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Genotoxic effects of PM10 and PM2.5 bound metals: metal bioaccessibility, free radical generation, and role of iron

  • Suman Yadav
  • Navanath Kumbhar
  • Rohi Jan
  • Ritwika Roy
  • P. Gursumeeran Satsangi
Original Paper

Abstract

The present study was undertaken to examine the possible genotoxicity of ambient particulate matter (PM10 and PM2.5) in Pune city. In both size fractions of PM, Fe was found to be the dominant metal by concentration, contributing 22% and 30% to the total mass of metals in PM10 and PM2.5, respectively. The speciation of soluble Fe in PM10 and PM2.5 was investigated. The average fraction of Fe3+ and Fe2+ concentrations in PM2.5 was 80.6% and 19.3%, respectively, while in PM2.5 this fraction was 71.1% and 29.9%, respectively. The dominance of Fe(III) state in both PM fractions facilitates the generation of hydroxyl radicals (·OH), which can damage deoxyribose nucleic acid (DNA), as was evident from the gel electrophoresis study. The DNA damage by ·OH was supported through the in silico density functional theory (DFT) method. DFT results showed that C8 site of guanine (G)/adenine (A) and C6 site of thymine (T)/cytosine (C) would be energetically more favorable for the attack of hydroxyl radicals, when compared with the C4 and C5 sites. The non-standard Watson–Crick base pairing models of oxidative products of G, A, T and C yield lower-energy conformations than canonical dA:dT and dG:dC base pairing. This study may pave the way to understand the structural consequences of base-mediated oxidative lesions in DNA and its role in human diseases.

Keywords

Bioaccessibility of metals Fe speciation Free radicals DNA damage In silico DFT study 

Notes

Acknowledgements

Authors wish to thank CSIR (24(0345)/16), New Delhi, and BCUD (15SCI001596) SPPU, Pune, for financial assistance. Authors also express their gratitude to Head, Department of Chemistry, Savitribai Phule Pune University for encouragement. IIT, SAIF—Mumbai is also acknowledged for analyzing the samples on ICP-AES and EPR.

