Organotypic modeling of human keratinocyte response to peroxisome proliferators

Cells Tissues Organs

Volumn 196, Issue 5, 2012, Pages 431-441

  Zhang, Carmen ^a   Gurevich, Igor ^b   Aneskievich, Brian J ^a,c  

^a Department of Pharmaceutical Sciences ^*  (United States)

^b Graduate Program in Toxicology   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Differentiation; Keratinocyte; Organotypic modeling; Peroxisome proliferator; Peroxisome proliferator activated receptor

Indexed keywords

BIOLOGICAL MARKER; CLOFIBRATE; FILAGGRIN; HEAT SHOCK PROTEIN 27; PEROXISOME PROLIFERATOR; PIRINIXIC ACID;

ANIMAL TISSUE; ARTICLE; BIOASSAY; CELL CULTURE; CELL GROWTH; CELL HYPERPLASIA; CLINICAL STUDY; CONTROLLED STUDY; EPIDERMIS; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; MOLECULAR MODEL; MONOLAYER CULTURE; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION;

BLOTTING, NORTHERN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CLOFIBRATE; ELECTROPHORESIS; HUMANS; IMMUNOHISTOCHEMISTRY; KERATINOCYTES; MICROSCOPY, FLUORESCENCE; PEROXISOME PROLIFERATORS; PYRIMIDINES;

MUS; RODENTIA;

EID: 84867744942     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000336268     Document Type: Article

References (52)

