You've come a long way: C-di-GMP signaling

Current Opinion in Microbiology

Volumn 15, Issue 2, 2012, Pages 140-146

  Sondermann, Holger ^a   Shikuma, Nicholas J ^b   Yildiz, Fitnat H ^b  

^a Cornell University ^*  (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC DIMERIC GUANOSINE MONOPHOSPHATE; CYCLIC GMP; CYCLIC GMP PHOSPHODIESTERASE; DINUCLEOTIDE; GUANYLATE CYCLASE; PROTEIN ALG44; PROTEIN DCGR; PROTEIN FIMX; PROTEIN GGDEF; PROTEIN LAPD; PROTEIN MRKH; PROTEIN PELD; PROTEIN PILZ; PROTEIN PLZ; PROTEIN PNPASE; PROTEIN POPA; PROTEIN YCGR; RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCAM1349; TRANSCRIPTION FACTOR CLP; TRANSCRIPTION FACTOR FLEQ; TRANSCRIPTION FACTOR VPST; UNCLASSIFIED DRUG;

BIOFILM; BURKHOLDERIA CENOCEPACIA; CLOSTRIDIUM DIFFICILE; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; KLEBSIELLA PNEUMONIAE; NONHUMAN; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; PSEUDOMONAS AERUGINOSA; PSEUDOMONAS FLUORESCENS; REGULATORY MECHANISM; REVIEW; RIBOSWITCH; SECOND MESSENGER; SIGNAL TRANSDUCTION; VIBRIO CHOLERAE; XANTHOMONAS AXONOPODIS; XANTHOMONAS CAMPESTRIS;

BACTERIA; BACTERIAL PROTEINS; BIOFILMS; CYCLIC GMP; GENE EXPRESSION REGULATION, BACTERIAL; RIBOSWITCH; SECOND MESSENGER SYSTEMS; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS);

EID: 84861801044     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2011.12.008     Document Type: Review

References (62)

