Research Article
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Effect of D-Ribose on Fusobacterium Nucleatum Planktonic Proliferation and Biofilm Maturation

Year 2022, Volume 13, Issue 3, 379 - 384, 01.07.2022
https://doi.org/10.31067/acusaglik.1000709

Abstract

Purpose: Periodontopathogenic biofilm structure is one of the most important factors in the etiology of inflammatory periodontal diseases. Quorum Sensing inhibitors (QSi) can inhibit biofilm development/maturation by inhibiting bacterial communication mechanism. In this study, we examined the effects of D-ribose (QSi) on the planktonic growth and bio.film formation characteristics of Fusobacterium nucleatum, an important periodontopathogenic species that has a binding function on early and late colonization types for the development of periodontopathogenic biofilm. Methods: The strain of F. nucleatum (ATCC 25586) and two clinical isolated strains (AHN 9910 and AHN 9508) were used in all tests. Planktonic proliferation (measured as colony forming units) and established biofilm tests (measured as total biofilm mass) were performed in the presence of 50mM D-ribose. Results: In planktonic growth tests, statistically significant increase was observed for F. nucleatum ATCC 25586 and AHN 9508 strains (p<0.05). In established biofilm tests, a mean-based decrease was observed for all species, but a statistically significant difference was found only for F. nucleatum AHN 9910. Conclusions: The fact that the presence of D-ribose can increase the planktonic growth of F. nucleatum and its inhibitory effect on biofilm development shows that it may have an adverse effect on biofilm development by disrupting the Quorum-Sensing system.

