Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins

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

Volumn 109, Issue 10, 2012, Pages 3766-3771

  Briegel, Ariane ^a   Li, Xiaoxiao ^b   Bilwes, Alexandrine M ^b   Hughes, Kelly T ^c   Jensen, Grant J ^a   Crane, Brian R ^b  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b Cornell University ^*  (United States)

^c UNIVERSITY OF UTAH   (United States)

Author keywords

Hybrid methods; Protein structure; Two component systems

Indexed keywords

CHEA KINASE; CHEW PROTEIN;

ARTICLE; CHEMORECEPTOR; DIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN MICROARRAY; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; X RAY CRYSTALLOGRAPHY;

BACILLUS SUBTILIS; BACTERIAL PHYSIOLOGICAL PHENOMENA; BACTERIAL PROTEINS; CHEMORECEPTOR CELLS; CHEMOTAXIS; CRYSTALLIZATION; CRYSTALLOGRAPHY, X-RAY; CYTOPLASM; DIMERIZATION; ELECTRON MICROSCOPE TOMOGRAPHY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; SALMONELLA ENTERICA;

BACTERIA (MICROORGANISMS);

EID: 84863229607     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1115719109     Document Type: Article

References (62)

1. Hazelbauer GL, Falke JJ, Parkinson JS (2008) Bacterial chemoreceptors: High-performance signaling in networked arrays. Trends Biochem Sci 33:9-19.
2. Kentner D, Sourjik V (2006) Spatial organization of the bacterial chemotaxis system. Curr Opin Microbiol 9:619-624. (Pubitemid 44791994)
3. Wadhams GH, Armitage JP (2004) Making sense of it all: Bacterial chemotaxis. Nat Rev Mol Cell Biol 5:1024-1037. (Pubitemid 39611538)
4. Greenfield D, et al. (2009) Self-organization of the Escherichia coli chemotaxis network imaged with super resolution light microscopy. PLoS Biol 7:e1000137.
5. Sourjik V, Berg HC (2000) Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37:740-751. (Pubitemid 30618137)
6. Englert DL, Adase CA, Jayaraman A, Manson MD (2010) Repellent taxis in response to nickel ion reqires neither Ni2+ transport nor the periplasmic NikA binding protein. J Bacteriol 192:2633-2637.
7. Milburn MV, et al. (1991) Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science 254:1342-1347. (Pubitemid 21917462)
8. Tam R, Saier MHJ (1993) Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol Rev 57:320-346. (Pubitemid 23170095)
9. Briegel A, et al. (2009) Universal architecture of bacterial chemoreceptor arrays. Proc Natl Acad Sci USA 106:17181-17186.
10. Bilwes AM, Alex LA, Crane BR, Simon MI (1999) Structure of CheA, a signal-transducing histidine kinase. Cell 96:131-141. (Pubitemid 29044160)
11. Bilwes AM, Park SY, Quezada CM, Simon MI, Crane BR (2003) Histidine Kinases in Signal Transduction, eds M Inouye and R Dutta (Academic, San Diego), pp 48-74.
12. Park S-Y, Quezada CM, Bilwes AM, Crane BR (2004) Subunit exchange by CheA histidine kinases from the mesophile Escherichia coli and the thermophile Thermotoga maritima. Biochemistry 43:2228-2240. (Pubitemid 38279968)
13. Quezada CM, Gradinaru G, Simon MI, Bilwes AM, Crane BR (2004) Helical shifts generate two distinct conformers in the atomic resolution structure of the CheA phosphotransferase domain from Thermotoga maritima. J Mol Biol 341:1283-1294. (Pubitemid 39092315)
14. Turner L, Ryu WS, Berg HC (2000) Real-time imaging of fluorescent flagellar filaments. J Bacteriol 182:2793-2801. (Pubitemid 30246910)
15. Kleene SJ, Hobson AC, Adler J (1979) Attractants and repellents influence methylation and demethylation of methyl-accepting chemotaxis proteins in an extract of Escherichia coli. Proc Natl Acad Sci USA 76:6309-6313. (Pubitemid 10163390)
