Diesel exhaust activates and primes microglia: Air pollution, neuroinflammation, and regulation of dopaminergic neurotoxicity

Environmental Health Perspectives

Volumn 119, Issue 8, 2011, Pages 1149-1155

  Levesque, Shannon ^a   Taetzsch, Thomas ^a   Lull, Melinda E ^a   Kodavanti, Urmila ^b   Stadler, Krisztian ^c   Wagner, Alison ^a   Johnson, Jo Anne ^d   Duke, Laura ^a   Kodavanti, Prasada ^b   Surace, Michael J ^a   Block, Michelle L ^a  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^c PENNINGTON BIOMEDICAL RESEARCH CENTER   (United States)

^d NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Air pollution; Brain; Microglia; Neuroinflammation; Oxidative stress; Parkinson's disease

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CALCIUM BINDING PROTEIN; CHEMOKINE; CYTOKINE; DOPAMINE; FRACTALKINE; HYDROGEN PEROXIDE; INTERLEUKIN 1BETA; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 1; NITRIC OXIDE; PROTEIN IBA 1; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

AIR POLLUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN REGION; CELL ACTIVATION; CELL IMMORTALIZATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENCEPHALITIS; EXHAUST GAS; GLIA; IN VITRO STUDY; LONG TERM EXPOSURE; MALE; MESENCEPHALON; MICROGLIA; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; RAT; REGULATORY MECHANISM; SUBSTANTIA NIGRA;

AIR POLLUTION; ANIMALS; CALCIUM-BINDING PROTEINS; CHEMOKINE CCL3; CHEMOKINE CX3CL1; DOPAMINERGIC NEURONS; HYDROGEN PEROXIDE; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; MICROFILAMENT PROTEINS; MICROGLIA; RATS; RATS, INBRED WKY; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA; VEHICLE EMISSIONS;

RATTUS;

EID: 79961033108     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1002986     Document Type: Article

References (45)

