cell 113:767–776PubMedGoogle Scholar
  16. de Boer PA, Crossley RE, Rothfield LI (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:641–649PubMedGoogle Scholar
  17. Defeu Soufo HJ, Graumann PL (2005) Bacillus subtilis actin-like protein MreB influences the positioning of the replication machinery and requires membrane proteins MreC/D and other actin-like proteins for proper localization. BMC Cell Biol 6:10PubMedPubMedCentralGoogle Scholar
  18. Del Sol R, Mullins JG, Grantcharova N, Flardh K, Dyson P (2006) Influence of CrgA on assembly of the cell division protein FtsZ during development of Streptomyces coelicolor. J Bacteriol 188:1540–1550PubMedPubMedCentralGoogle Scholar
  19. Divakaruni AV, Loo RR, Xie Y, Loo JA, Gober JW (2005) The cell-shape protein MreC interacts with extracytoplasmic proteins including cell wall assembly complexes in Caulobacter crescentus. Proc Natl Acad Sci USA 102:18602–18607PubMedGoogle Scholar
  20. Dye NA, Pincus Z, Theriot JA, Shapiro L, Gitai Z (2005) Two independent spiral structures control cell shape in Caulobacter. Proc Natl Acad Sci USA 102:18608–18613PubMedGoogle Scholar
  21. Erickson HP (2001) Cytoskeleton. Evolution in bacteria. Nature 413:30PubMedGoogle Scholar
  22. Errington J (2003) Dynamic proteins and a cytoskeleton in bacteria. Nat Cell Biol 5:175–178PubMedGoogle Scholar
  23. Errington J, Daniel RA, Scheffers DJ (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67:52–65PubMedPubMedCentralGoogle Scholar
  24. Espeli O, Nurse P, Levine C, Lee C, Marians KJ (2003) SetB: an integral membrane protein that affects chromosome segregation in Escherichia coli. Mol Microbiol 50:495–509PubMedGoogle Scholar
  25. Esue O, Cordero M, Wirtz D, Tseng Y (2005) The assembly of MreB, a prokaryotic homolog of actin. J Biol Chem 280:2628–2635PubMedGoogle Scholar
  26. Esue O, Wirtz D, Tseng Y (2006) GTPase activity, structure, and mechanical properties of filaments assembled from bacterial cytoskeleton protein MreB. J Bacteriol 188:968–976PubMedPubMedCentralGoogle Scholar
  27. Feucht A, Lucet I, Yudkin MD, Errington J (2001) Cytological and biochemical characterization of the FtsA cell division protein of Bacillus subtilis. Mol Microbiol 40:115–125PubMedGoogle Scholar
  28. Figge RM, Divakaruni AV, Gober JW (2004) MreB, the cell shape-determining bacterial actin homologue, co-ordinates cell wall morphogenesis in Caulobacter crescentus. Mol Microbiol 51:1321–1332PubMedGoogle Scholar
  29. Gerdes K, Moller-Jensen J, Ebersbach G, Kruse T, Nordstrom K (2004) Bacterial mitotic machineries. Cell 116:359–366PubMedGoogle Scholar
  30. Gitai Z (2005) The new bacterial cell biology: moving parts and subcellular architecture. Cell 120:577–586PubMedGoogle Scholar
  31. Gitai Z, Dye N, Shapiro L (2004) An actin-like gene can determine cell polarity in bacteria. Proc Natl Acad Sci USA 101:8643–8648PubMedGoogle Scholar
  32. Gitai Z, Dye NA, Reisenauer A, Wachi M, Shapiro L (2005) MreB actin-mediated segregation of a specific region of a bacterial chromosome. Cell 120:329–341PubMedGoogle Scholar
  33. Graumann PL (2004) Cytoskeletal elements in bacteria. Curr Opin Microbiol 7:565–571PubMedGoogle Scholar
  34. Graumann PL, Soufo HJD (2004) An intracellular actin motor in bacteria? BioEssays 26:1209–1216PubMedGoogle Scholar
