Publikationsserver der Universitätsbibliothek Marburg
Titel:Biochemistry of the key spatial regulators MipZ and PopZ in Caulobacter crescentus
Autor:Refes, Yacine
Weitere Beteiligte: Thanbichler, Martin (Prof. Dr)
Veröffentlicht:2018
URI:https://archiv.ub.uni-marburg.de/diss/z2018/0079
URN: urn:nbn:de:hebis:04-z2018-00794
DOI: https://doi.org/10.17192/z2018.0079
DDC:570 Biowissenschaften, Biologie
Titel (trans.):Biochemie der wichtigsten räumlichen Regulatoren MipZ und PopZ in Caulobacter crescentus
Publikationsdatum:2018-10-15
Lizenz:https://creativecommons.org/licenses/by-nc-nd/4.0/

Dokument

Schlagwörter:
PopZ, Cell division, PopZ, Chromosomensegregation, MipZ, MipZ, Chromosomensegregation, MipZ, Chromosome segregation, Caulobacter crescentus, Zellteilung, Caulobacter crescentus, Caulobacter crescentus, PopZ, Zellteilung

Summary:
Bacteria are known to tightly control the spatial distribution of certain proteins by positioning them to distinct regions of the cell, particularly the cell poles. These regions represent important organizing platforms for several processes essential for bacterial survival and reproduction. The proteins localized at the cell poles are recruited to these positions by interaction with other polar proteins or protein complexes. The α-proteobacterium Caulobacter crescentus possesses a self-organizing polymeric polar matrix constituted of the scaffolding protein PopZ. PopZ recruits to the cell poles several proteins involved in various essential processes such as chromosome segregation and the regulation of cell division. This latter process is controlled by the spatial regulator MipZ, which coordinates chromosome segregation with cell division. The two essential proteins PopZ and MipZ both physically interact with the centromere binding protein ParB, an essential element of the chrosomome segregation system of Caulobacter crescentus. The main function of the ATPase MipZ is to position the cell division apparatus by spatially restricting the localization of the key cell division protein FtsZ to midcell. MipZ accomplishes this function by interacting with chromosomal DNA and forming a shallow gradient, with a high concentration at the cell poles and a low concentration near the midcell, therefore permitting FtsZ polymerization solely at midcell. The formation of the MipZ bipolar gradient is intimately linked to the establishment of the multimeric matrix PopZ at the cell poles, which insures the anchorage of ParB-parS complexes at the cell poles. In this study, we have uncovered the inhibitory mode of action of the polar element MipZ on FtsZ polymerization and identified the interaction regions of MipZ with its three interaction partners, ParB, FtsZ and the chromosomal DNA. We found that similarly to the FtsZ assembly inhibitor from Escherichia coli MinC, MipZ is capable of inhibiting FtsZ polymerization as well as shortening FtsZ polymers into smaller oligomers. Our results show also that the inhibitory effect of MipZ on FtsZ polymerization is independent of its ability to stimulate the FtsZ GTPase activity. Mapping of the binding interfaces of MipZ revealed that the DNA- and ParB-binding regions are overlapping and mainly constituted of positively charged residues, whereas two distinct regions appear to be involved in FtsZ-binding. We also purified the polar factor PopZ from soluble fractions and provided relevant data related to its secondary structure composition and its assembly into higher-order structures. Our in vitro analysis on PopZ, revealed among others that it is mainly composed of α-helices and unstructured regions and forms relatively straight filament-like structures differing from what was previously reported. Altogether, the data obtained in this work bring more knowledge about two key elements of C. crescentus.

Bibliographie / References

  1. 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.
  2. Rowlett VW, Margolin W. 2014. 3D-SIM super-resolution of FtsZ and its membrane tethers in Escherichia coli cells. Biophys J 107:L17-20.
  3. Karimova G, Pidoux J, Ullmann A, Ladant D. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proceedings of the National Academy of Sciences of the United States of America 95:5752-5756.
  4. Veiga H, Jorge AM, Pinho MG. 2011. Absence of nucleoid occlusion effector Noc impairs formation of orthogonal FtsZ rings during Staphylococcus aureus cell division. Mol Microbiol 80:1366-1380.
  5. Thanbichler M, Iniesta AA, Shapiro L. 2007. A comprehensive set of plasmids for vanillate-and xylose-inducible gene expression in Caulobacter crescentus. Nucleic Acids Res 35:e137.
  6. Woldemeskel SA, 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.
  7. Hu Z, Lutkenhaus J. 2003. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol Microbiol 47:345- 355.
  8. Ingerman E, Nunnari J. 2005. A continuous, regenerative coupled GTPase assay for dynamin-related proteins. Methods Enzymol 404:611-619.
  9. Lam H, Schofield WB, Jacobs-Wagner C. 2006. A landmark protein essential for establishing and perpetuating the polarity of a bacterial cell. Cell 124:1011-1023.
  10. Perez AM, Mann TH, Lasker K, Ahrens DG, Eckart MR, Shapiro L. 2017. A Localized complex of two protein oligomers controls the orientation of cell polarity. MBio 8.
  11. Hu Z, Lutkenhaus J. 2000. Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J Bacteriol 182:3965-3971.
  12. Zhou H, Schulze R, Cox S, Saez C, Hu Z, Lutkenhaus J. 2005. Analysis of MinD mutations reveals residues required for MinE stimulation of the MinD ATPase and residues required for MinC interaction. J Bacteriol 187:629-638.
  13. Walshaw J, Gillespie MD, Kelemen GH. 2010. A novel coiled-coil repeat variant in a class of bacterial cytoskeletal proteins. Journal of structural biology 170:202-215.
  14. Bramkamp M, Emmins R, Weston L, Donovan C, Daniel RA, Errington J. 2008. A novel component of the division-site selection system of Bacillus subtilis and a new mode of action for the division inhibitor MinCD. Mol Microbiol 70:1556-1569.
