Publikationsserver der Universitätsbibliothek Marburg

Titel:Cell differentiation specific inhibition of cell division guarantees the formation of diploid spores during development of Myxococcus xanthus
Autor:Huneke-Vogt, Sabrina
Weitere Beteiligte: Sogaard-Andersen, Lotte (Prof. Dr. MD)
Veröffentlicht:2017
URI:https://archiv.ub.uni-marburg.de/diss/z2017/0710
DOI: https://doi.org/10.17192/z2017.0710
URN: urn:nbn:de:hebis:04-z2017-07101
DDC:570 Biowissenschaften, Biologie
Titel (trans.):Zelltyp-spezifische Inhibition der Zellteilung garantiert die Bildung von diploiden Sporen während des Entwicklungsprogramms von Myxococcus xanthus
Publikationsdatum:2017-11-13
Lizenz:https://rightsstatements.org/vocab/InC-NC/1.0/

Dokument

Schlagwörter:
chromosome, Zellzyklus, Chromosom, Replikation, sporulation, Cell division, Zellteilung, cell cycle, replication, Sporenbildung

Summary:
Als Antwort auf nahrungslimitierende Bedingungen initiiert das im Boden lebende Bakterium Myxococcus xanthus ein komplexes Entwicklungsprogramm. Dieses führt zur Bildung von Fruchtkörpern in denen die stäbchenförmigen Zellen zu kugelförmigen, diploiden Myxosporen differenzieren, welche extreme Umweltbedingungen überdauern können. Einige Zellen, die als „peripheral rods“ bezeichnet werden bleiben haploid außerhalb der Fruchtkörper. Replikation ist essentiell für die Fruchtkörperbildung und Sporulation. Unter vegetativen Bedingungen wachsen die Zellen asynchron hinsichtlich ihres Zellzyklus. Sie enthalten ein bis zwei Chromosomen und auf Replikation folgt Zellteilung. In dieser Arbeit wurde der Mechanismus der zur Bildung von diploiden Sporen führt untersucht. Wir bestätigten durch die Analyse einzelner Zellen sowie Zellpopulationen, dass Myxosporen zwei Chromosomen beinhalten. Unsere Ergebnisse wiesen darauf hin, dass sich „peripheral rods“ in verschiedenen Phasen des Zellzyklus befinden und in der Lage sind zu replizieren. Um die Regulierung der Zellteilung zu untersuchen haben wir uns auf das Haupt-Zellteilungsprotein FtsZ sowie dessen Regulatoren PomX, PomY und PomZ fokussiert. In Experimenten, bei denen zukünftige Sporen und „peripheral rods“ getrennt wurden, konnten wir zeigen, dass die Proteinlevel während des Entwicklungsprogramms spezifisch in künftigen Sporen abnehmen. Damit einhergehend war die Präsenz jedes dieser Proteine nicht essentiell für Fruchtkörperbildung und Sporulation. Transkriptionelle Analyse offenbarte eine Abnahme der Anzahl der Tranksripte von ftsZ, pomX, pomY und pomZ bei Nahrungslimitation. Zudem wird FtsZ kontinuierlich degradiert, sowohl während vegetativen als auch während nahrungslimitierenden Bedingungen. Wir folgerten, dass FtsZ Proteolyse die Synthese übertrifft, was zu einer Abnahme des Proteinlevels und der Inhibition von Zellteilung in künftigen Sporen führt. Konstitutive ftsZ Expression beeinflusste nicht den Sporulations-prozess, resultierte jedoch in die Bildung von Sporen die weniger als zwei Chromosomen beinhalteten. Folglich reicht die Eliminierung von FtsZ aus um Zellteilung zu inhibieren und diploide Sporen zu bilden. In diesen Vorgang, jedoch nicht in die transkriptionelle Regulation, ist wahrscheinlich die ATP-abhängige Protease LonD indirekt involviert. Sporulation an sich ist unabhängig vom Chromosomengehalt, allerdings beeinflusst die DNA Menge die Morphologie der Sporen. Zellen die mehr Chromosomen als WT Zellen beinhalten und das Entwicklungsprogramm starten, formen Sporen, die eine höhere Durchschnittsgröße und einen höheren DNA Gehalt aufweisen. Obwohl die Abnahme von FtsZ und ftsZ Transkripten spezifisch während nahrungslimitierenden Bedingungen stattfindet scheint dies unabhängig von der „stringent response“ und RelA zu sein. Außerdem wird FtsZ unabhängig vom globalen Vorkommen des sekundären Botenstoffes zyklisches di-GMP reguliert, welches eine essentielle Rolle im multizellulären Verhalten von M. xanthus spielt.

Bibliographie / References

  1. Sugimoto, S., K. Yamanaka, S. Nishikori, A. Miyagi, T. Ando & T. Ogura, (2010) AAA+ chaperone ClpX regulates dynamics of prokaryotic cytoskeletal protein FtsZ. J Biol Chem 285: 6648-6657.
  2. Giglio, K.M., N. Caberoy, G. Suen, D. Kaiser & A.G. Garza, (2011) A cascade of coregulating enhancer binding proteins initiates and propagates a multicellular developmental program. Proc Natl Acad Sci U S A 108: E431-439.
  3. Manoil, C. & D. Kaiser, (1980a) Accumulation of guanosine tetraphosphate and guanosine pentaphosphate in Myxococcus xanthus during starvation and myxospore formation. J Bacteriol 141: 297-304.
  4. Mittal, S. & L. Kroos, (2009) A combination of unusual transcription factors binds cooperatively to control Myxococcus xanthus developmental gene expression. Proc Natl Acad Sci U S A 106: 1965-1970.
  5. Ueki, T. & S. Inouye, (2005a) Activation of a development-specific gene, dofA, by FruA, an essential transcription factor for development of Myxococcus xanthus. J Bacteriol 187: 8504-8506.
  6. Duncan, L., S. Alper, F. Arigoni, R. Losick & P. Stragier, (1995) Activation of cell- specific transcription by a serine phosphatase at the site of asymmetric division. Science 270: 641-644.
  7. Kirstein, J., N. Moliere, D.A. Dougan & K. Turgay, (2009) Adapting the machine: adaptor proteins for Hsp100/Clp and AAA+ proteases. Nat Rev Microbiol 7: 589- 599.
  8. Mukherjee, S., A.C. Bree, J. Liu, J.E. Patrick, P. Chien & D.B. Kearns, (2015) Adaptor- mediated Lon proteolysis restricts Bacillus subtilis hyperflagellation. Proc Natl Acad Sci U S A 112: 250-255.
  9. Wolanski, M., D. Jakimowicz & J. Zakrzewska-Czerwinska, (2012) AdpA, key regulator for morphological differentiation regulates bacterial chromosome replication. Open biology 2: 120097.
  10. Fogel, M.A. & M.K. Waldor, (2006) A dynamic, mitotic-like mechanism for bacterial chromosome segregation. Genes & development 20: 3269-3282.
  11. Wang, X.D., P.A. de Boer & L.I. Rothfield, (1991) A factor that positively regulates cell division by activating transcription of the major cluster of essential cell division genes of Escherichia coli. EMBO J 10: 3363-3372.
  12. Jakimowicz, D., P. Zydek, A. Kois, J. Zakrzewska-Czerwinska & K.F. Chater, (2007) Alignment of multiple chromosomes along helical ParA scaffolding in sporulating Streptomyces hyphae. Mol Microbiol 65: 625-641.
  13. Veening, J.W., H. Murray & J. Errington, (2009) A mechanism for cell cycle regulation of sporulation initiation in Bacillus subtilis. Genes & development 23: 1959- 1970.
