Ligand activation of peroxisome proliferator-activated receptor-β/ δ inhibits cell proliferation in human HaCaT keratinocytes

Molecular Pharmacology

Volumn 74, Issue 5, 2008, Pages 1429-1442

  Borland, Michael G ^a   Foreman, Jennifer E ^a   Girroir, Elizabeth E ^a   Zolfaghari, Reza ^a   Sharma, Arun K ^b   Amin, Shantu ^b   Gonzalez, Frank J ^c   Ross, A Catharine ^a   Peters, Jeffrey M ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b PENN STATE CANCER INSTITUTE   (United States)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

[2 METHYL 4 [4 METHYL 2 (4 TRIFLUOROMETHYLPHENYL) 5 THIAZOLYLMETHYLTHIO]PHENOXY]ACETIC ACID; [4 [2 (3 FLUORO 4 TRIFLUOROMETHYLPHENYL) 4 METHYL 5 THIAZOLYLMETHYLTHIO] 2 METHYLPHENOXY]ACETIC ACID; LIPOCORTIN 5; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PROTEIN KINASE B; RETINOIC ACID; RETINOIC ACID RECEPTOR; RETINOID X RECEPTOR;

ARTICLE; CELL CYCLE; CELL GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DRUG INHIBITION; FLOW CYTOMETRY; GENE EXPRESSION; GENOTYPE; HUMAN; HUMAN CELL; KERATINOCYTE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

ANNEXIN A5; BLOTTING, WESTERN; CASPASE 3; CASPASE 7; CELL LINE; CELL PROLIFERATION; FLOW CYTOMETRY; HUMANS; KERATINOCYTES; LIGANDS; PHOSPHORYLATION; POLYMERASE CHAIN REACTION; PPAR DELTA; PPAR-BETA; THIAZOLES; TRETINOIN;

EID: 54349120502     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.108.050609     Document Type: Article

References (53)

