Advertisement

Lipid Signalling in the Pathology of Autism Spectrum Disorders

  • Christine Wong
  • Dorota Anna Crawford

Abstract

Autism spectrum disorders (ASDs) result from multifaceted deficits and manifest differently in every individual. The developmental abnormalities of ASDs could be a consequence of genetic aberrations, environmental stressors, or interactions between the two during critical periods of neurodevelopment. Increasing attention has been devoted to investigating lipid signalling molecules since lipids play pivotal roles in the development and function of the human brain and body by acting as regulatory molecules that modulate growth and maintenance. Growing evidence supports the idea that altered fatty acid metabolic pathways may be involved in the pathogenesis of autism and contribute to the variable expression of autism-related traits. This chapter provides an overview of the abnormalities associated with the synthesis of lipid signalling metabolites in individuals with ASDs due to genetic and environmental factors, including dietary lipid imbalances, oxidative stress, and immunological triggers. In particular, the deficits associated with the lipid metabolic pathway for prostaglandin biosynthesis are discussed in further detail. The existing literature provides compelling evidence for the contribution of altered lipid neurobiology to the pathology of ASDs and reveals potential molecular mechanisms that may be important for the development of novel treatments and interventions.

Keywords

Autism Spectrum Disorder Essential Fatty Acid Rett Syndrome Lipid Signalling Abnormal Lipid Metabolism 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abrahams BS, Geschwind DH. Advances in autism genetics: on the threshold of a new neurobiology. Nat Rev Genet. 2008;9(5):341–55.PubMedGoogle Scholar
  2. Abu-Khalil A, Fu L, Grove EA, Zecevic N, Geschwind DH. Wnt genes define distinct boundaries in the developing human brain: implications for human forebrain patterning. J Comp Neurol. 2004;474(2):276–88.PubMedGoogle Scholar
  3. Adibhatla RM, Hatcher JF. Altered lipid metabolism in brain injury and disorders. Subcell Biochem. 2008;49:241–68.PubMedGoogle Scholar
  4. Al-Gadani Y, El-Ansary A, Attas O, Al-Ayadhi L. Metabolic biomarkers related to oxidative stress and antioxidant status in Saudi autistic children. Clin Biochem. 2009;42(10–11):1032–40.PubMedGoogle Scholar
  5. Amaral DG, Schumann CM, Nordahl CW. Neuroanatomy of autism. Trends Neurosci. 2008;31(3):137–45.PubMedGoogle Scholar
  6. Amminger GP, Berger GE, Schafer MR, Klier C, Friedrich MH, Feucht M. Omega-3 fatty acids supplementation in children with autism: a double-blind randomized, placebo-controlled pilot study. Biol Psychiatry. 2007;61(4):551–3.PubMedGoogle Scholar
  7. Aneja A, Tierney E. Autism: the role of cholesterol in treatment. Int rev psychiatry (Abingdon, England). 2008;20(2):165–70.Google Scholar
  8. Ashwood P, Van de Water J. A review of autism and the immune response. Clin Dev Immunol. 2004;11(2):165–74.PubMedGoogle Scholar
  9. Ashwood P, Wills S, Van de Water J. The immune response in autism: a new frontier for autism research. J Leukoc Biol. 2006;80(1):1–15.PubMedGoogle Scholar
  10. Atladottir HO, Thorsen P, Ostergaard L, et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010;40(12):1423–30.PubMedGoogle Scholar
  11. Bandim JM, Ventura LO, Miller MT, Almeida HC, Costa AE. Autism and mobius sequence: an exploratory study of children in northeastern Brazil. Arq Neuropsiquiatr. 2003;61(2A):181–5.PubMedGoogle Scholar
