ParP prevents dissociation of CheA from chemotactic signaling arrays and tethers them to a polar anchor

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 2, 2014, Pages

  Ringgaard, Simon ^a,b   Zepeda Rivera, Martha ^a,b   Wu, Xiaoji ^a   Schirner, Kathrin ^b   Davis, Brigid M ^a,b   Waldor, Matthew K ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Diffusion and capture; Pole development; Protein inheritance; Protein localization; Protein sequestration

Indexed keywords

CHEA KINASE; MEMBRANE PROTEIN; PROTEIN PARC; PROTEIN PARP; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CELL CYCLE REGULATION; CHEMOTAXIS; ENZYME ACTIVITY; HYDROLYSIS; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIBRIO PARAHAEMOLYTICUS;

DIFFUSION AND CAPTURE; POLE DEVELOPMENT; PROTEIN INHERITANCE; PROTEIN LOCALIZATION; PROTEIN SEQUESTRATION;

AGAR; BACTERIAL PROTEINS; CELL POLARITY; CHEMOTAXIS; COMPUTATIONAL BIOLOGY; DNA TOPOISOMERASE IV; ESCHERICHIA COLI; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; MEMBRANE PROTEINS; MICROSCOPY, FLUORESCENCE; SIGNAL TRANSDUCTION; TIME-LAPSE IMAGING; VIBRIO CHOLERAE; VIBRIO PARAHAEMOLYTICUS;

EID: 84892600214     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1315722111     Document Type: Article

References (44)

