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Abstract

This review focuses primarily on the beneficial effects for human health of exposure to ultraviolet radiation (UVR). UVR stimulates anti-inflammatory and immunosuppressive pathways in skin that modulate psoriasis, atopic dermatitis, and vitiligo; suppresses cutaneous lesions of graft-versus-host disease; and regulates some infection and vaccination outcomes. While polymorphic light eruption and the cutaneous photosensitivity of systemic lupus erythematosus are triggered by UVR, polymorphic light eruption also frequently benefits from UVR-induced immunomodulation. For systemic diseases such as multiple sclerosis, type 1 diabetes, asthma, schizophrenia, autism, and cardiovascular disease, any positive consequences of UVR exposure are more speculative, but could occur through the actions of UVR-induced regulatory cells and mediators, including 1,25-dihydroxy vitamin D, interleukin-10, and nitric oxide. Reduced UVR exposure is a risk factor for the development of several inflammatory, allergic, and autoimmune conditions, including diseases initiated in early life. This suggests that UVR-induced molecules can regulate cell maturation in developing organs.

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2019-01-24
2024-04-18
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Literature Cited

  1. 1.  Berneburg M, Rocken M, Benedix F 2005. Phototherapy with narrowband versus broadband UVB. Acta Derm. Venereol. 85:98–108
    [Google Scholar]
  2. 2.  Mueller SN, Zaid A, Carbone FR 2014. Tissue-resident T cells: dynamic players in skin immunity. Front. Immunol. 5:332
    [Google Scholar]
  3. 3.  Fajuyigbe D, Young AR 2016. The impact of skin colour on human photobiological responses. Pigment Cell Melanoma Res 29:607–18
    [Google Scholar]
  4. 4.  Norval M, McLoone P, Lesiak A, Narbutt J 2008. The effect of chronic ultraviolet radiation on the human immune system. Photochem. Photobiol. 84:19–28
    [Google Scholar]
  5. 5.  Halliday GM 2005. Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat. Res. 571:107–20
    [Google Scholar]
  6. 6.  Brem R, Macpherson P, Guven M, Karran P 2017. Oxidative stress induced by UVA photoactivation of the tryptophan UVB photoproduct 6-formylindolo[3,2-b]carbazole (FICZ) inhibits nucleotide excision repair in human cells. Sci. Rep. 7:4310
    [Google Scholar]
  7. 7.  Kelly DA, Young AR, McGregor JM, Seed PT, Potten CS, Walker SL 2000. Sensitivity to sunburn is associated with susceptibility to ultraviolet radiation–induced suppression of cutaneous cell-mediated immunity. J. Exp. Med. 191:561–66
    [Google Scholar]
  8. 8.  Dopico XC, Evangelou M, Ferreira RC, Guo H, Pekalski ML et al. 2015. Widespread seasonal gene expression reveals annual differences in human immunity and physiology. Nat. Commun. 6:7000
    [Google Scholar]
  9. 9.  Bustamante M, Hernandez-Ferrer C, Sarria Y, Harrison GI, Nonell L et al. 2017. The acute effects of ultraviolet radiation on the blood transcriptome are independent of plasma 25OHD3. Environ. Res. 159:239–48
    [Google Scholar]
  10. 10.  Schweintzger N, Gruber-Wackernagel A, Reginato E, Bambach I, Quehenberger F et al. 2015. Levels and function of regulatory T cells in patients with polymorphic light eruption: relation to photohardening. Br. J. Dermatol. 173:519–26
    [Google Scholar]
  11. 11.  Milliken SV, Wassall H, Lewis BJ, Logie J, Barker RN et al. 2012. Effects of ultraviolet light on human serum 25-hydroxyvitamin D and systemic immune function. J. Allergy Clin. Immunol. 129:1554–61
    [Google Scholar]
  12. 12.  Yu C, Fitzpatrick A, Cong D, Yao C, Yoo J et al. 2017. Nitric oxide induces human CLA+CD25+Foxp3+ regulatory T cells with skin-homing potential. J. Allergy Clin. Immunol. 140:1441–44
    [Google Scholar]
  13. 13.  Kammeyer A, Pavel S, Asghar SS, Bos JD, Teunissen MB 1997. Prolonged increase of cis-urocanic acid levels in human skin and urine after single total-body ultraviolet exposures. Photochem. Photobiol. 65:593–98
    [Google Scholar]
  14. 14.  Holliman G, Lowe D, Cohen H, Felton S, Raj K 2017. Ultraviolet radiation-induced production of nitric oxide: a multi-cell and multi-donor analysis. Sci. Rep. 7:11105
    [Google Scholar]
