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Abstract

The FtsZ protein is a highly conserved bacterial tubulin homolog. In vivo, the functional form of FtsZ is the polymeric, ring-like structure (Z-ring) assembled at the future division site during cell division. While it is clear that the Z-ring plays an essential role in orchestrating cytokinesis, precisely what its functions are and how these functions are achieved remain elusive. In this article, we review what we have learned during the past decade about the Z-ring's structure, function, and dynamics, with a particular focus on insights generated by recent high-resolution imaging and single-molecule analyses. We suggest that the major function of the Z-ring is to govern nascent cell pole morphogenesis by directing the spatiotemporal distribution of septal cell wall remodeling enzymes through the Z-ring's GTP hydrolysis–dependent treadmilling dynamics. In this role, FtsZ functions in cell division as the counterpart of the cell shape–determining actin homolog MreB in cell elongation.

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2020-05-06
2024-04-13
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Literature Cited

  1. 1. 
    Aaron M, Charbon G, Lam H, Schwarz H, Vollmer W, Jacobs-Wagner C 2007. The tubulin homologue FtsZ contributes to cell elongation by guiding cell wall precursor synthesis in Caulobacter crescentus. Mol. Microbiol 64:938–52
    [Google Scholar]
  2. 2. 
    Aarsman ME, Piette A, Fraipont C, Vinkenvleugel TM, Nguyen-Distèche M, den Blaauwen T 2005. Maturation of the Escherichia coli divisome occurs in two steps. Mol. Microbiol. 55:1631–45
    [Google Scholar]
  3. 3. 
    Adams DW, Errington J. 2009. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat. Rev. Microbiol. 7:642–53
    [Google Scholar]
  4. 4. 
    Addinall S, Bi E, Lutkenhaus J 1996. FtsZ ring formation in fts mutants. J. Bacteriol. 178:3877–84
    [Google Scholar]
  5. 5. 
    Addinall S, Lutkenhaus J. 1996. FtsA is localized to the septum in an FtsZ-dependent manner. J. Bacteriol. 178:7167–72
    [Google Scholar]
  6. 6. 
    Addinall SG, Lutkenhaus J. 1996. FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol. Microbiol 22:231–37
    [Google Scholar]
  7. 7. 
    Alatossava T, Jütte H, Kuhn A, Kellenberger E 1985. Manipulation of intracellular magnesium content in polymyxin B nonapeptide-sensitized Escherichia coli by ionophore A23187. J. Bacteriol. 162:413–19
    [Google Scholar]
  8. 8. 
    Alexeeva S, Gadella TW, Verheul J, Verhoeven GS, den Blaauwen T 2010. Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol. Microbiol. 77:384–98
    [Google Scholar]
  9. 9. 
    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. 186:5775–81
    [Google Scholar]
  10. 10. 
    Andreu JM et al. 2010. The antibacterial cell division inhibitor PC190723 is an FtsZ polymer-stabilizing agent that induces filament assembly and condensation. J. Biol. Chem. 285:14239–46
    [Google Scholar]
  11. 11. 
    Arjes HA, Lai B, Emelue E, Steinbach A, Levin P 2015. Mutations in the bacterial cell division protein FtsZ highlight the role of GTP binding and longitudinal subunit interactions in assembly and function. BMC Microbiol 15:209
    [Google Scholar]
  12. 12. 
    Auer GK, Weibel DB. 2017. Bacterial cell mechanics. Biochemistry 56:3710–24
    [Google Scholar]
  13. 13. 
    Baranova N, Radler P, Hernández-Rocamora VM, Alfonso C, López-Pelegrín M et al. 2020. Diffusion and capture permits dynamic coupling between treadmilling FtsZ filaments and cell division proteins. Nat. Microbiol 5407–17
  14. 14. 
    Begg K, Dewar S, Donachie W 1995. A new Escherichia coli cell division gene, ftsK. J. Bacteriol. 177:6211–22
    [Google Scholar]
  15. 15. 
    Berezuk AM, Glavota S, Roach EJ, Goodyear MC, Krieger JR, Khursigara CM 2018. Outer membrane lipoprotein RlpA is a novel periplasmic interaction partner of the cell division protein FtsK in Escherichia coli. Sci. Rep 8:12933
    [Google Scholar]
  16. 16. 
    Bernhardt TG, de Boer P 2005. SlmA, a nucleoid-associated. FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol. Cell 18:555–64
    [Google Scholar]
  17. 17. 
    Bi E, Lutkenhaus J. 1990. FtsZ regulates frequency of cell division in Escherichia coli. J. . Bacteriol 172:2765–68
    [Google Scholar]
  18. 18. 
    Bi E, Lutkenhaus J. 1991. FtsZ ring structure associated with division in Escherichia coli. . Nature 354:161–64
    [Google Scholar]
  19. 19. 
    Bisson-Filho AW, Discola KF, Castellen P, Blasios V, Martins A et al. 2015. FtsZ filament capping by MciZ, a developmental regulator of bacterial division. PNAS 112:E2130–38
    [Google Scholar]
  20. 20. 
    Bisson-Filho AW, Hsu Y-P, Squyres GR, Kuru E, Wu F et al. 2017. Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355:739–43
    [Google Scholar]
  21. 21. 
    Biteen JS, Goley ED, Shapiro L, Moerner W 2012. Three-dimensional super-resolution imaging of the midplane protein FtsZ in live Caulobacter crescentus cells using astigmatism. ChemPhysChem 13:1007–12
    [Google Scholar]
  22. 22. 
    Boer DP, Crossley R, Rothfield L 1992. Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J. . Bacteriol 174:63–70
    [Google Scholar]
  23. 23. 
    Boes A, Olatunji S, Breukink E, Terrak M 2019. Regulation of the peptidoglycan polymerase activity of PBP1b by antagonist actions of the core divisome proteins FtsBLQ and FtsN. mBio 10:220
    [Google Scholar]
  24. 24. 
    Bork P, Sander C, Valencia A 1992. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. PNAS 89:7290–94
    [Google Scholar]
  25. 25. 
    Bramhill D, Thompson C. 1994. GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. PNAS 91:5813–17
    [Google Scholar]
  26. 26. 
    Briegel A, Dias DP, Li Z, Jensen RB, Frangakis AS, Jensen GJ 2006. Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography. Mol. Microbiol. 62:5–14
    [Google Scholar]
  27. 27. 
    Buddelmeijer N, Beckwith J. 2002. Assembly of cell division proteins at the E. coli cell center. Curr. Opin. Microbiol. 5:553–57
    [Google Scholar]
  28. 28. 
    Buddelmeijer N, Beckwith J. 2004. A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region. Mol. Microbiol. 52:1315–27
    [Google Scholar]
  29. 29. 