  15. Hay NA, Tipper DJ, Gygi D, Hughes C. 1999. A novel membrane protein influencing cell shape and multicellular swarming of Proteus mirabilis. J Bacteriol 181:2008-2016.
  16. Waidner B, Specht M, Dempwolff F, Haeberer K, Schaetzle S, Speth V, Kist M, Graumann PL. 2009. A novel system of cytoskeletal elements in the human pathogen Helicobacter pylori. PLoS Pathog 5:e1000669.
  17. Kraemer JA, Erb ML, Waddling CA, Montabana EA, Zehr EA, Wang H, Nguyen K, Pham DS, Agard DA, Pogliano J. 2012. A phage tubulin assembles dynamic filaments by an atypical mechanism to center viral DNA within the host cell. Cell 149:1488-1499.
  18. Bowman GR, Comolli LR, Zhu J, Eckart M, Koenig M, Downing KH, Moerner WE, Earnest T, Shapiro L. 2008. A polymeric protein anchors the chromosomal origin/ParB complex at a bacterial cell pole. Cell 134:945-955.
  19. Volkov A, Mascarenhas J, Andrei-Selmer C, Ulrich HD, Graumann PL. 2003. A prokaryotic condensin/cohesin-like complex can actively compact chromosomes from a single position on the nucleoid and binds to DNA as a ring-like structure. Mol Cell Biol 23:5638-5650.
  20. Barilla D, Hayes F. 2003. Architecture of the ParF*ParG protein complex involved in prokaryotic DNA segregation. Mol Microbiol 49:487-499.
  21. Szwedziak P, Wang Q, Bharat TA, Tsim M, Lowe J. 2014. Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. eLife 3:e04601.
  22. Cambridge J, Blinkova A, Magnan D, Bates D, Walker JR. 2014. A replication- inhibited unsegregated nucleoid at mid-cell blocks Z-ring formation and cell division independently of SOS and the SlmA nucleoid occlusion protein in Escherichia coli. J Bacteriol 196:36-49.
  23. Tsang MJ, Bernhardt TG. 2015. A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division. Mol Microbiol 95:925-944.
  24. Ebersbach G, Briegel A, Jensen GJ, Jacobs-Wagner C. 2008. A self-associating protein critical for chromosome attachment, division, and polar organization in Caulobacter. Cell 134:956-968.
  25. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, Comolli LR, Moerner WE, Shapiro L. 2010. A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12:791-798.
  26. Koonin EV. 1993. A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. J Mol Biol 229:1165-1174.
  27. Donovan C, Sieger B, Kramer R, Bramkamp M. 2012. A synthetic Escherichia coli system identifies a conserved origin tethering factor in Actinobacteria. Mol Microbiol 84:105-116.
  28. Vecchiarelli AG, Han YW, Tan X, Mizuuchi M, Ghirlando R, Biertumpfel C, Funnell BE, Mizuuchi K. 2010. ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol Microbiol 78:78-91.
  29. Wang X, Montero Llopis P, Rudner DZ. 2014. Bacillus subtilis chromosome organization oscillates between two distinct patterns. Proceedings of the National Academy of Sciences of the United States of America 111:12877-12882.
  30. Gregory JA, Becker EC, Pogliano K. 2008. Bacillus subtilis MinC destabilizes FtsZ- rings at new cell poles and contributes to the timing of cell division. Genes Dev 22:3475- 3488.
  31. Wang X, Brandao HB, Le TB, Laub MT, Rudner DZ. 2017. Bacillus subtilis SMC complexes juxtapose chromosome arms as they travel from origin to terminus. Science 355:524-527.
  32. Koch MK, McHugh CA, Hoiczyk E. 2011. BacM, an N-terminally processed bactofilin of Myxococcus xanthus, is crucial for proper cell shape. Mol Microbiol 80:1031-1051.
  33. Huitema E, Pritchard S, Matteson D, Radhakrishnan SK, Viollier PH. 2006. Bacterial birth scar proteins mark future flagellum assembly site. Cell 124:1025-1037.
  34. Adams DW, Errington J. 2009. Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7:642-653.
  35. Leonard TA, Butler PJ, Lowe J. 2005. Bacterial chromosome segregation: structure and DNA binding of the Soj dimer--a conserved biological switch. EMBO J 24:270-282.
  36. Lutkenhaus J, Pichoff S, Du S. 2012. Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton (Hoboken) 69:778-790.
  37. Ptacin JL, Gahlmann A, Bowman GR, Perez AM, von Diezmann AR, Eckart MR, Moerner WE, Shapiro L. 2014. Bacterial scaffold directs pole-specific centromere segregation. Proceedings of the National Academy of Sciences of the United States of America 111:E2046-2055.
  38. Kuhn J, Briegel A, Morschel E, Kahnt J, Leser K, Wick S, Jensen GJ, Thanbichler M. 2010. Bactofilins, a ubiquitous class of cytoskeletal proteins mediating polar localization of a cell wall synthase in Caulobacter crescentus. EMBO J 29:327-339.
  39. Poindexter JS. 1964. Biological Properties and Classification of the Caulobacter Group. Bacteriol Rev 28:231-295.
  40. Caulobacter PopZ forms an intrinsically disordered hub in organizing bacterial cell poles. Proceedings of the National Academy of Sciences of the United States of America 113:12490-12495.
  41. Bowman GR, Comolli LR, Gaietta GM, Fero M, Hong SH, Jones Y, Lee JH, Downing KH, Ellisman MH, McAdams HH, Shapiro L. 2010. Caulobacter PopZ forms a polar subdomain dictating sequential changes in pole composition and function. Mol Microbiol 76:173-189.
  42. Mohl DA, Gober JW. 1997. Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus. Cell 88:675-684.
  43. Skerker JM, Laub MT. 2004. Cell-cycle progression and the generation of asymmetry in Caulobacter crescentus. Nat Rev Microbiol 2:325-337.
