In vivo organization of the FtsZ-ring by ZapA and ZapB revealed by quantitative super-resolution microscopy

Molecular Microbiology

Volumn 89, Issue 6, 2013, Pages 1099-1120

  Buss, Jackson ^a   Coltharp, Carla ^a   Huang, Tao ^b   Pohlmeyer, Chris ^a   Wang, Shih Chin ^a   Hatem, Christine ^a   Xiao, Jie ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Oregon Health and Science University Department of Biomedical Engineering   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FTSZ PROTEIN; MATP PROTEIN; UNCLASSIFIED DRUG; ZAPA PROTEIN; ZAPB PROTEIN;

ARTICLE; BACTERIAL CELL; CELL COMPONENT; CELL DIVISION; CELL LENGTH; CELLULAR DISTRIBUTION; CELLULAR PARAMETERS; CONTROLLED STUDY; DEPOLYMERIZATION; ESCHERICHIA COLI; GENE DELETION; IN VIVO STUDY; MICROSCOPY; MOLECULAR DYNAMICS; NONHUMAN; PHOTOACTIVATED LOCALIZATION MICROSCOPY; PRIORITY JOURNAL; PROTEIN CLUSTER; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTOFILAMENT; QUANTITATIVE ANALYSIS; RING LIKE STRUCTURE; STRUCTURE ANALYSIS; WILD TYPE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

BACTERIAL PROTEINS; CARRIER PROTEINS; CELL CYCLE PROTEINS; CYTOSKELETAL PROTEINS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE DELETION; MACROMOLECULAR SUBSTANCES; MICROSCOPY; PROTEIN MULTIMERIZATION;

EID: 84884282214     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/mmi.12331     Document Type: Article

References (98)

1. Aarsman, M.E., Piette, A., Fraipont, C., Vinkenvleugel, T.M., Nguyen-Disteche, M., and den Blaauwen, T. (2005) Maturation of the Escherichia coli divisome occurs in two steps. Mol Microbiol 55: 1631-1645.
2. Adams, D.W., and Errington, J. (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7: 642-653.
3. Addinall, S.G., and Lutkenhaus, J. (1996) FtsZ-spirals and -arcs determine the shape of the invaginating septa in some mutants of Escherichia coli. Mol Microbiol 22: 231-237.
4. Addinall, S.G., Bi, E., and Lutkenhaus, J. (1996) FtsZ ring formation in fts mutants. J Bacteriol 178: 3877-3884.
5. Addinall, S.G., Cao, C., and Lutkenhaus, J. (1997) Temperature shift experiments with an ftsZ84(Ts) strain reveal rapid dynamics of FtsZ localization and indicate that the Z ring is required throughout septation and cannot reoccupy division sites once constriction has initiated. J Bacteriol 179: 4277-4284.
6. Alexeeva, S., Gadella, T.W.J., Verheul, J., Verhoeven, G.S., and Den Blaauwen, T. (2010) Direct interactions of early and late assembling division proteins in Escherichia coli cells resolved by FRET. Mol Microbiol 77: 384-398.
7. Anderson, D.E., Gueiros-Filho, F.J., and Erickson, H.P. (2004) Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J Bacteriol 186: 5775-5781.
8. Ando, R., Mizuno, H., and Miyawaki, A. (2004) Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306: 1370-1373.
9. Annibale, P., Vanni, S., Scarselli, M., Rothlisberger, U., and Radenovic, A. (2011) Identification of clustering artifacts in photoactivated localization microscopy. Nat Methods 8: 527-528.
10. Baba, T., Ara, T., Hasegawa, M., Takai, Y., Okumura, Y., Baba, M., etal. (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2: 2006.0008.
11. Bernhardt, T.G., and de Boer, P.A. (2005) SlmA, a nucleoid-associated, FtsZ binding protein required for blocking septal ring assembly over chromosomes in E. coli. Mol Cell 18: 555-564.
12. Betzig, E., Patterson, G.H., Sougrat, R., Lindwasser, O.W., Olenych, S., Bonifacino, J.S., etal. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642-1645.
13. Bi, E., and Lutkenhaus, J. (1992) Isolation and characterization of ftsZ alleles that affect septal morphology. J Bacteriol 174: 5414-5423.
14. Bi, E.F., and Lutkenhaus, J. (1991) FtsZ ring structure associated with division in Escherichia coli. Nature 354: 161-164.
