Advertisement

Superantigens and Biofilms in Sinus Diseases

  • Fazilet Altin
  • Husamettin Yasar
  • Martin Desrosiers
Chapter

Abstract

Superantigens (SAgs) are a group of microbial antigens that are differentiated by various properties from normal protein or peptide antigens. SAgs are very potent T-cell mitogens that can stimulate T lymphocytes to proliferate at lower concentrations (0.1 pg/mL) than conventional antigens, resulting in fever, shock, and even death. SAgs are defined as pathogenic agents of a wide variety of diseases, such as toxic shock syndrome, Kawasaki disease, acute rheumatoid fever, food poisoning, as well as many autoimmune disorders. SAgs are recognized by T-cell receptors (TCRs), particularly with TCR beta-chains (Vß), but also with Dß, Jß, Vα, and Jα, and are also presented to T cells with the aid of class II major histocompatibility complex (MHC) molecules. During presentation, these SAgs bind to amino acid residues outside the peptide-binding domain. The binding of the SAgs to the class II molecules on antigen-presenting cells (APCs) and to the TCRs produces a strong stimulatory signal. SAgs are divided into two groups: exogenous and endogenous. Biofilms are organized, heterogeneous bacterial communities embedded in a complex extracellular polymeric substance (EPS). Biofilm formation can be in vivo, in living cells, or in vitro, on non-living surfaces. Biofilm provides bacteria for protection against host defense, mechanical trauma, and temperature changes. Although increased biofilms have been demonstrated in patients with cardiorenal syndrome (CRS), there is still uncertainty about their role in etiopathogenesis, therefore more thorough investigation is necessary to prevent CRS. Understanding of the role of biofilms in the pathogenesis of CRS, resolving communication among them, developing existing treatments, and breaking antibiotic resistance will result in beneficial outcomes for both patients and physicians.

