Skip to main content

Advertisement

SpringerLink
Log in

Staphylococcus aureus genomic pattern and atopic dermatitis: may factors other than superantigens be involved?

  • Article
  • Published:
European Journal of Clinical Microbiology & Infectious Diseases Aims and scope Submit manuscript

Abstract

The purpose of this investigation was to compare the genotypic profiles of Staphylococcus aureus isolated from atopic dermatitis (AD) patients and from control subjects, and to study the relationship between clinical severity, immune response, and genomic pattern of S. aureus isolated from AD patients. We selected 32 patients with AD and S. aureus skin colonization and 31 atopic controls with no history of AD who where asymptomatic carriers of S. aureus. Microarray-based genotyping was performed on S. aureus isolates. In AD patients, clinical severity was assessed using the Scoring Atopic Dermatitis index and total IgE levels and staphylococcal superantigen-specific IgE levels (SEA, SEB, SEC, TSST1) were determined. The genes lukE, lukD, splA, splB, ssl8, and sasG were more frequent in isolates from AD patients. CC30 was more common in isolates from atopic controls than in AD patients. There was a correlation between total IgE and clinical severity, but an association between clinical severity, immune response, and the presence of S. aureus superantigen genes, including enterotoxin genes, could not be demonstrated. Finally, a correlation was found between AD severity and other S. aureus genes, such as sasG and scn. S. aureus factors besides superantigens could be related to the worsening and onset of AD.

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.

Fig. 1

Similar content being viewed by others

References

  1. Ong PY, Leung DY (2010) The infectious aspects of atopic dermatitis. Immunol Allergy Clin North Am 30:309–321

    Article  PubMed Central  PubMed  Google Scholar 

  2. Lebon A, Labout JA, Verbrugh HA, Jaddoe VW, Hofman A, van Wamel WJ, van Belkum A, Moll HA (2009) Role of Staphylococcus aureus nasal colonization in atopic dermatitis in infants: the generation R study. Arch Pediatr Adolesc Med 163:745–749

    Article  PubMed  Google Scholar 

  3. Kim DW, Park JY, Park KD, Kim TH, Lee WJ, Lee SJ, Kim J (2009) Are there predominant strains and toxins of Staphylococcus aureus in atopic dermatitis patients? Genotypic characterization and toxin determination of S. aureus isolated in adolescent and adult patients with atopic dermatitis. J Dermatol 36:75–81

    Article  CAS  PubMed  Google Scholar 

  4. Yeung M, Balma-Mena A, Shear N, Simor A, Pope E, Walsh S, McGavin MJ (2011) Identification of major clonal complexes and toxin producing strains among Staphylococcus aureus associated with atopic dermatitis. Microbes Infect 13:189–197

    Article  CAS  PubMed  Google Scholar 

  5. Lomholt H, Andersen KE, Kilian M (2005) Staphylococcus aureus clonal dynamics and virulence factors in children with atopic dermatitis. J Invest Dermatol 125:977–982

    Article  CAS  PubMed  Google Scholar 

  6. Lin YT, Shau WY, Wang LF, Yang YH, Hwang YW, Tsai MJ, Tsao PN, Chiang BL (2000) Comparison of serum specific IgE antibodies to staphylococcal enterotoxins between atopic children with and without atopic dermatitis. Allergy 55:641–646

    Article  CAS  PubMed  Google Scholar 

  7. Zollner TM, Wichelhaus TA, Hartung A, Von Mallinckrodt C, Wagner TOF, Brade V, Kaufmann R (2000) Colonization with superantigen-producing Staphylococcus aureus is associated with increased severity of atopic dermatitis. Clin Exp Allergy 30:994–1000

    Article  CAS  PubMed  Google Scholar 

  8. Schlievert PM, Case LC, Strandberg KL, Abrams BB, Leung DY (2008) Superantigen profile of Staphylococcus aureus isolates from patients with steroid-resistant atopic dermatitis. Clin Infect Dis 46:1562–1567

    Article  PubMed Central  PubMed  Google Scholar 

  9. Oranje AP, Glazenburg EJ, Wolkerstorfer A, de Waard-van der Spek FB (2007) Practical issues on interpretation of scoring atopic dermatitis: the SCORAD index, objective SCORAD and the three-item severity score. Br J Dermatol 157:645–648

