The malondialdehyde-derived fluorophore DHP-lysine is a potent sensitizer of UVA-induced photooxidative stress in human skin cells

Journal of Photochemistry and Photobiology B: Biology

Volumn 101, Issue 3, 2010, Pages 251-264

  Lamore, Sarah D ^a   Azimian, Sara ^a   Horn, David ^a   Anglin, Bobbi L ^a   Uchida, Koji ^b   Cabello, Christopher M ^a   Wondrak, Georg T ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b NAGOYA UNIVERSITY   (Japan)

Author keywords

DHP lysine; Lipid peroxidation; Photosensitization; Skin photooxidative stress; UVA

Indexed keywords

ANTIOXIDANT; CATALASE; DIHYDROPYRIDINE DERIVATIVE; DIHYDROPYRIDINE LYSINE; EPITOPE; HEME OXYGENASE 1; HEXANOIC ACID DERIVATIVE; HYDROGEN PEROXIDE; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE P38; PEPTIDE; PHOTOSENSITIZING AGENT; REACTIVE OXYGEN METABOLITE; SINGLET OXYGEN; SUPEROXIDE; SUPEROXIDE DISMUTASE; TERT BUTYLOXYCARBONYL 2 AMINO 6 ( 3,5 DIFORMYL 4 METHYL 4H PYRIDIN 1 YL)HEXANOIC ACID TERT BUTYLESTER; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; ARTICLE; CELL DEATH; CELL LINE; CELL PROLIFERATION; CELL PROTECTION; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRACELLULAR MEMBRANE; KERATINOCYTE; OXIDATIVE STRESS; PHOTODYNAMICS; PHOTOOXIDATION; PHOTOSENSITIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; SKIN CELL; SKIN FIBROBLAST; ULTRAVIOLET A RADIATION;

APOPTOSIS; CATALASE; FIBROBLASTS; HEME OXYGENASE-1; HUMANS; KERATINOCYTES; LYSINE; MALONDIALDEHYDE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOTOSENSITIZING AGENTS; PYRIDINES; REACTIVE OXYGEN SPECIES; SKIN; SODIUM AZIDE; SUPEROXIDE DISMUTASE; ULTRAVIOLET RAYS;

EID: 77958151524     PISSN: 10111344     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jphotobiol.2010.07.010     Document Type: Article

References (63)

