Persistent organic pollutants modify gut microbiota–host metabolic homeostasis in mice through aryl hydrocarbon receptor activation

Environmental Health Perspectives

Volumn 123, Issue 7, 2015, Pages 679-688

  Zhang, Limin ^a,b   Nichols, Robert G ^a   Correll, Jared ^a   Murray, Iain A ^a   Tanaka, Naoki ^c   Smith, Philip B ^a   Hubbard, Troy D ^a   Sebastian, Aswathy ^a   Albert, Istvan ^a   Hatzakis, Emmanuel ^a   Gonzalez, Frank J ^c   Perdew, Gary H ^a   Patterson, Andrew D ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^c NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZOFURAN; ALANINE AMINOTRANSFERASE; ALKALINE PHOSPHATASE; AMINO ACID; AROMATIC HYDROCARBON RECEPTOR; BILE ACID; FARNESOID X RECEPTOR; GLUCOSE; GLYCOGEN; IMMUNOGLOBULIN A; INTERLEUKIN 10; INTERLEUKIN 1BETA; LIPID; LIPOPOLYSACCHARIDE; MESSENGER RNA; MYOSIN VB; PEPTIDES AND PROTEINS; PHOSPHATIDYLCHOLINE; RECEPTOR; RNA 16S; SERUM AMYLOID PROTEIN A1; SERUM AMYLOID PROTEIN A3; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNSATURATED FATTY ACID; 2,3,7,8-TETRACHLORODIBENZOFURAN; BENZOFURAN DERIVATIVE; CELL RECEPTOR; FARNESOID X-ACTIVATED RECEPTOR; POLLUTANT;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BUTYRIVIBRIO; CONTROLLED STUDY; DIET; ENTERITIS; FECES ANALYSIS; FERMENTATION; GENE EXPRESSION; GENE SEQUENCE; GLUCONEOGENESIS; GLYCOGENOLYSIS; GRAM NEGATIVE ANAEROBIC BACTERIA; HISTOPATHOLOGY; IMMUNE RESPONSE; INTESTINE FLORA; INTRACELLULAR SIGNALING; LACTATE BLOOD LEVEL; LIPOGENESIS; MALE; METABOLIC DISORDER; METABOLISM; METABOLOMICS; MOUSE; NONHUMAN; OSCILLOBACTER; PERSISTENT ORGANIC POLLUTANT; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; QUADRUPOLE MASS SPECTROMETRY; REAL TIME POLYMERASE CHAIN REACTION; RNA EXTRACTION; SCANNING ELECTRON MICROSCOPY; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GASTROINTESTINAL TRACT; GENETICS; HOMEOSTASIS; KNOCKOUT MOUSE; LIVER; MICROBIOLOGY; MICROFLORA; POLLUTANT; SIGNAL TRANSDUCTION; TOXICITY;

BACTERIA (MICROORGANISMS); BACTEROIDETES; BUTYRIVIBRIO; FIRMICUTES; MUS;

ANIMALS; BENZOFURANS; BILE ACIDS AND SALTS; DIET; ENVIRONMENTAL POLLUTANTS; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HOMEOSTASIS; LIVER; MALE; METABOLOMICS; MICE, INBRED C57BL; MICE, KNOCKOUT; MICROBIOTA; RECEPTORS, ARYL HYDROCARBON; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RNA, RIBOSOMAL, 16S; SIGNAL TRANSDUCTION;

EID: 84936159079     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1409055     Document Type: Article

References (65)

