Wood Smoke Particle Sequesters Cell Iron to Impact a Biological Effect

Chemical Research in Toxicology

Volumn 28, Issue 11, 2015, Pages 2104-2111

  Ghio, Andrew J ^a   Soukup, Joleen M ^a   Dailey, Lisa A ^a   Tong, Haiyan ^a   Kesic, Matthew J ^b   Scott Budinger, G R ^c   Mutlu, Gökhan M ^d  

^a U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^b METHODIST UNIVERSITY   (United States)

^c NORTHWESTERN UNIVERSITY   (United States)

^d Department of Medicine   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FERRIC AMMONIUM CITRATE; FERRITIN; HUMIC ACID; INTERLEUKIN 6; INTERLEUKIN 8; IRON; IRON 57; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; TRANSCRIPTION FACTOR NRF2; DMRT1 PROTEIN; HUMIC SUBSTANCE; IL6 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE; SMOKE; TRANSCRIPTION FACTOR;

AIRBORNE PARTICLE; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BIOLOGICAL ACTIVITY; CELL METABOLISM; CHEMOLUMINESCENCE; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME PHOSPHORYLATION; EPITHELIUM CELL; EXPOSURE; HOST CELL; HUMAN; HUMAN CELL; HUMIC SUBSTANCE; IRON CHELATION; MITOCHONDRION; NORMAL HUMAN; OXIDATION; RESPIRATORY EPITHELIUM; SMOKE; WOOD; WOOD SMOKE PARTICLE; ADVERSE EFFECTS; CELL LINE; CELL NUCLEUS; GENETICS; METABOLISM;

CELL LINE; CELL NUCLEUS; HUMANS; HUMIC SUBSTANCES; INTERLEUKIN-6; INTERLEUKIN-8; IRON; MITOCHONDRIA; MITOGEN-ACTIVATED PROTEIN KINASES; SMOKE; TRANSCRIPTION FACTORS; WOOD;

EID: 84947125108     PISSN: 0893228X     EISSN: 15205010     Source Type: Journal    
DOI: 10.1021/acs.chemrestox.5b00270     Document Type: Article

References (47)

