Exposure to ozone induces a systemic inflammatory response: Possible source of the neurological alterations induced by this gas

Inhalation Toxicology

Volumn 26, Issue 8, 2014, Pages 485-491

  González Guevara, Edith ^a,b   Martínez Lazcano, Juan Carlos ^a   Custodio, Verónica ^a   Hernández Cerón, Miguel ^a   Rubio, Carmen ^a   Paz, Carlos ^a  

^a NATIONAL INSTITUTE OF NEUROLOGY AND NEUROSURGERY   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Brain; Cytokines; GFAP; Inflammation; NF B; Ozone

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; OZONE; TUMOR NECROSIS FACTOR ALPHA; AIR POLLUTANT; OXIDIZING AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENVIRONMENTAL EXPOSURE; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOHISTOCHEMISTRY; MALE; NERVOUS SYSTEM INFLAMMATION; NEUROLOGIC DISEASE; NONHUMAN; PNEUMONIA; PRIORITY JOURNAL; RAT; AIR POLLUTANT; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; INFLAMMATION; LUNG; METABOLISM; TOXICITY; WISTAR RAT;

AIR POLLUTANTS; ANIMALS; CEREBRAL CORTEX; GLIAL FIBRILLARY ACIDIC PROTEIN; INFLAMMATION; INTERLEUKIN-6; LUNG; MALE; NF-KAPPA B; OXIDANTS; OZONE; RATS, WISTAR; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84904001629     PISSN: 08958378     EISSN: 10917691     Source Type: Journal    
DOI: 10.3109/08958378.2014.922648     Document Type: Article

References (54)

