Effects of solar radiation on the human immune system.

On UV irradiation of the skin, a complex cascade of immunological changes results, initiated by cutaneous chromophores and ending in suppression of some local and systemic immune responses. In this review, the stages in this process are outlined first, concentrating on the roles of DNA and urocanic acid as photoreceptors. Evidence indicating UV-induced immunomodulation of delayed hypersensitivity and resistance to infectious diseases in human subjects follows. Aspects of genetic susceptibility to the immunosuppressive effects of UV exposure and extrapolation of the data obtained in animal models to the human situation are included. Finally uncertain and unknown factors relating to the impact of UV on the human immune system are discussed.

[1]  S. Ullrich.  Does Exposure to UV Radiation Induce a Shift to a Th‐2‐like Immune Reaction? , 1996, Photochemistry and photobiology.

[2]  M. Norval,et al.  A monoclonal antibody to cis-urocanic acid prevents the ultraviolet-induced changes in Langerhans cells and delayed hypersensitivity responses in mice, although not preventing dendritic cell accumulation in lymph nodes draining the site of irradiation and contact hypersensitivity responses. , 1995, The Journal of investigative dermatology.

[3]  B. Sutherland,et al.  UV‐DNA Damage in Mouse and Human Cells Induces the Expression of Tumor Necrosis Factor α , 1998, Photochemistry and photobiology.

[4]  J. Streilein,et al.  Ultraviolet B-exposed and soluble factor-pre-incubated epidermal Langerhans cells fail to induce contact hypersensitivity and promote DNP-specific tolerance. , 1997, The Journal of investigative dermatology.

[5]  Patki Ah.  Hypothesis: solar ultraviolet radiation and the initial skin lesion of leprosy. , 1991 .

[6]  G. Murphy,et al.  cis-Urocanic Acid Induces Mast Cell Degranulation and Release of Preformed TNF--α: A Possible Mechanism Linking UVB and cis-Urocanic Acid to Immunosuppression of Contact Hypersensitivity , 1999, Skin Pharmacology and Physiology.

[7]  P. Friedmann,et al.  Antigenic stimulation during ultraviolet therapy in man does not result in immunological tolerance. , 1989, Clinical and experimental immunology.

[8]  V. Vincek,et al.  Genetic mapping and physical cloning of UVB susceptibility region in mice. , 1999, The Journal of investigative dermatology.

[9]  H. Wulf,et al.  Urocanic acid isomers: relation to body site, pigmentation, stratum corneum thickness and photosensitivity , 1997, Archives of Dermatological Research.

[10]  A. Ženíšek,et al.  Sun-screening effect of urocanic acid. , 1955, Biochimica et Biophysica Acta.

[11]  A. Zajícová,et al.  Urocanic acid enhances IL-10 production in activated CD4+ T cells. , 1998, Journal of immunology.

[12]  R. de Waal Malefyt,et al.  In contrast to their murine counterparts, normal human keratinocytes and human epidermoid cell lines A431 and HaCaT fail to express IL‐10 mRNA and protein , 1997, Clinical and experimental immunology.

[13]  T. Hamilton,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. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Frederick,et al.  BIOLOGICALLY EFFECTIVE DOSES OF SUNLIGHT FOR IMMUNE SUPPRESSION AT VARIOUS LATITUDES AND THEIR RELATIONSHIP TO CHANGES IN STRATOSPHERIC OZONE , 1990, Photochemistry and photobiology.

[15]  H. Lim,et al.  HIV, UV and immunosuppression , 1999, Photodermatology, photoimmunology & photomedicine.

[16]  H. Wulf,et al.  The sunscreening effect of urocanic acid , 1996, Photodermatology, photoimmunology & photomedicine.

[17]  B. Skov,et al.  Communications: high dermal mast cell prevalence is a predisposing factor for basal cell carcinoma in humans. , 2000, The Journal of investigative dermatology.

[18]  H. van Loveren,et al.  Cells with UV-specific DNA damage are present in murine lymph nodes after in vivo UV irradiation. , 1995, The Journal of investigative dermatology.

[19]  E. Korpi,et al.  Stereospecific modulation of GABA(A) receptor function by urocanic acid isomers. , 2000, European journal of pharmacology.

[20]  H. van Loveren,et al.  UV-induced changes in the immune response to microbial infections in human subjects and animal models. , 1999, Journal of epidemiology.

[21]  R. Manfredini,et al.  Seasonal variation in herpes zoster infection , 2000, The British journal of dermatology.

[22]  S. Ullrich,et al.  Immune suppression and skin cancer development: regulation by NKT cells , 2000, Nature Immunology.

[23]  C. Seymour,et al.  Penicillamine‐induced elastosis perforans serpiginosa and cutis laxa in Wilson’s disease , 2000 .

[24]  P. Sjövall,et al.  Local and systemic effect of ultraviolet irradiation (UVB and UVA) on human allergic contact dermatitis. , 1986, Acta dermato-venereologica.

[25]  S. Banks,et al.  Prevention of ultraviolet-light-induced herpes labialis by sunscreen , 1991, The Lancet.

