UVB light suppresses nitric oxide production by murine keratinocytes and macrophages

Biochemical Pharmacology

Volumn 64, Issue 10, 2002, Pages 1469-1481

  Sur, Runa ^a   Heck, Diane E ^a   Mariano, Thomas M ^b   Jin, Yang ^b   Murphy, William J ^c   Laskin, Jeffrey D ^b  

^a RUTGERS UNIVERSITY   (United States)

^b RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

Interferon ; Nitric oxide; Psoriasis; Skin; Ultraviolet light

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MESSENGER RNA; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; STAT1 PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL GROWTH; CONTROLLED STUDY; DNA BINDING; EPIDERMIS CELL; GENE; GENE EXPRESSION; GENETIC TRANSFECTION; INFLAMMATION; KERATINOCYTE; MACROPHAGE; MOUSE; NONHUMAN; NOS2 GENE; PHOSPHORYLATION; PRIORITY JOURNAL; RADIATION DOSE; REPORTER GENE; ULTRAVIOLET B RADIATION;

ANIMALS; DNA-BINDING PROTEINS; GENE EXPRESSION; GENES, REPORTER; KERATINOCYTES; MACROPHAGES; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE TYPE II; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TRANS-ACTIVATORS; ULTRAVIOLET RAYS;

EID: 0037111938     PISSN: 00062952     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-2952(02)01419-3     Document Type: Article

References (77)

