Advances in DNA damage induced by environmental chemical carcinogens
Review Article
Genome Instability & Disease 3, 317–330 (2022)
Abstract
Chemical carcinogens, which are exogenous DNA-damaging agents, are ubiquitous in both the industry and living environments. The carcinogens pose a threat to the integrity of genetic information by causing diverse types of DNA damage through various pathways. Subsequently, the organism activates a DNA damage response mechanism to repair the damage caused by chemical carcinogens. However, incorrect or ineffective repair processes, along with DNA damage accumulation, may lead to genomic instability and mutations, which play a critical role in carcinogenesis. However, the types of DNA damage induced by a large variety of chemical carcinogens may vary due to the different physicochemical properties of chemicals and ultimately affect the carcinogenic process. In this review, we discuss the mechanisms of DNA damage and ultimately carcinogenesis by various environmental chemical carcinogens, namely heavy metals, polycyclic aromatic hydrocarbons, and aromatic amines. We also summarize the potential types of DNA damage that are closely associated with carcinogens.
Introduction
Cancer control has always been a challenge in the medical field. In addition to genetic factors, numerous environmental factors, including chemical, physical, and biological carcinogens, contribute to cancer occurrence and development (Belpomme et al., 2007). Approximately 80% of human cancers are caused by exposure to chemical carcinogens (Higginson, 1993). More than sixty chemicals, which are widespread in the industry and living environments, have been identified as Group 1 carcinogens by the International Agency for Research on Cancer (IARC) (Ian et al., 2022).
Most chemical carcinogens are exogenous DNA-damaging agents, which threaten the integrity of the genetic information. To counter this threat, through billions of years of evolution, living organisms have developed DNA damage response (DDR) systems, which detect and repair DNA damage (Jackson & Bartek, 2009). However, a faulty repair mechanism can cause the accumulation of DNA errors, which are a major source of genomic instability and mutations (Guo et al., 2019; Saitoh & Oda, 2021; Schiewer & Knudsen, 2019), leading to the inactivation of tumor suppressor genes and activation of oncogenes. Thus, DNA damage is regarded as an early event in carcinogenesis (Basu, 2018; Roos et al., 2016). Identifying chemical-induced DNA damage and exploring its role in carcinogenesis may contribute to cancer prevention and therapy. However, due to the diversity in chemicals, the types of DNA damage induced by different physicochemical properties of chemical carcinogens may vary. In this review, we focus on major common chemical carcinogens and describe their role in inducing DNA damage and ultimately carcinogenesis, according to chemical classifications.
Types of DNA damage
Exposure to carcinogens causes various types of DNA damage, such as single-stand breaks (SSBs), double-strand breaks (DSBs), bulky DNA adducts, DNA base modification, and intra/inter-strand crosslinks (Barnes et al., 2018; Poirier, 2012) (Fig. 1).
Fig. 1
Types of DNA damage
DNA single-strand break
DNA SSBs are discontinuities in one strand of the DNA double helix and are usually associated with damage or mismatches at the 5'- and/or 3'-terminus. These are the most common type of DNA damage in cells, occurring several times per cell per day. DNA SSBs can arise from oxidized nucleotides/bases during oxidative stress, intermediate products of DNA repair pathways, and aborted activities of cellular enzymes. If DNA SSBs are not repaired quickly or accurately, they will subsequently develop into DNA DSBs (Higo et al. 2017), which pose a serious threat to genetic stability and cell survival (Abbotts & Wilson, 2017).
DNA double-strand breaks
DSBs occur when two complementary DNA strands are simultaneously broken at the same location or in close proximity to each other. Although only 10–50 DNA DSBs occur per cell per day, which is 1/20–1/30 of DNA SSBs, DSBs are highly deleterious, because they can lead to cell death, as well as deletions, translocations, and DNA fusions, if unrepaired or improperly repaired. DSBs are mainly caused by ionizing radiation and environmental pollutant exposures. In addition, DSBs can be caused directly or indirectly by other types of DNA damage. For example, replication forks progress to SSBs or inter-strand crosslinks, which might result in further DNA double-strand damage during cell replication. Accumulation of DSB damage leads to genetic instability, which in turn may increase the risk of cancer development (Khanna & Jackson, 2001).
