DNA adduct

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A metabolite of benzo[a]pyrene forms an intercalated DNA adduct, at center Benzopyrene DNA adduct 1JDG.png
A metabolite of benzo[a]pyrene forms an intercalated DNA adduct, at center

In molecular genetics, a DNA adduct is a segment of DNA bound to a cancer-causing chemical. This process could lead to the development of cancerous cells, or carcinogenesis. DNA adducts in scientific experiments are used as biomarkers of exposure. They are especially useful in quantifying an organism's exposure to a carcinogen. [1] The presence of such an adduct indicates prior exposure to a potential carcinogen, but it does not necessarily indicate the presence of cancer in the subject animal.

Contents

DNA adducts are researched in laboratory settings. A typical experimental design for studying DNA adducts is to induce them with known carcinogens. A scientific journal will often incorporate the name of the carcinogen with their experimental design. For example, the term "DMBA-DNA adduct" in a scientific journal refers to a piece of DNA that has DMBA (7,12-dimethylbenz(a)anthracene) attached to it.   [2]

Carcinogens' impact

Several diseases, including cancer, develop from mutated DNA. These mutations are caused by carcinogens through external and internal factors. Carcinogens are chemical or physical agents that cause DNA damage, which may later develop into cancer. They can initiate mutagenesis in DNA by interfering with the replication process. [3] These interactions typically cause chemical adducts to form in the cell. This allows for DNA adducts to serve as biomarkers of exposure to carcinogens from the environment. They are attractive biomarkers because they are stable, abundant, and easily characterizable. Exposure to them can directly or indirectly cause DNA damage. In the direct case, a carcinogen can bind to DNA and cause it to distort or become cross-linked. Although DNA repair happens under normal circumstances, sometimes the DNA will not repair itself. This could be the start of a mutation, or mutagenesis. Repeated mutations can lead to carcinogenesis – the beginnings of cancer. [4]

The presence of endogenous carcinogens contributes to levels of DNA adducts in a patient. This can bias the quantification of carcinogens that are from environmental exposure. Ongoing research on DNA adducts seeks to overcome these complications. It is the hope that in future medical practices DNA adducts may serve to guide therapeutic treatments that are more targeted and effective. [5]

Mechanism of DNA damage

Adduct formation is determined by the structures of reactive chemicals, the movement(s) of electrophiles, and the capacity of the compounds to bind with DNA, potentially driving adduct formation to specific nucleophilic sites. The N3 and N7 locations (nucleotide positioning) of guanine and adenine are believed to be the most nucleophilic, and hence, they form adducts selectively over exocyclic oxygen atoms. The generation of DNA adducts is also influenced by certain steric factors. Guanine's N7 position is exposed in the major groove of double-helical DNA, making it more suitable for adduction than when compared to adenine's N3 position, which is orientated in the minor groove. [6]

Figure 2: Reactive Sites of Interest for Nucleic Acids in DNA Adduct Formation Nucleic Acids in DNA Adduct Formation.png
Figure 2: Reactive Sites of Interest for Nucleic Acids in DNA Adduct Formation

Many compounds require enzyme metabolic activation to become mutagenic and cause DNA damage. Furthermore, reactive intermediates can be produced in the body as a result of oxidative stress, thus harming the DNA. Some chemical carcinogens, metabolites, as well as endogenous compounds generated by inflammatory processes cause oxidative stress. This can result in the formation of a reactive oxygen species (ROS) or reactive nitrogen species (RNS). ROS and RNS are known to cause DNA damage via oxidative processes. Figure 2 shows each of the reactive sites for the nucleic acids involved in adduction and damage, with each form of transfer distinguished by arrow color. These positions are of interest to researchers studying DNA adduct formation. Research has indicated that many different chemicals may change human DNA and that lifestyle and host characteristics can impact the extent of DNA damage. Humans are constantly exposed to a diverse combination of potentially dangerous substances that might cause DNA damage. [6]

Chemicals that form DNA adducts

Figure 3: DNA damaged by carcinogenic 2-aminofluorene DNA damaged by carcinogenic 2-aminofluorene AF.jpg
Figure 3: DNA damaged by carcinogenic 2-aminofluorene

Detection methods

32P-postlabeling assay:

Liquid chromatography–mass spectrometry (LC–MS):

Fluorescence labeling:

Enzyme linked immunosorbent assay (ELISA):

DNA adduct as biomarkers of exposure

Beef diet

Human consumption of more than 2.5–3.5 oz (70–100 g) of red meat (beef, lamb or pork) a day increases the risk of colon cancer, but eating chicken does not have this risk. [21] [22] The increased risk of colon cancer from red meat may be due to higher increases in DNA adducts from digestion of red meat. When rats were fed either beef or chicken, three types of DNA adducts in colon tissue were significantly higher after consumption of beef than after consumption of chicken. [23] These adducts were a type of methyl-cytosine (possibly N3-methyl-cytosine), an adduct of two malondialdehyde molecules with guanine, and carboxyl-adenine. [24]

Tobacco use

Human exposure to tobacco smoke has been associated with an increased risk of lung cancer. Tobacco smoke can impose great risk to DNA, with chemicals such as formaldehyde and acetaldehyde reacting directly with DNA to form adducts. In addition, there are other tobacco-specific carcinogens to consider in humans that are activated metabolically, such as nicotine-derived nitrosamine ketone (NNK) and N'-nitrosonornicotine (NNN). These carcinogens end up forming adducts when reacted with DNA, with those being called pyridyl oxobutyl (POB) adducts. [25]

Figure 4: Effects of Tobacco on Healthy Human DNA Effects of Carcinogen Exposure on Healthy DNA.png
Figure 4: Effects of Tobacco on Healthy Human DNA

Further analysis has been conducted on the topic, determining that 1,3-Butadiene (BD) is a human carcinogen that is found in cigarette smoke among other synthetic polymer industries. Tests were conducted to understand the differences in the level of urinary BD-DNA adducts among various ethnic groups – white, Japanese American, and Native Hawaiian. It was determined that Japanese American smokers exhibited heightened levels of urinary BD-induced guanine adducts than white and Native Hawaiian individuals, while there were no differences in outcome by ethnicity among non-smokers. Understanding the epigenetic and genetic factors driving these differences in urinary BD-DNA adduct presence is the next step for this research, serving as a link between sociology and the life sciences. [26]

Airborne particulate matter

Particulate matter (PM), broadly known as air pollution, is considered a group 1 carcinogen by the International Agency for Research on Cancer; while it is unclear if a direct link between cancer and PM exposure exists, it is likely that PM exposure leads to some degree of cell damage. Upon further investigation, it was determined that PM exposure causes oxidative stress – creating reactive oxygen species, forming DNA adducts, and inducing double-strand breaks (DSBs). In regards to DNA adduct formation, this analysis was conducted after looking at leukocytes from residents of heavily-populated cities (e.g. pollution, long-term traffic); a common component of PMs, polycyclic aromatic hydrocarbon (PAH), was one of the many molecules considered to be highly correlated with the presence of DNA bulky lesions in these individuals. These findings support the theory that DNA adduct presence indicates a level of carcinogenic activity. [27]

See also

Related Research Articles

<span class="mw-page-title-main">Carcinogen</span> Substance, radionuclide, or radiation directly involved in causing cancer

A carcinogen is any agent that promotes the development of cancer. Carcinogens can include synthetic chemicals, naturally occurring substances, physical agents such as ionizing and non-ionizing radiation, and biologic agents such as viruses and bacteria. Most carcinogens act by creating mutations in DNA that disrupt a cell's normal processes for regulating growth, leading to uncontrolled cellular proliferation. This occurs when the cell's DNA repair processes fail to identify DNA damage allowing the defect to be passed down to daughter cells. The damage accumulates over time. This is typically a multi-step process during which the regulatory mechanisms within the cell are gradually dismantled allowing for unchecked cellular division.

Mutagenesis is a process by which the genetic information of an organism is changed by the production of a mutation. It may occur spontaneously in nature, or as a result of exposure to mutagens. It can also be achieved experimentally using laboratory procedures. A mutagen is a mutation-causing agent, be it chemical or physical, which results in an increased rate of mutations in an organism's genetic code. In nature mutagenesis can lead to cancer and various heritable diseases, and it is also a driving force of evolution. Mutagenesis as a science was developed based on work done by Hermann Muller, Charlotte Auerbach and J. M. Robson in the first half of the 20th century.