1. Al Kholaifi A., A. Amer, B. Jeffery, T.J. Gray, R.A. Roberts, D.R. Bell (2008) Species specific kinetics and zonation of hepatic DNA synthesis induced by ligands of PPARalpha. Toxicol Sci 104: 74-85.
2. Aneskievich B.J., E. Fuchs (1992) Terminal differentiation in keratinocytes involves positive as well as negative regulation by retinoic acid receptors and retinoid X receptors at retinoid response elements. Mol Cell Bio 12: 4862-4871.
3. Batheja P., Y. Song, P. Wertz, B. Michniak-Kohn (2009) Effects of growth conditions on the barrier properties of a human skin equivalent. Pharm Res 26: 1689-1700.
4. Boudjelal M., J.J. Voorhees, G.J. Fisher (2002) Retinoid signaling is attenuated by proteasome- mediated degradation of retinoid receptors in human keratinocyte HaCaTcells. Exp Cell Res 274: 130-137.
5. Burdick A.D., M.T. Bility, E.E. Girroir, A.N. Billin, T.M. Willson, F.J. Gonzalez, J.M. Peters (2007) Ligand activation of peroxisome proliferator-activated receptor-beta/ delta(PPARbeta/delta) inhibits cell growth of human N/TERT-1 keratinocytes. Cell Signal 19: 1163-1171.
6. Burdick A.D., D.J. Kim, M.A. Peraza, F.J. Gonzalez, J.M. Peters (2006) The role of peroxisome proliferator-activated receptor-beta/delta in epithelial cell growth and differentiation. Cell Signal 18: 9-20.
7. Cheung C., T.E. Akiyama, J.M. Ward, C.J. Nicol, L. Feigenbaum, C. Vinson, F.J. Gonzalez (2004) Diminished hepatocellular proliferation in mice humanized for the nuclear receptor peroxisome proliferator-activated receptor alpha. Cancer Res 64: 3849-3854.
8. Chong H.C., M.J. Tan, V. Philippe, S.H. Tan, C.K. Tan, C.W. Ku, Y.Y. Goh, W. Wahli, L. Michalik, N.S. Tan (2009) Regulation of epithelialmesenchymal IL-1 signaling by PPARbeta/ delta is essential for skin homeostasis and wound healing. J Cell Biol 184: 817-831.
9. Choudhury A.I., Chahal S., Bell A.R., Tomlinson S.R., Roberts R.A., Salter A.M., Bell D.R. (2000) Species differences in peroxisome proliferation: Mechanisms and relevance. Mutat Re 448: 201-222.
10. Di-Poi N., N.S. Tan, L. Michalik, W. Wahli, B. Desvergne (2002) Antiapoptotic role of PPARbeta in keratinocytes via transcriptional control of the Akt1 signaling pathway. Mol Cell 10: 721-733.
11. Dubrac S., M. Schmuth (2006) (P)PARsing epidermal development. J Invest Dermatol 126: 241-242.
12. Flores A.M., L. Li, N.G. McHugh, B.J. Aneskievich (2005) Enzyme association with PPARgamma: Evidence of a new role for 15-lipoxygenase type 2. Chem Biol Interact 151: 121- 132.
13. Gani O.A., I. Sylte (2008) Molecular recognition of docosahexaenoic acid by peroxisome proliferator- activated receptors and retinoid-X receptor alpha. J Mol Graph Model 27: 217- 224.
14. Garcia M.C., D.M. Ray, B. Lackford, M. Rubino, K. Olden, J.D. Roberts (2009) Arachidonic acid stimulates cell adhesion through a novel p38 MAPK-RhoA signaling pathway that involves heat shock protein 27. J Biol Chem 284: 20936-20945.
15. Gonzalez F.J., Y.M. Shah (2008) PPARalpha: Mechanism of species differences and hepatocarcinogenesis of peroxisome proliferators. Toxicology 246: 2-8.
16. Hanley K., Y. Jiang, S.S. He, M. Friedman, P.M. Elias, D.D. Bikle, M.L. Williams, K.R. Feingold (1998) Keratinocyte differentiation is stimulated by activators of the nuclear hormone receptor PPARalpha. J Invest Dermatol 110: 368-375.
17. Heise R., J. Mey, M.M. Neis, Y. Marquardt, S. Joussen, H. Ott, T. Wiederholt, P. Kurschat, M. Megahed, D.R. Bickers, H.F. Merk, J.M. Baron (2006) Skin retinoid concentrations are modulated by CYP26AI expression restricted to basal keratinocytes in normal human skin and differentiated 3D skin models. J Invest Dermatol 126: 2473-2480.
18. Jiang Y.J., B. Lu, P. Kim, G. Paragh, G. Schmitz, P.M. Elias, K.R. Feingold (2008) PPAR and LXR activators regulate ABCA12 expression in human keratinocytes. J Invest Dermatol 128: 104-109.