1. Churg, A., Zay, K., and Li, K. (1997) Mechanisms of mineral dust-induced emphysema Environ. Health Perspect. 105 (Suppl 5) 1215-1218 10.2307/3433535
2. Grobbelaar, J. P. and Bateman, E. D. (1991) Hut lung: a domestically acquired pneumoconiosis of mixed aetiology in rural women Thorax 46, 334-340 10.1136/thx.46.5.334
3. Ozbay, B., Uzun, K., Arslan, H., and Zehir, I. (2001) Functional and radiological impairment in women highly exposed to indoor biomass fuels Respirology 6, 255-258 10.1046/j.1440-1843.2001.00339.x
4. Pinkerton, K. E., Green, F. H., Saiki, C., Vallyathan, V., Plopper, C. G., Gopal, V., Hung, D., Bahne, E. B., Lin, S. S., Menache, M. G., and Schenker, M. B. (2000) Distribution of particulate matter and tissue remodeling in the human lung Environ. Health Perspect. 108, 1063-1069 10.1289/ehp.001081063
5. Pratt, P. C., Jutabha, P., and Klugh, G. A. (1963) The relationship between pigment deposits and lesions in normal and centrilobular emphysematous lungs Am. Rev. Respir. Dis. 87, 245-256
6. Rudell, B., Blomberg, A., Helleday, R., Ledin, M. C., Lundback, B., Stjernberg, N., Horstedt, P., and Sandstrom, T. (1999) Bronchoalveolar inflammation after exposure to diesel exhaust: comparison between unfiltered and particle trap filtered exhaust Occup. Environ. Med. 56, 527-534 10.1136/oem.56.8.527
7. Weiss, W. (1969) Cigarette smoking and diffuse pulmonary fibrosis Am. Rev. Respir. Dis. 99, 67-72
8. Ghio, A. J., Jaskot, R. H., and Hatch, G. E. (1994) Lung injury after silica instillation is associated with an accumulation of iron in rats Am. J. Physiol. 267, L686-692
9. Koerten, H. K., Brederoo, P., Ginsel, L. A., and Daems, W. T. (1986) The endocytosis of asbestos by mouse peritoneal macrophages and its long-term effect on iron accumulation and labyrinth formation Eur. J. Cell Biol. 40, 25-36
10. Ghio, A. J., Churg, A., and Roggli, V. L. (2004) Ferruginous bodies: implications in the mechanism of fiber and particle toxicity Toxicol. Pathol. 32, 643-649 10.1080/01926230490885733
11. Ghio, A. J., Stonehuerner, J., Pritchard, R. J., Piantadosi, C. A., Quigley, D. R., Dreher, K. L., and Costa, D. L. (1996) Humic-like substances in air pollution particulates correlate with concentrations of transition metals and oxidant generation Inhalation Toxicol. 8, 479-494 10.3109/08958379609005441
12. Ghio, A. J., Stonehuerner, J., and Quigley, D. R. (1994) Humic-like substances in cigarette smoke condensate and lung tissue of smokers Am. J. Physiol. 266, L382-388
13. Sporn, T. A. and Roggli, V. L. (2008) Pneumoconioses, Mineral and Vegetable. In Dail and Hammar's Pulmonary Pathology. Vol. I. Nonneoplastic Lung Disease (Tomashefski, J. F. J., Cagle, P. T., Farver, C. F., and Fraire, A. E., Eds.) p 933, Springer.
14. Ghio, A. J., Carter, J. D., Samet, J. M., Reed, W., Quay, J., Dailey, L. A., Richards, J. H., and Devlin, R. B. (1998) Metal-dependent expression of ferritin and lactoferrin by respiratory epithelial cells Am. J. Physiol. 274, L728-736
15. Greenawalt, J. W. (1974) The isolation of outer and inner mitochondrial membranes Methods Enzymol. 31, 310-323 10.1016/0076-6879(74)31033-6
16. Kesic, M., Ward, M., Semmes, O. J., and Green, P. L. (2009) Site-specific phosphorylation regulates human T-cell leukemia virus type 2 Rex function in vivo J. Virol. 83, 8859-8868 10.1128/JVI.00908-09
17. Ghio, A. J., Tong, H., Soukup, J. M., Dailey, L. A., Cheng, W. Y., Samet, J. M., Kesic, M. J., Bromberg, P. A., Turi, J. L., Upadhyay, D., Scott Budinger, G. R., and Mutlu, G. M. (2013) Sequestration of mitochondrial iron by silica particle initiates a biological effect Am. J. Physiol. Lung Cell Mol. Physiol. 305, L712-724 10.1152/ajplung.00099.2013
18. Gunshin, H., Mackenzie, B., Berger, U. V., Gunshin, Y., Romero, M. F., Boron, W. F., Nussberger, S., Gollan, J. L., and Hediger, M. A. (1997) Cloning and characterization of a mammalian proton-coupled metal-ion transporter Nature 388, 482-488 10.1038/41343