References

  • Socransky SS, Haffajee AD, Dzink JL, et al. Associations between microbial species in subgingival plaque samples. Oral Microbiol Immunol. 1988 Mar;3(1):1-7. doi: 10.1111/j.1399-302x.1988.tb00596.x. PMID: 3268742.
  • Bolstad AI, Jensen HB and Bakken V. Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin Microbiol Rev. 1996 Jan;9(1):55-71. doi: 10.1128/CMR.9.1.55. PMID: 8665477; PMCID: PMC172882.
  • Gursoy UK, Pöllänen M, Könönen E, et al. Biofilm formation enhances the oxygen tolerance and invasiveness of Fusobacterium nucleatum in an oral mucosa culture model. J Periodontol. 2010 Jul;81(7):1084-91. doi: 10.1902/jop.2010.090664. PMID: 20350156.
  • Penesyan A, Gillings M and Paulsen IT. Antibiotic discovery: combatting bacterial resistance in cells and in biofilm communities. Molecules. 2015 Mar 24;20(4):5286-98. doi: 10.3390/molecules20045286. PMID: 25812150; PMCID: PMC6272253.
  • Taylor PK, Yeung AT and Hancock RE. Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol. 2014 Dec 10;191:121-30. doi: 10.1016/j.jbiotec.2014.09.003. Epub 2014 Sep 18. PMID: 25240440.
  • Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis. 2015 May;34(5):877-86. doi: 10.1007/s10096-015-2323-z. Epub 2015 Jan 29. PMID: 25630538.
  • Schauder S, Shokat K, Surette MG, et al. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol. 2001 Jul;41(2):463-76. doi: 10.1046/j.1365-2958.2001.02532.x. PMID: 11489131.
  • Gospodarek E, Bogiel T and Zalas-Wiecek P. Communication between microorganisms as a basis for production of virulence factors. Pol J Microbiol. 2009;58(3):191-8. PMID: 19899610.
  • Pan J, Ren D. Quorum sensing inhibitors: a patent overview. Expert Opin Ther Pat. 2009 Nov;19(11):1581-601. doi: 10.1517/13543770903222293. PMID: 19732032.
  • Harjai K, Gupta RK and Sehgal H. Attenuation of quorum sensing controlled virulence of Pseudomonas aeruginosa by cranberry. Indian J Med Res. 2014 Mar;139(3):446-53. PMID: 24820840; PMCID: PMC4069740
  • Liu L, Wu R, Zhang J, et al. D-Ribose Interferes with Quorum Sensing to Inhibit Biofilm Formation of Lactobacillus paraplantarum L-ZS9. Front Microbiol. 2017 Sep 26;8:1860. doi: 10.3389/fmicb.2017.01860. PMID: 29018429; PMCID: PMC5622935.
  • Armbruster CE, Pang B, Murrah K, et al. RbsB (NTHI_0632) mediates quorum signal uptake in nontypeable Haemophilus influenzae strain 86-028NP. Mol Microbiol. 2011 Nov;82(4):836-50. doi: 10.1111/j.1365-2958.2011.07831.x. Epub 2011 Oct 20. PMID: 21923771; PMCID: PMC3609414.
  • Cho YJ, Song HY, Ben Amara H, et al. In Vivo Inhibition of Porphyromonas gingivalis Growth and Prevention of Periodontitis With Quorum-Sensing Inhibitors. J Periodontol. 2016 Sep;87(9):1075-82. doi: 10.1902/jop.2016.160070. Epub 2016 May 13. PMID: 27177290.
  • Brackman G, Celen S, Baruah K, et al. AI-2 quorum-sensing inhibitors affect the starvation response and reduce virulence in several Vibrio species, most likely by interfering with LuxPQ. Microbiology (Reading). 2009 Dec;155(Pt 12):4114-4122. doi: 10.1099/mic.0.032474-0. Epub 2009 Sep 24. PMID: 19778962.
  • Roy V, Meyer MT, Smith JA, et al. AI-2 analogs and antibiotics: a synergistic approach to reduce bacterial biofilms. Appl Microbiol Biotechnol. 2013 Mar;97(6):2627-38. doi: 10.1007/s00253-012-4404-6. Epub 2012 Oct 4. PMID: 23053069.
  • Gursoy UK, Könönen E, Luukkonen N, et al. Human neutrophil defensins and their effect on epithelial cells. J Periodontol. 2013 Jan;84(1):126-33. doi: 10.1902/jop.2012.120017. Epub 2012 Mar 23. PMID: 22443519.
  • Keskin M, Könönen E, Söderling E, et al. Increased proliferation and decreased membrane permeability as defense mechanisms of Fusobacterium nucleatum against human neutrophilic peptide-1. Anaerobe. 2014 Dec;30:35-40. doi: 10.1016/j.anaerobe.2014.08.001. Epub 2014 Aug 12. PMID: 25132418.
  • Jang YJ, Choi YJ, Lee SH, et al. Autoinducer 2 of Fusobacterium nucleatum as a target molecule to inhibit biofilm formation of periodontopathogens. Arch Oral Biol. 2013 Jan;58(1):17-27. doi: 10.1016/j.archoralbio.2012.04.016. Epub 2012 May 26. PMID: 22633049.
  • Trizna, E., Latypova, L., Kurbangalieva, A. et al. 2(5H)-Furanone Derivatives as Inhibitors of Staphylococcal Biofilms. BioNanoSci. 6, 423–426 (2016). https://doi.org/10.1007/s12668-016-0258-1
  • Sharafutdinov IS, Trizna EY, Baidamshina DR, et al. Antimicrobial Effects of Sulfonyl Derivative of 2(5H)-Furanone against Planktonic and Biofilm Associated Methicillin-Resistant and -Susceptible Staphylococcus aureus. Front Microbiol. 2017 Nov 20;8:2246. doi: 10.3389/fmicb.2017.02246. PMID: 29209288; PMCID: PMC5701942.
  • Griffiths JC, Borzelleca JF, St Cyr J. Sub-chronic (13-week) oral toxicity study with D-ribose in Wistar rats. Food Chem Toxicol. 2007 Jan;45(1):144-52. doi: 10.1016/j.fct.2006.08.012. Epub 2006 Aug 30. PMID: 17011102.
  • Kim AR, Ahn KB, Kim HY, Seo HS, Kum KY, Yun CH, Han SH. Streptococcus gordonii lipoproteins induce IL-8 in human periodontal ligament cells. Mol Immunol. 2017 Nov;91:218-224. doi: 10.1016/j.molimm.2017.09.009. Epub 2017 Sep 30. PMID: 28963931.
  • Wilson C, Lukowicz R, Merchant S, et al. Quantitative and Qualitative Assessment Methods for Biofilm Growth: A Mini-review. Res Rev J Eng Technol. 2017 Dec;6(4):http://www.rroij.com/open-access/quantitative-and-qualitative-assessment-methods-for-biofilm-growth-a-minireview-.pdf. Epub 2017 Oct 24. PMID: 30214915; PMCID: PMC6133255.
  • Pokusaeva K, Neves AR, Zomer A, et al. Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol. 2010 May;3(3):311-23. doi: 10.1111/j.1751-7915.2009.00152.x. Epub 2009 Oct 15. PMID: 21255330; PMCID: PMC3815373.
  • Walker A, Cerdeño-Tárraga A, Bentley S. Faecal matters. Nat Rev Microbiol. 2006 Aug;4(8):572-3. doi: 10.1038/nrmicro1483. PMID: 16888877.
  • Lopilato JE, Garwin JL, Emr SD, et al. D-ribose metabolism in Escherichia coli K-12: genetics, regulation, and transport. J Bacteriol. 1984 May;158(2):665-73. doi: 10.1128/jb.158.2.665-673.1984. PMID: 6327616; PMCID: PMC215481.
  • Flynn KJ, Baxter NT and Schloss PD. Metabolic and Community Synergy of Oral Bacteria in Colorectal Cancer. mSphere. 2016 May 11;1(3):e00102-16. doi: 10.1128/mSphere.00102-16. PMID: 27303740; PMCID: PMC4888883.
  • Costerton JW, Stewart PS and Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999 May 21;284(5418):1318-22. doi: 10.1126/science.284.5418.1318. PMID: 10334980.
  • Ben Amara H, Song HY, Ryu E, et al. Effects of quorum-sensing inhibition on experimental periodontitis induced by mixed infection in mice. Eur J Oral Sci. 2018 Dec;126(6):449-457. doi: 10.1111/eos.12570. Epub 2018 Sep 19. PMID: 30230039.
  • Gerits E, Verstraeten N, Michiels J. New approaches to combat Porphyromonas gingivalis biofilms. J Oral Microbiol. 2017 Mar 15;9(1):1300366. doi: 10.1080/20002297.2017.1300366. PMID: 28473880; PMCID: PMC5405727.

