PCB126 inhibits adipogenesis of human preadipocytes

Toxicology in Vitro

Volumn 29, Issue 1, 2015, Pages 132-141

  Gadupudi, Gopi ^a   Gourronc, Francoise A ^a   Ludewig, Gabriele ^a   Robertson, Larry W ^a   Klingelhutz, Aloysius J ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

Adipocytes; AhR; Diabetes; PCBs; PPAR ; Preadipocytes

Indexed keywords

3,3',4,4',5 PENTACHLOROBIPHENYL; CYTOCHROME P450 1A1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; 3,4,5,3',4'-PENTACHLOROBIPHENYL; POLYCHLORINATED BIPHENYL;

ADIPOGENESIS; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; INHIBITION KINETICS; METABOLIC SYNDROME X; PPAR GAMMA GENE; PROADIPOCYTE; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SENSITIVITY ANALYSIS; TRANSCRIPTION REGULATION; UPREGULATION; ADIPOCYTE; ANTAGONISTS AND INHIBITORS; CELL SURVIVAL; DOSE RESPONSE; DRUG EFFECTS; FLOW CYTOMETRY; METABOLISM;

ADIPOCYTES; ADIPOGENESIS; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOCHROME P-450 CYP1A1; DOSE-RESPONSE RELATIONSHIP, DRUG; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; HUMANS; POLYCHLORINATED BIPHENYLS; PPAR GAMMA; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 84908295893     PISSN: 08872333     EISSN: 18793177     Source Type: Journal    
DOI: 10.1016/j.tiv.2014.09.015     Document Type: Article

References (69)

