Combinatorial pathway disruption is a powerful approach to delineate metabolic impacts of endocrine disruptors

. 2022 Dec ; 596 (24) : 3107-3123. [epub] 20220822

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, přehledy, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid35957500

The prevalence of metabolic diseases, such as obesity, diabetes, metabolic syndrome and chronic liver diseases among others, has been rising for several years. Epidemiology and mechanistic (in vivo, in vitro and in silico) toxicology have recently provided compelling evidence implicating the chemical environment in the pathogenesis of these diseases. In this review, we will describe the biological processes that contribute to the development of metabolic diseases targeted by metabolic disruptors, and will propose an integrated pathophysiological vision of their effects on several organs. With regard to these pathomechanisms, we will discuss the needs, and the stakes of evolving the testing and assessment of endocrine disruptors to improve the prevention and management of metabolic diseases that have become a global epidemic since the end of last century.

Zobrazit více v PubMed

Cano R, Pérez JL, Dávila LA, Ortega Á, Gómez Y, Valero-Cedeño NJ, et al. Role of endocrine-disrupting chemicals in the pathogenesis of non-alcoholic fatty liver disease: a comprehensive review. Int J Mol Sci. 2021;22:4807.

Grün F, Blumberg B. Environmental obesogens: organotins and endocrine disruption via nuclear receptor signaling. Endocrinology. 2006;147:S50-5.

Heindel JJ, Blumberg B, Cave M, Machtinger R, Mantovani A, Mendez MA, et al. Metabolism disrupting chemicals and metabolic disorders. Reprod Toxicol. 2017;68:3-33.

Bulka CM, Persky VW, Daviglus ML, Durazo-Arvizu RA, Argos M. Multiple metal exposures and metabolic syndrome: a cross-sectional analysis of the National Health and Nutrition Examination Survey 2011-2014. Environ Res. 2019;168:397-405.

Xu P, Liu A, Li F, Tinkov AA, Liu L, Zhou J-C. Associations between metabolic syndrome and four heavy metals: a systematic review and meta-analysis. Environ Pollut. 2021;273:116480.

Planchart A, Green A, Hoyo C, Mattingly CJ. Heavy metal exposure and metabolic syndrome: evidence from human and model system studies. Curr Environ Health Rep. 2018;5:110-24.

Roy C, Tremblay P-Y, Ayotte P. Is mercury exposure causing diabetes, metabolic syndrome and insulin resistance? A systematic review of the literature. Environ Res. 2017;156:747-60.

Tinkov AA, Ajsuvakova OP, Skalnaya MG, Popova EV, Sinitskii AI, Nemereshina ON, et al. Mercury and metabolic syndrome: a review of experimental and clinical observations. Biometals. 2015;28:231-54.

Kim S-K, Park S, Chang S-J, Kim S-K, Song JS, Kim H-R, et al. Pesticides as a risk factor for metabolic syndrome: population-based longitudinal study in Korea. Mol Cell Toxicol. 2019;15:431-41.

Park S-K, Son H-K, Lee S-K, Kang J-H, Chang Y-S, Jacobs DR, et al. Relationship between serum concentrations of organochlorine pesticides and metabolic syndrome among non-diabetic adults. J Prev Med Public Health. 2010;43:1.

Rosenbaum PF, Weinstock RS, Silverstone AE, Sjödin A, Pavuk M. Metabolic syndrome is associated with exposure to organochlorine pesticides in Anniston, AL, United States. Environ Int. 2017;108:11-21.

Mustieles V, Fernández MF, Martin-Olmedo P, González-Alzaga B, Fontalba-Navas A, Hauser R, et al. Human adipose tissue levels of persistent organic pollutants and metabolic syndrome components: combining a cross-sectional with a 10-year longitudinal study using a multi-pollutant approach. Environ Int. 2017;104:48-57.

Mondal D, Lopez-Espinosa M-J, Armstrong B, Stein CR, Fletcher T. Relationships of perfluorooctanoate and perfluorooctane sulfonate serum concentrations between mother-child pairs in a population with perfluorooctanoate exposure from drinking water. Environ Health Perspect. 2012;120:752-7.

Braun JM, Chen A, Romano ME, Calafat AM, Webster GM, Yolton K, et al. Prenatal perfluoroalkyl substance exposure and child adiposity at 8 years of age: the HOME study: prenatal PFAS exposure and child adiposity. Obesity. 2016;24:231-7.

Halldorsson TI, Rytter D, Haug LS, Bech BH, Danielsen I, Becher G, et al. Prenatal exposure to perfluorooctanoate and risk of overweight at 20 years of age: a prospective cohort study. Environ Health Perspect. 2012;120:668-73.

Averina M, Brox J, Huber S, Furberg A-S. Exposure to perfluoroalkyl substances (PFAS) and dyslipidemia, hypertension and obesity in adolescents. The fit futures study. Environ Res. 2021;195:110740.

