Ligand activation of peroxisome proliferator-activated receptor-β/δ and inhibition of cyclooxygenase-2 enhances inhibition of skin tumorigenesis

Toxicological Sciences

Volumn 113, Issue 1, 2009, Pages 27-36

  Bility, Moses T ^a   Zhu, Bokai ^a   Kang, Boo H ^b   Gonzalez, Frank J ^c   Peters, Jeffrey M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Preclinical Research Center   (South Korea)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Cyclooxygenase 2; Differentiation; Nonsteroidal anti inflammatory drugs; Peroxisome proliferator activated receptor

Indexed keywords

7,12 DIMETHYLBENZ[A]ANTHRACENE; [4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY]ACETIC ACID; CYCLOOXYGENASE 2; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; KERATIN; MESSENGER RNA; NIMESULIDE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROSTAGLANDIN E2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINEOPLASTIC ACTIVITY; ARTICLE; BIOASSAY; CANCER CELL CULTURE; CARCINOGENESIS; CELL CYCLE G2 PHASE; CELL CYCLE M PHASE; CELL CYCLE PROGRESSION; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE MODEL; DRUG EFFICACY; DRUG POTENTIATION; ENZYME INHIBITION; EX VIVO STUDY; FEMALE; FLOW CYTOMETRY; IN VIVO STUDY; INHIBITION KINETICS; KERATINOCYTE; KERATOACANTHOMA; MOUSE; NONHUMAN; PROTEIN EXPRESSION; RECEPTOR UPREGULATION; SKIN CANCER; SQUAMOUS CELL CARCINOMA; TIME; TISSUE DIFFERENTIATION; TREATMENT OUTCOME; TUMOR VOLUME; WILD TYPE;

9,10-DIMETHYL-1,2-BENZANTHRACENE; ANIMALS; ANTICARCINOGENIC AGENTS; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CYCLOOXYGENASE 2 INHIBITORS; DINOPROSTONE; DISEASE MODELS, ANIMAL; FEMALE; KERATINOCYTES; KERATINS; KERATOACANTHOMA; LIGANDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PAPILLOMA; PPAR DELTA; PPAR-BETA; RNA, MESSENGER; SKIN NEOPLASMS; SULFONAMIDES; THIAZOLES; TIME FACTORS;

MUS;

EID: 75249088705     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfp212     Document Type: Article

References (35)