References

  1. Adhikari, A., Kumar, A., Heizer, A. N., Palmer, B. J., Pottiboyina, V., Liang, Y., et al. (2013). Hydroxyl ion addition to one-electron oxidized thymine: Unimolecular interconversion of C5 to C6 OH-adducts. Journal of American Chemical Society, 135, 3121–3135.CrossRefGoogle Scholar
  2. Arunan, E., Desiraju, G. R., Klein, R. A., Sadlej, J., Scheiner, S., Alkorta, I., et al. (2011). Definition of the hydrogen bond (IUPAC Recommendations 2011). Pure and Applied Chemistry, 83, 1637–1641.CrossRefGoogle Scholar
  3. Balakrishnaiah, G., Kumar, K. R., Gopal, K. R., Reddy, R. R., Reddy, L. S. S., Narasimhulu, K., et al. (2011). Characterization of PM, PM10, PM2.5 mass concentrations at a tropical semi-arid station in Anantpur, India. Indian Journal of Radio and Space Physics, 40, 95–104.Google Scholar
  4. Banerjee, A., Santos, W. L., & Verdine, J. L. (2006). Structure of a DNA glycosylase searching for lesions. Science, 311, 1153–1157.CrossRefGoogle Scholar
  5. Banerjee, A., Yang, W., Karplus, M., & Verdine, J. L. (2005). Structure of a repair enzyme interrogating undamaged DNA elucidates recognition of damaged DNA. Nature, 434, 612–618.CrossRefGoogle Scholar
  6. Becke, A. D. (1993). Density-functional thermochemistry. III. The role of exact Exchange. Journal of Chemical Physics, 98, 5648–5652.CrossRefGoogle Scholar
  7. Biswas, S., Verma, V., Schauer, J. J., Cassee, F. R., Cho, A. K., & Sioutas, C. (2009). Oxidative potential of semi volatile and non-volatile particulate matter (PM) from heavy-duty vehicles retrofitted with emission control technologies. Environmental Science and Technology, 43(10), 3905–3912.CrossRefGoogle Scholar
  8. Bourdat, A. G., Douki, T., Frelon, S., Gasparutto, D., & Cadet, J. (2000). Tandem base lesions are generated by hydroxyl radical isolated DNA in aerated aqueous solution. Journal of American Chemical Society, 122, 4549–4556.CrossRefGoogle Scholar
  9. Brown, K. L., Basu, A. K., & Stone, M. P. (2009). The cis-(5R, 6S)-thymine glycol lesion occupies the wobble position when mismatched with deoxyguanosine in DNA. Biochemistry, 48, 9722–9733.CrossRefGoogle Scholar
  10. Brown, K. L., Roginskaya, M., Zou, Y., Altamirano, A., Basu, A. K., & Stone, M. P. (2010). Binding of the human nucleotide excision repair proteins XPA and XPC/HR23B to the 5R-thymine glycol lesion and structure of the cis-(5R, 6S) thymine glycol epimer in the 5’-GTgG-3’ sequence: destabilization of two base pairs at the lesion site. Nucleic Acids Research, 38, 428–440.CrossRefGoogle Scholar
  11. Burade, S. S., Saha, T., Bhuma, Naresh, Kumbhar, N. M., Kotmale, A., Rajamohanan, P. R., et al. (2017). Self-assembly of fluorinated sugar amino acid derived α, γ-cyclic peptides into transmembrane anion transport. Organic Letters, 19, 5948–5951.CrossRefGoogle Scholar
  12. Cadet, J., Douki, T., & Ravanat, J.-L. (2010). Oxidatively generated base damage to cellular DNA. Free Radical Biology & Medicine, 49, 9–21.CrossRefGoogle Scholar
  13. Cadet, J., & Wagner, R. (2013). DNA base damage by reactive oxygen species, oxidizing agents, and UV radiation. Cold Spring Harbor Perspectives in Biology, 5, a012559.CrossRefGoogle Scholar
  14. Canepari, S., Perrino, C., Olivieri, F., & Astolfi, M. L. (2008). Characterisation of the traffic sources of PM through size-segregated sampling, sequential leaching and ICP analysis. Atmospheric Environment, 42(35), 8161–8175.CrossRefGoogle Scholar
  15. Cassee, F. R., Héroux, M. E., Miriam, E., Nijland, G., & Kelly, F. J. (2013). Particulate matter beyond mass: recent health evidence on the role of fractions, chemical constituents and sources of emission. Inhalation Toxicology, 25(14), 802–812.CrossRefGoogle Scholar
  16. Charrier, J. G., & Anastasio, C. (2011). Impacts of antioxidants on hydroxyl radical production from individual and mixed transition metals in a surrogate lung fluid. Atmospheric Environment, 45, 7555–7562.CrossRefGoogle Scholar
