Imiquimod-induced TLR7 signaling enhances repair of DNA damage induced by ultraviolet Light in bone marrow-derived cells

Journal of Immunology

Volumn 187, Issue 4, 2011, Pages 1664-1673

  Fishelevich, Rita ^a   Zhao, Yuming ^a   Tuchinda, Papapit ^a   Liu, Hannah ^a   Nakazono, Ayako ^a   Tammaro, Antonella ^a   Meng, Tzu Ching ^b   Lee, Jim ^b   Gaspari, Anthony A ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b Graceway Pharmaceuticals LLC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; IMIQUIMOD; MYELOID DIFFERENTIATION FACTOR 88; PYRIMIDINE DIMER; TOLL LIKE RECEPTOR 7; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN PRESENTING CELL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BONE MARROW CELL; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; DNA REPAIR GENE; ENZYME LOCALIZATION; EXCISION REPAIR; FEMALE; GENE; GENE EXPRESSION; GENE TARGETING; GENETIC ANALYSIS; IL 12 GENE; INNATE IMMUNITY; LYMPH NODE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIATION PROTECTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ULTRAVIOLET B RADIATION; WILD TYPE; XERODERMA PIGMENTOSUM GENE;

AMINOQUINOLINES; ANIMALS; ANTINEOPLASTIC AGENTS; BONE MARROW CELLS; CELL LINE; DNA DAMAGE; DNA REPAIR; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; MEMBRANE GLYCOPROTEINS; MICE; MICE, KNOCKOUT; MYELOID DIFFERENTIATION FACTOR 88; PYRIMIDINE DIMERS; SIGNAL TRANSDUCTION; SKIN NEOPLASMS; TOLL-LIKE RECEPTOR 7; ULTRAVIOLET RAYS; XERODERMA PIGMENTOSUM GROUP A PROTEIN;

EID: 80051946731     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100755     Document Type: Article

References (54)

