Inherent regulation of EAL domain-catalyzed hydrolysis of second messenger cyclic di-GMP

Journal of Biological Chemistry

Volumn 289, Issue 10, 2014, Pages 6978-6990

  Sundriyal, Amit ^a   Massa, Claudia ^a   Samoray, Dietrich ^a   Zehender, Fabian ^a,b   Sharpe, Timothy ^a   Jenal, Urs ^a   Schirmer, Tilman ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b NanoTemper Technologies GmbH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DIMERIZATION; ESTERS;

CATALYTIC DOMAINS; CENTRAL NODES; GENERIC MECHANISM; HOMODIMERS; PHOSPHODIESTERASES; SECOND MESSENGER; SUBSTRATE BINDING;

MOLECULAR BIOLOGY;

CALCIUM ION; CYCLIC DI GMP; CYCLIC GMP; DIMER; MAGNESIUM ION; MONOMER; PHOSPHODIESTERASE; UNCLASSIFIED DRUG; YAHA PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; DIMERIZATION; EAL DOMAIN; ENZYME ACTIVITY; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN HYDROLYSIS; PROTEIN SECONDARY STRUCTURE; REGULATORY MECHANISM; THERMODYNAMICS;

ALLOSTERIC REGULATION; BACTERIAL SIGNAL TRANSDUCTION; C-DI-GMP SIGNALING; CHROMATOGRAPHY; CRYSTAL STRUCTURE; PHOSPHODIESTERASES; SECOND MESSENGER;

3',5'-CYCLIC-GMP PHOSPHODIESTERASES; AMINO ACID SEQUENCE; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; CYCLIC GMP; ESCHERICHIA COLI PROTEINS; HYDROLYSIS; MOLECULAR SEQUENCE DATA; PROTEIN MULTIMERIZATION; PROTEIN STRUCTURE, TERTIARY; SECOND MESSENGER SYSTEMS;

EID: 84896790464     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.516195     Document Type: Article

References (37)

