Toward spatially regulated division of protocells: Insights into the e. coli min system from in vitro studies

Life

Volumn 4, Issue 4, 2014, Pages 915-928

  Kretschmer, Simon ^a   Schwille, Petra ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

Author keywords

Bottom up synthetic biology; Cell division; Membranes; Min proteins; Pattern formation; Protocell; Self organization

Indexed keywords

ESCHERICHIA COLI;

EID: 84922013152     PISSN: None     EISSN: 20751729     Source Type: Journal    
DOI: 10.3390/life4040915     Document Type: Review

References (76)

1. Luisi, P.L.; Ferri, F.; Stano, P. Approaches to semi-synthetic minimal cells: A review. Naturwissenschaften 2006, 93, 1-13.
2. Dzieciol, A.J.; Mann, S. Designs for life: Protocell models in the laboratory. Chem. Soc. Rev. 2012, 41, 79-85.
3. Mushegian, A.R.; Koonin, E.V. A minimal gene set for cellular life derived by comparison of complete bacterial genomes. Proc. Natl. Acad. Sci. USA 1996, 93, 10268-10273.
4. Hutchison, C.A.; Peterson, S.N.; Gill, S.R.; Cline, R.T.; White, O.; Fraser, C.M.; Smith, H.O.; Venter, J.C. Global Transposon Mutagenesis and a Minimal Mycoplasma Genome. Science 1999, 286, 2165-2169.
5. Schwille, P. Bottom-Up Synthetic Biology: Engineering in a Tinkerer's World. Science 2011, 333, 1252-1254.
6. Sole, R.V.; Munteanu, A.; Rodriguez-Caso, C.; Macia, J. Synthetic protocell biology: From reproduction to computation. Philos. Trans. R. Soc. B 2007, 362, 1727-1739.
7. Chen, I.A.; Walde, P. From Self-Assembled Vesicles to Protocells. Cold Spring Harb. Perspect. Biol. 2010, 2, doi:10.1101/cshperspect.a002170.
8. Noireaux, V.; Libchaber, A. A vesicle bioreactor as a step toward an artificial cell assembly. Proc. Natl. Acad. Sci. USA 2004, 101, 17669-17674.
9. Rasmussen, S.; Chen, L.; Nilsson, M.; Abe, S. Bridging nonliving and living matter. Artif. Life 2003, 9, 269-316.
10. Martos, A.; Jimenez, M.; Rivas, G.; Schwille, P. Towards a bottom-up reconstitution of bacterial cell division. Trends Cell Biol. 2012, 22, 634-643.
11. Osawa, M.; Anderson, D.E.; Erickson, H.P. Reconstitution of Contractile FtsZ Rings in Liposomes. Science 2008, 320, 792-794.
12. Vicente, M.; Rico, A.I. The order of the ring: Assembly of Escherichia coli cell division components. Mol. Microbiol. 2006, 61, 5-8.
13. Lutkenhaus, J.; Pichoff, S.; Du, S. Bacterial cytokinesis: From Z ring to divisome. Cytoskeleton 2012, 69, 778-790.
14. Wu, L.J.; Errington, J. Nucleoid occlusion and bacterial cell division. Nat. Rev. Microbiol. 2012, 10, 8-12.
15. Bernhardt, T.G.; de Boer, P.A. SlmA, a Nucleoid-Associated, FtsZ Binding Protein Required for Blocking Septal Ring Assembly over Chromosomes in E. coli. Mol. Cell 2005, 18, 555-564.
16. Dajkovic, A.; Lan, G.; Sun, S.X.; Wirtz, D.; Lutkenhaus, J. MinC Spatially Controls Bacterial Cytokinesis by Antagonizing the Scaffolding Function of FtsZ. Curr. Biol. 2008, 18, 235-244.
17. De Boer, P.A.; Crossley, R.E.; Hand, A.R.; Rothfield, L.I. The MinD protein is a membrane ATPase required for the correct placement of the Escherichia coli division site. EMBO J. 1991, 10, 4371-4380.
18. Hu, Z.; Mukherjee, A.; Pichoff, S.; Lutkenhaus, J. The MinC component of the division site selection system in Escherichia coli interacts with FtsZ to prevent polymerization. Proc. Natl. Acad. Sci. USA 1999, 96, 14819-14824.
