Collaborative protein filaments

EMBO Journal

Volumn 34, Issue 18, 2015, Pages 2312-2320

  Ghosal, Debnath ^a,b   Löwe, Jan ^a  

^a MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^b CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

actin tubulin cytoskeleton; bacterial cytoskeleton; cytomotive; DNA membrane assisted filaments; matrix assisted filaments

Indexed keywords

COLLABORATIVE PROTEIN FILAMENT; CYTOSKELETON PROTEIN; DAN FILAMENT; DIVIVA PROTEIN; DNA; DYNAMIN; FTSA PROTEIN; FTSZ PROTEIN; MINCD PROTEIN; RECA PROTEIN; UNCLASSIFIED DRUG; BACTERIAL DNA; BACTERIAL PROTEIN;

CELL DIVISION; CELL WALL; CHROMOSOME SEGREGATION; CYTOKINESIS; CYTOSKELETON; DNA REPAIR; EUKARYOTE; GENE SILENCING; LIPID MEMBRANE; NOMENCLATURE; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FAMILY; PROTEIN FUNCTION; REVIEW; BACTERIUM; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY;

BACTERIA; BACTERIAL PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; CYTOSKELETON; DNA REPAIR; DNA, BACTERIAL; GENE SILENCING; HUMANS;

EID: 84941734569     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201591756     Document Type: Review

References (61)