16. Lupas A, Stock J (1989) Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J Biol Chem 264:17337-17342. (Pubitemid 19255565)
17. Toews ML, Goy MF, Springer MS, Adler J (1979) Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. Proc Natl Acad Sci USA 76:5544-5548. (Pubitemid 10161656)
18. Duke TAJ, Bray D (1999) Heightened sensitivity of a lattice of membrane receptors. Proc Natl Acad Sci USA 96:10104-10108. (Pubitemid 29422519)
19. Endres RG, Wingreen NS (2006) Precise adaptation in bacterial chemotaxis through "assistance neighborhoods". Proc Natl Acad Sci USA 103:13040-13044. (Pubitemid 44338913)
20. Gestwicki JE, Kiessling LL (2002) Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415:81-84. (Pubitemid 34062453)
21. Li G, Weis RM (2000) Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100:357-365. (Pubitemid 30353091)
22. Li M, Hazelbauer GL (2005) Adaptational assistance in clusters of bacterial chemoreceptors. Mol Microbiol 56:1617-1626. (Pubitemid 40780655)
23. Sourjik V, Berg H (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99:123-127. (Pubitemid 34060327)
24. Sourjik V, Berg HC (2004) Functional interactions between receptors in bacterial chemotaxis. Nature 428:437-441. (Pubitemid 38419690)
25. Briegel A, et al. (2008) Location and architecture of the Caulobacter crescentus chemoreceptor array. Mol Microbiol 69:30-41. (Pubitemid 351832749)
26. Khursigara CM, Wu X, Subramaniam S (2008) Chemoreceptors in Caulobacter crescentus: Trimers of receptor dimers in a partially ordered hexagonally packed array. J Bacteriol 190:6805-6810.
27. Kim KK, Yokota H, Kim SH (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400:787-792. (Pubitemid 29399543)
28. Coleman MD, Bass RB, Mehan RS, Falke JJ (2005) Conserved glycine residues in the cytoplasmic domain of the aspartate receptor play essential roles in kinase coupling and on-off switching. Biochemistry 44:7687-7695. (Pubitemid 40740752)
29. Park S-Y, et al. (2006) Reconstruction of the chemotaxis receptor-kinase assembly. Nat Struct Mol Biol 13:400-407. (Pubitemid 43881579)
30. Pollard AM, Bilwes AM, Crane BR (2009) The structure of a soluble chemoreceptor suggests a mechanism for propagating conformational signals. Biochemistry 48:1936-1944.
31. Griswold IJ, et al. (2002) The solution structure and interactions of CheW from Thermotoga maritima. Nat Struct Mol Biol 9:121-125. (Pubitemid 34132414)
32. Zhao J, Parkinson JS (2006) Mutational analysis of the chemoreceptor-coupling domain of the Escherichia coli chemotaxis signaling kinase CheA. J Bacteriol 188:3299-3307.
33. Bhatnagar J, et al. (2010) Structure of the ternary complex formed by a chemotaxis receptor signalling domain, the CheA histidine kinase, and the coupling protein CheW as determined by pulsed dipolar ESR spectroscopy. Biochemistry 49:3824-3841.
34. Boukhvalova M, VanBruggen R, Stewart RC (2002) CheA kinase and chemoreceptor interaction surfaces on CheW. J Biol Chem 277:23596-23603. (Pubitemid 34952196)
35. Underbakke ES, Zhu YM, Kiessling LL (2011) Protein footprinting in a complex milieu: Identifying the interaction surfaces of the chemotaxis adaptor protein CheW. J Mol Biol 409:483-495.
36. 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 102:15623-15628. (Pubitemid 41528106)
37. Levit MN, Grebe TW, Stock JB (2002) Organization of the receptor-kinas signaling array that regulates the Escherichia coli chemotaxis. J Biol Chem 277:36748-36754.