Keywords

Superantigen Exogenous Endogenous Biofilm Antibiotic resistance 

References

  1. 1.
    White J, Herman A, Pullen AM, et al. The Vβ-specific superantigen staphylococcal enterotoxin B: stimulation of mature T cells and clonal deletion in neonatal mice. Cell. 1989;56(13):27–35.PubMedGoogle Scholar
  2. 2.
    Proft T, Fraser JD. Bacterial superantigens. Clin Exp Immunol. 2003;133:299–306.PubMedPubMedCentralGoogle Scholar
  3. 3.
    Bohach G, Fast D, Nelson R, et al. Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit Rev Microbiol. 1990;17:251–72.PubMedGoogle Scholar
  4. 4.
    Drake CG, Kotzin BL. Superantigens: biology, immunology, and potential role in disease. J Clin Immunol. 1992;12(3):149.PubMedGoogle Scholar
  5. 5.
    Herman A, Kappler J, Marrack P, et al. Superantigens: mechanism of T-cell stimulation and role in immune responses. Annu Rev Immunol. 1991;9:745–72.PubMedGoogle Scholar
  6. 6.
    Marrack P, Kappler J. The staphylococcal enterotoxins and their relatives. Science. 1990;248:705–11.PubMedGoogle Scholar
  7. 7.
    Fraser JD. Clarifying the mechanism of superantigen toxicity. PLoS Biol. 2011 Sep;9(9):e1001145.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Miethke T, Wahl C, Heeg K, et al. T cell-mediated lethal shock triggered in mice by the superantigen staphylococcal enterotoxin B. Critical role of tumor necrosis factor. J Exp Med. 1992;175:91–8.PubMedGoogle Scholar
  9. 9.
    Dellabona P, Peccoud J, Kappler J, et al. Superantigens interact with MHC class II molecules outside of the antigen groove. Cell. 1990;62:1115–21.PubMedGoogle Scholar
  10. 10.
    Seth A, Stern L, Ottenhoff T, et al. Binary and ternary complexes between T-cell receptor, class II MHC and superantigen in vitro. Nature. 1994;369:324–7.PubMedGoogle Scholar
  11. 11.
    Huber BT, Hsu PN, Sutkowski N. Virus-encoded superantigens. Microbiol Rev. 1996;60(3):473–82.PubMedPubMedCentralGoogle Scholar
  12. 12.
    Solanki LS, Srivastava N, Singh S. Superantigens: a brief review with special emphasis on dermatologic diseases. Dermatol Online J. 2008;14(2):3.PubMedGoogle Scholar
  13. 13.
    Acharya KR, Baker MD. Superantigen: structure-function relationships. Int J Med Microbiol. 2004;293:529–37.PubMedGoogle Scholar
  14. 14.
    Carnoy C, Loiez C, Faveeuw C, Grangette C, Desreumaux P, Simonet M. Impact of the Yersinia pseudotuberculosis-derived mitogen (YPM) on the murine immune system. In: Skurnik M, Bengoechea JA, Granfors K, editors. The genus Yersinia. Advances in experimental medicine and biology, vol. 529. Boston, MA: Springer; 2004.Google Scholar
  15. 15.
    Sissons JPG. Superantigens and infectious disease. Lancet. 1993;341:1627–8.PubMedGoogle Scholar
  16. 16.
    Murray DL, Earhart CA, et al. Localization of biologically important regions on toxic shock syndrome toxin 1. Infect Immun. 1996;64(1):371–4.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Kotb M. Bacterial pyrogenic exotoxins as superantigens. Clin Microbiol Rev. 1995;8(3):411–26.PubMedPubMedCentralGoogle Scholar
  18. 18.
    Plano LRW, Gutman DM, Woischnik M, Collins CM. Recombinant Staphylococcus aureus exfoliative toxins are not bacterial superantigens. Infect Immun. 2000;68(5):3048.PubMedPubMedCentralGoogle Scholar
  19. 19.
    Todd J, et al. Toxic-shock syndrome associated with phage-group-I staphylococci. Lancet. 1978;312(8100):1116–8.Google Scholar
  20. 20.
    Bergdoll MS, et al. A new staphylococcal enterotoxin, enterotoxin F, associated with toxic-shock syndrome Staphylococcus aureus isolates. Lancet. 1981;317(8228):1017–21.Google Scholar
  21. 21.
    Uchiyama T, Yan XJ, Imanishi K, Yagi J. Bacterialsuperantigens—mechanism of T cell activation by the superantigens and their role in the pathogenesis of infectious diseases. Microbiol Immunol. 1994;38(4):245–56.PubMedGoogle Scholar
  22. 22.
    McCormick J, Yarwood J, Schlievert P. Toxic shock syndrome and bacterial superantigens. An update. Annu Rev Microbiol. 2001;55:77–104.PubMedGoogle Scholar
  23. 23.
    Kelly FC, Dack GM. Experimental Staphylococcus food poisoning: a study of the growth of a food poisoning Staphylococcus and the production of an enterotoxic substance in bread and meat. Am J Public Health Nations Health. 1936 Nov;26(11):1077–82.PubMedPubMedCentralGoogle Scholar
