S-Aryl-l-cysteine sulphoxides and related organosulphur compounds alter oral biofilm development and AI-2-based cell-cell communication

Journal of Applied Microbiology

Volumn 117, Issue 5, 2014, Pages 1472-1486

  Kasper, S H ^a   Samarian, D ^b   Jadhav, A P ^c   Rickard, A H ^b   Musah, R A ^c   Cady, N C ^a  

^a SUNY POLYTECHNIC INSTITUTE   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^c STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Biofilm; Cell cell signalling; Dental plaque; Microfluidics; Oral

Indexed keywords

AMINO ACIDS; BACTERIA; CELL ADHESION; CELL SIGNALING; CELLS; MICROFLUIDICS; MOLECULES; SYNTHESIS (CHEMICAL);

ANTIBIOFILMS; BIOFILM FORMATION; CELL-CELL COMMUNICATIONS; CELL-CELL SIGNALING; DENTAL PLAQUES; L-CYSTEINE; ORAL; ORAL BACTERIA; ORAL CAVITY; QUORUM-SENSING;

BIOFILMS;

CYSTEINE; CYSTEINE SULFOXIDE; ORGANOSULFUR DERIVATIVE; UNCLASSIFIED DRUG; ANTIINFECTIVE AGENT; SULFOXIDE; SULFUR DERIVATIVE;

ACTINOMYCES; ACTINOMYCES ORIS; ARTICLE; BACTERIAL GENE; BACTERIAL METABOLISM; BIOFILM; BIOLUMINESCENCE; BIOSYNTHESIS; CELL COMMUNICATION; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; GENETIC TRANSCRIPTION; HUMAN; IC50; MOLECULAR LIBRARY; NONHUMAN; QUORUM SENSING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STREPTOCOCCUS MUTANS; STREPTOCOCCUS SANGUINIS; VIBRIO HARVEYI; BACTERIA; CHEMISTRY; DRUG EFFECTS; GENETICS; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; TOOTH PLAQUE; VIBRIO;

ACTINOMYCES; ANTI-BACTERIAL AGENTS; BACTERIA; BIOFILMS; CYSTEINE; DENTAL PLAQUE; HUMANS; QUORUM SENSING; STREPTOCOCCUS MUTANS; STREPTOCOCCUS SANGUIS; SULFOXIDES; SULFUR COMPOUNDS; TRANSCRIPTION, GENETIC; VIBRIO;

EID: 84908003349     PISSN: 13645072     EISSN: 13652672     Source Type: Journal    
DOI: 10.1111/jam.12616     Document Type: Article

References (75)

