In vitro toxicity and epigenotoxicity of different types of ambient particulate matter

Toxicological Sciences

Volumn 148, Issue 2, 2015, Pages 473-487

  Miousse, Isabelle R ^a   Chalbot, Marie Cecile G ^a   Pathak, Rupak ^b   Lu, Xiaoyan ^c   Nzabarushimana, Etienne ^a,d   Krager, Kimberly ^b   Aykin Burns, Nukhet ^b   Hauer Jensen, Martin ^b   Demokritou, Philip ^c   Kavouras, Ilias G ^a   Koturbash, Igor ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d INDIANA UNIVERSITY   (United States)

Author keywords

Ambient particulate matter; Chromosomal aberrations; DNA methylation; Satellite DNA; Transposable elements

Indexed keywords

DNA METHYLTRANSFERASE; SATELLITE DNA; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNA (CYTOSINE-5-)-METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; PARTICULATE MATTER; TRANSPOSON;

AGRICULTURE; ANIMAL CELL; ARTICLE; BIOMASS; CELL LINE RAW 264.7; CHROMOSOME ABERRATION; CONTROLLED STUDY; CYTOTOXICITY; DEMETHYLATION; DNA METHYLATION; DUST; ENZYME ACTIVITY; EPIGENETICS; EXHAUST GAS; GENE EXPRESSION; GENE SILENCING; GENOTOXICITY; IN VITRO STUDY; MACROPHAGE; MOUSE; NONHUMAN; OXIDATION REDUCTION POTENTIAL; OXIDATIVE STRESS; PARTICULATE MATTER; POLLEN; PROTEIN EXPRESSION; RETROPOSON; SMOKE; SOIL; TRANSCRIPTION INITIATION; TRANSPOSON; UNITED STATES; ANIMAL; CHEMICALLY INDUCED; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PATHOLOGY; PROCEDURES; RAW 264.7 CELL LINE; TIME FACTOR; TOXICITY;

ANIMALS; CHROMOSOME ABERRATIONS; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; DNA TRANSPOSABLE ELEMENTS; DNA, SATELLITE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPIGENESIS, GENETIC; EPIGENOMICS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; MACROPHAGES; MICE; PARTICULATE MATTER; RAW 264.7 CELLS; TIME FACTORS;

EID: 84952901941     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfv200     Document Type: Article

References (61)

