Secondary metabolites and other small molecules as intercellular pathogenic signals

FEMS Microbiology Letters

Volumn 314, Issue 1, 2011, Pages 10-17

  Dufour, Nicholas ^a   Rao, Reeta Prusty ^b  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b WORCESTER POLYTECHNIC INSTITUTE   (United States)

Author keywords

Antimicrobial therapies; Cell cell communication; Intercellular signal; Pathogenesis; Secondary metabolite; Small molecule signaling

Indexed keywords

ALCOHOL DERIVATIVE; AROMATIC ALCOHOL; HOMOSERINE LACTONE; INDOLEACETIC ACID; LACTONE DERIVATIVE; OLIGOPEPTIDE; UNCLASSIFIED DRUG;

ANTIMICROBIAL THERAPY; ASPERGILLUS NIDULANS; BACTERIAL COLONIZATION; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; CANDIDA ALBICANS; CELL COMMUNICATION; FUNGAL METABOLISM; FUNGAL VIRULENCE; GENE EXPRESSION REGULATION; GRAM POSITIVE BACTERIUM; INFECTION; METABOLITE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SACCHAROMYCES CEREVISIAE; SECONDARY METABOLITE; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; FUNGI; HUMANS; MYCOSES; SIGNAL TRANSDUCTION;

EID: 78650107672     PISSN: 03781097     EISSN: 15746968     Source Type: Journal    
DOI: 10.1111/j.1574-6968.2010.02154.x     Document Type: Review

References (72)

