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A Comparative Analysis of Biofilm Characteristics of Dual-Species Periodontopathogenic Biofilm based on Fusobacterium nucleatum and the Dual- Species Biofilm Response in the Presence of Antimicrobial Peptide

Year 2020, Volume: 2 Issue: 1, 1 - 10, 31.01.2020

Abstract

Fusobacterium nucleatum (F.nucleatum), which acts as a linking periodontopathogenic bacteria, has the ability of coaggregation with early and late colonization species. It is the most intense gram-negative bacteria found in periodontal health and increases in periodontal diseased areas numerically. In this study, comparative analyses of dual and mono-biofilm structural characteristics formed by Porphyromonas gingivalis and Prevotella intermedia with F. nucleatum have been evaluated. In all results, more biofilm formation was observed in dual-species compared to mono-species biofilms. Biofilm formation of F. nucleatum-P.intermedia has increased in the presence of Human Neutrophilic Peptide (HNP-1). In this study it is concluded that dual-periodontopathogenic coaggregations based on F. nucleatum could produce more intense biofilm structure than single-species ones, and the increase in dual-species biofilm mass in the presence of low doses of HNP-1 may be a defense mechanism of dual periodontopathogenic biofilm.

References

  • Akins, R. E., Tuan, R. S. (1995). Ultrafast protein determinations using microwave enhancement. Molecular Biotechnology, 4(1), 17–24. Doi: 10.1007/bf02907468 Bolstad, A. I., Jensen, H. B., Bakken, V. (1996). Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clinical Microbiology Reviews, 9(1), 55–71. Doi: 10.1128/cmr.9.1.55
  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254. Doi: 10.1006/abio.1976.9999
  • Dale, B. A., Tao, R., Kimball, J. R., Jurevic, R. J. (2006). Oral antimicrobial peptides and biological control of caries. BMC Oral Health, 6(S1). Doi: 10.1186/1472-6831-6-s1-s13
  • Ebersole, J. L., Dawson, D., Emecen-Huja, P., Nagarajan, R., Howard, K., Grady, M. E., Gonzalez, O. A. (2017). The periodontal war: microbes and immunity. Periodontology 2000, 75(1), 52–115. Doi: 10.1111/prd.12222
  • Fanali, C., Inzitari, R., Cabras, T., Pisano, E., Castagnola, M., Celletti, R., Messana, I. (2008). α-Defensin levels in whole saliva of totally edentulous subjects. International Journal of Immunopathology and Pharmacology, 21(4), 845–849. Doi: 10.1177/039463200802100409
  • Flemming, H. C., Wingender, J. (2010). The biofilm matrix. Nature Reviews Microbiology, 8(9), 623–633. Doi: 10.1038/nrmicro2415
  • Goebel, C., Mackay, L., Vickers, E., Mather, L. (2000). Determination of defensin HNP-1, HNP-2, and HNP-3 in human saliva by using LC/MS. Peptides, 21(6), 757–765. Doi: 10.1016/s0196-9781(00)00205-9
  • Jang, Y. J., Choi, Y. J., Lee, S. H., Jun, H. K., Choi, B. K. (2013). Autoinducer 2 of Fusobacterium nucleatum as a target molecule to inhibit biofilm formation of periodontopathogens. Archives of Oral Biology, 58(1), 17–27. Doi: 10.1016/j.archoralbio.2012.04.016
  • Keskin, M., Könönen, E., Söderling, E., Isik, G., Firatli, E., Uitto, V.J., Gürsoy, U.K. (2014). Increased proliferation and decreased membrane permeability as defense mechanisms of Fusobacterium nucleatum against human neutrophilic peptide-1. Anaerobe, 30, 35–40. Doi: 10.1016/j.anaerobe.2014.08.001
  • Kolenbrander, P. E., Andersen, R. N. (1989). Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas (Bacteroides) gingivalis by lactose and related sugars. Infect Immun, 57, 3204-3209.
  • Kolenbrander, P. E., Andersen, R. N., Moore, L. V. (1989). Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect Immun, 57, 3194-3203.
  • Kolenbrander, P. E., London, J. (1993). Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175, 3247-3252
  • Lamont, R. J., Hajishengallis, G. (2015). Polymicrobial synergy and dysbiosis in inflammatory disease. Trends in Molecular Medicine, 21(3), 172–183. Doi: 10.1016/j.molmed.2014.11.004
