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PMID: 17307739 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

PilZ domain proteins bind cyclic diguanylate and regulate diverse processes in Vibrio cholerae.

The Journal of biological chemistry ·Vol. 282 ·No. 17 ·2007-04-27 ·Pages 12860-70

Pratt JT, Tamayo R, Tischler AD, Camilli A

Abstract

Cyclic diguanylate (c-di-GMP) is an allosteric activator and second messenger implicated in the regulation of a variety of biological processes in diverse bacteria. In Vibrio cholerae, c-di-GMP has been shown to inversely regulate biofilm-specific and virulence gene expression, suggesting that c-di-GMP signaling is important for the transition of V. cholerae from the environment to the host. However, the mechanism behind this regulation remains unknown. Recently, it was proposed that the PilZ protein domain represents a c-di-GMP-binding domain. Here we show that V. cholerae PilZ proteins bind c-di-GMP specifically and are involved in the regulation of biofilm formation, motility, and virulence. These findings confirm a role for PilZ proteins as c-di-GMP-sensing proteins within the c-di-GMP signaling network.

MeSH Terms
Bacterial Proteins/metabolism Biofilms/growth & development Cyclic GMP/analogs & derivatives,metabolism Protein Structure, Tertiary/physiology Signal Transduction/physiology Vibrio cholerae/growth & development,pathogenicity
Chemicals
Bacterial Proteins bis(3',5')-cyclic diguanylic acid Cyclic GMP
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Pratt Jason T
Howard Hughes Medical Institute and the Department of Molecular Biology and Microbiology, Tufts University School of Medicine, Boston, Massachusetts 02111, USA.
Tamayo Rita
Tischler Anna D
Camilli Andrew
References (55)
55 references, click to expand
  1. Steps in the development of a Vibrio cholerae El Tor biofilm.
    Mol Microbiol. 1999 Nov;34(3):586-95 PMID: 10564499
  2. Regulation and temporal expression patterns of Vibrio cholerae virulence genes during infection.
    Cell. 1999 Dec 10;99(6):625-34 PMID: 10612398
  3. Two novel flagellar components and H-NS are involved in the motor function of Escherichia coli.
    J Mol Biol. 2000 Oct 27;303(3):371-82 PMID: 11031114
  4. VpsR, a Member of the Response Regulators of the Two-Component Regulatory Systems, Is Required for Expression of vps Biosynthesis Genes and EPS(ETr)-Associated Phenotypes in Vibrio cholerae O1 El Tor.
    J Bacteriol. 2001 Mar;183(5):1716-26 PMID: 11160103
  5. The novel sigma54- and sigma28-dependent flagellar gene transcription hierarchy of Vibrio cholerae.
    Mol Microbiol. 2001 Mar;39(6):1595-609 PMID: 11260476
  6. Selection for in vivo regulators of bacterial virulence.
    Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6889-94 PMID: 11391007
  7. Whole genome DNA microarray expression analysis of biofilm development by Vibrio cholerae O1 E1 Tor.
    Methods Enzymol. 2001;336:3-18 PMID: 11398407
  8. Genetic data indicate that proteins containing the GGDEF domain possess diguanylate cyclase activity.
    FEMS Microbiol Lett. 2001 Oct 16;204(1):163-7 PMID: 11682196
  9. Pseudomonas biofilm formation and antibiotic resistance are linked to phenotypic variation.
    Nature. 2002 Apr 18;416(6882):740-3 PMID: 11961556
  10. Role of the GGDEF regulator PleD in polar development of Caulobacter crescentus.
    Mol Microbiol. 2003 Mar;47(6):1695-708 PMID: 12622822
  11. FimX, a multidomain protein connecting environmental signals to twitching motility in Pseudomonas aeruginosa.
    J Bacteriol. 2003 Dec;185(24):7068-76 PMID: 14645265