Qi W, Clark JM, Timme-Laragy AR, Park Y. Per- and polyfluoroalkyl substances and obesity, type 2 diabetes and non-alcoholic fatty liver disease: a review of epidemiologic findings. Toxicol Environ Chem. 2020;102:1-36.

Liu G, Zhang B, Hu Y, Rood J, Liang L, Qi L, et al. Associations of perfluoroalkyl substances with blood lipids and apolipoproteins in lipoprotein subspecies: the POUNDS-lost study. Environ Health. 2020;19:5.

Mi X, Yang Y-Q, Zeeshan M, Wang Z-B, Zeng X-Y, Zhou Y, et al. Serum levels of per- and polyfluoroalkyl substances alternatives and blood pressure by sex status: isomers of C8 health project in China. Chemosphere. 2020;261:127691.

Stojanoska MM, Milosevic N, Milic N, Abenavoli L. The influence of phthalates and bisphenol A on the obesity development and glucose metabolism disorders. Endocrine. 2017;55:666-81.

Teppala S, Madhavan S, Shankar A. Bisphenol A and metabolic syndrome: results from NHANES. Int J Endocrinol. 2012;2012:1-5.

Kim KY, Lee E, Kim Y. The association between bisphenol A exposure and obesity in children-a systematic review with meta-analysis. Int J Environ Res Public Health. 2019;16:2521.

Provvisiero D, Pivonello C, Muscogiuri G, Negri M, de Angelis C, Simeoli C, et al. Influence of bisphenol A on type 2 diabetes mellitus. Int J Environ Res Public Health. 2016;13:989.

Rochester JR, Bolden AL. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ Health Perspect. 2015;123:643-50.

Golestanzadeh M, Riahi R, Kelishadi R. Association of exposure to phthalates with cardiometabolic risk factors in children and adolescents: a systematic review and meta-analysis. Environ Sci Pollut Res. 2019;26:35670-86.

Radke EG, Galizia A, Thayer KA, Cooper GS. Phthalate exposure and metabolic effects: a systematic review of the human epidemiological evidence. Environ Int. 2019;132:104768.

James-Todd TM, Huang T, Seely EW, Saxena AR. The association between phthalates and metabolic syndrome: the National Health and Nutrition Examination Survey 2001-2010. Environ Health. 2016;15:52.

Poursafa P, Dadvand P, Amin MM, Hajizadeh Y, Ebrahimpour K, Mansourian M, et al. Association of polycyclic aromatic hydrocarbons with cardiometabolic risk factors and obesity in children. Environ Int. 2018;118:203-10.

Zhang B, Pan B, Zhao X, Fu Y, Li X, Yang A, et al. The interaction effects of smoking and polycyclic aromatic hydrocarbons exposure on the prevalence of metabolic syndrome in coke oven workers. Chemosphere. 2020;247:125880.

Hu H, Kan H, Kearney GD, Xu X. Associations between exposure to polycyclic aromatic hydrocarbons and glucose homeostasis as well as metabolic syndrome in nondiabetic adults. Sci Total Environ. 2015;505:56-64.

La Merrill M, Emond C, Kim MJ, Antignac J-P, Le Bizec B, Clément K, et al. Toxicological function of adipose tissue: focus on persistent organic pollutants. Environ Health Perspect. 2013;121:162-9.

Audano M, Pedretti S, Caruso D, Crestani M, De Fabiani E, Mitro N. Regulatory mechanisms of the early phase of white adipocyte differentiation: an overview. Cell Mol Life Sci. 2022;79:139.

Costa V, Gallo MA, Letizia F, Aprile M, Casamassimi A, Ciccodicola A. PPARG: gene expression regulation and next-generation sequencing for unsolved issues. PPAR Res. 2010;2010:409168.

Longo M, Zatterale F, Naderi J, Parrillo L, Formisano P, Raciti GA, et al. Adipose tissue dysfunction as determinant of obesity-associated metabolic complications. Int J Mol Sci. 2019;20:E2358.

Chamorro-García R, Sahu M, Abbey RJ, Laude J, Pham N, Blumberg B. Transgenerational inheritance of increased fat depot size, stem cell reprogramming, and hepatic steatosis elicited by prenatal exposure to the obesogen tributyltin in mice. Environ Health Perspect. 2013;121:359-66.

Li B, Guo J, Xi Z, Xu J, Zuo Z, Wang C. Tributyltin in male mice disrupts glucose homeostasis as well as recovery after exposure: mechanism analysis. Arch Toxicol. 2017;91:3261-9.

Bertuloso BD, Podratz PL, Merlo E, de Araújo JFP, Lima LCF, de Miguel EC, et al. Tributyltin chloride leads to adiposity and impairs metabolic functions in the rat liver and pancreas. Toxicol Lett. 2015;235:45-59.

