1932

Abstract

Electron cryotomography (ECT) can produce three-dimensional images of biological samples such as intact cells in a near-native, frozen-hydrated state to macromolecular resolution (∼4 nm). Because one of its first and most common applications has been to bacterial chemoreceptor arrays, ECT's contributions to this field illustrate well its past, present, and future. While X-ray crystallography and nuclear magnetic resonance spectroscopy have revealed the structures of nearly all the individual components of chemoreceptor arrays, ECT has revealed the mesoscale information about how the components are arranged within cells. Receptors assemble into a universally conserved 12-nm hexagonal lattice linked by CheA/CheW rings. Membrane-bound arrays are single layered; cytoplasmic arrays are double layered. Images of in vitro reconstitutions have led to a model of how arrays assemble, and images of native arrays in different states have shown that the conformational changes associated with signal transduction are subtle, constraining models of activation and system cooperativity. Phase plates, better detectors, and more stable stages promise even higher resolution and broader application in the near future.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-biophys-070816-033555
2017-05-22
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/biophys/46/1/annurev-biophys-070816-033555.html?itemId=/content/journals/10.1146/annurev-biophys-070816-033555&mimeType=html&fmt=ahah

Literature Cited

  1. Adler J. 1.  1966. Chemotaxis in bacteria. Science 153:708–16 [Google Scholar]
  2. Ahrén B. 2.  2009. Islet G protein-coupled receptors as potential targets for treatment of type 2 diabetes. Nat. Rev. Drug Discov. 8:369–85 [Google Scholar]
  3. Airola M, Watts KJ, Bilwes AM, Crane BR. 3.  2010. Structure of concatenated HAMP domains provides a mechanism for signal transduction. Structure 18:436–48 [Google Scholar]
  4. Al-Amoudi A, Chang J-J, Leforestier A, McDowall A, Salamin LM. 4.  et al. 2004. Cryo-electron microscopy of vitreous sections. EMBO J 23:3585–88 [Google Scholar]
  5. Alberts B. 5.  2015. Molecular Biology of the Cell 1 New York: Garland Science, Taylor and Francis Group
  6. Alley MRK, Maddock JR, Shapiro L. 6.  1992. Polar localization of a bacterial chemoreceptor. Genes Dev 6:825–36 [Google Scholar]
  7. Alon U, Surette MG, Barakai N, Leibler S. 7.  1999. Robustness in bacterial chemotaxis. Nature 397:168–71 [Google Scholar]
  8. Asano S, Fukuda Y, Beck F, Aufderheide A, Förster F. 8.  et al. 2015. A molecular census of 26S proteasomes in intact neurons. Science 347:439–42 [Google Scholar]
  9. Baumeister W, Steven AC. 9.  2000. Macromolecular electron microscopy in the era of structural genomics. Trends Biochem. Sci. 25:624–31 [Google Scholar]
  10. Bilwes AM, Alex LA, Crane BR, Simon MI. 10.  1999. Structure of CheA, a signal-transducing histidine kinase. Cell 96:131–41 [Google Scholar]
  11. Bilwes AM, Park S-Y, Quezada CM, Simon MI, Crane BR. 11.  2003. Structure and function of CheA, the histidine kinase central to bacterial chemotaxis. Histidine Kinases in Signal Transduction M Inouye, R Dutta 48–74 San Diego, CA: Academic [Google Scholar]
  12. Borkovich KA, Kaplan N, Hess JF, Simon MI. 12.  1989. Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer. PNAS 86:1208–12 [Google Scholar]
