Biomimetic membrane systems to study cellular organization

Journal of Structural Biology

Volumn 168, Issue 1, 2009, Pages 143-151

  Loose, Martin ^a,b   Schwille, Petra ^a,b  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

Author keywords

Actin based motility; Bacterial cytoskeleton; Cytoskeleton; Membrane; Reaction diffusion

Indexed keywords

ACTIN; BINDING PROTEIN; CELL EXTRACT; FTSZ PROTEIN; LIPID; TUBULIN;

ACTIN POLYMERIZATION; ARTICLE; BACTERIAL CELL; CAULOBACTER CRESCENTUS; CELL DIVISION; CELL INTERACTION; CELL MEMBRANE; CELL MOTILITY; CONFORMATIONAL TRANSITION; CYTOSKELETON; ESCHERICHIA COLI; IN VITRO STUDY; LIPID BILAYER; LIPID MEMBRANE; MEMBRANE VESICLE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROKARYOTE; PROTEIN BINDING;

ACTINS; ANIMALS; CELL MEMBRANE; CYTOSKELETON; HUMANS; LIPID BILAYERS; MEMBRANE PROTEINS; MEMBRANES, ARTIFICIAL; MODELS, THEORETICAL;

BACTERIA (MICROORGANISMS);

EID: 69249215233     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2009.03.016     Document Type: Article

References (104)

