Dose-dependent metabolic reprogramming and differential gene expression in TCDD-elicited hepatic fibrosis

Toxicological Sciences

Volumn 154, Issue 2, 2016, Pages 253-266

  Nault, Rance ^a,b   Fader, Kelly A ^a,b   Ammendolia, Dustin A ^a   Dornbos, Peter ^a,b   Potter, Dave ^c   Sharratt, Bonnie ^c   Kumagai, Kazuyoshi ^b   Harkema, Jack R ^b   Lunt, Sophia Y ^a   Matthews, Jason ^d   Zacharewski, Tim ^a,b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c Canada N1G 3M5   (Canada)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

AhR; Matrisome; Metabolomic; NAFLD; RNA Seq

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; ALANINE; ASCORBIC ACID; ASPARTIC ACID; COLLAGEN; ELASTIN; GAMMA INTERFERON; GLUCOKINASE; GLUCOSE; GLUCOSE TRANSPORTER 2; GLUCURONIC ACID; GLUTAMIC ACID; GLYCOGEN PHOSPHORYLASE; HEAT SHOCK PROTEIN 47; HYDROXYPROLINE; HYDROXYPYRUVATE REDUCTASE; INTERLEUKIN 10; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 6; MESSENGER RNA; NERVE CELL ADHESION MOLECULE; OSTEOPONTIN; PROLINE; PROTEIN LYSINE 6 OXIDASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; RNA; TUMOR NECROSIS FACTOR; VIMENTIN; AUTACOID; CYTOKINE; GLYCOGEN; POLYCHLORINATED DIBENZODIOXIN; TRANSCRIPTOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOSYNTHESIS; CELL ACTIVATION; CITRIC ACID CYCLE; COMPARATIVE STUDY; CONTROLLED STUDY; CROSS LINKING; DISEASE SEVERITY; EXTRACELLULAR MATRIX; FATTY LIVER; FEMALE; FOOD INTAKE; GENE EXPRESSION; GLUCONEOGENESIS; GLUCOSE TOLERANCE; GLYCOGEN LIVER LEVEL; GLYCOGEN METABOLISM; GLYCOLYSIS; HEPATITIS; HISTOPATHOLOGY; HYDROXYLATION; LIPID STORAGE; LIQUID CHROMATOGRAPHY-MASS SPECTROMETRY; LIVER FIBROSIS; LIVER TISSUE; METABOLOMICS; MOUSE; MYOFIBROBLAST; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; QUANTITATIVE ANALYSIS; RNA SEQUENCE; TISSUE LEVEL; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; ENERGY METABOLISM; GENE EXPRESSION REGULATION; GENETICS; LIVER; LIVER CIRRHOSIS; METABOLISM; NONALCOHOLIC FATTY LIVER; NUCLEAR REPROGRAMMING; PATHOLOGY; TIME FACTOR; TOXIC HEPATITIS;

ANIMALS; ASCORBIC ACID; CELLULAR REPROGRAMMING; CHEMICAL AND DRUG INDUCED LIVER INJURY; COLLAGEN; CYTOKINES; DOSE-RESPONSE RELATIONSHIP, DRUG; ENERGY METABOLISM; EXTRACELLULAR MATRIX; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE; GLYCOGEN; INFLAMMATION MEDIATORS; LIVER; LIVER CIRRHOSIS; MICE, INBRED C57BL; NON-ALCOHOLIC FATTY LIVER DISEASE; POLYCHLORINATED DIBENZODIOXINS; PROLINE; TIME FACTORS; TRANSCRIPTOME;

EID: 85013766988     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfw163     Document Type: Article

References (55)