1. Alushin GM, Lander GC, Kellogg EH, Zhang R, Baker D, Nogales E, (2014) High-resolution microtubule structures reveal the structural transitions in alphabeta-tubulin upon GTP hydrolysis. Cell 157: 1117-1129
2. Ausmees N, Kuhn JR, Jacobs-Wagner C, (2003) The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115: 705-713
3. van Baarle S, Celik IN, Kaval KG, Bramkamp M, Hamoen LW, Halbedel S, (2013) Protein-protein interaction domains of Bacillus subtilis DivIVA. J Bacteriol 195: 1012-1021
4. Bharat TA, Murshudov GN, Sachse C, Löwe J, (2015) Structures of actin-like ParM filaments show architecture of plasmid-segregating spindles. Nature 523: 106-110
5. Bowen JR, Hwang D, Bai X, Roy D, Spiliotis ET, (2011) Septin GTPases spatially guide microtubule organization and plus end dynamics in polarizing epithelia. J Cell Biol 194: 187-197
6. Bramkamp M, (2012) Structure and function of bacterial dynamin-like proteins. Biol Chem 393: 1203-1214
7. Cho H, McManus HR, Dove SL, Bernhardt TG, (2011) Nucleoid occlusion factor SlmA is a DNA-activated FtsZ polymerization antagonist. Proc Natl Acad Sci USA 108: 3773-3778
8. Dai K, Lutkenhaus J, (1992) The proper ratio of FtsZ to FtsA is required for cell division to occur in Escherichia coli. J Bacteriol 174: 6145-6151
9. Dame RT, Luijsterburg MS, Krin E, Bertin PN, Wagner R, Wuite GJ, (2005) DNA bridging: a property shared among H-NS-like proteins. J Bacteriol 187: 1845-1848
10. Dunn K, Chrysogelos S, Griffith J, (1982) Electron microscopic visualization of recA-DNA filaments: evidence for a cyclic extension of duplex DNA. Cell 28: 757-765
11. von der Ecken J, Muller M, Lehman W, Manstein DJ, Penczek PA, Raunser S, (2015) Structure of the F-actin-tropomyosin complex. Nature 519: 114-117
12. Edwards DH, Errington J, (1997) The Bacillus subtilis DivIVA protein targets to the division septum and controls the site specificity of cell division. Mol Microbiol 24: 905-915
13. van den Ent F, Izore T, Bharat TA, Johnson CM, Löwe J, (2014) Bacterial actin MreB forms antiparallel double filaments. Elife 3: e02634
14. Fink G, Löwe J, (2015) Reconstitution of a prokaryotic minus end-tracking system using TubRC centromeric complexes and tubulin-like protein TubZ filaments. Proc Natl Acad Sci USA, 112: E1845-E1850
15. Flory J, Tsang SS, Muniyappa K, (1984) Isolation and visualization of active presynaptic filaments of recA protein and single-stranded DNA. Proc Natl Acad Sci USA 81: 7026-7030
16. Gayathri P, Fujii T, Moller-Jensen J, van den Ent F, Namba K, Löwe J, (2012) A bipolar spindle of antiparallel ParM filaments drives bacterial plasmid segregation. Science 338: 1334-1337
17. Ghosal D, Trambaiolo D, Amos LA, Löwe J, (2014) MinCD cell division proteins form alternating copolymeric cytomotive filaments. Nat Commun 5: 5341
18. Hester CM, Lutkenhaus J, (2007) Soj (ParA) DNA binding is mediated by conserved arginines and is essential for plasmid segregation. Proc Natl Acad Sci USA 104: 20326-20331
19. Howard M, Gerdes K, (2010) What is the mechanism of ParA-mediated DNA movement? Mol Microb iol 78: 9-12
20. Hu Z, Saez C, Lutkenhaus J, (2003) Recruitment of MinC, an inhibitor of Z-ring formation, to the membrane in Escherichia coli: role of MinD and MinE. J Bacteriol 185: 196-203
21. Hui MP, Galkin VE, Yu X, Stasiak AZ, Stasiak A, Waldor MK, Egelman EH, (2010) ParA2, a Vibrio cholerae chromosome partitioning protein, forms left-handed helical filaments on DNA. Proc Natl Acad Sci USA 107: 4590-4595
22. Ivanov V, Mizuuchi K, (2010) Multiple modes of interconverting dynamic pattern formation by bacterial cell division proteins. Proc Natl Acad Sci USA 107: 8071-8078
23. Lara B, Rico AI, Petruzzelli S, Santona A, Dumas J, Biton J, Vicente M, Mingorance J, Massidda O, (2005) Cell division in cocci: localization and properties of the Streptococcus pneumoniae FtsA protein. Mol Microbiol 55: 699-711
24. Lenarcic R, Halbedel S, Visser L, Shaw M, Wu LJ, Errington J, Marenduzzo D, Hamoen LW, (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28: 2272-2282
25. Leonard TA, Butler PJ, Löwe J, (2005) Bacterial chromosome segregation: structure and DNA binding of the Soj dimer-a conserved biological switch. EMBO J 24: 270-282
26. Lesterlin C, Ball G, Schermelleh L, Sherratt DJ, (2014) RecA bundles mediate homology pairing between distant sisters during DNA break repair. Nature 506: 249-253
27. Lim CJ, Lee SY, Kenney LJ, Yan J, (2012a) Nucleoprotein filament formation is the structural basis for bacterial protein H-NS gene silencing. Sci Rep 2: 509
28. Lim CJ, Lee SY, Teramoto J, Ishihama A, Yan J, (2013) The nucleoid-associated protein Dan organizes chromosomal DNA through rigid nucleoprotein filament formation in E. coli during anoxia. Nucleic Acids Res 41: 746-753
29. Lim CJ, Whang YR, Kenney LJ, Yan J, (2012b) Gene silencing H-NS paralogue StpA forms a rigid protein filament along DNA that blocks DNA accessibility. Nucleic Acids Res 40: 3316-3328
30. Lim HC, Surovtsev IV, Beltran BG, Huang F, Bewersdorf J, Jacobs-Wagner C, (2014) Evidence for a DNA-relay mechanism in ParABS-mediated chromosome segregation. Elife 3: e02758
