Active Oxygen Mechanisms of UV Inflammation

  • Alice P. Pentland
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 366)

Summary

Active oxygen radicals are important in the pathogenesis of UV irradiation injury. The initiating mechanisms involve the generation of hydroxyl radicals, superoxide, and organic hydroperoxides due to photochemical reactions. These active oxygen species lead to DNA strand breakage, mutation and the generation of inflammatory mediators such as cytokines and arachidonic acid metabolites which amplify the irradiation-induced inflammation. Several compounds have recently been utilized to successfully decrease these effects. Improved understanding of the mechanisms by which active oxygen species induce injury in skin now promises improved treatment.

Keywords

Tyrosine Glutathione Ozone Aspirin Adduct 

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References

  1. 1.
    L.C. Harber and D.R. Bickers, and A. Lamola, Principles of light absorption and photochemistry, in: Photosensitivity Diseases. W.B. Saunders Co.; Second ed., Philadelphia (1989).Google Scholar
  2. 2.
    R.S. Cotran and M.A. Pathak, The pattern of vascular leakage induced by monochromatic UV irradiation in rats, guinea pigs and hairless mice, J Invest Dermatol. 51:155–164 (1968).PubMedGoogle Scholar
  3. 3.
    G. Logan and D.L. Wilhelm, Vascular permeability changes in inflammation: I. The role of endogenous permeability factors in ultraviolet injury. Br J Exp Pathol. 47:300–314 (1966).PubMedGoogle Scholar
  4. 4.
    N.A. Soter, Acute effects of ultraviolet radiation on the skin. Semin Dermatol. 9:11–15 (1990)PubMedGoogle Scholar
  5. 5.
    D.E. Brash, J.A. Rudolph, J.A. Simon, A. Lin, G.J. McKenna, H.P. Baden, A.J. Halperin and J Ponten, A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc Natl Acad Sci. 88:10124–10128 (1991).PubMedCrossRefGoogle Scholar
  6. 6.
    D.R. Bickers and L.C. Harber, Non-melanonia skin cancer and melanomas in: Photosensitivity Diseases. Saunders Co., Second ed., Philadelphia: W.B. (1989).Google Scholar
  7. 7.
    I.E. Kochevar, M.A. Pathak and J.A. Parrish, Photophysics, photochemistry, and photobiology. in: Dermatology in General Medicine. T.B. Fitzpatrick, A.Z. Eisen, K. Wolff, I.M. Freedberg and K.F. Austen eds., Fourth ed. McGraw-Hill, New York (1993).Google Scholar
  8. 8.
    A. Bachern, Time factors of erythema and pigmentation produced by ultraviolet rays of difference wavelengths. J Invest Dermatol. 25:215–218 (1955).CrossRefGoogle Scholar
  9. 9.
    J.L.M. Hawk and J. A. Parrish, Responses of normal skin to ultraviolet radiation, in: Photoimmunology. J.A. Parrish, M.L. Kriple and W.L. Morrison eds., Plenum Medical Book, New York (1983).Google Scholar
  10. 10.
    R.R. Anderson and J. A. Parrish, The optics of human skin. J Invest Dermatol. 77:13–19 (1981).PubMedCrossRefGoogle Scholar
  11. 11.
    M.A. Pathak and K. Stratton, Free radicals in human skin before and after exposure to light. Arch Derm and Biophysics. 123:468–476 (1968).CrossRefGoogle Scholar
  12. 12.
    E. Pelle, D. Maes, G.A. Padulo, E.-K. Kim, and W.P. Smith, An in vitro model to test relative antioxidant potential: Ultraviolet-induced lipid peroxidation in liposomes. Arch of Biochem and Biophys. 283:234–240 (1990).CrossRefGoogle Scholar
  13. 13.
    I. Fridovich, The biology of oxygen radicals. Science 201:875–880 (1978).PubMedCrossRefGoogle Scholar
  14. 14.
    R. Dixit, H. Mukhtar and D.R. Bickers, Studies on the role of reactive oxygen species in mediating lipid peroxide formation in epidermal microsomes of rat skin. J Invest Dermatol. 81:369–375 (1983).PubMedCrossRefGoogle Scholar
  15. 15.
    A. Petkau, Protection and repair of irradiated membranes, in: Free Radicals, Aging, and Degenerative Disease, Alan R. Liss, Inc. (1986).Google Scholar
  16. 16.
