Role of membrane lipids in bacterial division-site selection

Current Opinion in Microbiology

Volumn 8, Issue 2, 2005, Pages 135-142

  Mileykovskaya, Eugenia ^a   Dowhan, William ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CARDIOLIPIN; MEMBRANE LIPID; PHOSPHOLIPID;

BACILLUS SUBTILIS; BACTERIAL MEMBRANE; CELL DIVISION; CELL PROTECTION; DNA REPLICATION; ESCHERICHIA COLI; EUKARYOTIC CELL; GENE MUTATION; LIPID COMPOSITION; LIPID RAFT; MOLECULAR INTERACTION; MOLECULAR MECHANICS; NONHUMAN; POLYMERIZATION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN LOCALIZATION; REVIEW; SCHIZOSACCHAROMYCES POMBE;

EID: 15744398051     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2005.02.012     Document Type: Review

References (46)

1. W. Margolin Themes and variations in prokaryotic cell division FEMS Microbiol Rev 24 2000 531 548
2. W. Dowhan, E. Mileykovskaya, and M. Bogdanov Diversity and versatility of lipid-protein interactions revealed by molecular genetic approaches Biochim Biophys Acta 1666 2004 19 39 The most recent review, several parts of which contain a comprehensive description of the role lipids play in bacterial cell cycle and cell division.
3. S. Rajagopalan, V. Wachtler, and M. Balasubramanian Cytokinesis in fission yeast: a story of rings, rafts and walls Trends Genet 19 2003 403 408 This is a review in which the authors discuss the nature, assembly and maintenance of the actomyosin ring. They clearly emphasize the role of lipid-rafts in yeast cytokinesis.
4. E. Mileykovskaya, and W. Dowhan Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange J Bacteriol 182 2000 1172 1175
5. F. Kawai, M. Shoda, R. Harashima, Y. Sadaie, H. Hara, and K. Matsumoto Cardiolipin domains in Bacillus subtilis marburg membranes J Bacteriol 186 2004 1475 1483 Authors used fluorescent dye 10-N-nonyl acridine orange for visualization of cardiolipin-rich membrane domains in B. subtilis. Enrichment in cardiolipin was found in septal regions and on the cell poles in exponentially growing cells and in engulfment and forespore membranes in the cells in different phases of sporulation. Mutants with a trace amount of cardiolipin exhibited delay in the sporulation process. This is the first report on the role of cardiolipin in sporulation.
6. N. Nanninga Cytokinesis in prokaryotes and eukaryotes: common principles and different solutions Microbiol Mol Biol Rev 65 2001 319 333
7. E. Mileykovskaya, W. Dowhan, R. Birke, D. Zheng, L. Lutterodt, and T.H. Haines Cardiolipin binds nonyl acridine orange by aggregating the dye at exposed hydrophobic domains on bilayer surfaces FEBS Lett 507 2001 187 190
8. P. Gangola, and B.P. Rosen Fura-2 measurements of intracellular [Ca2+] in Escherichia coli Prog Clin Biol Res 252 1988 215 220
9. Dowhan W, Bogdanov M: Functional roles of lipids in membranes. In Biochemistry of Lipids, Lipoproteins and Membranes, vol 36, edn 4. Edited by Vance DE, Vance JE: Elsevier; 2002:1-35.
10. J. Michiels, C. Xi, J. Verhaert, and J. Vanderleyden The functions of Ca(2+) in bacteria: a role for EF-hand proteins? Trends Microbiol 10 2002 87 93
11. P.L. Ferguson, and G.S. Shaw Human S100B protein interacts with the Escherichia coli division protein FtsZ in a calcium-sensitive manner J Biol Chem 279 2004 18806 18813
12. S. Hiraga, C. Ichinose, T. Onogi, H. Niki, and M. Yamazoe Bidirectional migration of SeqA-bound hemimethylated DNA clusters and pairing of oriC copies in Escherichia coli Genes Cells 5 2000 327 341
13. K. Pogliano, J. Pogliano, and E. Becker Chromosome segregation in Eubacteria Curr Opin Microbiol 6 2003 586 593
14. Boeneman K, Crooke E: Chromosomal replication and the cell membrane. Curr Opin Microbiol 2005, 8: in press.
