UV immunosuppression and cutaneous malignancies

Expert Review of Dermatology

Volumn 6, Issue 1, 2011, Pages 61-74

  Jou, Paul C ^a   McCormick, Tom S ^a   Baron, Elma D ^a,b  

^a UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

^b LOUIS STOKES CLEVELAND VA MEDICAL CENTER   (United States)

Author keywords

basal cell carcinoma; dermal dendritic cell; DNA damage; IL 10; IL 12; Langerhans cell; melanoma; monocytes; regulatory T lymphocyte; skin cancer; squamous cell carcinoma; UV immunosuppression

Indexed keywords

CD11B ANTIGEN; COMPLEMENT FACTOR I; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; EPIGALLOCATECHIN GALLATE; ESTROGEN; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 4; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NITRIC OXIDE; OSTEOCLAST DIFFERENTIATION FACTOR; PYRIMIDINE DIMER; REACTIVE OXYGEN METABOLITE; RECEPTOR ACTIVATOR OF NUCLEAR FACTOR KAPPA B; SEROTONIN ANTAGONIST; SMALL INTERFERING RNA; STAT3 PROTEIN; SUNSCREEN; T LYMPHOCYTE RECEPTOR; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UROCANIC ACID; VITAMIN D;

ANTIGEN PRESENTING CELL; BASAL CELL CARCINOMA; CANCER RISK; CARCINOGENESIS; CD4+ CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL INFILTRATION; CELL MIGRATION; CELLULAR IMMUNITY; CHROMATOPHORE; CONTACT ALLERGY; DNA DAMAGE; DNA REPAIR; DRUG EFFECT; DRUG MECHANISM; GRAFT REJECTION; GRAFT VERSUS HOST REACTION; HUMAN; HUMORAL IMMUNITY; IMMUNE DEFICIENCY; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IMMUNOSUPPRESSIVE TREATMENT; LANGERHANS CELL; MALIGNANT TRANSFORMATION; MAST CELL; NATURAL KILLER T CELL; NONHUMAN; ORGAN TRANSPLANTATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; RADIATION EXPOSURE; RADIATION INDUCED NEOPLASM; RADIATION PROTECTION; REGULATORY T LYMPHOCYTE; REVIEW; RISK FACTOR; RNA INTERFERENCE; SKIN CARCINOMA; SKIN DISEASE; SKIN PENETRATION; SKIN PROTECTION; SQUAMOUS CELL CARCINOMA; T LYMPHOCYTE ACTIVATION; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION; ULTRAVIOLET RADIATION; UNITED STATES;

EID: 79851494835     PISSN: 17469872     EISSN: None     Source Type: Journal    
DOI: 10.1586/edm.10.72     Document Type: Review

References (125)

