Gestational exposure to air pollution alters cortical volume, microglial morphology, and microglia-neuron interactions in a sex-specific manner

Frontiers in Synaptic Neuroscience

Volumn 9, Issue MAY, 2017, Pages

  Bolton, Jessica L ^a   Marinero, Steven ^b   Hassanzadeh, Tania ^a   Natesan, Divya ^a   Le, Dominic ^a   Belliveau, Christine ^a   Mason, S N ^b   Auten, Richard L ^b   Bilbo, Staci D ^a,b,c  

^a DUKE UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Air pollution; Brain development; Cortical volume; Microglia; Microglia neuron interactions

Indexed keywords

CYTOKINE; TOLL LIKE RECEPTOR 4;

AIR POLLUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN SIZE; CELL ACTIVATION; CELL INTERACTION; CELL MATURATION; CELL STRUCTURE; CONTROLLED STUDY; EMBRYO; EXHAUST GAS; FEMALE; MALE; MENTAL DISEASE; MICROGLIA; MOUSE; NEURAL STEM CELL; NONHUMAN; PERINATAL PERIOD; PRENATAL EXPOSURE; PROGENY; SEX DIFFERENCE;

EID: 85020110865     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2017.00010     Document Type: Article

References (69)

1. Ackman, J. B., Siddiqi, F., Walikonis, R. S., and LoTurco, J. J. (2006). Fusion of microglia with pyramidal neurons after retroviral infection. J. Neurosci. 26, 11413-11422. doi: 10.1523/JNEUROSCI.3340-06.2006
2. Alvarez-Dolado, M., Pardal, R., Garcia-Verdugo, J. M., Fike, J. R., Lee, H. O., Pfeffer, K., et al. (2003). Fusion of bone-marrow-derived cells with Purkinje neurons, cardiomyocytes and hepatocytes. Nature 425, 968-973. doi: 10.1038/nature02069
3. Bale, T. L., and Epperson, C. N. (2017). Sex as a biological variable: who, what, when, why, and how. Neuropsychopharmacology 42, 386-396. doi: 10.1038/npp.2016.215
4. Bandeira, F., Lent, R., and Herculano-Houzel, S. (2009). Changing numbers of neuronal and non-neuronal cells underlie postnatal brain growth in the rat. Proc. Natl. Acad. Sci. U.S.A. 106, 14108-14113. doi: 10.1073/pnas.0804650106
5. Bilbo, S. D., and Schwarz, J. M. (2012). The immune system and developmental programming of brain and behavior. Front. Neuroendocrinol. 33:267-286. doi: 10.1016/j.yfrne.2012.08.006
6. Bland, S. T., Beckley, J. T., Young, S., Tsang, V., Watkins, L. R., Maier, S. F., et al. (2009). Enduring consequences of early-life infection on glial and neural cell genesis within cognitive regions of the brain. Brain Behav. Immun. 24, 329-338. doi: 10.1016/j.bbi.2009.09.012
7. Blinzinger, K., and Kreutzberg, G. (1968). Displacement of synaptic terminals from regenerating motoneurons by microglial cells. Z Zellforsch. Mikrosk. Anat. 85, 145-157. doi: 10.1007/BF00325030
8. Block, M. L., and Calderon-Garciduenas, L. (2009). Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci. 32, 506-516. doi: 10.1016/j.tins.2009.05.009
9. Block, M. L., Elder, A., Auten, R. L., Bilbo, S. D., Chen, H., Chen, J. C., et al. (2012). The outdoor air pollution and brain health workshop. Neurotoxicology 33, 972-984. doi: 10.1016/j.neuro.2012.08.014
10. Block, M. L., Zecca, L., and Hong, J. S. (2007). Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 8, 57-69. doi: 10.1038/nrn2038
11. Bolton, J. L., Auten, R. L., and Bilbo, S. D. (2014). Prenatal air pollution exposure induces sexually dimorphic fetal programming of metabolic and neuroinflammatory outcomes in adult offspring. Brain Behav. Immun. 37, 30-44. doi: 10.1016/j.bbi.2013.10.029
12. Bolton, J. L., Huff, N. C., Smith, S. H., Mason, S. N., Foster, W. M., Auten, R. L., et al. (2013). Maternal stress and effects of prenatal air pollution on offspring mental health outcomes in mice. Environ. Health Perspect. 121, 1075-1082. doi: 10.1289/ehp.1306560
13. Bolton, J. L., Smith, S. H., Huff, N. C., Gilmour, M. I., Foster, W. M., Auten, R. L., 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. doi: 10.1096/fj.12-210989
14. Carter, C. J., and Blizard, R. A. (2016). Autism genes are selectively targeted by environmental pollutants including pesticides, heavy metals, bisphenol A, phthalates and many others in food, cosmetics or household products. Neurochem. Int. 101, 83-109. doi: 10.1016/j.neuint.2016.10.011
