Skip to main content
SpringerLink
Log in

In Vitro Reconstitution of the Initial Stages of the Bacterial Cell Division Machinery

  • Original Paper
  • Published:
Journal of Biological Physics Aims and scope Submit manuscript

Abstract

Fission of many prokaryotes as well as some eukaryotic organelles depends on the self-assembly of the FtsZ protein into a membrane-associated ring structure early in the division process. Different components of the machinery are then sequentially recruited. Although the assembly order has been established, the molecular interactions and the understanding of the force-generating mechanism of this dividing machinery have remained elusive. It is desirable to develop simple reconstituted systems that attempt to reproduce, at least partially, some of the stages of the process. High-resolution studies of Escherichia coli FtsZ filaments’ structure and dynamics on mica have allowed the identification of relevant interactions between filaments that suggest a mechanism by which the polymers could generate force on the membrane. Reconstituting the membrane-anchoring protein ZipA on E. coli lipid membrane on surfaces is now providing information on how the membrane attachment regulates FtsZ polymer dynamics and indicates the important role played by the lipid composition of the membrane.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Harry, E., Monahan, L., Thompson, L.: Bacterial cell division: the mechanism and its precision. Int. Rev. Cytol. 253, 27–93 (2006). doi:10.1016/S0074-7696(06)53002-5

    Article  Google Scholar 

  2. Vicente, M., Rico, A.I.: The order of the ring: assembly of Escherichia coli cell division components. Mol. Microbiol. 61(1), 5–8 (2006)

    Article  Google Scholar 

  3. Surrey, T., Nédélec, F., Leibler, S., Karsenti, E.: Physical properties determining self-organization of motors and microtubules. Science 292(5519), 1167–1171 (2001). doi:10.1126/science.1059758

    Article  ADS  Google Scholar 

  4. Karsenti, E., Nédélec, F., Surrey, T.: Modelling microtubule patterns. Nat. Cell Biol. 8(11), 1204–1211 (2006). doi:10.1038/ncb1498

    Article  Google Scholar 

  5. Leduc, C., Campas, O., Zeldovich, K.B., Roux, A., Jolimaitre, P., Bourel-Bonnet, L., Goud, B., Joanny, J.F., Bassereau, P., Prost, J.: Cooperative extraction of membrane nanotubes by molecular motors. Proc. Natl. Acad. Sci. U. S. A. 101(49), 17096–17101 (2004). doi:10.1073/pnas.0406598101

    Article  ADS  Google Scholar 

  6. Footer, M.J., Kerssemakers, J.W.J., Theriot, J.A., Dogterom, M.: Direct measurement of force generation by actin filament polymerization using an optical trap. Proc. Natl. Acad. Sci. U. S. A. 104(7), 2181–2186 (2007). doi:10.1073/pnas.0607052104

    Article  ADS  Google Scholar 

  7. Lagomarsino, M.C., Tanase, C., Vos, J.W., Emons, A.M.C., Mulder, B.M., Dogterom, M.: Microtubule organization in three-dimensional confined geometries: evaluating the role of elasticity through a combined in vitro and modeling approach. Biophys. J. 92(3), 1046–1057 (2007). doi:10.1529/biophysj.105.076893

    Article  ADS  Google Scholar 

  8. Brunner, C., Wahnes, C., Vogel, V.: Cargo pick-up from engineered loading stations by kinesin driven molecular shuttles. Lab Chip 7, 1263–1271 (2007). doi:10.1039/b707301a

    Article  Google Scholar 

  9. Clemmens, J., Hess, H., Doot, R., Matzke, C.M., Bachand, G.D., Vogel, V.: Motor-protein “roundabouts”: microtubules moving on kinesin-coated tracks through engineered networks. Lab Chip 4, 83–86 (2004)

    Article  Google Scholar 

  10. Shih, Y.-L., Rothfield, L.: The bacterial cytoskeleton. Microbiol. Mol. Biol. Rev. 70(3), 729–754 (2006). doi:10.1128/MMBR.00017-06

    Article  Google Scholar 

  11. Dai, K., Lutkenhaus, J.: FtsZ is an essential cell division gene in Escherichia coli. J. Bacteriol. 173(11), 3500–3506 (1991)

