Advertisement

Archives of Toxicology

, Volume 92, Issue 12, pp 3443–3457 | Cite as

Next-generation sequencing approaches for the study of genome and epigenome toxicity induced by sulfur mustard

  • Yunes Panahi
  • Amir Fattahi
  • Fatemeh Zarei
  • Navid Ghasemzadeh
  • Abbas Mohammadpoor
  • Sina Abroon
  • Jafar Nouri Nojadeh
  • Mehran Khojastefard
  • Abolfazl Akbarzadeh
  • Tohid Ghasemnejad
Review Article
  • 96 Downloads

Abstract

Sulfur mustard (SM) is an extensive nucleophilic and alkylating agent that targets different tissues. The genotoxic property of SM is the most threatening effect, because it is associated with detrimental inflammations and susceptibility to several kinds of cancer. Moreover, SM causes a wide variety of adverse effects on DNA which result in accumulation of DNA adducts, multiple mutations, aneuploidies, and epigenetic aberrations in the genome. However, these adverse effects are still not known well, possibly because no valid biomarkers have been developed for detecting them. The advent of next-generation sequencing (NGS) has provided opportunities for the characterization of these alterations with a higher level of molecular detail and cost-effectivity. The present review introduces NGS approaches for the detection of SM-induced DNA adducts, mutations, chromosomal structural variation, and epigenetic aberrations, and also comparing and contrasting them with regard to which might be most advantageous.

Keywords

Sulfur mustard Genotoxicity Epigenome toxicity NGS 

Notes

Acknowledgements

We would like to dedicate this article to the victims of chemical weapon-exposed countries.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abel HJ, Duncavage EJ (2013) Detection of structural DNA variation from next generation sequencing data: a review of informatic approaches. Cancer Genet 206:432–440Google Scholar
  2. Abolghasemi H et al (2010) Childhood physical abnormalities following paternal exposure to sulfur mustard gas in Iran: a case–control study. Confl Health 4:13Google Scholar
  3. Alkan C, Coe BP, Eichler EE (2011a) Genome structural variation discovery and genotyping. Nat Rev Genet 12:363Google Scholar
  4. Alkan C, Sajjadian S, Eichler EE (2011b) Limitations of next-generation genome sequence assembly. Nat Methods 8:61Google Scholar
  5. Ari Ş, Arikan M (2016) Next-generation sequencing: advantages, disadvantages, and future. In: Plant omics: trends and applications. Springer, Berlin, pp 109–135Google Scholar
  6. Auerbach C (1949) Chemical mutagenesis. Biol Rev 24:355–391Google Scholar
  7. Balali-Mood M, Hefazi M (2006) Comparison of early and late toxic effects of sulfur mustard in Iranian veterans. Basic Clin Pharmacol Toxicol 99:273–282Google Scholar
  8. Ball MP et al (2009) Targeted and genome-scale methylomics reveals gene body signatures in human cell lines. Nat Biotechnol 27:361–368.  https://doi.org/10.1038/nbt.1533 CrossRefGoogle Scholar
  9. Batal M et al (2013) Temporal and spatial features of the formation of DNA adducts in sulfur mustard-exposed skin. Toxicol Appl Pharmacol 273:644–650Google Scholar
  10. Batal M, Boudry I, Mouret S, Cléry-Barraud C, Wartelle J, Bérard I, Douki T (2014) DNA damage in internal organs after cutaneous exposure to sulphur mustard. Toxicol Appl Pharmacol 278:39–44Google Scholar
  11. Behravan E, Moallem SA, Khateri S, Maraghi E, Jowsey P, Blain PG, Balali-Mood M (2013) Deoxyribonucleic acid damage in Iranian veterans 25 years after wartime exposure to sulfur mustard. J Res Med Sci 18:239Google Scholar
  12. Bennett RA, Behrens E, Zinn A, Duncheon C, Lamkin TJ (2014) Mustard gas surrogate, 2-chloroethyl ethylsulfide (2-CEES), induces centrosome amplification and aneuploidy in human and mouse cells. Cell Biol Toxicol 30:195–205Google Scholar