1. Berger J, Leibowitz MD, Doebber TW, Elbrecht A, Zhang B, Zhou G, Biswas C, Cullinan CA, Hayes NS, Li Y, Tanen M, Ventre J, Wu MS, Berger GD, Mosley R, Marquis R, Santini C, Sahoo SP, Tolman RL, Smith RG, and Moller DE (1999) Novel peroxisome proliferator-activated receptor (PPAR) γ and PPARδ ligands produce distinct biological effects. J Biol Chem 274:6718-6725.
2. Burdick AD, Bility MT, Girroir EE, Billin AN, Willson TM, Gonzalez FJ, and Peters JM (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.
3. Burdick AD, Kim DJ, Peraza MA, Gonzalez FJ, and Peters JM (2006) The role of peroxisome proliferator-activated receptor-β/δ in epithelial growth and differentiation. Cell Signal 18:9-20.
4. Chen CF, Goyette P, and Lohnes D (2004) RARγ acts as a tumor suppressor in mouse keratinocytes. Oncogene 23:5350-5359.
5. Chen LC, Kirchhoff S, and De Luca LM (1994a) Effect of excess dietary retinoic acid on skin papilloma and carcinoma formation induced by a complete carcinogenesis protocol in female Sencar mice. Cancer Lett 78:63-67.
6. Chen LC, Sly L, and De Luca LM (1994b) High dietary retinoic acid prevents malignant conversion of skin papillomas induced by a two-stage carcinogenesis protocol in female SENCAR mice. Carcinogenesis 15:2383-2386.
7. Chen WC, Sass JO, Seltmann H, Nau H, Orfanos CE, and Zouboulis CC (2000) Biological effects and metabolism of 9-cis-retinoic acid and its metabolite 9,13-di-cis-retinoic acid in HaCaT keratinocytes in vitro: comparison with all-transretinoic acid. Arch Dermatol Res 292:612-620.
8. Darwiche N, Celli G, Tennenbaum T, Glick AB, Yuspa SH, and De Luca LM (1995) Mouse skin tumor progression results in differential expression of retinoic acid and retinoid X receptors. Cancer Res 55:2774-2782.
9. Darwiche N, Scita G, Jones C, Rutberg S, Greenwald E, Tennenbaum T, Collins SJ, De Luca LM, and Yuspa SH (1996) Loss of retinoic acid receptors in mouse skin and skin tumors is associated with activation of the ras(Ha) oncogene and high risk for premalignant progression. Cancer Res 56:4942-4949.
10. Demerjian M, Man MQ, Choi EH, Brown BE, Crumrine D, Chang S, Mauro T, Elias PM, and Feingold KR (2006) Topical treatment with thiazolidinediones, activators of peroxisome proliferator-activated receptor-γ, normalizes epidermal homeostasis in a murine hyperproliferative disease model. Exp Dermatol 15:154-160.
11. Di-Poï N, Tan NS, Michalik L, Wahli W, and Desvergne B (2002) Antiapoptotic role of PPARβ in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol Cell 10:721-733.
12. Girroir EE, Hollingshead HE, Billin AN, Willson TM, Robertson GP, Sharma AK, Amin S, Gonzalez FJ, and Peters JM (2008) Peroxisome proliferator-activated receptor-β/δ (PPAR β/δ) ligands inhibit growth of UACC903 and MCF7 human cancer cell lines. Toxicology 243:236-243.
13. Grimaldi PA (2007) Regulatory functions of PPARβ in metabolism: implications for the treatment of metabolic syndrome. Biochim Biophys Acta 1771:983-990.
14. Gupta RA, Wang D, Katkuri S, Wang H, Dey SK, and DuBois RN (2004) Activation of nuclear hormone receptor peroxisome proliferator-activated receptor-δ accelerates intestinal adenoma growth. Nat Med 10:245-247.
15. Hanley K, Jiang Y, He SS, Friedman M, Elias PM, Bikle DD, Williams ML, and Feingold KR (1998) Keratinocyte differentiation is stimulated by activators of the nuclear hormone receptor PPARα. J Invest Dermatol 110:368-375.
16. Hansen LA, Sigman CC, Andreola F, Ross SA, Kelloff GJ, and De Luca LM (2000) Retinoids in chemoprevention and differentiation therapy. Carcinogenesis 21:1271-1279.
17. Henseleit U, Rosenbach T, and Kolde G (1996) Induction of apoptosis in human HaCaT keratinocytes. Arch Dermatol Res 288:676-683.