  14. Singh, J.K., R.D. Makde, V. Kumar & D. Panda, (2007) A membrane protein, EzrA, regulates assembly dynamics of FtsZ by interacting with the C-terminal tail of FtsZ. Biochemistry 46: 11013-11022.
  15. Weart, R.B., A.H. Lee, A.C. Chien, D.P. Haeusser, N.S. Hill & P.A. Levin, (2007) A metabolic sensor governing cell size in bacteria. Cell 130: 335-347.
  16. Hauser, P.M. & D. Karamata, (1992) A method for the determination of bacterial spore DNA content based on isotopic labelling, spore germination and diphenylamine assay; ploidy of spores of several Bacillus species. Biochimie 74: 723-733.
  17. Skotnicka, D., G.T. Smaldone, T. Petters, E. Trampari, J. Liang, V. Kaever, J.G. Malone, M. Singer & L. Sogaard-Andersen, (2016) A Minimal Threshold of c-di- GMP Is Essential for Fruiting Body Formation and Sporulation in Myxococcus xanthus. PLoS Genet 12: e1006080.
  18. Hill, N.S., P.J. Buske, Y. Shi & P.A. Levin, (2013) A moonlighting enzyme links Escherichia coli cell size with central metabolism. PLoS Genet 9: e1003663.
  19. Beaufay, F., J. Coppine, A. Mayard, G. Laloux, X. De Bolle & R. Hallez, (2015) A NAD- dependent glutamate dehydrogenase coordinates metabolism with cell division in Caulobacter crescentus. EMBO J 34: 1786-1800.
  20. Keseler, I.M. & D. Kaiser, (1995) An early A-signal-dependent gene in Myxococcus xanthus has a sigma 54-like promoter. J Bacteriol 177: 4638-4644.
  21. Ishikawa, S., Y. Kawai, K. Hiramatsu, M. Kuwano & N. Ogasawara, (2006) A new FtsZ- interacting protein, YlmF, complements the activity of FtsA during progression of cell division in Bacillus subtilis. Mol Microbiol 60: 1364-1380.
  22. Bramkamp, M., R. Emmins, L. Weston, C. Donovan, R.A. Daniel & J. Errington, (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.
  23. Sass, P., M. Josten, K. Famulla, G. Schiffer, H.G. Sahl, L. Hamoen & H. Brotz- Oesterhelt, (2011) Antibiotic acyldepsipeptides activate ClpP peptidase to degrade the cell division protein FtsZ. Proc Natl Acad Sci U S A 108: 17474- 17479.
  24. Szwedziak, P., Q. Wang, T.A. Bharat, M. Tsim & J. Lowe, (2014) Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. eLife 3: e04601.
  25. Konovalova, A., S. Lobach & L. Sogaard-Andersen, (2012) A RelA-dependent two- tiered regulated proteolysis cascade controls synthesis of a contact-dependent intercellular signal in Myxococcus xanthus. Mol Microbiol 84: 260-275.
  26. Kuspa, A., L. Plamann & D. Kaiser, (1992b) A-signalling and the cell density requirement for Myxococcus xanthus development. J Bacteriol 174: 7360-7369.
  27. Pazos, M., P. Natale & M. Vicente, (2013) A specific role for the ZipA protein in cell division: stabilization of the FtsZ protein. J Biol Chem 288: 3219-3226.
  28. Anderson, D.E., F.J. Gueiros-Filho & H.P. Erickson, (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J Bacteriol 186: 5775-5781.
  29. Schwedock, J., J.R. McCormick, E.R. Angert, J.R. Nodwell & R. Losick, (1997) Assembly of the cell division protein FtsZ into ladder-like structures in the aerial hyphae of Streptomyces coelicolor. Mol Microbiol 25: 847-858.
  30. Ben-Yehuda, S. & R. Losick, (2002) Asymmetric cell division in B. subtilis involves a spiral-like intermediate of the cytokinetic protein FtsZ. Cell 109: 257-266.
  31. Dworkin, M. & S.M. Gibson, (1964) A System for Studying Microbial Morphogenesis: Rapid Formation of Microcysts in Myxococcus xanthus. Science 146: 243-244.
  32. Gregory, J.A., E.C. Becker & K. Pogliano, (2008) Bacillus subtilis MinC destabilizes FtsZ-rings at new cell poles and contributes to the timing of cell division. Genes & development 22: 3475-3488.
  33. Errington, J., (1993) Bacillus subtilis sporulation: regulation of gene expression and control of morphogenesis. Microbiological reviews 57: 1-33.
  34. Adams, D.W. & J. Errington, (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7: 642-653.
  35. Erickson, H.P., D.W. Taylor, K.A. Taylor & D. Bramhill, (1996) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci U S A 93: 519-523.
  36. Sherratt, D.J., (2003) Bacterial chromosome dynamics. Science 301: 780-785.
  37. Boutte, C.C. & S. Crosson, (2013) Bacterial lifestyle shapes stringent response activation. Trends Microbiol 21: 174-180.
  38. Pesavento, C. & R. Hengge, (2009) Bacterial nucleotide-based second messengers. Curr Opin Microbiol 12: 170-176.
  39. Claessen, D., D.E. Rozen, O.P. Kuipers, L. Sogaard-Andersen & G.P. van Wezel, (2014) Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat Rev Microbiol 12: 115-124.
  40. Trusca, D., S. Scott, C. Thompson & D. Bramhill, (1998) Bacterial SOS checkpoint protein SulA inhibits polymerization of purified FtsZ cell division protein. J Bacteriol 180: 3946-3953.
  41. O'Connor, K.A. & D.R. Zusman, (1991a) Behavior of peripheral rods and their role in the life cycle of Myxococcus xanthus. J Bacteriol 173: 3342-3355.
  42. Shi, X., S. Wegener-Feldbrugge, S. Huntley, N. Hamann, R. Hedderich & L. Sogaard- Andersen, (2008) Bioinformatics and experimental analysis of proteins of two- component systems in Myxococcus xanthus. J Bacteriol 190: 613-624.
  43. Inouye, M., S. Inouye & D.R. Zusman, (1979a) Biosynthesis and self-assembly of protein S, a development-specific protein of Myxococcus xanthus. Proc Natl Acad Sci U S A 76: 209-213.
  44. Jelsbak, L. & L. Sogaard-Andersen, (2003) Cell behavior and cell-cell communication during fruiting body morphogenesis in Myxococcus xanthus. J Microbiol Meth 55: 829-839.
  45. Collier, J., (2016) Cell cycle control in Alphaproteobacteria. Curr Opin Microbiol 30: 107-113.
  46. Mohl, D.A. & J.W. Gober, (1997) Cell cycle-dependent polar localization of chromosome partitioning proteins in Caulobacter crescentus. Cell 88: 675-684.
  47. Kelly, A.J., M.J. Sackett, N. Din, E. Quardokus & Y.V. Brun, (1998) Cell cycle- dependent transcriptional and proteolytic regulation of FtsZ in Caulobacter. Genes & development 12: 880-893.
  48. Treuner-Lange, A., L. Søgaard-Andersen, M. Singer, (2014) Cell Cycle Regulation in Myxococcus xanthus during vegetative growth and development: Regulatory links between DNA replication and cell division. In: Myxobateria: Genomics, Cellular and Molecular Biology. pp. 79-90.
  49. Ferullo, D.J., D.L. Cooper, H.R. Moore & S.T. Lovett, (2009) Cell cycle synchronization of Escherichia coli using the stringent response, with fluorescence labeling assays for DNA content and replication. Methods 48: 8-13.
