Role of bacterial superantigens in atopic dermatitis: Implications for future therapeutic strategies

American Journal of Clinical Dermatology

Volumn 7, Issue 5, 2006, Pages 273-279

  Cardona, Ivan D ^a   Sang, Hyun Cho ^b   Leung, Donald Y M ^a,c  

^a NATIONAL JEWISH MEDICAL AND RESEARCH CENTER   (United States)

^b The Catholic University of Korea   (South Korea)

^c UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFECTIVE AGENT; ANTIINFLAMMATORY AGENT; AZITHROMYCIN; CALCINEURIN INHIBITOR; CATHELICIDIN; CEFALEXIN; CEFUROXIME AXETIL; CEPHALOSPORIN; CERAMIDE; CHLORHEXIDINE; CLARITHROMYCIN; CLINDAMYCIN; CLOXACILLIN; CORTICOSTEROID; COTRIMOXAZOLE; CRYSTAL VIOLET; CYTOKINE RECEPTOR ANTAGONIST; DICLOXACILLIN; ERYTHROMYCIN; FUSIDIC ACID; IMMUNOGLOBULIN E; IMMUNOGLOBULIN E ANTIBODY; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; OXACILLIN; PSEUDOMONIC ACID; SPHINGOLIPID; SUPERANTIGEN; TACROLIMUS; TRICLOSAN; UNINDEXED DRUG;

ATOPIC DERMATITIS; BACTERIAL COLONIZATION; BACTERIUM ADHERENCE; CELL HOMING; COMBINATION CHEMOTHERAPY; HELPER CELL; HUMAN; IMMUNOGLOBULIN PRODUCTION; IMMUNOREACTIVITY; INNATE IMMUNITY; LYMPHOCYTE MIGRATION; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS; MONOTHERAPY; NONHUMAN; PATHOGENESIS; PHOTOTHERAPY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SKIN INFLAMMATION; STAPHYLOCOCCUS AUREUS; STAPHYLOCOCCUS INFECTION; ANIMAL; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; MICROBIOLOGY; MULTIMODALITY CANCER THERAPY;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTI-INFLAMMATORY AGENTS; COMBINED MODALITY THERAPY; DERMATITIS, ATOPIC; HUMANS; LYMPHOCYTE ACTIVATION; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; SUPERANTIGENS;

EID: 34249336624     PISSN: 11750561     EISSN: None     Source Type: Journal    
DOI: 10.2165/00128071-200607050-00001     Document Type: Review

References (76)

