Investigating the Function and the Interaction Network of the Flagellar Regulator ATPase FlhG

Motility plays a key role for the superior survival strategy of many bacteria. Sophisticated, macromolecular machines, called flagella, serve as bacterial locomotion organelles. These flagella appear in distinct spatial arrangements along the bacterial cell, constituting the flagellation patterns, w...

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Main Author: Schuhmacher, Jan Simon
Contributors: Bange, Gert (Dr.) (Thesis advisor)
Format: Dissertation
Language:English
Published: Philipps-Universität Marburg 2015
Chemie
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1. Kirkpatrick CL & Viollier PH (2011) Poles Apart: Prokaryotic Polar Organelles and Their Spatial Regulation. Cold Spring Harbor Perspectives in Biology 3(3).


2. McPherson A (1982) Preparation and analysis of protein crystals (John Wiley & Sons).


3. Carpenter PB, Hanlon DW, Kirsch ML, & Ordal GW (1994) Novel aspects of chemotactic sensory transduction in Bacillus subtilis. Res Microbiol 145(5-6):413-419. Bibliography 159


4. Adams DW, Wu LJ, & Errington J (2015) Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. EMBO J 34(4):491-501.


5. Srivatsan A, et al. (2008) High-precision, whole-genome sequencing of laboratory strains facilitates genetic studies. PLoS Genet 4(8):e1000139.


6. Fleurie A, et al. (2014) Interplay of the serine/threonine-kinase StkP and the paralogs DivIVA and GpsB in pneumococcal cell elongation and division. PLoS Genet 10(4):e1004275.


7. Schuhmacher JS (2012) Structure and Function of a MinD-like ATPase. Master Thesis (Heidelberg University, Heidelberg).


8. Wu LJ, et al. (2009) Noc protein binds to specific DNA sequences to coordinate cell division with chromosome segregation. EMBO J 28(13):1940-1952.


9. Ahmadian MR, Stege P, Scheffzek K, & Wittinghofer A (1997) Confirmation of the arginine-finger hypothesis for the GAP-stimulated GTP-hydrolysis reaction of Ras. Nat Struct Biol 4(9):686-689.


10. Ozin AJ, Claret L, Auvray F, & Hughes C (2003) The FliS chaperone selectively binds the disordered flagellin C-terminal D0 domain central to polymerisation. FEMS Microbiol Lett 219(2):219-224.


11. Marston AL, Thomaides HB, Edwards DH, Sharpe ME, & Errington J (1998) Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev 12(21):3419-3430.


12. Armitage JP & Macnab RM (1987) Unidirectional, intermittent rotation of the flagellum of Rhodobacter sphaeroides. J Bacteriol 169(2):514-518.


13. Garcia N, et al. (1998) The flagellar switch genes fliM and fliN of Rhodobacter sphaeroides are contained in a large flagellar gene cluster. J Bacteriol 180(15):3978- 3982.


14. Lackner LL, Raskin DM, & de Boer PA (2003) ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J Bacteriol 185(3):735-749.


15. Dyer CM & Dahlquist FW (2006) Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM. J Bacteriol 188(21):7354-7363.


16. Shiomi D & Margolin W (2007) The C-terminal domain of MinC inhibits assembly of the Z ring in Escherichia coli. J Bacteriol 189(1):236-243.


17. Muff TJ, Foster RM, Liu PJ, & Ordal GW (2007) CheX in the three-phosphatase system of bacterial chemotaxis. J Bacteriol 189(19):7007-7013.


18. Poggio S, et al. (2007) A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides. J Bacteriol 189(8):3208-3216.


19. Tavares JR, de Souza RF, Meira GL, & Gueiros-Filho FJ (2008) Cytological characterization of YpsB, a novel component of the Bacillus subtilis divisome. J Bacteriol 190(21):7096-7107.


20. Amin DN & Hazelbauer GL (2010) The chemoreceptor dimer is the unit of conformational coupling and transmembrane signaling. J Bacteriol 192(5):1193-1200.


21. Mukherjee S, Babitzke P, & Kearns DB (2013) FliW and FliS function independently to control cytoplasmic flagellin levels in Bacillus subtilis. J Bacteriol 195(2):297-306.


22. Galeva A, et al. (2014) Bacterial flagellin-specific chaperone FliS interacts with anti-s factor FlgM. J Bacteriol 196(6):1215-1221.