  13. Boulware S, Fields T, McIvor E, Powell KL, Abel EL, Vasquez KM, MacLeod MC (2012) 2, 6-Dithiopurine, a nucleophilic scavenger, protects against mutagenesis in mouse skin treated in vivo with 2-(chloroethyl) ethyl sulfide, a mustard gas analog. Toxicol Appl Pharmacol 263:203–209Google Scholar
  14. Brunner AL et al (2009) Distinct DNA methylation patterns characterize differentiated human embryonic stem cells and developing human fetal liver. Genome Res 19:1044–1056Google Scholar
  15. Bryan DS, Ransom M, Adane B, York K, Hesselberth JR (2014) High resolution mapping of modified DNA nucleobases using excision repair enzymes. Genome Res 24:1534–1542Google Scholar
  16. Buermans H, Den Dunnen J (2014) Next generation sequencing technology: advances and applications. Biochim Biophys Acta (BBA) Mol Basis Dis 1842:1932–1941Google Scholar
  17. Choi M et al (2009) Genetic diagnosis by whole exome capture and massively parallel DNA sequencing. Proc Natl Acad Sci 106:19096–19101Google Scholar
  18. Colaneri A, Staffa N, Fargo DC, Gao Y, Wang T, Peddada SD, Birnbaumer L (2011) Expanded methyl-sensitive cut counting reveals hypomethylation as an epigenetic state that highlights functional sequences of the genome. Proc Natl Acad Sci 108:9715–9720Google Scholar
  19. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499Google Scholar
  20. Dewey FE et al (2014) Clinical interpretation and implications of whole-genome sequencing. JAMA 311:1035–1045Google Scholar
  21. Ding J, Taylor MS, Jackson AP, Reijns MA (2015) Genome-wide mapping of embedded ribonucleotides and other noncanonical nucleotides using emRiboSeq and EndoSeq. Nat Protoc 10:1433Google Scholar
  22. Dugac AV, Ruzic A, Samarzija M, Badovinac S, Kehler T, Jakopovic M (2015) Persistent endothelial dysfunction turns the frequent exacerbator COPD from respiratory disorder into a progressive pulmonary and systemic vascular disease. Med Hypotheses 84:155–158Google Scholar
  23. Dupont C, Armant DR, Brenner CA (2009) Epigenetics: definition, mechanisms and clinical perspective. In: Seminars in reproductive medicine. Vol 5. Thieme Medical Publishers, Stuttgart, pp 351–357Google Scholar
  24. Eid J et al (2009) Real-time DNA sequencing from single polymerase molecules. Science 323:133–138Google Scholar
  25. Emison ES, Smith WJ (1996) Cytometric analysis of DNA damage in cultured human epithelial cells after exposure to sulfur mustard. J Am Coll Toxicol 15:S9–S18Google Scholar
  26. Fidder A, Moes GW, Scheffer AG, van der Schans GP, Baan RA, de Jong LP, Benschop HP (1994) Synthesis, characterization, and quantitation of the major adducts formed between sulfur mustard and DNA of calf thymus and human blood. Chem Res Toxicol 7:199–204Google Scholar
  27. Fouse SD, Nagarajan RP, Costello JF (2010) Genome-scale DNA methylation analysis. Epigenomics 2:105–117Google Scholar
  28. Fox M, Scott D (1980) The genetic toxicology of nitrogen and sulphur mustard. Mutat Res Rev Genet Toxicol 75:131–168Google Scholar
  29. Fraineau S, Palii CG, Allan DS, Brand M (2015) Epigenetic regulation of endothelial-cell-mediated vascular repair. FEBS J 282:1605–1629Google Scholar
  30. Gerhauser C, Heilmann K, Pudenz M (2015) Genome-wide DNA methylation profiling in dietary intervention studies: a user’s perspective. Curr Pharmacol Rep 1:31–45Google Scholar
  31. Ghabili K, Agutter PS, Ghanei M, Ansarin K, Shoja MM (2010) Mustard gas toxicity: the acute and chronic pathological effects. J Appl Toxicol 30:627–643Google Scholar
  32. Ghanei M, Vosoghi AA (2002) An epidemiologic study to screen for chronic myelocytic leukemia in war victims exposed to mustard gas. Environ Health Perspect 110:519Google Scholar
  33. Gibson P, Brink R, Stahmann M (1950) The mutagenic action of mustard gas on zea mays. J Hered 41:232–238Google Scholar
