3D-SIM Super Resolution Microscopy Reveals a Bead-Like Arrangement for FtsZ and the Division Machinery: Implications for Triggering Cytokinesis

PLoS Biology

Volumn 10, Issue 9, 2012, Pages

  Strauss, Michael P ^a   Liew, Andrew T F ^a   Turnbull, Lynne ^a   Whitchurch, Cynthia B ^a   Monahan, Leigh G ^a   Harry, Elizabeth J ^a  

^a UNIVERSITY OF TECHNOLOGY SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; EZRA PROTEIN; FTSZ PROTEIN; PROTEIN PBP2; UNCLASSIFIED DRUG;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL CELL; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOKINESIS; MICROSCOPY; NONHUMAN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; STAPHYLOCOCCUS AUREUS; STRUCTURE ANALYSIS; THREE DIMENSIONAL STRUCTURED ILLUMINATION MICROSCOPY;

BACILLUS SUBTILIS; BACTERIAL PROTEINS; CYTOKINESIS; CYTOSKELETAL PROTEINS; GREEN FLUORESCENT PROTEINS; IMAGING, THREE-DIMENSIONAL; MICROBIAL VIABILITY; MICROSCOPY; MODELS, BIOLOGICAL; MOVEMENT; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; STAPHYLOCOCCUS AUREUS; TIME-LAPSE IMAGING;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); COCCOIDEA; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

EID: 84866719247     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001389     Document Type: Article

References (64)

