A Host-Produced Autoinducer-2 Mimic Activates Bacterial Quorum Sensing

Cell Host and Microbe

Volumn 19, Issue 4, 2016, Pages 470-480

  Ismail, Anisa S ^a   Valastyan, Julie S ^a,b   Bassler, Bonnie L ^a,b  

^a PRINCETON UNIVERSITY   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOINDUCER 1 PROTEIN; AUTOINDUCER 2 PROTEIN; BACTERIAL PROTEIN; LACTATE DEHYDROGENASE; LSRB PROTEIN; LUXP PROTEIN; PROTEIN; TRANSKETOLASE; UNCLASSIFIED DRUG; HOMOSERINE; LACTONE; N-OCTANOYLHOMOSERINE LACTONE;

A549 CELL LINE; ARTICLE; BACTERIAL CELL; BACTERIAL COUNT; BACTERIAL STRAIN; CACO 2 CELL LINE; CELL COMPONENT; CELL COUNT; CELL DEATH; CELL FUNCTION; CELL GROWTH; CELL MEMBRANE PERMEABILITY; CELL STIMULATION; CELL STRESS; COCULTURE; CONTROLLED STUDY; CYTOTOXICITY; ENZYME ACTIVITY; ENZYME RELEASE; EPITHELIUM CELL; ESCHERICHIA COLI; FEMALE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE IDENTIFICATION; GENE INACTIVATION; HELA CELL LINE; HOST BACTERIAL SYMBIOSIS; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; INCUBATION TIME; JURKAT CELL LINE; MICROBIAL ACTIVITY; MOLECULAR INTERACTION; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEIN SYNTHESIS; QUORUM SENSING; SALMONELLA ENTERICA SEROVAR TYPHIMURIUM; SIGNAL TRANSDUCTION; SYMBIOSIS; TIGHT JUNCTION; U937 CELL LINE; VIBRIO HARVEYI; ANALOGS AND DERIVATIVES; ANIMAL; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; SALMONELLOSIS;

ANIMALS; BACTERIAL PROTEINS; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, BACTERIAL; HOMOSERINE; HOST-PATHOGEN INTERACTIONS; HUMANS; LACTONES; QUORUM SENSING; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM;

EID: 84961226707     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2016.02.020     Document Type: Article

References (66)