    Article  CAS  PubMed  Google Scholar 

  10. Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, Kadlec K, Kearns A, Laurent F, O’Brien FG, Pearson J, Ruppelt A, Schwarz S, Scicluna E, Slickers P, Tan HL, Weber S, Ehricht R (2011) A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 6:e17936

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  11. Monecke S, Slickers P, Ehricht R (2008) Assignment of Staphylococcus aureus isolates to clonal complexes based on microarray analysis and pattern recognition. FEMS Immunol Med Microbiol 53:237–251

    Article  CAS  PubMed  Google Scholar 

  12. Paganelli R, Ansotegui IJ, Sastre J, Lange CE, Roovers MH, de Groot H, Lindholm NB, Ewan PW (1998) Specific IgE antibodies in the diagnosis of atopic disease. Clinical evaluation of a new in vitro test system, UniCAP, in six European allergy clinics. Allergy 53:763–768

    Article  CAS  PubMed  Google Scholar 

  13. Boguniewicz M, Leung DY (2010) Recent insights into atopic dermatitis and implications for management of infectious complications. J Allergy Clin Immunol 125:4–13

    Article  PubMed Central  PubMed  Google Scholar 

  14. Corrigan RM, Rigby D, Handley P, Foster TJ (2007) The role of Staphylococcus aureus surface protein SasG in adherence and biofilm formation. Microbiology 153:2435–2446

    Article  CAS  PubMed  Google Scholar 

  15. Geoghegan JA, Corrigan RM, Gruszka DT, Speziale P, O’Gara JP, Potts JR, Foster TJ (2010) Role of surface protein SasG in biofilm formation by Staphylococcus aureus. J Bacteriol 192:5663–5673

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Garcia BL, Summers BJ, Ramyar KX, Tzekou A, Lin Z, Ricklin D, Lambris JD, Laity JH, Geisbrecht BV (2013) A structurally dynamic N-terminal helix is a key functional determinant in staphylococcal complement inhibitor (SCIN) proteins. J Biol Chem 288:2870–2881

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Holtfreter S, Grumann D, Schmudde M, Nguyen HTT, Eichler P, Strommenger B, Kopron K, Kolata J, Giedrys-Kalemba S, Steinmetz I, Witte W, Bröker BM (2007) Clonal distribution of superantigen genes in clinical Staphylococcus aureus isolates. J Clin Microbiol 45:2669–2680

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Argudín MA, Mendoza MC, Méndez FJ, Martín MC, Guerra B, Rodicio MR (2009) Clonal complexes and diversity of exotoxin gene profiles in methicillin-resistant and methicillin-susceptible Staphylococcus aureus isolates from patients in a spanish Hospital. J Clin Microbiol 47:2097–2105

    Article  PubMed Central  PubMed  Google Scholar 

  19. Nomura I, Tanaka K, Tomita H, Katsunuma T, Ohya Y, Ikeda N, Takeda T, Saito H, Akasawa A (1999) Evaluation of the staphylococcal exotoxins and their specific IgE in childhood atopic dermatitis. J Allergy Clin Immunol 104:441–446

    Article  CAS  PubMed  Google Scholar 

  20. Tomi NS, Kränke B, Aberer E (2005) Staphylococcal toxins in patients with psoriasis, atopic dermatitis, and erythroderma, and in healthy control subjects. J Am Acad Dermatol 53:67–72

    Article  PubMed  Google Scholar 

  21. Akiyama H, Toi Y, Kanzaki H, Tada J, Arata J (1996) Prevalence of producers of enterotoxins and toxic shock syndrome toxin-1 among Staphylococcus aureus strains isolated from atopic dermatitis lesions. Arch Dermatol Res 288:418–420

    Article  CAS  PubMed  Google Scholar 

  22. Kozman A, Yao Y, Bina P, Saha C, Yao W, Kaplan MH, Travers JB (2010) Encoding a superantigen by Staphylococcus aureus does not affect clinical characteristics of infected atopic dermatitis lesions. Br J Dermatol 163:1308–1311

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Bunikowski R, Mielke ME, Skarabis H, Worm M, Anagnostopoulos I, Kolde G, Wahn U, Renz H (2000) Evidence for a disease-promoting effect of Staphylococcus aureus-derived exotoxins in atopic dermatitis. J Allergy Clin Immunol 105:814–819