1. Autret N, Raynaud C, Dubail I, Berche P & Charbit A (2003) Identification of the agr locus of Listeria monocytogenes: role in bacterial virulence. Infect Immun 71: 4463-4471.
2. Barber CE, Tang JL, Feng JX et al. (1997) A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule. Mol Microbiol 24: 555-566.
3. Bassler BL (2002) Small talk. Cell-to-cell communication in bacteria. Cell 109: 421-424.
4. Bassler BL, Wright M & Silverman MR (1994) Multiple signalling systems controlling expression of luminescence in Vibrio harveyi: sequence and function of genes encoding a second sensory pathway. Mol Microbiol 13: 273-286.
5. Beaugerie L & Petit J-C (2004) Antibiotic-associated diarrhoea. Best Pract Res Clin Ga 18: 337-352.
6. Boon C, Deng Y, Wang LH et al. (2008) A novel DSF-like signal from Burkholderia cenocepacia interferes with Candida albicans morphological transition. ISME J 2: 27-36.
7. Camilli A & Bassler B (2006) Bacterial small-molecule signaling pathways. Science 311: 1113-1116.
8. Carman RJ, Simon MA, Fernández H, Miller MA & Bartholomew MJ (2004) Ciprofloxacin at low levels disrupts colonization resistance of human fecal microflora growing in chemostats. Regul Toxicol Pharm 40: 319-326.
9. Chen H & Fink GR (2006) Feedback control of morphogenesis in fungi by aromatic alcohols. Gene Dev 20: 1150-1161.
10. Chen H, Fujita M, Feng Q, Clardy J & Fink GR (2004) Tyrosol is a quorum-sensing molecule in Candida albicans. P Natl Acad Sci USA 101: 5048-5052.
11. Chen X, Schauder S, Potier N, Van Dorsselaer A, Pelczer I, Bassler BL & Hughson FM (2002) Structural identification of a bacterial quorum-sensing signal containing boron. Nature 415: 545-549.
12. Deveau A, Piispanen AE, Jackson AA & Hogan DA (2010) Farnesol induces hydrogen peroxide resistance in Candida albicans yeast by inhibiting the Ras-cyclic AMP signaling pathway. Eukaryot Cell 9: 569-577.
13. Déziel E, Lépine F, Milot S, He J, Mindrinos M, Tompkins R & Rahme L (2004) Analysis of Pseudomonas aeruginosa 4-hydroxy-2-alkylquinolines (HAQs) reveals a role for 4-hydroxy-2-heptylquinoline in cell-to-cell communication. P Natl Acad Sci USA 101: 1339-1344.
14. Dow JM, Crossman L, Findlay K, He YQ, Feng JX & Tang JL (2003) Biofilm dispersal in Xanthomonas campestris is controlled by cell-cell signaling and is required for full virulence to plants. P Natl Acad Sci USA 100: 10995-11000.
15. Duan K, Dammel C, Stein J, Rabin H & Surette MG (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50: 1477-1491.
16. Fan J, Li Y, Vodovotz Y, Billiar TR & Wilson MA (2007) Neutrophil NAD(P)H oxidase is required for hemorrhagic shock-enhanced TLR2 up-regulation in alveolar macrophages in response to LPS. Shock 28: 213-218.
17. Higgins D, Pomianek M, Kraml C, Taylor R, Semmelhack M & Bassler B (2007) The major Vibrio cholerae autoinducer and its role in virulence factor production. Nature 450: 883-886.
18. Hogan DA (2006) Talking to themselves: autoregulation and quorum sensing in fungi. Eukaryot Cell 5: 613-619.
19. Hogan DA & Kolter R (2002) Pseudomonas-Candida interactions: an ecological role for virulence factors. Science 296: 2229-2232.
20. Hogan DA, Vik A & Kolter R (2004) A Pseudomonas aeruginosa quorum-sensing molecule influences Candida albicans morphology. Mol Microbiol 54: 1212-1223.
21. Hornby JM, Jensen EC, Lisec AD et al. (2001) Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Appl Environ Microb 67: 2982-2992.
22. Huang TP & Wong AC (2007) A cyclic AMP receptor protein-regulated cell-cell communication system mediates expression of a FecA homologue in Stenotrophomonas maltophilia. Appl Environ Microb 73: 5034-5040.
23. Jacob F & Monod J (1961) Genetic regulatory mechanisms in the synthesis of proteins. J Mol Biol 3: 318-356.
24. Jain C, Yun M, Politz SM & Rao RP (2009) A pathogenesis assay using Saccharomyces cerevisiae and Caenorhabditis elegans reveals novel roles for yeast AP-1, Yap1, and host dual oxidase BLI-3 in fungal pathogenesis. Eukaryot Cell 8: 1218-1227.
25. Ji G, Beavis R & Novick R (1995) Cell density control of staphylococcal virulence mediated by an octapeptide pheromone. P Natl Acad Sci USA 92: 12055-12059.
26. Ji G, Beavis R & Novick R (1997) Bacterial interference caused by autoinducing peptide variants. Science 276: 2027-2030.
27. Kleerebezem M, Quadri L, Kuipers O & De Vos W (1997) Quorum sensing by peptide pheromones and two-component signal-transduction systems in Gram-positive bacteria. Mol Microbiol 24: 895-904.
28. Koh AY, Kohler JR, Coggshall KT, Van Rooijen N & Pier GB (2008) Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog 4: e35.
29. Kontoyiannis DP & Lewis RE (2002) Antifungal drug resistance of pathogenic fungi. Lancet 359: 1135-1144.
30. Kurtoglu S, Uzum K, Hallac IK & Coskum A (1997) 5-Hydroxy-3-indole acetic acid levels in infantile colic: is serotoninergic tonus responsible for this problem? Acta Paediatr 86: 764-765.
31. Lazdunski A, Stewart G & Williams P (1995) Multiple N-acyl-l-homoserine lactone signal molecules regulate production of virulence determinants and secondary metabolites in Pseudomonas aeruginosa. P Natl Acad Sci USA 92: 9427-9431.
32. Lewenza S, Visser MB & Sokol PA (2002) Interspecies communication between Burkholderia cepacia and Pseudomonas aeruginosa. Can J Microbiol 48: 707-716.
33. Lo HJ, Kohler JR, DiDomenico B, Loebenberg D, Cacciapuoti A & Fink GR (1997) Nonfilamentous C. albicans mutants are avirulent. Cell 90: 939-949.
34. Lorenz MC & Fink GR (2001) The glyoxylate cycle is required for fungal virulence. Nature 412: 83-86.
35. Lorenz MC & Fink GR (2002) Life and death in a macrophage: role of the glyoxylate cycle in virulence. Eukaryot Cell 1: 657-662.
36. Machan Z, Taylor G, Pitt T, Cole P & Wilson R (1992) 2-Heptyl-4-hydroxyquinoline N-oxide, an antistaphylococcal agent produced by Pseudomonas aeruginosa. J Antimicrob Chemoth 30: 615-623.