  24. 24.
    Dack GM. Staphylococci in relation to food poisoning. Am J Public Health Nations Health. 1937 May;27(5):440–3.PubMedPubMedCentralGoogle Scholar
  25. 25.
    Denison GA. Epidemiology and symptomatology of Staphylococcus food poisoning: a report of recent outbreaks. Am J Public Health Nations Health. 1936;26(12):1168–75.PubMedPubMedCentralGoogle Scholar
  26. 26.
    Bergdoll MS, Wong L. A: staphylococcal intoxications. In: Foodborne intoxications. Amsterdam: Elsevier; 2006. p. 524–52.Google Scholar
  27. 27.
    Spaulding AR, Salgado-Pabón W, Kohler PL, Horswill AR, Leung DYM, Schlievert PM. Staphylococcal and streptococcal superantigen exotoxins. Clin Microbiol Rev. 2013;26(3):422–47.  https://doi.org/10.1128/CMR.00104-12.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Dick GF, Dick GH. Landmark article Jan 26, 1924: the etiology of scarlet fever. J Am Med Assoc. 1983;250(22):3096.Google Scholar
  29. 29.
    Proft T, Streptococcal Superantigens FJD. Biological properties and potential role in disease. In: Ferretti JJ, Stevens DL, Fischetti VA, editors. Streptococcus pyogenes: basic biology to clinical manifestations [Internet]. Oklahoma City, OK: University of Oklahoma Health Sciences Center; 2016. https://www.ncbi.nlm.nih.gov/books/NBK333435/.Google Scholar
  30. 30.
    Proft T, Fraser JD. Streptococcal superantigens. Chem Immunol Allergy. 2007;93:1–23.PubMedGoogle Scholar
  31. 31.
    Commons RJ, Smeesters PR, Proft T, Fraser JD, Robins-Browne R, Curtis N. Streptococcal superantigens: categorization and clinical associations. Trends Mol Med. 2014;20(1):48–62.  https://doi.org/10.1016/j.molmed.2013.10.004. Epub 2013 Nov 6.CrossRefPubMedGoogle Scholar
  32. 32.
    Cole BC, Griffiths MM. Triggering and exacerbation of autoimmune arthritis by the mycoplasma arthritidissuperantigen MAM. Arthritis Rheum. 1993;36:994–1002.PubMedGoogle Scholar
  33. 33.
    Ito Y, Abe J, Yoshino K, Takeda T, Koshaka T. Sequence analysis of the gene for a novel superantigen produced by Yersinia pseudotuberculosis and expression of the recombinant protein. J Immunol. 1995;154:5896–906.PubMedGoogle Scholar
  34. 34.
    Luo W, Yu H, Cao Z, Schoeb TR, Marron M, Dybvig K. Association of mycoplasma arthritidis mitogen with lethal toxicity but not with arthritis in mice. Infect Immun. 2008;76(11):4989–98.  https://doi.org/10.1128/IAI.00667-08.CrossRefPubMedPubMedCentralGoogle Scholar
  35. 35.
    Van Zele T, Gevaert P, Watelet JB, Claeys G, Holtappels G, Claeys C, et al. Staphylococcus aureus colonization and IgE antibody formation to enterotoxins is increased in nasal polyposis. J Allergy Clin Immunol. 2004;114(4):981–3.PubMedGoogle Scholar
  36. 36.
    Ou J, Wang J, Xu Y, Tao ZZ, Kong YG, Chen SM, Shi WD. Staphylococcus aureus superantigens are associated with chronic rhinosinusitis with nasal polyps: a meta-analysis. Eur Arch Otorhinolaryngol. 2014;271(10):2729–36.  https://doi.org/10.1007/s00405-014-2955-0. Epub 2014 Mar 7.CrossRefPubMedGoogle Scholar
  37. 37.
    Thunberg U, Hugosson S, Monecke S, Ehricht R, Söderquist B. Molecular characteristics of Staphylococcus aureus associated with chronic rhinosinusitis. APMIS. 2015;123(1):37–44.  https://doi.org/10.1111/apm.12299. Epub 2014 Aug 6.CrossRefPubMedGoogle Scholar
  38. 38.
    Van Zele T, Vaneechoutte M, Holtappels G, Gevaert P, van Cauwenberge P, Bachert C. Detection of enterotoxin DNA in Staphylococcus aureus strains obtained from the middle meatus in control sand nasal polyp patients. Am J Rhinol. 2008;22(3):223–7.PubMedGoogle Scholar
  39. 39.
    Kern RC, Conley DB, Walsh W, et al. Perspectives on the etiology of chronic rhinosinusitis: an immune barrier hypothesis. Am J Rhinol. 2008;22(6):549–59.  https://doi.org/10.2500/ajr.2008.22.3228.CrossRefPubMedPubMedCentralGoogle Scholar
  40. 40.
    Wang M, Shi P, Chen B, Zhang H, Jian J, Chen X, et al. The role of superantigens in chronic rhinosinusitis with nasal polyps. J Otorhinolaryngol Relat Spec. 2008;70(2):97–103.  https://doi.org/10.1159/000114532. Epub 2008 Apr 15.CrossRefGoogle Scholar