  17. Chen, H., Johnson, F., Grollman, A. P., & Patel, D. J. (1996). Structural studies of the ionizing radiation adduct 7, 8-dihydro-8-oxoadenine (A Oxo) positioned opposite thymine and guanine in DNA duplexes. Magnetic Resonance in Chemistry, 34, 23.CrossRefGoogle Scholar
  18. Chen, J., Wang, W., Hongjie, L., & Lihong, R. (2012). Determination of road dust loadings and chemical characteristics using resuspension. Environmental Monitoring and Assessment, 184(3), 1693–1709.CrossRefGoogle Scholar
  19. Cheng, Q., Gu, J., Compaan, K. R., & Schaefer, H. F. (2010). Hydroxyl radical reactions with adenine: reactant complexes, transition states, and product complexes. Chemistry - A European Journal, 16, 11848–11858.CrossRefGoogle Scholar
  20. Colson, A. O., & Sevilla, M. D. (1995). Ab Initio molecular orbital calculations of radicals formed by H and OH addition to the DNA bases: electron affinities and ionization potentials. Journal of physical chemistry, 99, 13033–13037.CrossRefGoogle Scholar
  21. Daigle, C. C., Chalupa, D. C., Gibb, F. R., Morrow, P. E., Oberdorster, G., & Utell, M. J. (2003). Ultrafine particle deposition in humans during rest and exercise. Inhalation Toxicology., 15, 539–552.CrossRefGoogle Scholar
  22. Davy, P. K., Gunchin, G., Markwitz, A., Trompetter, W. J., Barry, B. J., Shagjjamba, D., et al. (2011). Air particulate matter pollution in Ulaanbaatar, Mongolia: Determination of composition, source contributions and source locations. Atmospheric Pollution Research, 2, 126–137.CrossRefGoogle Scholar
  23. Di Pietro, A., Visalli, G., Munaò, F., Baluce, B., La Maestra, S., Primerano, P., et al. (2009). Oxidative damage in human epithelial alveolar cells exposed in vitro to oil fly ash transition metals. International Journal of Hygiene and Environmental Health, 212, 196–208.CrossRefGoogle Scholar
  24. Doelman, C. J., & Bast, A. (1990). Oxygen radicals in lung pathology. Free Radical Biology and Medicine., 9(5), 381–400.CrossRefGoogle Scholar
  25. Donahue, P. S., Szulik, M. W., & Stone, M. P. (2014). Solution NMR structure of DNA dodecamer with A: C mismatch. Protein data bank (2MO7.pdb,  https://doi.org/10.2210/pdb2mo7/pdb).
  26. Donaldson, K., Li, X. Y., & MacNee, W. (1998). Ultrafine (nanometre) particle mediated lung injury. Journal of Aerosol Science, 29(5–6), 553–560.CrossRefGoogle Scholar
  27. Donaldson, K., & Stone, V. (2003). Current hypotheses on mechanisms of toxicity of ultrafine particles. Annali dell’Istituto Superiore di Sanita (Ann Ist Super Sanita), 39(3), 405–410.Google Scholar
  28. Dumont, E., & Monari, A. (2015). Understanding DNA under oxidative stress and sensitization: The role of molecular modeling. Frontiers in Chemistry, 3, 43.CrossRefGoogle Scholar
  29. Faiola, C., Johansen, A. M., Rybka, S., Nieber, A., Thomas, C., Bryner, S., et al. (2011). Ultrafine particulate ferrous iron and anthracene associations with mitochondrial dysfunction. Aerosol Science and Technology, 45, 1109–1122.CrossRefGoogle Scholar
  30. Farrugia, G., & Balzan, R. (2012). Oxidative stress and programmed cell death in yeast. Frontiers in Oncology, 2(64), 1–21.Google Scholar
  31. Freidovich, I. (1999). Fundamental aspects of reactive oxygen species, or what’s the matter with oxygen? Annals New York Academy of Sciences, 893, 13–18.CrossRefGoogle Scholar
  32. Fromme, J. C., Banerjee, A., Huang, S. J., & Verdine, J. L. (2004). Structural basis for removal of adenine mispaired with 8-oxoguanine by MutY adenine DNA glycosylase. Nature, 427, 652–656.CrossRefGoogle Scholar
  33. Gates, K. S. (2009). An overview of chemical processes that damage cellular DNA: Spontaneous hydrolysis, alkylation, and reactions with radicals. Chemical Research in Toxicology, 22, 1747–1760.CrossRefGoogle Scholar
