New insights into the mechanisms of polymorphic light eruption: Resistance to ultraviolet radiation-induced immune suppression as an aetiological factor

Experimental Dermatology

Volumn 18, Issue 4, 2009, Pages 350-356

  Wolf, Peter ^a   Byrne, Scott N ^b   Gruber wackernagel, Alexandra ^a  

^a MEDICAL UNIVERSITY OF GRAZ   (Austria)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

Immune suppression; Polymorphic light eruption; T regulatory cells; UV radiation; UV resistance

Indexed keywords

CD11B ANTIBODY; CD11B ANTIGEN; CYTOKINE; DERMATOLOGICAL AGENT; ESTRADIOL; ESTROGEN RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 4; NEUROPEPTIDE; PROSTAGLANDIN E2; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ARTICLE; AUTOIMMUNE DISEASE; CANCER RISK; CELLULAR IMMUNITY; DISEASE PREDISPOSITION; DNA DAMAGE; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOPATHOLOGY; IMMUNOREGULATION; MACROPHAGE MIGRATION; MAST CELL; MELANOMA; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PHOTODERMATOSIS; RADIATION DOSE; RADIATION INJURY; REGULATORY T LYMPHOCYTE; RISK FACTOR; SEX DIFFERENCE; SKIN CANCER; SKIN CARCINOGENESIS; SUN EXPOSURE; ULTRAVIOLET RADIATION;

AUTOIMMUNITY; HUMANS; IMMUNE SYSTEM; IMMUNOSUPPRESSION; NEOPLASMS, RADIATION-INDUCED; PHOTOSENSITIVITY DISORDERS; RISK FACTORS; SKIN NEOPLASMS; ULTRAVIOLET RAYS;

EID: 63149142642     PISSN: 09066705     EISSN: 16000625     Source Type: Journal    
DOI: 10.1111/j.1600-0625.2009.00859.x     Document Type: Article

References (94)

