Docosahexaenoic acid reverts resistance to UV-induced apoptosis in human keratinocytes: Involvement of COX-2 and HuR

Journal of Nutritional Biochemistry

Volumn 22, Issue 9, 2011, Pages 874-885

  Serini, Simona ^a   Donato, Valentina ^b   Piccioni, Elisabetta ^a   Trombino, Sonia ^b   Monego, Giovanni ^c   Toesca, Amelia ^c   Innocenti, Idanna ^b   Missori, Mauro ^d   De Spirito, Marco ^c   Celleno, Leonardo ^c   Fasano, Elena ^a   Ranelletti, Franco O ^c   Calviello, Gabriella ^a  

^a CATHOLIC UNIVERSITY   (Italy)

^b UNIVERSITY OF CALABRIA   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d ISC CNR   (Italy)

Author keywords

Apoptosis; COX 2; DHA; HuR; Keratinocytes; UVR

Indexed keywords

CASPASE 3; CYCLOOXYGENASE 2; CYCLOOXYGENASE 2 INHIBITOR; DOCOSAHEXAENOIC ACID; HUR PROTEIN; MESSENGER RNA; OMEGA 3 FATTY ACID; PROTEIN BAX; PROTEIN BCL 2; SMALL INTERFERING RNA;

ANTIGEN EXPRESSION; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; KERATINOCYTE; LONG TERM EXPOSURE; RADIATION EXPOSURE; SKIN CANCER; SKIN CARCINOGENESIS; ULTRAVIOLET RADIATION;

APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CELLS, CULTURED; CYCLOOXYGENASE 2; DOCOSAHEXAENOIC ACIDS; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; KERATINOCYTES; RNA, MESSENGER; TRANSFECTION; ULTRAVIOLET RAYS;

EID: 80051474683     PISSN: 09552863     EISSN: 18734847     Source Type: Journal    
DOI: 10.1016/j.jnutbio.2010.08.004     Document Type: Article

References (83)

