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Behavioural Neurology
Volume 2015, Article ID 426263, 10 pages
http://dx.doi.org/10.1155/2015/426263
Research Article

Autism-Like Behavior and Epigenetic Changes Associated with Autism as Consequences of In Utero Exposure to Environmental Pollutants in a Mouse Model

1Center for Environmental and Genetic Medicine, Institute of Biosciences and Technology, Texas A&M University System Health Science Center, Houston, TX 77030, USA
2Department of Nutritional Sciences, The University of Texas at Austin, Austin, TX 78723, USA
3Department of Biochemistry & Biophysics, Texas A&M University, College Station, TX 77843, USA

Received 10 June 2015; Revised 1 October 2015; Accepted 1 October 2015

Academic Editor: João Quevedo

Copyright © 2015 Denise S. Hill et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. American Psychiatric Association, Diagnostic and Statistical Manual of Mental Disorders, American Psychiatric Association, Arlington, Va, USA, 2013, http://dsm.psychiatryonline.org.
  2. L. E. Buxton and R. N. Murdoch, “Lectins, calcium ionophore A23187 and peanut oil as deciduogenic agents in the uterus of pseudopregnant mice: effects of tranylcypromine, indomethacin, iproniazid and propranolol,” Australian Journal of Biological Sciences, vol. 35, no. 1, pp. 63–72, 1982. View at Google Scholar · View at Scopus
  3. C. Ladd-Acosta, K. D. Hansen, E. Briem, M. D. Fallin, W. E. Kaufmann, and A. P. Feinberg, “Common DNA methylation alterations in multiple brain regions in autism,” Molecular Psychiatry, vol. 19, no. 8, pp. 862–871, 2014. View at Publisher · View at Google Scholar · View at Scopus
  4. J. M. LaSalle, “A genomic point-of-view on environmental factors influencing the human brain methylome,” Epigenetics, vol. 6, no. 7, pp. 862–869, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. J. Lv, Y. Xin, W. Zhou, and Z. Qiu, “The epigenetic switches for neural development and psychiatric disorders,” Journal of Genetics and Genomics, vol. 40, no. 7, pp. 339–346, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. A. M. Persico and T. Bourgeron, “Searching for ways out of the autism maze: genetic, epigenetic and environmental clues,” Trends in Neurosciences, vol. 29, no. 7, pp. 349–358, 2006. View at Publisher · View at Google Scholar
  7. K. C. Kim, C. S. Choi, J.-W. Kim et al., “MeCP2 modulates sex differences in the postsynaptic development of the valproate animal model of autism,” Molecular Neurobiology, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Chahrour, Y. J. Sung, C. Shaw et al., “MeCP2, a key contributor to neurological disease, activates and represses transcription,” Science, vol. 320, no. 5880, pp. 1224–1229, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. R. P. Nagarajan, A. R. Hogart, Y. Gwye, M. R. Martin, and J. M. LaSalle, “Reduced MeCP2 expression is frequent in autism frontal cortex and correlates with aberrant MECP2 promoter methylation,” Epigenetics, vol. 1, no. 4, pp. e1–e11, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Ornoy, “Neuroteratogens in man: an overview with special emphasis on the teratogenicity of antiepileptic drugs in pregnancy,” Reproductive Toxicology, vol. 22, no. 2, pp. 214–226, 2006. View at Publisher · View at Google Scholar · View at Scopus
  11. A. Ornoy, “Valproic acid in pregnancy: how much are we endangering the embryo and fetus?” Reproductive Toxicology, vol. 28, no. 1, pp. 1–10, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. R. H. Finnell, G. D. Bennett, S. B. Karras, and V. K. Mohl, “Common hierarchies of susceptibility to the induction of neural tube defects in mouse embryos by valproic acid and its 4-propyl-4-pentenoic acid metabolite,” Teratology, vol. 38, no. 4, pp. 313–320, 1988. View at Publisher · View at Google Scholar · View at Scopus