15. T. Mizushima, Y. Ishikawa, E. Obana, M. Hase, T. Kubota, T. Katayama, T. Kunitake, E. Watanabe, and K. Sekimizu Influence of cluster formation of acidic phospholipids on decrease in the affinity for ATP of DnaA protein J Biol Chem 271 1996 3633 3638
16. N. Ichihashi, K. Kurokawa, M. Matsuo, C. Kaito, and K. Sekimizu Inhibitory effects of basic or neutral phospholipid on acidic phospholipid-mediated dissociation of adenine nucleotide bound to DnaA protein, the initiator of chromosomal DNA replication J Biol Chem 278 2003 28778 28786
17. L. Wu, and J. Errington Coordination of cell division and chromosome segregation by a nucleoid occlusion protein in Bacillus subtilis Cell 117 2004 915 925
18. P. Burn Amphitropic proteins: a new class of membrane proteins Trends Biochem Sci 13 1988 79 83
19. J.E. Johnson, and R.B. Cornell Amphitropic proteins: regulation by reversible membrane interactions Mol Membr Biol 16 1999 217 235
20. H. Erickson, D. Taylor, K. Taylor, and D. Bramhill Bacterial cell division protein FtsZ assembles into protofilament sheets and minirings, structural homologs of tubulin polymers Proc Natl Acad Sci USA 93 1996 519 523
21. E. Mileykovskaya, Q. Sun, W. Margolin, and W. Dowhan Localization and function of early cell division proteins in filamentous Escherichia coli cells lacking phosphatidylethanolamine J Bacteriol 180 1998 4252 4257
22. C. Koppelman, M. Aarsman, J. Postmus, E. Pas, A. Muijsers, D. Scheffers, N. Nanninga, and T. den Blaauwen R174 of Escherichia coli FtsZ is involved in membrane interaction and protofilament bundling, and is essential for cell division Mol Microbiol 51 2004 645 657
23. H. Shimada, M. Koizumi, K. Kuroki, M. Mochizuki, H. Fujimoto, H. Ohta, T. Masuda, and K. Takamiya ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase Plant Cell Physiol 45 2004 960 967
24. D. Raychaudhuri ZipA is a MAP-Tau homolog and is essential for structural integrity of the cytokinetic FtsZ ring during bacterial cell division EMBO J 18 1999 2372 2383
25. L. Yim, G. Vandenbussche, J. Mingorance, S. Rueda, M. Casanova, J. Ruysschaert, and M. Vicente Role of the carboxy terminus of Escherichia coli FtsA in self-interaction and cell division J Bacteriol 182 2000 6366 6373
26. B. Geissler, D. Elraheb, and W. Margolin A gain-of-function mutation in ftsA bypasses the requirement for the essential cell division gene zipA in Escherichia coli Proc Natl Acad Sci USA 100 2003 4197 4202
27. M. Sanchez, A. Valencia, M.-J. Ferrandiz, C. Sandler, and M. Vicente Correlation between the structure and biochemical activities of FtsA, an essential cell division protein of the actin family EMBO J 13 1994 4919 4925
28. Z. Hu, E. Gogol, and J. Lutkenhaus Dynamic assembly of MinD on phospholipid vesicles regulated by ATP and MinE Proc Natl Acad Sci USA 99 2002 6761 6766
29. D. Raskin, and P. de Boer Rapid pole-to-pole oscillation of a protein required for directing division to the middle of Escherichia coli Proc Natl Acad Sci USA 96 1999 4971 4976
30. H. Stahlberg, E. Kutejova, K. Muchova, M. Gregorini, A. Lustig, S. Muller, V. Olivieri, A. Engel, A. Wilkinson, and I. Barak Oligomeric structure of the Bacillus subtilis cell division protein DivIVA determined by transmission electron microscopy Mol Microbiol 52 2004 1281 1290
31. E. Harry, and P. Lewis Early targeting of Min proteins to the cell poles in germinated spores of Bacillus subtilis: evidence for division apparatus-independent recruitment of Min proteins to the division site Mol Microbiol 47 2003 37 48