18. Hollingshead HE, Killins RL, Borland MG, Girroir EE, Billin AN, Willson TM, Sharma AK, Amin S, Gonzalez FJ, and Peters JM (2007) Peroxisome proliferator-activated receptor-β/δ (PPARβ/δ) ligands do not potentiate growth of human cancer cell lines. Carcinogenesis 28:2641-2649.
19. Kanekura T, Higashi Y, and Kanzaki T (2000) Inhibitory effects of 9-cis-retinoic acid and pyrrolidinedithiocarbamate on cyclooxygenase (COX)-2 expression and cell growth in human skin squamous carcinoma cells. Cancer Lett 161:177-183.
20. Kim DJ, Akiyama TE, Harman FS, Burns AM, Shan W, Ward JM, Kennett MJ, Gonzalez FJ, and Peters JM (2004) Peroxisome proliferator-activated receptor β(δ) -dependent regulation of ubiquitin C expression contributes to attenuation of skin carcinogenesis. J Biol Chem 279:23719-23727.
21. Kim DJ, Bility MT, Billin AN, Willson TM, Gonzalez FJ, and Peters JM (2006) PPARβ/δ selectively induces differentiation and inhibits cell proliferation. Cell Death Differ 13:53-60.
22. Kim DJ, Murray IA, Burns AM, Gonzalez FJ, Perdew GH, and Peters JM (2005) Peroxisome Proliferator-activated Receptor-β/δ Inhibits Epidermal Cell Proliferation by Down-regulation of Kinase Activity. J Biol Chem 280:9519-9527.
23. Klaassen I, Brakenhoff RH, Smeets SJ, Snow GB, and Braakhuis BJ (2001) Metabolism and growth inhibition of four retinoids in head and neck squamous normal and malignant cells. Br J Cancer 85:630-635.
24. Lee CH, Olson P, and Evans RM (2003) Lipid metabolism, metabolic diseases, and peroxisome proliferator-activated receptors. Endocrinology 144:2201-2207.
25. Lee CH, Olson P, Hevener A, Mehl I, Chong LW, Olefsky JM, Gonzalez FJ, Ham J, Kang H, Peters JM, et al. (2006) PPARδ regulates glucose metabolism and insulin sensitivity. Proc Natl Acad Sci U S A 103:3444-3449.
26. Man MQ, Barish GD, Schmuth M, Crumrine D, Barak Y, Chang S, Jiang Y, Evans RM, Elias PM, and Feingold KR (2008) Deficiency of PPARβ/δ in the epidermis results in defective cutaneous permeability barrier homeostasis and increased inflammation. J Invest Dermatol 128:370-377.
27. Marin HE, Peraza MA, Billin AN, Willson TM, Ward JM, Kennett MJ, Gonzalez FJ, and Peters JM (2006) Ligand activation of peroxisome proliferator-activated receptor β inhibits colon carcinogenesis. Cancer Res 66:4394-4401.
28. Martinasso G, Maggiora M, Trombetta A, Canuto RA, and Muzio G (2006) Effects of di(2-ethylhexyl) phthalate, a widely used peroxisome proliferator and plasticizer, on cell growth in the human keratinocyte cell line NCTC 2544. J Toxicol Environ Health A 69:353-365.
29. Matsuura H, Adachi H, Smart RC, Xu X, Arata J, and Jetten AM (1999) Correlation between expression of peroxisome proliferator-activated receptor β and squamous differentiation in epidermal and tracheobronchial epithelial cells. Mol Cell Endocrinol 147:85-92.
30. Memezawa A, Takada I, Takeyama K, Igarashi M, Ito S, Aiba S, Kato S, and Kouzmenko AP (2007) Id2 gene-targeted crosstalk between Wnt and retinoid signaling regulates proliferation in human keratinocytes. Oncogene 26:5038-5045.
31. Michalik L, Desvergne B, Tan NS, Basu-Modak S, Escher P, Rieusset J, Peters JM, Kaya G, Gonzalez FJ, 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.
32. Mukherjee R, Jow L, Croston GE, and Paterniti JR Jr (1997) Identification, characterization, and tissue distribution of human peroxisome proliferator-activated receptor (PPAR) isoforms PPARγ2 versus PPARγ1 and activation with retinoid X receptor agonists and antagonists. J Biol Chem 272:8071-8076.
33. Pelton P (2006) GW-501516 GlaxoSmithKline/Ligand. Curr Opin Investig Drugs 7:360-370.
34. Peraza MA, Burdick AD, Marin HE, Gonzalez FJ, and Peters JM (2006) The toxicology of ligands for peroxisome proliferator-activated receptors (PPAR). Toxicol Sci 90:269-295.
35. Peters JM, Cheung C, and Gonzalez FJ (2005) Peroxisome proliferator-activated receptor-alpha and liver cancer: where do we stand? J Mol Med 83:774-785.
