The cross-talk between electrophiles, antioxidant defence and the endocannabinoid system in fibroblasts and keratinocytes after UVA and UVB irradiation

Journal of Dermatological Science

Volumn 81, Issue 2, 2016, Pages 107-117

  Gegotek, Agnieszka ^a   Biernacki, Michał ^a   Ambrozewicz, Ewa ^a   Surazyński, Arkadiusz ^a   Wroński, Adam ^a   Skrzydlewska, Elzbieta ^a  

^a MEDICAL UNIVERSITY OF BIALYSTOK   (Poland)

Author keywords

Fibroblasts; Keratinocytes; Nrf2; ROS; UV radiation

Indexed keywords

ANTIOXIDANT; ELECTROPHILE; ENDOCANNABINOID; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; REACTIVE OXYGEN METABOLITE; SUPEROXIDE; TRANSCRIPTION FACTOR NRF1; TRANSCRIPTION FACTOR NRF2; APOPTOSIS REGULATORY PROTEIN; NFE2L2 PROTEIN, HUMAN; NRF1 PROTEIN, HUMAN; NUCLEAR RESPIRATORY FACTOR 1;

ARTICLE; CELL DEATH; CONTROLLED STUDY; HUMAN; HUMAN CELL; KERATINOCYTE; LIPID PEROXIDATION; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PRIORITY JOURNAL; SKIN FIBROBLAST; ULTRAVIOLET A RADIATION; ULTRAVIOLET B RADIATION; CELL COMMUNICATION; CELL LINE; COMPARATIVE STUDY; FIBROBLAST; METABOLISM; OXIDATION REDUCTION REACTION; RADIATION RESPONSE; SIGNAL TRANSDUCTION; ULTRAVIOLET RADIATION;

ANTIOXIDANTS; APOPTOSIS REGULATORY PROTEINS; CELL COMMUNICATION; CELL LINE; ENDOCANNABINOIDS; FIBROBLASTS; HUMANS; KERATINOCYTES; LIPID PEROXIDATION; NF-E2-RELATED FACTOR 2; NF-KAPPA B; NUCLEAR RESPIRATORY FACTOR 1; OXIDATION-REDUCTION; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; SUPEROXIDES; ULTRAVIOLET RAYS;

EID: 84957428912     PISSN: 09231811     EISSN: 1873569X     Source Type: Journal    
DOI: 10.1016/j.jdermsci.2015.11.005     Document Type: Article

References (69)