32. T. Szeto, S. Rowland, L. Rothfield, and G. King 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 2002 15693 15698 This paper is the first report that provides evidence that the highly conserved C-terminal motif of MinD is essential for membrane localization of the protein. MinD has the potential to form an amphipathic helix, which usually directly interacts with membrane phospholipids.
33. Z. Hu, and J. Lutkenhaus A conserved sequence at the C-terminus of MinD is required for binding to the membrane and targeting MinC to the septum Mol Microbiol 47 2003 345 355 Authors demonstrated that C-terminal motif of MinD is responsible for MinD and MinC binding to the septum and for MinD binding to liposomes. They also demonstrate by size-exclusion chromatography that the motif is not essential for ATP-induced MinD dimerization in solution. A model for MinD dimer formation based upon the nitrogenase dimer is suggested.
34. H. Zhou, and J. Lutkenhaus Membrane binding by MinD involves insertion of hydrophobic residues within the C-terminal amphipathic helix into the bilayer J Bacteriol 185 2003 4326 4335 This paper demonstrates direct interaction of the C-terminal motif of MinD with lipids. MinD mutants with tryptophan substitutions retained the ability to bind to the membrane and activate MinC. Fluorescence spectroscopy of these mutants demonstrates for the first time the insertion of tryptophan residues into the hydrophobic phase of bilayer.
35. T. Szeto, S. Rowland, C. Habrukowich, and G. King The MinD membrane targeting sequence is a transplantable lipid-binding helix J Biol Chem 278 2003 40050 40056 In this paper authors use CD spectropolarimetry to study synthetic peptides corresponding to C-terminal membrane-targeting sequences (MTS) of E. coli and B. subtilis MinDs. Interactions with liposomes containing anionic phospholipids induce random coil-to-helix transition in the structure of peptides. Using GFP-MTSs the authors found that the BsMTS can localize to the cell membrane, whereas the EcMTS cannot. However, multivalent EcMTS associated stably with the E. coli cell membrane. This result leads to the model of cooperative polymerization of EcMinD on the cell membrane, in which increasing the number of attached ATP-MinDs promotes the gradual increase in the affinity of the multivalent MTS for the membrane. MinE-induced hydrolysis of ATP reverses the process.
36. L. Lackner, D. Raskin, and P. De Boer ATP-dependent interactions between Escherichia coli Min proteins and the phospholipid membrane in vitro J Bacteriol 185 2003 735 749 This paper shows cooperative kinetics of ATP-dependent MinD binding to liposomes. It also demonstrates MinD-dependent recruitment of MinC to the membrane and MinE-stimulated dissociation of MinD and MinC from vesicles.
37. E. Mileykovskaya, I. Fishov, X. Fu, B. Corbin, W. Margolin, and W. Dowhan Effects of phospholipid composition on MinD-membrane interactions in vitro and in vivo J Biol Chem 278 2003 22193 22198 The paper demonstrates cooperative kinetics of ATP-dependent MinD binding to liposomes of different phospholipid composition. A higher affinity of MinD for anionic over zwitterionic phospholipids was found. Aberrant dynamic behavior of GFP-MinD was found in an E. coli mutant with increased anionic phospholipid content due to lack of phosphatidylethanolamine. This paper is the first report indicating that cell division site selection may be dependent on membrane phospholipid composition. It is also the first report of FRET between MinD monomers on a lipid surface, directly indicating MinD oligomerization.
38. K. Suefuji, R. Valluzzi, and D. RayChaudhuri Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE Proc Natl Acad Sci USA 99 2002 16776 16781