1. Simon J.C., Pfieger D., Schopf E. Recent advances in phototherapy. Eur. J. Dermatol. 10:2000;642-645.
2. Laskin J.D., Heck D.E., Laskin D.L. Multifunctional role of nitric oxide in inflammation. Trends Endocrinol. Metab. 5:1994;377-382.
3. Heck DE. Nitric oxide biosynthesis and metabolism in keratinocytes: the functions and consequences of nitric oxide production in the skin. In: Laskin JD, Laskin DL, editors. Cellular and molecular biology of nitric oxide. New York: Marcel Dekker; 1999, p. 293-307.
4. Heck D.E., Laskin D.L., Gardner C.R., Laskin J.D. Epidermal growth factor suppresses nitric oxide and hydrogen peroxide production by keratinocytes. Potential role for nitric oxide in the regulation of wound healing. J. Biol. Chem. 267:1992;21277-21280.
5. Morhenn V.B. Langerhans cells may trigger the psoriatic disease process via production of nitric oxide. Immunol. Today. 18:1997;433-436.
6. Wang R., Ghahary A., Shen Y.J., Scott P.G., Tredget E.E. Human dermal fibroblasts produce nitric oxide and express both constitutive and inducible nitric oxide synthase isoforms. J. Invest. Dermatol. 106:1996;419-427.
7. Hoffmann G., Schobersberger W., Rieder J., Smolny M., Seibel M., Furhapter C., Fritsch P., Sepp N. Human dermal microvascular endothelial cells express inducible nitric oxide synthase in vitro. J. Invest. Dermatol. 112:1999;387-390.
8. Rocha I.M., Guillo L.A. Lipopolysaccharide and cytokines induce nitric oxide synthase and produce nitric oxide in cultured normal human melanocytes. Arch. Dermatol. Res. 293:2001;245-248.
9. Ormerod A.D., Weller R., Copeland P., Benjamin N., Ralston S.H., Grabowksi P., Herriot R. Detection of nitric oxide and nitric oxide synthases in psoriasis. Arch. Dermatol. Res. 290:1998;3-8.
10. Ormerod A.D., Dwyer C.M., Reid A., Copeland P., Thompson W.D. Inducible nitric oxide synthase demonstrated in allergic and irritant contact dermatitis. Acta Dermatol. Venereol. 77:1997;436-440.
11. Taniuchi S., Kojima T., Hara K., Yamamoto A., Sasai M., Takahashi H., Kobayashi Y. Increased serum nitrate levels in infants with atopic dermatitis. Allergy. 56:2001;693-695.
12. Deliconstantinos G., Villiotou V., Stavrides J.C. Inhibition of ultraviolet B-induced skin erythema by N-nitro-L-arginine and N-monomethyl-L-arginine. J. Dermatol. Sci. 15:1997;23-35.
13. Hobbs A.J., Higgs A., Moncada S. Inhibition of nitric oxide synthase as a potential therapeutic target. Annu. Rev. Pharmacol. Toxicol. 39:1999;191-220.
14. Ackermann L., Harvima I.T., Pelkonen J., Ritamäki-Salo V., Naukkarinen A., Harvima R.J., Horsmanheimo M. Mast cells in psoriatic skin are strongly positive for interferon-gamma. Br. J. Dermatol. 140:1999;624-633.
15. Werfel T., Morita A., Grewe M., Renz H., Wahn U., Krutmann J., Kapp A. Allergen specificity of skin-infiltrating T cells is not restricted to a type-2 cytokine pattern in chronic skin lesions of atopic dermatitis. J. Invest. Dermatol. 107:1996;871-876.
16. Luger T.A., Schwarz T. The role of cytokines and neuroendocrine hormones in cutaneous immunity and inflammation. Allergy. 50:1995;292-302.
17. DeGeorge G.L., Heck D.E., Laskin J.D. Arginine metabolism in keratinocytes and macrophages during nitric oxide biosynthesis. Biochem. Pharmacol. 54:1997;103-112.
18. Jeevan A., Bucana C.D., Dong Z., Dizon V.V., Thomas S.L., Lloyd T.E., Kripke M.L. Ultraviolet radiation reduces phagocytosis and intracellular killing of mycobacteria and inhibits nitric oxide production by macrophages in mice. J. Leukoc. Biol. 57:1995;883-890.
19. Garssen J., Vandebriel R.J., van Loveren H. Molecular aspects of UVB-induced immunosuppression. Arch. Toxicol. S19:1997;97-109.