1. Alves, C., Vicente, A., Pio, C., Kiss, G., Hoffer, A., Decesari, S., Prevǒt, A. S. H., Minguillon, M. C., Querol, X., and Hillamo, R. (2012). Organic compounds in aerosols from selected European sites-Biogenic versus anthropogenic sources. Atmos. Environ. 59, 243-255.
2. Baccarelli, A., Wright, R. O., Bollati, V., Tarantini, L., Litonjua, A. A., Suh, H. H., Zanobetti, A., Sparrow, D., Vokonas, P. S., and Schwartz, J. (2009). Rapid DNA methylation changes after exposure to traffic particles. Am. J. Res. Critic. Care Med. 179, 572-578.
3. Biswas, S., Verma, V., Schauer, J. J., Cassee, F. R., Cho, A. K., and Sioutas, C. (2009). Oxidative potential of semi-volatile and non volatile particulate matter (PM) from heavy-duty vehicles retrofitted with emission control technologies. Environ. Sci. Technol. 43, 3905-3912.
4. Bouzinba-Segard, H., Guais, A., and Francastel, C. (2006). Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc. Natl. Acad. Sci. U.S.A. 103, 8709-8714.
5. Byun, H. M., Motta, V., Panni, T., Bertazzi, P. A., Apostoli, P., Hou, L., and Baccarelli, A. A. (2013). Evolutionary age of repetitive element subfamilies and sensitivity of DNA methylation to airborne pollutants. Part. Fibre Toxicol. 10, 28.
6. Chalbot, M., McElroy, B., and Kavouras, I. (2013a). Sources, trends and regional impacts of fine particulate matter in southern Mississippi valley: Significance of emissions from sources in the Gulf of Mexico coast. Atmos. Chem. Phys. 13, 3721-3732.
7. Chalbot, M., Nikolich, G., Etyemezian, V., Dubois, D. W., King, J., Shafer, D., DaCosta, G. G., Hinton, J. F., and Kavouras, I. (2013b). Soil humic-like organic compounds in prescribed fire emissions by nuclear magnetic resonance spectroscopy. Environ. Pollut. 181, 167-171.
8. Chalbot, M. C., da Costa, G. G., and Kavouras, I. G. (2013c). NMR analysis of the water-soluble fraction of airborne pollen particles. Appl. Magn. Reson. 44, 1347-1358.
9. Chalbot, M. C., and Kavouras, I. G. (2014). Nuclear magnetic resonance spectroscopy for determining the functional content of organic aerosols: A review. Environ. Pollut. 191, 232-249.
10. Crouse, D. L., Peters, P. A., van, D. A., Goldberg, M. S., Villeneuve, P. J., Brion, O., Khan, S., Atari, D. O., Jerrett, M., Pope, C. A., et al. (2012). Risk of nonaccidental and cardiovascular mortality in relation to long-term exposure to low concentrations of fine particulate matter: A Canadian national-level cohort study. Environ. Health Perspect. 120, 708-714.
11. de Koning, A. P., Gu, W., Castoe, T. A., Batzer, M. A., and Pollock, D. D. (2011). Repetitive elements may comprise over twothirds of the human genome. PLoS Genet. 7, e1002384.
12. Decesari, S., Mircea, M., Cavalli, F., Fuzzi, S., Moretti, F., Tagliavini, E., and Facchini, M. C. (2007). Source attribution of water-soluble organic aerosol by nuclear magnetic resonance spectroscopy. Environ. Sci. Technol. 41, 2479-2484.
13. Dominici, F., Peng, R. D., Bell, M. L., Pham, L., McDermott, A., Zeger, S. L., and Samet, J. M. (2006). Fine particulate air pollution and hospital admission for cardiovascular and respiratory diseases. JAMA. 295, 1127-1134.
14. Dominici, F., Peng, R. D., Zeger, S. L., White, R. H., and Samet, J. M. (2007). Particulate air pollution and mortality in the United States: Did the risks change from 1987 to 2000? Am. J. Epidemiol. 166, 880-888.
15. Ehrlich, M., Hopkins, N. E., Jiang, G., Dome, J. S., Yu, M. C., Woods, C. B., Tomlinson, G. E., Chintagumpala, M., Champagne, M., Dillerg, L., et al. (2003). Satellite DNA hypomethylation in karyotyped Wilms tumors. Cancer Genet. Cytogenet. 141, 97-105.
