Structural basis of a rationally rewired protein-protein interface critical to bacterial signaling

Structure

Volumn 21, Issue 9, 2013, Pages 1636-1647

  Podgornaia, Anna I ^a,b   Casino, Patricia ^c,d   Marina, Alberto ^c,e   Laub, Michael T ^b  

^a Massachusetts Institute of Technology Cambridge   (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^c INSTITUTO DE BIOMEDICINA DE VALENCIA   (Spain)

^d INSTITUT DE BIOLOGIA MOLECULAR DE BARCELONA   (Spain)

^e INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; PHOSPHOTRANSFERASE; PROTEIN HISTIDINE KINASE;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME SPECIFICITY; ESCHERICHIA COLI; MOLECULAR EVOLUTION; MOLECULAR RECOGNITION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; THERMOTOGA MARITIMA; WILD TYPE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; THERMOTOGA MARITIMA;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; ESCHERICHIA COLI; MODELS, MOLECULAR; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; THERMOTOGA MARITIMA;

EID: 84883489489     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2013.07.005     Document Type: Article

References (35)

1. A. Aharoni, L. Gaidukov, O. Khersonsky, S. McQ Gould, C. Roodveldt, D.S. Tawfik, and D.S. Tawfik The 'evolvability' of promiscuous protein functions Nat. Genet. 37 2005 73 76
2. D. Albanesi, M. Martín, F. Trajtenberg, M.C. Mansilla, A. Haouz, P.M. Alzari, D. de Mendoza, and A. Buschiazzo Structural plasticity and catalysis regulation of a thermosensor histidine kinase Proc. Natl. Acad. Sci. USA 106 2009 16185 16190
3. E. Alm, K. Huang, and A. Arkin The evolution of two-component systems in bacteria reveals different strategies for niche adaptation PLoS Comput. Biol. 2 2006 e143
4. O. Ashenberg, A.E. Keating, and M.T. Laub Helix bundle loops determine whether histidine kinases autophosphorylate in cis or in trans J. Mol. Biol. 425 2013 1198 1209
5. C.H. Bell, S.L. Porter, A. Strawson, D.I. Stuart, and J.P. Armitage Using structural information to change the phosphotransfer specificity of a two-component chemotaxis signalling complex PLoS Biol. 8 2010 e1000306
6. M.S. Breen, C. Kemena, P.K. Vlasov, C. Notredame, and F.A. Kondrashov Epistasis as the primary factor in molecular evolution Nature 490 2012 535 538
7. E.J. Capra, and M.T. Laub Evolution of two-component signal transduction systems Annu. Rev. Microbiol. 66 2012 325 347
8. E.J. Capra, B.S. Perchuk, E.A. Lubin, O. Ashenberg, J.M. Skerker, and M.T. Laub Systematic dissection and trajectory-scanning mutagenesis of the molecular interface that ensures specificity of two-component signaling pathways PLoS Genet. 6 2010 e1001220
9. E.J. Capra, B.S. Perchuk, J.M. Skerker, and M.T. Laub Adaptive mutations that prevent crosstalk enable the expansion of paralogous signaling protein families Cell 150 2012 222 232
10. P. Casino, V. Rubio, and A. Marina Structural insight into partner specificity and phosphoryl transfer in two-component signal transduction Cell 139 2009 325 336
11. P. Casino, V. Rubio, and A. Marina The mechanism of signal transduction by two-component systems Curr. Opin. Struct. Biol. 20 2010 763 771
12. T.S. Chen, and A.E. Keating Designing specific protein-protein interactions using computation, experimental library screening, or integrated methods Protein Sci. 21 2012 949 963
13. F.M. Codoñer, and M.A. Fares Why should we care about molecular coevolution? Evol. Bioinform. Online 4 2008 29 38
14. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
15. S.L. Fisher, S.K. Kim, B.L. Wanner, and C.T. Walsh Kinetic comparison of the specificity of the vancomycin resistance VanSfor two response regulators, VanR and PhoB Biochemistry 35 1996 4732 4740