    Buske P, Levin P. 2013. A flexible C-terminal linker is required for proper FtsZ assembly in vitro and cytokinetic ring formation in vivo. Mol. Microbiol. 89:249–63
    [Google Scholar]
  30. 30. 
    Buske PJ, Mittal A, Pappu RV, Levin P 2015. An intrinsically disordered linker plays a critical role in bacterial cell division. Semin. Cell Dev. Biol. 37:3–10
    [Google Scholar]
  31. 31. 
    Buss J, Coltharp C, Huang T, Pohlmeyer C, Wang SC et al. 2013. In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy. Mol. Microbiol. 89:1099–120
    [Google Scholar]
  32. 32. 
    Buss J, Coltharp C, Shtengel G, Yang X, Hess H, Xiao J 2015. A multi-layered protein network stabilizes the Escherichia coli FtsZ-ring and modulates constriction dynamics. PLOS Genet 11:e1005128
    [Google Scholar]
  33. 33. 
    Buss JA, Peters NT, Xiao J, Bernhardt TG 2017. ZapA and ZapB form an FtsZ-independent structure at midcell. Mol. Microbiol. 104:652–63
    [Google Scholar]
  34. 34. 
    Cayley S, Lewis BA, Guttman HJ, Record MT 1991. Characterization of the cytoplasm of Escherichia coli K-12 as a function of external osmolarity: implications for protein-DNA interactions in vivo. J. Mol. Biol. 222:281–300
    [Google Scholar]
  35. 35. 
    Cayley SD, Guttman HJ, Record TM 2000. Biophysical characterization of changes in amounts and activity of Escherichia coli cell and compartment water and turgor pressure in response to osmotic stress. Biophys. J. 78:1748–64
    [Google Scholar]
  36. 36. 
    Chen Y, Erickson HP. 2005. Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J. Biol. Chem. 280:22549–54
    [Google Scholar]
  37. 37. 
    Chen Y, Erickson HP. 2009. FtsZ filament dynamics at steady state: subunit exchange with and without nucleotide hydrolysis. Biochemistry 48:6664–73
    [Google Scholar]
  38. 38. 
    Chen Y, Milam SL, Erickson HP 2012. SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry 51:3100–9
    [Google Scholar]
  39. 39. 
    Cho H, Wivagg CN, Kapoor M, Barry Z, Rohs PDA et al. 2016. Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously. Nat. Microbiol. 1:16172
    [Google Scholar]
  40. 40. 
    Coltharp C, Buss J, Plumer TM, Xiao J 2016. Defining the rate-limiting processes of bacterial cytokinesis. PNAS 113:E1044–53
    [Google Scholar]
  41. 41. 
    Coltharp C, Xiao J. 2016. Beyond force generation: Why is a dynamic ring of FtsZ polymers essential for bacterial cytokinesis?. Bioessays 39:1600179
    [Google Scholar]
  42. 42. 
    Coltharp C, Xiao J. 2016. How do bacteria divide and multiply. Atlas of Science May 2. https://atlasofscience.org/how-do-bacteria-divide-and-multiply/
    [Google Scholar]
  43. 43. 
    Coltharp C, Yang X, Xiao J 2014. Quantitative analysis of single-molecule superresolution images. Curr. Opin. Struc. Biol. 28:112–21
    [Google Scholar]
  44. 44. 
    Corbin BD, Wang Y, Beuria TK, Margolin W 2007. Interaction between cell division proteins FtsE and FtsZ. J. Bacteriol. 189:3026–35
    [Google Scholar]
  45. 45. 
    de Boer P, Crossley R, Rothfield L 1992. The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359:254–56
    [Google Scholar]
  46. 46. 
    de Boer PA. 2010. Advances in understanding E. coli cell fission. Curr. Opin. Microbiol. 13:730–37
    [Google Scholar]
  47. 47. 
    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 56:641–49
    [Google Scholar]
  48. 48. 
    de Pedro M, Quintela J, Höltje J, Schwarz H 1997. Murein segregation in Escherichia coli. J. . Bacteriol 179:2823–34
    [Google Scholar]
  49. 49. 
    de Pedro MA, Cava F 2015. Structural constraints and dynamics of bacterial cell wall architecture. Front. Microbiol. 6:449
    [Google Scholar]
  50. 50. 
    den Blaauwen T, de Pedro MA, Nguyen-Distèche M, Ayala JA 2008. Morphogenesis of rod-shaped sacculi. FEMS Microbiol. Rev. 32:321–44
    [Google Scholar]
  51. 51. 
    Dhaked H, Ray S, Battaje R, Banerjee A, Panda D 2019. Regulation of Streptococcus pneumoniae FtsZ assembly by divalent cations: paradoxical effects of Ca2+ on the nucleation and bundling of FtsZ polymers. FEBS J 286:3629–46
    [Google Scholar]
  52. 52. 
    Du S, Lutkenhaus J. 2014. SlmA antagonism of FtsZ assembly employs a two-pronged mechanism like MinCD. PLOS Genet 10:e1004460
    [Google Scholar]
  53. 53. 
    Durand-Heredia J, Rivkin E, Fan G, Morales J, Janakiraman A 2012. Identification of ZapD as a cell division factor that promotes the assembly of FtsZ in Escherichia coli. J. . Bacteriol 194:3189–98
    [Google Scholar]
  54. 54. 
    Ebersbach G, Galli E, Møller-Jensen J, Löwe J, Gerdes K 2008. Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol. Microbiol. 68:720–35
    [Google Scholar]
  55. 55. 
    Egan AJ, Vollmer W. 2013. The physiology of bacterial cell division. Ann. N. Y. Acad. Sci. 1277:8–28
    [Google Scholar]
  56. 56. 
    Eraso JM, Markillie LM, Mitchell HD, Taylor RC, Orr G, Margolin WM 2014. The highly conserved MraZ protein is a transcriptional regulator in Escherichia coli. J. Bacteriol 196:112053–66
    [Google Scholar]
  57. 57. 
    Erickson H, Taylor D, Taylor K, Bramhill D 1996. Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. PNAS 93:519–23
    [Google Scholar]
  58. 58. 
    Erickson HP. 1995. FtsZ, a prokaryotic homolog of tubulin. Cell 80:367–70
    [Google Scholar]
  59. 59. 
    Erickson HP. 2009. Modeling the physics of FtsZ assembly and force generation. PNAS 106:9238–43
    [Google Scholar]
  60. 60. 
    Erickson HP. 2017. How bacterial cell division might cheat turgor pressure: a unified mechanism of septal division in Gram-positive and Gram-negative bacteria. Bioessays 39:8 https://doi.org/10.1002/bies.201700045
    [Crossref] [Google Scholar]
  61. 61. 
    Erickson HP, Anderson DE, Osawa M 2010. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol. Mol. Biol. Rev. 74:504–28
    [Google Scholar]
  62. 62. 
