Prenatal Exposure to Urban Air Nanoparticles in Mice Causes Altered Neuronal Differentiation and Depression-Like Responses

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Davis, David A ^a   Bortolato, Marco ^e   Godar, Sean C ^b   Sander, Thomas K ^a   Iwata, Nahoko ^a   Pakbin, Payam ^c   Shih, Jean C ^b   Berhane, Kiros ^d   McConnell, Rob ^d   Sioutas, Constantinos ^c   Finch, Caleb E ^a   Morgan, Todd E ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c NONE   (United States)

^d UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^e UNIVERSITY OF KANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NANOPARTICLE;

ADULT ANIMAL; AEROSOL; AIR POLLUTION; AMBIENT AIR; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANXIETY; ARTICLE; BIRTH WEIGHT; BRAIN CORTEX; BRAIN NERVE CELL; CELL COUNT; CONTROLLED STUDY; DEPRESSION; ENCEPHALITIS; EXHAUST GAS; EXPERIMENTAL TEST; FEMALE; LITTER SIZE; MATING; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FUNCTION; NEWBORN; NONHUMAN; OOCYTE MATURATION; PARTICULATE MATTER; PILOT STUDY; POSTNATAL GROWTH; PREGNANCY; PRENATAL EXPOSURE; PYRAMIDAL NERVE CELL; SEX DIFFERENCE; TAIL SUSPENSION TEST; URBAN AREA;

AIR POLLUTANTS; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELLS, CULTURED; CITIES; DEPRESSIVE DISORDER; FEMALE; HIPPOCAMPUS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; MAZE LEARNING; MICE; MICE, INBRED C57BL; NANOPARTICLES; NEURITES; NEURONS; PARTICULATE MATTER; PILOT PROJECTS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

MUS; RODENTIA;

EID: 84878425761     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0064128     Document Type: Article

References (57)