1. Han J, Colditz GA, Hunter DJ. Risk factors for skin cancers: a nested case-control study within the Nurses' Health Study Int. J. Epidemiol. 35(6), 1514-1521 (2006). (Pubitemid 46178928)
2. Jerant AF, Johnson JT, Sheridan CD. Early detection and treatment of skin cancer. Am. Fam. Physician 62(2), 357-368, 375-376, 381-382 (2000).
3. Wang SQ, Balagula Y, Osterwalder U. Photoprotection: a review of the current and future technologies. Dermatol. Ther. 23(1), 31-47 (2010).
4. MacKie RM, Hauschild A, Eggermont AMM. Epidemiology of cutaneous melanoma. Ann. Oncol. 20(Suppl. 6), vi1-vi7 (2009).
5. Young A, Wikonkái NM. The chronic effects of ultraviolet radiation on the skin: photocarcinogenesis. In: Photodermatology. Lim HW, Hönigsmann H, Hawk JLM (Eds). Informa Healthcare USA, NY, USA, 107-117 (2007).
6. Wang Y, DiGiovanna JJ, Stern JB et al. Evidence of ultraviolet type mutations in xeroderma pigmentosum melanomas. Proc. Natl Acad. Sci. USA 106(15), 6279-6284 (2009)
7. Burnet M. Concepts of autoimmune disease and their implication for therapy Perspect. Biol. Med. 10(2), 141-151 (1967).
8. Dunn GP, Old LJ, Schreiber RD. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21(2), 134-148 (2004).
9. Baron ED. The immune system and nonmelanoma skin cancers. In: Molecular Mechanisms of Basal Cell and Squamous Cell Carcinomas. Reichrath J (Ed.). Landes Biosciences, TX, USA, 43-48 (2006).
10. Jemec GB, Holm EA. Nonmelanoma skin cancer in organ transplant patients. Transplantation 75(3), 253-257 (2003). (Pubitemid 36222943)
11. Veness MJ. Defning patients with high-risk cutaneous squamous cell carcinoma. Australas. J. Dermatol. 47(1), 28-33 (2006).
12. Le Mire L, Hollywood K, Gray D et al. Melanomas in renal transplant recipients. Br. J. Dermatol. 154(3), 472-477 (2006). (Pubitemid 43382655)
13. Jensen P, Hansen S, Moller B et al. Skin cancer in kidney and heart transplant recipients and different long-term immunosuppressive therapy regimens. J. Am. Acad. Deramatol. 40(2), 177-186 (1999). (Pubitemid 29072794)
14. Frezza EE, Fung JJ, van Thiel DH. Non-lymphoid cancer after liver transplantation. Hepatogastroenterology 44(16), 1172-1181 (1997). (Pubitemid 27326179)
15. Dantal J, Hourmant M, Cantarovich D et al. Effect of long-term immunosuppression on kidney-graft recipients on cancer incidence: randomised comparison of two cyclosporin regimens. Lancet 351(9103), 623-628 (1998). (Pubitemid 28098444)
16. Wilkins K, Turner R, Dolev JC et al. Cutaneous malignancy and human immunodefciency virus disease. J. Am. Acad. Dermatol. 54(2), 189-206 (2006). (Pubitemid 43144386)
17. Nguyen P, Vin-Christian K, Ming ME et al. Aggressive squamous cell carcinomas in persons infected with the human immunodefciency virus. Arch. Dermatol. 138(6), 758-763 (2002). (Pubitemid 34625520)
18. Pardoll D. Does the immune system see tumors as foreign or self? Annu. Rev. Immunol. 21, 807-839 (2003). (Pubitemid 37174548)
19. Santo Domingo D, Baron ED. Melanoma and nonmelanoma skin cancers and the immune system. In: Sunlight, Vitamin D and Skin Cancer. Reichrath J (Ed.). Landes Bioscience, TX, USA, 187-202 (2008).
20. Farnoush A, Mackenzie IC. Sequential histological changes and mast cell response in skin during chemically-induced carcinogenesis. J. Oral Pathol. 12(4), 300-306 (1983).
21. Coussens LM, Werb Z. Matrix metalloproteinases and the development of cancer. Chem. Biol. 3(11), 895-904 (1996). (Pubitemid 27017088)
22. Coussens LM, Tinkle CL, Hanahan D et al. MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis. Cell 103(3), 481-490 (2000).
23. Harrell MI, Iritani BM, Ruddell A. Tumor-induced sentinel lymph node lymphangiogenesis and increased lymph fow precede melanoma metastasis. Am. J. Pathol. 170(2), 774-786 (2007). (Pubitemid 47339411)