1. Ahmed, N.A., Petersen, F.C. and Scheie, A.A. (2009) AI-2/LuxS is involved in increased biofilm formation by Streptococcus intermedius in the presence of antibiotics. Antimicrob Agents Chemother 53, 4258-4263.
2. Ajdić, D., McShan, W.M., McLaughlin, R.E., Savić, G., Chang, J., Carson, M.B., Primeaux, C., Tian, R. et al. (2002) Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen. Proc Natl Acad Sci USA 99, 14434-14439.
3. Blehert, D.S., Palmer, R.J., Xavier, J.B., Almeida, J.S. and Kolenbrander, P.E. (2003) Autoinducer 2 production by Streptococcus gordonii DL1 and the biofilm phenotype of a luxS mutant are influenced by nutritional conditions. J Bacteriol 185, 4851-4860.
4. Brackman, G., Celen, S., Baruah, K., Bossier, P., Van Calenbergh, S., Nelis, H.J. and Coenye, T. (2009) AI-2 quorum-sensing inhibitors affect the starvation response and reduce virulence in several Vibrio species, most likely by interfering with LuxPQ. Microbiology 155, 4114-4122.
5. Cady, N.C., McKean, K.A., Behnke, J., Kubec, R., Mosier, A.P., Kasper, S.H., Burz, D.S. and Musah, R.A. (2012) Inhibition of biofilm formation, quorum sensing and infection in Pseudomonas aeruginosa by natural products-inspired organosulfur compounds. PLoS One 7, e38492.
6. Costerton, J.W. (1999) Bacterial biofilms: a common cause of persistent infections. Science 284, 1318-1322.
7. Costerton, J. and Keller, D. (2007) Oral periopathogens and systemic effects. Gen Dent 55, 210-215.
8. Dige, I., Raarup, M.K., Nyengaard, J.R., Kilian, M. and Nyvad, B. (2009) Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155, 2116-2126.
9. Duan, K., Dammel, C., Stein, J., Rabin, H. and Surette, M.G. (2003) Modulation of Pseudomonas aeruginosa gene expression by host microflora through interspecies communication. Mol Microbiol 50, 1477-1491.
10. Duque, C., Stipp, R.N., Wang, B., Smith, D.J., Ho, F., Kuramitsu, H.K., Duncan, M.J. and Mattos-Graner, R.O. (2011) Downregulation of GbpB, a component of the VicRK regulon, affects biofilm formation and cell surface characteristics of Streptococcus mutans. Infect Immun 79, 786-796.
11. Federle, M.J. and Bassler, B.L. (2003) Interspecies communication in bacteria. J Clin Invest 112, 1291-1299.
12. Ge, X., Kitten, T., Chen, Z., Lee, S.P., Munro, C.L. and Xu, P. (2008) Identification of Streptococcus sanguinis genes required for biofilm formation and examination of their role in endocarditis virulence. Infect Immun 76, 2551-2559.
13. Gilbert, P., Allison, D.G. and Mcbain, A.J. (2002) Biofilms in vitro and in vivo: do singular mechanisms imply cross-resistance? J Appl Microbiol 92, 98-110.
14. Givskov, M., Nys, R.D.E., Manefield, M., Gram, L., Maximilien, R.I.A., Eberl, L.E.O., Molin, S., Steinberg, P.D. et al. (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178, 6618-6622.
15. Greenberg, E.P., Hastings, J.W. and Ulitzur, S. (1979) Induction of luciferase synthesis in Beneckea harveyi by other marine bacteria. Arch Microbiol 120, 87-91.
16. Gutierrez, J.A., Crowder, T., Rinaldo-Matthis, A., Ho, M.-C., Almo, S.C. and Schramm, V.L. (2009) Transition state analogs of 5'-methylthioadenosine nucleosidase disrupt quorum sensing. Nat Chem Biol 5, 251-257.
17. Hall-Stoodley, L., Costerton, J.W. and Stoodley, P. (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2, 95-108.
18. He, Q., Kubec, R., Jadhav, A.P. and Musah, R.A. (2011) First insights into the mode of action of a "lachrymatory factor synthase"-implications for the mechanism of lachrymator formation in Petiveria alliacea, Allium cepa and Nectaroscordum species. Phytochemistry 72, 1939-1946.
19. He, Z., Wang, Q., Hu, Y., Liang, J., Jiang, Y., Ma, R., Tang, Z. and Huang, Z. (2012) Use of the quorum sensing inhibitor furanone C-30 to interfere with biofilm formation by Streptococcus mutans and its luxS mutant strain. Int J Antimicrob Agents 40, 30-35.
20. Hentzer, M., Riedel, K., Rasmussen, T.B., Heydorn, A., Andersen, J.B., Parsek, M.R., Rice, S.A., Eberl, L. et al. (2002) Inhibition of quorum sensing in Pseudomonas aeruginosa biofilm bacteria by a halogenated furanone compound. Microbiology 148, 87-102.
21. Heydorn, A., Nielsen, A.T., Hentzer, M., Sternberg, C., Givskov, M., Ersbøll, B.K. and Molin, S. (2000) Quantification of biofilm structures by the novel computer program COMSTAT. Microbiology 146, 2395-2407.
22. Hojo, K., Nagaoka, S., Ohshima, T. and Maeda, N. (2009) Bacterial interactions in dental biofilm development. J Dent Res 88, 982-990.