<span class="mw-page-title-main">Mutagen</span> Physical or chemical agent that increases the rate of genetic mutation

In genetics, a mutagen is a physical or chemical agent that permanently changes genetic material, usually DNA, in an organism and thus increases the frequency of mutations above the natural background level. As many mutations can cause cancer in animals, such mutagens can therefore be carcinogens, although not all necessarily are. All mutagens have characteristic mutational signatures with some chemicals becoming mutagenic through cellular processes.

Genotoxicity is the property of chemical agents that damage the genetic information within a cell causing mutations, which may lead to cancer. While genotoxicity is often confused with mutagenicity, all mutagens are genotoxic, but some genotoxic substances are not mutagenic. The alteration can have direct or indirect effects on the DNA: the induction of mutations, mistimed event activation, and direct DNA damage leading to mutations. The permanent, heritable changes can affect either somatic cells of the organism or germ cells to be passed on to future generations. Cells prevent expression of the genotoxic mutation by either DNA repair or apoptosis; however, the damage may not always be fixed leading to mutagenesis.

<span class="mw-page-title-main">Polycyclic aromatic hydrocarbon</span> Hydrocarbon composed of multiple aromatic rings

A polycyclic aromatic hydrocarbon (PAH) is a class of organic compounds that is composed of multiple aromatic rings. The simplest representative is naphthalene, having two aromatic rings, and the three-ring compounds anthracene and phenanthrene. PAHs are uncharged, non-polar and planar. Many are colorless. Many of them are found in coal and in oil deposits, and are also produced by the incomplete combustion of organic matter—for example, in engines and incinerators or when biomass burns in forest fires.

Benzo(<i>a</i>)pyrene Carcinogenic compound found in smoke and soot

Benzo[a]pyrene (BaP or B[a]P) is a polycyclic aromatic hydrocarbon and the result of incomplete combustion of organic matter at temperatures between 300 °C (572 °F) and 600 °C (1,112 °F). The ubiquitous compound can be found in coal tar, tobacco smoke and many foods, especially grilled meats. The substance with the formula C20H12 is one of the benzopyrenes, formed by a benzene ring fused to pyrene. Its diol epoxide metabolites, more commonly known as BPDE, react with and bind to DNA, resulting in mutations and eventually cancer. It is listed as a Group 1 carcinogen by the IARC. In the 18th century a scrotal cancer of chimney sweepers, the chimney sweeps' carcinoma, was already known to be connected to soot.

<span class="mw-page-title-main">Chemical hazard</span> Non-biological hazards of hazardous materials

Chemical hazards are hazards present in hazardous chemicals and hazardous materials. Exposure to certain chemicals can cause acute or long-term adverse health effects. Chemical hazards are usually classified separately from biological hazards (biohazards). Chemical hazards are classified into groups that include asphyxiants, corrosives, irritants, sensitizers, carcinogens, mutagens, teratogens, reactants, and flammables. In the workplace, exposure to chemical hazards is a type of occupational hazard. The use of personal protective equipment may substantially reduce the risk of adverse health effects from contact with hazardous materials.

<span class="mw-page-title-main">4-Nitroquinoline 1-oxide</span> Chemical compound

4-Nitroquinoline 1-oxide is a quinoline derivative and a tumorigenic compound used in the assessment of the efficacy of diets, drugs, and procedures in the prevention and treatment of cancer in animal models. It induces DNA lesions usually corrected by nucleotide excision repair.

<span class="mw-page-title-main">Sudan I</span> Chemical compound

Sudan I is an organic compound typically classified as an azo dye. It is an orange-red solid used to color waxes, oils, petrol, solvents, and polishes. Historically, Sudan I served as a food coloring agent, notably for curry powder and chili powder. However, along with its derivatives Sudan III and Sudan IV, the compound has been banned in many countries due to its classification as a category 3 carcinogenic hazard by the International Agency for Research on Cancer. Nevertheless, Sudan I remains valuable as a coloring reagent for non-food-related uses, such as in the formulation of orange-colored smoke.

The International Agency for Research on Cancer is an intergovernmental agency forming part of the World Health Organization of the United Nations. Its role is to conduct and coordinate research into the causes of cancer. It also collects and publishes surveillance data regarding the occurrence of cancer worldwide.