  12. Bell JG, MacKinlay EE, Dick JR, MacDonald DJ, Boyle RM, Glen AC. Essential fatty acids and phospholipase A2 in autistic spectrum disorders. Prostaglandins Leukot Essent Fatty Acids. 2004;71(4):201–4.PubMedGoogle Scholar
  13. Bell JG, Miller D, MacDonald DJ, et al. The fatty acid compositions of erythrocyte and plasma polar lipids in children with autism, developmental delay or typically developing controls and the effect of fish oil intake. Br J Nutr. 2010;103(8):1160–7.PubMedGoogle Scholar
  14. Boland LM, Drzewiecki MM, Timoney G, Casey E. Inhibitory effects of polyunsaturated fatty acids on Kv4/KChIP potassium channels. Am J Physiol Cell Physiol. 2009;296(5):C1003–14.PubMedGoogle Scholar
  15. Breyer RM, Bagdassarian CK, Myers SA, Breyer MD. Prostanoid receptors: subtypes and signaling. Annu Rev Pharmacol Toxicol. 2001;41:661–90.PubMedGoogle Scholar
  16. Brown AS, Derkits EJ. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry. 2010;167(3):261–80.PubMedGoogle Scholar
  17. Buchanan FG, DuBois RN. Connecting COX-2 and Wnt in cancer. Cancer Cell. 2006;9(1):6–8.PubMedGoogle Scholar
  18. Buechling T, Boutros M. Wnt signaling signaling at and above the receptor level. Curr Top Dev Biol. 2011;97:21–53.PubMedGoogle Scholar
  19. Bukelis I, Porter FD, Zimmerman AW, Tierney E. Smith-Lemli-Opitz syndrome and autism spectrum disorder. Am J Psychiatry. 2007;164(11):1655–61.PubMedGoogle Scholar
  20. Burks SR, Wright CL, McCarthy MM. Exploration of prostanoid receptor subtype regulating estradiol and prostaglandin E2 induction of spinophilin in developing preoptic area neurons. Neuroscience. 2007;146(3):1117–27.PubMedGoogle Scholar
  21. Buyske S, Williams TA, Mars AE, et al. Analysis of case-parent trios at a locus with a deletion allele: association of GSTM1 with autism. BMC Genet. 2006;7:8.PubMedGoogle Scholar
  22. Calderon F, Kim HY. Docosahexaenoic acid promotes neurite growth in hippocampal neurons. J Neurochem. 2004;90(4):979–88.PubMedGoogle Scholar
  23. Castellone MD, Teramoto H, Williams BO, Druey KM, Gutkind JS. Prostaglandin E2 promotes colon cancer cell growth through a Gs-axin-beta-catenin signaling axis. Science. 2005;310(5753):1504–10.PubMedGoogle Scholar
  24. Chauhan A, Chauhan V, Brown WT, Cohen I. Oxidative stress in autism: increased lipid peroxidation and reduced serum levels of ceruloplasmin and transferrin – the antioxidant proteins. Life Sci. 2004;75(21):2539–49.PubMedGoogle Scholar
  25. Choe E. Chemistry and Reactions of Reactive Oxygen Species in Lipid Oxidation. In A. Kamal-Eldin & D. Min (Eds.), Lipid Oxidation Pathways. 2010;2:31–50. Urbana, IL: AOCS Publishing.Google Scholar
  26. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol. 2008;79(1):50–7.PubMedGoogle Scholar
  27. Ciani L, Salinas PC. WNTs in the vertebrate nervous system: from patterning to neuronal connectivity. Nat Rev Neurosci. 2005;6(5):351–62.PubMedGoogle Scholar
  28. Clandinin MT, Jumpsen J, Suh M. Relationship between fatty acid accretion, membrane composition, and biologic functions. J Pediatr. 1994;125(5 Pt 2):S25–32.PubMedGoogle Scholar
  29. Craddock N, Lendon C. Chromosome workshop: chromosomes 11, 14, and 15. Am J Med Genet. 1999;88(3):244–54.PubMedGoogle Scholar
  30. Crawford MA, Hassam AG, Stevens PA. Essential fatty acid requirements in pregnancy and lactation with special reference to brain development. Prog Lipid Res. 1981;20:31–40.PubMedGoogle Scholar
  31. Crawford MA, Doyle W, Drury P, Lennon A, Costeloe K, Leighfield M. n-6 and n-3 fatty acids during early human development. J Intern Med Suppl. 1989;731:159–69.PubMedGoogle Scholar