Bulky DNA adducts
Bulky DNA adducts are indicators of genotoxic aromatic chemical exposure and reflect an individual's capacity to activate carcinogens metabolically and repair DNA damage. Most carcinogens require metabolic activation, and bulky DNA adducts result from the covalent interactions of electrophilic chemical carcinogens with the nucleophilic sites in DNA (Ewa & Danuta, 2017). DNA adducts of these carcinogens can be formed on various ring nitrogen, exocyclic nitrogen, and oxygen atoms of nucleobases. The type of DNA adducts formed depends on the structure of the reactive chemical, nature of the electrophile, and ability of the compound to intercalate with DNA (Hwa Yun et al., 2020), which may direct specific nucleophilic sites on DNA bases to form adducts. DNA adducts interfere with DNA transcription and replication and, if not repaired, can lead to cancer-specific mutations. Therefore, the formation of DNA adducts is a critical step in initiating carcinogenesis.
DNA base modification
DNA base modification is induced by oxidation, methylation, and alkylation changes (Gavande et al., 2016; Lord & Ashworth, 2012). Exposure to certain chemicals can directly or indirectly generate reactive oxygen species (ROS), which can lead to oxidative stress (Klaunig, 2018). The nitrogenous bases of DNA are easily oxidized by endogenous and exogenous oxidants, causing extensive oxidative DNA damage (Marnett, 2000). In addition to chain scission due to a direct attack on the phosphate backbone, nitrogenous bases can be modified by free radicals. If these lesions are not repaired or repair attempts fail, mutations and strand breaks subsequently occur, permanently altering the DNA sequence (Klages-Mundt & Li, 2017). Thus, DNA oxidation products are direct risk factors for genome stability. Guanine is most easily destroyed by oxidants owing to its low reduction potential. It generally pairs with cytosine, whereas the most common type of oxidized base damage, 8-oxo-7,8-dihydroguanine (8-oxoG), may lead to its mismatches with adenine through conformational changes (Poetsch, 2020). This is a common pathway for oxidative DNA damage-induced mutations. Therefore, 8-oxoG is the most abundant form of oxidative DNA damage, which has been extensively studied. Alkylation is the most mutagenic type of base lesions, mainly from alkylating agents’ exposure, such as formaldehyde, ethanol, and polycyclic aromatic hydrocarbons (Bauer et al., 2015). O6-alkylG is the most likely alkylation site to cause mutations (Drabløs et al., 2004). Adding alkyl groups at the guanine O6 site causes G:C → T:A transversion. Transferring the methyl of S-adenosylmethionine to the base causes DNA methylation. The methylation of cytosine to 5-methylcytosine at CpG site is a typical event of DNA base modification. Abnormal DNA methylation patterns at the CpG sites are often observed in cancer (Li et al., 2013).
Inter-/intra-strand crosslinks
Unwinding the DNA double helix is essential for cellular processes, such as DNA replication and transcription. Cross-linking reagents function by forming irreversible covalent crosslinks between two nucleotide residues of the same DNA strand (i.e., intra-strand crosslinks) or opposite strands (i.e., inter-strand crosslinks), hindering DNA strand separation. Thus, DNA cross-linking is extremely toxic to cells and forms the molecular basis for cellular chromosomal aberrations that affect cellular function and DNA replication.
Carcinogenic chemical-induced DNA damage
Carcinogenic chemicals are extremely diverse in structure and function and can be divided into the following two categories: direct-acting and indirect-acting carcinogens, according to the difference in inducing DNA damage directly or indirectly, respectively (Lutz, 1986). Direct-acting carcinogens, due to their electrophilic groups, can directly induce DNA damage by interacting with nitrogen and oxygen atoms in DNA and other cellular components without the need for metabolic activation or any molecular modification (Cohen & Arnold, 2011; Ravanat & Douki, 2016). Due to the relative inactivity of the parent compound, indirect-acting carcinogens typically require metabolic bioactivation by intracellular cytochrome P450 enzymes to carcinogenic metabolites or reactive intermediates, such as polycyclic aromatic hydrocarbons, heterocyclic aromatic amines, and N-nitrosamines, which can exert genotoxic effects (Harris et al., 2020). Most chemical carcinogens belong to this category.