16. Ehrlich, M. and Lacey, M. (2013). DNA hypomethylation and hemimethylation in cancer. Adv. Exp. Med. Biol. 754, 31-56.
17. Fragou, D., Fragou, A., Kouidou, S., Njau, S., and Kovatsi, L. (2011). Epigenetic mechanisms in metal toxicity. Toxicol Mech. Methods 21, 343-352.
18. Graham, B., Mayol-Bracero, O. L., Guyon, P., Roberts, G. C., Decesari, S., Facchini, M. C., Artaxo, P., Maenhaut, W., Kö II, P., and Andreae, M. O. (2002). Water-soluble organic compounds in biomass burning aerosols over Amazonia 1. Characterization by NMR and GC-MS. J. Geophys. Res. 107, LBA-14.
19. Guenatri, M., Bailly, D., Maison, C., and Almouzni, G. (2004). Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 166, 493-505.
20. Guo, L., Byun, H. M., Zhong, J., Motta, V., Barupal, J., Zheng, Y., Dou, C., Zhang, F., McCracken, J. P., Diaz, A., et al. (2014). Effects of short-term exposure to inhalable particulate matter on DNA methylation of tandem repeats. Environ. Mol. Mutagen. 55, 322-335.
21. Haider, S., Cordeddu, L., Robinson, E., Movassagh, M., Siggens, L., Vujic, A., Choy, M. K., Goddard, M., Lio, P., and Foo, R. (2012). The landscape of DNA repeat elements in human heart failure. Genome Biol. 13, R90.
22. Halatek, T., Stepnik, M., Stetkiewicz, J., Krajnow, A., Kur, B., Szymczak, W., Rydzynski, K., Dybing, E., and Cassee, F. R. (2011). The inflammatory response in lungs of rats exposed on the airborne particles collected during different seasons in four European cities. J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng. 46, 1469-1481.
23. Happo, M. S., Salonen, R. O., Halinen, A. I., Jalava, P. I., Pennanen, A. S., Dormans, J. A., Gerlofs-Nijland, M. E., Cassee, F. R., Kosma, V. M., Sillanpaa, M., et al. (2010). Inflammation and tissue damage in mouse lung by single and repeated dosing of urban air coarse and fine particles collected from six European cities. Inhal. Toxicol. 22, 402-416.
24. Havers, N., Burba, P., Lambert, J., and Klockow, D. (1998). Spectroscopic characterization of humic-like substances in airborne particulate matter. J. Atmos. Chem. 29, 45-54.
25. Hou, L., Zhang, X., Zheng, Y., Wang, S., Dou, C., Guo, L., Byun, H. M., Motta, V., McCracken, J., Diaz, A., et al. (2014). Altered methylation in tandem repeat element and elemental component levels in inhalable air particles. Environ. Mol. Mutagen. 55, 256-265.
26. ISCN (1978). Report of the Standing Commitee on Human Cytogenetic Nomenclature. Cytogenet. Cell. Genet. 21, 309-404.
27. Jalava, P. I., Hirvonen, M. R., Sillanpaa, M., Pennanen, A. S., Happo, M. S., Hillamo, R., Cassee, F. R., Gerlofs-Nijland, M., Borm, P. J., Schins, R. P., et al. (2009). Associations of urban air particulate composition with inflammatory and cytotoxic responses in RAW 246.7 cell line. Inhal. Toxicol. 21, 994-1006.
28. Jalava, P. I., Salonen, R. O., Pennanen, A. S., Happo, M. S., Penttinen, P., Halinen, A. I., Sillanpaa, M., Hillamo, R., and Hirvonen, M. R. (2008). Effects of solubility of urban air fine and coarse particles on cytotoxic and inflammatory responses in RAW264.7 macrophage cell line. Toxicol. Appl. Pharmacol. 229, 146-160.
29. Jalava, P. I., Salonen, R. O., Pennanen, A. S., Sillanpaa, M., Halinen, A. I., Happo, M. S., Hillamo, R., Brunekreef, B., Katsouyanni, K., Sunyer, J., et al. (2007). Heterogeneities in inflammatory and cytotoxic responses of RAW 264.7 macrophage cell line to urban air coarse, fine, and ultrafine particles from six European sampling campaigns. Inhal. Toxicol. 19, 213-225.
30. Janssen, N. A., Yang, A., Strak, M., Steenhof, M., Hellack, B., Gerlofs-Nijland, M. E., Kuhlbusch, T., Kelly, F., Harrison, R., Brunekreef, B., et al. (2014). Oxidative potential of particulate matter collected at sites with different source characteristics. Sci. Total Environ. 472, 572-581.