  32. De Felice C, Ciccoli L, Leoncini S, et al. Systemic oxidative stress in classic Rett syndrome. Free Radic Biol Med. 2009;47(4):440–8.PubMedGoogle Scholar
  33. de la Cochetière MF, Rougé C, Darmaun D, Rozé JC, Potel G, Gras-Leguen C. Intestinal microbiota in neonates and preterm infants: a review. Curr Pediatr Rev. 2007;3:21–34.Google Scholar
  34. de Vries HE, Blom-Roosemalen MC, van Oosten M, et al. The influence of cytokines on the integrity of the blood–brain barrier in vitro. J Neuroimmunol. 1996;64(1):37–43.PubMedGoogle Scholar
  35. Deth R, Muratore C, Benzecry J, Power-Charnitsky VA, Waly M. How environmental and genetic factors combine to cause autism: a redox/methylation hypothesis. Neurotoxicology. 2008;29(1):190–201.PubMedGoogle Scholar
  36. Dubois A, Rattaz C, Pry R, Baghdadli A. Autism and pain – a literature review. Pain Res Manag. 2010;15(4):245–53.PubMedGoogle Scholar
  37. Evans T. Fishing for a WNT-PGE2 link: beta-catenin is caught in the stem cell net-work. Cell Stem Cell. 2009;4(4):280–2.PubMedGoogle Scholar
  38. Evans TA, Siedlak SL, Lu L, et al. The autistic phenotype exhibits a remarkably localized modification of brain protein by products of free radical-induced lipid oxidation. Am J Biotechno Biochem. 2008;4(2):61–72.Google Scholar
  39. Farooqui AA, Horrocks LA, Farooqui T. Modulation of inflammation in brain: a matter of fat. J Neurochem. 2007;101(3):577–99.PubMedGoogle Scholar
  40. Fatemi SH, Halt AR, Realmuto G, et al. Purkinje cell size is reduced in cerebellum of patients with autism. Cell Mol Neurobiol. 2002;22(2):171–5.PubMedGoogle Scholar
  41. Fatemi SH, Pearce DA, Brooks AI, Sidwell RW. Prenatal viral infection in mouse causes differential expression of genes in brains of mouse progeny: a potential animal model for schizophrenia and autism. Synapse. 2005;57(2):91–9.PubMedGoogle Scholar
  42. Fatemi SH, Reutiman TJ, Folsom TD, et al. Maternal infection leads to abnormal gene regulation and brain atrophy in mouse offspring: implications for genesis of neurodevelopmental disorders. Schizophr Res. 2008;99(1–3):56–70.PubMedGoogle Scholar
  43. Ferrucci L, Cherubini A, Bandinelli S, et al. Relationship of plasma polyunsaturated fatty acids to circulating inflammatory markers. J Clin Endocrinol Metab. 2006;91(2):439–46.PubMedGoogle Scholar
  44. Filomeni G, Ciriolo MR. Redox control of apoptosis: an update. Antioxid Redox Signal. 2006;8(11–12):2187–92.PubMedGoogle Scholar
  45. Fitzgerald DW, Bezak K, Ocheretina O, et al. The effect of HIV and HPV coinfection on cervical COX-2 expression and systemic prostaglandin E2 levels. Cancer Prev Res (Phila). 2012;5(1):34–40.Google Scholar
  46. Galceran J, Farinas I, Depew MJ, Clevers H, Grosschedl R. Wnt3a-/-- like phenotype and limb deficiency in Lef1(-/-)Tcf1(-/-) mice. Genes Dev. 1999;13(6):709–17.PubMedGoogle Scholar
  47. Gaulden J, Reiter JF. Neur-ons and neur-offs: regulators of neural induction in vertebrate embryos and embryonic stem cells. Hum Mol Genet. 2008;17(R1):R60–6.PubMedGoogle Scholar
  48. Genest DR, Di Salvo D, Rosenblatt MJ, Holmes LB. Terminal transverse limb defects with tethering and omphalocele in a 17 week fetus following first trimester misoprostol exposure. Clin Dysmorphol. 1999;8(1):53–8.PubMedGoogle Scholar
  49. Genetos DC, Yellowley CE, Loots GG. Prostaglandin E2 signals through PTGER2 to regulate sclerostin expression. PLoS One. 2011;6(3):e17772.PubMedGoogle Scholar
  50. Ghanizadeh A, Akhondzadeh S, Hormozi, Makarem A, Abotorabi M, Firoozabadi A. Glutathione-related Factors and Oxidative Stress in Autism, a Review. Curr Med Chem. 2012;19(23):4000–5.PubMedGoogle Scholar