  15. 15.  Hart PH, Gorman S, Finlay-Jones JJ 2011. Modulation of the immune system by UV radiation: more than just the effects of vitamin D?. Nat. Rev. Immunol. 11:584–96
    [Google Scholar]
  16. 16.  Hart PH, Norval M 2018. Ultraviolet radiation-induced immunosuppression and its relevance for skin carcinogenesis. Photochem. Photobiol. Sci. In press. https//doi.org/10.1039/C7PP00312A
    [Crossref]
  17. 17.  Ullrich SE, Byrne SN 2012. The immunologic revolution: photoimmunology. J. Investig. Dermatol. 132:896–905
    [Google Scholar]
  18. 18.  Hatakeyama M, Fukunaga A, Washio K, Taguchi K, Oda Y et al. 2017. Anti-inflammatory role of Langerhans cells and apoptotic keratinocytes in ultraviolet-B-induced cutaneous inflammation. J. Immunol. 199:2937–47
    [Google Scholar]
  19. 19.  Suwanpradid J, Holcomb ZE, MacLeod AS Emerging skin T-cell functions in response to environmental insults. J. Investig. Dermatol. 137:288–94
    [Google Scholar]
  20. 20.  van der Aar AM, Sibiryak DS, Bakdash G, van Capel TM, van der Kleij HP et al. 2011. Vitamin D3 targets epidermal and dermal dendritic cells for induction of distinct regulatory T cells. J. Allergy Clin. Immunol. 127:1532–40
    [Google Scholar]
  21. 21.  Correale J, Farez MF 2013. Modulation of multiple sclerosis by sunlight exposure: role of cis-urocanic acid. J. Neuroimmunol. 261:134–40
    [Google Scholar]
  22. 22.  Song EJ, Gordon-Thomson C, Cole L, Stern H, Halliday GM et al. 2013. 1α,25-Dihydroxyvitamin D3 reduces several types of UV-induced DNA damage and contributes to photoprotection. J. Steroid Biochem. Mol. Biol. 136:131–38
    [Google Scholar]
  23. 23.  MacLeod AS, Rudolph R, Corriden R, Ye I, Garijo O, Havran WL 2014. Skin-resident T cells sense ultraviolet radiation-induced injury and contribute to DNA repair. J. Immunol. 192:5695–702
    [Google Scholar]
  24. 24.  Schwarz A, Bruhs A, Schwarz T 2017. The short-chain fatty acid sodium butyrate functions as a regulator of the skin immune system. J. Investig. Dermatol. 137:855–64
    [Google Scholar]
  25. 25.  Felton S, Navid F, Schwarz A, Schwarz T, Glaser R, Rhodes LE 2013. Ultraviolet radiation-induced upregulation of antimicrobial proteins in health and disease. Photochem. Photobiol. Sci. 12:29–36
    [Google Scholar]
  26. 26.  Patra V, Byrne SN, Wolf P 2016. The skin microbiome: Is it affected by UV-induced immunosuppression?. Front. Microbiol. 7:1235
    [Google Scholar]
  27. 27.  Bernard JJ, Cowing-Zitron C, Nakatsuji T, Muehleisen B, Muto J et al. 2012. Ultraviolet radiation damages self noncoding RNA and is detected by TLR3. Nat. Med. 18:1286–90
    [Google Scholar]
  28. 28.  Slominski AT, Zmijewski MA, Skobowiat C, Zbytek B, Slominski RM, Steketee JD 2012. Sensing the environment: regulation of local and global homeostasis by the skin's neuroendocrine system. Adv. Anat. Embryol. Cell Biol. 212:v, vii, 1–115
    [Google Scholar]
  29. 29.  Skobowiat C, Postlethwaite AE, Slominski AT 2017. Skin exposure to ultraviolet B rapidly activates systemic neuroendocrine and immunosuppressive responses. Photochem. Photobiol. 93:1008–15
    [Google Scholar]
  30. 30.  Liu D, Fernandez BO, Hamilton A, Lang NN, Gallagher JMC et al. 2014. UVA irradiation of human skin vasodilates arterial vasculature and lowers blood pressure independently of nitric oxide synthase. J. Investig. Dermatol. 134:1839–46
    [Google Scholar]
  31. 31.  Renz H, Holt PG, Inouye M, Logan AC, Prescott SL, Sly PD 2017. An exposome perspective: early-life events and immune development in a changing world. J. Allergy Clin. Immunol. 140:24–40
    [Google Scholar]
  32. 32.  Hornsby E, Pfeffer PE, Laranjo N, Cruikshank W, Tuzova M et al. 2017. Vitamin D supplementation during pregnancy: effect on the neonatal immune system in a randomized controlled trial. J. Allergy Clin. Immunol. 141:269–78
    [Google Scholar]
  33. 33.  Miller KM, Hart PH, de Klerk NH, Davis EA, Lucas RM 2017. Are low sun exposure and/or vitamin D risk factors for type 1 diabetes?. Photochem. Photobiol. Sci. 16:381–98
    [Google Scholar]
  34. 34.  Munger KL, Hongell K, Åivo J, Soilu-Hänninen M, Surcel HM, Ascherio A 2017. 25–Hydroxyvitamin D deficiency and risk of MS among women in the Finnish Maternity Cohort. Neurology 89:1578–83
    [Google Scholar]