  50. Huisman, O., R. D'Ari & S. Gottesman, (1984) Cell-division control in Escherichia coli: specific induction of the SOS function SfiA protein is sufficient to block septation. Proc Natl Acad Sci U S A 81: 4490-4494.
  51. Justice, S.S., J. Garcia-Lara & L.I. Rothfield, (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: 410-423.
  52. Hodgkin, J. & D. Kaiser, (1977) Cell-to-cell stimulation of movement in nonmotile mutants of Myxococcus. Proc Natl Acad Sci U S A 74: 2938-2942.
  53. Domian, I.J., K.C. Quon & L. Shapiro, (1997) Cell type-specific phosphorylation and proteolysis of a transcriptional regulator controls the G1-to-S transition in a bacterial cell cycle. Cell 90: 415-424.
  54. Koushik, S.V., H. Chen, C. Thaler, H.L. Puhl, 3rd & S.S. Vogel, (2006) Cerulean, Venus, and VenusY67C FRET reference standards. Biophysical journal 91: L99-L101.
  55. Fadda, D., C. Pischedda, F. Caldara, M.B. Whalen, D. Anderluzzi, E. Domenici & O. Massidda, (2003) Characterization of divIVA and other genes located in the chromosomal region downstream of the dcw cluster in Streptococcus pneumoniae. J Bacteriol 185: 6209-6214.
  56. Ni, T., F. Ye, X. Liu, J. Zhang, H. Liu, J. Li, Y. Zhang, Y. Sun, M. Wang, C. Luo, H. Jiang, L. Lan, J. Gan, A. Zhang, H. Zhou & C.G. Yang, (2016) Characterization of Gain-of-Function Mutant Provides New Insights into ClpP Structure. ACS chemical biology 11: 1964-1972.
  57. Boynton, T.O., J.L. McMurry & L.J. Shimkets, (2013) Characterization of Myxococcus xanthus MazF and implications for a new point of regulation. Mol Microbiol 87: 1267-1276.
  58. Reyes-Lamothe, R., E. Nicolas & D.J. Sherratt, (2012) Chromosome replication and segregation in bacteria. Annual review of genetics 46: 121-143.
  59. Laemmli, U.K., (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
  60. Tojo, N., S. Inouye & T. Komano, (1993a) Cloning and nucleotide sequence of the Myxococcus xanthus lon gene: indispensability of lon for vegetative growth. J Bacteriol 175: 2271-2277.
  61. Williams, B., N. Bhat, P. Chien & L. Shapiro, (2014) ClpXP and ClpAP proteolytic activity on divisome substrates is differentially regulated following the Caulobacter asymmetric cell division. Mol Microbiol 93: 853-866.
  62. Camberg, J.L., J.R. Hoskins & S. Wickner, (2009) ClpXP protease degrades the cytoskeletal protein, FtsZ, and modulates FtsZ polymer dynamics. Proc Natl Acad Sci U S A 106: 10614-10619.
  63. Kottel, R.H., K. Bacon, D. Clutter & D. White, (1975) Coats from Myxococcus xanthus: characterization and synthesis during myxospore differentiation. J Bacteriol 124: 550-557.
  64. Viswanathan, P., T. Ueki, S. Inouye & L. Kroos, (2007) Combinatorial regulation of genes essential for Myxococcus xanthus development involves a response regulator and a LysR-type regulator. Proc Natl Acad Sci U S A 104: 7969-7974.
  65. Huntley, S., N. Hamann, S. Wegener-Feldbrugge, A. Treuner-Lange, M. Kube, R. Reinhardt, S. Klages, R. Muller, C.M. Ronning, W.C. Nierman & L. Sogaard- Andersen, (2011) Comparative genomic analysis of fruiting body formation in Myxococcales. Molecular biology and evolution 28: 1083-1097.
  66. Woese, C.R., (1958) Comparison of the x-ray sensitivity of bacterial spores. J Bacteriol 75: 5-8.
  67. Hilbert, D.W. & P.J. Piggot, (2004) Compartmentalization of gene expression during Bacillus subtilis spore formation. Microbiol Mol Biol Rev 68: 234-262.
  68. Bravo, A., G. Serrano-Heras & M. Salas, (2005) Compartmentalization of prokaryotic DNA replication. FEMS microbiology reviews 29: 25-47.
  69. Gomez-Santos, N., A. Treuner-Lange, A. Moraleda-Munoz, E. Garcia-Bravo, R. Garcia-Hernandez, M. Martinez-Cayuela, J. Perez, L. Sogaard-Andersen & J. Munoz-Dorado, (2012) Comprehensive set of integrative plasmid vectors for copper-inducible gene expression in Myxococcus xanthus. Appl Environ Microbiol 78: 2515-2521.
  70. Rueda, S., M. Vicente & J. Mingorance, (2003) Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J Bacteriol 185: 3344-3351.
  71. Willemse, J., A.M. Mommaas & G.P. van Wezel, (2012) Constitutive expression of ftsZ overrides the whi developmental genes to initiate sporulation of Streptomyces coelicolor. Antonie Van Leeuwenhoek 101: 619-632.
  72. Flärdh, K., T. Garrido & M. Vicente, (1997) Contribution of individual promoters in the ddlB-ftsZ region to the transcription of the essential cell-division gene ftsZ in Escherichia coli. Mol Microbiol 24: 927-936.
  73. Sitnikov, D.M., J.B. Schineller & T.O. Baldwin, (1996) Control of cell division in Escherichia coli: regulation of transcription of ftsQA involves both rpoS and SdiA-mediated autoinduction. Proc Natl Acad Sci U S A 93: 336-341.
  74. Dewar, S.J. & R. Dorazi, (2000) Control of division gene expression in Escherichia coli. FEMS microbiology letters 187: 1-7.
  75. Wu, L.J. & J. Errington, (2004) Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis. Cell 117: 915- 925.
  76. Cordell, S.C., E.J. Robinson & J. Lowe, (2003) Crystal structure of the SOS cell division inhibitor SulA and in complex with FtsZ. Proc Natl Acad Sci U S A 100: 7889- 7894.
  77. Shimkets, L.J. & H. Rafiee, (1990) CsgA, an extracellular protein essential for Myxococcus xanthus development. J Bacteriol 172: 5299-5306.
  78. Skotnicka, D., T. Petters, J. Heering, M. Hoppert, V. Kaever & L. Sogaard-Andersen, (2015) Cyclic Di-GMP Regulates Type IV Pilus-Dependent Motility in Myxococcus xanthus. J Bacteriol 198: 77-90.
  79. Berleman, J.E. & J.R. Kirby, (2009) Deciphering the hunting strategy of a bacterial wolfpack. FEMS microbiology reviews 33: 942-957.
  80. Ben-Yehuda, S., M. Fujita, X.S. Liu, B. Gorbatyuk, D. Skoko, J. Yan, J.F. Marko, J.S. Liu, P. Eichenberger, D.Z. Rudner & R. Losick, (2005) Defining a centromere- like element in Bacillus subtilis by Identifying the binding sites for the chromosome-anchoring protein RacA. Mol Cell 17: 773-782.
  81. Rosenberg, E., M. Katarski & P. Gottlieb, (1967) Deoxyribonucleic acid synthesis during exponential growth and microcyst formation in Myxococcus xanthus. J Bacteriol 93: 1402-1408.
  82. Zusman, D. & E. Rosenberg, (1968) Deoxyribonucleic acid synthesis during microcyst germination in Myxococcus xanthus. J Bacteriol 96: 981-986.