1. L. Abrami, M. Fivaz, P.E. Glauser, N. Sugimoto, C. Zurzolo, and F.G. van der Goot Sensitivity of polarized epithelial cells to the pore-forming toxin aerolysin Infect. Immun. 71 2003 739 746
2. F. Bäckhed, R.E. Ley, J.L. Sonnenburg, D.A. Peterson, and J.I. Gordon Host-bacterial mutualism in the human intestine Science 307 2005 1915 1920
3. T. Bansal, R.C. Alaniz, T.K. Wood, and A. Jayaraman The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation Proc. Natl. Acad. Sci. USA 107 2010 228 233
4. B.L. Bassler, M. Wright, R.E. Showalter, and M.R. Silverman Intercellular signalling in Vibrio harveyi: sequence and function of genes regulating expression of luminescence Mol. Microbiol. 9 1993 773 786
5. B.L. Bassler, M. Wright, and M.R. Silverman Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway Mol. Microbiol. 13 1994 273 286
6. B.L. Bearson, and S.M. Bearson The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium Microb. Pathog. 44 2008 271 278
7. S. Björck, E. Jennische, A. Dahlström, and H. Ahlman Influence of topical rectal application of drugs on dextran sulfate-induced colitis in rats Dig. Dis. Sci. 42 1997 824 832
8. J.R. Brestoff, and D. Artis Commensal bacteria at the interface of host metabolism and the immune system Nat. Immunol. 14 2013 676 684
9. R. Bücker, S.M. Krug, R. Rosenthal, D. Günzel, A. Fromm, M. Zeitz, T. Chakraborty, M. Fromm, H.J. Epple, and J.D. Schulzke Aerolysin from Aeromonas hydrophila perturbs tight junction integrity and cell lesion repair in intestinal epithelial HT-29/B6 cells J. Infect. Dis. 204 2011 1283 1292
10. J.G. Cao, and E.A. Meighen Purification and structural identification of an autoinducer for the luminescence system of Vibrio harveyi J. Biol. Chem. 264 1989 21670 21676
11. E. Cario, I.M. Rosenberg, S.L. Brandwein, P.L. Beck, H.C. Reinecker, and D.K. Podolsky Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors J. Immunol. 164 2000 966 972
12. X. Chen, S. Schauder, N. Potier, A. Van Dorsselaer, I. Pelczer, B.L. Bassler, and F.M. Hughson Structural identification of a bacterial quorum-sensing signal containing boron Nature 415 2002 545 549
13. T. Chinen, and A.Y. Rudensky The effects of commensal microbiota on immune cell subsets and inflammatory responses Immunol. Rev. 245 2012 45 55
14. H. Chu, and S.K. Mazmanian Innate immune recognition of the microbiota promotes host-microbial symbiosis Nat. Immunol. 14 2013 668 675
15. M.J. Federle Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signaling Contrib. Microbiol. 16 2009 18 32
16. S. Ferluga, and V. Venturi OryR is a LuxR-family protein involved in interkingdom signaling between pathogenic Xanthomonas oryzae pv. oryzae and rice J. Bacteriol. 191 2009 890 897
17. P.P. Freestone, R.D. Haigh, P.H. Williams, and M. Lyte Stimulation of bacterial growth by heat-stable, norepinephrine-induced autoinducers FEMS Microbiol. Lett. 172 1999 53 60
18. B.K. Hammer, and B.L. Bassler Quorum sensing controls biofilm formation in Vibrio cholerae Mol. Microbiol. 50 2003 101 104
19. J.L. Han, and H.L. Lin Intestinal microbiota and type 2 diabetes: from mechanism insights to therapeutic perspective World J. Gastroenterol. 20 2014 17737 17745
20. J.M. Henke, and B.L. Bassler Three parallel quorum-sensing systems regulate gene expression in Vibrio harveyi J. Bacteriol. 186 2004 6902 6914
21. D.A. Higgins, M.E. Pomianek, C.M. Kraml, R.K. Taylor, M.F. Semmelhack, and B.L. Bassler The major Vibrio cholerae autoinducer and its role in virulence factor production Nature 450 2007 883 886
22. D.T. Hughes, and V. Sperandio Inter-kingdom signalling: communication between bacteria and their hosts Nat. Rev. Microbiol. 6 2008 111 120
23. A.S. Ismail, C.L. Behrendt, and L.V. Hooper Reciprocal interactions between commensal bacteria and gamma delta intraepithelial lymphocytes during mucosal injury J. Immunol. 182 2009 3047 3054
24. X. Ke, L.C. Miller, and B.L. Bassler Determinants governing ligand specificity of the Vibrio harveyi LuxN quorum-sensing receptor Mol. Microbiol. 95 2015 127 142