19. Kane C.D., O.L. Francone, K.A. Stevens (2006) Differential regulation of the cynomolgus, human, and rat acyl-CoA oxidase promoters by PPARalpha. Gene 380: 84-94.
20. Keller H., P.R. Devchand, M. Perroud, W. Wahli (1997) PPAR alpha structure-function relationships derived from species-specific differences in responsiveness to hypolipidemic agents. Biol Chem 378: 651-655.
21. Kim H.J., N. Chakravarti, N. Oridate, C. Choe, F.X. Claret, R. Lotan (2006) N-(4-hydroxyphenyl retinamide-induced apoptosis triggered by reactive oxygen species is mediated by activation of MAPKs in head and neck squamous carcinoma cells. Oncogene 25: 2785-2794.
22. Klaunig J.E., M.A. Babich, K.P. Baetcke, J.C. Cook, J.C. Corton, R.M. David, J.G. DeLuca, D.Y. Lai, R.H. McKee, J.M. Peters, R.A. Roberts, P.A. Fenner-Crisp (2003) PPARalpha agonist-induced rodent tumors: Modes of action and human relevance. Crit Rev Toxicol 33: 655-780.
23. Komuves L.G., K. Hanley, A.M. Lefebvre, M.Q. Man, D.C. Ng, D.D. Bikle, M.L. Williams, P.M. Elias, J. Auwerx, K.R. Feingold (2000) Stimulation of PPARalpha promotes epidermal keratinocyte differentiation in vivo. J Invest Dermatol 115: 353-360.
24. Kostenko S., U. Moens (2009) Heat shock protein 27 phosphorylation: kinases, phosphatases, functions and pathology. Cell Mol Life Sci 66: 3289-3307.
25. Lawrence J.W., Y. Li, S. Chen, J.G. DeLuca, J.P. Berger, D.R. Umbenhauer, D.E. Moller, G. Zhou (2001) Differential gene regulation in human versus rodent hepatocytes by peroxisome proliferator-activated receptor (PPAR) alpha. J Biol Chem 276: 31521-31527.
26. Lee D.D., O. Stojadinovic, A. Krzyzanowska, C. Vouthounis, M. Blumenberg, M. Tomic-Canic (2009) Retinoid-responsive transcriptional changes in epidermal keratinocytes. J Cell Physiol 220: 427-439.
27. Leigh I.M., F.M. Watt (1994) Keratinocyte Methods. Cambridge, Cambridge University Press. Maloney E.K., D.J. Waxman (1999) trans-Activation of PPARalpha and PPARgamma by structurally diverse environmental chemicals. Toxicol Appl Pharmacol 161: 209-218.
28. Margulis A., W. Zhang, J.A. Garlick (2005) In vitro fabrication of engineered human skin. Methods Mol Biol 289: 61-70.
29. Michalik L., J. Auwerx, J.P. Berger, V.K. Chatterjee, C.K. Glass, F.J. Gonzalez, P.A. Grimaldi, T. Kadowaki, M.A. Lazar, S. O'Rahilly, C.N. Palmer, J. Plutzky, J.K. Reddy, B.M. Spiegelman, B. Staels, W. Wahli (2006) International Union of Pharmacology. 61. Peroxisome proliferator-activated receptors. Pharmacol Rev 58: 726-741.
30. Michalik L., W. Wahli (2007) Peroxisome proliferator- activated receptors (PPARs) in skin health, repair and disease. Biochim Biophys Acta 1771: 991-998.
31. Morimura K., C. Cheung, J.M. Ward, J.K. Reddy, F.J. Gonzalez (2006) Differential susceptibility of mice humanized for peroxisome proliferator- activated receptor alpha to Wy- 14,643-induced liver tumorigenesis. Carcinogenesis 27: 1074-1080.
32. Motojima K. (2000) Differential effects of PPARalpha activators on induction of ectopic expression of tissue-specific fatty acid binding protein genes in the mouse liver. Int J Biochem Cell Biol 32: 1085-1092.
33. O'Shaughnessy R.F., J.C. Welti, J.C. Cooke, A.A. Avilion, B. Monks, M.J. Birnbaum, C. Byrne (2007) AKT-dependent HspB1 (Hsp27) activity in epidermal differentiation. J Biol Chem 282: 17297-17305.
34. Peraza M.A., A.D. Burdick, H.E. Marin, F.J. Gonzalez, J.M. Peters (2006) The toxicology of ligands for peroxisome proliferator-activated receptors (PPAR). Toxicol Sci 90: 269- 295.
35. Peters J.M., C. Cheung, F.J. Gonzalez (2005) Peroxisome proliferator-activated receptor-alpha and liver cancer: Where do we stand? J Mol Med 83: 774-785.
36. Poumay Y., F. Herphelin, P. Smits, I.Y. De Potter, M.R. Pittelkow (1999) High-cell-density phorbol ester and retinoic acid upregulate involucrin and downregulate suprabasal keratin 10 in autocrine cultures of human epidermal keratinocytes. Mol Cell Biol Res Commun 2: 138-144.