  13. O. S. Cohen, E. I. Varlinskaya, C. A. Wilson, S. J. Glatt, and S. M. Mooney, “Acute prenatal exposure to a moderate dose of valproic acid increases social behavior and alters gene expression in rats,” International Journal of Developmental Neuroscience, vol. 31, no. 8, pp. 740–750, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. M. R. Favre, T. R. Barkat, D. LaMendola, G. Khazen, H. Markram, and K. Markram, “General developmental health in the VPA-rat model of autism,” Frontiers in Behavioral Neuroscience, vol. 7, article 88, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. R. H. Finnell, B. C. Wlodarczyk, J. C. Craig, J. A. Piedrahita, and G. D. Bennett, “Strain-dependent alterations in the expression of folate pathway genes following teratogenic exposure to valproic acid in a mouse model,” American Journal of Medical Genetics, vol. 70, no. 3, pp. 303–311, 1997. View at Publisher · View at Google Scholar · View at Scopus
  16. D. N. Hovland Jr., A. F. Machado, W. J. Scott Jr., and M. D. Collins, “Differential sensitivity of the SWV and C57BL/6 mouse strains to the teratogenic action of single administrations of cadmium given throughout the period of anterior neuropore closure,” Teratology, vol. 60, no. 1, pp. 13–21, 1999. View at Publisher · View at Google Scholar · View at Scopus
  17. B. J. Wlodarczyk, A. M. Palacios, T. M. George, and R. H. Finnell, “Antiepileptic drugs and pregnancy outcomes,” American Journal of Medical Genetics, Part A, vol. 158, no. 8, pp. 2071–2090, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Duenas-Gonzalez, M. Candelaria, C. Perez-Plascencia, E. Perez-Cardenas, E. de la Cruz-Hernandez, and L. A. Herrera, “Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors,” Cancer Treatment Reviews, vol. 34, no. 3, pp. 206–222, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. B. Monti, E. Polazzi, and A. Contestabile, “Biochemical, molecular and epigenetic mechanisms of valproic acid neuroprotection,” Current Molecular Pharmacology, vol. 2, no. 1, pp. 95–109, 2009. View at Publisher · View at Google Scholar · View at Scopus
  20. R. J. Berry, “Maternal prenatal folic acid supplementation is associated with a reduction in development of autistic disorder,” Journal of Pediatrics, vol. 163, no. 1, pp. 303–304, 2013. View at Publisher · View at Google Scholar · View at Scopus
  21. M. A. Faucher, “Folic acid supplementation before and in early pregnancy may decrease risk for autism,” Journal of Midwifery & Women's Health, vol. 58, no. 4, pp. 471–472, 2013. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Kałuzna-Czaplińska, E. Zurawicz, M. Michalska, and J. Rynkowski, “A focus on homocysteine in autism,” Acta Biochimica Polonica, vol. 60, no. 2, pp. 137–142, 2013. View at Google Scholar · View at Scopus
  23. L. R. Schaevitz and J. E. Berger-Sweeney, “Gene-environment interactions and epigenetic pathways in autism: the importance of one-carbon metabolism,” ILAR Journal, vol. 53, no. 3-4, pp. 322–340, 2012. View at Publisher · View at Google Scholar · View at Scopus
  24. P. E. Goines and P. Ashwood, “Cytokine dysregulation in autism spectrum disorders (ASD): possible role of the environment,” Neurotoxicology and Teratology, vol. 36, pp. 67–81, 2013. View at Publisher · View at Google Scholar · View at Scopus
  25. F. Dardenne, S. Van dongen, I. Nobels, R. Smolders, W. De Coen, and R. Blust, “Mode of action clustering of chemicals and environmental samples on the bases of bacterial stress gene inductions,” Toxicological Sciences, vol. 101, no. 2, pp. 206–214, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. P. B. Tchounwou, C. G. Yedjou, A. K. Patlolla, and D. J. Sutton, “Heavy metal toxicity and the environment,” in Molecular, Clinical and Environmental Toxicology, vol. 101 of Experientia Supplementum, pp. 133–164, Springer, 2012. View at Publisher · View at Google Scholar