  34. Gilbert RM, Rowland S, Davison CL, Papirmeister B (1975) Involvement of separate pathways in the repair of mutational and lethal lesions induced by a monofunctional sulfur mustard mutation research/fundamental and molecular. Mech Mutagen 28:257–275Google Scholar
  35. Goodwin S, McPherson JD, McCombie WR (2016) Coming of age: ten years of next-generation sequencing technologies. Nat Rev Genet 17:333–351Google Scholar
  36. Gregus Z, Klaassen CD (2001) Mechanisms of toxicity Casarett and Doull’s toxicology: the basic science of poisons Vol. 6, McGraw-Hill, New York, pp 35–82Google Scholar
  37. Gupta PK (2008) Single-molecule DNA sequencing technologies for future genomics research. Trends Biotechnol 26:602–611Google Scholar
  38. Haque F, Li J, Wu H-C, Liang X-J, Guo P (2013) Solid-state and biological nanopore for real-time sensing of single chemical and sequencing of. DNA Nano Today 8:56–74Google Scholar
  39. Hart J, Verbruggen M, Maletta G (2017) 1.7. Actual use of chemical weapons in Syria for the Policy and Operations Evaluations Department of the Dutch Ministry of Foreign Affairs:79Google Scholar
  40. Heather JM, Chain B (2016) The sequence of sequencers: the history of sequencing. DNA Genom 107:1–8Google Scholar
  41. Hosseini-khalili A et al (2009) Mustard gas exposure and carcinogenesis of lung. Mutat Res Genet Toxicol Environ Mutagen 678:1–6Google Scholar
  42. Hu J, Adar S, Selby CP, Lieb JD, Sancar A (2015) Genome-wide analysis of human global and transcription-coupled excision repair of UV damage at single-nucleotide resolution. Genes Dev 29:948–960Google Scholar
  43. Hu J, Lieb JD, Sancar A, Adar S (2016) Cisplatin DNA damage and repair maps of the human genome at single-nucleotide resolution. Proc Natl Acad Sci 113:11507–11512Google Scholar
  44. Hu J, Adebali O, Adar S, Sancar A (2017) Dynamic maps of UV damage formation and repair for the human genome. Proc Natl Acad Sci 114(26):6758–6763Google Scholar
  45. Imani S, Panahi Y, Salimian J, Fu J, Ghanei M (2015) Epigenetic: a missing paradigm in cellular and molecular pathways of sulfur mustard lung: a prospective and comparative study. Iran J Basic Med Sci 18:723Google Scholar
  46. Ives SJ et al (2014) Vascular dysfunction and chronic obstructive. Pulm Dis Hypertens 63:459–467Google Scholar
  47. Jafari M, Nateghi M, Rabbani A (2010) Interaction of sulfur mustard with rat liver salt fractionated chromatin. Int J Biol Macromol 46:104–108Google Scholar
  48. Jost P, Svobodová H, Zemankova S, Stetina R (2010) The relationship of DNA Cross-links induced with sulphur mustard (SM) in human and Chinese hamster cell lines to the cell viability. Toxicol Lett 196:S172Google Scholar
  49. Jowsey PA, Williams FM, Blain PG (2010) The role of homologous recombination in the cellular response to sulphur mustard. Toxicol Lett 197:12–18Google Scholar
  50. Jowsey PA, Williams FM, Blain PG (2012) DNA damage responses in cells exposed to sulphur mustard. Toxicol Lett 209:1–10Google Scholar
  51. Jung M, Kadam S, Xiong W, Rauch TA, Jin S-G, Pfeifer GP (2015) MIRA-seq for DNA methylation analysis of CpG Islands. Epigenomics 7:695–706Google Scholar
  52. Kadalayil L et al (2014) Exome sequence read depth methods for identifying copy number changes. Brief Bioinform 16:380–392Google Scholar
  53. Kehe K, Szinicz L (2005) Medical aspects of sulphur mustard poisoning. Toxicology 214:198–209Google Scholar
  54. Khan F, Niaz K, Hassan FI, Abdollahi M (2017) An evidence-based review of the genotoxic and reproductive effects of sulfur mustard. Arch Toxicol 91:1143–1156Google Scholar
  55. Kircher M, Brendel M (1983) DNA alkylation by mustard gas in yeast strains of different repair capacity. Chem Biol Interact 44:27–39Google Scholar
  56. Koboldt DC, Steinberg KM, Larson DE, Wilson RK, Mardis ER (2013) The next-generation sequencing revolution and its impact on genomics. Cell 155:27–38Google Scholar