1. Sourjik V, Armitage JP (2010) Spatial organization in bacterial chemotaxis. EMBO J 29(16):2724-2733.
2. Briegel A, et al. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106(40):17181-17186.
3. Briegel A, et al. (2012) Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. Proc Natl Acad Sci USA 109(10):3766-3771.
4. Liu J, et al. (2012) Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells. Proc Natl Acad Sci USA 109(23): E1481-E1488.
5. Zhang P, Khursigara CM, Hartnell LM, Subramaniam S (2007) Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. Proc Natl Acad Sci USA 104(10):3777-3781.
6. Kentner D, Thiem S, Hildenbeutel M, Sourjik V (2006) Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61(2):407-417.
7. Skidmore JM, et al. (2000) Polar clustering of the chemoreceptor complex in Escherichia coli occurs in the absence of complete CheA function. J Bacteriol 182(4): 967-973.
8. Studdert CA, Parkinson JS (2005) Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc Natl Acad Sci USA 102(43):15623-15628.
9. Thiem S, Sourjik V (2008) Stochastic assembly of chemoreceptor clusters in Escherichia coli. Mol Microbiol 68(5):1228-1236.
10. Sourjik V, Berg HC (2000) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37(4):740-751.
11. Alley MR, Maddock JR, Shapiro L (1992) Polar localization of a bacterial chemoreceptor. Genes Dev 6(5):825-836.
12. Maddock JR, Shapiro L (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259(5102):1717-1723.
13. Wadhams GH, Warren AV, Martin AC, Armitage JP (2003) Targeting of two signal transduction pathways to different regions of the bacterial cell. Mol Microbiol 50(3):763-770.
14. Bardy SL, Maddock JR (2005) Polar localization of a soluble methyl-accepting protein of Pseudomonas aeruginosa. J Bacteriol 187(22):7840-7844.
15. Ringgaard S, Schirner K, Davis BM, Waldor MK (2011) A family of ParA-like ATPases promotes cell pole maturation by facilitating polar localization of chemotaxis proteins. Genes Dev 25(14):1544-1555.
16. Yamaichi Y, et al. (2012) A multidomain hub anchors the chromosome segregation and chemotactic machinery to the bacterial pole. Genes Dev 26(20):2348-2360.
17. Gerdes K, Howard M, Szardenings F (2010) Pushing and pulling in prokaryotic DNA segregation. Cell 141(6):927-942.
18. Lutkenhaus J (2012) The ParA/MinD family puts things in their place. Trends Microbiol 20(9):411-418.
19. Thompson SR, Wadhams GH, Armitage JP (2006) The positioning of cytoplasmic protein clusters in bacteria. Proc Natl Acad Sci USA 103(21):8209-8214.
20. Savage DF, Afonso B, Chen AH, Silver PA (2010) Spatially ordered dynamics of the bacterial carbon fixation machinery. Science 327(5970):1258-1261.
21. Ding Z, et al. (2002) A novel cytology-based, two-hybrid screen for bacteria applied to protein-protein interaction studies of a type IV secretion system. J Bacteriol 184(20): 5572-5582.
22. Lenarcic R, et al. (2009) Localisation of DivIVA by targeting to negatively curved membranes. EMBO J 28(15):2272-2282.
23. Miller AS, Kohout SC, Gilman KA, Falke JJ (2006) CheA Kinase of bacterial chemotaxis: Chemical mapping of four essential docking sites. Biochemistry 45(29):8699-8711.
24. Griswold IJ, et al. (2002) The solution structure and interactions of CheW from Thermotoga maritima. Nat Struct Biol 9(2):121-125.
25. Zhao J, Parkinson JS (2006) Mutational analysis of the chemoreceptor-coupling domain of the Escherichia coli chemotaxis signaling kinase CheA. J Bacteriol 188(9): 3299-3307.
26. Barill? D, Carmelo E, Hayes F (2007) The tail of the ParG DNA segregation protein remodels ParF polymers and enhances ATP hydrolysis via an arginine finger-like motif. Proc Natl Acad Sci USA 104(6):1811-1816.
27. Sourjik V (2004) Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol 12(12):569-576.
28. Pratto F, et al. (2008) Streptococcus pyogenes pSM19035 requires dynamic assembly of ATP-bound ParA and ParB on parS DNA during plasmid segregation. Nucleic Acids Res 36(11):3676-3689.
29. Kiekebusch D, Michie KA, Essen LO, Löwe J, ThanbichlerM(2012) Localized dimerization and nucleoid binding drive gradient formation by the bacterial cell division inhibitor MipZ. Mol Cell 46(3):245-259.
30. Easter J, Jr., Gober JW (2002) ParB-stimulated nucleotide exchange regulates a switch in functionally distinct ParA activities. Mol Cell 10(2):427-434.
31. Hu Z, Lutkenhaus J (2001) Topological regulation of cell division in E. coli spatiotemporal oscillation of MinD requires stimulation of its ATPase by MinE and phospholipid. Mol Cell 7(6):1337-1343.
32. Roberts MAJ, Wadhams GH, Hadfield KA, Tickner S, Armitage JP (2012) ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proc Natl Acad Sci USA 109(17):6698-6703.
33. Thiem S, Kentner D, Sourjik V (2007) Positioning of chemosensory clusters in E. coli and its relation to cell division. EMBO J 26(6):1615-1623.
34. Greenfield D, et al. (2009) Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol 7(6):e1000137.
35. Wang H, Wingreen NS, Mukhopadhyay R (2008) Self-organized periodicity of protein clusters in growing bacteria. Phys Rev Lett 101(21):218101.
36. Shiomi D, Yoshimoto M, Homma M, Kawagishi I (2006) Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol Microbiol 60(4):894-906.
37. Rudner DZ, Pan Q, Losick RM (2002) Evidence that subcellular localization of a bacterial membrane protein is achieved by diffusion and capture. Proc Natl Acad Sci USA 99(13):8701-8706.
38. Deich J, Judd EM, McAdams HH, Moerner WE (2004) Visualization of the movement of single histidine kinase molecules in live Caulobacter cells. Proc Natl Acad Sci USA 101(45):15921-15926.
39. Miller VL, Mekalanos JJ (1988) A novel suicide vector and its use in construction of insertion mutations: Osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR. J Bacteriol 170(6):2575-2583.
40. 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(46):19369-19374.
41. Jensen LJ, et al. (2009) STRING 8?a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 37(Database issue):D412-D416.
42. Edgar RC (2004) MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32(5):1792-1797.
43. Letunic I, Bork P (2011) Interactive Tree Of Life v2: Online annotation and display of phylogenetic trees made easy. Nucleic Acids Res 39(Web Server issue):W475-8.
44. Ringgaard S, Löwe J, Gerdes K (2007) Centromere pairing by a plasmid-encoded type I ParB protein. J Biol Chem 282(38):28216-28225.