1. Makrantonaki E., Zouboulis C.C. Skin alterations and diseases in advanced age. Drug Discovery Today Dis. Mech. 2008, 5:e153-e162.
2. Damian D.L., Barnetson R.S.C., Halliday G.M. Low-dose UVA and UVB have different time courses for suppression of contact hypersensitivity to a recall antigen in humans. J. Invest. Dermatol. 1999, 112:939-944.
3. Cadet J., Berger M., Douki T., Morin B., Raoul S., Ravanat J.L., et al. Effects of UV and visible radiation on DNA-final base damage. Biol. Chem. 1997, 378:1275-1286.
4. Riahi Y., Cohen G., Shamni O., Sasson S. Signaling and cytotoxic functions of 4-hydroxyalkenals. Am. J. Physiol. 2010, 299:E879-E886.
5. Milne G.L., Musiek E.S., Morrow J.D. The cyclopentenone (A2/J2) isoprostanes-unique, highly reactive products of arachidonate peroxidation. Antioxid. Redox Signal. 2005, 7:210-220.
6. Bíró T., Tóth B.I., Haskó G., Paus R., Pacher P. The endocannabinoid system of the skin in health and disease: novel perspectives and therapeutic opportunities. Trends Pharmacol. Sci. 2009, 30:411-420.
7. Hillard C.J. Biochemistry and pharmacology of the endocannabinoids arachidonylethanolamide and 2-arachidonylglycerol. Prostaglandins Other Lipid Mediat. 2000, 61:3-18.
8. Gasperi V., Dainese E., Oddi S., Sabatucci A., Maccarrone M. GPR55 and its interaction with membrane lipids: comparison with other endocannabinoid-binding receptors. Curr. Med. Chem. 2013, 20:64-78.
9. Felder C.C., Joyce K.E., Briley E.M., Mansouri J., Mackie K., Blond O., et al. Comparison of the pharmacology and signal transduction of the human cannabinoid CB1 and CB2 receptors. Mol. Pharmacol. 1995, 48:443-450.
10. Zheng D., Bode A.M., Zhao Q., Cho Y.Y., Zhu F., Ma W.Y., et al. The cannabinoid receptors are required for ultraviolet-induced inflammation and skin cancer development. Cancer Res. 2008, 68:3992-3998.
11. Lin J.Y., Selim M.A., Shea C.R., Grichnik J.M., Omar M.M., Monteiro-Riviere N.A., et al. UV photoprotection by combination topical antioxidants vitamin C and vitamin E. J. Am. Acad. Dermatol. 2003, 48:866-874.
12. Hazneci E., Karabulut A.B., Öztürk Ç., Batçioğlu K., Doğan G., Karaca Ş., et al. A comparative study of superoxide dismutase, catalase, and glutathione peroxidase activities and nitrate levels in vitiligo patients. Int. J. Dermatol. 2005, 44:636-640.
13. Atsushi M., Keizo N., Yukie K., Junsei M., Tomonori H., Nobuhiko H., et al. The novel Nrf2-interacting factor KAP1 regulates susceptibility to oxidative stress by promoting the Nrf2-mediated cytoprotective response. Biochem. J. 2011, 436:387-397.
14. Li N., Alam J., Venkatesan M.I., Eiguren-Fernandez A., Schmitz D., Di Stefano E., et al. Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflammatory and oxidizing effects of diesel exhaust chemicals. J. Immunol. 2004, 173:3467-3481.
15. Shibata T., Ohta T., Tong K.I., Kokubu A., Odogawa R., Tsuta K., et al. Cancer related mutations in NRF2 impair its recognition by Keap1-Cul3 E3 ligase and promote malignancy. Proc. Nat. Acad. Sci. U. S. A. 2008, 105:13568-13573.
16. Itoh K., Chiba T., Takahashi S., Ishii T., Igarashi K., Katoh Y., et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997, 236:313-322.
17. Gegotek A., Skrzydlewska E. The role of transcription factor Nrf2 in skin cells metabolism. Arch. Dermatol. Res. 2015, 307:385-396.
18. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72:248-254.
19. Kuzkaya N., Weissmann N., Harrison D.G., Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitricoxide synthase. J. Biol. Chem. 2003, 278:22546-22554.
20. Prajda N., Weber G. Malignant transformation-linked imbalance: decreased xanthine oxidase activity in hepatomas. FEBS Lett. 1975, 59:245-249.
21. Misra H.P., Fridovich I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J. Biol. Chem. 1972, 247:3170-3175.
22. Sykes J.A., McCormac F.X., O'Breien T.J. Preliminary study of the superoxide dismutase content of some human tumors. Cancer Res. 1978, 38:2759-2762.
23. Aebi H. Catalase in vitro. Methods Enzymol. 1984, 105:121-126.
24. Paglia D.E., Valentine W.N. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J. Lab. Clin. Med. 1967, 70:158-169.
25. Maeso N., Garcia-Martinez D., Ruperez F.J., Cifuentes A., Barbas C. Capillary electrophoresis of glutathione to monitor oxidative stress and response to antioxidant treatments in an animal model. J. Chromatogr. B 2005, 822:61-69.
