Oligoribonuclease is a central feature of cyclic diguanylate signaling in Pseudomonas aeruginosa

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 36, 2015, Pages 11359-11364

  Cohen, Dorit ^a   Mechold, Undine ^b   Nevenzal, Hadas ^a   Yarmiyhu, Yafit ^a   Randall, Trevor E ^c   Bay, Denice C ^d   Rich, Jacquelyn D ^c   Parsek, Matthew R ^e   Kaever, Volkhard ^f   Harrison, Joe J ^c   Banin, Ehud ^a  

^a BAR ILAN UNIVERSITY   (Israel)

^b INSTITUT PASTEUR   (France)

^c UNIVERSITY OF CALGARY   (Canada)

^d UNIVERSITY OF MANITOBA   (Canada)

^e UNIVERSITY OF WASHINGTON   (United States)

^f HANNOVER MEDICAL SCHOOL   (Germany)

Author keywords

Biofilm; Cyclic diguanylate; EAL domain; Oligoribonuclease; Pseudomonas aeruginosa

Indexed keywords

ALANINE; CYCLIC DIGUANYLATE; CYCLIC GMP; EXONUCLEASE; GLUTAMIC ACID; LEUCINE; NUCLEASE; OLIGOMER; OLIGORIBONUCLEASE; POLYMER; RIBONUCLEASE; RNA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; BIS(3',5')-CYCLIC DIGUANYLIC ACID; DEOXYDIGUANOSINE DIPHOSPHOSPHATE; DEOXYGUANOSINE PHOSPHATE; DIGUANYLATE CYCLASE; ESCHERICHIA COLI PROTEIN; EXORIBONUCLEASE; LYASE; PHOSPHODIESTERASE;

ARTICLE; BACTERIAL CELL; CATALYSIS; CELL LYSATE; ENZYME ACTIVITY; ENZYME DEGRADATION; GENE EXPRESSION; IN VITRO STUDY; NEGATIVE FEEDBACK; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; GENE EXPRESSION REGULATION; GENETICS; HOMEOSTASIS; METABOLISM; MUTATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CYCLIC GMP; DEOXYGUANINE NUCLEOTIDES; ESCHERICHIA COLI PROTEINS; EXORIBONUCLEASES; GENE EXPRESSION REGULATION, BACTERIAL; HOMEOSTASIS; MUTATION; PHOSPHORIC DIESTER HYDROLASES; PHOSPHORUS-OXYGEN LYASES; PSEUDOMONAS AERUGINOSA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

EID: 84941236860     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421450112     Document Type: Article

References (45)

