Docosahexaenoic acid inhibits UVB-induced activation of NF-κB and expression of COX-2 and NOX-4 in HR-1 hairless mouse skin by blocking MSK1 signaling

PLoS ONE

Volumn 6, Issue 11, 2011, Pages

  Rahman, Md Mostafizur ^a   Kundu, Joydeb Kumar ^a   Shin, Jun Wan ^a   Na, Hye Kyung ^b   Surh, Young Joon ^a,c  

^a Seoul National University   (South Korea)

^b Sungsin Women's University   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACID; I KAPPA B KINASE ALPHA; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROTEIN P50; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; STRESS ACTIVATED PROTEIN KINASE 1; SYNAPTOTAGMIN I;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; FEMALE; IN VIVO STUDY; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHARMACOLOGICAL BLOCKING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; SKIN INFLAMMATION; SKIN PROTECTION; ULTRAVIOLET B RADIATION;

ADMINISTRATION, TOPICAL; ANIMALS; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACIDS; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; MAP KINASE SIGNALING SYSTEM; MICE; MICE, HAIRLESS; NADPH OXIDASE; NF-KAPPA B; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RIBOSOMAL PROTEIN S6 KINASES, 90-KDA; SKIN; ULTRAVIOLET RAYS;

EID: 82155164210     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0028065     Document Type: Article

References (58)

