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Cited by 15Bacterial Genetics and BiotechnologyBiochemical and Structural CharacterizationProtein Structure and Dynamics

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The coiled-coil domain of Escherichia coli FtsLB is a structurally detuned element critical for modulating its activation in bacterial cell division

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Craven, Samuel J., Condon, Samson G.F., Díaz Vázquez, Gladys, Cui, Qiang, Senes, Alessandro·2022·Journal of Biological Chemistry
DOI 10.1016/j.jbc.2021.101460PMC PMC8749076

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Abstract

The FtsLB complex is a key regulator of bacterial cell division, existing in either an off state or an on state, which supports the activation of septal peptidoglycan synthesis. In Escherichia coli, residues known to be critical for this activation are located in a region near the C-terminal end of the periplasmic coiled-coil domain of FtsLB, raising questions about the precise role of this conserved domain in the activation mechanism. Here, we investigate an unusual cluster of polar amino acids found within the core of the FtsLB coiled coil. We hypothesized that these amino acids likely reduce the structural stability of the domain and thus may be important for governing conformational changes. We found that mutating these positions to hydrophobic residues increased the thermal stability of FtsLB but caused cell division defects, suggesting that the coiled-coil domain is a "detuned" structural element. In addition, we identified suppressor mutations within the polar cluster, indicating that the precise identity of the polar amino acids is important for fine-tuning the structural balance between the off and on states. We propose a revised structural model of the tetrameric FtsLB (named the "Y-model") in which the periplasmic domain splits into a pair of coiled-coil branches. In this configuration, the hydrophilic terminal moieties of the polar amino acids remain more favorably exposed to water than in the original four-helix bundle model ("I-model"). We propose that a shift in this architecture, dependent on its marginal stability, is involved in activating the FtsLB complex and triggering septal cell wall reconstruction.

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Research works printed but not linked: 70

