The multi-output incoherent feedforward loop constituted by the transcriptional regulators LasR and RsaL confers robustness to a subset of quorum sensing genes in: Pseudomonas aeruginosa

Molecular BioSystems

Volumn 13, Issue 6, 2017, Pages 1080-1089

  Bondí, Roslen ^a,b   Longo, Francesca ^a,c   Messina, Marco ^a   D'Angelo, Francesca ^a   Visca, Paolo ^a   Leoni, Livia ^a   Rampioni, Giordano ^a  

^a ROMA TRE UNIVERSITY   (Italy)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; GAMMA BUTYROLACTONE; HOMOSERINE; HOMOSERINE LACTONE; LASR PROTEIN, PSEUDOMONAS AERUGINOSA; N-(3-OXODODECANOYL)HOMOSERINE LACTONE; REPRESSOR PROTEIN; RSAL PROTEIN, PSEUDOMONAS AERUGINOSA; TRANSACTIVATOR PROTEIN;

ANALOGS AND DERIVATIVES; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; QUORUM SENSING;

4-BUTYROLACTONE; BACTERIAL PROTEINS; GENE EXPRESSION REGULATION; HOMOSERINE; PSEUDOMONAS AERUGINOSA; QUORUM SENSING; REPRESSOR PROTEINS; TRANS-ACTIVATORS;

EID: 85021645620     PISSN: 1742206X     EISSN: 17422051     Source Type: Journal    
DOI: 10.1039/c7mb00040e     Document Type: Article

References (69)

