Biophysical Reviews

, Volume 5, Issue 2, pp 63–77 | Cite as

Macromolecular interactions of the bacterial division FtsZ protein: from quantitative biochemistry and crowding to reconstructing minimal divisomes in the test tube

  • Germán Rivas
  • Carlos Alfonso
  • Mercedes Jiménez
  • Begoña Monterroso
  • Silvia Zorrilla
Review

Abstract

The division of Escherichia coli is an essential process strictly regulated in time and space. It requires the association of FtsZ with other proteins to assemble a dynamic ring during septation, forming part of the functionally active division machinery, the divisome. FtsZ reversibly interacts with FtsA and ZipA at the cytoplasmic membrane to form a proto-ring, the first molecular assembly of the divisome, which is ultimately joined by the rest of the division-specific proteins. In this review we summarize the quantitative approaches used to study the activity, interactions, and assembly properties of FtsZ under well-defined solution conditions, with the aim of furthering our understanding of how the behavior of FtsZ is controlled by nucleotides and physiological ligands. The modulation of the association and assembly properties of FtsZ by excluded-volume effects, reproducing in part the natural crowded environment in which this protein has evolved to function, will be described. The subsequent studies on the reactivity of FtsZ in membrane-like systems using biochemical, biophysical, and imaging technologies are reported. Finally, we discuss the experimental challenges to be met to achieve construction of the minimum protein set needed to initiate bacterial division, without cells, in a cell-like compartment. This integrated approach, combining quantitative and synthetic strategies, will help to support (or dismiss) conclusions already derived from cellular and molecular analysis and to complete our understanding on how bacterial division works.

Keywords

Physical biochemistry Mechanistic biochemistry Synthetic biology Protein–protein interactions Protein–membrane interactions Biophysical methods 

Notes

Acknowledgments

GR will always be in debt to Allen Minton for his teachings and advice on many aspects of the scientific process, for his motivation and enthusiasm about science and life in general, and for being so generous with his time and knowledge. It is a real privilege to have such an exceptional maestro, a genuine scholar. Thanks for our friendship. The other authors of this review, particularly BM, share these feelings and are deeply grateful to Allen. His frequent visits to our lab have always been very inspirational and educational for all of us.

We also thank the members of our laboratory contributing to the works here reviewed, and Miguel Vicente (CNB-CSIC) for useful discussions and advice on bacterial division. This work was supported by the Spanish government through grants BIO2008-04478-C03 and BIO2011-28941-C03-03 to GR, and BFU2010-14910 and BIO2011-28941-C03-02 to SZ; by the European Commission through contract HEALTH-F3-2009-223432, by the Human Frontiers Science Program through grant RGP0050/2010-C102, and by Comunidad de Madrid through grant S-BIO-0260/2006 to GR; by the CSIC through grants 200980I186 and 201020I001 to SZ and CA, respectively. BM is a JAE postdoctoral associate from the European Social Fund and the Spanish Consejo Superior de Investigaciones Científicas (CSIC).

Conflicts of interest

None.