  44. Galli E, Poidevin M, Le Bars R, Desfontaines JM, Muresan L, Paly E, Yamaichi Y, Barre FX. 2016. Cell division licensing in the multi-chromosomal Vibrio cholerae bacterium. Nat Microbiol 1:16094.
  45. Vecchiarelli AG, Hwang LC, Mizuuchi K. 2013. Cell-free study of F plasmid partition provides evidence for cargo transport by a diffusion-ratchet mechanism. Proceedings of the National Academy of Sciences of the United States of America 110:E1390-1397.
  46. Eswaramoorthy P, Erb ML, Gregory JA, Silverman J, Pogliano K, Pogliano J, Ramamurthi KS. 2011. Cellular architecture mediates DivIVA ultrastructure and regulates min activity in Bacillus subtilis. MBio 2.
  47. Eisheuer S. 2016. Characterization of the division apparatus in the budding bacterium Hyphomonas neptunium. Doctoral thesis. Philipps-Universität Marburg.
  48. Ouellette SP, Karimova G, Subtil A, Ladant D. 2012. Chlamydia co-opts the rod shape-determining proteins MreB and Pbp2 for cell division. Mol Microbiol 85:164-178.
  49. Marczynski GT. 1999. Chromosome methylation and measurement of faithful, once and only once per cell cycle chromosome replication in Caulobacter crescentus. J Bacteriol 181:1984-1993.
  50. van Raaphorst R, Kjos M, Veening JW. 2017. Chromosome segregation drives division site selection in Streptococcus pneumoniae. Proceedings of the National Academy of Sciences of the United States of America 114:E5959-E5968.
  51. Chemes LB, Alonso LG, Noval MG, de Prat-Gay G. 2012. Circular dichroism techniques for the analysis of intrinsically disordered proteins and domains. Methods Mol Biol 895:387-404.
  52. Laemmli UK. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
  53. Lan G, Daniels BR, Dobrowsky TM, Wirtz D, Sun SX. 2009. Condensation of FtsZ filaments can drive bacterial cell division. Proceedings of the National Academy of Sciences of the United States of America 106:121-126.
  54. Knopp J. 2017. Construction and characterization of 16 mipZ mutants of Caulobacter crescentus. Bachelor thesis. Philipps-Universität Marburg.
  55. Yu W, Herbert S, Graumann PL, Gotz F. 2010. Contribution of SMC (structural maintenance of chromosomes) and SpoIIIE to chromosome segregation in Staphylococci. J Bacteriol 192:4067-4073.
  56. Jones LJ, Carballido-Lopez R, Errington J. 2001. Control of cell shape in bacteria: helical, actin-like filaments in Bacillus subtilis. Cell 104:913-922.
  57. Quisel JD, Lin DC, Grossman AD. 1999. Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell 4:665-672.
  58. Wu LJ, Errington J. 2004. Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117:915-925.
  59. Ely B, Scott LE. 2014. Correction of the Caulobacter crescentus NA1000 genome annotation. PLoS One 9:e91668.
  60. Garner EC, Bernard R, Wang W, Zhuang X, Rudner DZ, Mitchison T. 2011. Coupled, circumferential motions of the cell wall synthesis machinery and MreB filaments in B. subtilis. Science 333:222-225.
  61. Lowe J, Amos LA. 1998. Crystal structure of the bacterial cell-division protein FtsZ. Nature 391:203-206.
  62. Cordell SC, Lowe J. 2001. Crystal structure of the bacterial cell division regulator MinD. FEBS Lett 492:160-165.
  63. Ramirez-Arcos S, Szeto J, Beveridge T, Victor C, Francis F, Dillon J. 2001. Deletion of the cell-division inhibitor MinC results in lysis of Neisseria gonorrhoeae. Microbiology 147:225-237.
  64. Wu W, Park KT, Holyoak T, Lutkenhaus J. 2011. Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC. Mol Microbiol 79:1515-1528.
  65. Alexeeva S, Gadella TW, Jr., 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 77:384-398.
  66. Livny J, Yamaichi Y, Waldor MK. 2007. Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189:8693-8703.
  67. Goehring NW, Beckwith J. 2005. Diverse paths to midcell: assembly of the bacterial cell division machinery. Curr Biol 15:R514-526.
  68. Letek M, Ordonez E, Vaquera J, Margolin W, Flardh K, Mateos LM, Gil JA. 2008. DivIVA is required for polar growth in the MreB-lacking rod-shaped actinomycete Corynebacterium glutamicum. J Bacteriol 190:3283-3292.
  69. Hu Z, Gogol EP, Lutkenhaus J. 2002. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proceedings of the National Academy of Sciences of the United States of America 99:6761-6766.
  70. Murray H, Errington J. 2008. Dynamic control of the DNA replication initiation protein DnaA by Soj/ParA. Cell 135:74-84.
  71. Ditkowski B, Holmes N, Rydzak J, Donczew M, Bezulska M, Ginda K, Kedzierski P, Zakrzewska-Czerwinska J, Kelemen GH, Jakimowicz D. 2013. Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor. Open biology 3:130006.
  72. Glaser P, Sharpe ME, Raether B, Perego M, Ohlsen K, Errington J. 1997. Dynamic, mitotic-like behavior of a bacterial protein required for accurate chromosome partitioning. Genes Dev 11:1160-1168.
  73. Marston AL, Errington J. 1999. Dynamic movement of the ParA-like Soj protein of B. subtilis and its dual role in nucleoid organization and developmental regulation. Mol Cell 4:673-682.
  74. Graumann PL, Knust T. 2009. Dynamics of the bacterial SMC complex and SMC-like proteins involved in DNA repair. Chromosome Res 17:265-275.
  75. Harry EJ, Lewis PJ. 2003. Early targeting of Min proteins to the cell poles in germinated spores of Bacillus subtilis: evidence for division apparatus-independent recruitment of Min proteins to the division site. Mol Microbiol 47:37-48.