26. Ivanović D., Popović A., Radulović D., Medenica M. Reversed-phase ion-pair HPLC determination of some watersoluble vitamins in pharmaceuticals. J. Pharm. Biomed. Anal. 1999, 18:999-1004.
27. Vatassery G.T., Brin M.F., Fahn S., Kayden H.J., Traber M.G. Effect of high doses of dietary vitamin E on the concentrations of vitamin E in several brain regions, plasma, liver, and adipose tissue of rats. J. Neurochem. 1988, 51:621-623.
28. Christie W.W. Preparation of ester derivatives of fatty acids for chromatographic analysis. Advances in Lipid Methodology -Two 1993, 69-111. Oily Press, Dundee. W.W. Christie (Ed.).
29. Luo X.P., Yazdanpanah M., Bhooi N., Lehotay D.C. Determination of aldehydes and other lipid peroxidation products in biological samples by gas chromatography-mass spectrometry. Anal. Biochem. 1995, 228:294-298.
30. Coolen S.A., van Buuren B., Duchateau G., Upritchard J., Verhagen H. Kinetics of biomarkers: biological and technical validity of isoprostanes in plasma. Amino Acids 2005, 29:429-436.
31. Lam P.M., Marczylo T.H., El-Talatini M., Finney M., Nallendran V., Taylor A.H., et al. Ultra performance liquid chromatography tandem mass spectrometry method for the measurement of anandamide in human plasma. Anal. Biochem. 2008, 380:195-201.
32. Dizdaroglu M., Jaruga P., Rodriguez H. Measurement of 8-hydroxy-2'-deoxyguanosine in DNA by highperformance liquid chromatography-mass spectrometry: comparison with measurement by gas chromatography-mass spectrometry. Nucleic Acids Res. 2001, 29:E12.
33. Levine R.L., Garland D., Oliver C.N., Amici A., Climent I., Lenz A.G., et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990, 186:464-478.
34. Rice-Evans C.A., Diplock A.T., Symons M.C.R. Techniques in free radicals research. Laboratory Techniques in Biochemistry and Molecular Biology 1991, Elsevier, Amsterdam. R.H. Burdon, P.H. van Knippenberg (Eds.).
35. Eissa S., Seada L.S. Quantitation of bcl-2 protein in bladder cancer tissue by enzyme immunoassay: comparison with Western blot and immunohistochemistry. Clin. Chem. 1998, 44:1423-1429.
36. Katiyar S.K., Matsui M.S., Mukhtar H. Kinetics of UV light-induced cyclobutane pyrimidine dimers in human skin in vivo: an immunohistochemical analysis of both epidermis and dermis. Photochem. Photobiol. 2000, 72:788-793.
37. Herrling T., Jung K., Fuchs J. Measurements of UV-generated free radicals/reactive oxygen species (ROS) in skin. Spectrochim. Acta A 2006, 63:840-845.
38. Deliconstantinos G., Villiotou V., Stavrides J.C. Alterations of nitric oxide synthase and xanthine oxidase activities of human keratinocytes by ultraviolet B radiation: potential role for peroxynitrite in skin inflammation. Biochem. Pharmacol. 1996, 51:1727-1738.
39. Hsieh R.J., Kinsella J.E. Oxidation of polyunsaturated fatty acids: mechanisms, products, and inhibition with emphasis on fish. Adv. Food Nutr. Res. 1989, 33:233-341.
40. Lawrence R.A. Reprint of glutathione peroxidase activity in selenium-deficient rat liver. Biochem. Biophys. Res. Commun. 2012, 425:503-509.
41. Esterbauer H., Schaur R.J., Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radical Biol. Med. 1991, 11:81-128.
42. Grimsrud P.A., Xie H., Griffin T.J., Bernlohr D.A. Oxidative stress and covalent modification of protein with bioactive aldehydes. J. Biol. Chem. 2008, 283:21837-21841.
43. Vistoli G., De Maddis D., Cipak A., Zarkovic N., Carini M., Aldini G. Advanced glycoxidation and lipoxidation end products (AGEs and ALEs): an overview of their mechanisms of formation. Free Radical Res. 2013, 47:3-27.
44. Shulaev V., Oliver D.J. Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol. 2006, 141:367-372.
45. Briganti S., Picardo M. Antioxidant activity, lipid peroxidation and skin diseases. What's new. J. Eur. Acad. Dermatol. Venereol. 2003, 17:663-669.
46. Lee Y., Shin D.H., Kim J.H., Hong S., Choi D., Kim Y.J., et al. Caffeic acid phenethyl ester-mediated Nrf2 activation and IκB kinase inhibition are involved in NFκB inhibitory effect: structural analysis for NFκB inhibition. Eur. J. Pharmacol. 2010, 643:21-28.
47. Braun S., Hanselmann C., Gassmann M.G., auf dem Keller U., Born-Berclaz C., Chan K., et al. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol. Cell. Biol. 2002, 22:5492-5505.