  51. Gilbert SF. Developmental biology. 7th ed. Sunderland: Sinauer Associates; 2003.Google Scholar
  52. Goessling W, North TE, Loewer S, et al. Genetic interaction of PGE2 and Wnt signaling regulates developmental specification of stem cells and regeneration. Cell. 2009;136(6):1136–47.PubMedGoogle Scholar
  53. Gorrindo P, Williams KC, Lee EB, Walker LS, McGrew SG, Levitt P. Gastrointestinal dysfunction in autism: parental report, clinical evaluation, and associated factors. Autism Res. 2012;5(2):101–8.PubMedGoogle Scholar
  54. Gross GA, Imamura T, Luedke C, et al. Opposing actions of prostaglandins and oxytocin determine the onset of murine labor. Proc Natl Acad Sci USA. 1998;95(20):11875–9.PubMedGoogle Scholar
  55. Guizy M, David M, Arias C, et al. Modulation of the atrial specific Kv1.5 channel by the n-3 polyunsaturated fatty acid, alpha-linolenic acid. J Mol Cell Cardiol. 2008;44(2):323–35.PubMedGoogle Scholar
  56. Haag M. Essential fatty acids and the brain. Can J Psychiatry. 2003;48(3):195–203.PubMedGoogle Scholar
  57. Hall AC, Lucas FR, Salinas PC. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. Cell. 2000;100(5):525–35.PubMedGoogle Scholar
  58. Harvey L, Boksa P. Prenatal and postnatal animal models of immune activation: Relevance to a range of neurodevelopmental disorders. Dev Neurobiol. Oct 2012;72(10):1335–48.PubMedGoogle Scholar
  59. Harvey RJ, Depner UB, Wassle H, et al. GlyR alpha3: an essential target for spinal PGE2-mediated inflammatory pain sensitization. Science. 2004;304(5672):884–7.PubMedGoogle Scholar
  60. Hinz B, Brune K. Cyclooxygenase-2 – 10 years later. J Pharmacol Exp Ther. 2002;300(2):367–75.PubMedGoogle Scholar
  61. Hoffman DR, Boettcher JA, Diersen-Schade DA. Toward optimizing vision and cognition in term infants by dietary docosahexaenoic and arachidonic acid supplementation: a review of randomized controlled trials. Prostaglandins Leukot Essent Fatty Acids. 2009;81(2–3):151–8.PubMedGoogle Scholar
  62. James SJ, Cutler P, Melnyk S, et al. Metabolic biomarkers of increased oxidative stress and impaired methylation capacity in children with autism. Am J Clin Nutr. 2004;80(6):1611–7.PubMedGoogle Scholar
  63. Jiang J, Ganesh T, Du Y, et al. Neuroprotection by selective allosteric potentiators of the EP2 prostaglandin receptor. Proc Natl Acad Sci USA. 2010;107(5):2307–12.PubMedGoogle Scholar
  64. Johnson SM, Hollander E. Evidence that eicosapentaenoic acid is effective in treating autism. J Clin Psychiatry. 2003;64(7):848–9.PubMedGoogle Scholar
  65. Jonakait GM, Ni L. Prostaglandins compromise basal forebrain cholinergic neuron differentiation and survival: action at EP1/3 receptors results in AIF-induced death. Brain Res. 2009;1285:30–41.PubMedGoogle Scholar
  66. Kaufmann WE, Worley PF, Taylor CV, Bremer M, Isakson PC. Cyclooxygenase-2 expression during rat neocortical development and in Rett syndrome. Brain Dev. 1997;19(1):25–34.PubMedGoogle Scholar
  67. Kitase Y, Barragan L, Qing H, et al. Mechanical induction of PGE2 in osteocytes blocks glucocorticoid-induced apoptosis through both the beta-catenin and PKA pathways. J Bone Miner Res. 2010;25(12):2657–68.PubMedGoogle Scholar
  68. Koch H, Huh SE, Elsen FP, et al. Prostaglandin E2-induced synaptic plasticity in neocortical networks of organotypic slice cultures. J Neurosci. 2010;30(35):11678–87.PubMedGoogle Scholar
  69. Kohane IS, McMurry A, Weber G, et al. The co-morbidity burden of children and young adults with autism spectrum disorders. PLoS One. 2012;7(4):e33224.PubMedGoogle Scholar
  70. Krey JF, Dolmetsch RE. Molecular mechanisms of autism: a possible role for Ca2+ signaling. Curr Opin Neurobiol. 2007;17(1):112–9.PubMedGoogle Scholar