1. Pao C, Norris P G, Corbett M, Hawk J L. Polymorphic light eruption: prevalence in Australia and England. Br J Dermatol 1994: 130: 62-64.
2. Stratigos A J, Antoniou C, Katsambas A D. Polymorphous light eruption. J Eur Acad Dermatol Venereol 2002: 16: 193-206.
3. Mastalier U, Kerl H, Wolf P. Clinical, laboratory, phototest and phototherapy findings in polymorphic light eruptions: A retrospective study of 133 patients. Eur J Dermatol 1998: 8: 554-559.
4. Holzle E, Plewig G, von Kries R, Lehmann P. Polymorphous light eruption. J Invest Dermatol 1987: 88: 32s-38s.
5. Norris P G, Hawk J L. Polymorphic light eruption. Photodermatol Photoimmunol Photomed 1990: 7: 186-191.
6. Tutrone W D, Spann C T, Scheinfeld N, Deleo V A. Polymorphic light eruption. Dermatol Ther 2003: 16: 28-39.
7. Naleway A L. Polymorphous light eruption. Int J Dermatol 2002: 41: 377-383.
8. Jansen C T. The natural history of polymorphous light eruptions. Arch Dermatol 1979: 115: 165-169.
9. Epstein S. Studies in abnormal human sensitivity to light. IV. Photoallergic concept of prurigo aestivalis. J Invest Dermatol 1942: 5: 289-298.
10. Norris P G, Morris J, McGibbon D M, Chu A C, Hawk J L. Polymorphic light eruption: An immunopathological study of evolving lesions. Br J Dermatol 1989: 120: 173-183.
11. Norris P G, Barker J N, Allen M H et al. Adhesion molecule expression in polymorphic light eruption. J Invest Dermatol 1992: 99: 504-508.
12. Norris P, Poston R N, Thomas D S, Thornhill M, Hawk J, Haskard D O. The expression of endothelial leukocyte adhesion molecule-1 (ELAM-1), intercellular adhesion molecule-1 (ICAM-1), and vascular cell adhesion molecule-1 (VCAM-1) in experimental cutaneous inflammation: A comparison of ultraviolet B erythema and delayed hypersensitivity. J Invest Dermatol 1991: 96: 763-770.
13. Jung E G, Bohnert E, Krutmann J, Elmets C A. Photobiology of ultraviolet induced DNA damage. In: Jung E G, Bohnert E, Krutmann J, Elmets C A, eds. Photoimmunology. Cambridge: Cambridge University Press, 1995: 3.
14. de Gruijl F R. Health effects from solar UV radiation. Radiat Prot Dosimetry 1997: 72: 177-196.
15. Cooper K D, Oberhelman L, Hamilton T A et al. UV exposure reduces immunization rates and promotes tolerance to epicutaneous antigens in humans: Relationship to dose, CD1a-DR+ epidermal macrophage induction, and Langerhans cell depletion. Proc Natl Acad Sci USA 1992: 89: 8497-8501.
16. Cooper K D. Cell-mediated immunosuppressive mechanisms induced by UV radiation. Photochem Photobiol 1996: 63: 400-406.
17. Yoshikawa T, Rae V, Bruins-Slot W, Van den Berg J W, Taylor J R, Streilein J W. Susceptibility to effects of UVB radiation on induction of contact hypersensitivity as a risk factor for skin cancer in humans. J Invest Dermatol 1990: 95: 530-536.
18. Fisher M S, Kripke M L. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci USA 1977: 74: 1688-1692.
19. Moloney F J, Comber H, O'Lorcain P, O'Kelly P, Conlon P J, Murphy G M. A population-based study of skin cancer incidence and prevalence in renal transplant recipients. Br J Dermatol 2006: 154: 498-504.
20. Kelly D A, Walker S L, McGregor J M, Young A R. A single exposure of solar simulated radiation suppresses contact hypersensitivity responses both locally and systemically in humans: Quantitative studies with high-frequency ultrasound. J Photochem Photobiol B 1998: 44: 130-142.
21. Damian D L, Barnetson R S, Halliday G M. Low-dose UVA and UVB have different time courses for suppression of contact hypersensitivity to a recall antigen in humans. J Invest Dermatol 1999: 112: 939-944.
22. Wolf P, Hoffmann C, Quehenberger F, Grinschgl S, Kerl H. Immune protection factors of chemical sunscreens measured in the local contact hypersensitivity model in humans. J Invest Dermatol 2003: 121: 1080-1087.
23. Fourtanier A, Moyal D, Maccario J et al. Measurement of sunscreen immune protection factors in humans: A consensus paper. J Invest Dermatol 2005: 125: 403-409.
24. Ullrich S E. Suppression of the immune response to allogeneic histocompatibility antigens by a single exposure to ultraviolet radiation. Transplantation 1986: 42: 287-291.
25. Ullrich S E. Systemic immunosuppression of cell-mediated immune reactions by a monofunctional psoralen plus ultraviolet A radiation. Photodermatol Photoimmunol Photomed 1991: 8: 116-122.
26. Maeda A, Schwarz A, Kernebeck K et al. Intravenous infusion of syngeneic apoptotic cells by photopheresis induces antigen-specific regulatory T cells. J Immunol 2005: 174: 5968-5976.
