4gcl Citations

SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid.

Proc Natl Acad Sci U S A 110 10586-91 (2013)
Related entries: 4gck, 4gct, 4gfk, 4gfl

Cited: 56 times
EuropePMC logo PMID: 23754405

Abstract

The spatial and temporal control of Filamenting temperature sensitive mutant Z (FtsZ) Z-ring formation is crucial for proper cell division in bacteria. In Escherichia coli, the synthetic lethal with a defective Min system (SlmA) protein helps mediate nucleoid occlusion, which prevents chromosome fragmentation by binding FtsZ and inhibiting Z-ring formation over the nucleoid. However, to perform its function, SlmA must be bound to the nucleoid. To deduce the basis for this chromosomal requirement, we performed biochemical, cellular, and structural studies. Strikingly, structures show that SlmA dramatically distorts DNA, allowing it to bind as an orientated dimer-of-dimers. Biochemical data indicate that SlmA dimer-of-dimers can spread along the DNA. Combined structural and biochemical data suggest that this DNA-activated SlmA oligomerization would prevent FtsZ protofilament propagation and bundling. Bioinformatic analyses localize SlmA DNA sites near membrane-tethered chromosomal regions, and cellular studies show that SlmA inhibits FtsZ reservoirs from forming membrane-tethered Z rings. Thus, our combined data indicate that SlmA DNA helps block Z-ring formation over chromosomal DNA by forming higher-order protein-nucleic acid complexes that disable FtsZ filaments from coalescing into proper structures needed for Z-ring creation.

Articles - 4gcl mentioned but not cited (3)

  1. SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Tonthat NK, Milam SL, Chinnam N, Whitfill T, Margolin W, Schumacher MA. Proc Natl Acad Sci U S A 110 10586-10591 (2013)
  2. SlmA antagonism of FtsZ assembly employs a two-pronged mechanism like MinCD. Du S, Lutkenhaus J. PLoS Genet 10 e1004460 (2014)
  3. Structures of the nucleoid occlusion protein SlmA bound to DNA and the C-terminal domain of the cytoskeletal protein FtsZ. Schumacher MA, Zeng W. Proc Natl Acad Sci U S A 113 4988-4993 (2016)


Reviews citing this publication (17)

  1. Subcellular Organization: A Critical Feature of Bacterial Cell Replication. Surovtsev IV, Jacobs-Wagner C. Cell 172 1271-1293 (2018)
  2. The keepers of the ring: regulators of FtsZ assembly. Ortiz C, Natale P, Cueto L, Vicente M. FEMS Microbiol Rev 40 57-67 (2016)
  3. The Min system and other nucleoid-independent regulators of Z ring positioning. Rowlett VW, Margolin W. Front Microbiol 6 478 (2015)
  4. Division site positioning in bacteria: one size does not fit all. Monahan LG, Liew AT, Bottomley AL, Harry EJ. Front Microbiol 5 19 (2014)
  5. Bacterial actin and tubulin homologs in cell growth and division. Busiek KK, Margolin W. Curr Biol 25 R243-R254 (2015)
  6. Coevolution of the Organization and Structure of Prokaryotic Genomes. Touchon M, Rocha EP. Cold Spring Harb Perspect Biol 8 a018168 (2016)
  7. Cell cycle regulation by the bacterial nucleoid. Adams DW, Wu LJ, Errington J. Curr Opin Microbiol 22 94-101 (2014)
  8. Guiding divisome assembly and controlling its activity. Tsang MJ, Bernhardt TG. Curr Opin Microbiol 24 60-65 (2015)
  9. Connecting the dots of the bacterial cell cycle: Coordinating chromosome replication and segregation with cell division. Hajduk IV, Rodrigues CD, Harry EJ. Semin Cell Dev Biol 53 2-9 (2016)
  10. Divided we stand: splitting synthetic cells for their proliferation. Caspi Y, Dekker C. Syst Synth Biol 8 249-269 (2014)
  11. The bacterial divisome: ready for its close-up. Rowlett VW, Margolin W. Philos Trans R Soc Lond B Biol Sci 370 20150028 (2015)
  12. Collaborative protein filaments. Ghosal D, Löwe J. EMBO J 34 2312-2320 (2015)
  13. Regulation of cytokinesis: FtsZ and its accessory proteins. Wang M, Fang C, Ma B, Luo X, Hou Z. Curr Genet 66 43-49 (2020)
  14. Bacterial Vivisection: How Fluorescence-Based Imaging Techniques Shed a Light on the Inner Workings of Bacteria. Cambré A, Aertsen A. Microbiol Mol Biol Rev 84 e00008-20 (2020)
  15. Bacterial cell division: experimental and theoretical approaches to the divisome. Broughton CE, Roper DI, Van Den Berg HA, Rodger A. Sci Prog 98 313-345 (2015)
  16. Insights into the assembly and regulation of the bacterial divisome. Cameron TA, Margolin W. Nat Rev Microbiol 22 33-45 (2024)
  17. Filamentous morphology of bacterial pathogens: regulatory factors and control strategies. Khan F, Jeong GJ, Tabassum N, Mishra A, Kim YM. Appl Microbiol Biotechnol 106 5835-5862 (2022)

