Table of Contents
Journal of Biophysics
Volume 2008, Article ID 267912, 11 pages
http://dx.doi.org/10.1155/2008/267912
Research Article

Flexibility of the Cytoplasmic Domain of the Phototaxis Transducer II from Natronomonas pharaonis

1Institute for Structural Biology (IBI-2), Research Center Jülich, 52425 Jülich, Germany
2Department of Structural Biology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15260, USA

Received 29 May 2008; Accepted 21 July 2008

Academic Editor: Thomas P. Burghardt

Copyright © 2008 Ivan L. Budyak et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. J. Falke, R. B. Bass, S. L. Butler, S. A. Chervitz, and M. A. Danielson, “The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes,” Annual Review of Cell and Developmental Biology, vol. 13, pp. 457–512, 1997. View at Publisher · View at Google Scholar
  2. W. D. Hoff, K.-H. Jung, and J. L. Spudich, “Molecular mechanism of photosignaling by archaeal sensory rhodopsins,” Annual Review of Biophysics and Biomolecular Structure, vol. 26, pp. 223–258, 1997. View at Publisher · View at Google Scholar
  3. W. Zhang, A. Brooun, M. M. Mueller, and M. Alam, “The primary structures of the Archaeon Halobacterium salinarium blue light receptor sensory rhodopsin II and its transducer, a methyl-accepting protein,” Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 16, pp. 8230–8235, 1996. View at Publisher · View at Google Scholar
  4. H. Luecke, B. Schobert, J. K. Lanyi, E. N. Spudich, and J. L. Spudich, “Crystal structure of sensory rhodopsin II at 2.4 angstroms: insights into color tuning and transducer interaction,” Science, vol. 293, no. 5534, pp. 1499–1503, 2001. View at Publisher · View at Google Scholar
  5. A. Royant, P. Nollert, K. Edman et al., “X-ray structure of sensory rhodopsin II at 2.1-Å?resolution,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 18, pp. 10131–10136, 2001. View at Publisher · View at Google Scholar
  6. V. I. Gordeliy, J. Labahn, R. Moukhametzianov et al., “Molecular basis of transmembrane signalling by sensory rhodopsin II–transducer complex,” Nature, vol. 419, no. 6906, pp. 484–487, 2002. View at Publisher · View at Google Scholar
  7. R. Moukhametzianov, J. P. Klare, R. Efremov et al., “Development of the signal in sensory rhodopsin and its transfer to the cognate transducer,” Nature, vol. 440, no. 7080, pp. 115–119, 2006. View at Publisher · View at Google Scholar
  8. Y. Sudo, H. Okuda, M. Yamabi et al., “Linker region of a halobacterial transducer protein interacts directly with its sensor retinal protein,” Biochemistry, vol. 44, no. 16, pp. 6144–6152, 2005. View at Publisher · View at Google Scholar
  9. E. Bordignon, J. P. Klare, M. Doebber et al., “Structural analysis of a HAMP domain: the linker region of the phototransducer in complex with sensory rhodopsin II,” The Journal of Biological Chemistry, vol. 280, no. 46, pp. 38767–38775, 2005. View at Publisher · View at Google Scholar
  10. H. Le Moual and D. E. Koshland Jr., “Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis,” Journal of Molecular Biology, vol. 261, no. 4, pp. 568–585, 1996. View at Publisher · View at Google Scholar
  11. A. Bateman, L. Coin, R. Durbin et al., “The Pfam protein families database,” Nucleic Acids Research, vol. 32, database issue, pp. D138–D141, 2004. View at Publisher · View at Google Scholar
  12. K.-H. Jung, E. N. Spudich, V. D. Trivedi, and J. L. Spudich, “An archaeal photosignal-transducing module mediates phototaxis in Escherichia coli,” Journal of Bacteriology, vol. 183, no. 21, pp. 6365–6371, 2001. View at Publisher · View at Google Scholar
  13. K. K. Kim, H. Yokota, and S.-H. Kim, “Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor,” Nature, vol. 400, no. 6746, pp. 787–792, 1999. View at Publisher · View at Google Scholar