  13. Borrock MJ, Kolonko EM, Kiessling LL. 13.  2008. Chemical probes of bacterial signal transduction reveal that repellents stabilize and attractants destabilize the chemoreceptor array. ASC Chem. Biol. 3:101–9 [Google Scholar]
  14. Bray D, Levin MD, Morton-Firth CJ. 14.  1998. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393:85–88 [Google Scholar]
  15. Briegel A. 15.  2005. Strukturuntersuchungen an Prokaryonten mit Kryo-Elektronentomographie PhD Thesis, Tech. Univ. München, Munich
  16. Briegel A, Ames P, Gumbart J, Oikonomou CM, Parkinson JS, Jensen GJ. 16.  2013. The mobility of two kinase domains in the Escherichia coli chemoreceptor array varies with signaling state. Mol. Microbiol. 89:831–41 [Google Scholar]
  17. Briegel A, Beeby M, Thanbichler M, Jensen GJ. 17.  2011. Activated chemoreceptor arrays remain intact and hexagonally packed. Mol. Microbiol. 82:748–57 [Google Scholar]
  18. Briegel A, Dias DP, Li Z, Jensen RB, Frangakis AS, Jensen GJ. 18.  2006. Multiple large filament bundles observed in Caulobacter crescentus by electron cryotomography. Mol. Microbiol. 62:5–14 [Google Scholar]
  19. Briegel A, Ding HJ, Li Z, Werner J, Gitai Z. 19.  et al. 2008. Location and architecture of the Caulobacter crescentus chemoreceptor array. Mol. Microbiol. 69:30–41 [Google Scholar]
  20. Briegel A, Ladinsky MS, Oikonomou C, Jones CW, Harris MJ. 20.  et al. 2014. Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling. eLife 3:e02151 [Google Scholar]
  21. Briegel A, Li X, Bilwes AM, Hughes KT, Jensen GJ, Crane BR. 21.  2012. Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. PNAS 109:3766–71 [Google Scholar]
  22. Briegel A, Ortega DR, Huang A, Oikonomou C, Gunsalus RP, Jensen GJ. 22.  2015. Structural conservation of chemotaxis machinery across Archaea and Bacteria. Environ. Microbiol. Rep. 7:414–19 [Google Scholar]
  23. Briegel A, Ortega DR, Mann P, Kjær A, Ringgaard S, Jensen GJ. 23.  2016. Chemotaxis cluster 1 proteins form cytoplasmic arrays in Vibrio cholerae and are stabilized by a double signaling domain receptor DosM. PNAS 113:10412–17 [Google Scholar]
  24. Briegel A, Ortega DR, Tocheva EI, Wuichet K, Li Z. 24.  et al. 2009. Universal architecture of bacterial chemoreceptor arrays. PNAS 106:17181–86 [Google Scholar]
  25. Briegel A, Wong ML, Hodges HL, Oikonomou C, Piasta KN. 25.  et al. 2014. New insights into bacterial chemoreceptor array structure and assembly from electron cryotomography. Biochemistry 53:1575–85 [Google Scholar]
  26. Brock FM, Murray RG. 26.  1988. The ultrastructure and ATPase nature of polar membrane in Campylobacter jejuni. Can. . J. Microbiol. 34:594–604 [Google Scholar]
  27. Cassidy CK, Himes BA, Alvarez FJ, Ma J, Zhao G. 27.  et al. 2015. CryoEM and computer simulations reveal a novel kinase conformational switch in bacterial chemotaxis signaling. eLife 4:e08419 [Google Scholar]
  28. Castaño-Díez D, Kudryashev M, Stahlberg H. 28.  2017. Dynamo Catalogue: geometrical tools and data management for particle picking in subtomogram averaging of cryo-electron tomograms. J. Struct. Biol. 197:135–44 [Google Scholar]
  29. Chen Y, Pfeffer S, Hrabe T, Schuller JM, Förster F. 29.  2013. Fast and accurate reference-free alignment of subtomograms. J. Struct. Biol. 182:235–45 [Google Scholar]
  30. Cho HS, Lee S-Y, Yan D, Pan X, Parkinson JS. 30.  et al. 2000. NMR structure of activated CheY. J. Mol. Biol. 297:543–51 [Google Scholar]