1. Vaughan S, Wickstead B, Gull K, Addinall SG, (2004) Molecular Evolution of FtsZ Protein Sequences Encoded Within the Genomes of Archaea, Bacteria, and Eukaryota. J Mol Evol 58: 19-39.
2. Osteryoung KW, Vierling E, (1995) Conserved cell and organelle division. Nature 376: 473-474.
3. Nogales E, Downing KH, Amos LA, Löwe J, (1998) Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol 5: 451-458.
4. Gamba P, Veening JW, Saunders NJ, Hamoen LW, Daniel RA, (2009) Two-step assembly dynamics of the Bacillus subtilis divisome. J Bacteriol 191: 4186-4194.
5. Goehring NW, Gonzalez MD, Beckwith J, (2006) Premature targeting of cell division proteins to midcell reveals hierarchies of protein interactions involved in divisome assembly. Mol Microbiol 61: 33-45.
6. Erickson HP, Anderson DE, Osawa M, (2010) FtsZ in Bacterial Cytokinesis: Cytoskeleton and Force Generator All in One. Microbiol Mol Biol Rev 74: 504-528.
7. Osawa M, Anderson DE, Erickson HP, (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320: 792-794.
8. Lan G, Wolgemuth CW, Sun SX, (2007) Z-ring force and cell shape during divisionin rod-like bacteria. Proc Natl Acad Sci U S A 104: 16110-16115.
9. Erickson HP, (2009) Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci U S A 106: 9238-9243.
10. de Boer P, Crossley R, Rothfield L, (1992) The essential bacterial cell division protein FtsZ is a GTPase. Nature 359: 254-256.
11. Löwe J, Amos LA, (1998) Crystal structure of the bacterial cell-division protein FtsZ. Nature 391: 203-206.
12. Mukherjee A, Lutkenhaus J, (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176: 2754-2758.
13. Romberg L, Simon M, Erickson HP, (2001) Polymerization of FtsZ, a Bacterial Homolog of Tubulin. J Biol Chem 276: 11743-11753.
14. Löwe J, Amos LA, (2000) Helical Tubes of FtsZ from Methanococcus jannaschii. Bioll Chem 381: 993-939.
15. Erickson HP, Taylor DW, Taylor KA, Bramhill D, (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.
16. González JM, Jiménez M, Vélez M, Mingorance J, Andreu JM, et al. (2003) Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J Biol Chem 278: 37664-37671.
17. Bramhill D, Thompson CM, (1994) GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci U S A 91: 5813-5817.
18. Yu XC, Margolin W, (1997) Ca2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. EMBO J 16: 5455-5463.
19. Li Z, Trimble MJ, Brun YV, Jensen GJ, (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26: 4694-4708.
20. Li Z, Jensen GJ, (2009) Electron cryotomography: a new view into microbial ultrastructure. Curr Opin Microbiol 12: 333-340.
21. Mingorance J, Riva S, Vεlez M, Gomez-Puertas P, Vicente M, (2010) Strong FtsZ is with the force: mechanisms to constrict bacteria. Trends Microbiol 18: 348-356.
22. Ben-Yehuda S, Losick R, (2002) Asymmetric Cell Division in B. subtilis Involves a Spiral-like Intermediate of the Cytokinetic Protein FtsZ. Cell 109: 257-266.
23. Thanbichler M, Shapiro L, (2006) MipZ, a Spatial Regulator Coordinating Chromosome Segregation with Cell Division in Caulobacter. Cell 126: 147-162.
24. Thanedar S, Margolin W, (2004) FtsZ Exhibits Rapid Movement and Oscillation Waves in Helix-like Patterns in Escherichia coli. Curr Biol 14: 1167-1173.
25. Peters PC, Migocki MD, Thoni C, Harry EJ, (2007) A new assembly pathway for the cytokinetic Z ring from a dynamic helical structure in vegetatively growing cells of Bacillus subtilis. Mol Microbiol 64: 487-499.
26. 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. J Bacteriol 186: 5775-5781.
27. Stricker J, Maddox P, Salmon ED, Erickson HP, (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluoresence recovery after photobleaching. Proc Natl Acad Sci U S A 99: 3171-3175.
28. Schermelleh L, Heintzmann R, Leonhardt H, (2010) A guide to super-resolution fluorescence microscopy. J Cell Biol 190: 165-175.
29. Jennings PC, Cox GC, Monahan LG, Harry EJ, (2010) Super-resolution imaging of the bacterial cytokinetic protein FtsZ. Micron 42: 336-341.
30. Niu L, Yu J, (2008) Investigating Intracellular Dynamics of FtsZ Cytoskeleton with Photo-activation Single-molecule Tracking. Biophys J 95: 2009-2016.
31. Fu G, Huang T, Jackson B, 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: 1-16 doi: 10.1371/journal.pone.0012680.
32. Gustafsson MGL, Shao L, Carlton PM, Wang CJ, Golubovskaya IN, et al. (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94: 4957-4970.
33. Levin PA, Kurtser IG, Grossman AD, (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.
34. García-Lara J, Masalha M, Foster SJ, (2005) Staphylococcus aureus: the search for novel targets. Drug Discov Today 10: 643-651.
35. Pinho MG, Errington J, (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50: 871-881.
36. Singh P, Panda D, (2010) FtsZ inhibition: a promising approach for antistaphylococcal therapy. Drug News Perpect 23: 295-304.