References

  1. Abkarian M, Loiseau E, Massiera G (2011) Continuous droplet interface crossing encapsulation (cDICE) for high throughput monodisperse vesicle design. Soft Matter 7:4610–4614CrossRefGoogle Scholar
  2. Adams DW, Errington J (2009) Bacterial cell division: assembly, maintenance and disassembly of the Z ring. Nat Rev Microbiol 7(9):642–653PubMedCrossRefGoogle Scholar
  3. Ahijado-Guzman R, Gomez-Puertas P, Alvarez-Puebla RA, Rivas G, Liz-Marzan LM (2012) Surface-enhanced raman scattering-based detection of the interactions between the essential cell division ftsz protein and bacterial membrane elements. ACS Nano 6(8):7514–7520PubMedCrossRefGoogle Scholar
  4. Alcorlo M, Jimenez M, Ortega A, Hermoso JM, Salas M, Minton AP, Rivas G (2009) Analytical ultracentrifugation studies of phage phi29 protein p6 binding to DNA. J Mol Biol 385(5):1616–1629PubMedCrossRefGoogle Scholar
  5. Arumugam S, Chwastek G, Schwille P (2011) Protein-membrane interactions: the virtue of minimal systems in systems biology. Wiley Interdiscip Rev Syst Biol Med 3(3):269–280PubMedCrossRefGoogle Scholar
  6. Arumugam S, Chwastek G, Fischer-Friedrich E, Ehrig C, Monch I, Schwille P (2012) Surface topology engineering of membranes for the mechanical investigation of the tubulin homologue FtsZ. Angew Chem 51(47):11858–11862CrossRefGoogle Scholar
  7. Attri AK, Minton AP (2005a) Composition gradient static light scattering: a new technique for rapid detection and quantitative characterization of reversible macromolecular hetero-associations in solution. Anal Biochem 346(1):132–138PubMedCrossRefGoogle Scholar
  8. Attri AK, Minton AP (2005b) New methods for measuring macromolecular interactions in solution via static light scattering: basic methodology and application to nonassociating and self-associating proteins. Anal Biochem 337(1):103–110PubMedCrossRefGoogle Scholar
  9. Baciu CL, Becker J, Janshoff A, Sonnichsen C (2008) Protein-membrane interaction probed by single plasmonic nanoparticles. Nano Lett 8(6):1724–1728PubMedCrossRefGoogle Scholar
  10. Bayburt TH, Sligar SG (2010) Membrane protein assembly into nanodiscs. FEBS Lett 584(9):1721–1727PubMedCrossRefGoogle Scholar
  11. Bayley H, Cronin B, Heron A, Holden MA, Hwang WL, Syeda R, Thompson J, Wallace M (2008) Droplet interface bilayers. Mol Biosyst 4(12):1191–1208PubMedCrossRefGoogle Scholar
  12. Chang YY, Cronan JE Jr (1986) Molecular cloning, DNA sequencing, and enzymatic analyses of two Escherichia coli pyruvate oxidase mutants defective in activation by lipids. J Bacteriol 167(1):312–318PubMedGoogle Scholar
  13. 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(23):22549–22554PubMedCrossRefGoogle Scholar
  14. Cisse I, Okumus B, Joo C, Ha T (2007) Fueling protein DNA interactions inside porous nanocontainers. Proc Natl Acad Sci USA 104(31):12646–12650PubMedCrossRefGoogle Scholar
  15. Collier CP, Simpson ML (2011) Micro/nanofabricated environments for synthetic biology. Curr Opin Biotechnol 22(4):516–526PubMedCrossRefGoogle Scholar
  16. Devaux PF, Seigneuret M (1985) Specificity of lipid-protein interactions as determined by spectroscopic techniques. Biochim Biophys Acta 822(1):63–125PubMedCrossRefGoogle Scholar
  17. Dix JA, Hom EFY, Verkman AS (2006) Fluorescence correlation spectroscopy simulations of photophysical phenomena and molecular interactions: a molecular dynamics/Monte Carlo approach. J Phys Chem B 110(4):1896–1906PubMedCrossRefGoogle Scholar
  18. Egan AJ, Vollmer W (2013) The physiology of bacterial cell division. Ann N Y Acad Sci 1277(1):8–28PubMedCrossRefGoogle Scholar
