Inter-kingdom signalling: communication between bacteria and their hosts

Microorganisms and their hosts communicate with each other through an array of hormonal signals. This cross-kingdom cell-to-cell signalling involves small molecules, such as hormones that are produced by eukaryotes and hormone-like chemicals that are produced by bacteria. Cell-to-cell signalling between bacteria, usually referred to as quorum sensing, was initially described as a means by which bacteria achieve signalling in microbial communities to coordinate gene expression within a population. Recent evidence shows, however, that quorum-sensing signalling is not restricted to bacterial cell-to-cell communication, but also allows communication between microorganisms and their hosts.

[1]  P. Sternberg,et al.  Multiple positive and negative regulators of signaling by the EGF-receptor. , 1999, Current opinion in cell biology.

[2]  M. Merighi,et al.  Role of Salmonella enterica Serovar Typhimurium Two-Component System PreA/PreB in Modulating PmrA-Regulated Gene Transcription , 2006, Journal of bacteriology.

[3]  George M. Hilliard,et al.  Pseudomonas aeruginosa anaerobic respiration in biofilms: relationships to cystic fibrosis pathogenesis. , 2002, Developmental cell.

[4]  Y. Nakaya,et al.  Modulation of pathogenicity with norepinephrine related to the type III secretion system of Vibrio parahaemolyticus. , 2007, The Journal of infectious diseases.

[5]  S. Bearson,et al.  The role of the QseC quorum-sensing sensor kinase in colonization and norepinephrine-enhanced motility of Salmonella enterica serovar Typhimurium. , 2008, Microbial pathogenesis.

[6]  Olga Khersonsky,et al.  Structure-reactivity studies of serum paraoxonase PON1 suggest that its native activity is lactonase. , 2005, Biochemistry.

[7]  S. McKnight,et al.  NPAS2: A Gas-Responsive Transcription Factor , 2002, Science.

[8]  J. Furness Types of neurons in the enteric nervous system. , 2000, Journal of the autonomic nervous system.

[9]  R. Bazzo,et al.  Molecular Insights into Quorum Sensing in the Human Pathogen Pseudomonas aeruginosa from the Structure of the Virulence Regulator LasR Bound to Its Autoinducer* , 2007, Journal of Biological Chemistry.

[10]  P. Rather,et al.  Providencia stuartii Genes Activated by Cell-to-Cell Signaling and Identification of a Gene Required for Production or Activity of an Extracellular Factor , 1999, Journal of bacteriology.

[11]  Vanessa Sperandio,et al.  Bacteria–host communication: The language of hormones , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[12]  E. Shiner,et al.  Inter-kingdom signaling: deciphering the language of acyl homoserine lactones. , 2005, FEMS microbiology reviews.

[13]  J. Hogenesch,et al.  The PAS superfamily: sensors of environmental and developmental signals. , 2000, Annual review of pharmacology and toxicology.

[14]  S. Tzipori,et al.  The pathogenesis of hemorrhagic colitis caused by Escherichia coli O157:H7 in gnotobiotic piglets. , 1986, The Journal of infectious diseases.

[15]  S. Dowd,et al.  Social stress increases fecal shedding of Salmonella typhimurium by early weaned piglets. , 2006, Current issues in intestinal microbiology.

[16]  V. Sperandio,et al.  O 157 : H 7 Escherichia coli Mechanism in Enterohemorrhagic Quorum Sensing Is a Global Regulatory , 2001 .

[17]  P. Rather,et al.  An extracellular factor regulating expression of the chromosomal aminoglycoside 2'-N-acetyltransferase of Providencia stuartii , 1997, Antimicrobial agents and chemotherapy.

[18]  Roger S Smith,et al.  The Pseudomonas Autoinducer N-(3-Oxododecanoyl) Homoserine Lactone Induces Cyclooxygenase-2 and Prostaglandin E2 Production in Human Lung Fibroblasts: Implications for Inflammation1 , 2002, The Journal of Immunology.