24. + T cells in patients with melanoma. J. Immunol. 175(9), 6169-6176 (2005). (Pubitemid 41508105)
25. + T-cell responses in antitumor immunity Curr. Opin. Immunol. 10(5), 588-594 (1998). (Pubitemid 28479193)
26. + regulatory T-cells leads to tumor rejection of B16F10 melanoma, when combined with interleukin-12 gene transfer. Exp. Dermatol. 13(10), 613-620 (2004). (Pubitemid 39345270)
27. Turk MJ, Guevara-Patino JA, Rizzuto GA et al. Concomitant tumor immunity to a poorly immunogenic melanoma is prevented by regulatory T-cells. Exp. Med. 200(6), 771-782 (2004). (Pubitemid 39299463)
28. Smyth MJ, Godfrey DI, Tapani JA. A fresh look at immunosurveillance and immunotherapy Nat Immunol. 2(4), 293-299 (2001).
29. Merad M, Ginhoux F, Collin M. Origin, homeostasis, and function of langerhans cells and other langerin-expressing dendritic cells. Nat Rev. Immunol. 8(12), 935-947 (2008).
30. Schwarz T, Halliday GM. Photoimmunology. In: Photodermatology. Lim HW, Hönigsmann H, Hawk JLM (Eds). Informa Healthcare USA, NY, USA, 55-74 (2007)
31. Hanneman KK, Cooper KD, Baron ED. Ultraviolet immunosuppression: mechanisms and consequences. Dermatol. Clin. 24, 19-25 (2006). (Pubitemid 41727631)
32. Toews GB, Bergstresser PR, Streilein JW. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J. Immunol. 124(1), 445-453 (1980). (Pubitemid 10182298)
33. Aberer W, Schuler G, Stingl G et al. Ultraviolet light depletes surface markers of Langerhans cells. J. Invest Dermatol. 76(3), 202-210 (1981). (Pubitemid 11154077)
34. Noonan FP, De Fabo EC, Kripke ML. Suppression of contact hypersensitivity by ultraviolet radiation: an experimental model. Springer Semin. Immunopathol. 4(3), 293-304 (1981). (Pubitemid 12178159)
35. Morrison WL, Bucana C, Kripke ML. Systemic suppression of contact hypersensitivity by UVB radiation is unrelated to UVB-induced alterations in the morphology and number of Langerhans cells. Immunology 52(2), 299-306 (1984). (Pubitemid 14109565)
36. Schwarz T, Urbanska A, Gschnait F, Luger TA. Inhibition of the induction of contact hypersensitivity by a UV-mediated epidermal cytokine. J. Invest Dermatol. 87(2), 289-291 (1986). (Pubitemid 16041746)
37. + epidermal macrophage induction, and Langerhans cell depletion. Proc. Natl Acad. Sci. USA 89(18), 8497-8501 (1992).
38. Bennett CL, van Rijn E, Steffen J et al. Inducible ablation of mouse Langerhans cells diminishes but fails to abrogate contact hypersensitivity. J. Cell Biol. 169(4), 569-576 (2005) (Pubitemid 41002850)
39. Kissenpfennig A, Henri S, Dubois B et al. Dynamics and functions of Langerhans cells in vivo: dermal dendritic cells colonize lymph node areas distinct from slower migrating Langerhans cells. Immunity 22(5), 643-654 (2005). (Pubitemid 40719199)
40. Kaplan DH, Jenison MC, Saeland S et al. Epidermal Langerhans cell-defcient mice develop enhanced contact hypersensitivity Immunity 23(6), 611-620 (2005). (Pubitemid 41779483)
41. + monocytic/macrophagic cells J. Invest. Dermatol. 107(5), 755-763 (1996). (Pubitemid 26371094)
42. Yoshida Y, Kang K, Berger M et al. Monocyte induction of IL-10 and down-regulation of IL-12 by iC3b deposited in ultraviolet-exposed human skin. J. Immunol. 161(11) 5873-5879 (1998). (Pubitemid 28535953)
43. Yoshida Y, Kang K, Chen G et al. Cellular fbronectin is induced in ultraviolet-exposed human skin and induces IL-10 production by monocytes/macrophages. J. Invest. Dermatol. 113(1), 49-55 (1999). (Pubitemid 29328158)
44. Takahara M, Kang K, Liu Liming et al. iC3b arrests monocytic cell differentiation into CD1c-expressing dendritic cell precursors: a mechanism for transiently decreased dendritic cells in vivo after human skin injury by ultraviolet B. J. Invest. Dermatol. 120(5), 802-809 (2003). (Pubitemid 36529082)
