A Multi-layered Protein Network Stabilizes the FtsZ-ring and Modulates Constriction Dynamics

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Bacterial cell division is a highly regulated process that must be coordinated with other cellular processes (i.e. DNA replication and chromosome segregation) to promote faithful reproduction. In Escherichia coli, this regulation is most often mediated through the polymerization of the prokaryotic tubulin homolog, FtsZ, which forms a ring-like structure (FtsZ-ring) at midcell. The establishment of the FtsZ-ring marks the site of division and enables the assembly of the macromolecular division machinery (divisome). Here we applied single-molecule based superresolution imaging to reveal the three-dimensional structure of FtsZ in the context of its regulatory proteins: ZapA, ZapB and MatP. We found that these four proteins exist in a multi-layered network that extends from the cell membrane to the chromosome. This layered organization not only helps to stabilize the FtsZ-ring, but also serves to coordinate division with DNA status by influencing constriction rate. Our results not only provide a comprehensive view of the divisome, but also allow new insight to be garnered regarding the structure and function of the divisome.

Vyšlo v časopise: A Multi-layered Protein Network Stabilizes the FtsZ-ring and Modulates Constriction Dynamics. PLoS Genet 11(4): e32767. doi:10.1371/journal.pgen.1005128
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005128

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Zdroje

1. Egan AJF, Vollmer W (2012) The physiology of bacterial cell division. Annals of the New York Academy of Sciences 1277 : 8–28. doi: 10.1111/j.1749-6632.2012.06818.x 23215820

2. Harry E, Monahan L, Thompson L (2006) Bacterial Cell Division: The Mechanism and Its Precison. International Review of Cytology. Elsevier, Vol. 253. pp. 27–94. doi: 10.1016/S0074-7696(06)53002-5

3. Bi EF, Lutkenhaus (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354 : 161–164. doi: 10.1038/354161a0 1944597

4. Addinall SG, Bi E, Lutkenhaus (1996) FtsZ ring formation in fts mutants. Journal of Bacteriology 178 : 3877–3884. 8682793

5. Osawa M, Anderson DE, Erickson HP (2009) Curved FtsZ protofilaments generate bending forces on liposome membranes. The EMBO Journal 28 : 3476–3484. doi: 10.1038/emboj.2009.277 19779463

6. Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of Contractile FtsZ Rings in Liposomes. Science 320 : 792–794. doi: 10.1126/science.1154520 18420899

7. Chen Y (2005) Rapid in Vitro Assembly Dynamics and Subunit Turnover of FtsZ Demonstrated by Fluorescence Resonance Energy Transfer. Journal of Biological Chemistry 280 : 22549–22554. doi: 10.1074/jbc.M500895200 15826938

8. Hale CA, de Boer PA (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. 9008158

9. Pichoff S, Lutkenhaus (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55 : 1722–1734. doi: 10.1111/j.1365-2958.2005.04522.x 15752196

10. Fu G, Huang T, Buss JA, Coltharp C, Hensel Z, et al. (2010) In Vivo Structure of the E. coli FtsZ-ring Revealed by Photoactivated Localization Microscopy (PALM). PLoS ONE 5: e12680. doi: 10.1371/journal.pone.0012680 20856929

11. Jennings PC, Cox G, Monahan LG, Harry E (2011) Super-resolution imaging of the bacterial cytokinetic protein FtsZ. Micron 42 : 336–341. doi: 10.1016/j.micron.2010.09.003 20933427

12. Biteen JS, Goley ED, Shapiro L, Moerner WE (2012) Three-Dimensional Super-Resolution Imaging of the Midplane Protein FtsZ in Live Caulobacter crescentusCells Using Astigmatism. ChemPhysChem 13 : 1007–1012. doi: 10.1002/cphc.201100686 22262316

13. Strauss MP, Liew ATF, Turnbull L, Whitchurch CB, Monahan LG, et al. (2012) 3D-SIM Super Resolution Microscopy Reveals a Bead-Like Arrangement for FtsZ and the Division Machinery: Implications for Triggering Cytokinesis. Plos Biol 10: e1001389. doi: 10.1371/journal.pbio.1001389 22984350

