SO2 Inhalation contributes to the development and progression of ischemic stroke in the brain

Toxicological Sciences

Volumn 114, Issue 2, 2010, Pages 226-236

  Sang, Nan ^a   Yun, Yang ^a   Li, Hongyan ^a   Hou, Li ^a   Han, Ming ^a   Li, Guangke ^a  

^a SHANXI UNIVERSITY   (China)

Author keywords

Air pollution; Endothelial dysfunction; Inflammatory response; Ischemic stroke; SO2 inhalation

Indexed keywords

CASPASE 3; CYCLOOXYGENASE 2; ENDOTHELIN 1; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERCELLULAR ADHESION MOLECULE 1; SULFUR DIOXIDE; MESSENGER RNA; NOS2 PROTEIN, RAT; PTGS2 PROTEIN, RAT;

AIR POLLUTION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN INFARCTION SIZE; BRAIN ISCHEMIA; CEREBROVASCULAR ACCIDENT; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENVIRONMENTAL EXPOSURE; GENE EXPRESSION; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; RAT; AIR POLLUTANT; ANIMAL; CEREBRAL ARTERY DISEASE; CHEMICALLY INDUCED DISORDER; DISEASE COURSE; DISEASE MODEL; DRUG EFFECT; EXPOSURE; GENETICS; METABOLISM; PATHOLOGY; STROKE; WISTAR RAT;

RATTUS; RATTUS NORVEGICUS;

AIR POLLUTANTS; ANIMALS; CYCLOOXYGENASE 2; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; ENDOTHELIN-1; GENE EXPRESSION; INFARCTION, MIDDLE CEREBRAL ARTERY; INHALATION EXPOSURE; INTERCELLULAR ADHESION MOLECULE-1; MALE; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, WISTAR; RNA, MESSENGER; STROKE; SULFUR DIOXIDE;

EID: 77951565288     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfq010     Document Type: Article

References (62)