1. Römling U, Galperin MY, Gomelsky M (2013) Cyclic di-GMP: The first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 77(1):1-52.
2. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat RevMicrobiol 7(4):263-273.
3. Schirmer T, Jenal U (2009) Structural and mechanistic determinants of c-di-GMP signalling. Nat Rev Microbiol 7(10):724-735.
4. 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(35):30829-30837.
5. Ryan RP, et al. (2006) Cell-cell signaling in Xanthomonas campestris involves an HDGYP domain protein that functions in cyclic di-GMP turnover. Proc Natl Acad Sci USA 103(17):6712-6717.
6. Bellini D, et al. (2014) Crystal structure of an HD-GYP domain cyclic-di-GMP phosphodiesterase reveals an enzyme with a novel trinuclear catalytic iron centre. Mol Microbiol 91(1):26-38.
7. Stelitano V, et al. (2013) C-di-GMP hydrolysis by Pseudomonas aeruginosa HD-GYP phosphodiesterases: Analysis of the reaction mechanism and novel roles for pGpG. PLoS One 8(9):e74920.
8. Ross P, et al. (1987) Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid. Nature 325(6101):279-281.
9. Mechold U, Fang G, Ngo S, Ogryzko V, Danchin A (2007) YtqI from Bacillus subtilis has both oligoribonuclease and pAp-phosphatase activity. Nucleic Acids Res 35(13):4552-4561.
10. Fang M, et al. (2009) Degradation of nanoRNA is performed by multiple redundant RNases in Bacillus subtilis. Nucleic Acids Res 37(15):5114-5125.
11. Ghosh S, Deutscher MP (1999) Oligoribonuclease is an essential component of the mRNA decay pathway. Proc Natl Acad Sci USA 96(8):4372-4377.
12. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci USA 102(40):14422-14427.
13. Goldman SR, et al. (2011) NanoRNAs prime transcription initiation in vivo. Mol Cell 42(6):817-825.
14. Jacobs MA, et al. (2003) Comprehensive transposon mutant library of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100(24):14339-14344.
15. Baraquet C, Murakami K, Parsek MR, Harwood CS (2012) The FleQ protein from Pseudomonas aeruginosa functions as both a repressor and an activator to control gene expression from the pel operon promoter in response to c-di-GMP. Nucleic Acids Res 40(15):7207-7218.
16. Niyogi SK, Datta AK (1975) A novel oligoribonuclease of Escherichia coli. I. Isolation and properties. J Biol Chem 250(18):7307-7312.
17. Datta AK, Niyogi K (1975) A novel oligoribonuclease of Escherichia coli. II. Mechanism of action. J Biol Chem 250(18):7313-7319.
18. Rao F, Yang Y, Qi Y, Liang ZX (2008) Catalytic mechanism of cyclic di-GMP-specific phosphodiesterase: A study of the EAL domain-containing RocR from Pseudomonas aeruginosa. J Bacteriol 190(10):3622-3631.
19. Sharma IM, Dhanaraman T, Mathew R, Chatterji D (2012) Synthesis and characterization of a fluorescent analogue of cyclic di-GMP. Biochemistry 51(27):5443-5453.
20. Tal R, et al. (1998) Three cdg operons control cellular turnover of cyclic di-GMP in Acetobacter xylinum: Genetic organization and occurrence of conserved domains in isoenzymes. J Bacteriol 180(17):4416-4425.
21. Schmidt AJ, Ryjenkov DA, Gomelsky M (2005) The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: Enzymatically active and inactive EAL domains. J Bacteriol 187(14):4774-4781.
22. Edgar R, Domrachev M, Lash AE (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30(1):207-210.
23. O'Toole GA, Kolter R (1998) Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: A genetic analysis. Mol Microbiol 28(3):449-461.
24. Peterson SB, et al. (2011) Different methods for culturing biofilms in vitro. Biofilm Infections, eds Bjarnsholt T, Jensen PØ, Moser C, Høiby N (Springer, New York), pp 251-266.
25. Spangler C, Böhm A, Jenal U, Seifert R, Kaever V (2010) A liquid chromatographycoupled tandem mass spectrometry method for quantitation of cyclic di-guanosine monophosphate. J Microbiol Methods 81(3):226-231.
26. Chugani S, et al. (2012) Strain-dependent diversity in the Pseudomonas aeruginosa quorum-sensing regulon. Proc Natl Acad Sci USA 109(41):E2823-E2831.
27. (T))) Method. Methods 25(4):402-408.
28. Kulasakara H, et al. (2006) Analysis of Pseudomonas aeruginosa diguanylate cyclases and phosphodiesterases reveals a role for bis-(3'-5')-cyclic-GMP in virulence. Proc Natl Acad Sci USA 103(8):2839-2844.
29. Altschul SF, et al. (1997) Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 25(17):3389-3402.
30. Papadopoulos JS, Agarwala R (2007) COBALT: Constraint-based alignment tool for multiple protein sequences. Bioinformatics 23(9):1073-1079.
31. Waterhouse AM, Procter JB, Martin DM, Clamp M, Barton GJ (2009) Jalview Version 2-a multiple sequence alignment editor and analysis workbench. Bioinformatics 25(9):1189-1191.
32. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572-1574.
33. Han MV, Zmasek CM (2009) phyloXML: XML for evolutionary biology and comparative genomics. BMC Bioinformatics 10:356.
34. Green MR, Sambrook J (2012) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY).
35. Choi KH, Kumar A, Schweizer HP (2006) A 10-min method for preparation of highly electrocompetent Pseudomonas aeruginosa cells: Application for DNA fragment transfer between chromosomes and plasmid transformation. J Microbiol Methods 64(3):391-397.
36. Schweizer HP (1991) Escherichia-Pseudomonas shuttle vectors derived from pUC18/19. Gene 97(1):109-121.
37. Hoang TT, Karkhoff-Schweizer RR, Kutchma AJ, Schweizer HP (1998) A broad-hostrange Flp-FRT recombination system for site-specific excision of chromosomallylocated DNA sequences: Application for isolation of unmarked Pseudomonas aeruginosa mutants. Gene 212(1):77-86.
38. Zhao K, et al. (2013) Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms. Nature 497(7449):388-391.
39. Tseng BS, et al. (2013) The extracellular matrix protects Pseudomonas aeruginosa biofilms by limiting the penetration of tobramycin. Environ Microbiol 15(10):2865-2878.
40. Milo R, Jorgensen P, Moran U, Weber G, Springer M (2010) BioNumbers-the database of key numbers in molecular and cell biology. Nucleic Acids Res 38(Database issue):D750-D753.
41. Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: Transposon mutagenesis in gram negative bacteria. Nat Biotechnol 1(9):784-791.
42. Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci USA 102(31):11076-11081.
43. Guzman LM, Belin D, Carson MJ, Beckwith J (1995) Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177(14):4121-4130.
44. Tomlin KL, Clark SR, Ceri H (2004) Green and red fluorescent protein vectors for use in biofilm studies of the intrinsically resistant Burkholderia cepacia complex. J Microbiol Methods 57(1):95-106.
45. Singh PK, et al. (2000) Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms. Nature 407(6805):762-764.