    N.J. Holbrook and A.J. Fornace, Jr., Response to adversity: molecular control of gene activation following genotoxic stress. New Biol. 3:825–833 (1991).PubMedGoogle Scholar
  17. 17.
    J.E. LeClerc, A. Borden and C.W. Lawrence, The thymine-thymine pyrimidine-pyrimidine (6–4) ultraviolet light photoproduct is highly mutagenic and specifically induces 3’thymine-to-cytosine transitions in Escherichia coli. Proc Natl Acad Sci. USA 88:9685–9689 (1991).CrossRefGoogle Scholar
  18. 18.
    D. L. Svoboda, C.A. Smith, J-S A. Taylor and A. Sancar, Effect of sequence, adduct type, and opposing lesions on the binding and repair of ultraviolet photodamage by DNA photolyase and (A)BC excinuclease. J Biol Chem. 268:10694–10700 (1993).PubMedGoogle Scholar
  19. 19.
    J. Piette, M. Paule, M. Louis and J. Decuyper, Damages induced in nucleic acids by photosensitization. Photochem and Photohiol. 44:793–802 (1986).CrossRefGoogle Scholar
  20. 20.
    Z.A. Ronai, M.E. Lambert and I.B. Weinstein, Inducible cellular responses to ultraviolet light irradiation and other mediators of DNA damage in mammalian cells. Cell Biol and Toxicology. 6:105–126 (1990).CrossRefGoogle Scholar
  21. 21.
    Y. Devary, R.A. Gottlieb, T. Smeal and M. Karin, The mammalian ultraviolet response is triggered by activation of src tyrosine kinases. Cell. 71:1081–1091.Google Scholar
  22. 22.
    Y. Devary, C. Rosette, J.A. DiDonato and M. Karin, NF-kB activation by ultraviolet light not dependent on a nuclear signal. Science. 261:1442–1445 (1993).PubMedCrossRefGoogle Scholar
  23. 23.
    Y.A. Vladimirov, Free radical lipid peroxidation in biomembranes: mechanism, regulation, and biological consequences, in: Free Radicals, Aging, and Degenerative Diseases, Plenum Press, New York (1986).Google Scholar
  24. 24.
    E.D. Wills, Mechanisms of lipid peroxide formation in animal tissues. Biochem J. 99:667–676, (1966).PubMedGoogle Scholar
  25. 25.
    M.K. Logani and R.E. Davies, Lipid oxidation: biologic effects and antioxidants — A review. Lipid. 15:485–495, (1980).CrossRefGoogle Scholar
  26. 26.
    J. Nishi, R. Ogura, M. Sugiyama, T. Hidaka and M. Kohno, Involvement of active oxygen in lipid peroxide radical reaction of epidermal homogenate following ultraviolet light exposure. J Invest Dermatol. 97:115–119 (1990).CrossRefGoogle Scholar
  27. 27.
    J. Fuchs, M.E. Huflejt, A.B. Rothfuss, A.B. Wilson, G. Carcamo and L. Packer, Impairment of enzymic and nonenzymic antioxidants in skin by UVB irradiation. J Invest Dermatol. 93:769–773 (1989).PubMedCrossRefGoogle Scholar
  28. 28.
    S.M. Keyse and R. M. Tyrrell, Induction of the heme oxygenase gene in human skin fibroblasts by hydrogen peroxide and UVA (365 nm) radiation: evidence for the involvement of the hydroxyl radical. Carcinogenesis. 11:787–791 (1990).PubMedCrossRefGoogle Scholar
  29. 29.
    D. Lautier, P. Luscher and R.M. Tyrrell, Endogenous glutathione levels modulated both constitutive and UVA radiation/hydrogen peroxide inducible expression of the human heme oxygenase gene. Carcinogenesis. 13:227–232 (1992).PubMedCrossRefGoogle Scholar
  30. 30.
    A.P. Pentland and M.G. Mahoney, Keratinocyte prostaglandin synthesis is enhanced by IL-1. J Invest Dermatol 94:43–46 (1990).PubMedCrossRefGoogle Scholar
  31. 31.
    T.S. Kupper, A.O. Chua, P. Flood, J. McGuire and U. Gubler, Interleukin 1 gene expression in cultured human keratinocytes is augmented by ultraviolet irradiation. J Clin Invest. 80:430–436 (1987).PubMedCrossRefGoogle Scholar
  32. 32.
    A. Kock, T. Schwarz, R. Kirnbauer, A. Urbanski, P. Perry, J.C. Ansel and T.A. Luger, Human keratinocytes are a source for tumor necrosis factor α: evidence for synthesis and release upon stimulation with endotoxin or ultraviolet light. J Exper Med. 172:1609–1614 (1990).CrossRefGoogle Scholar
  33. 33.
    M. Grewe, U. Trefzer, A. Ballhorn, K. Gyufko, H. Henninger and J. Krutmann, Analysis of the mechanism of ultraviolet (UV) B radiation-induced prostaglandin E2 synthesis by human epidermoid carcinoma cells. J Invest Derm. 4:528–531 (1993).CrossRefGoogle Scholar
