Exposure to inhaled particulate matter activates early markers of oxidative stress, inflammation and unfolded protein response in rat striatum

Toxicology Letters

Volumn 222, Issue 2, 2013, Pages 146-154

  Guerra, R ^a   Vera Aguilar, E ^a   Uribe Ramirez, M ^a   Gookin, G ^b   Camacho, J ^a   Osornio Vargas, A R ^c   Mugica Alvarez, V ^d   Angulo Olais, R ^d   Campbell, A ^e   Froines, J ^f   Kleinman, T M ^b   De Vizcaya Ruiz, A ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ALBERTA   (Canada)

^d UNIVERSIDAD AUTÓNOMA METROPOLITANA AZCAPOTZALCO   (Mexico)

^e WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Central nervous system; Inflammation; Oxidative stress; Particulate matter; Striatum; Unfolded protein response

Indexed keywords

CASPASE 3; I KAPPA B; INTERLEUKIN 1BETA; TRANSCRIPTION FACTOR NRF2; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; FRONTAL CORTEX; GEL MOBILITY SHIFT ASSAY; HIPPOCAMPUS; MALE; NONHUMAN; OLFACTORY BULB; OXIDATIVE STRESS; PARTICULATE MATTER; PRIORITY JOURNAL; RAT; UNFOLDED PROTEIN RESPONSE;

ACTIVATING TRANSCRIPTION FACTOR 6; ATF6; BIP; CENTRAL NERVOUS SYSTEM; EUKARYOTIC TRANSLATION INITIATION FACTOR 2-ALPHA KINASE 3; GEL SHIFT MOBILITY ASSAY; GSMA; HEAT SHOCK 70KDA PROTEIN 5 (GLUCOSE-REGULATED PROTEIN, 78KDA); HEME OXYGENASE 1; HO-1; IL-1Β; INFLAMMATION; INOSITOL-REQUIRING PROTEIN 1; INTERLEUKIN 1 BETA; IRE1Α; NF-ΚB; NRF-2; NUCLEAR FACTOR (ERYTHROID-DERIVED 2)-LIKE 2; NUCLEAR FACTOR KAPPA-LIGHT-CHAIN-ENHANCER OF ACTIVATED B CELLS; OXIDATIVE STRESS; PAHS; PARTICULATE MATTER; PERK; PM; POLYCYCLIC AROMATIC HYDROCARBONS; SOD; STRIATUM; SUPEROXIDE DISMUTASE; TNFΑ; TUMOR NECROSIS FACTOR-ALPHA; UNFOLDED PROTEIN RESPONSE; UPR; VACES; VERSATILE AEROSOL CONCENTRATOR SYSTEM; X-BOX BINDING PROTEIN 1; XBP-1; XBP-1 SPLICED FORM; XBP-1 UNSPLICED FORM; XBP-1S; XBP-1U;

AIR POLLUTANTS; ANIMALS; BIOLOGICAL MARKERS; CENTRAL NERVOUS SYSTEM AGENTS; CORPUS STRIATUM; DNA-BINDING PROTEINS; HEAT-SHOCK PROTEINS; HEME OXYGENASE (DECYCLIZING); MALE; MEXICO; NERVE TISSUE PROTEINS; NEURONS; OXIDATIVE STRESS; PARTICLE SIZE; PARTICULATE MATTER; RATS; RATS, SPRAGUE-DAWLEY; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS; UNFOLDED PROTEIN RESPONSE; UP-REGULATION;

EID: 84882750149     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.07.012     Document Type: Article

References (48)

