Fibroblast growth factor (Fgf) 21 is a novel target gene of the aryl hydrocarbon receptor (AhR)

Toxicology and Applied Pharmacology

Volumn 278, Issue 1, 2014, Pages 65-71

  Cheng, Xingguo ^a   Vispute, Saurabh G ^a   Liu, Jie ^b   Cheng, Christine ^c   Kharitonenkov, Alexei ^c   Klaassen, Curtis D ^b  

^a ST JOHN'S UNIVERSITY   (United States)

^b UNIVERSITY OF KANSAS SCHOOL OF MEDICINE   (United States)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

AhR; DEHP; Fgf21; Liver; TCDD; White adipose tissue

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR; FIBROBLAST GROWTH FACTOR 21; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; IN VITRO STUDY; LIPID OXIDATION; LIVER; LIVER CELL; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN EXPRESSION; WHITE ADIPOSE TISSUE; WILD TYPE;

AHR; DEHP; FGF21; LIVER; TCDD; WHITE ADIPOSE TISSUE;

ADIPOSE TISSUE, WHITE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BINDING SITES; CELL LINE; DIETHYLHEXYL PHTHALATE; DOSE-RESPONSE RELATIONSHIP, DRUG; FIBROBLAST GROWTH FACTORS; HEPATOCYTES; HUMANS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN; TIME FACTORS; UP-REGULATION;

EID: 84899893219     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2014.04.013     Document Type: Article

References (38)