1. Adler H., Fisher W., Cohen A., and Hardigree A. Miniature Escherichia coli cell deficient in DNA. Proc. Natl. Acad. Sci. USA 57 2 (1967) 321-326
2. Akin O., and Mullins R.D. Capping protein increases the rate of actin-based motility by promoting filament nucleation by the Arp2/3 complex. Cell 133 5 (2008) 841-851
3. Allard J.F., and Cytrynbaum E.N. Force generation by a dynamic Z-ring in Escherichia coli cell division. Proc. Natl. Acad. Sci. USA 106 1 (2009) 145-150
4. Anderson D.E., Gueiros-Filho F.J., and Erickson H.P. Assembly dynamics of FtsZ rings in Bacillus subtilis and Escherichia coli and effects of FtsZ-regulating proteins. J. Bacteriol. 186 17 (2004) 5775-5781
5. Athale C., Dinarina A., Mora-Coral M., Pugieux C., Nedelec F., and Karsenti E. Regulation of microtubule dynamics by reaction cascades around chromosomes. Science 322 5905 (2008) 1243-1247
6. Ausmees N., Kuhn J., and Jacobs-Wagner C. The bacterial cytoskeleton an intermediate filament-like function in cell shape. Cell 115 (2003) 705-713
7. Bacia K., Scherfeld D., Kahya N., and Schwille P. Fluorescence correlation spectroscopy relates rafts in model and native membranes. Biophys. J. 87 2 (2004) 1034-1043
8. Bastiaens P., Caudron M., Niethammer P., and Karsenti E. Gradients in the self-organization of the mitotic spindle. Trends Cell Biol. 16 3 (2006) 125-134
9. Begg K., Nikolaichik Y., Crossland N., and Donachie W.D. Roles of FtsA and FtsZ in activation of division sites. J. Bacteriol. 180 4 (1998) 881-884
10. Bernheim-Groswasser A., Wiesner S., Golsteyn R.M., Carlier M.-F., and Sykes C. The dynamics of actin-based motility depend on surface parameters. Nature 417 6886 (2002) 308-311
11. Bi E.F., and Lutkenhaus J. FtsZ ring structure associated with division in Escherichia coli. Nature 354 6349 (1991) 161-164
12. Bork P., Sander C., and Valencia A. An ATPase domain common to prokaryotic cell cycle proteins, sugar kinases, actin, and hsp70 heat shock proteins. Proc. Natl. Acad. Sci. USA 89 16 (1992) 7290-7294
13. Boukellal H., Campas O., Joanny J.-F., Prost J., and Sykes C. Soft listeria: actin-based propulsion of liquid drops. Phys. Rev. E 69 6 Pt 1 (2004) 061906
14. Brian A.A., and McConnell H.M. Allogeneic stimulation of cytotoxic T cells by supported planar membranes. Proc. Natl. Acad. Sci. USA 81 19 (1984) 6159-6163
15. Bugyi B., Clainche C.L., Romet-Lemonne G., and Carlier M.-F. How do in vitro reconstituted actin-based motility assays provide insight into in vivo behavior?. FEBS Lett. 582 14 (2008) 2086-2092
16. Cameron L.A., Footer M.J., van Oudenaarden A., and Theriot J.A. Motility of ActA protein-coated microspheres driven by actin polymerization. Proc. Natl. Acad. Sci. USA 96 9 (1999) 4908-4913
17. Carlier M.F., and Pantaloni D. Control of actin dynamics in cell motility. J. Mol. Biol. 269 4 (1997) 459-467
18. Caudron M., Bunt G., Bastiaens P., and Karsenti E. Spatial coordination of spindle assembly by chromosome-mediated signaling gradients. Science 309 5739 (2005) 1373-1376
19. Chhabra E.S., and Higgs H.N. The many faces of actin: matching assembly factors with cellular structures. Nat. Cell Biol. 9 10 (2007) 1110-1121
20. Co C., Wong D.T., Gierke S., Chang V., and Taunton J. Mechanism of actin network attachment to moving membranes: barbed end capture by N-WASP WH2 domains. Cell 128 5 (2007) 901-913
21. Crane J.M., and Tamm L.K. Fluorescence microscopy to study domains in supported lipid bilayers. Methods Mol. Biol. 400 (2007) 481-488
22. Dai K., and Lutkenhaus J. The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J. Bacteriol. 174 19 (1992) 6145-6151
23. Dajkovic A., and Lutkenhaus J. Z ring as executor of bacterial cell division. J. Mol. Microbiol. Biotechnol. 11 3-5 (2006) 140-151
24. Daniels B.R., Perkins E.M., Dobrowsky T.M., Sun S.X., and Wirtz D. Asymmetric enrichment of Pie-1 in the Caenorhabditis elegans zygote mediated by binary counter diffusion. J. Cell Biol. 184 4 (2009) 473-479
25. de Boer P.A., Crossley R.E., Hand A.R., and Rothfield L.I. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 10 13 (1991) 4371-4380
26. de Boer P.A., Crossley R.E., and Rothfield L.I. 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 4 (1989) 641-649