  35. Gueiros-Filho FJ, Losick R (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16:2544–2556PubMedPubMedCentralGoogle Scholar
  36. Hamoen LW, Meile JC, de Jong W, Noirot P, Errington J (2006) SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol Microbiol 59:989–999PubMedGoogle Scholar
  37. Haselbeck R, Wall D, Jiang B, Ketela T, Zyskind J, Bussey H, Foulkes JG, Roemer T (2002) Comprehensive essential gene identification as a platform for novel antiinfective drug discovery. Curr Pharm Des 8:1155–1172PubMedGoogle Scholar
  38. Higashitani A, Higashitani N, Horiuchi K (1995) A cell division inhibitor SulA of Escherichia coli directly interacts with FtsZ through GTP hydrolysis. Biochem Biophys Res Commun 209:198–204PubMedGoogle Scholar
  39. Höltje JV (1998) Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol Mol Biol Rev 62:181–203PubMedPubMedCentralGoogle Scholar
  40. Huang Q, Kirikae F, Kirikae T, Pepe A, Amin A, Respicio L, Slayden RA, Tonge, PJ, Ojima I (2006) Targeting FtsZ for antituberculosis drug discovery: Noncytotoxic taxanes as novel antituberculosis agents. J Med Chem 49:463–466PubMedPubMedCentralGoogle Scholar
  41. Ishikawa S, Kawai Y, Hiramatsu K, Kuwano M, Ogasawara N (2006) A new FtsZ-interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis. Mol Microbiol 60:1364–1380PubMedGoogle Scholar
  42. Iwai N, Nagai K, Wachi M (2002) Novel S-bezylsiothiourea compound that induces spherical cells in Escherichia coli probably by acting on a rod-shaped-determining protein(s) other than penicillin-binding protein 2. Biosci Biotechnol Biochem 66:2658–2662PubMedGoogle Scholar
  43. Jennings LD, Foreman KW, Rush TS, Tsao DH, Mosyak L, Kincaid SL, Sukhdeo MN, Sutherland AG, Ding W, Kenny CH, Sabus CL, Liu H, Dushin EG, Moghazeh SL, Labthavikul P, Petersen PJ, Tuckman M, Haney SA, Ruzin AV (2004a) Combinatorial synthesis of substituted 3-(2-indolyl)piperidines and 2-phenyl indoles as inhibitors of ZipA–FtsZ interaction. Bioorg Med Chem 12:5115–5131PubMedGoogle Scholar
  44. Jennings LD, Foreman KW, Rush TS, Tsao DH, Mosyak L, Li Y, Sukhdeo MN, Ding W, Dushin EG, Kenny CH, Moghazeh SL, Petersen PJ, Ruzin AV, Tuckman M, Sutherland AG (2004b) Design and synthesis of indolo[2,3-a]quinolizin-7-one inhibitors of the ZipA–FtsZ interaction. Bioorg Med Chem Lett 14:1427–1431PubMedGoogle Scholar
  45. Kawai Y, Ogasawara N (2006) Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152:1129–1141PubMedGoogle Scholar
  46. Kawai Y, Moriya S, Ogasawara N (2003) Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol Microbiol 47:1113–1122PubMedGoogle Scholar
  47. Kenny CH, Ding W, Kelleher K, Benard S, Dushin EG, Sutherland AG, Mosyak L, Kriz R, Ellestad G (2003) Development of a fluorescence polarization assay to screen for inhibitors of the FtsZ/ZipA interaction. Anal Biochem 323:224–233PubMedGoogle Scholar
  48. Komeili A, Li Z, Newman DK, Jensen GJ (2006) Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311:242–245PubMedGoogle Scholar
  49. Kruse T, Bork-Jensen J, Gerdes K (2005) The morphogenetic MreBCD proteins of Escherichia coli form an essential membrane-bound complex. Mol Microbiol 55:78–89PubMedGoogle Scholar
  50. Kruse T, Blagoev B, Lobner-Olesen A, Wachi M, Sasaki K, Iwai N, Mann M, Gerdes K (2006) Actin homolog MreB and RNA polymerase interact and are both required for chromosome segregation in Escherichia coli. Genes Dev 20:113–124PubMedPubMedCentralGoogle Scholar