  76. Jun S, Mulder B. 2006. Entropy-driven spatial organization of highly confined polymers: lessons for the bacterial chromosome. Proceedings of the National Academy of Sciences of the United States of America 103:12388-12393.
  77. Evinger M, Agabian N. 1977. Envelope-associated nucleoid from Caulobacter crescentus stalked and swarmer cells. J Bacteriol 132:294-301.
  78. Pichoff S, Lutkenhaus J. 2001. Escherichia coli division inhibitor MinCD blocks septation by preventing Z-ring formation. J Bacteriol 183:6630-6635.
  79. Flardh K. 2003. Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol Microbiol 49:1523-1536.
  80. Lim HC, Surovtsev IV, Beltran BG, Huang F, Bewersdorf J, Jacobs-Wagner C. 2014. Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation. eLife 3:e02758.
  81. Bailey MW, Bisicchia P, Warren BT, Sherratt DJ, Mannik J. 2014. Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLoS Genet 10:e1004504.
  82. Hernandez-Rocamora VM, Alfonso C, Margolin W, Zorrilla S, Rivas G. 2015. Evidence That Bacteriophage lambda Kil Peptide Inhibits Bacterial Cell Division by Disrupting FtsZ Protofilaments and Sequestering Protein Subunits. J Biol Chem 290:20325-20335.
  83. Shen B, Lutkenhaus J. 2010. Examination of the interaction between FtsZ and MinCN in E. coli suggests how MinC disrupts Z rings. Mol Microbiol 75:1285-1298.
  84. Oliva MA, Halbedel S, Freund SM, Dutow P, Leonard TA, Veprintsev DB, Hamoen LW, Lowe J. 2010. Features critical for membrane binding revealed by DivIVA crystal structure. EMBO J 29:1988-2001.
  85. Banigan EJ, Gelbart MA, Gitai Z, Wingreen NS, Liu AJ. 2011. Filament depolymerization can explain chromosome pulling during bacterial mitosis. PLoS Comput Biol 7:e1002145.
  86. Aylett CH, Wang Q, Michie KA, Amos LA, Lowe J. 2010. Filament structure of bacterial tubulin homologue TubZ. Proceedings of the National Academy of Sciences of the United States of America 107:19766-19771.
  87. Meier EL, Goley ED. 2014. Form and function of the bacterial cytokinetic ring. Curr Opin Cell Biol 26:19-27.
  88. Szwedziak P, Wang Q, Freund SM, Lowe J. 2012. FtsA forms actin-like protofilaments. EMBO J 31:2249-2260.
  89. Bigot S, Sivanathan V, Possoz C, Barre FX, Cornet F. 2007. FtsK, a literate chromosome segregation machine. Mol Microbiol 64:1434-1441.
  90. Erickson HP. 1995. FtsZ, a prokaryotic homolog of tubulin? Cell 80:367-370.
  91. Bisson-Filho AW, Discola KF, Castellen P, Blasios V, Martins A, Sforca ML, Garcia W, Zeri AC, Erickson HP, Dessen A, Gueiros-Filho FJ. 2015. FtsZ filament capping by MciZ, a developmental regulator of bacterial division. Proceedings of the National Academy of Sciences of the United States of America 112:E2130-2138.
  92. Erickson HP, Anderson DE, Osawa M. 2010. FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74:504-528.
  93. Krol E, Scheffers DJ. 2013. FtsZ polymerization assays: simple protocols and considerations. Journal of visualized experiments: JoVE:e50844.
  94. Mignolet J, Holden S, Berge M, Panis G, Eroglu E, Theraulaz L, Manley S, Viollier PH. 2016. Functional dichotomy and distinct nanoscale assemblies of a cell cycle- controlled bipolar zinc-finger regulator. eLife 5.
  95. Lukaszewicz M, Kostelidou K, Bartosik AA, Cooke GD, Thomas CM, Jagura- Burdzy G. 2002. Functional dissection of the ParB homologue (KorB) from IncP-1 plasmid RK2. Nucleic Acids Res 30:1046-1055.
  96. Jenkins C, Samudrala R, Anderson I, Hedlund BP, Petroni G, Michailova N, Pinel N, Overbeek R, Rosati G, Staley JT. 2002. Genes for the cytoskeletal protein tubulin in the bacterial genus Prosthecobacter. Proceedings of the National Academy of Sciences of the United States of America 99:17049-17054.
  97. Autret S, Nair R, Errington J. 2001. Genetic analysis of the chromosome segregation protein Spo0J of Bacillus subtilis: evidence for separate domains involved in DNA binding and interactions with Soj protein. Mol Microbiol 41:743-755.
  98. Ma X, Margolin W. 1999. Genetic and functional analyses of the conserved C-terminal core domain of Escherichia coli FtsZ. J Bacteriol 181:7531-7544.
  99. Szeto J, Ramirez-Arcos S, Raymond C, Hicks LD, Kay CM, Dillon JA. 2001. Gonococcal MinD affects cell division in Neisseria gonorrhoeae and Escherichia coli and exhibits a novel self-interaction. J Bacteriol 183:6253-6264.
  100. Ireton K, Gunther NWt, Grossman AD. 1994. spo0J is required for normal chromosome segregation as well as the initiation of sporulation in Bacillus subtilis. J Bacteriol 176:5320-5329.
  101. McCormick JR, Su EP, Driks A, Losick R. 1994. Growth and viability of Streptomyces coelicolor mutant for the cell division gene ftsZ. Mol Microbiol 14:243-254.
  102. Holden SJ, Pengo T, Meibom KL, Fernandez Fernandez C, Collier J, Manley S. 2014. High throughput 3D super-resolution microscopy reveals Caulobacter crescentus in vivo Z-ring organization. Proceedings of the National Academy of Sciences of the United States of America 111:4566-4571.
