The immunologic revolution: Photoimmunology

Journal of Investigative Dermatology

Volumn 132, Issue 3 PART 2, 2012, Pages 896-905

  Ullrich, Stephen E ^a   Byrne, Scott N ^b  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF SYDNEY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALARMIN; CYTOKINE; UNCLASSIFIED DRUG; UROCANIC ACID;

ADAPTIVE IMMUNITY; B LYMPHOCYTE; CELL FUNCTION; DNA REPAIR; HUMAN; IMMUNE RESPONSE; IMMUNOLOGY; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; LANGERHANS CELL; LYMPH NODE; MAST CELL; NATURAL KILLER T CELL; NONHUMAN; PRIORITY JOURNAL; RADIATION EXPOSURE; REVIEW; ULTRAVIOLET RADIATION;

EID: 84856901018     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2011.405     Document Type: Review

References (86)

1. Alappatt C, Johnson CA, Clay KL et al. (2000) Acute keratinocyte damage stimulates platelet-activating factor production. Arch Dermatol Res 292:256-9 (Pubitemid 30265051)
2. Alard P, Kurimoto I, Niizeki H et al. (2001) Hapten-specific tolerance induced by acute, low-dose ultraviolet B radiation of skin requires mast cell degranulation. Eur J Immunol 31:1736-46 (Pubitemid 32547336)
3. Alard P, Niizeki H, Hanninen L et al. (1999) Local ultraviolet B irradiation impairs contact hypersensitivity induction by triggering release of tumor necrosis factor-alpha from mast cells. Involvement of mast cells and Langerhans cells in susceptibility to ultraviolet B. J Invest Dermatol 113:983-90
4. Alves-Filho JC, Sonego F, Souto FO et al. (2010) Interleukin-33 attenuates sepsis by enhancing neutrophil influx to the site of infection. Nat Med 16:708-12
5. Anglin Jr. JH, Bever AT, Everett MA et al. (1961) Ultraviolet- lightinduced alterations in urocanic acid in vivo. Biochim Biophys Acta 53: 408-9
6. Barresi C, Stremnitzer C, Mlitz V et al. (2010) Increased sensitivity of histidinemic mice to UVB radiation suggests a crucial role of endogenous urocanic acid in photoprotection. J Invest Dermatol 131:188-94
7. Beissert S, Ruhlemann D, Mohammad T et al. (2001) IL-12 prevents the inhibitory effects of cis-urocanic acid on tumor antigen presentation by Langerhans cells: Implications for photocarcinogenesis. J Immunol 167:6232-8 (Pubitemid 33081552)
8. Brown EL, Rivas JM, Ullrich SE et al. (1995) Modulation of immunity to Borrelia burgdorferi by ultraviolet irradiation: Differential effect on Th1 and Th2 immune responses. Eur J Immunol 25:3017-22
9. Bulavin DV, Higashimoto Y, Popoff IJ et al. (2001) Initiation of a G2/M checkpoint after ultraviolet radiation requires p38 kinase. Nature 411:102-7 (Pubitemid 32428198)
10. Byrne SN, Beaugie C, O'Sullivan C et al. (2011) The immune-modulating cytokine and endogenous alarmin interleukin-33 is upregulated in skin exposed to inflammatory UVB radiation. Am J Pathol 179: 211-22
11. Byrne SN, Halliday GM (2005) B cells activated in lymph nodes in response to ultraviolet irradiation or by interleukin-10 inhibit dendritic cell induction of immunity. J Invest Dermatol 124:570-8 (Pubitemid 40381580)
12. Byrne SN, Limon-Flores AY, Ullrich SE (2008) Mast cell migration from the skin to the draining lymph nodes upon ultraviolet irradiation represents a key step in the induction of immune suppression. J Immunol 180:4648-55