Articles citing this publication (36)

  1. Nucleoid occlusion protein Noc recruits DNA to the bacterial cell membrane. Adams DW, Wu LJ, Errington J. EMBO J 34 491-501 (2015)
  2. Bacterial FtsZ protein forms phase-separated condensates with its nucleoid-associated inhibitor SlmA. Monterroso B, Zorrilla S, Sobrinos-Sanguino M, Robles-Ramos MA, López-Álvarez M, Margolin W, Keating CD, Rivas G. EMBO Rep 20 e45946 (2019)
  3. LocZ is a new cell division protein involved in proper septum placement in Streptococcus pneumoniae. Holečková N, Doubravová L, Massidda O, Molle V, Buriánková K, Benada O, Kofroňová O, Ulrych A, Branny P. mBio 6 e01700-14 (2014)
  4. The Kil peptide of bacteriophage λ blocks Escherichia coli cytokinesis via ZipA-dependent inhibition of FtsZ assembly. Haeusser DP, Hoashi M, Weaver A, Brown N, Pan J, Sawitzke JA, Thomason LC, Court DL, Margolin W. PLoS Genet 10 e1004217 (2014)
  5. Spatial coordination between chromosomes and cell division proteins in Escherichia coli. Männik J, Bailey MW. Front Microbiol 6 306 (2015)
  6. MinCD cell division proteins form alternating copolymeric cytomotive filaments. Ghosal D, Trambaiolo D, Amos LA, Löwe J. Nat Commun 5 5341 (2014)
  7. ZapA and ZapB form an FtsZ-independent structure at midcell. Buss JA, Peters NT, Xiao J, Bernhardt TG. Mol Microbiol 104 652-663 (2017)
  8. The Escherichia coli divisome: born to divide. Natale P, Pazos M, Vicente M. Environ Microbiol 15 3169-3182 (2013)
  9. Evidence That Bacteriophage λ Kil Peptide Inhibits Bacterial Cell Division by Disrupting FtsZ Protofilaments and Sequestering Protein Subunits. Hernández-Rocamora VM, Alfonso C, Margolin W, Zorrilla S, Rivas G. J Biol Chem 290 20325-20335 (2015)
  10. FtsZ Polymers Tethered to the Membrane by ZipA Are Susceptible to Spatial Regulation by Min Waves. Martos A, Raso A, Jiménez M, Petrášek Z, Rivas G, Schwille P. Biophys J 108 2371-2383 (2015)
  11. GTPase domain driven dimerization of SEPT7 is dispensable for the critical role of septins in fibroblast cytokinesis. Abbey M, Hakim C, Anand R, Lafera J, Schambach A, Kispert A, Taft MH, Kaever V, Kotlyarov A, Gaestel M, Menon MB. Sci Rep 6 20007 (2016)
  12. Structural and functional characterization of a ketosteroid transcriptional regulator of Mycobacterium tuberculosis. Crowe AM, Stogios PJ, Casabon I, Evdokimova E, Savchenko A, Eltis LD. J Biol Chem 290 872-882 (2015)
  13. The Nucleoid Occlusion SlmA Protein Accelerates the Disassembly of the FtsZ Protein Polymers without Affecting Their GTPase Activity. Cabré EJ, Monterroso B, Alfonso C, Sánchez-Gorostiaga A, Reija B, Jiménez M, Vicente M, Zorrilla S, Rivas G. PLoS One 10 e0126434 (2015)
  14. Regulation of alkane degradation pathway by a TetR family repressor via an autoregulation positive feedback mechanism in a Gram-positive Dietzia bacterium. Liang JL, Nie Y, Wang M, Xiong G, Wang YP, Maser E, Wu XL. Mol Microbiol 99 338-359 (2016)
  15. Noc Corrals Migration of FtsZ Protofilaments during Cytokinesis in Bacillus subtilis. Yu Y, Zhou J, Gueiros-Filho FJ, Kearns DB, Jacobson SC. mBio 12 e02964-20 (2021)
  16. FtsZ placement in nucleoid-free bacteria. Pazos M, Casanova M, Palacios P, Margolin W, Natale P, Vicente M. PLoS One 9 e91984 (2014)
  17. Structural basis of operator sites recognition and effector binding in the TetR family transcription regulator FadR. Yeo HK, Park YW, Lee JY. Nucleic Acids Res 45 4244-4254 (2017)
  18. Repair on the go: E. coli maintains a high proliferation rate while repairing a chronic DNA double-strand break. Darmon E, Eykelenboom JK, Lopez-Vernaza MA, White MA, Leach DR. PLoS One 9 e110784 (2014)