1. Hengge, R. (2009) Principles of c-di-GMP signalling in bacteria. Nat. Rev. Microbiol. 7, 263-273
2. Römling, U., Galperin, M. Y., and Gomelsky, M. (2013) Cyclic di-GMP/ The first 25 years of a universal bacterial second messenger. Microbiol. Mol. Biol. Rev. 77, 1-52
3. Wassmann, P., Chan, C., Paul, R., Beck, A., Heerklotz, H., Jenal, U., and Schirmer, T. (2007) Structure of BeF3-modified response regulator PleD. Implications for diguanylate cyclase activation, catalysis, and feedback inhibition. Structure 15, 915-927
4. Paul, R., Abel, S., Wassmann, P., Beck, A., Heerklotz, H., and Jenal, U. (2007) Activation of the diguanylate cyclase PleD by phosphorylationmediated dimerization. J. Biol. Chem. 282, 29170-29177
5. De, N., Pirruccello, M., Krasteva, P. V., Bae, N., Raghavan, R. V., and Sondermann, H. (2008) Phosphorylation-independent regulation of the diguanylate cyclase WspR. PLoS Biol. 6, e67
6. Schirmer, T., and Jenal, U. (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat. Rev. Microbiol. 7, 724-735
7. Zähringer, F., Lacanna, E., Jenal, U., Schirmer, T., and Boehm, A. (2013) Structure and signaling mechanism of a zinc-sensory diguanylate cyclase. Structure 21, 1149-1157
8. Christen, M., Christen, B., Folcher, M., Schauerte, A., and Jenal, U. (2005) Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 280, 30829-30837
9. Schmidt, A. J., Ryjenkov, D. A., and Gomelsky, M. (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase. Enzymatically active and inactive EAL domains. J. Bacteriol. 187, 4774-4781
10. Rao, F., Yang, Y., Qi, Y., and Liang, Z.-X. (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase. A study of the EAL domaincontaining RocR from Pseudomonas aeruginosa. J. Bacteriol. 190, 3622-3631
11. Minasov, G., Padavattan, S., Shuvalova, L., Brunzelle, J. S., Miller, D. J., Baslé, A., Massa, C., Collart, F. R., Schirmer, T., and Anderson, W. F. (2009) Crystal structures of YkuI and its complex with second messenger cyclic di-GMP suggest catalytic mechanism of phosphodiester bond cleavage by EAL domains. J. Biol. Chem. 284, 13174-13184
12. Barends, T. R., Hartmann, E., Griese, J. J., Beitlich, T., Kirienko, N. V., Ryjenkov, D. A., Reinstein, J., Shoeman, R. L., Gomelsky, M., and Schlichting, I. (2009) Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 459, 1015-1018
13. Tchigvintsev, A., Xu, X., Singer, A., Chang, C., Brown, G., Proudfoot, M., Cui, H., Flick, R., Anderson, W. F., Joachimiak, A., Galperin, M. Y., Savchenko, A., and Yakunin, A. F. (2010) Structural insight into the mechanism of c-di-GMP hydrolysis by EAL domain phosphodiesterases. J. Mol. Biol. 402, 524-538
14. Navarro, M. V., De, N., Bae, N., Wang, Q., and Sondermann, H. (2009) Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 17, 1104-1116
15. Navarro, M. V., Newell, P. D., Krasteva, P. V., Chatterjee, D., Madden, D. R., O'Toole, G. A., and Sondermann, H. (2011) Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol. 9, e1000588
16. Claret, L., Miquel, S., Vieille, N., Ryjenkov, D. A., Gomelsky, M., and Darfeuille-Michaud, A. (2007) The flagellar factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-dependent pathway. J. Biol. Chem. 282, 33275-33283
17. Zähringer, F., Massa, C., and Schirmer, T. (2011) Efficient enzymatic production of the bacterial second messenger c-di-GMP by the diguanylate cyclase YdeH from E. coli. Appl. Biochem. Biotechnol. 163, 71-79
18. Gentner, M., Allan, M. G., Zaehringer, F., Schirmer, T., and Grzesiek, S. (2012) Oligomer formation of the bacterial second messenger c-di-GMP. Reaction rates and equilibrium constants indicate a monomeric state at physiological concentrations. J. Am. Chem. Soc. 134, 1019-1029
19. Leslie, A. G. (2006) The integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 62, 48-57
20. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
21. Evans, P. (2006) Scaling and assessment of data quality. Acta Crystallogr.D Biol. Crystallogr. 62, 72-82
22. Brünger, A. (1992) Free R-value. A novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475
23. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674
24. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255
25. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
26. Laskowski, R. A., Moss, D. S., and Thornton, J. M. (1993) Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067
27. Seidel, S. A., Dijkman, P. M., Lea, W. A., van den Bogaart, G., Jerabek-Willemsen, M., Lazic, A., Joseph, J. S., Srinivasan, P., Baaske, P., Simeonov, A., Katritch, I., Melo, F. A., Ladbury, J. E., Schreiber, G., Watts, A., Braun, D., and Duhr, S. (2013) Microscale thermophoresis quantifies biomolecular interactions under previously challenging conditions. Methods 59, 301-315
28. Wang, Z. X. (1995) An exact mathematical expression for describing competitive binding of two different ligands to a protein molecule. FEBS Lett. 360, 111-114
29. Benfield, C. T., Mansur, D. S., McCoy, L. E., Ferguson, B. J., Bahar, M. W., Oldring, A. P., Grimes, J. M., Stuart, D. I., Graham, S. C., and Smith, G. L. (2011) Mapping the IB kinase (IKK+)-binding interface of the B14 protein, a vaccinia virus inhibitor of IKK+-mediated activation of nuclear factor B. J. Biol. Chem. 286, 20727-20735
30. Lebowitz, J., Lewis, M. S., and Schuck, P. (2002) Modern analytical ultracentrifugation in protein science. A tutorial review. Protein Sci. 11, 2067-2079
31. Rao, F., Qi, Y., Chong, H. S., Kotaka, M., Li, B., Li, J., Lescar, J., Tang, K., and Liang, Z.-X. (2009) The functional role of a conserved loop in EAL domain-based cyclic di-GMP-specific phosphodiesterase. J. Bacteriol. 191, 4722-4731
32. Tarnawski, M., Barends, T. R., Hartmann, E., and Schlichting, I. (2013) Structures of the catalytic EAL domain of the Escherichia coli direct oxygen sensor. Acta Crystallogr. D Biol. Crystallogr. 69, 1045-1053
33. Walker, G. M. (1994) The roles of magnesium in biotechnology. Crit. Rev. Biotechnol. 14, 311-354
34. Kurokawa, H., Lee, D.-S., Watanabe, M., Sagami, I., Mikami, B., Raman, C. S., and Shimizu, T. (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor. J. Biol. Chem. 279, 20186-20193
35. Chen, M. W., Kotaka, M., Vonrhein, C., Bricogne, G., Rao, F., Chuah, M. L., Svergun, D., Schneider, G., Liang, Z.-X., and Lescar, J. (2012) Structural insights into the regulatory mechanism of the response regulator RocR from Pseudomonas aeruginosa in cyclic di-GMP signaling. J. Bacteriol. 194, 4837-4846
36. Robert-Paganin, J., Nonin-Lecomte, S., and Réty, S. (2012) Crystal structure of an EAL domain in complex with reaction product 5pGpG. PLoS ONE 7, e52424
37. Gao, R., and Stock, A. M. (2010) Molecular strategies for phosphorylationmediated regulation of response regulator activity. Curr. Opin. Microbiol. 13, 160-167