27. Delatour V., Helfer E., Didry D., Le K.H.D., Gaucher J.-F., Carlier M.-F., and Romet-Lemonne G. Arp2/3 controls the motile behavior of N-WASP-functionalized GUVs and modulates N-WASP surface distribution by mediating transient links with actin filaments. Biophys. J. 94 12 (2008) 4890-4905
28. Doherty G.J., and McMahon H.T. Mediation, modulation, and consequences of membrane-cytoskeleton interactions. Annu. Rev. Biophys. 37 (2008) 65-95
29. Doubrovinski K., and Kruse K. Cytoskeletal waves in the absence of molecular motors. EPL-Europhys. Lett. 83 1 (2008) 18003
30. Fischer-Friedrich E., van Yen R.N., and Kruse K. Surface waves of min-proteins. Phys. Biol. 4 1 (2007) 38-47
31. Fujiwara T., Ritchie K., Murakoshi H., Jacobson K., and Kusumi A. Phospholipids undergo hop diffusion in compartmentalized cell membrane. J. Cell Biol. 157 6 (2002) 1071-1081
32. Ghosh B., and Sain A. Origin of contractile force during cell division of bacteria. Phys. Rev. Lett. 101 17 (2008) 178101
33. Giardini P.A., Fletcher D.A., and Theriot J.A. Compression forces generated by actin comet tails on lipid vesicles. Proc. Natl. Acad. Sci. USA 100 11 (2003) 6493-6498
34. Groves J.T., Parthasarathy R., and Forstner M.B. Fluorescence imaging of membrane dynamics. Annu. Rev. Biomed. Eng. 10 (2008) 311-338
35. Hale C.A., Meinhardt H., and de Boer P.A. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J. 20 7 (2001) 1563-1572
36. Heuvingh J., Franco M., Chavrier P., and Sykes C. Arf1-mediated actin polymerization produces movement of artificial vesicles. Proc. Natl. Acad. Sci. USA 104 43 (2007) 16928-16933
37. Higgs H.N., and Pollard T.D. Activation by Cdc42 and PIP(2) of Wiskott-Aldrich syndrome protein (WASP) stimulates actin nucleation by Arp2/3 complex. J. Cell Biol. 150 6 (2000) 1311-1320
38. Howard M., Rutenberg A.D., and de Vet S. Dynamic compartmentalization of bacteria: accurate division in E. coli. Phys. Rev. Lett. 87 27 Pt 1 (2001) 278102
39. Hu Z., Gogol E.P., and Lutkenhaus J. Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE. Proc. Natl. Acad. Sci. USA 99 10 (2002) 6761-6766
40. Hu Z., and Lutkenhaus J. Topological regulation of cell division in Escherichia coli involves rapid pole to pole oscillation of the division inhibitor minc under the control of MinD and MinE. Mol. Microbiol. 34 1 (1999) 82-90
41. Hu Z., and Lutkenhaus J. Topological regulation of cell division in E. coli. Spatiotemporal oscillation of MinD requires stimulation of its ATPase and MinE and phospholipid. Mol. Cell 7 6 (2001) 1337-1343
42. Huang K.C., Meir Y., and Wingreen N.S. Dynamic structures in Escherichia coli: spontaneous formation of MinE rings and MinD polar zones. Proc. Natl. Acad. Sci. USA 100 22 (2003) 12724-12728
43. Iijima M., Huang Y.E., and Devreotes P. Temporal and spatial regulation of chemotaxis. Dev. Cell 3 4 (2002) 469-478
44. Janmey P.A., and Lindberg U. Cytoskeletal regulation: rich in lipids. Nat. Rev. Mol. Cell. Biol. 5 8 (2004) 658-666
45. Janshoff A., and Steinem C. Scanning force microscopy of artificial membranes. ChemBioChem 2 11 (2001) 798-808
46. Jones L., Carballido-Lopez R., and Errington J. Control of cell shape in bacteria helical, actin-like filaments in Bacillus subtilis. Cell 104 6 (2001) 913-922
47. Karsenti E. Self-organization in cell biology: a brief history. Nat. Rev. Mol. Cell biol. 9 3 (2008) 255-262
48. Kruse K. A dynamic model for determining the middle of Escherichia coli. Biophys. J. 82 2 (2002) 618-627
49. Kruse K., Howard M., and Margolin W. An experimentalist's guide to computational modelling of the min system. Mol. Microbiol. 63 5 (2007) 1279-1284
50. Lackner L.L., Raskin D.M., and de Boer P.A.J. ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro. J. Bacteriol. 185 3 (2003) 735-749
51. Lan G., Daniels B.R., Dobrowsky T.M., Wirtz D., and Sun S.X. Condensation of FtsZ filaments can drive bacterial cell division. Proc. Natl. Acad. Sci. USA 106 1 (2009) 121-126
52. Leaver M., Dominguez-Cuevas P., Coxhead J.M., Daniel R.A., and Errington J. Life without a wall or division machine in Bacillus subtilis. Nature 457 7231 (2009) 849-853