37. Mashburn L & Whiteley M (2005) Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437: 422-425.
38. McCusker JH (2006) Saccharomyces cerevisiae: an emerging and model pathogenic fungus. ASM Press, Washington, DC.
39. McKnight SL, Iglewski BH & Pesci EC (2000) The Pseudomonas quinolone signal regulates rhl quorum sensing in Pseudomonas aeruginosa. J Bacteriol 182: 2702-2708.
40. Menon V, Li D, Chauhan N, Rajnarayanan R, Dubrovska A, West AH & Calderone R (2006) Functional studies of the Ssk1p response regulator protein of Candida albicans as determined by phenotypic analysis of receiver domain point mutants. Mol Microbiol 62: 997-1013.
41. Miller MB & Bassler BL (2001) Quorum sensing in bacteria. Annu Rev Microbiol 55: 165-199.
42. Muh U, Schuster M, Heim R, Singh A, Olson E & Greenberg E (2006) Novel Pseudomonas aeruginosa quorum-sensing inhibitors identified in an ultra-high-throughput screen. Antimicrob Agents Ch 50: 3674-3679.
43. Nickerson KW, Atkin AL & Hornby JM (2006) Quorum sensing in dimorphic fungi: farnesol and beyond. Appl Environ Microb 72: 3805-3813.
44. Normanly J & Bartel B (1999) Redundancy as a way of life - IAA metabolism. Curr Opin Plant Biol 2: 207-213.
45. Novick R (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48: 1429-1449.
46. Ohtani K, Yuan Y, Hassan S, Wang R, Wang Y & Shimizu T (2009) Virulence gene regulation by the agr system in Clostridium perfringens. J Bacteriol 191: 3919-3927.
47. Otto M, Süßmuth R, Vuong C, Jung G & Götz F (1999) Inhibition of virulence factor expression in Staphylococcus aureus by the Staphylococcus epidermidis agr pheromone and derivatives. FEBS Lett 450: 257-262.
48. Parsek MR & Greenberg EP (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13: 27-33.
49. Pesci EC, Milbank JB, Pearson JP, McKnight S, Kende AS, Greenberg EP & Iglewski BH (1999) Quinolone signaling in the cell-to-cell communication system of Pseudomonas aeruginosa. P Natl Acad Sci USA 96: 11229-11234.
50. Peters BM, Jabra-Rizk MA, Scheper MA, Leid JG, Costerton JW & Shirtliff ME (2010) Microbial interactions and differential protein expression in Staphylococcus aureus-Candida albicans dual-species biofilms. FEMS Immunol Med Mic 59: 493-503.
51. Prusty R, Grisafi P & Fink G (2004) The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae. P Natl Acad Sci USA 101: 4153-4157.
52. Rao RP, Hunter A, Kashpur O & Normanly J (2010) Aberrant synthesis of indole-3-acetic acid in Saccharomyces cerevisiae triggers morphogenic transition, a virulence trait of pathogenic fungi. Genetics 185: 211-220.
53. Rasko DA & Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9: 117-128.
54. Riedel K, Hentzer M, Geisenberger O et al. (2001) N-acylhomoserine-lactone-mediated communication between Pseudomonas aeruginosa and Burkholderia cepacia in mixed biofilms. Microbiology 147: 3249-3262.
55. Ryan RP, Fouhy Y, Garcia BF et al. (2008) Interspecies signalling via the Stenotrophomonas maltophilia diffusible signal factor influences biofilm formation and polymyxin tolerance in Pseudomonas aeruginosa. Mol Microbiol 68: 75-86.
56. Sakinc T, Kulczak P, Henne K & Gatermann S (2006) Cloning of an agr homologue of Staphylococcus saprophyticus. FEMS Microbiol Lett 237: 157-161.
57. Schaefer A, Val D, Hanzelka B, Cronan J & Greenberg E (1996) Generation of cell-to-cell signals in quorum sensing: acyl homoserine lactone synthase activity of a purified Vibrio fischeri LuxI protein. P Natl Acad Sci USA 93: 9505-9509.
58. Schauder S & Bassler BL (2001) The languages of bacteria. Gene Dev 15: 1468-1480.
59. Schuster M & Peter Greenberg E (2006) A network of networks: quorum-sensing gene regulation in Pseudomonas aeruginosa. Int J Med Microbiol 296: 73-81.
60. Semighini CP, Hornby JM, Dumitru R, Nickerson KW & Harris SD (2006) Farnesol-induced apoptosis in Aspergillus nidulans reveals a possible mechanism for antagonistic interactions between fungi. Mol Microbiol 59: 753-764.
61. Semighini CP, Murray N & Harris SD (2008) Inhibition of Fusarium graminearum growth and development by farnesol. FEMS Microbiol Lett 279: 259-264.
62. Shirtliff ME, Peters BM & Jabra-Rizk MA (2009) Cross-kingdom interactions: Candida albicans and bacteria. FEMS Microbiol Lett 299: 1-8.
63. Slater H, Alvarez-Morales A, Barber CE, Daniels MJ & Dow JM (2000) A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris. Mol Microbiol 38: 986-1003.
64. Surette MG, Miller MB & Bassler BL (1999) Quorum sensing in Escherichia coli, Salmonella typhimurium, and Vibrio harveyi: a new family of genes responsible for autoinducer production. P Natl Acad Sci USA 96: 1639-1644.
65. Taga ME & Bassler BL (2003) Chemical communication among bacteria. P Natl Acad Sci USA 100 (suppl 2): 14549-14554.
66. Venturi V, Friscina A, Bertani I, Devescovi G & Aguilar C (2004) Quorum sensing in the Burkholderia cepacia complex. Res Microbiol 155: 238-244.
67. Walters M & Sperandio V (2006) Quorum sensing in Escherichia coli and Salmonella. Int J Med Microbiol 296: 125-131.
68. Wang LH, He Y, Gao Y et al. (2004) A bacterial cell-cell communication signal with cross-kingdom structural analogues. Mol Microbiol 51: 903-912.
69. Woodward AW & Bartel B (2005) Auxin: regulation, action, and interaction. Ann Bot (London) 95: 707-735.
70. Xavier KB & Bassler BL (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6: 191-197.
71. Xavier KB & Bassler BL (2005) Regulation of uptake and processing of the quorum-sensing autoinducer AI-2 in Escherichia coli. J Bacteriol 187: 238-248.
72. Xu XL, Lee RT, Fang HM et al. (2008) Bacterial peptidoglycan triggers Candida albicans hyphal growth by directly activating the adenylyl cyclase Cyr1p. Cell Host Microbe 4: 28-39.