1. Leung DY, Meissner HC, Fulton DR, et al. Toxic shock syndrome toxin-secreting Staphylococcus aureus in Kawasaki syndrome. Lancet 1993 Dec 4; 342 (8884): 1385-8
2. Leyden JJ, Marples RR, Kligman AM. Staphylococcus aureus in the lesions of atopic dermatitis. Br J Dermatol 1974 May; 90 (5): 525-30
3. Dahl MV. Staphylococcus aureus and atopic dermatitis. Arch Dermatol 1983 Oct; 119 (10): 840-6
4. Aly R, Maibach HI, Shinefield HR. Microbial flora of atopic dermatitis. Arch Dermatol 1977 Jun; 113 (6): 780-2
5. Marrack P, Kappler J. The staphylococcal enterotoxins and their relatives. Science 1990 Jun 1; 248 (4959): 1066
6. Hauk PJ, Hamid QA, Chrousos GP, et al. Induction of corticosteroid insensitivity in human PBMCs by microbial superantigens. J Allergy Clin Immunol 2000 Apr; 105 (4): 782-7
7. Hauk PJ, Leung DY. Tacrolimus (FK506): new treatment approach in superantigen-associated diseases like atopic dermatitis? J Allergy Clin Immunol 2001 Feb; 107 (2): 391-2
8. Bax R, Bywater R, Cornaglia G, et al. Surveillance of antimicrobial resistance: what, how and whither? Clin Microbiol Infect 2001 Jun; 7 (6): 316-25
9. Heritage J, Wilcox M, Sandoe J. Antimicrobial resistance potential. Lancet 2001 Sep 29; 358 (9287): 1099-100
10. Zetola N, Francis JS, Nuermberger EL, et al. Community-acquired methicillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis 2005 May; 5 (5): 275-86
11. Fridkin SK, Hageman JC, Morrison M, et al. Methicillin-resistant Staphylococcus aureus disease in three communities. N Engl J Med 2005 Apr 7; 352 (14): 1436-44
12. Leung DY. Infection in atopic dermatitis. Curr Opin Pediatr 2003 Aug; 15 (4): 399-404
13. Chu D, Haake A, Holbrook K, et al. The structure and development of skin. In: Freedberg IM, Eisen AZ, Wolff K, et al., editors. Fitzpatrick's dermatology in general medicine. New York: McGraw-Hill, 2003: 58-88
14. Leung DY. Atopic dermatitis and the immune system: the role of superantigens and bacteria. J Am Acad Dermatol 2001 Jul; 45 (1 Suppl.): S13-6
15. Cho SH, Strickland I, Boguniewicz M, et al. Fibronectin and fibrinogen contribute to the enhanced binding of Staphylococcus aureus to atopic skin. J Allergy Clin Immunol 2001 Aug; 108 (2): 269-74
16. Akiyama H, Hamada T, Huh WK, et al. Confocal laser scanning microscopic observation of glycocalyx production by Staphylococcus aureus in skin lesions of bullous impetigo, atopic dermatitis and pemphigus foliaceus. Br J Dermatol 2003 Mar; 148 (3): 526-32
17. Morishita Y, Tada J, Sato A, et al. Possible influences of Staphylococcus aureus on atopic dermatitis: the colonizing features and the effects of staphylococcal enterotoxins. Clin Exp Allergy 1999 Aug; 29 (8): 1110-7
18. Arikawa J, Ishibashi M, Kawashima M, et al. Decreased levels of sphingosine, a natural antimicrobial agent, may be associated with vulnerability of the stratum corneum from patients with atopic dermatitis to colonization by Staphylococcus aureus. J Invest Dermatol 2002 Aug; 119 (2): 433-9
19. Mempel M, Schmidt T, Weidinger S, et al. Role of Staphylococcus aureus surface-associated proteins in the attachment to cultured HaCaT keratinocytes in a new adhesion assay. J Invest Dermatol 1998 Sep; 111 (3): 452-6
20. Postlethwaite AE, Holness MA, Katai H, et al. Human fibroblasts synthesize elevated levels of extracellular matrix proteins in response to interleukin 4. J Clin Invest 1992 Oct; 90 (4): 1479-85
21. Christophers E, Henseler T. Contrasting disease patterns in psoriasis and atopic dermatitis. Arch Dermatol Res 1987; 279 Suppl.: S48-51
22. Grice K, Sattar H, Baker H, et al. The relationship of transepidermal water loss to skin temperature in psoriasis and eczema. J Invest Dermatol 1975 May; 64 (5): 313-5
23. Nomura I, Goleva E, Howell MD, et al. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J Immunol 2003 Sep 15; 171 (6): 3262-9
24. Ong PY, Ohtake T, Brandt C, et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N Engl J Med 2002 Oct 10; 347 (15): 1151-60
25. Gallo RL, Murakami M, Ohtake T, et al. Biology and clinical relevance of naturally occurring antimicrobial peptides. J Allergy Clin Immunol 2002 Dec; 110 (6): 823-31
26. Howell MD, Novak N, Bieber T, et al. Interleukin-10 downregulates anti-microbial peptide expression in atopic dermatitis. J Invest Dermatol 2005 Oct; 125 (4): 738-45
27. Laouini D, Kawamoto S, Yalcindag A, et al. Epicutaneous sensitization with superantigen induces allergic skin inflammation. J Allergy Clin Immunol 2003 Nov; 112 (5): 981-7