  • Lamont, R. J., Koo, H., Hajishengallis, G. (2018). The oral microbiota: dynamic communities and host interactions. Nature Reviews Microbiology, 16(12), 745–759. Doi: 10.1038/s41579-018-0089-x
  • Lu, T. K., Collins, J. J. (2007). Dispersing biofilms with engineered enzymatic bacteriophage. Proceedings of the National Academy of Sciences, 104(27), 11197–11202. Doi: 10.1073/pnas.0704624104
  • Lundy, F. T., Nelson, J., Lockhart, D., Greer, B., Harriott, P., Marley, J. J. (2008). Antimicrobial activity of truncated α-defensin (human neutrophil peptide (HNP)-1) analogues without disulphide bridges. Molecular Immunology, 45(1), 190–193. Doi: 10.1016/j.molimm.2007.04.018
  • Merritt, K., Gaind, A., Anderson, J. M. (1998). Detection of bacterial adherence on biomedical polymers. Journal of Biomedical Materials Research, 39(3), 415–422. Doi: 10.1002/(sici)1097-4636(19980305)39:3<415::aid-jbm10>3.0.co;2-9
  • Okuda, T., Kokubu, E., Kawana, T., Saito, A., Okuda, K., Ishihara, K. (2012). Synergy in biofilm formation between Fusobacterium nucleatum and Prevotella species. Anaerobe, 18(1), 110–116. Doi: 10.1016/j. anaerobe.2011.09.003
  • Pitts, B., Hamilton, M. A., Zelver, N., Stewart, P. S. (2003). A microtiter-plate screening method for biofilm disinfection and removal. Journal of Microbiological Methods, 54(2), 269–276. Doi: 10.1016/s0167-7012(03)00034-4
  • Puklo, M., Guentsch, A., Hiemstra, P. S., Eick, S., Potempa, J. (2008). Analysis of neutrophil-derived antimicrobial peptides in gingival crevicular fluid suggests importance of cathelicidin LL-37 in the innate immune response against periodontogenic bacteria. Oral Microbiology and Immunology, 23(4), 328–335. Doi: 10.1111/j.1399-302x.2008.00433.x
  • Rickard, A. H., Gilbert, P., High, N. J., Kolenbrander, P. E., Handley, P. S. (2003). Bacterial coaggregation: an integral process in the development of multi-species biofilms.Trends in Microbiology,11(2), 94–100. Doi: 10.1016/s0966-842x(02)00034-3
  • Roth, J. R., Binder, M., Gerhard, U. J. (1978). Conjugation of lectins with fluorochromes: an approach to histochemical double labeling of carbohydrate components. Histochemistry, 56(3-4), 265–273. Doi: 10.1007/bf00495988
  • Saito, Y., Fujii, R., Nakagawa, K. I., Kuramitsu, H. K., Okuda, K., Ishihara, K. (2007). Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiology and Immunology, 23(1), 1–6. Doi: 10.1111/j.1399-302x.2007.00380.x
  • Sato, K., Anzai, J. I. (2006). Fluorometric determination of sugars using fluorescein-labeled concanavalin A–glycogen conjugates. Analytical and Bioanalytical Chemistry, 384(6), 1297–1301. Doi: 10.1007/s00216-005-0279-z
  • Shaddox, L., Alfant, B., Tobler, J., Walker, C. (2010). Perpetuation of subgingival biofilms in an in vitro model. Molecular Oral Microbiology, 25(1), 81–87. Doi: 10.1111/j.2041-1014.2009.00549.x
  • Socransky, S., Haffajee, A., Cugini, M., Smith, C., Kent, R. L. (1998). Microbial complexes in subgingival plaque. Journal of Clinical Periodontology, 25(2), 134–144. Doi: 10.1111/j.1600-051x.1998.tb02419.x
  • Stepanović, S., Vuković, D., Dakić, I., Savić, B., Švabić-Vlahović, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40(2), 175–179. Doi: 10.1016/s0167-7012(00)00122-6
  • Teles, R., Sakellari, D., Teles, F., Konstantinidis, A., Kent, R., Socransky, S., Haffajee, A. (2010). Relationships among gingival crevicular fluid biomarkers, clinical parameters of periodontal disease, and the subgingival microbiota. Journal of Periodontology, 81(1), 89–98. Doi: 10.1902/jop.2009.090397
  • Walker, C., Sedlacek, M. J. (2007). An in vitro biofilm model of subgingival plaque. Oral Microbiology and Immunology, 22(3), 152–161. Doi: 10.1111/j.1399-302x.2007.00336.x
  • Yang, Y., Sreenivasan, P. K., Subramanyam, R., Cummins, D. (2006). Multiparameter assessments to determine the effects of sugars and antimicrobials on a polymicrobial oral biofilm. Applied and Environmental Microbiology, 72(10), 6734–6742. Doi: 10.1128/aem.01013-06
Year 2020, Volume: 2 Issue: 1, 1 - 10, 31.01.2020