1. de Gruijl FR, (2002) Photocarcinogenesis: UVA vs. UVB radiation. Skin Pharmacol Appl Skin Physiol 15: 316-320.
2. Halliday GM, (2005) Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat Res 571: 107-120.
3. Jiang F, Zhang Y, Dusting GJ, (2011) NADPH oxidase-mediated redox signaling: roles in cellular stress response, stress tolerance, and tissue repair. Pharmacol Rev 63: 218-242.
4. Shono T, Yokoyama N, Uesaka T, Kuroda J, Takeya R, et al. (2008) Enhanced expression of NADPH oxidase Nox4 in human gliomas and its roles in cell proliferation and survival. Int J Cancer 123: 787-792.
5. Wang R, Dashwood WM, Nian H, Lohr CV, Fischer KA, et al. (2011) NADPH oxidase overexpression in human colon cancers and rat colon tumors induced by 2-amino-1-methyl-6-phenylimidazo[4,5-b]pyridine (PhIP). Int J Cancer 128: 2581-2590.
6. Graham KA, Kulawiec M, Owens KM, Li X, Desouki MM, et al. (2010) NADPH oxidase 4 is an oncoprotein localized to mitochondria. Cancer Biol Ther 10: 223-231.
7. Tobar N, Guerrero J, Smith PC, Martinez J, (2010) NOX4-dependent ROS production by stromal mammary cells modulates epithelial MCF-7 cell migration. Br J Cancer 103: 1040-1047.
8. Yamaura M, Mitsushita J, Furuta S, Kiniwa Y, Ashida A, et al. (2009) NADPH oxidase 4 contributes to transformation phenotype of melanoma cells by regulating G2-M cell cycle progression. Cancer Res 69: 2647-2654.
9. Beak SM, Lee YS, Kim JA, (2004) NADPH oxidase and cyclooxygenase mediate the ultraviolet B-induced generation of reactive oxygen species and activation of nuclear factor-κB in HaCaT human keratinocytes. Biochimie 86: 425-429.
10. Kundu JK, Surh YJ, (2008) Inflammation: gearing the journey to cancer. Mutat Res 659: 15-30.
11. An KP, Athar M, Tang X, Katiyar SK, Russo J, et al. (2002) Cyclooxygenase-2 expression in murine and human nonmelanoma skin cancers: implications for therapeutic approaches. Photochem Photobiol 76: 73-80.
12. Muller-Decker K, Neufang G, Berger I, Neumann M, Marks F, et al. (2002) Transgenic cyclooxygenase-2 overexpression sensitizes mouse skin for carcinogenesis. Proc Natl Acad Sci U S A 99: 12483-12488.
13. Tiano HF, Loftin CD, Akunda J, Lee CA, Spalding J, et al. (2002) Deficiency of either cyclooxygenase (COX)-1 or COX-2 alters epidermal differentiation and reduces mouse skin tumorigenesis. Cancer Res 62: 3395-3401.
14. Pentland AP, Schoggins JW, Scott GA, Khan KN, Han R, (1999) Reduction of UV-induced skin tumors in hairless mice by selective COX-2 inhibition. Carcinogenesis 20: 1939-1944.
15. Bachelor MA, Cooper SJ, Sikorski ET, Bowden GT, (2005) Inhibition of p38 mitogen-activated protein kinase and phosphatidylinositol 3-kinase decreases UVB-induced activator protein-1 and cyclooxygenase-2 in a SKH-1 hairless mouse model. Mol Cancer Res 3: 90-99.
16. Dickinson SE, Olson ER, Zhang J, Cooper SJ, Melton T, et al. (2011) p38 MAP kinase plays a functional role in UVB-induced mouse skin carcinogenesis. Mol Carcinog 50: 469-478.
17. Kim AL, Labasi JM, Zhu Y, Tang X, McClure K, et al. (2005) Role of p38 MAPK in UVB-induced inflammatory responses in the skin of SKH-1 hairless mice. J Invest Dermatol 124: 1318-1325.
18. Kim JK, Kim Y, Na KM, Surh Y-J, Kim TY, (2007) [6]-Gingerol prevents UVB-induced ROS production and COX-2 expression in vitro and in vivo. Free Radic Res 41: 603-614.
19. Chang EJ, Kundu JK, Liu L, Shin JW, Surh Y-J, (2011) Ultraviolet B radiation activates NF-κB and induces iNOS expression in HR-1 hairless mouse skin: role of IκB kinase-beta. Mol Carcinog 50: 310-317.
20. Chun KS, Surh YJ, (2004) Signal transduction pathways regulating cyclooxygenase-2 expression: potential molecular targets for chemoprevention. Biochem Pharmacol 68: 1089-1100.