  34. 34.
    J.B. Warren, R.K. Loi and M.L. Coughlan, Involvement of nitric oxide synthase in the delayed vasodilator response to ultraviolet light irradiation of rat skin in vivo. Br. J Pharmacol. 109:802–806 (1993).PubMedCrossRefGoogle Scholar
  35. 35.
    D. Salvemini, T.P. Misko, J.L. Masferrer, K. Seibert, M.G. Currie and P. Needleman, Nitric oxide activates cyclooxygenase enzymes. Proc Natl Acad Sci. 90:7240–7244 (1993).PubMedCrossRefGoogle Scholar
  36. 36.
    W.L. Smith, Prostanoid biosynthesis and mechanisms of action. Am J Phys. 11:F181–F191 (1992).Google Scholar
  37. 37.
    W.S. Miller, F.R. Ruderman, and J.G. Smith Jr., Aspirin and ultraviolet light-induced erythema in man. Arch Dermatol. 95:357–358 (1967).PubMedCrossRefGoogle Scholar
  38. 38.
    A.K. Black, N. Fincham, M.W. Greaves, and C.N. Hensby, Time course changes in levels of arachidonic acid and prostaglandins D2 E2 F2 in human skin following ultraviolet irradiation. Br J Clin Pharmacol. 10:453–457 (1980).PubMedCrossRefGoogle Scholar
  39. 39.
    D.S. Snyder and W.H. Eaglstein, Intradermal anti-prostaglandin agents and sunburn. J Invest Dermatol. 62:47–50 (1974).CrossRefGoogle Scholar
  40. 40.
    A.K. Black, M.W. Greaves, C.N. Hensby and N.A. Plummer, Increased prostaglandins E2 and F in human skin at 6 and 24h after ultraviolet B irradiation (290–320 nm). Br J Clin Pharmacol. 5:431–436 (1978).PubMedCrossRefGoogle Scholar
  41. 41.
    V.A. DeLeo, H. Horlick, D. Hanson, M. Eisinger and L.C. Harber, Ultraviolet radiation stimulates the release of arachidonic acid from mammalian cells in culture. Photchem Photobiol. 41:51–56 (1985).CrossRefGoogle Scholar
  42. 42.
    A.P. Pentland, M. Mahoney, S.C. Jacobs and M.J. Holtzman, Enhanced prostaglandin synthesis after ultraviolet injury is mediated by endogenous histamine stimulation. J Clin Invest. 86:566–574 (1990).PubMedCrossRefGoogle Scholar
  43. 43.
    B.A. Gilchrest, N.A. Soter, J.S. Stoff and M.C. Mihm, The human sunburn reaction: histologic and biochemical studies. J Am Acad Dermatol. 5:411–422 (1981).PubMedCrossRefGoogle Scholar
  44. 44.
    V. DeLeo, S. Scheide, J. Meshulam, D. Hanson and A. Cardullo, Ultraviolet radiation alters choline phospholipid metabolism in human keratinocytes. J Invest Dermatol. 91:303–308 (1988).PubMedCrossRefGoogle Scholar
  45. 45.
    A.P. Pentland and S.C. Jacobs, Bradykinin-induced prostaglandin synthesis is enhanced in keratinocytes and fibroblasts by UV injury. Am J Physiol. 261:R543–R547 (1991).PubMedGoogle Scholar
  46. 46.
    C.H. Kang-Rotondo, C.C. Miller, A.R. Morrison and A.P. Pentland. Enhanced keratinocyte prostaglandin synthesis after UV injury is due to increased phospholipase activity. Am J Physiol. 264:C396–C401 (1993).PubMedGoogle Scholar
  47. 47.
    C.C. Miller, P. Hale and A.P. Pentland, Ultraviolet B injury increases prostaglandin synthesis through a tyrosine kinase-dependent pathway. Evidence for UVB-induced epidermal growth factor receptor activation. J Biol Chem. 269:3529–3533 (1994).PubMedGoogle Scholar
  48. 48.
    W.L. Smith, Prostanoid biosynthesis and mechanisms of action. Am J Physiol. 263:F181–F191 (1992).PubMedGoogle Scholar
  49. 49.
    J.D. Clark, L.L. Lin, R.W. Kris, C.S. Ramesha, L.A. Sutzman, X.L. Lin, N. Milona, and J.L. Knopf, A novel arachidonic acid-selective cytosolic phospholipase A2 contains a Ca++-dependent translocation domain with homology to PKC and GAP. Cell. 65:1043–1051 (1991).PubMedCrossRefGoogle Scholar
  50. 50.
    J.H. Gronich, J.V. Bonventre and R.A. Nemenoff, Purification of a high-molecular mass form of phospholipase A2 from rat kidney is activated at physiological Ca++ concentrations. Biochem J. 271:37–43 (1990).PubMedGoogle Scholar
  51. 51.