14. Buss JA, Coltharp C, Huang T, Pohlmeyer C, Wang S-C, et al. (2013) In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy. Mol Microbiol 89 : 1099–1120. doi: 10.1111/mmi.12331 23859153

15. Holden SJ, Pengo T, Meibom KL, Fernandez Fernandez C, Collier J, et al. (2014) High throughput 3D super-resolution microscopy reveals Caulobacter crescentus in vivo Z-ring organization. Proc Natl Acad Sci USA 111 : 4566–4571. doi: 10.1073/pnas.1313368111 24616530

16. Stricker J, Maddox P, Salmon ED, Erickson HP (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proceedings of the National Academy of Sciences 99 : 3171–3175. doi: 10.1073/pnas.052595099 11854462

17. Anderson DE, Gueiros-Filho FJ, Erickson HP (2004) Assembly Dynamics of FtsZ Rings in Bacillus subtilis and Escherichia coli and Effects of FtsZ-Regulating Proteins. Journal of Bacteriology 186 : 5775–5781. doi: 10.1128/JB.186.17.5775-5781.2004 15317782

18. Gueiros-Filho FJ (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes & Development 16 : 2544–2556. doi: 10.1101/gad.1014102

19. Ebersbach G, Galli E, Møller-Jensen J, Löwe J, Gerdes K (2008) Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol Microbiol 68 : 720–735. doi: 10.1111/j.1365-2958.2008.06190.x 18394147

20. Durand-Heredia J, Yu HH, De Carlo S, Lesser CF, Janakiraman A (2011) Identification and Characterization of ZapC, a Stabilizer of the FtsZ Ring in Escherichia coli. Journal of Bacteriology 193 : 1405–1413. doi: 10.1128/JB.01258-10 21216995

21. Hale CA, Shiomi D, Liu B, Bernhardt T, Margolin W, et al. (2011) Identification of Escherichia coli ZapC (YcbW) as a Component of the Division Apparatus That Binds and Bundles FtsZ Polymers. Journal of Bacteriology 193 : 1393–1404. doi: 10.1128/JB.01245-10 21216997

22. Durand-Heredia J, Rivkin E, Fan G, Morales J, Janakiraman A (2012) Identification of ZapD as a Cell Division Factor That Promotes the Assembly of FtsZ in Escherichia coli. Journal of Bacteriology 194 : 3189–3198. doi: 10.1128/JB.00176-12 22505682

23. Marteyn BS, Karimova G, Fenton AK, Gazi AD, West N, et al. (2014) ZapE is a novel cell division protein interacting with FtsZ and modulating the Z-ring dynamics. mBio 5: e00022–14. doi: 10.1128/mBio.00022-14 24595368

24. Small E, Marrington R, Rodger A, Scott DJ, Sloan K, et al. (2007) FtsZ Polymer-bundling by the Escherichia coli ZapA Orthologue, YgfE, Involves a Conformational Change in Bound GTP. Journal of Molecular Biology 369 : 210–221. doi: 10.1016/j.jmb.2007.03.025 17428494

25. Dajkovic A, Pichoff S, Lutkenhaus, Wirtz D (2010) Cross-linking FtsZ polymers into coherent Z rings. Mol Microbiol 78 : 651–668. doi: 10.1111/j.1365-2958.2010.07352.x 20969647

26. Galli E, Gerdes K (2010) Spatial resolution of two bacterial cell division proteins: ZapA recruits ZapB to the inner face of the Z-ring. Mol Microbiol 76 : 1514–1526. doi: 10.1111/j.1365-2958.2010.07183.x 20487275

27. Galli E, Gerdes K (2011) FtsZ-ZapA-ZapB Interactome of Escherichia coli. Journal of Bacteriology 194 : 292–302. doi: 10.1128/JB.05821-11 22056926

28. Mercier R, Petit M-A, Schbath S, Robin S, Karoui El M, et al. (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135 : 475–485. doi: 10.1016/j.cell.2008.08.031 18984159

29. Espeli O, Borne R, Dupaigne P, Thiel A, Gigant E, et al. (2012) A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. The EMBO Journal 31 : 3198–3211. doi: 10.1038/emboj.2012.128 22580828