<i>N</i>-Nitrosonornicotine Chemical compound

N-Nitrosonornicotine (NNN) is a tobacco-specific nitrosamine produced during the curing and processing of tobacco.

4-Aminobiphenyl (4-ABP) is an organic compound with the formula C6H5C6H4NH2. It is an amine derivative of biphenyl. It is a colorless solid, although aged samples can appear colored. 4-Aminobiphenyl was commonly used in the past as a rubber antioxidant and an intermediate for dyes. Exposure to this aryl-amine can happen through contact with chemical dyes and from inhalation of cigarette smoke. Researches showed that 4-aminobiphenyl is responsible for bladder cancer in humans and dogs by damaging DNA. Due to its carcinogenic effects, commercial production of 4-aminobiphenyl ceased in the United States in the 1950s.

<i>o</i>-Toluidine Aryl amine

o-Toluidine (ortho-toluidine) is an organic compound with the chemical formula CH3C6H4NH2. It is the most important of the three isomeric toluidines. It is a colorless liquid although commercial samples are often yellowish. It is a precursor to the herbicides metolachlor and acetochlor.

<i>N</i>-Nitrosodiethylamine Chemical compound

N-Nitrosodiethylamine (NDEA) is an organic compound with the formula Et2NNO (Et = C2H5). A member of the nitrosamines, it is a light-sensitive, volatile, clear yellow oil that is soluble in water, lipids, and other organic solvents. It has an amine or aromatic odor. It is used as gasoline and lubricant additive, antioxidant, and stabilizer for industry materials. When heated to decomposition, N-nitrosodiethylamine emits toxic fumes of nitrogen oxides. N-Nitrosodiethylamine affects DNA integrity, probably by alkylation, and is used in experimental research to induce liver tumorigenesis. It is carcinogenic and mutagenic. NDEA has also been found to perturb amino acid biosynthesis including arginine, as well as DNA damage repair and mitochondrial genome maintenance in yeast.

A co-carcinogen is a chemical that promotes the effects of a carcinogen in the production of cancer. Usually, the term is used to refer to chemicals that are not carcinogenic on their own, such that an equivalent amount of the chemical is insufficient to initiate carcinogenesis. A chemical can be co-carcinogenic with other chemicals or with nonchemical carcinogens, such as UV radiation.

Benzo(<i>j</i>)fluoranthene Chemical compound

Benzo[j]fluoranthene (BjF) is an organic compound with the chemical formula C20H12. Classified as a polycyclic aromatic hydrocarbon (PAH), it is a colourless solid that is poorly soluble in most solvents. Impure samples can appear off white. Closely related isomeric compounds include benzo[a]fluoranthene (BaF), benzo[b]fluoranthene (BbF), benzo[e]fluoranthene (BeF), and benzo[k]fluoranthene (BkF). BjF is present in fossil fuels and is released during incomplete combustion of organic matter. It has been traced in the smoke of cigarettes, exhaust from gasoline engines, emissions from the combustion of various types of coal and emissions from oil heating, as well as an impurity in some oils such as soybean oil.

<span class="mw-page-title-main">Chlornaphazine</span> Chemical compound

Chlornaphazine, a derivative of 2-naphthylamine, is a nitrogen mustard that was developed in the 1950s for the treatment of polycythemia and Hodgkin's disease. However, a high incidence of bladder cancers in patients receiving treatment with chlornaphthazine led to use of the drug being discontinued.

<span class="mw-page-title-main">2-Amino-1-methyl-6-phenylimidazo(4,5-b)pyridine</span> Chemical compound


PhIP (2-Amino-1-methyl-6-phenylimidazo[4,5-b]pyridine) is one of the most abundant heterocyclic amines (HCAs) in cooked meat. PhIP is formed at high temperatures from the reaction between creatine or creatinine, amino acids, and sugar. PhIP formation increases with the temperature and duration of cooking and also depends on the method of cooking and the variety of meat being cooked. The U.S. Department of Health and Human Services National Toxicology Program has declared PhIP as "reasonably anticipated to be a human carcinogen". International Agency for Research on Cancer (IARC), part of World Health Organization, has classified PhIP as IARC Group 2B carcinogen. There is sufficient evidence in experimental animals, as well as in vitro models, for the carcinogenicity of PhIP.