20. Billack B., Heck D.E., Porterfield D.M., Malchow R.P., Smith P.J.S., Gardner C.R., Laskin D.L., Laskin J.D. Minimal amidine structure for inhibition of nitric oxide biosynthesis. Biochem. Pharmacol. 61:2001;1581-1586.
21. Pawlowski J.E., Nesterov A., Scheinman R.I., Johnson T.R., Kraft A.S. NF-κB does not modulate sensitivity of renal carcinoma cells to TNFα-related apoptosis-inducing ligand (TRAIL). Anticancer Res. 20:2000;4243-4255.
22. Guaiquil V.H., Farber C.M., Golde D.W., Vera J.C. Efficient transport and accumulation of Vitamin C in HL-60 cells depleted of glutathione. J. Biol. Chem. 272:1997;9915-9921.
23. Murphy W.J., Muroi M., Zhang C.X., Suzuki T., Russel S.W. Both basal and enhancer κB elements are required for full induction of the mouse inducible nitric oxide synthase gene. J. Endotoxin Res. 3:1996;381-393.
24. Gao J., Morrison D.C., Parmely T.J., Russel S.W., Murphy W.J. An interferon-γ-activated site (GAS) is necessary for full expression of the mouse iNOS gene in response to interferon-γ and lipopolysaccharide. J. Biol. Chem. 272:1997;1226-1230.
25. Yamamoto H., Crow M., Cheng L., Lakatta E., Kinsella J. PDGF receptor-to-nucleus signaling of p91 (STAT1α) transcription factor in rat smooth muscle cells. Exp. Cell Res. 222:1996;125-130.
26. Griffith O.W. Depletion of glutathione by inhibition of biosynthesis. Methods Enzymol. 77:1981;59-63.
27. Griffith O.W. Biologic and pharmacologic regulation of mammalian glutathione synthesis. Free Radic. Biol. Med. 27:1999;922-935.
28. Rao K.M. Molecular mechanisms regulating iNOS expression in various cell types. J. Toxicol. Environ. Health B Crit. Rev. 3:2000;27-58.
29. Chen B.C., Chou C.F., Lin W.W. Pyrimidinoceptor-mediated potentiation of inducible nitric-oxide synthase induction in J774 macrophages. Role of intracellular calcium. J. Biol. Chem. 273:1998;29754-29763.
30. Isoherranen K., Punnonen K., Jansen C., Uotila P. Ultraviolet irradiation induces cyclooxygenase-2 expression in keratinocytes. Br. J. Dermatol. 140:1999;1017-1022.
31. Rosen C.F., Gajic D., Drucker D.J. Ultraviolet radiation induction of ornithine decarboxylase in rat keratinocytes. Cancer Res. 50:1990;2631-2635.
32. Ponten F., Lindman H., Bostrom A., Berne B., Bergh J. Induction of p53 expression in skin by radiotherapy and UV radiation: a randomized study. J. Natl. Cancer Inst. 93:2001;82-83.
33. Marschall C., Lengyel E., Nobutoh T., Braungart E., Douwes K., Simon A., Magdolen V., Reuning U., Degitz K. UVB increases urokinase-type plasminogen activator receptor (uPAR) expression. J. Invest. Dermatol. 113:1999;69-76.
34. Sachi Y., Hirota K., Masutani H., Toda K., Okamoto T., Takigawa M., Yodoi J. Induction of ADF/TRX by oxidative stress in keratinocytes and lymphoid cells. Immunol. Lett. 44:1995;189-193.
35. Lee H.S., Kooshesh F., Sauder D.N., Kondo S. Modulation of TGF-β 1 production from human keratinocytes by UVB. Exp. Dermatol. 6:1997;105-110.
36. Soriani M., Hejmadi V., Tyrrell R.M. Modulation of c-jun and c-fos transcription by UVB and UVA radiations in human dermal fibroblasts and KB cells. Photochem. Photobiol. 71:2000;551-558.
37. Köck A., Schwarz T., Kirnbauer R., Urbanski A., Perry P., Ansel J.C., Luger T.A. Human keratinocytes are a source for tumor necrosis factor α: evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J. Exp. Med. 172:1990;1609-1614.
38. Kondo S., Sauder D.N., Kono T., Galley K.A., McKenzie R.C. Differential modulation of interleukin-1 α (IL-1 α) and interleukin-1 β (IL-1 β) in human epidermal keratinocytes by UVB. Exp. Dermatol. 3:1994;29-39.