1. Aris RM, Christian D, Hearne PQ, et al. (1993). Ozone-induced airway inflammation in human subjects as determined by airway lavage and biopsy. Am Rev Respir Dis 148:1363-72.
2. Arito H, Uchiyama I, Yokoyama E. (1992). Acute effects of ozone on EEG activity, sleep-wakefulness and heart rate in rats. Ind Health 30: 23-34.
3. Arsalane K, Gosset P, Vanhee D, et al. (1995). Ozone stimulates synthesis of inflammatory cytokines by alveolar macrophages in vitro. Am J Respir Cell Mol Biol 13:60-8.
4. Avila-Costa MR, Col?́n-Barenque L, Fortoul TI, et al. (1999). Memory deterioration in an oxidative stress model and its correlation with cytological changes on rat hippocampus CA1. Neurosci Lett 270: 107-9.
5. Banks WA. (2005). Blood-brain barrier transport of cytokines: a mechanism for neuropathology. Curr Pharm Des 11:973-84. (Pubitemid 40331299)
6. Cho HY, Liu-Yi Z, Kleeberger SR. (2001). Ozone-induced lung inflammation and hyperreactivity are mediated via tumor necrosis factor-a receptors. Am J Physiol Lung Cell Mol Physiol 280:L537-46.
7. Cho HY, Morgan DL, Bauer AK, Kleeberger SR. (2007). Signal transduction pathways of tumor necrosis factor-mediated lung injury induced by ozone in mice. Am J Respir Crit Care Med 175:829-39. (Pubitemid 46631795)
8. Cottet-Emard JM, Dalmaz Y, Pequignot J, et al. (1997). Long-term exposure to ozone alters peripheral and central catecholamine activity in rats. Pflügers Arch-Eur J Physiol 433:744-9. (Pubitemid 27140498)
9. Craig L, Brook JR, Chiotti Q, et al. (2008). Air pollution and public heatlh: a guidance document for risk managers. J Toxicol Environ Health A 71:588-698. (Pubitemid 351998829)
10. Custodio V, González E, Rubio C, Paz C. (2010). Brain noradrenaline changes in rats prenatally exposed to ozone. Environ Toxicol Pharmacol 30:91-4.
11. Dales RE, Cakmak S, Blanco-Vidal C. (2009). Air pollution and hospitalization for headache in Chile. Am J Epidemiol 170:1057-66.
12. Dantzer R, Kelley KW. (2007). Twenty years of research on cytokineinduced sickness behavior. Brain Behav Immun 21:153-60. (Pubitemid 46038917)
13. Devlin RB, McDonnel WF, Becker S, et al. (1996). Time-dependent changes of inflammatory mediators in the lungs of humans exposed to 0.4 ppm ozone for 2 hr: a comparison of mediators found in bronchoalveolar lavage fluid 1 and 18 hr efter exposure. Toxicol Appl Pharmacol 138:176-85.
14. Dorado-Mart́nez C, Paredes-Carbajal C, Mascher D, et al. (2001). Effects of different ozone doses on memory, motor activity and lipid peroxidation levels in rats. Int J Neurosci 108, 149-61.
15. Genc S, Zadeoglulari Z, Fuss SH, Genc K. (2012). The adverse effects of air pollution on the nervous system. J Toxicol 2012:782462. doi: 10.1155/2012/782462.
16. Gonzalez-Piña R, Paz C. (1997). Brain monoamine changes in rats after short periods of ozone exposure. Neurochem Res 22:63-6. (Pubitemid 27081993)
17. Graham JA, Menzel DB, Miller FJ, et al. (1981). Influence of ozone on pentobarbital-induced sleeping time in mice, rats, and hamsters. Toxicol Appl Pharmacol 61:64-73. (Pubitemid 11029904)
18. Haddad EB, Salmon M, Koto H, et al. (1996). Ozone induction of cytokine-induced neutrophil chemoattractant (CINC) and nuclear factor-kappa b in rat lung: inhibition by corticosteroids. FEBS Lett 379:265-8. (Pubitemid 26049453)
19. Harkema JR, Wanger JG. (2005). Epithelial and inflammatory responses in the airways of laboratory rats coexposed to ozone and biogenic substances: enhancement of toxicant-induced airway injury. Exp Toxicol Pathol 57:129-41. (Pubitemid 40884485)
20. Haro R, Paz C. (1993). Effects of ozone exposure during pregnancy on ontogeny of sleep in rats. Neurosci Lett 164:67-70. (Pubitemid 24040683)
21. Hatch GE, Slade R, Harris LP, et al. (1994). Ozone dose and effect in humans and rats. A comparison using oxygen-18 labelling and bronchoalveolar lavage. Am J Respir Crit Care Med 150:676-83. (Pubitemid 24291494)
22. Huitrón-Reséndiz S, Custodio-Ram?́rez V, Escalante-Membrillo C, et al. (1994). Sleep alterations and brain regional changes of serotonin and its metabolite in rats exposed to ozone. Neurosci Lett 177:119-22.
23. Ibrahim AD, Birmingham NP, Lewandowski R, et al. (2010). Acute exposure to ozone exacerbates acetaminophen-induced liver injury in mice. Toxicol Sci 115:267-85.
24. Kari F, Hatch G, Slade R, et al. (1997). Dietary restriction mitigates ozone-induced lung inflammation in rats: a role for endogenous antioxidants. Am J Respir Cell Mol Biol 17:740-7. (Pubitemid 127348665)
25. Kavlock RJ, Datson G, Grabowski CT. (1979). Studies on the developmental toxicity of ozone: I. prenatal effects. Toxicol Appl Pharmacol 48:19-28. (Pubitemid 9189408)
26. Kavlock RJ, Meyer E, Grabowski CT. (1980). Studies in the developmental toxicity of ozone: postnatal effects. Toxicol Lett 5:3-9. (Pubitemid 10170965)