25. B. Kneidinger, C. Marolda, M. Graninger, A. Zamyatina, F. McArthur, P. Kosma, M.A. Valvano, and P. Messner Biosynthesis pathway of ADP-L-glycero-beta-D-manno-heptose in Escherichia coli J. Bacteriol. 184 2002 363 369
26. T. Long, K.C. Tu, Y. Wang, P. Mehta, N.P. Ong, B.L. Bassler, and N.S. Wingreen Quantifying the integration of quorum-sensing signals with single-cell resolution PLoS Biol. 7 2009 e68
27. W.D. Loomis, and R.W. Durst Chemistry and biology of boron Biofactors 3 1992 229 239
28. M. Lyte, and M.T. Bailey Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma J. Surg. Res. 70 1997 195 201
29. M. Lyte, and S. Ernst Catecholamine induced growth of gram negative bacteria Life Sci. 50 1992 203 212
30. S.K. Mazmanian, C.H. Liu, A.O. Tzianabos, and D.L. Kasper An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system Cell 122 2005 107 118
31. F. McArthur, C.E. Andersson, S. Loutet, S.L. Mowbray, and M.A. Valvano Functional analysis of the glycero-manno-heptose 7-phosphate kinase domain from the bifunctional HldE protein, which is involved in ADP-L-glycero-D-manno-heptose biosynthesis J. Bacteriol. 187 2005 5292 5300
32. K.H. McClean, M.K. Winson, L. Fish, A. Taylor, S.R. Chhabra, M. Camara, M. Daykin, J.H. Lamb, S. Swift, B.W. Bycroft, and et al. Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acylhomoserine lactones Microbiology 143 1997 3703 3711
33. M.B. Miller, K. Skorupski, D.H. Lenz, R.K. Taylor, and B.L. Bassler Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae Cell 110 2002 303 314
34. S.T. Miller, K.B. Xavier, S.R. Campagna, M.E. Taga, M.F. Semmelhack, B.L. Bassler, and F.M. Hughson Salmonella typhimurium recognizes a chemically distinct form of the bacterial quorum-sensing signal AI-2 Mol. Cell 15 2004 677 687
35. M.B. Neiditch, M.J. Federle, S.T. Miller, B.L. Bassler, and F.M. Hughson Regulation of LuxPQ receptor activity by the quorum-sensing signal autoinducer-2 Mol. Cell 18 2005 507 518
36. M.B. Neiditch, M.J. Federle, A.J. Pompeani, R.C. Kelly, D.L. Swem, P.D. Jeffrey, B.L. Bassler, and F.M. Hughson Ligand-induced asymmetry in histidine sensor kinase complex regulates quorum sensing Cell 126 2006 1095 1108
37. W.L. Ng, and B.L. Bassler Bacterial quorum-sensing network architectures Annu. Rev. Genet. 43 2009 197 222
38. A. Panja, E. Siden, and L. Mayer Synthesis and regulation of accessory/proinflammatory cytokines by intestinal epithelial cells Clin. Exp. Immunol. 100 1995 298 305
39. M.W. Parker, J.T. Buckley, J.P. Postma, A.D. Tucker, K. Leonard, F. Pattus, and D. Tsernoglou Structure of the Aeromonas toxin proaerolysin in its water-soluble and membrane-channel states Nature 367 1994 292 295
40. L.W. Peterson, and D. Artis Intestinal epithelial cells: regulators of barrier function and immune homeostasis Nat. Rev. Immunol. 14 2014 141 153
41. G.D. Pullinger, S.C. Carnell, F.F. Sharaff, P.M. van Diemen, F. Dziva, E. Morgan, M. Lyte, P.P. Freestone, and M.P. Stevens Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases QseC and QseE Infect. Immun. 78 2010 372 380
42. S. Rakoff-Nahoum, J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis Cell 118 2004 229 241
43. J. Roignot, X. Peng, and K. Mostov Polarity in mammalian epithelial morphogenesis Cold Spring Harb. Perspect. Biol. 5 2013 5
44. F.M. Ruemmele, J.F. Beaulieu, S. Dionne, E. Levy, E.G. Seidman, N. Cerf-Bensussan, and M.J. Lentze Lipopolysaccharide modulation of normal enterocyte turnover by toll-like receptors is mediated by endogenously produced tumour necrosis factor alpha Gut 51 2002 842 848
45. S.T. Rutherford, and B.L. Bassler Bacterial quorum sensing: its role in virulence and possibilities for its control Cold Spring Harb. Perspect. Med. 2 2012 2
46. G. Samak, K.K. Chaudhry, R. Gangwar, D. Narayanan, J.H. Jaggar, and R. Rao Calcium/Ask1/MKK7/JNK2/c-Src signalling cascade mediates disruption of intestinal epithelial tight junctions by dextran sulfate sodium Biochem. J. 465 2015 503 515
