Effects of parabens on adipocyte differentiation

Toxicological Sciences

Volumn 131, Issue 1, 2013, Pages 56-70

  Hu, Pan ^a   Chen, Xin ^a   Whitener, Rick J ^b   Boder, Eric T ^b   Jones, Jeremy O ^c   Porollo, Aleksey ^d   Chen, Jiangang ^e   Zhao, Ling ^a  

^a CHANGCHUN UNIVERSITY OF CHINESE MEDICINE   (China)

^b University of Tennessee   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^d UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF TENNESSEE   (United States)

Author keywords

Adipocyte differentiation; Endocrine disrupting compound; Glucocorticoid receptor; Paraben; Peroxisome proliferator activated receptor

Indexed keywords

4 HYDROXYBENZOIC ACID ESTER; ALKYL GROUP; AROMATIC COMPOUND; BENZOIC ACID; BENZYL PARABEN; BUTYL PARABEN; GLUCOCORTICOID RECEPTOR; LIPID; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SMALL INTERFERING RNA;

ADIPOCYTE; ADIPOGENESIS; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL DIFFERENTIATION; CELL STRUCTURE; CONTROLLED STUDY; LIPID STORAGE; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; STROMA CELL;

3T3-L1 CELLS; ADIPOCYTES; ADIPOGENESIS; ANILIDES; ANIMALS; BINDING, COMPETITIVE; CELL CULTURE TECHNIQUES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; MICE; MIFEPRISTONE; MOLECULAR STRUCTURE; PARABENS; PPAR GAMMA; PROTEIN BINDING; RECEPTORS, GLUCOCORTICOID; STRUCTURE-ACTIVITY RELATIONSHIP;

MURINAE;

EID: 84872367647     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs262     Document Type: Article

References (52)