37. Haydon DJ, Stokes NR, Ure R, Galbraith G, Bennett JM, et al. (2008) An inhibitor of FtsZ with potent and selective anti-staphylococcal activity. Science 321: 1673-1675.
38. Lock RL, Harry EJ, (2008) Cell-division inhibitors: new insights for future antibiotics. Mol Microbiol 7: 324-338.
39. Liew ATF, Theis T, Jensen SO, García-Lara J, Foster SJ, et al. (2011) A simple plasmid-based system that allows rapid generation of tightly controlled gene expression in Staphylococcus aureus. Microbiology 157: 666-676.
40. Pinho MG, Errington J, (2003) Dispersed mode of Staphylococcus aureus cell wall synthesis in the absence of the division machinery. Mol Microbiol 50: 871-881.
41. Harry E, Monahan L, Thompson L, Kwang WJ (2006) Bacterial Cell Division: The Mechanism and Its Precison. International Review of Cytology: Academic Press. pp 27-94.
42. Sievers J, Errington J, (2000) The Bacillus subtilis cell division protein FtsL localizes to sites of septation and interacts with DivIC. Mol Microbiol 36: 846-855.
43. Daniel RA, Errington J, (2001) Intrinsic instability of the essential cell division protein FtsL of Bacillus subtilis and a role for DivIB protein in FtsL turnover. Mol Microbiol 36: 278-289.
44. Daniel RA, Harry EJ, Errington J, (2000) Role of penicillin-binding protein PBP 2B in assembly and functioning of the division machinery of Bacillus subtilis. Mol Microbiol 35: 299-311.
45. Levin PA, Losick R, (1994) Characterization of a Cell Division Gene from Bacillus subtilis That Is Required for Vegetative and Sporulation Septum Formation. J Bacteriol 176: 1451-1459.
46. Haeusser DP, Schwartz RL, Smith AM, Oates ME, Levin PA, (2004) EzrA prevents aberrant cell division by modulating assembly of the cytoskeletal protein FtsZ. Mol Microbiol 52: 801.
47. Claessen D, Emmins R, Hamoen LW, Daniel RA, Errington J, et al. (2008) Control of the cell elongation-division cycle by shuttling of PBP1 protein in Bacillus subtilis. Mol Microbiol 64: 1029-1046.
48. Steele VR, Bottomley AL, García-Lara J, Kasturiarachchi J, Foster SJ, (2011) Multiple essential roles for EzrA in cell division of Staphylococcus aureus. Mol Microbiol 82: 542-555.
49. Jorge AM, Hoiczyk E, Gomes JP, Pinho MG, (2011) EzrA Contributes to the Regulation of Cell Size in Staphylococcus aureus. PLoS ONE 6.
50. Steele VR, Bottomley AL, Garcia-Lara J, Kasturiarachchi J, Foster SJ, (2011) Multiple essential roles for EzrA in cell division of Staphylococcus aureus. Mol Microbiol 80: 542-555.
51. Pinho MG, Errington J, (2005) Recruitment of penicillin-binding protein PBP2 to the division site of Staphylococcus aureus is dependent on its transpeptidation substrates. Mol Microbiol 55: 799-807.
52. Ma XL, Ehrhardt DW, Margolin W, (1996) Colocalization of cell division proteins FtsZ and FtsA to cytoskeletal structures in living Escherichia coli cells by using green fluorescent protein. Proc Natl Acad Sci U S A 93: 12998-13003.
53. Chen Y, Erickson HP, (2005) Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J Biol Chem 280: 22549-22554.
54. Osawa M, Erickson HP, (2011) Inside-out Z rings - constriction with and without GTP hydrolysis. Mol Microbiol 81: 571-579.
55. Daniel RA, Harry EJ, Katis VL, Wake GR, Errington J, (1998) Characterization of the essential cell division gene ftsL (yIID) of Bacillus subtilis and its role in the assembly of the division apparatus. Mol Microbiol 29: 593-604.
56. Hamoen LW, Meile JC, de Jong W, Noirot P, Errington J, (2006) SepF, a novel FtsZ-interacting protein required for a late step in cell division. Mol Microbiol 59: 989-999.
57. Kawai Y, Ogasawara N, (2006) Bacillus subtilis EzrA and FtsL synergistically regulate FtsZ ring dynamics during cell division. Microbiology 152: 1129-1141.
58. Novick RP, (1991) Genetic systems in staphylococci. Methods Ezymol 204: 587.
59. Reguera G, (2010) Bacillus. Cellular and molecular biology. Int Microbiol 10: 227.
60. Schermelleh L, Carlton PM, Haase S, Shao L, Winoto L, et al. (2008) Subdiffraction Multicolor Imaging of the Nuclear Periphery with 3D Structured Illumination Microscopy. Science 320: 1332-1336.
61. Carlton PM, Boulanger J, Kervrann C, Sibarita J-B, Salamero J, et al. (2010) Fast live simultaneous multiwavelength four-dimensional optical microscopy. Proc Natl Acad Sci U S A 107: 16016-16022.
62. Swedlow JR, Hu K, Andrews PD, Roos DS, Murray JM, (2002) Measuring tubulin content in Toxoplasma gondii: A comparison of laser-scanning confocal and wide-field fluorescence microscopy. Proc Natl Acad Sci U S A 99: 2014-2019.
63. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, et al. (2002) sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J Bacteriol 184: 5457-5467.
64. Cooper EL, García-Lara J, Foster SJ, (2009) YsxC, an essential protein in Staphylococcus aureus crucial for ribosome assembly/stability. BMC microbiology 9: 266.