53. Li Z., Trimble M.J., Brun Y.V., and Jensen G.J. The structure of FtsZ filaments in vivo suggests a force-generating role in cell division. EMBO J. 26 22 (2007) 4694-4708
54. Liu A.P., and Fletcher D.A. Actin polymerization serves as a membrane domain switch in model lipid bilayers. Biophys. J. 91 11 (2006) 4064-4070
55. Loose M., Fischer-Friedrich E., Ries J., Kruse K., and Schwille P. Spatial regulators for bacterial cell division self-organize into surface waves in vitro. Science 320 5877 (2008) 789-792
56. Loewe J., and Amos L.A. Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int. J. Biochem. Cell Biol. 41 2 (2009) 323-329
57. Loewe J., van den Ent F., and Amos L.A. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33 (2004) 177-198
58. Lu C., Reedy M., and Erickson H. Straight and curved conformations of FtsZ are regulated by GTP hydrolysis. J. Bacteriol. 182 1 (2000) 164-170
59. Lutkenhaus J. Assembly dynamics of the bacterial mincde system and spatial regulation of the Z-ring. Annu. Rev. Biochem. 76 (2007) 539-562
60. Manahan C.L., Iglesias P.A., Long Y., and Devreotes P.N. Chemoattractant signaling in dictyostelium discoideum. Annu. Rev. Cell Dev. Biol. 20 (2004) 223-253
61. Margolin W. Ftsz and the division of prokaryotic cells and organelles. Nat. Rev. Mol. Cell Biol. 6 11 (2005) 862-871
62. McMahon H.T., and Gallop J.L. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438 7068 (2005) 590-596
63. Meacci G., and Kruse K. Min-oscillations in Escherichia coli induced by interactions of membrane-bound proteins. Phys. Biol. 2 1-2 (2005) 89-97
64. Meacci G., Ries J., Fischer-Friedrich E., Kahya N., Schwille P., and Kruse K. Mobility of min-proteins in Escherichia coli measured by fluorescence correlation spectroscopy. Phys. Biol. 3 4 (2006) 255-263
65. Meinhardt H., and de Boer P.A. Pattern formation in Escherichia coli: a model for the pole-to-pole oscillations of Min proteins and the localization of the division site. Proc. Natl. Acad. Sci. USA 98 25 (2001) 14202-14207
66. Meyers J., Craig J., and Odde D.J. Potential for control of signaling pathways via cell size and shape. Curr. Biol. 16 17 (2006) 1685-1693
67. Michie K.A., and Loewe J. Dynamic filaments of the bacterial cytoskeleton. Annu. Rev. Biochem. 75 (2006) 467-492
68. Mingeot-Leclercq M.-P., Deleu M., Brasseur R., and Dufrene Y.F. Atomic force microscopy of supported lipid bilayers. Nat. Protoc. 3 10 (2008) 1654-1659
69. Misteli T. The concept of self-organization in cellular architecture. J. Cell Biol. 155 2 (2001) 181-185
70. Mogilner A. On the edge: modeling protrusion. Curr. Opin. Cell Biol. 18 1 (2006) 32-39
71. Nabi I.R. The polarization of the motile cell. J. Cell Sci. 112 Pt 12 (1999) 1803-1811
72. Neves S.R., Tsokas P., Sarkar A., Grace E.A., Rangamani P., Taubenfeld S.M., Alberini C.M., Schaff J.C., Blitzer R.D., Moraru I.I., and Iyengar R. Cell shape and negative links in regulatory motifs together control spatial information flow in signaling networks. Cell 133 4 (2008) 666-680
73. Oliva M.A., Cordell S.C., and Loewe J. Structural insights into FtsZ protofilament formation. Nat. Struct. Mol. Biol. 11 12 (2004) 1243-1250
74. Osawa M., Anderson D.E., and Erickson H.P. Reconstitution of contractile FtsZ rings in liposomes. Science 320 5877 (2008) 792-794
75. Paolo G.D., and Camilli P.D. Phosphoinositides in cell regulation and membrane dynamics. Nature 443 7112 (2006) 651-657
76. Papayannopoulos V., Co C., Prehoda K.E., Snapper S., Taunton J., and Lim W.A. A polybasic motif allows N-WASP to act as a sensor of PIP(2) density. Mol. Cell. 17 2 (2005) 181-191
77. Pichoff S., and Lutkenhaus J. Unique and overlapping roles for ZipA and FtsA in septal ring assembly in Escherichia coli. EMBO J. 21 4 (2002) 685-693
78. Pichoff S., and Lutkenhaus J. Tethering the Z-ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol. Microbiol. 55 6 (2005) 1722-1734
79. Pollard T.D., and Borisy G.G. Cellular motility driven by assembly and disassembly of actin filaments. Cell 112 4 (2003) 453-465