  57. Korbel JO et al (2007) Paired-end mapping reveals extensive structural variation in the. human genome. Science 318:420–426Google Scholar
  58. Korkmaz A, Yaren H, Topal T, Oter S (2006) Molecular targets against mustard toxicity: implication of cell surface receptors, peroxynitrite production, and PARP activation. Arch Toxicol 80:662–670Google Scholar
  59. Korkmaz A, Tan D-X, Reiter R (2008a) Acute and delayed sulfur mustard toxicity; novel mechanisms and future studies. Interdiscip Toxicol 1:22–26Google Scholar
  60. Korkmaz A et al (2008b) Epigenetic perturbations in the pathogenesis of mustard toxicity; hypothesis and preliminary results. Interdiscip Toxicol 1:236–241Google Scholar
  61. Korkmaz A, Topal T, Aykutlug O, Ates K, Uysal B, Kalkan F, Oter S (2016) Revealing the epigenetic mechanisms on the pathogenesis of lung damage caused by chemical warfare agent mustard analogue mechlorethamine. Toxicol Lett 258:S253Google Scholar
  62. Kurdyukov S, Bullock M (2016) DNA methylation analysis: choosing the right method. Biology 5:3Google Scholar
  63. Laird PW (2010) Principles and challenges of genome-wide DNA methylation analysis. Nat Rev Genet 11:191Google Scholar
  64. Laskin JD et al (2010) Oxidants and antioxidants in sulfur mustard-induced injury. Ann N Y Acad Sci 1203:92–100Google Scholar
  65. Lawley P (1989) Mutagens as carcinogens: development of current concepts. Mutat Res Fundam Mol Mechanisms Mutagen 213:3–25Google Scholar
  66. Le Scouarnec S, Gribble S (2012) Characterising chromosome rearrangements: recent technical advances in molecular cytogenetics. Heredity 108:75Google Scholar
  67. Lemaire M-A, Schwartz A, Rahmouni AR, Leng M (1991) Interstrand cross-links are preferentially formed at the d (GC) sites in the reaction between cis-diamminedichloroplatinum (II) and DNA. Proc Natl Acad Sci 88:1982–1985Google Scholar
  68. Levene MJ, Korlach J, Turner SW, Foquet M, Craighead HG, Webb WW (2003) Zero-mode waveguides for single-molecule analysis at high concentrations. Science 299:682–686Google Scholar
  69. Lewis CJ, Mardaryev AN, Sharov AA, Fessing MY, Botchkarev VA (2014) The epigenetic regulation of wound healing. Adv Wound Care 3:468–475Google Scholar
  70. Li W, Hu J, Adebali O, Adar S, Yang Y, Chiou Y-Y, Sancar A (2017) Human genome-wide repair map of DNA damage caused by the cigarette smoke carcinogen benzo [a] pyrene. Proc Natl Acad Sci 114:6752–6757Google Scholar
  71. Liu-Lee VW, Heddle JA, Arlett CF, Broughton B (1984) Genetic effects of specific DNA lesions in mammalian cells. Mutat Res Fundam Mol Mech Mutagen 127:139–147Google Scholar
  72. Ludlum DB, Tong WP, Mehta JR, Kirk MC, Papimeister B (1984) Formation of O6-ethylthioethyldeoxyguanosine from the reaction of chloroethyl ethyl sulfide with deoxyguanosine. Cancer Res 44:5698–5701Google Scholar
  73. Ludlum DB, Kent S, Mehta JR (1986) Formation of O 6-ethylthioethylguanine in DNA by reaction with the sulfur mustard, chloroethyl sulfide, and its apparent lack of repair by O 6-alkylguanine-DNA alkyltransferase. Carcinogenesis 7:1203–1206Google Scholar
  74. Ludlum DB, Austin-Ritchie P, Hagopian M, Niu T-Q, Yu D (1994) Detection of sulfur mustard-induced DNA modifications. Chem Biol Interact 91:39–49Google Scholar
  75. Mahdieh N, Rabbani B (2013) An overview of mutation detection methods in genetic disorders. Iran J Pediatr 23:375Google Scholar
  76. Mansour Razavi S, Salamati P, Saghafinia M, Abdollahi M (2012) A review on delayed toxic effects of sulfur mustard in Iranian veterans DARU. J Pharm Sci 20:51Google Scholar
  77. Mao P, Smerdon MJ, Roberts SA, Wyrick JJ (2016) Chromosomal landscape of UV damage formation and repair at single-nucleotide resolution. Proc Natl Acad Sci 113:9057–9062Google Scholar