Cancer is caused by genetic changes leading to uncontrolled cell growth and tumor formation. The basic cause of sporadic (non-familial) cancers is DNA damage and genomic instability. A minority of cancers are due to inherited genetic mutations. Most cancers are related to environmental, lifestyle, or behavioral exposures. Cancer is generally not contagious in humans, though it can be caused by oncoviruses and cancer bacteria. The term "environmental", as used by cancer researchers, refers to everything outside the body that interacts with humans. The environment is not limited to the biophysical environment, but also includes lifestyle and behavioral factors.

<span class="mw-page-title-main">Glycidamide</span> Chemical compound

Glycidamide is an organic compound with the formula H2NC(O)C2H3O. It is a colorless oil. Structurally, it contains adjacent amides and epoxide functional groups. It is a bioactive, potentially toxic or even carcinogenic metabolite of acrylonitrile and acrylamide. It is a chiral molecule.

References

  1. ↑ Poirier MC (June 1997). "DNA adducts as exposure biomarkers and indicators of cancer risk". Environmental Health Perspectives. 105 (Suppl 4): 907–912. doi:10.1289/ehp.97105s4907. PMC   1470061 . PMID   9255579.
  2. ↑ Maltzman TH, Christou M, Gould MN, Jefcoate CR (November 1991). "Effects of monoterpenoids on in vivo DMBA-DNA adduct formation and on phase I hepatic metabolizing enzymes". Carcinogenesis. 12 (11): 2081–2087. doi:10.1093/carcin/12.11.2081. PMID   1934293.
  3. ↑ Barnes JL, Zubair M, John K, Poirier MC, Martin FL (October 2018). "Carcinogens and DNA damage". Biochemical Society Transactions. 46 (5): 1213–1224. doi:10.1042/BST20180519. PMC   6195640 . PMID   30287511.
  4. ↑ Weston A, Poirier MC (2005). "Carcinogen–DNA Adduct Formation and DNA Repair.". In Wexler P (ed.). Encyclopedia of Toxicology. Elsevier. pp. 440–445. doi:10.1016/B0-12-369400-0/00191-5. ISBN   978-0-12-369400-3.
  5. ↑ Yimit A, Adebali O, Sancar A, Jiang Y (January 2019). "Differential damage and repair of DNA-adducts induced by anti-cancer drug cisplatin across mouse organs". Nature Communications. 10 (1): 309. Bibcode:2019NatCo..10..309Y. doi:10.1038/s41467-019-08290-2. PMC   6338751 . PMID   30659176.
  6. 1 2 Hwa Yun B, Guo J, Bellamri M, Turesky RJ (March 2020). "DNA adducts: Formation, biological effects, and new biospecimens for mass spectrometric measurements in humans". Mass Spectrometry Reviews. 39 (1–2): 55–82. Bibcode:2020MSRv...39...55H. doi:10.1002/mas.21570. PMC   6289887 . PMID   29889312.
  7. ↑ IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2010). "Some non-heterocyclic polycyclic aromatic hydrocarbons and some related exposures". IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 92: 1–853. PMC   4781319 . PMID   21141735.
  8. ↑ IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2014). "Diesel and Gasoline Engine Exhausts and Some Nitroarenes". IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 105: 9–699. PMC   4781216 . PMID   26442290.
  9. ↑ IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2007). "Smokeless tobacco and some tobacco-specific N-nitrosamines". IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 89: 1–592. PMC   4781254 . PMID   18335640.
  10. ↑ IARC Working Group on the Evaluation of Carcinogenic Risks to Humans (2002). "Some traditional herbal medicines, some mycotoxins, naphthalene and styrene". IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 82: 1–556. PMC   4781602 . PMID   12687954.
  11. ↑ "IARC monographs on the evaluation of the carcinogenic risk of chemicals to man: some aziridines, N-, S- & O-mustards and selenium". IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Man. 9: 1–268. 1975. PMID   1234596.