19. Hu, Z.; Lutkenhaus, J. Topological Regulation of Cell Division in E. coli: Spatiotemporal Oscillation of MinD Requires Stimulation of Its ATPase by MinE and Phospholipid. Mol. Cell 2001, 7, 1337-1343.
20. Hu, Z.; 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. 1999, 34, 82-90.
21. Raskin, D.M.; 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 1999, 96, 4971-4976.
22. Adler, H.I.; Fisher, W.D.; Cohen, A.; Hardigree, A.A. Miniature Escherichia coli cells deficient in DNA. Proc. Natl. Acad. Sci. USA 1967, 57, 321-326.
23. Loose, M.; Kruse, K.; Schwille, P. Protein Self-Organization: Lessons from the Min System. Annu. Rev. Biophys. 2011, 40, 315-336.
24. Lutkenhaus, J. Min oscillation in bacteria. Adv. Exp. Med. Biol. 2008, 641, 49-61.
25. Shih, Y.L.; Zheng, M. Spatial control of the cell division site by the Min system in Escherichia coli. Environ. Microbiol. 2013, 15, 3229-3239.
26. Hu, Z.; Lutkenhaus, J. Analysis of MinC Reveals Two Independent Domains Involved in Interaction with MinD and FtsZ. J. Bacteriol. 2000, 182, 3965-3971.
27. Cordell, S.C.; Anderson, R.E.; Lowe, J. Crystal structure of the bacterial cell division inhibitor MinC. EMBO J. 2001, 20, 2454-2461.
28. Johnson, J.E.; Lackner, L.L.; de Boer, P.A. Targeting of DMinC/MinD and DMinC/DicB Complexes to Septal Rings in Escherichia coli Suggests a Multistep Mechanism for MinC-Mediated Destruction of Nascent FtsZ Rings. J. Bacteriol. 2002, 184, 2951-2962.
29. Shen, B.; Lutkenhaus, J. Examination of the interaction between FtsZ and MinCN in E. coli suggests how MinC disrupts Z rings. Mol. Microbiol. 2010, 75, 1285-1298.
30. Raskin, D.M.; de Boer, P.A. MinDE-Dependent Pole-to-Pole Oscillation of Division Inhibitor MinC in Escherichia coli. J. Bacteriol. 1999, 181, 6419-6424.
31. Lutkenhaus, J.; Sundaramoorthy, M. MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol. Microbiol. 2003, 48, 295-303.
32. Lackner, L.L.; Raskin, D.M.; de Boer, P.A.J. ATP-Dependent Interactions between Escherichia coli Min Proteins and the Phospholipid Membrane in Vitro. J. Bacteriol. 2003, 185, 735-749.
33. Szeto, T.H.; Rowland, S.L.; Habrukowich, C.L.; King, G.F. The MinD Membrane Targeting Sequence is a Transplantable Lipid-Binding Helix. J. Biol. Chem. 2003, 278, 40050-40056.
34. Szeto, T.H.; Rowland, S.L.; Rothfield, L.I.; 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 2002, 99, 15693-15698.
35. Hu, Z.; Lutkenhaus, J. A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum. Mol. Microbiol. 2003, 47, 345-355.
36. Renner, L.D.; Weibel, D.B. MinD and MinE Interact with Anionic Phospholipids and Regulate Division Plane Formation in Escherichia coli. J. Biol. Chem. 2012, 287, 38835-38844.
37. Ma, L.; King, G.F.; Rothfield, L. Positioning of the MinE binding site on the MinD surface suggests a plausible mechanism for activation of the Escherichia coli MinD ATPase during division site selection. Mol. Microbiol. 2004, 54, 99-108.
38. Ma, L.Y.; King, G.; Rothfield, L. Mapping the MinE Site Involved in Interaction with the MinD Division Site Selection Protein of Escherichia coli. J. Bacteriol. 2003, 185, 4948-4955.
39. Pichoff, S.; Vollrath, B.; Touriol, C.; Bouche, J.P. Deletion analysis of gene minE which encodes the topological specificity factor of cell division in Escherichia coli. Mol. Microbiol. 1995, 18, 321-329.