1. Mendola P, Selevan SG, Gutter S, Rice D, (2002) Environmental factors associated with a spectrum of neurodevelopmental deficits. Ment Retard Dev Disabil Res Rev 8: 188-197.
2. Bellinger DC, (2012) A strategy for comparing the contributions of environmental chemicals and other risk factors to neurodevelopment of children. Environ Health Perspect 120: 501-507.
3. Volk HE, Lurmann F, Penfold B, Hertz-Picciotto I, McConnell R, (2012) Traffic-Related Air Pollution, Particulate Matter, and Autism. JAMA Psychiatry 70: 71-77.
4. Volk HE, Hertz-Picciotto I, Delwiche L, Lurmann F, McConnell R, (2011) Residential proximity to freeways and autism in the CHARGE study. Environ Health Perspect 119: 873-877.
5. Mortensen PB, Pedersen CB, Westergaard T, Wohlfahrt J, Ewald H, et al. (1999) Effects of family history and place and season of birth on the risk of schizophrenia. N Engl J Med 340: 603-608.
6. Marcelis M, Takei N, van Os J, (1999) Urbanization and risk for schizophrenia: does the effect operate before or around the time of illness onset? Psychol Med 29: 1197-1203.
7. Lederbogen F, Kirsch P, Haddad L, Streit F, Tost H, et al. (2011) City living and urban upbringing affect neural social stress processing in humans. Nature 474: 498-501.
8. Perera FP, Wang S, Vishnevetsky J, Zhang B, Cole KJ, et al. (2011) Polycyclic aromatic hydrocarbons-aromatic DNA adducts in cord blood and behavior scores in New York city children. Environ Health Perspect 119: 1176-1181.
9. Perera FP, Tang D, Wang S, Vishnevetsky J, Zhang B, et al. (2012) Prenatal polycyclic aromatic hydrocarbon (PAH) exposure and child behavior at age 6-7 years. Environ Health Perspect 120: 921-926.
10. Pedersen CB, Raaschou-Nielsen O, Hertel O, Mortensen PB, (2004) Air pollution from traffic and schizophrenia risk. Schizophr Res 66: 83-85.
11. Calderon-Garciduenas L, Engle R, Mora-Tiscareno A, Styner M, Gomez-Garza G, et al. (2011) Exposure to severe urban air pollution influences cognitive outcomes, brain volume and systemic inflammation in clinically healthy children. Brain Cogn 77: 345-355.
12. Currie J, Neidell M, Schmieder JF, (2009) Air pollution and infant health: Lessons from New Jersey. J Health Econ 28: 688-703.
13. Guxens M, Aguilera I, Ballester F, Estarlich M, Fernandez-Somoano A, et al. (2012) Prenatal exposure to residential air pollution and infant mental development: modulation by antioxidants and detoxification factors. Environ Health Perspect 120: 144-149.
14. Perera FP, Rauh V, Whyatt RM, Tsai WY, Tang D, et al. (2006) Effect of prenatal exposure to airborne polycyclic aromatic hydrocarbons on neurodevelopment in the first 3 years of life among inner-city children. Environ Health Perspect 114: 1287-1292.
15. Bolton JL, Smith SH, Huff NC, Gilmour MI, Foster WM, et al. (2012) Prenatal air pollution exposure induces neuroinflammation and predisposes offspring to weight gain in adulthood in a sex-specific manner. FASEB J 26: 4743-4754.
16. Win-Shwe TT, Mitsushima D, Yamamoto S, Fujitani Y, Funabashi T, et al. (2009) Extracellular glutamate level and NMDA receptor subunit expression in mouse olfactory bulb following nanoparticle-rich diesel exhaust exposure. Inhal Toxicol 21: 828-836.
17. Suzuki T, Oshio S, Iwata M, Saburi H, Odagiri 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.
18. Yokota S, Mizuo K, Moriya N, Oshio S, Sugawara I, et al. (2009) Effect of prenatal exposure to diesel exhaust on dopaminergic system in mice. Neurosci Lett 449: 38-41.
19. Sugamata M, Ihara T, Takano H, Oshio S, Takeda K, (2006) Maternal diesel exhaust exposure damages newborn murine. J Health Sci 52: 82-84.
20. Sugamata M, Ihara T, Sugamata M, Takeda K, (2006) Maternal exposure to diesel exhaust leads to pathological similarity to autism in newborns. J Health Sci 52: 486-488.
21. Auten RL, Gilmour MI, Krantz QT, Potts EN, Mason SN, et al. (2012) Maternal diesel inhalation increases airway hyperreactivity in ozone-exposed offspring. Am J Respir Cell Mol Biol 46: 454-460.
22. Ning Z, Geller MD, Moore KF, Sheesley R, Schauer JJ, et al. (2007) Daily variation in chemical characteristics of urban ultrafine aerosols and inference of their sources. Environ Sci Technol 41: 6000-6006.
23. Nel A, Xia T, Madler L, Li N, (2006) Toxic potential of materials at the nanolevel. Science 311: 622-627.
24. Oberdörster G, Oberdörster E, Oberdörster J, (2005) Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect 113: 823-839.
25. Morgan TE, Davis DA, Iwata N, Tanner JA, Snyder D, et al. (2011) Glutamatergic neurons in rodent models respond to nanoscale particulate urban air pollutants in vivo and in vitro. Environ Health Perspect 119: 1003-1009.
26. Zhang H, Liu H, Davies KJ, Sioutas C, Finch CE, et al. (2012) Nrf2-regulated phase II enzymes are induced by chronic ambient nanoparticle exposure in young mice with age-related impairments. Free Radic Biol Med.
27. Eagleson KL, Campbell DB, Thompson BL, Bergman MY, Levitt P, (2011) The autism risk genes MET and PLAUR differentially impact cortical development. Autism Res 4: 68-83.