  12. ↑ IARC Monographs Working Group on the Evaluation of Carcinogenic Risks to Humans (2010). "Some aromatic amines, organic dyes, and related exposures". IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. 99: 1–658. PMC   5046080 . PMID   21528837.
  13. ↑ https://www.cabdirect.org/cabdirect/abstract/19952006807 [ bare URL ]
  14. ↑ Wyatt MD, Pittman DL (December 2006). "Methylating agents and DNA repair responses: Methylated bases and sources of strand breaks". Chemical Research in Toxicology. 19 (12): 1580–1594. doi:10.1021/tx060164e. PMC   2542901 . PMID   17173371.
  15. ↑ Singer B (October 1985). "In vivo formation and persistence of modified nucleosides resulting from alkylating agents". Environmental Health Perspectives. 62: 41–48. doi:10.1289/ehp.856241. PMC   1568687 . PMID   4085444.
  16. ↑ Guengerich FP, McCormick WA, Wheeler JB (November 2003). "Analysis of the kinetic mechanism of haloalkane conjugation by mammalian theta-class glutathione transferases". Chemical Research in Toxicology. 16 (11): 1493–1499. doi:10.1021/tx034157r. PMID   14615977.
  17. 1 2 Balbo S, Turesky RJ, Villalta PW (March 2014). "DNA adductomics". Chemical Research in Toxicology. 27 (3): 356–366. doi:10.1021/tx4004352. PMC   3997222 . PMID   24437709.
  18. ↑ Singh R, Farmer PB (February 2006). "Liquid chromatography-electrospray ionization-mass spectrometry: the future of DNA adduct detection". Carcinogenesis. 27 (2): 178–196. doi:10.1093/carcin/bgi260. PMID   16272169.
  19. ↑ Boffetta P, Hainaut P (2019). Encyclopedia of cancer (Third ed.). Amsterdam: Academic Press. ISBN   978-0-12-812485-7. OCLC   1061558350.
  20. ↑ Brown K (2012). "Methods for the Detection of DNA Adducts". In Parry JM, Parry E (eds.). Genetic Toxicology. Methods in Molecular Biology. Vol. 817. New York, NY: Springer. pp. 207–230. doi:10.1007/978-1-61779-421-6_11. ISBN   978-1-61779-421-6. PMID   22147575.
  21. ↑ Aykan NF (February 2015). "Red Meat and Colorectal Cancer". Oncology Reviews. 9 (1): 288. doi:10.4081/oncol.2015.288. PMC   4698595 . PMID   26779313.
  22. ↑ Wolk A (February 2017). "Potential health hazards of eating red meat". Journal of Internal Medicine. 281 (2): 106–122. doi: 10.1111/joim.12543 . PMID   27597529. S2CID   24130100.
  23. ↑ Hemeryck LY, Van Hecke T, Vossen E, De Smet S, Vanhaecke L (September 2017). "DNA adductomics to study the genotoxic effects of red meat consumption with and without added animal fat in rats". Food Chemistry. 230: 378–387. doi:10.1016/j.foodchem.2017.02.129. PMID   28407925.
  24. ↑ Kastan MB (April 2008). "DNA damage responses: mechanisms and roles in human disease: 2007 G.H.A. Clowes Memorial Award Lecture". Molecular Cancer Research. 6 (4): 517–524. doi: 10.1158/1541-7786.MCR-08-0020 . PMID   18403632.
  25. ↑ Ma B, Stepanov I, Hecht SS (March 2019). "Recent Studies on DNA Adducts Resulting from Human Exposure to Tobacco Smoke". Toxics. 7 (1): 16. doi: 10.3390/toxics7010016 . PMC   6468371 . PMID   30893918.
  26. ↑ Jokipii Krueger CC, Park SL, Madugundu G, Patel Y, Le Marchand L, Stram DO, Tretyakova N (May 2021). "Ethnic differences in excretion of butadiene-DNA adducts by current smokers". Carcinogenesis. 42 (5): 694–704. doi:10.1093/carcin/bgab020. PMC   8163050 . PMID   33693566.
  27. ↑ Quezada-Maldonado EM, Sánchez-Pérez Y, Chirino YI, García-Cuellar CM (October 2021). "Airborne particulate matter induces oxidative damage, DNA adduct formation and alterations in DNA repair pathways". Environmental Pollution. 287: 117313. Bibcode:2021EPoll.28717313Q. doi:10.1016/j.envpol.2021.117313. PMID   34022687.
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