Heavy metals
Almost all heavy metals are toxic (Khanam et al., 2020; Shahjahan et al., 2022). However, owing to their chemical and physiological properties, heavy metals are still widely used in industrial fields, such as alloying, smelting, and manufacturing commercial products (Ali et al., 2019). In addition to industrial production, waste from industrial processes is a major source of environmental metal pollution and human metal exposure (Vardhan et al., 2019). Heavy metals such as arsenic, cadmium (Cd), and chromium are classified as group 1 carcinogens by the IARC (Ian et al., 2022). Numerous epidemiological studies have shown that occupational exposure to these heavy metals is associated with increased risks of several severe cancers (Khlifi et al., 2013).
Several common mechanisms are involved in the development of cancers induced by heavy metals. Heavy metals cause redox processes that convert high-valent metal ions to low-valent metal ions while also generating a lot of free radicals, which trigger oxidative stress responses and cause various types of DNA damage. Additionally, heavy metals can inhibit the DNA repair pathways by interacting with DNA repair proteins or binding directly to the zinc finger structural domain, leading to the unrepaired or improperly repaired DNA damages (Hartwig, 1998; Hartwig & Schwerdtle, 2002).
Cadmium
The heavy metal Cd is an environmental contaminant found in natural and industrial emissions (Lin et al., 2018; Schwartz & Reis, 2000). Cd is highly toxic and exposure to it causes lung and kidney cancers (García-Esquinas et al., 2014; Il'yasova & Schwartz, 2005). The effects of Cd on genome stability are presumably indirect, mainly via an increase in oxidative stress, causing DNA damage, and inhibiting DNA damage repair (Joseph, 2009; Rani et al., 2014). Oxidative stress can occur indirectly by forming complexes with small peptides and proteins through sulfhydryl groups (SH) (Bishak et al., 2015). It can also be generated by replacing redox-active bio-metals (e.g., iron and copper) in the cytoplasm and membrane proteins through the Fenton reaction (Filipic et al., 2006), leading to various types of DNA damage, including oxidative DNA damage, DNA strand breaks, and DNA–protein crosslinks (Fatur et al., 2002; Tarhonska et al., 2022). Inhibition of DNA repair is also an important mechanism in Cd-induced cancers, resulting in insufficient repair mechanisms and accumulation of DNA damages, thus promoting cancer development (Giaginis et al., 2006). Malignant cells transformed in vitro by exposure to low doses of Cd present abnormal gene expression profiles in DNA repair signaling pathways (Oldani et al., 2020; Tan et al., 2019), with DNA SSBs and DSBs, which induce micronuclei, gene mutations, and genomic instability (Filipič, 2012). Cd can interact with DNA repair proteins to inhibit major DNA repair pathways. For example, Cd can inhibite the base excision repair by reducing the activity of 8-oxoguanine glycosylase (OGG1) (Bravard et al., 2010) and downregulate the binding of XPA protein to DNA impeding nucleotide excision repair (Kopera et al., 2004), or interference with mismatch recognition proteins, MSH2-MSH6 and MSH2-MSH3, to initiate DNA mismatch repair (Banerjee & Flores-Rozas, 2005; Wieland et al., 2009). In addition, Cd can alter the structure and function of p53 by displacing zinc, thus impairing p53 activity (Hamann et al., 2012; Hartwig, 2010; Yu et al., 2011).