  27. D. A. Geier, J. K. Kern, P. G. King, L. K. Sykes, and M. R. Geier, “Hair toxic metal concentrations and autism spectrum disorder severity in young children,” International Journal of Environmental Research and Public Health, vol. 9, no. 12, pp. 4486–4497, 2012. View at Publisher · View at Google Scholar · View at Scopus
  28. D. A. Rossignol, S. J. Genuis, and R. E. Frye, “Environmental toxicants and autism spectrum disorders: a systematic review,” Translational Psychiatry, vol. 4, no. 2, article e360, 2014. View at Publisher · View at Google Scholar
  29. M. Garrecht and D. W. Austin, “The plausibility of a role for mercury in the etiology of autism: a cellular perspective,” Toxicological and Environmental Chemistry, vol. 93, no. 6, pp. 1251–1273, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. J. K. Kern, D. A. Geier, T. Audhya, P. G. King, L. K. Sykes, and M. R. Geier, “Evidence of parallels between mercury intoxication and the brain pathology in autism,” Acta Neurobiologiae Experimentalis, vol. 72, no. 2, pp. 113–153, 2012. View at Google Scholar · View at Scopus
  31. Y. Arai, J. Ohgane, S. Yagi et al., “Epigenetic assessment of environmental chemicals detected in maternal peripheral and cord blood samples,” Journal of Reproduction and Development, vol. 57, no. 4, pp. 507–517, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. D. Lonsdale, R. J. Shamberger, and M. E. Obrenovich, “Dysautonomia in autism spectrum disorder: case reports of a family with review of the literature,” Autism Research and Treatment, vol. 2011, Article ID 129795, 7 pages, 2011. View at Publisher · View at Google Scholar
  33. H. Yasuda, M. Kobayashi, Y. Yasuda, and T. Tsutsui, “Estimation of autistic children by metallomics analysis,” Scientific Reports, vol. 3, no. 1199, pp. 1–7, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. T. Schneider and R. Przewłocki, “Behavioral alterations in rats prenatally to valproic acid: animal model of autism,” Neuropsychopharmacology, vol. 30, no. 1, pp. 80–89, 2005. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Macrì, G. Laviola, M. P. Leussis, and S. L. Andersen, “Abnormal behavioral and neurotrophic development in the younger sibling receiving less maternal care in a communal nursing paradigm in rats,” Psychoneuroendocrinology, vol. 35, no. 3, pp. 392–402, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Li, R. Budin, A. S. Fleming, and S. Kapur, “Effects of chronic typical and atypical antipsychotic drug treatment on maternal behavior in rats,” Schizophrenia Research, vol. 75, no. 2-3, pp. 325–336, 2005. View at Publisher · View at Google Scholar · View at Scopus
  37. M. H. Bassant, M. Picard, D. Olichon, F. Cathala, and L. Court, “Changes in the serotonergic, noradrenergic and dopaminergic levels in the brain of scrapie-infected rats,” Brain Research, vol. 367, no. 1-2, pp. 360–363, 1986. View at Publisher · View at Google Scholar · View at Scopus
  38. N. Albelda and D. Joel, “Animal models of obsessive-compulsive disorder: exploring pharmacology and neural substrates,” Neuroscience and Biobehavioral Reviews, vol. 36, no. 1, pp. 47–63, 2012. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Angoa-Pérez, M. J. Kane, D. I. Briggs, D. M. Francescutti, and D. M. Kuhn, “Marble burying and nestlet shredding as tests of repetitive, compulsive-like behaviors in mice,” Journal of Visualized Experiments, vol. 82, Article ID e50978, 2013. View at Publisher · View at Google Scholar · View at Scopus