1. Scharffetter-Kochanek K., Wlaschek M., Brenneisen P., Schauen M., Blaudschun R., Wenk J. UV-induced reactive oxygen species in photocarcinogenesis and photoaging. Biol. Chem. 1997, 378:1247-1257.
2. Wondrak G.T., Jacobson M.K., Jacobson E.L. Endogenous UVA-photosensitizers: mediators of skin photodamage and novel targets for skin photoprotection. Photochem. Photobiol. Sci. 2006, 5:215-237.
3. Brash D.E., Rudolph J.A., Simon J.A., Lin A., McKenna G.J., Baden H.P., Halperin A.J., Ponten J. A role for sunlight in skin cancer: UV-induced p53 mutations in squamous cell carcinoma. Proc. Natl. Acad. Sci. USA 1991, 88:10124-10128.
4. Gasparro F.P. Sunscreens, skin photobiology, and skin cancer: the need for UVA protection and evaluation of efficacy. Environ. Health Perspect. 2000, 108(Suppl. 1):71-78.
5. Halliday G.M. Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat. Res. 2005, 571:107-120.
6. Cadet J., Douki T., Ravanat J.L., Di Mascio P. Sensitized formation of oxidatively generated damage to cellular DNA by UVA radiation. Photochem. Photobiol. Sci. 2009, 8:903-911.
7. Valencia A., Kochevar I.E. Nox1-based NADPH oxidase is the major source of UVA-induced reactive oxygen species in human keratinocytes. J. Invest. Dermatol. 2008, 128:214-222.
8. Salet C., Moreno G. Photodynamic action increases leakage of the mitochondrial electron transport chain. Int. J. Radiat. Biol. 1995, 67:477-480.
9. Kvam E., Tyrrell R.M. Induction of oxidative DNA base damage in human skin cells by UV and near visible radiation. Carcinogenesis 1997, 18:2379-2384.
10. Dalle Carbonare M., Pathak M.A. Skin photosensitizing agents and the role of reactive oxygen species in photoaging. J. Photochem. Photobiol. B 1992, 14:105-124.
11. Foote C.S. Definition of type I and type II photosensitized oxidation. Photochem. Photobiol. 1991, 54:659.
12. Menon E.L., Morrison H. Formation of singlet oxygen by urocanic acid by UVA irradiation and some consequences thereof. Photochem. Photobiol. 2002, 75:565-569.
13. Sato K., Taguchi H., Maeda T., Minami H., Asada Y., Watanabe Y., Yoshikawa K. The primary cytotoxicity in ultraviolet-a-irradiated riboflavin solution is derived from hydrogen peroxide. J. Invest. Dermatol. 1995, 105:608-612.
14. Baier J., Maisch T., Maier M., Engel E., Landthaler M., Baumler W. Singlet oxygen generation by UVA light exposure of endogenous photosensitizers. Biophys. J. 2006, 91:1452-1459.
15. Wondrak G.T., Roberts M.J., Jacobson M.K., Jacobson E.L. 3-hydroxypyridine chromophores are endogenous sensitizers of photooxidative stress in human skin cells. J. Biol. Chem. 2004, 279:30009-30020.
16. Kipp C., Young A.R. The soluble eumelanin precursor 5,6-dihydroxyindole-2-carboxylic acid enhances oxidative damage in human keratinocyte DNA after UVA irradiation. Photochem. Photobiol. 1999, 70:191-198.
17. Wondrak G.T., Jacobson E.L., Jacobson M.K. Photosensitization of DNA damage by glycated proteins. Photochem. Photobiol. Sci. 2002, 1:355-363.
18. Wondrak G.T., Roberts M.J., Jacobson M.K., Jacobson E.L. Photosensitized growth inhibition of cultured human skin cells: mechanism and suppression of oxidative stress from solar irradiation of glycated proteins. J. Invest. Dermatol. 2002, 119:489-498.
19. Young A.R. Chromophores in human skin. Phys. Med. Biol. 1997, 42:789-802.
20. Heck D.E., Vetrano A.M., Mariano T.M., Laskin J.D. UVB light stimulates production of reactive oxygen species: unexpected role for catalase. J. Biol. Chem. 2003, 278:22432-22436.
21. Wondrak G.T., Jacobson M.K., Jacobson E.L. Identification of quenchers of photoexcited states as novel agents for skin photoprotection. J. Pharmacol. Exp. Ther. 2005, 312:482-491.
22. Slatter D.A., Bolton C.H., Bailey A.J. The importance of lipid-derived malondialdehyde in diabetes mellitus. Diabetologia 2000, 43:550-557.
