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化学进展 2022, Vol. 34 Issue (1): 227-236 DOI: 10.7536/PC210443 前一篇   

• 综述 •

致癌性卤代醌类消毒副产物造成 DNA 损伤的分子机理研究

朱本占1,2,*(), 张静1,2, 唐苗1,2, 黄春华1,3, 邵杰1,2,*()   

  1. 1 中国科学院生态环境研究中心 环境化学与生态毒理学国家重点实验室 北京 100085
    2 中国科学院大学 北京 100049
  • 收稿日期:2021-04-25 修回日期:2021-06-26 出版日期:2022-01-20 发布日期:2021-07-29
  • 通讯作者: 朱本占, 邵杰
  • 基金资助:
    中国科学院战略性先导科技专项项目(XDB14030100); 中国科学院基础前沿科学研究计划从“0”到“1”原始创新项目(ZDBS-LY-SLH027); 国家自然科学基金项目(21976200); 国家自然科学基金项目(21207150); 国家自然科学基金项目(21836005); 国家自然科学基金项目(21621064); 国家自然科学基金项目(21321004); 中科院生态环境研究中心青年科学家基金(RCEES-QN-20130052F)
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Mechanism Investigation on DNA Damage Induced by Carcinogenic Haloquinoid Disinfection Byproducts

Benzhan Zhu1,2(), Jing Zhang1,2, Miao Tang1,2, Chunhua Huang1,3, Jie Shao1,2()   

  1. 1 State Key Laboratory of Environmental Chemistry and Ecotoxicology, Research Center for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085,China
    2 University of Chinese Academy of Sciences, Beijing 100049, China
  • Received:2021-04-25 Revised:2021-06-26 Online:2022-01-20 Published:2021-07-29
  • Contact: Benzhan Zhu, Jie Shao
  • Supported by:
    Strategic Priority Research Program Chinese Academy Sciences(XDB14030100); from "0" to "1" Original Innovation Project of the Basic Frontier Science Research Program of the Chinese Academy of Sciences(ZDBS-LY-SLH027); Natianal Natural Science Foundation of China(21976200); Natianal Natural Science Foundation of China(21207150); Natianal Natural Science Foundation of China(21836005); Natianal Natural Science Foundation of China(21621064); Natianal Natural Science Foundation of China(21321004); Young Scientist Foundation of Research Center for Eco-Environmental Sciences(RCEES-QN-20130052F)

卤代醌是一类卤代芳烃类环境污染物的致癌中间体,也是在饮用水中新发现的氯化消毒副产物。我们最近发现卤代醌和 H2O2 或有机氢过氧化物体系可以不依赖过渡金属离子,而产生高活性的羟基/烷氧自由基和醌氧/醌碳自由基。目前尚不清楚这些卤代醌类致癌物和氢过氧化物共存能否诱导 DNA 产生氧化损伤和修饰,以及其潜在的分子机制是什么。我们的研究发现 DNA 在四氯-1,4-苯醌/H2O2体系中可被氧化产生 8-氧脱氧鸟苷、DNA 链断裂和三种甲基氧化产物,这些反应不依赖过渡金属离子,且由于卤代醌与 DNA 的嵌入作用而导致其氧化作用增强。其他卤代醌也观察到了类似的现象,而且通常比经典的 Fenton 体系更有效。我们进一步将研究从纯化的 DNA 扩展到了活细胞的基因组 DNA。同时还发现卤代醌和有机氢过氧化物(如叔丁基过氧化氢或在正常生理条件下产生的 13S-过氧羟基-9Z,11E-十八碳二烯酸(13-HPODE))共存时,可通过独特的醌氧自由基介导机制诱导 DNA 氧化生成致突变性更强的咪唑啉酮类产物 dIz。这些发现为解释普遍存在的卤代醌类致癌中间体和消毒副产物的潜在基因毒性、致突变性和致癌性提供了新思路。

关键词： 卤代醌, 氢过氧化物, 自由基, DNA 损伤, 基因毒性

Halobenzoquinones (HBQs) are a class of toxic intermediates of the haloaromatic persistent organic pollutants and newly identified chlorination disinfection byproducts in drinking water and swimming pool water. The highly reactive hydroxyl/alkoxyl radicals and quinone enoxy/ketoxy radicals were found to be produced by HBQs with H2O2 or organic hydroperoxides metal-independently. However, it remains unknown whether HBQs and hydroperoxides can induce DNA damage, and if so, what are the underlying molecular mechanisms. We found that 8-oxodeoxyguanosine (8-oxodG), DNA strand breaks and three methyl oxidation products could be generated from DNA oxidation by tetrachloro-1,4-benzoquinone (TCBQ) and H2O2 via an intercalation-enhanced oxidation mechanism. Analogous effects were observed with other HBQs, which are generally more effective than the classic iron-mediated Fenton system. Further investigations were extended from isolated DNA to genomic DNA in living cells. Potent oxidation of DNA to the more mutagenic imidazolone dIz was also found to be induced by HBQs and organic hydroperoxides such as the physiologically-relevant hydroperoxide 13S-hydroperoxy-9Z,11E-octadecadienoic acid (13-HPODE) via a unique quinone-enoxy radical-mediated mechanism. These findings should provide new perspectives to explain the potential genotoxicity, mutagenesis, and carcinogenicity for the ubiquitously-present haloaromatic persistent organic pollutants.