  40. P. Jedynak, P. Jaholkowski, G. Wozniak, C. Sandi, L. Kaczmarek, and R. K. Filipkowski, “Lack of cyclin D2 impairing adult brain neurogenesis alters hippocampal-dependent behavioral tasks without reducing learning ability,” Behavioural Brain Research, vol. 227, no. 1, pp. 159–166, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. M. J. Millan, S. Girardon, J. Mullot, M. Brocco, and A. Dekeyne, “Stereospecific blockade of marble-burying behaviour in mice by selective, non-peptidergic neurokinin1 (NK1) receptor antagonists,” Neuropharmacology, vol. 42, no. 5, pp. 677–684, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. S. S. Moy, R. J. Nonneman, G. O. Shafer et al., “Disruption of social approach by MK-801, amphetamine and fluoxetine in adolescent C57BL/6J mice,” Neurotoxicology and Teratology, vol. 36, pp. 36–46, 2013. View at Publisher · View at Google Scholar
  43. T. L. Schaefer, C. V. Vorhees, and M. T. Williams, “Mouse plasmacytoma-expressed transcript 1 knock out induced 5-HT disruption results in a lack of cognitive deficits and an anxiety phenotype complicated by hypoactivity and defensiveness,” Neuroscience, vol. 164, no. 4, pp. 1431–1443, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. S. N. Umathe, J. M. Vaghasiya, N. S. Jain, and P. V. Dixit, “Neurosteroids modulate compulsive and persistent behavior in rodents: implications for obsessive-compulsive disorder,” Progress in Neuro-Psychopharmacology and Biological Psychiatry, vol. 33, no. 7, pp. 1161–1166, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. M. Yang, J. L. Silverman, and J. N. Crawley, “UNIT 8.26 Automated three-chambered social approach task for mice,” in Current Protocols in Neuroscience, chapter 8, John Wiley & Sons, 2011. View at Publisher · View at Google Scholar
  46. J. L. Neul, “The relationship of Rett syndrome and MECP2 disorders to autism,” Dialogues in Clinical Neuroscience, vol. 14, no. 3, pp. 253–262, 2012. View at Google Scholar · View at Scopus
  47. N. M. Williams, “Molecular mechanisms in 22q11 deletion syndrome,” Schizophrenia Bulletin, vol. 37, no. 5, pp. 882–889, 2011. View at Publisher · View at Google Scholar
  48. J. Wang, D. Duncan, Z. Shi, and B. Zhang, “WEB-based gene set analysis toolkit (WebGestalt): update 2013,” Nucleic Acids Research, vol. 41, no. 1, pp. W77–W83, 2013. View at Publisher · View at Google Scholar
  49. K. Iwata, H. Matsuzaki, N. Takei, T. Manabe, and N. Mori, “Animal models of autism: an epigenetic and environmental viewpoint,” Journal of Central Nervous System Disease, vol. 2, pp. 37–44, 2010. View at Publisher · View at Google Scholar
  50. K. C. Kim, P. Kim, H. S. Go et al., “The critical period of valproate exposure to induce autistic symptoms in Sprague-Dawley rats,” Toxicology Letters, vol. 201, no. 2, pp. 137–142, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. T. Gaugler, L. Klei, S. J. Sanders et al., “Most genetic risk for autism resides with common variation,” Nature Genetics, vol. 46, no. 8, pp. 881–885, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. S. J. Sanders, M. T. Murtha, A. R. Gupta et al., “De novo mutations revealed by whole-exome sequencing are strongly associated with autism,” Nature, vol. 484, no. 7397, pp. 237–241, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. S. Idring, C. Magnusson, M. Lundberg et al., “Parental age and the risk of autism spectrum disorders: findings from a Swedish population-based cohort,” International Journal of Epidemiology, vol. 43, no. 1, pp. 107–115, 2014. View at Publisher · View at Google Scholar · View at Scopus
  54. M. R. Herbert, “Contributions of the environment and environmentally vulnerable physiology to autism spectrum disorders,” Current Opinion in Neurology, vol. 23, no. 2, pp. 103–110, 2010. View at Publisher · View at Google Scholar