27. Gonzalez-Amaro R, Baranda L, Salazar-Gonzalez J F, Abud-Mendoza C, Moncada B. Immune sensitization against epidermal antigens in polymorphous light eruption. J Am Acad Dermatol 1991: 24: 70-73.
28. Hofer A, Legat F J, Wackernagel A et al. Topical DNA repair enzymes can prevent polymorphous light eruption. J Invest Dermatol 2005: 125(Suppl.): A5 (abstr).
29. Yarosh D B, O'Connor A, Alas L, Potten C, Wolf P. Photoprotection by topical DNA repair enzymes: Molecular correlates of clinical studies. Photochem Photobiol 1999: 69: 136-140.
30. Yarosh D, Klein J, O'Connor A, Hawk J, Rafal E, Wolf P. Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: A randomised study. Xeroderma Pigmentosum Study Group. Lancet 2001: 357: 926-929.
31. Wolf P, Maier H, Mullegger R R et al. Topical treatment with liposomes containing T4 endonuclease V protects human skin in vivo from ultraviolet-induced upregulation of interleukin-10 and tumor necrosis factor-alpha. J Invest Dermatol 2000: 114: 149-156.
32. Wolf P, Yarosh D B, Kripke M L. Effects of sunscreens and a DNA excision repair enzyme on ultraviolet radiation-induced inflammation, immune suppression, and cyclobutane pyrimidine dimer formation in mice. J Invest Dermatol 1993: 101: 523-527.
33. Wolf P, Cox P, Yarosh D B, Kripke M L. Sunscreens and T4N5 liposomes differ in their ability to protect against ultraviolet-induced sunburn cell formation, alterations of dendritic epidermal cells, and local suppression of contact hypersensitivity. J Invest Dermatol 1995: 104: 287-292.
34. Legat F J, Griesbacher T, Schicho R et al. Repeated subinflammatory ultraviolet B irradiation increases substance P and calcitonin gene-related peptide content and augments mustard oil-induced neurogenic inflammation in the skin of rats. Neurosci Lett 2002: 329: 309-313.
35. Legat F J, Jaiani L T, Wolf P et al. The role of calcitonin gene-related peptide in cutaneous immunosuppression induced by repeated subinflammatory ultraviolet irradiation exposure. Exp Dermatol 2004: 13: 242-250.
36. Legat F J, Wolf P. Photodamage to the cutaneous sensory nerves: Role in photoaging and carcinogenesis of the skin? Photochem Photobiol Sci 2006: 5: 170-176.
37. Legat F J, Bretterklieber A, Haar M et al. The effects of topical capsaicin pretreatment on the induction of polymorphous light eruption (PLE) by solar simulated light. J Invest Dermatol 2007: 127(Suppl.): S44 (abstr).
38. Shreedhar V, Giese T, Sung V W, Ullrich S E. A cytokine cascade including prostaglandin E2, IL-4, and IL-10 is responsible for UV-induced systemic immune suppression. J Immunol 1998: 160: 3783-3789.
39. Cooper K D, Fox P, Neises G, Katz S I. Effects of ultraviolet radiation on human epidermal cell alloantigen presentation: Initial depression of Langerhans cell-dependent function is followed by the appearance of T6- Dr+ cells that enhance epidermal alloantigen presentation. J Immunol 1985: 134: 129-137.
40. Cooper K D, Neises G R, Katz S I. Antigen-presenting OKM5+ melanophages appear in human epidermis after ultraviolet radiation. J Invest Dermatol 1986: 86: 363-370.
41. Baadsgaard O, Wulf H C, Wantzin G L, Cooper K D. UVB and UVC, but not UVA, potently induce the appearance of T6- DR+ antigen-presenting cells in human epidermis. J Invest Dermatol 1987: 89: 113-118.
42. Cooper K D, Duraiswamy N, Hammerberg C et al. Neutrophils, differentiated macrophages, and monocyte/macrophage antigen presenting cells infiltrate murine epidermis after UV injury. J Invest Dermatol 1993: 101: 155-163.
43. Kang K, Hammerberg C, Meunier L, Cooper K D. CD11b+ macrophages that infiltrate human epidermis after in vivo ultraviolet exposure potently produce IL-10 and represent the major secretory source of epidermal IL-10 protein. J Immunol 1994: 153: 5256-5264.
44. Stevens S R, Shibaki A, Meunier L, Cooper K D. Suppressor T cell-activating macrophages in ultraviolet-irradiated human skin induce a novel, TGF-beta-dependent form of T cell activation characterized by deficient IL-2r alpha expression. J Immunol 1995: 155: 5601-5607.
45. Hammerberg C, Duraiswamy N, Cooper K D. Reversal of immunosuppression inducible through ultraviolet-exposed skin by in vivo anti-CD11b treatment. J Immunol 1996: 157: 5254-5261.
46. Kölgen W, Van Weelden H, Den Hengst S et al. CD11b+ cells and ultraviolet-B-resistant CD1a+ cells in skin of patients with polymorphous light eruption. J Invest Dermatol 1999: 113: 4-10.
47. Schornagel I J, Sigurdsson V, Nijhuis E H, Bruijnzeel-Koomen C A, Knol E F. Decreased neutrophil skin infiltration after UVB exposure in patients with polymorphous light eruption. J Invest Dermatol 2004: 123: 202-206.