Contents

1 Introduction

2 Potent oxidative DNA damage by HBQs and H2O2 via an intercalation-enhanced oxidation mechanism

3 Detection of HQ-induced DNA damage by photoelectrochemical DNA sensor

4 Genotoxicity and mutagenesis induced by TCHQ in mammalian cells

5 Potent methyl oxidation of 5-methyl-2'-deoxycytidine (5mCyt) by HBQs and H2O2

6 Genome-wide DNA methylation alterations induced by HBQs and other redox-active quinones at cellular level

7 Potent oxidation of DNA by HBQs/organic hydroperoxides to the more mutagenic imidazolone dIz via the reactive haloquinone-enoxy radicals

8 Conclusion

Key words: halobenzoquinones, hydroperoxides, free radicals, DNA damage, genotoxicity
()
图1 TCBQ 和 TCHQ 是 PCP 主要的两种具有遗传毒性和致癌性的醌类代谢产物
Fig.1 TCBQ and TCHQ are two major genotoxic and carcinogenic quinoid metabolites of PCP
图2 卤代醌可通过不依赖过渡金属离子的过程经过亲核取代及均裂分解的反应机制促进氢过氧化物的分解,产生烷氧/羟基自由基、醌碳自由基及醌氧自由基
Fig. 2 Mechanism of enhancement by HBQs of the decomposition of hydroperoxides and formation of alkoxyl/hydroxyl radicals and quinone ketoxy/enoxy radicals metal-independently via nucleophilic substitution followed by homolytical decompositionreaction.
图3 本文提到的卤代醌的化学结构
Fig. 3 The chemical structures of HQs in this study
图4 TCBQ/H2O2 体系通过不依赖金属离子的过程产生 5 mC 甲基氧化产物的可能机理[63]:首先,TCBQ/H2O2体系产生的·OH可夺取 5mC的甲基上的氢生成相应的自由基,其与 O2结合后生成对应的过氧自由基中间体;这种过氧自由基很不稳定,转化成氢过氧化物 5HpmC,其与 TCBQ发生亲核取代及均裂反应生成5-CH2O·;该自由基进一步歧化生成5HmC和 5fC
Fig. 4 Proposed mechanism for the formation of 5mCyt oxidation products by TCBQ and H2O2 via a metal-independent pathway (modified according to Ref 63). First, ·OH produced by TCBQ/H2O2 may abstract hydrogen atom from the methyl group of 5mC, leading to the formation of 5-(2'-deoxycytidylyl)methyl radical, which then combines with O2 to form its corresponding peroxyl radical. The unstable peroxyl radical can transform into 5HpmC. 5HmC and 5fC were produced via dismutation of 5-CH2O· formed through a nucleophilic substitution followed homolytical decomposition reaction.
图5 TCBQ 和t-BuOOH 不依赖过渡金属离子通过醌氧自由基中间体生成 Gua 氧化产物的机制[79]:首先,TCBQ/t-BuOOH体系产生的醌氧自由基可夺取Gua上的氢生成Gua·+,其在生理条件下生成Gua(-H)·。该自由基与O2结合后生成氢过氧化物。该过氧化物经过一系列重排生成Iz。通过类似机理,开始生成的8-oxoG通过单电子氧化和重排反应也可以生成Iz,Iz不稳定进一步水解生成Oz
Fig. 5 Proposed mechanism for the formation of Gua oxidation products by TCBQ and t-BuOOH via quinone enoxy radical intermediates in a metal-independent pathway (modified according to Ref 79). First, the quinone enoxy radical produced by TCBQ/t-BuOOH may abstract one electron from Gua to generate Gua·+, which deprotonates at physiological pH to produce Gua(-H)·. Gua(-H)· combines with O2 and then transforms into the corresponding hydroperoxide 5-HOO-Gua(-H). The decarboxylation of 5-HOO-Gua(-H) and further rearrangement lead to the formation of the imidazolone lesion. In a similar way, the initially produced 8-oxoG would result in the formation of Iz after one-electron oxidation and rearrangement. The imidazolone lesion could further hydrolyze to form the oxazolone (Oz) lesion.
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