  1. Du, 2017, Assembly and activation of the Escherichia coli divisome, Mol. Microbiol., 105, 177, 10.1111/mmi.13696 · DOI
  2. den Blaauwen, 2017, The divisome at 25: The road ahead, Curr. Opin. Microbiol., 36, 85, 10.1016/j.mib.2017.01.007 · DOI
  3. Egan, 2020, Regulation of peptidoglycan synthesis and remodelling, Nat. Rev. Microbiol., 18, 446, 10.1038/s41579-020-0366-3 · DOI · Paper page
  4. Egan, 2013, The physiology of bacterial cell division, Ann. N. Y. Acad. Sci., 1277, 8, 10.1111/j.1749-6632.2012.06818.x · DOI
  5. Booth, 2019, Structural basis for the coordination of cell division with the synthesis of the bacterial cell envelope, Protein Sci. Publ. Protein Soc., 28, 2042, 10.1002/pro.3722 · DOI
  6. Mercer, 2002, The Escherichia coli cell division protein FtsW is required to recruit its cognate transpeptidase, FtsI (PBP3), to the division site, J. Bacteriol., 184, 904, 10.1128/jb.184.4.904-912.2002 · DOI
  7. Fraipont, 2011, The integral membrane FtsW protein and peptidoglycan synthase PBP3 form a subcomplex in Escherichia coli, Microbiol. Read. Engl., 157, 251, 10.1099/mic.0.040071-0 · DOI
  8. Cho, 2016, Bacterial cell wall biogenesis is mediated by SEDS and PBP polymerase families functioning semi-autonomously, Nat. Microbiol., 1, 16172, 10.1038/nmicrobiol.2016.172 · DOI
  9. Meeske, 2016, SEDS proteins are a widespread family of bacterial cell wall polymerases, Nature, 537, 634, 10.1038/nature19331 · DOI
  10. Taguchi, 2019, FtsW is a peptidoglycan polymerase that is functional only in complex with its cognate penicillin-binding protein, Nat. Microbiol., 4, 587, 10.1038/s41564-018-0345-x · DOI
  11. Mohammadi, 2011, Identification of FtsW as a transporter of lipid-linked cell wall precursors across the membrane, EMBO J., 30, 1425, 10.1038/emboj.2011.61 · DOI
  12. Mohammadi, 2014, Specificity of the transport of lipid II by FtsW in Escherichia coli, J. Biol. Chem., 289, 14707, 10.1074/jbc.M114.557371 · DOI
  13. Leclercq, 2017, Interplay between Penicillin-binding proteins and SEDS proteins promotes bacterial cell wall synthesis, Sci. Rep., 7, 43306, 10.1038/srep43306 · DOI
  14. Botta, 1981, Evidence for involvement of penicillin-binding protein 3 in murein synthesis during septation but not during cell elongation, J. Bacteriol., 145, 333, 10.1128/jb.145.1.333-340.1981 · DOI
  15. Nakagawà, 1979, Purified penicillin binding proteins 1Bs from Escherichia coli membrane showing activities of both peptidoglycan polymerase and peptidoglycan crosslinking enzyme, Agric. Biol. Chem., 43, 1379
  16. Yang, 2021, A two-track model for the spatiotemporal coordination of bacterial septal cell wall synthesis revealed by single-molecule imaging of FtsW, Nat. Microbiol., 6, 584, 10.1038/s41564-020-00853-0 · DOI
  17. McCausland, 2021, Treadmilling FtsZ polymers drive the directional movement of sPG-synthesis enzymes via a Brownian ratchet mechanism, Nat. Commun., 12, 609, 10.1038/s41467-020-20873-y · DOI
  18. Gerding, 2009, Self-enhanced accumulation of FtsN at division sites and roles for other proteins with a SPOR domain (DamX, DedD, and RlpA) in Escherichia coli cell constriction, J. Bacteriol., 191, 7383, 10.1128/JB.00811-09 · DOI
  19. Ursinus, 2004, Murein (peptidoglycan) binding property of the essential cell division protein FtsN from Escherichia coli, J. Bacteriol., 186, 6728, 10.1128/JB.186.20.6728-6737.2004 · DOI
  20. Yang, 2004, Solution structure and domain architecture of the divisome protein FtsN, Mol. Microbiol., 52, 651, 10.1111/j.1365-2958.2004.03991.x · DOI
  21. Liu, 2015, Roles for both FtsA and the FtsBLQ subcomplex in FtsN-stimulated cell constriction in Escherichia coli, Mol. Microbiol., 95, 945, 10.1111/mmi.12906 · DOI
  22. Pichoff, 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, 10.1111/mmi.12907 · DOI
  23. Park, 2021, FtsA acts through FtsW to promote cell wall synthesis during cell division in Escherichia coli, Proc. Natl. Acad. Sci. U. S. A., 118, 10.1073/pnas.2107210118 · DOI
  24. Tsang, 2015, A role for the FtsQLB complex in cytokinetic ring activation revealed by an ftsL allele that accelerates division, Mol. Microbiol., 95, 925, 10.1111/mmi.12905 · DOI
  25. Marmont, 2020, A conserved subcomplex within the bacterial cytokinetic ring activates cell wall synthesis by the FtsW-FtsI synthase, Proc. Natl. Acad. Sci., 117, 23879, 10.1073/pnas.2004598117 · DOI