1. Alaluusua S, Lukinmaa PL. 2006. Developmental dental toxicity of dioxin and related compounds—a review. Int J Dent 56:323–331.
2. Angrish MM, Dominici CY, Zacharewski TR. 2013. TCDD-elicited effects on liver, serum, and adipose lipid composition in C57BL/6 mice. Toxicol Sci 131:108–115.
3. Arsenescu V, Arsenescu RI, King V, Swanson H, Cassis LA. 2008. Polychlorinated biphenyl-77 induces adipocyte differentiation and proinfamma-tory adipokines and promotes obesity and atherosclerosis. Environ Health Perspect 116:761–768; doi:10.1289/ehp.10554.
4. Bitoun M, Tappaz M. 2000a. Gene expression of taurine transporter and taurine biosynthetic enzymes in brain of rats with acute or chronic hyperosmotic plasma. A comparative study with gene expression of myo-inositol transporter, betaine transporter and sorbitol biosynthetic enzyme. Brain Res Mol Brain Res 77:10–18.
5. Bitoun M, Tappaz M. 2000b. Gene expression of taurine transporter and taurine biosynthetic enzymes in hyperosmotic states: a comparative study with the expression of the genes involved in the accumulation of other osmolytes. Adv Exp Med Biol 483:239–248.
6. Bjeldanes LF, Kim JY, Grose KR, Bartholomew JC, Bradfield CA. 1991. Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc Natl Acad Sci USA 88:9543–9547.
7. Caselli M, Holton J, Boldrini P, Vaira D, Calò G. 2010. Morphology of segmented filamentous bacteria and their patterns of contact with the follicle-associated epithelium of the mouse terminal ileum. Gut Microbes 1:367–372.
8. Chan CC, Hwang SJ, Lee FY, Wang SS, Chang FY, Li CP, et al. 1997. Prognostic value of plasma endo-toxin levels in patients with cirrhosis. Scand J Gastroentero 32:942–946.
9. Chassaing B, Srinivasan G, Delgado MA, Young AN, Gewirtz AT, Vijay-Kumar M. 2012. Fecal lipocalin 2, a sensitive and broadly dynamic non-invasive biomarker for intestinal inflammation. PloS One 7:e44328; doi:10.1371/journal.pone.0044328.
10. Choi JJ, Eum SY, Rampersaud E, Daunert S, Abreu MT, Toborek M. 2013. Exercise attenuates PCB-induced changes in the mouse gut microbiome. Environ Health Perspect 121:725–730; doi:10.1289/ ehp.1306534.
11. Claudel T, Staels B, Kuipers F. 2005. The Farnesoid X receptor: a molecular link between bile acid and lipid and glucose metabolism. Arterioscler Thromb Vasc Biol 25:2020–2030.
12. Claus SP, Tsang TM, Wang Y, Cloarec O, Skordi E, Martin FP, et al. 2008. Systemic multicompartmental effects of the gut microbiome on mouse metabolic phenotypes. Mol Syst Biol 4:219; doi:10.1038/msb.2008.56.
13. Coen M, Lenz EM, Nicholson JK, Wilson ID, Pognan F, Lindon JC. 2003. An integrated metabonomic investigation of acetaminophen toxicity in the mouse using NMR spectroscopy. Chem Res Toxicol 16:295–303.
14. DeVito MJ, Birnbaum LS. 1995. The importance of pharmacokinetics in determining the relative potency of 2,3,7,8-tetrachlorodibenzo-p-dioxin and 2,3,7,8-tetrachlorodibenzofuran. Fundam Appl Toxicol 24:145–148.
15. Diani-Moore S, Ram P, Li X, Mondal P, Youn DY, Sauve AA, et al. 2010. Identification of the aryl hydrocarbon receptor target gene TiPARP as a mediator of suppression of hepatic gluconeo-genesis by 2,3,7,8-tetrachlorodibenzo-p-dioxin and of nicotinamide as a corrective agent for this effect. J Biol Chem 285:38801–38810.
16. DiNatale BC, Schroeder JC, Francey LJ, Kusnadi A, Perdew GH. 2010. Mechanistic insights into the events that lead to synergistic induction of inter-leukin 6 transcription upon activation of the aryl hydrocarbon receptor and infammatory signaling. J Biol Chem 285:24388–24397.
17. Folch BJ, Lees M, Sloane Stanley GH. 1957. A simple method for the isolation and purification of total lipides from animal tissues. J Biol Chem 226:497–509.
18. Greenblum S, Turnbaugh PJ, Borenstein E. 2012. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proc Natl Acad Sci USA 109:594–599.
19. Hautekiet V, Geert V, Marc V, Rony G. 2008. Development of a sanitary risk index for Salmonella seropreva-lence in Belgian pig farms. Prev Vet Med 86:75–92.
20. Hayashi H, Takada T, Suzuki H, Onuki R, Hofmann AF, Sugiyama Y. 2005. Transport by vesicles of glycine-and taurine-conjugated bile salts and taurolitho-cholate 3-sulfate: a comparison of human BSEP with rat Bsep. Biochim Biophys Acta 1738:54–62.
