Liver and Pancreatic Toxicity of Endocrine-Disruptive Chemicals: Focus on Mitochondrial Dysfunction and Oxidative Stress
Abstract
:1. Introduction
2. Data Sources
3. Mitochondrial Dysfunction and Oxidative Stress Are Common Pathomechanisms of EDC Toxicity and Metabolic Pathologies
4. EDCs and Liver Toxicity
4.1. Bisphenols (BPs)
4.2. Alkylphenols
4.3. Polychlorinated Biphenyls (PCBs)
4.4. Triazines
4.5. Phthalates
4.6. Per- and Polyfluoroalkyl Substances (PFASs)
4.7. Polychlorinated Diphenyl Ethers (PCDEs)
4.8. Mixtures of EDCs
Endocrine Disruptor | Experimental Model | Dose | Duration | Effects | Ref. |
---|---|---|---|---|---|
Bisphenol A (BPA) | HepG2 cells | to M | Acute: 24, 48 (and 72) h |
| [50] |
Bisphenol A (BPA) | HepG2 cells | 10 or 100 nM | Acute: 2, 6, 12 or 24 h |
| [51] |
Mouse liver | 1.2 mg/kg bw/day | Chronic: 5 days |
| ||
Bisphenol A (BPA) | Mouse liver | BPA water 50 μg/kg/day | Chronic: 10 weeks |
| [56] |
Bisphenol A (BPA) | Mouse liver | 50 µg/kg along with HFD (after 12 weeks of HFD feeding) | Chronic: 3 weeks |
| [58] |
Bisphenol A | Mouse liver | 50 mg/kg/bw along with HFCCD bw | Chronic: 8 weeks |
| [59] |
Bisphenol A (BPA) | Neonatal rat liver | 1.47 ng/mL | Acute: 1 h |
| [103] |
Bisphenol A (BPA) | Rat liver | 30 mg/kg bw/day | Chronic: 6 weeks |
| [57] |
Bisphenol A (BPA) | Rat liver | 50 mg/kg/day | Chronic: 4 weeks |
| [52] |
Bisphenol A (BPA) | Rat liver | 150 mg/kg, 250 mg/kg and 500 mg/kg | Chronic: 14 days |
| [53] |
Bisphenol A (BPA) | Rat liver | 10 and 50 mg/kg | Chronic: 30 days |
| [54] |
Bisphenol A (BPA) | Rat liver | 0.5 mg/kg (low dose), 5 mg/kg (medium dose, NOAEL) or 50 mg/kg (high dose) | Chronic: 30 days |
| [55] |
Bisphenol A (BPA) | Rat liver | 100 mg/kg | Chronic: 30 days |
| [66] |
Bisphenol A (BPA) | Rat liver | 90 and 270 mg/kg bw | Chronic: 30 days |
| [60] |
Bisphenol A (BPA) | Rat liver (L-NAME-induced hypertensive Wistar rats) | 50 µg/kg | Chronic: 30 days |
| [67] |
Bisphenol A (BPA) | Rat offspring liver | 40 µg/kg/day | Chronic: during gestation and lactation |
| [61] |
Bisphenol A | Rat liver (from pregnant rats and female postnatal day-6 offspring) | 0.036 mg/kg bw/day and 3.42 mg/kg bw/day | Chronic: during premating, mating, pregnancy, lactation |
| [62] |
Bisphenol A (BPA) | Common carp (Cyprinus carpio) liver | 0.1, 1, 10, 100 and 1000 µg/L | Chronic: 30 days |
| [63] |
Bisphenol A (BPA) | Common carp (Cyprinus carpio) liver | 4.5 and 6 mg/L | Chronic: 30 days |
| [64] |
Bisphenol A (BPA) and S (BPS) | Rat liver | 50 or 500 μg/kg/day of BPA or BPS; 50 μg/kg/day of both BPA and BPS | Chronic: 20 weeks |
| [69] |
Bisphenol S (BPS) | Mouse liver | 100 µg/kg/day in drinking water | Chronic: 10 weeks |
| [104] |
Bisphenol S (BPS) | Mouse liver | 0.1–1 mM | Acute: 12 h |
| [70] |
Bisphenol S (BPS) | Fish (Labeo rohita) liver | Groups II, III and IV were exposed to 80 mg BPS/L, Groups V, VI and VII were exposed to 100 mg BPS/L, and Groups VIII, IX and X to 120 mg BPS/L | Chronic: 7, 14 and 21 days |
| [72] |
Bisphenols: bisphenol A (BPA), bisphenol F (BPF) and bisphenol AF (BPAF) | Mouse offspring liver | 100 ng/g bw/day | Chronic: from the 7th day of pregnancy to the 21st day after delivery |
| [68] |
Bisphenol A (BPA) + nonylphenol (NP) | Rat liver | 100 µg/kg | Chronic: 56 consecutive days |
| [75] |
Nonylphenol (NP) | Zebrafish (Danio rerio) liver | 50 and 100 μg/L | Chronic: 21 days |
| [76] |
Polychlorinated biphenyls (PCBs) | Rat liver | Contaminated (two times the TDI) goat milk administered daily by gavage (6 µL/g bw) | Chronic: 8 weeks |
| [84] |