1. Andresen, J., Shafi, N. I., and Bryan, R. M. J. (2006). Endothelial influences on cerebrovascular tone. J. Appl. Physiol. 100, 318-327.
2. Beckett, W. S., McDonnell, W. F., Horstman, D. H., and House, D. E. (1985). Role of the parasympathetic nervous system in acute lung response to ozone. J. Appl. Physiol. 59, 1879-1885.
3. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
4. Brondani, R., Rieder, C. R. M., Valente, D., Araújo, L. F., and Clausell, N. (2007). Levels of vascular cell adhesion molecule-1 and endothelin-1 in ischemic stroke: a longitudinal prospective study. Clin. Biochem. 40, 282-284.
5. Bulletin of Environmental status in China. (2008). Available at: http://www.mep.gov.cn/gzfw/xzzx/wdxz/200906/P020090609397520028674.pdf.
6. 2stress as observed at different stages of plant development. Flora 202, 268-280.
7. Cai, F., Li, C. R., Wu, J. L., Chen, J. G., Liu, C., Min, Q., Yu, W., Ouyang, C. H., and Chen, J. H. (2006). Theaflavin ameliorates cerebral ischemia-reperfusion injury in rats through its anti-inflammatory effect and modulation of STAT-1. Mediators Inflamm. 2006, 30490.
8. Chang, Y., Hsieh, C. Y., Peng, Z. A., Yen, T. L., Hsiao, G., Chou, D. S., Chen, C. M., and Sheu, J. R. (2009). Neuroprotective mechanisms of puerarin in middle cerebral artery occlusion-induced brain infarction in rats. J. Biomed. Sci. 16, 9.
9. Chen, P., Shibata, M., Zidovetzki, R., Fisher, M., Zlokovic, B. V., and Hofman, F. M. (2001). Endothelin-1 and monocyte chemoattractant protein-1 modulation in ischemia and human brain-derived endothelial cell cultures. J. Neuroimmunol. 116, 62-73.
10. Dalhamn, T. (1971). Studies on the effect of sulfur dioxide on ciliary activity in rabbit trachea in vivo and on the reabsorptional capacity of the nasal cavity. Am. Rev. Respir. Dis. 83, 566-567.
11. del Zoppo, G., Ginis, I., Hallenbeck, J. M., Iadecola, C., Wang, X., and Feurstein, G. Z. (2000). Inflammation and stroke: putative role for cytokines, adhesion molecules and iNOS in brain response to ischemia. Brain Pathol. 10, 95-112.
12. Ding, Y. C., Young, C. N., Li, J., Luan, X. D., McAllister, J. P., Clark, J. D., and Diaz, F. G. (2003). Reduced inflammatory mediator expression by pre-reperfusion infusion into ischemic territory in rats: a real-time polymerase chain reaction analysis. Neurosci. Lett. 353, 173-176.
13. Doré, S., Otsuka, T., Mito, T., Sugo, N., Hand, T., Wu, L., Hurn, P. D., and Traystman, R. J. (2003). Neuronal overexpression of cyclooxygenase-2 increases cerebral infarction. Ann. Neurol. 54, 155-162.
14. Dutch Expert Committee on Occupational Standards. (2003). Sulphur Dioxide; Health-Based Recommended Occupational Exposure Limit, 5th ed. (ISBN 90-5549-507-7). Health Council of the Netherlands Press, Hague, The Netherlands.
15. El-Dars, F. M., Mohamed, A. M., and Aly, H. A. (2004). Monitoring ambient sulfur dioxide levels at some residential environments in the Greater Cairo urban region-Egypt. Environ. Monit. Assess. 95, 269-286.
16. Environmental Protection Agency. (2002). National Ambient Air Quality Standards (NAAQS). Available at: http://www.epa.gov/ttnnaaqs/.
17. GB 3095-1996. (1996). Ambient Air Quality Standard (In China). Available at: http://kjs.mep.gov.cn/hjbhbz/bzwb/dqhjbh/dqhjzlbz/199612/t19961206_67502.htm.
18. Gorlach, C., Hortobagyi, T., Hortobagyi, S., Benyo, Z., and Wahl, M. (2001). Inhibition of endothelin-1 by the competitive ET (A) receptor antagonist Ro 61-1790 reduces lesion volume after cold injury in the rat. Pflugers Arch. 441, 844-849.
19. Govoni, S., Masoero, E., Favalli, L., Rozza, A., Scelsi, R., Viappiani, S., Buccellati, C., Sala, A., and Folco, G. (2001). The cycloxygenase-2 inhibitor SC58236 is neuroprotective in an in vivomodel of focal ischemia in the rat. Neurosci. Lett. 303, 91-94.
20. 2 determination and method sensitivity analysis. J. Environ. Monit. 3, 666-670.