  31. Cianfrocco MA, Leschziner AE. 31.  2015. Low cost, high performance processing of single particle cryo-electron microscopy data in the cloud. eLife 4:e06664 [Google Scholar]
  32. Comolli LR, Luef B, Chan CS. 32.  2011. High-resolution 2D and 3D cryo-TEM reveals structural adaptations of two stalk-forming bacteria to an Fe-oxidizing lifestyle. Environ. Microbiol. 13:2915–29 [Google Scholar]
  33. Danev R, Buijsse B, Khoshouei M, Plitzko JM, Baumeister W. 33.  2014. Volta potential phase plate for in-focus phase contrast transmission electron microscopy. PNAS 111:15635–40 [Google Scholar]
  34. De Rosier DJ, Klug A. 34.  1968. Reconstruction of three-dimensional structures from electron micrographs. Nature 217:130–34 [Google Scholar]
  35. Dierksen K, Typke D, Hegerl R, Walz J, Sackmann E, Baumeister W. 35.  1995. Three-dimensional structure of lipid vesicles embedded in vitreous ice and investigated by automated electron tomography. Biophys. J. 68:1416–22 [Google Scholar]
  36. Djordjevic S, Goudreau PN, Xu Q, Stock AM, West AH. 36.  1998. Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. PNAS 95:1381–86 [Google Scholar]
  37. Djordjevic S, Stock AM. 37.  1997. Crystal structure of the chemotaxis receptor methyltransferase CheR suggests a conserved structural motif for binding S-adenosylmethionine. Structure 5:545–58 [Google Scholar]
  38. Dorsam RT, Gutkind JS. 38.  2007. G-protein-coupled receptors and cancer. Nat. Rev. 7:79–94 [Google Scholar]
  39. Dubochet J, Adrian M, Chang J, Homo J-C, Lepault J. 39.  et al. 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21:129–228 [Google Scholar]
  40. Dubochet J, Lepault J, Freeman R, Berriman JA, Homo J-C. 40.  1982. Electron microscopy of frozen water and aqueous solutions. J. Microsc. 128:219–37 [Google Scholar]
  41. Dubochet J, Zuber B, Eltsov M, Bouchet-Marquis C, Al-Amoudi A, Livolant F. 41.  2007. How to “read” a vitreous section. Methods Cell Biol 79:385–406 [Google Scholar]
  42. 42. Editorial. 2016. Method of the year 2015. Nat. Methods 13:1 [Google Scholar]
  43. Englert DL, Adase CA, Jayaraman A, Manson MD. 43.  2010. Repellent taxis in response to nickel ion requires neither Ni2+ transport nor the periplasmic NikA binding protein. J. Bacteriol. 192:2633–37 [Google Scholar]
  44. Erbse AH, Falke JJ. 44.  2009. The core signaling proteins of bacterial chemotaxis assemble to form an ultrastable complex. Biochemistry 48:6975–87 [Google Scholar]
  45. Falke JJ, Erbse AH. 45.  2009. The piston rises again. Structure 17:1149–51 [Google Scholar]
  46. Falke JJ, Hazelbauer GL. 46.  2001. Transmembrane signaling in bacterial chemoreceptors. Trends Biochem. Sci. 26:257–65 [Google Scholar]
  47. Farley MM, Hu B, Margolin W, Liu J. 47.  2016. Minicells, back in fashion. J. Bacteriol. 198:1186–95 [Google Scholar]
  48. Fernandez JJ, Li S, Crowther RA. 48.  2006. CTF determination and correction in electron cryotomography. Ultramicroscopy 106:587–96 [Google Scholar]
  49. Fu X, Himes BA, Ke D, Rice WJ, Ning J, Zhang P. 49.  2014. Controlled bacterial lysis for electron tomography of native cell membranes. Structure 22:1875–82 [Google Scholar]
  50. Fukuda Y, Laugks U, Lučić V, Baumeister W, Danev R. 50.  2015. Electron cryotomography of vitrified cells with a Volta phase plate. J. Struct. Biol. 190:143–54 [Google Scholar]
  51. Gan L, Jensen GJ. 51.  2012. Electron tomography of cells. Q. Rev. Biophys. 45:27–56 [Google Scholar]