  34. Ghio, A. J., Stonehuerner, J., Dailey, L. A., & Carter, J. D. (1999). Metals associated with both the water–soluble and insoluble fractions of an ambient air pollution particle catalyze an oxidative stress. Inhalation Toxicology, 11, 37–49.CrossRefGoogle Scholar
  35. Greenwell, L. L., Moreno, T., Jones, T. P., & Richards, R. J. (2002). Particle-induced oxidative damage is ameliorated by pulmonary antioxidants. Free Radical Biology and Medicine, 329, 898–905.CrossRefGoogle Scholar
  36. Gugamsetty, B., Wei, H., Liu, C. N., Awasthi, A., Hsu, S. C., Tsai, C. J., et al. (2012). Source characterization and apportionment of PM10, PM2.5 and PM0.1 by using positive matrix factorization. Aerosol Air Quality and Research, 12, 476–491.CrossRefGoogle Scholar
  37. Gupta, I., & Kumar, R. (2006). Trends of particulate matter in four cities in India. Atmospheric Environment, 40, 2552–2566.CrossRefGoogle Scholar
  38. Halliwell, B., & Gutteridge, J. M. C. (1986). Oxygen free-radicals and iron in relation to biology and medicine—Some problems and concepts. Archives of Biochemistry and Biophysics, 246, 501–514.CrossRefGoogle Scholar
  39. Halliwell, B., & Gutteridge, J. M. C. (1999). Free radicals in biology and medicine. Oxford: Oxford University Press.Google Scholar
  40. Han, J. Y., Takeshita, K., & Utsumi, H. (2001). Noninvasive detection of hydroxyl radical generation in lung by diesel exhaust particles. Free Radical Biology and Medicine, 30, 516–525.CrossRefGoogle Scholar
  41. Heal, M. R., Hibbs, L. R., Agius, R. M., & Beverland, I. J. (2005). Total and water-soluble trace metal content of urban background PM10, PM2.5 and black smoke in Edinburgh. UK. Atmospheric Environment, 39, 1417–1430.CrossRefGoogle Scholar
  42. Hehre, W. J., Radom, L., Schleyer, P. V. R., & Pople, J. A. (1986). Ab initio molecular orbital theory. New York: Wiley.Google Scholar
  43. Hsu, S. C., Lin, F. J., & Jeng, W. L. (2005). Seawater solubility of marine aerosols associated natural and anthropogenic metals. Atmospheric Environment, 39, 3989–4001.CrossRefGoogle Scholar
  44. Huang, X., Cheng, J., Bo, D., Betha, R., & Balasubramanian, R. (2016). Bioaccessibility of airborne particulate-bound trace elements in Shanghai and health risk assessment. Frontiers in Environmental Science, 4(76), 1–10.Google Scholar
  45. Ji, Y. J., Xia, Y. Y., Zhao, M. W., Huang, B. D., & Li, F. (2005). Theoretical study of the % OH reaction with cytosine. Journal of Molecular Structure: THEOCHEM, 723, 123–129.CrossRefGoogle Scholar
  46. Jiang, S. Y. N., Yang, F., Chan, K., & Ning, Z. (2014). Water solubility of metals in coarse PM and PM2.5 in typical urban environment in Hong Kong. Atmospheric Pollution Research, 5, 236–244.CrossRefGoogle Scholar
  47. Kam, W., Ning, Z., Shafer, M. M., Schauer, J. J., & Sioutas, C. (2011). Chemical characterization and redox potential of coarse and fine particulate matter (PM) in underground and ground-level rail systems of the Los Angeles Metro. Environmental Science and Technology, 45, 6769–6776.CrossRefGoogle Scholar
  48. Karthikeyan, S., Joshi, U. M., & Balasubramanian, R. (2006). Microwave assisted sample preparation for determining water-soluble fraction of trace elements in urban airborne particulate matter: Evaluation of bioavailability. Analytica Chimica Acta, 576(1), 23–30.CrossRefGoogle Scholar
  49. Kelly, F. J., & Fussell, J. C. (2012). Size, source and chemical composition as determinants of toxicity attributable to ambient particulate matter. Atmospheric Environment, 60, 504–526.CrossRefGoogle Scholar
  50. Kersten, M., Kriews, M., & Forstner, U. (1991). Partitioning of trace metals released from polluted marine aerosols in coastal seawater. Marine Chemistry, 36, 165–182.CrossRefGoogle Scholar
  51. Khayatian, G., Hassanpoor, S., Nasiri, F., & Zolali, A. (2012). Preconcentration, determination and speciation of iron by solid-phase extraction using dimethyl (e)-2-[(z)-1-acetyl)-2-hydroxy-1-propenyl]-2-butenedioate. Química Nova, 35(3), 535–540.CrossRefGoogle Scholar