45. Toichi E, Lu KQ, Swick AR, McCormick TS et al. Skin-infltrating monocytes/macrophages migrate to draining lymph nodes and produce IL-10 after contact sensitizer exposure to UV-irradiated skin. J. Invest. Dermatol. 128(11), 2705-2715 (2008).
46. Ritter U, Meißner A, Scheidig C et al. CD8α-and langerin-negative dendritic cells but not Langerhans cells, act as principle antigen-presenting cells in leishmaniasis. Eur. J. Immunol. 34(6), 1542-1550 (2004). (Pubitemid 39256035)
47. Fukunaga A, Khaskhely NM, Sreevidya CS et al. Dermal dendritic cells, no Langerhans cells, play an essential role in inducing an immune response. J. Immunol. 180(5), 3057-3064 (2008)
48. + dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204(13), 3119-3131 (2007).
49. + dendritic cells survey the skin in the steady state. J. Exp. Med. 204(13), 3133-3146 (2007).
50. + dendritic cells. J. Exp. Med. 204(13), 3147-3156 (2007).
51. Bobr A, Olvera-Gomez I, Igyarto BZ et al. Acute ablation of langerhans cells enhances skin immune responses. J. Immunol. 185(8), 4724-4728 (2010).
52. Fukunaga A, Khaskhely NM, Ma Y et al. Langerhans cells serve as immunoregulatory cells by activating NKT cells. J. Immunol. 185(8), 4633-4640 (2010).
53. Yoshiki R, Kabashima K, Sakabe J et al. The mandatory role of IL-10 producing OX40 ligand-expressing mature Langerhans cells in local UVB-induced immunosuppression. J. Immunol. 184(10), 5670-5677 (2010)
54. Schwartz T Mechanisms of UV-induced immunosuppression. Keio J. Med. 54(4), 165-171 (2005).
55. Schwarz A, Noordegraaf M, Maeda A et al. Langerhans cells are required for UVR-induced immunosuppression. J. Invest. Dermatol. 130(5), 1419-1427 (2010).
56. + Treg cells: highly potent regulators of diabetes that require TRANCE-RANK signals. Immunity 16(2), 183-191 (2002). (Pubitemid 34211959)
57. Loser K, Mehling A, Loeser S et al. Epidermal RANKL controls regulatory T cell numbers via activation of dendritic cells. Nat Med. 12(12), 1372-1379 (2006). (Pubitemid 44924495)
58. Norman AW. Sunlight, season, skin pigmentation, vitamin D, and 25-hydroxyvitamin D: integral components of the vitamin D endocrine system. Am. J. Clin. Nutr. 67(6), 1108-1110 (1998) (Pubitemid 28259494)
59. Schwarz T 25 Years of UV-induced immunosuppression mediated by T cells-from disregarded T suppressor cells to the highly respected regulatory T cells. Photochem. Photobiol. 84(1), 10-18 (2008). (Pubitemid 350265098)
60. Schwarz A, Beissert S, Grosse-Heitmeyer K. Evidence for functional relevance of CTLA-4 in ultraviolet-radiation-induced tolerance. J. Immunol. 165(4), 1824-1831 (2000). (Pubitemid 30643132)
61. + T regulatory cells and is dependent on host-derived IL-10. J. Immunol. 176(4), 2635-2644 (2006). (Pubitemid 43201716)
62. + T cells in lymph nodes of UVB-irradiated mice suppress immune responses to new antigens both in vitro and in vivo. J. Invest. Dermatol. 127(4), 915-924 (2007). (Pubitemid 46434643)
63. Rana S, Byrne SN, MacDonald LJ. Ultraviolet B suppresses immunity by inhibiting effector and memory T cells. Am. J. Pathol. 24(1), 127-137 (2010).
64. Balato A, Ununtmaz D, Gaspari AA. Natural killer T cells: an unconventional T-cell subset with diverse effector and regulatory functions. J. Invest. Dermatol. 129(7), 1628-1642 (2009).
65. Crowe N Y, Croquet JM, Berzins SP et al. Differential antitumor immunity mediated by NKT cell subsets in vivo. J. Exp. Med. 202(9), 1279-1288 (2005). (Pubitemid 41586958)
66. Terabe M, Swann J, Ambrosino E et al. A nonclassical non- Vα14Jα18 CD1d-restricted (type II) NKT cell is suffcient for down-regulation of tumor immunosurveillance. J. Exp. Med. 202(12), 1627-1633 (2005). (Pubitemid 41815868)
67. Moodycliffe AM, Nghiem D, Clydesdale G et al. Immunosuppression and skin cancer development: regulation by NKT cells. Nat Immunol. 1(6), 521-525 (2000).