Arsenic
Arsenic exposure mainly originates from arsenic-contaminated water or organisms growing in arsenic-contaminated soil (Mondal et al., 2021). The most common toxic inorganic forms are arsenic (III) and arsenic (V) (Yamamura & Amachi, 2014). Arsenic (III) is transported into cells via aquaporin 9, a water/glycerol transporting protein (Stamatelos et al., 2011); arsenic (V) enters cells through phosphate transporters (Chen et al., 2021). Purine nucleoside phosphorylase reduces arsenic (V) to the more toxic arsenic (III) (Németi & Gregus, 2007). Long-term arsenic exposure is associated with increased risks of various cancers in the bladder, lung, kidney, liver, prostate, and skin (Li et al., 2022a; Maiti et al., 2012; Mostafa et al., 2008; Saint-Jacques et al., 2014; Wang et al., 2014). Arsenic does not directly interact with DNA but leads to cancer mainly by inducing oxidative stress and inhibiting DNA repair pathways (Chen et al., 2019; Huang et al., 2004; Nail et al., 2022). Oxidative stress can generate ROS and reactive nitrogen species through mitochondrial dysfunction, antioxidant imbalance, and the activation of NADPH oxidase and nitric oxide synthase. These species attack DNA bases, cause DNA damage, and generate DNA oxidative damage products such as 8-hydroxy-2′-deoxy-guanosine, 5-methylcytosine, and 5-hydroxymethylcytosine, which are widely used as biomarkers for DNA oxidative damage (De Vizcaya-Ruiz et al., 2009; Niedzwiecki et al., 2015; Tsai et al., 2021; Wang et al., 2021). Chronic arsenic exposure can induce malignant transformation of various cells, including human bronchial epithelial cells (Stueckle et al., 2012), rat liver epithelial cells (Liu & Waalkes, 2008), human prostate epithelial RWPE-1 cells (Treas et al., 2013), and mouse embryonic fibroblasts (Barguilla et al., 2020), causing oxidative DNA damage (Tokar et al., 2014). In addition to its independent toxicity, arsenic mainly acts as an auxiliary carcinogen, enhancing the carcinogenic effects of other carcinogens at environmental concentrations (Burns et al., 2004; Li et al., 2019; Zhou et al., 2019, 2021). Thus, the DNA repair systems are highly sensitive to arsenic exposure even at low concentrations (Zhou et al., 2021). The primary mechanism for co-carcinogenesis is the inhibition of DNA repair pathways by direct binding to zinc finger domains, which can alter the activity of DNA repair proteins involved in the repair of nucleotide excision, base excision, DSB, and mismatch (Zhou et al., 2021). Chronic arsenic exposure is more likely to lead to faulty repairs which destabilize the genome, ultimately causing cancer (Nail et al., 2022). Several epigenetic changes have also been observed in the arsenic-induced DNA damage. For example, the DNA methylation biomarker N7-methylguanine is elevated after arsenic exposure (Tsai et al., 2021), and the histone demethylase JHDM2A inhibits nucleosides in arsenic-induced lesions acid levels express DDB2, which is a key factor in DNA repair (Li et al., 2022a).
Chromium (VI)
Chromium is abundant in the earth’s crust and is often used in industrial production. It can coexist in multiple valence states in the environment; however, only chromium (III) and (VI) are considerably toxic (Sawicka et al., 2021) and are important carcinogens of the digestive and respiratory systems (Balali-Mood et al., 2021; Deng et al., 2019; Yatera et al., 2018). Chromium (VI) is more carcinogenic than the other valence states mainly because it is absorbed by the cell and rapidly reduced to intermediates chromium (V), chromium (IV), and chromium (III), and producing a large amount of active hydroxyl radicals (Luo et al., 1996). These species can induce various types of DNA damage, including DNA adduct formation, SSBs, DSBs, and the crosslinks of DNA duplexes and DNA–protein (Arakawa et al., 2012; DeLoughery et al., 2015; Ferreira et al., 2019; VonHandorf et al., 2021; Wang et al., 2017; Wise et al., 2008). Epidemiological studies have shown significant positive associations between environmental exposure to chromium and DNA damage levels and the risk of lung, stomach, and oral cancer (Sharma et al., 2012; Welling et al., 2015; Yuan et al., 2011). Long-term exposure to chromium (VI) can cause DNA DSBs (DeLoughery et al., 2015) and reduce E2F1 transcription factor levels. E2F1 is the predominant transcription factor for the DNA repair protein RAD51, which is involved in DNA DSB repair via homologous recombination (Choi & Kim, 2019). Chromium (VI) can inhibit the formation of RAD51 nuclear foci, leading to the failure to repair DSBs (Browning & Wise, 2017b; Browning et al., 2016b; Qin et al., 2014; Speer et al., 2021). In addition, chromium (VI) specifically targets the genomic regions around the binding sites for the transcription factors CTCF and AP1 in the nucleosomal architecture of euchromatin. These changes alter the DNA-binding capacity of key transcription factors, which in turn leads to altered chromatin states that disrupt gene transcription in functionally relevant biological processes (VonHandorf et al., 2018). This leads to the main tumor manifestations, such as malignant cell migration and invasion (Ma et al., 2022).