  78. Mao P, Brown AJ, Malc EP, Mieczkowski PA, Smerdon MJ, Roberts SA, Wyrick JJ (2017) Genome-wide maps of alkylation damage, repair, and mutagenesis in yeast reveal mechanisms of mutational heterogeneity. Genome Res 27:1674–1684Google Scholar
  79. Marzese DM, Hoon DS (2015) Emerging technologies for studying DNA methylation for the molecular diagnosis of cancer. Expert Rev Mol Diagn 15:647–664Google Scholar
  80. Maslov AY, Quispe-Tintaya W, Gorbacheva T, White RR, Vijg J (2015) High-throughput sequencing in mutation detection: a new generation of genotoxicity tests? Mutat Res Fundam Mol Mech Mutagen 776:136–143Google Scholar
  81. Mason-Suares H, Landry L, Lebo MS (2016) Detecting copy number variation via next generation technology. Curr Genet Med Rep 4:74–85Google Scholar
  82. Masser DR et al (2016) Bisulfite oligonucleotide-capture sequencing for targeted base-and strand-specific absolute 5-methylcytosine quantitation. Age 38:49Google Scholar
  83. Masta A, Gray PJ, Phillips DR (1996) Effect of sulphur mustard on the initiation and elongation of transcription. Carcinogenesis 17:525–532Google Scholar
  84. Matijasevic Z, Volkert MR (2007) Base excision repair sensitizes cells to sulfur mustard and chloroethyl ethyl sulfide. DNA Repair 6:733–741Google Scholar
  85. Matijasevic Z, Precopio ML, Snyder JE, Ludlum DB (2001) Repair of sulfur mustard-induced DNA damage in mammalian cells measured by a host cell reactivation assay. Carcinogenesis 22:661–664Google Scholar
  86. Matouk CC, Marsden PA (2008) Epigenetic regulation of vascular endothelial gene expression. Circ Res 102:873–887Google Scholar
  87. Meaburn E, Schulz R (2012) Next generation sequencing in epigenetics: insights and challenges. In: Seminars in cell & developmental biology. Vol 2. Elsevier, Amsterdam, pp 192–199Google Scholar
  88. Meier B et al (2014) C. elegans whole-genome sequencing reveals mutational signatures related to carcinogens and DNA repair deficiency. Genome Res 24:1624–1636Google Scholar
  89. Meldrum C, Doyle MA, Tothill RW (2011) Next-generation sequencing for cancer diagnostics: a practical perspective. Clin Biochem Rev 32:177Google Scholar
  90. Merk O, Speit G (1999) Detection of crosslinks with the comet assay in relationship to genotoxicity and cytotoxicity. Environ Mol Mutagen 33:167–172Google Scholar
  91. Metzker ML (2010) Sequencing technologies—the next generation. Nat Rev Genet 11:31Google Scholar
  92. Morozova O, Marra MA (2008) Applications of next-generation sequencing technologies in functional genomics. Genomics 92:255–264Google Scholar
  93. Ning B et al (2014) Toxicogenomics and cancer susceptibility: advances with next-generation sequencing. J Environ Sci Health Part C 32:121–158Google Scholar
  94. Olkhov-Mitsel E, Bapat B (2012) Strategies for discovery and validation of methylated and hydroxymethylated. DNA biomarkers. Cancer Med 1:237–260Google Scholar
  95. Ordulu Z et al (2014) Describing sequencing results of structural chromosome rearrangements with a suggested next-generation cytogenetic nomenclature. Am J Hum Genet 94:695–709Google Scholar
  96. Panahi Y, Fattahi A, Nejabati HR, Abroon S, Latifi Z, Akbarzadeh A, Ghasemnejad T (2018) DNA repair mechanisms in response to genotoxicity of warfare agent sulfur mustard. Environ Toxicol Pharmacol 58:230–236Google Scholar
  97. Park PJ (2009) ChIP–seq: advantages and challenges of a maturing technology. Nat Rev Genet 10:669Google Scholar
  98. Peterson CL, Laniel M-A (2004) Histones and histone modifications. Curr Biol 14:R546–R551Google Scholar
  99. Povirk LF, Shuker DE (1994) DNA damage and mutagenesis induced by nitrogen mustards. Mutat Res Rev Genet Toxicol 318:205–226Google Scholar
  100. Rauch TA, Pfeifer GP (2010) DNA methylation profiling using the methylated-CpG island recovery assay (MIRA). Methods 52:213–217Google Scholar