15. Biteen, J.S., Goley, E.D., Shapiro, L., and Moerner, W.E. (2012) Three-dimensional super-resolution imaging of the midplane protein FtsZ in live Caulobacter crescentus cells using astigmatism. Chemphyschem 13: 1007-1012.
16. Bramhill, D., and Thompson, C.M. (1994) GTP-dependent polymerization of Escherichia coli FtsZ protein to form tubules. Proc Natl Acad Sci USA 91: 5813-5817.
17. Buddelmeijer, N., and Beckwith, J. (2002) Assembly of cell division proteins at the E. coli cell center. Curr Opin Microbiol 5: 553-557.
18. Buss, J., Coltharp, C., and Xiao, J. (2013) Super-resolution imaging of the bacterial division machinery. J Vis Exp (71): e50048. doi:10.3791/50048
19. Caplan, M.R., and Erickson, H.P. (2003) Apparent cooperative assembly of the bacterial cell division protein FtsZ demonstrated by isothermal titration calorimetry. J Biol Chem 278: 13784-13788.
20. Chen, Y., and Erickson, H.P. (2005) Rapid in vitro assembly dynamics and subunit turnover of FtsZ demonstrated by fluorescence resonance energy transfer. J Biol Chem 280: 22549-22554.
21. Chen, Y., Bjornson, K., Redick, S.D., and Erickson, H.P. (2005) A rapid fluorescence assay for FtsZ assembly indicates cooperative assembly with a dimer nucleus. Biophys J 88: 505-514.
22. Chen, Y., Milam, S.L., and Erickson, H.P. (2012) SulA inhibits assembly of FtsZ by a simple sequestration mechanism. Biochemistry 51: 3100-3109.
23. Cho, H., and Bernhardt, T.G. (2013) Identification of the SlmA active site responsible for blocking bacterial cytokinetic ring assembly over the chromosome. PLoS Genet 9: e1003304.
24. Coltharp, C., Kessler, R.P., and Xiao, J. (2012) Accurate construction of photoactivated localization microscopy (PALM) images for quantitative measurements. PLoS ONE 7: e51725.
25. Dai, K., and Lutkenhaus, J. (1991) ftsZ is an essential cell division gene in Escherichia coli. J Bacteriol 173: 3500-3506.
26. Dajkovic, A., Mukherjee, A., and Lutkenhaus, J. (2008) Investigation of regulation of FtsZ assembly by SulA and development of a model for FtsZ polymerization. J Bacteriol 190: 2513-2526.
27. Dajkovic, A., Pichoff, S., Lutkenhaus, J., and Wirtz, D. (2010) Cross-linking FtsZ polymers into coherent Z rings. Mol Microbiol 78: 651-668.
28. Datsenko, K.A., and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645.
29. Deich, J., Judd, E.M., McAdams, H.H., and Moerner, W.E. (2004) Visualization of the movement of single histidine kinase molecules in live Caulobacter cells. Proc Natl Acad Sci USA 101: 15921-15926.
30. Den Blaauwen, T., Buddelmeijer, N., Aarsman, M.E., Hameete, C.M., and Nanninga, N. (1999) Timing of FtsZ assembly in Escherichia coli. J Bacteriol 181: 5167-5175.
31. Di Lallo, G., Fagioli, M., Barionovi, D., Ghelardini, P., and Paolozzi, L. (2003) Use of a two-hybrid assay to study the assembly of a complex multicomponent protein machinery: bacterial septosome differentiation. Microbiology 149: 3353-3359.
32. Domadia, P., Swarup, S., Bhunia, A., Sivaraman, J., and Dasgupta, D. (2007) Inhibition of bacterial cell division protein FtsZ by cinnamaldehyde. Biochem Pharmacol 74: 831-840.
33. Durand-Heredia, J., Rivkin, E., Fan, G., Morales, J., and Janakiraman, A. (2012) Identification of ZapD as a cell division factor that promotes the assembly of FtsZ in Escherichia coli. J Bacteriol 194: 3189-3198.
34. Durand-Heredia, J.M., Yu, H.H., De Carlo, S., Lesser, C.F., and Janakiraman, A. (2011) Identification and characterization of ZapC, a stabilizer of the FtsZ ring in Escherichia coli. J Bacteriol 193: 1405-1413.