Polycyclic aromatic hydrocarbons
Polycyclic aromatic hydrocarbons are ubiquitous persistent environmental pollutants formed mainly from the incomplete combustion of organic matter. Several polycyclic aromatic hydrocarbons have been identified in the environment, some of which are carcinogens, such as benzo[a]pyrene (Bukowska et al., 2022; Reizer et al., 2019). Benzo[a]pyrene is also an indicator of carcinogenicity of other polycyclic aromatic hydrocarbons (Agency for Toxic Substances & Disease Registry, 2022). Deng et al. treated male mice with benzo[a]pyrene for 24 h and observed DNA damage in the liver and lung, which was significantly higher than that in the kidney, stomach, and brain (Deng et al., 2018), thus identifying the target organs for benzo[a]pyrene. Numerous epidemiological studies have associated benzo[a]pyrene exposure with increased risks for many types of cancers, including those of the lung, kidney, liver, bladder, breast, skin, and stomach (Amadou et al., 2021; Dybing et al., 2008; Enuneku et al., 2021; Gürbüz et al., 2021; Labib et al., 2012; Nakayama et al., 1984; Xue et al., 2022; Zhao et al., 2018). Although benzo[a]pyrene has been classified as a human carcinogen, it is an indirect carcinogen. Its metabolic activation is catalyzed by cytochrome P450 (CYP) enzymes (e.g., CYP1A1 and CYP1B1) to produce the ultimate carcinogenic form of benzo(a)pyrene, 7,8-dihydrodiol-9,10-epoxide (BPDE) (Moorthy et al., 2015; Reed et al., 2018; Tsutomu & Yoshiaki, 2003). As a reactive electrophile, BPDE can be alkylated and bind covalently to the exocyclic amino group of guanine and nucleophilic sites in DNA, forming N2-guanine adducts BPDE-N2-dG, which can induce a frameshift or base substitution mutation, such as G to T transversion, as well as GC → TA and GC → CG mutations (Zhao et al., 2006). Therefore, BPDE has the potential to activate oncogenes and cause cancers by DNA damage accumulation, increasing the frequency of DNA base mutations (Shimada, 2006; Tung et al., 2010; Wei et al., 1991).
Generally, DNA damage activates a cell cycle checkpoint, leading to the induction of transcriptional programs and the enhancement of DNA repair pathways (Sancar et al., 2004). DNA damage caused by benzo[a]pyrene exposure mainly involves BPDE-DNA adducts, base mismatches, and DNA DSBs. Correspondingly, nucleotide excision repair mechanisms eliminate DNA adducts, and base excision repair maintains genome integrity and corrects modifications in the DNA bases (Allmann et al., 2020b; Kress et al., 2019), whereas homologous recombination is involved in the repair of DNA DSBs (Li & Heyer, 2008). These DNA repair mechanisms are inhibited after benzo[a]pyrene exposure (Allmann et al., 2020b; Tung et al., 2014; Yang et al., 2007), leading to aberrant DNA damage repair, which is key to the accumulation of irreparable DNA damage (Tung et al., 2014).
