The c-di-GMP recognition mechanism of the PilZ domain of bacterial cellulose synthase subunit A

Biochemical and Biophysical Research Communications

Volumn 431, Issue 4, 2013, Pages 802-807

  Fujiwara, Takaaki ^a   Komoda, Keisuke ^a   Sakurai, Naofumi ^a   Tajima, Kenji ^a   Tanaka, Isao ^a   Yao, Min ^a  

^a HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Bacterial cellulose synthase; Binding stoichiometry; C di GMP; Isothermal titration calorimetry; PilZ domain; X ray crystallography

Indexed keywords

BACTERIAL ENZYME; CELLULOSE SYNTHASE SUBUNIT A; CYCLIC DIMERIC GUANOSINE MONOPHOSPHATE; CYCLIC GMP; SYNTHETASE; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; MOLECULAR INTERACTION; NONHUMAN; PILZ DOMAIN; PRIORITY JOURNAL;

ALANINE; AMINO ACID SUBSTITUTION; CRYSTALLOGRAPHY, X-RAY; CYCLIC GMP; GLUCONACETOBACTER XYLINUS; GLUCOSYLTRANSFERASES; MODELS, CHEMICAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM DIFFICILE; FIRMICUTES; GLUCONACETOBACTER XYLINUS; PROTEOBACTERIA; PSEUDOMONAS AERUGINOSA; VIBRIO CHOLERAE; XANTHOMONAS CAMPESTRIS;

EID: 84875261797     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2012.12.103     Document Type: Article

References (28)