35. Ebersbach, G., Galli, E., Moller-Jensen, J., Lowe, J., and Gerdes, K. (2008) Novel coiled-coil cell division factor ZapB stimulates Z ring assembly and cell division. Mol Microbiol 68: 720-735.
36. Erickson, H.P., Taylor, D.W., Taylor, K.A., and Bramhill, D. (1996a) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci USA 93: 519-523.
37. Erickson, H.P., Taylor, D.W., Taylor, K.A., and Bramhill, D. (1996b) Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers. Proc Natl Acad Sci USA 93: 519-523.
38. Erickson, H.P., Anderson, D.E., and Osawa, M. (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74: 504-528.
39. Errington, J., Daniel, R.A., and Scheffers, D.J. (2003) Cytokinesis in bacteria. Microbiol Mol Biol Rev 67: 52-65.
40. Espeli, O., Borne, R., Dupaigne, P., Thiel, A., Gigant, E., Mercier, R., and Boccard, F. (2012) A MatP-divisome interaction coordinates chromosome segregation with cell division in E. coli. EMBO J 31: 3198-3211.
41. Esue, O., Cordero, M., Wirtz, D., and Tseng, Y. (2005) The assembly of MreB, a prokaryotic homolog of actin. J Biol Chem 280: 2628-2635.
42. Fu, G., Huang, T., Buss, J., Coltharp, C., Hensel, Z., and Xiao, J. (2010) In vivo structure of the E. coli FtsZ-ring revealed by photoactivated localization microscopy (PALM). PLoS ONE 5: e12680.
43. Galli, E., and 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.
44. Galli, E., and Gerdes, K. (2012) FtsZ-ZapA-ZapB interactome of Escherichia coli. J Bacteriol 194: 292-302.
45. Gamba, P., Veening, J.W., Saunders, N.J., Hamoen, L.W., and Daniel, R.A. (2009) Two-step assembly dynamics of the Bacillus subtilis divisome. J Bacteriol 191: 4186-4194.
46. Goehring, N.W., Gueiros-Filho, F., and Beckwith, J. (2005) Premature targeting of a cell division protein to midcell allows dissection of divisome assembly in Escherichia coli. Genes Dev 19: 127-137.
47. Gueiros-Filho, F.J., and Losick, R. (2002) A widely conserved bacterial cell division protein that promotes assembly of the tubulin-like protein FtsZ. Genes Dev 16: 2544-2556.
48. Hale, C.A., Shiomi, D., Liu, B., Bernhardt, T.G., Margolin, W., Niki, H., and de Boer, P.A.J. (2011) Identification of Escherichia coli ZapC (YcbW) as a component of the division apparatus that binds and bundles FtsZ polymers. J Bacteriol 193: 1393-1404.
49. Harry, E., Monahan, L., and Thompson, L. (2006) Bacterial cell division: the mechanism and its precison. Int Rev Cytol 253: 27-94.
50. Huecas, S., Llorca, O., Boskovic, J., Martín-Benito, J., Valpuesta, J.M., and Andreu, J.M. (2008) Energetics and geometry of FtsZ polymers: nucleated self-assembly of single protofilaments. Biophys J 94: 1796-1806.
51. Jennings, P.C., Cox, G.C., Monahan, L.G., and Harry, E.J. (2011) Super-resolution imaging of the bacterial cytokinetic protein FtsZ. Micron 42: 336-341.
52. Khlebnikov, A., Datsenko, K.A., Skaug, T., Wanner, B.L., and Keasling, J.D. (2001) Homogeneous expression of the P(BAD) promoter in Escherichia coli by constitutive expression of the low-affinity high-capacity AraE transporter. Microbiology 147: 3241-3247.
53. Kim, S.Y., Gitai, Z., Kinkhabwala, A., Shapiro, L., and Moerner, W.E. (2006) Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc Natl Acad Sci USA 103: 10929-10934.
54. Kitagawa, M., Ara, T., Arifuzzaman, M., Ioka-Nakamichi, T., Inamoto, E., Toyonaga, H., and Mori, H. (2005) 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 Res 12: 291-299.
55. Landgraf, D., Okumus, B., Chien, P., Baker, T.A., and Paulsson, J. (2012) Segregation of molecules at cell division reveals native protein localization. Nat Methods 9: 480-482.