30. Bailey MW, Bisicchia P, Warren BT, Sherratt DJ, Männik J (2014) Evidence for divisome localization mechanisms independent of the Min system and SlmA in Escherichia coli. PLoS Genet 10: e1004504. doi: 10.1371/journal.pgen.1004504 25101671

31. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, et al. (2006) Imaging Intracellular Fluorescent Proteins at Nanometer Resolution. Science 313 : 1642–1645. doi: 10.1126/science.1127344 16902090

32. Coltharp C, Kessler RP, Xiao J (2012) Accurate Construction of Photoactivated Localization Microscopy (PALM) Images for Quantitative Measurements. PLoS ONE 7: e51725. doi: 10.1371/journal.pone.0051725 23251611

33. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nature Methods 3 : 793–796. doi: 10.1038/nmeth929 16896339

34. Veatch SL, Machta BB, Shelby SA, Chiang EN, Holowka DA, et al. (2012) Correlation Functions Quantify Super-Resolution Images and Estimate Apparent Clustering Due to Over-Counting. PLoS ONE 7: e31457. doi: 10.1371/journal.pone.0031457 22384026

35. Sengupta P, Jovanovic-Talisman T, Lippincott-Schwartz J (2013) Quantifying spatial organization in point-localization superresolution images using pair correlation analysis. Nat Protoc 8 : 345–354. doi: 10.1038/nprot.2013.005 23348362

36. Coltharp C, Yang X, Xiao J (2014) Quantitative analysis of single-molecule superresolution images. Curr Opin Struct Biol 28C: 112–121. doi: 10.1016/j.sbi.2014.08.008

37. Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM, et al. (2009) Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proceedings of the National Academy of Sciences 106 : 3125–3130. doi: 10.1073/pnas.0813131106 19202073

38. Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, et al. (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468 : 580–584. doi: 10.1038/nature09621 21107430

39. Matias VRF, Beveridge TJ (2005) Cryo-electron microscopy reveals native polymeric cell wall structure in Bacillus subtilis 168 and the existence of a periplasmic space. Mol Microbiol 56 : 240–251. doi: 10.1111/j.1365-2958.2005.04535.x 15773993

40. Sleytr UB, Schuster B, Egelseer E-M, Pum D (2014) S-layers: principles and applications. FEMS Microbiology Reviews 38 : 823–864. doi: 10.1111/1574-6976.12063 24483139

41. Zhang M, Chang H, Zhang Y, Yu J, Wu L, et al. (2012) Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nature Methods: 1–6. doi: 10.1038/nmeth.2021 22312634

42. Bernhardt T, de Boer PA (2005) SlmA, a Nucleoid-Associated, FtsZ Binding Protein Required for Blocking Septal Ring Assembly over Chromosomes in. Molecular Cell 18 : 555–564. doi: 10.1016/j.molcel.2005.04.012 15916962

43. Dupaigne P, Tonthat NK, Espeli O, Whitfill T, Boccard FEDER, et al. (2012) Molecular Basis for a Protein-Mediated DNA-Bridging Mechanism that Functions in Condensation of the E. coli Chromosome. Molecular Cell 48 : 560–571. doi: 10.1016/j.molcel.2012.09.009 23084832

44. Geissler B, Shiomi D, Margolin W (2007) The ftsA* gain-of-function allele of Escherichia coli and its effects on the stability and dynamics of the Z ring. Microbiology 153 : 814–825. doi: 10.1099/mic.0.2006/001834-0 17322202

45. Erickson HP, Anderson DE, Osawa M (2010) FtsZ in Bacterial Cytokinesis: Cytoskeleton and Force Generator All in One. Microbiology and Molecular Biology Reviews 74 : 504–528. doi: 10.1128/MMBR.00021-10 21119015

46. Weiss DS (2004) Bacterial cell division and the septal ring. Mol Microbiol 54 : 588–597. doi: 10.1111/j.1365-2958.2004.04283.x 15491352

47. Rowlett VW, Margolin W (2014) 3D-SIM super-resolution of FtsZ and its membrane tethers in Escherichia coli cells. Biophysical Journal 107: L17–L20. doi: 10.1016/j.bpj.2014.08.024 25418183

48. Popp D, Iwasa M, Narita A, Erickson HP, Maéda Y (2009) FtsZ condensates: An in vitro electron microscopy study. Biopolymers 91 : 340–350. doi: 10.1002/bip.21136 19137575

