Cyclic di-GMP signalling and the regulation of bacterial virulence

Microbiology (United Kingdom)

Volumn 159, Issue PART7, 2013, Pages 1286-1297

  Ryan, Robert P ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CYCLIC AMP; CYCLIC DI GUANOSINE MONOPHOSPHATE; GUANOSINE PHOSPHATE; PA2572 PROTEIN; PA4108 PROTEIN; PA4781 PROTEIN; PROTEOME; UNCLASSIFIED DRUG; XANTHAN;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BINDING SITE; BIOFILM; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; CONSENSUS SEQUENCE; CRYSTAL STRUCTURE; DNA BINDING; ENZYME ACTIVITY; ENZYME SPECIFICITY; ENZYME SYNTHESIS; ESCHERICHIA COLI; GENE CLUSTER; GENETIC TRANSCRIPTION; INTRACELLULAR SIGNALING; METAL BINDING; NEGATIVE FEEDBACK; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; REGULATORY MECHANISM; RIBOSWITCH; RNA SEQUENCE; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TURNOVER TIME;

BACTERIAL PROTEINS; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; MOLECULAR SEQUENCE DATA; PROTEIN INTERACTION MAPS; SIGNAL TRANSDUCTION; VIRULENCE; XANTHOMONAS CAMPESTRIS;

BACTERIA (MICROORGANISMS);

EID: 84879835990     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.068189-0     Document Type: Article

References (43)