1. Alexander D.L., Ganem L.G., Fernandez-Salguero P., Gonzalez F., Jefcoate C.R. Aryl-hydrocarbon receptor is an inhibitory regulator of lipid synthesis and of commitment to adipogenesis. J. Cell Sci. 1998, 111(Pt 22):3311-3322.
2. Alonso-Magdalena P., Quesada I., Nadal A. Endocrine disruptors in the etiology of type 2 diabetes mellitus. Nat. Rev. Endocrinol. 2011, 7:346-353.
3. Arsenescu V., Arsenescu R.I., King V., Swanson H., Cassis L.A. Polychlorinated biphenyl-77 induces adipocyte differentiation and proinflammatory adipokines and promotes obesity and atherosclerosis. Environ. Health Perspect. 2008, 116:761-768.
4. Baker N.A., Karounos M., English V., Fang J., Wei Y., Stromberg A., Sunkara M., Morris A.J., Swanson H.I., Cassis L.A. Coplanar polychlorinated biphenyls impair glucose homeostasis in lean C57BL/6 mice and mitigate beneficial effects of weight loss on glucose homeostasis in obese mice. Environ. Health Perspect. 2013, 121:105-110.
5. Barnes D.M., Hanlon P.R., Kircher E.A. Effects of inorganic HgCl2 on adipogenesis. Toxicol. Sci. 2003, 75:368-377.
6. Beischlag T.V., Luis Morales J., Hollingshead B.D., Perdew G.H. The aryl hydrocarbon receptor complex and the control of gene expression. Crit. Rev. Eukaryot. Gene Expr. 2008, 18:207-250.
7. Bernstein R.L., Hyun W.C., Davis J.H., Fulwyler M.J., Pershadsingh H.A. Flow cytometric analysis of mature adipocytes. Cytometry 1989, 10:469-474.
8. Bourez S., Joly A., Covaci A., Remacle C., Larondelle Y., Schneider Y.J., Debier C. Accumulation capacity of primary cultures of adipocytes for PCB-126: influence of cell differentiation stage and triglyceride levels. Toxicol. Lett. 2012, 214:243-250.
9. Bourez S., Van den Daelen C., Le Lay S., Poupaert J., Larondelle Y., Thome J.P., Schneider Y.J., Dugail I., Debier C. The dynamics of accumulation of PCBs in cultured adipocytes vary with the cell lipid content and the lipophilicity of the congener. Toxicol. Lett. 2013, 216:40-46.
10. Cawthorn W.P., Scheller E.L., MacDougald O.A. Adipose tissue stem cells: the great WAT hope. Trends Endocrinol. Metab. 2012, 23:270-277.
11. Choi E.Y., Lee H., Dingle R.W., Kim K.B., Swanson H.I. Development of novel CH223191-based antagonists of the aryl hydrocarbon receptor. Mol. Pharmacol. 2012, 81:3-11.
12. Cimafranca M.A., Hanlon P.R., Jefcoate C.R. TCDD administration after the pro-adipogenic differentiation stimulus inhibits PPARgamma through a MEK-dependent process but less effectively suppresses adipogenesis. Toxicol. Appl. Pharmacol. 2004, 196:156-168.
13. Cinti S. The adipose organ at a glance. Dis. Model Mech. 2012, 5:588-594.
14. Darimont C., Zbinden I., Avanti O., Leone-Vautravers P., Giusti V., Burckhardt P., Pfeifer A.M., Mace K. Reconstitution of telomerase activity combined with HPV-E7 expression allow human preadipocytes to preserve their differentiation capacity after immortalization. Cell Death Differ. 2003, 10:1025-1031.
15. Denison M.S., Nagy S.R. Activation of the aryl hydrocarbon receptor by structurally diverse exogenous and endogenous chemicals. Annu. Rev. Pharmacol. Toxicol. 2003, 43:309-334.
16. Dunmore S.J., Brown J.E. The role of adipokines in beta-cell failure of type 2 diabetes. J. Endocrinol. 2013, 216:T37-45.
17. Everett C.J., Frithsen I.L., Diaz V.A., Koopman R.J., Simpson W.M., Mainous A.G. Association of a polychlorinated dibenzo-p-dioxin, a polychlorinated biphenyl, and DDT with diabetes in the 1999-2002 National Health and Nutrition Examination Survey. Environ. Res. 2007, 103:413-418.
18. Everett C.J., Frithsen I., Player M. Relationship of polychlorinated biphenyls with type 2 diabetes and hypertension. J. Environ. Monit. 2011, 13:241-251.
19. Forgacs A.L., Kent M.N., Makley M.K., Mets B., DelRaso N., Jahns G.L., Burgoon L.D., Zacharewski T.R., Reo N.V. Comparative metabolomic and genomic analyses of TCDD-elicited metabolic disruption in mouse and rat liver. Toxicol. Sci. 2012, 125:41-55.
20. Gourronc F.A., Robertson M.M., Herrig A.K., Lansdorp P.M., Goldman F.D., Klingelhutz A.J. Proliferative defects in dyskeratosis congenita skin keratinocytes are corrected by expression of the telomerase reverse transcriptase, TERT, or by activation of endogenous telomerase through expression of papillomavirus E6/E7 or the telomerase RNA component, TERC. Exp. Dermatol. 2010, 19:279-288.
21. Green H., Kehinde O. An established preadipose cell line and its differentiation in culture. II. Factors affecting the adipose conversion. Cell 1975, 5:19-27.
22. Gregoire F.M., Smas C.M., Sul H.S. Understanding adipocyte differentiation. Physiol. Rev. 1998, 78:783-809.
23. Guilherme A., Virbasius J.V., Puri V., Czech M.P. Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat. Rev. Mol. Cell Biol. 2008, 9:367-377.
24. Harwood H.J. The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 2012, 63:57-75.