  52. Gegner JA, Graham DR, Roth AF, Dahlquist FW. 52.  1992. Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70:975–82 [Google Scholar]
  53. Gestwicki JE, Kiessling LL. 53.  2002. Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415:81–84 [Google Scholar]
  54. Gilkey CM, Staehlin LA. 54.  1986. Advances in ultrarapid freezing for the preservation of cellular ultrastructure. J. Electron. Microsc. Tech. 3:177–210 [Google Scholar]
  55. Greenfield D, McEvoy AL, Shroff H, Crooks GE, Wingreen NS. 55.  et al. 2009. Self-organization of the Escherichia coli chemotaxis network imaged with super resolution light microscopy. PLOS Biol 7:e1000137 [Google Scholar]
  56. Grimm R, Barmann M, Hackl W, Typke D, Sackmann E, Baumeister W. 56.  1997. Energy filtered electron tomography of ice-embedded actin and vesicles. Biophys. J. 72:482–89 [Google Scholar]
  57. Hart RG. 57.  1968. Electron microscopy of unstained biological material: the polytropic montage. Science 159:1464–67 [Google Scholar]
  58. Hazelbauer GL, Falke JJ, Parkinson JS. 58.  2008. Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem. Sci. 33:9–19 [Google Scholar]
  59. Homma M, Shiomi D, Homma M, Kawagishi I. 59.  2004. Attractant binding alters arrangement of chemoreceptor dimers within its cluster at the cell pole. PNAS 101:3462–67 [Google Scholar]
  60. Hoppe W, Gassmann J, Hunsmann N, Schramm HJ, Sturm M. 60.  1974. Three dimensional reconstruction of negativly stained yeast fatty-acid synthease molecules from tilt series in the electron microscope. Hoppe-Seylers Z. Physiol. Chem. 355:1483–87 [Google Scholar]
  61. Horowitz RA, Koster AJ, Walz J, Woodcock CL. 61.  1997. Automated electron microscope tomography of frozen-hydrated chromatin: The irregular three-dimensional zigzag architecture persists in compact, isolated fibers. J. Struct. Biol. 120:353–62 [Google Scholar]
  62. Houben L, Thust A, Urban K. 62.  2006. Atomic-precision determination of the reconstruction of a 90° tilt boundary in YBa2Cu3O7–delta by aberration corrected HRTEM. Ultramicroscopy 106:200–14 [Google Scholar]
  63. Hulko M, Berndt F, Gruber M, Linder JU, Truffault V. 63.  et al. 2006. The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929–40 [Google Scholar]
  64. Khoshouei M, Pfeffer S, Baumeister W, Förster F, Danev R. 64.  2017. Subtomogram analysis using the Volta phase plate. J. Struct. Biol. 197:94–101 [Google Scholar]
  65. Khursigara CM, Lan G, Neumann S, Wu X, Ravindran S. 65.  et al. 2011. Lateral density of receptor arrays in the membrane plane influences sensitivity of the E. coli chemotaxis response. EMBO J 30:1719–29 [Google Scholar]
  66. Khursigara CM, Wu X, Subramaniam S. 66.  2008. Chemoreceptors in Caulobacter crescentus: trimers of receptor dimers in a partially ordered hexagonally packed array. J. Bacteriol. 190:6805–10 [Google Scholar]
  67. Khursigara CM, Wu X, Zhang P, Lefman J, Subramaniam S. 67.  2008. Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors. PNAS 105:16555–60 [Google Scholar]
  68. Kim KK, Yokota H, Kim S-H. 68.  1999. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400:787–92 [Google Scholar]
  69. Kimanius D, Forsberg BO, Scheres SHW, Lindahl E. 69.  2017. Accelerated cryo-EM structure determination with parallelisation using GPUs in RELION-2. eLife In press. https://doi.org/10.7554/eLife.18722