[19]  William A. Goddard,et al.  Predicted 3 D structure for the human 2 adrenergic receptor and its binding site for agonists and antagonists , 2004 .

[20]  E. Koonin,et al.  Evolution of cell-cell signaling in animals: did late horizontal gene transfer from bacteria have a role? , 2004, Trends in genetics : TIG.

[21]  Juan E. González,et al.  l-Canavanine Made by Medicago sativa Interferes with Quorum Sensing in Sinorhizobium meliloti , 2005, Journal of bacteriology.

[22]  Rachel E. Klevit,et al.  Recognition of Antimicrobial Peptides by a Bacterial Sensor Kinase , 2005, Cell.

[23]  Vanessa Sperandio,et al.  Global Effects of the Cell-to-Cell Signaling Molecules Autoinducer-2, Autoinducer-3, and Epinephrine in a luxS Mutant of Enterohemorrhagic Escherichia coli , 2007, Infection and Immunity.

[24]  T. Muir,et al.  Chemical signaling among bacteria and its inhibition. , 2003, Chemistry & biology.

[25]  J. Yu,et al.  A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[26]  D. Larrouy,et al.  Coupling of the alpha 2-adrenergic receptor to the inhibitory G-protein Gi and adenylate cyclase in HT29 cells. , 1993, The Biochemical journal.

[27]  M. Lyte The role of catecholamines in gram-negative sepsis. , 1992, Medical hypotheses.

[28]  C. L. Burton,et al.  The Growth Response of Escherichia coli to Neurotransmitters and Related Catecholamine Drugs Requires a Functional Enterobactin Biosynthesis and Uptake System , 2002, Infection and Immunity.

[29]  P. Kylsten,et al.  A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[30]  T. A. Springer,et al.  IL-8 Production in Human Lung Fibroblasts and Epithelial Cells Activated by the Pseudomonas Autoinducer N-3-Oxododecanoyl Homoserine Lactone Is Transcriptionally Regulated by NF-κB and Activator Protein-21 , 2001, The Journal of Immunology.

[31]  Richard Phipps,et al.  The Pseudomonas aeruginosa quorum-sensing molecule N-(3-oxododecanoyl)homoserine lactone contributes to virulence and induces inflammation in , 2002 .

[32]  W. Broughton,et al.  Molecular Basis of Symbiotic Promiscuity , 2000, Microbiology and Molecular Biology Reviews.

[33]  Structure of the GAF domain, a ubiquitous signaling motif and a new class of cyclic GMP receptor , 2000, The EMBO journal.

[34]  J. Alverdy,et al.  Gut-Derived Sepsis Occurs When the Right Pathogen With the Right Virulence Genes Meets the Right Host: Evidence for In Vivo Virulence Expression in Pseudomonas aeruginosa , 2000, Annals of surgery.

[35]  A. Buchman,et al.  Clonidine reduces diarrhea and sodium loss in patients with proximal jejunostomy: a controlled study. , 2006, JPEN. Journal of parenteral and enteral nutrition.

[36]  A. Ninfa,et al.  Phosphorylation and dephosphorylation of a bacterial transcriptional activator by a transmembrane receptor. , 1989, Genes & development.

[37]  O. Zaborina,et al.  Recognition of Host Immune Activation by Pseudomonas aeruginosa , 2005, Science.

[38]  T. McDaniel,et al.  A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[39]  E. Koonin,et al.  Pineal Serotonin N-Acetyltransferase: Expression Cloning and Molecular Analysis , 1995, Science.

[40]  E. Greenberg,et al.  Inactivation of a Pseudomonas aeruginosa quorum-sensing signal by human airway epithelia. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[41]  C. Sasakawa,et al.  EspG, a Novel Type III System-Secreted Protein from Enteropathogenic Escherichia coli with Similarities to VirA of Shigella flexneri , 2001, Infection and Immunity.

[42]  S. Rice,et al.  Modification of In Vivo and In Vitro T- and B-Cell-Mediated Immune Responses by the Pseudomonas aeruginosa Quorum-Sensing Molecule N-(3-Oxododecanoyl)-l-Homoserine Lactone , 2003, Infection and Immunity.

