Metabolic impact of persistent organic pollutants on gut microbiota

Tian, Yuan; Gui, Weihua; Rimal, Bipin; Koo, Imhoi; Smith, Philip B.; Nichols, Robert G.; Cai, Jingjing; Liu, Qing; Patterson, Andrew D.

doi:10.1080/19490976.2020.1848209

Cited by 32 publications

(17 citation statements)

References 64 publications

(88 reference statements)

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“…However, there are few regulatory guidelines that address microbiome toxicity by environmental pollutant exposure. In our previous studies, we reported that POPs rapidly and significantly altered the bacterial community structural, metabolic, and transcriptional levels in both in vitro and in vivo models indicating microbial toxicity following environment pollutant exposure [ 25 , 31 , 36 ]. We observed rapid changes in microbial community structure and overall metabolism and more dramatic metabolic and gene expression changes on microbiota in adulthood by early life PCB 126 exposure.…”

Section: Discussionmentioning

confidence: 99%

“…Early life exposure to PCB 126 showed delayed toxicity and resulted in delayed mortality as well as growth impairment and delayed development in the zebrafish model [ 13 ]. Recent studies demonstrated that PCB 126 significantly altered the gut microbial ecosystem in adult mice and in in vitro models identifying significant microbial toxicity following environment pollutant exposure [ 20 , 25 ]. However, a systematic investigation of the long-term consequences of early life, Short-Term PCB 126 exposure on host and bacterial metabolism has not been described.…”

Section: Introductionmentioning

confidence: 99%

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Early Life Short-Term Exposure to Polychlorinated Biphenyl 126 in Mice Leads to Metabolic Dysfunction and Microbiota Changes in Adulthood

Tian

Rimal

Gui

et al. 2022

IJMS

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Early life exposure to environmental pollutants may have long-term consequences and harmful impacts on health later in life. Here, we investigated the short- and long-term impact of early life 3,3′,4,4′,5-pentacholorobiphenyl (PCB 126) exposure (24 μg/kg body weight for five days) in mice on the host and gut microbiota using 16S rRNA gene sequencing, metagenomics, and 1H NMR- and mass spectrometry-based metabolomics. Induction of Cyp1a1, an aryl hydrocarbon receptor (AHR)-responsive gene, was observed at 6 days and 13 weeks after PCB 126 exposure consistent with the long half-life of PCB 126. Early life, Short-Term PCB 126 exposure resulted in metabolic abnormalities in adulthood including changes in liver amino acid and nucleotide metabolism as well as bile acid metabolism and increased hepatic lipogenesis. Interestingly, early life PCB 126 exposure had a greater impact on bacteria in adulthood at the community structure, metabolic, and functional levels. This study provides evidence for an association between early life environmental pollutant exposure and increased risk of metabolic disorders later in life and suggests the microbiome is a key target of environmental chemical exposure.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Early Life Short-Term Exposure to Polychlorinated Biphenyl 126 in Mice Leads to Metabolic Dysfunction and Microbiota Changes in Adulthood

Tian

Rimal

Gui

et al. 2022

IJMS

Self Cite

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“…Thus, the effects of TCDD on the structure and function of the skin may alter the growth characteristics and life cycle of microbiota. Additionally, TCDD may have direct effects on the cutaneous microbiome and its metabolic capacity, as reported by others for the gut microbiome [ 80 ], which could influence epidermal structure and function. Overall, the influence of DLCs on the skin microbiome is understudied but reports on the gut microbiome in mice have shown that DLC exposure results in dysbiotic gut microbiota and alterations in microbiota-host metabolic homeostasis [ 81 , 82 , 83 ].…”

Section: Discussionmentioning

confidence: 96%

Cutaneous Effects of In Utero and Lactational Exposure of C57BL/6J Mice to 2,3,7,8-Tetrachlorodibenzo-p-dioxin