Abstract

References

  • Akins, R. E., Tuan, R. S. (1995). Ultrafast protein determinations using microwave enhancement. Molecular Biotechnology, 4(1), 17–24. Doi: 10.1007/bf02907468 Bolstad, A. I., Jensen, H. B., Bakken, V. (1996). Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clinical Microbiology Reviews, 9(1), 55–71. Doi: 10.1128/cmr.9.1.55
  • Bradford, M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1-2), 248–254. Doi: 10.1006/abio.1976.9999
  • Dale, B. A., Tao, R., Kimball, J. R., Jurevic, R. J. (2006). Oral antimicrobial peptides and biological control of caries. BMC Oral Health, 6(S1). Doi: 10.1186/1472-6831-6-s1-s13
  • Ebersole, J. L., Dawson, D., Emecen-Huja, P., Nagarajan, R., Howard, K., Grady, M. E., Gonzalez, O. A. (2017). The periodontal war: microbes and immunity. Periodontology 2000, 75(1), 52–115. Doi: 10.1111/prd.12222
  • Fanali, C., Inzitari, R., Cabras, T., Pisano, E., Castagnola, M., Celletti, R., Messana, I. (2008). α-Defensin levels in whole saliva of totally edentulous subjects. International Journal of Immunopathology and Pharmacology, 21(4), 845–849. Doi: 10.1177/039463200802100409
  • Flemming, H. C., Wingender, J. (2010). The biofilm matrix. Nature Reviews Microbiology, 8(9), 623–633. Doi: 10.1038/nrmicro2415
  • Goebel, C., Mackay, L., Vickers, E., Mather, L. (2000). Determination of defensin HNP-1, HNP-2, and HNP-3 in human saliva by using LC/MS. Peptides, 21(6), 757–765. Doi: 10.1016/s0196-9781(00)00205-9
  • Jang, Y. J., Choi, Y. J., Lee, S. H., Jun, H. K., Choi, B. K. (2013). Autoinducer 2 of Fusobacterium nucleatum as a target molecule to inhibit biofilm formation of periodontopathogens. Archives of Oral Biology, 58(1), 17–27. Doi: 10.1016/j.archoralbio.2012.04.016
  • Keskin, M., Könönen, E., Söderling, E., Isik, G., Firatli, E., Uitto, V.J., Gürsoy, U.K. (2014). Increased proliferation and decreased membrane permeability as defense mechanisms of Fusobacterium nucleatum against human neutrophilic peptide-1. Anaerobe, 30, 35–40. Doi: 10.1016/j.anaerobe.2014.08.001
  • Kolenbrander, P. E., Andersen, R. N. (1989). Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas (Bacteroides) gingivalis by lactose and related sugars. Infect Immun, 57, 3204-3209.
  • Kolenbrander, P. E., Andersen, R. N., Moore, L. V. (1989). Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect Immun, 57, 3194-3203.
  • Kolenbrander, P. E., London, J. (1993). Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol 175, 3247-3252
  • Lamont, R. J., Hajishengallis, G. (2015). Polymicrobial synergy and dysbiosis in inflammatory disease. Trends in Molecular Medicine, 21(3), 172–183. Doi: 10.1016/j.molmed.2014.11.004
  • Lamont, R. J., Koo, H., Hajishengallis, G. (2018). The oral microbiota: dynamic communities and host interactions. Nature Reviews Microbiology, 16(12), 745–759. Doi: 10.1038/s41579-018-0089-x
  • Lu, T. K., Collins, J. J. (2007). Dispersing biofilms with engineered enzymatic bacteriophage. Proceedings of the National Academy of Sciences, 104(27), 11197–11202. Doi: 10.1073/pnas.0704624104
  • Lundy, F. T., Nelson, J., Lockhart, D., Greer, B., Harriott, P., Marley, J. J. (2008). Antimicrobial activity of truncated α-defensin (human neutrophil peptide (HNP)-1) analogues without disulphide bridges. Molecular Immunology, 45(1), 190–193. Doi: 10.1016/j.molimm.2007.04.018
  • Merritt, K., Gaind, A., Anderson, J. M. (1998). Detection of bacterial adherence on biomedical polymers. Journal of Biomedical Materials Research, 39(3), 415–422. Doi: 10.1002/(sici)1097-4636(19980305)39:3<415::aid-jbm10>3.0.co;2-9