1. Akunda, J.K., Lao, H.C., Lee, C.A., Sessoms, A.R., Slade, R.M., and Langenbach, R. (2004). Genetic deficiency or pharmacological inhibition of cyclooxygenase-1 or -2 induces mouse keratinocyte differentiation in vitro and in vivo. FASEB J. 18, 185-187.
2. Bility, M.T., Devlin-Durante, M.K., Blazanin, N., Glick, A.B., Ward, J.M., Kang, B.H., Kennett, M.J., Gonzalez, F.J., and Peters, J.M. (2008). Ligand activation of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) inhibits chemically-induced skin tumorigenesis. Carcinogenesis 29, 2406-2414.
3. Borland, M.G., Foreman, J.E., Girroir, E.E., Zolfaghari, R., Sharma, A.K., Amin, S.M., Gonzalez, F.J., Ross, A.C., and Peters, J.M. (2008). Ligand activation of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) inhibits cell proliferation in human HaCaT keratinocytes. Mol. Pharmacol. 74, 1429-1442.
4. Burdick, A.D., Bility, M.T., Girroir, E.E., Billin, A.N., Willson, T.M., Gonzalez, F.J., and Peters, J.M. (2007). Ligand activation of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) inhibits cell growth of human N/TERT-1 keratinocytes. Cell. Signal. 19, 1163-1171.
5. Burdick, A.D., Kim, D.J., Peraza, M.A., Gonzalez, F.J., and Peters, J.M. (2006). The role of peroxisome proliferator-activated receptor-β/δ in epithelial cell growth and differentiation. Cell. Signal. 18, 9-20.
6. Fischer, S.M., Lo, H.H., Gordon, G.B., Seibert, K., Kelloff, G., Lubet, R.A., and Conti, C.J. (1999). Chemopreventive activity of celecoxib, a specific cyclooxygenase-2 inhibitor, and indomethacin against ultraviolet lightinduced skin carcinogenesis. Mol. Carcinog. 25, 231-240.
7. Fischer, S.M., Pavone, A., Mikulec, C., Langenbach, R., and Rundhaug, J.E. (2007). Cyclooxygenase-2 expression is critical for chronic UV-induced murine skin carcinogenesis. Mol. Carcinog. 46, 363-371.
8. Foreman, J.E., Sorg, J.M., McGinnis, K.S., Rigas, B., Williams, J.L., Clapper, M.L., Gonzales, F.J., and Peters, J.M. (2009). Regulation of peroxisome proliferator-activated receptor-β/δ by the APC/b-CATENIN pathway and nonsteroidal anti-inflammatory drugs. Mol. Carcinog. doi: 10.1002/mc.20546.
9. Girroir, E.E., Hollingshead, H.E., He, P., Zhu, B., Perdew, G.H., and Peters, J.M. (2008). Quantitative expression patterns of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) protein in mice. Biochem. Biophys. Res. Commun. 371, 456-461.
10. Grimaldi, P.A. (2007). Regulatory functions of PPARβ in metabolism: implications for the treatment of metabolic syndrome. Biochim. Biophys. Acta 1771, 983-990.
11. Hennings, H., Robinson, V.A., Michael, D.M., Pettit, G.R., Jung, R., and Yuspa, S.H. (1990). Development of an in vitro analogue of initiated mouse epidermis to study tumor promoters and antipromoters. Cancer Res. 50, 4794-4800.
12. Hollingshead, H.E., Borland, M.G., Billin, A.N., Willson, T.M., Gonzalez, F.J., and Peters, J.M. (2008). Ligand activation of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) and inhibition of cyclooxygenase 2 (COX2) attenuate colon carcinogenesis through independent signaling mechanisms. Carcinogenesis 29, 169-176.
13. Hull, M.A., Ko, S.C., and Hawcroft, G. (2004). Prostaglandin EP receptors: targets for treatment and prevention of colorectal cancer? Mol. Cancer Ther. 3, 1031-1039.
14. Kilgore, K.S., and Billin, A.N. (2008). PPARβ/δ ligands as modulators of the inflammatory response. Curr. Opin. Investig. Drugs 9, 463-469.
15. Kim, D.J., Akiyama, T.E., Harman, F.S., Burns, A.M., Shan, W., Ward, J.M., Kennett, M.J., Gonzalez, F.J., and Peters, J.M. (2004). Peroxisome proliferator-activated receptor beta (delta)-dependent regulation of ubiquitin C expression contributes to attenuation of skin carcinogenesis. J. Biol. Chem. 279, 23719-23727.
16. Kim, D.J., Bility, M.T., Billin, A.N., Willson, T.M., Gonzalez, F.J., and Peters, J.M. (2006a). PPARβ/δ selectively induces differentiation and inhibits cell proliferation. Cell Death Differ. 13, 53-60.
17. Kim, D.J., Murray, I.A., Burns, A.M., Gonzalez, F.J., Perdew, G.H., and Peters, J.M. (2005). Peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) inhibits epidermal cell proliferation by down-regulation of kinase activity. J. Biol. Chem. 280, 9519-9527.