68. Girardi M, Oppenheim DE, Steele CR et al. Regulation of cutaneous malignancy by γô T cells. Science 294(5542), 605-609 (2001).
69. Pardoll DM. Immunology. Stress, NK receptors and immune surveillance. Science 294(5542), 534-536 (2004).
70. Kim J, Modlin RL, Moy RL et al. IL-10 production in cutaneous basal and squamous cell carcinomas. a mechanism for evading the local T cell immune response. J. Immunol. 155(4), 2240-2247 (1995).
71. Rivas JM, Ullrich SE. Systemic suppression of DTH by supernatants from UV-irradiated keratinocytes: an essential role for interleukin-10. J. Immunol. 149(12), 3865-3871 (1992). (Pubitemid 23068866)
72. Enk AH, Saloga J, Becker D et al. Induction of hapten-specifc tolerance by interleukin-10 in vivo. J. Exp. Med. 179(4), 1397-1402 (1994). (Pubitemid 24091802)
73. Loser K, Apelt J, Voskort M. IL-10 controls ultraviolet-induced carcinogenesis in mice. J. Immunol. 179(1), 165-171 (2007).
74. Li-Weber M, Krammer PH. Regulation of IL4 gene expression by T cells and therapeutic perspectives. Nat Rev. Immunol. 3(7), 534-543 (2003). (Pubitemid 37328673)
75. Moore RJ, Owens DM, Stamp G et al. Mice defcient in tumor necrosis factor-α are resistant to skin carcinogenesis. Nat Med. 5(7), 828-831 (1999). (Pubitemid 29318619)
76. Schmitt DA, Owen-Schaub L, Ullrich SE. Effect of IL-12 on immune suppression and suppressor cell induction by ultraviolet radiation. J. Immunol. 154(10), 5114-5120 (1995).
77. Schmitt DA, Walterscheid JP, Ullrich SE. Reversal of ultraviolet radiation induced immunosuppression by recombinant interleukin-12: suppression of cytokine production. Immunology 101(1), 90-96 (2000).
78. Schwartz A, Stander S, Berneburg M et al. Interleukin-12 suppresses ultraviolet radiation-induced apoptosis by inducing DNA repair. J. Exp. Med. 4(1), 26-31 (2002). (Pubitemid 34071977)
79. Schwarz A, Maeda A, Kernebeck K et al. Prevention of UV radiation-induced immunosuppression by IL-12 is dependent on DNA repair. J. Exp. Med. 201(2), 173-179 (2005). (Pubitemid 40189425)
80. Walters IB, Ozawa M, Cardinale I et al. Narrowband (312-nm) UV-B suppresses interferon γ and interleukin (IL) 12 and increases IL-4 transcripts: differential regulation of cytokines at the single-cell level. Arch. Dermatol. 139(2), 155-161 (2003). (Pubitemid 36216253)
81. Schwarz A, Maeda A, Ständer S et al. IL-18 reduces ultraviolet radiation-induced DNA damage and thereby immunosuppression. J. Immunol. 176(5), 2896-2901 (2010).
82. Aoki M, Pawankar R, Niimi Y et al. Mast cells in basal cell carcinoma express VEGF, IL-8, and RANTES. Int Arch. Allergy Immunol. 130(3), 216-223 (2003). (Pubitemid 36359525)
83. Aoki M, Pawankar R, Niimi Y et al. Human mast cells release metalloproteinase-9 on contact with activated T cells: juxtacrine regulation by TNF-α. J. Immunol. 167(7), 4008-4016 (2001).
84. Hart PH, Grimbaldeston MA, Swift GJ et al. Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J. Exp. Med. 187(12), 2045-2053 (1998). (Pubitemid 28285574)
85. Byrne SN, Limón-Flores AY, Ullrich SE. Mast cells migration from the skin to the draining lymph nodes upon ultraviolet irradiation represents a key step in the induction of immune suppression. J. Immunol. 180(7), 4648-4655 (2007).
86. Yarosh DB. DNA repair, immunosuppression, and skin cancer. Cutis 74(Suppl. 5), 10-13 (2004). (Pubitemid 39612327)
87. Proietti De Santis L, Garcia CL, Balajee AS et al. Transcription coupled repair effciency determines the cell cycle progression and apoptosis after UV exposure in hamster cells. DNA Repair (AMST) 1(3), 209-223 (2002). (Pubitemid 34465483)
88. Costa RM, Chiganças V, Galhardo Rda S, Carvalho H, Menck CF. The eukaryotic nucleotide excision repair pathway. Biochimie 85(11), 1083-1099 (2003). (Pubitemid 38142363)