  83. Jakimowicz, D., S. Mouz, J. Zakrzewska-Czerwinska & K.F. Chater, (2006) Developmental control of a parAB promoter leads to formation of sporulation- associated ParB complexes in Streptomyces coelicolor. J Bacteriol 188: 1710- 1720.
  84. Rosario, C.J. & M. Singer, (2010) Developmental expression of dnaA is required for sporulation and timing of fruiting body formation in Myxococcus xanthus. Mol Microbiol 76: 1322-1333.
  85. Rajagopalan, R., Z. Sarwar, A. G. Garza & L. Kroos, (2014) Developmental Gene Regulation. In: Myxobacteria: Genomics, Cellular and Molecular Biology. pp.
  86. Wireman, J.W. & M. Dworkin, (1977) Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J Bacteriol 129: 798-802.
  87. Gonzy-Treboul, G., C. Karmazyn-Campelli & P. Stragier, (1992) Developmental regulation of transcription of the Bacillus subtilis ftsAZ operon. J Mol Biol 224: 967-979.
  88. Jakimowicz, D., B. Gust, J. Zakrzewska-Czerwinska & K.F. Chater, (2005) Developmental-stage-specific assembly of ParB complexes in Streptomyces coelicolor hyphae. J Bacteriol 187: 3572-3580.
  89. O'Connor, K.A. & D.R. Zusman, (1991b) Development in Myxococcus xanthus involves differentiation into two cell types, peripheral rods and spores. J Bacteriol 173: 3318-3333.
  90. LeDeaux, J.R., N. Yu & A.D. Grossman, (1995) Different roles for KinA, KinB, and KinC in the initiation of sporulation in Bacillus subtilis. J Bacteriol 177: 861-863.
  91. Hale, C.A. & P.A. de Boer, (1997) Direct binding of FtsZ to ZipA, an essential component of the septal ring structure that mediates cell division in E. coli. Cell 88: 175-185.
  92. Pinho, M.G. & J. Errington, (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50: 871-881.
  93. Livny, J., Y. Yamaichi & M.K. Waldor, (2007) Distribution of centromere-like parS sites in bacteria: insights from comparative genomics. J Bacteriol 189: 8693-8703.
  94. Goehring, N.W. & J. Beckwith, (2005) Diverse paths to midcell: assembly of the bacterial cell division machinery. Current Biology 15: R514-526.
  95. Messer, W. & C. Weigel, (1997) DnaA initiator-also a transcription factor. Mol Microbiol 24: 1-6.
  96. Zusman, D. & E. Rosenberg, (1970) DNA cycle of Myxococcus xanthus. J Mol Biol 49: 609-619. List of publications:
  97. Gonzalez, D. & J. Collier, (2013) DNA methylation by CcrM activates the transcription of two genes required for the division of Caulobacter crescentus. Mol Microbiol 88: 203-218.
  98. Tzeng, L., T.N. Ellis & M. Singer, (2006) DNA replication during aggregation phase is essential for Myxococcus xanthus development. J Bacteriol 188: 2774-2779.
  99. Tzeng, L. & M. Singer, (2005) DNA replication during sporulation in Myxococcus xanthus fruiting bodies. Proc Natl Acad Sci U S A 102: 14428-14433.
  100. Mott, M.L. & J.M. Berger, (2007) DNA replication initiation: mechanisms and regulation in bacteria. Nat Rev Microbiol 5: 343-354.
  101. Marston, A.L. & J. Errington, (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.
  102. Grantcharova, N., U. Lustig & K. Flardh, (2005) Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2). J Bacteriol 187: 3227-3237.
  103. Singer, M. & D. Kaiser, (1995) Ectopic production of guanosine penta-and tetraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Genes & development 9: 1633-1644.
  104. Jelsbak, L., M. Givskov & D. Kaiser, (2005) Enhancer-binding proteins with a forkhead- associated domain and the sigma54 regulon in Myxococcus xanthus fruiting body development. Proc Natl Acad Sci U S A 102: 3010-3015.
  105. RayChaudhuri, D. & J.T. Park, (1992) Escherichia coli cell-division gene ftsZ encodes a novel GTP-binding protein. Nature 359: 251-254.
  106. Lim, H.C., I.V. Surovtsev, B.G. Beltran, F. Huang, J. Bewersdorf & C. Jacobs-Wagner, (2014) Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation. eLife 3: e02758.
  107. Kroos, L. & D. Kaiser, (1987) Expression of many developmentally regulated genes in Myxococcus depends on a sequence of cell interactions. Genes & development 1: 840-854.
  108. Lopez, D. & R. Kolter, (2010) Extracellular signals that define distinct and coexisting cell fates in Bacillus subtilis. FEMS microbiology reviews 34: 134-149.
  109. Buske, P.J. & P.A. Levin, (2012) Extreme C terminus of bacterial cytoskeletal protein FtsZ plays fundamental role in assembly independent of modulatory proteins. J Biol Chem 287: 10945-10957.
  110. Haeusser, D.P., R.L. Schwartz, A.M. Smith, M.E. Oates & P.A. Levin, (2004) EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol Microbiol 52: 801-814.
  111. Kuner, J.M. & D. Kaiser, (1982) Fruiting Body Morphogenesis in Submerged Cultures of Myxococcus xanthus. Journal of Bacteriology 151: 458-461.
  112. Erickson, H.P., D.E. Anderson & M. Osawa, (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74: 504-528.
  113. Dai, K. & J. Lutkenhaus, (1991) ftsZ is an essential cell division gene in Escherichia coli. J Bacteriol 173: 3500-3506.
  114. Bi, E.F. & J. Lutkenhaus, (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
  115. Addinall, S.G. & J. Lutkenhaus, (1996) FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol Microbiol 22: 231-237.
  116. Inouye, M., S. Inouye & D.R. Zusman, (1979b) Gene expression during development of Myxococcus xanthus: pattern of protein synthesis. Developmental biology 68: 579-591.
  117. Flärdh, K., E. Leibovitz, M.J. Buttner & K.F. Chater, (2000) Generation of a non- sporulating strain of Streptomyces coelicolor A3(2) by the manipulation of a developmentally controlled ftsZ promoter. Mol Microbiol 38: 737-749.
  118. Laub, M.T., S.L. Chen, L. Shapiro & H.H. McAdams, (2002) Genes directly controlled by CtrA, a master regulator of the Caulobacter cell cycle. Proc Natl Acad Sci U S A 99: 4632-4637.
  119. Haney, S.A., E. Glasfeld, C. Hale, D. Keeney, Z. He & P. de Boer, (2001) Genetic analysis of the Escherichia coli FtsZ-ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J Biol Chem 276: 11980-11987.
  120. Carniol, K., S. Ben-Yehuda, N. King & R. Losick, (2005) Genetic dissection of the sporulation protein SpoIIE and its role in asymmetric division in Bacillus subtilis. J Bacteriol 187: 3511-3520.
  121. Müller, F.D., A. Treuner-Lange, J. Heider, S.M. Huntley & P.I. Higgs, (2010) Global transcriptome analysis of spore formation in Myxococcus xanthus reveals a locus necessary for cell differentiation. BMC genomics 11: 264.
  122. Yang, X., Z. Lyu, A. Miguel, R. McQuillen, K.C. Huang & J. Xiao, (2017) GTPase activity-coupled treadmilling of the bacterial tubulin FtsZ organizes septal cell wall synthesis. Science 355: 744-747.
  123. Mukherjee, A. & J. Lutkenhaus, (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176: 2754-2758.
  124. Manoil, C. & D. Kaiser, (1980b) Guanosine pentaphosphate and guanosine tetraphosphate accumulation and induction of Myxococcus xanthus fruiting body development. J Bacteriol 141: 305-315.