    Google Scholar 

  12. Margolin, W.: FtsZ and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6, 862–871 (2005). doi:10.1038/nrm1745

    Article  Google Scholar 

  13. Dajkovic, A., Lutkenhaus, J.: Z ring as executor of bacterial cell division. J. Mol. Microbiol. Biotechnol. 11, 140–151 (2006). doi:10.1159/000094050

    Article  Google Scholar 

  14. Romberg, L., Levin, P.A.: Assembly dynamics of the bacterial cell division protein FtsZ: poised at the edge of stability. Annu. Rev. Microbiol. 57, 125–154 (2003). doi:10.1146/annurev.micro.57.012903.074300

    Article  Google Scholar 

  15. Stricker, J., Maddox, P., Salmon, E.D., Erickson, H.P.: Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. U. S. A. 99, 3171–3175 (2002). doi:10.1073/pnas.052595099

    Article  ADS  Google Scholar 

  16. Hale, C.A., de Boer, P.A.J.: 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 (1997). doi:10.1016/S0092-8674(00)81838-3

    Article  Google Scholar 

  17. Rivas, G., López, A., Mingorance, J., Ferrandiz, M.J., Zorrilla, S., Minton, A., Vicente, M., Andreu, J.M.: Magnesium-induced linear self-association of the FtsZ bacterial cell division protein monomer—the primary steps for the FtsZ assembly. J. Biol. Chem. 275, 11740–11749 (2000). doi:10.1074/jbc.275.16.11740

    Article  Google Scholar 

  18. RayChaudhuri, D.: ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division. EMBO J. 18, 2372–2383 (1999). doi:10.1093/emboj/18.9.2372

    Article  Google Scholar 

  19. Moreno-Herrero, F., de Pablo, P.J., Fernández-Sánchez, R., Colchero, J., Gómez-Herrero, J., Baró, A.M.: Scanning force microscopy jumping and tapping modes in liquids. Appl. Phys. Lett. 81(14), 2620–2622 (2002). doi:10.1063/1.1509856

    Article  ADS  Google Scholar 

  20. Levy, D.C.M., Rigaud, J.L.: Two-dimensional crystallization of membrane proteins: the lipid layer strategy. FEBS Lett. 504, 187–193 (2001). doi:10.1016/S0014-5793(01)02748-X

    Article  Google Scholar 

  21. Mingorance, J., Tadros, M., Vicente, M., González, J.M., Rivas, G., Vélez, M.: Visualization of single Escherichia coli FtsZ filament dynamics with atomic force microscopy. J. Biol. Chem. 280, 20909–20914 (2005). doi:10.1074/jbc.M503059200

    Article  Google Scholar 

  22. González, J.M., Vélez, M., Jiménez, M., Alfonso, C., Schuck, P., Mingorance, J., Vicente, M., Minton, A.P., Rivas, G.: The cooperative behavior of E. coli cell division protein FtsZ assembly involves the preferential cyclization of long single-stranded fibrils. Proc. Natl. Acad. Sci. U. S. A. 102, 1895–1900 (2005). doi:10.1073/pnas.0409517102

    Article  ADS  Google Scholar 

  23. Carlier, M., Didry, D., Melki, R., Chabre, M., Pantaloni, D.: Stabilization of microtubules by inorganic phosphate and its structural analogues, the fluoride complexes of aluminium and beryllium. Biochemistry 28, 3628 (1989). doi:10.1021/bi00434a073

    Article  Google Scholar 

  24. Bigay, J.D.P., Pfister, C., Chabre, M.: Fluoride complexes of aluminium or beryllium act on G-proteins as reversibly bound analogues of the gamma phosphate of GTP. EMBO J. 6, 2907–2913 (1987)

    Google Scholar 

  25. RayChaudhuri, D., Park, J.T.: A point mutation converts Escherichia coli FtsZ septation GTPase to an ATPase. J. Biol. Chem. 269, 22941–22944 (1994)

    Google Scholar 

  26. Hörger, I., Velasco, E., Mingorance, J., Rivas, G., Vélez, M., Tarazona, P.: Langevin computer simulations of FtsZ filaments and the force generating mechanism during cell division. Phys. Rev., E 77, 011902 (2008)

    Article  ADS  Google Scholar 

  27. Pichoff, S., Lutkenhaus, J.: Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55(6), 1722–1734 (2005). doi:10.1111/j.1365-2958.2005.04522.x