89. Ford JM. Regulation of DNA damage recognition and nucleotide excision repair: another role for p53. Mutat Res. 577(1-2), 195-202 (2005). (Pubitemid 41225499)
90. Besaratinia A, Synold TW, Chen HH et al. DNA lesions induced by UV A1 and B radiation in human cells: comparative analyses in the overall genome and in the p53 tumor suppressor gene. Proc. Natl Acad. Sci. USA 102(29), 10058-10063 (2005). (Pubitemid 41023325)
91. Batista LF, Kaina B, Meneghini R et al. How DNA lesions are turned into powerful killing structures: insights from UV-induced apoptosis. Mutat. Res. 681(2-3), 197-208 (2009).
92. Zhang X, Wu RS, Fu W et al. Production of reactive oxygen species and 8-hydroxyl-2́deoxyguanosine in KB cells co-exposed to benzo [a] pyrene and UV-A radiation. Chemosphere 55(10), 1303-1308 (2004). (Pubitemid 38479528)
93. Javeri A, Huang XX, Bernerd F et al. Human 8-oxoguanine-DNA glycosylase 1 protein and gene are expressed more abundantly in the superfcial than basal layer of human epidermis. DNA Repair 7(9) 1542-1550 (2008).
94. Cooper KD. Cell-mediated immunosuppressive mechanisms induced by UV radiation. Photochem. Photobiol. 63(4), 400-406 (1996). (Pubitemid 126468307)
95. Barresi C, Stremnitzer C, Mlitz V et al. Increased sensitivity of histidiniemic mice to UVB radiation suggests a crucial role of endogenous urocanic acid in photoprotection. J. Invest Dermatol. 131(1), 188-194 (2011).
96. Kammeyer A, Eggelte TA, Overmars H et al. Oxidative breakdown and conversion of urocanic acid isomers by hydroxyl radical generating systems. Biochem. Biophys. Acta 1526(2), 277-285 (2001). (Pubitemid 32532132)
97. Kurimoto I, Streilein JW. cis-urocanic acid suppression of contact hypersensitivity induction is mediated via tumor necrosis factor-α. J. Immunol. 148(10), 3072-3078 (1992).
98. Beissert ST, Mohammad H, Torri A et al. Regulation of tumor antigen presentation by urocanic acid. J. Immunol. 159(1), 92-96 (1997).
99. Gruner SW, Diezel H, Stoppe H et al. Inhibition of skin allograft rejection and acute graft-versus-host disease by cis-urocanic acid. J. Invest Dermatol. 98(4), 459-462 (1992).
100. Filipec ME, Letko Z, Haskova D et al. The effect of urocanic acid on graft rejection in an experimental model of orthotopic corneal transplantation in rabbits. Graefes Arch. Clin. Exp. Ophthalmol. 236(1), 65-68 (1998).
101. Kaneko K, Smetana-Just U, Matsui M et al. cis-urocanic acid initiates gene transcription in primary human keratinocytes. J. Immunol. 181(1), 217-224 (2008).
102. Halliday GM. Common links among the pathways leading to UV-induced immunosuppression. J. Invest. Dermatol. 130(5), 1209-1212 (2010).
103. Sreevidya CS, Fukunaga A, Khaskhely NM et al. Agents that reverse UV-induced immune suppression and photocarcinogenesis affect DNA repair. J. Invest Dermatol. 130(5), 1428-1437 (2010).
104. Katiyar SK, Challa A, McCormick TS, Cooper KD, Mukhtar H. Prevention of UVB-induced immunosuppression in mice by green tea polyphenol (-)-epigallocatechin-3-gallate may be associated with alterations in IL-10 and IL-12 production. Carcinogenesis 20(11), 2117-2124 (1999). (Pubitemid 29535313)
105. Kuchel JM, Barnetson RSC, Zhuang L et al. Tamarind inhibits solar-simulated ultraviolet radiation-induced suppression of recall responses in humans. Lett Drug Design Discov. 2(2), 165-171 (2005). (Pubitemid 40388759)
106. Camouse MM, Domingo DS, Swain FR et al. Topical application of green and white tea extracts provides protection from solar-simulated ultraviolet light in human skin. Exp. Dermatol. 18(6), 522-526 (2009).
107. Yamaguchi LF, Kato MJ, Di Mascio P. et al. Bifavonoids from Araucaria angustifolia protects against UV-induced damage. Phytochemistry 70(5), 615-620 (2009).
108. Afaq F, Zaid MA, Khan N et al. Protective effect of pomegranate-derived products on UVB-mediated damage in human reconstituted skin. Exp. Dermatol. 18(6), 553-561 (2009).