15. Chen, Z., Jalabi, W., Hu, W., Park, H. J., Gale, J. T., Kidd, G. J., et al. (2014). Microglial displacement of inhibitory synapses provides neuroprotection in the adult brain. Nat. Commun. 5, 4486. doi: 10.1038/ncomms5486
16. Costa, L. G., Cole, T. B., Coburn, J., Chang, Y. C., Dao, K., and Roque, P. J. (2015). Neurotoxicity of traffic-related air pollution. Neurotoxicology 59, 133-139. doi: 10.1016/j.neuro.2015.11.008
17. Courchesne, E., Mouton, P. R., Calhoun, M. E., Semendeferi, K., Ahrens-Barbeau, C., Hallet, M. J., et al. (2011). Neuron number and size in prefrontal cortex of children with autism. JAMA 306, 2001-2010. doi: 10.1001/jama.2011.1638
18. Courchesne, E., Press, G. A., and Yeung-Courchesne, R. (1993). Parietal lobe abnormalities detected with MR in patients with infantile autism. AJR.Am. J. Roentgenol. 160, 387. doi: 10.2214/ajr.160.2.8424359
19. Cunningham, C. L., Martinez-Cerdeno, V., and Noctor, S. C. (2013). Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33, 4216-4233. doi: 10.1523/JNEUROSCI.3441-12.2013
20. Cusulin, C., Monni, E., Ahlenius, H., Wood, J., Brune, J. C., Lindvall, O., et al. (2012). Embryonic stem cell-derived neural stem cells fuse with microglia and mature neurons. Stem Cells 30, 2657-2671. doi: 10.1002/stem.1227
21. Egaas, B., Courchesne, E., and Saitoh, O. (1995). Reduced size of corpus callosum in autism. Arch. Neurol. 52, 794. doi: 10.1001/archneur.1995.00540320070014
22. Ginhoux, F., Greter, M., Leboeuf, M., Nandi, S., See, P., Gokhan, S., et al. (2010). Fate mapping analysis reveals that adult microglia derive from primitive macrophages. Science (New York, N.Y.) 330, 841-845. doi: 10.1126/science.1194637
23. Glaser, J., Green, G., and Hendricks, S. (2007). Stereology for Biological Research. Williston, VT: MBF Press.
24. Godbout, J. P., Chen, J., Abraham, J., Richwine, A. F., Berg, B. M., Kelley, K. W., et al. (2005). Exaggerated neuroinflammation and sickness behavior in aged mice following activation of the peripheral innate immune system. FASEB J. 19, 1329-1331. doi: 10.1096/fj.05-3776fje
25. Gomez-Gonzalez, B., and Escobar, A. (2010). Prenatal stress alters microglial development and distribution in postnatal rat brain. Acta Neuropathol. 119, 303-315. doi: 10.1007/s00401-009-0590-4
26. Graeber, M. B., Streit, W. J., and Kreutzberg, G. W. (1988). Axotomy of the rat facial nerve leads to increased CR3 complement receptor expression by activated microglial cells. J. Neurosci. Res. 21, 18-24. doi: 10.1002/jnr.490210104
27. Gundersen, H. J., and Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. J. Microsc. 147, 229-263. doi: 10.1111/j.1365-2818.1987.tb02837.x
28. Hanamsagar, R., Alter, M. D., Block, C. S., Sullivan, H., Bolton, J. L., and Bilbo, S. D. (2017). Generation of a microglial developmental index in mice and in humans reveals a sex difference in maturation and immune reactivity. Glia (in press).
29. Hartz, A. M., Bauer, B., Block, M. L., Hong, J. S., and Miller, D. S. (2008). Diesel exhaust particles induce oxidative stress, proinflammatory signaling, and P-glycoprotein up-regulation at the blood-brain barrier. FASEB J. 22, 2723-2733. doi: 10.1096/fj.08-106997
30. Herbert, M. R. (2005). Large brains in autism: the challenge of pervasive abnormality. Neuroscientist 11, 417-440. doi: 10.1177/0091270005278866
31. Inoue, K., Takano, H., Sakurai, M., Oda, T., Tamura, H., Yanagisawa, R., et al. (2006a). Pulmonary exposure to diesel exhaust particles enhances coagulatory disturbance with endothelial damage and systemic inflammation related to lung inflammation. Exp. Biol. Med. (Maywood, N.J.) 231, 1626-1632.
32. Inoue, K., Takano, H., Yanagisawa, R., Hirano, S., Ichinose, T., Shimada, A., et al. (2006b). The role of toll-like receptor 4 in airway inflammation induced by diesel exhaust particles. Arch. Toxicol. 80, 275-279. doi: 10.1007/s00204-005-0040-6
