Mechanisms involved in ultraviolet light-induced immunosuppression

European Journal of Dermatology

Volumn 13, Issue 6, 2003, Pages 515-523

  Aubin, François ^a  

^a UNIVERSITY HOSPITAL OF BESANÇON   (France)

Author keywords

Immunology; Immunosuppression; Ultraviolet radiation

Indexed keywords

DNA; FAS ANTIGEN; INTERLEUKIN 10;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; CHROMATOPHORE; CONTROLLED STUDY; CUTANEOUS PARAMETERS; DERMIS; ENVIRONMENTAL FACTOR; EPIDERMIS; IMMUNE DEFICIENCY; IMMUNOPATHOGENESIS; KERATINOCYTE; LANGERHANS CELL; MACROPHAGE; MOLECULAR BIOLOGY; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NONHUMAN; PREMATURE AGING; REVIEW; SKIN CANCER; SKIN CARCINOGENESIS; SUPPRESSOR CELL; T LYMPHOCYTE; ULTRAVIOLET RADIATION;

ANIMALS; ANTIGEN PRESENTATION; HUMANS; IMMUNE TOLERANCE; KERATINOCYTES; LANGERHANS CELLS; MACROPHAGES; MAST CELLS; NEUTROPHILS; SKIN; SUPPRESSOR FACTORS, IMMUNOLOGIC; T-LYMPHOCYTES; ULTRAVIOLET RAYS;

EID: 0346158419     PISSN: 11671122     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (100)