  19. Elcock AH (2010) Models of macromolecular crowding effects and the need for quantitative comparisons with experiment. Curr Opin Struct Biol 20(2):196–206PubMedCrossRefGoogle Scholar
  20. Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. Trends Biochem Sci 26(10):597–604PubMedCrossRefGoogle Scholar
  21. Erickson HP (2009) Modeling the physics of FtsZ assembly and force generation. Proc Natl Acad Sci USA 106(23):9238–9243PubMedCrossRefGoogle Scholar
  22. Erickson HP, Anderson DE, Osawa M (2010) FtsZ in bacterial cytokinesis: cytoskeleton and force generator all in one. Microbiol Mol Biol Rev 74(4):504–528PubMedCrossRefGoogle Scholar
  23. Fodeke AA, Minton AP (2010) Quantitative characterization of polymer-polymer, protein-protein, and polymer-protein interaction via tracer sedimentation equilibrium. J Phys Chem B 114(33):10876–10880PubMedCrossRefGoogle Scholar
  24. Forlin M, Lentini R, Mansy SS (2012) Cellular imitations. Curr Opin Chem Biol 16(5–6):586–592PubMedCrossRefGoogle Scholar
  25. Galush WJ, Shelby SA, Mulvihill MJ, Tao A, Yang P, Groves JT (2009) A nanocube plasmonic sensor for molecular binding on membrane surfaces. Nano Lett 9(5):2077–2082PubMedCrossRefGoogle Scholar
  26. 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(Pt 3):814–825PubMedCrossRefGoogle Scholar
  27. González JM, Jiménez M, Vélez M, Mingorance J, Andreu JM, Vicente M, Rivas G (2003) Essential cell division protein FtsZ assembles into one monomer-thick ribbons under conditions resembling the crowded intracellular environment. J Biol Chem 278(39):37664–37671PubMedCrossRefGoogle Scholar
  28. González JM, Velez M, Jiménez M, Alfonso C, Schuck P, Mingorance J, Vicente M, Minton AP, Rivas G (2005) Cooperative behavior of Escherichia coli cell-division protein FtsZ assembly involves the preferential cyclization of long single-stranded fibrils. Proc Natl Acad Sci USA 102(6):1895–1900PubMedCrossRefGoogle Scholar
  29. Goodsell DS (2010) The machinery of life, 2nd edn. Copernicus Books (Springer Science + Business Media), New YorkGoogle Scholar
  30. Hall D, Minton AP (2003) Macromolecular crowding: qualitative and semiquantitative successes, quantitative challenges. Biochim Biophys Acta 1649(2):127–139PubMedCrossRefGoogle Scholar
  31. Haney SA, Glasfeld E, Hale C, Keeney D, He Z, de Boer P (2001) Genetic analysis of the Escherichia coli FtsZ.ZipA interaction in the yeast two-hybrid system. Characterization of FtsZ residues essential for the interactions with ZipA and with FtsA. J Biol Chem 276(15):11980–11987PubMedCrossRefGoogle Scholar
  32. Hernández-Rocamora VM, García-Montañés C, Rivas G, Llorca O (2012a) Reconstitution of the Escherichia coli cell division ZipA-FtsZ complexes in nanodiscs as revealed by electron microscopy. J Struct Biol 180(3):531–538PubMedCrossRefGoogle Scholar
  33. Hernández-Rocamora VM, Reija B, García C, Natale P, Alfonso C, Minton AP, Zorrilla S, Rivas G, Vicente M (2012b) Dynamic interaction of the Escherichia coli cell division ZipA and FtsZ proteins evidenced in nanodiscs. J Biol Chem 287(36):30097–30104PubMedCrossRefGoogle Scholar
  34. Herrig A, Janke M, Austermann J, Gerke V, Janshoff A, Steinem C (2006) Cooperative adsorption of ezrin on PIP2-containing membranes. Biochemistry 45(43):13025–13034PubMedCrossRefGoogle Scholar
  35. Herzfeld J (2004) Crowding-induced organization in cells: spontaneous alignment and sorting of filaments with physiological control points. J Mol Recognit 17(5):376–381PubMedCrossRefGoogle Scholar