21. Park S, Ahn JY, Lim MJ, Kim MH, Yun YS, et al. (2010) Sustained expression of NADPH oxidase 4 by p38 MAPK-Akt signaling potentiates radiation-induced differentiation of lung fibroblasts. J Mol Med (Berl) 88: 807-816.
22. Manea A, Tanase LI, Raicu M, Simionescu M, (2010) Transcriptional regulation of NAD(P)H oxidase isoforms, Nox1 and Nox4, by nuclear factor-kappaB in human aortic smooth muscle cells. Biochem Biophys Res Commun 396: 901-907.
23. Kefaloyianni E, Gaitanaki C, Beis I, (2006) ERK1/2 and p38-MAPK signalling pathways, through MSK1, are involved in NF-κB transactivation during oxidative stress in skeletal myoblasts. Cell Signal 18: 2238-2251.
24. Murakami A, Ohigashi H, (2007) Targeting NOX, INOS and COX-2 in inflammatory cells: chemoprevention using food phytochemicals. Int J Cancer 121: 2357-2363.
25. Jho DH, Cole SM, Lee EM, Espat NJ, (2004) Role of omega-3 fatty acid supplementation in inflammation and malignancy. Integr Cancer Ther 3: 98-111.
26. Kundu JK, Choi KS, Fujii H, Sun BX, Surh Y-J, (2009) Oligonol, a lychee fruit-derived low molecular weight polyphenol formulation, inhibits UVB-induced cyclooxygenase-2 expression, and induces NAD(P)H:quinone oxidoreductase-1 expression in hairless mouse skin. Journal of Functional Foods 1: 98-108.
27. Vila-del Sol V, Fresno M, (2005) Involvement of TNF and NF-κB in the transcriptional control of cyclooxygenase-2 expression by IFN-gamma in macrophages. J Immunol 174: 2825-2833.
28. Otkjaer K, Kragballe K, Johansen C, Funding AT, Just H, et al. (2007) IL-20 gene expression is induced by IL-1beta through mitogen-activated protein kinase and NF-κB-dependent mechanisms. J Invest Dermatol 127: 1326-1336.
29. Vermeulen L, De Wilde G, Van Damme P, Vanden Berghe W, Haegeman G, (2003) Transcriptional activation of the NF-κB p65 subunit by mitogen- and stress-activated protein kinase-1 (MSK1). EMBO J 22: 1313-1324.
30. Lewis DA, Spandau DF, (2008) UVB-induced activation of NF-κB is regulated by the IGF-1R and dependent on p38 MAPK. J Invest Dermatol 128: 1022-1029.
31. Sharma SD, Meeran SM, Katiyar SK, (2007) Dietary grape seed proanthocyanidins inhibit UVB-induced oxidative stress and activation of mitogen-activated protein kinases and nuclear factor-kappaB signaling in in vivo SKH-1 hairless mice. Mol Cancer Ther 6: 995-1005.
32. Kaur G, Cameron-Smith D, Garg M, Sinclair AJ, (2011) Docosapentaenoic acid (22:5n-3): a review of its biological effects. Prog Lipid Res 50: 28-34.
33. Nauseef WM, (2008) Biological roles for the NOX family NADPH oxidases. J Biol Chem 283: 16961-16965.
34. Surh Y-J, Kundu JK, (2005) Signal transduction network leading to COX-2 induction: a road map in search of cancer chemopreventives. Arch Pharm Res 28: 1-15.
35. Chamulitrat W, Stremmel W, Kawahara T, Rokutan K, Fujii H, et al. (2004) A constitutive NADPH oxidase-like system containing gp91phox homologs in human keratinocytes. J Invest Dermatol 122: 1000-1009.
36. Zhao Y, Chaiswing L, Bakthavatchalu V, Oberley TD, Clair DK St, (2006) Ras mutation promotes p53 activation and apoptosis of skin keratinocytes. Carcinogenesis 27: 1692-1698.
37. Diebold I, Petry A, Hess J, Gorlach A, (2010) The NADPH oxidase subunit NOX4 is a new target gene of the hypoxia-inducible factor-1. Mol Biol Cell 21: 2087-2096.
38. Djordjevic T, BelAiba RS, Bonello S, Pfeilschifter J, Hess J, et al. (2005) Human urotensin II is a novel activator of NAD(P)H oxidase in human pulmonary artery smooth muscle cells. Arterioscler Thromb Vasc Biol 25: 519-525.
39. Cucoranu I, Clempus R, Dikalova A, Phelan PJ, Ariyan S, et al. (2005) NAD(P)H oxidase 4 mediates transforming growth factor-beta1-induced differentiation of cardiac fibroblasts into myofibroblasts. Circ Res 97: 900-907.
40. Wingler K, Wunsch S, Kreutz R, Rothermund L, Paul M, et al. (2001) Upregulation of the vascular NAD(P)H-oxidase isoforms Nox1 and Nox4 by the renin-angiotensin system in vitro and in vivo. Free Radic Biol Med 31: 1456-1464.