1. Brash DE, Ziegler A, Jonason AS, Simon JA, Kunala S, Leffell DJ. J Invest Dermatol Symp Proc 1996; 1: 136-42.
2. Ullrich SE. Photoimmune suppression and photocarcinogenesis. Front Biosci 2002; 7: d684-703.
3. Kripke ML. Antigenicity of murine skin tumors induced by ultraviolet light. J Natl Cancer Inst 1974; 53: 1333-6.
4. Sleijffers A, Garssen J, Van Loveren H. Ultraviolet radiation, resistance to infectious diseases, and vaccination responses. Methods 2002; 28: 111-21.
5. Norval M. Immunosuppression induced by ultraviolet radiation: relevance to public health. Bull World Health Organ 2002; 80: 906-7.
6. Nghiem DX, Kazimi N, Clydesdale G, Ananthaswamy HN, Kripke ML, Ullrich SE. Ultraviolet a radiation suppresses an established immune response: implications for sunscreen design. J Invest Dermatol 2001; 117: 1193-9.
7. Donawho CK, Muller HK, Bucana CD, Kripke ML. Enhanced growth of murine melanoma in ultraviolet-irradiated skin is associated with local inhibition of immune effector mechanisms. J Immunol 1996; 157: 781-6.
8. Beissert S, Schwarz T. Mechanisms involved in ultraviolet light-induced immunosuppression. J Invest Dermatol Symp Proc 1999; 4: 61-4.
9. Toews GB, Bergstresser PR, Streilein JW. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J Immunol 1980; 124: 445-53.
10. Niizeki H, Inoko H, Wayne Streilein J. Polymorphisms in the TNF region confer susceptibility to UVB-induced impairment of contact hypersensitivity induction in mice and humans. Methods 2002; 28: 46-54.
11. Aubin F, Kripke ML, Ullrich SE. Activation of keratinocytes with psoralen plus UVA radiation induces the release of soluble factors that suppress delayed and contact hypersensitivity. J Invest Dermatol 1991; 97: 995-1000.
12. Norval M, Gibbs NK, Gilmour J. The role of urocanic acid in UV-induced immunosuppression: recent advances (1992-1994). Photochem Photobiol 1995; 62: 209-17.
13. De Fabo EC, Noonan FP. Mechanism of immune suppression by ultraviolet irradiation in vivo. I. Evidence for the existence of a unique photoreceptor in skin and its role in photoimmunology. J Exp Med 1983; 158: 84-98.
14. Moodycliffe AM, Bucana CD, Kripke ML, Norval M, Ullrich SE. Differential effects of a monoclonal antibody to cis-urocanic acid on the suppression of delayed and contact hypersensitivity following ultraviolet irradiation. J Immunol 1996; 157: 2891-9.
15. Zak-Prelich M, Norval M, Venner TJ, Bisset Y, Walker C, Rafferty TS, Sauder DN, McKenzie RC. cis-Urocanic acid does not induce the expression of immunosuppressive cytokines in murine keratinocytes. Photochem Photobiol 2001; 73: 238-44.
16. Applegate LA, Ley RD, Alcalay J, Kripke ML. Identification of the molecular target for the suppression of contact hypersensitivity by ultraviolet radiation. J Exp Med 1989; 170: 1117-31.
17. Yarosh D, Bucana C, Cox P, Alas L, Kibitel J, Kripke M. Localization of liposomes containing a DNA repair enzyme in murine skin. J Invest Dermatol 1994; 103: 461-8.
18. Kripke ML, Cox PA, Alas LG, Yarosh DB. Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice. Proc Natl Acad Sci USA 1992; 89: 7516-20.
19. Nishigori C, Yarosh DB, Ullrich SE, Vink AA, Bucana CD, Roza L, Kripke ML. Evidence that DNA damage triggers interleukin 10 cytokine production in UV-irradiated murine keratinocytes. Proc Natl Acad Sci USA 1996; 93: 10354-9.
20. Kibitel J, Hejmadi V, Alas L, O'Connor A, Sutherland BM, Yarosh D. UV-DNA damage in mouse and human cells induces the expression of tumor necrosis factor alpha. Photochem Photobiol 1998; 67: 541-6.
21. Wolf P, Maier H, Mullegger RR, Chadwick CA, Hofmann-Wellenhof R, Soyer HP, Hofer A, Smolle J, Horn M, Cerroni L, Yarosh D, Klein J, Bucana C, Dunner K Jr, Potten CS, Honigsmann H, Kerl H, Kripke ML. 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: 149-56.
22. Stege H, Roza L, Vink AA, Grewe M, Ruzicka T, Grether-Beck S, Krutmann J. Enzyme plus light therapy to repair DNA damage in ultraviolet-B-irradiated human skin. Proc Natl Acad Sci USA 2000; 97: 1790-5.