  36. Hyman AA, Simons K (2012) Cell biology. Beyond oil and water–phase transitions in cells. Science 337(6098):1047–1049PubMedCrossRefGoogle Scholar
  37. Janmey PA, Kinnunen PK (2006) Biophysical properties of lipids and dynamic membranes. Trends Cell Biol 16(10):538–546PubMedCrossRefGoogle Scholar
  38. Jiao M, Li HT, Chen J, Minton AP, Liang Y (2010) Attractive protein-polymer interactions markedly alter the effect of macromolecular crowding on protein association equilibria. Biophys J 99(3):914–923PubMedCrossRefGoogle Scholar
  39. Jimenez M, Rivas G, Minton AP (2007) Quantitative characterization of weak self-association in concentrated solutions of immunoglobulin G via the measurement of sedimentation equilibrium and osmotic pressure. Biochemistry 46(28):8373–8378PubMedCrossRefGoogle Scholar
  40. Jiménez M, Martos A, Vicente M, Rivas G (2011) Reconstitution and organization of Escherichia coli proto-ring elements (FtsZ and FtsA) inside giant unilamellar vesicles obtained from bacterial inner membranes. J Biol Chem 286(13):11236–11241PubMedCrossRefGoogle Scholar
  41. Keating CD (2012) Aqueous phase separation as a possible route to compartmentalization of biological molecules. Acc Chem Res 45(12):2114–2124PubMedCrossRefGoogle Scholar
  42. Krupka M, Rivas G, Rico AI, Vicente M (2012) Key role of two terminal domains in the bidirectional polymerization of FtsA protein. J Biol Chem 287(10):7756–7765PubMedCrossRefGoogle Scholar
  43. Kuthan H (2001) Self-organisation and orderly processes by individual protein complexes in the bacterial cell. Prog Biophys Mol Biol 75(1–2):1–17PubMedCrossRefGoogle Scholar
  44. Lavalette D, Hink MA, Tourbez M, Tetreau C, Visser AJ (2006) Proteins as micro viscosimeters: brownian motion revisited. Eur Biophys J Biophys Lett 35(6):517–522CrossRefGoogle Scholar
  45. Liu AP, Fletcher DA (2009) Biology under construction: in vitro reconstitution of cellular function. Nat Rev 10(9):644–650CrossRefGoogle Scholar
  46. Loose M, Fischer-Friedrich E, Ries J, Kruse K, Schwille P (2008) Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science (New York) 320(5877):789–792CrossRefGoogle Scholar
  47. Loose M, Fischer-Friedrich E, Herold C, Kruse K, Schwille P (2011a) Min protein patterns emerge from rapid rebinding and membrane interaction of MinE. Nat Struct Mol Biol 18(5):577–583PubMedCrossRefGoogle Scholar
  48. Loose M, Kruse K, Schwille P (2011b) Protein self-organization: lessons from the min system. Annu Rev Biophys 40:315–336PubMedCrossRefGoogle Scholar
  49. Lopez-Montero I, Arriaga LR, Rivas G, Velez M, Monroy F (2010) Lipid domains and mechanical plasticity of Escherichia coli lipid monolayers. Chem Phys Lipids 163(1):56–63PubMedCrossRefGoogle Scholar
  50. Lopez-Montero I, Mateos-Gil P, Sferrazza M, Navajas PL, Rivas G, Velez M, Monroy F (2012) Active membrane viscoelasticity by the bacterial FtsZ-division protein. Langmuir 28(10):4744–4753PubMedCrossRefGoogle Scholar
  51. Lopez-Montero I, Lopez-Navajas P, Mingorance J, Velez M, Vicente M, Monroy F (2013) Membrane reconstruction of FtsZ-ZipA complex inside giant spherical vesicles made of E. coli lipid: large membrane dilation and analysis of membrane plasticity. Biochim Biophys Acta 1828:687–698Google Scholar
  52. Lu C, Stricker J, Erickson HP (1998) FtsZ from Escherichia coli, Azotobacter vinelandii, and Thermotoga maritima—quantitation, GTP hydrolysis, and assembly. Cell Motil Cytoskeleton 40(1):71–86PubMedCrossRefGoogle Scholar