47. S. Schauder, K. Shokat, M.G. Surette, and B.L. Bassler The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule Mol. Microbiol. 41 2001 463 476
48. G. Schenk, R.G. Duggleby, and P.F. Nixon Properties and functions of the thiamin diphosphate dependent enzyme transketolase Int. J. Biochem. Cell Biol. 30 1998 1297 1318
49. P. Schnupf, V. Gaboriau-Routhiau, M. Gros, R. Friedman, M. Moya-Nilges, G. Nigro, N. Cerf-Bensussan, and P.J. Sansonetti Growth and host interaction of mouse segmented filamentous bacteria in vitro Nature 520 2015 99 103
50. M.F. Semmelhack, S.R. Campagna, M.J. Federle, and B.L. Bassler An expeditious synthesis of DPD and boron binding studies Org. Lett. 7 2005 569 572
51. Y. Shen, M.L. Giardino Torchia, G.W. Lawson, C.L. Karp, J.D. Ashwell, and S.K. Mazmanian Outer membrane vesicles of a human commensal mediate immune regulation and disease protection Cell Host Microbe 12 2012 509 520
52. R.S. Smith, S.G. Harris, R. Phipps, and B. Iglewski The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in vivo J. Bacteriol. 184 2002 1132 1139
53. S. Subramoni, J.F. Gonzalez, A. Johnson, M. Péchy-Tarr, L. Rochat, I. Paulsen, J.E. Loper, C. Keel, and V. Venturi Bacterial subfamily of LuxR regulators that respond to plant compounds Appl. Environ. Microbiol. 77 2011 4579 4588
54. M.G. Surette, M.B. Miller, and B.L. Bassler Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production Proc. Natl. Acad. Sci. USA 96 1999 1639 1644
55. L.R. Swem, D.L. Swem, C.T. O'Loughlin, R. Gatmaitan, B. Zhao, S.M. Ulrich, and B.L. Bassler A quorum-sensing antagonist targets both membrane-bound and cytoplasmic receptors and controls bacterial pathogenicity Mol. Cell 35 2009 143 153
56. M.E. Taga, and B.L. Bassler Chemical communication among bacteria Proc. Natl. Acad. Sci. USA 100 Suppl 2 2003 14549 14554
57. M.E. Taga, S.T. Miller, and B.L. Bassler Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium Mol. Microbiol. 50 2003 1411 1427
58. M. Teplitski, J.B. Robinson, and W.D. Bauer Plants secrete substances that mimic bacterial N-acyl homoserine lactone signal activities and affect population density-dependent behaviors in associated bacteria Mol. Plant Microbe Interact. 13 2000 637 648
59. M. Teplitski, H. Chen, S. Rajamani, M. Gao, M. Merighi, R.T. Sayre, J.B. Robinson, B.G. Rolfe, and W.D. Bauer Chlamydomonas reinhardtii secretes compounds that mimic bacterial signals and interfere with quorum sensing regulation in bacteria Plant Physiol. 134 2004 137 146
60. J.A. Thompson, R.A. Oliveira, A. Djukovic, C. Ubeda, and K.B. Xavier Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota Cell Rep. 10 2015 1861 1871
61. G. Tomasello, P. Tralongo, P. Damiani, E. Sinagra, B. Di Trapani, M.N. Zeenny, I.H. Hussein, A. Jurjus, and A. Leone Dismicrobism in inflammatory bowel disease and colorectal cancer: changes in response of colocytes World J. Gastroenterol. 20 2014 18121 18130
62. V. Venturi, and C. Fuqua Chemical signaling between plants and plant-pathogenic bacteria Annu. Rev. Phytopathol. 51 2013 17 37
63. K.L. Visick, J. Foster, J. Doino, M. McFall-Ngai, and E.G. Ruby Vibrio fischeri lux genes play an important role in colonization and development of the host light organ J. Bacteriol. 182 2000 4578 4586
64. L. Wen, R.E. Ley, P.Y. Volchkov, P.B. Stranges, L. Avanesyan, A.C. Stonebraker, C. Hu, F.S. Wong, G.L. Szot, J.A. Bluestone, and et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes Nature 455 2008 1109 1113
65. K.B. Xavier, S.T. Miller, W. Lu, J.H. Kim, J. Rabinowitz, I. Pelczer, M.F. Semmelhack, and B.L. Bassler Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in enteric bacteria ACS Chem. Biol. 2 2007 128 136
66. A. Zargar, D.N. Quan, K.K. Carter, M. Guo, H.O. Sintim, G.F. Payne, and W.E. Bentley Bacterial secretions of nonpathogenic Escherichia coli elicit inflammatory pathways: a closer investigation of interkingdom signaling MBio 6 2015 e00025