23. Schwarz T. UV light affects cell membrane and cytoplasmic targets. J Photochem Photobiol B 1998; 44: 91-6.
24. Walterscheid JP, Ullrich SE, Nghiem DX. Platelet-activating factor, a molecular sensor for cellular damage, activates systemic immune suppression. J Exp Med 2002; 195: 171-9.
25. Prescott SM, Zimmerman GA, Stafforini DM, McIntyre TM. Platelet-activating factor and related lipid mediators. Annu Rev Biochem 2000; 69: 419-45.
26. Devary Y, Gottlieb RA, Smeal T, Karin M. The mammalian ultraviolet response is triggered by activation of Src tyrosine kinases. Cell 1992; 71: 1081-91.
27. Simon MM, Aragane Y, Schwarz A, Luger TA, Schworz T. UVB light induces nuclear factor kappa B (NF kappa B) activity independently from chromosomal DNA damage in cell-free cytosolic extracts. J Invest Dermatol 1994; 102: 422-7.
28. Rosette C, Karin M. Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 1996; 274: 1194-7.
29. Aragane Y, Kulms D, Luger TA, Schwarz T. Down-regulation of interferon gamma-activated STAT1 by UV light. Proc Natl Acad Sci USA 1997; 94 11490-5.
30. Kulms D, Schwarz T. Mechanisms of UV-induced signal transduction. J Dermatol 2002; 29: 189-96.
31. Kolgen W, Both H, van Weelden H, Guikers KL, Bruijnzeel-Koomen CA, Knol EF, van Vloten WA, De Gruijl FR. Epidermal langerhans cell depletion after artificial ultraviolet B irradiation of human skin in vivo: apoptosis versus migration. J Invest Dermatol 2002; 118: 812-7.
32. Vink AA, Strickland FM, Bucana C, Cox PA, Roza L, Yarosh DB, Kripke ML. Localization of DNA damage and its role in altered antigen-presenting cell function in ultraviolet-irradiated mice. J Exp Med 1996; 183: 1491-500.
33. Dandie GW, Clydesdale GJ, Jacobs I, Muller HK. Effects of UV on the migration and function of epidermal antigen presenting cells. Mutat Res 1998; 422: 147-54.
34. Schwarz A, Grabbe S, Grosse-Heitmeyer K, Roters B, Riemann H, Luger TA, Trinchieri G, Schwarz T. Ultraviolet light-induced immune tolerance is mediated via the Fas/Fas-ligand system. J Immunol 1998; 160: 4262-70.
35. Nakagawa S, Koomen CW, Bos JD, Teunissen MB. Differential modulation of human epidermal Langerhans cell maturation by ultraviolet B radiation. J Immunol 1999; 163: 5192-200.
36. Simon JC, Cruz PD Jr, Bergstresser PR, Tigelaar RE. Low dose ultraviolet B-irradiated Langerhans cells preferentially activate CD4 + cells of the T helper 2 subset. J Immunol 1990; 145: 2087-91.
37. Ullrich SE, Schmitt DA. The role of cytokines in UV-induced systemic immune suppression. J Dermatol Sci 2000; 23 Suppl 1: S10-2.
38. Vink AA, Moodycliffe AM, Shreedhar V, Ullrich SE, Roza L, Yarosh DB, Kripke ML. 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: 5255-60.
39. Kurimoto I, Arana M, Streilein JW. Role of dermal cells from normal and ultraviolet B-damaged skin in induction of contact hypersensitivity and tolerance. J Immunol 1994; 152: 3317-23.
40. Hammerberg C, Duraiswamy N, Cooper KD. Active induction of unresponsiveness (tolerance) to DNFB by in vivo ultraviolet-exposed epidermal cells is dependent upon infiltrating class II MHC + CD11bbright monocytic/macrophagic cells. J Immunol 1994; 153: 4915-24.
41. Meunier L, Bata-Csorgo Z, Cooper KD. In human dermis, ultraviolet radiation induces expansion of a CD36 + CD11b + CD1-macrophage subset by infiltration and proliferation; CD1 + Langerhans-like dendritic antigen-presenting cells are concomitantly depleted. J Invest Dermatol 1995; 105: 782-8.
42. Kang K, Gilliam AC, Chen G, Tootell E, Cooper KD. In human skin, UVB initiates early induction of IL-10 over IL-12 preferentially in the expanding dermal monocytic/macrophagic population. J Invest Dermatol 1998; 111: 31-8.
43. Hammerberg C, Katiyar SK, Carroll MC, Cooper KD. Activated complement component 3 (C3) is required for ultraviolet induction of immunosuppression and antigenic tolerance. J Exp Med 1998; 187: 1133-8.