40. Zhao, C.R.; de Boer, P.A.; Rothfield, L.I. Proper placement of the Escherichia coli division site requires two functions that are associated with different domains of the MinE protein. Proc. Natl. Acad. Sci. USA 1995, 92, 4313-4317.
41. Wu, W.; Park, K.T.; Holyoak, T.; Lutkenhaus, J. Determination of the structure of the MinD-ATP complex reveals the orientation of MinD on the membrane and the relative location of the binding sites for MinE and MinC. Mol. Microbiol. 2011, 79, 1515-1528.
42. Hsieh, C.W.; Lin, T.Y.; Lai, H.M.; Lin, C.C.; Hsieh, T.S.; Shih, Y.L. Direct MinE-membrane interaction contributes to the proper localization of MinDE in E. coli. Mol. Microbiol. 2010, 75, 499-512.
43. Park, K.T.; Wu, W.; Battaile, K.P.; Lovell, S.; Holyoak, T.; Lutkenhaus, J. The Min Oscillator Uses MinD-Dependent Conformational Changes in MinE to Spatially Regulate Cytokinesis. Cell 2011, 146, 396-407.
44. Ghasriani, H.; Ducat, T.; Hart, C.T.; Hafizi, F.; Chang, N.; Al-Baldawi, A.; Ayed, S.H.; Lundstrom, P.; Dillon, J.A.; Goto, N.K.; et al. Appropriation of the MinD protein-interaction motif by the dimeric interface of the bacterial cell division regulator MinE. Proc. Natl. Acad. Sci. USA 2010, 107, 18416-18421.
45. Kang, G.B.; Song, H.E.; Kim, M.K.; Youn, H.S.; Lee, J.G.; An, J.Y.; Chun, J.S.; Jeon, H.; Eom, S.H. Crystal structure of Helicobacter pylori MinE, a cell division topological specificity factor. Mol. Microbiol. 2010, 76, 1222-1231.
46. King, G.F.; Shih, Y.L.; Maciejewski, M.W.; Bains, N.P.; Pan, B.; Rowland, S.L.; Mullen, G.P.; Rothfield, L.I. Structural basis for the topological specificity function of MinE. Nat. Struct. Biol. 2000, 7, 1013-1017.
47. Zheng, M.; Chiang, Y.L.; Lee, H.L.; Kong, L.R.; Hsu, S.T.; Hwang, I.S.; Rothfield, L.I.; Shih, Y.L. Self-Assembly of MinE on the Membrane Underlies Formation of the MinE Ring to Sustain Function of the Escherichia coli Min System. J. Biol. Chem. 2014, 289, 21252-21266.
48. Hale, C.A.; Meinhardt, H.; de Boer, P.A. Dynamic localization cycle of the cell division regulator MinE in Escherichia coli. EMBO J. 2001, 20, 1563-1572.
49. Raskin, D.M.; de Boer, P.A. The MinE Ring: An FtsZ-Independent Cell Structure Required for Selection of the Correct Division Site in E. coli. Cell 1997, 91, 685-694.
50. Jia, S.; Keilberg, D.; Hot, E.; Thanbichler, M.; Sogaard-Andersen, L.; Lenz, P. Effect of the Min System on Timing of Cell Division in Escherichia coli. PLoS One 2014, 9, doi:10.1371/ journal.pone.0103863.
51. Di Ventura, B.; Knecht, B.; Andreas, H.; Godinez, W.J.; Fritsche, M.; Rohr, K.; Nickel, W.; Heermann, D.W.; Sourjik, V. Chromosome segregation by the Escherichia coli Min system. Mol. Syst. Biol. 2013, 9, doi:10.1038/msb.2013.44.
52. Loose, M.; Fischer-Friedrich, E.; Ries, J.; Kruse, K.; Schwille, P. Spatial Regulators for Bacterial Cell Division Self-Organize into Surface Waves in Vitro. Science 2008, 320, 789-792.
53. Camazine, S. Self-Organization in Biological Systems; Princeton University Press: Princeton, NJ, USA, 2001.
54. Nettesheim, S.; Vonoertzen, A.; Rotermund, H.H.; Ertl, G. Reaction-diffusion patterns in the catalytic CO oxidation on Pt(110): Front propagation and spiral waves. J. Chem. Phys. 1993, 98, 9977-9985.
55. Sagues, F.; Epstein, I.R. Nonlinear chemical dynamics. Dalton Trans. 2003, doi:10.1039/B210932H.
56. Martos, A.; Petrasek, Z.; Schwille, P. Propagation of MinCDE waves on free-standing membranes. Environ. Microbiol. 2013, 15, 3319-3326.