1. R. Milo S. Shen-Orr S. Itzkovitz N. Kashtan D. Chklovskii U. Alon Network motifs: simple building blocks of complex networks Science 2002 298 824 827
2. U. Alon Network motifs: theory and experimental approaches Nat. Rev. Genet. 2007 8 450 461
3. S. Mangan U. Alon Structure and function of the feed-forward loop network motif Proc. Natl. Acad. Sci. U. S. A. 2003 100 11980 11985
4. Y. Hart U. Alon The utility of paradoxical components in biological circuits Mol. Cell 2013 49 213 221
5. T. I. Lee N. J. Rinaldi F. Robert D. T. Odom Z. Bar-Joseph G. K. Gerber N. M. Hannett C. T. Harbison C. M. Thompson I. Simon J. Zeitlinger E. G. Jennings H. L. Murray D. B. Gordon B. Ren J. J. Wyrick J. B. Tagne T. L. Volkert E. Fraenkel D. K. Gifford R. A. Young Transcriptional regulatory networks in Saccharomyces cerevisiae Science 2002 298 799 804
6. L. A. Boyer T. I. Lee M. F. Cole S. E. Johnstone S. S. Levine J. P. Zucker M. G. Guenther R. M. Kumar H. L. Murray R. G. Jenner D. K. Gifford D. A. Melton R. Jaenisch R. A. Young Core transcriptional regulatory circuitry in human embryonic stem cells Cell 2005 122 947 956
7. G. Swiers R. Patient M. Loose Genetic regulatory networks programming hematopoietic stem cells and erythroid lineage specification Dev. Biol. 2006 294 525 540
8. H. D. MacGillavry F. J. Stam M. M. Sassen L. Kegel W. T. Hendriks J. Verhaagen A. B. Smit R. E. van Kesteren NFIL3 and cAMP response element-binding protein form a transcriptional feedforward loop that controls neuronal regeneration-associated gene expression J. Neurosci. 2009 29 15542 15550
9. N. Chevrier P. Mertins M. N. Artyomov A. K. Shalek M. Iannacone M. F. Ciaccio I. Gat-Viks E. Tonti M. M. DeGrace K. R. Clauser M. Garber T. M. Eisenhaure N. Yosef J. Robinson A. Sutton M. S. Andersen D. E. Root U. von Andrian R. B. Jones H. Park S. A. Carr A. Regev I. Amit N. Hacohen Systematic discovery of TLR signaling components delineates viral-sensing circuits Cell 2011 147 853 867
10. R. J. Johnston Jr Y. Otake P. Sood N. Vogt R. Behnia D. Vasiliauskas E. McDonald B. Xie S. Koenig R. Wolf T. Cook B. Gebelein E. Kussell H. Nakagoshi C. Desplan Interlocked feedforward loops control cell-type-specific Rhodopsin expression in the Drosophila eye Cell 2011 145 956 968
11. K. Takeda D. Shao M. Adler P. G. Charest W. F. Loomis H. Levine A. Groisman W. J. Rappel R. A. Firtel Incoherent feedforward control governs adaptation of activated Ras in a eukaryotic chemotaxis pathway Sci. Signaling 2012 5 205 ra2 10.1126/scisignal.2002413
12. A. Nakajima S. Ishihara D. Imoto S. Sawai Rectified directional sensing in long-range cell migration Nat. Commun. 2014 5 5367
13. P. Bu L. Wang K. Y. Chen T. Srinivasan P. K. Murthy K. L. Tung A. K. Varanko H. J. Chen Y. Ai S. King S. M. Lipkin X. Shen A miR-34a-Numb feedforward loop triggered by inflammation regulates asymmetric stem cell division in intestine and colon cancer Cell Stem Cell 2016 18 189 202
14. P. Eichenberger M. Fujita S. T. Jensen E. M. Conlon D. Z. Rudner S. T. Wang C. Ferguson K. Haga T. Sato J. S. Liu R. Losick The program of gene transcription for a single differentiating cell type during sporulation in Bacillus subtilis PLoS Biol. 2004 2 10 e328 10.1371/journal.pbio.0020328
15. S. Mangan S. Itzkovitz A. Zaslaver U. Alon The incoherent feed-forward loop accelerates the response-time of the gal system of Escherichia coli. J. Mol. Biol. 2006 356 1073 1081
16. S. Kaplan A. Bren E. Dekel U. Alon The incoherent feedforward loop can generate non-monotonic input functions for genes Mol. Syst. Biol. 2008 4 203
17. M. Schuster M. L. Urbanowski E. P. Greenberg Promoter specificity in Pseudomonas aeruginosa quorum sensing revealed by DNA binding of purified LasR Proc. Natl. Acad. Sci. U. S. A. 2004 101 15833 15839
18. G. Rampioni I. Bertani E. Zennaro F. Polticelli V. Venturi L. Leoni The quorum-sensing negative regulator RsaL of Pseudomonas aeruginosa binds to the lasI promoter J. Bacteriol. 2006 188 815 819
19. G. Rampioni M. Schuster E. P. Greenberg I. Bertani M. Grasso V. Venturi E. Zennaro L. Leoni RsaL provides quorum sensing homeostasis and functions as a global regulator of gene expression in Pseudomonas aeruginosa Mol. Microbiol. 2007 66 1557 1565
20. M. Schuster E. P. Greenberg A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa Int. J. Med. Microbiol. 2006 296 73 81
21. P. Williams M. Cámara Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules Curr. Opin. Microbiol. 2009 12 182 191
22. K. B. Gilbert T. H. Kim R. Gupta E. P. Greenberg M. Schuster Global position analysis of the Pseudomonasaeruginosa quorum-sensing transcription factor LasR Mol. Microbiol. 2009 73 1072 1085