25. Hausman D.B., DiGirolamo M., Bartness T.J., Hausman G.J., Martin R.J. The biology of white adipocyte proliferation. Obes. Rev. 2001, 2:239-254.
26. Henriksen G.L., Ketchum N.S., Michalek J.E., Swaby J.A. Serum dioxin and diabetes mellitus in veterans of Operation Ranch Hand. Epidemiology 1997, 8:252-258.
27. Hestermann E.V., Stegeman J.J., Hahn M.E. Relative contributions of affinity and intrinsic efficacy to aryl hydrocarbon receptor ligand potency. Toxicol. Appl. Pharmacol. 2000, 168:160-172.
28. Hotamisligil G.S. Inflammation and metabolic disorders. Nature 2006, 444:860-867.
29. Hsu H.F., Tsou T.C., Chao H.R., Kuo Y.T., Tsai F.Y., Yeh S.C. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin on adipogenic differentiation and insulin-induced glucose uptake in 3T3-L1 cells. J. Hazard. Mater. 2010, 182:649-655.
30. Kamstra J.H., Hruba E., Blumberg B., Janesick A., Mandrup S., Hamers T., Legler J. Transcriptional and epigenetic mechanisms underlying enhanced in vitro adipocyte differentiation by the brominated flame retardant BDE-47. Environ. Sci. Technol. 2014, 48:4110-4119.
31. Kim M.J., Marchand P., Henegar C., Antignac J.P., Alili R., Poitou C., Bouillot J.L., Basdevant A., Le Bizec B., Barouki R., Clement K. Fate and complex pathogenic effects of dioxins and polychlorinated biphenyls in obese subjects before and after drastic weight loss. Environ. Health Perspect. 2011, 119:377-383.
32. Knittle J.L., Timmers K., Ginsberg-Fellner F., Brown R.E., Katz D.P. The growth of adipose tissue in children and adolescents. Cross-sectional and longitudinal studies of adipose cell number and size. J. Clin. Investig. 1979, 63:239-246.
33. La Merrill M., Emond C., Kim M.J., Antignac J.P., Le Bizec B., Clement K., Birnbaum L.S., Barouki R. Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ. Health Perspect. 2013, 121:162-169.
34. Lee Y.H., Chen S.Y., Wiesner R.J., Huang Y.F. Simple flow cytometric method used to assess lipid accumulation in fat cells. J. Lipid Res. 2004, 45:1162-1167.
35. Lee D.H., Lind P.M., Jacobs D.R., Salihovic S., van Bavel B., Lind L. Polychlorinated biphenyls and organochlorine pesticides in plasma predict development of type 2 diabetes in the elderly: the prospective investigation of the vasculature in Uppsala Seniors (PIVUS) study. Diabetes Care 2011, 34:1778-1784.
36. Li W., Vogel C.F.A., Fujiyoshi P., Matsumura F. Development of a human adipocyte model derived from human mesenchymal stem cells (hMSC) as a tool for toxicological studies on the action of TCDD. Biol. Chem. 2008, 389:169-177.
37. Lind L., Penell J., Luttropp K., Nordfors L., Syvanen A.C., Axelsson T., Salihovic S., van Bavel B., Fall T., Ingelsson E., Lind P.M. Global DNA hypermethylation is associated with high serum levels of persistent organic pollutants in an elderly population. Environ. Int. 2013, 59:456-461.
38. Manikkam M., Tracey R., Guerrero-Bosagna C., Skinner M.K. Dioxin (TCDD) induces epigenetic transgenerational inheritance of adult onset disease and sperm epimutations. PLoS ONE 2012, 7:e46249.
39. Mimura J., Fujii-Kuriyama Y. Functional role of AhR in the expression of toxic effects by TCDD. Biochim. Biophys. Acta 2003, 1619:263.
40. Mlinar B., Marc J. New insights into adipose tissue dysfunction in insulin resistance. Clin. Chem. Lab. Med. 2011, 49:1925-1935.
41. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 1983, 65:55-63.
42. Narbonne J.F., Robertson L.W. 7th International PCB Workshop: chemical mixtures in a complex world. Environ. Sci. Pollut. Res. Int. 2014, 21:6269-6275.
43. Okey A.B. An aryl hydrocarbon receptor odyssey to the shores of toxicology: the Deichmann Lecture, International Congress of Toxicology-XI. Toxicol. Sci.: an Official Journal of the Society of Toxicology 2007, 98:5-38.
44. Ovando B.J., Ellison C.A., Vezina C.M., Olson J.R. Toxicogenomic analysis of exposure to TCDD, PCB126 and PCB153: identification of genomic biomarkers of exposure to AhR ligands. BMC Genom. 2010, 11:583.
45. Patel R.D., Murray I.A., Flaveny C.A., Kusnadi A., Perdew G.H. Ah receptor represses acute-phase response gene expression without binding to its cognate response element. Lab. Invest. 2009, 89:695-707.
46. Puga A., Ma C., Marlowe J.L. The aryl hydrocarbon receptor cross-talks with multiple signal transduction pathways. Biochem. Pharmacol. 2009, 77:713-722.
47. Regnier S.M., Sargis R.M. Adipocytes under assault: environmental disruption of adipose physiology. Biochim. Biophys. Acta 2014, 1842:520-533.
48. Rodriguez A.M., Elabd C., Delteil F., Astier J., Vernochet C., Saint-Marc P., Guesnet J., Guezennec A., Amri E.Z., Dani C., Ailhaud G. Adipocyte differentiation of multipotent cells established from human adipose tissue. Biochem. Biophys. Res. Commun. 2004, 315:255-263.
49. Roos V., Ronn M., Salihovic S., Lind L., van Bavel B., Kullberg J., Johansson L., Ahlstrom H., Lind P.M. Circulating levels of persistent organic pollutants in relation to visceral and subcutaneous adipose tissue by abdominal MRI. Obesity (Silver Spring) 2013, 21:413-418.