23. Ye X., Tong Z., Dang Y., Tu Q., Weng Y., Liu J., Zhang Z. Effects of blood glucose fluctuation on skin biophysical properties, structure and antioxidant status in an animal model. Clin. Exp. Dermatol. 2010, 35:78-82.
24. Sander C.S., Hamm F., Elsner P., Thiele J.J. Oxidative stress in malignant melanoma and non-melanoma skin cancer. Br. J. Dermatol. 2003, 148:913-922.
25. Yan S.X., Hong X.Y., Hu Y., Liao K.H. Tempol, one of nitroxides, is a novel ultraviolet-A1 radiation protector for human dermal fibroblasts. J. Dermatol. Sci. 2005, 37:137-143.
26. Slatter D.A., Murray M., Bailey A.J. Formation of a dihydropyridine derivative as a potential cross-link derived from malondialdehyde in physiological systems. FEBS Lett. 1998, 421:180-184.
27. Del Rio D., Stewart A.J., Pellegrini N. A review of recent studies on malondialdehyde as toxic molecule and biological marker of oxidative stress. Nutr. Metab. Cardiovasc. Dis. 2005, 15:316-328.
28. Uchida K. Lipofuscin-like fluorophores originated from malondialdehyde. Free Radic. Res. 2006, 40:1335-1338.
29. Ishii T., Kumazawa S., Sakurai T., Nakayama T., Uchida K. Mass spectroscopic characterization of protein modification by malondialdehyde. Chem. Res. Toxicol. 2006, 19:122-129.
30. Mahmoodi H., Hadley M., Chang Y.X., Draper H.H. Increased formation and degradation of malondialdehyde-modified proteins under conditions of peroxidative stress. Lipids 1995, 30:963-966.
31. Yamada S., Kumazawa S., Ishii T., Nakayama T., Itakura K., Shibata N., Kobayashi M., Sakai K., Osawa T., Uchida K. Immunochemical detection of a lipofuscin-like fluorophore derived from malondialdehyde and lysine. J. Lipid Res. 2001, 42:1187-1196.
32. Terman A., Brunk U.T. Oxidative stress, accumulation of biological 'garbage' and aging. Antioxid. Redox. Signal. 2006, 8:197-204.
33. Kikugawa K., Ido Y. Studies on peroxidized lipids. V. Formation and characterization of 1,4-dihydropyridine-3,5-dicarbaldehydes as model of fluorescent components in lipofuscin. Lipids 1984, 19:600-608.
34. Widmer R., Ziaja I., Grune T. Protein oxidation and degradation during aging: role in skin aging and neurodegeneration. Free Radic. Res. 2006, 40:1259-1268.
35. Jung T., Bader N., Grune T. Lipofuscin: formation, distribution, and metabolic consequences. Ann NY Acad. Sci. 2007, 1119:97-111.
36. Sparrow J.R., Nakanishi K., Parish C.A. The lipofuscin fluorophore A2E mediates blue light-induced damage to retinal pigmented epithelial cells. Invest. Ophthalmol. Vis. Sci. 2000, 41:1981-1989.
37. Wondrak G.T., Cabello C.M., Villeneuve N.F., Zhang S., Ley S., Li Y., Sun Z., Zhang D.D. Cinnamoyl-based Nrf2-activators targeting human skin cell photo-oxidative stress. Free Radic. Biol. Med. 2008, 45:385-395.
38. Wondrak G.T. NQO1-activated phenothiazinium redox cyclers for the targeted bioreductive induction of cancer cell apoptosis. Free Radic. Biol. Med. 2007, 43:178-190.
39. Ohkawa H., Ohishi N., Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem. 1979, 95:351-358.
40. Kraljic I., El Mohsni S. A new method for the detection of singlet oxygen in aqueous solutions. Photochem. Photobiol. 1978, 28:577-581.
41. Wright A., Hawkins C.L., Davies M.J. Photo-oxidation of cells generates long-lived intracellular protein peroxides. Free Radic. Biol. Med. 2003, 34:637-647.
42. Bachelor M.A., Bowden G.T. UVA-mediated activation of signaling pathways involved in skin tumor promotion and progression. Semin. Cancer Biol. 2004, 14:131-138.
43. Klotz L.O., Briviba K., Sies H. Mitogen-activated protein kinase activation by singlet oxygen and ultraviolet A. Methods Enzymol. 2000, 319:130-143.
44. Buchczyk D.P., Klotz L.O., Lang K., Fritsch C., Sies H. High efficiency of 5-aminolevulinate-photodynamic treatment using UVA irradiation. Carcinogenesis 2001, 22:879-883.
