Structural basis of histidine kinase autophosphorylation deduced by integrating genomics, molecular dynamics, and mutagenesis

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

Volumn 109, Issue 26, 2012, Pages

  Dago, Angel E ^a   Schug, Alexander ^b,c   Procaccini, Andrea ^d,e   Hoch, James A ^a   Weigt, Martin ^d,f   Szurmant, Hendrik ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

^c UMEÅ UNIVERSITY   (Sweden)

^d Human Genetics Foundation   (Italy)

^e POLITECNICO DI TORINO   (Italy)

^f SORBONNE UNIVERSITÉ   (France)

Author keywords

Biological physics; Coevolution; Protein structure prediction; Signal transduction; Two component system

Indexed keywords

ADENOSINE TRIPHOSPHATE; CYCLIC AMP DEPENDENT PROTEIN KINASE; HISTIDINE; HYBRID PROTEIN; PROTEIN HISTIDINE KINASE; PROTEIN KINASE D;

ARTICLE; AUTOPHOSPHORYLATION; BACILLUS SUBTILIS; BIOSENSOR; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME CONFORMATION; ESCHERICHIA COLI; GENOMICS; MACROMOLECULE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; SEQUENCE ANALYSIS;

BACILLUS SUBTILIS; GENOMICS; MODELS, MOLECULAR; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN CONFORMATION; PROTEIN KINASES;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 84863006375     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1201301109     Document Type: Article

References (44)