56. Lando, D., Endesfelder, U., Berger, H., Subramanian, L., Dunne, P.D., McColl, J., etal. (2012) Quantitative single-molecule microscopy reveals that CENP-ACnp1 deposition occurs during G2 in fission yeast. Open Biol 2: 120078. doi:10.1098/rsob.120078.
57. Leake, M.C., Chandler, J.H., Wadhams, G.H., Bai, F., Berry, R.M., and Armitage, J.P. (2006) Stoichiometry and turnover in single, functioning membrane protein complexes. Nature 443: 355-358.
58. Li, Z., Trimble, M.J., Brun, Y.V., and Jensen, G.J. (2007) The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J 26: 4694-4708.
59. Low, H.H., Moncrieffe, M.C., and Lowe, J. (2004) The crystal structure of ZapA and its modulation of FtsZ polymerisation. J Mol Biol 341: 839-852.
60. Lutkenhaus, J. (1993) FtsZ ring in bacterial cytokinesis. Mol Microbiol 9: 403-409.
61. Lutkenhaus, J. (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562.
62. Lutkenhaus, J.F., Wolf-Watz, H., and Donachie, W.D. (1980) Organization of genes in the ftsA-envA region of the Escherichia coli genetic map and identification of a new fts locus (ftsZ). J Bacteriol 142: 615-620.
63. Ma, X., Ehrhardt, D.W., and 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 USA 93: 12998-13003.
64. McKinney, S.A., Murphy, C.S., Hazelwood, K.L., Davidson, M.W., and Looger, L.L. (2009) A bright and photostable photoconvertible fluorescent protein. Nat Methods 6: 131-133.
65. Maggi, S., Massidda, O., Luzi, G., Fadda, D., Paolozzi, L., and Ghelardini, P. (2008) Division protein interaction web: identification of a phylogenetically conserved common interactome between Streptococcus pneumoniae and Escherichia coli. Microbiology 154: 3042-3052.
66. Margolin, W. (2005) FtsZ and the division of prokaryotic cells and organelles. Nat Rev Mol Cell Biol 6: 862-871.
67. Mercier, R., Petit, M.-A., Schbath, S., Robin, S., Karoui, M.E., Boccard, F., and Espéli, O. (2008) The MatP/matS site-specific system organizes the terminus region of the E. coli chromosome into a macrodomain. Cell 135: 475-485.
68. Milam, S.L., Osawa, M., and Erickson, H.P. (2012) Negative-stain electron microscopy of inside-out FtsZ rings reconstituted on artificial membrane tubules show ribbons of protofilaments. Biophys J 103: 59-68.
69. Mileykovskaya, E., and Dowhan, W. (2005) Role of membrane lipids in bacterial division-site selection. Curr Opin Microbiol 8: 135-142.
70. Mohammadi, T., Ploeger, G.E., Verheul, J., Comvalius, A.D., Martos, A., Alfonso, C., etal. (2009) The GTPase activity of Escherichia coli FtsZ determines the magnitude of the FtsZ polymer bundling by ZapA in vitro. Biochemistry 48: 11056-11066.
71. Möll, A., Schlimpert, S., Briegel, A., Jensen, G.J., and Thanbichler, M. (2010) DipM, a new factor required for peptidoglycan remodelling during cell division in Caulobacter crescentus. Mol Microbiol 77: 90-107.
72. Monahan, L.G., Robinson, A., and Harry, E.J. (2009) Lateral FtsZ association and the assembly of the cytokinetic Z ring in bacteria. Mol Microbiol 74: 1004-1017.
73. Mukherjee, A., and Lutkenhaus, J. (1994) Guanine nucleotide-dependent assembly of FtsZ into filaments. J Bacteriol 176: 2754-2758.
74. Mukherjee, A., and Lutkenhaus, J. (1999) Analysis of FtsZ assembly by light scattering and determination of the role of divalent metal cations. J Bacteriol 181: 823-832.
75. Mullineaux, C.W., Nenninger, A., Ray, N., and Robinson, C. (2006) Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J Bacteriol 188: 3442-3448.
76. Nagai, T., Ibata, K., Park, E.S., Kubota, M., Mikoshiba, K., and Miyawaki, A. (2002) A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat Biotechnol 20: 87-90.