39. Urbanski A., Schwarz T., Neuner P., Krutmann J., Kirnbauer R., Kock A., Luger T.A. Ultraviolet light induces increased circulating interleukin-6 in humans. J. Invest. Dermatol. 94:1990;808-811.
40. Kondo S., Kono T., Sauder D.N., McKenzie R.C. IL-8 gene expression and production in human keratinocytes and their modulation by UVB. J. Invest. Dermatol. 101:1993;690-694.
41. Enk C.D., Sredni D., Blauvelt A., Katz S.I. Induction of IL-10 gene expression in human keratinocytes by UVB exposure in vivo and in vitro. J. Immunol. 154:1995;4851-4856.
42. Kondo S., Yoneta A., Yazawa H., Kamada A., Jimbow K. Downregulation of CXCR-2 but not CXCR-1 expression by human keratinocytes by UVB. J. Cell Physiol. 182:2000;366-370.
43. Potter T., Gohde W., Wedemeyer N., Kohnlein W. Keratinocytes exposed to ultraviolet radiation reveal three down-regulated genes with potential function in differentiation and cell cycle control. Radiat. Res. 154:2000;151-158.
44. Finch P.W., Murphy F., Cardinale I., Krueger J.G. Altered expression of keratinocyte growth factor and its receptor in psoriasis. Am. J. Pathol. 151:1997;1619-1628.
45. Isoherranen K., Sauroja I., Jansen C., Punnonen K. UV irradiation induces downregulation of bcl-2 expression in vitro and in vivo. Arch. Dermatol. Res. 291:1999;212-216.
46. Bergstresser P.R., Elmets C.A., Takashima A., Mukhtar H. Photocarcinogenesis. Photodermatol. Photoimmunol. Photomed. 11:1996;181-184.
47. Peus D., Pittelkow M.R. Reactive oxygen species as mediators of UVB-induced mitogen-activated protein kinase activation in keratinocytes. Curr. Probl. Dermatol. 29:2001;114-127.
48. Tyrrell R.M. Ultraviolet radiation and free radical damage to skin. Biochem. Soc. Symp. 61:1995;47-53.
49. Afaq F., Mukhtar H. Effects of solar radiation on cutaneous detoxification pathways. J. Photochem. Photobiol. B. 63:2001;61-69.
50. Karasek M.A. Progress in our understanding of the biology of psoriasis. Cutis. 64:1999;319-322.
51. Kuhn A., Fehsel K., Lehmann P., Krutmann J., Ruzicka T., Kolb-Bachofen V. Abberant timing in epidermal expression of inducible nitric oxide synthase after UV irradiation in cutaneous lupus erythematosus. J. Invest. Dermatol. 111:1998;149-153.
52. Deliconstantinos G., Villiotou V., Stavrides J.C. Increase of particulate nitric oxide synthase activity and peroxynitrite synthesis in UVB-irradiated keratinocyte membranes. Biochem. J. 320:1996;997-1003.
53. Kang-Rotondo C.H., Major S., Chiang T.M., Myers L.K., Kang E.S. Upregulation of nitric oxide synthase in cultured human keratinocytes after ultraviolet B and bradykinin. Photodermatol. Photoimmunol. Photomed. 12:1996;57-65.
54. Sasaki M., Yamaoka J., Miyachi Y. The effect of ultraviolet B irradiation on nitric oxide synthase expression in murine keratinocytes. Exp. Dermatol. 9:2000;417-422.
55. Yamaoka S., Sasaki M., Miyachi Y. Ultraviolet B radiation downregulates inducible nitric oxide synthase expression induced by IFN-γ or tumor necrosis factor-α in murine keratinocyte PAM 212 cells. Arch. Dermatol. Res. 292:2000;312-319.
56. Kyriakis J.M., Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol. Rev. 81:2001;807-869.
57. Peus D., Vasa R.A., Beyerle A., Meves A., Krautmacher C., Pittelkow M.R. UVB activates ERK1/2 and p38 signaling pathways via reactive oxygen species in cultured keratinocytes. J. Invest. Dermatol. 112:1999;751-756.
58. Shimizu H., Banno Y., Sumi N., Naganawa T., Kitajima Y., Nozawa Y. Activation of p38 mitogen-activated protein kinase and caspases in UVB-induced apoptosis of human keratinocyte HaCaT cells. J. Invest. Dermatol. 112:1999;769-774.
59. Chen W., Bowden G.T. Activation of p38 MAP kinase and ERK are required for ultraviolet-B induced c-fos gene expression in human keratinocytes. Oncogene. 18:1999;7469-7476.