Polychlorinated biphenyls (PCBs)—PCB126 | Mouse liver | 1.53 μmol/kg | Chronic: 10 weeks |
| [85] |
Polychlorinated biphenyls (PCBs) and 2,3,7,8-Tetrachlorodibenzo-p-dioxin (TCDD) | Rat liver | TCDD at 3, 10 or 100 ng/kg/day; PCB 126 at 10, 100 or 1000 ng/kg/day; PCB 153 at 10, 100 or 1000 μg/kg/day; Binary mixture of PCB 126 and PCB 153 (10 ng/kg/day + 10 μg/kg/day, 100 ng/kg/day + 100 μg/kg/day or 1000 ng/kg/day + 1000 μg/kg/day | Chronic: 13 and 52 weeks |
| [81] |
Atrazine (ATZ) and its metabolite diaminochlorotriazine (DACT) | Mouse liver | ATZ and DACT (100 and 200 mg/kg/bw, respectively) | Chronic: 1 week |
| [86] |
Atrazine (ATZ) | HepG2 cells | 0.05–2 mM | Acute: 3 h and 6 h |
| [87] |
Di (2-ethylhexyl) phthalate (DEHP) | HSC-T6 cells | 50 and 100 µM | Chronic: 3.5 months |
| [93] |
Di (2-ethylhexyl) phthalate (DEHP) | Rat liver | 600 mg/kg/day | Chronic: 12 weeks |
| [94] |
Di (2-ethylhexyl) phthalate (DEHP) | Female quail (Coturnix japonica) liver | 250, 500 and 1000 mg/kg bw/day | Chronic: 45 days |
| [95] |
Mono-(2-ethylhexyl) phthalate (MEHP) | Zebrafish liver | 31.25, 62.5, 125, 250, 500 or 1000 mg/L | Acute: 24 h |
| [96] |
Perfluorooctane sulphonate (PFOS) | Rat liver | Single dose of 1 or 10 mg/kg body | Chronic: 28 consecutive days |
| [97] |
Polychlorinated diphenyl ethers (PCDEs) | Zebrafish liver | 1, 10 and 50 μg/L | Chronic: 14 days |
| [99] |
Endocrine disruptors mixture | Rabbit liver | 10 × ADI | Chronic: 12 months |
| [101] |
5. EDCs and Pancreatic Toxicity
5.1. Bisphenols (BPs)
5.2. Alkylphenols
5.3. Organotins
5.4. Mixture of EDCs
6. Discussion
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
List of Abbreviations
8-OHdG | 8-hydroxydeoxyguanosine |
α-SMA | alpha-smooth muscle actin |
ACE | angiotensin-converting enzyme |
ADI | acceptable daily intake |
ALP | alkaline phosphatase |
ALT | alanine aminotransferase |
AST | aspartate aminotransferase |
ATP | adenosine triphosphate |
ATZ | atrazine |
Bax | Bcl-2-associated X |
Bcl-2 | B-cell lymphoma-2 |
BPA | bisphenol A |
BPAF | bisphenol AF |
BPF | bisphenol F |
BPS | bisphenol S |
BPs | bisphenols |
BuPB | butylparaben |
BW | body weight |
CAT | catalase |
CoA | coenzyme A |
COX | cyclooxygenase |
COX-2 | cyclooxygenase-2 |
COX5B | cytochrome c oxidase subunit 5B mitochondrial |
COQ9 | ubiquinone biosynthesis protein COQ9_mitochondrial |
DACT | diaminochlorotriazine |
DDE | dichlorodiphenyldichloroethylene |
DEHP | di-(2-ethylhexyl) phthalate |
DES | diethylstilbestrol |
DNA | deoxyribonucleic acid |
EDCs | endocrine-disruptive chemicals |
ERK | extracellular signal-regulated kinase |
ETS | electron transport system |
F1 | first-generation adult mice offspring |
F2 | second-generation adult mice offspring |
GPx | glutathione peroxidase |
GPx3 | glutathione peroxidase 3 |
GR | glutathione reductase |
GSH | reduced glutathione |
GSHPx | glutathione peroxidase |
GSIS | glucose-stimulated insulin secretion |
GSSG | glutathione disulfide |
GST | glutathione-S-transferase |
H2O2 | hydrogen peroxide |
HFCCD | high-fat/high-cholesterol/high-cholic acid diet |
HFD | high-fat diet |
HSC | hepatic stellate cells |
IL-1β | interleukin-1β |
IL-6 | interleukin-6 |
iNOS | inducible nitric oxide synthase |
JAK/STAT | Janus kinase/signal transduction and transcription activation |
L-NAME | N-nitro-L-arginine methyl ester |
LPO | lipid peroxidation |
MAFLD | metabolic-associated fatty liver disease |
MAPK | mitogen-activated protein kinase |
MDA | malondialdehyde |
MDC | metabolism-disrupting chemicals |
MEHP | mono(2-ethylhexyl) phthalate |
MePB | methylparaben |
mtDNA | mitochondrial DNA |