    R.J. Mayer and L.A. Marshall, New insights on mammalian phospholipase A2(s); comparison of arachidonoyl-selective and nonselective enzymes. FASEB J. 7:339–348 (1993).PubMedGoogle Scholar
  52. 52.
    L.L. Lin, A.Y. Lin and J.L. Knopf, Cytosolic phospholipase A2 is coupled to hormonally regulated release of arachidonic acid. Proc Natl Acad Sci. USA 89:6146–6151 (1992).Google Scholar
  53. 53.
    L.L. Lin, M. Wartman, A.Y. Lin, J.L. Knopf, A. Seth, and R. J. Davies, cPLA2 is phosphorylated and activated by MAP kinase. Cell. 72:69–278 (1993).CrossRefGoogle Scholar
  54. 54.
    R.A. Nemenoff, S. Winitz, N.X. Quian, V. Van Putten, G.L. Johnson and L.E. Heasley, Phosphorylation and activation of a high molecular weight form of phospholipase A2 by p42 microtubule-associated protein 2 kinase and protein kinase C. J Biol Chem. 268:1640–1663 (1993).Google Scholar
  55. 55.
    B.J. Pulverer, J.M. Kyriakis, J. Avruch, E. Nikolakaki and J.R. Woodgett, Phosphorylation of c-jun mediated by MAP kinases. Nature. 353:670–674 (1991).PubMedCrossRefGoogle Scholar
  56. 56.
    S.A. Moodie, B.M. Willumsen, M.J. Weber and A. Wolfman, Complexes of Ras GTP with Raf-1 and mitogen-activated protein kinase. Science. 260:1658–1661 (1993).PubMedCrossRefGoogle Scholar
  57. 57.
    R. Muller, D. Mumberg and F.C. Lucibello, Signals and genes in the control of cell cycle progression. Biochem et Biophys Acta. 1155:151–179 (1993).Google Scholar
  58. 58.
    A. Gresham, J. Masferrar, A. Morrison and A.P. Pentland, Cytosolic phospholipase A2 synthesis is enhanced in human keratinocytes by acute UVB irradiation. J Invest Dermatol. 100:595A (1993).Google Scholar
  59. 59.
    W.G. Hoeck, C.S. Ramesha, D.J. Chang, N. Fan and R.A. Heller, Cytoplasmic phospholipase A2 activity and gene expression are stimulated by tumor necrosis factor: Dexamtheansone blocks the induced synthesis. Proc Natl Acad Sci. USA 90:4475–4479 (1993).PubMedCrossRefGoogle Scholar
  60. 60.
    V. Kagan, E. Witt, R. Goldman, G. Scita and L. Packer, Ultraviolet lightinduced generation of vitamin E radicals and their recycling. A possible photosensitizing effect of vitamin E in skin. Free Rad Res Comm. 16:51–64 (1992).CrossRefGoogle Scholar
  61. 61.
    H.J. Forman and A.B. Fisher, Antioxidant defenses. in: Gilbert DL eds., Oxygen and Living Processes-An interdisciplinary Approach. Springer-Verlag, New York, 1981.Google Scholar
  62. 62.
    D.A. Gamache, A.A. Fawzy and R.C. Franson, Preferential hydrolysis of peroxidized phospholipid by lysosomal phospholipase C. Biochim Biophys Acta. 958:116–124 (1988).PubMedCrossRefGoogle Scholar
  63. 63.
    A.P. Pentland, A.R. Morrison, S.C. Jacobs, L. Hruza, J.S. Hebert and L. Packer, Tocopherol analogs suppress arachidonic acid metabolism via phospholipase inhibition. J. Biol Chem. 267:15578–15584 (1992).PubMedGoogle Scholar
  64. 64.
    A. Meister and M.E. Anderson, Glutathione. Ann Rev Biochem. 52:711–760 (1983).PubMedCrossRefGoogle Scholar
  65. 65.
    R.M. Tyrell and M. Pidoux, Endogenous glutathione protects human skin fibroblasts against the cytotoxic action of UVB, UVA and near-visible radiations. Photochem Photobiol. 44:561–564 (1986).CrossRefGoogle Scholar
  66. 66.
    M.J. Connor and L.A. Wheeler, Depletion of cutaneous glutathione by ultraviolet radiation. Photochem Photobiol. 46:239–245 (1987).PubMedCrossRefGoogle Scholar
  67. 67.
    K. Hanada, R.W. Gange and M.J. Connor, Effect of glutathione depletion on sunburn cell formation in the hairless mouse. J Invest Dermatol. 96:838–840 (1991).PubMedCrossRefGoogle Scholar
  68. 68.
    C.A. Rice-Evans and A. T. Diplock, Current status of antioxidant therapy. Free Rod Biol and Med. 15:77–96 (1993).CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1994

Authors and Affiliations

  • Alice P. Pentland
    • 1
  1. 1.Division of Dermatology, School of MedicineWashington UniversitySt. LouisUSA

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