  19. A cell length-dependent transition in MinD-dynamics promotes a switch in division-site placement and preservation of proliferating elongated Vibrio parahaemolyticus swarmer cells. Muraleedharan S, Freitas C, Mann P, Glatter T, Ringgaard S. Mol Microbiol 109 365-384 (2018)
  20. Structure of AmtR, the global nitrogen regulator of Corynebacterium glutamicum, in free and DNA-bound forms. Palanca C, Rubio V. FEBS J 283 1039-1059 (2016)
  21. The Bacterial DNA Binding Protein MatP Involved in Linking the Nucleoid Terminal Domain to the Divisome at Midcell Interacts with Lipid Membranes. Monterroso B, Zorrilla S, Sobrinos-Sanguino M, Robles-Ramos MÁ, Alfonso C, Söderström B, Meiresonne NY, Verheul J, den Blaauwen T, Rivas G. mBio 10 e00376-19 (2019)
  22. The nucleoid occlusion protein SlmA is a direct transcriptional activator of chitobiose utilization in Vibrio cholerae. Klancher CA, Hayes CA, Dalia AB. PLoS Genet 13 e1006877 (2017)
  23. A DNA-binding protein defines the precise region of chromosome capture during Bacillus sporulation. Miller AK, Brown EE, Mercado BT, Herman JK. Mol Microbiol 99 111-122 (2016)
  24. Escherichia coli CrfC Protein, a Nucleoid Partition Factor, Localizes to Nucleoid Poles via the Activities of Specific Nucleoid-Associated Proteins. Taniguchi S, Kasho K, Ozaki S, Katayama T. Front Microbiol 10 72 (2019)
  25. Asymmetric constriction of dividing Escherichia coli cells induced by expression of a fusion between two min proteins. Rowlett VW, Margolin W. J Bacteriol 196 2089-2100 (2014)
  26. Crystal Structure of TetR Family Repressor AlkX from Dietzia sp. Strain DQ12-45-1b Implicated in Biodegradation of n-Alkanes. Liang JL, Gao Y, He Z, Nie Y, Wang M, JiangYang JH, Zhang XC, Shu WS, Wu XL. Appl Environ Microbiol 83 e01447-17 (2017)
  27. Dynamics of the Bacillus subtilis Min System. Feddersen H, Würthner L, Frey E, Bramkamp M. mBio 12 e00296-21 (2021)
  28. The Nucleoid Occlusion Protein SlmA Binds to Lipid Membranes. Robles-Ramos MÁ, Margolin W, Sobrinos-Sanguino M, Alfonso C, Rivas G, Monterroso B, Zorrilla S. mBio 11 e02094-20 (2020)
  29. Intrinsic characteristics of Min proteins on the cell division of Helicobacter pylori. Nishida Y, Takeuchi H, Morimoto N, Umeda A, Kadota Y, Kira M, Okazaki A, Matsumura Y, Sugiura T. FEMS Microbiol Lett 363 fnw025 (2016)
  30. The DNA binding domain of the Vibrio vulnificus SmcR transcription factor is flexible and binds diverse DNA sequences. Newman JD, Russell MM, Fan L, Wang YX, Gonzalez-Gutierrez G, van Kessel JC. Nucleic Acids Res 49 5967-5984 (2021)
  31. A DNA-Binding Protein Tunes Septum Placement during Bacillus subtilis Sporulation. Brown EE, Miller AK, Krieger IV, Otto RM, Sacchettini JC, Herman JK. J Bacteriol 201 e00287-19 (2019)
  32. Efficient Multiscale Models of Polymer Assembly. Ruiz-Martinez A, Bartol TM, Sejnowski TJ, Tartakovsky DM. Biophys J 111 185-196 (2016)
  33. Bacterial division ring stabilizing ZapA versus destabilizing SlmA modulate FtsZ switching between biomolecular condensates and polymers. Monterroso B, Robles-Ramos MÁ, Sobrinos-Sanguino M, Luque-Ortega JR, Alfonso C, Margolin W, Rivas G, Zorrilla S. Open Biol 13 220324 (2023)
  34. In long bacterial cells, the Min system can act off-center. MacCready JS, Vecchiarelli AG. Mol Microbiol 109 268-272 (2018)
  35. Protein aggregates act as a deterministic disruptor during bacterial cell size homeostasis. Mortier J, Govers SK, Cambré A, Van Eyken R, Verheul J, den Blaauwen T, Aertsen A. Cell Mol Life Sci 80 360 (2023)
  36. Structures of the DarR transcription regulator reveal unique modes of second messenger and DNA binding. Schumacher MA, Lent N, Chen VB, Salinas R. Nat Commun 14 7239 (2023)