  • Okuda, T., Kokubu, E., Kawana, T., Saito, A., Okuda, K., Ishihara, K. (2012). Synergy in biofilm formation between Fusobacterium nucleatum and Prevotella species. Anaerobe, 18(1), 110–116. Doi: 10.1016/j. anaerobe.2011.09.003
  • Pitts, B., Hamilton, M. A., Zelver, N., Stewart, P. S. (2003). A microtiter-plate screening method for biofilm disinfection and removal. Journal of Microbiological Methods, 54(2), 269–276. Doi: 10.1016/s0167-7012(03)00034-4
  • Puklo, M., Guentsch, A., Hiemstra, P. S., Eick, S., Potempa, J. (2008). Analysis of neutrophil-derived antimicrobial peptides in gingival crevicular fluid suggests importance of cathelicidin LL-37 in the innate immune response against periodontogenic bacteria. Oral Microbiology and Immunology, 23(4), 328–335. Doi: 10.1111/j.1399-302x.2008.00433.x
  • Rickard, A. H., Gilbert, P., High, N. J., Kolenbrander, P. E., Handley, P. S. (2003). Bacterial coaggregation: an integral process in the development of multi-species biofilms.Trends in Microbiology,11(2), 94–100. Doi: 10.1016/s0966-842x(02)00034-3
  • Roth, J. R., Binder, M., Gerhard, U. J. (1978). Conjugation of lectins with fluorochromes: an approach to histochemical double labeling of carbohydrate components. Histochemistry, 56(3-4), 265–273. Doi: 10.1007/bf00495988
  • Saito, Y., Fujii, R., Nakagawa, K. I., Kuramitsu, H. K., Okuda, K., Ishihara, K. (2007). Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiology and Immunology, 23(1), 1–6. Doi: 10.1111/j.1399-302x.2007.00380.x
  • Sato, K., Anzai, J. I. (2006). Fluorometric determination of sugars using fluorescein-labeled concanavalin A–glycogen conjugates. Analytical and Bioanalytical Chemistry, 384(6), 1297–1301. Doi: 10.1007/s00216-005-0279-z
  • Shaddox, L., Alfant, B., Tobler, J., Walker, C. (2010). Perpetuation of subgingival biofilms in an in vitro model. Molecular Oral Microbiology, 25(1), 81–87. Doi: 10.1111/j.2041-1014.2009.00549.x
  • Socransky, S., Haffajee, A., Cugini, M., Smith, C., Kent, R. L. (1998). Microbial complexes in subgingival plaque. Journal of Clinical Periodontology, 25(2), 134–144. Doi: 10.1111/j.1600-051x.1998.tb02419.x
  • Stepanović, S., Vuković, D., Dakić, I., Savić, B., Švabić-Vlahović, M. (2000). A modified microtiter-plate test for quantification of staphylococcal biofilm formation. Journal of Microbiological Methods, 40(2), 175–179. Doi: 10.1016/s0167-7012(00)00122-6
  • Teles, R., Sakellari, D., Teles, F., Konstantinidis, A., Kent, R., Socransky, S., Haffajee, A. (2010). Relationships among gingival crevicular fluid biomarkers, clinical parameters of periodontal disease, and the subgingival microbiota. Journal of Periodontology, 81(1), 89–98. Doi: 10.1902/jop.2009.090397
  • Walker, C., Sedlacek, M. J. (2007). An in vitro biofilm model of subgingival plaque. Oral Microbiology and Immunology, 22(3), 152–161. Doi: 10.1111/j.1399-302x.2007.00336.x
  • Yang, Y., Sreenivasan, P. K., Subramanyam, R., Cummins, D. (2006). Multiparameter assessments to determine the effects of sugars and antimicrobials on a polymicrobial oral biofilm. Applied and Environmental Microbiology, 72(10), 6734–6742. Doi: 10.1128/aem.01013-06
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Details

Primary Language English
Subjects Health Care Administration
Journal Section Research Article
Authors

Mutlu Keskin This is me 0000-0002-4929-800X

Publication Date January 31, 2020
Acceptance Date December 3, 2019
Published in Issue Year 2020 Volume: 2 Issue: 1

Cite

APA Keskin, M. (2020). A Comparative Analysis of Biofilm Characteristics of Dual-Species Periodontopathogenic Biofilm based on Fusobacterium nucleatum and the Dual- Species Biofilm Response in the Presence of Antimicrobial Peptide. Aurum Journal of Health Sciences, 2(1), 1-10.