1. Arimura, N., Horiba, T., Imagawa, M., Shimizu, M., and Sato, R. (2004). The peroxisome proliferator-activated receptor gamma regulates expression of the perilipin gene in adipocytes. J. Biol. Chem. 279, 10070-10076.
2. Bando, H., Mohri, S., Yamashita, F., Takakura, Y., and Hashida, M. (1997). Effects of skin metabolism on percutaneous penetration of lipophilic drugs. J. Pharm. Sci. 86, 759-761.
3. Boberg, J., Metzdorff, S., Wortziger, R., Axelstad, M., Brokken, L., Vinggaard, A. M., Dalgaard, M., and Nellemann, C. (2008). Impact of diisobutyl phthalate and other PPAR agonists on steroidogenesis and plasma insulin and leptin levels in fetal rats. Toxicology 250, 75-81.
4. Boberg, J., Taxvig, C., Christiansen, S., and Hass, U. (2010). Possible endocrine disrupting effects of parabens and their metabolites. Reprod. Toxicol. 30, 301-312.
5. Byford, J. R., Shaw, L. E., Drew, M. G., Pope, G. S., Sauer, M. J., and Darbre, P. D. (2002). Oestrogenic activity of parabens in MCF7 human breast cancer cells. J. Steroid Biochem. Mol. Biol. 80, 49-60.
6. Calafat, A. M., Ye, X., Wong, L. Y., Bishop, A. M., and Needham, L. L. (2010). Urinary concentrations of four parabens in the U.S. population: NHANES 2005-2006. Environ. Health Perspect. 118, 679-685.
7. Chamorro-García, R., Kirchner, S., Li, X., Janesick, A., Casey, S. C., Chow, C., and Blumberg, B. (2012). Bisphenol A diglycidyl ether induces adipogenic differentiation of multipotent stromal stem cells through a peroxisome proliferator-activated receptor gamma-independent mechanism. Environ. Health Perspect. 120, 984-989.
8. Charmandari, E., Raji, A., Kino, T., Ichijo, T., Tiulpakov, A., Zachman, K., and Chrousos, G. P. (2005). A novel point mutation in the ligand-binding domain (LBD) of the human glucocorticoid receptor (hGR) causing generalized glucocorticoid resistance: The importance of the C terminus of hGR LBD in conferring transactivational activity. J. Clin. Endocrinol. Metab. 90, 3696-3705.
9. Chen, J., Ahn, K. C., Gee, N. A., Gee, S. J., Hammock, B. D., and Lasley, B. L. (2007). Antiandrogenic properties of parabens and other phenolic containing small molecules in personal care products. Toxicol. Appl. Pharmacol. 221, 278-284.
10. Danielsen, M., Hinck, L., and Ringold, G. M. (1989). Mutational analysis of the mouse glucocorticoid receptor. Cancer Res. 49(8 Suppl), 2286s-2291s.
11. Darbre, P. D. (2004). Underarm cosmetics and breast cancer. Eur. J. Cancer Prev. 13, 153.
12. Darbre, P. D., Aljarrah, A., Miller, W. R., Coldham, N. G., Sauer, M. J., and Pope, G. S. (2004). Concentrations of parabens in human breast tumours. J. Appl. Toxicol. 24, 5-13.
13. Darbre, P. D., Byford, J. R., Shaw, L. E., Horton, R. A., Pope, G. S., and Sauer, M. J. (2002). Oestrogenic activity of isobutylparaben in vitro and in vivo. J. Appl. Toxicol. 22, 219-226.
14. Darbre, P. D., and Harvey, P. W. (2008). Paraben esters: Review of recent studies of endocrine toxicity, absorption, esterase and human exposure, and discussion of potential human health risks. J. Appl. Toxicol. 28, 561-578.
15. Dawson, K., Zhao, L., Adkins, Y., Vemuri, M., Rodriguez, R. L., Gregg, J. P., Kelley, D. S., and Hwang, D. H. (2012). Modulation of blood cell gene expression by DHA supplementation in hypertriglyceridemic men. J. Nutr. Biochem. 23, 616-621.
16. Draper, N., and Stewart, P. M. (2005). 11Beta-hydroxysteroid dehydrogenase and the pre-receptor regulation of corticosteroid hormone action. J. Endocrinol. 186, 251-271.
17. El Hussein, S., Muret, P., Berard, M., Makki, S., and Humbert, P. (2007). Assessment of principal parabens used in cosmetics after their passage through human epidermis-dermis layers (ex-vivo study). Exp. Dermatol. 16, 830-836.