Bhuju

Olesen

Muenyi

et al. 2021

Toxics

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To determine the cutaneous effects of in utero and lactational exposure to the AHR ligand 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), pregnant C57BL/6J mice were exposed by gavage to a vehicle or 5 μg TCDD/kg body weight at embryonic day 12 and epidermal barrier formation and function were studied in their offspring from postnatal day 1 (P1) through adulthood. TCDD-exposed pups were born with acanthosis. This effect was AHR-dependent and subsided by P6 with no evidence of subsequent inflammatory dermatitis. The challenge of adult mice with MC903 showed similar inflammatory responses in control and treated animals, indicating no long-term immunosuppression to this chemical. Chloracne-like sebaceous gland hypoplasia and cyst formation were observed in TCDD-exposed P21 mice, with concomitant microbiome dysbiosis. These effects were reversed by P35. CYP1A1 and CYP1B1 expression in the skin was increased in the exposed mice until P21, then declined. Both CYP proteins co-localized with LRIG1-expressing progenitor cells at the infundibulum. CYP1B1 protein also co-localized with a second stem cell niche in the isthmus. These results indicate that this exposure to TCDD causes a chloracne-like effect without inflammation. Transient activation of the AhR, due to the shorter half-life of TCDD in mice, likely contributes to the reversibility of these effects.

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“…Purine-mediated inflammatory responses have been extensively explored indicating an evolved extracellular role as danger signals released during events such as cell lysis, apoptosis, and degranulation [ 46 ]. Reductions in metabolites associated with lysine degradation, nicotinamide metabolism, and butanoate metabolism are all indicative of suppressed metabolism of bioactive molecules in the gut [ 47 ].…”

Section: Discussionmentioning

confidence: 99%

Effects of Acute 2,3,7,8-Tetrachlorodibenzo-p-Dioxin Exposure on the Circulating and Cecal Metabolome Profile

Dopkins

Neameh

Hall

et al. 2021

IJMS

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2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) is a polyhalogenated planar hydrocarbon belonging to a group of highly toxic and persistent environmental contaminants known as “dioxins”. TCDD is an animal teratogen and carcinogen that is well characterized for causing immunosuppression through activation of aryl hydrocarbon receptor (AHR). In this study, we investigated the effect of exposure of mice to an acute dose of TCDD on the metabolic profile within the serum and cecal contents to better define the effects of TCDD on host physiology. Our findings demonstrated that within the circulating metabolome following acute TCDD exposure, there was significant dysregulation in the metabolism of bioactive lipids, amino acids, and carbohydrates when compared with the vehicle (VEH)-treated mice. These widespread changes in metabolite abundance were identified to regulate host immunity via modulating nuclear factor-kappa B (NF-κB) and extracellular signal-regulated protein kinase (ERK1/2) activity and work as biomarkers for a variety of organ injuries and dysfunctions that follow TCDD exposure. Within the cecal content of mice exposed to TCDD, we were able to detect changes in inflammatory markers that regulate NF-κB, markers of injury-related inflammation, and changes in lysine degradation, nicotinamide metabolism, and butanoate metabolism, which collectively suggested an immediate suppression of broad-scale metabolic processes in the gastrointestinal tract. Collectively, these results demonstrate that acute TCDD exposure results in immediate irregularities in the circulating and intestinal metabolome, which likely contribute to TCDD toxicity and can be used as biomarkers for the early detection of individual exposure.

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Metabolic impact of persistent organic pollutants on gut microbiota

Cited by 32 publications

References 64 publications

Early Life Short-Term Exposure to Polychlorinated Biphenyl 126 in Mice Leads to Metabolic Dysfunction and Microbiota Changes in Adulthood

Early Life Short-Term Exposure to Polychlorinated Biphenyl 126 in Mice Leads to Metabolic Dysfunction and Microbiota Changes in Adulthood

Cutaneous Effects of In Utero and Lactational Exposure of C57BL/6J Mice to 2,3,7,8-Tetrachlorodibenzo-p-dioxin

Effects of Acute 2,3,7,8-Tetrachlorodibenzo-p-Dioxin Exposure on the Circulating and Cecal Metabolome Profile

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