  52. Kothai, P., Saradhi, I. V., Pandit, G. G., Markwitz, A., & Puranik, V. D. (2011). Chemical characterization and source identification of particulate matter at an urban site of Navi Mumbai, India. Aerosol and Air Quality Research, 11, 560–569.CrossRefGoogle Scholar
  53. Krahn, J. M., Beard, W. A., Miller, H., Grollman, A. P., & Wilson, S. H. (2003). Structure of DNA polymerase β with the mutagenic DNA lesion 8-oxodeoxyguanine reveals structural insights into its coding potential. Structure, 11, 121–127.CrossRefGoogle Scholar
  54. Kulshrestha, A., Satsangi, P. G., Masih, J., & Taneja, A. (2009). Metal concentration of PM2.5 and PM10 particles and seasonal variations in urban and rural environment of Agra, India. Science of the Total Environment, 407, 6196–6204.CrossRefGoogle Scholar
  55. Kumagai, Y., Kato, J. I., Hoshino, K., Akasaka, T., Sato, K., & Ikeda, H. (1996). Quinolone-resistant mutants of Escherichia coli DNA topo-isomerase IV par C gene. Antimicrobial Agents and Chemotherapy, 40, 710–714.CrossRefGoogle Scholar
  56. Kumar, A., Pottiboyina, V., & Sevilla, M. D. (2011). Hydroxyl radical (OH·) reaction with guanine in an aqueous environment: A DFT study. Journal of Physical chemistry B, 115, 15129–15137.CrossRefGoogle Scholar
  57. Kumbhar, N. M., Kumbhar, B. V., & Sonawane, K. D. (2012). Structural significance of hypermodified nucleic acid base hydroxywybutine (OHyW) which occur at 37th position in the anticodon loop of yeast tRNAPhe. Journal of Molecular Graphics and Modelling, 38, 174–185.CrossRefGoogle Scholar
  58. Leonard, G. A., Guy, A., Brown, T., Teoule, R., & Hunter, W. N. (1992). Conformation of guanine-8-oxoadenine base pairs in the crystal structure of d(CGCGAATT(O8A)GCG). Biochemistry, 31, 8415–8420.CrossRefGoogle Scholar
  59. Li, N., Xia, T., & Nel, A. E. (2008). The role of oxidative stress in ambient particulate matter-induced lung diseases and its implications in the toxicity of engineered nanoparticles. Free Radical Biology and Medicine, 44, 1689–1699.CrossRefGoogle Scholar
  60. Lin, Z.-Q., Xi, Z.-G., Yang, D.-F., Chao, F.-H., Zhang, H.-S., Zhang, W., et al. (2009). Oxidative damage to lung tissue and peripheral blood in endotracheal PM2.5-treated rats. Biomedical and Environmental Sciences, 22, 223–228.CrossRefGoogle Scholar
  61. Lu, S., Feng, M., Yao, Z., Jing, A., Yufang, Z., & Wu, M. (2011). Physicochemical characterization and cytotoxicity of ambient coarse, fine and ultrafine particulate matters in Shanghai atmosphere. Atmospheric Environment, 45, 736–744.CrossRefGoogle Scholar
  62. Lu, S., Zhenkun, Y., Xiaohui, C., Minghong, W., Guoying, S., Jiamo, F., et al. (2008). The relationship between physicochemical characterization and the potential toxicity of fine particulates (PM2.5) in Shanghai atmosphere. Atmospheric Environment, 42, 7205–7214.CrossRefGoogle Scholar
  63. Majestic, B. J., Schauer, J. J., & Shafer, M. (2006). Development of a wet-chemical method for the speciation of iron in atmospheric aerosols. Environmental Science and Technology, 40, 2346–2351.CrossRefGoogle Scholar
  64. Markad, P., Kumbhar, N. M., & Dhavale, D. D. (2016). Synthesis of the C8’-epimeric thymine pyranosyl amino acid core of amipurimycin. Beilstein Journal of Organic Chemistry, 12, 1765–1771.CrossRefGoogle Scholar
  65. McAuley-Hecht, K. E., Leonard, G. A., Gibson, N. J., Thomson, J. B., Watson, W. P., Hunter, W. N., et al. (1994). Crystal structure of a DNA duplex containing 8-hydroxydeoxy-guanine-adenine base pairs. Biochemistry, 33, 10266–10270.CrossRefGoogle Scholar
  66. McGeer, J., Henningsen, G., Lanno R., Fisher, N., Sappington, K., Drexler J., Beringer, M. (2004). Issue paper on the bioavailability and bioaccumulation of metals. U.S. Environmental Protection Agency, Risk Assessment Forum.Google Scholar