1. Adams A.C., Kharitonenkov A. FGF21: the center of a transcriptional nexus in metabolic regulation. Curr. Diabetes Rev. 2012, 8:285-293.
2. Adams A.C., Coskun T., Cheng C.C., LS O.F., Dubois S.L., Kharitonenkov A. Fibroblast growth factor 21 is not required for the antidiabetic actions of the thiazoladinediones. Mol. Metab. 2013, 2:205-214.
3. Amakura Y., Tsutsumi T., Sasaki K., Nakamura M., Yoshida T., Maitani T. Influence of food polyphenols on aryl hydrocarbon receptor-signaling pathway estimated by in vitro bioassay. Phytochemistry 2008, 69:3117-3130.
4. Anwar-Mohamed A., El-Kadi A.O. Sulforaphane induces CYP1A1 mRNA, protein, and catalytic activity levels via an AhR-dependent pathway in murine hepatoma Hepa 1c1c7 and human HepG2 cells. Cancer Lett. 2009, 275:93-101.
5. Badman M.K., Pissios P., Kennedy A.R., Koukos G., Flier J.S., Maratos-Flier E. Hepatic fibroblast growth factor 21 is regulated by PPARalpha and is a key mediator of hepatic lipid metabolism in ketotic states. Cell Metab. 2007, 5:426-437.
6. Beenken A., Mohammadi M. The FGF family: biology, pathophysiology and therapy. Nat. Rev. Drug Discov. 2009, 8:235-253.
7. Berglund E.D., Li C.Y., Bina H.A., Lynes S.E., Michael M.D., Shanafelt A.B., Kharitonenkov A., Wasserman D.H. Fibroblast growth factor 21 controls glycemia via regulation of hepatic glucose flux and insulin sensitivity. Endocrinology 2009, 150:4084-4093.
8. Cheng X., Maher J., Dieter M.Z., Klaassen C.D. Regulation of mouse organic anion-transporting polypeptides (Oatps) in liver by prototypical microsomal enzyme inducers that activate distinct transcription factor pathways. Drug Metab. Dispos. 2005, 33:1276-1282.
9. Croutch C.R., Lebofsky M., Schramm K.W., Terranova P.F., Rozman K.K. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin (HxCDD) alter body weight by decreasing insulin-like growth factor I (IGF-I) signaling. Toxicol. Sci. 2005, 85:560-571.
10. Ding X., Lichti K., Kim I., Gonzalez F.J., Staudinger J.L. Regulation of constitutive androstane receptor and its target genes by fasting, cAMP, hepatocyte nuclear factor alpha, and the coactivator peroxisome proliferator-activated receptor gamma coactivator-1alpha. J. Biol. Chem. 2006, 281:26540-26551.
11. Fon Tacer K., Bookout A.L., Ding X., Kurosu H., John G.B., Wang L., Goetz R., Mohammadi M., Kuro-o M., Mangelsdorf D.J., Kliewer S.A. Research resource: comprehensive expression atlas of the fibroblast growth factor system in adult mouse. Mol. Endocrinol. 2010, 24:2050-2064.
12. Fried K.W., Schneider C.M., Schramm K.W., Datta A., Chahbane N., Corsten C., Powell D.R., Lenoir D., Kettrup A., Terranova P., Georg G.I., Rozman K.K. From dioxin to drug lead-the development of 2,3,7,8-tetrachlorophenothiazine. Chem. Med. Chem. 2007, 2:890-897.
13. Galman C., Lundasen T., Kharitonenkov A., Bina H.A., Eriksson M., Hafstrom I., Dahlin M., Amark P., Angelin B., Rudling M. The circulating metabolic regulator FGF21 is induced by prolonged fasting and PPARalpha activation in man. Cell Metab. 2008, 8:169-174.
14. IARC IARC monographs on the evaluation of carcinogenic risks to humans. Vol 69: Polychlorinated Dibenzo-para-dioxins and Polychlorinated Dibenzofurans 1997, International Agency for Research on Cancer.
15. Inagaki T., Dutchak P., Zhao G., Ding X., Gautron L., Parameswara V., Li Y., Goetz R., Mohammadi M., Esser V., Elmquist J.K., Gerard R.D., Burgess S.C., Hammer R.E., Mangelsdorf D.J., Kliewer S.A. Endocrine regulation of the fasting response by PPARalpha-mediated induction of fibroblast growth factor 21. Cell Metab. 2007, 5:415-425.
16. Inagaki T., Lin V.Y., Goetz R., Mohammadi M., Mangelsdorf D.J., Kliewer S.A. Inhibition of growth hormone signaling by the fasting-induced hormone FGF21. Cell Metab. 2008, 8:77-83.
17. Izumiya Y., Bina H.A., Ouchi N., Akasaki Y., Kharitonenkov A., Walsh K. FGF21 is an Akt-regulated myokine. FEBS Lett. 2008, 582:3805-3810.
18. Kharitonenkov A., Shiyanova T.L., Koester A., Ford A.M., Micanovic R., Galbreath E.J., Sandusky G.E., Hammond L.J., Moyers J.S., Owens R.A., Gromada J., Brozinick J.T., Hawkins E.D., Wroblewski V.J., Li D.S., Mehrbod F., Jaskunas S.R., Shanafelt A.B. FGF-21 as a novel metabolic regulator. J. Clin. Invest. 2005, 115:1627-1635.
19. Kharitonenkov A., Wroblewski V.J., Koester A., Chen Y.F., Clutinger C.K., Tigno X.T., Hansen B.C., Shanafelt A.B., Etgen G.J. The metabolic state of diabetic monkeys is regulated by fibroblast growth factor-21. Endocrinology 2007, 148:774-781.
