The HAMP Domain Structure Implies Helix Rotation in Transmembrane Signaling

Cell

Volumn 126, Issue 5, 2006, Pages 929-940

  Hulko, Michael ^a   Berndt, Franziska ^b   Gruber, Markus ^a   Linder, Jürgen U ^b   Truffault, Vincent ^a   Schultz, Anita ^b   Martin, Jörg ^a   Schultz, Joachim E ^b   Lupas, Andrei N ^a   Coles, Murray ^a  

^a MAX PLANCK INSTITUTE FOR DEVELOPMENTAL BIOLOGY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ALANINE; HELIX LOOP HELIX PROTEIN; PHOSPHATASE; PROTEIN HISTIDINE KINASE; RECEPTOR;

ARTICLE; CHEMOTAXIS; CONFORMATION; ESCHERICHIA COLI; IN VITRO STUDY; IN VIVO STUDY; MYCOBACTERIUM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN STRUCTURE; ROTATION; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; WILD TYPE;

ARCHAEA;

EID: 33748183257     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cell.2006.06.058     Document Type: Article

References (46)

1. Alberti S., Oehler S., von Wilcken-Bergmann B., and Müller-Hill B. Genetic analysis of the leucine heptad repeats of Lac repressor: evidence for a 4-helical bundle. EMBO J. 12 (1993) 3227-3236
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., and Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997) 3389-3402
3. Appleman J.A., and Stewart V. Mutational analysis of a conserved signal-transducing element: the HAMP linker of the Escherichia coli nitrate sensor NarX. J. Bacteriol. 185 (2003) 89-97
4. Appleman J.A., Chen L.L., and Stewart V. Probing conservation of HAMP linker structure and signal transduction mechanism through analysis of hybrid sensor kinases. J. Bacteriol. 185 (2003) 4872-4882
5. Aravind L., and Ponting C.P. The cytoplasmic helical linker domain of receptor histidine kinase and methyl-accepting proteins is common to many prokaryotic signalling proteins. FEMS Microbiol. Lett. 176 (1999) 111-116
6. Berg H.C. Random Walks in Biology (1993), Princeton University Press, Princeton, NJ
7. Bordignon E., Klare J.P., Doebber M., Wegener A.A., Martell S., Engelhard M., and Steinhoff H.J. Structural analysis of a HAMP domain: the linker region of the phototransducer in complex with sensory rhodopsin II. J. Biol. Chem. 280 (2005) 38767-38775
8. Butler S.L., and Falke J.J. Cysteine and disulfide scanning reveals two amphiphilic helices in the linker region of the aspartate chemoreceptor. Biochemistry 37 (1998) 10746-10756
9. Chervitz S.A., and Falke J.J. Molecular mechanism of transmembrane signaling by the aspartate receptor: a model. Proc. Natl. Acad. Sci. USA 93 (1996) 2545-2550
10. Cochran A.G., and Kim P.S. Imitation of Escherichia coli aspartate receptor signaling in engineered dimers of the cytoplasmic domain. Science 271 (1996) 1113-1116
11. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
12. Crick F.H.C. The packing of α-helices: simple coiled-coils. Acta Crystallogr. 6 (1953) 689-697
13. Deng Y., Liu J., Zheng Q., Eliezer D., Kallenbach N.R., and Lu M. Antiparallel four-stranded coiled coil specified by a 3-3-1 hydrophobic heptad repeat. Structure 14 (2006) 247-255
14. Diercks T., Coles M., and Kessler H. An efficient strategy for assignment of cross-peaks in 3D heteronuclear NOESY experiments. J. Biomol. NMR 15 (1999) 177-180
15. Farrow N.A., Muhandiram R., Singer A.U., Pascal S.M., Kay C.M., Gish G., Shoelson S.E., Pawson T., Forman-Kay J.D., and Kay L.E. Backbone dynamics of a free and phosphopeptide-complexed Src homology 2 domain studied by 15N NMR relaxation. Biochemistry 33 (1994) 5984-6003
16. Gemmecker G., Jahnke W., and Kessler H. Measurement of fast proton exchange rates in isotopically labeled compounds. J. Am. Chem. Soc. 115 (1993) 11620-11621
17. Gernert K.M., Surles M.C., Labean T.H., Richardson J.S., and Richardson D.C. The Alacoil: a very tight, antiparallel coiled-coil of helices. Protein Sci. 4 (1995) 2252-2260
18. Gruber M., and Lupas A.N. Historical review: another 50th anniversary-new periodicities in coiled coils. Trends Biochem. Sci. 28 (2003) 679-685
19. Jin T., and Inouye M. Transmembrane signaling. Mutational analysis of the cytoplasmic linker region of Taz1-1, a Tar-EnvZ chimeric receptor in Escherichia coli. J. Mol. Biol. 244 (1994) 477-481
20. Kim K.K., Yokota H., and Kim S.H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400 (1999) 787-792
21. Koide S., Jahnke W., and Wright P.E. Measurement of intrinsic exchange rates of amide protons in a 15N-labeled peptide. J. Biomol. NMR 6 (1995) 306-312
22. Koretke K.K., Lupas A.N., Warren P.V., Rosenberg M., and Brown J.R. Evolution of two-component signal transduction. Mol. Biol. Evol. 17 (2000) 1956-1970
