Skip to main content
SpringerLink
Log in

Suppression of Bacterial Adhesion: Modern Approaches, Problems, and Prospects

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The paper analyzes problems related to bacterial infections and modern approaches to the suppression of bacterial adhesion. The development of an infection depends upon the pathogen’s ability to colonize the surface of epithelial cells of the host organism and to reach the deeper tissues and organs. The initial stage in the development of any bacterial infection is manifested in pathogenic attachment—microbial adhesion to the surface of host cells. The adhesion specificity is due to the presence of complementary microbial structures and eukaryotic host cells sensitive to them. The development of infection may be stopped during any of its stages. To interrupt infection during the initial phase, i.e., adhesion, one promising solution is the use of various types of antiadhesive therapy (subinhibitory doses of antibacterial drugs, enzyme inhibitors, sugars, glycomimetics, peptide-like substances, cranberry juice, juniper extract, etc.). Adhesion may also be inhibited by the administration of vaccines that stimulate the production of specific antibodies to bacterial adhesins or ready-made antibodies in the form of commercial products containing antisera or immunoglobulins. The development of modern approaches to the interruption of microorganic adhesion with antiadhesive therapy agents is an efficient method for the treatment and prevention of bacterial infections, particularly those caused by microorganisms polyresistant to antimicrobial chemotherapeutical drugs.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

REFERENCES

  1. Almant, M., Moreau, V., Kovensky, J., et al., Clustering of Escherichia coli type-1 fimbrial adhesins by using multimeric heptyl α-dmannoside probes with a carbohydrate core, Clustering Chem., 2011, vol. 36, no. 17, pp. 10029–10038.

    Article  CAS  Google Scholar 

  2. Arciola, C.R., Speziale, P., and Montanaro, L., Perspectives on DNA vaccines. Targeting staphylococcal adhesins to prevent implant infections, J. Artif. Organs, 2009, vol. 32, no. 9, pp. 635–641.

    Article  CAS  Google Scholar 

  3. Braga, P.C., Sasso, M.D., and Sala, M.T., Sub-MIC concentrations of cefodizime interfere with various factors affecting bacterial virulence, J. Antimicrob. Chemother., 2000, vol. 45, no. 1, pp. 15–25.

    Article  CAS  PubMed  Google Scholar 

  4. Brannon, J.R. and Hadjifrangiskou, M., The arsenal of pathogens and antivirulence therapeutic strategies for disarming them, Drug. Des. Dev. Ther., 2016, vol. 10, pp. 1795–1806.

    CAS  Google Scholar 

  5. Bravo, D., Blondel, C.J., Hoare, A., et al., Type IV (B) pili are required for invasion but not for adhesion of Salmonella enterica serovar Typhi into BHK epithelial cells in a cystic fibrosis transmembrane conductance regulator-independent manner, Microb. Pathog., 2011, vol. 51, no. 5, pp. 373–377.

    Article  CAS  PubMed  Google Scholar 

  6. Burger, O., Ofek, I., Tabak, M., et al., A high molecular mass constituent of cranberry juice inhibits Helicobacter pylori adhesion to human gastric mucus, FEMS Immunol. Med. Microbiol., 2000, vol. 29, no. 4, pp. 295–301.

    Article  CAS  PubMed  Google Scholar 

  7. Burger, O., Weiss, E., Sharon, N., et al., Inhibition of Helicobacter pylori adhesion to human gastric mucus by a high-molecular-weight constituent of cranberry juice, Crit. Rev. Food Sci. Nutr., 2002, vol. 42, no. 3, pp. 279–284.

    Article  CAS  PubMed  Google Scholar 

  8. Cachia, P.J. and Hodges, R.S., Synthetic peptide vaccine and antibody therapeutic development: prevention and treatment of Pseudomonas aeruginosa,Biopolymers, 2003, vol. 71, no. 2, pp. 141–168.

    Article  CAS  PubMed  Google Scholar 

  9. Cho, J.A., Chinnapen, D.J., Aamar, E., et al., Insights on the trafficking and retro-translocation of glycosphingolipid-binding bacterial toxins, Front. Cell Infect. Microbiol., 2012, no. 2, p. 51.