  51. Lappchen T, Hartog AF, Pinas VA, Koomen GJ, den Blaauwen T (2005) GTP analogue inhibits polymerization and GTPase activity of the bacterial protein FtsZ without affecting its eukaryotic homologue tubulin. Biochemistry 44:7879–7884PubMedGoogle Scholar
  52. Lara B, Rico AI, Petruzzelli S, Santona A, Dumas J, Biton J, Vicente M, Mingorance J, Massidda O (2005) Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol Microbiol 55:699–711PubMedGoogle Scholar
  53. Leonard TA, Butler PJ, Löwe J (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer—a conserved biological switch. EMBO J 24:270–282PubMedPubMedCentralGoogle Scholar
  54. Levin PA, Kurtser IG, Grossman AD (1999) Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc Natl Acad Sci USA 96:9642–9647PubMedGoogle Scholar
  55. Lewis PJ (2004) Bacterial subcellular architecture: recent advances and future prospects. Mol Microbiol 54:1135–1150PubMedGoogle Scholar
  56. Löwe J, Amos LA (1998) Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203–206PubMedGoogle Scholar
  57. Löwe J, van den Ent F, Amos LA (2004) Molecules of the bacterial cytoskeleton. Annu Rev Biophys Biomol Struct 33:177–198PubMedGoogle Scholar
  58. Lutkenhaus J, Sundaramoorthy M (2003) MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol Microbiol 48:295–303PubMedGoogle Scholar
  59. Margalit DN, Romberg L, Mets RB, Hebert AM, Mitchison TJ, Kirschner MW, RayChaudhuri D (2004) Targeting cell division: small-molecule inhibitors of FtsZ GTPase perturb cytokinetic ring assembly and induce bacterial lethality. Proc Natl Acad Sci USA 101:11821–11826PubMedGoogle Scholar
  60. Margolin W (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6:862–871PubMedPubMedCentralGoogle Scholar
  61. Mayer F (2003) Cytoskeletons in prokaryotes. Cell Biol Int 27:429–438PubMedGoogle Scholar
  62. Mazza P, Noens EE, Schirner K, Grantcharova N, Mommaas AM, Koerten HK, Muth G, Flardh K, van Wezel GP, Wohlleben W (2006) MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol Microbiol 60:838–852PubMedGoogle Scholar
  63. Michie KA, Löwe J (2006) Dynamic filaments of the bacterial cytoskeleton. Ann Rev Biochem 75:467–492PubMedGoogle Scholar
  64. Moller-Jensen J, Jensen RB, Löwe J, Gerdes K (2002) Prokaryotic DNA segregation by an actin-like filament. EMBO J 21:3119–3127PubMedPubMedCentralGoogle Scholar
  65. Moreira IS, Fernandes PA, Ramos MJ (2006) Detailed microscopic study of the full zipA:FtsZ interface. Proteins 63:811–821PubMedGoogle Scholar
  66. Mosyak L, Zhang Y, Glasfeld E, Haney S, Stahl M, Seehra J, Somers WS (2000) The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 19:3179–3191PubMedPubMedCentralGoogle Scholar
  67. Moy FJ, Glasfeld E, Mosyak L, Powers R (2000) Solution structure of ZipA, a crucial component of Escherichia coli cell division. Biochemistry 39:9146–9156PubMedGoogle Scholar
  68. Mukherjee A, Cao C, Lutkenhaus J (1998) Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichia coli. Proc Natl Acad Sci USA 95:2885–2890PubMedGoogle Scholar
  69. Nilsen T, Yan AW, Gale G, Goldberg MB (2005) Presence of multiple sites containing polar material in spherical Escherichia coli cells that lack MreB. J Bacteriol 187:6187–6196PubMedPubMedCentralGoogle Scholar