  53. Lutkenhaus J, Pichoff S, Du S (2012) Bacterial cytokinesis: from Z ring to divisome. Cytoskeleton (Hoboken) 69(10):778–790CrossRefGoogle Scholar
  54. Maeda YT, Nakadai T, Shin J, Uryu K, Noireaux V, Libchaber A (2012) Assembly of MreB filaments on liposome membranes: a synthetic biology approach. ACS Synth Biol 1(2):53–59CrossRefGoogle Scholar
  55. Margolin W (2000) Organelle division: self-assembling GTPase caught in the middle. Curr Biol 10(9):R328–R330PubMedCrossRefGoogle Scholar
  56. Marguet M, Sandre O, Lecommandoux S (2012) Polymersomes in “gelly” polymersomes: toward structural cell mimicry. Langmuir 28(4):2035–2043PubMedCrossRefGoogle Scholar
  57. Martino C, Kim SH, Horsfall L, Abbaspourrad A, Rosser SJ, Cooper J, Weitz DA (2012) Protein expression, aggregation, and triggered release from polymersomes as artificial cell-like structures. Angew Chem Int Ed Engl 51:6416–6420Google Scholar
  58. Martos A, Alfonso C, López-Navajas P, Ahijado-Guzman R, Mingorance J, Minton AP, Rivas G (2010) Characterization of self-association and heteroassociation of bacterial cell division proteins FtsZ and ZipA in solution by composition gradient-static light scattering. Biochemistry 49(51):10780–10787PubMedCrossRefGoogle Scholar
  59. Martos A, Jimenez M, Rivas G, Schwille P (2012a) Towards a bottom-up reconstitution of bacterial cell division. Trends Cell Biol 22(12):634–643PubMedCrossRefGoogle Scholar
  60. Martos A, Monterroso B, Zorrilla S, Reija B, Alfonso C, Mingorance J, Rivas G, Jimenez M (2012b) Isolation, characterization and lipid-binding properties of the recalcitrant FtsA division protein from Escherichia coli. PLoS One 7(6):e39829PubMedCrossRefGoogle Scholar
  61. Mateos-Gil P, Paez A, Horger I, Rivas G, Vicente M, Tarazona P, Velez M (2012) Depolymerization dynamics of individual filaments of bacterial cytoskeletal protein FtsZ. Proc Natl Acad Sci USA 109:8133–8138PubMedCrossRefGoogle Scholar
  62. Matosevic S (2012) Synthesizing artificial cells from giant unilamellar vesicles: state-of-the art in the development of microfluidic technology. Bioessays 34(11):992–1001PubMedCrossRefGoogle Scholar
  63. Menendez M, Rivas G, Diaz JF, Andreu JM (1998) Control of the structural stability of the tubulin dimer by one high affinity bound magnesium ion at nucleotide N-site. J Biol Chem 273(1):167–176PubMedCrossRefGoogle Scholar
  64. Mingorance J, Rivas G, Velez M, Gomez-Puertas P, Vicente M (2010) Strong FtsZ is with the force: mechanisms to constrict bacteria. Trends Microbiol 18(8):348–356PubMedCrossRefGoogle Scholar
  65. Minton AP (1983) The effect of volume occupancy upon the thermodynamic activity of proteins: some biochemical consequences. Mol Cell Biochem 55(2):119–140PubMedCrossRefGoogle Scholar
  66. Minton AP (1990) Holobiochemistry: the effect of local environment upon the equilibria and rates of biochemical reactions. Int J Biochem 22(10):1063–1067PubMedCrossRefGoogle Scholar
  67. Minton AP (2000) Implications of macromolecular crowding for protein assembly. Curr Opin Struct Biol 10(1):34–39PubMedCrossRefGoogle Scholar
  68. Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276(14):10577–10580PubMedCrossRefGoogle Scholar
  69. Minton AP (2006) How can biochemical reactions within cells differ from those in test tubes? J Cell Sci 119(Pt 14):2863–2869PubMedCrossRefGoogle Scholar
  70. Minton AP (2012) Hard quasispherical particle models for the viscosity of solutions of protein mixtures. J Phys Chem B 116(31):9310–9315PubMedCrossRefGoogle Scholar