1. Ahmed, S., Bott, D., Gomez, A., Tamblyn, L., Rasheed, A., Cho, T., MacPherson, L., Sugamori, K. S., Yang, Y., Grant, D. M., et al. (2015). Loss of the mono-ADP-ribosyltransferase, Tiparp, increases sensitivity to dioxin-induced steatohepatitis and lethality. J. Biol. Chem. 290, 16824-16840
2. Baffy, G., Brunt, E. M., and Caldwell, S. H. (2012). Hepatocellular carcinoma in non-alcoholic fatty liver disease: An emerging menace. J. Hepatol. 56, 1384-1391
3. Barbul, A. (2008). Proline precursors to sustain Mammalian collagen synthesis. J. Nutr. 138, 2021S-2024S
4. Braun, L., Csala, M., Poussu, A., Garzo, T., Mandl, J., and Banhegyi, G. (1996). Glutathione depletion induces glycogenolysis dependent ascorbate synthesis in isolated murine hepatocytes. FEBS Lett. 388, 173-176
5. Brenner, D. A., Kisseleva, T., Scholten, D., Paik, Y. H., Iwaisako, K., Inokuchi, S., Schnabl, B., Seki, E., De Minicis, S., Oesterreicher, C., et al. (2012). Origin of myofibroblasts in liver fibrosis. Fibrogenesis Tissue Repair 5(Suppl 1), S17
6. Brenner, D. A., Paik, Y. H., and Schnabl, B. (2015). Role of gut microbiota in liver disease. J. Clinical Gastroenterol. 49(Suppl 1), S25-S27
7. Chen, Y., Choi, S. S., Michelotti, G.A., Chan, I. S., Swiderska-Syn, M., Karaca, G. F., Xie, G., Moylan, C. A., Garibaldi, F., Premont, R., et al. (2012). Hedgehog controls hepatic stellate cell fate by regulating metabolism. Gastroenterology 143, 1319-1329.e1-11
8. Cheng, X., Vispute, S. G., Liu, J., Cheng, C., Kharitonenkov, A., and Klaassen, C. D. (2014). Fibroblast growth factor (Fgf) 21 is a novel target gene of the aryl hydrocarbon receptor (AhR). Toxicol. Appl. Pharmacol. 278(1), 65-71
9. Clasquin, M. F., Melamud, E., and Rabinowitz, J. D. (2012). LC-MS data processing with MAVEN: A metabolomic analysis and visualization engine. Curr. Protoc. Bioinformatics. Chapter 14, Unit14 11
10. De Tullio, M. C. (2012). Beyond the antioxidant: The double life of vitamin C. Subcell. Biochem. 56, 49-65
11. Dere, E., Lo, R., Celius, T., Matthews, J., and Zacharewski, T. R. (2011). Integration of genome-wide computation DRE search, AhR ChIP-chip and gene expression analyses of TCDDelicited responses in the mouse liver. BMC Genomics 12, 365
12. Dranoff, J. A., and Wells, R. G. (2010). Portal fibroblasts: Underappreciated mediators of biliary fibrosis. Hepatology 51, 1438-1444
13. Fader, K. A., Nault, R., Ammendolia, D. A., Harkema, J. R., Williams, K. J., Crawford, R. B., Kaminski, N. E., Potter, D., Sharratt, B., and Zacharewski, T. R. (2015). 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin alters lipid metabolism and depletes immune cell populations in the Jejunum of C57BL/6 mice. Toxicol. Sci. 148, 567-580
14. Fernandez-Salguero, P. M., Hilbert, D. M., Rudikoff, S., Ward, J. M., and Gonzalez, F. J. (1996). Aryl-hydrocarbon receptordeficient mice are resistant to 2, 3, 7, 8-tetrachlorodibenzo-pdioxin-induced toxicity. Toxicol. Appl. Pharmacol. 140, 173-179
15. Frantz, C., Stewart, K. M., and Weaver, V. M. (2010). The extracellular matrix at a glance. J. Cell Sci. 123, 4195-4200
16. Girer, N.G., Murray, I.A., Omiecinski, C. J., and Perdew, G. H. (2016). Hepatic aryl hydrocarbon receptor attenuates fibroblast growth factor 21 expression. J. Biol. Chem. 291(29), 15378-15387
17. Glaser, S. S., Gaudio, E., Miller, T., Alvaro, D., and Alpini, G. (2009). Cholangiocyte proliferation and liver fibrosis. Expert Rev. Mol. Med. 11, e7
18. Harvey, W. A., Jurgensen, K., Pu, X., Lamb, C. L., Cornell, K. A., Clark, R. J., Klocke, C., and Mitchell, K. A. (2016). Exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) increases human hepatic stellate cell activation. Toxicology 344-346, 26-33
19. Hassan, M. Q., Mohammadpour, H., Hermansky, S. J., Murray, W. J., and Stohs, S. J. (1987). Comparative effects of BHA and ascorbic acid on the toxicity of 2, 3, 7, 8-tetrachlorodibenzo-pdioxin (TCDD) in rats. Gen. Pharmacol. 18, 547-550
20. He, J., Hu, B., Shi, X., Weidert, E. R., Lu, P., Xu, M., Huang, M., Kelley, E. E., and Xie, W. (2013). Activation of the aryl hydrocarbon receptor sensitizes mice to nonalcoholic steatohepatitis by deactivating mitochondrial sirtuin deacetylase Sirt3. Mol. Cell. Biol. 33, 2047-2055