Aromatic amines
Aromatic amines (AAs) are a class of chemicals found in consumer products such as dyes, pesticides, and tobacco smoke. One in eight of all known or suspected human carcinogens exists as or can be converted to an AA (Wang et al., 2019). Several AAs have been identified as carcinogens and mutagens, including o-toluidine (o-Tol), 2-aminonaphthalene, and 4-aminobiphenyl (4-ABP), which are the most important risk factors for bladder cancer (Bellamri et al., 2019; Nauwelaers et al., 2011; Tajima et al., 2020).
The key to bladder cancer caused by these AAs is the formation of DNA adducts (Bellamri et al., 2019; Tajima et al., 2020). For example, approximately 80% of 4-ABP molecules form DNA adducts at the C8 atoms of guanine (Nauwelaërs et al., 2013), synthesized as described for N-(deoxyguanosin-8-yl) adducts. The remaining 4-ABP molecules are activated to carcinogenic N-oxidation intermediates by cytochrome P450 1A2 to produce the genotoxic N-hydroxy-4-ABP metabolite, which can further interact with DNA to form adducts, causing oxidative DNA damage and DNA DSBs (Marnett, 2000; Shahab et al., 2013; Torino et al., 2001). In addition, 4-ABP can cause bladder cancer by inducing mutations characterized by a high frequency of G:C → T:A transversion, and appropriate alkyl substitution can modify the mutagenicity of 4-ABP (Chen et al., 2005; Glende et al., 2001; Yoon et al., 2012).
DNA damage repair in chemical carcinogenesis
In response to different types of DNA damage induced by endogenous or exogenous stimuli, organisms mount DDR to sense, eliminate, or tolerate damage to maintain genetic stability and integrity (Chang et al., 2017; Sadoughi et al., 2021). DNA damage accumulation and aberrant DNA damage repair play a critical role in the accumulation of mutations. Unrepaired or incorrectly repaired DNA damage may ultimately lead to genomic instability and mutations, which increase the risks of cancers. DNA repair pathways are parts of the DDR, including base excision repair, nucleotide excision repair, mismatch repair, non-homologous end joining (NHEJ), and homologous recombination (HR). In general, specific types of DNA damages are amenable to being repaired by particular DNA repair pathways. For example, exposure to PM2.5, Cr(VI), and benzo[a]pyrene can easily lead to DSBs and are commonly accompanied with the reduced expression of DNA repair proteins (e.g., Lig4, Dclre1c, and RAD51), indicating the inhibition of HR and NHEJ (Allmann et al., 2020; Browning & Wise, 2017a; Browning et al., 2016a; Zeng et al., 2021). Both HR and NHEJ are two common ways for repairing DSBs. Compared to HR, NHEJ is faster but also more error-prone, because it disregards sequence homology, does not rely on homologous DNA sequences, and only rejoins damaged DNA ends via DNA ligases (Ciccia & Elledge, 2010); therefore, NHEJ in non-homologous DNA sequences makes aberrant repair of DSBs a potential mechanism for mutagenesis. Therefore, targeting DNA repair pathways is a promising therapeutic strategy for cancers (Huang & Zhou, 2021; Jin & Oh, 2019; Motegi et al., 2019). The DNA damage repair and carcinogenic mechanisms of the chemical carcinogens investigated in this study are shown in Table 1. A better understanding of the complex interaction between DNA damage and repair is critical for elucidating chemical carcinogenesis mechanisms and studying the etiology of cancer in the future.