21. Gümü̧lü, S., Bi·lmen, S., Korgun, D., Yargi̧oǧlu, P., and Aǧar, A. (2001). Age-related changes in antioxidant enzyme activities and lipid peroxidation in lungs of control and sulfur dioxide exposed rats. Free Radic. Res. 3, 621-627.
22. Gunnison, A. F., and Palmes, E. D. (1974). S-sulfonates in human plasma following inhalation of sulfur dioxide. Am. Ind. Hyg. Assoc. J. 35, 288-291.
23. Haider, S. S., and Hasan, M. (1984). Neurochemical changes by inhalation of environmental pollutants sulfur dioxide and hydrogen sulfide: degradation of total lipids, elevation of lipid peroxidation and enzyme activity in discrete regions of the guinea pig brain and spinal cord. Ind. Health. 22, 23-31.
24. Hong, Y. C., Lee, J. T., Kim, H., Ha, E. H., Schwartz, J., and Christiani, D. C. (2002). Effects of air pollutants on acute stroke mortality. Environ. Health Perspect. 110, 187-191.
25. Hu, X., Johansson, I. M., Brännström, T., Olsson, T., and Wester, P. (2002). Long-lasting neuronal apoptotic cell death in regions with severe ischemia after photothrombotic ring stroke in rats. Acta Neuropathol. 104, 462-470.
26. Iadecola, C., Niwa, K., Nogawa, S., Zhao, X., Nagayama, M., Araki, E., Morham, S., and Ross, M. E. (2001). Reduced susceptibility to ischemic brain injury and N-methyl-D-aspartate-mediated neurotoxicity in cyclooxygenase-2-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 98, 1294-1299.
27. Jiang, M. H., Kaku, T., Hada, J., and Hayashi, Y. (1999). 7-Nitroindazole reduces nitric oxide concentration in rat hippocampus after transient forebrain ischemia. Eur. J. Pharmacol. 380, 117-121.
28. 2 exposure on rat lung tumorigenesis. Cancer Lett. 139, 189-197.
29. Klijn, C. J. M., and Hankey, G. J. (2003). Management of acute ischemic stroke: new guidelines from the American stroke association and European stroke initiative. Lancet. Neurol. 2, 698-701.
30. Langley-Evans, S. C., Philips, G. J., and Jackson, A. A. (1996). Sulphur dioxide: a potent glutathione depleting agent. Comp. Biochem. Physiol. 114, 89-98.
31. Leung, J. W. C., Chung, S. S. M., and Chung, S. K. (2009). Endothelial endothelin-1 over-expression using receptor tyrosine kinase tie-1 promoter leads to more severe vascular permeability and blood brain barrier breakdown after transient middle cerebral artery occlusion. Brain Res. 1266, 121-129.
32. 2 derivative-induced hippocampal neuronal injury. Ecotoxicol. Environ. Saf. 72, 236-241.
33. Lin, X. Q., Dai, Y. C., Zhu, G. C., and Wan, L. D. (2009). Changes of endothelin-1 expression in cerebral basilar arteries of scald rats. Burns 35, 98-103.
34. Lüscher, T. F., and Barton, M. (2000). Endothelins and endothelin receptor antagonists: therapeutic considerations for a novel class of cardiovascular drugs. Circulation 102, 2434-2440.
35. Macrae, I. M., Dawson, D. A., Norrie, J. D., and McCulloch, J. (1993). Inhibition of nitric oxide synthesis: effects on cerebral blood flow and glucose utilisation in the rat. J. Cereb. Blood Flow Metab. 13, 985-992.
36. Meng, Z. Q. (2003). Oxidative damage of sulfur dioxide on various organs of mice: sulfur dioxide is a systemic oxidative damage agent. Inhal. Toxicol. 5, 181-195.
37. Meng, Z. Q., Li, R. J., and Zhang, X. (2005). Levels of sulfite in three organs from mice exposed to sulfur dioxide. Inhal. Toxicol. 17, 309-313.
38. 2 derivatives on sodium currents in acutelyisolated rat hippocampalCA1 neurons. Acta Physiol. Sinica 54, 267-270.
39. Meng, Z. Q., and Zhang, B. (2001). Oxidation damage of sulfur dioxide inhalation on rat brain tissue cells. Acta Environ. Sci. 27, 464-546.
40. Meng, Z. Q., and Zhang, L. (1990). Chromosomal aberrations and sisterchromatid exchanges in lymphocytes of workers exposed to sulphur dioxide. Mutat. Res. 241, 15-20.