  55. P. Grandjean and P. Landrigan, “Developmental neurotoxicity of industrial chemicals,” The Lancet, vol. 368, no. 9553, pp. 2167–2178, 2006. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Blaurock-Busch, O. R. Amin, H. H. Dessoki, and T. Rabah, “Toxic metals and essential elements in hair and severity of symptoms among children with autism,” Maedica, vol. 7, no. 1, pp. 38–48, 2012. View at Google Scholar
  57. M. Fujimoto, K. Sakai, and T. Ueda, “Significance of amikacin administered orally prior to operation for prevention of postoperative infections in colonic cancer surgery,” The Japanese Journal of Antibiotics, vol. 39, no. 11, pp. 2889–2896, 1986. View at Google Scholar
  58. S. Hernberg, “Lead poisoning in a historical perspective,” American Journal of Industrial Medicine, vol. 38, no. 3, pp. 244–254, 2000. View at Publisher · View at Google Scholar · View at Scopus
  59. P. J. Landrigan, A. S. McKinney, L. C. Hopkins, W. W. Rhodes Jr., W. A. Price, and D. H. Cox, “Chronic lead absorption. Result of poor ventilation in an indoor pistol range,” The Journal of the American Medical Association, vol. 234, no. 4, pp. 394–397, 1975. View at Publisher · View at Google Scholar · View at Scopus
  60. P. J. Landrigan, R. H. Baloh, W. F. Barthel, R. H. Whitworth, N. W. Staehling, and B. F. Rosenblum, “Neuropsychological dysfunction in children with chronic low-level lead absorption,” The Lancet, vol. 305, no. 7909, pp. 708–712, 1975. View at Publisher · View at Google Scholar · View at Scopus
  61. H. L. Needleman, “Lead levels and children's psychologic performance,” The New England Journal of Medicine, vol. 301, no. 3, p. 163, 1979. View at Publisher · View at Google Scholar · View at Scopus
  62. H. L. Needleman, C. Gunnoe, A. Leviton et al., “Deficits in psychologic and classroom performance of children with elevated dentine lead levels,” The New England Journal of Medicine, vol. 300, no. 13, pp. 689–695, 1979. View at Publisher · View at Google Scholar · View at Scopus
  63. H. Needleman and A. Leviton, “Lead and neurobehavioural deficit in children,” The Lancet, vol. 314, no. 8133, p. 104, 1979. View at Publisher · View at Google Scholar · View at Scopus
  64. H. L. Needleman and A. Leviton, “Neurologic effects of exposure to lead,” Journal of Pediatrics, vol. 94, no. 3, pp. 505–506, 1979. View at Publisher · View at Google Scholar · View at Scopus
  65. B. P. Lanphear, R. Hornung, J. Khoury et al., “Low-level environmental lead exposure and children's intellectual function: an international pooled analysis,” Environmental Health Perspectives, vol. 113, no. 7, pp. 894–899, 2005. View at Publisher · View at Google Scholar · View at Scopus
  66. B. C. Henn, A. S. Ettinger, J. Schwartz et al., “Early postnatal blood manganese levels and children's neurodevelopment,” Epidemiology, vol. 21, no. 4, pp. 433–439, 2010. View at Publisher · View at Google Scholar · View at Scopus
  67. Z. Su, M.-F. Chai, P.-L. Lu, R. An, J. Chen, and X.-C. Wang, “AtMTM1, a novel mitochondrial protein, may be involved in activation of the manganese-containing superoxide dismutase in Arabidopsis,” Planta, vol. 226, no. 4, pp. 1031–1039, 2007. View at Publisher · View at Google Scholar · View at Scopus
  68. L. Takser, D. Mergler, G. Hellier, J. Sahuquillo, and G. Huel, “Manganese, monoamine metabolite levels at birth, and child psychomotor development,” NeuroToxicology, vol. 24, no. 4-5, pp. 667–674, 2003. View at Publisher · View at Google Scholar · View at Scopus
  69. C.-C. Lin, Y.-C. Chen, F.-C. Su et al., “In utero exposure to environmental lead and manganese and neurodevelopment at 2 years of age,” Environmental Research, vol. 123, pp. 52–57, 2013. View at Publisher · View at Google Scholar · View at Scopus