[26]  Crosby,et al.  Urocanic acid isomers in patients with basal cell carcinoma and cutaneous malignant melanoma , 1998, The British journal of dermatology.

[27]  C. Bucana,et al.  Evidence that DNA damage triggers interleukin 10 cytokine production in UV-irradiated murine keratinocytes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[28]  J. V. D. van den Berg,et al.  Susceptibility to effects of UVB radiation on induction of contact hypersensitivity as a risk factor for skin cancer in humans. , 1990, The Journal of investigative dermatology.

[29]  L. Aurelian,et al.  Cutaneous ultraviolet radiation inhibits herpes simplex virus-induced lymphoproliferation in latently infected subjects. , 1994, Clinical Immunology and Immunopathology.

[30]  F. Gruijl,et al.  Risk Assessment of UVB Effects on Resistance to Infectious Diseases , 1996, Photochemistry and photobiology.

[31]  S. Beissert,et al.  Regulation of tumor antigen presentation by urocanic acid. , 1997, Journal of immunology.

[32]  M. Kripke.  Immunologic mechanisms in UV radiation carcinogenesis. , 1981, Advances in cancer research.

[33]  Simon,et al.  Ultraviolet B induced suppression of induction of contact sensitivity in human skin is not associated with tumour necrosis factor‐alpha‐308 or interleukin‐10 genetic polymorphisms , 1998 .

[34]  P. Hart,et al.  Cis‐UROCANIC ACID SYNERGIZES WITH HISTAMINE FOR INCREASED PGE2 PRODUCTION BY HUMAN KERATINOCYTES: LINK TO INDOMETHACIN‐INHIBITABLE UVB‐INDUCED IMMUNOSUPPRESSION , 1995, Photochemistry and photobiology.

[35]  Wide‐frequency Hydrophone Detection of Laser‐induced Photoacoustic Signals in Photosynthesis , 1999 .

[36]  M. A. Rie,et al.  Photoisomerization spectrum of urocanic acid in human skin and in vitro: effects of simulated solar and artificial ultraviolet radiation , 1995, The British journal of dermatology.

[37]  L. Becker,et al.  Diminished immune response in sun-damaged skin. , 1980, Archives of dermatology.

[38]  F. Gruijl,et al.  UVB exposure‐induced systemic modulation of Th1‐ and Th2‐mediated immune responses , 1999, Immunology.

[39]  R. Chervenak,et al.  Control of acute cutaneous herpes simplex virus infection : T cell-mediated viral clearance is dependent upon interferon-γ (IFN-γ) , 1994 .

[40]  M. Kripke,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. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[41]  M. Norval,et al.  Differential effects of UVA1 and UVB radiation on Langerhans cell migration in mice. , 2000, Journal of photochemistry and photobiology. B, Biology.

[42]  L. Applegate,et al.  Identification of the molecular target for the suppression of contact hypersensitivity by ultraviolet radiation , 1989, The Journal of experimental medicine.

[43]  M. Kermici,et al.  Evidence for the existence of a self-regulated enzymatic process within the human stratum corneum -an unexpected role for urocanic acid. , 2000, The Journal of investigative dermatology.

[44]  L. Bishop,et al.  Exposure to Ultraviolet Radiation Enhances Mortality and Pathology Associated with Influenza Virus Infection in Mice¶ , 2000, Photochemistry and photobiology.

[45]  S. Howie,et al.  Exposure to low-dose ultraviolet radiation suppresses delayed-type hypersensitivity to herpes simplex virus in mice. , 1986, The Journal of investigative dermatology.

[46]  T. Luger,et al.  Effect of ultraviolet light on the release of neuropeptides and neuroendocrine hormones in the skin: mediators of photodermatitis and cutaneous inflammation. , 1999, The journal of investigative dermatology. Symposium proceedings.

[47]  Kimber,et al.  The effects of ultraviolet radiation on the human immune system , 1999, The British journal of dermatology.

[48]  J. García-Foncillas,et al.  Effects of low concentrations of cis‐ and trans‐urocanic acid on cytokine elaboration by keratinocytes , 1996, Photodermatology, photoimmunology & photomedicine.

[49]  P. Cruz,et al.  FRAP DNA-dependent protein kinase mediates a late signal transduced from ultraviolet-induced DNA damage. , 2000, The Journal of investigative dermatology.

[50]  T. Kamiyama,et al.  UV-B Irradiation Increases Susceptibility of Mice to Malarial Infection , 2000, Infection and Immunity.

[51]  R Trembath,et al.  Ultraviolet B induced suppression of induction of contact sensitivity in human skin is not associated with tumour necrosis factor-alpha-308 or interleukin-10 genetic polymorphisms. , 1998, The British journal of dermatology.

[52]  H. Wulf,et al.  Seasonal Variation in Urocanic Acid Isomers in Human Skin , 1997, Photochemistry and photobiology.

[53]  L. Skov,et al.  Contrasting effects of ultraviolet-A and ultraviolet-B exposure on induction of contact sensitivity in human skin. , 1997, Clinical and experimental immunology.

[54]  M. Norval,et al.  Differential effect of phototherapy on the activities of human natural killer cells and cytotoxic T cells. , 1998, Journal of photochemistry and photobiology. B, Biology.