37. Rendl M., J. Ban, P. Mrass, C. Mayer, B. Lengauer, L. Eckhart, W. Declerq, E. Tschachler (2002) Caspase-14 expression by epidermal keratinocytes is regulated by retinoids in a differentiation-associated manner. J Invest Dermatol 119: 1150-1155.
38. Rheinwald J.G., H. Green (1975) Serial cultivation of strains of human epidermal keratinocytes: The formation of keratinizing colonies from single cells. Cell 6: 331-344.
39. Rivier M., I. Castiel, I. Safonova, G. Ailhaud, S. Michel (2000) Peroxisome proliferator activated receptor-alpha enhances lipid metabolism in a skin equivalent model. J Invest Dermatol 114: 681-687.
40. Robitaille H., C. Simard-Bisson, D. Larouche, R.M. Tanguay, R. Blouin, L. Germain (2010) The small heat-shock protein Hsp27 undergoes ERK-dependent phosphorylation and redistribution to the cytoskeleton in response to dual leucine zipper-bearing kinase expression. J Invest Dermatol 130: 74-85.
41. Schmuth M., C.M. Haqq, W.J. Cairns, J.C. Holder, S. Dorsam, S. Chang, P. Lau, A.J. Fowler, G. Chuang, A.H. Moser, B.E. Brown, M. Mao-Qiang, Y. Uchida, K. Schoonjans, J. Auwerx, P. Chambon, T.M. Willson, P.M. Elias K.R. Feingold (2004) Peroxisome proliferator- activated receptor (PPAR)-beta/delta stimulates differentiation and lipid accumulation in keratinocytes. J Invest Dermatol 122: 971-983.
42. Schmuth M., Y.J. Jiang, S. Dubrac, P.M. Elias, K.R. Feingold (2008) Thematic review series: skin lipids - peroxisome proliferator-activated receptors and liver X receptors in epidermal biology. J Lipid Res 49: 499-509.
43. Seo T., W.S. Blaner, R.J. Deckelbaum R.J. (2005) Omega-3 fatty acids: Molecular approaches to optimal biological outcomes. Curr Opin Lipidol 16: 11-18.
44. Sheu M.Y., A.J. Fowler, J. Kao, M. Schmuth, K. Schoonjans, J. Auwerx, J.W. Fluhr, M.Q. Man, P.M. Elias, K.R. Feingold (2002) Topical peroxisome proliferator activated receptor alpha activators reduce inflammation in irritant and allergic contact dermatitis models. J Invest Dermatol 118: 94-101.
45. Storey A., F. McArdle, P.S. Friedmann, M.J. Jackson, L.E. Rhodes (2005) Eicosapentaenoic acid and docosahexaenoic acid reduce UVBand TNF-alpha-induced IL-8 secretion in keratinocytes and UVB-induced IL-8 in fibroblasts. J Invest Dermatol 124: 248-255.
46. Takeuchi S., T. Matsuda, S. Kobayashi, T. Takahashi, H. Kojima (2006) In vitro screening of 200 pesticides for agonistic activity via mouse peroxisome proliferator-activated receptor (PPAR)alpha and PPARgamma and quantitative analysis of in vivo induction pathway. Toxicol Appl Pharmacol 217: 235- 244.
47. Thomas A.C., D. Tattersall, E.E. Norgett, E.A. O'Toole, D.P. Kelsell (2009) Premature terminal differentiation and a reduction in specific proteases associated with loss ofABCA12 in Harlequin ichthyosis. Am J Pathol 174: 970-978.
48. Thrash B.R., C.W. Menges, R.H. Pierce, D.J. Mc- Cance (2006) AKT1 provides an essential survival signal required for differentiation and stratification of primary human keratinocytes. J Biol Chem 281: 12155-12162.
49. Turksen K., Y. Choi, E. Fuchs (1991) Transforming growth factor alpha induced collagen degradation and cell migration in differentiating human epidermal raft cultures. Cell Regul 2: 613-625.
50. Varga T., Z. Czimmerer, L. Nagy (2011) PPARs are a unique set of fatty acid regulated transcription factors controlling both lipid metabolism and inflammation. Biochim Biophys Acta 1812: 1007-1022.
51. Westergaard M., J. Henningsen, M.L. Svendsen, C. Johansen, U.B. Jensen, H.D. Schroder, I. Kratchmarova, R.K. Berge, L. Iversen, L. Bolund, K. Kragballe, K. Kristiansen (2001) Modulation of keratinocyte gene expression and differentiation by PPAR-selective ligands and tetradecylthioacetic acid. J Invest Dermatol 116: 702-712.
52. Yang Q., A. Yamada, S. Kimura, J.M. Peters, F.J. Gonzalez (2006) Alterations in skin and stratified epithelia by constitutively activated PPARalpha. J Invest Dermatol 126: 374- 385.