60. Ramaswamy N.T., Ronai Z., Pelling J.C. Rapid activation of JNK1 in UV-B irradiated epidermal keratinocytes. Oncogene. 16:1998;1501-1505.
61. Hsi L.C., Wilson L., Nixon J., Eling T.E. 15-Lipoxygenase-1 metabolites down-regulate peroxisome proliferator-activated receptor γ via the MAPK signaling pathway. J. Biol. Chem. 276:2001;34545-34552.
62. Adams M., Reginato M.J., Shao D., Lazar M.A., Chatterjee V.K. Transcriptional activation by peroxisome proliferator-activated receptor γ is inhibited by phosphorylation at a consensus mitogen-activated protein kinase site. J. Biol. Chem. 272:1997;5128-5132.
63. Hu E., Kim J.B., Sarraf P., Spiegelman B.M. Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARγ Science. 274:1996;2100-2103.
64. Ricote M., Li A.C., Willson T.M., Kelly C.J., Glass C.K. The peroxisome proliferator-activated receptor-γ is a negative regulator of macrophage activation. Nature. 391:1998;79-82.
65. Ricote M., Welch J.S., Glass C.K. Regulation of macrophage gene expression by the peroxisome proliferator-activated receptor-γ Horm. Res. 54:2000;275-280.
66. Li M., Pascual G., Glass C.K. Peroxisome proliferator-activated receptor γ-dependent repression of the inducible nitric oxide synthase gene. Mol. Cell Biol. 20:2000;4699-4707.
67. Mazars A., Lallemand F., Prunier C., Marais J., Ferrand N., Pessah M., Cherqui G., Atfi A. Evidence for a role of the JNK cascade in Smad7-mediated apoptosis. J. Biol. Chem. 276:2001;36797-36803.
68. Quan T., He T., Voorhees J.J., Fisher G.J. Ultraviolet irradiation blocks cellular responses to transforming growth factor-β by down-regulating its type-II receptor and inducing Smad7. J. Biol. Chem. 276:2001;26349-26356.
69. Werner F., Jain M.K., Feinberg M.W., Sibinga N.E.S., Pellacani A., Wiesel P., Chin M.T., Topper J.N., Perrella M.A., Lee M.E. Transforming growth factor-β1 inhibition of macrophage activation is mediated via Smad3. J. Biol. Chem. 275:2000;36653-36658.
70. Murphy WJ. Transcriptional regulation of the genes encoding nitric oxide synthase. In: Laskin JD, Laskin DL, editors. Cellular and molecular biology of nitric oxide. New York: Marcel Dekker; 1999, p. 1-56.
71. Xie Q., Kashiwabara Y., Nathan C. Role of transcription factor NF-κB/Rel in induction of nitric oxide synthase. J. Biol. Chem. 269:1994;4705-4708.
72. Lowenstein C.J., Alley E.W., Raval P., Snowman A.M., Snyder S.H., Russel S.W., Murphy W.J. Macrophage nitric oxide synthase gene: two upstream regions mediate induction of interferon-γ and lipopolysaccharide. Proc. Natl. Acad. Sci. U.S.A. 90:1993;9730-9734.
73. Helenius M., Makelainen L., Salminen A. Attenuation of NF-κB signaling response to UVB light during cellular senescence. Exp. Cell Res. 248:1999;194-202.
74. Tobin D., van Hogerlinden M., Toftgard R. UVB-induced association of tumor necrosis factor (TNF) receptor 1/TNF receptor-associated factor-2 mediates activation of Rel proteins. Proc. Natl. Acad. Sci. U.S.A. 95:1998;565-569.
75. Liu G., Chen N., Kaji A., Bode A.M., Ryan C.A., Dong Z. Proteinase inhibitors I and II from potatoes block UVB-induced AP-1 activity by regulating the AP-1 protein compositional patterns in JB6 cells. Proc. Natl. Acad. Sci. U.S.A. 98:2001;5786-5791.
76. Huber M.A., Denk A., Peter R.U., Weber L., Kraut N., Wirth T. The IKK-2/IκBα/NF-κB pathway plays a key role in the regulation of CCR3 and eotaxin-1 in fibroblasts: a critical link to dermatitis in IκBα-deficient mice. J. Biol. Chem. 277:2002;1268-1275.
77. Aragane Y., Kulms D., Luger T.A., Schwarz T. Down-regulation of interferon γ-activated STAT1 by UV light. Proc. Natl. Acad. Sci. U.S.A. 94:1997;11490-11495.