  35. 35.  Mahill SK, Capon F, Barker JN 2016. Update on psoriasis immunopathogenesis and targeted immunotherapy. Semin. Immunopathol. 38:11–27
    [Google Scholar]
  36. 36.  Ganguly D, Chamilos G, Lande R, Gregorio J, Meller S et al. 2009. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J. Exp. Med. 206:1983–94
    [Google Scholar]
  37. 37.  Lande R, Botti E, Jandus C, Dojcinovic D, Fanelli G et al. 2014. The antimicrobial peptide LL37 is a T-cell autoantigen in psoriasis. Nat. Comm. 5:5621
    [Google Scholar]
  38. 38.  Wolf P, Weger W, Patra V, Gruber-Wackernagel A, Byrne SN 2016. Desired response to phototherapy vs photoaggravation in psoriasis: What makes the difference?. Exp. Dermatol. 25:937–44
    [Google Scholar]
  39. 39.  Furuhashi T, Saito C, Torii K, Nishida E, Yamazaki S, Morita A 2013. Photo(chemo)therapy reduces circulating Th17 cells and restores circulating regulatory T cells in psoriasis. PLOS ONE 8:e54895
    [Google Scholar]
  40. 40.  Weatherhead SC, Farr PM, Jamieson D, Hallinan JS, Lloyd JJ et al. 2011. Keratinocyte apoptosis in epidermal remodeling and clearance of psoriasis induced by UV radiation. J. Investig. Dermatol. 131:1916–26
    [Google Scholar]
  41. 41.  Rutter KJ, Watson REB, Cotterell LF, Brenn T, Griffiths CEM, Rhodes LE 2009. Severely photosensitive psoriasis—a phenotypically defined patient subset. J. Investig. Dermatol. 129:2861–67
    [Google Scholar]
  42. 42.  Silverberg JI, Hanifin J, Simpson EL 2013. Climatic factors are associated with childhood eczema prevalence in the United States. J. Investig. Dermatol. 133:1752–59
    [Google Scholar]
  43. 43.  Hoffjan S, Stemmler S 2015. Unravelling the complex genetic background of atopic dermatitis: from genetic association results towards novel therapeutic strategies. Arch. Dermatol. Res. 307:659–70
    [Google Scholar]
  44. 44.  Garritsen FM, Brouwer MWD, Limpens J, Spuls PI 2014. Photo(chemo)therapy in the management of atopic dermatitis: an updated systematic review with implications for practice and research. Br. J. Dermatol. 170:501–13
    [Google Scholar]
  45. 45.  Tintle S, Shemer A, Suárez-Fariñas M, Fujita H, Gilleaudeau P et al. 2011. Reversal of atopic dermatitis with narrow-band UVB phototherapy and biomarkers for therapeutic response. J. Allergy Clin. Immunol. 128:583–93
    [Google Scholar]
  46. 46.  Suárez-Fariñas M, Gittler JK, Shemer A, Cardinale I, Krueger JG, Guttman-Yassky E 2013. Residual genomic signature of atopic dermatitis despite clinical resolution with narrow-band UVB. J. Allergy Clin. Immunol. 131:577–79
    [Google Scholar]
  47. 47.  Gambichler T, Kreuter A, Tomi NS, Othlinghaus N, Altmeyer P, Skrygan M 2008. Gene expression of cytokines in atopic eczema before and after ultraviolet A1 phototherapy. Br. J. Dermatol. 158:1117–20
    [Google Scholar]
  48. 48.  Grabbe J, Welker P, Humke S, Grewe M, Schöpf E et al. 1996. High-dose ultraviolet A1 (UVA1), but not UVA/UVB therapy, decreases IgE-binding cells in lesional skin of patients with atopic eczema. J. Investig. Dermatol. 107:419–22
    [Google Scholar]
  49. 49.  Yoshimura M, Namura S, Akamatsu H, Horio T 1996. Antimicrobial effects of phototherapy and photochemotherapy in vivo and in vitro. Br. J. Dermatol. 135:528–32
    [Google Scholar]
  50. 50.  Gambichler T, Skrygan M, Tomi NS, Altmeyer P, Kreuter A 2006. Changes of antimicrobial peptide mRNA expression in atopic eczema following phototherapy. Br. J. Dermatol. 155:1275–78
    [Google Scholar]
  51. 51.  Silva SH, Guedes ACM, Gontijo B, Ramos AM, Carmo LS et al. 2006. Influence of narrow-band UVB phototherapy on cutaneous microbiota of children with atopic dermatitis. J. Eur. Acad. Dermatol. Venereol. 20:1114–20
    [Google Scholar]
  52. 52.  Muehleisen B, Gallo RL 2013. Vitamin D in allergic disease: shedding light on a complex problem. J. Allergy Clin. Immunol. 131:324–29
    [Google Scholar]
  53. 53.  Vähävihu K, Ala-Houhala M, Peric M, Karisola P, Kautiainen H et al. 2010. Narrowband ultraviolet B treatment improves vitamin D balance and alters antimicrobial peptide expression in skin lesions of psoriasis and atopic dermatitis. Br. J. Dermatol. 163:321–28
    [Google Scholar]
  54. 54.  Ellenbogen E, Wesselmann U, Hofmann SC, Lehmann P 2016. Photosensitive atopic dermatitis—a neglected subset: clinical, laboratory, histological and photobiological workup. J. Eur. Acad. Dermatol. Venereol. 3:270–75