  125. Kroos, L., (2017) Highly Signal-Responsive Gene Regulatory Network Governing Myxococcus Development. Trends in genetics : TIG 33: 3-15.
  126. Levin, P.A., I.G. Kurtser & A.D. Grossman, (1999) Identification and characterization of a negative regulator of FtsZ ring formation in Bacillus subtilis. Proc Natl Acad Sci U S A 96: 9642-9647.
  127. Ueki, T. & S. Inouye, (2005b) Identification of a gene involved in polysaccharide export as a transcription target of FruA, an essential factor for Myxococcus xanthus development. J Biol Chem 280: 32279-32284.
  128. Ueki, T. & S. Inouye, (2003) Identification of an activator protein required for the induction of fruA, a gene essential for fruiting body development in Myxococcus xanthus. Proc Natl Acad Sci U S A 100: 8782-8787.
  129. Kawai, Y., S. Moriya & N. Ogasawara, (2003) Identification of a protein, YneA, responsible for cell division suppression during the SOS response in Bacillus subtilis. Mol Microbiol 47: 1113-1122.
  130. Bhat, N.H., R.H. Vass, P.R. Stoddard, D.K. Shin & P. Chien, (2013) Identification of ClpP substrates in Caulobacter crescentus reveals a role for regulated proteolysis in bacterial development. Mol Microbiol 88: 1083-1092.
  131. Youderian, P., N. Burke, D.J. White & P.L. Hartzell, (2003) Identification of genes required for adventurous gliding motility in Myxococcus xanthus with the transposable element mariner. Mol Microbiol 49: 555-570.
  132. Kuspa, A., L. Plamann & D. Kaiser, (1992a) Identification of heat-stable A-factor from Myxococcus xanthus. J Bacteriol 174: 3319-3326.
  133. Lobedanz, S. & L. Sogaard-Andersen, (2003) Identification of the C-signal, a contact- dependent morphogen coordinating multiple developmental responses in Myxococcus xanthus. Genes & development 17: 2151-2161.
  134. Willemse, J. & G.P. van Wezel, (2009) Imaging of Streptomyces coelicolor A3(2) with reduced autofluorescence reveals a novel stage of FtsZ localization. PLoS One 4: e4242.
  135. Del Sol, R., J.G. Mullins, N. Grantcharova, K. Flardh & P. Dyson, (2006) Influence of CrgA on assembly of the cell division protein FtsZ during development of Streptomyces coelicolor. J Bacteriol 188: 1540-1550.
  136. Dewar, S.J., K.J. Begg & W.D. Donachie, (1992) Inhibition of cell division initiation by an imbalance in the ratio of FtsA to FtsZ. J Bacteriol 174: 6314-6316.
  137. Ptacin, J.L. & L. Shapiro, (2010) Initiating bacterial mitosis: understanding the mechanism of ParA-mediated chromosome segregation. Cell cycle 9: 4033- 4034.
  138. Zhang, H., N.N. Rao, T. Shiba & A. Kornberg, (2005) Inorganic polyphosphate in the social life of Myxococcus xanthus: motility, development, and predation. Proc Natl Acad Sci U S A 102: 13416-13420.
  139. Kuroda, A., K. Nomura, N. Takiguchi, J. Kato & H. Ohtake, (2006) Inorganic polyphosphate stimulates lon-mediated proteolysis of nucleoid proteins in Escherichia coli. Cellular and molecular biology 52: 23-29.
  140. Sogaard-Andersen, L., F.J. Slack, H. Kimsey & D. Kaiser, (1996) Intercellular C- signaling in Myxococcus xanthus involves a branched signal transduction pathway. Genes & development 10: 740-754.
  141. Ryter, A., B. Bloom & J.P. Aubert, (1966) Intracellular localization ribonucleic acids synthesized during sporulation in Bacillus subtilis. Comptes rendus hebdomadaires des seances de l'Academie des sciences. Serie D: Sciences naturelles 262: 1305-1307.
  142. Hoiczyk, E., M.W. Ring, C.A. McHugh, G. Schwar, E. Bode, D. Krug, M.O. Altmeyer, J.Z. Lu & H.B. Bode, (2009) Lipid body formation plays a central role in cell fate determination during developmental differentiation of Myxococcus xanthus. Mol Microbiol 74: 497-517.
  143. Lenarcic, R., S. Halbedel, L. Visser, M. Shaw, L.J. Wu, J. Errington, D. Marenduzzo & L.W. Hamoen, (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28: 2272-2282.
  144. Kiekebusch, D., K.A. Michie, L.O. Essen, J. Lowe & M. Thanbichler, (2012) Localized dimerization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46: 245-259.
  145. Camberg, J.L., M.G. Viola, L. Rea, J.R. Hoskins & S. Wickner, (2014) Location of dual sites in E. coli FtsZ important for degradation by ClpXP; one at the C-terminus and one in the disordered linker. PLoS One 9: e94964.
  146. Holeckova, N., L. Doubravova, O. Massidda, V. Molle, K. Buriankova, O. Benada, O. Kofronova, A. Ulrych & P. Branny, (2014) LocZ is a new cell division protein involved in proper septum placement in Streptococcus pneumoniae. mBio 6: e01700-01714.
  147. Fleurie, A., C. Lesterlin, S. Manuse, C. Zhao, C. Cluzel, J.P. Lavergne, M. Franz- Wachtel, B. Macek, C. Combet, E. Kuru, M.S. VanNieuwenhze, Y.V. Brun, D. Sherratt & C. Grangeasse, (2014) MapZ marks the division sites and positions FtsZ rings in Streptococcus pneumoniae. Nature 516: 259-262.
  148. Nariya, H. & M. Inouye, (2008) MazF, an mRNA interferase, mediates programmed cell death during multicellular Myxococcus development. Cell 132: 55-66.
  149. Sinha, N.K. & D.P. Snustad, (1972) Mechanism of inhibition of deoxyribonucleic acid synthesis in Escherichia coli by hydroxyurea. J Bacteriol 112: 1321-1324.
  150. Szeto, T.H., S.L. Rowland, L.I. Rothfield & G.F. King, (2002) Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc Natl Acad Sci U S A 99: 15693-15698.
  151. Raskin, D.M. & P.A. de Boer, (1999) MinDE-dependent pole-to-pole oscillation of division inhibitor MinC in Escherichia coli. J Bacteriol 181: 6419-6424.
  152. Thanbichler, M. & L. Shapiro, (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126: 147-162.
  153. Rudner, D.Z. & R. Losick, (2001) Morphological coupling in development: lessons from prokaryotes. Developmental cell 1: 733-742.
  154. Munoz-Dorado, J., F.J. Marcos-Torres, E. Garcia-Bravo, A. Moraleda-Munoz & J. Perez, (2016) Myxobacteria: Moving, Killing, Feeding, and Surviving Together. Frontiers in microbiology 7: 781.
  155. Lee, B., C. Holkenbrink, A. Treuner-Lange & P.I. Higgs, (2012) Myxococcus xanthus developmental cell fate production: heterogeneous accumulation of developmental regulatory proteins and reexamination of the role of MazF in developmental lysis. J Bacteriol 194: 3058-3068.
  156. McCleary, W.R., B. Esmon & D.R. Zusman, (1991) Myxococcus xanthus protein C is a major spore surface protein. J Bacteriol 173: 2141-2145.
  157. Higgs, P.I., P.L. Hartzell, C. Holkenbrink and E. Hoiczyk, (2014) Myxococcus xanthus vegetative and developmental cell heterogeneity. In: Myxobacteria: Genomics, Cellular and Molecular Biology. pp. 51-77.