21. Hooper LV, Midtvedt T, Gordon JI. 2002. How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annu Rev Nutr 22:283–307.
22. Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. 2003. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 4:269–273.
23. Howell G III, Mangum L. 2011. Exposure to bioaccumu la-tive organochlorine compounds alters adipo genesis, fatty acid uptake, and adipokine production in NIH3T3-L1 cells. Toxicol In Vitro 25:394–402.
24. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, et al. 2009. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 139:485–498.
25. Jääskeläinen T, Paananen J, Lindström J, Eriksson JG, Tuomilehto J, Uusitupa M, et al. 2013. Genetic predisposition to obesity and lifestyle factors—the combined analyses of twenty-six known BMI- and fourteen known waist:hip ratio (WHR)-associated variants in the Finnish Diabetes Prevention Study. Br J Nutr 110:1856–1865.
26. Jiang C, Xie C, Li F, Zhang L, Nichols RG, Krausz KW, et al. 2015. Intestinal farnesoid X receptor signaling promotes nonalcoholic fatty liver disease. J Clin Invest 125:386–402.
27. Jin UH, Lee SO, Sridharan G, Lee K, Davidson LA, Jayaraman A, et al. 2014. Microbiome-derived tryptophan metabolites and their aryl hydrocarbon receptor-dependent agonist and antagonist activities. Mol Pharmacol 85:777–788.
28. Jones KC, Bennett BG. 1989. Human exposure to environmental polychlorinated dibenzo-p-dioxins and dibenzofurans: an exposure commitment assessment for 2,3,7,8-TCDD. Sci Total Environ 78:99–116.
29. Lee DH, Porta M, Jacobs DR, Vandenberg LN. 2014. Chlorinated persistent organic pollutants, obesity, and type 2 diabetes. Endocr Rev 35:557–601.
30. Li F, Jiang C, Krausz KW, Li Y, Albert I, Hao H, et al. 2013. Microbiome remodelling leads to inhibition of intestinal farnesoid X receptor signalling and decreased obesity. Nat Commun 4:2384; doi:10.1038/ncomms3384.
31. Lin RS, Lee FY, Lee SD, Tsai YT, Lin HC, Lu RH, et al. 1995. Endotoxemia in patients with chronic liver diseases: relationship to severity of liver diseases, presence of esophageal varices, and hyper-dynamic circulation. J Hepatol 22:165–172.
32. Macpherson AJ, Geuking MB, McCoy KD. 2012. Homeland security: IgA immunity at the frontiers of the body. Trends Immunol 33:160–167.
33. Maher JM, Cheng X, Slitt, AL, Dieter MZ, Klaassen CD. 2005. Induction of the multidrug resistance-associated protein family of transporters by chemical activators of receptor-mediated pathways in mouse liver. Drug Metab Dispos 33:956–962.
34. Marshall NB, Kerkvliet NI. 2010. Dioxin and immune regulation: emerging role of aryl hydrocarbon receptor in the generation of regulatory T cells. Ann NY Acad Sci 1183:25–37.
35. Mathis D, Benoist C. 2012. The infuence of the micro-biota on type-1 diabetes: on the threshold of a leap forward in our understanding. Immunol Rev 245:239–249.
36. Matsubara T, Tanaka N, Krausz KW, Manna SK, Kang DW, Anderson ER, et al. 2012. Metabolomics identifies an inflammatory cascade involved in dioxin- and diet-induced steatohepatitis. Cell Metab 16:634–644.
37. Maurice CF, Haiser HJ, Turnbaugh PJ. 2013. Xeno-biotics shape the physiology and gene expression of the active human gut microbiome. Cell 152:39–50.
38. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. 2005. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122:107–118.
39. Monteleone I, MacDonald TT, Pallone F, Monteleone G. 2012. The aryl hydrocarbon receptor in infamma-tory bowel disease: linking the environment to disease pathogenesis. Curr Opin Gastroenterol 28:310–313.
40. Monteleone I, Pallone F, Monteleone G. 2013. Aryl hydrocarbon receptor and colitis. Semin Immunopathol 35:671–675.
41. Myre M, Imbeault P. 2014. Persistent organic pollutants meet adipose tissue hypoxia: does cross-talk contribute to inflammation during obesity? Obes Rev 15:19–28.
42. Nagalingam NA, Lynch SV. 2012. Role of the micro-biota in inflammatory bowel diseases. Inflamm Bowel Dis 18:968–984.
43. Nakatani T, Yamamoto A, Ogaki S. 2011. A survey of dietary intake of plychlorinated dibenzo-p-dioxins, polychlorinated dibenzofurans, and dioxin-like coplanar poly chlorinated biphenyls from food during 2000–2002 in Osaka City, Japan. Arch Environ Contam Toxicol 60:543–555.
44. Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, et al. 2012. Host-gut microbiota metabolic interactions. Science 336:1262–1267.
45. Ozeki J, Uno S, Ogura M, Choi M, Maeda T, Sakurai K, et al. 2011. Aryl hydrocarbon receptor ligand 2,3,7,8-tetrachlorodibenzo-p-dioxin enhances liver damage in bile duct-ligated mice. Toxicology 280:10–17.
46. Peterson DA, McNulty NP, Guruge JL, Gordon JI. 2007. IgA response to symbiotic bacteria as a mediator of gut homeostasis. Cell Host Microbe 2:328–339.
47. Ren A, Qiu X, Jin L, Ma J, Li Z, Zhang L, et al. 2011. Association of selected persistent organic pollutants in the placenta with the risk of neural tube defects. Proc Natl Acad Sci USA 108:12770–12775.
48. Roche Diagnostics. 2013. Short Fragment Removal for the Amplicon Library Preparation Procedure. TCB No. 2011-007. Available: http://454.com/downloads/my454/documentation/technical-bulletins/TCB-11007_ShortFragmentRemovalProcedureAmplicon LibraryPrep_May2013.pdf [accessed 12 June 2015].
49. Russell JB. 1985. Fermentation of cellodextrins by cellulolytic and noncellulolytic rumen bacteria. Appl Environ Microbiol 49:572–576.
50. Said EA, Dupuy FP, Trautmann L, Zhang Y, Shi Y, El-Far M, et al. 2010. Programmed death-1-induced interleukin-10 production by monocytes impairs CD4+ T cell activation during HIV infection. Nat Med 16:452–459.
51. Sayin SI, Wahlström A, Felin J, Jäntti S, Marschall HU, Bamberg K, et al. 2013. Gut microbiota regulates bile acid metabolism by reducing the levels of tauro-beta-muricholic acid, a naturally occurring FXR antagonist. Cell Metab 17:225–235.
52. Schecter A, Startin J, Wright C, Kelly M, Päpke O, Lis A, et al. 1994. Congener-specific levels of dioxins and dibenzo furans in U.S. food and estimated daily dioxin toxic equivalent intake. Environ Health Perspect 102:962–966.
53. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541.
54. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, et al. 2010. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring) 18:190–195.
55. Snedeker SM, Hay AG. 2012. Do interactions between gut ecology and environmental chemicals contribute to obesity and diabetes? Environ Health Perspect 120:332–339; doi:10.1289/ehp.1104204.
56. Stappenbeck TS, Hooper LV, Gordon JI. 2002. Developmental regulation of intestinal angiogen-esis by indigenous microbes via Paneth cells. Proc Natl Acad Sci USA 99:15451–15455.
57. Tian Y, Zhang L, Wang Y, Tang H. 2012. Age-related topographical metabolic signatures for the rat gastro intestinal contents. J Proteome Res 11:1397–1411.
58. Tremaroli V, Bäckhed F. 2012. Functional interactions between the gut microbiota and host metabolism. Nature 489:242–249.
59. World Health Organization. 1998. Executive Summary: Assessment of the Health Risk of Dioxins: Re-Evaluation of the Tolerable Daily Intake (TDI). WHO Consultation, May 25–29 1998, Geneva, Switzerland. Geneva:WHO European Centre for Environment and Health, International Programme on Chemical Safety. Available: http://www.who.int/ipcs/publications/en/exe-sum-final.pdf [accessed 28 May 2015].
60. Wu JF, An YP, Yao JW, Wang YL, Tang HR. 2010. An optimised sample preparation method for NMR-based faecal metabonomic analysis. Analyst 135:1023–1030.
61. Xun L, Topp E, Orser CS. 1992. Glutathione is the reducing agent for the reductive dehalogenation of tetrachloro-p-hydroquinone by extracts from a Flavobacterium sp. Biochem Biophys Res Commun 182:361–366.
62. Yap IK, Clayton TA, Tang H, Everett JR, Hanton G, Provost JP, et al. 2006. An integrated metabonomic approach to describe temporal metabolic disregu-lation induced in the rat by the model hepatotoxin allyl formate. J Proteome Res 5:2675–2684.
63. Yoshimoto S, Loo TM, Atarashi K, Kanda H, Sato S, Oyadomari S, et al. 2013. Obesity-induced gut microbial metabolite promotes liver cancer through senescence secretome. Nature 499:97–101.
64. Zelante T, Iannitti RG, Cunha C, De Luca A, Giovannini G, Pieraccini G, et al. 2013. Tryptophan catabolites from microbiota engage aryl hydrocarbon receptor and balance mucosal reactivity via interleukin-22. Immunity 39:372–385.
65. Zhang L, Ye Y, An Y, Tian Y, Wang Y, Tang H. 2011. Systems responses of rats to afatoxin B1 expo sure revealed with metabonomic changes in multiple biological matrices. J Proteome Res 10:614–623.