Yang M, Chen M, Wang J, Xu M, Sun J, Ding L, et al. Bisphenol A promotes adiposity and inflammation in a nonmonotonic dose-response way in 5-week-old male and female C57BL/6J mice fed a low-calorie diet. Endocrinology. 2016;157:2333-45.

Aaseth J, Javorac D, Djordjevic AB, Bulat Z, Skalny AV, Zaitseva IP, et al. The role of persistent organic pollutants in obesity: a review of laboratory and epidemiological studies. Toxics. 2022;10:65.

Jia Y, Liu T, Zhou L, Zhu J, Wu J, Sun D, et al. Effects of di-(2-ethylhexyl) phthalate on lipid metabolism by the JAK/STAT pathway in rats. Int J Environ Res Public Health. 2016;13:E1085.

Cohen IC, Cohenour ER, Harnett KG, Schuh SM. BPA, BPAF and TMBPF alter adipogenesis and fat accumulation in human mesenchymal stem cells, with implications for obesity. Int J Mol Sci. 2021;22:5363.

Reina-Pérez I, Olivas-Martínez A, Mustieles V, Ruiz-Ojeda FJ, Molina-Molina JM, Olea N, et al. Bisphenol F and bisphenol S promote lipid accumulation and adipogenesis in human adipose-derived stem cells. Food Chem Toxicol. 2021;152:112216.

Ramskov Tetzlaff CN, Svingen T, Vinggaard AM, Rosenmai AK, Taxvig C. Bisphenols B, E, F, and S and 4-cumylphenol induce lipid accumulation in mouse adipocytes similarly to bisphenol A. Environ Toxicol. 2020;35:543-52.

Brulport A, Le Corre L, Chagnon M-C. Chronic exposure of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) induces an obesogenic effect in C57BL/6J mice fed a high fat diet. Toxicology. 2017;390:43-52.

Wahlang B, Falkner KC, Gregory B, Ansert D, Young D, Conklin DJ, et al. Polychlorinated biphenyl 153 is a diet-dependent obesogen that worsens nonalcoholic fatty liver disease in male C57BL6/J mice. J Nutr Biochem. 2013;24:1587-95.

Wu H, Yu W, Meng F, Mi J, Peng J, Liu J, et al. Polychlorinated biphenyls-153 induces metabolic dysfunction through activation of ROS/NF-κB signaling via downregulation of HNF1b. Redox Biol. 2017;12:300-10.

Laurenzana EM, Coslo DM, Vigilar MV, Roman AM, Omiecinski CJ. Activation of the constitutive androstane receptor by monophthalates. Chem Res Toxicol. 2016;29:1651-61.

Ellero-Simatos S, Claus SP, Benelli C, Forest C, Letourneur F, Cagnard N, et al. Combined transcriptomic-(1)H NMR metabonomic study reveals that monoethylhexyl phthalate stimulates adipogenesis and glyceroneogenesis in human adipocytes. J Proteome Res. 2011;10:5493-502.

Gadupudi G, Gourronc FA, Ludewig G, Robertson LW, Klingelhutz AJ. PCB126 inhibits adipogenesis of human preadipocytes. Toxicol In Vitro. 2015;29:132-41.

Mullerova D, Pesta M, Dvorakova J, Cedikova M, Kulda V, Dvorak P, et al. Polychlorinated biphenyl 153 in lipid medium modulates differentiation of human adipocytes. Physiol Res. 2017;66:653-62.

Kim MJ, Pelloux V, Guyot E, Tordjman J, Bui L-C, Chevallier A, et al. Inflammatory pathway genes belong to major targets of persistent organic pollutants in adipose cells. Environ Health Perspect. 2012;120:508-14.

Ahmed S, Atlas E. Bisphenol S- and bisphenol A-induced adipogenesis of murine preadipocytes occurs through direct peroxisome proliferator-activated receptor gamma activation. Int J Obes (Lond). 2016;40:1566-73.

Hu P, Chen X, Whitener RJ, Boder ET, Jones JO, Porollo A, et al. Effects of parabens on adipocyte differentiation. Toxicol Sci. 2013;131:56-70.

Liu S, Yang R, Yin N, Wang Y-L, Faiola F. Environmental and human relevant PFOS and PFOA doses alter human mesenchymal stem cell self-renewal, adipogenesis and osteogenesis. Ecotoxicol Environ Saf. 2019;169:564-72.

Shoucri BM, Hung VT, Chamorro-García R, Shioda T, Blumberg B. Retinoid X receptor activation during adipogenesis of female mesenchymal stem cells programs a dysfunctional adipocyte. Endocrinology. 2018;159:2863-83.

Kim SH, Park MJ. Phthalate exposure and childhood obesity. Ann Pediatr Endocrinol Metab. 2014;19:69-75.