    Espéli O, Borne R, Dupaigne P, Thiel A, Gigant E et al. 2012. A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 31:3198–211
    [Google Scholar]
  63. 63. 
    Fleurie A, Lesterlin C, Manuse S, Zhao C, Cluzel C et al. 2014. MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature 516:259–62
    [Google Scholar]
  64. 64. 
    Fu G, Huang T, Buss J, Coltharp C, Hensel Z, Xiao J 2010. In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLOS ONE 5:e12680
    [Google Scholar]
  65. 65. 
    Galli E, Gerdes K. 2012. FtsZ-ZapA-ZapB interactome of Escherichia coli. J. Bacteriol 194:292–302
    [Google Scholar]
  66. 66. 
    Gamba P, Veening JW, Saunders NJ, Hamoen LW, Daniel RA 2009. Two-step assembly dynamics of the Bacillus subtilis divisome. J. Bacteriol. 191:4186–94
    [Google Scholar]
  67. 67. 
    Gangola P, Rosen B. 1987. Maintenance of intracellular calcium in Escherichia coli. J. Biol. Chem 262:12570–74
    [Google Scholar]
  68. 68. 
    Gardner KA, Moore DA, Erickson HP 2013. The C-terminal linker of Escherichia coliFtsZ functions as an intrinsically disordered peptide. Mol. Microbiol. 89:264–75
    [Google Scholar]
  69. 69. 
    Ghosh B, Sain A. 2008. Origin of contractile force during cell division of bacteria. Phys. Rev. Lett. 101:178101
    [Google Scholar]
  70. 70. 
    Goehring NW, Beckwith J. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr. Biol. 15:R514–26
    [Google Scholar]
  71. 71. 
    Goehring NW, Gueiros-Filho F, Beckwith J 2005. Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. . Gene Dev 19:127–37
    [Google Scholar]
  72. 72. 
    Goley ED, Yeh Y-C, Hong S-H, Fero MJ, Abeliuk E et al. 2011. Assembly of the Caulobacter cell division machine. Mol. Microbiol. 80:1680–98
    [Google Scholar]
  73. 73. 
    González JM, Jiménez M, Vélez M, Mingorance J, Andreu JM et al. 2003. Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J. Biol. Chem. 278:37664–71
    [Google Scholar]
  74. 74. 
    Gottesman S, Halpern E, Trisler P 1981. Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J. Bacteriol. 148:265–73
    [Google Scholar]
  75. 75. 
    Grenga L, Luzi G, Paolozzi L, Ghelardini P 2008. The Escherichia coli FtsK functional domains involved in its interaction with its divisome protein partners. FEMS Microbiol. Lett. 287:163–67
    [Google Scholar]
  76. 76. 
    Gueiros-Filho FJ, Losick R. 2002. A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Gene Dev 16:2544–56
    [Google Scholar]
  77. 77. 
    Haeusser DP, Margolin W. 2016. Splitsville: structural and functional insights into the dynamic bacterial Z ring. Nat. Rev. Microbiol. 14:305–19
    [Google Scholar]
  78. 78. 
    Hale CA, de Boer P 1997. Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. . Cell 88:175–85
    [Google Scholar]
  79. 79. 
    Hale CA, Rhee AC, de Boer PA 2000. ZipA-induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J. Bacteriol. 182:5153–66
    [Google Scholar]
  80. 80. 
    Hale CA, Shiomi D, Liu B, Bernhardt TG, Marggolin W et al. 2011. Identification of Escherichia coli ZapC (YcbW) as a component of the division apparatus that binds and bundles FtsZ polymers. J. Bacteriol. 193:1393–404
    [Google Scholar]
  81. 81. 
    Handler AA, Lim J, Losick R 2008. Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis. Mol. Microbiol 68:588–99
    [Google Scholar]
  82. 82. 
    Harry E, Monahan L, Thompson L 2006. Bacterial cell division: the mechanism and its precision. Int. Rev. Cytol. 253:27–94
    [Google Scholar]
  83. 83. 
    Haydon DJ, Stokes NR, Ure R, Galbraith G, Bennett JM et al. 2008. An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321:1673–75
    [Google Scholar]
  84. 84. 
    Heidrich C, Templin MF, Ursinus A, Merdanovic M, Berger J et al. 2001. Involvement of N-acetylmuramyl-L-alanine amidases in cell separation and antibiotic-induced autolysis of Escherichia coli. Mol. Microbiol 41:167–78
    [Google Scholar]
  85. 85. 
    Hirota Y, Ryter A, Jacob F 1968. Thermosensitive mutants of E. coli affected in the processes of DNA synthesis and cellular division. Cold Spring Harb. Symp. Quant. Biol. 33:677–93
    [Google Scholar]
  86. 86. 
    Holden S. 2018. Probing the mechanistic principles of bacterial cell division with super-resolution microscopy. Curr. Opin. Microbiol. 43:84–91
    [Google Scholar]
  87. 87. 
    Holden SJ, Pengo T, Meibom KL, Fernandez C, Collier J, Manley S 2014. High throughput 3D super-resolution microscopy reveals Caulobacter crescentus in vivo Z-ring organization. PNAS 111:4566–71
    [Google Scholar]
  88. 88. 
    Höltje J. 1998. Growth of the stress-bearing and shape-maintaining murein sacculus of Escherichia coli. Microbiol. Mol. Biol. Rev 62:181–203
    [Google Scholar]
  89. 89. 
    Hörger I, Velasco E, Mingorance J, Rivas G, Tarazona P, Vélez M 2008. Langevin computer simulations of bacterial protein filaments and the force-generating mechanism during cell division. Phys. Rev. E 77:011902
    [Google Scholar]
  90. 90. 
    Housman M, Milam SL, Moore DA, Osawa M, Erickson HP 2016. FtsZ protofilament curvature is the opposite of tubulin rings. Biochemistry 55:4085–91
    [Google Scholar]
  91. 91. 
    Hsin J, Gopinathan A, Huang KC 2012. Nucleotide-dependent conformations of FtsZ dimers and force generation observed through molecular dynamics simulations. PNAS 109:9432–37
    [Google Scholar]
  92. 92. 
    Huang KH, Durand-Heredia J, Janakiraman A 2013. FtsZ ring stability: of bundles, tubules, crosslinks, and curves. J. Bacteriol. 195:1859–68
    [Google Scholar]
  93. 93. 
    Huecas S, Llorca O, Boskovic J, Martín-Benito J, Valpuesta JM, Andreu JM 2008. Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments. Biophys. J. 94:1796–806
    [Google Scholar]
  94. 94. 
    Huecas S, Ramírez-Aportela E, Vergoñós A, Núñez-Ramírez R, Llorca O et al. 2017. Self-organization of FtsZ polymers in solution reveals spacer role of the disordered C-terminal tail. Biophys. J. 113:1831–44
    [Google Scholar]
  95. 95. 