23. Koretke K.K., Volker C., Bower M.L., and Lupas A.N. In Histidine Kinases In Signal Transduction. In: Inouye M., and Dutta R. (Eds) (2003), Academic Press, New York 483-506
24. Kyte J., and Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157 (1982) 105-132
25. Laskowski R.A., MacArthur M.W., Moss D.S., and Thornton J.M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26 (1993) 283-291
26. Linder J.U., Hammer A., and Schultz J.E. The effect of HAMP domains on class IIIb adenylyl cyclases from Mycobacterium tuberculosis. Eur. J. Biochem. 271 (2004) 2446-2451
27. Lupas A.N., and Gruber M. The structure of alpha-helical coiled coils. Adv. Protein Chem. 70 (2005) 37-78
28. Miller A.S., and Falke J.J. Side chains at the membrane-water interface modulate the signaling state of a transmembrane receptor. Biochemistry 43 (2004) 1763-1770
29. Moukhametzianov R., Klare J.P., Efremov R., Baeken C., Goppner A., Labahn J., Engelhard M., Buldt G., and Gordeliy V.I. Development of the signal in sensory rhodopsin and its transfer to the cognate transducer. Nature 440 (2006) 115-119
30. Ottemann K.M., Xiao W., Shin Y.K., and Koshland Jr. D.E. A piston model for transmembrane signaling of the aspartate receptor. Science 285 (1999) 1751-1754
31. Schwieters C.D., Kuszewski J.J., Tjandra N., and Clore G.M. The Xplor-NIH NMR Molecular Structure Determination Package. J. Magn. Res. 160 (2003) 66-74
32. Scott W.G., and Stoddard B.L. Transmembrane signalling and the aspartate receptor. Structure 2 (1994) 877-887
33. Singh M., Berger B., Kim P.S., Berger J.M., and Cochran A.G. Computational learning reveals coiled coil-like motifs in histidine kinase linker domains. Proc. Natl. Acad. Sci. USA 95 (1998) 2738-2743
34. Sinha S.C., Wetterer M., Sprang S.R., Schultz J.E., and Linder J.U. Origin of asymmetry in adenylyl cyclases: structures of Mycobacterium tuberculosis Rv1900c. EMBO J. 24 (2005) 663-673
35. Solan A., Ratia K., and Fairman R. Exploring the role of alanine in the structure of the Lac repressor tetramerization domain, a ferritin-like Alacoil. J. Mol. Biol. 317 (2002) 601-612
36. Tao W., Malone C.L., Ault A.D., Deschenes R.J., and Fassler J.S. A cytoplasmic coiled-coil domain is required for histidine kinase activity of the yeast osmosensor, SLN1. Mol. Microbiol. 43 (2002) 459-473
37. Tews I., Findeisen F., Sinning I., Schultz A., Schultz J.E., and Linder J.U. The structure of a pH-sensing mycobacterial adenylyl cyclase holoenzyme. Science 308 (2005) 1020-1023
38. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., and Higgins D.G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25 (1997) 4876-4882
39. Tokishita S., Kojima A., and Mizuno T. Transmembrane signal transduction and osmoregulation in Escherichia coli: functional importance of the transmembrane regions of membrane-located protein kinase, EnvZ. J. Biochem. (Tokyo) 111 (1992) 707-713
40. Truffault V., Coles M., Diercks T., Abelmann K., Eberhardt S., Luttgen H., Bacher A., and Kessler H. The solution structure of the N-terminal domain of riboflavin synthase. J. Mol. Biol. 309 (2001) 949-960
41. Utsumi R., Brissette R.E., Rampersaud A., Forst S.A., Oosawa K., and Inouye M. Activation of bacterial porin gene expression by a chimeric signal transducer in response to aspartate. Science 245 (1989) 1246-1249
42. Wang A.C., and Bax A. Reparametrization of the karplus relation for 3J(H.alpha.-N) and 3J(HN-C′) in Peptides from uniformly 13C/15N-enriched human ubiquitin. J. Am. Chem. Soc. 117 (1995) 1810-1813
43. Williams S.B., and Stewart V. Functional similarities among two-component sensors and methyl-accepting chemotaxis proteins suggest a role for linker region amphipathic helices in transmembrane signal transduction. Mol. Microbiol. 33 (1999) 1093-1102
44. Yadav M.K., Redman J.E., Leman L.J., Alvarez-Gutierrez J.M., Zhang Y., Stout C.D., and Ghadiri M.R. Structure-based engineering of internal cavities in coiled-coil peptides. Biochemistry 44 (2005) 9723-9732
45. Yadav M.K., Leman L.J., Price D.J., Brooks III C.L., Stout C.D., and Ghadiri M.R. Coiled coils at the edge of configurational heterogeneity. Structural analyses of parallel and antiparallel homotetrameric coiled coils reveal configurational sensitivity to a single solvent-exposed amino acid substitution. Biochemistry 45 (2006) 4463-4473
46. Zhu Y., and Inouye M. Analysis of the role of the EnvZ linker region in signal transduction using a chimeric Tar/EnvZ receptor protein, Tez1. J. Biol. Chem. 278 (2003) 22812-22819