1. Beissert, S., and T. Schwarz. 2009. Ultraviolet-induced immunosuppression: Implications for photocarcinogenesis. Cancer Treat. Res. 146: 109-121.
2. Murphy, G. M. 2009. Ultraviolet radiation and immunosuppression. Br. J. Dermatol. 161(Suppl 3): 90-95.
3. Ghoreishi, M., and J. P. Dutz. 2006. Tolerance induction by transcutaneous immunization through ultraviolet-irradiated skin is transferable through CD4+ CD25+ T regulatory cells and is dependent on host-derived IL-10. J. Immunol. 176: 2635-2644. (Pubitemid 43201716)
4. 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. (Pubitemid 23068866)
5. Schwarz, A., M. Noordegraaf, A. Maeda, K. Torii, B. E. Clausen, and T. Schwarz. 2010. Langerhans cells are required for UVR-induced immunosuppression. J. Invest. Dermatol. 130: 1419-1427.
6. Toichi, E., T. S. McCormick, and K. D. Cooper. 2002. Cell surface and cytokine phenotypes of skin immunocompetent cells involved in ultraviolet-induced immunosuppression. Methods 28: 104-110.
7. Simon, J. C., T. Mosmann, D. Edelbaum, E. Schopf, P. R. Bergstresser, and P. D. Cruz Jr. 1994. In vivo evidence that ultraviolet B-induced suppression of allergic contact sensitivity is associated with functional inactivation of Th1 cells. Photodermatol. Photoimmunol. Photomed. 10: 206-211. (Pubitemid 24357437)
8. Saijo, S., E. Kodari, M. L. Kripke, and F. M. Strickland. 1996. UVB irradiation decreases the magnitude of the Th1 response to hapten but does not increase the Th2 response. Photodermatol. Photoimmunol. Photomed. 12: 145-153. (Pubitemid 27023513)
9. Maeda, A., S. Beissert, T. Schwarz, and A. Schwarz. 2008. Phenotypic and functional characterization of ultraviolet radiation-induced regulatory T cells. J. Immunol. 180: 3065-3071.
10. Sontag, Y., C. L. Guikers, A. A. Vink, F. R. De Gruijl, H. Van Loveren, J. Garssen, L. Roza, M. L. Kripke, J. C. Van der Leun, and W. A. Van Vloten. 1995. Cells with UV-specific DNA damage are present in murine lymph nodes after in vivo UV irradiation. J. Invest. Dermatol. 104: 734-738.
11. Fisher, M. S., and M. L. Kripke. 1977. Systemic alteration induced in mice by ultraviolet light irradiation and its relationship to ultraviolet carcinogenesis. Proc. Natl. Acad. Sci. USA 74: 1688-1692. (Pubitemid 8087041)
12. Yarosh, D., J. Klein, A. O'Connor, J. Hawk, E. Rafal, P. Wolf; Xeroderma Pigmentosum Study Group. 2001. Effect of topically applied T4 endonuclease V in liposomes on skin cancer in xeroderma pigmentosum: A randomised study. Lancet 357: 926-929. (Pubitemid 32247282)
13. Schwarz, A., A. Maeda, D. Gan, T. Mammone, M. S. Matsui, and T. Schwarz. 2008. Green tea phenol extracts reduce UVB-induced DNA damage in human cells via interleukin-12. Photochem. Photobiol. 84: 350-355. (Pubitemid 351424031)
14. Schwarz, A., S. Ständer, M. Berneburg, M. Böhm, 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)
15. Majewski, S., C. Jantschitsch, A. Maeda, T. Schwarz, and A. Schwarz. 2010. IL- 23 antagonizes UVR-induced immunosuppression through two mechanisms: Reduction of UVR-induced DNA damage and inhibition of UVR-induced regulatory T cells. J. Invest. Dermatol. 130: 554-562.
16. Sreevidya, C. S., A. Fukunaga, N. M. Khaskhely, T. Masaki, R. Ono, C. Nishigori, and S. E. Ullrich. 2010. Agents that reverse UV-Induced immune suppression and photocarcinogenesis affect DNA repair. J. Invest. Dermatol. 130: 1428-1437.
17. Thatcher, T. H., I. Luzina, R. Fishelevich, and A. A. Gaspari. 2006. Topical imiquimod treatment prevents ultraviolet-light induced loss of contact hypersensitivity and immune tolerance. J. Investig. Dermatol. 126: 821-831.
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. (Pubitemid 10182298)
19. 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. (Pubitemid 13051345)
20. Magram, J., S. E. Connaughton, R. R. Warrier, D. M. Carvajal, C. Y. Wu, J. Ferrante, C. Stewart, U. Sarmiento, D. A. Faherty, and M. K. Gately. 1996. IL- 12-deficient mice are defective in IFN gamma production and type 1 cytokine responses. Immunity 4: 471-481. (Pubitemid 26354656)
21. Elliott, J., M. B. Coulter-Mackie, J. H. Jung, D. I. Rodenhiser, and S. M. Singh. 1991. A method for transforming lymphocytes from very small blood volumes suitable for paediatric samples. Hum. Genet. 86: 615-616.
22. Heo, D. S., J. -G. Park, K. Hata, R. Day, R. B. Herberman, and T. L. Whiteside. 1990. Evaluation of tetrazolium-based semiautomatic colorimetric assay for measurement of human antitumor cytotoxicity. Cancer Res. 50: 3681-3690. (Pubitemid 20194116)
23. Sikder, H., Y. Zhao, A. Balato, A. Chapoval, R. Fishelevich, P. Gade, I. S. Singh, D. V. Kalvakolanu, P. F. Johnson, and A. A. Gaspari. 2009. A central role for transcription factor C/EBP-b in regulating CD1d gene expression in human keratinocytes. J. Immunol. 183: 1657-1666.
24. Ade, N., D. Antonios, S. Kerdine-Romer, F. Boisleve, F. Rousset, and M. Pallardy. 2007. NF-kappaB plays a major role in the maturation of human dendritic cells induced by NiSO(4) but not by DNCB. Toxicol. Sci. 99: 488-501. (Pubitemid 351753065)
25. Zhao, Y., R. Fishelevich, J. P. Petrali, L. Zheng, M. A. Anatolievna, A. Deng, R. L. Eckert, and A. A. Gaspari. 2008. Activation of keratinocyte protein kinase C zeta in psoriasis plaques. J. Invest. Dermatol. 128: 2190-2197.