[43]  G. Caetano-Anollés,et al.  Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[44]  A. Prince,et al.  Diverse Pseudomonas aeruginosa gene products stimulate respiratory epithelial cells to produce interleukin-8. , 1995, The Journal of clinical investigation.

[45]  B. Finlay,et al.  Enteropathogenic E. coli (EPEC) Transfers Its Receptor for Intimate Adherence into Mammalian Cells , 1997, Cell.

[46]  V. Sperandio,et al.  Transcriptional regulation of flhDC by QseBC and σ 28 (FliA) in enterohaemorrhagic Escherichia coli , 2005, Molecular microbiology.

[47]  Lian-Hui Zhang,et al.  Quorum quenching enzyme activity is widely conserved in the sera of mammalian species , 2005, FEBS letters.

[48]  E. Eldrup,et al.  DOPA, dopamine, and DOPAC concentrations in the rat gastrointestinal tract decrease during fasting. , 2000, American journal of physiology. Endocrinology and metabolism.

[49]  B. Arulanandam,et al.  Production of Shiga-like toxins by Escherichia coli O157:H7 can be influenced by the neuroendocrine hormone norepinephrine. , 1996, The Journal of laboratory and clinical medicine.

[50]  J. Downward The ins and outs of signalling , 2001, Nature.

[51]  D. Pritchard,et al.  Synthetic analogues of the bacterial signal (quorum sensing) molecule N-(3-oxododecanoyl)-L-homoserine lactone as immune modulators. , 2003, Journal of medicinal chemistry.

[52]  M. Lyte,et al.  Catecholamine induced growth of gram negative bacteria. , 1992, Life sciences.

[53]  P. Freestone,et al.  Involvement of enterobactin in norepinephrine-mediated iron supply from transferrin to enterohaemorrhagic Escherichia coli. , 2003, FEMS microbiology letters.

[54]  S. Roychoudhury,et al.  Inhibitors of two-component signal transduction systems: inhibition of alginate gene activation in Pseudomonas aeruginosa. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[55]  H. Dyson,et al.  Structure of the Escherichia coli quorum sensing protein SdiA: activation of the folding switch by acyl homoserine lactones. , 2006, Journal of molecular biology.

[56]  T. B. Rasmussen,et al.  Rational design and synthesis of new quorum-sensing inhibitors derived from acylated homoserine lactones and natural products from garlic. , 2005, Organic & biomolecular chemistry.

[57]  M. Stevens,et al.  The Neuroendocrine Stress Hormone Norepinephrine Augments Escherichia coli O157:H7-Induced Enteritis and Adherence in a Bovine Ligated Ileal Loop Model of Infection , 2004, Infection and Immunity.

[58]  D. Shih,et al.  Paraoxonase-2 deficiency enhances Pseudomonas aeruginosa quorum sensing in murine tracheal epithelia. , 2007, American journal of physiology. Lung cellular and molecular physiology.

[59]  M. Freeman,et al.  Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase , 2007, Proceedings of the National Academy of Sciences.

[60]  J. Gordon,et al.  Commensal Host-Bacterial Relationships in the Gut , 2001, Science.

[61]  B. Kenny,et al.  Targeting of an enteropathogenic Escherichia coli (EPEC) effector protein to host mitochondria , 2000, Cellular microbiology.

[62]  Linden T. Hu,et al.  Borrelia burgdorferi intercepts host hormonal signals to regulate expression of outer surface protein A , 2007, Proceedings of the National Academy of Sciences.

[63]  Nicola C. Reading,et al.  A Novel Two-Component Signaling System That Activates Transcription of an Enterohemorrhagic Escherichia coli Effector Involved in Remodeling of Host Actin , 2007, Journal of bacteriology.

[64]  B. P. McNamara,et al.  A novel proline-rich protein, EspF, is secreted from enteropathogenic Escherichia coli via the type III export pathway. , 1998, FEMS microbiology letters.