[55]  M. Green,et al.  Induction of interleukin-6 production by ultraviolet radiation in normal human epidermal keratinocytes and in a human keratinocyte cell line is mediated by DNA damage. , 1998, The Journal of investigative dermatology.

[56]  C. Hourseau,et al.  Immunosuppression induced by chronic solar-simulated irradiation in humans and its prevention by sunscreens , 2000 .

[57]  F. Gillardon,et al.  Calcitonin gene-related peptide, substance P and nitric oxide are involved in cutaneous inflammation following ultraviolet irradiation. , 1995, European journal of pharmacology.

[58]  F. Noonan,et al.  Dermal Mast Cells Determine Susceptibility to Ultraviolet B–induced Systemic Suppression of Contact Hypersensitivity Responses in Mice , 1998, The Journal of experimental medicine.

[59]  M. Norval,et al.  Role of tumour necrosis factor-alpha in ultraviolet B light-induced dendritic cell migration and suppression of contact hypersensitivity. , 1994, Immunology.

[60]  N. Nishimura,et al.  Interferon-γ is Involved in Photoimmunoprotection by UVA (320–400 nm) Radiation in Mice , 1999 .

[61]  J. Vandenbroucke,et al.  Incidence of skin cancer after renal transplantation in The Netherlands. , 1990, Transplantation.

[62]  M. Picot,et al.  Immunosuppression induced by acute solar-simulated ultraviolet exposure in humans: prevention by a sunscreen with a sun protection factor of 15 and high UVA protection. , 1997, Journal of the American Academy of Dermatology.

[63]  H. van Loveren,et al.  Transcription-Coupled and Global Genome Repair Differentially Influence UV-B-Induced Acute Skin Effects and Systemic Immunosuppression1 , 2000, The Journal of Immunology.

[64]  D. Hug,et al.  The degradation of L-histidine and trans- and cis-urocanic acid by bacteria from skin and the role of bacterial cis-urocanic acid isomerase. , 1999, Journal of photochemistry and photobiology. B, Biology.

[65]  G. Halliday,et al.  Ultraviolet radiation induced suppression of Mantoux reactions in humans. , 1998, The Journal of investigative dermatology.

[66]  S. Straus,et al.  Reactivation of latent herpes simplex virus infection by ultraviolet light: a human model. , 1987, Journal of the American Academy of Dermatology.

[67]  C. Potten,et al.  Sensitivity to Sunburn Is Associated with Susceptibility to Ultraviolet Radiation–Induced Suppression of Cutaneous Cell–Mediated Immunity , 2000, The Journal of experimental medicine.

[68]  C. Bucana,et al.  Localization of DNA damage and its role in altered antigen-presenting cell function in ultraviolet-irradiated mice , 1996, The Journal of experimental medicine.

[69]  K. Cooper,et al.  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. , 1995, The Journal of investigative dermatology.

[70]  J. McGregor,et al.  A single exposure of solar simulated radiation suppresses contact hypersensitivity responses both locally and systemically in humans: quantitative studies with high-frequency ultrasound. , 1998, Journal of photochemistry and photobiology. B, Biology.

[71]  J. Taylor,et al.  Suppressive and enhancing effects of ultraviolet B radiation on expression of contact hypersensitivity in man. , 1995, The Journal of investigative dermatology.

[72]  M. Norval,et al.  The effect of UV therapy on immune function in patients with psoriasis , 1993, The British journal of dermatology.

[73]  R. McKenzie,et al.  Changes in biologically active ultraviolet radiation reaching the Earth's surface. , 1998, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[74]  P. Hart,et al.  A Critical Role for Dermal Mast Cells in Cis‐Urocanic Acid‐induced Systemic Suppression of Contact Hypersensitivity Responses in Mice , 1999, Photochemistry and photobiology.

[75]  M. Norval,et al.  cis-Urocanic Acid does not Induce the Expression of Immunosuppressive Cytokines in Murine Keratinocytes¶,† , 2001, Photochemistry and photobiology.

[76]  A. Lehmann,et al.  Photocarcinogenesis and inhibition of intercellular adhesion molecule 1 expression in cells of DNA-repair-defective individuals. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[77]  L. Tuomisto,et al.  Urocanic acid binds to GABA but not to histamine (H1, H2, or H3) receptors. , 1998, The Journal of investigative dermatology.

[78]  M. Norval,et al.  UROCANIC ACID ANALOGUES AND THE SUPPRESSION OF THE DELAYED TYPE HYPERSENSITIVITY RESPONSE TO Herpes simplex VIRUS , 1989, Photochemistry and photobiology.

[79]  M. S. Fisher,et al.  Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. 1977. , 1977, Bulletin of the World Health Organization.

[80]  T. F. Cestari,et al.  Ultraviolet radiation decreases the granulomatous response to lepromin in humans. , 1995, The Journal of investigative dermatology.

[81]  J. Bluestone,et al.  Evidence for Functional Relevance of CTLA-4 in Ultraviolet-Radiation-Induced Tolerance1 , 2000, The Journal of Immunology.