21. Huang, G., and Elferink, C. J. (2012). A novel nonconsensus xenobiotic response element capable of mediating aryl hydrocarbon receptor-dependent gene expression. Mol. Pharmacol. 81, 338-347
22. Jiang, J., Johnson, L. C., Knight, J., Callahan, M. F., Riedel, T. J., Holmes, R. P., and Lowther, W. T. (2012). Metabolism of [13C5]hydroxyproline in vitro and in vivo: Implications for primary hyperoxaluria. Am. J. Physiol. Gastrointest. Liver pPhysiol. 302, G637-G643
23. Kalluri, R., and Weinberg, R. A. (2009). The basics of epithelialmesenchymal transition. J. Clin. Invest. 119, 1420-1428
24. Katayama, A., Nakatsuka, A., Eguchi, J., Murakami, K., Teshigawara, S., Kanzaki, M., Nunoue, T., Hida, K., Wada, N., Yasunaka, T., et al. (2015). Beneficial impact of Gpnmb and its significance as a biomarker in nonalcoholic steatohepatitis. Sci. Rep. 5, 16920
25. Keppler, D., and Decker, K. (1974). Glycogen determination with amyloglucosidase. In Methods of enzymatic analysis, pp. 1127-1131. Academic Press, New York
26. Kopec, A. K., Boverhof, D. R., Nault, R., Harkema, J. R., Tashiro, C., Potter, D., Sharratt, B., Chittim, B., and Zacharewski, T. R. (2013). Toxicogenomic evaluation of long-term hepatic effects of TCDD in immature, ovariectomized C57BL/6 mice. Toxicol. Sci. 135, 465-475
27. Lamouille, S., Xu, J., and Derynck, R. (2014). Molecular mechanisms of epithelial-mesenchymal transition. Nat. Rev. Mol. Cell Biol. 15, 178-196
28. Lee, J. H., Wada, T., Febbraio, M., He, J., Matsubara, T., Lee, M. J., Gonzalez, F. J., and Xie, W. (2010). A novel role for the dioxin receptor in fatty acid metabolism and hepatic steatosis. Gastroenterology 139, 653-663
29. Lin, Z., Tian, H., Lam, K. S., Lin, S., Hoo, R. C., Konishi, M., Itoh, N., Wang, Y., Bornstein, S. R., Xu, A., et al. (2013). Adiponectin mediates the metabolic effects of FGF21 on glucose homeostasis and insulin sensitivity in mice. Cell Metabolism 17, 779-789
30. Loskutoff, D. J., and Quigley, J. P. (2000). PAI-1, fibrosis, and the elusive provisional fibrin matrix. J. Clin. Invest. 106, 1441-1443
31. Lu, P., Yan, J., Liu, K., Garbacz, W. G., Wang, P., Xu, M., Ma, X., and Xie, W. (2015). Activation of aryl hydrocarbon receptor dissociates fatty liver from insulin resistance by inducing fibroblast growth factor 21. Hepatology 61, 1908-1919
32. Lunt, S. Y., Muralidhar, V., Hosios, A. M., Israelsen, W. J., Gui, D. Y., Newhouse, L., Ogrodzinski, M., Hecht, V., Xu, K., Acevedo, P. N., et al. (2015). Pyruvate kinase isoform expression alters nucleotide synthesis to impact cell proliferation. Mol. Cell. 57, 95-107
33. Morris, S. M. Jr. (2009). Recent advances in arginine metabolism: Roles and regulation of the arginases. Br. J. Pharmacol. 157, 922-930
34. Naba, A., Clauser, K. R., Ding, H., Whittaker, C. A., Carr, S. A., and Hynes, R. O. (2016). The extracellular matrix: Tools and insights for the "omics" era. Matrix Biol. 49, 10-24
35. Nault, R., Colbry, D., Brandenberger, C., Harkema, J. R., and Zacharewski, T. R. (2015a). Development of a computational high-throughput tool for the quantitative examination of dose-dependent histological features. Toxicol. Pathol. 43, 366-375
36. Nault, R., Fader, K. A., Kirby, M. P., Ahmed, S., Matthews, J., Jones, A. D., Lunt, S. Y., and Zacharewski, T. R. (2016). Pyruvate kinase isoform switching and hepatic metabolic reprogramming by the environmental contaminant 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Toxicol. Sci. 149, 358-371
37. Nault, R., Fader, K. A., and Zacharewski, T. (2015b). RNA-Seq versus oligonucleotide array assessment of dose-dependent TCDD-elicited hepatic gene expression in mice. BMC Genomics 16, 373
38. Omenetti, A., Syn, W. K., Jung, Y., Francis, H., Porrello, A., Witek, R. P., Choi, S. S., Yang, L., Mayo, M. J., Gershwin, M. E., et al. (2009). Repair-related activation of hedgehog signaling promotes cholangiocyte chemokine production. Hepatology 50, 518-527