[65]  M. Ishiguro,et al.  Synthesis of Pseudomonas quorum-sensing autoinducer analogs and structural entities required for induction of apoptosis in macrophages. , 2006, Bioorganic & medicinal chemistry letters.

[66]  Matthew R. Parsek,et al.  Quorum-sensing signals indicate that cystic fibrosis lungs are infected with bacterial biofilms , 2000, Nature.

[67]  V. Sperandio,et al.  Transcriptional autoregulation by quorum sensing Escherichia coli regulators B and C (QseBC) in enterohaemorrhagic E. coli (EHEC) , 2005, Molecular microbiology.

[68]  P. Valet,et al.  Characterization and distribution of alpha 2-adrenergic receptors in the human intestinal mucosa. , 1993, The Journal of clinical investigation.

[69]  R. Cortese,et al.  The crystal structure of the quorum sensing protein TraR bound to its autoinducer and target DNA , 2002, The EMBO journal.

[70]  D. Pritchard,et al.  Alleviation of insulitis and moderation of diabetes in NOD mice following treatment with a synthetic Pseudomonas aeruginosasignal molecule, N-(3-oxododecanoyl)-L-homoserine lactone , 2005, Acta Diabetologica.

[71]  S. Kjelleberg,et al.  Halogenated furanones inhibit quorum sensing through accelerated LuxR turnover. , 2002, Microbiology.

[72]  Ulrike Mathesius,et al.  Plant responses to bacterial quorum sensing signals. , 2004, Current opinion in plant biology.

[73]  K. Nealson,et al.  Cellular Control of the Synthesis and Activity of the Bacterial Luminescent System , 1970, Journal of bacteriology.

[74]  Vanessa Sperandio,et al.  Autoinducer 3 and Epinephrine Signaling in the Kinetics of Locus of Enterocyte Effacement Gene Expression in Enterohemorrhagic Escherichia coli , 2006, Infection and Immunity.

[75]  D. Wheeler,et al.  The Pseudomonas aeruginosaQuorum-Sensing Signal MoleculeN-(3-Oxododecanoyl)-l-Homoserine Lactone Has Immunomodulatory Activity , 1998, Infection and Immunity.

[76]  G. Sonnenfeld,et al.  Norepinephrine as a growth stimulating factor in bacteria--mechanistic studies. , 2000, Life sciences.

[77]  X. Tu,et al.  EspH, a new cytoskeleton‐modulating effector of enterohaemorrhagic and enteropathogenic Escherichia coli , 2003, Molecular microbiology.

[78]  M. Surette,et al.  Ecological Behavior of Lactobacillus reuteri 100-23 Is Affected by Mutation of the luxS Gene , 2005, Applied and Environmental Microbiology.

[79]  P. Freestone,et al.  The Mammalian Neuroendocrine Hormone Norepinephrine Supplies Iron for Bacterial Growth in the Presence of Transferrin or Lactoferrin , 2000, Journal of bacteriology.

[80]  B. Arulanandam,et al.  Norepinephrine-induced expression of the K99 pilus adhesin of enterotoxigenic Escherichia coli. , 1997, Biochemical and biophysical research communications.

[81]  G. Li,et al.  Pseudomonas aeruginosa autoinducer modulates host cell responses through calcium signalling , 2006, Cellular microbiology.

[82]  V. Sperandio,et al.  The QseC sensor kinase: A bacterial adrenergic receptor , 2006, Proceedings of the National Academy of Sciences.

[83]  J. Kaper,et al.  Role of plasmid-encoded adherence factors in adhesion of enteropathogenic Escherichia coli to HEp-2 cells , 1987, Infection and immunity.

[84]  M. Petric,et al.  ESCHERICHIA COLI CYTOTOXIN, HAEMOLYTIC-URAEMIC SYNDROME, AND HAEMORRHAGIC COLITIS , 1983, The Lancet.

[85]  D. Monack,et al.  In vivo negative selection screen identifies genes required for Francisella virulence , 2007, Proceedings of the National Academy of Sciences.