28. Lin YT, Wang CT, Hsu CT, et al. Differential susceptibility to staphylococcal superantigen (SsAg)-induced apoptosis of CD4+ T cells from atopic dermatitis patients and healthy subjects: the inhibitory effect of IL-4 on SsAg-induced apoptosis. J Immunol 2003 Jul 15; 171 (2): 1102-8
29. Leung DY, Soter NA. Cellular and immunologic mechanisms in atopic dermatitis. J Am Acad Dermatol 2001 Jan; 44 (1 Suppl.): S1-12
30. Travers JB, Norris DA, Leung DY. The keratinocyte as a target for staphylococcal bacterial toxins. J Investig Dermatol Symp Proc 2001 Dec; 6 (3): 225-30
31. Yarwood JM, Leung DY, Schlievert PM. Evidence for the involvement of bacterial superantigens in psoriasis, atopic dermatitis, and Kawasaki syndrome. FEMS Microbiol Lett 2000 Nov 1; 192 (1): 1-7
32. Zollner TM, Wichelhaus TA, Hartung A, et al. Colonization with superantigen-producing Staphylococcus aureus is associated with increased severity of atopic dermatitis. Clin Exp Allergy 2000 Jul; 30 (7): 994-1000
33. Taskapan MO, Kumar P. Role of staphylococcal superantigens in atopic dermatitis: from colonization to inflammation. Ann Allergy Asthma Immunol 2000 Jan; 84 (1): 3-10
34. Strickland I, Hauk PJ, Trumble AE, et al. Evidence for superantigen involvement in skin homing of T cells in atopic dermatitis. J Invest Dermatol 1999 Feb; 112 (2): 249-53
35. Bunikowski R, Mielke M, Skarabis H, et al. Prevalence and role of serum IgE antibodies to the Staphylococcus aureus-derived superantigens SEA and SEB in children with atopic dermatitis. J Allergy Clin Immunol 1999 Jan; 103 (1 Pt 1): 119-24
36. Leung DY, Hauk P, Strickland I, et al. The role of superantigens in human diseases: therapeutic implications for the treatment of skin diseases. Br J Dermatol 1998 Dec; 139 Suppl. 53: 17-29
37. Bunikowski R, Mielke ME, Skarabis H, et al. Evidence for a disease-promoting effect of Staphylococcus aureus-derived exotoxins in atopic dermatitis. J Allergy Clin Immunol 2000; 105: 814-9
38. Proft T, Fraser JD. Bacterial superantigens. Clin Exp Immunol 2003 Sep; 133 (3): 299-306
39. Carlsson R, Fischer H, Sjogren HO. Binding of staphylococcal enterotoxin A to accessory cells is a requirement for its ability to activate human T cells. J Immunol 1988 Apr 15; 140 (8): 2484-8
40. Breuer K, Kapp A, Werfel T. Bacterial infections and atopic dermatitis. Allergy 2001 Nov; 56 (11): 1034-41
41. Nomura I, Tanaka K, Tomita H, et al. Evaluation of the staphylococcal exotoxins and their specific IgE in childhood atopic dermatitis. J Allergy Clin Immunol 1999 Aug; 104 (2 Pt 1): 441-6
42. Tomi NS, Kranke B, Aberer E. Staphylococcal toxins in patients with psoriasis, atopic dermatitis, and erythroderma, and in healthy controls. J Am Acad Dermatol 2005; 53: 67-72
43. Yagi S, Wakaki N, Ikeda N, et al. Presence of staphylococcal exfoliative toxin A in sera of patients with atopic dermatitis. Clin Exp Allergy 2004; 34: 984-93
44. Strange P, Skov L, Lisby S, et al. Staphylococcal enterotoxin B applied on intact normal and intact atopic skin induces dermatitis. Arch Dermatol 1996 Jan; 132 (1): 27-33
45. Skov L, Olsen JV, Giorno R, et al. Application of staphylococcal enterotoxin B on normal and atopic skin induces up-regulation of T cells by a superantigen-mediated mechanism. J Allergy Clin Immunol 2000 Apr; 105 (4): 820-6
46. Michie CA, Davis T. Atopic dermatitis and staphylococcal superantigens. Lancet 1996 Feb 3; 347 (8997): 324
47. Wachs GN, Maibach HI. Co-operative double-blind trial of an antibiotic/corticoid combination in impetiginized atopic dermatitis. Br J Dermatol 1976 Sep; 95 (3): 323-8
48. Lever R, Hadley K, Downey D, et al. Staphylococcal colonization in atopic dermatitis and the effect of topical mupirocin therapy. Br J Dermatol 1988 Aug; 119 (2): 189-98
49. Saloga J, Leung DY, Reardon C, et al. Cutaneous exposure to the superantigen staphylococcal enterotoxin B elicits a T-cell-dependent inflammatory response. J Invest Dermatol 1996 May; 106 (5): 982-8
50. Herz U, Schnoy N, Borelli S, et al. A human-SCID mouse model for allergic immune response bacterial superantigen enhances skin inflammation and suppresses IgE production. J Invest Dermatol 1998 Mar; 110 (3): 224-31
51. Zollner TM, Munk ME, Keller T, et al. The superantigen exfoliative toxin induces cutaneous lymphocyte-associated antigen expression in peripheral human T lymphocytes. Immunol Lett 1996 Jan; 49 (1-2): 111-6
52. Leung DY, Gately M, Trumble A, et al. Bacterial superantigens induce T cell expression of the skin-selective homing receptor, the cutaneous lymphocyte-associated antigen, via stimulation of interleukin 12 production. J Exp Med 1995 Feb 1; 181 (2): 747-53