  158. Ramamurthi, K.S. & R. Losick, (2009) Negative membrane curvature as a cue for subcellular localization of a bacterial protein. Proc Natl Acad Sci U S A 106: 13541-13545.
  159. Diodati, M.E., F. Ossa, N.B. Caberoy, I.R. Jose, W. Hiraiwa, M.M. Igo, M. Singer & A.G. Garza, (2006) Nla18, a key regulatory protein required for normal growth and development of Myxococcus xanthus. J Bacteriol 188: 1733-1743.
  160. Ring, M.W., G. Schwar, V. Thiel, J.S. Dickschat, R.M. Kroppenstedt, S. Schulz & H.B. Bode, (2006) Novel iso-branched ether lipids as specific markers of developmental sporulation in the myxobacterium Myxococcus xanthus. J Biol Chem 281: 36691-36700.
  161. Wu, L.J. & J. Errington, (2012) Nucleoid occlusion and bacterial cell division. Nat Rev Microbiol 10: 8-12.
  162. Adams, D.W., L.J. Wu & J. Errington, (2015) Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J 34: 491-501.
  163. Leslie, D.J., C. Heinen, F.D. Schramm, M. Thüring, C.D. Aakre, S.M. Murray, M.T. Laub & K. Jonas, (2015) Nutritional Control of DNA Replication Initiation through the Proteolysis and Regulated Translation of DnaA. PLoS Genet 11: e1005342.
  164. Dworkin, M., (1962) Nutritional requirements for vegetative growth of Myxococcus xanthus. J Bacteriol 84: 250-257.
  165. Lyons, N.A. & R. Kolter, (2015) On the evolution of bacterial multicellularity. Curr Opin Microbiol 24: 21-28.
  166. Francis, F., S. Ramirez-Arcos, H. Salimnia, C. Victor & J.R. Dillon, (2000) Organization and transcription of the division cell wall (dcw) cluster in Neisseria gonorrhoeae. Gene 251: 141-151.
  167. Donczew, M., P. Mackiewicz, A. Wrobel, K. Flardh, J. Zakrzewska-Czerwinska & D. Jakimowicz, (2016) ParA and ParB coordinate chromosome segregation with cell elongation and division during Streptomyces sporulation. Open biology 6: 150263.
  168. Kim, H.J., M.J. Calcutt, F.J. Schmidt & K.F. Chater, (2000) Partitioning of the linear chromosome during sporulation of Streptomyces coelicolor A3(2) involves an oriC-linked parAB locus. J Bacteriol 182: 1313-1320.
  169. Gust, B., G.L. Challis, K. Fowler, T. Kieser & K.F. Chater, (2003) PCR-targeted Streptomyces gene replacement identifies a protein domain needed for biosynthesis of the sesquiterpene soil odor geosmin. Proc Natl Acad Sci U S A 100: 1541-1546.
  170. Handler, A.A., J.E. Lim & R. Losick, (2008) Peptide inhibitor of cytokinesis during sporulation in Bacillus subtilis. Mol Microbiol 68: 588-599.
  171. Balaban, N.Q., (2011) Persistence: mechanisms for triggering and enhancing phenotypic variability. Current opinion in genetics & development 21: 768-775.
  172. Marston, A.L., H.B. Thomaides, D.H. Edwards, M.E. Sharpe & J. Errington, (1998) Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes & development 12: 3419-3430.
  173. Treuner-Lange, A., K. Aguiluz, C. van der Does, N. Gomez-Santos, A. Harms, D. Schumacher, P. Lenz, M. Hoppert, J. Kahnt, J. Munoz-Dorado & L. Sogaard- Andersen, (2013) PomZ, a ParA-like protein, regulates Z-ring formation and cell division in Myxococcus xanthus. Mol Microbiol 87: 235-253.
  174. Willemse, J., J.W. Borst, E. de Waal, T. Bisseling & G.P. van Wezel, (2011) Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes & development 25: 89-99.
  175. Potrykus, K. & M. Cashel, (2008) (p)ppGpp: still magical? Annual review of microbiology 62: 35-51.
  176. Shapiro, L. & R. Losick, (1997) Protein localization and cell fate in bacteria. Science 276: 712-718.
  177. Viola, M.G., C.J. LaBreck, J. Conti & J.L. Camberg, (2017) Proteolysis-Dependent Remodeling of the Tubulin Homolog FtsZ at the Division Septum in Escherichia coli. PLoS One 12: e0170505.
  178. Ruvolo, M.V., K.E. Mach & W.F. Burkholder, (2006) Proteolysis of the replication checkpoint protein Sda is necessary for the efficient initiation of sporulation after transient replication stress in Bacillus subtilis. Mol Microbiol 60: 1490-1508.
  179. Grünenfelder, B., G. Rummel, J. Vohradsky, D. Roder, H. Langen & U. Jenal, (2001) Proteomic analysis of the bacterial cell cycle. Proc Natl Acad Sci U S A 98: 4681-4686.
  180. Ben-Yehuda, S., D.Z. Rudner & R. Losick, (2003) RacA, a bacterial protein that anchors chromosomes to the cell poles. Science 299: 532-536.
  181. Wu, L.J. & J. Errington, (2003) RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol 49: 1463-1475.
  182. Stricker, J., P. Maddox, E.D. Salmon & H.P. Erickson, (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci U S A 99: 3171-3175.
  183. Liu, Z., A. Mukherjee & J. Lutkenhaus, (1999) Recruitment of ZipA to the division site by interaction with FtsZ. Mol Microbiol 31: 1853-1861.
  184. Konovalova, A., L. Sogaard-Andersen & L. Kroos, (2014) Regulated proteolysis in bacterial development. FEMS microbiology reviews 38: 493-522.
  185. Rolbetzki, A., M. Ammon, V. Jakovljevic, A. Konovalova & L. Sogaard-Andersen, (2008) Regulated secretion of a protease activates intercellular signaling during fruiting body formation in M. xanthus. Developmental cell 15: 627-634.
  186. Konovalova, A., (2010) Regulation of secretion of the signalling protease PopC in Myxococcus xanthus. PhD thesis.
  187. Chater, K.F., (2001) Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex? Curr Opin Microbiol 4: 667-673.
  188. Bulyha, I., C. Schmidt, P. Lenz, V. Jakovljevic, A. Hone, B. Maier, M. Hoppert & L. Sogaard-Andersen, (2009) Regulation of the type IV pili molecular machine by dynamic localization of two motor proteins. Mol Microbiol 74: 691-706.
  189. Burkholder, W.F., I. Kurtser & A.D. Grossman, (2001) Replication initiation proteins regulate a developmental checkpoint in Bacillus subtilis. Cell 104: 269-279.
  190. Ruban-Osmialowska, B., D. Jakimowicz, A. Smulczyk-Krawczyszyn, K.F. Chater & J. Zakrzewska-Czerwinska, (2006) Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor. J Bacteriol 188: 7311-7316.
  191. Pomerantz, R.T. & M. O'Donnell, (2007) Replisome mechanics: insights into a twin DNA polymerase machine. Trends Microbiol 15: 156-164.
  192. Sudo, S.Z. & M. Dworkin, (1969) Resistance of vegetative cells and microcysts of Myxococcus xanthus. J Bacteriol 98: 883-887.
  193. Bath, J., L.J. Wu, J. Errington & J.C. Wang, (2000) Role of Bacillus subtilis SpoIIIE in DNA transport across the mother cell-prespore division septum. Science 290: 995-997.
