NFAT regulates induction of COX-2 and apoptosis of keratinocytes in response to ultraviolet radiation exposure

FASEB Journal

Volumn 22, Issue 12, 2008, Pages 4218-4227

  Flockhart, R J ^a   Diffey, B L ^a   Farr, P M ^b   Lloyd, J ^b   Reynolds, N J ^a  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b ROYAL VICTORIA INFIRMARY   (United Kingdom)

Author keywords

Action spectrum; Cyclosporin A; Skin equivalents; UVB

Indexed keywords

CYCLOOXYGENASE 2; CYCLOSPORIN A; PROTEIN NFAT2; TRANSCRIPTION FACTOR NFAT; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; BINDING SITE; CARCINOGENESIS; CONTROLLED STUDY; HUMAN; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ULTRAVIOLET B RADIATION;

CELL LINE; CYCLOOXYGENASE 2; CYCLOSPORINE; ENZYME INDUCTION; HUMANS; KERATINOCYTES; NFATC TRANSCRIPTION FACTORS; PROTEIN TRANSPORT; TRANSCRIPTIONAL ACTIVATION; ULTRAVIOLET RAYS;

EID: 57349155737     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.08-113076     Document Type: Article

References (65)

1. Shaw, J. P., Utz, P. J., Durand, D. B., Toole, J. J., Emmel, E. A., and Crabtree, G. R. (1988) Identification of a putative regulator of early T cell activation genes. Science 241, 202-205
2. Kiani, A., Rao, A., and Aramburu, J. (2000) Manipulating immune responses with immunosuppressive agents that target NFAT. Immunity 12, 359-372
3. Hill-Eubanks, D. C., Gomez, M. F., Stevenson, A. S., and Nelson, M. T. (2003) NFAT regulation in smooth muscle. Trends Cardiovasc. Med. 13, 56-62
4. Schulz, R. A., and Yutzey, K. E. (2004) Calcineurin signaling and NFAT activation in cardiovascular and skeletal muscle development. Dev. Biol. 266, 1-16
5. Asagiri, M., Sato, K., Usami, T., Ochi, S., Nishina, H., Yoshida, H., Morita, I., Wagner, E. F., Mak, T. W., Serfling, E., and Takayanagi, H. (2005) Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J. Exp. Med. 202, 1261-1269
6. Al-Daraji, W. I., Grant, K. R., Ryan, K., Saxton, A., and Reynolds, N. J. (2002) Localization of calcineurin/NFAT in human skin and psoriasis and inhibition of calcineurin/NFAT activation in human keratinocytes by cyclosporin A. J. Invest. Dermatol. 118, 779-788
7. Santini, M. P., Talora, C., Seki, T., Bolgan, L., and Dotto, G. P. (2001) Cross talk among calcineurin, Sp1/Sp3, and NFAT in control of p21(WAF1/CIP1) expression in keratinocyte differentiation. Proc. Natl. Acad. Sci. U. S. A. 98, 9575-9580
8. Mammucari, C., di Vignano, A. T., Sharov, A. A., Neilson, J., Havrda, M. C., Roop, D. R., Botchkarev, V. A., Crabtree, G. R., and Dotto, G. P. (2005) Integration of Notch 1 and calcineurin/ NFAT signaling pathways in keratinocyte growth and differentiation control. Dev. Cell. 8, 665-676
9. Benedito, A. B., Lehtinen, M., Massol, R., Lopes, U. G., Kirchhausen, T., Rao, A., and Bonni, A. (2005) The transcription factor NFAT3 mediates neuronal survival. J. Biol. Chem. 280, 2818-2825
10. Jayanthi, S., Deng, X., Ladenheim, B., McCoy, M. T., Cluster, A., Cai, N. S., and Cadet, J. L. (2005) Calcineurin/NFAT-induced up-regulation of the Fas ligand/Fas death pathway is involved in methamphetamine-induced neuronal apoptosis. Proc. Natl. Acad. Sci. U. S. A. 102, 868-873
11. McCaffrey, P. G., Luo, C., Kerppola, T. K., Jain, J., Badalian, T. M., Ho, A. M., Burgeon, E., Lane, W. S., Lambert, J. N., Curran, T., Verdine, G. L., Rao, A., and Hogan, P. G. (1993) Isolation of the cyclosporin-sensitive T cell transcription factor NFATp. Science 262, 750-754