  103. Skerker JM, Shapiro L. 2000. Identification and cell cycle control of a novel pilus system in Caulobacter crescentus. EMBO J 19:3223-3234.
  104. Lin DC, Grossman AD. 1998. Identification and characterization of a bacterial chromosome partitioning site. Cell 92:675-685.
  105. Cho H, Bernhardt TG. 2013. Identification of the SlmA active site responsible for blocking bacterial cytokinetic ring assembly over the chromosome. PLoS Genet 9:e1003304.
  106. Goley ED, Dye NA, Werner JN, Gitai Z, Shapiro L. 2010. Imaging-based identification of a critical regulator of FtsZ protofilament curvature in Caulobacter. Mol Cell 39:975-987.
  107. Kim SK, Shim J. 1999. Interaction between F plasmid partition proteins SopA and SopB. Biochem Biophys Res Commun 263:113-117.
  108. Bagchi S, Tomenius H, Belova LM, Ausmees N. 2008. Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol Microbiol 70:1037- 1050.
  109. Rico AI, Krupka M, Vicente M. 2013. In the beginning, Escherichia coli assembled the proto-ring: an initial phase of division. J Biol Chem 288:20830-20836.
  110. Sontag CA, Staley JT, Erickson HP. 2005. In vitro assembly and GTP hydrolysis by bacterial tubulins BtubA and BtubB. The Journal of cell biology 169:233-238.
  111. Ramos A, Honrubia MP, Valbuena N, Vaquera J, Mateos LM, Gil JA. 2003. Involvement of DivIVA in the morphology of the rod-shaped actinomycete Brevibacterium lactofermentum. Microbiology 149:3531-3542.
  112. Horger I, Velasco E, Mingorance J, Rivas G, Tarazona P, Velez M. 2008. Langevin computer simulations of bacterial protein filaments and the force-generating mechanism during cell division. Phys Rev E Stat Nonlin Soft Matter Phys 77:011902.
  113. Lenarcic R, Halbedel S, Visser L, Shaw M, Wu LJ, Errington J, Marenduzzo D, Hamoen LW. 2009. Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28:2272-2282.
  114. Kiekebusch D, Michie KA, Essen LO, Lowe J, Thanbichler M. 2012. Localized dimerization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46:245-259.
  115. Holeckova N, Doubravova L, Massidda O, Molle V, Buriankova K, Benada O, Kofronova O, Ulrych A, Branny P. 2014. LocZ is a new cell division protein involved in proper septum placement in Streptococcus pneumoniae. MBio 6:e01700-01714.
  116. Komeili A, Li Z, Newman DK, Jensen GJ. 2006. Magnetosomes are cell membrane invaginations organized by the actin-like protein MamK. Science 311:242-245.
  117. Ravin NV, Rech J, Lane D. 2003. Mapping of functional domains in F plasmid partition proteins reveals a bipartite SopB-recognition domain in SopA. J Mol Biol 329:875-889.
  118. Dmowski M, Jagura-Burdzy G. 2011. Mapping of the interactions between partition proteins Delta and Omega of plasmid pSM19035 from Streptococcus pyogenes. Microbiology 157:1009-1020.
  119. He B. 2014. Study of a sociable molecule. Mapping the binding interfaces of the cell division regulator MipZ in Caulobacter crescentus. Doctoral thesis. Philipps-Universität Marburg.
  120. Fleurie A, Lesterlin C, Manuse S, Zhao C, Cluzel C, Lavergne JP, Franz-Wachtel M, Macek B, Combet C, Kuru E, VanNieuwenhze MS, Brun YV, Sherratt D, Grangeasse C. 2014. MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature 516:259-262.
  121. Shtylla B. 2017. Mathematical modeling of spatiotemporal protein localization patterns in C. crescentus bacteria: A mechanism for asymmetric FtsZ ring positioning. Journal of theoretical biology 433:8-20.
  122. Blaauwen T. 2005. Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol 55:1631-1645.
  123. Szeto TH, Rowland SL, Rothfield LI, King GF. 2002. Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 99:15693-15698.
  124. Pilhofer M, Ladinsky MS, McDowall AW, Petroni G, Jensen GJ. 2011. Microtubules in bacteria: Ancient tubulins build a five-protofilament homolog of the eukaryotic cytoskeleton. PLoS Biol 9:e1001213.
  125. Arumugam S, Petrasek Z, Schwille P. 2014. MinCDE exploits the dynamic nature of FtsZ filaments for its spatial regulation. Proceedings of the National Academy of Sciences of the United States of America 111:E1192-1200.
  126. Hernandez-Rocamora VM, Garcia-Montanes C, Reija B, Monterroso B, Margolin W, Alfonso C, Zorrilla S, Rivas G. 2013. MinC protein shortens FtsZ protofilaments by preferentially interacting with GDP-bound subunits. J Biol Chem 288:24625-24635.
  127. Lutkenhaus J, Sundaramoorthy M. 2003. MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol Microbiol 48:295-303.
  128. Raskin DM, de Boer PA. 1999. MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181:6419-6424.
  129. Patrick JE, Kearns DB. 2008. MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol Microbiol 70:1166-1179.
  130. Thanbichler M, Shapiro L. 2006. MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126:147-162.
  131. Berge M, Campagne S, Mignolet J, Holden S, Theraulaz L, Manley S, Allain FH, Viollier PH. 2016. Modularity and determinants of a (bi-)polarization control system from free-living and obligate intracellular bacteria. eLife 5.
  132. Tonthat NK, Arold ST, Pickering BF, Van Dyke MW, Liang S, Lu Y, Beuria TK, Margolin W, Schumacher MA. 2011. Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30:154-164.
  133. Ringgaard S, van Zon J, Howard M, Gerdes K. 2009. Movement and equipositioning of plasmids by ParA filament disassembly. Proceedings of the National Academy of Sciences of the United States of America 106:19369-19374.