  26. Park, 2020, Essential role for FtsL in activation of septal peptidoglycan synthesis, mBio, 11, e03012, 10.1128/mBio.03012-20 · DOI
  27. Li, 2021, Genetic analysis of the septal peptidoglycan synthase FtsWI complex supports a conserved activation mechanism for SEDS-bPBP complexes, PLoS Genet., 17, e1009366, 10.1371/journal.pgen.1009366 · DOI
  28. Khadria, 2013, The transmembrane domains of the bacterial cell division proteins FtsB and FtsL form a stable high-order oligomer, Biochemistry, 52, 7542, 10.1021/bi4009837 · DOI
  29. Condon, 2018, The FtsLB subcomplex of the bacterial divisome is a tetramer with an uninterrupted FtsL helix linking the transmembrane and periplasmic regions, J. Biol. Chem., 293, 1623, 10.1074/jbc.RA117.000426 · DOI
  30. Gonzalez, 2010, Multiple interaction domains in FtsL, a protein component of the widely conserved bacterial FtsLBQ cell division complex, J. Bacteriol., 192, 2757, 10.1128/JB.01609-09 · DOI
  31. Ghigo, 1999, Localization of FtsL to the Escherichia coli septal ring, Mol. Microbiol., 31, 725, 10.1046/j.1365-2958.1999.01213.x · DOI
  32. Ghigo, 2000, Cell division in Escherichia coli: Role of FtsL domains in septal localization, function, and oligomerization, J. Bacteriol., 182, 116, 10.1128/JB.182.1.116-129.2000 · DOI
  33. Goehring, 2006, Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly, Mol. Microbiol., 61, 33, 10.1111/j.1365-2958.2006.05206.x · DOI
  34. Choi, 2018, Structural insights into the FtsQ/FtsB/FtsL complex, a key component of the divisome, Sci. Rep., 8, 18061, 10.1038/s41598-018-36001-2 · DOI
  35. Kureisaite-Ciziene, 2018, Structural analysis of the interaction between the bacterial cell division proteins FtsQ and FtsB, mBio, 9, 10.1128/mBio.01346-18 · DOI
  36. LaPointe, 2013, Structural organization of FtsB, a transmembrane protein of the bacterial divisome, Biochemistry, 52, 2574, 10.1021/bi400222r · DOI
  37. Villanelo, 2011, A model for the Escherichia coli FtsB/FtsL/FtsQ cell division complex, BMC Struct. Biol., 11, 28, 10.1186/1472-6807-11-28 · DOI
  38. Buddelmeijer, 2004, A complex of the Escherichia coli cell division proteins FtsL, FtsB and FtsQ forms independently of its localization to the septal region, Mol. Microbiol., 52, 1315, 10.1111/j.1365-2958.2004.04044.x · DOI
  39. Masson, 2009, Central domain of DivIB caps the C-terminal regions of the FtsL/DivIC coiled-coil rod, J. Biol. Chem., 284, 27687, 10.1074/jbc.M109.019471 · DOI
  40. Gonzalez, 1996, Buried polar residues and structural specificity in the GCN4 leucine zipper, Nat. Struct. Biol., 3, 1011, 10.1038/nsb1296-1011 · DOI
  41. Wagschal, 1999, The role of position a in determining the stability and oligomerization state of alpha-helical coiled coils: 20 amino acid stability coefficients in the hydrophobic core of proteins, Protein Sci. Publ. Protein Soc., 8, 2312, 10.1110/ps.8.11.2312 · DOI
  42. Testa, 2009, CC+: A relational database of coiled-coil structures, Nucleic Acids Res., 37, D315, 10.1093/nar/gkn675 · DOI
  43. Glas, 2015, The soluble periplasmic domains of Escherichia coli cell division proteins FtsQ/FtsB/FtsL form a trimeric complex with submicromolar affinity, J. Biol. Chem., 290, 21498, 10.1074/jbc.M115.654756 · DOI
  44. Gonzalez, 2009, Divisome under construction: Distinct domains of the small membrane protein FtsB are necessary for interaction with multiple cell division proteins, J. Bacteriol., 191, 2815, 10.1128/JB.01597-08 · DOI
  45. Schmidt, 2017, The accommodation index measures the perturbation associated with insertions and deletions in coiled-coils: Application to understand signaling in histidine kinases, Protein Sci. Publ. Protein Soc., 26, 414, 10.1002/pro.3095 · DOI
  46. Bhate, 2018, Structure and function of the transmembrane domain of NsaS, an antibiotic sensing histidine kinase in Staphylococcus aureus, J. Am. Chem. Soc., 140, 7471, 10.1021/jacs.7b09670 · DOI
  47. Albanesi, 2009, Structural plasticity and catalysis regulation of a thermosensor histidine kinase, Proc. Natl. Acad. Sci. U. S. A., 106, 16185, 10.1073/pnas.0906699106 · DOI
  48. Fernández, 2019, Transmembrane Prolines mediate signal sensing and Decoding in Bacillus subtilis DesK histidine kinase, mBio, 10, 10.1128/mBio.02564-19 · DOI