  71. Minton AP (2013) Quantitative assessment of the relative contributions of steric repulsion and chemical interactions to macromolecular crowding. Biopolymers 99(4):239–244PubMedCrossRefGoogle Scholar
  72. Minton AP, Wilf J (1981) Effect of macromolecular crowding upon the structure and function of an enzyme: glyceraldehyde-3-phosphate dehydrogenase. Biochemistry 20(17):4821–4826PubMedCrossRefGoogle Scholar
  73. Monterroso B, Ahijado-Guzman R, Reija B, Alfonso C, Zorrilla S, Minton AP, Rivas G (2012a) Mg(2+)-linked self-assembly of FtsZ in the presence of GTP or a GTP analogue involves the concerted formation of a narrow size distribution of oligomeric species. Biochemistry 51:4541–4550PubMedCrossRefGoogle Scholar
  74. Monterroso B, Rivas G, Minton AP (2012b) An equilibrium model for the Mg(2+)-linked self-assembly of FtsZ in the presence of GTP or a GTP analogue. Biochemistry 51:6108–6113PubMedCrossRefGoogle Scholar
  75. Nagarajan S, Amir D, Grupi A, Goldenberg DP, Minton AP, Haas E (2011) Modulation of functionally significant conformational equilibria in adenylate kinase by high concentrations of trimethylamine oxide attributed to volume exclusion. Biophys J 100(12):2991–2999PubMedCrossRefGoogle Scholar
  76. Nanninga N (1998) Morphogenesis of Escherichia coli. Microbiol Mol Biol Rev 62(1):110–129PubMedGoogle Scholar
  77. Nath A, Atkins WM, Sligar SG (2007) Applications of phospholipid bilayer nanodiscs in the study of membranes and membrane proteins. Biochemistry 46(8):2059–2069PubMedCrossRefGoogle Scholar
  78. Noireaux V, Maeda YT, Libchaber A (2011) Development of an artificial cell, from self-organization to computation and self-reproduction. Proc Natl Acad Sci USA 108(9):3473–3480PubMedCrossRefGoogle Scholar
  79. Ohashi T, Hale CA, de Boer PA, Erickson HP (2002) 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):4313–4315PubMedCrossRefGoogle Scholar
  80. Osawa M, Erickson HP (2011) Inside-out Z rings–constriction with and without GTP hydrolysis. Mol Microbiol 81(2):571–579PubMedCrossRefGoogle Scholar
  81. Osawa M, Anderson DE, Erickson HP (2008) Reconstitution of contractile FtsZ Rings in Liposomes. Science 320(5877):792–794PubMedCrossRefGoogle Scholar
  82. Pazos M, Natale P, Vicente M (2012) A specific role for the ZipA protein in cell division: stabilization of the FtsZ protein. J Biol Chem 288(5):3219–3226PubMedCrossRefGoogle Scholar
  83. Peters RJRW, Louzao I, van Hest JCM (2012) From polymeric nanoreactors to artificial organelles. Chem Sci 3(2):335–342CrossRefGoogle Scholar
  84. Phillip Y, Schreiber G (2013) Formation of protein complexes in crowded environments—From in vitro to in vivo. FEBS Lett. doi:10.1016/j.febslet.2013.01.007 PubMedGoogle Scholar
  85. Pichoff S, Lutkenhaus J (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55(6):1722–1734PubMedCrossRefGoogle Scholar
  86. Pichoff S, Shen B, Sullivan B, Lutkenhaus J (2012) FtsA mutants impaired for self-interaction bypass ZipA suggesting a model in which FtsA’s self-interaction competes with its ability to recruit downstream division proteins. Mol Microbiol 83(1):151–167PubMedCrossRefGoogle Scholar
  87. Popp D, Iwasa M, Narita A, Erickson HP, Maeda Y (2009) FtsZ condensates: an in vitro electron microscopy study. Biopolymers 91(5):340–350PubMedCrossRefGoogle Scholar
  88. Record MT, Courtenay ES, Cayley S, Guttman HJ (1998) Biophysical compensation mechanisms buffering E-coli protein-nucleic acid interactions against changing environments. Trends Biochem Sci 23(5):190–194PubMedCrossRefGoogle Scholar