  12. PilZ domain is part of the bacterial c-di-GMP binding protein.
    Bioinformatics. 2006 Jan 1;22(1):3-6 PMID: 16249258
  13. 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. 2006 Apr 25;103(17):6712-7 PMID: 16611728
  14. Transcriptome and phenotypic responses of Vibrio cholerae to increased cyclic di-GMP level.
    J Bacteriol. 2006 May;188(10):3600-13 PMID: 16672614
  15. 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 Oct 13;281(41):30310-4 PMID: 16920715
  16. NMR structure and binding studies confirm that PA4608 from Pseudomonas aeruginosa is a PilZ domain and a c-di-GMP binding protein.
    Proteins. 2007 Feb 1;66(2):266-71 PMID: 17096419
  17. Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid.
    Nature. 1987 Jan 15-21;325(6101):279-81 PMID: 18990795
  18. HmsP, a putative phosphodiesterase, and HmsT, a putative diguanylate cyclase, control Hms-dependent biofilm formation in Yersinia pestis.
    Mol Microbiol. 2004 Oct;54(1):75-88 PMID: 15458406
  19. Role of the GGDEF protein family in Salmonella cellulose biosynthesis and biofilm formation.
    Mol Microbiol. 2004 Oct;54(1):264-77 PMID: 15458421
  20. Biochemistry of vibrio cholerae virulence. II. Skin permeability factor-cholera enterotoxin production in a chemically defined medium.
    Infect Immun. 1971 Nov;4(5):611-8 PMID: 5170548
  21. Enzyme-linked immunosorbent assays for cholera serology.
    Infect Immun. 1973 May;7(5):759-63 PMID: 4202959
  22. Trans-complementation-dependent replication of a low molecular weight origin fragment from plasmid R6K.
    Cell. 1978 Dec;15(4):1199-208 PMID: 728998
  23. Ecological relationships between Vibrio cholerae and planktonic crustacean copepods.
    Appl Environ Microbiol. 1983 Jan;45(1):275-83 PMID: 6337551
  24. Studies on transformation of Escherichia coli with plasmids.
    J Mol Biol. 1983 Jun 5;166(4):557-80 PMID: 6345791
  25. Genetic analysis of the cholera toxin-positive regulatory gene toxR.
    J Bacteriol. 1985 Aug;163(2):580-5 PMID: 2991197
  26. Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin.
    Proc Natl Acad Sci U S A. 1987 May;84(9):2833-7 PMID: 2883655
  27. A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR.
    J Bacteriol. 1988 Jun;170(6):2575-83 PMID: 2836362
  28. Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans.
    J Exp Med. 1988 Oct 1;168(4):1487-92 PMID: 2902187
  29. Cyclic diguanylic acid and cellulose synthesis in Agrobacterium tumefaciens.
    J Bacteriol. 1989 Dec;171(12):6649-55 PMID: 2556370
  30. Attachment of Vibrio cholerae serogroup O1 to zooplankton and phytoplankton of Bangladesh waters.
    Appl Environ Microbiol. 1990 Jun;56(6):1977-80 PMID: 2383016
  31. A series of wide-host-range low-copy-number vectors that allow direct screening for recombinants.
    Gene. 1991 Jan 2;97(1):39-47 PMID: 1847347
  32. Polypeptide composition of bacterial cyclic diguanylic acid-dependent cellulose synthase and the occurrence of immunologically crossreacting proteins in higher plants.
    Proc Natl Acad Sci U S A. 1991 Jun 15;88(12):5472-6 PMID: 1647035
  33. Construction of an eae deletion mutant of enteropathogenic Escherichia coli by using a positive-selection suicide vector.
    Infect Immun. 1991 Dec;59(12):4310-7 PMID: 1937792
  34. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter.
    J Bacteriol. 1995 Jul;177(14):4121-30 PMID: 7608087
  35. Precise large deletions by the PCR-based overlap extension method.
    Mol Biotechnol. 1995 Aug;4(1):13-5 PMID: 8521036
  36. Use of recombinase gene fusions to identify Vibrio cholerae genes induced during infection.