    [Google Scholar]
  55. 55.  Rhodes LE, Bock M, Janssens AS, Ling TC, Anastasopoulou L et al. 2010. Polymorphic light eruption occurs in 18% of Europeans and does not show higher prevalence with increasing latitude: multicenter survey of 6,895 individuals residing from the Mediterranean to Scandinavia. J. Investig. Dermatol. 130:626–28
    [Google Scholar]
  56. 56.  Gruber-Wackernagel A, Byrne SN, Wolf P 2014. Polymorphous light eruption: clinic aspects and pathogenesis. Dermatol. Clin. 32:315–34
    [Google Scholar]
  57. 57.  Schornagel IJ, Sigurdsson V, Nijhuis EH, Bruijnzeel-Koomen CA, Knol EF 2004. Decreased neutrophil skin infiltration after UVB exposure in patients with polymorphous light eruption. J. Investig. Dermatol. 123:202–6
    [Google Scholar]
  58. 58.  Wolf P, Gruber-Wackernagel A, Bambach I, Schmidbauer U, Mayer G et al. 2014. Photohardening of polymorphic light eruption patients decreases baseline epidermal Langerhans cell density while increasing mast cell numbers in the papillary dermis. Exp. Dermatol. 23:428–30
    [Google Scholar]
  59. 59.  Palmer RA, Friedmann PS 2004. Ultraviolet radiation causes less immunosuppression in patients with polymorphic light eruption than in controls. J. Investig. Dermatol. 122:291–94
    [Google Scholar]
  60. 60.  Gruber-Wackernagel A, Obermayer-Pietsch B, Byrne SN, Wolf P 2012. Patients with polymorphic light eruption have decreased serum levels of 25-hydroxyvitamin-D3 that increase upon 311 nm UVB photohardening. Photochem. Photobiol. Sci. 11:1831–36
    [Google Scholar]
  61. 61.  Janssens AS, Pavel S, Out-Luiting JJ, Willemze R, de Gruijl FR 2005. Normalized ultraviolet (UV) induction of Langerhans cell depletion and neutrophil infiltrates after artificial UVB hardening of patients with polymorphic light eruption. Br. J. Dermatol. 152:1268–74
    [Google Scholar]
  62. 62.  Tsokos GC, Lo MS, Costa Reis P, Sullivan KE 2016. New insights into the immunopathogenesis of systemic lupus erythematosus. Nat. Rev. Rheumatol. 12:716–30
    [Google Scholar]
  63. 63.  Takagi H, Arimura K, Uto T, Fukaya T, Nakamura T et al. 2016. Plasmacytoid dendritic cells orchestrate TLR7-mediated innate and adaptive immunity for the initiation of autoimmune inflammation. Sci. Rep. 6:24477
    [Google Scholar]
  64. 64.  Li ZJ, Sohn KC, Choi DK, Shi G, Hong D et al. 2014. Roles of TLR7 in activation of NF-κB signaling of keratinocytes by imiquimod. PLOS ONE 8:e77159
    [Google Scholar]
  65. 65.  Yokogawa A, Takaishi M, Nakajima K, Kamijima R, Fujimoto C et al. 2014. Epicutaneous application of Toll-like receptor 7 agonists leads to systemic autoimmunity in wild-type mice: a new model of systemic lupus erythematosus. Arthritis Rheumatol 66:694–706
    [Google Scholar]
  66. 66.  Kemp MG, Lindsey-Boltz LA, Sancar A 2015. UV light potentiates STING (Stimulator of Interferon Genes)-dependent innate immune signaling through deregulation of ULK1 (Unc51-like Kinase 1). J. Biol. Chem. 290:12184–94
    [Google Scholar]
  67. 67.  Birner P, Heider S, Petzelbauer P, Wolf P, Kornauth C et al. 2016. Interleukin-6 receptor alpha blockade improves skin lesions in a murine model of systemic lupus erythematosus. Exp. Dermatol. 25:305–10
    [Google Scholar]
  68. 68.  Shoenfeld Y, Giacomelli R, Azrielant S, Berardicurti O, Reynolds JA, Bruce IN 2018. Vitamin D and systemic lupus erythematosus—the hype and the hope. Autoimmun. Rev. 17:19–23
    [Google Scholar]
  69. 69.  Schmidt E, Tony HP, Bröcker EB, Kneitz C 2007. Sun-induced life-threatening lupus nephritis. Ann. N.Y. Acad. Sci. 1108:35–40
    [Google Scholar]
  70. 70.  McGrath H Jr. 2017. Ultraviolet-A1 irradiation therapy for systemic lupus erythematosus. Lupus 26:1239–51
    [Google Scholar]
  71. 71.  Szegedi A, Simics E, Aleksza M, Horkay I, Gaal K et al. 2005. Ultraviolet-A1 phototherapy modulates Th1/Th2 and Tc1/Tc2 balance in patients with systemic lupus erythematosus. Rheumatology 44:925–31
    [Google Scholar]
  72. 72.  van den Boorn JG, Konijnenberg D, Dellemijn TA, van der Veen JP, Bos JD et al. 2009. Autoimmune destruction of skin melanocytes by perilesional T cells from vitiligo patients. J. Investig. Dermatol. 129:2220–32
    [Google Scholar]