16. M.Y. Galperin A census of membrane-bound and intracellular signal transduction proteins in bacteria: bacterial IQ, extroverts and introverts BMC Microbiol. 5 2005 35
17. R. Gao, and A.M. Stock Biological insights from structures of two-component proteins Annu. Rev. Microbiol. 63 2009 133 154
18. W. Hsing, and T.J. Silhavy Function of conserved histidine-243 in phosphatase activity of EnvZ, the sensor for porin osmoregulation in Escherichia coli J. Bacteriol. 179 1997 3729 3735
19. E.L. Humphris, and T. Kortemme Prediction of protein-protein interface sequence diversity using flexible backbone computational protein design Structure 16 2008 1777 1788
20. T.N. Huynh, and V. Stewart Negative control in two-component signal transduction by transmitter phosphatase activity Mol. Microbiol. 82 2011 275 286
21. M.M. Igo, A.J. Ninfa, J.B. Stock, and T.J. Silhavy Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor Genes Dev. 3 1989 1725 1734
22. S. Jagadeesan, P. Mann, C.W. Schink, and P.I. Higgs A novel "four-component" two-component signal transduction mechanism regulates developmental progression in Myxococcus xanthus J. Biol. Chem. 284 2009 21435 21445
23. O. Keskin, A. Gursoy, B. Ma, and R. Nussinov Principles of protein-protein interactions: what are the preferred ways for proteins to interact? Chem. Rev. 108 2008 1225 1244
24. M.T. Laub, and M. Goulian Specificity in two-component signal transduction pathways Annu. Rev. Genet. 41 2007 121 145
25. R.A. Lee, M. Razaz, and S. Hayward The DynDom database of protein domain motions Bioinformatics 19 2003 1290 1291
26. K.B. Levin, O. Dym, S. Albeck, S. Magdassi, A.H. Keeble, C. Kleanthous, and D.S. Tawfik Following evolutionary paths to protein-protein interactions with high affinity and selectivity Nat. Struct. Mol. Biol. 16 2009 1049 1055
27. I. Matsumura, and A.D. Ellington In vitro evolution of beta-glucuronidase into a beta-galactosidase proceeds through non-specific intermediates J. Mol. Biol. 305 2001 331 339
28. E.A. Ortlund, J.T. Bridgham, M.R. Redinbo, and J.W. Thornton Crystal structure of an ancient protein: evolution by conformational epistasis Science 317 2007 1544 1548
29. Y. Pazy, A.C. Wollish, S.A. Thomas, P.J. Miller, E.J. Collins, R.B. Bourret, and R.E. Silversmith Matching biochemical reaction kinetics to the timescales of life: structural determinants that influence the autodephosphorylation rate of response regulator proteins J. Mol. Biol. 392 2009 1205 1220
30. J.M. Skerker, M.S. Prasol, B.S. Perchuk, E.G. Biondi, and M.T. Laub Two-component signal transduction pathways regulating growth and cell cycle progression in a bacterium: a system-level analysis PLoS Biol. 3 2005 e334
31. J.M. Skerker, B.S. Perchuk, A. Siryaporn, E.A. Lubin, O. Ashenberg, M. Goulian, and M.T. Laub Rewiring the specificity of two-component signal transduction systems Cell 133 2008 1043 1054
32. C.A. Smith, and T. Kortemme Backrub-like backbone simulation recapitulates natural protein conformational variability and improves mutant side-chain prediction J. Mol. Biol. 380 2008 742 756
33. A.M. Stock, V.L. Robinson, and P.N. Goudreau Two-component signal transduction Annu. Rev. Biochem. 69 2000 183 215
34. D.M. Weinreich, N.F. Delaney, M.A. Depristo, and D.L. Hartl Darwinian evolution can follow only very few mutational paths to fitter proteins Science 312 2006 111 114
35. J. Zapf, M. Madhusudan, C.E. Grimshaw, J.A. Hoch, K.I. Varughese, and J.M. Whiteley A source of response regulator autophosphatase activity: the critical role of a residue adjacent to the Spo0F autophosphorylation active site Biochemistry 37 1998 7725 7732