1. 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.
2. Paul R., Weiser S., Amiot N.C., Chan C., Schirmer T., Giese B., Jenal U. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 2004, 18:715-727.
3. 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.
4. Schmidt A.J., Ryjenkov D.A., Gomelsky M. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains. J Bacteriol 2005, 187:4774-4781.
5. Ryan R.P., Fouhy Y., Lucey J.F., Crossman L.C., Spiro S., He Y.W., Zhang L.H., Heeb S., Camara M., Williams P., et al. 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, 103:6712-6717.
6. Galperin M.Y. Diversity of structure and function of response regulator output domains. Curr Opin Microbiol 2010, 13:150-159.
7. Barends T.R., Hartmann E., Griese J.J., Beitlich T., Kirienko N.V., Ryjenkov D.A., Reinstein J., Shoeman R.L., Gomelsky M., Schlichting I. Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase. Nature 2009, 459:1015-1018.
8. Tarutina M., Ryjenkov D.A., Gomelsky M. An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J Biol Chem 2006, 281:34751-34758.
9. Tuckerman J.R., Gonzalez G., Sousa E.H., Wan X., Saito J.A., Alam M., Gilles-Gonzalez M.A. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry 2009, 48:9764-9774.
10. Wan X., Tuckerman J.R., Saito J.A., Freitas T.A., Newhouse J.S., Denery J.R., Galperin M.Y., Gonzalez G., Gilles-Gonzalez M.A., Alam M. Globins synthesize the second messenger bis-(3'-5')-cyclic diguanosine monophosphate in bacteria. J Mol Biol 2009, 388:262-270.
11. Chang A.L., Tuckerman J.R., Gonzalez G., Mayer R., Weinhouse H., Volman G., Amikam D., Benziman M., Gilles-Gonzalez M.A. Phosphodiesterase A1, a regulator of cellulose synthesis in Acetobacter xylinum, is a heme-based sensor. Biochemistry 2001, 40:3420-3426.
12. Qi Y., Rao F., Luo Z., Liang Z.X. A flavin cofactor-binding PAS domain regulates c-di-GMP synthesis in AxDGC2 from Acetobacter xylinum. Biochemistry 2009, 48:10275-10285.
13. Carlson H.K., Vance R.E., Marletta M.A. H-NOX regulation of c-di-GMP metabolism and biofilm formation in Legionella pneumophila. Mol Microbiol 2010, 77:930-942.
14. Kanazawa T., Ren S., Maekawa M., Hasegawa K., Arisaka F., Hyodo M., Hayakawa Y., Ohta H., Masuda S. Biochemical and physiological characterization of a BLUF protein-EAL protein complex involved in blue light-dependent degradation of cyclic diguanylate in the purple bacterium Rhodopseudomonas palustris. Biochemistry 2010, 49:10647-10655.
15. Tischler A.D., Camilli A. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation. Mol Microbiol 2004, 53:857-869.
16. Hickman J.W., Tifrea D.F., Harwood C.S. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 2005, 102:14422-14427.
17. Kuchma S.L., Connolly J.P., O'Toole G.A. A three-component regulatory system regulates biofilm maturation and type III secretion in Pseudomonas aeruginosa. J Bacteriol 2005, 187:1441-1454.
18. Kulasekara H.D., Ventre I., Kulasekara B.R., Lazdunski A., Filloux A., Lory S. A novel two-component system controls the expression of Pseudomonas aeruginosa fimbrial cup genes. Mol Microbiol 2005, 55:368-380.
19. Paul R., Abel S., Wassmann P., Beck A., Heerklotz H., Jenal U. Activation of the diguanylate cyclase PleD by phosphorylation-mediated dimerization. J Biol Chem 2007, 282:29170-29177.
20. Wassmann P., Chan C., Paul R., Beck A., Heerklotz H., Jenal U., Schirmer T. Structure of BeF3-modified response regulator PleD: implications for diguanylate cyclase activation, catalysis, and feedback inhibition. Structure 2007, 15:915-927.
21. De N., Navarro M.V., Raghavan R.V., Sondermann H. Determinants for the activation and autoinhibition of the diguanylate cyclase response regulator WspR. J Mol Biol 2009, 393:619-633.
22. Duerig A., Abel S., Folcher M., Nicollier M., Schwede 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.
23. Abel S., Chien P., Wassmann P., Schirmer T., Kaever V., Laub M.T., Baker T.A., Jenal U. Regulatory cohesion of cell cycle and cell differentiation through interlinked phosphorylation and second messenger networks. Mol Cell 2011, 43:550-560.
24. Lee V.T., Matewish J.M., Kessler J.L., Hyodo M., Hayakawa Y., Lory S. A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 2007, 65:1474-1484.
25. Beyhan S., Odell L.S., Yildiz F.H. Identification and characterization of cyclic diguanylate signaling systems controlling rugosity in Vibrio cholerae. J Bacteriol 2008, 190:7392-7405.
26. Kazmierczak B.I., Lebron M.B., Murray T.S. Analysis of FimX, a phosphodiesterase that governs twitching motility in Pseudomonas aeruginosa. Mol Microbiol 2006, 60:1026-1043.
27. Navarro M.V., De N., Bae N., Wang Q., Sondermann H. Structural analysis of the GGDEF-EAL domain-containing c-di-GMP receptor FimX. Structure 2009, 17:1104-1116.
28. Newell P.D., Monds R.D., O'Toole G.A. LapD is a bis-(3',5')-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci USA 2009, 106:3461-3466.
29. Newell P.D., Boyd C.D., Sondermann H., O'Toole G.A. A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage. PLoS Biol 2011, 9:e1000587.
30. Navarro M.V., Newell P.D., Krasteva P.V., Chatterjee D., Madden D.R., O'Toole G.A., Sondermann H. Structural basis for c-di-GMP-mediated inside-out signaling controlling periplasmic proteolysis. PLoS Biol 2011, 9:e1000588.