23. H. Kang J. Gan J. Zhao W. Kong J. Zhang M. Zhu F. Li Y. Song J. Qin H. Liang Crystal structure of Pseudomonas aeruginosa RsaL bound to promoter DNA reaffirms its role as a global regulator involved in quorum-sensing Nucleic Acids Res. 2016 45 699 710
24. V. Venturi Regulation of quorum sensing in Pseudomonas FEMS Microbiol. Rev. 2006 30 274 291
25. S. P. Brown D. M. Cornforth N. Mideo Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control Trends Microbiol. 2012 20 336 342
26. R. Bondí M. Messina I. De Fino A. Bragonzi G. Rampioni L. Leoni Affecting Pseudomonas aeruginosa phenotypic plasticity by quorum sensing dysregulation hampers pathogenicity in murine chronic lung infection PLoS One 2014 9 11 e112105 10.1371/journal.pone.0112105
27. S. Basu R. Mehreja S. Thiberge M. T. Chen R. Weiss Spatiotemporal control of gene expression with pulse-generating networks Proc. Natl. Acad. Sci. U. S. A. 2004 101 6355 6360
28. H. W. Ma B. Kumar U. Ditges F. Gunzer J. Buer A. P. Zeng An extended transcriptional regulatory network of Escherichia coli and analysis of its hierarchical structure and network motifs Nucleic Acids Res. 2004 32 6643 6649
29. R. Entus B. Aufderheide H. M. Sauro Design and implementation of three incoherent feed-forward motif based biological concentration sensors Syst. Synth. Biol. 2007 1 119 128
30. L. Goentoro O. Shoval M. W. Kirschner U. Alon The incoherent feedforward loop can provide fold-change detection in gene regulation Mol. Cell 2009 36 894 899
31. L. Bleris Z. Xie D. Glass A. Adadey E. Sontag Y. Benenson Synthetic incoherent feedforward circuits show adaptation to the amount of their genetic template Mol. Syst. Biol. 2011 7 519
32. M. Osella C. Bosia D. Corá M. Caselle The role of incoherent microRNA-mediated feedforward loops in noise buffering PLoS Comput. Biol. 2011 7 3 e1001101 10.1371/journal.pcbi.1001101
33. G. Rodrigo S. F. Elena Structural discrimination of robustness in transcriptional feedforward loops for pattern formation PLoS One 2011 6 2 e16904 10.1371/journal.pone.0016904
34. G. Buzi M. Khammash Implementation considerations, not topological differences, are the main determinants of noise suppression properties in feedback and incoherent feedforward circuits PLoS Comput. Biol. 2016 12 6 e1004958 10.1371/journal.pcbi.1004958
35. X. Li J. J. Cassidy C. A. Reinke S. Fischboeck R. W. Carthew A microRNA imparts robustness against environmental fluctuation during development Cell 2009 137 273 282
36. M. S. Ebert P. A. Sharp Roles for microRNAs in conferring robustness to biological processes Cell 2012 149 515 524
37. F. Longo G. Rampioni R. Bondì F. Imperi G. M. Fimia P. Visca E. Zennaro L. Leoni A new transcriptional repressor of the Pseudomonas aeruginosa quorum sensing receptor gene lasR PLoS One 2013 8 7 e69554 10.1371/journal.pone.0069554
38. A. M. Albus E. C. Pesci L. J. Runyen-Janecky S. E. West B. H. Iglewski Vfr controls quorum sensing in Pseudomonas aeruginosa J. Bacteriol. 1987 179 3928 3935
39. R. Simon U. Priefer A. Puhler A broad host range mobilization system for in vivo genetic-engineering: transposon mutagenesis in Gram-negative bacteria Biotechnology 1983 1 784 791
40. J. Sambrook, E. F. Fritsch and T. Maniatis, Molecular cloning: a laboratory manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 2nd edn, 1989
41. D. H. Figurski D. R. Helinski Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans Proc. Natl. Acad. Sci. U. S. A. 1979 76 1648 1652
42. D. L. Milton R. O'Toole P. Horstedt H. Wolf-Watz Flagellin A is essential for the virulence of Vibrio anguillarum J. Bacteriol. 1996 178 1310 1319
43. T. T. Hoang R. R. Karkhoff-Schweizer A. J. Kutchma H. P. Schweizer 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 1998 212 77 86
44. C. N. Wilder S. P. Diggle M. Schuster Cooperation and cheating in Pseudomonas aeruginosa: the roles of the lasrhl and pqs quorum-sensing systems ISME J. 2011 5 1332 1343
45. J. H. Miller, Experiments in molecular genetics, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, 1972
46. D. E. Ohman R. P. Burns B. H. Iglewski Corneal infections in mice with toxin A and elastase mutants of Pseudomonas aeruginosa J. Infect. Dis. 1980 142 547 555
47. E. Kessler M. Israel N. Landshman A. Chechick S. Blumberg In vitro inhibition of Pseudomonas aeruginosa elastase by metal-chelating peptide derivatives Infect. Immun. 1982 38 716 723
48. G. Rampioni M. Schuster E. P. Greenberg E. Zennaro L. Leoni Contribution of the RsaL global regulator to Pseudomonas aeruginosa virulence and biofilm formation FEMS Microbiol. Lett. 2009 301 210 217