  73. 73.  Harris JE, Harris TH, Weninger W, Wherry EJ, Hunter CA, Turka LA 2012. A mouse model of vitiligo with focused epidermal depigmentation requires IFN-γ for autoreactive CD8+ T-cell accumulation in the skin. J. Investig. Dermatol. 132:1869–76
    [Google Scholar]
  74. 74.  Jian Z, Li K, Song P, Zhu G, Zhu L et al. 2014. Impaired activation of the Nrf2–ARE signaling pathway undermines H2O2-induced oxidative stress response: a possible mechanism for melanocyte degeneration in vitiligo. J. Investig. Dermatol. 134:2221–30
    [Google Scholar]
  75. 75.  Frisoli ML, Harris JE 2017. Vitiligo: Mechanistic insights lead to novel treatments. J. Allergy Clin. Immunol. 140:654–62
    [Google Scholar]
  76. 76.  Bae JM, Jung HM, Hong BY, Lee JH, Choi WJ et al. 2017. Phototherapy for vitiligo: a systematic review and meta-analysis. JAMA Dermatol 153:666–74
    [Google Scholar]
  77. 77.  Goldstein NB, Koster MI, Hoaglin LG, Spoelstra NS, Kechris KJ et al. 2015. Narrow band ultraviolet B treatment for human vitiligo is associated with proliferation, migration, and differentiation of melanocyte precursors. J. Investig. Dermatol. 135:2068–76
    [Google Scholar]
  78. 78.  Yamada T, Hasegawa S, Inoue Y, Date Y, Yamamoto N et al. 2013. Wnt/β-catenin and Kit signaling sequentially regulate melanocyte stem cell differentiation in UVB-induced epidermal pigmentation. J. Investig. Dermatol. 133:2753–62
    [Google Scholar]
  79. 79.  Tembhre MK, Sharma VK, Sharma A, Chattopadhyay P, Gupta S 2013. T helper and regulatory T cell cytokine profile in active, stable and narrow band ultraviolet B treated generalized vitiligo. Clin. Chim. Acta 424:27–32
    [Google Scholar]
  80. 80.  Sehrawat M, Arora TC, Chauhan A, Kar HK, Poonia A, Jairath V 2014. Correlation of vitamin D levels with pigmentation in vitiligo patients treated with NBUVB therapy. ISRN Dermatol 2014:493213
    [Google Scholar]
  81. 81.  Hegazy RA, Fawzy MM, Gawdat HI, Samir N, Rashed LA 2014. T helper 17 and Tregs: a novel proposed mechanism for NB-UVB in vitiligo. Exp. Dermatol. 23:283–86
    [Google Scholar]
  82. 82.  Moftah NH, El-Barbary RA, Ismail MA, Ali NA 2014. Effect of narrow band-ultraviolet B on CD4+CD25highFoxP3+ T-lymphocytes in the peripheral blood of vitiligo patients. Photodermatol. Photoimmunol. Photomed. 30:254–61
    [Google Scholar]
  83. 83.  Mosenson JA, Eby JM, Hernandez C, Le Poole IC 2013. A central role for inducible heat-shock protein 70 in autoimmune vitiligo. Exp. Dermatol. 22:566–69
    [Google Scholar]
  84. 84.  Garburcheon-Singh KB, Frenandez-Penas P 2015. Phototherapy for the treatment of cutaneous graft versus host disease. Australas. J. Dermatol. 56:93–99
    [Google Scholar]
  85. 85.  Kavand S, Lehman JS, Hashmi S, Gibson LE, El-Azhary RA 2017. Cutaneous manifestations of graft-versus-host disease: role of the dermatologist. Int. J. Dermatol. 56:131–40
    [Google Scholar]
  86. 86.  Kreutz M, Karrer S, Hoffmann P, Gottfried E, Szeimies RM et al. 2012. Whole-body UVB irradiation during allogeneic hematopoietic cell transplantation is safe and decreases acute graft-versus-host disease. J. Investig. Dermatol. 132:179–87
    [Google Scholar]
  87. 87.  Gruner S, Diezel W, Stoppe H, Oesterwitz H, Henke W 1992. Inhibition of skin allograft rejection and acute graft-versus-host disease by cis-urocanic acid. J. Investig. Dermatol. 98:459–62
    [Google Scholar]
  88. 88.  Iyama S, Murase K, Sato T, Hashimoto A, Tatekoshi A et al. 2014. Narrowband ultraviolet B phototherapy ameliorates acute graft-versus-host disease by a mechanism involving in vivo expansion of CD4+CD25+Foxp3+ regulatory T cells. Int. J. Hematol. 99:471–76
    [Google Scholar]
  89. 89.  Norval M, Garssen J, Van Loveren H, El-Ghorr AA 1999. UV-induced changes in the immune response to microbial infections in human subjects and animal models. J. Epidemiol. 9:Suppl.S84–92
    [Google Scholar]
  90. 90.  Moyal D, Fourtanier A 2008. Broad-spectrum sunscreens provide better protection from solar ultraviolet-simulated radiation and natural sunlight-induced immunosuppression in human beings. J. Am. Acad. Dermatol. 58:Suppl. 2S149–54
    [Google Scholar]
  91. 91.  Sivapirabu G, Yiasemides E, Halliday GM, Park J, Damian DL 2009. Topical nicotinamide modulates cellular energy metabolism and provides broad-spectrum protection against ultraviolet radiation-induced immunosuppression in humans. Br. J. Dermatol. 161:1357–64