80. Przybylo M., Sykora J., Humpolickova J., Benda A., Zan A., and Hof M. Lipid diffusion in giant unilamellar vesicles is more than 2 times faster than in supported phospholipid bilayers under identical conditions. Langmuir 22 22 (2006) 9096-9099
81. Raskin D.M., and de Boer P.A. MinDE-dependent pole-to-pole oscillation of division inhibitor minc in Escherichia coli. J. Bacteriol. 181 20 (1999) 6419-6424
82. Raskin D.M., and de Boer P.A. Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli. Proc. Natl. Acad. Sci. USA 96 9 (1999) 4971-4976
83. Richter R.P., Berat R., and Brisson A.R. Formation of solid-supported lipid bilayers: an integrated view. Langmuir 22 8 (2006) 3497-3505
84. Richter R.P., and Brisson A.R. Following the formation of supported lipid bilayers on mica: a study combining AFM, QCM-D, and ellipsometry. Biophys. J. 88 5 (2005) 3422-3433
85. Rohatgi R., Ho H.Y., and Kirschner M.W. Mechanism of N-WASP activation by Cdc42 and phosphatidylinositol 4, 5-bisphosphate. J. Cell. Biol. 150 6 (2000) 1299-1310
86. Sackmann E. Supported membranes: scientific and practical applications. Science 271 5245 (1996) 43-48
87. Sackmann E., and Tanaka M. Supported membranes on soft polymer cushions: fabrication, characterization and applications. Trends Biotechnol. 18 2 (2000) 58-64
88. Scherfeld D., Kahya N., and Schwille P. Lipid dynamics and domain formation in model membranes composed of ternary mixtures of unsaturated and saturated phosphatidylcholines and cholesterol. Biophys. J. 85 6 (2003) 3758-3768
89. Sens P., Johannes L., and Bassereau P. Biophysical approaches to protein-induced membrane deformations in trafficking. Curr. Opin. Cell Biol. 20 4 (2008) 476-482
90. Stricker J., Maddox P., Salmon E., and Erickson H. Rapid assembly dynamics of the Escherichia coli FtsZ-ring demonstrated by fluorescence recovery after photobleaching. Proc. Natl. Acad. Sci. USA 99 (2002) 3171-3175
91. Suefuji K., Valluzz R., and RayChaudhuri D. Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE. Proc. Natl. Acad. Sci. USA 99 (2002) 16776-16781
92. Svitkina T.M., and Borisy G.G. Arp2/3 complex and actin depolymerizing factor/cofilin in dendritic organization and treadmilling of actin filament array in lamellipodia. J. Cell Biol. 145 5 (1999) 1009-1026
93. Szeto T.H., Rowland S.L., Rothfield L.I., and King G.F. Membrane localization of MinD is mediated by a C-terminal motif that is conserved across eubacteria, archaea, and chloroplasts. Proc. Natl. Acad. Sci. USA 99 24 (2002) 15693-15698
94. Takenawa T., and Suetsugu S. The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat. Rev. Mol. Cell Biol. 8 1 (2007) 37-48
95. Tamm L.K., and McConnell H.M. Supported phospholipid bilayers. Biophys. J. 47 1 (1985) 105-113
96. Thanbichler M., and Shapiro L. Getting organized-how bacterial cells move proteins and DNA. Nat. Rev. Microbiol. 6 1 (2008) 28-40
97. Trichet L., Campas O., Sykes C., and Plastino J. VASP governs actin dynamics by modulating filament anchoring. Biophys. J. 92 3 (2007) 1081-1089
98. Turing A. The chemical basis for morphogenesis. Philos. Trans. R. Soc. Lond. B 237 (1952) 37
99. Upadhyaya A., Chabot J.R., Andreeva A., Samadani A., and van Oudenaarden A. Probing polymerization forces by using actin-propelled lipid vesicles. Proc. Natl. Acad. Sci. USA 100 8 (2003) 4521-4526
100. Upadhyaya A., and van Oudenaarden A. Biomimetic systems for studying actin-based motility. Curr. Biol. 13 18 (2003) R734-R744
101. Wagner M.L., and Tamm L.K. Tethered polymer-supported planar lipid bilayers for reconstitution of integral membrane proteins: silane-polyethyleneglycol-lipid as a cushion and covalent linker. Biophys. J. 79 3 (2000) 1400-14014
102. Weiner O.D., Marganski W.A., Wu L.F., Altschuler S.J., and Kirschner M.W. An actin-based wave generator organizes cell motility. PLoS Biol. 5 9 (2007) e221
103. Wiesner S., Helfer E., Didry D., Ducouret G., Lafuma F., Carlier M.-F., and Pantaloni D. A biomimetic motility assay provides insight into the mechanism of actin-based motility. J. Cell Biol. 160 3 (2003) 387-398
104. Yarar D., To W., Abo A., and Welch M.D. The Wiskott-Aldrich syndrome protein directs actin-based motility by stimulating actin nucleation with the Arp2/3 complex. Curr. Biol. 9 10 (1999) 555-558