1. Kwa R.E., Campana K., Moy R.L. Biology of cutaneous squamous cell carcinoma. J Am Acad Dermatol 1992, 26:1-26.
2. Madan V., Lear J.T., Szeimies R.M. Non-melanoma skin cancer. Lancet 2010, 375:673-685.
3. Molho-Pessach V., Lotem M. Ultraviolet radiation and cutaneous carcinogenesis. Curr Probl Dermatol 2007, 35:14-27.
4. Raj D., Brash D.E., Grossman D. Keratinocyte apoptosis in epidermal development and disease. J Invest Dermatol 2006, 126:243-257.
5. Erb P., Ji J., Kump E., Mielgo A., Wernli M. Apoptosis and pathogenesis of melanoma and nonmelanoma skin cancer. Adv Exp Med Biol 2008, 624:283-295.
6. Fischer S.M., Pavone A., Mikulec C., Langenbach R., Rundhaug J.E. Cyclooxygenase-2 expression is critical for chronic UV-induced murine skin carcinogenesis. Mol Carcinog 2007, 46:363-371.
7. Dempke W., Rie C., Grothey A., Schmoll H.J. Cyclooxygenase-2: a novel target for cancer chemotherapy?. J Cancer Res Clin Oncol 2001, 127:411-417.
8. Buckman S.Y., Gresham A., Hale P., Hruza G., Anast J., Masferrer J., et al. COX-2 expression is induced by UVB exposure in human skin: implications for the development of skin cancer. Carcinogenesis 1998, 19:723-729.
9. An K.P., Athar M., Tang X., Katiyar S.K., Russo J., Beech J., et al. Cyclooxygenase-2 expression in murine and human nonmelanoma skin cancers: implications for therapeutic approaches. Photochem Photobiol 2002, 76:73-80.
10. Trifan O.C., Hla T. Cyclooxygenase-2 modulates cellular growth and promotes tumorigenesis. J Cell Mol Med 2003, 7:207-222.
11. Akunda J.K., Chun K.S., Sessoms A.R., Lao H.C., Fischer S.M., Langenbach R. Cyclooxygenase-2 deficiency increases epidermal apoptosis and impairs recovery following acute UVB exposure. Mol Carcinog 2007, 46:354-362.
12. Tong X., Van Dross R.T., Abu-Yousif A., Morrison A.R., Pelling J.C. Apigenin prevents UVB-induced cyclooxygenase 2 expression: coupled mRNA stabilization and translational inhibition. Mol Cell Biol 2007, 27:283-296.
13. Sengupta S., Jang B.C., Wu M.T., Paik J.H., Furneaux H., Hla T. The RNA-binding protein HuR regulates the expression of cyclooxygenase-2. J Biol Chem 2003, 278:25227-25233.
14. Calviello G., Di Nicuolo F., Gragnoli S., Piccioni E., Serini S., Maggiano N., et al. n-3 PUFAs reduce VEGF expression in human colon cancer cells modulating the COX-2/PGE2 induced ERK-1 and -2 and HIF-1alpha induction pathway. Carcinogenesis 2004, 25:2303-2310.
15. Calviello G., Resci F., Serini S., Piccioni E., Toesca A., Boninsegna A., et al. Docosahexaenoic acid induces proteasome-dependent degradation of beta-catenin, down-regulation of survivin and apoptosis in human colorectal cancer cells not expressing COX-2. Carcinogenesis 2007, 28:1202-1209.
16. Vecchini A., Ceccarelli V., Susta F., Caligiana P., Orvietani P., Binaglia L., et al. Dietary alpha-linolenic acid reduces COX-2 expression and induces apoptosis of hepatoma cells. J Lipid Res 2004, 45:308-316.
17. Narayanan N.K., Narayanan B.A., Reddy B.S. A combination of docosahexaenoic acid and celecoxib prevents prostate cancer cell growth in vitro and is associated with modulation of nuclear factor-kappaB, and steroid hormone receptors. Int J Oncol 2005, 26:785-792.
18. Lim K., Han C., Dai Y., Shen M., Wu T. Omega-3 polyunsaturated fatty acids inhibit hepatocellular carcinoma cell growth through blocking beta-catenin and cyclooxygenase-2. Mol Cancer Ther 2009, 8:3046-3055.
19. Calviello G., Serini S., Piccioni E. n-3 polyunsaturated fatty acids and the prevention of colorectal cancer: molecular mechanisms involved. Curr Med Chem. 2007, 14:3059-3069.
20. Edwards I.J., O'Flaherty J.T. Omega-3 fatty acids and PPARgamma in cancer. PPAR Res 2008, 358052:2008.
21. Siddiqui R.A., Shaikh S.R., Sech L.A., Yount H.R., Stillwell W., Zaloga G.P. Omega 3-fatty acids: health benefits and cellular mechanisms of action. Mini Rev Med Chem 2004, 4:859-871.
22. Hardman W.E. Omega-3 fatty acids to augment cancer therapy. J Nutr. 2002, 132:3508S-3512S.