  194. Serrano, M., A. Neves, C.M. Soares, C.P. Moran, Jr. & A.O. Henriques, (2004) Role of the anti-sigma factor SpoIIAB in regulation of sigmaG during Bacillus subtilis sporulation. J Bacteriol 186: 4000-4013.
  195. de Boer, P.A., R.E. Crossley & L.I. Rothfield, (1992b) Roles of MinC and MinD in the site-specific septation block mediated by the MinCDE system of Escherichia coli. J Bacteriol 174: 63-70.
  196. Garza, A.G., J.S. Pollack, B.Z. Harris, A. Lee, I.M. Keseler, E.F. Licking & M. Singer, (1998) SdeK is required for early fruiting body development in Myxococcus xanthus. J Bacteriol 180: 4628-4637.
  197. Hamoen, L.W., J.C. Meile, W. de Jong, P. Noirot & J. Errington, (2006) SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol Microbiol 59: 989-999.
  198. Zhang, L., J. Willemse, D. Claessen & G.P. van Wezel, (2016) SepG coordinates sporulation-specific cell division and nucleoid organization in Streptomyces coelicolor. Open biology 6: 150164.
  199. Kaiser, D., (2004) Signaling in myxobacteria. Annual review of microbiology 58: 75-98.
  200. Bernhardt, T.G. & P.A. de Boer, (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over Chromosomes in E. coli. Mol Cell 18: 555-564.
  201. Shimkets, L.J., (1990) Social and developmental biology of the Myxobacteria. Microbiological reviews 54: 473-501.
  202. Kaiser, D., (1979) Social gliding is correlated with the presence of pili in Myxococcus xanthus. Proc Natl Acad Sci U S A 76: 5952-5956.
  203. Lau, I.F., S.R. Filipe, B. Soballe, O.A. Okstad, F.X. Barre & D.J. Sherratt, (2003) Spatial and temporal organization of replicating Escherichia coli chromosomes. Mol Microbiol 49: 731-743.
  204. Berkmen, M.B. & A.D. Grossman, (2006) Spatial and temporal organization of the Bacillus subtilis replication cycle. Mol Microbiol 62: 57-71.
  205. Julien, B., A.D. Kaiser & A. Garza, (2000) Spatial control of cell differentiation in Myxococcus xanthus. Proc Natl Acad Sci U S A 97: 9098-9103.
  206. Boonstra, M., I.G. de Jong, G. Scholefield, H. Murray, O.P. Kuipers & J.W. Veening, (2013) Spo0A regulates chromosome copy number during sporulation by directly binding to the origin of replication in Bacillus subtilis. Mol Microbiol 87: 925-938.
  207. Tan, I.S. & K.S. Ramamurthi, (2014) Spore formation in Bacillus subtilis. Environmental microbiology reports 6: 212-225.
  208. Müller, F.D., C.W. Schink, E. Hoiczyk, E. Cserti & P.I. Higgs, (2012) Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83: 486-505.
  209. Piggot, P.J. & D.W. Hilbert, (2004) Sporulation of Bacillus subtilis. Curr Opin Microbiol 7: 579-586.
  210. Shereda, R.D., A.G. Kozlov, T.M. Lohman, M.M. Cox & J.L. Keck, (2008) SSB as an organizer/mobilizer of genome maintenance complexes. Crit Rev Biochem Mol Biol 43: 289-318.
  211. Lu, C., M. Reedy & H.P. Erickson, (2000) Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J Bacteriol 182: 164-170.
  212. Flärdh, K. & M.J. Buttner, (2009) Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat Rev Microbiol 7: 36-49.
  213. Oliva, M.A., S.C. Cordell & J. Lowe, (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11: 1243-1250.
  214. Thanbichler, M., (2010) Synchronization of chromosome dynamics and cell division in bacteria. Cold Spring Harbor perspectives in biology 2: a000331.
  215. Hurley, K.A., T.M. Santos, G.M. Nepomuceno, V. Huynh, J.T. Shaw & D.B. Weibel, (2016) Targeting the Bacterial Division Protein FtsZ. Journal of medicinal chemistry 59: 6975-6998.
  216. Pichoff, S. & J. Lutkenhaus, (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55: 1722-1734.
  217. Gronewold, T.M. & D. Kaiser, (2001) The act operon controls the level and time of C- signal production for Myxococcus xanthus development. Mol Microbiol 40: 744- 756.
  218. Kroos, L., (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annual review of genetics 41: 13-39.
  219. Edwards, D.H. & J. Errington, (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24: 905-915.
  220. Loose, M. & T.J. Mitchison, (2014) The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nature cell biology 16: 38-46.
  221. Messer, W., (2002) The bacterial replication initiator DnaA. DnaA and oriC, the bacterial mode to initiate DNA replication. FEMS microbiology reviews 26: 355- 374.
  222. Jensen, R.B. & L. Shapiro, (1999) The Caulobacter crescentus smc gene is required for cell cycle progression and chromosome segregation. Proc Natl Acad Sci U S A 96: 10661-10666.
  223. Weart, R.B., S. Nakano, B.E. Lane, P. Zuber & P.A. Levin, (2005) The ClpX chaperone modulates assembly of the tubulin-like protein FtsZ. Mol Microbiol 57: 238-249.
  224. Shen, B. & J. Lutkenhaus, (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.
  225. Duan, Y., J.D. Huey & J.K. Herman, (2016) The DnaA inhibitor SirA acts in the same pathway as Soj (ParA) to facilitate oriC segregation during Bacillus subtilis sporulation. Mol Microbiol 102: 530-544.
  226. Radhakrishnan, S.K., M. Thanbichler & P.H. Viollier, (2008) The dynamic interplay between a cell fate determinant and a lysozyme homolog drives the asymmetric division cycle of Caulobacter crescentus. Genes & development 22: 212-225.
  227. Giglio, K.M., C. Zhu, C. Klunder, S. Kummer & A.G. Garza, (2015) The enhancer binding protein Nla6 regulates developmental genes that are important for Myxococcus xanthus sporulation. J Bacteriol 197: 1276-1287.
  228. Nordstrom, K., R. Bernander & S. Dasgupta, (1991) The Escherichia coli cell cycle: one cycle or multiple independent processes that are co-ordinated? Mol Microbiol 5: 769-774.
  229. de Boer, P., R. Crossley & L. Rothfield, (1992a) The essential bacterial cell-division protein FtsZ is a GTPase. Nature 359: 254-256.
  230. Dworkin, M. & H. Voelz, (1962) The formation and germination of microcysts in Myxococcus xanthus. J Gen Microbiol 28: 81-85.
  231. Ellehauge, E., M. Norregaard-Madsen & L. Sogaard-Andersen, (1998) The FruA signal transduction protein provides a checkpoint for the temporal co-ordination of intercellular signals in Myxococcus xanthus development. Mol Microbiol 30: 807-817.
  232. Harris, B.Z., D. Kaiser & M. Singer, (1998) The guanosine nucleotide (p)ppGpp initiates development and A-factor production in Myxococcus xanthus. Genes & development 12: 1022-1035.
  233. Cunningham, K.A. & W.F. Burkholder, (2009) The histidine kinase inhibitor Sda binds near the site of autophosphorylation and may sterically hinder autophosphorylation and phosphotransfer to Spo0F. Mol Microbiol 71: 659-677.
  234. Tojo, N., S. Inouye & T. Komano, (1993b) The lonD gene is homologous to the lon gene encoding an ATP-dependent protease and is essential for the development of Myxococcus xanthus. J Bacteriol 175: 4545-4549.
  235. Hu, Z., A. Mukherjee, S. Pichoff & J. Lutkenhaus, (1999) The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc Natl Acad Sci U S A 96: 14819-14824.