Year 2022, Volume 13, Issue 3, 379 - 384, 01.07.2022
https://doi.org/10.31067/acusaglik.1000709

Abstract

References

  • Socransky SS, Haffajee AD, Dzink JL, et al. Associations between microbial species in subgingival plaque samples. Oral Microbiol Immunol. 1988 Mar;3(1):1-7. doi: 10.1111/j.1399-302x.1988.tb00596.x. PMID: 3268742.
  • Bolstad AI, Jensen HB and Bakken V. Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin Microbiol Rev. 1996 Jan;9(1):55-71. doi: 10.1128/CMR.9.1.55. PMID: 8665477; PMCID: PMC172882.
  • Gursoy UK, Pöllänen M, Könönen E, et al. Biofilm formation enhances the oxygen tolerance and invasiveness of Fusobacterium nucleatum in an oral mucosa culture model. J Periodontol. 2010 Jul;81(7):1084-91. doi: 10.1902/jop.2010.090664. PMID: 20350156.
  • Penesyan A, Gillings M and Paulsen IT. Antibiotic discovery: combatting bacterial resistance in cells and in biofilm communities. Molecules. 2015 Mar 24;20(4):5286-98. doi: 10.3390/molecules20045286. PMID: 25812150; PMCID: PMC6272253.
  • Taylor PK, Yeung AT and Hancock RE. Antibiotic resistance in Pseudomonas aeruginosa biofilms: towards the development of novel anti-biofilm therapies. J Biotechnol. 2014 Dec 10;191:121-30. doi: 10.1016/j.jbiotec.2014.09.003. Epub 2014 Sep 18. PMID: 25240440.
  • Olsen I. Biofilm-specific antibiotic tolerance and resistance. Eur J Clin Microbiol Infect Dis. 2015 May;34(5):877-86. doi: 10.1007/s10096-015-2323-z. Epub 2015 Jan 29. PMID: 25630538.
  • Schauder S, Shokat K, Surette MG, et al. The LuxS family of bacterial autoinducers: biosynthesis of a novel quorum-sensing signal molecule. Mol Microbiol. 2001 Jul;41(2):463-76. doi: 10.1046/j.1365-2958.2001.02532.x. PMID: 11489131.
  • Gospodarek E, Bogiel T and Zalas-Wiecek P. Communication between microorganisms as a basis for production of virulence factors. Pol J Microbiol. 2009;58(3):191-8. PMID: 19899610.
  • Pan J, Ren D. Quorum sensing inhibitors: a patent overview. Expert Opin Ther Pat. 2009 Nov;19(11):1581-601. doi: 10.1517/13543770903222293. PMID: 19732032.
  • Harjai K, Gupta RK and Sehgal H. Attenuation of quorum sensing controlled virulence of Pseudomonas aeruginosa by cranberry. Indian J Med Res. 2014 Mar;139(3):446-53. PMID: 24820840; PMCID: PMC4069740
  • Liu L, Wu R, Zhang J, et al. D-Ribose Interferes with Quorum Sensing to Inhibit Biofilm Formation of Lactobacillus paraplantarum L-ZS9. Front Microbiol. 2017 Sep 26;8:1860. doi: 10.3389/fmicb.2017.01860. PMID: 29018429; PMCID: PMC5622935.
  • Armbruster CE, Pang B, Murrah K, et al. RbsB (NTHI_0632) mediates quorum signal uptake in nontypeable Haemophilus influenzae strain 86-028NP. Mol Microbiol. 2011 Nov;82(4):836-50. doi: 10.1111/j.1365-2958.2011.07831.x. Epub 2011 Oct 20. PMID: 21923771; PMCID: PMC3609414.
  • Cho YJ, Song HY, Ben Amara H, et al. In Vivo Inhibition of Porphyromonas gingivalis Growth and Prevention of Periodontitis With Quorum-Sensing Inhibitors. J Periodontol. 2016 Sep;87(9):1075-82. doi: 10.1902/jop.2016.160070. Epub 2016 May 13. PMID: 27177290.
  • Brackman G, Celen S, Baruah K, et al. AI-2 quorum-sensing inhibitors affect the starvation response and reduce virulence in several Vibrio species, most likely by interfering with LuxPQ. Microbiology (Reading). 2009 Dec;155(Pt 12):4114-4122. doi: 10.1099/mic.0.032474-0. Epub 2009 Sep 24. PMID: 19778962.
  • Roy V, Meyer MT, Smith JA, et al. AI-2 analogs and antibiotics: a synergistic approach to reduce bacterial biofilms. Appl Microbiol Biotechnol. 2013 Mar;97(6):2627-38. doi: 10.1007/s00253-012-4404-6. Epub 2012 Oct 4. PMID: 23053069.