    Huisman O, D'Ari R, Gottesman S 1984. Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. PNAS 81:4490–94
    [Google Scholar]
  96. 96. 
    Ize B, Stanley NR, Buchanan G, Palmer T 2003. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48:1171–82
    [Google Scholar]
  97. 97. 
    Jacq M, Adam V, Bourgeois D, Moriscot C, Di Guilmi A-M et al. 2015. Remodeling of the Z-ring nanostructure during the Streptococcus pneumoniae cell cycle revealed by photoactivated localization microscopy. mBio 6:e01108–15
    [Google Scholar]
  98. 98. 
    Jennings PC, Cox GC, Monahan LG, Harry EJ 2011. Super-resolution imaging of the bacterial cytokinetic protein FtsZ. Micron 42:336–41
    [Google Scholar]
  99. 99. 
    Johnson JW, Fisher JF, Mobashery S 2013. Bacterial cell-wall recycling. Ann. N. Y. Acad. Sci. 1277:54–75
    [Google Scholar]
  100. 99a. 
    Judd EM, Comolli LR, Chen JC, Downing KH, Moerner WE, McAdams HH 2015. Distinct constrictive processes, separated in time and space, divide caulobacter inner and outer membranes. J. Bacteriol 187:6874–82
    [Google Scholar]
  101. 100. 
    Justice SS, García-Lara J, Rothfield LI 2000. Cell division inhibitors SulA and MinC/MinD block septum formation at different steps in the assembly of the Escherichia coli division machinery. Mol. Microbiol. 37:410–23
    [Google Scholar]
  102. 101. 
    Karimova G, Dautin N, Ladant D 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:2233–43
    [Google Scholar]
  103. 102. 
    Kelly AJ, Sackett MJ, Din N, Quardokus E, Brun YV 1998. Cell cycle-dependent transcriptional and proteolytic regulation of FtsZ inCaulobacter. . Gene Dev 12:880–93
    [Google Scholar]
  104. 103. 
    Kuru E, Tekkam N, Hall E, Brun YV, Nieuwenhze MS 2015. Synthesis of fluorescent D-amino acids and their use for probing peptidoglycan synthesis and bacterial growth in situ. Nat. Protoc. 10:33–52
    [Google Scholar]
  105. 104. 
    Lallo DG, Fagioli M, Barionovi D, Ghelardini P, Paolozzi L 2003. Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149:3353–59
    [Google Scholar]
  106. 105. 
    Lan G, Daniels BR, Dobrowsky TM, Wirtz D, Sun SX 2009. Condensation of FtsZ filaments can drive bacterial cell division. PNAS 106:121–26
    [Google Scholar]
  107. 106. 
    Lan G, Wolgemuth CW, Sun SX 2007. Z-ring force and cell shape during division in rod-like bacteria. PNAS 104:16110–15
    [Google Scholar]
  108. 107. 
    Lange R, Hengge-Aronis R. 1994. The nIpD gene is located in an operon with rpoS on the Escherichia coli chromosome and encodes a novel lipoprotein with a potential function in cell wall formation. Mol. Microbiol. 13:733–43
    [Google Scholar]
  109. 108. 
    Läppchen T, Pinas VA, Hartog AF, Koomen GJ, Schaffner-Barbero C et al. 2008. Probing FtsZ and tubulin with C8-substituted GTP analogs reveals differences in their nucleotide binding sites. Chem. Biol. 15:189–99
    [Google Scholar]
  110. 109. 
    Leaver M, Domínguez-Cuevas P, Coxhead J, Daniel R, Errington J 2009. Life without a wall or division machine in Bacillus subtilis. . Nature 457:849–53
    [Google Scholar]
  111. 110. 
    Leisch N, Verheul J, Heindl NR, Gruber-Vodicka HR, Pende N et al. 2012. Growth in width and FtsZ ring longitudinal positioning in a gammaproteobacterial symbiont. Curr. Biol. 22:R831–32
    [Google Scholar]
  112. 111. 
    Leung AK, Lucile White E, Ross LJ, Reynolds RC, DeVito JA, Borhani DW 2004. Structure of Mycobacterium tuberculosis FtsZ reveals unexpected, G protein-like conformational switches. J. Mol. Biol. 342:953–70
    [Google Scholar]
  113. 112. 
    Levin P, Kurtser IG, Grossman AD 1999. Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. . PNAS 96:9642–47
    [Google Scholar]
  114. 113. 
    Levin P, Losick R. 1996. Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. . Gene Dev 10:478–88
    [Google Scholar]
  115. 114. 
    Li Y, Hsin J, Zhao L, Cheng Y, Shang W et al. 2013. FtsZ protofilaments use a hinge-opening mechanism for constrictive force generation. Science 341:392–95
    [Google Scholar]
  116. 115. 
    Li Y, Shao S, Xu X, Su X, Sun Y, Wei S 2018. MapZ forms a stable ring structure that acts as a nanotrack for FtsZ treadmilling in Streptococcus mutans. . ACS Nano 12:6137–46
    [Google Scholar]
  117. 116. 
    Li Z, Trimble MJ, Brun YV, Jensen GJ 2007. The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26:4694–708
    [Google Scholar]
  118. 117. 
    Liu B, Hale CA, Persons L, Phillips-Mason PJ, de Boer PA 2019. Roles of the DedD protein in Escherichia coli cell constriction. J. Bacteriol. 201:e00698–18
    [Google Scholar]
  119. 118. 
    Liu B, Persons L, Lee L, de Boer PA 2015. Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in Escherichia coli.. Mol. Microbiol 95:945–70
    [Google Scholar]
  120. 119. 
    Liu G, Draper CG, Donachie W 1998. FtsK is a bifunctional protein involved in cell division and chromosome localization in Escherichia coli. Mol. Microbiol 29:893–903
    [Google Scholar]
  121. 120. 
    Liu Z, Mukherjee A, Lutkenhaus J 1999. Recruitment of ZipA to the division site by interaction with FtsZ. Mol. Microbiol. 31:1853–61
    [Google Scholar]
  122. 121. 
    Loose M, Mitchison TJ. 2013. The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat. Cell Biol. 16:38–46
    [Google Scholar]
  123. 122. 
    Low HH, Moncrieffe MC, Löwe J 2004. The crystal structure of ZapA and its modulation of FtsZ polymerisation. J. Mol. Biol. 341:839–52
    [Google Scholar]
  124. 123. 
    Löwe J, Amos LA. 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203–6
    [Google Scholar]
  125. 124. 
    Löwe J, Amos LA. 1999. Tubulin-like protofilaments in Ca2+-induced FtsZ sheets. EMBO J 18:2364–71
    [Google Scholar]
  126. 125. 
    Lu C, Reedy M, Erickson HP 2000. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182:164–70
    [Google Scholar]
  127. 126. 