  70. Ohashi Y, Chijiiwa Y, Suzuki K, Takahashi K, Nanamiya H, Sato T, Hosoya Y, Ochi K, Kawamura F (1999) The lethal effect of a benzamide derivative, 3-methoxybenzamide, can be suppressed by mutations within a cell division gene, ftsZ, in Bacillus subtilis. J Bacteriol 181:1348–1351PubMedPubMedCentralGoogle Scholar
  71. Paradis-Bleau C, Sanschagrin F, Levesque RC (2004) Identification of Pseudomonas aeruginosa FtsZ peptide inhibitors as a tool for development of novel antimicrobials. J Antimicrob Chemother 54:278–280PubMedGoogle Scholar
  72. Paradis-Bleau C, Sanschagrin F, Levesque RC (2005) Peptide inhibitors of the essential cell division protein FtsA. Protein Engineering Design and Selection 18:85–91Google Scholar
  73. Peterson JR, Mitchison TJ (2002) Small molecules, big impact: a history of chemical inhibitors and the cytoskeleton. Chem Biol 9:1275–1285PubMedGoogle Scholar
  74. Pichoff S, Lutkenhaus J (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55:1722–1734PubMedGoogle Scholar
  75. Projan SJ (2003) Why is big pharma getting out of antibacterial drug discovery? Curr Opin Microbiol 6:427–430PubMedGoogle Scholar
  76. Raskin DM, de Boer PA (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 96:4971–4976PubMedGoogle Scholar
  77. Reynolds RC, Srivastava S, Ross LJ, Suling WJ, White EL (2004) A new 2-carbamoyl pteridine that inhibits mycobacterial FtsZ. Bioorg Med Chem Lett 14:3161–3164PubMedGoogle Scholar
  78. Rico AI, Garcia-Ovalle M, Mingorance J, Vicente M (2004) Role of two essential domains of Escherichia coli FtsA in localization and progression of the division ring. Mol Microbiol 53:1359–1371PubMedGoogle Scholar
  79. Romberg L, Levin PA (2003) Assembly dynamics of the bacterial cell division protein FTSZ: poised at the edge of stability. Annu Rev Microbiol 57:125–154PubMedPubMedCentralGoogle Scholar
  80. Rush TS, Grant JA, Mosyak L, Nicholls A (2005) A shape-based 3-D scaffold hopping method and its application to a bacterial protein-protein interaction. J Med Chem 48:1489–1495PubMedGoogle Scholar
  81. Scheffel A, Gruska M, Faivre D, Linaroudis A, Plitzko JM, Schuler D (2006) An acidic protein aligns magnetosomes along a filamentous structure in magnetotactic bacteria. Nature 440:110–114PubMedGoogle Scholar
  82. Schilstra MJ, Slot JW, van der Meide PH, Posthuma G, Cremers AF, Bosch L (1984) Immunocytochemical localization of the elongation factor Tu in E. coli cells. FEBS Lett 165:175–179PubMedGoogle Scholar
  83. Shih YL, Le T, Rothfield L (2003) Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles. Proc Natl Acad Sci USA 100:7865–7870PubMedGoogle Scholar
  84. Shih YL, Kawagishi I, Rothfield L (2005) The MreB and Min cytoskeletal-like systems play independent roles in prokaryotic polar differentiation. Mol Microbiol 58:917–928PubMedGoogle Scholar
  85. Slovak PM, Porter SL, Armitage JP (2006) Differential localization of Mre proteins with PBP2 in Rhodobacter sphaeroides. J Bacteriol 188:1691–1700PubMedPubMedCentralGoogle Scholar
  86. Soufo HJ, Graumann PL (2003) Actin-like proteins MreB and Mbl from Bacillus subtilis are required for bipolar positioning of replication origins. Curr Biol 13:1916–1920PubMedGoogle Scholar