  14. S.-H. Kim, W. Wang, and K. K. Kim, “Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 18, pp. 11611–11615, 2002. View at Publisher · View at Google Scholar
  15. S. H. Kim, ““Frozen” dynamic dimer model for transmembrane signaling in bacterial chemotaxis receptors,” Protein Science, vol. 3, no. 2, pp. 159–165, 1994. View at Google Scholar
  16. S. K. Seeley, G. K. Wittrock, L. K. Thompson, and R. M. Weis, “Oligomers of the cytoplasmic fragment from the Escherichia coli aspartate receptor dissociate through an unfolded transition state,” Biochemistry, vol. 35, no. 50, pp. 16336–16345, 1996. View at Publisher · View at Google Scholar
  17. J. Wu, D. G. Long, and R. M. Weis, “Reversible dissociation and unfolding of the Escherichia coli aspartate receptor cytoplasmic fragment,” Biochemistry, vol. 34, no. 9, pp. 3056–3065, 1995. View at Publisher · View at Google Scholar
  18. S. K. Seeley, R. M. Weis, and L. K. Thompson, “The cytoplasmic fragment of the aspartate receptor displays globally dynamic behavior,” Biochemistry, vol. 35, no. 16, pp. 5199–5206, 1996. View at Publisher · View at Google Scholar
  19. O. J. Murphy III, X. Yi, R. M. Weis, and L. K. Thompson, “Hydrogen exchange reveals a stable and expandable core within the aspartate receptor cytoplasmic domain,” The Journal of Biological Chemistry, vol. 276, no. 46, pp. 43262–43269, 2001. View at Publisher · View at Google Scholar
  20. I. L. Budyak, V. Pipich, O. S. Mironova, R. Schlesinger, G. Zaccai, and J. Klein-Seetharaman, “Shape and oligomerization state of the cytoplasmic domain of the phototaxis transducer II from Natronobacterium pharaonis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 42, pp. 15428–15433, 2006. View at Publisher · View at Google Scholar
  21. N. Sreerama and R. W. Woody, “Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set,” Analytical Biochemistry, vol. 287, no. 2, pp. 252–260, 2000. View at Publisher · View at Google Scholar
  22. I. H. van Stokkum, H. J. Spoelder, M. Bloemendal, R. van Grondelle, and F. C. Groen, “Estimation of protein secondary structure and error analysis from circular dichroism spectra,” Analytical Biochemistry, vol. 191, no. 1, pp. 110–118, 1990. View at Publisher · View at Google Scholar
  23. N. Sreerama, S. Y. Venyaminov, and R. W. Woody, “Estimation of protein secondary structure from circular dichroism spectra: inclusion of denatured proteins with native proteins in the analysis,” Analytical Biochemistry, vol. 287, no. 2, pp. 243–251, 2000. View at Publisher · View at Google Scholar
  24. P. Pancoska, E. Bitto, V. Janota, M. Urbanova, V. P. Gupta, and T. A. Keiderling, “Comparison of and limits of accuracy for statistical analyses of vibrational and electronic circular dichroism spectra in terms of correlations to and predictions of protein secondary structure,” Protein Science, vol. 4, no. 7, pp. 1384–1401, 1995. View at Google Scholar
  25. R. Pribić, I. H. M. van Stokkum, D. Chapman, P. I. Haris, and M. Bloemendal, “Protein secondary structure from Fourier transform infrared and/or circular dichroism spectra,” Analytical Biochemistry, vol. 214, no. 2, pp. 366–378, 1993. View at Publisher · View at Google Scholar
  26. J. D. Hirst and C. L. Brooks III, “Helicity, circular dichroism and molecular dynamics of proteins,” Journal of Molecular Biology, vol. 243, no. 2, pp. 173–178, 1994. View at Publisher · View at Google Scholar
  27. D. I. Freedberg, R. Ishima, J. Jacob et al., “Rapid structural fluctuations of the free HIV protease flaps in solution: relationship to crystal structures and comparison with predictions of dynamics calculations,” Protein Science, vol. 11, no. 2, pp. 221–232, 2002. View at Publisher · View at Google Scholar
  28. W. H. Press, B. P. Flannery, S. A. Teukolsky, and W. T. Vetterling, Numerical Recipes in C, Cambridge University Press, Cambridge, UK, 1988.