13. Byrne SN, Spinks N, Halliday GM (2002) Ultraviolet A irradiation of C57BL/6 mice suppresses systemic contact hypersensitivity or enhances secondary immunity depending on dose. J Invest Dermatol 119:858-64 (Pubitemid 35340911)
14. Chacon-Salinas R, Limon-Flores AY, Chavez-Blanco AD et al. (2011) Mast cell-derived IL-10 suppresses germinal center formation by affecting T follicular helper cell function. J Immunol 186:25-31
15. De Fabo EC, Noonan FP (1983) 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 157:84-98 (Pubitemid 13073514)
16. de Visser KE, Korets LV, Coussens LM (2005) De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent. Cancer Cell 7:411-23 (Pubitemid 40719125)
17. Dudeck A, Dudeck J, Scholten J et al. (2011) Mast cells are key promoters of contact allergy that mediate the adjuvant effects of haptens. Immunity 34:973-84
18. El-Ghorr AA, Horsburgh G, Norval M (1998) The effect of UVB irradiation on antibody responses during herpes simplex virus type 1 (HSV-1) infections of mice. Photodermatol Photoimmunol Photomed 14:17-25 (Pubitemid 28172733)
19. Elmets CA, Bergstresser PR, Tigelaar RE et al. (1983) Analysis of the mechanism of unresponsiveness produced by haptens painted on skin to low dose UV radiation. J Exp Med 158:781-94 (Pubitemid 13051345)
20. Fisher MS, Kripke ML (1977) Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc Natl Acad Sci USA 74:1688-92 (Pubitemid 8087041)
21. Fisher MS, Kripke ML (1978) Further studies on the tumor-specific suppressor cells induced by ultraviolet radiation. J Immunol 121:1139-44 (Pubitemid 9007544)
22. Fisher MS, Kripke ML (1982) Suppressor T lymphocytes control the development of primary skin cancers in ultraviolet-irradiated mice. Science 216:1133-4 (Pubitemid 12063276)
23. Fukunaga A, Khaskhely NM, Ma Y et al. (2010) Langerhans cells serve as immunoregulatory cells by activating NKT cells. J Immunol 185: 4633-40
24. Fukunaga A, Khaskhely NM, Sreevidya CS et al. (2008) Dermal dendritic cells, and not Langerhans cells, play an essential role in inducing an immune response. J Immunol 180:3057-64
25. Galli SJ, Grimbaldeston M, Tsai M (2008) Immunomodulatory mast cells: Negative, as well as positive, regulators of immunity. Nat Rev Immunol 8:478-86 (Pubitemid 351733419)
26. Gibbs NK, Tye J, Norval M (2008) Recent advances in urocanic acid photochemistry, photobiology and photoimmunology. Photochem Photobiol Sci 7:655-67 (Pubitemid 351798454)
27. Gorman S, Tan JW, Thomas JA et al. (2005) Primary defect in UVBinduced systemic immunomodulation does not relate to immature or functionally impaired APCs in regional lymph nodes. J Immunol 174:6677-85 (Pubitemid 40705629)
28. Greene MI, Sy MS, Kripke M et al. (1979) Impairment of antigen-presenting cell function by ultraviolet radiation. Proc Natl Acad Sci USA 76: 6591-5 (Pubitemid 10163444)
29. Grimbaldeston MA, Chen CC, Piliponsky AM et al. (2005) Mast cell-deficient W-sash c-kit mutant Kit W-sh/W-sh mice as a model for investigating mast cell biology in vivo. Am J Pathol 167:835-48 (Pubitemid 41216366)
30. Grimbaldeston MA, Green A, Darlington S et al. (2003) Susceptibility to basal cell carcinoma is associated with high dermal mast cell prevalence in non-sun-exposed skin for an Australian populations. Photochem Photobiol 78:633-9
31. Grimbaldeston MA, Nakae S, Kalesnikoff J et al. (2007) Mast cell-derived interleukin 10 limits skin pathology in contact dermatitis and chronic irradiation with ultraviolet B. Nat Immunol 8:1095-104 (Pubitemid 47423757)