  89. Reija B, Monterroso B, Jiménez M, Vicente M, Rivas G, Zorrilla S (2011) Development of a homogeneous fluorescence anisotropy assay to monitor and measure FtsZ assembly in solution. Anal Biochem 418(1):89–96PubMedCrossRefGoogle Scholar
  90. Richmond DL, Schmid EM, Martens S, Stachowiak JC, Liska N, Fletcher DA (2011) Forming giant vesicles with controlled membrane composition, asymmetry, and contents. Proc Natl Acad Sci USA 108(23):9431–9436PubMedCrossRefGoogle Scholar
  91. Rivas G, Minton AP (2004) Non-ideal tracer sedimentation equilibrium: a powerful tool for the characterization of macromolecular interactions in crowded solutions. J Mol Recognit 17(5):362–367PubMedCrossRefGoogle Scholar
  92. Rivas G, Fernandez JA, Minton AP (1999) Direct observation of the self-association of dilute proteins in the presence of inert macromolecules at high concentration via tracer sedimentation equilibrium: theory, experiment, and biological significance. Biochemistry 38(29):9379–9388PubMedCrossRefGoogle Scholar
  93. Rivas G, López A, Mingorance J, Ferrándiz MJ, Zorrilla S, Minton AP, Vicente M, Andreu JM (2000) Magnesium-induced linear self-association of the FtsZ bacterial cell division protein monomer. The primary steps for FtsZ assembly. The J Biol Chem 275(16):11740–11749CrossRefGoogle Scholar
  94. Rivas G, Fernandez JA, Minton AP (2001) Direct observation of the enhancement of noncooperative protein self-assembly by macromolecular crowding: Indefinite linear self-association of bacterial cell division protein FtsZ. Proc Natl Acad Sci USA 98(6):3150–3155PubMedCrossRefGoogle Scholar
  95. Rueda S, Vicente M, Mingorance J (2003) Concentration and assembly of the division ring proteins FtsZ, FtsA, and ZipA during the Escherichia coli cell cycle. J Bacteriol 185(11):3344–3351PubMedCrossRefGoogle Scholar
  96. Salvarelli E, Krupka M, Rivas G, Vicente M, Mingorance J (2011) Independence between GTPase active sites in the Escherichia coli cell division protein FtsZ. FEBS Lett 585(24):3880–3883PubMedCrossRefGoogle Scholar
  97. Schweizer J, Loose M, Bonny M, Kruse K, Monch I, Schwille P (2012) Geometry sensing by self-organized protein patterns. Proc Natl Acad Sci USA 109(38):15283–15288PubMedCrossRefGoogle Scholar
  98. Sezgin E, Schwille P (2012) Model membrane platforms to study protein-membrane interactions. Mol Membr Biol 29(5):144–154PubMedCrossRefGoogle Scholar
  99. Spitzer J, Poolman B (2009) The role of biomacromolecular crowding, ionic strength, and physicochemical gradients in the complexities of life’s emergence. Microbiol Mol Biol Rev 73(2):371–388PubMedCrossRefGoogle Scholar
  100. Stadler B, Price AD, Chandrawati R, Hosta-Rigau L, Zelikin AN, Caruso F (2009) Polymer hydrogel capsules: en route toward synthetic cellular systems. Nanoscale 1(1):68–73PubMedCrossRefGoogle Scholar
  101. Strauss MP, Liew AT, Turnbull L, Whitchurch CB, Monahan LG, Harry EJ (2012) 3D-SIM super resolution microscopy reveals a bead-like arrangement for FtsZ and the division machinery: implications for triggering cytokinesis. PLoS Biol 10(9):e1001389PubMedCrossRefGoogle Scholar
  102. Stricker J, Maddox P, Salmon ED, Erickson HP (2002) Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc Natl Acad Sci USA 99(5):3171–3175PubMedCrossRefGoogle Scholar
  103. Szwedziak P, Wang Q, Freund SM, Lowe J (2012) FtsA forms actin-like protofilaments. EMBO J 31(10):2249–2260PubMedCrossRefGoogle Scholar
  104. Takiguchi K, Negishi M, Tanaka-Takiguchi Y, Homma M, Yoshikawa K (2011) Transformation of actoHMM assembly confined in cell-sized liposome. Langmuir 27(18):11528–11535PubMedCrossRefGoogle Scholar