48. Zhao R., Hou Y., Xue P., Woods C.G., Fu J., Feng B., et al. Long isoforms of NRF1 contribute to arsenic-induced antioxidant response in human keratinocytes. Environ. Health Perspect. 2010, 119:56-62.
49. Mera K., Kawahara K.I., Tada K.I., Kawai K., Hashiguchi T., Maruyama I., et al. ER signaling is activated to protect human HaCaT keratinocytes from ER stress induced by environmental doses of UVB. Biochem. Biophys. Res. Commun. 2010, 397:350-354.
50. Novotny V., Prieschl E.E., Csonga R., Fabjani G., Baumruker T. Nrf1 in a complex with fosB, c-jun, junD and ATF2 forms the AP1 component at the TNFα promoter in stimulated mast cells. Nucleic Acids Res. 1998, 26:5480-5485.
51. Yang H., Magilnick N., Lee C., Kalmaz D., Ou X., Chan J.Y., et al. Nrf1 and Nrf2 regulate rat glutamate-cysteine ligase catalytic subunit transcription indirectly via NF-κB and AP-1. Mol. Cell. Biol. 2005, 25:5933-5946.
52. Konstantinopoulos P.A., Spentzos D., Fountzilas E., Francoeur N., Sanisetty S., Grammatikos A.P., et al. Keap1 mutations and Nrf2 pathway activation in epithelial ovarian cancer. Cancer Res. 2011, 71:5081-5089.
53. Huang Y., Li W., Kong A.N. Anti-oxidative stress regulator NF-E2-related factor 2 mediates the adaptive induction of antioxidant and detoxifying enzymes by lipid peroxidation metabolite 4-hydroxynonenal. Cell Biosci. 2012, 2:40-47.
54. Buelna-Chontal M., Zazueta C. Redox activation of Nrf2 & NF-κB: A double end sword?. Cell. Signal. 2013, 25:2548-2557.
55. Rushworth S.A., Zaitseva L., Murray M.Y., Shah N.M., Bowles K.M., MacEwan D.J. The high Nrf2 expression in human acute myeloid leukemia is driven by NF-κB and underlies its chemo-resistance. Blood 2012, 120:5188-5198.
56. Azzolina A., Bongiovanni A., Lampiasi N. Substance P induces TNF-α and IL-6 production through NFκB in peritoneal mast cells. Biochim. Biophys. Acta 2003, 1643:75-83.
57. Lau W.K.W., Chan S.C.H., Law A.C.K., Ip M.S.M., Mak J.C.W. The Role of MAPK and Nrf2 pathways in ketanserin-elicited attenuation of cigarette smoke-induced IL-8 production in human bronchial epithelial cells. Toxicol. Sci. 2012, 125:569-577.
58. Gómez R., Conde J., Scotece M., López V., Lago F., Reino G., et al. Endogenous cannabinoid anandamide impairs cell growth and induces apoptosis in chondrocytes. J. Orthop. Res. 2014, 32:1137-1146.
59. Zheng R., Heck D.E., Mishin V., Black A.T., Shakarjian M.P., Kong A.N.T., et al. Modulation of keratinocyte expression of antioxidants by 4-hydroxynonenal, a lipid peroxidation end product. Toxicol. Appl. Pharmacol. 2014, 275:113-121.
60. Sancho R., Calzado M.A., Di Marzo V., Appendino G., Muñoz E. Anandamide inhibits nuclear factor-κB activation through a cannabinoid receptor-independent pathway. Mol. Pharmacol. 2003, 63:429-438.
61. Okada S., Muto A., Ogawa E., Nakanome A., Katoh Y., Ikawa S., et al. Bach1-dependent and-independent regulation of heme oxygenase-1 in keratinocytes. J. Biol. Chem. 2010, 285:23581-23589.
62. Guo R., Chen J., Zhu F., Biswas A.K., Berton T.R., Mitchell D.L., et al. E2F1 localizes to sites of UV-induced DNA damage to enhance nucleotide excision repair. J. Biol. Chem. 2010, 285:19308-19315.
63. Wakabayashi N., Slocum S.L., Skoko J.J., Shin S., Kensler T.W. When NRF2 talks, who'gs listening?. Antioxid. Redox Signal. 2010, 13:1649-1663.
64. Barrera G., Pizzimenti S., Laurora S., Briatore F., Toaldo C., Dianzani M.U. 4-Hydroxynonenal and cell cycle. Biofactors 2005, 24:151-157.
65. Bode A.M., Dong Z. Post-translational modification of p53 in tumorigenesis. Nat. Rev. Cancer 2004, 4:793-805.
66. Guéraud F., Atalay M., Bresgen N., Cipak A., Eckl P.M., Huc L., et al. Chemistry and biochemistry of lipid peroxidation products. Free Radical Res. 2010, 44:1098-1124.
67. Pappa A., Chen C., Koutalos Y., Townsend A.J., Vasiliou V. Aldh3a1 protects human corneal epithelial cells from ultraviolet-and 4-hydroxy-2-nonenal-induced oxidative damage. Free Radical Biol. Med. 2003, 34:1178-1189.
68. Poli G., Leonarduzzi G., Biasi F., Chiarpotto E. Oxidative stress and cell signalling. Curr. Med. Chem. 2004, 11:1163-1182.
69. Kutuk O., Arisan E.D., Tezil T., Shoshan M.C., Basaga H. Cisplatin overcomes Bcl-2-mediated resistance to apoptosis via preferential engagement of Bak: critical role of Noxa-mediated lipid peroxidation. Carcinogenesis 2009, 30:1517-1527.