23. Jakobsen, T.H., Bragason, S.K., Phipps, R.K., Christensen, L.D., van Gennip, M., Alhede, M., Skindersoe, M., Larsen, T.O. et al. (2012a) Food as a source for quorum sensing inhibitors: iberin from horseradish revealed as a quorum sensing inhibitor of Pseudomonas aeruginosa. Appl Environ Microbiol 78, 2410-2421.
24. Jakobsen, T.H., van Gennip, M., Phipps, R.K., Shanmugham, M.S., Christensen, L.D., Alhede, M., Skindersoe, M.E., Rasmussen, T.B., et al. (2012b) Ajoene, a sulfur-rich molecule from garlic, inhibits genes controlled by quorum sensing. Antimicrob Agents Chemother 56, 2314-2325.
25. Johnson, T.B. and Ambler, J.A. (1914) The alkylation and hydrolysis of aliphatic sulfonamides. A new synthesis of sarcosine. Annales 87, 372-385.
26. Kalia, V.C. (2013) Quorum sensing inhibitors: an overview. Biotechnol Adv 31, 224-245.
27. Koh, C., Sam, C., Yin, W., Tan, L.Y. and Krishnan, T. (2013) Plant-derived natural products as sources of anti-quorum sensing compounds. Sensors 13, 6217-6228.
28. Kolenbrander, P.E. and London, J. (1993) Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175, 3247-3252.
29. Kolenbrander, P.E., Andersen, R.N., Blehert, D.S., Egland, P.G., Foster, J.S. and Palmer, R.J. Jr (2002) Communication among Oral Bacteria. Microbiol Mol Biol Rev 66, 486-505.
30. Kolenbrander, P.E., Palmer, R.J., Rickard, A.H., Jakubovics, N.S., Chalmers, N.I. and Diaz, P.I. (2006) Bacterial interactions and successions during plaque development. Periodontol 2000 42, 47-79.
31. Kolenbrander, P.E., Palmer, R.J., Periasamy, S. and Jakubovics, N.S. (2010) Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol 8, 471-480.
32. Kubec, R., Kim, S. and Musah, R.A. (2002) S-Substituted cysteine derivatives and thiosulfinate formation in Petiveria alliacea-part II. Phytochemistry 61, 675-680.
33. Lee, J., Wu, J., Deng, Y., Wang, J. and Wang, C. (2013) A cell-cell communication signal integrates quorum sensing and stress response. Nat Chem Biol 9, 339-343.
34. Lewis, K. (2007) Persister cells, dormancy and infectious disease. Nat Rev Microbiol 5, 48-56.
35. Lönn-Stensrud, J., Petersen, F.C., Benneche, T. and Scheie, A.A. (2007) Synthetic bromated furanone inhibits autoinducer-2-mediated communication and biofilm formation in oral Streptococci. Oral Microbiol Immunol 22, 340-346.
36. March, J.C. and Bentley, W.E. (2004) Quorum sensing and bacterial cross-talk in biotechnology. Curr Opin Biotechnol 15, 495-502.
37. Marsh, P.D. (2005) Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 32, 7-15.
38. Marsh, P.D., Moter, A. and Devine, D.A. (2011) Dental plaque biofilms: communities, conflict and control. Periodontol 2000 55, 16-35.
39. Mcnab, R., Ford, S.K., El-Sabaeny, A., Barbieri, B., Cook, G.S. and Lamont, R.J. (2003) LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J Bacteriol 185, 274-284.
40. Merritt, J., Qi, F., Goodman, S.D., Maxwell, H., Shi, W. and Anderson, M.H. (2003) Mutation of luxS affects biofilm formation in Streptococcus mutans. Infect Immun 71, 1972-1979.
41. Merritt, J., Kreth, J., Shi, W. and Qi, F. (2005) LuxS controls bacteriocin production in Streptococcus mutans through a novel regulatory component. Mol Microbiol 57, 960-969.
42. Musah, R.A., He, Q., Kubec, R. and Jadhav, A. (2009) Studies of a novel cysteine sulfoxide lyase from Petiveria alliacea: the first heteromeric alliinase. Plant Physiol 151, 1304-1316.
43. Nance, W.C., Dowd, S.E., Samarian, D., Chludzinski, J., Delli, J., Battista, J. and Rickard, A.H. (2013) A high-throughput microfluidic dental plaque biofilm system to visualize and quantify the effect of antimicrobials. J Antimicrob Chemother 68, 2550-2560.
44. Njoroge, J. and Sperandio, V. (2009) Jamming bacterial communication: new approaches for the treatment of infectious diseases. EMBO Mol Med 1, 201-210.
45. O'Toole, G.A., Pratt, L.A., Watnick, P.I., Newman, D.K., Weaver, V.B. and Kolter, R. (1999) Genetic approaches to study of biofilms. Methods Enzymol 310, 91-109.
46. Paju, S. and Scannapieco, F.A. (2007) Oral biofilms, periodontitis, and pulmonary infections. Oral Dis 13, 508-512.
47. Parsek, M.R. and Greenberg, E.P. (2000) Acyl-homoserine lactone quorum sensing in gram-negative bacteria: a signaling mechanism involved in associations with higher organisms. Proc Natl Acad Sci USA 97, 8789-8793.
48. Rasmussen, T.B. and Givskov, M. (2006a) Quorum sensing inhibitors: a bargain of effects. Microbiology 152, 895-904.