Fang M, Webster TF, Ferguson PL, Stapleton HM. Characterizing the peroxisome proliferator-activated receptor (PPARγ) ligand binding potential of several major flame retardants, their metabolites, and chemical mixtures in house dust. Environ Health Perspect. 2015;123:166-72.

Amir S, Shah STA, Mamoulakis C, Docea AO, Kalantzi O-I, Zachariou A, et al. Endocrine disruptors acting on estrogen and androgen pathways cause reproductive disorders through multiple mechanisms: a review. Int J Environ Res Public Health. 2021;18:1464.

TTB V, Jeung E-B. An evaluation of estrogenic activity of parabens using uterine calbindin-d9k gene in an immature rat model. Toxicol Sci. 2009;112:68-77.

Foulds CE, Treviño LS, York B, Walker CL. Endocrine-disrupting chemicals and fatty liver disease. Nat Rev Endocrinol. 2017;13:445-57.

Deierlein AL, Rock S, Park S. Persistent endocrine-disrupting chemicals and fatty liver disease. Curr Environ Health Rep. 2017;4:439-49.

Chen N, Shan Q, Qi Y, Liu W, Tan X, Gu J. Transcriptome analysis in normal human liver cells exposed to 2, 3, 3′, 4, 4′, 5-hexachlorobiphenyl (PCB 156). Chemosphere. 2020;239:124747.

Shan Q, Li H, Chen N, Qu F, Guo J. Understanding the multiple effects of PCBs on lipid metabolism. Diabetes Metab Syndr Obes. 2020;13:3691-702.

Liang X, Xie G, Wu X, Su M, Yang B. Effect of prenatal PFOS exposure on liver cell function in neonatal mice. Environ Sci Pollut Res Int. 2019;26:18240-6.

Marmugi A, Ducheix S, Lasserre F, Polizzi A, Paris A, Priymenko N, et al. Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology. 2012;55:395-407.

Küblbeck J, Niskanen J, Honkakoski P. Metabolism-disrupting chemicals and the constitutive androstane receptor CAR. Cells. 2020;9:E2306.

Wyde ME, Kirwan SE, Zhang F, Laughter A, Hoffman HB, Bartolucci-Page E, et al. Di-n-butyl phthalate activates constitutive androstane receptor and pregnane X receptor and enhances the expression of steroid-metabolizing enzymes in the liver of rat fetuses. Toxicol Sci. 2005;86:281-90.

Eveillard A, Mselli-Lakhal L, Mogha A, Lasserre F, Polizzi A, Pascussi J-M, et al. Di-(2-ethylhexyl)-phthalate (DEHP) activates the constitutive androstane receptor (CAR): a novel signalling pathway sensitive to phthalates. Biochem Pharmacol. 2009;77:1735-46.

Bjork JA, Butenhoff JL, Wallace KB. Multiplicity of nuclear receptor activation by PFOA and PFOS in primary human and rodent hepatocytes. Toxicology. 2011;288:8-17.

Kojima H, Takeuchi S, Sanoh S, Okuda K, Kitamura S, Uramaru N, et al. Profiling of bisphenol A and eight its analogues on transcriptional activity via human nuclear receptors. Toxicology. 2019;413:48-55.

Yue S, Yu J, Kong Y, Chen H, Mao M, Ji C, et al. Metabolomic modulations of HepG2 cells exposed to bisphenol analogues. Environ Int. 2019;129:59-67.

Kubota T, Kubota N, Kadowaki T. Imbalanced insulin actions in obesity and type 2 diabetes: key mouse models of insulin signaling pathway. Cell Metab. 2017;25:797-810.

Mu W, Cheng X-F, Liu Y, Lv Q-Z, Liu G-L, Zhang J-G, et al. Potential nexus of non-alcoholic fatty liver disease and type 2 diabetes mellitus: insulin resistance between hepatic and peripheral tissues. Front Pharmacol. 2018;9:1566.

Rotondo E, Chiarelli F. Endocrine-disrupting chemicals and insulin resistance in children. Biomedicines. 2020;8:E137.

Sargis RM. The hijacking of cellular signaling and the diabetes epidemic: mechanisms of environmental disruption of insulin action and glucose homeostasis. Diabetes Metab J. 2014;38:13-24.

Jayashree S, Indumathi D, Akilavalli N, Sathish S, Selvaraj J, Balasubramanian K. Effect of bisphenol-A on insulin signal transduction and glucose oxidation in liver of adult male albino rat. Environ Toxicol Pharmacol. 2013;35:300-10.

Yang B, Zou W, Hu Z, Liu F, Zhou L, Yang S, et al. Involvement of oxidative stress and inflammation in liver injury caused by perfluorooctanoic acid exposure in mice. Biomed Res Int. 2014;2014:409837.

Huc L, Lemarié A, Guéraud F, Héliès-Toussaint C. Low concentrations of bisphenol A induce lipid accumulation mediated by the production of reactive oxygen species in the mitochondria of HepG2 cells. Toxicol In Vitro. 2012;26:709-17.