1. Gambin Y, et al. (2011) Visualizing a one-way protein encounter complex by ultrafast single-molecule mixing. Nat Meth 8:239-241.
2. Gebhardt JC, Bornschlogl T, Rief M (2010) Full distance-resolved folding energy land-scape of one single protein molecule. Proc Natl Acad Sci USA 107:2013-2018.
3. Olsson U, Wolf-Watz M (2010) Overlap between folding and functional energy land-scapes for adenylate kinase conformational change. Nat Commun 1:111.
4. Onuchic JN, Wolynes PG (2004) Theory of protein folding. Curr Opin Struct Biol 14:70-75. (Pubitemid 38249595)
5. Shaw DE, et al. (2010) Atomic-level characterization of the structural dynamics of proteins. Science 330:341-346.
6. Szurmant H, White RA, Hoch JA (2007) Sensor complexes regulating two-component signal transduction. Curr Opin Struct Biol 17:706-715. (Pubitemid 350186100)
7. Dutta R, Inouye M (2000) GHKL, an emergent ATPase/kinase superfamily. Trends Biochem Sci 25:24-28. (Pubitemid 30060426)
8. Casino P, Rubio V, Marina A (2009) Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction. Cell 139:325-336.
9. Marina A, Waldburger CD, HendricksonWA (2005) Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein. EMBO J 24:4247-4259. (Pubitemid 41828900)
10. Bick MJ, et al. (2009) How to switch off a histidine kinase: Crystal structure of Geobacillus stearothermophilus KinB with the inhibitor Sda. J Mol Biol 386:163-177.
11. Lunt B, et al. (2010) Inference of direct residue contacts in two-component signaling. Methods Enzymol 471:17-41.
12. WeigtM, White RA, Szurmant H, Hoch JA, Hwa T (2009) Identification of direct residue contacts in protein-protein interaction by message passing. Proc Natl Acad Sci USA 106:67-72.
13. Altschuh D, Lesk AM, Bloomer AC, Klug A (1987) Correlation of co-ordinated amino acid substitutions with function in viruses related to tobacco mosaic virus. J Mol Biol 193:693-707.
14. Göbel U, Sander C, Schneider R, Valencia A (1994) Correlated mutations and residue contacts in proteins. Proteins 18:309-317. (Pubitemid 24111530)
15. Neher E (1994) How frequent are correlated changes in families of protein sequences? Proc Natl Acad Sci USA 91:98-102.
16. Shindyalov IN, Kolchanov NA, Sander C (1994) Can three-dimensional contacts in protein structures be predicted by analysis of correlated mutations? Protein Eng 7:349-358. (Pubitemid 24063134)
17. Fodor AA, Aldrich RW (2004) Influence of conservation on calculations of amino acid covariance in multiple sequence alignments. Proteins 56:211-221. (Pubitemid 38850156)
18. Lockless SW, Ranganathan R (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286:295-299. (Pubitemid 29484693)
19. Morcos F, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci USA 108:E1293-E1301.
20. Schug A, et al. (2010) Computational modeling of phosphotransfer complexes in two-component signaling. Methods Enzymol 471:43-58.
21. Schug A, Weigt M, Onuchic JN, Hwa T, Szurmant H (2009) High-resolution protein complexes from integrating genomic information with molecular simulation. Proc Natl Acad Sci USA 106:22124-22129.
22. Burbulys D, Trach KA, Hoch JA (1991) Initiation of sporulation in B subtilis is controlled by a multicomponent phosphorelay. Cell 64:545-552. (Pubitemid 121002970)
23. Zapf J, Sen U, Madhusudan, Hoch JA, Varughese KI (2000) A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 8:851-862.
24. Lindorff-Larsen K, et al. (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins 78:1950-1958.
25. Oostenbrink C, Villa A, Mark AE, van Gunsteren WF (2004) A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. J Comput Chem 25:1656-1676.
26. Lange OF, et al. (2008) Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 320:1471-1475. (Pubitemid 351929422)
27. Whitford PC, Miyashita O, Levy Y, Onuchic JN (2007) Conformational transitions of adenylate kinase: Switching by cracking. J Mol Biol 366:1661-1671. (Pubitemid 46215597)
28. Miyashita O, Onuchic JN, Wolynes PG (2003) Nonlinear elasticity, proteinquakes, and the energy landscapes of functional transitions in proteins. Proc Natl Acad Sci USA 100:12570-12575. (Pubitemid 37339939)
29. Finn RD, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38:D211-D222.
30. Edgar R (2004) MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5:113.
31. Durbin R, Eddy SR, Krogh A, Mitchison G (1998) Biological Sequence Analysis: Probabilistic Models of Proteins and Nucleic Acids (Cambridge Univ Press, Cambridge).
32. Pruitt KD, Tatusova T, KlimkeW, Maglott DR (2009) NCBI reference sequences: Current status, policy and new initiatives. Nucleic Acids Res 37:D32-D36.
33. Ninfa EG, Atkinson MR, Kamberov ES, Ninfa AJ (1993) Mechanism of autophosphorylation of Escherichia coli nitrogen regulator II (NRII or NtrB): Trans-phosphorylation between subunits. J Bacteriol 175:7024-7032. (Pubitemid 23322455)
34. Cai SJ, Inouye M (2003) Spontaneous subunit exchange and biochemical evidence for trans-autophosphorylation in a dimer of Escherichia coli histidine kinase (EnvZ). J Mol Biol 329:495-503.
35. Pena-Sandoval GR, Georgellis D (2010) The ArcB sensor kinase of Escherichia coli autophosphorylates by an intramolecular reaction. J Bacteriol 192:1735-1739.
36. Tomomori C, et al. (1999) Solution structure of the homodimeric core domain of Escherichia coli histidine kinase EnvZ. Nat Struct Biol 6:729-734. (Pubitemid 29360231)
37. Cai SJ, Khorchid A, Ikura M, Inouye M (2003) Probing catalytically essential domain orientation in histidine kinase EnvZ by targeted disulfide crosslinking. J Mol Biol 328:409-418. (Pubitemid 36407583)
38. Stewart RC (2010) Protein histidine kinases: Assembly of active sites and their regulation in signaling pathways. Curr Opin Microbiol 13:133-141.
39. Sayers EW, et al. (2009) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 37:D5-D15.
40. Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755-763.
41. Schug A, Onuchic JN (2010) From protein folding to protein function and biomolecular binding by energy landscape theory. Curr Opin Pharmacol 10:709-714.
42. Whitford PC, et al. (2009) An all-atom structure-based potential for proteins: Bridging minimal models with all-atom empirical forcefields. Proteins 75:430-441.
43. Hess B, Kutzner C, van der Spoel D, Lindahl E (2008) GROMACS 4: Algorithms for highly efficient, load-balanced, and scalable molecular simulation. J Chem Theory Comput 4:435-447.
44. Grimshaw CE, et al. (1998) Synergistic kinetic interactions between components of the phosphorelay controlling sporulation in Bacillus subtilis. Biochemistry 37:1365-1375. (Pubitemid 28135726)