Abstract
Short-lived protein interactions determine signal transduction specificity among genetically amplified, structurally identical two-component signaling systems. Interacting protein pairs evolve recognition precision by varying residues at specific positions in the interaction surface consistent with constraints of charge, size, and chemical properties. Such positions can be detected by covariance analyses of two-component protein databases. Here, covariance is shown to identify a cluster of co-evolving dynamic residues in two-component proteins. NMR dynamics and structural studies of both wild-type and mutant proteins in this cluster suggest that motions serve to precisely arrange the site of phosphoryl transfer within the complex.
MeSH Terms
Analysis of Variance
Bacterial Proteins/chemistry,metabolism
Binding Sites
Magnetic Resonance Spectroscopy
Protein Binding
Protein Structure, Secondary
Protein Structure, Tertiary
Proteins/chemistry,metabolism
Signal Transduction
Chemicals
Bacterial Proteins
Proteins
Spo0F protein, Bacillus subtilis
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Szurmant Hendrik
Division of Cellular Biology, Department of Molecular and Experimental Medicine, The Scripps Research Institute, La Jolla, California 92037, USA.
Bobay Benjamin G
White Robert A
Sullivan Daniel M
Thompson Richele J
Hwa Terence
Hoch James A
Cavanagh John
References (15)
15 references, click to expand
-
Structure of the entire cytoplasmic portion of a sensor histidine-kinase protein.
EMBO J. 2005 Dec 21;24(24):4247-59
PMID: 16319927
-
Functional dynamics of response regulators using NMR relaxation techniques.
Methods Enzymol. 2007;423:149-65
PMID: 17609130
-
Rewiring the specificity of two-component signal transduction systems.
Cell. 2008 Jun 13;133(6):1043-54
PMID: 18555780
-
Features of protein-protein interactions in two-component signaling deduced from genomic libraries.
Methods Enzymol. 2007;422:75-101
PMID: 17628135
-
Molecular recognition in signal transduction: the interaction surfaces of the Spo0F response regulator with its cognate phosphorelay proteins revealed by alanine scanning mutagenesis.
J Mol Biol. 1997 Sep 19;272(2):200-12
PMID: 9299348
-
High-resolution NMR structure and backbone dynamics of the Bacillus subtilis response regulator, Spo0F: implications for phosphorylation and molecular recognition.
Biochemistry. 1997 Aug 19;36(33):10015-25
PMID: 9254596
-
Keeping signals straight in phosphorelay signal transduction.
J Bacteriol. 2001 Sep;183(17):4941-9
PMID: 11489844
-
Alanine mutants of the Spo0F response regulator modifying specificity for sensor kinases in sporulation initiation.
Mol Microbiol. 1999 Jul;33(2):389-95
PMID: 10411754
-
Altered recognition mutants of the response regulator PhoB: a new genetic strategy for studying protein-protein interactions.
Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14361-6
PMID: 8962056
-
Millisecond-timescale motions contribute to the function of the bacterial response regulator protein Spo0F.
Nature. 1999 Jul 15;400(6741):289-93
PMID: 10421374
-
Structural classification of bacterial response regulators: diversity of output domains and domain combinations.
J Bacteriol. 2006 Jun;188(12):4169-82
PMID: 16740923
-
Two-component and phosphorelay signal transduction.
Curr Opin Microbiol. 2000 Apr;3(2):165-70
PMID: 10745001
-
Histidine kinases and response regulator proteins in two-component signaling systems.
Trends Biochem Sci. 2001 Jun;26(6):369-76
PMID: 11406410
-
A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction.
Structure. 2000 Aug 15;8(8):851-62
PMID: 10997904
-
The crystal structure of beryllofluoride Spo0F in complex with the phosphotransferase Spo0B represents a phosphotransfer pretransition state.
J Bacteriol. 2006 Jul;188(13):4970-7
PMID: 16788205