Han R, Zhang F, Wan C, Liu L, Zhong Q, Ding W. Effect of perfluorooctane sulphonate-induced Kupffer cell activation on hepatocyte proliferation through the NF-κB/TNF-α/IL-6-dependent pathway. Chemosphere. 2018;200:283-94.

Han M, Liu X, Liu S, Su G, Fan X, Chen J, et al. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) induces hepatic stellate cell (HSC) activation and liver fibrosis in C57BL6 mouse via activating Akt and NF-κB signaling pathways. Toxicol Lett. 2017;273:10-9.

Shi H, Jan J, Hardesty JE, Falkner KC, Prough RA, Balamurugan AN, et al. Polychlorinated biphenyl exposures differentially regulate hepatic metabolism and pancreatic function: implications for nonalcoholic steatohepatitis and diabetes. Toxicol Appl Pharmacol. 2019;363:22-33.

Soriano S, Alonso-Magdalena P, García-Arévalo M, Novials A, Muhammed SJ, Salehi A, et al. Rapid insulinotropic action of low doses of bisphenol-A on mouse and human islets of Langerhans: role of estrogen receptor β. PLoS One. 2012;7:e31109.

Martinez-Pinna J, Marroqui L, Hmadcha A, Lopez-Beas J, Soriano S, Villar-Pazos S, et al. Oestrogen receptor β mediates the actions of bisphenol-A on ion channel expression in mouse pancreatic beta cells. Diabetologia. 2019;62:1667-80.

Alonso-Magdalena P, Ropero AB, Carrera MP, Cederroth CR, Baquié M, Gauthier BR, et al. Pancreatic insulin content regulation by the estrogen receptor ER alpha. PLoS One. 2008;3:e2069.

Alonso-Magdalena P, Morimoto S, Ripoll C, Fuentes E, Nadal A. The estrogenic effect of bisphenol A disrupts pancreatic beta-cell function in vivo and induces insulin resistance. Environ Health Perspect. 2006;114:106-12.

Alonso-Magdalena P, Vieira E, Soriano S, Menes L, Burks D, Quesada I, et al. Bisphenol A exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring. Environ Health Perspect. 2010;118:1243-50.

Li L, Wang F, Zhang J, Wang K, De X, Li L, et al. Typical phthalic acid esters induce apoptosis by regulating the PI3K/Akt/Bcl-2 signaling pathway in rat insulinoma cells. Ecotoxicol Environ Saf. 2021;208:111461.

Li J, Zheng L, Wang X, Yao K, Shi L, Sun X, et al. Taurine protects INS-1 cells from apoptosis induced by Di(2-ethylhexyl) phthalate via reducing oxidative stress and autophagy. Toxicol Mech Methods. 2019;29:445-56.

Sun X, Lin Y, Huang Q, Shi J, Qiu L, Kang M, et al. Di(2-ethylhexyl) phthalate-induced apoptosis in rat INS-1 cells is dependent on activation of endoplasmic reticulum stress and suppression of antioxidant protection. J Cell Mol Med. 2015;19:581-94.

She Y, Jiang L, Zheng L, Zuo H, Chen M, Sun X, et al. The role of oxidative stress in DNA damage in pancreatic β cells induced by di-(2-ethylhexyl) phthalate. Chem Biol Interact. 2017;265:8-15.

Qin W-P, Cao L-Y, Li C-H, Guo L-H, Colbourne J, Ren X-M. Perfluoroalkyl substances stimulate insulin secretion by islet β cells via G protein-coupled receptor 40. Environ Sci Technol. 2020;54:3428-36.

Zhang L, Duan X, Sun W, Sun H. Perfluorooctane sulfonate acute exposure stimulates insulin secretion via GPR40 pathway. Sci Total Environ. 2020;726:138498.

Duan X, Sun W, Sun H, Zhang L. Perfluorooctane sulfonate continual exposure impairs glucose-stimulated insulin secretion via SIRT1-induced upregulation of UCP2 expression. Environ Pollut. 2021;278:116840.

Wan HT, Cheung LY, Chan TF, Li M, Lai KP, Wong CKC. Characterization of PFOS toxicity on in-vivo and ex-vivo mouse pancreatic islets. Environ Pollut. 2021;289:117857.

Chen Y-W, Lan K-C, Tsai J-R, Weng T-I, Yang C-Y, Liu S-H. Tributyltin exposure at noncytotoxic doses dysregulates pancreatic β-cell function in vitro and in vivo. Arch Toxicol. 2017;91:3135-44.

Huang C-F, Yang C-Y, Tsai J-R, Wu C-T, Liu S-H, Lan K-C. Low-dose tributyltin exposure induces an oxidative stress-triggered JNK-related pancreatic β-cell apoptosis and a reversible hypoinsulinemic hyperglycemia in mice. Sci Rep. 2018;8:5734.