12. Northrop, J. P., Ho, S. N., Chen, L., Thomas, D. J., Timmerman, L. A., Nolan, G. P., Admon, A., and Crabtree, G. R. (1994) NF-AT components define a family of transcription factors targeted in T-cell activation. Nature 369, 497-502
13. Hoey, T., Sun, Y. L., Williamson, K., and Xu, X. (1995) Isolation of two new members of the NF-AT gene family and functional characterization of the NF-AT proteins. Immunity 2, 461-472
14. Masuda, E. S., Naito, Y., Tokumitsu, H., Campbell, D., Saito, F., Hannum, C., Arai, K., and Arai, N. (1995) NFATx, a novel member of the nuclear factor of activated T cells family that is expressed predominantly in the thymus. Mol. Cell. Biol. 15, 2697-2706
15. Lopez-Rodriguez, C., Aramburu, J., Rakeman, A. S., and Rao, A. (1999) NFAT5, a constitutively nuclear NFAT protein that does not cooperate with Fos and Jun. Proc. Natl. Acad. Sci. U. S. A. 96, 7214-7219
16. Miyakawa, H., Woo, S. K., Dahl, S. C., Handler, J. S., and Kwon, H. M. (1999) Tonicity-responsive enhancer binding protein, a rel-like protein that stimulates transcription in response to hypertonicity. Proc. Natl. Acad. Sci. U. S. A. 96, 2538-2542
17. Hogan, P. G., Chen, L., Nardone, J., and Rao, A. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17, 2205-2232
18. Macian, F., Lopez-Rodriguez, C., and Rao, A. (2001) Partners in transcription: NFAT and AP-1. Oncogene 20, 2476-2489
19. Horsley, V., and Pavlath, G. K. (2002) NFAT: ubiquitous regulator of cell differentiation and adaptation. J. Cell Biol. 156, 771-774
20. Beals, C. R., Sheridan, C. M., Turck, C. W., Gardner, P., and Crabtree, G. R. (1997) Nuclear export of NF-ATc enhanced by glycogen synthase kinase-3. Science 275, 1930-1934
21. Graef, I. A., Mermelstein, P. G., Stankunas, K., Neilson, J. R., Deisseroth, K., Tsien, R. W., and Crabtree, G. R. (1999) L-type calcium channels and GSK-3 regulate the activity of NF-ATc4 in hippocampal neurons. Nature 401, 703-708
22. Vyas, D. R., Spangenburg, E. E., Abraha, T. W., Childs, T. E., and Booth, F. W. (2002) GSK-3beta negatively regulates skeletal myotube hypertrophy. Am. J. Physiol. Cell. Physiol. 283, C545-C551
23. Zhu, J., Shibasaki, F., Price, R., Guillemot, J. C., Yano, T., Dotsch, V., Wagner, G., Ferrara, P., and McKeon, F. (1998) Intramolecular masking of nuclear import signal on NF-AT4 by casein kinase I and MEKK1. Cell 93, 851-861
24. Okamura, H., Garcia-Rodriguez, C., Martinson, H., Qin, J., Virshup, D. M., and Rao, A. (2004) A conserved docking motif for CK1 binding controls the nuclear localization of NFAT1. Mol. Cell. Biol. 24, 4184-4195
25. Diffey, B. L. (2002) Sources and measurement of ultraviolet radiation. Methods 28, 4-13
26. Heck, D. E., Gerecke, D. R., Vetrano, A. M., and Laskin, J. D. (2004) Solar ultraviolet radiation as a trigger of cell signal transduction. Toxicol. Appl. Pharmacol. 195, 288-297
27. De Gruijl, F. R., Sterenborg, H. J., Forbes, P. D., Davies, R. E., Cole, C., Kelfkens, G., van Weelden, H., Slaper, H., and van der Leun, J. C. (1993) Wavelength dependence of skin cancer induction by ultraviolet irradiation of albino hairless mice. Cancer Res. 53, 53-60
28. Ichihashi, M., Ueda, M., Budiyanto, A., Bito, T., Oka, M., Fukunaga, M., Tsuru, K., and Horikawa, T. (2003) UV-induced skin damage. Toxicology 189, 21-39
29. Setlow, R. B. (1974) The wavelengths in sunlight effective in producing skin cancer: a theoretical analysis. Proc. Natl. Acad. Sci. U. S. A. 71, 3363-3366
30. Horio, T. (1998) Skin disorders that improve by exposure to sunlight. Clin. Dermatol. 16, 59-65