57. Schweizer, J.; Loose, M.; Bonny, M.; Kruse, K.; Monch, I.; Schwille, P. Geometry sensing by self-organized protein patterns. Proc. Natl. Acad. Sci. USA 2012, 109, 15283-15288.
58. Zieske, K.; Schwille, P. Reconstitution of Pole-to-Pole Oscillations of Min proteins in Microengineered Polydimethylsiloxane Compartments. Angew. Chem. 2013, 52, 459-462.
59. Meacci, G.; Kruse, K. Min-oscillations in Escherichia coli induced by interactions of membrane-bound proteins. Phys. Biol. 2005, 2, 89-97.
60. Loose, M.; Fischer-Friedrich, E.; Herold, C.; Kruse, K.; Schwille, P. Min protein patterns emerge from rapid rebinding and membrane interaction of MinE. Nat. Struct. Mol. Biol. 2011, 18, 577-583.
61. Przybylo, M.; Sykora, J.; Humpolickova, J.; Benda, A.; Zan, A.; Hof, M. Lipid Diffusion in Giant Unilamellar Vesicles is More than 2 Times Faster than in Supported Phospholipid Bilayers under Identical Conditions. Langmuir 2006, 22, 9096-9099.
62. Ivanov, V.; Mizuuchi, K. Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins. Proc. Natl. Acad. Sci. USA 2010, 107, 8071-8078.
63. Vecchiarelli, A.G.; Li, M.; Mizuuchi, M.; Mizuuchi, K. Differential affinities of MinD and MinE to anionic phospholipid influence Min patterning dynamics in vitro. Mol. Microbiol. 2014, 93, 453-463.
64. Corbin, B.D.; Yu, X.C.; Margolin, W. Exploring intracellular space: Function of the Min system in round-shaped Escherichia coli. EMBO J. 2002, 21, 1998-2008.
65. Fu, X.; Shih, Y.L.; Zhang, Y.; Rothfield, L.I. The MinE ring required for proper placement of the division site is a mobile structure that changes its cellular location during the Escherichia coli division cycle. Proc. Natl. Acad. Sci. USA 2001, 98, 980-985.
66. Zieske, K.; Schweizer, J.; Schwille, P. Surface topology assisted alignment of Min protein waves. FEBS Lett. 2014, 588, 2545-2549.
67. Rivas, G.; Vogel, S.K.; Schwille, P. Reconstitution of cytoskeletal protein assemblies for large-scale membrane transformation. Curr. Opin. Chem. Biol. 2014, 22, 18-26.
68. Osawa, M.; Erickson, H.P. Liposome division by a simple bacterial division machinery. Proc. Natl. Acad. Sci. USA 2013, 110, 11000-11004.
69. Loose, M.; Mitchison, T.J. The bacterial cell division proteins FtsA and FtsZ self-organize into dynamic cytoskeletal patterns. Nat. Cell Biol. 2014, 16, 38-46.
70. Schwille, P. Bacterial Cell Division: A Swirling Ring to Rule Them All? Curr. Biol. 2014, 24, R157-R159.
71. Arumugam, S.; Petrasek, Z.; Schwille, P. MinCDE exploits the dynamic nature of FtsZ filaments for its spatial regulation. Proc. Natl. Acad. Sci. USA 2014, 111, E1192-E1200.
72. Zieske, K.; Schwille, P. Reconstitution of self-organizing protein gradients as spatial cues in cell-free systems. eLife 2014, 3, doi:10.7554/eLife.03949.
73. Arumugam, S.; Chwastek, G.; Fischer-Friedrich, E.; Ehrig, C.; Monch, I.; Schwille, P. Surface Topology Engineering of Membranes for the Mechanical Investigation of the Tubulin Homologue FtsZ. Angew. Chem. 2012, 51, 11858-11862.
74. Van Swaay, D.; de Mello, A. Microfluidic methods for forming liposomes. Lab Chip 2013, 13, 752-767.
75. Pautot, S.; Frisken, B.J.; Weitz, D.A. Engineering asymmetric vesicles. Proc. Natl. Acad. Sci. USA 2003, 100, 10718-10721.
76. Stachowiak, J.C.; Richmond, D.L.; Li, T.H.; Liu, A.P.; Parekh, S.H.; Fletcher, D.A. Unilamellar vesicle formation and encapsulation by microfluidic jetting. Proc. Natl. Acad. Sci. USA 2008, 105, 4697-4702.