23. Schweinitzer T & Josenhans C (2010) Bacterial energy taxis: a global strategy? Arch Microbiol 192(7):507-520.


24. Pascal BD, et al. (2012) HDX workbench: software for the analysis of H/D exchange MS data. J Am Soc Mass Spectrom 23(9):1512-1521.


25. Mackenzie C, et al. (2001) The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth Res 70(1):19-41.


26. Hoff WD, van der Horst MA, Nudel CB, & Hellingwerf KJ (2009) Prokaryotic phototaxis. Methods Mol Biol 571:25-49.


27. Engen JR & Smith DL (2001) Investigating protein structure and dynamics by hydrogen exchange MS. Anal Chem 73(9):256A-265A.


28. Potrykus K & Cashel M (2008) (p)ppGpp: still magical? Annu Rev Microbiol 62:35-51.


29. Gass J & Khosla C (2007) Prolyl endopeptidases. Cell Mol Life Sci 64(3):345-355.


30. Agirrezabala X, et al. (2013) The ribosome triggers the stringent response by RelA via a highly distorted tRNA. EMBO Rep 14(9):811-816.


31. Geiger T, Kästle B, Gratani FL, Goerke C, & Wolz C (2014) Two small (p)ppGpp synthases in Staphylococcus aureus mediate tolerance against cell envelope stress conditions. J Bacteriol 196(4):894-902.


32. Capra EJ & Laub MT (2012) Evolution of two-component signal transduction systems. Annu Rev Microbiol 66:325-347.


33. Alexandre G (2010) Coupling metabolism and chemotaxis-dependent behaviours by energy taxis receptors. Microbiology 156(Pt 8):2283-2293.


34. Szurmant H & Ordal GW (2004) Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68(2):301-319.


35. Dalebroux ZD, Svensson SL, Gaynor EC, & Swanson MS (2010) ppGpp conjures bacterial virulence. Microbiol Mol Biol Rev 74(2):171-199.


36. Romling U, Galperin MY, & Gomelsky M (2013) Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77(1):1-52.


37. Mechold U, Potrykus K, Murphy H, Murakami KS, & Cashel M (2013) Differential regulation by ppGpp versus pppGpp in Escherichia coli. Nucleic Acids Res 41(12):6175- 6189.


38. Garcia RA, Pantazatos D, & Villarreal FJ (2004) Hydrogen/deuterium exchange mass spectrometry for investigating protein-ligand interactions. Assay Drug Dev Technol 2(1):81-91.


39. Wales TE & Engen JR (2006) Hydrogen exchange mass spectrometry for the analysis of protein dynamics. Mass Spectrom Rev 25(1):158-170.


40. Marston AL & Errington J (1999) Selection of the midcell division site in Bacillus subtilis through MinD-dependent polar localization and activation of MinC. Mol Microbiol 33(1):84- 96. Bibliography 158


41. Karoui ME & Errington J (2001) Isolation and characterization of topological specificity mutants of minD in Bacillus subtilis. Mol Microbiol 42(5):1211-1221.


42. Wu LJ & Errington J (2003) RacA and the Soj-Spo0J system combine to effect polar chromosome segregation in sporulating Bacillus subtilis. Mol Microbiol 49(6):1463-1475.


43. Lemos JA, Lin VK, Nascimento MM, Abranches J, & Burne RA (2007) Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol Microbiol 65(6):1568-1581.


44. Nanamiya H, et al. (2008) Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol Microbiol 67(2):291-304.


45. Patrick JE & Kearns DB (2008) MinJ (YvjD) is a topological determinant of cell division in Bacillus subtilis. Mol Microbiol 70(5):1166-1179.


46. Muff TJ & Ordal GW (2008) The diverse CheC-type phosphatases: chemotaxis and beyond. Mol Microbiol 70(5):1054-1061.


47. Bramkamp M, et al. (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(6):1556-1569.


48. 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(2):410-424.


49. 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(5):1285-1298.


50. 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(6):1515-1528.


51. Park KT, Wu W, Lovell S, & Lutkenhaus J (2012) Mechanism of the asymmetric activation of the MinD ATPase by MinE. Mol Microbiol 85(2):271-281.


52. Kanjee U, Ogata K, & Houry WA (2012) Direct binding targets of the stringent response alarmone (p)ppGpp. Mol Microbiol 85(6):1029-1043.


53. Kalbitzer HR, Goody RS, & Wittinghofer A (1984) Electron-paramagnetic-resonance studies of manganese(II) complexes with elongation factor Tu from Bacillus stearothermophilus. Observation of a GTP hydrolysis intermediate state complex. Eur J Biochem 141(3):591-597.