41. Moe KT, Aulia S, Jiang F, Chua YL, Koh TH, et al. (2006) Differential upregulation of Nox homologues of NADPH oxidase by tumor necrosis factor-alpha in human aortic smooth muscle and embryonic kidney cells. J Cell Mol Med 10: 231-239.
42. Richard D, Wolf C, Barbe U, Kefi K, Bausero P, et al. (2009) Docosahexaenoic acid down-regulates endothelial Nox 4 through a sPLA2 signalling pathway. Biochem Biophys Res Commun 389: 516-522.
43. Serini S, Donato V, Piccioni E, Trombino S, Monego G, et al. (2010) Docosahexaenoic acid reverts resistance to UV-induced apoptosis in human keratinocytes: involvement of COX-2 and HuR. J Nutr Biochem.
44. An WS, Kim HJ, Cho KH, Vaziri ND, (2009) Omega-3 fatty acid supplementation attenuates oxidative stress, inflammation, and tubulointerstitial fibrosis in the remnant kidney. Am J Physiol Renal Physiol 297: F895-903.
45. Machida T, Hiramatsu M, Hamaue N, Minami M, Hirafuji M, (2005) Docosahexaenoic acid enhances cyclooxygenase-2 induction by facilitating p44/42, but not p38, mitogen-activated protein kinase activation in rat vascular smooth muscle cells. J Pharmacol Sci 99: 113-116.
46. Karin M, (1999) How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18: 6867-6874.
47. Wang TM, Chen CJ, Lee TS, Chao HY, Wu WH, et al. (2011) Docosahexaenoic acid attenuates VCAM-1 expression and NF-κB activation in TNF-alpha-treated human aortic endothelial cells. J Nutr Biochem 22: 187-194.
48. Mullen A, Loscher CE, Roche HM, (2010) Anti-inflammatory effects of EPA and DHA are dependent upon time and dose-response elements associated with LPS stimulation in THP-1-derived macrophages. J Nutr Biochem 21: 444-450.
49. Manea A, Tanase LI, Raicu M, Simionescu M, (2010) Jak/STAT signaling pathway regulates nox1 and nox4-based NADPH oxidase in human aortic smooth muscle cells. Arterioscler Thromb Vasc Biol 30: 105-112.
50. Lo HW, Cao X, Zhu H, Ali-Osman F, (2010) Cyclooxygenase-2 is a novel transcriptional target of the nuclear EGFR-STAT3 and EGFRvIII-STAT3 signaling axes. Mol Cancer Res 8: 232-245.
51. Lee CF, Qiao M, Schroder K, Zhao Q, Asmis R, (2010) Nox4 is a novel inducible source of reactive oxygen species in monocytes and macrophages and mediates oxidized low density lipoprotein-induced macrophage death. Circ Res 106: 1489-1497.
52. McCoy CE, Campbell DG, Deak M, Bloomberg GB, Arthur JS, (2005) MSK1 activity is controlled by multiple phosphorylation sites. Biochem J 387: 507-517.
53. Reber L, Vermeulen L, Haegeman G, Frossard N, (2009) Ser276 phosphorylation of NF-κB p65 by MSK1 controls SCF expression in inflammation. PLoS One 4: e4393.
54. Sedeek M, Callera G, Montezano A, Gutsol A, Heitz F, et al. (2010) Critical role of Nox4-based NADPH oxidase in glucose-induced oxidative stress in the kidney: implications in type 2 diabetic nephropathy. Am J Physiol Renal Physiol 299: F1348-1358.
55. Park HS, Jung HY, Park EY, Kim J, Lee WJ, et al. (2004) Cutting edge: direct interaction of TLR4 with NAD(P)H oxidase 4 isozyme is essential for lipopolysaccharide-induced production of reactive oxygen species and activation of NF-κB. J Immunol 173: 3589-3593.
56. Groeger AL, Cipollina C, Cole MP, Woodcock SR, Bonacci G, et al. (2010) Cyclooxygenase-2 generates anti-inflammatory mediators from omega-3 fatty acids. Nat Chem Biol 6: 433-441.
57. Sun YP, Oh SF, Uddin J, Yang R, Gotlinger K, et al. (2007) Resolvin D1 and its aspirin-triggered 17R epimer. Stereochemical assignments, anti-inflammatory properties, and enzymatic inactivation. J Biol Chem 282: 9323-9334.
58. Yan Y, Wang B, Zuo YG, Qu T, (2006) Inhibitory effects of mizolastine on ultraviolet B-induced leukotriene B4 production and 5-lipoxygenase expression in normal human dermal fibroblasts in vitro. Photochem Photobiol 82: 665-669.