    Article  CAS  PubMed  Google Scholar 

  24. Pascolini C, Sinagra J, Pecetta S, Bordignon V, De Santis A, Cilli L, Cafiso V, Prignano G, Capitanio B, Passariello C, Stefani S, Cordiali-Fei P, Ensoli F (2011) Molecular and immunological characterization of Staphylococcus aureus in pediatric atopic dermatitis: implications for prophylaxis and clinical management. Clin Dev Immunol 2011:e718708

    Article  Google Scholar 

  25. Monecke S, Luedicke C, Slickers P, Ehricht R (2009) Molecular epidemiology of Staphylococcus aureus in asymptomatic carriers. Eur J Clin Microbiol Infect Dis 28:1159–1165

    Article  CAS  PubMed  Google Scholar 

  26. Lo WT, Wang SR, Tseng MH, Huang CF, Chen SJ, Wang CC (2010) Comparative molecular analysis of meticillin-resistant Staphylococcus aureus isolates from children with atopic dermatitis and healthy subjects in Taiwan. Br J Dermatol 162:1110–1116

    Article  PubMed  Google Scholar 

  27. McCarthy AJ, Lindsay JA (2010) Genetic variation in Staphylococcus aureus surface and immune evasion genes is lineage associated: implications for vaccine design and host–pathogen interactions. BMC Microbiol 10:173

    Article  PubMed Central  PubMed  Google Scholar 

  28. Melles DC, Gorkink RF, Boelens HA, Snijders SV, Peeters JK, Moorhouse MJ, van der Spek PJ, van Leeuwen WB, Simons G, Verbrugh HA, van Belkum A (2004) Natural population dynamics and expansion of pathogenic clones of Staphylococcus aureus. J Clin Invest 114:1732–1740

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  29. Capoluongo E, Giglio AA, Lavieri MM, Lesnoni-La Parola I, Ferraro C, Cristaudo A, Belardi M, Leonetti F, Mastroianni A, Cambieri A, Amerio P, Ameglio F (2001) Genotypic and phenotypic characterization of Staphylococcus aureus strains isolated in subjects with atopic dermatitis. Higher prevalence of exfoliative B toxin production in lesional strains and correlation between the markers of disease intensity and colonization density. J Dermatol Sci 26:145–155

    Article  CAS  PubMed  Google Scholar 

  30. Wüthrich B (1978) Serum IgE in atopic dermatitis: relationship to severity of cutaneous involvement and course of disease as well as coexistence of atopic respiratory diseases. Clin Allergy 8:241–248

    Article  PubMed  Google Scholar 

  31. Breuer K, Wittmann M, Bösche B, Kapp A, Werfel T (2000) Severe atopic dermatitis is associated with sensitization to staphylococcal enterotoxin B (SEB). Allergy 55:551–555

    Article  CAS  PubMed  Google Scholar 

  32. Guzik TJ, Bzowska M, Kasprowicz A, Czerniawska-Mysik G, Wójcik K, Szmyd D, Adamek-Guzik T, Pryjma J (2005) Persistent skin colonization with Staphylococcus aureus in atopic dermatitis: relationship to clinical and immunological parameters. Clin Exp Allergy 35:448–455

    Article  CAS  PubMed  Google Scholar 

  33. Cho SH, Strickland I, Tomkinson A, Fehringer AP, Gelfand EW, Leung DY (2001) Preferential binding of Staphylococcus aureus to skin sites of Th2-mediated inflammation in a murine model. J Invest Dermatol 116:658–663

    Article  CAS  PubMed  Google Scholar 

  34. Leung DY, Harbeck R, Bina P, Reiser RF, Yang E, Norris DA, Hanifin JM, Sampson HA (1993) Presence of IgE antibodies to staphylococcal exotoxins on the skin of patients with atopic dermatitis. Evidence for a new group of allergens. J Clin Invest 92:1374–1380

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. Baker BS (2006) The role of microorganisms in atopic dermatitis. Clin Exp Immunol 144:1–9

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  36. Nissen D, Pedersen LJ, Skov PS, Vejlsgaard GL, Poulsen LK, Jarløv JO, Karlsmark T, Nolte H (1997) IgE-binding components of staphylococcal enterotoxins in patients with atopic dermatitis. Ann Allergy Asthma Immunol 79:403–408