32. Grimbaldeston MA, Pearce AL, Robertson BO et al. (2004) Association between melanoma and dermal mast cell prevalence in sun-unexposed skin. Br J Dermatol 150:895-903 (Pubitemid 38903521)
33. Grimbaldeston MA, Skov L, Baadsgaard O et al. (2000) Communications: High dermal mast cell prevalence is a predisposing factor for basal cell carcinoma in humans. J Invest Dermatol 115:317-20 (Pubitemid 30637205)
34. Hammerberg C, Katiyar SK, Carroll MC et al. (1998) Activated complement component 3 (C3) is required for ultraviolet induction of immunosuppression and antigenic tolerance. J Exp Med 187:1133-8 (Pubitemid 28176413)
35. Hart PH, Grimbaldeston MA, Swift GJ et al. (1998) Dermal mast cells determine susceptibility to ultraviolet B-induced systemic suppression of contact hypersensitivity responses in mice. J Exp Med 187:2045-53 (Pubitemid 28285574)
36. Hart PH, Townley SL, Grimbaldeston MA et al. (2002) Mast cells, neuropeptides, histamine, and prostaglandins in UV-induced systemic immunosuppression. Methods 28:79-89
37. Ishii S, Shimizu T (2000) Platelet-activating factor (PAF) receptor and genetically engineered PAF receptor mutant mice. Prog Lipid Res 39:41-82 (Pubitemid 30145442)
38. Kripke ML (1974) Antigenicity of murine skin tumors induced by ultraviolet light. J Natl Cancer Inst 53:1333-6
39. Kripke ML (1994) Ultraviolet radiation and immunology: Something new under the sun-presidential address. Cancer Res 54:6102-5
40. Kripke ML, Cox PA, Alas LG et al. (1992) Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice. Proc Natl Acad Sci USA 89:7516-20
41. Kronenberg M, Gapin L (2002) The unconventional lifestyle of NKT cells. Nat Rev Immunol 2:557-68 (Pubitemid 37328731)
42. Laihia JK, Kallio JP, Taimen P et al. (2010) Protodynamic intracellular acidification by cis-urocanic acid promotes apoptosis of melanoma cells in vitro and in vivo. J Invest Dermatol 130:2431-9
43. Lappin MB, Kimber I, Dearman RJ et al. (1996) Exposure of UVB-sensitive mice to immunosuppressive doses of UVB in vivo fails to affect the accessory function or the phenotype of draining lymph node dendritic cells. Exp Dermatol 5:286-94 (Pubitemid 26405651)
44. Li H, Nourbakhsh B, Safavi F et al. (2011) Kit (W-sh) mice develop earlier and more severe experimental autoimmune encephalomyelitis due to absence of immune suppression. J Immunol 187:274-82
45. Ma W, Lim W, Gee K et al. (2001) The p38 mitogen-activated kinase pathway regulates the human interleukin-10 promoter via the activation of Sp1 transcription factor in lipopolysaccharide-stimulated human macrophages. J Biol Chem 276:13664-74
46. Marathe GK, Johnson C, Billings SD et al. (2005) Ultraviolet B radiation generates platelet-activating factor-like phospholipids underlying cutaneous damage. J Biol Chem 280:35448-57 (Pubitemid 41532735)
47. Matsumura Y, Byrne SN, Nghiem DX et al. (2006) A role for inflammatory mediators in the induction of immunoregulatory B cells. J Immunol 177:4810-7 (Pubitemid 44469816)
48. Matthews YJ, Halliday GM, Phan TA et al. (2010) Wavelength dependency for UVA-induced suppression of recall immunity in humans. J Dermatol Sci 59:192-7
49. Mizoguchi A, Mizoguchi E, Takedatsu H et al. (2002) Chronic intestinal inflammatory condition generates IL-10-producing regulatory B cell subset characterized by CD1d upregulation. Immunity 16:219-30 (Pubitemid 34211962)