31. Jiang, R., Jones, M. J., Sava, F., Kobor, M. S., and Carlsten, C. (2014). Short-term diesel exhaust inhalation in a controlled human crossover study is associated with changes in DNA methylation of circulating mononuclear cells in asthmatics. Part. Fibre Toxicol. 11, 71.
32. Koturbash, I., Scherhag, A., Sorrentino, J., Sexton, K., Bodnar, W., Tryndyak, V., Latendresse, J. R., Swenberg, J. A., Beland, F. A., Pogribny, I. P., et al. (2011). Epigenetic alterations in liver of C57BL/6J mice after short-term inhalational exposure to 1, 3-butadiene. Environ. Health Perspect. 119, 635-640.
33. Kroll, A., Gietl, J. K., Wiesmüller, G. A., Günsel, A., Wohlleben, W., Schnekenburger, J., and Klemm, O. (2013). In vitro toxicology of ambient particulate matter: Correlation of cellular effects with particle size and components. Environ. Toxicol. 28, 76-86.
34. Lee, R., Nasonova, E., and Ritter, S. (2005). Chromosome aberration yields and apoptosis in human lymphocytes irradiated with Fe-ions of differing LET. Adv. Space Res. 35, 268-75.
35. Loxham, M., Morgan-Walsh, R. J., Cooper, M. J., Blume, C., Swindle, E. J., Dennison, P. W., Howarth, P. H., Cassee, F. R., Teagle, D. A., Palmer, M. R., et al. (2015). The effects on bronchial epithelial mucociliary cultures of coarse, fine, and ultrafine particulatematter from an underground railway station. Toxicol. Sci. 145, 98-107.
36. Lu, X., Miousse, I. R., Pirela, S. V., Melnyk, S., Koturbash, I., and Demokritou, P. (2015). Short-term exposure to engineered nanomaterials affects cellular epigenome. Nanotoxicology. DOI:10.3109/17435390.2015.1025115.
37. Madrigano, J., Baccarelli, A., Mittleman, M. A., Wright, R. O., Sparrow, D., Vokonas, P. S., Tarantini, L., and Schwartz, J. (2011). Prolonged exposure to particulate pollution, genes associated with glutathione pathways, and DNA methylation in a cohort of older men. Environ. Health Perspect. 119, 977-982.
38. Marple, V. A., Rubow, K. L., Turner, W., and Spengler, J. D. (1987). Low flow rate sharp cut impactors for indoor air sampling: Design and calibration. JAPCA. 37, 1303-1307.
39. Martens, J. H., O'Sullivan, R. J., Braunschweig, U., Opravil, S., Radolf, M., Steinlein, P., and Jenuwein, T. (2005). The profile of repeat-associated histone lysine methylation states in the mouse epigenome. EMBO J. 24, 800-812.
40. Michael, S., Montag, M., and Dott, W. (2013). Pro-inflammatory effects and oxidative stress in lung macrophages and epithelial cells induced by ambient particulate matter. Environ. Pollut. 183, 19-29.
41. Miousse, I. R., Chalbot, M. C., Aykin-Burns, N., Wang, X., Basnakian, A., Kavouras, I. G., and Koturbash, I. (2014a). Epigenetic alterations induced by ambient particulate matter in mouse macrophages. Environ. Mol. Mutagen. 55, 428-435.
42. Miousse, I. R., Chalbot, M. C., Lumen, A., Ferguson, A., Kavouras, I. G., and Koturbash, I. (2015). Response of transposable elements to environmental stressors. Mutat. Res. Rev. Mutat. Res. 335, 11-19.
43. Miousse, I. R., Shao, L., Chang, J., Feng, W., Wang, Y., Allen, A. R., Turner, J., Stewart, B., Raber, J., Zhou, D., et al. (2014b). Exposure to low-dose (56)Fe-ion radiation induces long-term epigenetic alterations in mouse bone marrow hematopoietic progenitor and stem cells. Radiat. Res. 182, 92-101.
44. Okano, M., Bell, D. W., Haber, D. A., and Li, E. (1999). DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99, 247-257.
45. Papait, R., Pistore, C., Negri, D., Pecoraro, D., Cantarini, L., and Bonapace, I. M. (2007). Np95 is implicated in pericentromeric heterochromatin replication and in major satellite silencing. Mol. Biol. Cell 18, 1098-1106.