39. Phang, J. M., Liu, W., Hancock, C. N., and Fischer, J. W. (2015). Proline metabolism and cancer: Emerging links to glutamine and collagen. Curr. Opin. Clin. Nutr. Metab. Care 18, 71-77
40. Pierre, S., Chevallier, A., Teixeira-Clerc, F., Ambolet-Camoit, A., Bui, L. C., Bats, A. S., Fournet, J. C., Fernandez-Salguero, P., Aggerbeck, M., Lotersztajn, S., et al. (2014). Aryl hydrocarbon receptor-dependent induction of liver fibrosis by dioxin. Toxicol. Sci. 137, 114-124
41. Ramezani-Moghadam, M., Wang, J., Ho, V., Iseli, T. J., Alzahrani, B., Xu, A., Van der Poorten, D., Qiao, L., George, J., and Hebbard, L. (2015). Adiponectin reduces hepatic stellate cell migration by promoting tissue inhibitor of metalloproteinase-1 (TIMP-1) secretion. J. Biol. Chem. 290, 5533-5542
42. Roberts, A. B., Kim, S. J., Noma, T., Glick, A. B., Lafyatis, R., Lechleider, R., Jakowlew, S. B., Geiser, A., O'Reilly, M. A., Danielpour, D. and., et al. (1991). Multiple forms of TGF-beta: Distinct promoters and differential expression. Ciba Found. Symp. 157, 7-15; discussion 15-28
43. Roca, H., Hernandez, J., Weidner, S., McEachin, R. C., Fuller, D., Sud, S., Schumann, T., Wilkinson, J. E., Zaslavsky, A., Li, H., et al. (2013). Transcription factors OVol15402 and OVol15402 induce the mesenchymal to epithelial transition in human cancer. PLoS One 8, e76773
44. Syn, W. K., Jung, Y., Omenetti, A., Abdelmalek, M., Guy, C. D., Yang, L., Wang, J., Witek, R. P., Fearing, C. M., Pereira, T. A., et al. (2009). Hedgehog-mediated epithelial-to-mesenchymal transition and fibrogenic repair in nonalcoholic fatty liver disease. Gastroenterology 137, 1478-1488.e8
45. Takuma, M., Ushijima, K., Kumazaki, M., Ando, H., and Fujimura, A. (2015). Influence of dioxin on the daily variation of insulin sensitivity in mice. Environ. Toxicol. Pharmacol. 40, 349-351
46. Taylor, K. W., Novak, R. F., Anderson, H. A., Birnbaum, L. S., Blystone, C., Devito, M., Jacobs, D., Kohrle, J., Lee, D. H., Rylander, L., et al. (2013). Evaluation of the association between persistent organic pollutants (POPs) and diabetes in epidemiological studies: A national toxicology program workshop review. Environ. Health Perspect. 121, 774-783
47. Thomas, T., MacKenzie, S. A., and Gallo, M. A. (1990). Regulation of polyamine biosynthesis by 2, 3, 7, 8-tetrachlorodibenzo-pdioxin (TCDD). Toxicol. Lett. 53, 315-325
48. Van Gool, B., Dedieu, S., Emonard, H., and Roebroek, A. J. (2015). The matricellular receptor LRP1 forms an interface for signaling and endocytosis in modulation of the extracellular tumor environment. Front. Pharmacol. 6, 271
49. Weng, H., Mertens, P. R., Gressner, A. M., and Dooley, S. (2007). IFN-gamma abrogates profibrogenic TGF-beta signaling in liver by targeting expression of inhibitory and receptor Smads. J. Hepatol. 46, 295-303
50. Wight, T. N., and Potter-Perigo, S. (2011). The extracellular matrix: An active or passive player in fibrosis? Am. J. Physiol. Gastrointest. Liver Physiol. 301, G950-G955
51. Xia, J., and Wishart, D. S. (2010). MetPA: A web-based metabolomics tool for pathway analysis and visualization. Bioinformatics 26, 2342-2344
52. Yao, L., Wang, C., Zhang, X., Peng, L., Liu, W., Liu, Y., He, J., Jiang, C., Ai, D., and Zhu, Y. (2016). Hyperhomocysteinemia activates the aryl hydrocarbon receptor/CD36 pathway to promote hepatic steatosis in mice. Hepatology 64, 92-105
53. Yeager, R. L., Reisman, S. A., Aleksunes, L. M., and Klaassen, C. D. (2009). Introducing the "TCDD-inducible AhR-Nrf2 gene battery". Toxicol. Sci. 111, 238-246
54. Yoshiji, H., Kuriyama, S., Miyamoto, Y., Thorgeirsson, U. P., Gomez, D. E., Kawata, M., Yoshii, J., Ikenaka, Y., Noguchi, R., Tsujinoue, H., et al. (2000). Tissue inhibitor of metalloproteinases-1 promotes liver fibrosis development in a transgenic mouse model. Hepatology 32, 1248-1254
55. Zhang, L., Nichols, R. G., Correll, J., Murray, I. A., Tanaka, N., Smith, P. B., Hubbard, T. D., Sebastian, A., Albert, I., Hatzakis, E., et al. (2015). Persistent organic pollutants modify gut microbiota-host metabolic homeostasis in mice through aryl hydrocarbon receptor activation. Environ. Health Perspect. 123, 679-688