49. F. Massai F. Imperi S. Quattrucci E. Zennaro P. Visca L. Leoni A multitask biosensor for micro-volumetric detection of N -3-oxo-dodecanoyl-homoserine lactone quorum sensing signal Biosens. Bioelectron. 2011 26 3444 3449
50. N. Kashtan S. Itzkovitz R. Milo U. Alon Efficient sampling algorithm for estimating subgraph concentrations and detecting network motifs Bioinformatics 2004 20 1746 1758
51. S. Su B. Chen Z. J. Jin L. Zhou Y. L. Fang C. Thawai G. Rampioni Y. W. He Characterization of the multiple molecular mechanisms underlying RsaL control of phenazine-1-carboxylic acid biosynthesis in the rhizosphere bacterium Pseudomonas aeruginosa PA1201 Mol. Microbiol. 2017 10.1111/mmi.13671
52. F. Ledgham C. Soscia A. Chakrabarty A. Lazdunski M. Foglino Global regulation in Pseudomonas aeruginosa: the regulatory protein AlgR2 (AlgQ) acts as a modulator of quorum sensing Res. Microbiol. 2003 154 207 213
53. M. Schuster C. P. Lostroh T. Ogi E. P. Greenberg Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis J. Bacteriol. 2003 185 2066 2079
54. M. Hentzer H. Wu J. B. Andersen K. Riedel T. B. Rasmussen N. Bagge N. Kumar M. A. Schembri Z. Song P. Kristoffersen M. Manefield J. W. Costerton S. Molin L. Eberl P. Steinberg S. Kjelleberg N. Høiby M. Givskov Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors EMBO J. 2003 22 3803 3815
55. V. E. Wagner D. Bushnell L. Passador A. I. Brooks B. H. Iglewski Microarray analysis of Pseudomonas aeruginosa quorum-sensing regulons: effects of growth phase and environment J. Bacteriol. 2003 185 2080 2095
56. M. Schuster E. P. Greenberg Early activation of quorum sensing in Pseudomonas aeruginosa reveals the architecture of a complex regulon BMC Genomics 2007 8 287 10.1186/1471-2164-8-287
57. D. M. Cornforth R. Popat L. McNally J. Gurney T. C. Scott-Phillips A. Ivens S. P. Diggle S. P. Brown Combinatorial quorum sensing allows bacteria to resolve their social and physical environment Proc. Natl. Acad. Sci. U. S. A. 2014 111 4280 4284
58. S. Furukawa S. L. Kuchma G. A. O'Toole Keeping their options open: acute versus persistent infections J. Bacteriol. 2006 188 1211 1217
59. C. Winstanley J. L. Fothergill The role of quorum sensing in chronic cystic fibrosis Pseudomonas aeruginosa infections FEMS Microbiol. Lett. 2009 290 1 9
60. A. K. Jones N. B. Fulcher G. J. Balzer M. L. Urbanowski C. L. Pritchett M. J. Schurr T. L. Yahr M. C. Wolfgang Activation of the Pseudomonas aeruginosa AlgU regulon through mucA mutation inhibits cyclic AMP/Vfr signaling J. Bacteriol. 2010 192 5709 5717
61. B. Ryall M. Carrara J. E. Zlosnik V. Behrends X. Lee Z. Wong K. E. Lougheed H. D. Williams The mucoid switch in Pseudomonas aeruginosa represses quorum sensing systems and leads to complex changes to stationary phase virulence factor regulation PLoS One 2014 9 5 e96166 10.1371/journal.pone.0096166
62. S. A. Beatson C. B. Whitchurch J. L. Sargent R. C. Levesque J. S. Mattick Differential regulation of twitching motility and elastase production by Vfr in Pseudomonasaeruginosa J. Bacteriol. 2002 184 3605 3613
63. R. S. Smith M. C. Wolfgang S. Lory An adenylate cyclase-controlled signaling network regulates Pseudomonas aeruginosa virulence in a mouse model of acute pneumonia Infect. Immun. 2004 72 1677 1684
64. H. Almblad J. J. Harrison M. Rybtke J. Groizeleau M. Givskov M. R. Parsek T. Tolker-Nielsen The cyclic AMP-Vfr signaling pathway in Pseudomonas aeruginosa is inhibited by cyclic di-GMP J. Bacteriol. 2015 197 2190 2200
65. V. Venturi G. Rampioni S. Pongor L. Leoni The virtue of temperance: built-in negative regulators of quorum sensing in Pseudomonas Mol. Microbiol. 2011 82 1060 1070
66. G. Rampioni I. Bertani C. R. Pillai V. Venturi E. Zennaro L. Leoni Functional characterization of the quorum sensing regulator RsaL in the plant-beneficial strain Pseudomonas putida WCS358 Appl. Environ. Microbiol. 2012 78 726 734
67. R. Hazan J. He G. Xiao V. Dekimpe Y. Apidianakis B. Lesic C. Astrakas E. Déziel F. Lépine L. G. Rahme Homeostatic interplay between bacterial cell-cell signaling and iron in virulence PLoS Pathog. 2010 6 3 e1000810 10.1371/journal.ppat.1000810
68. G. Rampioni C. Pustelny M. P. Fletcher V. J. Wright M. Bruce K. P. Rumbaugh S. Heeb M. Cámara P. Williams Transcriptomic analysis reveals a global alkyl-quinolone-independent regulatory role for PqsE in facilitating the environmental adaptation of Pseudomonas aeruginosa to plant and animal hosts Environ. Microbiol. 2010 12 1659 1673
69. G. Rampioni M. Falcone S. Heeb E. Frangipani M. P. Fletcher J. F. Dubern P. Visca L. Leoni M. Cámara P. Williams Unravelling the genome-wide contributions of specific 2-alkyl-4-quinolones and PqsE to quorum sensing in Pseudomonas aeruginosa PLoS Pathog. 2016 12 11 e1006029 10.1371/journal.ppat.1006029