31. Fischer, T., Alsins, J., and Berne, B. (1984) Ultraviolet-action spectrum and evaluation of ultraviolet lamps for psoriasis healing. Int. J. Dermatol. 23, 633-637
32. Parrish, J. A., and Jaenicke, K. F. (1981) Action spectrum for phototherapy of psoriasis. J. Invest. Dermatol. 76, 359-362
33. Maziere, C., Morliere, P., Louandre, C., Conte, M. A., Gomilla, C., Santus, R., Antonicelli, F., Hornebeck, W., and Maziere, J. C. (2005) Low UVA doses activate the transcription factor NFAT in human fibroblasts by a calcium-calcineurin pathway. Free Radic. Biol. Med. 39, 1629-1637
34. Huang, C., Mattjus, P., Ma, W. Y., Rincon, M., Chen, N. Y., Brown, R. E., and Dong, Z. (2000) Involvement of nuclear factor of activated T cells activation in UV response. Evidence from cell culture and transgenic mice. J. Biol. Chem. 275, 9143-9149
35. Blanke, C. (2004) Role of COX-2 inhibitors in cancer therapy. Cancer Invest. 22, 271-282
36. Meric, J. B., Rottey, S., Olaussen, K., Soria, J. C., Khayat, D., Rixe, O., and Spano, J. P. (2006) Cyclooxygenase-2 as a target for anticancer drug development. Crit. Rev. Oncol. Hematol. 59, 51-64
37. Onguru, O., Casey, M. B., Kajita, S., Nakamura, N., and Lloyd, R. V. (2005) Cyclooxygenase-2 and thromboxane synthase in non-endocrine and endocrine tumors: a review. Endocr. Pathol. 16, 253-277
38. Sinicrope, F. A., and Gill, S. (2004) Role of cyclooxygenase-2 in colorectal cancer. Cancer Metastasis Rev. 23, 63-75
39. Buckman, S. Y., Gresham, A., Hale, P., Hruza, G., Anast, J., Masferrer, J., and Pentland, A. P. (1998) COX-2 expression is induced by UVB exposure in human skin: implications for the development of skin cancer. Carcinogenesis 19, 723-729
40. Fischer, S. M., Lo, H. H., Gordon, G. B., Seibert, K., Kelloff, G., Lubet, R. A., and Conti, C. J. (1999) Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, and indomethacin against ultraviolet light-induced skin carcinogenesis. Mol. Carcinog. 25, 231-240
41. Akunda, J. K., Chun, K. S., Sessoms, A. R., Lao, H. C., Fischer, S. M., and Langenbach, R. (2007) Cyclooxygenase-2 deficiency increases epidermal apoptosis and impairs recovery following acute UVB exposure. Mol. Carcinog. 46, 354-362
42. Iniguez, M. A., Martinez-Martinez, S., Punzon, C., Redondo, J. M., and Fresno, M. (2000) An essential role of the nuclear factor of activated T cells in the regulation of the expression of the cyclooxygenase-2 gene in human T lymphocytes. J. Biol. Chem. 275, 23627-23635
43. Hedin, K. E., Bell, M. P., Kalli, K. R., Huntoon, C. J., Sharp, B. M., and McKean, D. J. (1997) Delta-opioid receptors expressed by Jurkat T cells enhance IL-2 secretion by increasing AP-1 complexes and activity of the NF-AT/AP-1-binding promoter element. J. Immunol. 159, 5431-5440
44. Farr, P. M., Diffey, B. L., Higgins, E. M., and Matthews, J. N. (1991) The action spectrum between 320 and 400 nm for clearance of psoriasis by psoralen photochemotherapy. Br. J. Dermatol. 124, 443-448
45. Turner, H., Gomez, M., McKenzie, E., Kirchem, A., Lennard, A., and Cantrell, D. A. (1998) Rac-1 regulates nuclear factor of activated T cells (NFAT) C1 nuclear translocation in response to Fcepsilon receptor type 1 stimulation of mast cells. J. Exp. Med. 188, 527-537
46. Lyakh, L., Ghosh, P., and Rice, N. R. (1997) Expression of NFAT-family proteins in normal human T cells. Mol. Cell. Biol. 17, 2475-2484
47. McKinlay, A. F., and Diffey, B. L. (1987) A reference action spectrum for ultraviolet induced erythema in human skin. CIE J. 6, 17-22