1. Abel, S., Chien, P., Wassmann, P., Schirmer, T., Kaever, V., Laub, M. T., Baker, T. A. & Jenal, U. (2011). Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 43, 550-560.
2. An, S.-Q., Febrer, M., McCarthy, Y., Tang, D.-J., Clissold, L., Kaithakottil, G., Swarbreck, D., Tang, J.-L., Rogers, J. & other authors (2013). High-resolution transcriptional analysis of the regulatory influence of cell-to-cell signalling reveals novel genes that contribute to Xanthomonas phytopathogenesis. Mol Microbiol 88, 1058-1069.
3. Andrade, M. O., Alegria, M. C., Guzzo, C. R., Docena, C., Rosa, M. C. P., Ramos, C. H. I. & Farah, C. S. (2006). The HD-GYP domain of RpfG mediates a direct linkage between the Rpf quorum-sensing pathway and a subset of diguanylate cyclase proteins in the phytopathogen Xanthomonas axonopodis pv citri. Mol Microbiol 62, 537-551.
4. Barber, C. E., Tang, J. L., Feng, J. X., Pan, M. Q., Wilson, T. J., Slater, H., Dow, J. M., Williams, P. & Daniels, M. J. (1997). A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24, 555-566.
5. Boyd, C. D. & O'Toole, G. A. (2012). Second messenger regulation of biofilm formation: breakthroughs in understanding c-di-GMP effector systems. Annu Rev Cell Dev Biol 28, 439-462.
6. Cheng, Z., He, Y. W., Lim, S. C., Qamra, R., Walsh, M. A., Zhang, L. H. & Song, H. (2010). Structural basis of the sensor-synthase interaction in autoinduction of the quorum sensing signal DSF biosynthesis. Structure 18, 1199-1209.
7. Chin, K. H., Lee, Y. C., Tu, Z. L., Chen, C. H., Tseng, Y. H., Yang, J. M., Ryan, R. P., McCarthy, Y., Dow, J. M. & other authors (2010). The cAMP receptor-like protein CLP is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris. J Mol Biol 396, 646-662.
8. Christen, M., Christen, B., Folcher, M., Schauerte, A. & 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. Chugani, S. & Greenberg, E. P. (2007). The influence of human respiratory epithelia on Pseudomonas aeruginosa gene expression. Microb Pathog 42, 29-35.
10. Dow, J. M., Crossman, L., Findlay, K., He, Y. Q., Feng, J. X. & Tang, J. L. (2003). Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. Proc Natl Acad Sci U S A 100, 10995-11000.
11. Galperin, M. Y., Natale, D. A., Aravind, L. & Koonin, E. V. (1999). A specialized version of the HD hydrolase domain implicated in signal transduction. J Mol Microbiol Biotechnol 1, 303-305.
12. Galperin, M. Y., Nikolskaya, A. N. & Koonin, E. V. (2001). Novel domains of the prokaryotic two-component signal transduction systems. FEMS Microbiol Lett 203, 11-21.
13. Hammer, B. K. & Bassler, B. L. (2009). Distinct sensory pathways in Vibrio cholerae El Tor and classical biotypes modulate cyclic dimeric GMP levels to control biofilm formation. J Bacteriol 191, 169-177.
14. He, Y. W., Wang, C., Zhou, L., Song, H., Dow, J. M. & Zhang, L. H. (2006). Dual signaling functions of the hybrid sensor kinase RpfC of Xanthomonas campestris involve either phosphorelay or receiver domain-protein interaction. J Biol Chem 281, 33414-33421.
15. Hengge, R. (2009). Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7, 263-273.
16. Ichikawa, J. K., Norris, A., Bangera, M. G., Geiss, G. K., van't Wout, A. B., Bumgarner, R. E. & Lory, S. (2000). Interaction of Pseudomonas aeruginosa with epithelial cells: identification of differentially regulated genes by expression microarray analysis of human cDNAs. Proc Natl Acad Sci U S A 97, 9659-9664.
17. Leduc, J. L. & Roberts, G. P. (2009). Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 191, 7121-7122.
18. Lovering, A. L., Capeness, M. J., Lambert, C., Hobley, L. & Sockett, R. E. (2011). The structure of an unconventional HD-GYP protein from Bdellovibrio reveals the roles of conserved residues in this class of cyclic-di-GMP phosphodiesterases. mBio 2, e00163-11.
19. Lu, X. H., An, S. Q., Tang, D. J., McCarthy, Y., Tang, J. L., Dow, J. M. & Ryan, R. P. (2012). RsmA regulates biofilm formation in Xanthomonas campestris through a regulatory network involving cyclic di-GMP and the Clp transcription factor. PLoS ONE 7, e52646.
20. McCarthy, Y., Ryan, R. P., O'Donovan, K., He, Y.-Q., Jiang, B.-L., Feng, J.-X., Tang, J.-L. & Dow, J. M. (2008). The role of PilZ domain proteins in the virulence of Xanthomonas campestris pv. campestris. Mol Plant Pathol 9, 819-826.
21. Newell, P. D., Boyd, C. D., Sondermann, H. & O'Toole, G. A. (2011). A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 9, e1000587.