  10. Chorell, E., Pinkner, J.S., Bengtsson, C., et al., Mapping pilicide anti-virulence effect in Escherichia coli, a comprehensive structure-activity study, Bioorg. Med. Chem., 2012, vol. 20, no. 9, pp. 3128–3142.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Dal, S.M., Bovio, C., Culici, M., and Braga, P.C., The combination of the SH metabolite of erdosteine (a mucoactive drug) and ciprofloxacin increases the inhibition of bacterial adhesiveness achieved by ciprofloxacin alone, Drugs Exp. Clin. Res., 2002, vol. 28, nos. 2–3, pp. 75–82.

    PubMed  Google Scholar 

  12. Escaich, S., Novel agents to inhibit microbial virulence and pathogenicity, Expert Opin. Ther. Pat., 2010, vol. 20, no. 10, pp. 1401–1418.

    Article  CAS  PubMed  Google Scholar 

  13. Frey, J., Biological safety concepts of genetically modified live bacterial vaccines, Vaccine, 2007, vol. 30, no. 25, pp. 5598–5605.

    Article  CAS  Google Scholar 

  14. Gao, X., Cai, K., Li, T., et al., Novel fusion protein protects against adherence and toxicity of enterohemorrhagic Escherichia coli O157:H7 in mice, Vaccine, 2011, vol. 38, no. 29, pp. 6656–6663.

    Article  CAS  Google Scholar 

  15. Gaudreau, M.C., Lacasse, P., and Talbot, B.G., Protective immune responses to a multi-gene DNA vaccine against Staphylococcus aureus,Vaccine, 2007, vol. 25, no. 5, pp. 814–824.

    Article  CAS  PubMed  Google Scholar 

  16. Ghosh, S., Chakraborty, K., Nagaraja, T., et al., An adhesion protein of Salmonella enterica serovar Typhi is required for pathogenesis and potential target for vaccine development, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, no. 8, pp. 3348–3353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Gomes, D.L., Peixoto, R.S., Barbosa, E.A., et al., SubMICs of penicillin and erythromycin enhance biofilm formation and hydrophobicity of Corynebacterium diphtheriae strains, J. Med. Microbiol., 2013, vol. 62, no. 5, pp. 754–760.

    Article  CAS  PubMed  Google Scholar 

  18. Hartlova, A., Cerveny, L., Hubalek, M., et al., Membrane rafts: a potential gateway for bacterial entry into host cells, Microbiol. Immunol., 2010, vol. 54, no. 4, pp. 237–245.

    Article  CAS  PubMed  Google Scholar 

  19. Hur, J. and Lee, J.H., Development of a novel live vaccine delivering enterotoxigenic Escherichia coli fimbrial antigens to prevent post-weaning diarrhea in piglets, Vet. Immunol. Immunopathol., 2012, vol. 146, nos. 3–4, pp. 283–288.

    Article  CAS  PubMed  Google Scholar 

  20. Hur, J., Stein, B.D., and Lee, J.H., A vaccine candidate for post-weaning diarrhea in swine constructed with a live attenuated Salmonella delivering Escherichia coli K88ab, K88ac, FedA, and FedF fimbrial antigens and its immune responses in a murine model, Can. J. Vet. Res., 2012, vol. 76, no. 3, pp. 186–194.

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Jantscher-Krenn, E., Zherebtsov, M., Nissan, C., et al., The human milk oligosaccharide disialyllacto-N-tetraose prevents necrotizing enterocolitis in neonatal rats, Gut, 2012, vol. 61, no. 10, pp. 1417–1425.

    Article  CAS  PubMed  Google Scholar 

  22. Kharseeva, G.G., Maskalenko, E.P., Alutina, E.L., and Brevdo, A.M., The effect of polyoxidonium on the adhesive properties of Corynebacterium diphtheriae,Zh. Mikrobiol., Epidemiol. Immunobiol., 2009, no. 2, pp. 11–15.