18. Esposito, E., Bortolotti, F., Nastruzzi, C., Menegatti, E., and Cortesi, R. (2003). Diffusion of preservatives from topical dosage forms: A comparative study. J. Cosmet. Sci. 54, 239-250.
19. Farmer, S. R. (2006). Transcriptional control of adipocyte formation. Cell Metab. 4, 263-273.
20. Frohnert, B. I., Hui, T. Y., and Bernlohr, D. A. (1999). Identification of a functional peroxisome proliferator-responsive element in the murine fatty acid transport protein gene. J. Biol. Chem. 274, 3970-3977.
21. Green, H., and Kehinde, O. (1975). An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 5, 19-27.
22. Greenberg, A. S., Egan, J. J., Wek, S. A., Moos, M. C. Jr, Londos, C., and Kimmel, A. R. (1993). Isolation of cDNAs for perilipins A and B: sequence and expression of lipid droplet-associated proteins of adipocytes. Proc. Natl. Acad. Sci. U.S.A. 90, 12035-12039.
23. Gregoire, F. M., Smas, C. M., and Sul, H. S. (1998). Understanding adipocyte differentiation. Physiol. Rev. 78, 783-809.
24. Grün, F., and Blumberg, B. (2006). Environmental obesogens: Organotins and endocrine disruption via nuclear receptor signaling. Endocrinology 147(6 Suppl), S50-S55.
25. Gumy, C., Chandsawangbhuwana, C., Dzyakanchuk, A. A., Kratschmar, D. V., Baker, M. E., and Odermatt, A. (2008). Dibutyltin disrupts glucocorticoid receptor function and impairs glucocorticoid-induced suppression of cytokine production. PLoS ONE 3, e3545.
26. Han, G. S., Wu, W. I., and Carman, G. M. (2006). The Saccharomyces cerevisiae lipin homolog is a Mg2+-dependent phosphatidate phosphatase enzyme. J. Biol. Chem. 281, 9210-9218.
27. Janjua, N. R., Mortensen, G. K., Andersson, A. M., Kongshoj, B., Skakkebaek, N. E., and Wulf, H. C. (2007). Systemic uptake of diethyl phthalate, dibutyl phthalate, and butyl paraben following whole-body topical application and reproductive and thyroid hormone levels in humans. Environ. Sci. Technol. 41, 5564-5570.
28. Jewell, C., Bennett, P., Mutch, E., Ackermann, C., and Williams, F. M. (2007). Inter-individual variability in esterases in human liver. Biochem. Pharmacol. 74, 932-939.
29. Johansson, M., Johansson, N., and Lund, B. O. (2005). Xenobiotics and the glucocorticoid receptor: Additive antagonistic effects on tyrosine aminotransferase activity in rat hepatoma cells. Basic Clin. Pharmacol. Toxicol. 96, 309-315.
30. Johansson, M., Nilsson, S., and Lund, B. O. (1998). Interactions between methylsulfonyl PCBs and the glucocorticoid receptor. Environ. Health Perspect. 106, 769-772.
31. Kim, J., Temple, K. A., Jones, S. A., Meredith, K. N., Basko, J. L., and Brady, M. J. (2007). Differential modulation of 3T3-L1 adipogenesis mediated by 11beta-hydroxysteroid dehydrogenase-1 levels. J. Biol. Chem. 282, 11038-11046.
32. Komatsu, H., Okamoto, H., Miyagawa, K., Hashida, M., and Sezaki, H. (1986). Percutaneous absorption of butylparaben from liposomes in vitro. Chem. Pharm. Bull. 34, 3423-3430.
33. Li, P., Callery, P. S., Gan, L. S., and Balani, S. K. (2007). Esterase inhibition by grapefruit juice flavonoids leading to a new drug interaction. Drug Metab. Dispos. 35, 1203-1208.
34. Marcolongo, P., Senesi, S., Gava, B., Fulceri, R., Sorrentino, V., Margittai, E., Lizák, B., Csala, M., Bánhegyi, G., and Benedetti, A. (2008). Metyrapone prevents cortisone-induced preadipocyte differentiation by depleting luminal NADPH of the endoplasmic reticulum. Biochem. Pharmacol. 76, 382-390.
35. Martin, G., Poirier, H., Hennuyer, N., Crombie, D., Fruchart, J. C., Heyman, R. A., Besnard, P., and Auwerx, J. (2000). Induction of the fatty acid transport protein 1 and acyl-CoA synthase genes by dimer-selective rexinoids suggests that the peroxisome proliferator-activated receptor-retinoid X receptor heterodimer is their molecular target. J. Biol. Chem. 275, 12612-12618.
36. Oishi, S. (2001). Effects of butylparaben on the male reproductive system in rats. Toxicol. Ind. Health 17, 31-39.
