A critical role for the proapoptotic protein bid in ultraviolet-induced immune suppression and cutaneous apoptosis

Journal of Immunology

Volumn 181, Issue 5, 2008, Pages 3077-3088

  Pradhan, Sanjay ^a   Hee, Kyung Kim ^a   Thrash, Christopher J ^a   Cox, Maureen A ^b   Mantena, Sudheer K ^a   Wu, Jian He ^a   Athar, Mohammad ^a   Katiyar, Santosh K ^a   Elmets, Craig A ^a   Timares, Laura ^a,b,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HAPTEN; PROTEIN BID; APOPTOSIS REGULATORY PROTEIN; BID PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA DAMAGE; FEMALE; HYPERSENSITIVITY; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; KERATINOCYTE; LANGERHANS CELL; LIFESPAN; LYMPH NODE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SKIN SENSITIZATION; ULTRAVIOLET RADIATION; WILD TYPE; ANIMAL; CYTOLOGY; MOUSE MUTANT; PHYSIOLOGY; RADIATION EXPOSURE; SKIN;

ANIMALS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; BH3 INTERACTING DOMAIN DEATH AGONIST PROTEIN; IMMUNE TOLERANCE; IMMUNOSUPPRESSION; KERATINOCYTES; LANGERHANS CELLS; MICE; MICE, KNOCKOUT; SKIN; ULTRAVIOLET RAYS;

EID: 51549095216     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.5.3077     Document Type: Article

References (46)