Table 1 DNA damage repair and carcinogenic mechanism of chemical carcinogens
OGG1 8-oxoguanine glycosylase, APE1 apurinic-apyrimidinic endonuclease I, XPA xeroderma pigmentosum group A, MSH2 mutS homolog 2, MSH6 mutS homolog 6, JHDM2A lysine demethylase 3A, DDB2 damage specific DNA binding protein 2, RAD51 RADiation sensitive 51, BPDE benzo(a)pyrene, 7,8-dihydrodiol-9,10-epoxide, XRCC5 X-ray repair cross complementing 5, DNA-PKcs DNA-dependent protein kinase catalytic subunit, EXO1 exonuclease 1
Epigenetic regulation in DNA damage carcinogenesis
There is a consensus on the regulatory function of epigenetics in the occurrence and development of cancers. DNA damage induced by exposure to chemical carcinogens is one of the crucial mechanisms in chemical carcinogenesis. Epigenetic alterations such as silencing of histone markers or histone demethylation, DNA hypermethylation, and abnormal expressions of noncoding RNAs can co-regulate DNA damage that is induced by chemical carcinogens through influencing the transcription of key transcription factors and the expression of DNA repair genes, eventually leading to the accumulation of DNA damage. Methylation is the function that has received the most attention among the roles of epigenetic changes by exposure to diverse environmental carcinogens (Verghese et al., 2022). For example, carcinogenic heavy metals inhibit the production of DNA repair genes by DNA hypermethylation, histone marker silencing, or histone demethylation, leading to enhanced genetic damage (Hu et al., 2018; Li et al., 2021, 2022b; Ren et al., 2019; Wang et al., 2018). Furthermore, benzo(a)pyrene and 4-ABP exposure causes CpG methylation, which improves the binding of BPDE adducts and N–OH-4-ABP to the CpG site and leads to p53 gene mutation in cancer (Feng et al., 2002; Wang et al., 2013). An active area of research in recent years has been the regulatory role of abnormal expressions of noncoding RNAs in environmental chemical carcinogenesis. For example, circRNAs, such as circ_Cabin1 and circNIPBL, can downregulate the functional DNA damage repair molecules Lig4, Dclre1c, and PARP1, inhibiting the NHEJ and base excision repair pathways and promoting DNA damage after 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and PM2.5 exposure, respectively (Liu et al., 2022; Zeng et al., 2021). LncRNA MT1DP might bind to SMARCAL1, competitively inhibit latter's interaction with RPA complex, and stimulate DNA replication through the ATR pathway to regulate Cd-induced DNA damage (Feng et al., 2022). However, the role of epigenetics in DNA damage-initiated carcinogenesis remains largely unknown and requires further exploration.
Conclusions and future perspectives
Common chemical carcinogens mainly form DNA adducts through the metabolic activation of CYP450 enzymes or generate ROS and hydroxyl radicals, which cause DNA damage and have an indirect carcinogenic effect. The following need to be considered: (1) almost all environmental chemical carcinogens can cause DNA damage; however, no specific type of DNA damage is unique to all chemical carcinogens. (2) Exposure to one chemical carcinogen can simultaneously cause multiple types of DNA damage. (3) The types of DNA damage differ with the chemical carcinogen. Chemical type-based DNA damage mechanisms help expand our understanding of the toxic effects of novel chemicals. It should also be noted that when DNA damage is induced by environmental chemical carcinogens, the activation or inhibition of various DNA repair pathways influences the development of cancer. The involvement of epigenetics in DNA damage repair is essential in environmental carcinogen exposure. For the purpose of elucidating the mechanisms of chemical carcinogenesis and investigating the etiology of cancer, it is crucial to have a deeper understanding of the intricate relationships between DNA damage and epigenetics.
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Funding
This study was supported by the National Natural Science Foundation of China (82173483 to Z.Y. and 82130095 to J.Y.)
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State Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou, 510120, China
Han Zhang, Yun Zhou & Yiguo Jiang
Institute for Chemical Carcinogenesis, Guangzhou Medical University, Guangzhou, 511436, China
Han Zhang, Wenfeng Lu, Yun Zhou & Yiguo Jiang
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Correspondence to Yun Zhou or Yiguo Jiang.
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Zhang, H., Lu, W., Zhou, Y. et al. Advances in DNA damage induced by environmental chemical carcinogens. GENOME INSTAB. DIS. 3, 317–330 (2022). https://doi.org/10.1007/s42764-022-00092-z
Received23 August 2022
Revised08 November 2022
Accepted08 November 2022
Published18 November 2022
Issue DateDecember 2022
DOIhttps://doi.org/10.1007/s42764-022-00092-z
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