41. Nakayama, M., Uchimura, K., Zhu, R. L., Nagayama, T., Rose, M. E., Stetler, R. A., Isakson, P. C., Chen, J., and Graham, S. H. (1998). Cyclooxygenase-2 inhibition prevents delayed death of CA1 hippocampal neurons following global ischemia. Proc. Natl. Acad. Sci. U.S.A. 95, 10954-10959.
42. Nogawa, S., Forster, C., Zhang, F., Nagayama, M., Ross, M. E., and Iadecola, C. (1998). Interaction between inducible nitric oxide synthase and cyclooxygenase-2 after cerebral ischemia. Proc. Natl. Acad. Sci. U.S.A. 95, 10966-10971.
43. Oberdörster, G., Sharp, Z., Atudorei, V., Elder, A., Gelein, R., Kreyling, W., and Cox, C. (2004). Translocation of inhaled ultrafine particles to the brain. Inhal. Toxicol. 16, 437-445.
44. Paul, J., Villeneuve, L. C., Dave, S., and Brian, H. R. (2006). Associations between outdoor air pollution and emergency department visits for stroke in Edmonton, Canada. Eur. J. Epidemiol. 21, 689-700.
45. Pereyra-Muñoz, N., Rugerio-Vargas, C., Angoa-Pérez, M., Borgonio-Pérez, G., and Rivas-Arancibia, S. (2006). Oxidative damage in substantia nigra and striatum of rats chronically exposed to ozone. J. Chem. Neuroanat. 31, 114-123.
46. 2+ content and the expression of immediate earlygene in rat hippocampus. Acta Sci. Circumstantiae 28, 2315-2320.
47. Shapiro, R. (1977). Genetic effects of bisulfite (sulfur dioxide). Mutat. Res. 38, 149-176.
48. Stoll, G., Jander, S., and Schroeter, M. (1998). Inflammation and glial responses in ischemic brain lesions. Prog. Neurobiol. 56, 149-171.
49. Stratman, U., Lehman, R. R., Steinbech, T., and Wessling, G. (1991). Effect of sulfur dioxide inhalation on the respiratory tract of the rat. Zentralbl. Hyg. Umweltmed. 192, 324-335.
50. Sugimoto, K., and Iadecola, C. (2002). Effects of aminoguanidine on cerebral ischemia in mice: comparison between mice with and without inducible nitric oxide synthase gene. Neurosci. Lett. 331, 25-28.
51. Szyszkowicz, M. (2008). Ambient air pollution and daily emergency department visits for ischemic stroke in Edmonton, Canada. Int. J. Occup. Med. Environ. Health 21, 295-300.
52. Thomson, E. M., Kumarathasan, P., Garciduenas, L. C., and Vincent, R. (2007). Air pollution alters brain and pituitary endothelin-1 and inducible nitric oxide synthase gene expression. Environ. Res. 105, 224-233.
53. Tsujino, I., Kawakami, Y., and Kaneko, A. (2005). Comparative simulation of gas transport in airway models of rat, dog, and human. Inhal. Toxicol. 17, 475-485.
54. Ulrich, D., Costantino, I., and Michael, A. M. (1999). Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391-397.
55. Volpe, M., and Cosentino, F. (2000). Abnormalities of endothelial function in the pathogenesis of stroke: the importance of endothelin. J. Cardiovasc. Pharmacol. 35, S45-S48.
56. Weimar, C., Kurth, T., Kraywinkel, K., Wagner, M., and Busse, O. (2002). Assessment of functioning and disability after ischemic stroke. Stroke 33, 2053-2059.
57. Wellenius, G. A., Schwartz, J., and Mittleman, M. A. (2005). Air pollution and hospital admissions for ischemic and hemorrhagic stroke among Medicare beneficiaries. Stroke 36, 2549-2553.
58. World Health Organization. (1987). Air Quality Guidelines for Europe. WHO Regional Publications (European Series No. 23), W.H.O., Copenhagen, Denmark.
59. Wu, D. M., and Meng, Z. Q. (2003). Effect of sulfur dioxide inhalation on the glutathione redox system in mice and protective role of sea buckthorn seed oil. Arch. Environ. Contam. Toxicol. 45, 423-428.
60. Zhao, H., Xu, X., Na, J., Hao, L., Huang, L., Li, G., and Xu, Q. (2008). Protective effects of salicylic acid and vitamin C on sulfur dioxide-induced lipid peroxidation in mice. Inhal. Toxicol. 20, 865-871.
61. Zheng, Z., and Yenari, M. A. (2004). Post-ischemic inflammation: molecular mechanisms and therapeutic implications. Neurol. Res. 26, 884-892.
62. Zimmermann, M., and Seifert, V. (1998). Endothelin and subarachnoid hemorrhage: an overview. Neurosurgery 43, 863-876.