  87. Stewart GC (2005) Taking shape: control of bacterial cell wall biosynthesis. Mol Microbiol 57:1177–1181PubMedGoogle Scholar
  88. Stokes NR, Sievers J, Barker S, Bennett JM, Brown DR, Collins I, Errington VM, Foulger D, Hall M, Halsey R, Johnson H, Rose V, Thomaides HB, Haydon DJ, Czaplewski LG, Errington J (2005) Novel inhibitors of bacterial cytokinesis identified by a cell-based antibiotic screening assay. J Biol Chem 280:39709–39715PubMedGoogle Scholar
  89. Sutherland AG, Alvarez J, Ding W, Foreman KW, Kenny CH, Labthavikul P, Mosyak L, Petersen PJ, Rush TS, Ruzin A, Tsao DH, Wheless KL (2003) Structure-based design of carboxybiphenylindole inhibitors of the ZipA–FtsZ interaction. Organic and Biomolecular Chemistry 1:4138–4140PubMedGoogle Scholar
  90. Thanedar S, Margolin W (2004) FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr Biol 14:1167–1173PubMedPubMedCentralGoogle Scholar
  91. Trachtenberg S (1998) Mollicutes—wall-less bacteria with internal cytoskeleton. J Struct Biol 124:244–256PubMedPubMedCentralGoogle Scholar
  92. Urgaonkar S, La Pierre HS, Meir I, Lund H, RayChaudhuri D, Shaw JT (2005) Synthesis of antimicrobial natural products targeting FtsZ: (+/−)-dichamanetin and (+/−)-2′ ″-hydroxy-5′ ′-benzylisouvarinol-B. Org Lett 7:5609–5612PubMedPubMedCentralGoogle Scholar
  93. van den Ent F, Löwe J (2000) Crystal structure of the cell division protein FtsA from Thermotoga maritima. Embo J 19:5300–5307PubMedPubMedCentralGoogle Scholar
  94. van den Ent F, Amos LA, Löwe J (2001) Prokaryotic origin of the actin cytoskeleton. Nature 413:39–44PubMedGoogle Scholar
  95. Vicente M, Rico AI, Martinez-Arteaga R, Mingorance J (2006) Septum enlightenment: assembly of bacterial division proteins. J Bacteriol 188:19–27PubMedPubMedCentralGoogle Scholar
  96. Vollmer W, Höltje JV (2001) Morphogenesis of Escherichia coli. Curr Opin Microbiol 4:625–633PubMedGoogle Scholar
  97. Wang J, Galgoci A, Kodali S, Herath KB, Jayasuriya H, Dorso K, Vicente F, Gonzalez A, Cully D, Bramhill D, Singh S (2003) Discovery of a small molecule that inhibits cell division by blocking FtsZ, a novel therapeutic target of antibiotics. J Biol Chem 278:44424–44428PubMedGoogle Scholar
  98. Weart RB, Nakano S, Lane BE, Zuber P, Levin PA (2005) The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol Microbiol 57:238–249PubMedPubMedCentralGoogle Scholar
  99. Weidel W, Pelzer H (1964) Bagshaped macromolecules—a new outlook on bacterial cell walls. Adv Enzymol 26:193–232Google Scholar
  100. Weiss DS (2004) Bacterial cell division and the septal ring. Mol Microbiol 54:588–597PubMedGoogle Scholar
  101. White EL, Suling WJ, Ross LJ, Seitz LE, Reynolds RC (2002) 2-Alkoxycarbonylaminopyridines: inhibitors of Mycobacterium tuberculosis FtsZ. J Antimicrob Chemother 50:111–114PubMedGoogle Scholar
  102. Williamson DL, Renaudin J, Bove JM (1991) Nucleotide sequence of the Spiroplasma citri fibril protein gene. J Bacteriol 173:4353–4362PubMedPubMedCentralGoogle Scholar
  103. Wolff J, Knuipling L (1993) Antimicrotubule properties of benzophenantridine alkaloids. Biochemistry 32:13334–13339PubMedGoogle Scholar
  104. Wu LJ, Errington J (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915–925PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Mikrobielle GenetikUniversität TübingenTübingenGermany

Personalised recommendations