50. Moodycliffe AM, Nghiem D, Clydesdale G et al. (2000) Immune suppression and skin cancer development: Regulation by NKT cells. Nat Immunol 1:521-5
51. Neill DR, Wong SH, Bellosi A et al. (2010) Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature 464: 1367-70
52. Niizeki H, Alard P, Streilein JW (1997) Cutting edge: Calcitonin gene-related peptide is necessary for ultraviolet B-impaired induction of contact hypersensitivity. J Immunol 159:5183-6 (Pubitemid 127470040)
53. Norval M, Halliday GM (2011) The consequences of UV-induced immunosuppression for human health. Photochem Photobiol 87:965-77
54. Norval M, Woods GM (2011) UV-induced immunosuppression and the efficacy of vaccination. Photochem Photobiol Sci 10:1267-74
55. Okamoto H, Kripke ML (1987) Effector and suppressor circuits of the immune response are activated in vivo by different mechanisms. Proc Natl Acad Sci USA 84:3841-5 (Pubitemid 17088375)
56. Oppenheim JJ, Yang D (2005) Alarmins: Chemotactic activators of immune responses. Curr Opin Immunol 17:359-65 (Pubitemid 40848537)
57. Ramos G, Kazimi N, Nghiem DX et al. (2004) Platelet activating factor receptor binding plays a critical role in jet fuel-induced immune suppression. Toxicol Appl Pharmacol 195:331-8 (Pubitemid 38338653)
58. Reeve VE, Bosnic M, Boehm-Wilcox C et al. (1998) Ultraviolet A radiation (320-400 nm) protects hairless mice from immunosuppression induced by ultraviolet B radiation (280-320 nm) or cis-urocanic acid. Int Arch Allergy Immunol 115:316-22 (Pubitemid 28143280)
59. Schmitt DA, Owen-Schaub L, Ullrich SE (1995) Effect of IL-12 on immune suppression and suppressor cell induction by ultraviolet radiation. J Immunol 154:5114-20
60. Schwarz A, Grabbe S, Aragane Y et al. (1996) Interleukin-12 prevents ultraviolet B-induced local immunosuppression and overcomes UVBinduced tolerance. J Invest Dermatol 106:1187-91 (Pubitemid 26195843)
61. Schwarz A, Stander S, Berneburg M et al. (2002) Interleukin-12 suppresses ultraviolet radiation-induced apoptosis by inducing DNA repair. Nat Cell Biol 4:26-31 (Pubitemid 34071977)
62. Schwarz T (2008) 25 years of UV-induced immunosuppression mediated by T cells-from disregarded T suppressor cells to highly respected regulatory T cells. Photochem Photobiol 84:10-8 (Pubitemid 350265098)
63. Shen L, Ji HF (2009) Molecular basis for cis-urocanic acid as a 5-HT(2A) receptor agonist. Bioorg Med Chem Lett 19:5307-9
64. Shimizu T (2009) Lipid mediators in health and disease: Enzymes and receptors as therapeutic targets for the regulation of immunity and inflammation. Annu Rev Pharmacol Toxicol 49:123-50
65. Slominski A, Wortsman J, Tobin DJ (2005) The cutaneous serotoninergic/melatoninergic system: Securing a place under the sun. FASEB J 19:176-94 (Pubitemid 40189259)
66. Spellman CW, Anderson WL, Bernhard EJ et al. (1984) Suppression of antibody responses to topically applied antigens by ultraviolet light irradiation. Induction of phototolerance. J Exp Med 160:1891-900 (Pubitemid 15194011)
67. Sreevidya CS, Fukunaga A, Khaskhely NM et al. (2010) Agents that reverse UV-induced immune suppression and photocarcinogenesis affect DNA repair. J Invest Dermatol 130:1428-37
68. Sreevidya CS, Khaskhely NM, Fukunaga A et al. (2008) Inhibition of photocarcinogenesis by platelet-activating factor or serotonin receptor antagonists. Cancer Res 68:3978-84