  • Gursoy UK, Könönen E, Luukkonen N, et al. Human neutrophil defensins and their effect on epithelial cells. J Periodontol. 2013 Jan;84(1):126-33. doi: 10.1902/jop.2012.120017. Epub 2012 Mar 23. PMID: 22443519.
  • Keskin M, Könönen E, Söderling E, et al. Increased proliferation and decreased membrane permeability as defense mechanisms of Fusobacterium nucleatum against human neutrophilic peptide-1. Anaerobe. 2014 Dec;30:35-40. doi: 10.1016/j.anaerobe.2014.08.001. Epub 2014 Aug 12. PMID: 25132418.
  • Jang YJ, Choi YJ, Lee SH, et al. Autoinducer 2 of Fusobacterium nucleatum as a target molecule to inhibit biofilm formation of periodontopathogens. Arch Oral Biol. 2013 Jan;58(1):17-27. doi: 10.1016/j.archoralbio.2012.04.016. Epub 2012 May 26. PMID: 22633049.
  • Trizna, E., Latypova, L., Kurbangalieva, A. et al. 2(5H)-Furanone Derivatives as Inhibitors of Staphylococcal Biofilms. BioNanoSci. 6, 423–426 (2016). https://doi.org/10.1007/s12668-016-0258-1
  • Sharafutdinov IS, Trizna EY, Baidamshina DR, et al. Antimicrobial Effects of Sulfonyl Derivative of 2(5H)-Furanone against Planktonic and Biofilm Associated Methicillin-Resistant and -Susceptible Staphylococcus aureus. Front Microbiol. 2017 Nov 20;8:2246. doi: 10.3389/fmicb.2017.02246. PMID: 29209288; PMCID: PMC5701942.
  • Griffiths JC, Borzelleca JF, St Cyr J. Sub-chronic (13-week) oral toxicity study with D-ribose in Wistar rats. Food Chem Toxicol. 2007 Jan;45(1):144-52. doi: 10.1016/j.fct.2006.08.012. Epub 2006 Aug 30. PMID: 17011102.
  • Kim AR, Ahn KB, Kim HY, Seo HS, Kum KY, Yun CH, Han SH. Streptococcus gordonii lipoproteins induce IL-8 in human periodontal ligament cells. Mol Immunol. 2017 Nov;91:218-224. doi: 10.1016/j.molimm.2017.09.009. Epub 2017 Sep 30. PMID: 28963931.
  • Wilson C, Lukowicz R, Merchant S, et al. Quantitative and Qualitative Assessment Methods for Biofilm Growth: A Mini-review. Res Rev J Eng Technol. 2017 Dec;6(4):http://www.rroij.com/open-access/quantitative-and-qualitative-assessment-methods-for-biofilm-growth-a-minireview-.pdf. Epub 2017 Oct 24. PMID: 30214915; PMCID: PMC6133255.
  • Pokusaeva K, Neves AR, Zomer A, et al. Ribose utilization by the human commensal Bifidobacterium breve UCC2003. Microb Biotechnol. 2010 May;3(3):311-23. doi: 10.1111/j.1751-7915.2009.00152.x. Epub 2009 Oct 15. PMID: 21255330; PMCID: PMC3815373.
  • Walker A, Cerdeño-Tárraga A, Bentley S. Faecal matters. Nat Rev Microbiol. 2006 Aug;4(8):572-3. doi: 10.1038/nrmicro1483. PMID: 16888877.
  • Lopilato JE, Garwin JL, Emr SD, et al. D-ribose metabolism in Escherichia coli K-12: genetics, regulation, and transport. J Bacteriol. 1984 May;158(2):665-73. doi: 10.1128/jb.158.2.665-673.1984. PMID: 6327616; PMCID: PMC215481.
  • Flynn KJ, Baxter NT and Schloss PD. Metabolic and Community Synergy of Oral Bacteria in Colorectal Cancer. mSphere. 2016 May 11;1(3):e00102-16. doi: 10.1128/mSphere.00102-16. PMID: 27303740; PMCID: PMC4888883.
  • Costerton JW, Stewart PS and Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1999 May 21;284(5418):1318-22. doi: 10.1126/science.284.5418.1318. PMID: 10334980.
  • Ben Amara H, Song HY, Ryu E, et al. Effects of quorum-sensing inhibition on experimental periodontitis induced by mixed infection in mice. Eur J Oral Sci. 2018 Dec;126(6):449-457. doi: 10.1111/eos.12570. Epub 2018 Sep 19. PMID: 30230039.
  • Gerits E, Verstraeten N, Michiels J. New approaches to combat Porphyromonas gingivalis biofilms. J Oral Microbiol. 2017 Mar 15;9(1):1300366. doi: 10.1080/20002297.2017.1300366. PMID: 28473880; PMCID: PMC5405727.