  29. C. Combet, C. Blanchet, C. Geourjon, and G. Deléage, “NPS@: network protein sequence analysis,” Trends in Biochemical Sciences, vol. 25, no. 3, pp. 147–150, 2000. View at Publisher · View at Google Scholar
  30. A. Lupas, M. Van Dyke, and J. Stock, “Predicting coiled coils from protein sequences,” Science, vol. 252, no. 5010, pp. 1162–1164, 1991. View at Publisher · View at Google Scholar
  31. P. Romero, Z. Obradovic, X. Li, E. C. Garner, C. J. Brown, and A. K. Dunker, “Sequence complexity of disordered protein,” Proteins, vol. 42, no. 1, pp. 38–48, 2001. View at Publisher · View at Google Scholar
  32. R. Thomson, T. C. Hodgman, Z. R. Yang, and A. K. Doyle, “Characterizing proteolytic cleavage site activity using bio-basis function neural networks,” Bioinformatics, vol. 19, no. 14, pp. 1741–1747, 2003. View at Publisher · View at Google Scholar
  33. Z. R. Yang, R. Thomson, P. McNeil, and R. M. Esnouf, “RONN: the bio-basis function neural network technique applied to the detection of natively disordered regions in proteins,” Bioinformatics, vol. 21, no. 16, pp. 3369–3376, 2005. View at Publisher · View at Google Scholar
  34. J. L. R. Arrondo, A. Muga, J. Castresana, and F. M. Goñi, “Quantitative studies of the structure of proteins in solution by Fourier-transform infrared spectroscopy,” Progress in Biophysics and Molecular Biology, vol. 59, no. 1, pp. 23–56, 1993. View at Publisher · View at Google Scholar
  35. E. R. Nightingale, “Phenomenological theory of ion solvation. Effective radii of hydrated ions,” Journal of Physical Chemistry, vol. 63, no. 9, pp. 1381–1387, 1959. View at Publisher · View at Google Scholar
  36. M. Ginzburg and B. Z. Ginzburg, “Distribution of non-electrolytes in Halobacterium cells. I. Halobacterium marismortui,” Biochimica et Biophysica Acta, vol. 584, no. 3, pp. 398–406, 1979. View at Google Scholar
  37. H. J. Dyson and P. E. Wright, “Nuclear magnetic resonance methods for elucidation of structure and dynamics in disordered states,” Methods in Enzymology, vol. 339, pp. 258–270, 2001. View at Publisher · View at Google Scholar
  38. J. Klein-Seetharaman, M. Oikawa, S. B. Grimshaw et al., “Long-range interactions within a nonnative protein,” Science, vol. 295, no. 5560, pp. 1719–1722, 2002. View at Publisher · View at Google Scholar
  39. J. H. B. Christian and J. A. Waltho, “Solute concentrations within cells of halophilic and non-halophilic bacteria,” Biochimica et Biophysica Acta, vol. 65, no. 3, pp. 506–508, 1962. View at Publisher · View at Google Scholar
  40. M. C. Lai and R. P. Gunsalus, “Glycine betaine and potassium ion are the major compatible solutes in the extremely halophilic methanogen Methanohalophilus strain Z7302,” Journal of Bacteriology, vol. 174, no. 22, pp. 7474–7477, 1992. View at Google Scholar
  41. F. Hofmeister, “Zur Lehre von der Wirkung der Salze,” Naunyn-Schmiedeberg's Archives of Pharmacology, vol. 24, no. 4-5, pp. 247–260, 1888. View at Publisher · View at Google Scholar
  42. P. R. Davis-Searles, A. J. Saunders, D. A. Erie, D. J. Winzor, and G. J. Pielak, “Interpreting the effects of small uncharged solutes on protein-folding equilibria,” Annual Review of Biophysics and Biomolecular Structure, vol. 30, pp. 271–306, 2001. View at Publisher · View at Google Scholar
  43. V. A. Parsegian, R. P. Rand, and D. C. Rau, “Osmotic stress, crowding, preferential hydration, and binding: a comparison of perspectives,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 8, pp. 3987–3992, 2000. View at Publisher · View at Google Scholar
  44. A. J. Saunders, P. R. Davis-Searles, D. L. Allen, G. J. Pielak, and D. A. Erie, “Osmolyte-induced changes in protein conformational equilibria,” Biopolymers, vol. 53, no. 4, pp. 293–307, 2000. View at Publisher · View at Google Scholar
  45. J. A. Schellman, “Fifty years of solvent denaturation,” Biophysical Chemistry, vol. 96, no. 2-3, pp. 91–101, 2002. View at Publisher · View at Google Scholar