28. Szatmari P, Paterson AD, Zwaigenbaum L, Roberts W, Brian J, et al. (2007) Mapping autism risk loci using genetic linkage and chromosomal rearrangements. Nat Genet 39: 319-328.
29. Misra C, Kim S, Shen S, Sioutas C, (2002) A high flow rate, very low pressure drop impactor for inertial separation of ultrafine from accumulation mode particles. Journal of Aerosol Science 33: 735-752.
30. Li N, Sioutas C, Cho A, Schmitz D, Misra C, et al. (2003) Ultrafine particulate pollutants induce oxidative stress and mitochondrial damage. Environ Health Perspect 111: 455-460.
31. Oakberg EF, Tyrrell PD, (1975) Labeling the zona pellucida of the mouse oocyte. Biol Reprod 12: 477-482.
32. Pedersen T, (1970) Follicle kinetics in the ovary of the cyclic mouse. Acta Endocrinol (Copenh) 64: 304-323.
33. Meirow D, Epstein M, Lewis H, Nugent D, Gosden RG, (2001) Administration of cyclophosphamide at different stages of follicular maturation in mice: effects on reproductive performance and fetal malformations. Hum Reprod 16: 632-637.
34. Banker GA, Cowan WM, (1977) Rat hippocampal neurons in dispersed cell culture. Brain Res 126: 397-342.
35. Dotti CG, Sullivan CA, Banker GA, (1988) The establishment of polarity by hippocampal neurons in culture. J Neurosci 8: 1454-1468.
36. Dehmelt L, Halpain S, (2007) Neurite outgrowth: a flick of the wrist. Curr Biol 17: R611-614.
37. Crawley JN (2000) What's wrong with my mouse? New York Wiley-Liss.
38. Scott AL, Bortolato M, Chen K, Shih JC, (2008) Novel monoamine oxidase A knock out mice with human-like spontaneous mutation. Neuroreport 19: 739-743.
39. Bortolato M, Godar SC, Davarian S, Chen K, Shih JC, (2009) Behavioral disinhibition and reduced anxiety-like behaviors in monoamine oxidase B-deficient mice. Neuropsychopharmacology 34: 2746-2757.
40. Campbell DB, Sutcliffe JS, Ebert PJ, Militerni R, Bravaccio C, et al. (2006) A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci U S A 103: 16834-16839.
41. Fatemi SH, Folsom TD, (2011) Dysregulation of fragile × mental retardation protein and metabotropic glutamate receptor 5 in superior frontal cortex of individuals with autism: a postmortem brain study. Mol Autism 2: 6.
42. Fatemi SH, Folsom TD, Kneeland RE, Liesch SB, (2011) Metabotropic glutamate receptor 5 upregulation in children with autism is associated with underexpression of both Fragile × mental retardation protein and GABAA receptor beta 3 in adults with autism. Anat Rec (Hoboken) 294: 1635-1645.
43. Westerdahl D, Fruin S, Sax T, Fine PM, Sioutas C, (2005) Mobile platform measurements of ultrafine particles and associated pollutant concentrations on freeways and residential streets in Los Angeles. Atmospheric Environment 39: 3597-3610.
44. Fruin S, Westerdahl D, Sax TM, Fine PM, Sioutas C, (2008) Measurements and Predictors of On - Road Ultrafine Particle Concentrations and Associated Pollutants For Freeways and Arterial Roads in Los Angeles. Atmospheric Environment 42: 207-219.
45. Kunzli N, Jerrett M, Garcia-Esteban R, Basagana X, Beckermann B, et al. (2010) Ambient air pollution and the progression of atherosclerosis in adults. PLoS One 5: e9096.
46. Perera F, Herbstman J, (2011) Prenatal environmental exposures, epigenetics, and disease. Reprod Toxicol 31: 363-373.
47. Hougaard KS, Jensen KA, Nordly P, Taxvig C, Vogel U, et al. (2008) Effects of prenatal exposure to diesel exhaust particles on postnatal development, behavior, genotoxicity and inflammation in mice. Part Fibre Toxicol 5: 3.
48. Cuppini R, Sartini S, Ambrogini P, Falcieri E, Maltarello MC, et al. (1999) Control of neuron outgrowth by NMDA receptors. J Submicrosc Cytol Pathol 31: 31-40.
49. Hirai S, Banba Y, Satake T, Ohno S, (2011) Axon formation in neocortical neurons depends on stage-specific regulation of microtubule stability by the dual leucine zipper kinase-c-Jun N-terminal kinase pathway. J Neurosci 31: 6468-6480.
50. Oliva AA Jr, Atkins CM, Copenagle L, Banker GA, (2006) Activated c-Jun N-terminal kinase is required for axon formation. J Neurosci 26: 9462-9470.
51. Lu A, Steiner MA, Whittle N, Vogl AM, Walser SM, et al. (2008) Conditional mouse mutants highlight mechanisms of corticotropin-releasing hormone effects on stress-coping behavior. Mol Psychiatry 13: 1028-1042.
52. Cryan JF, Mombereau C, Vassout A, (2005) The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice. Neurosci Biobehav Rev 29: 571-625.
53. Steru L, Chermat R, Thierry B, Simon P, (1985) The tail suspension test: a new method for screening antidepressants in mice. Psychopharmacology (Berl) 85: 367-370.
54. Liu X, Gershenfeld HK, (2001) Genetic differences in the tail-suspension test and its relationship to imipramine response among 11 inbred strains of mice. Biol Psychiatry 49: 575-581.
55. Kessler RC, (2003) Epidemiology of women and depression. J Affect Disord 74: 5-13.
56. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, et al. (2011) Neuron number and size in prefrontal cortex of children with autism. JAMA 306: 2001-2010.
57. Courchesne E, Campbell K, Solso S, (2011) Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res 1380: 138-145.