39. Y. Shih, T. Le, and L. Rothfield Division site selection in Escherichia coli involves dynamic redistribution of Min proteins within coiled structures that extend between the two cell poles Proc Natl Acad Sci USA 100 2003 7865 7870 Using fluorescence microscopy the authors showed that Min proteins are not randomly distributed in the polar zones of E. coli cells but organized into extended membrane-associated helical structures that wind around the cell between two cell poles. The authors suggest that pole-to-pole oscillation of Min proteins occurs by dynamic redistribution of the proteins within this helical structure.
40. M. Wikstrom, J. Xie, M. Bogdanov, E. Mileykovskaya, P. Heacock, A. Wieslander, and W. Dowhan Monoglucosyldiacylglycerol, a foreign lipid, can substitute for phosphatidylethanolamine in essential membrane-associated functions in Escherichia coli J Biol Chem 279 2004 10484 10493 This report demonstrates that the non-bilayer-prone neutral glycolipid monoglucosyl diacylglycerol (MGlcDAG), synthesized by the MGlcDAG synthase from A. laidlawii in E. coli, corrects functioning of several membrane systems including the division machinery impaired in phosphatidylethanolamine-lacking mutants. Experiments support the essential nature of the non-bilayer properties of MGlcDAG as a substitute for non-bilayer-forming phosphatidylethanolamine as well as the importance of both lipids in dilution of the high anionic lipid surface charge resulting from increased anionic phospholipid content.
41. K. Farsad, N. Ringstad, K. Takei, S.R. Floyd, K. Rose, and P. De Camilli Generation of high curvature membranes mediated by direct endophilin bilayer interactions J Cell Biol 155 2001 193 200
42. V. Norris, C. Woldringh, and E. Mileykovskaya A hypothesis to explain division site selection in Escherichia coli by combining nucleoid occlusion and Min FEBS Lett 561 2004 3 10 The hypothesis is based on the assumption that MinD has a preference for binding to phospholipid tubular structures since it converts round-shaped liposomes into tubes. According to the model, the lipid-protein composition of the mid-cell domain allows formation of phospholipid tubes extending into the cytoplasm, which serve as a substrate for FtsZ binding. It is suggested that disassembly of FtsZ converts the tubes into invagination folds, and the Min system inhibits division by removing these tubes at the cell poles.
43. K. Emoto, and M. Umeda Membrane lipid control of cytokinesis Cell Struct Funct 26 2001 659 665
44. Nishibori A, Kusaka J, Hara H, Umeda M, Matsumoto K: Phosphatidylethanolamine domains and localization of phospholipid synthases in Bacillus subtilis membranes. J Bacteriol 2005, 187: in press. By using a PE-specific peptide probe the authors demonstrated localization of PE in the septum area of B. subtilis membranes and homogeneous distribution of PE along the E. coli membrane. PE was also localized in engulfment membranes of sporulating B. subtilis cells. The majority of GFP-tagged lipid synthases were also localized to the septal area of B. subtilis. Interestingly, PE, CL and lipid synthases were localized as dots along the membrane in filamentous cells lacking Z-rings.
45. Pichoff S, Lutkenhaus J: Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 2005, 49: in press. The authors demonstrate for the first time that a conserved C-terminal amphipathic helix in FtsA, which has the ability to directly interact with membrane phospholipids, is essential for FtsA function in tethering the Z ring to the membrane. The MinD C-terminal amphipathic helix functionally substitutes for this domain of FtsA.
46. C. Lopez, H. Heras, S. Ruzal, C. Sanchez-Rivas, and E. Rivas Variations of the envelope composition of Bacillus subtilis during growth in hyperosmotic medium Curr Microbiol 36 1998 55 61