    [Google Scholar]
  92. 92.  Norval M 2006. The effect of ultraviolet radiation on human viral infections. Photochem. Photobiol. 82:1495–504
    [Google Scholar]
  93. 93.  Korostil IA, Regan DG 2016. Varicella-zoster virus in Perth, Western Australia: seasonality and reactivation. PLOS ONE 11:e0151319
    [Google Scholar]
  94. 94.  Cahoon EK, Engels EA, Freedman DM, Norval M, Pfeiffer RM 2016. Ultraviolet radiation and Kaposi sarcoma incidence in a nationwide US cohort of HIV-infected men. J. Natl. Cancer Inst 109:djw267
    [Google Scholar]
  95. 95.  Autier P, Mullie P, Macacu A, Dragomir M, Boniol M et al. 2017. Effect of vitamin D supplements on non-skeletal disorders: a systematic review of meta-analyses and randomised trials. Lancet Diabetes Endocrinol 5:986–1004
    [Google Scholar]
  96. 96.  Martineau AR, Jolliffe DA, Hooper RL, Greenberg L, Aloia JF et al. 2017. Vitamin D supplementation to prevent acute respiratory tract infections: systematic review and meta-analysis of individual participant data. BMJ 356:i6583
    [Google Scholar]
  97. 97.  Bolland MJ, Avenell A 2017. Do vitamin D supplements help to prevent respiratory tract infections?. BMJ 356:j456
    [Google Scholar]
  98. 98.  Boere TM, Visser DH, van Furth AM, Lips P, Cobelens FG 2017. Solar ultraviolet B exposure and global variation in tuberculosis incidence: an ecological analysis. Eur. Respir. J. 49:1601979
    [Google Scholar]
  99. 99.  Venturini E, Facchini L, Martinez-Alier N, Novelli V, Galli L et al. 2014. Vitamin D and tuberculosis: a multicentre study in children. BMJ Infect. Dis. 14:652
    [Google Scholar]
  100. 100.  Zeng J, Wu G, Yang W, Gu X, Liang VV et al. 2015. A serum vitamin D level <25nmol/L pose high tuberculosis risk: a meta-analysis. PLOS ONE 10:e0126014
    [Google Scholar]
  101. 101.  Ralph AP, Lucas RM, Norval M 2013. Vitamin D and solar ultraviolet radiation in the risk and treatment of tuberculosis. Lancet Infect. Dis. 13:77–88
    [Google Scholar]
  102. 102.  Norval M, Woods GM 2011. UV-induced immunosuppression and the efficacy of vaccination. Photochem. Photobiol. 10:1267–74
    [Google Scholar]
  103. 103.  Colditz GA, Brewer TF, Berkey CS, Wilson ME, Burdick E et al. 1994. Efficacy of BCG vaccine in the prevention of tuberculosis: meta-analysis of the published literature. JAMA 271:698–702
    [Google Scholar]
  104. 104.  Sleijffers A, Garssen J, de Gruijl FR, Boland GJ, van Hattum J et al. 2001. Influence of ultraviolet B exposure on immune responses following hepatitis B vaccination in human volunteers. J. Investig. Dermatol. 117:1144–50
    [Google Scholar]
  105. 105.  Sleijffers A, Yucesoy B, Kashon M, Garssen J, de Gruijl FR et al. 2003. Cytokine polymorphisms play a role in susceptibility to ultraviolet B–induced modulation of immune responses after hepatitis B vaccination. J. Immunol. 170:3423–28
    [Google Scholar]
  106. 106.  Sleijffers A, Kammeyer A, de Gruijl FR, Boland GJ, van Hattum J et al. 2003. Epidermal cis-urocanic acid levels correlate with lower specific cellular immune responses after hepatitis B vaccination of ultraviolet B–exposed humans. Photochem. Photobiol. 77:271–75
    [Google Scholar]
  107. 107.  Bryson KJ, Nash AA, Norval M 2014. Does vitamin D protect against respiratory viral infections?. Epidemiol. Infect. 142:1789–96
    [Google Scholar]
  108. 108.  Sadarangani SP, Whitaker JA, Poland GA 2015. “Let there be light”: the role of vitamin D in the immune response to vaccines. Expert Rev. Vaccines 14:1427–40
    [Google Scholar]
  109. 109.  Fell GL, Robinson KC, Mao J, Woolf CJ, Fisher DE 2014. Skin β-endorphin mediates addiction to UV light. Cell 157:1527–34
    [Google Scholar]
  110. 110.  Magina S, Esteves-Pinto C, Moura E, Serrão MP, Moura D et al. 2011. Inhibition of basal and ultraviolet B–induced melanogenesis by cannabinoid CB1 receptors: a keratinocyte-dependent effect. Arch. Dermatol. Res. 303:201–10
    [Google Scholar]
  111. 111.  Watad A, Azrielant S, Bragazzi NL, Sharif K, David P et al. 2017. Seasonality and autoimmune diseases: the contribution of the four seasons to the mosaic of autoimmunity. J. Autoimmun. 82:13–30
    [Google Scholar]