31. Monds R.D., Newell P.D., Gross R.H., O'Toole G.A. Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 2007, 63:656-679.
32. Newell P.D., Yoshioka S., Hvorecny K.L., Monds R.D., O'Toole G.A. Systematic analysis of diguanylate cyclases that promote biofilm formation by Pseudomonas fluorescens Pf0-1. J Bacteriol 2011, 193:4685-4698.
33. Qi Y., Chuah M.L., Dong X., Xie K., Luo Z., Tang K., Liang Z.X. Binding of cyclic diguanylate in the non-catalytic EAL domain of FimX induces a long-range conformational change. J Biol Chem 2011, 286:2910-2917.
34. 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.
35. 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.
36. Leduc J.L., Roberts G.P. Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri. J Bacteriol 2009, 191:7121-7122.
37. 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., Wang A.H., et al. 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 2010, 396:646-662.
38. Fazli M., O'Connell A., Nilsson M., Niehaus K., Dow J.M., Givskov M., Ryan R.P., Tolker-Nielsen T. The CRP/FNR family protein Bcam1349 is a c-di-GMP effector that regulates biofilm formation in the respiratory pathogen Burkholderia cenocepacia. Mol Microbiol 2011.
39. Krasteva P.V., Fong J.C., Shikuma N.J., Beyhan S., Navarro M.V., Yildiz F.H., Sondermann H. Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 2010, 327:866-868.
40. Wilksch J.J., Yang J., Clements A., Gabbe J.L., Short K.R., Cao H., Cavaliere R., James C.E., Whitchurch C.B., Schembri M.A., et al. MrkH, a novel c-di-GMP-dependent transcriptional activator, controls Klebsiella pneumoniae biofilm formation by regulating type 3 fimbriae expression. PLoS Pathog 2011, 7:e1002204.
41. Amikam D., Galperin M.Y. PilZ domain is part of the bacterial c-di-GMP binding protein. Bioinformatics 2006, 22:3-6.
42. 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.
43. Benach J., Swaminathan S.S., Tamayo R., Handelman S.K., Folta-Stogniew E., Ramos J.E., Forouhar F., Neely H., Seetharaman J., Camilli A., et al. The structural basis of cyclic diguanylate signal transduction by PilZ domains. Embo J 2007, 26:5153-5166.
44. 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, 398:97-110.
45. 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 Biol Chem 2011, 286:14304-14314.
46. Christen M., Kulasekara H.D., Christen B., Kulasekara B.R., Hoffman L.R., Miller S.I. Asymmetrical distribution of the second messenger c-di-GMP upon bacterial cell division. Science 2010, 328:1295-1297.
47. Fang X., Gomelsky M. A post-translational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 2010, 76:1295-1305.
48. Paul K., Nieto V., Carlquist W.C., Blair D.F., Harshey R.M. The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a 'backstop brake' mechanism. Mol Cell 2010, 38:128-139.
49. Boehm A., Kaiser M., Li H., Spangler C., Kasper C.A., Ackermann M., Kaever V., Sourjik V., Roth V., Jenal U. Second messenger-mediated adjustment of bacterial swimming velocity. Cell 2010, 141:107-116.
50. Pratt J.T., Tamayo R., Tischler A.D., Camilli A. PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem 2007, 282:12860-12870.
51. Merighi M., Lee V.T., Hyodo M., Hayakawa Y., Lory S. The second messenger bis-(3'-5')-cyclic-GMP and its PilZ domain-containing receptor Alg44 are required for alginate biosynthesis in Pseudomonas aeruginosa. Mol Microbiol 2007, 65:876-895.
52. Lee E.R., Baker J.L., Weinberg Z., Sudarsan N., Breaker R.R. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 2010, 329:845-848.
53. Sudarsan N., Lee E.R., Weinberg Z., Moy R.H., Kim J.N., Link K.H., Breaker R.R. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 2008, 321:411-413.
54. Kulshina N., Baird N.J., Ferre-D'Amare A.R. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat Struct Mol Biol 2009, 16:1212-1217.
55. 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.
56. Smith K.D., Shanahan C.A., Moore E.L., Simon A.C., Strobel S.A. Structural basis of differential ligand recognition by two classes of bis-(3'-5')-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc Natl Acad Sci USA 2011, 108:7757-7762.
57. Ross P., Weinhouse H., Aloni Y., Michaeli D., Weinberger-Ohana P., Mayer R., Braun S., de Vroom E., van der Marel G.A., van Boom J.H., et al. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 1987, 325:279-281.
58. Tuckerman J.R., Gonzalez G., Gilles-Gonzalez M.A. Cyclic di-GMP activation of polynucleotide phosphorylase signal-dependent RNA processing. J Mol Biol 2011, 407:633-639.
59. Fong J.C., Yildiz F.H. Interplay between cyclic AMP-cyclic AMP receptor protein and cyclic di-GMP signaling in Vibrio cholerae biofilm formation. J Bacteriol 2008, 190:6646-6659.
60. Weber H., Pesavento C., Possling A., Tischendorf G., Hengge R. Cyclic-di-GMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol 2006, 62:1014-1034.
61. Witte G., Hartung S., Buttner K., Hopfner K.P. Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol Cell 2008, 30:167-178.
62. Christen M., Christen B., Allan M.G., Folcher M., Jeno P., Grzesiek S., Jenal U. 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.