23. Calviello G., Serini S., Piccioni E., Celleno L. Beneficial effects of n-3 PUFAs on UV-induced skin damage and tumorigenesis. Fish Oils and Health 2008, 141-158. E.P. Heikkinen (Ed.).
24. Rhodes L.E., Shahbakhti H., Azurdia R.M., Moison R.M., Steenwinkel M.J., Homburg M.I., et al. Effect of eicosapentaenoic acid, an omega-3 polyunsaturated fatty acid, on UVR-related cancer risk in humans. An assessment of early genotoxic markers. Carcinogenesis 2003, 24:919-925.
25. Ramesh G., Das U.N. Effect of free fatty acids on two-stage skin carcinogenesis in mice. Cancer Lett 1996, 100:199-209.
26. Godar D.E. UV doses worldwide. Photochem Photobiol 2005, 81:736-749.
27. Hill L.L., Ouhtit A., Loughlin S.M., Kripke M.L., Ananthaswamy H.N., Owen-Schaub L.B. Fas ligand: a sensor for DNA damage critical in skin cancer etiology. Science 1999, 285:898-900.
28. Murphy G., Young A.R., Wulf H.C., Kulms D., Schwarz T. The molecular determinants of sunburn cell formation. Exp Dermatol 2001, 10:155-160.
29. Serini S., Piccioni E., Merendino N., Calviello G. Dietary polyunsaturated fatty acids as inducers of apoptosis: implications for cancer. Apoptosis 2009, 14:135-152.
30. Kang K.S., Wang P., Yamabe N., Fukui M., Jay T., Zhu B.T. Docosahexaenoic acid induces apoptosis in MCF-7 cells in vitro and in vivo via reactive oxygen species formation and caspase 8 activation. PLoS One 2010, e10296:5.
31. Kato T., Kolenic N., Pardini R.S. Docosahexaenoic acid (DHA), a primary tumor suppressive omega-3 fatty acid, inhibits growth of colorectal cancer independent of p53 mutational status. Nutr. Cancer 2007, 58:178-187.
32. Hossain Z., Hosokawa M., Takahashi K. Growth inhibition and induction of apoptosis of colon cancer cell lines by applying marine phospholipid. Nutr Cancer 2009, 61:123-130.
33. Calviello G., Palozza P., Piccioni E., Maggiano N., Frattucci A., Franceschelli P., et al. Dietary supplementation with eicosapentaenoic and docosahexaenoic acid inhibits growth of Morris hepatocarcinoma 3924A in rats: effects on proliferation and apoptosis. Int J Cancer 1998, 75:699-705.
34. Lim K., Han C., Xu L., Isse K., Demetris A.J., Wu T. Cyclooxygenase-2-derived prostaglandin E2 activates beta-catenin in human cholangiocarcinoma cells: evidence for inhibition of these signaling pathways by omega 3 polyunsaturated fatty acids. Cancer Res 2008, 68:553-560.
35. Zhang J., Bowden G.T. UVB irradiation regulates Cox-2 mRNA stability through AMPK and HuR in human keratinocytes. Mol Carcinog 2008, 47:974-983.
36. Nishigori C. Cellular aspects of photocarcinogenesis. Photochem Photobiol Sci 2006, 5:208-214.
37. Gorman A., McCarthy J., Finucane D., Reville W., Cotter T.G. Techniques in apoptosis 1996, 7-9. Portland Press Ltd., London. T.G. Cotter, S.J. Martin (Eds.).
38. Ueno T., Toi M., Linder S. Detection of epithelial cell death in the body by cytokeratin 18 measurement. Biomed Pharmacother 2005, 59:S359-362.
39. Calviello G., Di Nicuolo F., Piccioni E., Marcocci M.E., Serini S., Maggiano N., et al. γ-Tocopheryl quinone induces apoptosis in cancer cells via caspase-9 activation and cytochrome c release. Carcinogenesis 2003, 24:427-433.
40. Serini S., Trombino S., Oliva F., Piccioni E., Monego G., Resci F., et al. Docosahexaenoic acid induces apoptosis in lung cancer cells by increasing MKP-1 and down-regulating p-ERK1/2 and p-p38 expression. Apoptosis 2008, 13:1172-1183.
41. 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.
42. Ranelletti F.O., Almadori G., Rocca B., Ferrandina G., Ciabattoni G., Habib A., et al. Prognostic significance of cyclooxygenase-2 in laryngeal squamous cell carcinoma. Int J Cancer. (Pred Oncol) 2001, 95:343-349.
43. Martin S.A., Ouchi T. BRCA1 phosphorylation regulates caspase-3 activation in UV-induced apoptosis. Cancer Res 2005, 65:10657-10662.