27. Krueger JM. (2009). The role of cytokines in sleep regulation. Curr Pharm Des 14:3408-16.
28. Manzer R, Dinarello CA, McConville G, Mason RJ. (2008). Ozone exposure of macrophages induces an alveolar epithelial chemokine response through IL-1{alpha}. Am J Respir Cell Mol Biol 38:318-23. (Pubitemid 351567701)
29. Mart́nez-Lazcano JC, González-Guevara E, Rubio MC, et al. (2013). The effects of ozone exposure and associated injury mechanisms on the central nervous system. Rev Neurosci 24, 337-52.
30. Medzhitov R. (2008). Origin and physiological roles of inflammation. Nature 454:428-35.
31. Mills NL, Donaldson K, Hadoke PW, et al. (2009). Adverse cardiovascular effects of air pollution. Nat Clin Pract Cardiovasc Med 6:36-44.
32. Narayan KM, Ali MK, Koplan JP. (2010). Global noncommunicable diseases-where worlds meet. N Engl J Med 363:1196-8.
33. Nichols BG, Woods JS, Luchtel DL, et al. (2001). Effects of ozone exposure on nuclear factor-kappaB activation and tumor necrosis factor-alpha expression in human nasal epithelial cells. Toxicol Sci 60: 356-62. (Pubitemid 32273325)
34. Okada S, Nakamura M, Katoh H, et al. (2006). Conditional ablation of Stat3 or Socs3 discloses a dual role for reactive astrocytes after spinal cord injury. Nat Med 12:829-34. (Pubitemid 44050074)
35. Pahl HL. (1999). Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene 18:6853-66.
36. Paz C, Bazán-Perkins B. (1992). Sleep-wake disorganization in cats exposed to ozone. Neurosci Lett 140:270-2.
37. Paz C, Huitrón-Reséndiz S. (1996). The effects of ozone exposure on the sleep-wake cycle and serotonin contents in the pons of the rat. Neurosci Lett 204:49-52. (Pubitemid 26053673)
38. Pryor WA, Squadrito GL, Friedman MA. (1995a). The cascade mechanism to explain ozone toxicity: the role of lipid ozonation products. Free Radic Biol Med 19:935-41.
39. Pryor WA, Squadrito GL, Friedman M. (1995b). A new mechanism for the toxicity of ozone. Toxicology Lett 82:287-93. (Pubitemid 26054715)
40. Rivas-Arancibia S, Dorado-Mart?́nez C, Colin-Barenque L, et al. (2003). Effect of acute ozone exposure on locomotor behavior and striatal function. Pharmacol Biochem Behav 74:891-900.
41. Rivas-Manzano P, Paz C. (1999). Cerebella morphological alterations in rats induced by prenatal ozone exposure. Neurosci Lett 276:37-40. (Pubitemid 29525519)
42. Rubio C, Paz C. (2003). Indomethacin reverts sleep disorders produced by ozone exposure in rats. Toxicology 191:89-96. (Pubitemid 37329456)
43. Slade R, Crissman K, Norwood J, Hatch G. (1993). Comparison of antioxidant substances in bronchoalveolar lavage cells and fluid from humans, guinea pigs, and rats. Exp Lung Res 19:469-84. (Pubitemid 23212956)
44. Song H, Tan W, Zhang X. (2011). Ozone induces inflammation in bronchial epithelial cells. J Asthma 48:79-83.
45. Sorace A, De Acetis L, Alleva E, Santucci D. (2001). Prolonged exposure to low doses of ozone: short-and long-term changes in behavioral performance in mice. Environ Res A 85: 122-34.
46. Stein B, Coswell PC, Baldwin AS. (1993). Functional and physical associations between NF-kB and C/EBP family members: a Rel domain-bZIP interaction. Mol Cell Biol 13:3964-74. (Pubitemid 23187624)
47. Sticozzi C, Belmonte G, Meine A, et al. (2013). IL-1b induces GFAP expression in vitro and in vivo and protects neurons from traumatic injury-associated apoptosis in rat brain striatum via NFkB/Ca2+calmodulin/ERK mitogen-activated protein kinase signaling pathway. Neuroscience 252:367-83.
48. Takahashi S, Kapás L, Fang J, et al. (1996). An interleukin-1 receptor fragment inhibits spontaneous sleep and muramyl dipeptide-induced sleep in rabbits. Am J Physiol Regul Integr Comp Physiol 271: R101-8.
49. Tanabe K, Matsushima N, Yamaguchi S, et al. (2010). Mechanisms of tumor necrosis factor-alpha-induced interleukin-6 synthesis in glioma cells. J Neuroinflammation 7:16-24.
50. Tarrant JM. (2010). Blood cytokines as biomarkers of in vivo toxicity in preclinical safety assessment: considerations for their use. Toxicol Sci 117:4-16.
51. Tepper JL, Weiss B, Cox C. (1982). Microanalysis of ozone depression of motor activity. Toxicol Appl Pharmacol 64:317-26. (Pubitemid 12097156)
52. Winquist A, Klein M, Tolbert P, et al. (2012). Comparison of emergency department and hospital admissions data for air pollution time-series studies. Environ Health 11:70-83.
53. World Health Organization. (2005). WHO Air quality guidelines for particulate matter, ozone, nitrogen dioxide and sulfur dioxide. Global update 2005. Summary of risk assessment. Available at: http://whqlibdoc.who.int/hq/ 2006/WHO-SDE-PHE-OEH-06.02-eng.pdf. [Last accessed: 10 Apr 2014].
54. Yamaguchi S, Tanabe K, Takai S, et al. (2009). Involvement of Rhokinase in tumor necrosis factor-alpha-induced interleukin-6 release from C6 glioma cells. Neurochem Int 55:438-45.