54. Mills E, Pultz IS, Kulasekara HD, & Miller SI (2011) The bacterial second messenger c-di- GMP: mechanisms of signalling. Cell Microbiol 13(8):1122-1129.


55. Egan AJ & Vollmer W (2013) The physiology of bacterial cell division. Ann N Y Acad Sci 1277:8-28. Bibliography 161


56. Lam KH, et al. (2013) Structural basis of FliG-FliM interaction in Helicobacter pylori. Mol Microbiol 88(4):798-812.


57. Pompeo F, Foulquier E, Serrano B, Grangeasse C, & Galinier A (2015) Phosphorylation of the cell division protein GpsB regulates PrkC kinase activity through a negative feedback loop in Bacillus subtilis. Mol Microbiol.


58. Ramakrishnan C, Dani VS, & Ramasarma T (2002) A conformational analysis of Walker motif A [GXXXXGKT (S)] in nucleotide-binding and other proteins. Protein Eng 15(10):783-798.


59. Dyson HJ & Wright PE (2004) Unfolded proteins and protein folding studied by NMR. Chem Rev 104(8):3607-3622.


60. Battye TGG, Kontogiannis L, Johnson O, Powell HR, & Leslie AGW (2011) iMOSFLM: a new graphical interface for diffraction-image processing with MOSFLM. Acta Crystallographica Section D 67(4):271-281.


61. McCoy AJ, et al. (2007) Phaser crystallographic software. Journal of Applied Crystallography 40(4):658-674.


62. Emsley P & Cowtan K (2004) Coot: model-building tools for molecular graphics. Acta Crystallographica Section D 60(12 Part 1):2126-2132.


63. Winn MD, et al. (2011) Overview of the CCP4 suite and current developments. Acta Crystallographica Section D 67(4):235-242.


64. Boyd CD & O'Toole GA (2012) Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems. Annu Rev Cell Dev Biol 28:439-462.


65. Sprang SR (1997) G protein mechanisms: insights from structural analysis. Annu Rev Biochem 66:639-678.


66. Stock AM, Robinson VL, & Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69:183-215.


67. Hoofnagle AN, Resing KA, & Ahn NG (2003) Protein analysis by hydrogen exchange mass spectrometry. Annu Rev Biophys Biomol Struct 32:1-25.


68. Jenal U & Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40:385-407.


69. Gilman AG (1987) G proteins: transducers of receptor-generated signals. Annu Rev Biochem 56:615-649.


70. Jain V, Kumar M, & Chatterji D (2006) ppGpp: stringent response and survival. J Microbiol 44(1):1-10.


71. Vladimirov N & Sourjik V (2009) Chemotaxis: how bacteria use memory. Biol Chem 390(11):1097-1104.


72. Adams PD, et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallographica Section D 66(2):213-221.


73. Szeto TH, Rowland SL, Habrukowich CL, & King GF (2003) The MinD membrane targeting sequence is a transplantable lipid-binding helix. J Biol Chem 278(41):40050- 40056.


74. Szurmant H, Bunn MW, Cannistraro VJ, & Ordal GW (2003) Bacillus subtilis hydrolyzes CheY-P at the location of its action, the flagellar switch. J Biol Chem 278(49):48611- 48616.


75. Rist W, Jorgensen TJ, Roepstorff P, Bukau B, & Mayer MP (2003) Mapping temperature- induced conformational changes in the Escherichia coli heat shock transcription factor s 32 by amide hydrogen exchange. J Biol Chem 278(51):51415-51421.


76. Szurmant H, Muff TJ, & Ordal GW (2004) Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J Biol Chem 279(21):21787-21792.


77. Parlitz R, et al. (2007) Escherichia coli signal recognition particle receptor FtsY contains an essential and autonomous membrane-binding amphipathic helix. J Biol Chem 282(44):32176-32184.


78. Stjepanovic G, et al. (2011) Lipids trigger a conformational switch that regulates signal recognition particle (SRP)-mediated protein targeting. J Biol Chem 286(26):23489-23497.


79. Sircar R, Greenswag AR, Bilwes AM, Gonzalez-Bonet G, & Crane BR (2013) Structure and activity of the flagellar rotor protein FliY: a member of the CheC phosphatase family. J Biol Chem 288(19):13493-13502.


80. Rao CV & Ordal GW (2009) The molecular basis of excitation and adaptation during chemotactic sensory transduction in bacteria. Contrib Microbiol 16:33-64.