  105. Theberge AB, Courtois F, Schaerli Y, Fischlechner M, Abell C, Hollfelder F, Huck WT (2010) Microdroplets in microfluidics: an evolving platform for discoveries in chemistry and biology. Angew Chem 49(34):5846–5868Google Scholar
  106. Tonthat NK, Arold ST, Pickering BF, Van Dyke MW, Liang S, Lu Y, Beuria TK, Margolin W, Schumacher MA (2011) Molecular mechanism by which the nucleoid occlusion factor, SlmA, keeps cytokinesis in check. EMBO J 30(1):154–164PubMedCrossRefGoogle Scholar
  107. van Oijen AM (2010) Single-molecule approaches to characterizing kinetics of biomolecular interactions. Curr Opin Biotechnol 22(1):75–80PubMedCrossRefGoogle Scholar
  108. Vendeville A, Lariviere D, Fourmentin E (2011) An inventory of the bacterial macromolecular components and their spatial organization. FEMS Microbiol Rev 35(2):395–414PubMedCrossRefGoogle Scholar
  109. Vicente M (2013) Crystal ball: Will test tubes ever undergo division? Microbiol Biotechnol 6:3–16CrossRefGoogle Scholar
  110. Vicente M, Rico AI (2006) The order of the ring: assembly of Escherichia coli cell division components. Mol Microbiol 61(1):5–8PubMedCrossRefGoogle Scholar
  111. Walde P, Cosentino K, Engel H, Stano P (2010) Giant vesicles: preparations and applications. ChemBioChem 11(7):848–865PubMedCrossRefGoogle Scholar
  112. Wilf J, Minton AP (1981) Evidence for protein self-association induced by excluded volume. Myoglobin in the presence of globular proteins. Biochim Biophys Acta 670(3):316–322PubMedCrossRefGoogle Scholar
  113. Wu LJ, Errington J (2012) Nucleoid occlusion and bacterial cell division. Nat Rev Microbiol 10(1):8–12Google Scholar
  114. Zhang B, Zhang Y, Wang Z, Zheng Y (2000) The role of Mg2+ cofactor in the guanine nucleotide exchange and GTP hydrolysis reactions of Rho family GTP-binding proteins. J Biol Chem 275(33):25299–25307PubMedCrossRefGoogle Scholar
  115. Zhou HX (2013) Influence of crowded cellular environments on protein folding, binding, and oligomerization: biological consequences and potentials of atomistic modeling. FEBS Lett. doi:10.1016/j.febslet.2013.01.064 Google Scholar
  116. Zhou HX, Rivas G, Minton AP (2008) Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annu Rev Biophys 37:375–397PubMedCrossRefGoogle Scholar
  117. Zieske K, Schwille P (2012) Reconstitution of pole-to-pole oscillations of min proteins in microengineered polydimethylsiloxane compartments. Angew Chem 52(1):459–462Google Scholar
  118. Zimmerman SB (2006) Shape and compaction of Escherichia coli nucleoids. J Struct Biol 156(2):255–261PubMedCrossRefGoogle Scholar
  119. Zorrilla S, Jimenez M, Lillo P, Rivas G, Minton AP (2004a) Sedimentation equilibrium in a solution containing an arbitrary number of solute species at arbitrary concentrations: theory and application to concentrated solutions of ribonuclease. Biophys Chem 108(1–3):89–100PubMedCrossRefGoogle Scholar
  120. Zorrilla S, Rivas G, Acuna AU, Lillo MP (2004b) Protein self-association in crowded protein solutions: a time-resolved fluorescence polarization study. Protein Sci 13(11):2960–2969PubMedCrossRefGoogle Scholar

Copyright information

© International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Germán Rivas
    • 1
  • Carlos Alfonso
    • 1
  • Mercedes Jiménez
    • 1
  • Begoña Monterroso
    • 1
  • Silvia Zorrilla
    • 2
  1. 1.Centro de Investigaciones Biológicas (CIB)MadridSpain
  2. 2.Instituto de Química Física “Rocasolano” (CSIC)MadridSpain

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