    Article  CAS  PubMed  Google Scholar 

  37. Ide F, Matsubara T, Kaneko M, Ichiyama T, Mukouyama T, Furukawa S (2004) Staphylococcal enterotoxin-specific IgE antibodies in atopic dermatitis. Pediatr Int 46:337–341

    Article  CAS  PubMed  Google Scholar 

  38. Arkwright PD, Cookson BD, Haeney MR, Sanyal D, Potter MR, David TJ (2001) Children with atopic dermatitis who carry toxin-positive Staphylococcus aureus strains have an expansion of blood CD5-B lymphocytes without an increase in disease severity. Clin Exp Immunol 125:184–189

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Mempel M, Lina G, Hojka M, Schnopp C, Seidl HP, Schäfer T, Ring J, Vandenesch F, Abeck D (2003) High prevalence of superantigens associated with the egc locus in Staphylococcus aureus isolates from patients with atopic eczema. Eur J Clin Microbiol Infect Dis 22:306–309

    CAS  PubMed  Google Scholar 

  40. Roche FM, Meehan M, Foster TJ (2003) The Staphylococcus aureus surface protein SasG and its homologues promote bacterial adherence to human desquamated nasal epithelial cells. Microbiology 149:2759–2767

    Article  CAS  PubMed  Google Scholar 

  41. Kuroda M, Ito R, Tanaka Y, Yao M, Matoba K, Saito S, Tanaka I, Ohta T (2008) Staphylococcus aureus surface protein SasG contributes to intercellular autoaggregation of Staphylococcus aureus. Biochem Biophys Res Commun 377:1102–1106

    Article  CAS  PubMed  Google Scholar 

  42. Chen H, Ricklin D, Hammel M, Garcia BL, McWhorter WJ, Sfyroera G, Wu YQ, Tzekou A, Li S, Geisbrecht BV, Woods VL Jr, Lambris JD (2010) Allosteric inhibition of complement function by a staphylococcal immune evasion protein. Proc Natl Acad Sci U S A 107:17621–17626

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Jongerius I, Puister M, Wu J, Ruyken M, van Strijp JAG, Rooijakkers SHM (2010) Staphylococcal complement inhibitor modulates phagocyte responses by dimerization of convertases. J Immunol 184:420–425

    Article  CAS  PubMed  Google Scholar 

  44. Verkaik NJ, Benard M, Boelens HA, de Vogel CP, Nouwen JL, Verbrugh HA, Melles DC, van Belkum A, van Wamel WJ (2011) Immune evasion cluster-positive bacteriophages are highly prevalent among human Staphylococcus aureus strains, but they are not essential in the first stages of nasal colonization. Clin Microbiol Infect 17:343–348

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

S. Monecke is an employee of Alere Technologies GmbH, Jena, Germany. A. Rojo, A. Aguinaga, J.R. Yuste, G. Gastaminza, and A. España have no conflicts of interest to declare.

Author information

Authors and Affiliations

  1. Department of Clinical Microbiology, Clínica Universidad de Navarra, Avenida. Pio XII nº36, 31008, Pamplona, Spain

    A. Rojo & A. Aguinaga

  2. Institute for Medical Microbiology and Hygiene, Dresden University of Technology, 01307, Dresden, Germany

    S. Monecke

  3. Alere Technologies GmbH, 07749, Jena, Germany

    S. Monecke

  4. Division of Infectious Diseases, Clínica Universidad de Navarra, Avenida. Pio XII nº36, 31008, Pamplona, Spain

    J. R. Yuste

  5. Department of Allergology, Clínica Universidad de Navarra, Avenida. Pio XII nº36, 31008, Pamplona, Spain

    G. Gastaminza

  6. Department of Dermatology, Clínica Universidad de Navarra, Avenida. Pio XII nº36, 31008, Pamplona, Spain

    A. España

Authors
  1. A. Rojo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. Aguinaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. Monecke
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J. R. Yuste
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. G. Gastaminza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. A. España
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. Rojo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rojo, A., Aguinaga, A., Monecke, S. et al. Staphylococcus aureus genomic pattern and atopic dermatitis: may factors other than superantigens be involved?. Eur J Clin Microbiol Infect Dis 33, 651–658 (2014). https://doi.org/10.1007/s10096-013-2000-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10096-013-2000-z

Keywords

Search

Navigation