49. Rasmussen, T.B. and Givskov, M. (2006b) Quorum-sensing inhibitors as anti-pathogenic drugs. Int J Med Microbiol 296, 149-161.
50. Rickard, A.H., Palmer, R.J., Blehert, D.S., Campagna, S.R., Semmelhack, M.F., Egland, P.G., Bassler, B.L. and Kolenbrander, P.E. (2006) Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol Microbiol 60, 1446-1456.
51. Roberts, A.P. and Mullany, P. (2010) Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev Anti Infect Ther 8, 1441-1450.
52. Scannapieco, F.A. (1999) Role of oral bacteria in respiratory infection. J Periodontol 70, 793-802.
53. Scannapieco, F.A., Bush, R.B. and Paju, S. (2003) Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review. Ann Periodontol 8, 38-53.
54. Schauder, S., Shokat, K., Surette, M.G. and Bassler, B.L. (2001) The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol 41, 463-476.
55. Schneider, C.A., Rasband, W.S. and Eliceiri, K.W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9, 671-675.
56. Selwitz, R.H., Ismail, A.I. and Pitts, N.B. (2007) Dental caries. Lancet 369, 51-59.
57. Semmelhack, M.F., Campagna, S.R., Federle, M.J. and Bassler, B.L. (2005) An expeditious synthesis of DPD and boron binding studies. Org Lett 7, 569-572.
58. Senadheera, M.D., Guggenheim, B., Grace, A., Huang, Y.C., Choi, J., David, C.I., Treglown, J.S., Goodman, S.D. et al. (2005) A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 187, 4064-4076.
59. Shao, H. and Demuth, D.R. (2010) Quorum sensing regulation of biofilm growth and gene expression by oral bacteria and periodontal pathogens. Periodontol 2000 52, 53-67.
60. Shemesh, M., Tam, A., Aharoni, R. and Steinberg, D. (2010) Genetic adaptation of Streptococcus mutans during biofilm formation on different types of surfaces. BMC Microbiol 10, 51.
61. Stewart, P.S. (2002) Mechanisms of antibiotic resistance in bacterial biofilms. Int J Med Microbiol 292, 107-113.
62. Stewart, P.S. and Costerton, J.W. (2001) Antibiotic resistance of bacteria in biofilms. Lancet 358, 135-138.
63. Stroeher, U.H., Paton, A.W., Ogunniyi, A.D. and Paton, J.C. (2003) Mutation of luxS of Streptococcus pneumoniae affects virulence in a mouse model. Infect Immun 71, 3206-3212.
64. Sztajer, H., Lemme, A., Vilchez, R., Schulz, S., Geffers, R., Yip, C.Y.Y., Levesque, C.M., Cvitkovitch, D.G. et al. (2008) Autoinducer-2-regulated genes in Streptococcus mutans UA159 and global metabolic effect of the luxS mutation. J Bacteriol 190, 401-415.
65. Vendeville, A., Winzer, K., Heurlier, K., Tang, C.M. and Hardie, K.R. (2005) Making "sense" of metabolism: autoinducer-2, LuxS and pathogenic bacteria. Nat Rev Microbiol 3, 383-396.
66. Vilchez, R., Lemme, A., Thiel, V., Schulz, S., Sztajer, H. and Wagner-Döbler, I. (2007) Analysing traces of autoinducer-2 requires standardization of the Vibrio harveyi bioassay. Anal Bioanal Chem 387, 489-496.
67. Wen, Z.T. and Burne, R.A. (2002) Functional genomics approach to identifying genes required for biofilm development by Streptococcus mutans. Appl Environ Microbiol 68, 1196-1203.
68. Wen, Z.T. and Burne, R.A. (2004) LuxS-mediated signaling in Streptococcus mutans is involved in regulation of acid and oxidative stress tolerance and biofilm formation. J Bacteriol 186, 2682-2691.
69. Wen, Z.T., Yates, D., Ahn, S. and Burne, R.A. (2010) Biofilm formation and virulence expression by Streptococcus mutans are altered when grown in dual-species model. BMC Microbiol 10, 111.
70. Winans, S.C. and Bassler, B.L. (2002) Mob psychology. J Bacteriol 184, 873-883.
71. Wu, H., Song, Z., Hentzer, M., Andersen, J.B., Molin, S., Givskov, M. and Høiby, N. (2004) Synthetic furanones inhibit quorum-sensing and enhance bacterial clearance in Pseudomonas aeruginosa lung infection in mice. J Antimicrob Chemother 53, 1054-1061.
72. Xavier, K.B. and Bassler, B.L. (2003) LuxS quorum sensing: more than just a numbers game. Curr Opin Microbiol 6, 191-197.
73. Yoshida, A., Ansai, T., Takehara, T. and Kuramitsu, H.K. (2005) LuxS-based signaling affects Streptococcus mutans biofilm formation. Appl Environ Microbiol 71, 2372-2380.
74. Zeigler, C.C., Persson, G.R., Wondimu, B., Marcus, C., Sobko, T. and Modéer, T. (2012) Microbiota in the oral subgingival biofilm is associated with obesity in adolescence. Obesity (Silver Spring) 20, 157-164.
75. Zhao, G., Wan, W., Mansouri, S., Alfaro, J.F., Bassler, B.L., Cornell, K.A. and Zhou, Z.S. (2003) Chemical synthesis of S-ribosyl-l-homocysteine and activity assay as a LuxS substrate. Bioorg Med Chem Lett 13, 3897-3900.