    Lu C, Stricker J, Erickson HP 2001. Site-specific mutations of FtsZ: effects on GTPase and in vitro assembly. BMC Microbiol 1:7
    [Google Scholar]
  128. 127. 
    Lutkenhaus J, Du S. 2013. E. coli cell cycle machinery. Sub-Cell Biochem 84:27–65
    [Google Scholar]
  129. 128. 
    Lyu Z, Coltharp C, Yang X, Xiao J 2016. Influence of FtsZ GTPase activity and concentration on nanoscale Z-ring structure in vivo revealed by three-dimensional superresolution imaging. Biopolymers 105:725–34
    [Google Scholar]
  130. 129. 
    Ma X, Ehrhardt DW, Margolin W 1996. Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using greenfluorescentprotein. PNAS 93:12998–3003
    [Google Scholar]
  131. 130. 
    Ma X, Margolin W. 1999. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J. Bacteriol. 181:7531–44
    [Google Scholar]
  132. 131. 
    MacCain WJ, Kannan S, Jameel DZ, Troutman JM, Young KD 2018. A defective undecaprenyl pyrophosphate synthase induces growth and morphological defects that are suppressed by mutations in the isoprenoid pathway of Escherichia coli.. J. Bacteriol 200:e00255–18
    [Google Scholar]
  133. 132. 
    Maggi S, Massidda O, Luzi G, Fadda D, Paolozzi L, Ghelardini P 2008. Division protein interaction web: identification of a phylogenetically conserved common interactome between Streptococcus pneumoniae and Escherichia coli. . Microbiology 154:3042–52
    [Google Scholar]
  134. 133. 
    Männik J, Bailey MW, O'Neill JC, Männik J 2017. Kinetics of large-scale chromosomal movement during asymmetric cell division in Escherichia coli. . PLOS Genet 13:e1006638
    [Google Scholar]
  135. 134. 
    Männik J, Castillo DE, Yang D, Siopsis G, Männik J 2016. The role of MatP. ZapA and ZapB in chromosomal organization and dynamics in Escherichia coli. Nucleic Acids Res. 44:1216–26
    [Google Scholar]
  136. 135. 
    Marteyn BS, Karimova G, Fenton AK, Gazi AD, West N et al. 2014. ZapE is a novel cell division protein interacting with FtsZ and modulating the Z-ring dynamics. mBio 5:e00022–14
    [Google Scholar]
  137. 136. 
    Mateos-Gil P, Paez A, Hörger I, Rivas G, Vicente M et al. 2012. Depolymerization dynamics of individual filaments of bacterial cytoskeletal protein FtsZ. PNAS 109:8133–38
    [Google Scholar]
  138. 137. 
    Mateos-Gil P, Tarazona P, Vélez M 2018. Bacterial cell division: modeling FtsZ assembly and force generation from single filament experimental data. FEMS Microbiol. Rev. 43:73–87
    [Google Scholar]
  139. 138. 
    Matsui T, Han X, Yu J, Yao M, Tanaka I 2014. Structural change in FtsZ induced by intermolecular interactions between bound GTP and the T7 loop. J. Biol. Chem. 289:3501–9
    [Google Scholar]
  140. 139. 
    Matsui T, Yamane J, Mogi N, Yamaguchi H, Takemoto H et al. 2012. Structural reorganization of the bacterial cell-division protein FtsZ from Staphylococcus aureus. Acta Crystallogr. D 68:1175–88
    [Google Scholar]
  141. 140. 
    McCausland JW, Yang X, Lyu Z, Söderström B, Xiao J, Liu J 2019. Treadmilling FtsZ polymers drive the directional movement of sPG-synthesis enzymes via a Brownian ratchet mechanism. bioRxiv 857813. https://doi.org/10.1101/857813
    [Crossref]
  142. 141. 
    Meier EL, Daitch AK, Yao Q, Bhargava A, Jensen GJ, Goley ED 2017. FtsEX-mediated regulation of the final stages of cell division reveals morphogenetic plasticity in Caulobacter crescentus. . PLOS Genet 13:e1006999
    [Google Scholar]
  143. 142. 
    Mercier R, Petit MA, Schbath S, Robin S, El Karoui M et al. 2008. The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135:475–85
    [Google Scholar]
  144. 143. 
    Milne J, Subramaniam R. 2009. Cryo-electron tomography of bacteria: progress, challenges and future prospects. Nat. Rev. Microbiol. 7:666–75
    [Google Scholar]
  145. 144. 
    Mohammadi T, Ploeger GE, Verheul J, Comvalius AD, Martos A et al. 2009. The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro. Biochemistry 48:11056–66
    [Google Scholar]
  146. 145. 
    Monteiro JM, Pereira AR, Reichmann NT, Saraiva BM, Fernandes PB et al. 2018. Peptidoglycan synthesis drives an FtsZ-treadmilling-independent step of cytokinesis. Nature 554:528–32
    [Google Scholar]
  147. 146. 
    Moore DA, Whatley ZN, Joshi CP, Osawa M, Erickson HP 2017. Probing for binding regions of the FtsZ protein surface through site-directed insertions: discovery of fully functional FtsZ-fluorescent proteins. J. Bacteriol. 199:e00553–16
    [Google Scholar]
  148. 147. 
    Mosyak L, Zhang Y, Glasfeld E, Haney S, Stahl M et al. 2000. The bacterial cell-division protein ZipA and its interaction with an FtsZ fragment revealed by X-ray crystallography. EMBO J 19:3179–91
    [Google Scholar]
  149. 148. 
    Mukherjee A, Dai K, Lutkenhaus J 1993. Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. PNAS 90:1053–57
    [Google Scholar]
  150. 149. 
    Mukherjee A, Cao C, Lutkenhaus J 1998. Inhibition of FtsZ polymerization by SulA, an inhibitor of septation in Escherichiacoli. . PNAS 95:2885–90
    [Google Scholar]
  151. 150. 
    Mukherjee A, Lutkenhaus J. 1994. Guanine nucleotide-dependent assembly of FtsZ into filaments. J. Bacteriol. 176:2754–58
    [Google Scholar]
  152. 151. 
    Nguyen LT, Oikonomou CM, Ding HJ, Kaplan M, Yao Q et al. 2019. Simulations suggest a constrictive force is required for Gram-negative bacterial cell division. Nat. Commun. 10:1259
    [Google Scholar]
  153. 152. 
    Nguyen LT, Oikonomou CM, Jensen GJ 2019. Simulations of proposed mechanisms of FtsZ-driven cell constriction. bioRxiv 737189. https://doi.org/10.1101/737189
    [Crossref]
  154. 153. 
    Nguyen-Distèche M, Fraipont C, Buddelmeijer N, Nanninga N 1998. The structure and function of Escherichia coli penicillin-binding protein 3. Cell Mol. Life Sci. 54:309–16
    [Google Scholar]
  155. 154. 