  23. Kharseeva, G.G., Frolova, Ya.N., and Mironov, A.Yu., Biofilms of pathogenic bacteria: biological properties and role in the chronicity of the infectious process, Usp. Sovrem. Biol., 2015, vol. 135, no. 4, pp. 346–354.

    Google Scholar 

  24. Klanĉnik, A., Zorko, Ŝ., Toplak, N., et al., Anti-adhesion activity of juniper (Juniperus communis L.) preparation against Campylobacter jejuni evaluated with PCR-based methods, Phytother. Res., 2018, vol. 32, no. 3, pp. 542–550.

    Article  PubMed  CAS  Google Scholar 

  25. Krachler, A.M. and Orth, K., Functional characterization of the interaction between bacterial adhesin multivalent adhesion molecule 7 (MAM7) protein and its host cell ligands, J. Biol. Chem., 2011, vol. 286, no. 45, pp. 38939–38947.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Krachler, A.M., Ham, H., and Orth, K., Outer membrane adhesion factor multivalent adhesion molecule 7 initiates host cell binding during infection by gram-negative pathogens, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, no. 28, pp. 11614–11619.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Krachler, A.M., Ham, H., and Orth, K., Turnabout is fair play: use of the bacterial multivalent adhesion molecule 7 as an antimicrobial agent, Virulence, 2012a, vol. 3, no. 1, pp. 68–71.

    Article  PubMed  PubMed Central  Google Scholar 

  28. Krachler, A.M., Mende, K., Murray, C., and Orth, K., In vitro characterization of multivalent adhesion molecule 7-based inhibition of multidrug-resistant bacteria isolated from wounded military personnel, Virulence, 2012b, vol. 3, no. 4, pp. 389–399.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Labrecque, J., Bodet, C., Chandad, F., and Grenier, D., Effects of a high-molecular-weight cranberry fraction on growth, biofilm formation and adherence of Porphyromonas gingivalis,J. Antimicrob. Chemother., 2006, vol. 58, no. 2, pp. 439–443.

    Article  CAS  PubMed  Google Scholar 

  30. Langermann, S., Palaszynski, S., and Barnhart, M., Prevention of mucosal Escherichia coli infection by FimH–adhesin-based systemic vaccination, Science, 1997, vol. 276, no. 5312, pp. 607–611.

    Article  CAS  PubMed  Google Scholar 

  31. Langermann, S., Möllby, R., and Burlein, J.E., Vaccination with FimH adhesin protects cynomolgus monkeys from colonization and infection by uropathogenic Escherichia coli,J. Infect. Dis., 2000, vol. 181, no. 2, pp. 774–778.

    Article  CAS  PubMed  Google Scholar 

  32. Leonov, V.V. and Mironov, A.Yu., Zhelezo i mikroorganizmy (Iron and Microorganisms), Khanty-Mansi: Pechatnyi Mir, 2016.

  33. Lillehoj, E.P., Kim, B.T., and Kim, K.C., Identification of Pseudomonas aeruginosa flagellin as an adhesin for Muc1 mucin, Am. J. Physiol., 2002, vol. 282, no. 4, pp. 751–756.

    Google Scholar 

  34. Lindén, S.K., Sheng, Y.H., Every, A.L., et al., MUC1 limits Helicobacter pylori infection both by steric hindrance and by acting as a releasable decoy, PLoS Pathog., 2009, vol. 5, no. 10, p. e1000617.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. Lorenzo-Gómez, M.F., Padilla-Fernández, B., García-Criado, F.J., et al., Evaluation of a therapeutic vaccine for the prevention of recurrent urinary tract infections versus prophylactic treatment with antibiotics, Int. Urogynecol. J., 2013, vol. 24, no. 1, pp. 127–134.

    Article  PubMed  Google Scholar 

  36. Mironov, A.Yu. and Leonov, V.V., Iron, virulence, and intermicrobial interactions of commensal microorganisms, Usp. Sovrem. Biol., 2016, vol. 136, no. 3, pp. 285–294.