Details

Primary Language English
Subjects Dentistry, Oral Surgery and Medicine, Medicine, Microbiology
Journal Section Research Article
Authors

Mutlu KESKİN> (Primary Author)
University Of Turku, Institute of Dentistry, Periodontology Department
0000-0002-1045-3930
Türkiye

Supporting Institution This study was supported by the Finnish Government CIMO Foundation (KM-12-8028), Turku University Foundation for research grants (U.K.G) and Finnish Dental Society Apollonia (U.K.G.).
Project Number KM-12-8028
Thanks The author appreciate Assoc. Prof. Ulvi Gursoy, Prof. Eija Könönen and laboratory technicians Oona Hällfors and Katja Sampalahti for their invaluable support.
Publication Date July 1, 2022
Application Date September 25, 2021
Acceptance Date May 15, 2022
Published in Issue Year 2022, Volume 13, Issue 3

Cite

EndNote %0 Acıbadem Üniversitesi Sağlık Bilimleri Dergisi Effect of D-Ribose on Fusobacterium Nucleatum Planktonic Proliferation and Biofilm Maturation %A Mutlu Keskin %T Effect of D-Ribose on Fusobacterium Nucleatum Planktonic Proliferation and Biofilm Maturation %D 2022 %J Acıbadem Üniversitesi Sağlık Bilimleri Dergisi %P 1309-470X-1309-5994 %V 13 %N 3 %R doi: 10.31067/acusaglik.1000709 %U 10.31067/acusaglik.1000709