  41. 41.
    Seiberling KA, Conley DB, Tripathi A, Grammer LC, Shuh L, Haines GK 3rd, Schleimer R, Kern RC. Superantigens and chronic rhinosinusitis: detection of staphylococcal exotoxins in nasal polyps. Laryngoscope. 2005;115(9):1580–5.PubMedGoogle Scholar
  42. 42.
    Bernstein JM, Ballow M, Schlievert PM, Rich G, Allen C, Dryja D. A superantigen hypothesis for the pathogenesis of chronic hyperplastic sinusitis with massive nasal polyposis. Am J Rhinol. 2003;17(6):321–6.PubMedGoogle Scholar
  43. 43.
    Hall-Stoodley L, Stoodley P. Biofilm formation and dispersal and the transmission of human pathogens. Trends Microbiol. 2005;13:7–10. [erratum in Trends Microbiol. 2005;13: 300–301].PubMedGoogle Scholar
  44. 44.
    Sanglard D. Resistance of human fungal pathogens to antifungal drugs. Curr Opin Microbiol. 2002;5:379–85.PubMedGoogle Scholar
  45. 45.
    Harvey RJ, Lund VJ. Biofilms and chronic rhinosinusitis: systematic review of evidence, current concepts and directions for research. Rhinology. 2007;45(1):3–13.PubMedGoogle Scholar
  46. 46.
    Rajput A, Thakur A, Sharma S, Kumar M. aBiofilm: a resource of anti-biofilm agents and their potential implications in targeting antibiotic drug resistance. Nucleic Acids Res. 2017;46:D894.  https://doi.org/10.1093/nar/gkx1157.CrossRefPubMedCentralGoogle Scholar
  47. 47.
    Klausen M, Aaes-Jorgensen A, Molin S, Tolker-Nielsen T. Involvement of bacterial migration in the development of complex multicellular structures in Pseudomonas aeruginosa biofilms. Mol Microbiol. 2003;50:61–8.PubMedGoogle Scholar
  48. 48.
    Jamal M, et al. Bacterial biofilm and associated infections. J Chin Med Assoc. 2018;81:7–11 . pii: S1726–4901(17)30258–7.  https://doi.org/10.1016/j.jcma.2017.07.012.CrossRefPubMedGoogle Scholar
  49. 49.
    Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2:95–108.PubMedGoogle Scholar
  50. 50.
    Solano C, Echeverz M, Lasa I. Biofilm dispersion and quorum sensing. Curr Opin Microbiol. 2014;18:96–104.  https://doi.org/10.1016/j.mib.2014.02.008. Epub 2014 Mar 20.CrossRefPubMedGoogle Scholar
  51. 51.
    Donlan RM. Biofilms: microbial life on surfaces. Emerg Infect Dis. 2002;8(9):881–90.  https://doi.org/10.3201/eid0809.020063.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Donlan RM, Costerton JW. Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev. 2002;15(2):167–93.  https://doi.org/10.1128/CMR.15.2.167-193.2002.CrossRefPubMedPubMedCentralGoogle Scholar
  53. 53.
    Peters BM, Jabra-Rizk MA, O’May GA, Costerton JW, Shirtliff ME. Polymicrobial interactions: impact on pathogenesis and human disease. Clin Microbiol Rev. 2012;25(1):193–213.  https://doi.org/10.1128/CMR.00013-11.CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Ann Rev Microbiol. 2002;56:187–209.Google Scholar
  55. 55.
    Mahenthiralingam E, Campbell ME, Speert DP. Nonmotility and phagocytic resistance of Pseudomonas aeruginosa isolates from chronically colonized patients with cystic fibrosis. Infect Immun. 1994;62:596–605.PubMedPubMedCentralGoogle Scholar
  56. 56.
    Suh JD, Ramakrishnan V, Palmer JN. Biofilms. Otolaryngol Clin N Am. 2010;43(3):521–30.Google Scholar
  57. 57.
    Cryer J, Chipor I, Perioff JR, et al. Evidence of bacterial biofilms in human chronic sinusitis. J Otorhinolaryngol Relat Spec. 2004;66:155–8.Google Scholar
  58. 58.
    Sanclement JA, Webster P, Thomas J, et al. Bacterial biofilms in surgical specimens of patients with chronic rhinosinusitis. Laryngoscope. 2005;115:578–82.PubMedGoogle Scholar
  59. 59.
    Prince AA, Steiger JD, Khalid AN, et al. Prevalence of biofilm-forming bacteria inchronic rhinosinusitis. Am J Rhinol. 2008;22(3):239–45.PubMedGoogle Scholar
  60. 60.
    Sanderson AR, Leid JG, Hunsaker D. Bacterial biofilms on the sinus mucosa of human subjects with chronic rhinosinusitis. Laryngoscope. 2006;116:1121–6.PubMedGoogle Scholar
  61. 61.
    Zernotti ME, Angel Villegas N, Roques Revol M, Baena-Cagnani CE, Arce Miranda JE, Paredes ME et al. Evidence of bacterial biofilms in nasal polyposis. J Investig Allergol Clin Immunol. 2010;20(5):380–5.Google Scholar