1. Raj, D., D. E. Brash, and D. Grossman. 2006. Keratinocyte apoptosis in epidermal development and disease. J. Invest. Dermatol. 126: 243-257. (Pubitemid 43323157)
2. Nickoloff, B. J., J. Z. Qin, V. Chaturvedi, P. Bacon, J. Panella, and M. F. Denning. 2002. Life and death signaling pathways contributing to skin cancer. J. Investig. Dermatol. Symp. Proc. 7: 27-35.
3. Krajewska, M., J. M. Zapata, I. Meinhold-Heerlein, H. Hedayat, A. Monks, H. Bettendorf, A. Shabaik, L. Bubendorf, O. P. Kallioniemi, H. Kim, et al. 2002. Expression of Bcl-2 family member Bid in normal and malignant tissues. Neoplasia 4: 129-140. (Pubitemid 34218681)
4. Zinkel, S. S., C. C. Ong, D. O. Ferguson, H. Iwasaki, K. Akashi, R. T. Bronson, J. L. Kutok, F. W. Alt, and S. J. Korsmeyer. 2003. Proapoptotic BID is required for myeloid homeostasis and tumor suppression. Genes Dev. 17: 229-239.
5. Danial, N. N., and S. J. Korsmeyer. 2004. Cell death: critical control points. Cell 116: 205-219. (Pubitemid 38167313)
6. Li, H., H. Zhu, C. J. Xu, and J. Yuan. 1998. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94: 491-501. (Pubitemid 28391865)
7. Wang, K., X. M. Yin, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, C. L. Keck, D. B. Zimonjic, N. C. Popescu, and S. J. Korsmeyer. 1998. BID, a proapoptotic BCL-2 family member, is localized to mouse chromosome 6 and human chromosome 22q11. Genomics 53: 235-238. (Pubitemid 28496614)
8. Barnhart, B. C., E. C. Alappat, and M. E. Peter. 2003. The CD95 type I/type II model. Semin. Immunol. 15: 185-193.
9. Hill, L. L., A. Ouhtit, S. M. Loughlin, M. L. Kripke, H. N. Ananthaswamy, and L. B. Owen-Schaub. 1999. Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science 285: 898-900.
10. Aragane, Y., D. Kulms, D. Metze, G. Wilkes, B. Poppelmann, T. A. Luger, and T. Schwarz. 1998. Ultraviolet light induces apoptosis via direct activation of CD95 (Fas/APO-1) independently of its ligand CD95L. J. Cell Biol. 140: 171-182. (Pubitemid 28070905)
11. Jiang, W., H. N. Ananthaswamy, H. K. Muller, and M. L. Kripke. 1999. p53 protects against skin cancer induction by UV-B radiation. Oncogene 18: 4247-4253. (Pubitemid 29377855)
12. Ziegler, A., A. S. Jonason, D. J. Leffell, J. A. Simon, H. W. Sharma, J. Kimmelman, L. Remington, T. Jacks, and D. E. Brash. 1994. Sunburn and p53 in the onset of skin cancer. Nature 372: 773-776.
13. Sax, J. K., P. Fei, M. E. Murphy, E. Bernhard, S. J. Korsmeyer, and W. S. El-Deiry. 2002. BID regulation by p53 contributes to chemosensitivity. Nat. Cell Biol. 4: 842-849.
14. Qin, J. Z., P. Bacon, J. Panella, L. A. Sitailo, M. F. Denning, and B. J. Nickoloff. 2004. Low-dose UV-radiation sensitizes keratinocytes to TRAIL-induced apoptosis. J. Cell. Physiol. 200: 155-166.
15. Kulms, D., E. Zeise, B. Poppelmann, and T. Schwarz. 2002. DNA damage, death receptor activation and reactive oxygen species contribute to ultraviolet radiation-induced apoptosis in an essential and independent way. Oncogene 21: 5844-5851. (Pubitemid 35007234)
16. Obata, M., and H. Tagami. 1985. Alteration in murine epidermal Langerhans cell population by various UV irradiations: quantitative and morphologic studies on the effects of various wavelengths of monochromatic radiation on Ia-bearing cells. J. Invest. Dermatol. 84: 139-145. (Pubitemid 15158458)
17. Hamakawa, M., A. Sugihara, H. Okamoto, and T. Horio. 2006. Ultraviolet B radiation suppresses Langerhans cell migration in the dermis by down-regulation of α4 integrin. Photodermatol. Photoimmunol. Photomed. 22: 116-123. (Pubitemid 43805795)
18. Toews, G. B., P. R. Bergstresser, and J. W. Streilein. 1980. Epidermal Langerhans cell density determines whether contact hypersensitivity or unresponsiveness follows skin painting with DNFB. J. Immunol. 124: 445-453.
19. Tang, A., and M. C. Udey. 1992. Effects of ultraviolet radiation on murine epidermal Langerhans cells: doses of ultraviolet radiation that modulate ICAM-1 (CD54) expression and inhibit Langerhans cell function cause delayed cytotoxicity in vitro. J. Invest. Dermatol. 99: 83-89.
20. Elmets, C. A., P. R. Bergstresser, R. E. Tigelaar, P. J. Wood, and J. W. Streilein. 1983. Analysis of the mechanism of unresponsiveness produced by haptens painted on skin exposed to low dose ultraviolet radiation. J. Exp. Med. 158: 781-794.
21. Beissert, S., A. Schwarz, and T. Schwarz. 2006. Regulatory T cells. J. Invest. Dermatol. 126: 15-24.
22. Schade, N., C. Esser, and J. Krutmann. 2005. Ultraviolet B radiation-induced immunosuppression: molecular mechanisms and cellular alterations. Photochem. Photobiol. Sci. 4: 699-708. (Pubitemid 41367020)
23. Rivas, J. M., and S. E. Ullrich. 1992. Systemic suppression of delayed-type hypersensitivity by supernatants from UV-irradiated keratinocytes: an essential role for keratinocyte-derived IL-10. J. Immunol. 149: 3865-3871.
24. Loser, K., A. Mehling, S. Loeser, J. Apelt, A. Kuhn, S. Grabbe, T. Schwarz, J. M. Penninger, and S. Beissert. 2006. Epidermal RANKL controls regulatory T-cell numbers via activation of dendritic cells. Nat. Med. 12: 1372-1379. (Pubitemid 44924495)