19. Moller, I. M. (2001) PLANT MITOCHONDRIA AND OXIDATIVE STRESS: Electron Transport, NADPH Turnover, and Metabolism of Reactive Oxygen Species Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 561-591 10.1146/annurev.arplant.52.1.561
20. Chen, Q., Vazquez, E. J., Moghaddas, S., Hoppel, C. L., and Lesnefsky, E. J. (2003) Production of reactive oxygen species by mitochondria: central role of complex III J. Biol. Chem. 278, 36027-36031 10.1074/jbc.M304854200
21. Grivennikova, V. G. and Vinogradov, A. D. (2006) Generation of superoxide by the mitochondrial Complex I Biochim. Biophys. Acta, Bioenerg. 1757, 553-561 10.1016/j.bbabio.2006.03.013
22. Callens, C., Coulon, S., Naudin, J., Radford-Weiss, I., Boissel, N., Raffoux, E., Wang, P. H., Agarwal, S., Tamouza, H., Paubelle, E., Asnafi, V., Ribeil, J. A., Dessen, P., Canioni, D., Chandesris, O., Rubio, M. T., Beaumont, C., Benhamou, M., Dombret, H., Macintyre, E., Monteiro, R. C., Moura, I. C., and Hermine, O. (2010) Targeting iron homeostasis induces cellular differentiation and synergizes with differentiating agents in acute myeloid leukemia J. Exp. Med. 207, 731-750 10.1084/jem.20091488
23. Chaston, T. B., Watts, R. N., Yuan, J., and Richardson, D. R. (2004) Potent antitumor activity of novel iron chelators derived from di-2-pyridylketone isonicotinoyl hydrazone involves fenton-derived free radical generation Clin. Cancer Res. 10, 7365-7374 10.1158/1078-0432.CCR-04-0865
24. Dendorfer, A., Heidbreder, M., Hellwig-Burgel, T., Johren, O., Qadri, F., and Dominiak, P. (2005) Deferoxamine induces prolonged cardiac preconditioning via accumulation of oxygen radicals Free Radical Biol. Med. 38, 117-124 10.1016/j.freeradbiomed.2004.10.015
25. Cakmak, I., van de Wetering, D. A., Marschner, H., and Bienfait, H. F. (1987) Involvement of Superoxide Radical in Extracellular Ferric Reduction by Iron-Deficient Bean Roots Plant Physiol. 85, 310-314 10.1104/pp.85.1.310
26. Rose, A. L., Salmon, T. P., Lukondeh, T., Neilan, B. A., and Waite, T. D. (2005) Use of superoxide as an electron shuttle for iron acquisition by the marine cyanobacterium Lyngbya majuscula Environ. Sci. Technol. 39, 3708-3715 10.1021/es048766c
27. Turi, J. L., Jaspers, I., Dailey, L. A., Madden, M. C., Brighton, L. E., Carter, J. D., Nozik-Grayck, E., Piantadosi, C. A., and Ghio, A. J. (2002) Oxidative stress activates anion exchange protein 2 and AP-1 in airway epithelial cells Am. J. Physiol. Lung Cell. Mol. Physiol. 283, L791-798 10.1152/ajplung.00398.2001
28. Barnes, R., Connelly, J. L., and Jones, O. T. (1972) The utilization of iron and its complexes by mammalian mitochondria Biochem. J. 128, 1043-1055 10.1042/bj1281043
29. Romslo, I. and Flatmark, T. (1973) Energy-dependent accumulation of iron by isolated rat liver mitochondria. II. Relationship to the active transport of Ca2+ Biochim. Biophys. Acta, Bioenerg. 325, 38-46 10.1016/0005-2728(73)90148-5
30. Tsuda, A., Takeda, S., Saito, H., Nishioka, J., Nojiri, Y., Kudo, I., Kiyosawa, H., Shiomoto, A., Imai, K., Ono, T., Shimamoto, A., Tsumune, D., Yoshimura, T., Aono, T., Hinuma, A., Kinugasa, M., Suzuki, K., Sohrin, Y., Noiri, Y., Tani, H., Deguchi, Y., Tsurushima, N., Ogawa, H., Fukami, K., Kuma, K., and Saino, T. (2003) A mesoscale iron enrichment in the western subarctic Pacific induces a large centric diatom bloom Science 300, 958-961 10.1126/science.1082000
31. Wang, T., Chiang, E. T., Moreno-Vinasco, L., Lang, G. D., Pendyala, S., Samet, J. M., Geyh, A. S., Breysse, P. N., Chillrud, S. N., Natarajan, V., and Garcia, J. G. (2010) Particulate matter disrupts human lung endothelial barrier integrity via ROS- and p38 MAPK-dependent pathways Am. J. Respir. Cell Mol. Biol. 42, 442-449 10.1165/rcmb.2008-0402OC
32. Perng, D. W., Chang, T. M., Wang, J. Y., Lee, C. C., Lu, S. H., Shyue, S. K., Lee, T. S., and Kou, Y. R. (2013) Inflammatory role of AMP-activated protein kinase signaling in an experimental model of toxic smoke inhalation injury Crit. Care Med. 41, 120-132 10.1097/CCM.0b013e318265f653