  62. 62.
    Healy DY, Leid JG, Sanderson AR, et al. Biofilms in chronic rhinosinusitis. Otolaryngol Head Neck Surg. 2008;138(5):641–7.PubMedGoogle Scholar
  63. 63.
    Post JC, Stoodley P, Hall-Stoodley L, Ehrlich GD. The role of biofilms in otolaryngologic infections. Curr Opin Otolaryngol Head Neck Surg. 2004;12:185–90.PubMedGoogle Scholar
  64. 64.
    Desrosiers MY, Kilty SJ. Treatment alternatives for chronic rhinosinusitis persisting after ESS: what to do when antibiotics, steroids and surgery fail. Rhinology. 2008;46:3–14.PubMedGoogle Scholar
  65. 65.
    Hai PVT, Lidstone C, Wallwork B. The effect of endoscopic sinus surgery on bacterial biofilms in chronic rhinosinusitis. Otolaryngol Head Neck Surg. 2010;142(3_suppl):S27–32 . First Published March 1.PubMedGoogle Scholar
  66. 66.
    Uren B, Psaltis A, Wormald PJ. Nasal lavage with mupirocin for the treatment of surgically recalcitrant chronic rhinosinusitis. Laryngoscope. 2008;118(9):1677–80.PubMedGoogle Scholar
  67. 67.
    Ha KR, Psaltis AJ, Butcher AR, Wormald PJ, Tan LW. In vitro activity of mupirocin on clinical isolates of Staphylococcus aureus and its potential implications in chronic rhinosinusitis. Laryngoscope. 2008;118(3):535–40.PubMedGoogle Scholar
  68. 68.
    Desrosiers M, Bendouah Z, Barbeau J. Effectiveness of topical antibiotics on Staphylococcus aureus biofilm in vitro. Am J Rhinol. 2007;21(2):149–53.PubMedGoogle Scholar
  69. 69.
    Chiu AG, Antunes MB, Palmer JN, Cohen NA. Evaluation of the in vivo efficacy of topical tobramycin against Pseudomonas sinonasal biofilms. J Antimicrob Chemother. 2007;59(6):1130–4.PubMedGoogle Scholar
  70. 70.
    Suh JD, Ramakrishnan V, Chiu AG. The role of topical therapies in the treatment of chronic rhinosinusitis. Braz J Otorhinolaryngol. 2011;77(6):680–1.PubMedGoogle Scholar
  71. 71.
    Alandejani T, Marsan J, Ferris W, Slinger R, Chan F. Effectiveness of honey on Staphylococcus aureus and Pseudomonas aeruginosa biofilms. Otolaryngol Head Neck Surg. 2009;141(1):114–8.PubMedGoogle Scholar
  72. 72.
    Chennupati SK, Chiu AG, Tamashiro E, Banks CA, Cohen MB, Bleier BS, et al. Effects of an LL-37- derived antimicrobial peptide in an animal model of biofilm Pseudomonas sinusitis. Am J Rhinol Allergy. 2009;23(1):46–51.PubMedGoogle Scholar
  73. 73.
    Chiu AG, Palmer JN, Woodworth BA, Doghramji L, Cohen MB, Prince A, et al. Baby shampoo nasal irrigations for the symptomatic post-functioal endoscopic sinus surgery patient. Am J Rhinol. 2008;22(1):34–7.PubMedGoogle Scholar
  74. 74.
    Desrosiers M, Myntti M, James G. Methods for removing bacterial biofilms: in vitro study using clinical chronic rhinosinusitis specimens. Am J Rhinol. 2007;21(5):527–32.PubMedGoogle Scholar
  75. 75.
    Wallwork B, Coman W, Mackay-Sim A, Greiff L, Cervin A. A double-blind, randomized, placebo-controlledtrial of macrolide in the treatmentof chronic rhinosinusitis. Laryngoscope. 2006;116(2):189–93.PubMedGoogle Scholar
  76. 76.
    Tateda K, Comte R, Pechere JC, et al. Suppression of Pseudomonas aeruginosaquorum-sensing systems by macrolides: a promising strategy or an orientalmystery? J Infect Chemother. 2007;13(6):357–67.PubMedGoogle Scholar
  77. 77.
    Giacometti A, Cirioni O, Gov Y, Ghiselli R, Del Prete MS, Mocchegiani F, et al. RNA III inhibiting peptide inhibits in vivo biofilm formation by drug-resistant Staphylococcus aureus. Antimicrob Agents Chemother. 2003;47(6):1979–83.PubMedPubMedCentralGoogle Scholar
  78. 78.
    Stewart P, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet. 2001;358(9276):135–8.Google Scholar
  79. 79.
    Cross JL, Ramadan HH, Thomas JG. The impact of a cation channel blocker (furosemide) on Pseudomonas aeruginosa PAO1 biofilm architecture. Otolaryngol Head Neck Surg. 2007;137(1):21–6.PubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Fazilet Altin
    • 1
  • Husamettin Yasar
    • 1
  • Martin Desrosiers
    • 2
  1. 1.Department of OtorhinolaryngologyUniversity of Health Sciences, Haseki Training and Research HospitalIstanbulTurkey
  2. 2.Department of OtorhinolaryngologyMontreal University, Center HospitalMontrealCanada

Personalised recommendations