    Article  Google Scholar 

  28. Ohashi, T., Hale, C.A., de Boer, P.A.J., Erickson, H.P.: Structural evidence that the P/Q domain of ZipA is an unstructured, flexible tether between the membrane and the C-terminal FtsZ-binding domain. J. Bacteriol. 184(15), 4313–4315 (2002). doi:10.1128/JB.184.15.4313-4315.2002

    Article  Google Scholar 

  29. Hale, C.A., Rhee, A.C., de Boer, P.A.J.: ZipA-Induced bundling of FtsZ polymers mediated by an interaction between C-terminal domains. J. Bacteriol. 182(18), 5153–5166 (2000). doi:10.1128/JB.182.18.5153-5166.2000

    Article  Google Scholar 

  30. Erickson, H., Taylor, D., Taylor, K.A., Bramhill, D.: 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 (1996). doi:10.1073/pnas.93.1.519

    Article  ADS  Google Scholar 

  31. Díaz, J.F., Kralicek, A., Mingorance, J., Palacios, J.M., Vicente, M., Andreu, J.M.: Activation of cell division protein FtsZ. J. Biol. Chem. 276(20), 17307–17315 (2001). doi:10.1074/jbc.M010920200

    Article  Google Scholar 

  32. Hörger, I., Velasco, E., Rivas, G., Vélez, M., Tarazona, P.: FtsZ bacterial cytoskeletal polymers on curved surfaces: the importance of lateral interactions. Biophys. J. 94, L81–L83 (2008). doi:10.1529/biophysj.107.128363

    Article  Google Scholar 

  33. Lu, C., Stricker, J., Erickson, H.P.: Site-specific mutations of FtsZ—effects on GTPase and in vitro assembly. BMC Microbiol. 1(7), 1471–1482 (2001)

    Google Scholar 

  34. Esue, O., Tseng, Y., Wirtz, D.: The rapid onset of elasticity during the assembly of the bacterial cell-division protein FtsZ. Biochem. Biophys. Res. Commun. 333, 508–516 (2005). doi:10.1016/j.bbrc.2005.05.152

    Article  Google Scholar 

  35. Andrews, S.S., Arkin, A.P.: A mechanical explanation for cytoskeletal rings and helices in bacteria. Biophys. J. 93, 1872–1884 (2007). doi:10.1529/biophysj.106.102343

    Article  ADS  Google Scholar 

  36. Erickson, H.P.: The FtsZ protofilament and attachment of ZipA—structural constraints on the FtsZ power stroke. Curr. Opin. Cell Biol. 13, 55–60 (2001). doi:10.1016/S0955-0674(00)00174-5

    Article  Google Scholar 

Download references

Acknowledgements

This work was financed by the Ministerio de Educación y Ciencia (MEC) under grants BFU2005-04087-C02, FIS2004-05035-C03-02, BCM2002-04617-C02-02 and the Comunidad Autónoma de Madrid (CAM) under NANOBIO-M (http://www.nanobiom.org), grant S-0505/MAT0283 and grant S-0505/ESP-0299.

Author information

Authors and Affiliations

  1. Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas, Madrid, Spain

    Pilar López Navajas & Germán Rivas

  2. Unidad de Investigación y Servicio de Microbiología, Hospital Universitario La Paz, Madrid, Spain

    Jesús Mingorance

  3. Dpto. de Física Teórica de la Materia Condensada, Universidad Autónoma de Madrid, Madrid, Spain

    Ines Hörger, Enrique Velasco & Pedro Tarazona

  4. Instituto Universitario de Ciencia de Materiales “Nicolás Cabrera”, Universidad Autónoma de Madrid, Madrid, Spain

    Pablo Mateos-Gil & Marisela Vélez

Authors
  1. Pilar López Navajas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Germán Rivas
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jesús Mingorance
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pablo Mateos-Gil
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ines Hörger
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Enrique Velasco
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pedro Tarazona
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Marisela Vélez
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marisela Vélez.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Navajas, P.L., Rivas, G., Mingorance, J. et al. In Vitro Reconstitution of the Initial Stages of the Bacterial Cell Division Machinery. J Biol Phys 34, 237–247 (2008). https://doi.org/10.1007/s10867-008-9118-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10867-008-9118-8

Keywords

Search

Navigation