26. Fishelevich, R., A. Malanina, I. Luzina, S. Atamas, M. J. Smyth, S. A. Porcelli, and A. A. Gaspari. 2006. Ceramide-dependent regulation of human epidermal keratinocyte CD1d expression during terminal differentiation. J. Immunol. 176: 2590-2599. (Pubitemid 43201711)
27. Moriwaki, S. -I., and K. H. Kraemer. 2001. Xeroderma pigmentosum - bridging a gap between clinic and laboratory. Photodermatol. Photoimmunol. Photomed. 17: 47-54. (Pubitemid 32280059)
28. Gorden, K. B., K. S. Gorski, S. J. Gibson, R. M. Kedl, W. C. Kieper, X. Qiu, M. A. Tomai, S. S. Alkan, and J. P. Vasilakos. 2005. Synthetic TLR agonists reveal functional differences between human TLR7 and TLR8. J. Immunol. 174: 1259-1268.
29. Akira, S., S. Uematsu, and O. Takeuchi. 2006. Pathogen recognition and innate immunity. Cell 124: 783-801. (Pubitemid 43261452)
30. Kawai, T., and S. Akira. 2010. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 11: 373-384.
31. Blasius, A. L., and B. Beutler. 2010. Intracellular toll-like receptors. Immunity 32: 305-315.
32. 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.
33. Brash, D. E., A. Ziegler, A. S. Jonason, J. A. Simon, S. Kunala, and D. J. Leffell. 1996. Sunlight and sunburn in human skin cancer: P53, apoptosis, and tumor promotion. J. Investig. Dermatol. Symp. Proc. 1: 136-142. (Pubitemid 126759356)
34. Carreau, M., E. Eveno, X. Quilliet, O. Chevalier-Lagente, A. Benoit, B. Tanganelli, M. Stefanini, W. Vermeulen, J. H. Hoeijmakers, A. Sarasin, et al. 1995. Development of a new easy complementation assay for DNA repair deficient human syndromes using cloned repair genes. Carcinogenesis 16: 1003-1009.
35. Khan, S. G., H. L. Levy, R. Legerski, E. Quackenbush, J. T. Reardon, S. Emmert, A. Sancar, L. Li, T. D. Schneider, J. E. Cleaver, and K. H. Kraemer. 1998. Xeroderma pigmentosum group C splice mutation associated with autism and hypoglycinemia. J. Invest. Dermatol. 111: 791-796. (Pubitemid 28509320)
36. Kripke, M. L., P. A. Cox, L. G. Alas, and D. B. Yarosh. 1992. Pyrimidine dimers in DNA initiate systemic immunosuppression in UV-irradiated mice. Proc. Natl. Acad. Sci. USA 89: 7516-7520.
37. Takeuchi, O., and S. Akira. 2010. Pattern recognition receptors and inflammation. Cell 140: 805-820.
38. Beutler, B., Z. Jiang, P. Georgel, K. Crozat, B. Croker, S. Rutschmann, X. Du, and K. Hoebe. 2006. Genetic analysis of host resistance: Toll-like receptor signaling and immunity at large. Annu. Rev. Immunol. 24: 353-389.
39. Larangé, A., D. Antonios, M. Pallardy, and S. Kerdine-Römer. 2009. TLR7 and TLR8 agonists trigger different signaling pathways for human dendritic cell maturation. J. Leukoc. Biol. 85: 673-683.
40. A. Gaspari, A., S. K. Tyring, and T. Rosen. 2009. Beyond a decade of 5% imiquimod topical therapy. J. Drugs Dermatol. 8: 467-474.
41. Sullivan, T. P., T. Dearaujo, V. Vincek, and B. Berman. 2003. Evaluation of superficial basal cell carcinomas after treatment with imiquimod 5% cream or vehicle for apoptosis and lymphocyte phenotyping. Dermatol. Surg. 29: 1181-1186. (Pubitemid 38009915)
42. Hurwitz, D. J., L. Pincus, and T. S. Kupper. 2003. Imiquimod: A topically applied link between innate and acquired immunity. Arch. Dermatol. 139: 1347-1350. (Pubitemid 37248285)
43. Stary, G., C. Bangert, M. Tauber, R. Strohal, T. Kopp, and G. Stingl. 2007. Tumoricidal activity of TLR7/8-activated inflammatory dendritic cells. J. Exp. Med. 204: 1441-1451. (Pubitemid 46919881)
44. Schön, M. P., and M. Schön. 2004. Immune modulation and apoptosis induction: Two sides of the antitumoral activity of imiquimod. Apoptosis 9: 291-298. (Pubitemid 38986952)
45. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241. (Pubitemid 38962578)
46. Zheng, L., N. Asprodites, A. H. Keene, P. Rodriguez, K. D. Brown, and E. Davila. 2008. TLR9 engagement on CD4 T lymphocytes represses gamma-radiation-induced apoptosis through activation of checkpoint kinase response elements. Blood 111: 2704-2713.
47. Li, X., S. Jiang, and R. I. Tapping. 2010. Toll-like receptor signaling in cell proliferation and survival. Cytokine 49: 1-9.
48. Clément, J. F., S. Meloche, and M. J. Servant. 2008. The IKK-related kinases: From innate immunity to oncogenesis. Cell Res. 18: 889-899.
49. Vallabhapurapu, S., and M. Karin. 2009. Regulation and function of NF-kappaB transcription factors in the immune system. Annu. Rev. Immunol. 27: 693-733.
50. Schwarz, T., and A. Schwarz. 2009. DNA repair and cytokine responses. J. Investig. Dermatol. Symp. Proc. 14: 63-66.
51. Arad, S., N. Konnikov, D. A. Goukassian, and B. A. Gilchrest. 2006. T-oligos augment UV-induced protective responses in human skin. FASEB J. 20: 1895-1897.
52. Goukassian, D. A., E. Helms, H. Van Steeg, C. Van Oostrom, J. Bhawan, and B. A. Gilchrest. 2004. Topical DNA oligonucleotide therapy reduces UVinduced mutations and photocarcinogenesis in hairless mice. Proc. Natl. Acad. Sci. USA 101: 3933-3938. (Pubitemid 38381080)
53. Katiyar, S. K., C. A. Elmets, and R. Agarwal. 1995. Protection against ultraviolet-B radiation-induced local and systemic suppression of contact hypersensitivity and edema responses in C3H/HeN mice by green tea polyphenols. Photochem. Photobiol. 62: 855-861.
54. Meeran, S. M., S. K. Mantena, and S. K. Katiyar. 2006. (-)-Epigallocatechin-3-gallate prevents photocarcinogenesis in mice through interleukin-12-dependent DNA repair. Cancer Res. 66: 5512-5520. (Pubitemid 43844980)