33. Li, R., Ning, Z., Cui, J., Khalsa, B., Ai, L., Takabe, W., Beebe, T., Majumdar, R., Sioutas, C., and Hsiai, T. (2009) Ultrafine particles from diesel engines induce vascular oxidative stress via JNK activation Free Radical Biol. Med. 46, 775-782 10.1016/j.freeradbiomed.2008.11.025
34. Li, C. J., Ning, W., Matthay, M. A., Feghali-Bostwick, C. A., and Choi, A. M. (2007) MAPK pathway mediates EGR-1-HSP70-dependent cigarette smoke-induced chemokine production Am. J. Physiol. Lung Cell. Mol. Physiol. 292, L1297-1303 10.1152/ajplung.00194.2006
35. Lee, T. S., Liu, Y. J., Tang, G. J., Yien, H. W., Wu, Y. L., and Kou, Y. R. (2008) Wood smoke extract promotes both apoptosis and proliferation in rat alveolar epithelial type II cells: the role of oxidative stress and heme oxygenase-1 Crit. Care Med. 36, 2597-2606 10.1097/CCM.0b013e318184979c
36. Albrecht, C., Borm, P. J., Adolf, B., Timblin, C. R., and Mossman, B. T. (2002) In vitro and in vivo activation of extracellular signal-regulated kinases by coal dusts and quartz silica Toxicol. Appl. Pharmacol. 184, 37-45 10.1006/taap.2002.9500
37. Samet, J. M., Stonehuerner, J., Reed, W., Devlin, R. B., Dailey, L. A., Kennedy, T. P., Bromberg, P. A., and Ghio, A. J. (1997) Disruption of protein tyrosine phosphate homeostasis in bronchial epithelial cells exposed to oil fly ash Am. J. Physiol. 272, L426-432
38. Yu, Y. and Richardson, D. R. (2011) Cellular iron depletion stimulates the JNK and p38 MAPK signaling transduction pathways, dissociation of ASK1-thioredoxin, and activation of ASK1 J. Biol. Chem. 286, 15413-15427 10.1074/jbc.M111.225946
39. Knorr-Wittmann, C., Hengstermann, A., Gebel, S., Alam, J., and Muller, T. (2005) Characterization of Nrf2 activation and heme oxygenase-1 expression in NIH3T3 cells exposed to aqueous extracts of cigarette smoke Free Radical Biol. Med. 39, 1438-1448 10.1016/j.freeradbiomed.2005.07.003
40. Deng, X., Rui, W., Zhang, F., and Ding, W. (2013) PM2.5 induces Nrf2-mediated defense mechanisms against oxidative stress by activating PIK3/AKT signaling pathway in human lung alveolar epithelial A549 cells Cell Biol. Toxicol. 29, 143-157 10.1007/s10565-013-9242-5
41. Cheng, S. E., Lee, I. T., Lin, C. C., Kou, Y. R., and Yang, C. M. (2010) Cigarette smoke particle-phase extract induces HO-1 expression in human tracheal smooth muscle cells: role of the c-Src/NADPH oxidase/MAPK/Nrf2 signaling pathway Free Radical Biol. Med. 48, 1410-1422 10.1016/j.freeradbiomed.2010.02.026
42. Chan, J. K., Charrier, J. G., Kodani, S. D., Vogel, C. F., Kado, S. Y., Anderson, D. S., Anastasio, C., and Van Winkle, L. S. (2013) Combustion-derived flame generated ultrafine soot generates reactive oxygen species and activates Nrf2 antioxidants differently in neonatal and adult rat lungs Part. Fibre Toxicol. 10, 34 10.1186/1743-8977-10-34
43. Chen, F., Sun, S., Kuhn, D. C., Gaydos, L. J., Shi, X., Lu, Y., and Demers, L. M. (1997) Involvement of NF-kappaB in silica-induced cyclooxygenase II gene expression in rat alveolar macrophages Am. J. Physiol. 272, L779-786
44. Li, N., Kim, S., Wang, M., Froines, J., Sioutas, C., and Nel, A. (2002) Use of a stratified oxidative stress model to study the biological effects of ambient concentrated and diesel exhaust particulate matter Inhalation Toxicol. 14, 459-486 10.1080/089583701753678571
45. Su, B. and Karin, M. (1996) Mitogen-activated protein kinase cascades and regulation of gene expression Curr. Opin. Immunol. 8, 402-411 10.1016/S0952-7915(96)80131-2
46. Xiao, G. G., Wang, M., Li, N., Loo, J. A., and Nel, A. E. (2003) Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line J. Biol. Chem. 278, 50781-50790 10.1074/jbc.M306423200
47. Dikalov, S., Alov, P., and Rangelova, D. (1993) Role of iron ion chelation by quinones in their reduction, OH-radical generation and lipid peroxidation Biochem. Biophys. Res. Commun. 195, 113-119 10.1006/bbrc.1993.2017