  134. Rybenkov VV, Herrera V, Petrushenko ZM, Zhao H. 2014. MukBEF, a chromosomal organizer. J Mol Microbiol Biotechnol 24:371-383.
  135. Sycuro LK, Wyckoff TJ, Biboy J, Born P, Pincus Z, Vollmer W, Salama NR. 2012. Multiple peptidoglycan modification networks modulate Helicobacter pylori's cell shape, motility, and colonization potential. PLoS Pathog 8:e1002603.
  136. Kiianitsa K, Solinger JA, Heyer WD. 2003. NADH-coupled microplate photometric assay for kinetic studies of ATP-hydrolyzing enzymes with low and high specific activities. Anal Biochem 321:266-271.
  137. Ramamurthi KS, Losick R. 2009. Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proceedings of the National Academy of Sciences of the United States of America 106:13541-13545.
  138. Petoukhov MV, Franke D, Shkumatov AV, Tria G, Kikhney AG, Gajda M, Gorba C, Mertens HD, Konarev PV, Svergun DI. 2012. New developments in the ATSAS program package for small-angle scattering data analysis. J Appl Crystallogr 45:342-350.
  139. Wu LJ, Ishikawa S, Kawai Y, Oshima T, Ogasawara N, Errington J. 2009. Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J 28:1940-1952.
  140. Cho H, McManus HR, Dove SL, Bernhardt TG. 2011. Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proceedings of the National Academy of Sciences of the United States of America 108:3773-3778.
  141. Adams DW, Wu LJ, Errington J. 2015. Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J 34:491-501.
  142. Stahlberg H, Kutejova E, Muchova K, Gregorini M, Lustig A, Muller SA, Olivieri V, Engel A, Wilkinson AJ, Barak I. 2004. Oligomeric structure of the Bacillus subtilis cell division protein DivIVA determined by transmission electron microscopy. Mol Microbiol 52:1281-1290.
  143. Bowman GR, Perez AM, Ptacin JL, Ighodaro E, Folta-Stogniew E, Comolli LR, Shapiro L. 2013. Oligomerization and higher-order assembly contribute to sub-cellular localization of a bacterial scaffold. Mol Microbiol 90:776-795.
  144. Du S, Park KT, Lutkenhaus J. 2015. Oligomerization of FtsZ converts the FtsZ tail motif (conserved carboxy-terminal peptide) into a multivalent ligand with high avidity for partners ZipA and SlmA. Mol Microbiol 95:173-188.
  145. Carballido-Lopez R. 2006. Orchestrating bacterial cell morphogenesis. Mol Microbiol 60:815-819.
  146. Surtees JA, Funnell BE. 1999. P1 ParB domain structure includes two independent multimerization domains. J Bacteriol 181:5898-5908.
  147. Hwang LC, Vecchiarelli AG, Han YW, Mizuuchi M, Harada Y, Funnell BE, Mizuuchi K. 2013. ParA-mediated plasmid partition driven by protein pattern self- organization. EMBO J 32:1238-1249.
  148. Bartosik AA, Lasocki K, Mierzejewska J, Thomas CM, Jagura-Burdzy G. 2004. ParB of Pseudomonas aeruginosa: interactions with its partner ParA and its target parS and specific effects on bacterial growth. J Bacteriol 186:6983-6998.
  149. Graham TG, Wang X, Song D, Etson CM, van Oijen AM, Rudner DZ, Loparo JJ. 2014. ParB spreading requires DNA bridging. Genes Dev 28:1228-1238.
  150. Golovanov AP, Barilla D, Golovanova M, Hayes F, Lian LY. 2003. ParG, a protein required for active partition of bacterial plasmids, has a dimeric ribbon-helix-helix structure. Mol Microbiol 50:1141-1153.
  151. Fiuza M, Letek M, Leiba J, Villadangos AF, Vaquera J, Zanella-Cleon I, Mateos LM, Molle V, Gil JA. 2010. Phosphorylation of a novel cytoskeletal protein (RsmP) regulates rod-shaped morphology in Corynebacterium glutamicum. J Biol Chem 285:29387-29397.
  152. Alley MR, Maddock JR, Shapiro L. 1992. Polar localization of a bacterial chemoreceptor. Genes Dev 6:825-836.
  153. Treuner-Lange A, Aguiluz K, van der Does C, Gomez-Santos N, Harms A, Schumacher D, Lenz P, Hoppert M, Kahnt J, Munoz-Dorado J, Sogaard-Andersen L. 2013. PomZ, a ParA-like protein, regulates Z-ring formation and cell division in Myxococcus xanthus. Mol Microbiol 87:235-253.
  154. Ma L, King GF, Rothfield L. 2004. Positioning of the MinE binding site on the MinD surface suggests a plausible mechanism for activation of the Escherichia coli MinD ATPase during division site selection. Mol Microbiol 54:99-108.
  155. Hirano M, Hirano T. 2004. Positive and negative regulation of SMC-DNA interactions by ATP and accessory proteins. EMBO J 23:2664-2673.
  156. Willemse J, Borst JW, de Waal E, Bisseling T, van Wezel GP. 2011. Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev 25:89-99.
  157. Wang Y, Jardetzky O. 2002. Probability-based protein secondary structure identification using combined NMR chemical-shift data. Protein Sci 11:852-861.
  158. Radnedge L, Youngren B, Davis M, Austin S. 1998. Probing the structure of complex macromolecular interactions by homolog specificity scanning: the P1 and P7 plasmid partition systems. EMBO J 17:6076-6085.
  159. Dominguez-Escobar J, Chastanet A, Crevenna AH, Fromion V, Wedlich-Soldner R, Carballido-Lopez R. 2011. Processive movement of MreB-associated cell wall biosynthetic complexes in bacteria. Science 333:225-228.
  160. Figge RM, Easter J, Gober JW. 2003. Productive interaction between the chromosome partitioning proteins, ParA and ParB, is required for the progression of the cell cycle in Caulobacter crescentus. Mol Microbiol 47:1225-1237.