25. Ullrich, S. E. 2007. Sunlight and skin cancer: lessons from the immune system. Mol. Carcinog. 46: 629-633. (Pubitemid 47255179)
26. Beissert, S., J. Hosoi, R. Kuhn, K. Rajewsky, W. Muller, and R. D. Granstein. 1996. Impaired immunosuppressive response to ultraviolet radiation in interleukin-10-deficient mice. J. Invest. Dermatol. 107: 553-557. (Pubitemid 26338578)
27. Nishigori, C., D. B. Yarosh, S. E. Ullrich, A. A. Vink, C. D. Bucana, L. Roza, and M. L. Kripke. 1996. Evidence that DNA damage triggers interleukin 10 cytokine production in UV-irradiated murine keratinocytes. Proc. Natl. Acad. Sci. USA 93: 10354-10359. (Pubitemid 26314626)
28. O'Connor, A., C. Nishigori, D. Yarosh, L. Alas, J. Kibitel, L. Burley, P. Cox, C. Bucana, S. Ullrich, and M. Kripke. 1996. DNA double strand breaks in epidermal cells cause immune suppression in vivo and cytokine production in vitro. J. Immunol. 157: 271-278. (Pubitemid 26190557)
29. Vink, A. A., A. M. Moodycliffe, V. Shreedhar, S. E. Ullrich, L. Roza, D. B. Yarosh, and M. L. Kripke. 1997. The inhibition of antigen-presenting activity of dendritic cells resulting from UV irradiation of murine skin is restored by in vitro photorepair of cyclobutane pyrimidine dimers. Proc. Natl. Acad. Sci. USA 94: 5255-5260. (Pubitemid 27214770)
30. Pradhan, S., J. Genebriera, W. L. Denning, K. Felix, C. A. Elmets, and L. Timares. 2006. CD4 T cell-induced, bid-dependent apoptosis of cutaneous dendritic cells regulates T cell expansion and immune responses. J. Immunol. 177: 5956-5967. (Pubitemid 44628809)
31. Katiyar, S. K., M. S. Matsui, and H. Mukhtar. 2000. Kinetics of UV light-induced cyclobutane pyrimidine dimers in human skin in vivo: an immunohistochemical analysis of both epidermis and dermis. Photochem. Photobiol. 72: 788-793.
32. Schwarz, A., A. Maeda, K. Kernebeck, H. van Steeg, S. Beissert, and T. Schwarz. 2005. Prevention of UV radiation-induced immunosuppression by IL-12 is dependent on DNA repair. J. Exp. Med. 201: 173-179. (Pubitemid 40189425)
33. Van den Broeck, W., A. Derore, and P. Simoens. 2006. Anatomy and nomenclature of murine lymph nodes: descriptive study and nomenclatory standardization in BALB/cAnNCrl mice. J. Immunol. Methods 312: 12-19. (Pubitemid 43795993)
34. Muller-Rover, S., H. Rossiter, R. Paus, B. Handjiski, E. M. Peters, J. E. Murphy, L. Mecklenburg, and T. S. Kupper. 2000. Overexpression of Bcl-2 protects from ultraviolet B-induced apoptosis but promotes hair follicle regression and chemotherapy-induced alopecia. Am. J. Pathol. 156: 1395-1405. (Pubitemid 30660015)
35. Hill, L. L., V. K. Shreedhar, M. L. Kripke, and L. B. Owen-Schaub. 1999. A critical role for Fas ligand in the active suppression of systemic immune responses by ultraviolet radiation. J. Exp. Med. 189: 1285-1294.
36. Timares, L., S. K. Katiyar, and C. A. Elmets. 2008. DNA damage, apoptosis, and Langerhans cells: activators of UV-induced immune tolerance. Photochem. Photobiol. 84: 422-436.
37. Schwarz, A., S. Grabbe, K. Grosse-Heitmeyer, B. Roters, H. Riemann, T. A. Luger, G. Trinchieri, and T. Schwarz. 1998. Ultraviolet light-induced immune tolerance is mediated via the Fas/Fas-ligand system. J. Immunol. 160: 4262-4270. (Pubitemid 28217281)
38. Kitajima, T., K. Ariizumi, P. R. Bergstresser, and A. Takashima. 1996. Ultraviolet B radiation sensitizes a murine epidermal dendritic cell line (XS52) to undergo apoptosis upon antigen presentation to T cells. J. Immunol. 157: 3312-3316. (Pubitemid 126449141)
39. Kolgen, W., H. Both, H. van Weelden, K. L. Guikers, C. A. Bruijnzeel-Koomen, E. F. Knol, W. A. van Vloten, and F. R. De Gruijl. 2002. Epidermal Langerhans cell depletion after artificial ultraviolet B irradiation of human skin in vivo: apoptosis versus migration. J. Invest. Dermatol. 118: 812-817. (Pubitemid 34526543)
40. Cruz, P. D., Jr., R. E. Tigelaar, and P. R. Bergstresser. 1990. Langerhans cells that migrate to skin after intravenous infusion regulate the induction of contact hypersensitivity. J. Immunol. 144: 2486-2492. (Pubitemid 20136647)
41. Applegate, L. A., R. D. Ley, J. Alcalay, and M. L. Kripke. 1989. Identification of the molecular target for the suppression of contact hypersensitivity by ultraviolet radiation. J. Exp. Med. 170: 1117-1131. (Pubitemid 19250683)
42. Vink, A. A., F. M. Strickland, C. Bucana, P. A. Cox, L. Roza, D. B. Yarosh, and M. L. Kripke. 1996. Localization of DNA damage and its role in altered antigen-presenting cell function in ultraviolet-irradiated mice. J. Exp. Med. 183: 1491-1500.
43. Schwarz, A., S. Stander, M. Berneburg, M. Bohm, D. Kulms, H. van Steeg, K. Grosse-Heitmeyer, J. Krutmann, and T. Schwarz. 2002. Interleukin-12 suppresses ultraviolet radiation-induced apoptosis by inducing DNA repair. Nat. Cell Biol. 4: 26-31. (Pubitemid 34071977)
44. + dendritic cells that develop and function independently of epidermal Langerhans cells. J. Exp. Med. 204: 3119-3131.
45. + dendritic cells survey the skin in the steady state. J. Exp. Med. 204: 3133-3146.
46. + dendritic cells. J. Exp. Med. 204: 3147-3156.