Ibrahim M, MacFarlane EM, Matteo G, Hoyeck MP, Rick KRC, Farokhi S, et al. Functional cytochrome P450 1A enzymes are induced in mouse and human islets following pollutant exposure. Diabetologia. 2020;63:162-78.

Martino L, Novelli M, Masini M, Chimenti D, Piaggi S, Masiello P, et al. Dehydroascorbate protection against dioxin-induced toxicity in the beta-cell line INS-1E. Toxicol Lett. 2009;189:27-34.

Novelli M, Beffy P, Masini M, Vantaggiato C, Martino L, Marselli L, et al. Selective beta-cell toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin on isolated pancreatic islets. Chemosphere. 2021;265:129103.

Cave MC, Clair HB, Hardesty JE, Falkner KC, Feng W, Clark BJ, et al. Nuclear receptors and nonalcoholic fatty liver disease. Biochim Biophys Acta. 2016;1859:1083-99.

Vanni R, Bussuan RM, Rombaldi RL, Arbex AK. Endocrine disruptors and the induction of insulin resistance. Curr Diabetes Rev. 2021;17:e102220187107.

Darbre PD. Endocrine disruptors and obesity. Curr Obes Rep. 2017;6:18-27.

Wilson ID, Nicholson JK. Gut microbiome interactions with drug metabolism, efficacy, and toxicity. Transl Res. 2017;179:204-22.

Hampl R, Stárka L. Endocrine disruptors and gut microbiome interactions. Physiol Res. 2020;69:S211-23.

Sarni ROS, Kochi C, Suano-Souza FI. Childhood obesity: an ecological perspective. J Pediatr (Rio J). 2022;98(Suppl 1):S38-46.

Santos-Marcos JA, Haro C, Vega-Rojas A, Alcala-Diaz JF, Molina-Abril H, Leon-Acuña A, et al. Sex differences in the gut microbiota as potential determinants of gender predisposition to disease. Mol Nutr Food Res. 2019;63:e1800870.

Tripathi A, Debelius J, Brenner DA, Karin M, Loomba R, Schnabl B, et al. The gut-liver axis and the intersection with the microbiome. Nat Rev Gastroenterol Hepatol. 2018;15:397-411.

Liu Y, Yao Y, Li H, Qiao F, Wu J, Du Z, et al. Influence of endogenous and exogenous estrogenic endocrine on intestinal microbiota in zebrafish. PLoS One. 2016;11:e0163895.

Lui JB, McGinn LS, Chen Z. Gut microbiota amplifies host-intrinsic conversion from the CD8 T cell lineage to CD4 T cells for induction of mucosal immune tolerance. Gut Microbes. 2016;7:40-7.

Koestel ZL, Backus RC, Tsuruta K, Spollen WG, Johnson SA, Javurek AB, et al. Bisphenol A (BPA) in the serum of pet dogs following short-term consumption of canned dog food and potential health consequences of exposure to BPA. Sci Total Environ. 2017;579:1804-14.

Reddivari L, Veeramachaneni DNR, Walters WA, Lozupone C, Palmer J, Hewage MKK, et al. Perinatal bisphenol A exposure induces chronic inflammation in rabbit offspring via modulation of gut bacteria and their metabolites. mSystems. 2017;2:e00093-17.

Javurek AB, Spollen WG, Johnson SA, Bivens NJ, Bromert KH, Givan SA, et al. Effects of exposure to bisphenol A and ethinyl estradiol on the gut microbiota of parents and their offspring in a rodent model. Gut Microbes. 2016;7:471-85.

Hu J, Raikhel V, Gopalakrishnan K, Fernandez-Hernandez H, Lambertini L, Manservisi F, et al. Effect of postnatal low-dose exposure to environmental chemicals on the gut microbiome in a rodent model. Microbiome. 2016;4:26.

Wang C, Yue S, Hao Z, Ren G, Lu D, Zhang Q, et al. Pubertal exposure to the endocrine disruptor mono-2-ethylhexyl ester at body burden level caused cholesterol imbalance in mice. Environ Pollut. 2019;244:657-66.

Jin Y, Zeng Z, Wu Y, Zhang S, Fu Z. Oral exposure of mice to carbendazim induces hepatic lipid metabolism disorder and gut microbiota dysbiosis. Toxicol Sci. 2015;147:116-26.

Zhang L, Nichols RG, Correll J, Murray IA, Tanaka N, Smith PB, et al. Persistent organic pollutants modify gut microbiota-host metabolic homeostasis in mice through aryl hydrocarbon receptor activation. Environ Health Perspect. 2015;123:679-88.

Kan H, Zhao F, Zhang X-X, Ren H, Gao S. Correlations of gut microbial community shift with hepatic damage and growth inhibition of Carassius auratus induced by pentachlorophenol exposure. Environ Sci Technol. 2015;49:11894-902.