  236. van Baarle, S. & M. Bramkamp, (2010) The MinCDJ system in Bacillus subtilis prevents minicell formation by promoting divisome disassembly. PLoS One 5: e9850. van Vliet, S. & M. Ackermann, (2015) Bacterial Ventures into Multicellularity: Collectivism through Individuality. PLoS biology 13: e1002162.
  237. Szeto, T.H., S.L. Rowland, C.L. Habrukowich & G.F. King, (2003) The MinD membrane targeting sequence is a transplantable lipid-binding helix. J Biol Chem 278: 40050-40056.
  238. de Boer, P.A., R.E. Crossley, A.R. Hand & L.I. Rothfield, (1991) The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J 10: 4371-4380.
  239. Rosario, C.J. & M. Singer, (2007) The Myxococcus xanthus developmental program can be delayed by inhibition of DNA replication. J Bacteriol 189: 8793-8800.
  240. Ossa, F., M.E. Diodati, N.B. Caberoy, K.M. Giglio, M. Edmonds, M. Singer & A.G. Garza, (2007) The Myxococcus xanthus Nla4 protein is important for expression of stringent response-associated genes, ppGpp accumulation, and fruiting body development. J Bacteriol 189: 8474-8483.
  241. Wu, S.S., J. Wu & D. Kaiser, (1997) The Myxococcus xanthus pilT locus is required for social gliding motility although pili are still produced. Mol Microbiol 23: 109-121.
  242. Crawford, E.W., Jr. & L.J. Shimkets, (2000a) The Myxococcus xanthus socE and csgA genes are regulated by the stringent response. Mol Microbiol 37: 788-799.
  243. Lee, B., P. Mann, V. Grover, A. Treuner-Lange, J. Kahnt & P.I. Higgs, (2011) The Myxococcus xanthus spore cuticula protein C is a fragment of FibA, an extracellular metalloprotease produced exclusively in aggregated cells. PLoS One 6: e28968.
  244. Cabre, E.J., B. Monterroso, C. Alfonso, A. Sanchez-Gorostiaga, B. Reija, M. Jimenez, M. Vicente, S. Zorrilla & G. Rivas, (2015) The Nucleoid Occlusion SlmA Protein Accelerates the Disassembly of the FtsZ Protein Polymers without Affecting Their GTPase Activity. PLoS One 10: e0126434.
  245. Overgaard, M., S. Wegener-Feldbrugge & L. Sogaard-Andersen, (2006) The orphan response regulator DigR is required for synthesis of extracellular matrix fibrils in Myxococcus xanthus. J Bacteriol 188: 4384-4394.
  246. Jakimowicz, D., K. Chater & J. Zakrzewska-Czerwinska, (2002) The ParB protein of Streptomyces coelicolor A3(2) recognizes a cluster of parS sequences within the origin-proximal region of the linear chromosome. Mol Microbiol 45: 1365- 1377.
  247. Scheffers, D. & A.J. Driessen, (2001) The polymerization mechanism of the bacterial cell division protein FtsZ. FEBS letters 506: 6-10.
  248. Schumacher, D., (2016) The PomXYZ cell division regulators self-organize on the nucleoid to position cell division at midcell in the rod-shaped bacterium Myxococcus xanthus. In., pp.
  249. Schumacher, D., S. Bergeler, A. Harms, J. Vonck, S. Huneke-Vogt, E. Frey & L. Sogaard-Andersen, (2017) The PomXYZ Proteins Self-Organize on the Bacterial Nucleoid to Stimulate Cell Division. Developmental cell 41: 299-314 e213.
  250. Andersen, (2017) The PomXYZ Proteins Self-Organize on the Bacterial Nucleoid to Stimulate Cell Division. Developmental cell 41: 299-314 e213.
  251. Dai, K. & J. Lutkenhaus, (1992) The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol 174: 6145-6151.
  252. Bush, M. & R. Dixon, (2012) The role of bacterial enhancer binding proteins as specialized activators of sigma54-dependent transcription. Microbiol Mol Biol Rev 76: 497-529.
  253. Li, Y., K. Sergueev & S. Austin, (2002) The segregation of the Escherichia coli origin and terminus of replication. Mol Microbiol 46: 985-996.
  254. Rahn-Lee, L., H. Merrikh, A.D. Grossman & R. Losick, (2011) The sporulation protein SirA inhibits the binding of DnaA to the origin of replication by contacting a patch of clustered amino acids. J Bacteriol 193: 1302-1307.
  255. Crawford, E.W., Jr. & L.J. Shimkets, (2000b) The stringent response in Myxococcus xanthus is regulated by SocE and the CsgA C-signaling protein. Genes & development 14: 483-492.
  256. Hu, Z. & J. Lutkenhaus, (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.
  257. Harms, A., A. Treuner-Lange, D. Schumacher & L. Sogaard-Andersen, (2013) Tracking of chromosome and replisome dynamics in Myxococcus xanthus reveals a novel chromosome arrangement. PLoS Genet 9: e1003802.
  258. Roy, S. & P. Ajitkumar, (2005) Transcriptional analysis of the principal cell division gene, ftsZ, of Mycobacterium tuberculosis. J Bacteriol 187: 2540-2550.
  259. Robinson, M., B. Son, D. Kroos & L. Kroos, (2014) Transcription factor MrpC binds to promoter regions of hundreds of developmentally-regulated genes in Myxococcus xanthus. BMC genomics 15: 1123.
  260. Levin, P.A. & R. Losick, (1996) Transcription factor Spo0A switches the localization of the cell division protein FtsZ from a medial to a bipolar pattern in Bacillus subtilis. Genes & development 10: 478-488.
  261. Garrido, T., M. Sanchez, P. Palacios, M. Aldea & M. Vicente, (1993) Transcription of ftsZ oscillates during the cell cycle of Escherichia coli. EMBO J 12: 3957-3965.
  262. Romeo, J.M. & D.R. Zusman, (1991) Transcription of the myxobacterial hemagglutinin gene is mediated by a sigma 54-like promoter and a cis-acting upstream regulatory region of DNA. J Bacteriol 173: 2969-2976.
  263. Feng, J., S. Michalik, A.N. Varming, J.H. Andersen, D. Albrecht, L. Jelsbak, S. Krieger, K. Ohlsen, M. Hecker, U. Gerth, H. Ingmer & D. Frees, (2013) Trapping and proteomic identification of cellular substrates of the ClpP protease in Staphylococcus aureus. Journal of proteome research 12: 547-558.
  264. Bisson-Filho, A.W., Y.P. Hsu, G.R. Squyres, E. Kuru, F. Wu, C. Jukes, Y. Sun, C. Dekker, S. Holden, M.S. VanNieuwenhze, Y.V. Brun & E.C. Garner, (2017) Treadmilling by FtsZ filaments drives peptidoglycan synthesis and bacterial cell division. Science 355: 739-743.
  265. Nogales, E., K.H. Downing, L.A. Amos & J. Lowe, (1998) Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol 5: 451-458.
  266. Iniesta, A.A., F. Garcia-Heras, J. Abellon-Ruiz, A. Gallego-Garcia & M. Elias-Arnanz, (2012) Two systems for conditional gene expression in Myxococcus xanthus inducible by isopropyl-beta-D-thiogalactopyranoside or vanillate. J Bacteriol 194: 5875-5885.
  267. Pichoff, S. & J. Lutkenhaus, (2002) Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J 21: 685-693.


* Das Dokument ist im Internet frei zugänglich - Hinweise zu den Nutzungsrechten