  49. Lesne, 2016, Balance between coiled-coil stability and dynamics regulates activity of BvgS sensor kinase in Bordetella, mBio, 7, e02089, 10.1128/mBio.02089-15 · DOI
  50. Buddelmeijer, 2002, YgbQ, a cell division protein in Escherichia coli and Vibrio cholerae, localizes in codependent fashion with FtsL to the division site, Proc. Natl. Acad. Sci. U. S. A., 99, 6316, 10.1073/pnas.092128499 · DOI
  51. Paintdakhi, 2016, Oufti: An integrated software package for high-accuracy, high-throughput quantitative microscopy analysis, Mol. Microbiol., 99, 767, 10.1111/mmi.13264 · DOI
  52. Efron, 1979, Bootstrap methods: Another look at the Jackknife, Ann. Stat., 7, 1, 10.1214/aos/1176344552 · DOI · Paper page
  53. Studier, 2005, Protein production by auto-induction in high density shaking cultures, Protein Expr. Purif., 41, 207, 10.1016/j.pep.2005.01.016 · DOI
  54. Boratyn, 2012, Domain enhanced lookup time accelerated BLAST, Biol. Direct, 7, 12, 10.1186/1745-6150-7-12 · DOI
  55. O’Leary, 2016, Reference sequence (RefSeq) database at NCBI: Current status, taxonomic expansion, and functional annotation, Nucleic Acids Res., 44, D733, 10.1093/nar/gkv1189 · DOI · Paper page
  56. Federhen, 2012, The NCBI taxonomy database, Nucleic Acids Res., 40, D136, 10.1093/nar/gkr1178 · DOI · Paper page
  57. Katoh, 2013, MAFFT multiple sequence alignment software version 7: Improvements in performance and usability, Mol. Biol. Evol., 30, 772, 10.1093/molbev/mst010 · DOI · Paper page
  58. Wickham, 2019, Welcome to the tidyverse, J. Open Source Soft, 4, 1686, 10.21105/joss.01686 · DOI · Paper page
  59. Zeileis, 2005, Zoo: S3 infrastructure for regular and irregular time series, J. Stat. Softw., 14, 1
  60. Chamberlain, 2013, taxize - taxonomic search and retrieval in R, F1000Research, 2, 191
  61. Winter, 2017, rentrez: an R package for the NCBI eUtils API, R. J., 9, 520
  62. Grigoryan, 2011, Probing designability via a generalized model of helical bundle geometry, J. Mol. Biol., 405, 1079, 10.1016/j.jmb.2010.08.058 · DOI
  63. Brooks, 1983, Charmm: A program for macromolecular energy, minimization, and dynamics calculations, J. Comput. Chem., 4, 187, 10.1002/jcc.540040211 · DOI
  64. Mirdita, 2021, ColabFold - Making protein folding accessible to all, Bioinformatics
  65. Steinegger, 2017, MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets, Nat. Biotechnol., 35, 1026, 10.1038/nbt.3988 · DOI · Paper page
  66. Huang, 2017, CHARMM36m: An improved force field for folded and intrinsically disordered proteins, Nat. Methods, 14, 71, 10.1038/nmeth.4067 · DOI
  67. Klauda, 2010, Update of the CHARMM all-atom additive force field for lipids: Validation on six lipid types, J. Phys. Chem. B, 114, 7830, 10.1021/jp101759q · DOI
  68. Phillips, 2005, Scalable molecular dynamics with NAMD, J. Comput. Chem., 26, 1781, 10.1002/jcc.20289 · DOI · Paper page
  69. Jo, 2008, CHARMM-GUI: A web-based graphical user interface for CHARMM, J. Comput. Chem., 29, 1859, 10.1002/jcc.20945 · DOI · Paper page
  70. Humphrey, 1996, Vmd: Visual molecular dynamics, J. Mol. Graph., 14, 27, 10.1016/0263-7855(96)00018-5 · DOI · Paper page

Metadata

Authors
Craven, S. J., Condon, S. G. F., Díaz Vázquez, G., Cui, Q., & Senes, A.
Affiliations
  • University of Wisconsin–Madison (US)
  • Boston University (US)
Corresponding author
Senes, Alessandro
ORCID
Venue
Journal of Biological Chemistry
Publisher
Elsevier BV
Published
2022-01
Volume
298
Issue
1
Pages
101460
ISSN
0021-9258 (ISSN-L)
DOI
10.1016/j.jbc.2021.101460
PMC
PMC8749076
OpenAlex
W4206137854
Cited by
15
References
3
Citations by year
2026: 1 · 2024: 4 · 2023: 4 · 2022: 6
FWCI
1.98
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Biological Chemistry (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • National Science Foundation (1829555)
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM099752, R35GM130339)
  • Division of Chemistry (CHE-1829555)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Keywords
coiled-coil domain, bacterial cell division, polar amino acids, protein thermal stability, protein conformational change, septal peptidoglycan synthesis, suppressor mutations, tetrameric protein structure, Escherichia coli
MeSH terms
Amino Acid Sequence, Amino Acids, Cell Division, Escherichia coli, Membrane Proteins, Models, Molecular, Cell Cycle Proteins, Escherichia coli Proteins

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