1. Abbott A. Dementia: a problem for our age. Nature 2011, 475:S2-S4.
2. Araujo S.A. Particulate air pollution, systemic oxidative stress, inflammation, and atherosclerosis. Air Quality, Atmosphere and Health 2011, 4:79-93.
3. Bandopadhyay R., de Belleroche J. Pathogenesis of Parkinson's disease: emerging role of molecular chaperones. Trends in Molecular Medicine 2010, 16:27-36.
4. Block M.L., Calderon-Garciduenas L. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends in Neuroscience 2009, 32:506-516.
5. Block M.L., Wu X., Pei Z., Li G., Wang T., Qin L., Wilson B., Yang J., Hong J.S., Veronesi B. Nanometer size diesel exhaust particles are selectively toxic to dopaminergic neurons: the role of microglia, phagocytosis, and NADPH oxidase. FASEB Journal 2004, 18:1618-1620.
6. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 1976, 72:248-254.
7. Calderon-Garciduenas L., Reed W., Maronpot R.R., Henriquez-Roldan C., Delgado-Chavez R., Calderon-Garciduenas A., Dragustinovis I., Franco-Lira M., Aragon-Flores M., Solt A.C., Altenburg M., Torres-Jardon R., Swenberg J.A. Brain inflammation and Alzheimer's-like pathology in individuals exposed to severe air pollution. Toxicologic Pathology 2004, 32:650-658.
8. Calderon-Garciduenas L., Solt A.C., Henriquez-Roldan C., Torres-Jardon R., Nuse B., Herritt L., Villarreal-Calderon R., Osnaya N., Stone I., Garcia R., Brooks D.M., Gonzalez-Maciel A., Reynoso-Robles R., Delgado-Chavez R., Reed W. Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the blood-brain barrier, ultrafine particulate deposition, and accumulation of amyloid beta-42 and alpha-synuclein in children and young adults. Toxicologic Pathology 2008, 36:289-310.
9. Campbell A., Oldham M., Becaria A., Bondy S.C., Meacher D., Sioutas C., Misra C., Mendez L.B., Kleinman M. Particulate matter in polluted air may increase biomarkers of inflammation in mouse brain. Neurotoxicology 2005, 26:133-140.
10. De Vizcaya-Ruiz A., Gutiérrez-Castillo M.E., Uribe-Ramirez M., Cebrián M.E., Mugica-Alvarez V., Sepúlveda J., Rosas I., Salinas E., Garcia-Cuéllar C., Martínez F., Alfaro-Moreno E., Torres-Flores V., Osornio-Vargas A., Sioutas C., Fine P.M., Singh M., Geller M.D., Kuhn T., Miguel A.H., Eiguren-Fernandez A., Schiestl R.H., Reliene R., Froines J. Characterization and in vitro biological effects of concentrated particulate matter from Mexico city. Atmospheric Environment 2006, 40:583-592.
11. Dorman D.C., Struve M.F., Wong B.A. Brain manganese concentrations in rats following manganese tetroxide inhalation are unaffected by dietary manganese intake. Neurotoxicology 2002, 23:185-195.
12. Dosunmu R., Wu J., Basha M.R., Zawia N.H. Environmental and dietary risk factors in Alzheimer's disease. Expert Review of Neurotherapeutics 2007, 7:887-900.
13. Elder A., Gelein R., Silva V., Feikert T., Opanashuk L., Carter J., Potter R., Maynard A., Ito Y., Finkelstein J., Oberdörster G. Translocation of inhaled ultrafine manganese oxide particles to the central nervous system. Environmental Health Perspectives 2006, 114:1172-1178.
14. Ferrer I. Altered mitochondria, energy metabolism, voltage-dependent anion channel, and lipid rafts converge to exhaust neurons in Alzheimer's disease. Journal of Bioenergetics and Biomembranes 2009, 41:425-431.
15. Foster W.M., Costa D.L. Air Pollutants and the Respiratory Tract 2005, Taylor & Francis, Boca Raton, FL.
16. Gerlofs-Nijland M.E., van Berlo D., Cassee F.R., Schins R.P., Wang K., Campbell A. Effect of prolonged exposure to diesel engine exhaust on proinflammatory markers in different regions of the rat brain. Particle and Fibre Toxicology 2010, 7:12.
17. Ghosh N., Ghosh R., Mandal S.C. Antioxidant protection: a promising therapeutic intervention in neurodegenerative disease. Free Radical Research 2011, 45:888-905.
18. Haines D.E. Neuroanatomy: An Atlas of Structures, Sections, and Systems 2012, Wolters Kluwer Health/Lippincott Williams & Wilkins, Philadelphia, pp. xi, 332p.
19. Johnson A., van der Meer M.A.A., Redish A.D. Integrating hippocampus and striatum in decision-making. Current Opinion in Neurobiology 2007, 17:692-697.
20. Katsouyanni K., Touloumi G., Spix C., Schwartz J., Balducci F., Medina S., Rossi G., Wojtyniak B., Sunyer J., Bacharova L., Schouten J.P., Ponka A., Anderson H.R. Short-term effects of ambient sulphur dioxide and particulate matter on mortality in 12 European cities: results from time series data from the APHEA project. Air Pollution and Health: a European Approach. British Medical Journal 1997, 314:1658-1663.
21. Kaufman R.J. Orchestrating the unfolded protein response in health and disease. Journal of Clinical Investigation 2002, 110:1389-1398.
22. Kim S., Jaques P.A., Chang M., Barone T., Xiong C., Friedlander S.K., Sioutas C. Versatile aerosol concentration enrichment system (VACES) for simultaneous in vivo and in vitro evaluation of toxic effects of ultrafine, fine and coarse ambient particles: part II. Field evaluation. Journal of Aerosol Science 2001, 32:1299-1314.