48. Schuler G, Steinman R M. Murine epidermal Langerhans cells mature into potent immunostimulatory dendritic cells in vitro. J Exp Med 1985: 161: 526-546.
49. Finkelman F D, Lees A, Birnbaum R, Gause W C, Morris S C. Dendritic cells can present antigen in vivo in a tolerogenic or immunogenic fashion. J Immunol 1996: 157: 1406-1414.
50. Steinbrink K, Wolfl M, Jonuleit H, Knop J, Enk A H. Induction of tolerance by IL-10-treated dendritic cells. J Immunol 1997: 159: 4772-4780.
51. Noonan F P, Bucana C, Sauder D N, De Fabo E C. Mechanism of systemic immune suppression by UV irradiation in vivo. II. The UV effects on number and morphology of epidermal Langerhans cells and the UV-induced suppression of contact hypersensitivity have different wavelength dependencies. J Immunol 1984: 132: 2408-2416.
52. Toews G B, Bergstresser P R, Streilein J W. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J Immunol 1980: 124: 445-453.
53. Vink A A, Strickland F M, Bucana C et al. Localization of DNA damage and its role in altered antigen-presenting cell function in ultraviolet-irradiated mice. J Exp Med 1996: 183: 1491-1500.
54. Vink A A, Moodycliffe A M, Shreedhar V et al. The inhibition of antigen-presenting activity of dendritic cells resulting from UV irradiation of murine skin is restored by in vitro photorepair of cyclobutane pyrimidine dimers. Proc Natl Acad Sci USA 1997: 94: 5255-5260.
55. Applegate L A, Ley R D, Alcalay J, Kripke M L. Identification of the molecular target for the suppression of contact hypersensitivity by ultraviolet radiation. J Exp Med 1989: 170: 1117-1131.
56. Stingl G, Gazze-Stingl L A, Aberer W, Wolff K. Antigen presentation by murine epidermal langerhans cells and its alteration by ultraviolet B light. J Immunol 1981: 127: 1707-1713.
57. Wackernagel A, Back B, Quehenberger F, Cerroni L, Kerl H, Wolf P. Langerhans cell resistance, CD11b+ cell influx, and cytokine mRNA expression in skin after UV exposure in patients with polymorphous light eruption as compared with healthy control subjects. J Invest Dermatol 2004: 122: 1342-1344.
58. Lu L F, Lind E F, Gondek D C et al. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 2006: 442: 997-1002.
59. Hart P H, Grimbaldeston M A, Swift G J, Jaksic A, Noonan F P, Finlay-Jones J J. Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J Exp Med 1998: 187: 2045-2053.
60. Grimbaldeston M A, Pearce A L, Robertson B O et al. Association between melanoma and dermal mast cell prevalence in sun-unexposed skin. Br J Dermatol 2004: 150: 895-903.
61. Ribatti D, Ennas M G, Vacca A et al. Tumor vascularity and tryptase-positive mast cells correlate with a poor prognosis in melanoma. Eur J Clin Invest 2003: 33: 420-425.
62. Iamaroon A, Pongsiriwet S, Jittidecharaks S, Pattanaporn K, Prapayasatok S, Wanachantararak S. Increase of mast cells and tumor angiogenesis in oral squamous cell carcinoma. J Oral Pathol Med 2003: 32: 195-199.
63. Galli S J, Kalesnikoff J, Grimbaldeston M A, Piliponsky A M, Williams C M, Tsai M. Mast cells as "tunable"effector and immunoregulatory cells: Recent advances. Annu Rev Immunol 2005: 23: 749-786.
64. Byrne S N, Limon-Flores A Y, Ullrich S E. Mast cell migration from the skin to the draining lymph nodes upon ultraviolet irradiation represents a key step in the induction of immune suppression. J Immunol 2008: 180: 4648-4655.
65. Kim M S, Kim Y K, Lee D H et al. Acute exposure of human skin to ultraviolet or infrared radiation or heat stimuli increases mast cell numbers and tryptase expression in human skin in vivo. Br J Dermatol 2009: 160: 393-402.
66. Teunissen M B, Piskin G, di Nuzzo S, Sylva-Steenland R M, de Rie M A, Bos J D. Ultraviolet B radiation induces a transient appearance of IL-4+ neutrophils, which support the development of Th2 responses. J Immunol 2002: 168: 3732-3739.
67. Kölgen W, van Meurs M, Jongsma M et al. Differential expression of cytokines in UV-B-exposed skin of patients with polymorphous light eruption: Correlation with Langerhans cell migration and immunosuppression. Arch Dermatol 2004: 140: 295-302.
68. Janssens A S, Pavel S, Out-Luiting J J, Willemze R, de Gruijl F R. Normalized ultraviolet (UV) induction of Langerhans cell depletion and neutrophil infiltrates after artificial UVB hardening of patients with polymorphic light eruption. Br J Dermatol 2005: 152: 1268-1274.
69. Janssens A S, Pavel S, Tensen C P et al. Reduced IL-1Ra/IL-1 ratio in ultraviolet B-exposed skin of patients with polymorphic light eruption. Exp Dermatol 2009: 18: 212-217.