  70. Kleene SJ, Hobson AC, Adler J. 70.  1979. Attractants and repellents influence methylation and demethylation of methyl-accepting chemotaxis proteins in an extract of Escherichia coli. . PNAS 76:6309–13 [Google Scholar]
  71. Koster AJ, Grimm R, Typke D, Hegerl R, Stoschek A. 71.  et al. 1997. Perspectives of molecular and cellular electron tomography. J. Struct. Biol. 120:276–308 [Google Scholar]
  72. Ladinsky MS. 72.  2010. Micromanipulator-assisted vitreous cryosectioning and sample preparation by high-pressure freezing. Methods Enzymol 481:165–94 [Google Scholar]
  73. Ladinsky MS, Pierson JM, McIntosh JR. 73.  2006. Vitreous cryo-sectioning of cells facilitated by a micromanipulator. J. Microsc. 224:129–34 [Google Scholar]
  74. Lai R-Z, Manson JMB, Bormans AF, Draheim RR, Nguyen NT, Manson MD. 74.  2005. Cooperative signaling among bacterial chemoreceptors. Biochemistry 44:14298–307 [Google Scholar]
  75. Lam KH, Ling TKW, Au SWN. 75.  2010. Crystal structure of activated CheY1 from Helicobacter pylori. . J. Bacteriol. 192:2324–34 [Google Scholar]
  76. Lamanna AC, Ordal GW, Kiessling LL. 76.  2005. Large increases in attractant concentration disrupt the polar localization of bacterial chemoreceptors. Mol. Microbiol. 57:774–85 [Google Scholar]
  77. Lefman J, Zhang P, Hirai T, Weis RM, Juliani J. 77.  et al. 2004. Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr. J. Bacteriol. 186:5052–61 [Google Scholar]
  78. Li G, Weis RM. 78.  2000. Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100:357–65 [Google Scholar]
  79. Li Y, Hu Y, Fu W, Xia B, Jin C. 79.  2007. Solution structure of the bacterial chemotaxis adaptor protein CheW from Escherichia coli. Biochem. Biophys. Res. Commun. 360:863–67 [Google Scholar]
  80. Liberman L, Berg HC, Sourjik V. 80.  2004. Effect of chemoreceptor modification on assembly and activity of the receptor-kinase complex in Escherichia coli. . J. Bacteriol. 186:6643–46 [Google Scholar]
  81. Liu J, Hu B, Morado DR, Jani S, Manson MD, Margolin W. 81.  2012. Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells. PNAS 109:E1481–88 [Google Scholar]
  82. Liu Y, Levit MN, Lurz R, Surette MG. 82.  1997. Receptor-mediated protein kinase activation and the mechanism of transmembrane signaling in bacterial chemotaxis. EMBO J 16:7231–40 [Google Scholar]
  83. Lupas A, Stock J. 83.  1989. Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. J. Biol. Chem. 264:17337–42 [Google Scholar]
  84. Lybarger SR, Maddock J. 84.  2001. Polarity in action: asymmetric protein localization in bacteria. J. Bacteriol. 183:3261–67 [Google Scholar]
  85. Maddock JR, Shapiro L. 85.  1993. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259:1717–23 [Google Scholar]
  86. Mesibov R, Ordal GW, Adler J. 86.  1973. The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range. Weber law and related phenomena. J. Gen. Physiol. 62:203–23 [Google Scholar]
  87. Milburn MV, Prive GG, Milligan DL, Scott WG, Yeh J. 87.  et al. 1991. Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science 254:1342–47 [Google Scholar]
  88. Murray RGE, Birch-Andersen A. 88.  1963. Specialized structure in the region of the flagella tuft in Spirillum serpens. . Can. J. Microbiol. 9:393–401 [Google Scholar]
  89. Narayan K, Subramaniam S. 89.  2015. Focused ion beams in biology. Nat. Methods 12:1021–31 [Google Scholar]
  90. Nicastro D, Schwartz CL, Pierson J, Gaudette R, Porter ME, McIntosh JR. 90.  2006. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313:944–48 [Google Scholar]