Chi Y, Lin Y, Lu Y, Huang Q, Ye G, Dong S. Gut microbiota dysbiosis correlates with a low-dose PCB126-induced dyslipidemia and non-alcoholic fatty liver disease. Sci Total Environ. 2019;653:274-82.

Liang Y, Liu D, Zhan J, Luo M, Han J, Wang P, et al. New insight into the mechanism of POP-induced obesity: evidence from DDE-altered microbiota. Chemosphere. 2020;244:125123.

Feng P, Ye Z, Kakade A, Virk A, Li X, Liu P. A review on gut remediation of selected environmental contaminants: possible roles of probiotics and gut microbiota. Nutrients. 2018;11:22.

Malaisé Y, Menard S, Cartier C, Gaultier E, Lasserre F, Lencina C, et al. Gut dysbiosis and impairment of immune system homeostasis in perinatally-exposed mice to bisphenol A precede obese phenotype development. Sci Rep. 2017;7:14472.

Fader KA, Nault R, Zhang C, Kumagai K, Harkema JR, Zacharewski TR. 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD)-elicited effects on bile acid homeostasis: alterations in biosynthesis, enterohepatic circulation, and microbial metabolism. Sci Rep. 2017;7:5921.

Natividad JM, Agus A, Planchais J, Lamas B, Jarry AC, Martin R, et al. Impaired aryl hydrocarbon receptor ligand production by the gut microbiota is a key factor in metabolic syndrome. Cell Metab. 2018;28:737-49.e4.

Fader KA, Nault R, Doskey CM, Fling RR, Zacharewski TR. 2,3,7,8-Tetrachlorodibenzo-p-dioxin abolishes circadian regulation of hepatic metabolic activity in mice. Sci Rep. 2019;9:6514.

Tilg H, Cani PD, Mayer EA. Gut microbiome and liver diseases. Gut. 2016;65:2035-44.

Weger BD, Rawashdeh O, Gachon F. At the intersection of microbiota and circadian clock: are sexual dimorphism and growth hormones the missing link to pathology?: circadian clock and microbiota: potential egffect on growth hormone and sexual development. Bioessays. 2019;41:e1900059.

Zhou C, Verma S, Blumberg B. The steroid and xenobiotic receptor (SXR), beyond xenobiotic metabolism. Nucl Recept Signal. 2009;7:e001.

Kim S, Choi S, Dutta M, Asubonteng JO, Polunas M, Goedken M, et al. Pregnane X receptor exacerbates nonalcoholic fatty liver disease accompanied by obesity- and inflammation-prone gut microbiome signature. Biochem Pharmacol. 2021;193:114698.

Shin K-H, Choi MH, Lim KS, Yu K-S, Jang I-J, Cho J-Y. Evaluation of endogenous metabolic markers of hepatic CYP3A activity using metabolic profiling and midazolam clearance. Clin Pharmacol Ther. 2013;94:601-9.

Zanger UM, Schwab M. Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther. 2013;138:103-41.

Sui Y, Helsley RN, Park S-H, Song X, Liu Z, Zhou C. Intestinal pregnane X receptor links xenobiotic exposure and hypercholesterolemia. Mol Endocrinol. 2015;29:765-76.

Grün F, Blumberg B. Minireview: the case for obesogens. Mol Endocrinol. 2009;23:1127-34.

Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004;56:311-7.

MacKay H, Patterson ZR, Abizaid A. Perinatal exposure to low-dose bisphenol-A disrupts the structural and functional development of the hypothalamic feeding circuitry. Endocrinology. 2017;158:768-77.

Tian S, Yan S, Meng Z, Huang S, Sun W, Jia M, et al. New insights into bisphenols induced obesity in zebrafish (Danio rerio): Activation of cannabinoid receptor CB1. Journal of Hazardous Materials. 2021;418:126100.

Rönn M, Lind L, Örberg J, Kullberg J, Söderberg S, Larsson A, et al. Bisphenol A is related to circulating levels of adiponectin, leptin and ghrelin, but not to fat mass or fat distribution in humans. Chemosphere. 2014;112:42-8.

Ariemma F, D'Esposito V, Liguoro D, Oriente F, Cabaro S, Liotti A, et al. Low-dose bisphenol-A impairs adipogenesis and generates dysfunctional 3T3-L1 adipocytes. PLoS One. 2016;11:e0150762.

Schmidt J-S, Schaedlich K, Fiandanese N, Pocar P, Fischer B. Effects of di(2-ethylhexyl) phthalate (DEHP) on female fertility and adipogenesis in C3H/N mice. Environ Health Perspect. 2012;120:1123-9.

Hao C. Perinatal exposure to diethyl-hexyl-phthalate induces obesity in mice. Front Biosci. 2013;5:725-33.

Fougerat A, Schoiswohl G, Polizzi A, Régnier M, Wagner C, Smati S, et al. ATGL-dependent white adipose tissue lipolysis controls hepatocyte PPARα activity. Cell Rep. 2022;39:110910.