    Niu L, Yu J. 2008. Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys. J. 95:2009–16
    [Google Scholar]
  156. 155. 
    Nogales E, Downing KH, Amos LA, Löwe J 1998. Tubulin and FtsZ form a distinct family of GTPases. Nat. Struct. Biol. 5:451–58
    [Google Scholar]
  157. 156. 
    Ogura T, Tomoyasu T, Yuki T, Morimura S, Begg KJ et al. 1991. Structure and function of the ftsH gene in Escherichia coli. Res. Microbiol 142:279–82
    [Google Scholar]
  158. 157. 
    Oikonomou CM, Jensen GJ. 2017. The development of cryo-EM and how it has advanced microbiology. Nat. Microbiol. 2:1577–79
    [Google Scholar]
  159. 158. 
    Oliva MA, Cordell SC, Löwe J 2004. Structural insights into FtsZ protofilament formation. Nat. Struct. Mol. Biol. 11:1243–50
    [Google Scholar]
  160. 159. 
    Oliva MA, Trambaiolo D, Löwe J 2007. Structural insights into the conformational variability of FtsZ. J. Mol. Biol. 373:1229–42
    [Google Scholar]
  161. 160. 
    Osawa M, Anderson DE, Erickson HP 2008. Reconstitution of contractile FtsZ rings in liposomes. Science 320:792–94
    [Google Scholar]
  162. 161. 
    Osawa M, Anderson DE, Erickson HP 2009. Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J 28:3476–84
    [Google Scholar]
  163. 162. 
    Osawa M, Erickson HP. 2011. Inside-out Z rings: constriction with and without GTP hydrolysis. Mol. Microbiol. 81:571–79
    [Google Scholar]
  164. 163. 
    Osawa M, Erickson HP. 2018. Turgor pressure and possible constriction mechanisms in bacterial division. Front. Microbiol. 9:111
    [Google Scholar]
  165. 164. 
    Paez A, Mateos-Gil P, Hörger I, Mingorance J, Rivas G et al. 2009. Simple modeling of FtsZ polymers on flat and curved surfaces: correlation with experimental in vitro observations. PMC Biophys 2:8
    [Google Scholar]
  166. 165. 
    Paradis-Bleau C, Markovski M, Uehara T, Lupoli TJ, Walker S et al. 2010. Lipoprotein cofactors located in the outer membrane activate bacterial cell wall polymerases. Cell 143:1110–20
    [Google Scholar]
  167. 166. 
    Pazos M, Natale P, Margolin W, Vicente M 2013. Interactions among the early Escherichia coli divisome proteins revealed by bimolecular fluorescence complementation. Environ. Microbiol. 15:3282–91
    [Google Scholar]
  168. 167. 
    Pende N, Wang J, Weber PM, Verheul J, Kuru E et al. 2018. Host-polarized cell growth in animal symbionts. Curr. Biol. 28:1039–51.e5
    [Google Scholar]
  169. 168. 
    Pereira AR, Hsin J, Król E, Tavares AC, Flores P et al. 2016. FtsZ-dependent elongation of a coccoid bacterium. mBio 7:e00908–16
    [Google Scholar]
  170. 169. 
    Perez AJ, Cesbron Y, Shaw BL, Bazan Villicana J, Tsui HT et al. 2019. Movement dynamics of divisome proteins and PBP2x:FtsW in cells of Streptococcus pneumoniae. . PNAS 116:3211–20
    [Google Scholar]
  171. 170. 
    Petiti M, Serrano B, Faure L, Lloubes R, Mignot T, Duché D 2019. Tol energy-driven localization of Pal and anchoring to the peptidoglycan promote outer-membrane constriction. J. Mol. Biol. 431:3275–88
    [Google Scholar]
  172. 171. 
    Pichoff S, Du S, Lutkenhaus J 2019. Roles of FtsEX in cell division. Res. Microbiol. 170:374–80
    [Google Scholar]
  173. 172. 
    Pichoff S, Lutkenhaus J. 2005. Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55:1722–34
    [Google Scholar]
  174. 173. 
    Pichoff S, Lutkenhaus J. 2007. Identification of a region of FtsA required for interaction with FtsZ. Mol. Microbiol. 64:1129–38
    [Google Scholar]
  175. 174. 
    Popp D, Iwasa M, Narita A, Erickson HP, Maéda Y 2009. FtsZ condensates: an in vitro electron microscopy study. Biopolymers 91:340–50
    [Google Scholar]
  176. 175. 
    Rajagopala SV, Sikorski P, Kumar A, Mosca R, Vlasblom J et al. 2014. The binary protein-protein interaction landscape of Escherichia coli.. Nat. Biotechnol 32:285–90
    [Google Scholar]
  177. 176. 
    Ramirez-Diaz D, Merino-Salomon A, Heymann M, Schwille P 2019. Bidirectional FtsZ filament treadmilling promotes membrane constriction via torsional stress. bioRxiv 587790. https://doi.org/10.1101/587790
    [Crossref]
  178. 177. 
    Ramirez-Diaz DA, García-Soriano DA, Raso A, Mücksch J, Feingold M et al. 2018. Treadmilling analysis reveals new insights into dynamic FtsZ ring architecture. PLOS Biol 16:e2004845
    [Google Scholar]
  179. 178. 
    Rand-Heredia J, Yu HH, Carlo S, Lesser CF, Janakiraman A 2011. Identification and characterization of ZapC, a stabilizer of the FtsZ ring in Escherichia coli. J. . Bacteriol 193:1405–13
    [Google Scholar]
  180. 179. 
    RayChaudhuri D, Park JT. 1992. Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359:251–54
    [Google Scholar]
  181. 180. 
    Raymond A, Lovell S, Lorimer D, Walchli J, Mixon M et al. 2009. Combined protein construct and synthetic gene engineering for heterologous protein expression and crystallization using Gene Composer. BMC Biotechnol 9:37
    [Google Scholar]
  182. 181. 
    Roach EJ, Kimber MS, Khursigara CM 2014. Crystal structure and site-directed mutational analysis reveals key residues involved in Escherichia coli ZapA function. J. Biol. Chem. 289:23276–86
    [Google Scholar]
  183. 182. 
    Romberg L, Levin P. 2003. Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu. Rev. Microbiol. 57:125–54
    [Google Scholar]
  184. 183. 
    Romberg L, Simon M, Erickson HP 2001. Polymerization of FtsZ, a bacterial homolog of tubulin: Is assembly cooperative?. J. Biol. Chem. 276:11743–53
    [Google Scholar]
  185. 184. 
    Rowlett V, Margolin W. 2013. The bacterial Min system. Curr. Biol. 23:R553–56
    [Google Scholar]
  186. 185. 