69. Stapelberg MP, Williams RB, Byrne SN et al. (2009) The alternative complement pathway seems to be a UVA sensor that leads to systemic immunosuppression. J Invest Dermatol 129:2694-701
70. Stein P, Rechtsteiner G, Warger T et al. (2011) UV exposure boosts transcutaneous immunization and improves tumor immunity: Cytotoxic T-cell priming through the skin. J Invest Dermatol 131:211-9
71. Streilein JW, Toews GT, Gilliam JN et al. (1980) Tolerance or hypersensitivity to 2,4-dinitro-1-fluorobenzene: The role of Langerhans cell density within epidermis. J Invest Dermatol 74:319-22 (Pubitemid 10034229)
72. Toews GB, Bergstresser PR, Streilein JW (1980) Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J Immunol 124:445-9
73. Travers JB, Berry D, Yao Y et al. (2010) Ultraviolet B radiation of human skin generates platelet-activating factor receptor agonists. Photochem Photobiol 86:949-54
74. Travers JB, Edenberg HJ, Zhang Q et al. (2008) Augmentation of UVB radiation-mediated early gene expression by the epidermal plateletactivating factor receptor. J Invest Dermatol 128:455-60
75. Ullrich SE (2005) Mechanisms underlying UV-induced immune suppression. Mutat Res 571:185-205 (Pubitemid 40313441)
76. Ullrich SE (2008) Immune modulation by phototherapy: Why immune suppression? Expert Rev Dermatol 3:7-9 (Pubitemid 351385921)
77. Ullrich SE (2011) Ultraviolet carcinogenesis and immune suppression. In: Weber RS, Moore BA (eds) Cutaneous Malignancy of the Head and Neck: A Multidisciplinary Approach. Plural Publishing: San Diego, CA, 57-78
78. Ullrich SE, Nghiem DX, Khaskina P (2007) Suppression of an established immune response by UVA-a critical role for mast cells. Photochem Photobiol 83:1095-100 (Pubitemid 47438536)
79. Vicari AP, Zlotnik A (1996) Mouse NK1.1+ T cells: A new family of T cells. Immunol Today 17:71-6 (Pubitemid 26045593)
80. Walterscheid JP, Nghiem DX, Kazimi N et al. (2006) Cis-urocanic acid, a sunlight-induced immunosuppressive factor, activates immune suppression via the 5-HT2A receptor. Proc Natl Acad Sci USA 103:17420-5 (Pubitemid 44788984)
81. Walterscheid JP, Ullrich SE, Nghiem DX (2002) Platelet-activating factor, a molecular sensor for cellular damage, activates systemic immune suppression. J Exp Med 195:171-9 (Pubitemid 34461261)
82. Wolf P, Nghiem DX, Walterscheid JP et al. (2006) Platelet-activating factor is crucial in psoralen and ultraviolet A-induced immune suppression, inflammation, and apoptosis. Am J Pathol 169:795-805 (Pubitemid 44411947)
83. Yoshida Y, Kang K, Berger M et al. (1998) Monocyte induction of IL-10 and down-regulation of IL-12 by iC3b deposited in ultraviolet-exposed human skin. J Immunol 161:5873-9 (Pubitemid 28535953)
84. Yoshikawa T, Rae V, Bruins-Slot W et al. (1990) Susceptibility to effects of UVB radiation on induction of contact hypersensitivity as a risk factor for skin cancer in humans. J Invest Dermatol 95:530-6
85. Zhang Q, Sitzman LA, Al-Hassani M et al. (2009) Involvement of plateletactivating factor in ultraviolet B-induced hyperalgesia. J Invest Dermatol 129:167-74
86. Zhang Q, Yao Y, Konger RL et al. (2008) UVB radiation-mediated inhibition of contact hypersensitivity reactions is dependent on the plateletactivating factor system. J Invest Dermatol 128:1780-7 (Pubitemid 351847378)