81. Ravikumar V, et al. (2014) Quantitative phosphoproteome analysis of Bacillus subtilis reveals novel substrates of the kinase PrkC and phosphatase PrpC. Mol Cell Proteomics 13(8):1965-1978.


82. Temeles GL, Gibbs JB, D'Alonzo JS, Sigal IS, & Scolnick EM (1985) Yeast and mammalian ras proteins have conserved biochemical properties. Nature 313(6004):700- 703.


83. Deckert G, et al. (1998) The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature 392(6674):353-358. Bibliography 160


84. Nelson KE, et al. (1999) Evidence for lateral gene transfer between Archaea and bacteria from genome sequence of Thermotoga maritima. Nature 399(6734):323-329.


85. Pausch P, et al. (2015) Co-translational capturing of nascent ribosomal proteins by their dedicated chaperones. Nat Commun 6:7494.


86. Wadhams GH & Armitage JP (2004) Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5(12):1024-1037.


87. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7(4):263-273.


88. Adams DW & Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7(9):642-653.


89. Porter SL, Wadhams GH, & Armitage JP (2011) Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9(3):153-165.


90. Evdokimov AG, et al. (2003) Similar modes of polypeptide recognition by export chaperones in flagellar biosynthesis and type III secretion. Nat Struct Biol 10(10):789-793.


91. Lanman J, et al. (2004) Key interactions in HIV-1 maturation identified by hydrogen- deuterium exchange. Nat Struct Mol Biol 11(7):676-677.


92. Lee SY, et al. (2001) Crystal structure of an activated response regulator bound to its target. Nat Struct Biol 8(1):52-56.


93. Kawamoto A, et al. (2013) Common and distinct structural features of Salmonella injectisome and flagellar basal body. Sci Rep 3:3369.


94. Evans LD, Poulter S, Terentjev EM, Hughes C, & Fraser GM (2013) A chain mechanism for flagellum growth. Nature 504(7479):287-290.


95. Titz B, Rajagopala SV, Ester C, Hauser R, & Uetz P (2006) Novel conserved assembly factor of the bacterial flagellum. J Bacteriol 188(21):7700-7706.


96. Wolfe AJ & Visick KL (2008) Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190(2):463-475.


97. Adler HI, Fisher WD, Cohen A, & Hardigree AA (1967) Miniature Escherichia coli cells deficient in DNA. Proc Natl Acad Sci USA 57(2):321-326.


98. Walker JE, Saraste M, Runswick MJ, & Gay NJ (1982) Distantly related sequences in the alpha-and beta-subunits of ATP synthase, myosin, kinases and other ATP-requiring enzymes and a common nucleotide binding fold. EMBO J 1(8):945-951.


99. Du X, Black GE, Lecchi P, Abramson FP, & Sprang SR (2004) Kinetic isotope effects in Ras-catalyzed GTP hydrolysis: evidence for a loose transition state. Proc Natl Acad Sci USA 101(24):8858-8863.


100. Feng L, et al. (2007) Genome and proteome of long-chain alkane degrading Geobacillus thermodenitrificans NG80-2 isolated from a deep-subsurface oil reservoir. Proc Natl Acad Sci USA 104(13):5602-5607.


101. Alexander RP & Zhulin IB (2007) Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc Natl Acad Sci USA 104(8):2885-2890.


102. Briegel A, et al. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106(40):17181-17186.


103. English BP, et al. (2011) Single-molecule investigations of the stringent response machinery in living bacterial cells. Proc Natl Acad Sci USA 108(31):E365-373.


104. Manne V, Bekesi E, & Kung HF (1985) Ha-ras proteins exhibit GTPase activity: point mutations that activate Ha-ras gene products result in decreased GTPase activity. Proc Natl Acad Sci USA 82(2):376-380.


105. Welch M, Oosawa K, Aizawa S, & Eisenbach M (1993) Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc Natl Acad Sci USA 90(19):8787-8791.


106. Mukherjee A, Dai K, & Lutkenhaus J (1993) Escherichia coli cell division protein FtsZ is a guanine nucleotide binding protein. Proc Natl Acad Sci USA 90(3):1053-1057.


107. Raskin DM & de Boer PA (1999) Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc Natl Acad Sci USA 96(9):4971- 4976.


108. Sourjik V & Berg HC (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99(1):123-127.


109. Katta V & Chait BT (1991) Conformational changes in proteins probed by hydrogen- exchange electrospray-ionization mass spectrometry. Rapid Commun Mass Spectrom 5(4):214-217. Bibliography 162


110. Hope MJ, Bally MB, Webb G, & Cullis PR (1985) Production of large unilamellar vesicles by a rapid extrusion procedure: characterization of size distribution, trapped volume and ability to maintain a membrane potential. Biochim Biophys Acta 812(1):55-65.