1. Hickman J.W., Harwood C.S. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 2008, 69:376-389.
2. Tao F., He Y.W., Wu D.H., Swarup S., Zhang L.H. The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J. Bacteriol. 2010, 192:1020-1029.
3. Duerig A., Abel S., Folcher M., Nicollier M., Schweda T., Amiot N., Giese B., Jenal U. Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev. 2009, 23:93-104.
4. Matthias C., Beat C., Martin G.A., Marc F., Paul J., Stephan G., Urs J. DgrA is a member of a new family of cyclic diguanosine monophosphate receptors and controls flagellar motor function in Caulobacter crescentus. Proc. Natl. Acad. Sci. USA 2007, 104:4112-4117.
5. Kulshina N., Baird N.J., Ferré-D'Amaré A.R. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat. Struct. Mol. Biol. 2009, 16:1212-1217.
6. Smith K.D., Lipchock S.V., Ames T.D., Wang J., Breaker R.R., Strobel S.A. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat. Struct. Mol. Biol. 2009, 16:1218-1223.
7. Ouyang S., Song X., Wang Y., Ru H., Shaw N., Jiang Y., Niu F., Zhu Y., Qiu W., Parvatiyar K., Li Y., Zhang R., Liu Z.J. Structural analysis of the STING adaptor protein reveals a hydrophobic dimer interface and mode of cyclic di-GMP binding. Immunity 2012, 29:1073-1086.
8. Ryjenkov D.A., Tarutina M., Moskvin O.V., Gomelsky M. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain. J. Bacteriol. 2005, 187:1792-1798.
9. Christen M., Christen B., Folcher M., Schauerte A., Jenal U. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP. J. Biol. Chem. 2005, 280:30829-30837.
10. Ryan R.P., Fouhy Y., Lucey J.F., Crossman L.C., Spiro S., He Y.W., Zhang L.H., Heeb S., Cámara M., Williams P., Dow J.M. Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc. Natl. Acad. Sci. USA 2006, 25:6712-6717.
11. Amikam D., Galperin M.Y. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 2006, 22:3-6.
12. Benach J., Swaminathan S.S., Tamayo R., Handelman S.K., Folta-Stogniew E., Ramos J.E., Forouchar F., Neely H., Seetharaman J., Camilli A., Hunt J.F. The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J. 2007, 26:5153-5166.
13. Ko J., Ryu K.S., Kim H., Shin J.S., Lee J.O., Cheong C., Choi B.S. Structure of PP4397 reveals the molecular basis for different c-di-GMP binding modes by Pilz domain proteins. J. Mol. Biol. 2010, 23:97-110.
14. Habazettl J., Allan M.G., Jenal U., Grzesiek S. Solution structure of the PilZ domain protein PA4608 complex with cyclic di-GMP identifies charge clustering as molecular readout. J. Mol. Biol. 2011, 22:14304-14314.
15. Kawano S., Tajima K., Uemori Y., Yamashita H., Erata T., Munekata M., Takai M. Cloning of cellulose synthesis related genes form Acetobacter xylinum ATCC23769 and ATCC53582: comparison of cellulose synthetic ability between strains. DNA Res. 2002, 9:149-156.
16. Hu S.Q., Gao Y.G., Tajima K., Sunagawa N., Zhou Y., Kawano S., Fujiwara T., Yoda T., Shimura D., Satoh Y., Munekata M., Tanaka I., Yao M. Structure of bacterial cellulose synthase subunit D octamer with four inner passageways. Proc. Natl. Acad. Sci. USA 2010, 107:17957-17961.
17. Weinhouse H., Sapir S., Amikam D., Shilo Y., Volman G., Ohana P., Benziman M. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett. 1997, 416:207-211.
18. Amikam D., Benziman M. Cyclic diguanylic acid and cellulose synthesis in agrobacteriumtumefaciens. J. Bacteriol. 1989, 171:6649-6655.
19. Ryjenkov D.A., Simm R., Romling U., Gomelsky M. The PilZ domain is a receptor for the second messenger c-di-GMP: the PilZ domain protein YcgR controls motility in enterobacteria. J. Biol. Chem. 2006, 281:30310-30314.
20. Kabsch W. XDS. Acta Cryst. D 2010, 66:125-132.
21. Adams P.D., Afonine P.V., Bunkoczi G., Chen V.B., Davis I.W., Echols N., Headd J.J., Hung L.W., Kapral G.J., Grosse-Kunstleve R.W., McCoy A.J., Moriarty N.W., Oeffner R., Read R.J., Richardson D.C., Richardson J.S., Terwilliger T.C., Zwart P.H. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Cryst. D 2010, 66:213-221.
22. Emsley P., Cowtan K. Coot: model-building tools for molecular graphics. Acta Cryst. D 2004, 60:2126-2132.
23. Chen V.B., Arendall W.B., Headd J.J., Keedy D.A., Immormino R.M., Kapral G.J., Murray L.W., Richardson J.S., Richardson D.C. Molprobity: all-atom structure validation for macromolecular crystallography. Acta Cryst. D 2010, 66:12-21.
24. Punta M., Coggill P.C., Eberhardt R.Y., Mistry J., Tate J., Boursnell C., Pang N., Forslund K., Ceric G., Clements J., Heger A., Holm L., Sonnhammer E.L., Eddy S.R., Bateman A., Finn R.D. The Pfam protein families database. Nucleic Acids Res. 2012, 40:290-301.
25. Holm L., Sacder C. DALI: a network tool for protein structure comparison. Trends Biochem. Sci. 1995, 20:478-480.
26. Guzzo C.R., Salinas R.K., Andrade M.O., Farah C.S. PilZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J. Mol. Biol. 2009, 393:848-866.
27. Li T.N., Chin K.H., Liu J.H., Wang A.H., Chou S.H. XC1028 from Xanthomonas campestris adopts a PilZ domain-like structure without a c-di-GMP switch. Proteins 2009, 75:282-288.
28. Chin K.H., Kuo W.T., Yu Y.J., Liao Y.T., Yang M.T., Chou S.H. Structural polymorphism of c-di-GMP bound to an EAL domain and in complex with a type II PilZ-domain protein. Acta Cryst. D 2012, 68:1380-1392.