  161. van den Ent F, Amos LA, Lowe J. 2001. Prokaryotic origin of the actin cytoskeleton. Nature 413:39-44.
  162. Clark ED. 2001. Protein refolding for industrial processes. Curr Opin Biotechnol 12:202-207.
  163. Ben-Yehuda S, Rudner DZ, Losick R. 2003. RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299:532-536.
  164. Wu LJ, Errington J. 2003. RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol 49:1463-1475.
  165. Sullivan NL, Marquis KA, Rudner DZ. 2009. Recruitment of SMC by ParB-parS organizes the origin region and promotes efficient chromosome segregation. Cell 137:697-707.
  166. Yamaguchi H, Miyazaki M. 2014. Refolding techniques for recovering biologically active recombinant proteins from inclusion bodies. Biomolecules 4:235-251.
  167. Jacq M, Adam V, Bourgeois D, Moriscot C, Di Guilmi AM, Vernet T, Morlot C. 2015. Remodeling of the Z-Ring Nanostructure during the Streptococcus pneumoniae cell cycle revealed by photoactivated localization microscopy. MBio 6.
  168. Jenal U. 2000. Signal transduction mechanisms in Caulobacter crescentus development and cell cycle control. FEMS Microbiol Rev 24:177-191.
  169. Erickson HP. 2009. Size and shape of protein molecules at the nanometer level determined by sedimentation, gel filtration, and electron microscopy. Biol Proced Online 11:32-51.
  170. Du S, Lutkenhaus J. 2014. SlmA antagonism of FtsZ assembly employs a two-pronged mechanism like MinCD. PLoS Genet 10:e1004460.
  171. 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 18:555-564.
  172. Tonthat NK, Milam SL, Chinnam N, Whitfill T, Margolin W, Schumacher MA. 2013. SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proceedings of the National Academy of Sciences of the United States of America 110:10586-10591.
  173. Hester CM, Lutkenhaus J. 2007. Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proceedings of the National Academy of Sciences of the United States of America 104:20326-20331.
  174. Laloux G, Jacobs-Wagner C. 2013. Spatiotemporal control of PopZ localization through cell cycle-coupled multimerization. The Journal of cell biology 201:827-841.
  175. Kiekebusch D, Thanbichler M. 2014. Spatiotemporal organization of microbial cells by protein concentration gradients. Trends Microbiol 22:65-73.
  176. Haeusser DP, Margolin W. 2016. Splitsville: structural and functional insights into the dynamic bacterial Z ring. Nat Rev Microbiol 14:305-319.
  177. Scholefield G, Whiting R, Errington J, Murray H. 2011. Spo0J regulates the oligomeric state of Soj to trigger its switch from an activator to an inhibitor of DNA replication initiation. Mol Microbiol 79:1089-1100.
  178. Lu C, Reedy M, Erickson HP. 2000. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J Bacteriol 182:164-170.
  179. Rittinger K, Walker PA, Eccleston JF, Smerdon SJ, Gamblin SJ. 1997. Structure at 1.65 A of RhoA and its GTPase-activating protein in complex with a transition-state analogue. Nature 389:758-762.
  180. Schindelin H, Kisker C, Schlessman JL, Howard JB, Rees DC. 1997. Structure of ADP x AIF4(-)-stabilized nitrogenase complex and its implications for signal transduction. Nature 387:370-376.
  181. Schumacher MA, Tonthat NK, Lee J, Rodriguez-Castaneda FA, Chinnam NB, Kalliomaa-Sanford AK, Ng IW, Barge MT, Shaw PL, Barilla D. 2015. Structures of archaeal DNA segregation machinery reveal bacterial and eukaryotic linkages. Science 349:1120-1124.
  182. Weihofen WA, Cicek A, Pratto F, Alonso JC, Saenger W. 2006. Structures of omega repressors bound to direct and inverted DNA repeats explain modulation of transcription. Nucleic Acids Res 34:1450-1458.
  183. Zhang H, Schumacher MA. 2017. Structures of partition protein ParA with nonspecific DNA and ParB effector reveal molecular insights into principles governing Walker-box DNA segregation. Genes Dev 31:481-492.
  184. Schumacher MA, Zeng W. 2016. Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ. Proceedings of the National Academy of Sciences of the United States of America 113:4988-4993.
  185. Vecchiarelli AG, Mizuuchi K, Funnell BE. 2012. Surfing biological surfaces: exploiting the nucleoid for partition and transport in bacteria. Mol Microbiol 86:513-523.
  186. Thanbichler M. 2010. Synchronization of chromosome dynamics and cell division in bacteria. Cold Spring Harb Perspect Biol 2:a000331.
  187. mM Mg-ATP (152). The absence of other peaks serves as a proof that ParA does not form oligomers larger than dimers (152).
  188. Edwards DH, Errington J. 1997. The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24:905- 915.
  189. van Teeffelen S, Wang S, Furchtgott L, Huang KC, Wingreen NS, Shaevitz JW, Gitai Z. 2011. The bacterial actin MreB rotates, and rotation depends on cell-wall assembly. Proceedings of the National Academy of Sciences of the United States of America 108:15822-15827.
  190. Murray H, Ferreira H, Errington J. 2006. The bacterial chromosome segregation protein Spo0J spreads along DNA from parS nucleation sites. Mol Microbiol 61:1352- 1361.
  191. Ausmees N, Kuhn JR, Jacobs-Wagner C. 2003. The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115:705-713.
  192. Carballido-Lopez R, Errington J. 2003. The bacterial cytoskeleton: in vivo dynamics of the actin-like protein Mbl of Bacillus subtilis. Dev Cell 4:19-28.
  193. Pichoff S, Du S, Lutkenhaus J. 2015. The bypass of ZipA by overexpression of FtsN requires a previously unknown conserved FtsN motif essential for FtsA-FtsN interaction supporting a model in which FtsA monomers recruit late cell division proteins to the Z ring. Mol Microbiol 95:971-987.