23. Kim S., Jaques P.A., Chang M., Froines J.R., Sioutas C. Versatile aerosol concentration enrichment system (VACES) for simultaneous in vivo and in vitro evaluation of toxic effects of ultrafine, fine and coarse ambient particles: part I. Development and laboratory characterization. Journal of Aerosol Science 2001, 32:1281-1297.
24. Kleinman M.T., Araujo J.A., Nel A., Sioutas C., Campbell A., Cong P.Q., Li H., Bondy S.C. Inhaled ultrafine particulate matter affects CNS inflammatory processes and may act via MAP kinase signaling pathways. Toxicology Letters 2008, 178:127-130.
25. Kleinman M.T., Hamade A., Meacher D., Oldham M., Sioutas C., Chakrabarti B., Stram D., Froines J.R., Cho A.K. Inhalation of concentrated ambient particulate matter near a heavily trafficked road stimulates antigen-induced airway responses in mice. Journal of the Air & Waste Management Association 2005, 55:1277-1288.
26. Kooter I.M., Boere A.J., Fokkens P.H., Leseman D.L., Dormans J.A., Cassee F.R. Response of spontaneously hypertensive rats to inhalation of fine and ultrafine particles from traffic: experimental controlled study. Particle and Fibre Toxicology 2006, 3:7.
27. Landrigan P.J., Sonawane B., Butler R.N., Trasande L., Callan R., Droller D. Early environmental origins of neurodegenerative disease in later life. Environmental Health Perspectives 2005, 113:1230-1233.
28. Li N., Sioutas C., Cho A., Schmitz D., Misra C., Sempf J., Wang M., Oberley T., Froines J., Nel A. Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environmental Health Perspectives 2003, 111:455-460.
29. Li N., Alam J., Venkatesan M.I., Eiguren-Fernandez A., Schmitz D., Di Stefano E., Slaughter N., Killeen E., Wang X., Huang A., Wang M., Miguel A.H., Cho A., Sioutas C., Nel A.E. Nrf2 is a key transcription factor that regulates antioxidant defense in macrophages and epithelial cells: protecting against the proinflammatory and oxidizing effects of diesel exhaust chemicals. Journal of Immunology 2004, 173:3467-3481.
30. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, CA) 2001, 25:402-408.
31. Malhotra J.D., Kaufman R.J. The endoplasmic reticulum and the unfolded protein response. Seminars in Cell & Developmental Biology 2007, 18:716-731.
32. Martínez A., Portero-Otin M., Pamplona R., Ferrer I. Protein targets of oxidative damage in human neurodegenerative diseases with abnormal protein aggregates. Brain Pathology 2010, 20:281-297.
33. Mautz W.J., Kleinman M.T. Animal quality and protocol approval. Methods in Inhalation Toxicology 1997, 1616. CRC Press, Boca Raton, FL. R.F. Phalen (Ed.).
34. Mazzoli-Rocha F., Fernandes S., Einicker-Lamas M., Araújo Zin W. Roles of oxidative stress in signaling and inflammation induced by particulate matter. Cell Biology and Toxicology 2010, 26:481-498.
35. Migliore L., Coppedè F. Environmental-induced oxidative stress in neurodegenerative disorders and aging. Mutation Research 2009, 674:73-84.
36. Mugica V., Ortiz E., Molina L., De Vizcaya-Ruiz A., Nebot A., Quintana R., Aguilar J., Alcántara E. PM composition and source reconciliation in Mexico city. Atmospheric Environment 2009, 43:5068-5074.
37. Oberdorster G., Sharp Z., Atudorei V., Elder A., Gelein R., Lunts A., Kreyling W., Cox C. Extrapulmonary translocation of ultrafine carbon particles following whole-body inhalation exposure of rats. Journal of Toxicology and Environmental Health, Part A 2002, 65:1531-1543.
38. Oberdorster G., Sharp Z., Atudorei V., Elder A., Gelein R., Kreyling W., Cox C. Translocation of inhaled ultrafine particles to the brain. Inhalation Toxicology 2004, 16:437-445.
39. Pope C.A. Epidemiology of fine particulate air pollution and human health: biologic mechanisms and who's at risk?. Environmental Health Perspectives 2000, 108(Suppl. 4):713-723.
40. Pope C.A., Dockery D.W. Health effects of fine particulate air pollution: lines that connect. Journal of the Air & Waste Management Association 2006, 56:709-742.
41. Ranft U., Schikowski T., Sugiri D., Krutmann J., Krämer U. Long-term exposure to traffic-related particulate matter impairs cognitive function in the elderly. Environmental Research 2009, 109:1004-1011.
42. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nature Reviews Molecular Cell Biology 2007, 8:519-529.
43. Schroder M., Kaufman R.J. The mammalian unfolded protein response. Annual Review of Biochemistry 2005, 74:739-789.
44. Tjälve H., Henriksson J. Uptake of metals in the brain via olfactory pathways. Neurotoxicology 1999, 20:181-195.
45. USEPA 1999. Compendium of Methods for the determination of toxic organic compounds in ambient air. Compendium Method TO-13A. United States Environmental Protection Agency EPA-625/R-96-010b.
46. Valko M., Morris H., Cronin M.T. Metals, toxicity and oxidative stress. Current Medicinal Chemistry 2005, 12:1161-1208.
47. 2.5 collected in northern Mexico city. Science of the Total Environment 2010, 408:5429-5438.
48. Zhang K., Kaufman R.J. From endoplasmic-reticulum stress to the inflammatory response. Nature 2008, 454:455-462.