53. Abernathy-Carver KJ, Sampson HA, Picker LJ, et al. Milk-induced eczema is associated with the expansion of T cells expressing cutaneous lymphocyte antigen. J Clin Invest 1995 Feb; 95 (2): 913-8
54. Leung DY, Boguniewicz M, Howell MD, et al. New insights into atopic dermatitis. J Clin Invest 2004 Mar; 113 (5): 651-7
55. Mangan DF, Robertson B, Wahl SM. IL-4 enhances programmed cell death (apoptosis) in stimulated human monocytes. J Immunol 1992 Mar 15; 148 (6): 1812-6
56. Bratton DL, May KR, Kailey JM, et al. Staphylococcal toxic shock syndrome toxin-1 inhibits monocyte apoptosis. J Allergy Clin Immunol 1999 May; 103 (5 Pt 1): 895-900
57. Ou LS, Goleva E, Hall C, et al. T regulatory cells in atopic dermatitis and subversion of their activity by superantigens. J Allergy Clin Immunol 2004 Apr; 113 (4): 756-63
58. Hofer MF, Harbeck RJ, Schlievert PM, et al. Staphylococcal toxins augment specific IgE responses by atopic patients exposed to allergen. J Invest Dermatol 1999 Feb; 112 (2): 171-6
59. Hofer MF, Lester MR, Schlievert PM, et al. Upregulation of IgE synthesis by staphylococcal toxic shock syndrome toxin-1 in peripheral blood mononuclear cells from patients with atopic dermatitis. Clin Exp Allergy 1995 Dec; 25 (12): 1218-27
60. Lester MR, Hofer MF, Renz H, et al. Modulatory effects of staphylococcal superantigen TSST-1 on IgE synthesis in atopic dermatitis. Clin Immunol Immunopathol 1995 Dec; 77 (3): 332-8
61. Neuber K, Steinrucke K, Ring J. Staphylococcal enterotoxin B affects in vitro IgE synthesis, interferon-gamma, interleukin-4 and interleukin-5 production in atopic eczema. Int Arch Allergy Immunol 1995 May-Jun; 107 (1-3): 179-82
62. Leung DY, Harbeck R, Bina P, et al. 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 1993 Sep; 92 (3): 1374-80
63. Hanifin JM, Cooper KD, Ho VC, et al. Guidelines of care for atopic dermatitis, developed in accordance with the American Academy of Dermatology (AAD)/American Academy of Dermatology Association 'Administrative Regulations for Evidence-Based Clinical Practice Guidelines'. J Am Acad Dermatol 2004 Mar; 50 (3): 391-404
64. Leung DY, Nicklas RA, Li JT, et al. Disease management of atopic dermatitis: an updated practice parameter. Joint Task Force on Practice Parameters. Ann Allergy Asthma Immunol 2004 Sep; 93 (3 Suppl. 2): S1-21
65. Boguniewicz M, Sampson H, Leung SB, et al. Effects of cefuroxime axetil on Staphylococcus aureus colonization and superantigen production in atopic dermatitis. J Allergy Clin Immunol 2001 Oct; 108 (4): 651-2
66. Abeck D, Mempel M. Staphylococcus aureus colonization in atopic dermatitis and its therapeutic implications. Br J Dermatol 1998 Dec; 139 Suppl. 53: 13-6
67. Yoshimura M, Namura S, Akamatsu H, et al. Antimicrobial effects of phototherapy and photochemotherapy in vivo and in vitro. Br J Dermatol 1996 Oct; 135 (4): 528-32
68. Stalder JF, Fleury M, Sourisse M, et al. Local steroid therapy and bacterial skin flora in atopic dermatitis. Br J Dermatol 1994 Oct; 131 (4): 536-40
69. Nilsson E, Henning C, Hjorleifsson ML. Density of the microflora in hand eczema before and after topical treatment with a potent corticosteroid. J Am Acad Dermatol 1986 Aug; 15 (2 Pt 1): 192-7
70. Nilsson EJ, Henning CG, Magnusson J. Topical corticosteroids and Staphylococcus aureus in atopic dermatitis. J Am Acad Dermatol 1992 Jul; 27 (1): 29-34
71. Pournaras CC, Lubbe J, Saurat JH. Staphylococcal colonization in atopic dermatitis treatment with topical tacrolimus (FK506). J Invest Dermatol 2001 Mar; 116 (3): 480-1
72. Remitz A, Kyllonen H, Granlund H, et al. Tacrolimus ointment reduces staphylococcal colonization of atopic dermatitis lesions. J Allergy Clin Immunol 2001 Jan; 107 (1): 196-7
73. Polano MK, De Vries HR. Analysis of the results obtained in the treatment of atopic dermatitis with corticosteroid- and neomycin-containing ointments. Dermatologica 1960 Apr; 120: 191-9
74. Li L, Goleva E, Hall CF, et al. Superantigen-induced corticosteroid resistance of human T cells occurs through activation of the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase (MEK-ERK) pathway. J Allergy Clin Immunol 2004 Nov; 114 (5): 1059-69
75. Savage PB, Li C, Taotafa U, et al. Antibacterial properties of cationic steroid antibiotics. FEMS Microbiol Lett 2002 Nov 19; 217 (1): 1-7
76. Schlievert PM. Will therapeutic peptides be kryptonite for superantigens? Nat Med 2000 Apr; 6 (4): 378-9