  194. Breuner A, Jensen RB, Dam M, Pedersen S, Gerdes K. 1996. The centromere-like parC locus of plasmid R1. Mol Microbiol 20:581-592.
  195. Shen B, Lutkenhaus J. 2009. The conserved C-terminal tail of FtsZ is required for the septal localization and division inhibitory activity of MinC(C)/MinD. Mol Microbiol 72:410-424.
  196. Shiomi D, Margolin W. 2007. The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J Bacteriol 189:236-243.
  197. Cha JH, Stewart GC. 1997. The divIVA minicell locus of Bacillus subtilis. J Bacteriol 179:1671-1683.
  198. Surtees JA, Funnell BE. 2001. The DNA binding domains of P1 ParB and the architecture of the P1 plasmid partition complex. J Biol Chem 276:12385-12394.
  199. Ebersbach G, Gerdes K. 2001. The double par locus of virulence factor pB171: DNA segregation is correlated with oscillation of ParA. Proceedings of the National Academy of Sciences of the United States of America 98:15078-15083.
  200. Brun YV, Marczynski G, Shapiro L. 1994. The expression of asymmetry during Caulobacter cell differentiation. Annu Rev Biochem 63:419-450.
  201. Marks ME, Castro-Rojas CM, Teiling C, Du L, Kapatral V, Walunas TL, Crosson S. 2010. The genetic basis of laboratory adaptation in Caulobacter crescentus. J Bacteriol 192:3678-3688.
  202. Ortiz C, Natale P, Cueto L, Vicente M. 2016. The keepers of the ring: regulators of FtsZ assembly. FEMS Microbiol Rev 40:57-67.
  203. van Baarle S, Bramkamp M. 2010. The MinCDJ system in Bacillus subtilis prevents minicell formation by promoting divisome disassembly. PLoS One 5:e9850.
  204. de Boer PA, Crossley RE, Hand AR, Rothfield LI. 1991. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J 10:4371-4380.
  205. Raskin DM, de Boer PA. 1997. The MinE ring: an FtsZ-independent cell structure required for selection of the correct division site in E. coli. Cell 91:685-694.
  206. Park KT, Wu W, Battaile KP, Lovell S, Holyoak T, Lutkenhaus J. 2011. The Min oscillator uses MinD-dependent conformational changes in MinE to spatially regulate cytokinesis. Cell 146:396-407.
  207. Rodrigues CD, Harry EJ. 2012. The Min system and nucleoid occlusion are not required for identifying the division site in Bacillus subtilis but ensure its efficient utilization. PLoS Genet 8:e1002561.
  208. Kang CM, Abbott DW, Park ST, Dascher CC, Cantley LC, Husson RN. 2005. The Mycobacterium tuberculosis serine/threonine kinases PknA and PknB: substrate identification and regulation of cell shape. Genes Dev 19:1692-1704.
  209. Cabre EJ, Monterroso B, Alfonso C, Sanchez-Gorostiaga A, Reija B, Jimenez M, Vicente M, Zorrilla S, Rivas G. 2015. The Nucleoid Occlusion SlmA Protein Accelerates the Disassembly of the FtsZ Protein Polymers without Affecting Their GTPase Activity. PLoS One 10:e0126434.
  210. Egan AJ, Vollmer W. 2013. The physiology of bacterial cell division. Ann N Y Acad Sci 1277:8-28.
  211. Schumacher D, Bergeler S, Harms A, Vonck J, Huneke-Vogt S, Frey E, Sogaard- Andersen L. 2017. The PomXYZ proteins self-organize on the bacterial nucleoid to stimulate cell division. Dev Cell 41:299-314 e213.
  212. Marston FA. 1986. The purification of eukaryotic polypeptides synthesized in Escherichia coli. Biochem J 240:1-12.
  213. Scheffzek K, Ahmadian MR, Kabsch W, Wiesmuller L, Lautwein A, Schmitz F, Wittinghofer A. 1997. The Ras-RasGAP complex: structural basis for GTPase activation and its loss in oncogenic Ras mutants. Science 277:333-338.
  214. Orlova A, Garner EC, Galkin VE, Heuser J, Mullins RD, Egelman EH. 2007. The structure of bacterial ParM filaments. Nat Struct Mol Biol 14:921-926.
  215. Hu Z, Lutkenhaus J. 2001. Topological regulation of cell division in E. coli. spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell 7:1337-1343.
  216. Leonard TA, Moller-Jensen J, Lowe J. 2005. Towards understanding the molecular basis of bacterial DNA segregation. Philos Trans R Soc Lond B Biol Sci 360:523-535.
  217. Larsen RA, Cusumano C, Fujioka A, Lim-Fong G, Patterson P, Pogliano J. 2007. Treadmilling of a prokaryotic tubulin-like protein, TubZ, required for plasmid stability in Bacillus thuringiensis. Genes Dev 21:1340-1352.
  218. Oliva MA, Martin-Galiano AJ, Sakaguchi Y, Andreu JM. 2012. Tubulin homolog TubZ in a phage-encoded partition system. Proceedings of the National Academy of Sciences of the United States of America 109:7711-7716.
  219. de Pereda JM, Leynadier D, Evangelio JA, Chacon P, Andreu JM. 1996. Tubulin secondary structure analysis, limited proteolysis sites, and homology to FtsZ. Biochemistry 35:14203-14215.
  220. Muller SA, Aebi U, Engel A. 2008. What transmission electron microscopes can visualize now and in the future. Journal of structural biology 163:235-245.
  221. Bowers LM, Shapland EB, Ryan KR. 2008. Who's in charge here? Regulating cell cycle regulators. Curr Opin Microbiol 11:547-552.

* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten
© UB Marburg 1997 - 2024 Universitätsbibliothek Marburg