77. Niu, L., and Yu, J. (2008) Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys J 95: 2009-2016.
78. Nogales, E., Downing, K.H., Amos, L.A., and Lowe, J. (1998) Tubulin and FtsZ form a distinct family of GTPases. Nat Struct Biol 5: 451-458.
79. Oliva, M.A., Cordell, S.C., and Lowe, J. (2004) Structural insights into FtsZ protofilament formation. Nat Struct Mol Biol 11: 1243-1250.
80. Osawa, M., Anderson, D.E., and Erickson, H.P. (2008) Reconstitution of contractile FtsZ rings in liposomes. Science 320: 792-794.
81. Osawa, M., Anderson, D.E., and Erickson, H.P. (2009) Curved FtsZ protofilaments generate bending forces on liposome membranes. EMBO J 28: 3476-3484.
82. Pacheco-Gómez, R., Cheng, X., Hicks, M.R., Smith, C.J.I., Roper, D.I., Addinall, S., etal. (2013) Tetramerization of ZapA is required for FtsZ bundling. Biochemical. Journal 449: 795-802.
83. Popp, D., Iwasa, M., Narita, A., Erickson, H.P., and Maéda, Y. (2009) FtsZ condensates: an in vitro electron microscopy study. Biopolymers 91: 340-350.
84. Renz, M., Daniels, B.R., Vámosi, G., Arias, I.M., and Lippincott-Schwartz, J. (2012) Plasticity of the asialoglycoprotein receptor deciphered by ensemble FRET imaging and single-molecule counting PALM imaging. Proc Natl Acad Sci USA 109: E2989-E2997.
85. Romberg, L., Simon, M., and Erickson, H.P. (2001) Polymerization of Ftsz, a bacterial homolog of tubulin. is assembly cooperative? J Biol Chem 276: 11743-11753.
86. Rust, M.J., Bates, M., and Zhuang, X. (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3: 793-795.
87. Sengupta, P., Jovanovic-Talisman, T., Skoko, D., Renz, M., Veatch, S.L., and Lippincott-Schwartz, J. (2011) Probing protein heterogeneity in the plasma membrane using PALM and pair correlation analysis. Nat Methods 8: 969-975.
88. Small, E., Marrington, R., Rodger, A., Scott, D.J., Sloan, K., Roper, D., etal. (2007) FtsZ polymer-bundling by the Escherichia coli ZapA orthologue, YgfE, involves a conformational change in bound GTP. J Mol Biol 369: 210-221.
89. Srinivasan, R., Mishra, M., Wu, L., Yin, Z., and Balasubramanian, M.K. (2008) The bacterial cell division protein FtsZ assembles into cytoplasmic rings in fission yeast. Genes Dev 22: 1741-1746.
90. Strauss, M.P., Liew, A.T.F., Turnbull, L., Whitchurch, C.B., Monahan, L.G., and Harry, E.J. (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.
91. Stricker, J., Maddox, P., Salmon, E.D., and Erickson, H.P. (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA 99: 3171-3175.
92. Swulius, M.T., and Jensen, G.J. (2012) The helical MreB cytoskeleton in Escherichia coli MC1000/pLE7 is an artifact of the N-terminal yellow fluorescent protein tag. J Bacteriol 194: 6382-6386.
93. Thiel, A., Valens, M., Vallet-Gely, I., Espéli, O., and Boccard, F. (2012) Long-range chromosome organization in E. coli: a site-specific system isolates the Ter macrodomain. PLoS Genet 8: e1002672.
94. Tonthat, N.K., Arold, S.T., Pickering, B.F., Van Dyke, M.W., Liang, S., Lu, Y., etal. (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30: 154-164.
95. Ulbrich, M.H., and Isacoff, E.Y. (2007) Subunit counting in membrane-bound proteins. Nat Methods 4: 319-321.
96. Wang, X., Possoz, C., and Sherratt, D.J. (2005) Dancing around the divisome: asymmetric chromosome segregation in Escherichia coli. Genes Dev 19: 2367-2377.
97. Ward, J.E., Jr, and Lutkenhaus, J. (1985) Overproduction of FtsZ induces minicell formation in E. coli. Cell 42: 941-949.
98. Zhang, M., Chang, H., Zhang, Y., Yu, J., Wu, L., Ji, W., etal. (2012) Rational design of true monomeric and bright photoactivatable fluorescent proteins. Nat Methods 9: 727-729.