33. Inoue, K., Takano, H., Yanagisawa, R., Hirano, S., Kobayashi, T., Ichinose, T., et al. (2006c). Effects of organic chemicals derived from ambient particulate matter on lung inflammation related to lipopolysaccharide. Arch. Toxicol. 80, 833-838. doi: 10.1007/s00204-006-0105-1
34. Kalla, R., Liu, Z., Xu, S., Koppius, A., Imai, Y., Kloss, C. U., et al. (2001). Microglia and the early phase of immune surveillance in the axotomized facial motor nucleus: impaired microglial activation and lymphocyte recruitment but no effect on neuronal survival or axonal regeneration in macrophage-colony stimulating factor-deficient mice. J. Comp. Neurol. 436, 182-201. doi: 10.1002/cne.1060
35. Kreutzberg, G. W. (1996). Microglia: a sensor for pathological events in the CNS. Trends Neurosci. 19, 312-318. doi: 10.1016/0166-2236(96)10049-7
36. Lee, A. S., Azmitia, E. C., and Whitaker-Azmitia, P. M. (2017). Developmental microglial priming in postmortem autism spectrum disorder temporal cortex. Brain Behav. Immun. 62, 193-202. doi: 10.1016/j.bbi.2017.01.019
37. Lyck, L., Kroigard, T., and Finsen, B. (2007). Unbiased cell quantification reveals a continued increase in the number of neocortical neurones during early post-natal development in mice. Eur. J. Neurosci. 26, 1749-1764. doi: 10.1111/j.1460-9568.2007.05763.x
38. McKinstry, S. U., Karadeniz, Y. B., Worthington, A. K., Hayrapetyan, V. Y., Ozlu, M. I., Serafin-Molina, K., et al. (2014). Huntingtin is required for normal excitatory synapse development in cortical and striatal circuits. J. Neurosci. 34, 9455-9472. doi: 10.1523/JNEUROSCI.4699-13.2014
39. Money, J., Bobrow, N. A., and Clarke, F. C. (1971). Autism and autoimmune disease: a family study. J. Autism Child Schizophr. 1, 146-160. doi: 10.1007/BF01537954
40. Morgan, J. T., Chana, G., Pardo, C. A., Achim, C., Semendeferi, K., Buckwalter, J., et al. (2010). Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism. Biol. Psychiatry 68, 368-376. doi: 10.1016/j.biopsych.2010.05.024
41. Mouton, P. R. (2002). Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists. Baltimore, MD: JHU Press.
42. Murphy, V. E., Gibson, P. G., Giles, W. B., Zakar, T., Smith, R., Bisits, A. M., et al. (2003). Maternal asthma is associated with reduced female fetal growth. Am. J. Respir. Crit. Care Med. 168, 1317. doi: 10.1164/rccm.200303-374oc
43. Nazeen, S., Palmer, N. P., Berger, B., and Kohane, I. S. (2016). Integrative analysis of genetic data sets reveals a shared innate immune component in autism spectrum disorder and its co-morbidities. Genome Biol. 17, 228. doi: 10.1186/s13059-016-1084-z
44. Noctor, S. C., Martinez-Cerdeno, V., Ivic, L., and Kriegstein, A. R. (2004). Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nat. Neurosci. 7, 136-144. doi: 10.1038/nn1172
45. Noctor, S. C., Martinez-Cerdeno, V., and Kriegstein, A. R. (2008). Distinct behaviors of neural stem and progenitor cells underlie cortical neurogenesis. J. Comp. Neurol. 508, 28-44. doi: 10.1002/cne.21669
46. Paolicelli, R. C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., et al. (2011). Synaptic pruning by microglia is necessary for normal brain development. Science 333, 1456-1458. doi: 10.1126/science.1202529
47. Pardo, C. A., Vargas, D. L., and Zimmerman, A. W. (2005). Immunity, neuroglia and neuroinflammation in autism. Int. Rev. Psychiatry 17, 485-495. doi: 10.1080/02646830500381930
48. Raivich, G., Gehrmann, J., and Kreutzberg, G. W. (1991). Increase of macrophage colony-stimulating factor and granulocyte-macrophage colony-stimulating factor receptors in the regenerating rat facial nucleus. J. Neurosci. Res. 30, 682-686. doi: 10.1002/jnr.490300412
49. Raz, R., Roberts, A. L., Lyall, K., Hart, J. E., Just, A. C., Laden, F., et al. (2014). Autism spectrum disorder and particulate matter air pollution before, during, and after pregnancy: a nested case-control analysis within the nurses' health study ii cohort. Environ. Health Perspect. 123, 264-270. doi: 10.1289/ehp.1408133