44. El-Mahdy M.A., Zhu Q., Wang Q.E., Wani G., Patnaik S., Zhao Q., et al. Naringenin protects HaCaT human keratinocytes against UVB-induced apoptosis and enhances the removal of cyclobutane pyrimidine dimers from the genome. Photochem Photobiol 2008, 84:307-316.
45. Abd Elmageed Z.Y., Gaur R.L., Williams M., Abdraboh M.E., Rao P.N., Raj M.H., et al. Characterization of coordinated immediate responses by p16INK4A and p53 pathways in UVB-irradiated human skin cells. J Invest Dermatol 2009, 129:175-183.
46. Burlando B., Parodi A., Volante A., Bassi A.M. Comparison of the irritation potentials of Boswellia serrata gum resin and of acetyl-11-keto-β-boswellic acid by in vitro cytotoxicity tests on human skin-derived cell lines. Toxicol Lett 2008, 177:144-149.
47. Moll R., Divo M., Langbein L. The human keratins: biology and pathology. Histochem Cell Biol 2008, 129:705-733.
48. Guzman E., Langowski J.L., Owen-Schaub L. Mad dogs, Englishmen and apoptosis: the role of cell death in UV-induced skin cancer. Apoptosis 2003, 8:315-325.
49. Smith M.L., Chen I.T., Zhan Q., O'Connor P.M., Fornace A.J. Involvement of the p53 tumor suppressor in repair of u.v.-type DNA damage. Oncogene 1995, 10:1053-1059.
50. Mund R.C., Pizato N., Bonatto S., Nunes E.A., Vicenzi T., Tanhoffer R., et al. Decreased tumor growth in Walker 256 tumor-bearing rats chronically supplemented with fish oil involves COX-2 and PGE2 reduction associated with apoptosis and increased peroxidation. Prostaglandins Leukot Essent Fatty Acids 2007, 76:113-120.
51. Chêne G., Dubourdeau M., Balard P., Escoubet-Lozach L., Orfila C., Berry A., et al. n-3 and n-6 polyunsaturated fatty acids induce the expression of COX-2 via PPARgamma activation in human keratinocyte HaCaT cells. Biochim Biophys Acta 2007, 1771:576-589.
52. Dixon D.A., Tolley N.D., King P.H., Nabors L.B., McIntyre T.M., Zimmerman G.A., et al. Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J Clin Invest 2001, 108:1657-1665.
53. Do S.I., Do I.G., Kim G.Y., Lee S., Kim Y.W., Park Y.K., et al. Correlation between cyclooxygenase-2 expression and HuR cytoplasmic translocation of breast cancer. Korean J Pathol 2008, 42:75-80.
54. Mrena J., Wiksten J.P., Thiel A., Kokkola A., Pohjola L., Lundin J., et al. Cyclooxygenase-2 is an independent prognostic factor in gastric cancer and its expression is regulated by the messenger RNA stability factor HuR. Clin Cancer Res 2005, 11:7362-7368.
55. Denkert C., Weichert W., Pest S., Koch I., Licht D., Köbel M., et al. Overexpression of the embryonic-lethal abnormal vision-like protein HuR in ovarian carcinoma is a prognostic factor and is associated with increased cyclooxygenase 2 expression. Cancer Res 2004, 64:189-195.
56. Lim S.J., Kim H.J., Kim J.Y., Park K., Lee C.M. Expression of HuR is associated with increased cyclooxygenase-2 expression in uterine cervical carcinoma. Int J Gynecol Pathol 2007, 26:229-234.
57. He Y.Y., Pi J., Huang J.L., Diwan B.A., Waalkes M.P., Chignell C.F. Chronic UVA irradiation of human HaCaT keratinocytes induces malignant transformation associated with acquired apoptotic resistance. Oncogene 2006, 25:3680-3688.
58. Chaturvedi V., Qin J.Z., Denning M.F., Choubey D., Diaz M.O., Nickoloff B.J. Apoptosis in proliferating, senescent, and immortalized keratinocytes. J Biol Chem 1999, 274:23358-23367.
59. Leccia M.T., Richard M.J., Joanny-Crisci F., Beani J.C. UV-A1 cytotoxicity and antioxidant defence in keratinocytes and fibroblasts. Eur J Dermatol 1998, 8:478-482.
60. Eberhart C.E., Coffey R.J., Radhika F.M., Giardello S., Ferenbach S., DuBois R.N. Up-regulation of cyclooxygenase-2 gene expression in human colorectal adenomas and adenocarcinomas. Gastroenterol 1996, 107:1183-1188.
61. Hida T., Yatabe Y., Achiwa H., Muramatsu H., Kozaki K., Nakamura S., et al. Increased expression of cyclooxygenase-2 occurs frequently in human lung cancers, specifically in adenocarcinomas. Cancer Res 1998, 58:3761-3764.
62. Bernard M.P., Bancos S., Sime P.J., Phipps R.P. Targeting cyclooxygenase-2 in hematological malignancies: rationale and promise. Curr Pharm Des 2008, 14:2051-2060.