  112. 112.  Dankers W, Colin EM, van Hamburg JP, Lubberts E 2017. Vitamin D in autoimmunity: molecular mechanisms and therapeutic potential. Front. Immunol. 7:697
    [Google Scholar]
  113. 113.  Rübsamen D, Kunze MM, Buderus V, Brauß TF, Bajer MM et al. 2014. Inflammatory conditions induce IRES-dependent translation of cyp24a1. PLOS ONE 9:e85314
    [Google Scholar]
  114. 114.  Bragazzi NL, Watad A, Neumann SG, Simon M, Brown SB et al. 2017. Vitamin D and rheumatoid arthritis: an ongoing mystery. Curr. Opin. Rheumatol. 29:378–88
    [Google Scholar]
  115. 115.  Lucas RM, Ponsonby AL, Dear K, Valery PC, Pender MP et al. 2011. Sun exposure and vitamin D are independent risk factors for CNS demyelination. Neurology 76:540–48
    [Google Scholar]
  116. 116.  Langer-Gould A, Lucas RM, Xiang AH, Wu J, Chen LH et al. 2018. Vitamin D-binding protein polymorphisms, 25-hydroxyvitamin D, sunshine and multiple sclerosis. Nutrients 10:184
    [Google Scholar]
  117. 117.  Simpson S, van der Mei I, Lucas RM, Ponsonby AL, Bradley S et al. 2018. Sun exposure across the life course significantly modulates early multiple sclerosis clinical course. Front. Neurol. 9:16
    [Google Scholar]
  118. 118.  Zivadinov R, Treu CN, Weinstock-Guttman B, Turner C, Bergsland N et al. 2013. Interdependence and contributions of sun exposure and vitamin D to MRI measures in multiple sclerosis. J. Neurol. Neurosurg. Psychiatry 84:1075–81
    [Google Scholar]
  119. 119.  Knippenberg S, Damoiseaux J, Bol Y, Hupperts R, Taylor BV et al. 2014. Higher levels of reported sun exposure, and not vitamin D status, are associated with less depressive symptoms and fatigue in multiple sclerosis. Acta Neurol. Scand. 129:123–31
    [Google Scholar]
  120. 120.  Breuer J, Schwab N, Schneider-Hohendorf T, Marziniak M, Mohan H et al. 2014. Ultraviolet B light attenuates the systemic immune response in central nervous system autoimmunity. Ann. Neurol. 75:739–58
    [Google Scholar]
  121. 121.  Hart PH, Lucas RM, Booth DR, Carroll WM, Nolan D et al. 2017. Narrowband UVB phototherapy for clinically isolated syndrome: a trial to deliver the benefits of vitamin D and other UVB-induced molecules. Front. Immunol. 8:3
    [Google Scholar]
  122. 122.  Muris AH, Smolders J, Rolf L, Thewissen M, Hupperts R et al. 2016. Immune regulatory effects of high dose vitamin D3 supplementation in a randomized controlled trial in relapsing remitting multiple sclerosis patients receiving IFNβ; the SOLARIUM study. J. Neuroimmunol. 300:47–56
    [Google Scholar]
  123. 123.  Becklund BR, Severson KS, Vang SV, DeLuca HF 2010. UV radiation suppresses experimental autoimmune encephalomyelitis independent of vitamin D production. PNAS 107:6418–23
    [Google Scholar]
  124. 124.  Luthold RV, Fernandes GR, Franco-de-Moraes AC, Folchetti LG, Ferreira SR 2017. Gut microbiota interactions with the immunomodulatory role of vitamin D in normal individuals. Metabolism 69:76–86
    [Google Scholar]
  125. 125.  Berer K, Gerdes LA, Cekanaviciute E, Jia X, Xiao L et al. 2017. Gut microbiota from multiple sclerosis patients enables spontaneous autoimmune encephalomyelitis in mice. PNAS 114:10719–24
    [Google Scholar]
  126. 126.  Yadav SK, Boppana S, Ito N, Mindur JE, Mathay MT et al. 2017. Gut dysbiosis breaks immunological tolerance toward the central nervous system during young adulthood. PNAS 114:E9318–27
    [Google Scholar]
  127. 127.  Kok LF, Marsh-Wakefield F, Marshall JE, Gillis C, Halliday GM, Byrne SN 2016. B cells are required for sunlight protection of mice from a CNS-targeted autoimmune attack. J. Autoimmun. 73:10–23
    [Google Scholar]
  128. 128.  Altieri B, Muscogiuri G, Barrea L, Mathieu C, Vallone CV et al. 2017. Does vitamin D play a role in autoimmune endocrine disorders? A proof of concept. Rev. Endocr. Metab. Disord. 18:335–46
    [Google Scholar]
  129. 129.  Krstic G 2011. Asthma prevalence associated with geographical latitude and regional isolation in the United States of America and Australia. PLOS ONE 6:e18492
    [Google Scholar]
  130. 130.  Hollams EM, Teo SM, Kusel M, Holt BJ, Holt KE et al. 2017. Vitamin D over the first decade and susceptibility to childhood allergy and asthma. J. Allergy Clin. Immunol. 139:472–81
    [Google Scholar]