  67. Moller, P., Danielsen, P. H., Karottki, D. G., Jantzen, K., Roursgaard, M., Klingberg, H., et al. (2014). Oxidative stress and inflammation generated DNA damage by exposure to air pollution particles. Mutation Research, 762, 133–166.CrossRefGoogle Scholar
  68. Ondov, J. M., Choquette, C. E., Zoller, W. H., Gordon, G. E., Biermann, A. H., & Hef, R. E. (1989). Atmospheric behavior of trace elements on particles emitted from a coal-fired power plant. Atmospheric Environment, 23(10), 2193–2204.CrossRefGoogle Scholar
  69. Pandey, P., Patel, D. K., Khan, A. H., Barman, S. C., Murthy, R. C., & Kisku, G. C. (2013). Temporal distribution of fine particulates (PM2.5, PM10), potentially toxic metals, PAHs and Metal-bound carcinogenic risk in the population of Lucknow City, India. Journal of Environmental Science and Health, Part A, 48, 730–745.CrossRefGoogle Scholar
  70. Pipal, A. S., Jan, R., Satsangi, P. G., Tiwari, S., & Taneja, A. (2014). Study of surface morphology, elemental composition and origin of atmospheric aerosols (PM2.5 and PM10) over Agra, India. Aerosol and Air Quality Research, 14, 1685–1700.CrossRefGoogle Scholar
  71. Praagh, M. V. (2008). Metal releases from municipal solid waste incineration air pollution control residue with mixed compost. Waste Management and Research, 26, 377–388.CrossRefGoogle Scholar
  72. Rahman, K. (2007). Studies on free radicals, antioxidants, and co-factors. Clinical Interventions in Aging, 2(2), 219–236.Google Scholar
  73. Raven, K. P., & Loeppert, R. H. (1997). Heavy metals in the environment: trace element composition of fertilizers and soil amend-ments. Journal of Environmental Quality, 26, 551–557.CrossRefGoogle Scholar
  74. Reichhardt, T. (1995). Weighting the health risks of airborne particulates. Environment Science and Technology, 29, 360–364.CrossRefGoogle Scholar
  75. Risom, L., Moller, P., & Loft, S. (2005). Oxidative stress-induced DNA damage by particulate air pollution. Mutation Research, 592, 119–137.CrossRefGoogle Scholar
  76. Rong-Ri, T., Dong-Qi, W., & Feng-Shou, Z. (2014). Damage mechanism of hydroxyl radicals toward adenine–thymine base pair. Chinese Physics B., 23(2), 027103.CrossRefGoogle Scholar
  77. Satsangi, P. G., & Yadav, S. (2014). Chemical and morphological study of PM10 and PM2.5 in Pune, India. International Journal of Environment and Waste Management, 13(2), 199–216.CrossRefGoogle Scholar
  78. Schins, R. P., Lightbody, J. H., Borm, P. J., Shi, T., Donaldson, K., & Stone, V. (2004). Inflammatory effects of coarse and fine particulate matter in relation to chemical and biological constituents. Toxicology and Applied Pharmacology, 195, 1–11.CrossRefGoogle Scholar
  79. Schyman, P., Eriksson, L. A., Zhang, R., & Laaksonen, A. (2008). Hydroxyl radical—Thymine adduct induced DNA damages. Chemical Physics Letters, 458, 186–189.CrossRefGoogle Scholar
  80. Shi, T., Schins, R. P. F., Knaapen, A. M., Kuhlbush, T., Pitz, M., Heinrich, J., et al. (2003). Hydroxyl radical generation by electron paramagnetic resonance as a new method to monitor ambient particulate matter composition. Journal of Environmental Monitoring, 5, 550–556.CrossRefGoogle Scholar
  81. Sholkovitz, E. R., Sedwick, P. N., Church, T. M., Baker, A. R., & Powell, C. F. (2012). Fractional solubility of aerosol iron: Synthesis of a globalscale data set. Geochimica et Cosmochimica Acta, 89, 173–189.CrossRefGoogle Scholar
  82. Sonntag, C. (2006). Free-radical-induced DNA damage and its repair: A chemical perspective. Berlin: Springer-Verlag.CrossRefGoogle Scholar
  83. Squadrito, G., Cueto, R., Dellinger, B., & Pryor, W. (2001). Quinoid redox cycling as a mechanism for sustained free radical generation by inhaled airborne particulate matter. Free radical biology & medicine, 31(9), 1132–1138.CrossRefGoogle Scholar
  84. Steiner, T. (2003). CH…O hydrogen bonding in crystals. Crystallography Review, 9, 177–228.CrossRefGoogle Scholar