46. Pathak, R., Pawar, S. A., Fu, Q., Gupta, P. K., Berbee, M., Garg, S., Sridharan, V., Wang, W., Biju, P. G., Krager, K. J., et al. (2014). Characterization of transgenic Gfrp knock-in mice: Implications for tetrahydrobiopterin in modulation of normal tissue radiation responses. Antioxid. Redox Signal. 20, 1436-1446.
47. Rogge, W. F., Hildemann, L. M., Mazurek, M. A., Cass, G. R., and Simoneit, B. R. T. (1993a). Sources of fine organic aerosol. 3. Road dust, tire debris, and organometallic brake lining dust: Roads as sources and sinks. Environ. Sci. Technol. 27, 1892-1904.
48. Rogge, W. F., Hildemann, L. M., Mazurek, M. A., Cass, G. R., and Simoneit, B. R. T. (1993b). Sources of fine organic aerosol. 4. Particulate abrasion products from leaf surfaces of urban plants. Environ. Sci. Technol. 27, 2700-2711.
49. Rogge, W. F., Hildemann, L. M., Mazurek, M. A., Cass, G. R., and Simoneit, B. R. T. (1998). Sources of fine organic aerosol. 9. Pine, oak, and synthetic log combustion in residential fireplaces. Environ. Sci. Technol. 32, 13-22.
50. Rückerl, R., Schneider, A., Breitner, S., Cyrys, J., and Peters, A. (2011). Health effects of particulate air pollution: A review of epidemiological evidence. Inhal. Toxicol. 23, 555-592.
51. Rudin, C. M., and Thompson, C. B. (2001). Transcriptional activation of short interspersed elements by DNA-damaging agents. Genes Chromosomes Cancer. 30, 64-71.
52. Schmittgen, T. D., and Livak, K. J. (2008). Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 3, 1101-1108.
53. Shi, T., Duffin, R., Borm, P. J. A., Li, H., Weishaupt, C., and Schins, R. P. F. (2006). Hydroxyl-radical-dependent DNA damage by ambient particulate matter from contrasting sampling locations. Environ. Res. 101, 18-24.
54. Steenhof, M., Gosens, I., Strak, M., Godri, K. J., Hoek, G., Cassee, F. R., Mudway, I. S., Kelly, F. J., Harrison, R. M., Lebret, E., et al. (2011). In vitro toxicity of particulate matter (PM) collected at different sites in the Netherlands is associated with PM composition, size fraction and oxidative potential-the RAPTES project. Part. Fibre Toxicol. 8, 26.
55. Ting, D. T., Lipson, D., Paul, S., Brannigan, B. W., Akhavanfard, S., Coffman, E. J., Contino, G., Deshpande, V., Iafrate, A. J., Letovsky, S., et al. (2011). Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 331, 593-596.
56. Tsuda, H., Takarabe, T., Kanai, Y., Fukutomi, T., and Hirohashi, S. (2002). Correlation of DNA hypomethylation at pericentromeric heterochromatin regions of chromosomes 16 and 1 with histological features and chromosomal abnormalities of human breast carcinomas. Am. J. Pathol. 161, 859-866.
57. Ugarkovic, D. (2005). Functional elements residing within satellite DNAs. EMBO Rep. 6, 1035-1039.
58. van Berlo, D., Hullmann, M., and Schins, R. P. (2012). Toxicology of ambient particulate matter. EXS. 101, 165-217.
59. Van Vaeck, L. and Van Cauwenberghe, K. A. (1985). Characteristic parameters of particle size distributions of primary organic constituents of ambient aerosols. Environ. Sci. Technol. 19, 707-716.
60. Wu, E. L., Engström, O., Jo, S., Stuhlsatz, D., Yeom, M. S., Klauda, J. B., and Im, W. (2013). Molecular dynamics and NMR spectroscopy studies of E. coli lipopolysaccharide structure and dynamics. Biophys. J, 105, 1444-1455.
61. Xu, G. L., Bestor, T. H., Bourc'his, D., Hsieh, C. L., Tommerup, N., Bugge, M., Hulten, M., Qu, X., Russo, J. J., and Viegas-Pequignot, E. (1999). Chromosome instability and immunodeficiency syndrome caused by mutations in a DNA methyltransferase gene. Nature 402, 187-191.