20. Kociba R.J., Keyes D.G., Beyer J.E., Carreon R.M., Wade C.E., Dittenber D.A., Kalnins R.P., Frauson L.E., Park C.N., Barnard S.D., Hummel R.A., Humiston C.G. Results of a two-year chronic toxicity and oncogenicity study of 2,3,7,8-tetrachlorodibenzo-p-dioxin in rats. Toxicol. Appl. Pharmacol. 1978, 46:279-303.
21. Lakshman M.R., Ghosh P., Chirtel S.J. Mechanism of action of 2,3,7,8-tetrachlorodibenzo-p-dioxin on intermediary metabolism in the rat. J. Pharmacol. Exp. Ther. 1991, 258:317-319.
22. Loaiza-Perez A.I., Kenney S., Boswell J., Hollingshead M., Alley M.C., Hose C., Ciolino H.P., Yeh G.C., Trepel J.B., Vistica D.T., Sausville E.A. Aryl hydrocarbon receptor activation of an antitumor aminoflavone: basis of selective toxicity for MCF-7 breast tumor cells. Mol. Cancer Ther. 2004, 3:715-725.
23. Lundasen T., Hunt M.C., Nilsson L.M., Sanyal S., Angelin B., Alexson S.E., Rudling M. PPARalpha is a key regulator of hepatic FGF21. Biochem. Biophys. Res. Commun. 2007, 360:437-440.
24. McLane K.E., Whitlock J.P. DNA sequence requirements for Ah receptor/Arnt recognition determined by in vitro transcription. Receptor 1994, 4:209-222.
25. Moyers J.S., Shiyanova T.L., Mehrbod F., Dunbar J.D., Noblitt T.W., Otto K.A., Reifel-Miller A., Kharitonenkov A. Molecular determinants of FGF-21 activity-synergy and cross-talk with PPARgamma signaling. J. Cell. Physiol. 2007, 210:1-6.
26. Muise E.S., Azzolina B., Kuo D.W., El-Sherbeini M., Tan Y., Yuan X., Mu J., Thompson J.R., Berger J.P., Wong K.K. Adipose fibroblast growth factor 21 is up-regulated by peroxisome proliferator-activated receptor gamma and altered metabolic states. Mol. Pharmacol. 2008, 74:403-412.
27. Nishimura T., Nakatake Y., Konishi M., Itoh N. Identification of a novel FGF, FGF-21, preferentially expressed in the liver. Biochim. Biophys. Acta 2000, 1492:203-206.
28. Petrick J.S., Klaassen C.D. Importance of hepatic induction of constitutive androstane receptor and other transcription factors that regulate xenobiotic metabolism and transport. Drug Metab. Dispos. 2007, 35:1806-1815.
29. Potthoff M.J., Inagaki T., Satapati S., Ding X., He T., Goetz R., Mohammadi M., Finck B.N., Mangelsdorf D.J., Kliewer S.A., Burgess S.C. FGF21 induces PGC-1{alpha} and regulates carbohydrate and fatty acid metabolism during the adaptive starvation response. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:10853-10858.
30. Schmidt J.V., Su G.H., Reddy J.K., Simon M.C., Bradfield C.A. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc. Natl. Acad. Sci. U. S. A. 1996, 93:6731-6736.
31. Suzuki M., Uehara Y., Motomura-Matsuzaka K., Oki J., Koyama Y., Kimura M., Asada M., Komi-Kuramochi A., Oka S., Imamura T. betaKlotho is required for fibroblast growth factor (FGF) 21 signaling through FGF receptor (FGFR) 1c and FGFR3c. Mol. Endocrinol. 2008, 22:1006-1014.
32. Tijet N., Boutros P.C., Moffat I.D., Okey A.B., Tuomisto J., Pohjanvirta R. Aryl hydrocarbon receptor regulates distinct dioxin-dependent and dioxin-independent gene batteries. Mol. Pharmacol. 2006, 69:140-153.
33. Tomaszewski K.E., Montgomery C.A., Melnick R.L. Modulation of 2,3,7,8-tetrachlorodibenzo-p-dioxin toxicity in F344 rats by di(2-ethylhexyl)phthalate. Chem. Biol. Interact. 1988, 65:205-222.
34. Wang H., Qiang L., Farmer S.R. Identification of a domain within peroxisome proliferator-activated receptor gamma regulating expression of a group of genes containing fibroblast growth factor 21 that are selectively repressed by SIRT1 in adipocytes. Mol. Cell. Biol. 2008, 28:188-200.
35. Ward J.M., Peters J.M., Perella C.M., Gonzalez F.J. Receptor and nonreceptor-mediated organ-specific toxicity of di(2-ethylhexyl)phthalate (DEHP) in peroxisome proliferator-activated receptor alpha-null mice. Toxicol. Pathol. 1998, 26:240-246.
36. Wente W., Efanov A.M., Brenner M., Kharitonenkov A., Koster A., Sandusky G.E., Sewing S., Treinies I., Zitzer H., Gromada J. Fibroblast growth factor-21 improves pancreatic beta-cell function and survival by activation of extracellular signal-regulated kinase 1/2 and Akt signaling pathways. Diabetes 2006, 55:2470-2478.
37. Whitlock J.P. Genetic and molecular aspects of 2,3,7,8-tetrachlorodibenzo-p-dioxin action. Annu. Rev. Pharmacol. Toxicol. 1990, 30:251-277.
38. Xu J., Stanislaus S., Chinookoswong N., Lau Y.Y., Hager T., Patel J., Ge H., Weiszmann J., Lu S.C., Graham M., Busby J., Hecht R., Li Y.S., Li Y., Lindberg R., Veniant M.M. Acute glucose-lowering and insulin-sensitizing action of FGF21 in insulin-resistant mouse models-association with liver and adipose tissue effects. Am. J. Physiol. Endocrinol. Metab. 2009, 297:E1105-E1114.