50. Ribak, C. E., Shapiro, L. A., Perez, Z. D., and Spigelman, I. (2009). Microglia-associated granule cell death in the normal adult dentate gyrus. Brain Struct. Funct. 214, 25-35. doi: 10.1007/s00429-009-0231-7
51. Roberts, A. L., Lyall, K., Hart, J. E., Laden, F., Just, A. C., Bobb, J. F., et al. (2013). Perinatal air pollutant exposures and autism spectrum disorder in the children of Nurses' Health Study II participants. Environ. Health Perspect. 121, 978-984. doi: 10.1289/ehp.1206187
52. Rossignol, D. A., Genuis, S. J., and Frye, R. E. (2014). Environmental toxicants and autism spectrum disorders: a systematic review. Transl. Psychiatry 4, e360. doi: 10.1038/tp.2014.4
53. Schafer, D. P., Lehrman, E. K., Heller, C. T., and Stevens, B. (2014). An engulfment assay: a protocol to assess interactions between CNS phagocytes and neurons. J. Vis. Exp. 8:51482. doi: 10.3791/51482
54. Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., et al. (2012). Microglia sculpt postnatal neural circuits in an activity and complement-dependent manner. Neuron 74, 691-705. doi: 10.1016/j.neuron.2012.03.026
55. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675. doi: 10.1038/nmeth.2089
56. Slotkin, T. A., and Seidler, F. J. (2015). Prenatal nicotine alters the developmental neurotoxicity of postnatal chlorpyrifos directed toward cholinergic systems: better, worse, or just "different". Brain Res. Bull. 110, 54-67. doi: 10.1016/j.brainresbull.2014.12.003
57. Snedecor, G. W., and Cochran, W. G. (1967). Statistical Methods. Ames, IA: Iowa State University Press.
58. Spear, L. P., and Brake, S. C. (1983). Periadolescence: age-dependent behavior and psychopharmacological responsivity in rats. Dev. Psychobiol. 16, 83-109. doi: 10.1002/dev.420160203
59. Stone, J. L., Merriman, B., Cantor, R. M., Yonan, A. L., Gilliam, T. C., Geschwind, D. H., et al. (2004). Evidence for sex-specific risk alleles in autism spectrum disorder. Am. J. Hum. Genet. 75, 1117. doi: 10.1086/426034
60. Suzuki, K., Sugihara, G., Ouchi, Y., Nakamura, K., Futatsubashi, M., Takebayashi, K., et al. (2013). Microglial activation in young adults with autism spectrum disorder. JAMA Psychiatry 70, 49-58. doi: 10.1001/jamapsychiatry.2013.272
61. Trapp, B. D., Wujek, J. R., Criste, G. A., Jalabi, W., Yin, X., Kidd, G. J., et al. (2007). Evidence for synaptic stripping by cortical microglia. Glia 55, 360-368. doi: 10.1002/glia.20462
62. Vargas, D. L., Nascimbene, C., Krishnan, C., Zimmerman, A. W., and Pardo, C. A. (2005). Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann. Neurol. 57, 67-81. doi: 10.1002/ana.20315
63. Volk, H. E., Hertz-Picciotto, I., Delwiche, L., Lurmann, F., and McConnell, R. (2011). Residential proximity to freeways and autism in the CHARGE study. Environ. Health Perspect. 119, 873-877. doi: 10.1289/ehp.1002835
64. Volk, H. E., Lurmann, F., Penfold, B., Hertz-Picciotto, I., and McConnell, R. (2013). Traffic-related air pollution, particulate matter, and autism. JAMA Psychiatry 70, 71-77. doi: 10.1001/jamapsychiatry.2013.266
65. Williamson, L. L., Sholar, P. W., Mistry, R. S., Smith, S. H., and Bilbo, S. D. (2011). Microglia and memory: modulation by early-life infection. J. Neurosci. 31, 15511-15521. doi: 10.1523/JNEUROSCI.3688-11.2011
66. Wu, C. H., Wen, C. Y., Shieh, J. Y., and Ling, E. A. (1992). A quantitative and morphometric study of the transformation of amoeboid microglia into ramified microglia in the developing corpus callosum in rats. J. Anat. 181, 423-430.
67. Wu, C. H., Wen, C. Y., Shieh, J. Y., and Ling, E. A. (1993). A quantitative study of the differentiation of microglial cells in the developing cerebral cortex in rats. J. Anat. 182, 403-413.
68. Yirmiya, R., and Goshen, I. (2011). Immune modulation of learning, memory, neural plasticity and neurogenesis. Brain Behav. Immun. 25, 181-213. doi: 10.1016/j.bbi.2010.10.015
69. Zhan, Y., Paolicelli, R. C., Sforazzini, F., Weinhard, L., Bolasco, G., Pagani, F., et al. (2014). Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat. Neurosci. 17, 400-406. doi: 10.1038/nn.3641