1. Antonini JM, Sriram K, Benkovic SA, Roberts JR, Stone S, Chen BT, et al. 2009. Mild steel welding fume causes manganese accumulation and subtle neuroinflammatory changes but not overt neuronal damage in discrete brain regions of rats after short-term inhalation exposure. Neurotoxicology 30(6):915-925.
2. Arimoto T, Kadiiska MB, Sato K, Corbett J, Mason RP. 2005. Synergistic production of lung free radicals by diesel exhaust particles and endotoxin. Am J Respir Crit Care Med 171(4):379-387.
3. Block ML, Calderon-Garciduenas L. 2009. Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci 32(9):506-516.
4. Block ML, Wu X, Pei Z, Li G, Wang T, Qin L, et al. 2004. Nanometer size diesel exhaust particles are selectively toxic to dopaminergic neurons: the role of microglia, phagocytosis, and NADPH oxidase. FASEB J 18(13):1618-1620.
5. Calderon-Garciduenas L, Mora-Tiscareno A, Ontiveros E, Gomez-Garza G, Barragan-Mejia G, Broadway J, et al. 2008a. Air pollution, cognitive deficits and brain abnormalities: a pilot study with children and dogs. Brain Cogn 68(2):117-127.
6. Calderon-Garciduenas L, Solt AC, Henriquez-Roldan C, Torres- Jardon R, Nuse B, Herritt L, et al. 2008b. Long-term air pollution exposure is associated with neuroinflammation, an altered innate immune response, disruption of the bloodbrain barrier, ultrafine particulate deposition, and accumulation of amyloid beta-42 and alpha-synuclein in children and young adults. Toxicol Pathol 36(2):289-310.
7. Cardona AE, Pioro EP, Sasse ME, Kostenko V, Cardona SM, Dijkstra IM, et al. 2006. Control of microglial neurotoxicity by the fractalkine receptor. Nat Neurosci 9(7):917-924.
8. Cheepsunthorn P, Radov L, Menzies S, Reid J, Connor JR. 2001. Characterization of a novel brain-derived microglial cell line isolated from neonatal rat brain. Glia 35(1):53-62.
9. Chen JC. 2010. Geographic determinants of stroke mortality: role of ambient air pollution. Stroke 41(5):839-841.
10. Choi J, Zheng Q, Katz HE, Guilarte TR. 2010. Silica-based nanoparticle uptake and cellular response by primary microglia. Environ Health Perspect 118:589-595.
11. Cruts B, van Etten L, Tornqvist H, Blomberg A, Sandstrom T, Mills NL, et al. 2008. Exposure to diesel exhaust induces changes in EEG in human volunteers. Part Fibre Toxicol 5:4; doi:10.1186/1743-8977-5-4 [Online 11 March 2008].
12. Dalfo E, Portero-Otin M, Ayala V, Martinez A, Pamplona R, Ferrer I. 2005. Evidence of oxidative stress in the neocortex in incidental Lewy body disease. J Neuropathol Exp Neurol 64(9):816-830.
13. Duan RS, Yang X, Chen ZG, Lu MO, Morris C, Winblad B, et al. 2008. Decreased fractalkine and increased IP-10 expression in aged brain of APP(swe) transgenic mice. Neurochem Res 33(6):1085-1089.
14. Fang F, Lue LF, Yan S, Xu H, Luddy JS, Chen D, et al. 2010. RAGE-dependent signaling in microglia contributes to neuroinflammation, Abeta accumulation, and impaired learning/memory in a mouse model of Alzheimer's disease. FASEB J 24(4):1043-1055.
15. Finkelstein M, Jerrett M. 2007. A study of the relationships between Parkinson's disease and markers of trafficderived environmental maganese air pollution in two Canadian cities. Environ Res 104(3):420-432.
16. Gerlofs-Nijland ME, van Berlo D, Cassee FR, Schins RP, Wang K, Campbell A. 2010. Effect of prolonged exposure to diesel engine exhaust on proinflammatory markers in different regions of the rat brain. Part Fibre Toxicol 7:12; doi:10.1186/1743-8977-7-12 [Online 17 May 2010].
17. Gottipolu RR, Wallenborn JG, Karoly ED, Schladweiler MC, Ledbetter AD, Krantz T, et al. 2009. One-month diesel exhaust inhalation produces hypertensive gene expression pattern in healthy rats. Environ Health Perspect 117:38-46.
18. Hartz AM, Bauer B, Block ML, Hong JS, Miller DS. 2008. Diesel exhaust particles induce oxidative stress, proinflammatory signaling, and P-glycoprotein up-regulation at the bloodbrain barrier. FASEB J 22(8):2723-2733.
19. Hawkes CH, Shephard BC, Daniel SE. 1997. Olfactory dysfunction in Parkinson's disease. J Neurol Neurosurg Psychiatry 62(5):436-446.
20. Hesterberg TW, Long CM, Lapin CA, Hamade AK, Valberg PA. 2010. Diesel exhaust particulate (DEP) and nanoparticle exposures: what do DEP human clinical studies tell us about potential human health hazards of nanoparticles? Inhal Toxicol 22(8):679-694.
21. Kim WG, Mohney RP, Wilson B, Jeohn GH, Liu B, Hong JS. 2000. Regional difference in susceptibility to lipopolysaccharide- induced neurotoxicity in the rat brain: role of microglia. J Neurosci 20(16):6309-6316.
22. Kovacs I, Torok I, Zombori J, Kasa P. 1998. Cholinergic structures and neuropathologic alterations in the olfactory bulb of Alzheimer's disease brain samples. Brain Res 789(1):167-170.