    Rowlett V, Margolin W. 2014. 3D-SIM super-resolution of FtsZ and its membrane tethers in Escherichia coli cells. Biophys. J. 107:L17–20
    [Google Scholar]
  187. 186. 
    Ruiz N. 2008. Bioinformatics identification of MurJ (MviN) as the peptidoglycan lipid II flippase in Escherichia coli. . PNAS 105:15553–57
    [Google Scholar]
  188. 187. 
    Salje J, Zuber B, Löwe J 2009. Electron cryomicroscopy of E. coli reveals filament bundles involved in plasmid DNA segregation. Science 323:509–12
    [Google Scholar]
  189. 188. 
    Sauvage E, Terrak M. 2016. Glycosyltransferases and transpeptidases/penicillin-binding proteins: valuable targets for new antibacterials. Antibiotics 5:12
    [Google Scholar]
  190. 189. 
    Scheffers DJ, de Wit JG, den Blaauwen T, Driessen AJM 2002. GTP hydrolysis of cell division protein FtsZ: evidence that the active site is formed by the association of monomers. Biochemistry 41:521–29
    [Google Scholar]
  191. 190. 
    Scheffers DJ, Driessen A. 2001. The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS Lett 506:6–10
    [Google Scholar]
  192. 191. 
    Schmidt KL, Peterson ND, Kustusch RJ, Wissel MC, Graham B et al. 2004. A predicted ABC transporter, FtsEX, is needed for cell division in Escherichia coli. J. . Bacteriol 186:785–93
    [Google Scholar]
  193. 192. 
    Schneider T, Sahl H-G. 2010. An oldie but a goodie: cell wall biosynthesis as antibiotic target pathway. Int. J. Med. Microbiol. 300:161–69
    [Google Scholar]
  194. 193. 
    Sham LT, Butler EK, Lebar MD, Kahne D, Bernhardt TG, Ruiz N 2014. Bacterial cell wall. MurJ is the flippase of lipid-linked precursors for peptidoglycan biogenesis. Science 345:220–22
    [Google Scholar]
  195. 194. 
    Shi H, Bratton BP, Gitai Z, Huang K 2018. How to build a bacterial cell: MreB as the foreman of E. coli construction. Cell 172:1294–305
    [Google Scholar]
  196. 195. 
    Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM et al. 2009. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. PNAS 106:3125–30
    [Google Scholar]
  197. 196. 
    Singh J, Makde RD, Kumar V, Panda D 2008. SepF increases the assembly and bundling of FtsZ polymers and stabilizes FtsZ protofilaments by binding along its length. J. Biol. Chem. 283:31116–24
    [Google Scholar]
  198. 197. 
    Small E, Addinall SG. 2003. Dynamic FtsZ polymerization is sensitive to the GTP to GDP ratio and can be maintained at steady state using a GTP-regeneration system. Microbiology 149:2235–42
    [Google Scholar]
  199. 198. 
    Small E, Marrington R, Rodger A, Scott DJ, Sloan K et al. 2007. FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J. Mol. Biol. 369:210–21
    [Google Scholar]
  200. 199. 
    Söderström B, Chan H, Shilling PJ, Skoglund U, Daley DO 2018. Spatial separation of FtsZ and FtsN during cell division. Mol. Microbiol. 107:387–401
    [Google Scholar]
  201. 200. 
    Söderström B, Mirzadeh K, Toddo S, van Heijne G, Skoglund U, Daley DO 2016. Coordinated disassembly of the divisome complex in Escherichia coli. Mol. Microbiol 101:425–38
    [Google Scholar]
  202. 201. 
    Söderström B, Skoog K, Blom H, Weiss DS, von Heijne G, Daley DO 2014. Disassembly of the divisome in Escherichia coli: evidence that FtsZ dissociates before compartmentalization. Mol. Microbiol. 92:1–9
    [Google Scholar]
  203. 202. 
    Stock J, Rauch B, Roseman S 1977. Periplasmic space in Salmonella typhimurium and Escherichia coli. J. Biol. Chem 252:7850–61
    [Google Scholar]
  204. 203. 
    Stouf M, Meile J-C, Cornet F 2013. FtsK actively segregates sister chromosomes in Escherichia coli. . PNAS 110:11157–62
    [Google Scholar]
  205. 204. 
    Strauss MP, Liew AT, Turnbull L, Whitchurch CB, Monahan LG, Harry EJ 2012. 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLOS Biol 10:e1001389
    [Google Scholar]
  206. 205. 
    Stricker J, Maddox P, Salmon E, Erickson HP 2002. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. PNAS 99:3171–75
    [Google Scholar]
  207. 206. 
    Sun N, Lu YJ, Chan FY, Du RL, Zheng YY et al. 2017. A thiazole orange derivative targeting the bacterial protein FtsZ shows potent antibacterial activity. Front. Microbiol. 8:855
    [Google Scholar]
  208. 207. 
    Sun Q, Margolin W. 1998. FtsZ dynamics during the division cycle of live Escherichia coli cells. J. Bacteriol. 180:2050–56
    [Google Scholar]
  209. 208. 
    Sundararajan K, Goley ED. 2017. The intrinsically disordered C-terminal linker of FtsZ regulates protofilament dynamics and superstructure in vitro. J. Biol. Chem. 292:20509–27
    [Google Scholar]
  210. 209. 
    Sundararajan K, Miguel A, Desmarais SM, Meier EL, Huang KC, Goley ED 2015. The bacterial tubulin FtsZ requires its intrinsically disordered linker to direct robust cell wall construction. Nat. Commun. 6:7281
    [Google Scholar]
  211. 210. 
    Sundararajan K, Vecchiarelli A, Mizuuchi K, Goley ED 2018. Species- and C-terminal linker-dependent variations in the dynamic behavior of FtsZ on membranes in vitro. Mol. Microbiol. 110:47–63
    [Google Scholar]
  212. 211. 
    Surovtsev IV, Morgan JJ, Lindahl PA 2008. Kinetic modeling of the assembly, dynamic steady state, and contraction of the FtsZ ring in prokaryotic cytokinesis. PLOS Comput. Biol. 4:e1000102
    [Google Scholar]
  213. 212. 
    Szwedziak P, Wang Q, Bharat TA, Tsim M, Löwe J 2014. Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. eLife 3:e04601
    [Google Scholar]
  214. 212a. 
    Taguchi A, Welsh MA, Marmont LS, Lee W, Sjodt Met al. 2019. FtsW is a peptidoglycan polymerase that is functional only in complex with its cognate penicillin-binding protein. Nat. Microbiol 4:587–94
    [Google Scholar]
  215. 213. 
    Tan CM, Therien AG, Lu J, Lee SH, Caron A et al. 2012. Restoring methicillin-resistant Staphylococcus aureus susceptibility to β-lactam antibiotics. Sci. Transl. Med. 4:126ra35
    [Google Scholar]
  216. 214. 