70. van de Pas C B, Kelly D A, Seed P T, Young A R, Hawk J L, Walker S L. Ultraviolet-radiation-induced erythema and suppression of contact hypersensitivity responses in patients with polymorphic light eruption. J Invest Dermatol 2004: 122: 295-299.
71. Ullrich S E, Yee G K, Kripke M L. Suppressor lymphocytes induced by epicutaneous sensitization of UV-irradiated mice control multiple immunological pathways. Immunology 1986: 58: 185-190.
72. Schwarz A, Maeda A, Wild M K et al. Ultraviolet radiation-induced regulatory T cells not only inhibit the induction but can suppress the effector phase of contact hypersensitivity. J Immunol 2004: 172: 1036-1043.
73. Byrne S N, Halliday G M. B cells activated in lymph nodes in response to ultraviolet irradiation or by interleukin-10 inhibit dendritic cell induction of immunity. J Invest Dermatol 2005: 124: 570-578.
74. Byrne S N, Ahmed J, Halliday G M. Ultraviolet B but not A radiation activates suppressor B cells in draining lymph nodes. Photochem Photobiol 2005: 81: 1366-1370.
75. Schwarz T, Halliday G M. Photoimmunology. In: Lim H H, Hönigsmann H, Hawk J L M, eds. Photodermatology. New York: Informa Healthcare, 2007: 55-74.
76. Ullrich S E, Kripke M L. Mechanisms in the suppression of tumor rejection produced in mice by repeated UV irradiation. J Immunol 1984: 133: 2786-2790.
77. Schwarz A, Beissert S, Grosse-Heitmeyer K et al. Evidence for functional relevance of CTLA-4 in ultraviolet-radiation-induced tolerance. J Immunol 2000: 165: 1824-1831.
78. McHugh R S, Whitters M J, Piccirillo C A et al. CD4(+)CD25(+) immunoregulatory T cells: Gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002: 16: 311-323.
79. Bruder D, Probst-Kepper M, Westendorf A M et al. Neuropilin-1: A surface marker of regulatory T cells. Eur J Immunol 2004: 34: 623-630.
80. Gorman S, Kuritzky L A, Judge M A et al. Topically applied 1,25-dihydroxyvitamin D3 enhances the suppressive activity of CD4+CD25+ cells in the draining lymph nodes. J Immunol 2007: 179: 6273-6283.
81. Khattri R, Cox T, Yasayko S A, Ramsdell F. An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 2003: 4: 337-342.
82. Fontenot J D, Gavin M A, Rudensky A Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003: 4: 330-336.
83. Valencia X, Yarboro C, Illei G, Lipsky P E. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol 2007: 178: 2579-2588.
84. Stoebner P E, Rahmoun M, Ferrand C, Meunier L, Yssel H, Pene J. A single sub-erythematous exposure of solar-simulated radiation on the elicitation phase of contact hypersensitivity induces IL-10-producing T-regulatory cells in human skin. Exp Dermatol 2006: 15: 615-624.
85. Palmer R A, Friedmann P S. Ultraviolet radiation causes less immunosuppression in patients with polymorphic light eruption than in controls. J Invest Dermatol 2004: 122: 291-294.
86. Damian D L, Patterson C R, Stapelberg M, Park J, Barnetson R S, Halliday G M. UV radiation-induced immunosuppression is greater in men and prevented by topical nicotinamide. J Invest Dermatol 2008: 128: 447-454.
87. Widyarini S, Domanski D, Painter N, Reeve V E. Estrogen receptor signaling protects against immune suppression by UV radiation exposure. Proc Natl Acad Sci USA 2006: 103: 12837-12842.
88. Aubin F. Why is polymorphous light eruption so common in young women? Arch Dermatol Res 2004: 296: 240-241.
89. Hiramoto K, Tanaka H, Yanagihara N, Sato E F, Inoue M. Effect of 17beta-estradiol on immunosuppression induced by ultraviolet B irradiation. Arch Dermatol Res 2004: 95: 307-311.
90. Lembo S, Fallon J, O'Kelly P, Murphy G M. Polymorphic light eruption and skin cancer prevalence: Is one protective against the other? Br J Dermatol 2008: 159: 1342-1347.
91. Wolf P, Quehenberger F, Mullegger R, Stranz B, Kerl H. Phenotypic markers, sunlight-related factors and sunscreen use in patients with cutaneous melanoma: An Austrian case-control study. Melanoma Res 1998: 8: 370-378.
92. Ruzicka T, Przybilla B. Eicosanoid release in polymorphous light eruption: Selective UV-A-induced LTB4 generation by peripheral blood leukocytes. Skin Pharmacol 1988: 1: 186-191.
93. Rhodes L E, Durham B H, Fraser W D, Friedmann P S. Dietary fish oil reduces basal and ultraviolet B-generated PGE2 levels in skin and increases the threshold to provocation of polymorphic light eruption. J Invest Dermatol 1995: 105: 532-535.
94. Rhodes L E. Polymorphic light eruption: Does a neutrophil defect Xcontribute to the pathogenesis? J Invest Dermatol 2004: 123: xiii-xv.