  85. Sun, Y., Guoshun, Z., Aohan, T., Ying, W., & Zhisheng, A. (2006). Chemical characteristics of PM2.5 and PM10 in haze-fog episodes in Beijing. Environmental Science and Technology, 40, 3148–3155.CrossRefGoogle Scholar
  86. Takahama, S., Gilardoni, S., & Russell, L. M. (2008). Single-particle oxidation state and morphology of atmospheric iron aerosols. Journal of Geophysical Research, 113(D22202), 1–16.Google Scholar
  87. Tian, L., Koshland, C. P., Yano, J., Yachandra, V. K., Yu, I. T. S., Lee, S. C., et al. (2009). Carbon-centered free radicals in particulate matter emissions from wood and coal combustion. Energy & Fuels, 23, 2523–2526.CrossRefGoogle Scholar
  88. Tiwari, S., Chate, D. M., Pragya, P., Kaushar, A., & Deewan, S. B. (2012). Variations in mass of the PM10, PM2.5 and PM1 during the monsoon and the winter at New Delhi. Aerosol and Air Quality Research, 12, 20–29.CrossRefGoogle Scholar
  89. Torshin, I. Y., Weber, I. T., & Harrison, R. W. (2002). Geometrical criteria of hydrogen bonds in proteins and identification of ‘bifurcated’ hydrogen bonds. Protein Engineering, 15, 359–363.CrossRefGoogle Scholar
  90. Valavanidis, A., Salika, A., & Theodoropoulou, A. (2000). Generation of hydroxyl radicals by urban suspended particulate air matter: The role of iron ions. Atmospheric Environment, 34, 2379–2386.CrossRefGoogle Scholar
  91. Valavanidis, A., Vlachogianni, T., Fiotakis, K., & Loridas, S. (2013). Pulmonary oxidative stress, inflammation and cancer: Respirable particulate matter, fibrous dusts and ozone as major causes of lung carcinogenesis through reactive oxygen species mechanisms. International Journal of Environmental Research and Public Health, 10, 3583–3590.CrossRefGoogle Scholar
  92. Valavanidis, A., Vlahogianni, T., Dassenakis, M., & Scoullos, M. (2006). Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicology and Environmental Safety, 64(2), 178–189.CrossRefGoogle Scholar
  93. Valko, M., Leibfritz, D., Moncol, J., Cronin, M. T. D., Mazur, M., & Telser, J. (2007). Free radicals and antioxidants in normal physiological functions and human disease. The International Journal of Biochemistry & Cell Biology, 39, 44–84.CrossRefGoogle Scholar
  94. Wagner, J. R., & Cadet, J. (2010). Oxidation reactions of cytosine DNA components by hydroxyl radical and one-electron oxidants in aerated aqueous solutions. Accounts of Chemical Research, 43, 564–571.CrossRefGoogle Scholar
  95. Xiao, Z., Shao, L., Zhang, N., Wang, J., & Wang, J. (2013). Heavy metal compositions and bioreactivity of airborne PM10 in a valley-shaped city in Northwestern China. Aerosol and Air Quality Research, 13, 1116–1125.CrossRefGoogle Scholar
  96. Yadav, S., Divya Praveen, O., & Satsangi, P. G. (2015). The effect of climate and meteorological changes on particulate matter in Pune. India. Environmental Monitoring and Assessment., 187, 402.CrossRefGoogle Scholar
  97. Yadav, S., & Satsangi, P. G. (2013). Characterization of particulate matter and its related metal toxicity in an urban location in South West India. Environmental Monitoring and Assessment, 185, 7365–7379.CrossRefGoogle Scholar
  98. Yun-Zhong, F., Sheng, Y., & Guoyao, W. (2002). Free radicals, antioxidants, and nutrition. Nutrition, 18, 872–879.CrossRefGoogle Scholar
  99. Zhang, R. B., & Eriksson, L. A. (2007). Effects of OH radical addition on proton transfer in the guanine–cytosine base pair. Journal of Physical Chemistry B, 111, 6571–6576.CrossRefGoogle Scholar

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© Springer Nature B.V. 2018

Authors and Affiliations

  • Suman Yadav
    • 1
    • 2
  • Navanath Kumbhar
    • 1
  • Rohi Jan
    • 1
  • Ritwika Roy
    • 1
  • P. Gursumeeran Satsangi
    • 1
  1. 1.Department of ChemistrySavitribai Phule Pune University (Formerly Pune University)PuneIndia
  2. 2.IDP in Climate StudiesIndian Institute of Technology BombayMumbaiIndia

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