44. Ahrens C, Grewe M, Berneburg M, Grether-Beck S, Quilliet X, Mezzina M, Sarasin A, Lehmann AR, Arlett CF, Krutmann J. Photocarcinogenesis and inhibition of intercellular adhesion molecule 1 expression in cells of DNA-repair-defective individuals. Proc Natl Acad Sci USA 1997; 94: 6837-41.
45. Kremer IB, Cooper KD, Teunissen MB, Stevens SR. Law expression of CD40 and B7 on macrophages infiltrating UV-exposed human skin; role in IL-2Ralpha-T cell activation. Eur J Immunol 1998; 28: 2936-46.
46. Teunissen MB, Piskin G, di Nuzzo S, Sylva-Steenlond RM, de Rie MA, Bos JD. Ultraviolet B radiation induces a transient appearance of IL-4 + neutrophils, which support the development of Th2 responses. J Immunol 2002; 168: 3732-9.
47. Hart PH, Grimbaldeston MA, Swift GJ, Jaksic A, Noonan FP, Finlay-Jones JJ. Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J Exp Med 1998; 187: 2045-53.
48. Macatonia SE, Knight SC, Edwards AJ, Griffiths S, Fryer P. Localization of antigen on lymph node dendritic cells after exposure to the contact sensitizer fluorescein isothiocyanate. Functional and morphological studies. J Exp Med 1987; 166: 1654-67.
49. Okamoto H, Kripke ML. Effector and suppressor circuits of the immune response are activated in vivo by different mechanisms. Proc Natl Acad Sci USA 1987; 84: 3841-5.
50. Fisher MS, Kripke ML. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci USA 1977; 74: 1688-92.
51. Daynes RA, Spellman CW. Evidence for the generation of suppressor cells by ultraviolet radiation. Cell Immunol 1977; 31: 182-7.
52. Elmets CA, Bergstresser PR, Tigelaar RE, Wood PJ, Streilein JW. Analysis of the mechanism of unresponsiveness produced by haptens pointed on skin exposed to low dose ultraviolet radiation. J Exp Med 1983; 158: 781-94.
53. Krasteva M, Aubin F, Laventurier S, Kehren J, Assossau O, Kanitakis J, Kaiserlian D, Nicolas JF. MHC class II-KO mice are resistant to the immunosuppressive effects of UV light. Eur J Dermatol 2002; 12: 10-9.
54. Rivas JM, Ullrich SE. The role of IL-4, IL-10, and TNF-alpha in the immune suppression induced by ultraviolet radiation. J Leukoc Biol 1994; 56: 769-75.
55. Moodycliffe AM, Nghiem D, Clydesdale G, Ullrich SE. Immune suppression and skin cancer development: regulation by NKT cells. Nat Immunol 2000; 1: 521-5.
56. Shreedhar VK, Pride MW, Sun Y, Kripke ML, Strickland FM. Origin and characteristics of ultraviolet-B radiation-induced suppressor T lymphocytes. J Immunol 1998; 161: 1327-35.
57. Schwarz A, Beissert S, Grosse-Heitmeyer K, Gunzer M, Bluestone JA, Grabbe S, Schwarz T. Evidence for functional relevance of CTLA-4 in ultraviolet-radiation-induced tolerance. J Immunol 2000; 165: 1824-31.
58. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG. A CD4 + T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997; 389: 737-42.
59. Moodycliffe AM, Shreedhar V, Ullrich SE, Walterscheid J, Bucana C, Kripke ML, Flores-Romo L. CD40-CD40 ligand interactions in vivo regulate migration of antigen-bearing dendritic cells from the skin to draining lymph nodes. J Exp Med 2000; 191: 2011-20.
60. Schwarz A, Grabbe S, Grosse-Heitmeyer K, Roters B, Riemann H, Luger TA, Trinchieri G, Schwarz T. Ultraviolet light-induced immune tolerance is mediated via the Fas/Fas-ligand system. J Immunol 1998; 160: 4262-70.
61. Hill LL, Shreedhar VK, Kripke ML, Owen-Schaub LB. A critical role for Fas ligand in the active suppression of systemic immune responses by ultraviolet radiation. J Exp Med 1999; 189: 1285-94.
62. Bittencourt MC, Perruche S, Contassot E, Fresnay S, Baron MH, Angonin R, Aubin F, Herve P, Tiberghien P, Saas P. Intravenous injection of apoptotic leukocytes enhances bone marrow engraftment across major histocompatibility barriers. Blood 2001; 98: 224-30.