49. Low HH, Moncrieffe MC, Löwe J (2004) The Crystal Structure of ZapA and its Modulation of FtsZ Polymerisation. Journal of Molecular Biology 341 : 839–852. doi: 10.1016/j.jmb.2004.05.031 15288790

50. Maggi S, Massidda O, Luzi G, Fadda D, Paolozzi L, et al. (2008) Division protein interaction web: identification of a phylogenetically conserved common interactome between Streptococcus pneumoniae and Escherichia coli. Microbiology 154 : 3042–3052. doi: 10.1099/mic.0.2008/018697-0 18832310

51. Alexeeva S, Gadella TWJ Jr, Verheul J, Verhoeven GS, Blaauwen den T (2010) Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol Microbiol 77 : 384–398. doi: 10.1111/j.1365-2958.2010.07211.x 20497333

52. Pazos M, Natale P, Margolin W, Vicente M (2013) Interactions among the early Escherichia coli divisome proteins revealed by bimolecular fluorescence complementation. Environ Microbiol 15 : 3282–3291. doi: 10.1111/1462-2920.12225 23957637

53. Monahan LG, Liew ATF, Bottomley AL, Harry E (2014) Division site positioning in bacteria: one size does not fit all. Front Microbio 5 : 19. doi: 10.3389/fmicb.2014.00019

54. de Boer PA, Crossley RE, Rothfield LI (1989) A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56 : 641–649. 2645057

55. Cho H, McManus HR, Dove SL, Bernhardt T (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci USA 108 : 3773–3778. doi: 10.1073/pnas.1018674108 21321206

56. Grenga L, Luzi G, Paolozzi L, Ghelardini P (2008) The Escherichia coli FtsK functional domains involved in its interaction with its divisome protein partners. FEMS Microbiology Letters 287 : 163–167. doi: 10.1111/j.1574-6968.2008.01317.x 18759781

57. Stouf M, Meile J-C, Cornet F (2013) FtsK actively segregates sister chromosomes in Escherichia coli. Proc Natl Acad Sci USA 110 : 11157–11162. doi: 10.1073/pnas.1304080110 23781109

58. Dai K, Lutkenhaus (1992) The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. Journal of Bacteriology 174 : 6145–6151. 1400163

59. Buss JA, Coltharp C, Xiao J (2013) Super-resolution Imaging of the Bacterial Division Machinery. JoVE. doi: 10.3791/50048

60. Huang B, Wang W, Bates M, Zhuang X (2008) Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319 : 810–813. doi: 10.1126/science.1153529 18174397

61. Hensel Z, Weng X, Lagda AC, Xiao J (2013) Transcription-Factor-Mediated DNA Looping Probed by High-Resolution, Single-Molecule Imaging in Live E. coli Cells. Plos Biol 11: e1001591. doi: 10.1371/journal.pbio.1001591 23853547

62. Churchman LS, Spudich JA (2012) Colocalization of Fluorescent Probes: Accurate and Precise Registration with Nanometer Resolution. Cold Spring Harbor Protocols 2012: pdb.top067918–pdb.top067918. doi: 10.1101/pdb.top067918 22301660

63. Mohammadi T, Ploeger GEJ, Verheul J, Comvalius AD, Martos A, et al. (2009) The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro. Biochemistry 48 : 11056–11066. doi: 10.1021/bi901461p 19842714

64. Kitagawa M, Ara T, Arifuzzaman M, Ioka-Nakamichi T, Inamoto E, et al. (2006) Complete set of ORF clones of Escherichia coli ASKA library (A Complete Set of E. coli K-12 ORF Archive): Unique Resources for Biological Research. DNA Research 12 : 291–299. doi: 10.1093/dnares/dsi012

65. Reshes G, Vanounou S, Fishov I, Feingold M (2008) Timing the start of division in E. coli: a single-cell study. Phys Biol 5 : 046001. doi: 10.1088/1478-3975/5/4/046001 18997273

66. Li Y, Hsin J, Zhao L, Cheng Y, Shang W, et al. (2013) FtsZ Protofilaments Use a Hinge-Opening Mechanism for Constrictive Force Generation. Science 341 : 392–395. doi: 10.1126/science.1239248 23888039