36. Peters JM, Hollingshead HE, and Gonzalez FJ (2008) Role of peroxisome-proliferator-activated receptor β/δ (PPARβ/δ) in gastrointestinal tract function and disease. Clin Sci (Lond) 115:107-127.
37. Peters JM, Lee SS, Li W, Ward JM, Gavrilova O, Everett C, Reitman ML, Hudson LD, and Gonzalez FJ (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.
38. Rieck M, Meissner W, Ries S, Müller-Brüsselbach S, and Müller R (2008) Ligand-mediated regulation of peroxisome proliferator-activated receptor (PPAR) β/δ: A comparative analysis of PPAR-selective agonists and all-trans retinoic acid. Mol Pharmacol 74:1269-1277.
39. Schmuth M, Haqq CM, Cairns WJ, Holder JC, Dorsam S, Chang S, Lau P, Fowler AJ, Chuang G, Moser AH, et al. (2004) Peroxisome proliferator-activated receptor (PPAR)-β/δ stimulates differentiation and lipid accumulation in keratinocytes. J Invest Dermatol 122:971-983.
40. Schug TT, Berry DC, Shaw NS, Travis SN, and Noy N (2007) Opposing effects of retinoic acid on cell growth result from alternate activation of two different nuclear receptors. Cell 129:723-733.
41. Shaw N, Elholm M, and Noy N (2003) Retinoic acid is a high affinity selective ligand for the peroxisome proliferator-activated receptor β/δ. J Biol Chem 278:41589-41592.
42. Sznaidman ML, Haffner CD, Maloney PR, Fivush A, Chao E, Goreham D, Sierra ML, LeGrumelec C, Xu HE, Montana VG, et al. (2003) Novel selective small molecule agonists for peroxisome proliferator-activated receptor δ (PPARδ)-synthesis and biological activity. Bioorg Med Chem Lett 13:1517-1521.
43. Tan NS, Michalik L, Noy N, Yasmin R, Pacot C, Heim M, Flühmann B, Desvergne B, and Wahli W (2001) Critical roles of PPARβ/δ in keratinocyte response to inflammation. Genes Dev 15:3263-3277.
44. Tennenbaum T, Lowry D, Darwiche N, Morgan DL, Gartsbein M, Hansen L, De Luca LM, Hennings H, and Yuspa SH (1998) Topical retinoic acid reduces skin papilloma formation but resistant papillomas are at high risk for malignant conversion. Cancer Res 58:1435-1443.
45. Tong PS, Mayes DM, and Wheeler LA (1988) Differential effects of retinoids on DNA synthesis in calcium-regulated murine epidermal keratinocyte cultures. J Invest Dermatol 90:861-868.
46. Verma AK (1987) Inhibition of both stage I and stage II mouse skin tumour promotion by retinoic acid and the dependence of inhibition of tumor promotion on the duration of retinoic acid treatment. Cancer Res 47:5097-5101.
47. Verma AK (1988) Inhibition of tumor promoter 12-O-tetradecanoylphorbol- 13-acetate-induced synthesis of epidermal ornithine decarboxylase messenger RNA and diacylglycerol-promoted mouse skin tumor formation by retinoic acid. Cancer Res 48:2168-2173.
48. Verma AK, Slaga TJ, Wertz PW, Mueller GC, and Boutwell RK (1980) Inhibition of skin tumor promotion by retinoic acid and its metabolite 5,6-epoxyretinoic acid. Cancer Res 40:2367-2371.
49. Wang D, Wang H, Guo Y, Ning W, Katkuri S, Wahli W, Desvergne B, Dey SK, and DuBois RN (2006) From the cover: crosstalk between peroxisome proliferator-activated receptor δ and VEGF stimulates cancer progression. Proc Natl Acad Sci U S A 103:19069-19074.
50. Weil M, Raff MC, and Braga VM (1999) Caspase activation in the terminal differentiation of human epidermal keratinocytes. Curr Biol 9:361-364.
51. Westergaard M, Henningsen J, Svendsen ML, Johansen C, Jensen UB, Schrøder HD, Kratchmarova I, Berge RK, 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.
52. Willson TM, Brown PJ, Sternbach DD, and Henke BR (2000) The PPARs: from orphan receptors to drug discovery. J Med Chem 43:527-550.
53. Xu H, Cheepala S, McCauley E, Coombes K, Xiao L, Fischer SM, and Clifford JL (2006) Chemoprevention of skin carcinogenesis by phenylretinamides: retinoid receptor-independent tumor suppression. Clin Cancer Res 12:969-979.