23. Kreyling WG, Semmler-Behnke M, Seitz J, Scymczak W, Wenk A, Mayer P, et al. 2009. Size dependence of the translocation of inhaled iridium and carbon nanoparticle aggregates from the lung of rats to the blood and secondary target organs. Inhal Toxicol 21(suppl 1):55-60.
24. Ling Z, Gayle DA, Ma SY, Lipton JW, Tong CW, Hong JS, et al. 2002. In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Mov Disord 17(1):116-124.
25. Ling Z, Zhu Y, Tong C, Snyder JA, Lipton JW, Carvey PM. 2006. Progressive dopamine neuron loss following supra-nigral lipopolysaccharide (LPS) infusion into rats exposed to LPS prenatally. Exp Neurol 199(2):499-512.
26. Ling Z, Zhu Y, Tong CW, Snyder JA, Lipton JW, Carvey PM. 2009. Prenatal lipopolysaccharide does not accelerate progressive dopamine neuron loss in the rat as a result of normal aging. Exp Neurol 216(2):312-320.
27. Liu B, Wang K, Gao HM, Mandavilli B, Wang JY, Hong JS. 2001. Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J Neurochem 77(1):182-189.
28. Ma JY, Ma JK. 2002. The dual effect of the particulate and organic components of diesel exhaust particles on the alteration of pulmonary immune/inflammatory responses and metabolic enzymes. J Environ Sci Health Part C Environ Carcinog Ecotoxicol Rev 20(2):117-147.
29. Oberdorster G, Sharp Z, Atudorei V, Elder A, Gelein R, Kreyling W, et al. 2004. Translocation of inhaled ultrafine particles to the brain. Inhal Toxicol 16(6-7):437-445.
30. Perry VH, Nicoll JA, Holmes C. 2010. Microglia in neurodegenerative disease. Nat Rev Neurol 6(4):193-201.
31. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, et al. 2004. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and proinflammatory gene expression in activated microglia. J Biol Chem 279(2):1415-1421.
32. Qin L, Wu X, Block ML, Liu Y, Breese GR, Hong JS, et al. 2007. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55(5):453-462.
33. Re DB, Przedborski S. 2006. Fractalkine: moving from chemotaxis to neuroprotection. Nat Neurosci 9(7):859-861.
34. Sriram K, Lin GX, Jefferson AM, Roberts JR, Wirth O, Hayashi Y, et al. 2010. Mitochondrial dysfunction and loss of Parkinson's disease-linked proteins contribute to neurotoxicity of manganese-containing welding fumes. FASEB J 24(12):4989-5002.
35. Stevens T, Krantz QT, Linak WP, Hester S, Gilmour MI. 2008. Increased transcription of immune and metabolic pathways in naive and allergic mice exposed to diesel exhaust. Toxicol Sci 102(2):359-370.
36. Suzuki T, Oshio S, Iwata M, Saburi H, Odagiri T, Udagawa T, et al. 2010. In utero exposure to a low concentration of diesel exhaust affects spontaneous locomotor activity and monoaminergic system in male mice. Part Fibre Toxicol 7:7; doi:10.1186/1743-8977-7-7 [Online 23 March 2010].
37. Tsukue N, Watanabe M, Kumamoto T, Takano H, Takeda K. 2009. Perinatal exposure to diesel exhaust affects gene expression in mouse cerebrum. Arch Toxicol 83(11):985-1000.
38. Valavanidis A, Fiotakis K, Vlachogianni T. 2008. Airborne particulate matter and human health: toxicological assessment and importance of size and composition of particles for oxidative damage and carcinogenic mechanisms. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 26(4):339-362.
39. van Berlo D, Albrecht C, Knaapen AM, Cassee FR, Gerlofs- Nijland ME, Kooter IM, et al. 2010. Comparative evaluation of the effects of short-term inhalation exposure to diesel engine exhaust on rat lung and brain. Arch Toxicol 84(7):553-562.
40. Verina T, Kiihl SF, Schneider JS, Guilarte TR. 2011. Manganese exposure induces microglia activation and dystrophy in the substantia nigra of non-human primates. Neurotoxicology 32(2):215-226.
41. Wang J, Liu Y, Jiao F, Lao F, Li W, Gu Y, et al. 2008. Timedependent translocation and potential impairment on central nervous system by intranasally instilled TiO(2) nanoparticles. Toxicology 254(1-2):82-90.
42. Wang S, Yan JY, Lo YK, Carvey PM, Ling Z. 2009. Dopaminergic and serotoninergic deficiencies in young adult rats prenatally exposed to the bacterial lipopolysaccharide. Brain Res 1265:196-204.
43. Werner E. 2003. Determination of cellular H2O2 production. Sci STKE 2003(168):PL3; doi:10.1126/stke.2003.168.pl3 [Online 4 February 2003].
44. Wynne AM, Henry CJ, Huang Y, Cleland A, Godbout JP. 2010. Protracted downregulation of CX3CR1 on microglia of aged mice after lipopolysaccharide challenge. Brain Behav Immun 24(7):1190-1201.
45. Yokota S, Mizuo K, Moriya N, Oshio S, Sugawara I, Takeda K. 2009. Effect of prenatal exposure to diesel exhaust on dopaminergic system in mice. Neurosci Lett 449(1):38-41.