[86]  M. Diener,et al.  Segment-specific effects of epinephrine on ion transport in the colon of the rat. , 1998, The American journal of physiology.

[87]  Peter L. Freddolino,et al.  Predicted 3D structure for the human beta 2 adrenergic receptor and its binding site for agonists and antagonists. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[88]  S. Zimmermann,et al.  Induction of Neutrophil Chemotaxis by the Quorum-Sensing Molecule N-(3-Oxododecanoyl)-l-Homoserine Lactone , 2006, Infection and Immunity.

[89]  I. Tatsuno,et al.  SepZ/EspZ Is Secreted and Translocated into HeLa Cells by the Enteropathogenic Escherichia coli Type III Secretion System , 2005, Infection and Immunity.

[90]  P. Nilsson,et al.  The Pseudomonas aeruginosa Quorum-Sensing Molecule N-3-(Oxododecanoyl)-l-Homoserine Lactone Inhibits T-Cell Differentiation and Cytokine Production by a Mechanism Involving an Early Step in T-Cell Activation , 2005, Infection and Immunity.

[91]  D. Pritchard,et al.  Bacterial N-acylhomoserine lactone-induced apoptosis in breast carcinoma cells correlated with down-modulation of STAT3 , 2004, Oncogene.

[92]  John C. Anderson,et al.  Structure of a bacterial quorum-sensing transcription factor complexed with pheromone and DNA , 2002, Nature.

[93]  K. Rumbaugh,et al.  Pseudomonas aeruginosa Autoinducer Enters and Functions in Mammalian Cells , 2004, Journal of bacteriology.

[94]  A. Zaborin,et al.  Dynorphin Activates Quorum Sensing Quinolone Signaling in Pseudomonas aeruginosa , 2007, PLoS pathogens.

[95]  M. Levine,et al.  Attaching and effacing activities of rabbit and human enteropathogenic Escherichia coli in pig and rabbit intestines , 1983, Infection and immunity.

[96]  G. Cornelis,et al.  The bacterial injection kit: Type III secretion systems , 2005, Annals of medicine.

[97]  K. Rumbaugh Convergence of hormones and autoinducers at the host/pathogen interface , 2007, Analytical and bioanalytical chemistry.

[98]  Marcelo P. Sircili,et al.  AI-3 Synthesis Is Not Dependent on luxS in Escherichia coli , 2006, Journal of bacteriology.

[99]  T. McDaniel,et al.  Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[100]  R. Rosen,et al.  GABA controls the level of quorum-sensing signal in Agrobacterium tumefaciens. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[101]  E. Greenberg,et al.  Census and consensus in bacterial ecosystems: the LuxR-LuxI family of quorum-sensing transcriptional regulators. , 1996, Annual review of microbiology.

[102]  T. Standiford,et al.  The Pseudomonas aeruginosa Autoinducer N-3-Oxododecanoyl Homoserine Lactone Accelerates Apoptosis in Macrophages and Neutrophils , 2003, Infection and Immunity.

[103]  R. Sunahara,et al.  Human paraoxonases (PON1, PON2, and PON3) are lactonases with overlapping and distinct substrate specificitiess⃞s⃞ The online version of this article (available at http://www.jlr.org) contains additional text, figures, and references. Published, JLR Papers in Press, March 16, 2005. DOI 10.1194/jlr.M , 2005, Journal of Lipid Research.

[104]  Kevin H. Gardner,et al.  Structural Basis of a Phototropin Light Switch , 2003, Science.

[105]  Nicola C. Reading,et al.  Quorum sensing: the many languages of bacteria. , 2006, FEMS microbiology letters.

[106]  E. Greenberg,et al.  Human and murine paraoxonase 1 are host modulators of Pseudomonas aeruginosa quorum-sensing. , 2005, FEMS microbiology letters.

[107]  M. Vasil,et al.  Siderophore-mediated signaling regulates virulence factor production in Pseudomonas aeruginosa , 2002, Proceedings of the National Academy of Sciences of the United States of America.