MMP | mitochondrial membrane potential |
MRC | mitochondrial respiratory chain |
NAC | N-acetylcysteine |
NAFLD | non-alcoholic fatty liver disease |
NF-κB | nuclear factor kappa-B |
NO | nitric oxide |
NOAEL | no observed adverse effect level |
NP | nonylphenol |
Nrf1 | nuclear respiratory factor 1 |
Nrf2 | nuclear factor erythroid 2-related factor factor 2 |
NTP | National Toxicology Program |
OCR | oxygen consumption rate |
Ogdh | oxoglutarate degydrogenase |
OH-PCBs | hydroxylated PCBs |
OP | octylphenol |
OXPHOS | oxidative phosphorylation |
PARP-1 | poly [ADP-ribose] polymerase 1 |
PCBs | polychlorinated biphenyls |
PCDEs | polychlorinated diphenyl ethers |
PFOA | perfluorooctanoic acid |
PFOS | perfluorooctane sulfonate |
PGC-1α | peroxisome proliferator-activated receptor-gamma coactivator 1α |
PKC | protein kinase C |
PND6 | postnatal day 6 |
POD | peroxidase |
PrPB | propylparaben |
RNS | reactive nitrogen species |
ROS | reactive oxygen species |
Sdhb | succinate dehydrogenase iron-sulfur subunit |
SOD | superoxide dismutase |
SIRT1 | sirtuin-1 |
SIRT3 | sirtuin-3 |
T-AOC | total antioxidant capacity |
TBARS | thiobarbituric acid reactive substances |
TBT | trybutyltin |
TCDD | 2,3,7,8-tetrachlorodibenzo-p-dioxin |
TCS | triclosan |
TFAM | mitochondrial transcription factor A |
TPP | triphenylphosphate |
TDI | tolerable daily intake |
TNF-α | tumor necrosis factor-α |
UCP2 | uncoupling protein 2 |
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Endocrine Disruptor | Experimental Model | Dose | Duration | Effects | Ref. |
---|---|---|---|---|---|
Bisphenol A (BPA) | β-cells of rat offspring | 50, 250 or 1250 µg/kg/day | Chronic: during gestation and lactation |
| [106] |
Bisphenol A (BPA) | Primary murine pancreatic islets | M | Acute: 24 or 48 h |
| [107] |
Bisphenol A (BPA) | Pancreatic islets of mice offspring | 10 µg/kg/d (low dose) and 10 mg/kg/d (high dose) | Chronic: during gestation and lactation |
| [109] |
Bisphenol A (BPA) | αTC1-9 murine cell line | From 0.1 pM to 1 µM | Acute: 24 h |
| [115] |
Tributyltin (TBT) | αTC1-9 murine cell line | From 0.1 pM to 1 µM | Acute: 24 h |
| [115] |
Tributyltin (TBT) | β-cell-derived RIN-m5F rat cell line; pancreatic islets of mice and humans | 0.05–0.2 μM | Acute: 0.5–4 h |
| [114] |
Octylphenol (OP) | Pancreatic islets of rats | 25 µg/L | Acute: 24 h |
| [111] |
Nonylphenol (NP) | |||||
Bisphenol A (BPA) | |||||
4-Nonylphenol (NP) | Pancreatic islets of rats | 60 mg/kg and 180 mg/kg | Chronic: 90 consecutive days |
| [112] |
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Lința, A.V.; Lolescu, B.M.; Ilie, C.A.; Vlad, M.; Blidișel, A.; Sturza, A.; Borza, C.; Muntean, D.M.; Crețu, O.M. Liver and Pancreatic Toxicity of Endocrine-Disruptive Chemicals: Focus on Mitochondrial Dysfunction and Oxidative Stress. Int. J. Mol. Sci. 2024, 25, 7420. https://doi.org/10.3390/ijms25137420
Lința AV, Lolescu BM, Ilie CA, Vlad M, Blidișel A, Sturza A, Borza C, Muntean DM, Crețu OM. Liver and Pancreatic Toxicity of Endocrine-Disruptive Chemicals: Focus on Mitochondrial Dysfunction and Oxidative Stress. International Journal of Molecular Sciences. 2024; 25(13):7420. https://doi.org/10.3390/ijms25137420
Chicago/Turabian StyleLința, Adina V., Bogdan M. Lolescu, Cosmin A. Ilie, Mihaela Vlad, Alexandru Blidișel, Adrian Sturza, Claudia Borza, Danina M. Muntean, and Octavian M. Crețu. 2024. "Liver and Pancreatic Toxicity of Endocrine-Disruptive Chemicals: Focus on Mitochondrial Dysfunction and Oxidative Stress" International Journal of Molecular Sciences 25, no. 13: 7420. https://doi.org/10.3390/ijms25137420