Simcox J, Geoghegan G, Maschek JA, Bensard CL, Pasquali M, Miao R, et al. Global analysis of plasma lipids identifies liver-derived acylcarnitines as a fuel source for brown fat thermogenesis. Cell Metab. 2017;26:509-22.e6.

Wang B, Tsakiridis EE, Zhang S, Llanos A, Desjardins EM, Yabut JM, et al. The pesticide chlorpyrifos promotes obesity by inhibiting diet-induced thermogenesis in brown adipose tissue. Nat Commun. 2021;12:5163.

Manikkam M, Tracey R, Guerrero-Bosagna C, Skinner MK. Plastics derived endocrine disruptors (BPA, DEHP and DBP) induce epigenetic transgenerational inheritance of obesity, reproductive disease and sperm epimutations. PLoS One. 2013;8:e55387.

Manikkam M, Haque MM, Guerrero-Bosagna C, Nilsson EE, Skinner MK. Pesticide methoxychlor promotes the epigenetic transgenerational inheritance of adult-onset disease through the female germline. PLoS One. 2014;9:e102091.

King SE, McBirney M, Beck D, Sadler-Riggleman I, Nilsson E, Skinner MK. Sperm epimutation biomarkers of obesity and pathologies following DDT induced epigenetic transgenerational inheritance of disease. Environ Epigenet. 2019;5:dvz008.

Skinner MK, Manikkam M, Tracey R, Guerrero-Bosagna C, Haque M, Nilsson EE. Ancestral dichlorodiphenyltrichloroethane (DDT) exposure promotes epigenetic transgenerational inheritance of obesity. BMC Med. 2013;11:228.

Grün F, Blumberg B. Perturbed nuclear receptor signaling by environmental obesogens as emerging factors in the obesity crisis. Rev Endocr Metab Disord. 2007;8:161-71.

le Maire A, Grimaldi M, Roecklin D, Dagnino S, Vivat-Hannah V, Balaguer P, et al. Activation of RXR-PPAR heterodimers by organotin environmental endocrine disruptors. EMBO Rep. 2009;10:367-73.

Grün F, Watanabe H, Zamanian Z, Maeda L, Arima K, Cubacha R, et al. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol. 2006;20:2141-55.

Chamorro-Garcia R, Diaz-Castillo C, Shoucri BM, Käch H, Leavitt R, Shioda T, et al. Ancestral perinatal obesogen exposure results in a transgenerational thrifty phenotype in mice. Nat Commun. 2017;8:2012.

Diaz-Castillo C, Chamorro-Garcia R, Shioda T, Blumberg B. Transgenerational self-reconstruction of disrupted chromatin organization after exposure to an environmental stressor in mice. Sci Rep. 2019;9:13057.

Qian Y, Liao J, Suen AHC, Lee AWT, Chung HS, Tang NLS, et al. Comparative analysis of single-cell parallel sequencing approaches in oocyte application. Int J Biochem Cell Biol. 2019;107:1-5.

Camsari C, Folger JK, Rajput SK, McGee D, Latham KE, Smith GW. Transgenerational effects of periconception heavy metal administration on adipose weight and glucose homeostasis in mice at maturity. Toxicol Sci. 2019;168:610-9.

Forgacs AL, Kent MN, Makley MK, Mets B, DelRaso N, Jahns GL, et al. Comparative metabolomic and genomic analyses of TCDD-elicited metabolic disruption in mouse and rat liver. Toxicol Sci. 2012;125:41-55.

Lee JH, Wada T, Febbraio M, He J, Matsubara T, Lee MJ, et al. A novel role for the dioxin receptor in fatty acid metabolism and hepatic steatosis. Gastroenterology. 2010;139:653-63.

Sui Y, Park S-H, Helsley RN, Sunkara M, Gonzalez FJ, Morris AJ, et al. Bisphenol A increases atherosclerosis in pregnane X receptor-humanized ApoE deficient mice. J Am Heart Assoc. 2014;3:e000492.

Ding S, Yuan C, Si B, Wang M, Da S, Bai L, et al. Combined effects of ambient particulate matter exposure and a high-fat diet on oxidative stress and steatohepatitis in mice. PLoS One. 2019;14:e0214680.

Drakvik E, Altenburger R, Aoki Y, Backhaus T, Bahadori T, Barouki R, et al. Statement on advancing the assessment of chemical mixtures and their risks for human health and the environment. Environ Int. 2020;134:105267.

Teeguarden JG, Tan Y-M, Edwards SW, Leonard JA, Anderson KA, Corley RA, et al. Completing the link between exposure science and toxicology for improved environmental health decision making: the aggregate exposure pathway framework. Environ Sci Technol. 2016;50:4579-86.

Najít záznam

Citační ukazatele

Možnosti archivace