  131. 131.  Pfeffer PE, Hawrylowicz CM 2018. Translating basic research into clinical practice: vitamin D in asthma—mechanisms of action and considerations for clinical trials. Chest 153:1229–39
    [Google Scholar]
  132. 132.  Jolliffe DA, Greenberg L, Hooper RL, Griffiths CJ, Camargo CA Jr. et al. 2017. Vitamin D supplementation to prevent asthma exacerbations: a systematic review and meta-analysis of individual participant data. Lancet Respir. Med. 5:881–90
    [Google Scholar]
  133. 133.  Vinkhuyzen AA, Eyles DW, Burne TH, Blanken LM, Kruithof CJ et al. 2016. Gestational vitamin D deficiency and autism-related traits: the Generation R Study. Mol. Psychiatry 23:240–46
    [Google Scholar]
  134. 134.  Cui X, Gooch H, Petty A, McGrath JJ, Eyles D 2017. Vitamin D and the brain: genomic and non-genomic actions. Mol. Cell. Endocrinol. 453:131–43
    [Google Scholar]
  135. 135.  Annweiler C, Bartha R, Karras SN, Gautier J, Roche F, Beauchet O 2015. Vitamin D and white matter abnormalities in older adults: a quantitative volumetric analysis of brain MRI. Exp. Gerontol. 63:41–47
    [Google Scholar]
  136. 136.  Wang T, Shan L, Du L, Feng J, Xi Z et al. 2016. Serum concentration of 25-hydroxyvitamin D in autism spectrum disorder: a systematic review and meta-analysis. Eur. Child Adolesc. Psychiatry 25:341–50
    [Google Scholar]
  137. 137.  Hart PH, Lucas RM, Walsh JP, Zosky GR, Whitehouse AJ et al. 2015. Vitamin D in fetal development: findings from a birth cohort study. Pediatrics 135:e167–73
    [Google Scholar]
  138. 138.  Grant WB, Cannell JJ 2013. Autism prevalence in the United States with respect to solar UV-B doses: an ecological study. Dermatoendocrinology 5:159–64
    [Google Scholar]
  139. 139.  Lindqvist PG, Landin-Olsson H 2017. The relationship between sun exposure and all-cause mortality. Photochem. Photobiol. Sci. 16:354–61
    [Google Scholar]
  140. 140.  Vimaleswaran KS, Cavadino A, Berry DJ, LifeLines Cohort Study Investigators, Jorde R et al. 2014. Association of vitamin D status with arterial blood pressure and hypertension risk: a Mendelian randomisation study. Lancet Diabetes Endocrinol 2:719–29
    [Google Scholar]
  141. 141.  Beveridge LA, Struthers AD, Khan F, Jorde R, Scragg R et al. 2015. Effect of vitamin D supplementation on blood pressure: a systematic review and meta-analysis incorporating individual patient data. JAMA Intern. Med. 175:745–54
    [Google Scholar]
  142. 142.  Geldenhuys S, Hart PH, Endersby R, Jacoby P, Feelisch M et al. 2014. Ultraviolet radiation suppresses obesity and symptoms of metabolic syndrome independently of vitamin D in mice fed a high-fat diet. Diabetes 69:3759–69
    [Google Scholar]
  143. 143.  Ye Z, Sharp SJ, Burgess S, Scott RA, Imamura F et al. 2015. Association between circulating 25-hydroxyvitamin D and incident type 2 diabetes: a Mendelian randomisation study. Lancet Diabetes Endocrinol 3:35–42
    [Google Scholar]
  144. 144.  Correa-Rodríguez M, Carrillo-Ávila JA, Schmidt-RioValle J, González-Jiménez E, Vargas S et al. 2018. Genetic association analysis of vitamin D receptor gene polymorphisms and obesity-related phenotypes. Gene 640:51–56
    [Google Scholar]
  145. 145.  Carrelli A, Bucovsky M, Horst R, Cremers S, Zhang C et al. 2017. Vitamin D storage in adipose tissue of obese and normal weight women. J. Bone Miner. Res. 32:237–42
    [Google Scholar]
  146. 146.  Witztum JL, Lichtman AH 2014. The influence of innate and adaptive immune responses on atherosclerosis. Annu. Rev. Pathol. Mech. Dis. 9:73–102
    [Google Scholar]
  147. 147.  Sasaki N, Yamashita T, Kasahara K, Fukunaga A, Yamaguchi T et al. 2017. UVB exposure prevents atherosclerosis by regulating immunoinflammatory responses. Arterioscler. Thromb. Vasc. Biol. 37:66–74
    [Google Scholar]
  148. 148.  Kim S, Kim H, Yim YS, Ha S, Atarashi K et al. 2017. Maternal gut bacteria promote neurodevelopmental abnormalities in mouse offspring. Nature 549:528–32
    [Google Scholar]
  149. 149.  Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G et al. 2012. Host-gut microbiota metabolic interactions. Science 336:1262–67
    [Google Scholar]
  150. 150.  Shin Yim Y, Park A, Berrios J, Lafourcade M, Pascual LM et al. 2017. Reversing behavioural abnormalities in mice exposed to maternal inflammation. Nature 549:482–87
    [Google Scholar]
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