  101. Razavi SM, Ghanei M, Salamati P, Safiabadi M (2013) Long-term effects of mustard gas on respiratory system of Iranian veterans after Iraq–Iran war: a review Chinese. J Traumatol 16:163–168Google Scholar
  102. Reis-Filho JS (2009) Next-generation sequencing. Breast Cancer Res 11:S12Google Scholar
  103. Rowell M, Kehe K, Balszuweit F, Thiermann H (2009) The chronic effects of sulfur. mustard exposure. Toxicology 263:9–11Google Scholar
  104. Savage JR, Breckon G (1981) Differential effects of sulphur mustard on S-phase cells of primary fibroblast cultures from Syrian hamsters. Mutat Res Fundam Mol Mech Mutagen 84:375–387Google Scholar
  105. Schatz MC, Delcher AL, Salzberg SL (2010) Assembly of large genomes using second-generation sequencing. Genome Res 20:1165–1173Google Scholar
  106. Scott D, Fox M, Fox B (1974a) Proceedings: the relationship between cell survival, chromosome aberrations and DNA repair in tumour cell lines of differential sensitivity to X-rays and sulphur mustard. Br J Cancer 29:99Google Scholar
  107. Scott D, Fox M, Fox BW (1974b) The relationship between chromosomal aberrations, survival and DNA repair in tumour cell lines of differential sensitivity to X-rays and sulphur mustard. Mutat Res Fundam Mol Mech Mutagen 22:207–221Google Scholar
  108. Shah SU (2012) Importance of Genotoxicity & S2A guidelines for genotoxicity testing for pharmaceuticals IOSR. J Pharm Biol Sci 1:43–54Google Scholar
  109. Shahin S, Cullinane C, Gray PJ (2001) Mitochondrial and nuclear DNA damage induced by sulphur mustard in keratinocytes. Chem Biol Interact 138:231–245Google Scholar
  110. Shakarjian MP et al (2009) Mechanisms mediating the vesicant actions of sulfur mustard after cutaneous exposure. Toxicol Sci 114:5–19Google Scholar
  111. Shakil FA, Kuramoto A, Yamakido M, Nishimoto Y, Kamada N (1993) Cytogenetic abnormalities of hematopoietic tissue in retired workers of the Ohkunojima poison gas factory. Hiroshima J Med Sci 42:159–165Google Scholar
  112. Shelby MD (1988) The genetic toxicity of human carcinogens and its implications. Mutat Res Genet Toxicol 204:3–15Google Scholar
  113. Shu X, Xiong X, Song J, He C, Yi C (2016) Base-resolution analysis of cisplatin–DNA adducts at the genome scale. Angew Chem Int Ed 55:14246–14249Google Scholar
  114. Shukla P, Mishra P (2010) A quantum chemical study of reactions of DNA bases with sulphur mustard: a chemical warfare agent. Theor Chem Acc 125:269–278Google Scholar
  115. Simons T et al (2017) Sulfur mustard-induced epigenetic modifications over time—a pilot study. Toxicol Lett 293:45–50Google Scholar
  116. Sloan DB, Broz AK, Sharbrough J, Wu Z (2018) Detecting rare mutations and DNA damage with sequencing-based methods. Trends Biotechnol.  https://doi.org/10.1016/j.tibtech.2018.02.009 CrossRefGoogle Scholar
  117. Soozangar N, Sadeghi MR, Jeddi F, Somi MH, Shirmohamadi M, Samadi N (2018) Comparison of genome-wide analysis techniques to DNA methylation analysis in human cancer. J Cell Physiol 233:3968–3981Google Scholar
  118. Soto J, Rodriguez-Antolin C, Vallespín E, de Castro Carpeño J, de Caceres II (2016) The impact of next-generation sequencing on the DNA methylation–based translational cancer research. Transl Res 169:1–18. e11Google Scholar
  119. Steinritz D, Emmler J, Hintz M, Worek F, Kreppel H, Szinicz L, Kehe K (2007) Apoptosis in sulfur mustard treated A549 cell cultures. Life Sci 80:2199–2201Google Scholar
  120. Steinritz D et al (2016) Epigenetic modulations in early endothelial cells and DNA hypermethylation in human skin after sulfur mustard exposure. Toxicol Lett 244:95–102Google Scholar
  121. Stetina R, Jilkova M, Svobodova H (2010) The induction of inter-strand DNA cross-links in different tissues of rats after percutaneous application of sulphur mustard (SM). Toxicol Lett 196:S162Google Scholar