    Mol Microbiol. 1995 Nov;18(4):671-83 PMID: 8817490
  37. c-di-GMP-binding protein, a new factor regulating cellulose synthesis in Acetobacter xylinum.
    FEBS Lett. 1997 Oct 20;416(2):207-11 PMID: 9369216
  38. Differential regulation of multiple flagellins in Vibrio cholerae.
    J Bacteriol. 1998 Jan;180(2):303-16 PMID: 9440520
  39. The Pfam protein families database.
    Nucleic Acids Res. 2004 Jan 1;32(Database issue):D138-41 PMID: 14681378
  40. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain.
    Genes Dev. 2004 Mar 15;18(6):715-27 PMID: 15075296
  41. Cyclic diguanylate (c-di-GMP) regulates Vibrio cholerae biofilm formation.
    Mol Microbiol. 2004 Aug;53(3):857-69 PMID: 15255898
  42. GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility.
    Mol Microbiol. 2004 Aug;53(4):1123-34 PMID: 15306016
  43. Nucleotide sequence and spatiotemporal expression of the Vibrio cholerae vieSAB genes during infection.
    J Bacteriol. 1998 May;180(9):2298-305 PMID: 9573178
  44. Distinct roles of an alternative sigma factor during both free-swimming and colonizing phases of the Vibrio cholerae pathogenic cycle.
    Mol Microbiol. 1998 May;28(3):501-20 PMID: 9632254
  45. Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: genetic organization and occurrence of conserved domains in isoenzymes.
    J Bacteriol. 1998 Sep;180(17):4416-25 PMID: 9721278
  46. Structural basis of activity and allosteric control of diguanylate cyclase.
    Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17084-9 PMID: 15569936
  47. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain.
    J Bacteriol. 2005 Mar;187(5):1792-8 PMID: 15716451
  48. A glutamate-alanine-leucine (EAL) domain protein of Salmonella controls bacterial survival in mice, antioxidant defence and killing of macrophages: role of cyclic diGMP.
    Mol Microbiol. 2005 Jun;56(5):1234-45 PMID: 15882417
  49. The phosphodiesterase activity of the HmsP EAL domain is required for negative regulation of biofilm formation in Yersinia pestis.
    FEMS Microbiol Lett. 2005 Jun 15;247(2):123-30 PMID: 15935569
  50. The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains.
    J Bacteriol. 2005 Jul;187(14):4774-81 PMID: 15995192
  51. Cyclic diguanylate regulates Vibrio cholerae virulence gene expression.
    Infect Immun. 2005 Sep;73(9):5873-82 PMID: 16113306
  52. Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP.
    J Biol Chem. 2005 Sep 2;280(35):30829-37 PMID: 15994307
  53. Roles of the regulatory proteins FlhF and FlhG in the Vibrio cholerae flagellar transcription hierarchy.
    J Bacteriol. 2005 Sep;187(18):6324-32 PMID: 16159765
  54. The EAL domain protein VieA is a cyclic diguanylate phosphodiesterase.
    J Biol Chem. 2005 Sep 30;280(39):33324-30 PMID: 16081414
  55. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels.
    Proc Natl Acad Sci U S A. 2005 Oct 4;102(40):14422-7 PMID: 16186483
Article Info
Journal
The Journal of biological chemistry
Abbr.
J Biol Chem
ISSN
0021-9258
DOI
10.1074/jbc.M611593200
Published
2007-04-27
Epub
2007-00-16
Pages
12860-70
Language
English
Region
United States
NLM ID
2985121R
PMCID
PMC2790426
Subset
IM
Grants
NIDDK NIH HHS · P30 DK34928 · United States
NIDDK NIH HHS · P30 DK034928 · United States
NIAID NIH HHS · R01 AI045746-06A1 · United States
Howard Hughes Medical Institute · United States
NIAID NIH HHS · R01 AI045746 · United States
NIAID NIH HHS · AI45746 · United States
External Links
PubMed source DOI: 10.1074/jbc.M611593200 PMC Full Text View journal details
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