22. Paul, R., Weiser, S., Amiot, N. C., Chan, C., Schirmer, T., Giese, B. & Jenal, U. (2004). Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18, 715-727.
23. Romling, U., Galperin, M. Y. & Gomelsky, M. (2013). Cyclic di-GMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77, 1-52.
24. Ross, P., Weinhouse, H., Aloni, Y., Michaeli, D., Weinberger-Ohana, P., Mayer, R., Braun, S., de Vroom, E., van der Marel, G. A. & other authors (1987). Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325, 279-281.
25. Ryan, R. P., Fouhy, Y., Lucey, J. F., Crossman, L. C., Spiro, S., He, Y. W., Zhang, L. H., Heeb, S., Cámara, M. & other authors (2006). Cell-cell signaling in Xanthomonas campestris involves an HD-GYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci U S A 103, 6712-6717.
26. Ryan, R. P., Fouhy, Y., Lucey, J. F., Jiang, B. L., He, Y. Q., Feng, J. X., Tang, J. L. & Dow, J. M. (2007). Cyclic di-GMP signalling in the virulence and environmental adaptation of Xanthomonas campestris. Mol Microbiol 63, 429-442.
27. Ryan, R. P., Lucey, J., O'Donovan, K., McCarthy, Y., Yang, L., Tolker-Nielsen, T. & Dow, J. M. (2010). HD-GYP domain proteins regulate biofilm formation and virulence in Pseudomonas aeruginosa. Environ Microbiol 11, 1126-1136.
28. Ryan, R. P., McCarthy, Y., Andrade, M., Farah, C. S., Armitage, J. P. & Dow, J. M. (2010). Cell-cell signal-dependent dynamic interactions between HD-GYP and GGDEF domain proteins mediate virulence in Xanthomonas campestris. Proc Natl Acad Sci USA 107, 5989-5994.
29. Ryan, R. P., McCarthy, Y., Kiely, P. A., O'Connor, R., Farah, C. S., Armitage, J. P. & Dow, J. M. (2012a). Dynamic complex formation between HD-GYP, GGDEF and PilZ domain proteins regulates motility in Xanthomonas campestris. Mol Microbiol 86, 557-567.
30. Ryan, R. P., Tolker-Nielsen, T. & Dow, J. M. (2012b). When the PilZ don't work: effectors for cyclic di-GMP action in bacteria. Trends Microbiol 20, 235-242.
31. Schirmer, T. & Jenal, U. (2009). Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7, 724-735.
32. Slater, H., Alvarez-Morales, A., Barber, C. E., Daniels, M. J. & Dow, J. M. (2000). A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38, 986-1003.
33. Sondermann, H., Shikuma, N. J. & Yildiz, F. H. (2012). You've come a long way: c-di-GMP signaling. Curr Opin Microbiol 15, 140-146.
34. Sultan, S. Z., Pitzer, J. E., Miller, M. R. & Motaleb, M. A. (2010). Analysis of a Borrelia burgdorferi phosphodiesterase demonstrates a role for cyclic-di-guanosine monophosphate in motility and virulence. Mol Microbiol 77, 128-142.
35. Sultan, S. Z., Pitzer, J. E., Boquoi, T., Hobbs, G., Miller, M. R. & Motaleb, M. A. (2011). Analysis of the HD-GYP domain cyclic dimeric GMP phosphodiesterase reveals a role in motility and the enzootic life cycle of Borrelia burgdorferi. Infect Immun 79, 3273-3283.
36. Tang, J. L., Liu, Y. N., Barber, C. E., Dow, J. M., Wootton, J. C. & Daniels, M. J. (1991). Genetic and molecular analysis of a cluster of rpf genes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris. Mol Gen Genet 226, 409-417.
37. Tao, F., He, Y. W., Wu, D. H., Swarup, S. & Zhang, L. H. (2010). The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors. J Bacteriol 192, 1020-1029.
38. Tischler, A. D. & Camilli, A. (2004). Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 53, 857-869.
39. Tschowri, N., Busse, S. & Hengge, R. (2009). The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. Genes Dev 23, 522-534.
40. Tschowri, N., Lindenberg, S. & Hengge, R. (2012). Molecular function and potential evolution of the biofilm-modulating blue light-signalling pathway of Escherichia coli. Mol Microbiol 85, 893-906.
41. Vojnov, A. A., Slater, H., Newman, M. A., Daniels, M. J. & Dow, J. M. (2001). Regulation of the synthesis of cyclic glucan in Xanthomonas campestris by a diffusible signal molecule. Arch Microbiol 176, 415-420.
42. Wang, L. H., He, Y. W., Gao, Y. F., Wu, J. E., Dong, Y. H., He, C. Z., Wang, S. X., Weng, L. X., Xu, J. L. & other authors (2004). A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51, 903-912.
43. Wolfgang, M. C., Jyot, J., Goodman, A. L., Ramphal, R. & Lory, S. (2004). Pseudomonas aeruginosa regulates flagellin expression as part of a global response to airway fluid from cystic fibrosis patients. Proc Natl Acad Sci U S A 101, 6664-6668.