45. Tyrrell R.M. Solar ultraviolet A radiation: an oxidizing skin carcinogen that activates heme oxygenase-1. Antioxid. Redox Signal. 2004, 6:835-840.
46. Dolmans D.E., Fukumura D., Jain R.K. Photodynamic therapy for cancer. Nat. Rev. Cancer 2003, 3:380-387.
47. Guptasarma P., Balasubramanian D., Matsugo S., Saito I. Hydroxyl radical mediated damage to proteins, with special reference to the crystallins. Biochemistry 1992, 31:4296-4303.
48. Luxford C., Morin B., Dean R.T., Davies M.J. Histone H1- and other protein- and amino acid-hydroperoxides can give rise to free radicals which oxidize DNA. Biochem. J. 1999, 344:125-134.
49. Davies M.J. Singlet oxygen-mediated damage to proteins and its consequences. Biochem. Biophys. Res. Commun. 2003, 305:761-770.
50. Camera E., Mastrofrancesco A., Fabbri C., Daubrawa F., Picardo M., Sies H., Stahl W. Astaxanthin, canthaxanthin and beta-carotene differently affect UVA-induced oxidative damage and expression of oxidative stress-responsive enzymes. Exp. Dermatol. 2009, 18:222-231.
51. Polte T., Tyrrell R.M. Involvement of lipid peroxidation and organic peroxides in UVA-induced matrix metalloproteinase-1 expression. Free Radic. Biol. Med. 2004, 36:1566-1574.
52. Davies M.J. Reactive species formed on proteins exposed to singlet oxygen. Photochem. Photobiol. Sci. 2004, 3:17-25.
53. von Montfort C., Sharov V.S., Metzger S., Schoneich C., Sies H., Klotz L.O. Singlet oxygen inactivates protein tyrosine phosphatase-1B by oxidation of the active site cysteine. Biol. Chem. 2006, 387:1399-1404.
54. Fu M.X., Requena J.R., Jenkins A.J., Lyons T.J., Baynes J.W., Thorpe S.R. The advanced glycation end product, Nepsilon-(carboxymethyl)lysine, is a product of both lipid peroxidation and glycoxidation reactions. J. Biol. Chem. 1996, 271:9982-9986.
55. Tanaka N., Tajima S., Ishibashi A., Uchida K., Shigematsu T. Immunohistochemical detection of lipid peroxidation products, protein-bound acrolein and 4-hydroxynonenal protein adducts, in actinic elastosis of photodamaged skin. Arch. Dermatol. Res. 2001, 293:363-367.
56. Thiele J.J., Hsieh S.N., Briviba K., Sies H. Protein oxidation in human stratum corneum: susceptibility of keratins to oxidation in vitro and presence of a keratin oxidation gradient in vivo. J. Invest. Dermatol. 1999, 113:335-339.
57. Sander C.S., Chang H., Salzmann S., Muller C.S., Ekanayake-Mudiyanselage S., Elsner P., Thiele J.J. Photoaging is associated with protein oxidation in human skin in vivo. J. Invest. Dermatol. 2002, 118:618-625.
58. Mizutari K., Ono T., Ikeda K., Kayashima K., Horiuchi S. Photo-enhanced modification of human skin elastin in actinic elastosis by N(epsilon)-(carboxymethyl)lysine, one of the glycoxidation products of the Maillard reaction. J. Invest. Dermatol. 1997, 108:797-802.
59. Sell D.R., Kleinman N.R., Monnier V.M. Longitudinal determination of skin collagen glycation and glycoxidation rates predicts early death in C57BL/6NNIA mice. Faseb J. 2000, 14:145-156.
60. Kueper T., Grune T., Prahl S., Lenz H., Welge V., Biernoth T., Vogt Y., Muhr G.M., Gaemlich A., Jung T., Boemke G., Elsasser H.P., Wittern K.P., Wenck H., Stab F., Blatt T. Vimentin is the specific target in skin glycation. J. Biol. Chem. 2007, 282:23427-23436.
61. Sitte N., Merker K., Grune T., Von Zglinicki T. Lipofuscin accumulation in proliferating fibroblasts in vitro: an indicator of oxidative stress. Exp. Gerontol. 2001, 36:475-486.
62. Hohn A., Jung T., Grimm S., Grune T. Lipofuscin-bound iron is a major intracellular source of oxidants: role in senescent cells. Free Radic. Biol. Med. 2010, 48:1100-1108.
63. Girotti A.W. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J. Photochem. Photobiol. B 2001, 63:103-113.