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DNA Damage in Nasal and Brain Tissues of Canines Exposed to Air Pollutants Is Associated with Evidence of Chronic Brain Inflammation and Neurodegeneration

Lilian Calderon-Garciduenas

Environmental Pathology Program, University of North Carolina at Chapel Hill, North Carolina 27599-7310, USA, liliancalderon888{at}hotmail.com, Instituto Nacional de Pediatría, Mexico City 14410, Mexico

Robert R. Maronpot

National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, USA

Ricardo Torres-Jardon

Centro de Ciencias de la Atmósfera, Universidad Nacional Autónoma de México, Mexico City

Carlos Henriquez-Roldan

Departamento de Estadística, Universidad de Valparaíso, Chile

Robert Schoonhoven

Department of Environmental Sciences and Engineering, University of North Carolina at Chapel Hill, North Carolina 27599-7310, USA

Hilda Acuna-Ayala

Instituto Nacional de Pediatría, Mexico City 14410, Mexico

Anna Villarreal-Calderon

Facultad de Medicina, NUCE, Universidad Nacional Autónoma de México, Mexico

Jun Nakamura

Department of Environmental Sciences and Engineering, University of North Carolina at Chapel Hill, North Carolina 27599-7310, USA

Reshan Fernando

RTI International, Research Triangle Park, North Carolina 27709, USA

William Reed

Department of Pediatrics and Center for Environmental Medicine, Asthma, and Lung Biology, University of North Carolina at Chapel Hill 27599-7310, USA

Biagio Azzarelli

Pathology Department, Indiana University, Indianapolis, Indiana 46202-5120, USA

James A. Swenberg

Department of Environmental Sciences and Engineering, University of North Carolina at Chapel Hill, North Carolina 27599-7310, USA

Acute, subchronic, or chronic exposures to particulate matter (PM) and pollutant gases affect people in urban areas and those exposed to fires, disasters, and wars. Respiratory tract inflammation, production of mediators of inflammation capable of reaching the brain, systemic circulation of PM, and disruption of the nasal respiratory and olfactory barriers are likely in these populations. DNA damage is crucial in aging and in age-associated diseases such as Alzheimer's disease. We evaluated apurinic/apyrimidinic (AP) sites in nasal and brain genomic DNA, and explored by immunohistochemistry the expression of nuclear factor NF{kappa}B p65, inducible nitric oxide synthase (iNOS), cyclo-oxygenase 2 (COX2), metallothionein I and II, apolipoprotein E, amyloid precursor protein (APP), and beta-amyloid1-42 in healthy dogs naturally exposed to urban pollution in Mexico City. Nickel (Ni) and vanadium (V) were measured by inductively coupled plasma mass spectrometry (ICP-MS). Forty mongrel dogs, ages 7 days—10 years were studied (14 controls from Tlaxcala and 26 exposed to urban pollution in South West Metropolitan Mexico City (SWMMC)). Nasal respiratory and olfactory epithelium were found to be early pollutant targets. Olfactory bulb and hippocampal AP sites were significantly higher in exposed than in control age matched animals. Ni and V were present in a gradient from olfactory mucosa > olfactory bulb > frontal cortex. Exposed dogs had (a) nuclear neuronal NF{kappa}B p65, (b) endothelial, glial and neuronal iNOS, (c) endothelial and glial COX2, (d) ApoE in neuronal, glial and vascular cells, and (e) APP and β amyloid1-42 in neurons, diffuse plaques (the earliest at age 11 months), and in subarachnoid blood vessels. Increased AP sites and the inflammatory and stress protein brain responses were early and significant in dogs exposed to urban pollution. Oil combustion PM-associated metals Ni and V were detected in the brain. There was an acceleration of Alzheimer's-type pathology in dogs chronically exposed to air pollutants. Respiratory tract inflammation and deteriorating olfactory and respiratory barriers may play a role in the observed neuropathology. These data suggest that Alzheimer's disease may be the sequela of air pollutant exposures and the resulting systemic inflammation.

Key Words: Urban pollution • Alzheimer's disease • ozone • ultrafine particulate matter • brain inflammation • combustion metals • nasal and olfactory pathology • blood—brain barrier • DNA oxidative damage.

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Toxicologic Pathology, Vol. 31, No. 5, 524-538 (2003)
DOI: 10.1080/01926230390226645
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