A c-di-GMP effector system controls cell adhesion by inside-out signaling and surface protein cleavage

PLoS Biology

Volumn 9, Issue 2, 2011, Pages

  Newell, Peter D ^a   Boyd, Chelsea D ^a   Sondermann, Holger ^b   O'Toole, George A ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC GMP; MEMBRANE PROTEIN; PROTEIN LAPA; PROTEIN LAPD; PROTEIN LAPG; UNCLASSIFIED DRUG; ADHESIN; ADHESIN, PSEUDOMONAS; BIS(3',5') CYCLIC DIGUANYLIC ACID; BIS(3',5')-CYCLIC DIGUANYLIC ACID; CYSTEINE PROTEINASE; DRUG DERIVATIVE; LECTIN;

ARTICLE; CELL ADHESION; CELL SURFACE; CONTROLLED STUDY; MUTATION; NONHUMAN; PHENOTYPE; PROTEIN BINDING; PROTEIN CLEAVAGE; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; PROTEIN STRUCTURE; PROTEIN TARGETING; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; BACTERIUM ADHERENCE; BINDING SITE; BIOFILM; CELL MEMBRANE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYSIOLOGY; PSEUDOMONAS FLUORESCENS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); PSEUDOMONAS FLUORESCENS;

ADHESINS, BACTERIAL; AMINO ACID SEQUENCE; BACTERIAL ADHESION; BINDING SITES; BIOFILMS; CELL MEMBRANE; CONSERVED SEQUENCE; CYCLIC GMP; CYSTEINE PROTEASES; LECTINS; MOLECULAR SEQUENCE DATA; PHENOTYPE; PSEUDOMONAS FLUORESCENS; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION;

EID: 79952266181     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1000587     Document Type: Article

References (37)