  46. F. Bonneté, D. Madern, and G. Zaccai, “Stability against denaturation mechanisms in halophilic malate dehydrogenase “adapt” to solvent conditions,” Journal of Molecular Biology, vol. 244, no. 4, pp. 436–447, 1994. View at Publisher · View at Google Scholar
  47. C. Ebel, L. Costenaro, M. Pascu et al., “Solvent interactions of halophilic malate dehydrogenase,” Biochemistry, vol. 41, no. 44, pp. 13234–13244, 2002. View at Publisher · View at Google Scholar
  48. L. Costenaro, G. Zaccai, and C. Ebel, “Link between protein-solvent and weak protein-protein interactions gives insight into halophilic adaptation,” Biochemistry, vol. 41, no. 44, pp. 13245–13252, 2002. View at Publisher · View at Google Scholar
  49. D. Madern, C. Ebel, and G. Zaccai, “Halophilic adaptation of enzymes,” Extremophiles, vol. 4, no. 2, pp. 91–98, 2000. View at Publisher · View at Google Scholar
  50. J. A. Schellman, “Protein stability in mixed solvents: a balance of contact interaction and excluded volume,” Biophysical Journal, vol. 85, no. 1, pp. 108–125, 2003. View at Google Scholar
  51. C. J. Camacho and C. Zhang, “FastContact: rapid estimate of contact and binding free energies,” Bioinformatics, vol. 21, no. 10, pp. 2534–2536, 2005. View at Publisher · View at Google Scholar
  52. S. R. Comeau, D. W. Gatchell, S. Vajda, and C. J. Camacho, “ClusPro: a fully automated algorithm for protein-protein docking,” Nucleic Acids Research, vol. 32, web server issue, pp. W96–W99, 2004. View at Publisher · View at Google Scholar
  53. K. D. Collins, “Ion hydration: implications for cellular function, polyelectrolytes, and protein crystallization,” Biophysical Chemistry, vol. 119, no. 3, pp. 271–281, 2006. View at Publisher · View at Google Scholar
  54. R. B. Bass and J. J. Falke, “Detection of a conserved α-helix in the kinase-docking region of the aspartate receptor by cysteine and disulfide scanning,” The Journal of Biological Chemistry, vol. 273, no. 39, pp. 25006–25014, 1998. View at Publisher · View at Google Scholar
  55. R. B. Bass, M. D. Coleman, and J. J. Falke, “Signaling domain of the aspartate receptor is a helical hairpin with a localized kinase docking surface: cysteine and disulfide scanning studies,” Biochemistry, vol. 38, no. 29, pp. 9317–9327, 1999. View at Publisher · View at Google Scholar
  56. M. G. Surette and J. B. Stock, “Role of α-helical coiled-coil interactions in receptor dimerization, signaling, and adaptation during bacterial chemotaxis,” The Journal of Biological Chemistry, vol. 271, no. 30, pp. 17966–17973, 1996. View at Publisher · View at Google Scholar
  57. M. A. Trammell and J. J. Falke, “Identification of a site critical for kinase regulation on the central processing unit (CPU) helix of the aspartate receptor,” Biochemistry, vol. 38, no. 1, pp. 329–336, 1999. View at Publisher · View at Google Scholar
  58. A. L. Fink, “Natively unfolded proteins,” Current Opinion in Structural Biology, vol. 15, no. 1, pp. 35–41, 2005. View at Publisher · View at Google Scholar
  59. R. M. Williams, Z. Obradovi, V. Mathura et al., “The protein non-folding problem: amino acid determinants of intrinsic order and disorder,” in Proceedings of the 6th Pacific Symposium on Biocomputing (PSB '01), pp. 89–100, The Big Island of Hawaii, Hawaii, USA, January 2001.
  60. R. L. Baldwin and B. H. Zimm, “Are denatured proteins ever random coils?” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 23, pp. 12391–12392, 2000. View at Publisher · View at Google Scholar
  61. P. H. Yancey, M. E. Clark, S. C. Hand, R. D. Bowlus, and G. N. Somero, “Living with water stress: evolution of osmolyte systems,” Science, vol. 217, no. 4566, pp. 1214–1222, 1982. View at Publisher · View at Google Scholar
  62. M. M. Dedmon, C. N. Patel, G. B. Young, and G. J. Pielak, “FlgM gains structure in living cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 20, pp. 12681–12684, 2002. View at Publisher · View at Google Scholar
  63. V. N. Uversky, J. R. Gillespie, and A. L. Fink, “Why are “natively unfolded” proteins unstructured under physiologic conditions?” Proteins, vol. 41, no. 3, pp. 415–427, 2000. View at Publisher · View at Google Scholar