48. Abbott, K. L., Friday, B. B., Thaloor, D., Murphy, T. J., and Pavlath, G. K. (1998) Activation and cellular localization of the cyclosporine A-sensitive transcription factor NF-AT in skeletal muscle cells. Mol. Biol. Cell 9, 2905-2916
49. Loh, C., Carew, J. A., Kim, J., Hogan, P. G., and Rao, A. (1996) T-cell receptor stimulation elicits an early phase of activation and a later phase of deactivation of the transcription factor NFAT1. Mol. Cell. Biol. 16, 3945-3954
50. Tang, Q., Chen, W., Gonzales, M. S., Finch, J., Inoue, H., and Bowden, G. T. (2001) Role of cyclic AMP-responsive element in the UVB induction of cyclooxygenase-2 transcription in human keratinocytes. Oncogene 20, 5164-5172
51. Tang, Q., Gonzales, M., Inoue, H., and Bowden, G. T. (2001) Roles of Akt and glycogen synthase kinase 3beta in the ultraviolet B induction of cyclooxygenase-2 transcription in human keratinocytes. Cancer Res. 61, 4329-4332
52. Mahns, A., Wolber, R., Stab, F., Klotz, L. O., and Sies, H. (2004) Contribution of UVB and UVA to UV-dependent stimulation of cyclooxygenase-2 expression in artificial epidermis. Photochem. Photobiol. Sci. 3, 257-262
53. Pu, W. T., Ma, Q., and Izumo, S. (2003) NFAT transcription factors are critical survival factors that inhibit cardiomyocyte apoptosis during phenylephrine stimulation in vitro. Circ. Res. 92, 725-731
54. Ding, J., Li, J., Xue, C., Wu, K., Ouyang, W., Zhang, D., Yan, Y., and Huang, C. (2006) Cyclooxygenase-2 induction by arsenite is through a nuclear factor of activated T-cell-dependent pathway and plays an antiapoptotic role in Beas-2B cells. J. Biol. Chem. 281, 24405-24413
55. Yarosh, D. B., Pena, A. V., Nay, S. L., Canning, M. T., and Brown, D. A. (2005) Calcineurin inhibitors decrease DNA repair and apoptosis in human keratinocytes following ultraviolet B irradiation. J. Invest. Dermatol. 125, 1020-1025
56. Penn, I. (1998) Occurrence of cancers in immunosuppressed organ transplant recipients. Clin. Transpl. 147-158
57. Sheil, A. G. (1998) Cancer in immune-suppressed organ transplant recipients: aetiology and evolution. Transplant Proc. 30, 2055-2057
58. Botti, C., Seregni, E., Ferrari, L., Martinetti, A., and Bombardieri, E. (1998) Immunosuppressive factors: role in cancer development and progression. Int. J. Biol. Markers 13, 51-69
59. 2+/calcineurin/NFAT signaling in cancerogenesis. Cell Cycle 6, 16-19
60. Jauliac, S., Lopez-Rodriguez, C., Shaw, L. M., Brown, L. F., Rao, A., and Toker, A. (2002) The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat. Cell Biol. 4, 540-544
61. Corral, R. S., Iniguez, M. A., Duque, J., Lopez-Perez, R., and Fresno, M. (2007) Bombesin induces cyclooxygenase-2 expression through the activation of the nuclear factor of activated T cells and enhances cell migration in Caco-2 colon carcinoma cells. Oncogene 26, 958-969
62. Yiu, G. K., and Toker, A. (2006) NFAT induces breast cancer cell invasion by promoting the induction of cyclooxygenase-2. J. Biol. Chem. 281, 12210-12217
63. Neal, J. W., and Clipstone, N. A. (2003) A constitutively active NFATc1 mutant induces a transformed phenotype in 3T3-L1 fibroblasts. J. Biol. Chem. 278, 17246-17254
64. Patel, R. N., Attur, M. G., Dave, M. N., Patel, I. V., Stuchin, S. A., Abramson, S. B., and Amin, A. R. (1999) A novel mechanism of action of chemically modified tetracyclines: inhibition of COX-2-mediated prostaglandin E2 production. J. Immunol. 163, 3459-3467
65. Sevigny, M. B., Li, C. F., Alas, M., and Hughes-Fulford, M. (2006) Glycosylation regulates turnover of cyclooxygenase-2. FEBS Lett. 580, 6533-6536