18. Kim, D.J., Prabhu, K.S., Gonzalez, F.J., and Peters, J.M. (2006b). Inhibition of chemically-induced skin carcinogenicity by sulindac is independent of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ). Carcinogenesis 27, 1105-1112.
19. Lee, C.H., Olson, P., and Evans, R.M. (2003). Minireview: lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144, 2201-2207.
20. Mazhar, D., Gillmore, R., and Waxman, J. (2005). COX and cancer. QJM 98, 711-718.
21. Michalik, L., Desvergne, B., Tan, N.S., Basu-Modak, S., Escher, P., Rieusset, J., Peters, J.M., Kaya, G., Gonzalez, F.J., Zakany, J., et al. (2001). Impaired skin wound healing in peroxisome proliferator-activated receptor (PPAR)α and PPARβ mutant mice. J. Cell Biol. 154, 799-814.
22. Paramio, J.M., Casanova, M.L., Segrelles, C., Mittnacht, S., Lane, E.B., and Jorcano, J.L. (1999). Modulation of cell proliferation by cytokeratins K10 and K16. Mol. Cell. Biol. 19, 3086-3094.
23. Peters, J.M., and Gonzalez, F.J. (2009). Sorting out the functional role(s) of peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) in cell proliferation and cancer. Biochim. Biophys. Acta 1796, 230-241.
24. Peters, J.M., Hollingshead, H.E., and Gonzalez, F.J. (2008). Role of peroxisome-proliferator-activated receptor β/δ (PPARβ/δ) in gastrointestinal tract function and disease. Clin. Sci. (Lond.) 115, 107-127.
25. Peters, J.M., Lee, S.S.T., Li, W., Ward, J.M., Gavrilova, O., Everett, C., Reitman, M.L., Hudson, L.D., and Gonzalez, F.J. (2000). Growth, adipose, brain and skin alterations resulting from targeted disruption of the mouse peroxisome proliferator-activated receptor β/δ. Mol. Cell. Biol. 20, 5119-5128.
26. Schmuth, M., Haqq, C.M., Cairns, W.J., Holder, J.C., Dorsam, S., Chang, S., Lau, P., Fowler, A.J., Chuang, G., Moser, A.H., et al. (2004). Peroxisome proliferator-activated receptor (PPAR)-β/δ stimulates differentiation and lipid accumulation in keratinocytes. J. Invest. Dermatol. 122, 971-983.
27. Shaik, M.S., Chatterjee, A., and Singh, M. (2004). Effect of a selective cyclooxygenase-2 inhibitor, nimesulide, on the growth of lung tumors and their expression of cyclooxygenase-2 and peroxisome proliferator-activated receptor-gamma. Clin. Cancer Res. 10, 1521-1529.
28. Shan, W., Nicol, C.J., Ito, S., Bility, M.T., Kennett, M.J., Ward, J.M., Gonzalez, F.J., and Peters, J.M. (2008a). Peroxisome proliferator-activated receptor-β/δ protects against chemically induced liver toxicity in mice. Hepatology 47, 225-235.
29. Shan, W., Palkar, P.S., Murray, I.A., McDevitt, E.I., Kennett, M.J., Kang, B.H., Isom, H.C., Perdew, G.H., Gonzalez, F.J., and Peters, J.M. (2008b). Ligand activation of peroxisome proliferator-activated receptor β/δ (PPARβ/δ) attenuates carbon tetrachloride hepatotoxicity by downregulating proinflammatory gene expression. Toxicol. Sci. 105, 418-428.
30. Strickland, J.E., Greenhalgh, D.A., Koceva-Chyla, A., Hennings, H., Restrepo, C., Balaschak, M., and Yuspa, S.H. (1988). Development of murine epidermal cell lines which contain an activated rasHa oncogene and form papillomas in skin grafts on athymic nude mouse hosts. Cancer Res. 48, 165-169.
31. Tiano, H.F., Loftin, C.D., Akunda, J., Lee, C.A., Spalding, J., Sessoms, A., Dunson, D.B., Rogan, E.G., Morham, S.G., Smart, R.C., 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.
32. Westergaard, M., Henningsen, J., Svendsen, M.L., Johansen, C., Jensen, U.B., Schroder, H.D., Kratchmarova, I., Berge, R.K., Iversen, L., Bolund, L., et al. (2001). Modulation of keratinocyte gene expression and differentiation by PPAR-selective ligands and tetradecylthioacetic acid. J. Invest. Dermatol. 116, 702-712.
33. Wilgus, T.A., Breza, T.S., Jr., Tober, K.L., and Oberyszyn, T.M. (2004). Treatment with 5-fluorouracil and celecoxib displays synergistic regression of ultraviolet light B-induced skin tumors. J. Invest. Dermatol. 122, 1488-1494.
34. Yuspa, S.H., Hawley-Nelson, P., Koehler, B., and Stanley, J.R. (1980). A survey of transformation markers in differentiating epidermal cell lines in culture. Cancer Res. 40, 4694-4703.
35. Yuspa, S.H., and Morgan, D.L. (1981). Mouse skin cells resistant to terminal differentiation associated with initiation of carcinogenesis. Nature 293, 72-74.