111. Borkovich KA & Simon MI (1990) The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63(6):1339-1348.


112. Garrity LF & Ordal GW (1995) Chemotaxis in Bacillus subtilis: how bacteria monitor environmental signals. Pharmacol Ther 68(1):87-104.


113. Muskotal A, et al. (2006) Interaction of FliS flagellar chaperone with flagellin. FEBS Lett 580(16):3916-3920.


114. Auvray F, Thomas J, Fraser GM, & Hughes C (2001) Flagellin polymerisation control by a cytosolic export chaperone. J Mol Biol 308(2):221-229.


115. Lanman J, et al. (2003) Identification of novel interactions in HIV-1 capsid protein assembly by high-resolution mass spectrometry. J Mol Biol 325(4):759-772.


116. Dyer CM, et al. (2004) Structure of the constitutively active double mutant CheYD13K Y106W alone and in complex with a FliM peptide. J Mol Biol 342(4):1325-1335.


117. Dyer CM, Vartanian AS, Zhou H, & Dahlquist FW (2009) A molecular mechanism of bacterial flagellar motor switching. J Mol Biol 388(1):71-84.


118. Koonin EV (1993) A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. J Mol Biol 229(4):1165-1174.


119. Zhao R, Pathak N, Jaffe H, Reese TS, & Khan S (1996) FliN is a major structural protein of the C-ring in the Salmonella typhimurium flagellar basal body. J Mol Biol 261(2):195- 208.


120. Hogg T, Mechold U, Malke H, Cashel M, & Hilgenfeld R (2004) Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response [corrected]. Cell 117(1):57-68. Bibliography 163


121. Thanbichler M & Shapiro L (2006) MipZ, a spatial regulator coordinating chromosome segregation with cell division in Caulobacter. Cell 126(1):147-162.


122. Park KT, et al. (2011) The Min oscillator uses MinD-dependent conformational changes in MinE to spatially regulate cytokinesis. Cell 146(3):396-407.


123. Lewis PJ & Marston AL (1999) GFP vectors for controlled expression and dual labelling of protein fusions in Bacillus subtilis. Gene 227(1):101-109.


124. Fülöp V & Jones DT (1999) Beta propellers: structural rigidity and functional diversity. Curr Opin Struct Biol 9(6):715-721.


125. Dajkovic A, Lan G, Sun SX, Wirtz D, & Lutkenhaus J (2008) MinC spatially controls bacterial cytokinesis by antagonizing the scaffolding function of FtsZ. Curr Biol 18(4):235- 244.


126. Porter SL, Wadhams GH, & Armitage JP (2008) Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends Microbiol 16(6):251-260.


127. Hazelbauer GL, Falke JJ, & Parkinson JS (2008) Bacterial chemoreceptors: high- performance signaling in networked arrays. Trends Biochem Sci 33(1):9-19.


128. Chen CK, Chan NL, & Wang AH (2011) The many blades of the beta-propeller proteins: conserved but versatile. Trends Biochem Sci 36(10):553-561. Bibliography 164


129. Eyles SJ & Kaltashov IA (2004) Methods to study protein dynamics and folding by mass spectrometry. Methods 34(1):88-99.


130. McPherson A & Gavira JA (2014) Introduction to protein crystallization. Acta Crystallogr F Struct Biol Commun 70(Pt 1):2-20.


131. Khan S, Zhao R, & Reese TS (1998) Architectural features of the Salmonella typhimurium flagellar motor switch revealed by disrupted C-rings. J Struct Biol 122(3):311-319.


132. Quisel JD, Lin DC, & Grossman AD (1999) Control of development by altered localization of a transcription factor in B. subtilis. Mol Cell 4(5):665-672.


133. 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(5):673-682.


134. 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(6):1337-1343.


135. Wendrich TM, Blaha G, Wilson DN, Marahiel MA, & Nierhaus KH (2002) Dissection of the mechanism for the stringent factor RelA. Mol Cell 10(4):779-788.


136. Adams DW, Wu LJ, & Errington J (2014) Cell cycle regulation by the bacterial nucleoid. Curr Opin Microbiol 22:94-101.


137. Salazar ME & Laub MT (2015) Temporal and evolutionary dynamics of two-component signaling pathways. Curr Opin Microbiol 24:7-14.


138. Maddock JR & Shapiro L (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259(5102):1717-1723.