63. Schworz A, Grabbe S, Mahnke K, Riemann H, Luger TA, Wysocka M, Trinchieri G, Schwarz T. Interleukin 12 breaks ultraviolet light induced immunosuppression by affecting CD8 + rather than CD4 + T cells. J Invest Dermatol 1998; 110: 272-6.
64. Schwarz A, Stander S, Berneburg M, Bohm M, Kulms D, van Steeg H, Grosse-Heitmeyer K, Krutmann J, Schwarz T. Interleukin-12 suppresses ultraviolet radiation-induced apoptosis by inducing DNA repair. Nat Cell Biol 2002; 4: 26-31.
65. Tomimori Y, Ikawa Y, Oyaizu N. Ultraviolet-irradiated apoptotic lymphocytes produce interleukin-10 by themselves. Immunol Lett 2000; 71: 49-54.
66. Takashima A, Bergstresser PR. Impact of UVB radiation on the epidermal cytokine network. Photochem Photobiol 1996; 63: 397-400.
67. Ullrich SE. The role of epidermal cytokines in the generation of cutaneous immune reactions and ultraviolet radiation-induced immune suppression. Photochem Photobiol 1995; 62: 389-401.
68. Shimizu T, Streilein JW. Local and systemic consequences of acute, low-dose ultraviolet B radiation are mediated by different immune regulatory mechanisms. Eur J Immunol 1994; 24: 1765-70.
69. Kondo S, Wang B, Fujisawa H, Shivji GM, Echtenacher B, Mak TW, Sauder DN. Effect of gene-targeted mutation in TNF receptor (p55) on contact hypersensitivity and ultraviolet B-induced immunosuppression. J Immunol 1995; 155: 3801-5.
70. Amerio P, Toto P, Feliciani C, Suzuki H, Shivji G, Wang B, Sauder DN. Rethinking the role of tumour necrosis factor-alpha in ultraviolet (UV) B-induced immunosuppression: altered immune response in UV-irradiated TNFR1R2 gene-targeted mutant mice. Br J Dermatol 2001; 144: 952-7.
71. Rivas JM, Ullrich SE. Systemic suppression of delayed-type hypersensitivity by supernatants from UV-irradiated keratinocytes. An essential role for keratinocyte-derived IL-10. J Immunol 1992; 149: 3865-71.
72. Niizeki H, Streilein JW. Hapten-specific tolerance induced by acute, low-dose ultraviolet B radiation of skin is mediated via interleukin-10. J Invest Dermatol 1997; 109: 25-30.
73. Beissert S, Hosoi J, Kuhn R, Rajewsky K, Muller W, Granstein RD. Impaired immunosuppressive response to ultraviolet radiation in interleukin-10-deficient mice. J Invest Dermatol 1996; 107: 553-7.
74. Kang K, Hammerberg C, Meunier L, Cooper KD. 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: 5256-64.
75. Araneo BA, Dowell T, Moan HB, Daynes RA. Regulation of murine lymphokine production in vivo. Ultraviolet radiation exposure depresses IL-2 and enhances IL-4 production by T cells through an IL-1-dependent mechanism. J Immunol 1989; 143: 1737-44.
76. Enk AH, Angeloni VL, Udey MC, Katz SI. Inhibition of Langerhans cell antigen-presenting function by IL-10. A role for IL-10 in induction of tolerance. J Immunol 1993; 151: 2390-8.
77. Shreedhar V, Giese T, Sung VW, Ullrich SE. A cytokine cascade including prostaglandin E2, IL-4, and IL-10 is responsible for UV-induced systemic immune suppression. J Immunol 1998; 160: 3783-9.
78. Buckman SY, Gresham A, Hale P, Hruza G, Anast J, Masferrer J, Pentland AP. COX-2 expression is induced by UVB exposure in human skin: implications for the development of skin cancer. Carcinogenesis 1998; 19: 723-9.
79. Calignano A, Cirino G, Meli R, Persico P. Isolation and identification of platelet-activating factor in UV-irradiated guinea pig skin. J Pharmacol Methods 1988; 19: 89-91.
80. Pei Y, Barber LA, Murphy RC, Johnson CA, Kelley SW, Dy LC, Fertel RH, Nguyen TM, Williams DA, Travers JB. Activation of the epidermal platelet-activating factor receptor results in cytokine and cyclooxygenase-2 biosynthesis. J Immunol 1998; 161: 1954-61.
81. Gillardon F, Moll I, Michel S, Benrath J, Weihe E, Zimmermann M. Calcitonin gene-related peptide and nitric oxide are involved in ultraviolet radiation-induced immunosuppression. Eur J Pharmacol 1995; 293: 395-400.
82. Luger TA, Schwarz T, Kalden H, Scholzen T, Schwarz A, Brzosko T. Role of epidermal cell-derived alpha-melanocyte stimulating hormone in ultraviolet light mediated local immunosuppression. Ann N Y Acad Sci 1999; 885: 209-16.