    Google Scholar 

  37. O’May, C. and Tufenkji, N., The swarming motility of Pseudomonas aeruginosa is blocked by cranberry proanthocyanidins and other tannin-containing materials, Appl. Environ. Microbiol., 2011, vol. 77, no. 9, pp. 3061–3067.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Ofek, I., Hasty, D.L., and Sharon, N., Anti-adhesion therapy of bacterial diseases: prospects and problems, FEMS Immunol. Med. Microbiol., 2003, vol. 38, pp. 181–191.

    Article  CAS  PubMed  Google Scholar 

  39. Parker, P., Sando, L., Pearson, R., et al., Bovine Muc1 inhibits binding of enteric bacteria to Caco-2 cells, Glycoconjugate J., 2010, vol. 27, no. 1, pp. 89–97.

    Article  CAS  Google Scholar 

  40. Pastores, G.M., Barnett, N.L., and Kolodny, E.H., An open-label, noncomparative study of miglustat in type I Gaucher disease: efficacy and tolerability over 24 months of treatment, Clin. Ther., 2005, vol. 27, no. 8, pp. 1215–1227.

    Article  CAS  PubMed  Google Scholar 

  41. Pompilio, A., Catavitello, C., Picciani, C., et al., Subinhibitory concentrations of moxifloxacin decrease adhesion and biofilm formation of Stenotrophomonas maltophilia from cystic fibrosis, J. Med. Microbiol., 2010, vol. 59, no. 1, pp. 76–81.

    Article  CAS  PubMed  Google Scholar 

  42. Radin, N.S., Preventing the binding of pathogens to the host by controlling sphingolipid metabolism, Microbes Infect., 2006, vol. 8, no. 3, pp. 938–945.

    Article  CAS  PubMed  Google Scholar 

  43. Richards, S.J., Jones, M.W., Hunaban, M., et al., Probing bacterial-toxin inhibition with synthetic glycopolymers prepared by tandem post-polymerization modification: role of linker length and carbohydrate density, Angew. Chem. Int. Ed. Engl., 2012, vol. 51, no. 31, pp. 7812–7816.

    Article  CAS  PubMed  Google Scholar 

  44. Roberts, P.A., Huebinger, R.M., Keen, E., Krachler, A.-M., and Jabbari, S., Predictive modeling of a novel anti-adhesion therapy to combat bacterial colonization of burn wounds, PLoS Comput. Biol., 2018, vol. 14, no. 5, p. e1006071.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  45. Sharon, N., Carbohydrates as future anti-adhesion drugs for infectious diseases, Biochim. Biophys. Acta, Gen. Subj., 2006, vol. 1760, no. 4, pp. 527–537.

    Article  CAS  Google Scholar 

  46. Sheth, H.B., Glasier, L.M., Ellert, N.W., et al., Development of an anti-adhesive vaccine for Pseudomonas aeruginosa targeting the C-terminal region of the pilin structural protein, Biomed. Pept., Proteins Nucleic Acids, 1995, vol. 1, no. 3, pp. 141–148.

    CAS  Google Scholar 

  47. Shmuely, H., Ofek, I., Weiss, E.I., et al., Cranberry components for the therapy of infectious disease, Curr. Opin. Biotechnol., 2012, vol. 23, no. 2, pp. 148–152.

    Article  CAS  PubMed  Google Scholar 

  48. Shoaf-Sweeney, K.D. and Hutkins, R.W., Adherence, antiadherence, and oligosaccharides preventing pathogens from sticking to the host, Adv. Food Nutr. Res., 2009, vol. 55, pp. 101–161.

    Article  CAS  PubMed  Google Scholar 

  49. Spaulding, C.N., Klein, R.D., Ruer, S., et al., Selective depletion of uropathogenic E. coli from the gut by a FimH antagonist, Nature, 2017a, vol. 546, no. 7659, pp. 528–532.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Spaulding, A., Takrouri, K., Mahalingam, P., et al., Compound design guidelines for evading the efflux and permeation barriers of Escherichia coli with the oxazolidinone class of antibacterials: test case for a general approach to improving whole cell gram-negative activity, Bioorg. Med. Chem. Lett., 2017b, vol. 27, no. 23, pp. 5310–5321.