  91. Ninfa EG, Stock A, Mowbray S, Stock JB. 91.  1991. Reconstitution of the bacterial chemotaxis signal transduction system from purified components. J. Biol. Chem. 266:9764–70 [Google Scholar]
  92. Palade GE. 92.  1952. A study of fixation for electron microscopy. J. Exp. Med. 95:285–98 [Google Scholar]
  93. Park S-Y, Borbat PP, Gonzalez-Bonet G, Bhatnagar J, Pollard AM. 93.  et al. 2006. Reconstruction of the chemotaxis receptor-kinase assembly. Nat. Struct. Mol. Biol. 13:400–7 [Google Scholar]
  94. Park S-Y, Quezada CM, Bilwes AM, Crane BR. 94.  2004. Subunit exchange by CheA histidine kinases from the mesophile Escherichia coli and the thermophile Thermotoga maritima. . Biochemistry 43:2228–40 [Google Scholar]
  95. Parkinson JS. 95.  2010. Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu. Rev. Microbiol. 64:101–22 [Google Scholar]
  96. Parkinson JS, Ames P, Studdert CA. 96.  2005. Collaborative signaling by bacterial chemoreceptors. Curr. Opin. Microbiol. 8:116–21 [Google Scholar]
  97. Pilhofer M, Aistleitner K, Ladinsky MS, Konig L, Horn M, Jensen GJ. 97.  2014. Architecture and host interface of environmental chlamydiae revealed by electron cryotomography. Environ. Microbiol. 16:417–29 [Google Scholar]
  98. Pilhofer M, Ladinsky MS, McDowall AW, Jensen GJ. 98.  2010. Bacterial TEM: new insights from cryo-microscopy. Methods Cell Biol 96:21–45 [Google Scholar]
  99. Quezada CM, Gradinaru G, Simon MI, Bilwes AM, Crane BR. 99.  2004. Helical shifts generate two distinct conformers in the atomic resolution structure of the CheA phosphotransferase domain from thermotoga maritima. J. Mol. Biol. 341:1283–94 [Google Scholar]
  100. Raddi G, Morado DR, Yan J, Haake DA, Yang XF, Liu J. 100.  2012. Three-dimensional structures of pathogenic and saprophytic Leptospira species revealed by cryo-electron tomography. J. Bacteriol. 194:1299–306 [Google Scholar]
  101. Samanta D, Borbat PP, Dzikovski B, Freed JH, Crane BR. 101.  2015. Bacterial chemoreceptor dynamics correlate with activity state and are coupled over long distances. PNAS 112:2455–60 [Google Scholar]
  102. Scheres SHW. 102.  2015. Semi-automated selection of cryo-EM particles in RELION-1.3. J. Struct. Biol. 189:114–22 [Google Scholar]
  103. Scheres SHW, Melero R, Vale M, Carazo J-M. 103.  2009. Averaging of electron subtomograms and random conical tilt reconstructions through likelihood optimization. Structure 17:1563–72 [Google Scholar]
  104. Schulmeister S, Ruttorf M, Thiem S, Kentner D, Lebiedz D, Sourjik V. 104.  2008. Protein exchange dynamics at chemoreceptor clusters in E. coli. . PNAS 105:6403–8 [Google Scholar]
  105. Schur FK, Obr M, Hagen WJ, Wan W, Jakobi AJ. 105.  et al. 2016. An atomic model of HIV-1 capsid-SP1 reveals structures regulating assembly and maturation. Science 353:506–8 [Google Scholar]
  106. Schuster SC, Swanson RV, Alex LA, Bourret RB, Simon MI. 106.  1993. Assembly and function of a quaternary signal transduction complex by surface plasmon resonance. Nature 365:343–47 [Google Scholar]
  107. Shi W, Yang Z, Geng Y, Wolinsky LE, Lovett MA. 107.  1998. Chemotaxis in Borrelia burgdorferi. . J. Bacteriol. 180:231–35 [Google Scholar]
  108. Skidmore JM, Ellefson DD, McNamara BP, Couto MMP, Wolfe AJ, Maddock JR. 108.  2000. Polar clustering of the chemoreceptor complex in Escherichia coli occurs in the absence of complete CheA function. J. Bacteriol. 182:967–73 [Google Scholar]