109. Matthews YJ, Halliday GM, Phan TA, Damian DL. A UVB wavelength dependency for local suppression of recall immunity in humans demonstrates a peak at 300nm. J. Invest. Dermatol. 130(6), 1680-1684 (2010).
110. Freeman SE, Hacham H, Grange RW et al. Wavelength dependence of pyrimidine dimer formation in DNA of human skin irradiated in situ with ultraviolet light. Proc. Natl Acad. Sci. USA 86(14), 5605-5609 (1989). (Pubitemid 19185593)
111. McLoone P, Simics E, Barton A et al. An action spectrum for the production of cis-urocanic acid in human skin in vivo. J. Invest. Dermatol. 124(5), 1071-1074 (2005). (Pubitemid 40629110)
112. Matthews YJ, Halliday GM, Phan TA, Damian DL. Wavelength dependency for UVA-induced suppression of recall immunity in humans. J. Dermatol. Sci. DOI: 10.1016/j.jdermsci.2010.07.005 (2010) (Epub ahead of print).
113. Furio L, Berthier-Vergnes O, Ducarre B et al. UVA radiation impairs phenotypic and functional maturation of human dermal dendritic cells. J. Invest. Dermatol. 125(5), 1032-1038 (2005).
114. Walterscheid JP, Ullrich SE, Nghiem DX. Platelet-activating factor, a molecular sensor for cellular damage, activates systemic immune suppression. J. Exp. Med. 195(2), 171-179 (2002). (Pubitemid 34461261)
115. Shreedhar V, Giese T, Sung VW et al. A cytokine cascade including prostaglandin E-2, IL-4, and IL-10 is responsible for UV-induced systemic immune suppression. J. Immunol. 160(8), 3783-3789 (1998). (Pubitemid 28176081)
116. Sasaki M, Yamaoka J, Miyachi Y. The effect of ultraviolet B irradiation on nitric oxide synthase expression in murine keratinocytes. Exp. Dermatol. 9(6), 417-422 (2000).
117. Warren JB, Loi RK, Coughlan ML. Involvement of nitric oxide synthase in the delayed vasodilator response to ultraviolet light irradiation of rat skin in vivo. Br. J. Pharmacol. 109(3), 802-806 (1993). (Pubitemid 23181064)
118. Zingarelli B, O'Connor M, Wong H et al. Peroxynitrite-mediated DNA strand breakage activates poly-adenosine diphosphate ribosyl synthase and causes cellular energy depletion in macrophages stimulated with bacterial lipopolysaccharide. J. Immunol. 156(1), 350-358 (1996). (Pubitemid 26006983)
119. Yuen KS, Nearn MR, Halliday GM. Nitric oxide-mediated depletion of Langerhans cells from the epidermis may be involved in UVA radiation-induced immunosuppression. Nitric Oxide 6(3), 313-318 (2002). (Pubitemid 34852375)
120. Russo PAJ, Halliday GM. Inhibition of nitric oxide and reactive oxygen species production improves the ability of a sunscreen to protect from sunburn, immunosuppression and photocarcinogenesis. Br. J. Dermatol. 155(2), 408-415 (2006). (Pubitemid 44050577)
121. Sano S, Chan KS, Kira M et al. Signal transducer and activator of transcription 3 is a key regulator of keratinocyte survival and proliferation following UV irradiation. Cancer Res. 65(13), 5720-5729 (2005). (Pubitemid 40911175)
122. Sumita N, Bito T, Nakajima K, Nishigori C. Stat3 activation is required for cell proliferation and tumorigenesis but not for cell viability in cutaneous squamous cell carcinoma cell lines. Exp. Dermatol. 15(4), 291-299 (2006). (Pubitemid 43349070)
123. Bito T, Sumita N, Masaki T et al. Ultraviolet light induces Stat3 activation in human keratinocytes and fbroblasts through reactive oxygen species and DNA damage. Exp. Dermatol. 19(7), 654-660 (2010).
124. Baron ED, Fourtanier A, Compan D et al. High ultraviolet A protection affords greater immune protection confrming that ultraviolet A contributes to photoimmunosuppression in humans. J. Invest. Dermatol. 121(4), 869-875 (2003). (Pubitemid 37239133)
125. Ke MS, Camouse MM, Swain FR et al. UV protective effects of DNA repair enzymes and RNA lotion. Photochem. Photobiol. 84(1), 180-184 (2008). (Pubitemid 350265092)