37. Oishi, S. (2002). Effects of butyl paraben on the male reproductive system in mice. Arch. Toxicol. 76, 423-429.
38. Park, J. S., Rhee, S. D., Kang, N. S., Jung, W. H., Kim, H. Y., Kim, J. H., Kang, S. K., Cheon, H. G., Ahn, J. H., and Kim, K. Y. (2011). Anti-diabetic and antiadipogenic effects of a novel selective 11β-hydroxysteroid dehydrogenase type 1 inhibitor, 2-(3-benzoyl)-4-hydroxy-1,1-dioxo-2H-1,2-benzothiazine-2-yl-1-phenylethanone (KR-66344). Biochem. Pharmacol. 81, 1028-1035.
39. Rastogi, S. C., Schouten, A., de Kruijf, N., and Weijland, J. W. (1995). Contents of methyl-, ethyl-, propyl-, butyl- and benzylparaben in cosmetic products. Contact Derm. 32, 28-30.
40. Sargis, R. M., Johnson, D. N., Choudhury, R. A., and Brady, M. J. (2010). Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity 18, 1283-1288.
41. Schlumpf, M., Kypke, K., Wittassek, M., Angerer, J., Mascher, H., Mascher, D., Vökt, C., Birchler, M., and Lichtensteiger, W. (2010). Exposure patterns of UV filters, fragrances, parabens, phthalates, organochlor pesticides, PBDEs, and PCBs in human milk: Correlation of UV filters with use of cosmetics. Chemosphere 81, 1171-1183.
42. Shaw, J., and deCatanzaro, D. (2009). Estrogenicity of parabens revisited: Impact of parabens on early pregnancy and an uterotrophic assay in mice. Reprod. Toxicol. 28, 26-31.
43. Soni, M. G., Carabin, I. G., and Burdock, G. A. (2005). Safety assessment of esters of p-hydroxybenzoic acid (parabens). Food Chem. Toxicol. 43, 985-1015.
44. Souza, S. C., de Vargas, L. M., Yamamoto, M. T., Lien, P., Franciosa, M. D., Moss, L. G., and Greenberg, A. S. (1998). Overexpression of perilipin A and B blocks the ability of tumor necrosis factor alpha to increase lipolysis in 3T3-L1 adipocytes. J. Biol. Chem. 273, 24665-24669.
45. Stofkova, A. (2009). Leptin and adiponectin: From energy and metabolic dysbalance to inflammation and autoimmunity. Endocr. Regul. 43, 157-168.
46. Taxvig, C., Dreisig, K., Boberg, J., Nellemann, C., Schelde, A. B., Pedersen, D., Boergesen, M., Mandrup, S., and Vinggaard, A. M. (2012). Differential effects of environmental chemicals and food contaminants on adipogenesis, biomarker release and PPARγ activation. Mol. Cell. Endocrinol. 361, 106-115.
47. Terasaka, S., Inoue, A., Tanji, M., and Kiyama, R. (2006). Expression profiling of estrogen-responsive genes in breast cancer cells treated with alkylphenols, chlorinated phenols, parabens, or bis- and benzoylphenols for evaluation of estrogenic activity. Toxicol. Lett. 163, 130-141.
48. van Meeuwen, J. A., van Son, O., Piersma, A. H., de Jong, P. C., and van den Berg, M. (2008). Aromatase inhibiting and combined estrogenic effects of parabens and estrogenic effects of other additives in cosmetics. Toxicol. Appl. Pharmacol. 230, 372-382.
49. Wilson, V. S., Bobseine, K., Lambright, C. R., and Gray, L. E. Jr. (2002). A novel cell line, MDA-kb2, that stably expresses an androgen- and glucocorticoid-responsive reporter for the detection of hormone receptor agonists and antagonists. Toxicol. Sci. 66, 69-81.
50. Xu, M., Chakraborti, P. K., Garabedian, M. J., Yamamoto, K. R., and Simons, S. S. (1996). Modular structure of glucocorticoid receptor domains is not equivalent to functional independence. Stability and activity of the steroid binding domain are controlled by sequences in separate domains. J. Biol. Chem. 271, 21430-21438.
51. Ye, X., Bishop, A. M., Reidy, J. A., Needham, L. L., and Calafat, A. M. (2006). Parabens as urinary biomarkers of exposure in humans. Environ. Health Perspect. 114, 1843-1846.
52. Zhang, P., O'Loughlin, L., Brindley, D. N., and Reue, K. (2008). Regulation of lipin-1 gene expression by glucocorticoids during adipogenesis. J. Lipid Res. 49, 1519-1528.