Integrated Systems Toxicology Division, National Health and Environmental Effects Research Laboratory, U.S. Environmental Protection Agency, 109 T.W. Alexander Dr, MD-B105-03, Research Triangle Park, NC, 27711, USA.
The Department of Veterinary and Biomedical Sciences and Center for Molecular Toxicology and Carcinogenesis, The Pennsylvania State University, University Park, PA, 16803, USA.
Arch Toxicol. 2018 Jan;92(1):83-119. doi: 10.1007/s00204-017-2094-7. Epub 2017 Dec 2.
A number of industrial chemicals and therapeutic agents cause liver tumors in rats and mice by activating the nuclear receptor peroxisome proliferator-activated receptor α (PPARα). The molecular and cellular events by which PPARα activators induce rodent hepatocarcinogenesis have been extensively studied elucidating a number of consistent mechanistic changes linked to the increased incidence of liver neoplasms. The weight of evidence relevant to the hypothesized mode of action (MOA) for PPARα activator-induced rodent hepatocarcinogenesis is summarized here. Chemical-specific and mechanistic data support concordance of temporal and dose-response relationships for the key events associated with many PPARα activators. The key events (KE) identified in the MOA are PPARα activation (KE1), alteration in cell growth pathways (KE2), perturbation of hepatocyte growth and survival (KE3), and selective clonal expansion of preneoplastic foci cells (KE4), which leads to the apical event-increases in hepatocellular adenomas and carcinomas (KE5). In addition, a number of concurrent molecular and cellular events have been classified as modulating factors, because they potentially alter the ability of PPARα activators to increase rodent liver cancer while not being key events themselves. These modulating factors include increases in oxidative stress and activation of NF-kB. PPARα activators are unlikely to induce liver tumors in humans due to biological differences in the response of KEs downstream of PPARα activation. This conclusion is based on minimal or no effects observed on cell growth pathways and hepatocellular proliferation in human primary hepatocytes and absence of alteration in growth pathways, hepatocyte proliferation, and tumors in the livers of species (hamsters, guinea pigs and cynomolgus monkeys) that are more appropriate human surrogates than mice and rats at overlapping dose levels. Despite this overwhelming body of evidence and almost universal acceptance of the PPARα MOA and lack of human relevance, several reviews have selectively focused on specific studies that, as discussed, contradict the consensus opinion and suggest uncertainty. In the present review, we systematically address these most germane suggested weaknesses of the PPARα MOA.
许多工业化学物质和治疗剂通过激活核受体过氧化物酶体增殖物激活受体 α(PPARα)在大鼠和小鼠中引起肝肿瘤。PPARα 激活剂诱导啮齿动物肝癌发生的分子和细胞事件已被广泛研究,阐明了与肝肿瘤发生率增加相关的许多一致的机制变化。这里总结了与 PPARα 激活剂诱导的啮齿动物肝癌发生的假设作用模式(MOA)相关的大量证据。化学特异性和机制数据支持与许多 PPARα 激活剂相关的关键事件的时间和剂量反应关系的一致性。MOA 中确定的关键事件(KE)包括 PPARα 激活(KE1)、细胞生长途径的改变(KE2)、肝细胞生长和存活的干扰(KE3)以及前肿瘤灶细胞的选择性克隆扩增(KE4),这导致了顶端事件——肝细胞腺瘤和癌的增加(KE5)。此外,许多同时发生的分子和细胞事件被归类为调节因子,因为它们可能改变 PPARα 激活剂增加啮齿动物肝癌的能力,而本身不是关键事件。这些调节因子包括氧化应激增加和 NF-kB 激活。由于 PPARα 激活下游 KE 反应的生物学差异,PPARα 激活剂不太可能在人类中引起肝肿瘤。这一结论基于在人类原代肝细胞中观察到的细胞生长途径和肝细胞增殖的最小或无影响,以及在物种(仓鼠、豚鼠和食蟹猴)肝脏中生长途径、肝细胞增殖和肿瘤的改变缺失,这些物种比小鼠和大鼠更适合作为重叠剂量水平的人类替代物。尽管有大量的证据和几乎普遍接受的 PPARα MOA 以及缺乏人类相关性,但一些综述选择性地关注了特定的研究,正如讨论的那样,这些研究与共识意见相矛盾,并表明存在不确定性。在本综述中,我们系统地解决了 PPARα MOA 最相关的这些弱点。