83. van der Pouw Kraan TC, Bœije LC, Smeenk RJ, Wijdenes J, Aarden LA. Prostaglandin-E2 is a potent inhibitor of human interleukin 12 production. J Exp Med 1995; 181: 775-9.
84. Magram J, Connaughton SE, Warrier RR, Carvajal DM, Wu CY, Ferrante J, Stewart C, Sarmiento U, Faherty DA, Gately MK. IL-12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 1996; 4: 471-81.
85. Schmitt DA, Owen-Schaub L, Ullrich SE. Effect of IL-12 on immune suppression and suppressor cell induction by ultraviolet radiation. J Immunol 1995; 154: 5114-20.
86. Schwarz A, Grabbe S, Aragane Y, Sandkuhl K, Riemann H, Luger TA, Kubin M, Trinchieri G, Schwarz T. Interleukin-12 prevents ultraviolet B-induced local immunosuppression and overcomes UVB-induced tolerance. J Invest Dermatol 1996; 106: 1187-91.
87. Schmitt DA, Walterscheid JP, Ullrich SE. Reversal of ultraviolet radiation-induced immune suppression by recombinant interleukin-12: suppression of cytokine production. Immunology 2000; 101: 90-6.
88. Petersen LJ, Church MK, Skov PS. Platelet-activating factor induces histamine release from human skin mast cells in vivo, which is reduced by local nerve blockade. J Allergy Clin Immunol 1997; 99: 640-7.
89. Garssen J, Buckley TL, Van Loveren H. A role for neuropeptides in UVB-induced systemic immunosuppression. Photochem Photobiol 1998; 68: 205-10.
90. Wille JJ, Kydonieus AF, Murphy GF. cis-urocanic acid induces mast cell degranulation and release of preformed TNF-alpha: A possible mechanism linking UVB and cis-urocanic acid to immunosuppression of contact hypersensitivity. Skin Pharmacol Appl Skin Physiol 1999; 12: 18-27
91. Hart PH, Grimbaldeston MA, Finlay-Jones JJ. Sunlight, immunosuppression and skin cancer: role of histamine and mast cells. Clin Exp Pharmacol Physiol 2001; 28: 1-8.
92. Jaksic A, Finlay-Jones JJ, Watson CJ, Spencer LK, Santucci I, Hart PH. Cis-urocanic acid synergizes with histamine for increased PGE2 production by human keratinocytes: link to indomethacin-inhibitable UVB-induced immunosuppression. Photochem Photobiol 1995; 61: 303-9.
93. Elenkov IJ, Webster E, Papanicolaou DA, Fleisher TA, Chrousas GP, Wilder RL. Histamine potently suppresses human IL-12 and stimulates IL-10 production via H2 receptors. J Immunol 1998; 161: 2586-93.
94. Nghiem DX, Kazimi N, Mitchell DL, Vink AA, Ananthaswamy HN, Kripke ML, Ullrich SE. Mechanisms underlying the suppression of established immune responses by ultraviolet radiation. J Invest Dermatol 2002; 119: 600-8.
95. Halliday GM, Bestak R, Yuen KS, Cavanagh LL, Barnetson RS. UVA-induced immunosuppression. Mutat Res 1998; 422: 139-45.
96. Dumay O, Karam A, Vian L, Moyal D, Hourseau C, Stoebner P, Peyron JL, Meynadier J, Cana JP, Meunier L. Ultraviolet Al exposure of human skin results in Langerhons cell depletion and reduction of epidermal antigen-presenting cell function: partial protection by a broad-spectrum sunscreen. Br J Dermatol 2001; 144: 1161-8.
97. Moyal DD, Fourtanier AM. Broad-spectrum sunscreens provide better protection from the suppression of the elicitation phase of delayed-type hypersensitivity response in humans. J Invest Dermatol 2001; 117: 1186-92.
98. Poon TS, Barnetson RS, Halliday GM. Prevention of immunosuppression by sunscreens in humans is unrelated to protection from erythema and dependent on protection from ultraviolet A in the face of constant ultraviolet B protection. J Invest Dermatol 2003; 121: 184-90.
99. Kolgen W, Von Weelden H, Den Hengst S, Guikers KL, Kiekens RC, Knol EF, Bruijnzeel-Koomen CA, Van Vloten WA, de Gruijl FR. CD11b + cells and ultraviolet-B-resistant CD1a + cells in skin of patients with polymorphous light eruption. J Invest Dermatol 1999; 113: 4-10.
100. Beissert S, Schwarz T. Role of immunomodulation in diseases responsive to phototherapy. Methods 2002; 28: 138-44.