1. Paul R, Weiser S, Amiot N. C, Chan C, Schirmer T, et al. (2004) Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev 18: 715-727.
2. 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.
3. Ryan R. P, Fouhy Y, Lucey J. F, Crossman L. C, Spiro S, et al. (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.
4. 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.
5. Hengge R, (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7: 263-273.
6. Weinhouse H, Sapir S, Amikam D, Shilo Y, Volman G, et al. (1997) c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum. FEBS Lett 416: 207-211.
7. Merighi M, Lee V. T, Hyodo M, Hayakawa Y, Lory S, (2007) 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 65: 876-895.
8. Lee V. T, Matewish J. M, Kessler J. L, Hyodo M, Hayakawa Y, et al. (2007) A cyclic-di-GMP receptor required for bacterial exopolysaccharide production. Mol Microbiol 65: 1474-1484.
9. Ryjenkov D. A, Simm R, Romling U, Gomelsky M, (2006) 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 281: 30310-30314.
10. Christen M, Christen B, Allan M. G, Folcher M, Jeno P, et al. (2007) 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 U S A 104: 4112-4117.
11. Pratt J. T, Tamayo R, Tischler A. D, Camilli A, (2007) PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae. J Biol Chem 282: 12860-12870.
12. Guzzo C. R, Salinas R. K, Andrade M. O, Farah C. S, (2009) PILZ protein structure and interactions with PILB and the FIMX EAL domain: implications for control of type IV pilus biogenesis. J Mol Biol 393: 848-866.
13. Hickman J. W, Harwood C. S, (2008) Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol Microbiol 69: 376-389.
14. 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.
15. Krasteva P. V, Fong J. C, Shikuma N. J, Beyhan S, Navarro M. V, et al. (2010) Vibrio cholerae VpsT regulates matrix production and motility by directly sensing cyclic di-GMP. Science 327: 866-868.
16. Duerig A, Abel S, Folcher M, Nicollier M, Schwede T, et al. (2009) Second messenger-mediated spatiotemporal control of protein degradation regulates bacterial cell cycle progression. Genes Dev 23: 93-104.
17. Newell P. D, Monds R. D, O'Toole G. A, (2009) LapD is a bis-(3′,5′)-cyclic dimeric GMP-binding protein that regulates surface attachment by Pseudomonas fluorescens Pf0-1. Proc Natl Acad Sci U S A 106: 3461-3466.
18. Paul K, Nieto V, Carlquist W. C, Blair D. F, Harshey R. M, (2010) The c-di-GMP binding protein YcgR controls flagellar motor direction and speed to affect chemotaxis by a "backstop brake" mechanism. Mol Cell 38: 128-139.
19. Boehm A, Kaiser M, Li H, Spangler C, Kasper C. A, et al. (2010) Second messenger-mediated adjustment of bacterial swimming velocity. Cell 141: 107-116.
20. Fang X, Gomelsky M, (2010) A posttranslational, c-di-GMP-dependent mechanism regulating flagellar motility. Mol Microbiol 76: 1295-1305.
21. Sudarsan N, Lee E. R, Weinberg Z, Moy R. H, Kim J. N, et al. (2008) Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321: 411-413.
22. Kulshina N, Baird N. J, Ferré-D'Amaré A. R, (2009) Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat Struct Mol Biol 16: 1212-1217.
23. Smith K. D, Lipchock S. V, Ames T. D, Wang J, Breaker R. R, et al. (2009) Structural basis of ligand binding by a c-di-GMP riboswitch. Nat Struct Mol Biol 16: 1218-1223.
24. Hinsa S. M, Espinosa-Urgel M, Ramos J. L, O'Toole G. A, (2003) Transition from reversible to irreversible attachment during biofilm formation by Pseudomonas fluorescens WCS365 requires an ABC transporter and a large secreted protein. Mol Microbiol 49: 905-918.
25. Monds R. D, Newell P. D, Gross R. H, O'Toole G. A, (2007) Phosphate-dependent modulation of c-di-GMP levels regulates Pseudomonas fluorescens Pf0-1 biofilm formation by controlling secretion of the adhesin LapA. Mol Microbiol 63: 656-679.
26. Navarro MVA. S, Newell P. D, Krasteva P. V, Chatterjee D, Madden DR, et al. (2011) Structural Basis for c-di-GMP-Mediated Inside-Out Signaling Controlling Periplasmic Proteolysis. PLoS Biol9 (2)e1000588. doi:10.1371/journal.pbio.1000588.
27. Monds R. D, Newell P. D, Wagner J. C, Schwartzman J. A, Lu W, et al. (2010) Di-adenosine tetraphosphate (Ap4A) metabolism impacts biofilm formation by Pseudomonas fluorescens via modulation of c-di-GMP-dependent pathways. J Bacteriol 192: 3011-3023.
28. Ginalski K, Kinch L, Rychlewski L, Grishin N. V, (2004) BTLCP proteins: a novel family of bacterial transglutaminase-like cysteine proteinases. Trends Biochem Sci 29: 392-395.
29. Monds R. D, Newell P. D, Schwartzman J. A, O'Toole G. A, (2006) Conservation of the Pho regulon in Pseudomonas fluorescens Pf0-1. Appl Environ Microbiol 72: 1910-1924.
30. Sanchez-Magraner L, Viguera A. R, Garcia-Pacios M, Garcillan M. P, Arrondo J. L, et al. (2007) The calcium-binding C-terminal domain of Escherichia coli alpha-hemolysin is a major determinant in the surface-active properties of the protein. J Biol Chem 282: 11827-11835.
31. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T, (2010) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75: 815-826.
32. MacEachran D. P, Stanton B. A, O'Toole G. A, (2008) Cif is negatively regulated by the TetR family repressor CifR. Infect Immun 76: 3197-3206.
33. Simon R, Priefer U. B, Puhler A, (1983) A broad host range system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Biotechnology (NY) 1: 784-791.
34. Hanahan D, (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580.
35. Compeau G, Al-Achi B. J, Platsouka E, Levy S. B, (1988) Survival of rifampin-resistant mutants of Pseudomonas fluorescens and Pseudomonas putida in soil systems. Appl Environ Microbiol 54: 2432-2438.
36. Shanks R. M, Caiazza N. C, Hinsa S. M, Toutain C. M, O'Toole G. A, (2006) Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol 72: 5027-5036.
37. Hoang T. T, Karkhoff-Schweizer R. R, Kutchma A. J, Schweizer H. P, (1998) A broad-host-range Flp-FRT recombination system for site-specific excision of chromosomally-located DNA sequences: application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212: 77-86.