    Thanedar S, Margolin W. 2004. FtsZ exhibits rapid movement and oscillation waves in helix-like patterns in Escherichia coli. Curr. Biol 14:1167–73
    [Google Scholar]
  217. 215. 
    Tomoyasu T, Gamer J, Bukau B, Kanemori M, Mori H et al. 1995. Escherichia coli FtsH is a membrane-bound, ATP-dependent protease which degrades the heat-shock transcription factor sigma 32. EMBO J 14:2551–60
    [Google Scholar]
  218. 216. 
    Tomoyasu T, Yamanaka K, Murata K, Suzaki T, Bouloc P et al. 1993. Topology and subcellular localization of FtsH protein in Escherichia coli. J. Bacteriol 175:1352–57
    [Google Scholar]
  219. 217. 
    Tsang MJ, Yakhnina AA, Bernhardt TG 2017. NlpD links cell wall remodeling and outer membrane invagination during cytokinesis in Escherichia coli. . PLOS Genet 13:e1006888
    [Google Scholar]
  220. 218. 
    Typas A, Banzhaf M, Gross CA, Vollmer W 2011. From the regulation of peptidoglycan synthesis to bacterial growth and morphology. Nat. Rev. Microbiol. 10:123–36
    [Google Scholar]
  221. 219. 
    Typas A, Banzhaf M, van den Berg van Saparoea B, Verheul J, Biboy J et al. 2010. Regulation of peptidoglycan synthesis by outer-membrane proteins. Cell 143:1097–109
    [Google Scholar]
  222. 220. 
    Uehara T, Dinh T, Bernhardt TG 2009. LytM-domain factors are required for daughter cell separation and rapid ampicillin-induced lysis in Escherichia coli. J. Bacteriol 191:5094–107
    [Google Scholar]
  223. 221. 
    Uehara T, Parzych KR, Dinh T, Bernhardt TG 2010. Daughter cell separation is controlled by cytokinetic ring-activated cell wall hydrolysis. EMBO J 29:1412–22
    [Google Scholar]
  224. 222. 
    van den Ent F, Amos LA, Löwe J 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413:39–44
    [Google Scholar]
  225. 223. 
    van den Ent F, Löwe J 2000. Crystal structure of the cell division protein FtsA from Thermotoga maritima. . EMBO J 19:5300–7
    [Google Scholar]
  226. 224. 
    van Mameren J, Vermeulen KC, Gittes F, Schmidt CF 2009. Leveraging single protein polymers to measure flexural rigidity. J. Phys. Chem. B 113:3837–44
    [Google Scholar]
  227. 225. 
    Varma A, de Pedro MA, Young KD 2007. FtsZ directs a second mode of peptidoglycan synthesis in Escherichia coli. J. Bacteriol 189:5692–704
    [Google Scholar]
  228. 226. 
    Vermassen A, Leroy S, Talon R, Provot C, Popowska M, Desvaux M 2019. Cell wall hydrolases in bacteria: insight on the diversity of cell wall amidases, glycosidases and peptidases toward peptidoglycan. Front. Microbiol. 10:331
    [Google Scholar]
  229. 227. 
    Vicente M, Gomez M, Ayala J 1998. Regulation of transcription of cell division genes in the Escherichia coli dcw cluster. Cell Mol. Life Sci. 54:317–24
    [Google Scholar]
  230. 228. 
    Virant D, Turkowyd B, Balinovic A, Endesfelder U 2017. Combining primed photoconversion and UV-photoactivation for aberration-free, live-cell compliant multi-color single-molecule localization microscopy imaging. Int. J. Mol. Sci. 18:1524
    [Google Scholar]
  231. 229. 
    Vollmer W. 2007. Structure and biosynthesis of the murein (peptidoglycan) sacculus. The Periplasm M Ehrmann 198–213 Sterling, VA: ASM Press
    [Google Scholar]
  232. 230. 
    Vollmer W, Blanot D, de Pedro MA 2008. Peptidoglycan structure and architecture. FEMS Microbiol. Rev. 32:149–67
    [Google Scholar]
  233. 231. 
    Vollmer W, Joris B, Charlier P, Foster S 2008. Bacterial peptidoglycan (murein) hydrolases. FEMS Microbiol. Rev. 32:259–86
    [Google Scholar]
  234. 232. 
    Wachi M, Okada IY, Matsuhashi M 1989. New mre genes mreC and mreD, responsible for formation of the rod shape of Escherichia coli cells. J. Bacteriol. 171:6511–16
    [Google Scholar]
  235. 233. 
    Weidel W, Pelzer H. 1964. Bagshaped macromolecules: a new outlook on bacterial cell. Adv. Enzymol. 26:193–232
    [Google Scholar]
  236. 234. 
    Weiss DS. 2004. Bacterial cell division and the septal ring. Mol. Microbiol. 54:588–97
    [Google Scholar]
  237. 235. 
    Woldemeskel S, McQuillen R, Hessel AM, Xiao J, Goley ED 2017. A conserved coiled-coil protein pair focuses the cytokinetic Z-ring in Caulobacter crescentus. Mol. . Microbiol 105:721–40
    [Google Scholar]
  238. 236. 
    Xiao J, Dufrêne YF. 2016. Optical and force nanoscopy in microbiology. Nat. Microbiol. 1:16186
    [Google Scholar]
  239. 237. 
    Xiao J, Goley ED. 2016. Redefining the roles of the FtsZ-ring in bacterial cytokinesis. Curr. Opin. Microbiol. 34:90–96
    [Google Scholar]
  240. 238. 
    Yang DC, Peters NT, Parzych KR, Uehara T, Markovski M, Bernhardt TG 2011. An ATP-binding cassette transporter-like complex governs cell-wall hydrolysis at the bacterial cytokinetic ring. PNAS 108:E1052–60
    [Google Scholar]
  241. 239. 
    Yang X, Lyu Z, Miguel A, McQuillen R, Huang KC, Xiao J 2017. GTPase activity-coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis. Science 355:744–47
    [Google Scholar]
  242. 240. 
    Yang X, McQuillen R, Lyu Z, Phillips-Mason P, De La Cruz A et al. 2019. FtsW exhibits distinct processive movements driven by either septal cell wall synthesis or FtsZ treadmilling in E. coli. bioRxiv 850073. https://doi.org/10.1101/850073
    [Crossref]
  243. 241. 
    Yao Q, Jewett AI, Chang YW, Oikonomou CM, Beeby M et al. 2017. Short FtsZ filaments can drive asymmetric cell envelope constriction at the onset of bacterial cytokinesis. EMBO J 36:1577–89
    [Google Scholar]
  244. 242. 
    Yi Q-M, Lutkenhaus J. 1985. The nucleotide sequence of the essential cell-division gene ftsZ of Escherichia coli. . Gene 36:241–47
    [Google Scholar]
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