31. Lin L, Thanbichler M, (2013) Nucleotide-independent cytoskeletal scaffolds in bacteria. Cytoskeleton (Hoboken) 70: 409-423
32. Lindsley JE, Cox MM, (1990) Assembly and disassembly of RecA protein filaments occur at opposite filament ends. Relationship to DNA strand exchange. J Biol Chem 265: 9043-9054
33. Liu Y, Chen H, Kenney LJ, Yan J, (2010) A divalent switch drives H-NS/DNA-binding conformations between stiffening and bridging modes. Genes Dev 24: 339-344
34. Low HH, Löwe J, (2006) A bacterial dynamin-like protein. Nature 444: 766-769
35. Low HH, Löwe J, (2010) Dynamin architecture-from monomer to polymer. Curr Opin Struct Biol 20: 791-798
36. Low HH, Sachse C, Amos LA, Löwe J, (2009) Structure of a bacterial dynamin-like protein lipid tube provides a mechanism for assembly and membrane curving. Cell 139: 1342-1352
37. Löwe J, Amos LA, (2009) Evolution of cytomotive filaments: the cytoskeleton from prokaryotes to eukaryotes. Int J Biochem Cell Biol 41: 323-329
38. Lutkenhaus J, (2007) Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu Rev Biochem 76: 539-562
39. Marston AL, Thomaides HB, Edwards DH, Sharpe ME, Errington J, (1998) Polar localization of the MinD protein of Bacillus subtilis and its role in selection of the mid-cell division site. Genes Dev 12: 3419-3430
40. Mavrakis M, Azou-Gros Y, Tsai FC, Alvarado J, Bertin A, Iv F, Kress A, Brasselet S, Koenderink GH, Lecuit T, (2014) Septins promote F-actin ring formation by crosslinking actin filaments into curved bundles. Nat Cell Biol 16: 322-334
41. Meniche X, Otten R, Siegrist MS, Baer CE, Murphy KC, Bertozzi CR, Sassetti CM, (2014) Subpolar addition of new cell wall is directed by DivIVA in mycobacteria. Proc Natl Acad Sci USA 111: E3243-E3251
42. Ogawa T, Yu X, Shinohara A, Egelman EH, (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259: 1896-1899
43. Oliva MA, Halbedel S, Freund SM, Dutow P, Leonard TA, Veprintsev DB, Hamoen LW, Löwe J, (2010) Features critical for membrane binding revealed by DivIVA crystal structure. EMBO J 29: 1988-2001
44. Pichoff S, Lutkenhaus J, (2005) Tethering the Z ring to the membrane through a conserved membrane targeting sequence in FtsA. Mol Microbiol 55: 1722-1734
45. Pilhofer M, Jensen GJ, (2013) The bacterial cytoskeleton: more than twisted filaments. Curr Opin Cell Biol 25: 125-133
46. Ptacin JL, Lee SF, Garner EC, Toro E, Eckart M, Comolli LR, Moerner WE, Shapiro L, (2010) A spindle-like apparatus guides bacterial chromosome segregation. Nat Cell Biol 12: 791-798
47. Ringgaard S, van Zon J, Howard M, Gerdes K, (2009) Movement and equipositioning of plasmids by ParA filament disassembly. Proc Natl Acad Sci USA 106: 19369-19374
48. Sieger B, Bramkamp M, (2014) Interaction sites of DivIVA and RodA from Corynebacterium glutamicum. Front Microbiol 5: 738
49. Stahlberg H, Kutejova E, Muchova K, Gregorini M, Lustig A, Muller SA, Olivieri V, Engel A, Wilkinson AJ, Barak I, (2004) Oligomeric structure of the Bacillus subtilis cell division protein DivIVA determined by transmission electron microscopy. Mol Microbiol 52: 1281-1290
50. Stowell MH, Marks B, Wigge P, McMahon HT, (1999) Nucleotide-dependent conformational changes in dynamin: evidence for a mechanochemical molecular spring. Nat Cell Biol 1: 27-32
51. Suefuji K, Valluzzi R, RayChaudhuri D, (2002) Dynamic assembly of MinD into filament bundles modulated by ATP, phospholipids, and MinE. Proc Natl Acad Sci USA 99: 16776-16781
52. Szeto TH, Rowland SL, King GF, (2001) The dimerization function of MinC resides in a structurally autonomous C-terminal domain. J Bacteriol 183: 6684-6687
53. Szwedziak P, Wang Q, Bharat TA, Tsim M, Löwe J, (2014) Architecture of the ring formed by the tubulin homologue FtsZ in bacterial cell division. Elife 3: e04601
54. Szwedziak P, Wang Q, Freund SM, Löwe J, (2012) FtsA forms actin-like protofilaments. EMBO J 31: 2249-2260
55. Teramoto J, Yoshimura SH, Takeyasu K, Ishihama A, (2010) A novel nucleoid protein of Escherichia coli induced under anaerobiotic growth conditions. Nucleic Acids Res 38: 3605-3618
56. Tonthat NK, Milam SL, Chinnam N, Whitfill T, Margolin W, Schumacher MA, (2013) SlmA forms a higher-order structure on DNA that inhibits cytokinetic Z-ring formation over the nucleoid. Proc Natl Acad Sci USA 110: 10586-10591
57. Vecchiarelli AG, Han YW, Tan X, Mizuuchi M, Ghirlando R, Biertumpfel C, Funnell BE, Mizuuchi K, (2010) ATP control of dynamic P1 ParA-DNA interactions: a key role for the nucleoid in plasmid partition. Mol Microbiol 78: 78-91
58. Vecchiarelli AG, Seol Y, Neuman KC, Mizuuchi K, (2014) A moving ParA gradient on the nucleoid directs subcellular cargo transport via a chemophoresis force. Bioarchitecture 4: 154-159
59. Walthers D, Li Y, Liu Y, Anand G, Yan J, Kenney LJ, (2011) Salmonella enterica response regulator SsrB relieves H-NS silencing by displacing H-NS bound in polymerization mode and directly activates transcription. J Biol Chem 286: 1895-1902
60. Wang H, Gayda RC, (1992) Quantitative determination of FtsA at different growth rates in Escherichia coli using monoclonal antibodies. Mol Microbiol 6: 2517-2524
61. Wickstead B, Gull K, (2011) The evolution of the cytoskeleton. J Cell Biol 194: 513-525