Nielsen G, Gondim D D, Cave M C, Heiger-Bernays W J, Webster T F, Schlezinger J J
Department of Environmental Health, School of Public Heath, Boston University, Boston, MA, USA.
Division of Gastroenterology, Hepatology and Nutrition, University of Louisville, Louisville, KY, USA.
Arch Toxicol. 2025 May;99(5):2087-2105. doi: 10.1007/s00204-025-03984-7. Epub 2025 Mar 1.
Per- and polyfluoroalkyl substances (PFAS) are a large group of persistent chemicals that are pervasive in the environment leading to widespread exposure for humans. Perfluorooctanoic acid (PFOA), one of the most commonly measured PFAS in people, disrupts liver and serum lipid homeostasis as shown in animal toxicity and human epidemiological studies. We tested the hypothesis that the effects of PFOA exposure in mice expressing mouse PPARα (mPPARα) are driven largely through PPARα-dependent mechanisms while non-PPARα dependent mechanisms will be more apparent in mice expressing human PPARα (hPPARα). Female and male mPPARα, hPPARα, and PPARα null mice were exposed to PFOA (0.5, 1.4 or 6.2 mg PFOA/L) via drinking water for 14 weeks. Concurrently, mice consumed an American diet containing human diet-relevant amounts of fat and cholesterol. Here, we focused on the effects in female mice, given the dearth of data reported on PFAS-induced effects in females. Increasing the duration of PFOA exposure reduced weight gain in all genotypes of female mice while end-of-study body fat was lower in PFOA exposed hPPARα and PPARα null mice. Serum cholesterol, but not triacylglyceride, concentrations were increased by PFOA exposure in a PPARα-dependent manner. Hepatic triacylglycerides were higher in vehicle-exposed mPPARα and PPARα null mice than hPPARα mice, and PFOA significantly reduced concentrations in mPPARα and PPARα null mice only. In contrast, PFOA increased hepatic cholesterol content in a PPARα-dependent manner. Changes in liver and serum cholesterol may be explained by a strong, PPARα-dependent downregulation of Cyp7a1 expression. PFOA significantly increased PPARα target gene expression in mPPARα mice. Other nuclear receptors were examined: CAR target gene expression was only induced by PFOA in hPPARα and PPARα null mice. PXR target gene expression was induced by PFOA in all genotypes. Results were similar in male mice with two exceptions: (1) vehicle-exposed male mice of all genotypes were equally susceptible to diet-induced hepatic steatosis; (2) male mice drank less water, resulting in lower serum PFOA levels, which may explain the less significant changes in lipid endpoints. Overall, our results show that PFOA modifies triacylglyceride and cholesterol homeostasis independently and that PPARα plays an important role in PFOA-induced increases in liver and serum cholesterol.
全氟和多氟烷基物质(PFAS)是一大类持久性化学物质,在环境中广泛存在,导致人类普遍暴露。全氟辛酸(PFOA)是人体中最常检测到的PFAS之一,动物毒性和人类流行病学研究表明,它会破坏肝脏和血清脂质稳态。我们检验了以下假设:在表达小鼠PPARα(mPPARα)的小鼠中,PFOA暴露的影响主要通过PPARα依赖性机制驱动,而非PPARα依赖性机制在表达人类PPARα(hPPARα)的小鼠中会更明显。雌性和雄性mPPARα、hPPARα和PPARα基因敲除小鼠通过饮用水接触PFOA(0.5、1.4或6.2毫克PFOA/升),持续14周。同时,小鼠食用含有与人类饮食相关量脂肪和胆固醇的美式饮食。鉴于关于PFAS对雌性影响的数据较少,我们在此重点关注雌性小鼠的影响。延长PFOA暴露时间会降低所有基因型雌性小鼠的体重增加,而在暴露于PFOA的hPPARα和PPARα基因敲除小鼠中,研究结束时的体脂较低。PFOA暴露以PPARα依赖性方式增加血清胆固醇浓度,但不影响甘油三酯浓度。在饮用对照剂的mPPARα和PPARα基因敲除小鼠中,肝脏甘油三酯含量高于hPPARα小鼠,PFOA仅显著降低mPPARα和PPARα基因敲除小鼠中的甘油三酯浓度。相反,PFOA以PPARα依赖性方式增加肝脏胆固醇含量。肝脏和血清胆固醇的变化可能是由于Cyp7a1表达的强烈PPARα依赖性下调所致。PFOA显著增加mPPARα小鼠中PPARα靶基因的表达。还检测了其他核受体:仅在hPPARα和PPARα基因敲除小鼠中,PFOA诱导CAR靶基因表达。在所有基因型中,PFOA均诱导PXR靶基因表达。雄性小鼠的结果相似,但有两个例外:(1)所有基因型饮用对照剂的雄性小鼠对饮食诱导的肝脂肪变性同样敏感;(2)雄性小鼠饮水量较少,导致血清PFOA水平较低,这可能解释了脂质终点变化不太显著的原因。总体而言,我们的结果表明,PFOA独立调节甘油三酯和胆固醇稳态,并且PPARα在PFOA诱导的肝脏和血清胆固醇升高过程中起重要作用。