63. Rundhaug J.E., Fischer S.M. Cyclo-oxygenase-2 plays a critical role in UV-induced skin carcinogenesis. Photochem Photobiol 2008, 84:322-329.
64. Rodust P.M., Stockfleth E., Ulrich C., Leverkus M., Eberle J. UV-induced squamous cell carcinoma-a role for antiapoptotic signalling pathways. Br J Dermatol 2009, 161:107-115.
65. Liao Z., Mason K.A., Milas L. Cyclo-oxygenase-2 and its inhibition in cancer: is there a role?. Drugs 2007, 67:821-845.
66. de Groot D.J., de Vries E.G., Groen H.J., de Jong S. Non-steroidal anti-inflammatory drugs to potentiate chemotherapy effects: from lab to clinic. Crit Rev Oncol Hematol 2007, 61:52-69.
67. Reddy B.S., Rao C.V., Seibert K. Evaluation of cyclooxygenase-2 inhibitor for potential chemopreventive properties in colon carcinogenesis. Cancer Res 1996, 56:4566-4569.
68. Oshima M., Dinchuk J.E., Kargman S.L. Suppression of intestinal polyposis in Apc716 knockout mice by inhibition of cyclooxygenase-2 (COX-2). Cell 1996, 87:803-809.
69. Kawamori T., Rao C.V., Seibert K., Reddy B.S. Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor against colon carcinogenesis. Cancer Res 1998, 58:409-412.
70. Marks F., Fürstenberger G. Cancer prevention through interruption on of multistage carcinogenesis: the lessons learnt by comparing mouse skin carcinogenesis and human large bowel cancer. Eur J Cancer 2000, 36:314-329.
71. Muüller-Decker K., Kopp-Schneider A., Marks F., Seibert K., Fürstenberger G. Localization of prostaglandin synthase isozymes in murine epidermal tumors: suppression of skin tumor promotion by inhibition of prostaglandin H synthase-2. Mol Carcinog 1998, 23:36-44.
72. Pentland A.P. Epidermal COX-2 induction following ultraviolet irradiation: suggested mechanism for the role of COX-2 inhibition in photoprotection. J Invest Dermatol 2003, 121:853-861.
73. Tsujii M., DuBois R.N. Alterations in cellular adhesion and apoptosis in epithelial cells overexpressing prostaglandin endoperoxide synthase 2. Cell 1995, 83:493-501.
74. Seed M.P., Freemantle C.N., Alam C.A., et al. Apoptosis induction and inhibition of colon-26 tumour growth and angiogenesis: findings on COX-1 and COX-2 inhibitors in vitro & in vivo and topical diclofenac in hyaluronan. Adv Exp Med Biol 1997, 433:339-342.
75. Ding X.Z., Tong W.G., Adrian T.E. Blockade of cyclooxygenase-2 inhibits proliferation and induces apoptosis in human pancreatic cancer cells. Anticancer Res 2000, 20:2625-2631.
76. Orengo I.F., Gerguis J., Phillips R., Guevara A., Lewis A.T., Black H.S. Celecoxib, a cyclooxygenase 2 inhibitor as a potential chemopreventive to UV-induced skin cancer: a study in the hairless mouse model. Arch Dermatol 2002, 138:751-755.
77. Moore D.E. Drug-induced cutaneous photosensitivity: incidence, mechanism, prevention and management. Drug Saf 2002, 25:345-372.
78. Abdel-Tawab M., Zettl H., Schubert-Zsilavecz M. Nonsteroidal anti-inflammatory drugs: a critical review on current concepts applied to reduce gastrointestinal toxicity. Curr Med Chem 2009, 16:2042-2063.
79. Peng S., Duggan A. Gastrointestinal adverse effects of non-steroidal anti-inflammatory drugs. Expert Opin Drug Saf 2005, 4:157-169.
80. Black H.S., Thornby J.I., Gerguis J., Lenger W. Influence of dietary omega-6, -3 fatty acid sources on the initiation and promotion stages of photocarcinogenesis. Photochem Photobiol 1992, 56:195-199.
81. Black H.S., Lenger W.A., Gerguis J., Thornby J.I. Relation of antioxidants and level of dietary lipid to epidermal lipid peroxidation and ultraviolet carcinogenesis. Cancer Res 1985, 45:6254-6259.
82. Hakim I.A., Harris R.B., Ritenbaugh C. Fat intake and risk of squamous cell carcinoma of the skin. Nutr Cancer 2000, 36:155-162.
83. Danno K., Ikai K., Imamura S. Anti-inflammatory effects of eicosapentaenoic acid on experimental skin inflammation models. Arch Dermatol Res 1993, 285:432-435.