  122. Steward D, Sass E, Fritz L, Sasser L (1989) Toxicology Studies on Lewisite and Sulfur Mustard Agents: Mutagenicity of Sulfur Mustard in the Salmonella Histidine Reversion Assay. Pacific Northwest Labs Richland WAGoogle Scholar
  123. Stewart D Mutagenicity study of sulfur mustard in the Salmonella histidine reversion test. In: Environmental Mutagenesis, 1987. Wiley-Liss Div John Wiley & Sons Inc 605 Third Ave, New York, NY 10158-0012, pp 103–104Google Scholar
  124. Szikriszt B et al (2016) A comprehensive survey of the mutagenic impact of common cancer cytotoxics. Genome Biol 17:99Google Scholar
  125. Takeshima Y et al (1994) p53 mutations in lung cancers from Japanese mustards gas workers. Carcinogenesis 15:2075–2079Google Scholar
  126. Toyota M et al (1999) Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. Cancer Res 59:2307–2312Google Scholar
  127. Venitt S (1968) Interstrand cross-links in the DNA of Escherichia coli B/r and Bs—1 and their removal by the resistant strain. Biochem Biophys Res Commun 31:355–360Google Scholar
  128. Vijayan V, Pathak U, Meshram GP (2014) Mutagenicity and antimutagenicity studies of DRDE-07 and its analogs against sulfur mustard in the in vitro Ames Salmonella/microsome assay. Mutat Res Genet Toxicol Environ Mutagen 773:39–45Google Scholar
  129. Walker I (1971) Intrastrand bifunctional alkylation of DNA in mammalian cells treated with mustard gas. Can J Biochem 49:332–336Google Scholar
  130. Wang W (2015) Detect copy number variations from read-depth of high-throughput sequencing data. The University of North Carolina at Chapel HillGoogle Scholar
  131. Wheeler GP, Alexander JA (1969) Effects of nitrogen mustard and cyclophosphamide upon the synthesis of DNA in vivo and in cell-free preparations. Cancer Res 29:98–109Google Scholar
  132. Wilson D, Sofinowski T, McNeill D (2003) Repair mechanisms for oxidative DNA damage. Front Biosci 8:d963-981Google Scholar
  133. Wulf H, Aasted A, Darre E, Niebuhr E (1985) Sister chromatid exchanges in fishermen exposed to leaking mustard gas shells. Lancet 325:690–691Google Scholar
  134. Xuan J, Yu Y, Qing T, Guo L, Shi L (2013) Next-generation sequencing in the clinic: promises and challenges. Cancer Lett 340:284–295Google Scholar
  135. Yanagida J et al (1988) Somatic mutation in peripheral lymphocytes of former workers at the Okunojima poison gas factory. Cancer Sci 79:1276–1283Google Scholar
  136. Zahir MH, Nouri DM, Jalilian N, Naderimanesh H, Bidaky S, Rostamzadeh J, Rezwani H (2002) Immunohaematological and cytogenetical studies on human population exposed to sulfur mustard. J Sci I R Iran 13:303–309Google Scholar
  137. Zhang ZD, Du J, Lam H, Abyzov A, Urban AE, Snyder M, Gerstein M (2011) Identification of genomic indels and structural variations using split reads. BMC Genom 12:375Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Chemical Injuries Research Center, System Biology and Poisoning InstituteBaqiyatallah University of Medical SciencesTehranIran
  2. 2.Department of Reproductive Biology, Faculty of Advanced Medical SciencesTabriz University of Medical SciencesTabrizIran
  3. 3.Department of Stem Cells and Developmental Biology at Cell Science Research CenterRoyan Institute for Stem Cell Biology and Technology, ACECRTehranIran
  4. 4.Department of Biochemistry, Faculty of MedicineShahid Sadoughi University of Medical SciencesYazdIran
  5. 5.Cellular and Molecular Research CenterUrmia University of Medical SciencesUrmiaIran
  6. 6.Stem Cell Research Center (SCRC)Tabriz University of Medical SciencesTabrizIran
  7. 7.Department of Medical Genetic, Faculty of MedicineTabriz University of Medical SciencesTabrizIran
  8. 8.Department of Medical Nanotechnology, Faculty of Advanced Medical SciencesTabriz University of Medical SciencesTabrizIran

Personalised recommendations