    Article  CAS  PubMed  Google Scholar 

  51. Svensson, M., Frendeus, B., Butters, T., et al., Glycolipid depletion in antimicrobial therapy, Mol. Microbiol., 2003, vol. 47, no. 2, pp. 453–461.

    Article  CAS  PubMed  Google Scholar 

  52. Svensson, M., Platt, F.M., and Svanborg, C., Glycolipid receptor depletion as an approach to specific antimicrobial therapy, FEMS Microbiol. Lett., 2006, vol. 258, no. 1, pp. 1–8.

    Article  CAS  PubMed  Google Scholar 

  53. Therrien, R., Lacasse, P., Grondin, G., Talbot B.G. Lack of protection of mice against Staphylococcus aureus despite a significant immune response to immunization with a DNA vaccine encoding collagen-binding protein, Vaccine, 2007, vol. 25, no. 7, pp. 5053–5061.

    Article  CAS  PubMed  Google Scholar 

  54. Toivanen, M., Ryynänen, A., Huttunen, S., et al., Binding of Neisseria meningitidis pili to berry polyphenolic fractions, J. Agric. Food Chem., 2009, vol. 57, no. 8, pp. 3120–3127.

    Article  CAS  PubMed  Google Scholar 

  55. Vorob’ev, A.A., Mironov, A.Yu., Nesvizhskii, Yu.V., and Nechaev, D.N., Uchenie ob infektsii (The Theory about Infection), Vorob’ev, A.A., Ed., Moscow: Russkii Vrach, 2000.

  56. Wagner, C. and Hensel, M., Adhesive mechanisms of Salmonella enterica,Adv. Exp. Med. Biol., 2011, vol. 715, pp. 17–34.

    Article  CAS  PubMed  Google Scholar 

  57. Wizemann, T.M., Adamou, J.E., and Langermann, S., Adhesins as targets for vaccine development, Emerging Infect. Dis., 1999, vol. 5, no. 3, pp. 395–403.

    Article  CAS  Google Scholar 

  58. Wojnicz, D. and Jankowski, S., Effects of subinhibitory concentrations of amikacin and ciprofloxacin on the hydrophobicity and adherence to epithelial cells of uropathogenic Escherichia coli strains, Int. J. Antimicrob. Agents, 2007, vol. 29, no. 6, pp. 700–704.

  59. Younson, J. and Kelly, C., The rational design of an anticaries peptide against Streptococcus mutans, Mol. Diversisty, 2004, vol. 8, no. 2, pp. 121–126.

  60. Zaporozhets, T.S., Makarenkova, I.D., Bakunina, I.Yu., et al., Inhibition of adhesion of C. diphtheriae to human buccal epithelium by glycolysis hydrolases from marine aquatic organisms, Biomed. Khim., 2010, vol. 56, no. 3, pp. 350–358.

    Article  CAS  Google Scholar 

  61. Zhang, C. and Zhang, W., Escherichia coli K88ac fimbriae expressing heat-labile and heat-stable (STa) toxin epitopes elicit antibodies that neutralize cholera toxin and STa toxin and inhibit adherence of K88ac fimbrial E. coli,Clin. Vaccine Immunol., 2010, vol. 17, no. 12, pp. 1859–1867.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Rostov-on-Don State Medical University, Ministry of Health of Russia, Rostov-on-Don, Russia

    G. G. Kharseeva & A. A. Alieva

  2. Gabrichevsky Moscow Research Institute of Epidemiology and Microbiology, Federal Service of Surveillance on Consumer Rights Protection and Human Wellbeing, Moscow, Russia

    A. Yu. Mironov

Authors
  1. G. G. Kharseeva
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Yu. Mironov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. A. Alieva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to G. G. Kharseeva.

Ethics declarations

Conflict of interests. The authors declare that they have no conflicts of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kharseeva, G.G., Mironov, A.Y. & Alieva, A.A. Suppression of Bacterial Adhesion: Modern Approaches, Problems, and Prospects. Biol Bull Rev 10, 158–165 (2020). https://doi.org/10.1134/S2079086420020036

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086420020036

Keywords

Search

Navigation