50. Rosen E.D., Sarraf P., Troy A.E., Bradwin G., Moore K., Milstone D.S., Spiegelman B.M., Mortensen R.M. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell 1999, 4:611-617.
51. Ruzzin J., Petersen R., Meugnier E., Madsen L., Lock E.J., Lillefosse H., Ma T., Pesenti S., Sonne S.B., Marstrand T.T., Malde M.K., Du Z.Y., Chavey C., Fajas L., Lundebye A.K., Brand C.L., Vidal H., Kristiansen K., Froyland L. Persistent organic pollutant exposure leads to insulin resistance syndrome. Environ. Health Perspect. 2010, 118:465-471.
52. Safe S.H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit. Rev. Toxicol. 1994, 24:87-149.
53. Safe S., Wang F., Porter W., Duan R., McDougal A. Ah receptor agonists as endocrine disruptors: antiestrogenic activity and mechanisms. Toxicol. Lett. 1998, 102-103:343-347.
54. Shimba S., Wada T., Tezuka M. Arylhydrocarbon receptor (AhR) is involved in negative regulation of adipose differentiation in 3T3-L1 cells: AhR inhibits adipose differentiation independently of dioxin. J. Cell Sci. 2001, 114:2809-2817.
55. Silverstone A.E., Rosenbaum P.F., Weinstock R.S., Bartell S.M., Foushee H.R., Shelton C., Pavuk M. Polychlorinated biphenyl (PCB) exposure and diabetes: results from the Anniston Community Health Survey. Environ. Health Perspect. 2012, 120:727-732.
56. Spalding K.L., Arner E., Westermark P.O., Bernard S., Buchholz B.A., Bergmann O., Blomqvist L., Hoffstedt J., Naslund E., Britton T., Concha H., Hassan M., Ryden M., Frisen J., Arner P. Dynamics of fat cell turnover in humans. Nature 2008, 453:783-787.
57. Tang Q.Q., Lane M.D. Adipogenesis: from stem cell to adipocyte. Annu. Rev. Biochem. 2012, 81:715-736.
58. Tang-Peronard J.L., Andersen H.R., Jensen T.K., Heitmann B.L. Endocrine-disrupting chemicals and obesity development in humans: a review. Obes. Rev. 2011, 12:622-636.
59. Taura D., Noguchi M., Sone M., Hosoda K., Mori E., Okada Y., Takahashi K., Homma K., Oyamada N., Inuzuka M., Sonoyama T., Ebihara K., Tamura N., Itoh H., Suemori H., Nakatsuji N., Okano H., Yamanaka S., Nakao K. Adipogenic differentiation of human induced pluripotent stem cells: comparison with that of human embryonic stem cells. FEBS Lett. 2009, 583:1029-1033.
60. Taxvig C., Dreisig K., Boberg J., Nellemann C., Schelde A.B., Pedersen D., Boergesen M., Mandrup S., Vinggaard A.M. Differential effects of environmental chemicals and food contaminants on adipogenesis, biomarker release and PPARgamma activation. Mol. Cell. Endocrinol. 2012, 361:106-115.
61. Tchkonia T., Morbeck D.E., Von Zglinicki T., Van Deursen J., Lustgarten J., Scrable H., Khosla S., Jensen M.D., Kirkland J.L. Fat tissue, aging, and cellular senescence. Aging Cell 2010, 9:667-684.
62. Terai M., Uyama T., Sugiki T., Li X.K., Umezawa A., Kiyono T. Immortalization of human fetal cells: the life span of umbilical cord blood-derived cells can be prolonged without manipulating p16INK4a/RB braking pathway. Mol. Biol. Cell 2005, 16:1491-1499.
63. Thayer K.A., Heindel J.J., Bucher J.R., Gallo M.A. Role of environmental chemicals in diabetes and obesity: a National Toxicology Program workshop review. Environ. Health Perspect. 2012, 120:779-789.
64. Tontonoz P., Spiegelman B.M. Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 2008, 77:289-312.
65. Uemura H., Arisawa K., Hiyoshi M., Kitayama A., Takami H., Sawachika F., Dakeshita S., Nii K., Satoh H., Sumiyoshi Y., Morinaga K., Kodama K., Suzuki T., Nagai M. Prevalence of metabolic syndrome associated with body burden levels of dioxin and related compounds among Japan's general population. Environ. Health Perspect. 2009, 117:568-573.
66. Vu B.G., Gourronc F.A., Bernlohr D.A., Schlievert P.M., Klingelhutz A.J. Staphylococcal superantigens stimulate immortalized human adipocytes to produce chemokines. PLoS ONE 2013, 8:e77988.
67. Ward E.M., Schulte P.A., Straif K., Hopf N.B., Caldwell J.C., Carreon T., DeMarini D.M., Fowler B.A., Goldstein B.D., Hemminki K., Hines C.J., Pursiainen K.H., Kuempel E., Lewtas J., Lunn R.M., Lynge E., McElvenny D.M., Muhle H., Nakajima T., Robertson L.W., Rothman N., Ruder A.M., Schubauer-Berigan M.K., Siemiatycki J., Silverman D., Smith M.T., Sorahan T., Steenland K., Stevens R.G., Vineis P., Zahm S.H., Zeise L., Cogliano V.J. Research recommendations for selected IARC-classified agents. Environ. Health Perspect. 2010, 118:1355-1362.
68. Ye R., Scherer P.E. Adiponectin, driver or passenger on the road to insulin sensitivity?. Mol. Metab. 2013, 2:133-141.
69. Zhang X., Soda Y., Takahashi K., Bai Y., Mitsuru A., Igura K., Satoh H., Yamaguchi S., Tani K., Tojo A., Takahashi T.A. Successful immortalization of mesenchymal progenitor cells derived from human placenta and the differentiation abilities of immortalized cells. Biochem. Biophys. Res. Commun. 2006, 351:853-859.