  109. Slivka PF, Falke JJ. 109.  2012. Isolated bacterial chemosensory array possesses quasi- and ultrastable components: functional links between array stability, cooperativity, and order. Biochemistry 51:10218–28 [Google Scholar]
  110. Studdert CA, Parkinson JS. 110.  2004. Crosslinking snapshots of bacterial chemoreceptor squads. PNAS 101:2117–22 [Google Scholar]
  111. Tam R, Saier MHJ. 111.  1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiol. Rev. 57:320–46 [Google Scholar]
  112. Toews ML, Goy MF, Springer MS, Adler J. 112.  1979. Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. . PNAS 76:5544–48 [Google Scholar]
  113. Turner L, Ryu WS, Berg HC. 113.  2000. Real-time imaging of fluorescent flagellar filaments. J. Bacteriol. 182:2793–801 [Google Scholar]
  114. Underbakke ES, Zhu Y, Kiessling LL. 114.  2011. Protein footprinting in a complex milieu: identifying the interaction surfaces of the chemotaxis adaptor protein CheW. J. Mol. Biol. 409:483–95 [Google Scholar]
  115. Villa E, Schaffer M, Plitzko JM, Baumeister W. 115.  2013. Opening windows into the cell: focused-ion-beam milling for cryo-electron tomography. Curr. Opin. Struct. Biol. 23:771–77 [Google Scholar]
  116. Wadhams GH, Armitage JP. 116.  2004. Making sense of it all: bacterial chemotaxis. Nat. Rev. Mol. Cell Biol. 5:1024–37 [Google Scholar]
  117. Walz J, Tamura T, Tamura N, Grimm R, Baumeister W, Koster AJ. 117.  1997. Tricorn protease exists as an icosahedral supermolecule in vivo. Mol. Cell 1:59–65 [Google Scholar]
  118. Weis RM, Hirai T, Chalah A, Kessel M, Peters PJ, Subramaniam S. 118.  2003. Electron microscopic analysis of membrane assemblies formed by the bacterial chemotaxis receptor Tsr. J. Bacteriol. 185:3636–43 [Google Scholar]
  119. Winkler H, Zhu P, Liu J, Ye F, Roux KH, Taylor KA. 119.  2009. Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes. J. Struct. Biol. 165:64–77 [Google Scholar]
  120. Wu K, Walukiewicz HE, Glekas GD, Ordal GW, Rao CV. 120.  2011. Attractant binding induces distinct structural changes to the polar and lateral signaling clusters in Bacillus subtilis chemotaxis. J. Biol. Chem. 286:2587–95 [Google Scholar]
  121. Wuichet K, Zhulin IB. 121.  2010. Origins and diversification of a complex signal transduction system in prokaryotes. Sci. Signal 3:ra50 [Google Scholar]
  122. Zanetti G, Riches JD, Fuller SD, Briggs JAG. 122.  2009. Contrast transfer function correction applied to cryo-electron tomography and sub-tomogram averaging. J. Struct. Biol. 168:305–12 [Google Scholar]
  123. Zhang P, Bos W, Heymann J, Gnaegi H, Kessel M. 123.  et al. 2004. Direct visualization of receptor arrays in frozen-hydrated sections and plunge-frozen specimens of E. coli engineered to overproduce the chemotaxis receptor Tsr. J. Microsc. 216:76–83 [Google Scholar]
  124. Zhang P, Khursigara CM, Hartnell LM, Subramaniam S. 124.  2007. Direct visualization of Escherichia coli chemotaxis receptor arrays using cryo-electron microscopy. PNAS 104:3777–81 [Google Scholar]
  125. Zhao R, Collins EJ, Bourret RB, Silversmith RE. 125.  2002. Structure and catalytic mechanism of the E. coli chemotaxis phosphatase CheZ. Nat. Struct. Biol. 9:570–75 [Google Scholar]
/content/journals/10.1146/annurev-biophys-070816-033555
Loading
/content/journals/10.1146/annurev-biophys-070816-033555
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error