38. Kentner D, Thiem SMH, Sourjik V (2006) Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61:407-417. (Pubitemid 44356572)
39. Asinas AE, Weis RM (2006) Competitive and cooperative interactions in receptor signaling complexes. J Biol Chem 281:30512-30523. (Pubitemid 44582108)
40. Miller AS, Kohout SC, Gilman KA, Falke JJ (2006) CheA kinase of bacterial chemotaxis: Chemical mapping of four essential docking sites. Biochemistry 45:8699-8711. (Pubitemid 44100667)
41. Li M, Hazelbauer GL (2011) Core unit of chemotaxis signaling complexes. Proc Natl Acad Sci USA 108:9390-9395.
42. Li M, Hazelbauer GL (2004) Cellular stoichiometry of the components of the chemotaxis signalling complex. J Bacteriol 186:3687-3694. (Pubitemid 38746043)
43. Erbse AH, Falke JJ (2009) The core signaling proteins of bacterial chemotaxis assemble to form an ultrastable complex. Biochemistry 48:6975-6987.
44. Alexander RP, Lowenthal AC, Harshey RM, Ottemann KM (2010) CheV: CheW-like coupling proteins at the core of the chemotaxis signaling network. Trends Microbiol 18:494-503.
45. Goldman JP, Levin MD, Bray D (2009) Signal amplification in a lattice of coupled protein kinases. Mol Biosyst 5:1853-1859.
46. Briegel A, Beeby M, Thanbichler M, Jensen GJ (2011) Activated chemoreceptor arrays remain intact and hexagonally packed. Mol Microbiol 82:748-757.
47. Karlinsey JE (2007) λ-red genetic engineering in Salmonella enterica serovar Typhimurium. Methods Enzymol 421:199-209.
48. Erhardt M, Hughes KT (2010) C-ring requirement in flagellar type III secretion is bypassed by FlhDC upregulation. Mol Microbiol 75:376-393.
49. Wozniak CE, Lee C, Hughes KT (2009) T-POP array identifies EcnR and PefI-SrgD as novel regulators of flagellar gene expression. J Bacteriol 191:1498-1508.
50. Iancu CV, et al. (2007) Electron cryotomography sample preparation using the Vitrobot. Nat Protoc 1:2813-2819.
51. TivolW, Briegel A, Jensen GJ (2008) An improved cryogen for plunge freezing. Microsc Microanal 14:375-379.
52. Suloway C, et al. (2009) Fully automated, sequential tilt-series acquisition with Leginon. J Struct Biol 167:11-18.
53. Mastronarde DN (2005) Automated electron microscope tomography using robust prediction of specimen movements. J Struct Biol 152:36-51.
54. Agulleiro JI, Fernandez JJ (2011) Fast tomographic reconstruction on multicore computers. Bioinformatics 27:582-583.
55. Nicastro D, et al. (2006) The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313:944-948. (Pubitemid 44267380)
56. Otwinowski Z, MinorW(1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 276:307-326. (Pubitemid 27085611)
57. McCoy AJ, et al. (2007) Phaser crystallographic software. J Appl Crystallogr 40:658-674. (Pubitemid 47080256)
58. McRee D, Israel M (2008) XtalView, protein structure solution and protein graphics, a short history. J Struct Biol 163:208-213.
59. Schröder GF, Brunger AT, LevittM(2007) Combining efficient conformational sampling with a deformable elastic network model facilitates structure refinement at low resolution. Structure 15:1630-1641. (Pubitemid 350213409)
60. Schröder GF, Levitt M, Brunger AT (2010) Super-resolution biomolecular crystallography with low-resolution data. Nature 464:1218-1222.
61. Brunger AT (2007) Version 1.2 of the Crystallography and NMR System. Nat Protoc 2:2728-2788.
62. Vu A, Wang X, Zhou H, Dahlquist FW (2012) The receptor CheW binding interface in bacterial chemotaxis. J Mol Biol 415:759-767.