  71. Kwiecien S, Konturek PC, Sliwowski Z, et al. Interaction between selective cyclooxygenase inhibitors and capsaicin-sensitive afferent sensory nerves in pathogenesis of stress-induced gastric lesions. Role of oxidative stress. J Physiol Pharmacol. 2012;63(2):143–51.PubMedGoogle Scholar
  72. Ladesich JB, Pottala JV, Romaker A, Harris WS. Membrane level of omega-3 docosahexaenoic acid is associated with severity of obstructive sleep apnea. J Clin Sleep Med. 2011;7(4):391–6.PubMedGoogle Scholar
  73. Lauritzen L, Hansen HS, Jorgensen MH, Michaelsen KF. The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina. Prog Lipid Res. 2001;40(1–2):1–94.PubMedGoogle Scholar
  74. Lawrence GD. The fats of life: essential fatty acids in health and disease. New Brunswick: Rutgers University Press; 2010.Google Scholar
  75. Legler DF, Bruckner M, Uetz-von Allmen E, Krause P. Prostaglandin E2 at new glance: novel insights in functional diversity offer therapeutic chances. Int J Biochem Cell Biol. 2010;42(2):198–201.PubMedGoogle Scholar
  76. Lennon PA, Cooper ML, Peiffer DA, et al. Deletion of 7q31.1 supports involvement of FOXP2 in language impairment: clinical report and review. Am J Med Genet A. 2007;143A(8):791–8.PubMedGoogle Scholar
  77. Libbey JE, Sweeten TL, McMahon WM, Fujinami RS. Autistic disorder and viral infections. J Neurovirol. 2005;11(1):1–10.PubMedGoogle Scholar
  78. Lin CJ, Chien SC, Chen CP. The use of misoprostol in termination of second-trimester pregnancy. Taiwan J Obstet Gynecol. 2011;50(3):275–82.PubMedGoogle Scholar
  79. Lin PI, Chien YL, Wu YY, et al. The WNT2 gene polymorphism associated with speech delay inherent to autism. Res Dev Disabil. 2012;33(5):1533–40.PubMedGoogle Scholar
  80. Liu XH, Kirschenbaum A, Weinstein BM, Zaidi M, Yao S, Levine AC. Prostaglandin E2 modulates components of the Wnt signaling system in bone and prostate cancer cells. Biochem Biophys Res Commun. 2010;394(3):715–20.PubMedGoogle Scholar
  81. Loftin CD, Tiano HF, Langenbach R. Phenotypes of the COX-deficient mice indicate physiological and pathophysiological roles for COX-1 and COX-2. Prostaglandins Other Lipid Mediat. 2002;68–69:177–85.PubMedGoogle Scholar
  82. Ma DQ, Cuccaro ML, Jaworski JM, et al. Dissecting the locus heterogeneity of autism: significant linkage to chromosome 12q14. Mol Psychiatry. 2007;12(4):376–84.PubMedGoogle Scholar
  83. Marin P, Hamon B, Glowinski J, Premont J. Nicotine-induced inhibition of neuronal phospholipase A2. J Pharmacol Exp Ther. 1997;280(3):1277–83.PubMedGoogle Scholar
  84. Martinez M. Tissue levels of polyunsaturated fatty acids during early human development. J Pediatr. 1992;120(4 Pt 2):S129–38.PubMedGoogle Scholar
  85. Meguid NA, Atta HM, Gouda AS, Khalil RO. Role of polyunsaturated fatty acids in the management of Egyptian children with autism. Clin Biochem. 2008;41(13):1044–8.PubMedGoogle Scholar
  86. Ming X, Johnson WG, Stenroos ES, Mars A, Lambert GH, Buyske S. Genetic variant of glutathione peroxidase 1 in autism. Brain Dev. 2010;32(2):105–9.PubMedGoogle Scholar
  87. Morales E, Bustamante M, Gonzalez JR, et al. Genetic variants of the FADS gene cluster and ELOVL gene family, colostrums LC-PUFA levels, breastfeeding, and child cognition. PLoS One. 2011;6(2):e17181.PubMedGoogle Scholar
  88. Morris CR, Agin MC. Syndrome of allergy, apraxia, and malabsorption: characterization of a neurodevelopmental phenotype that responds to omega 3 and vitamin E supplementation. Altern Ther Health Med. 2009;15(4):34–43.PubMedGoogle Scholar
  89. Mostafa GA, El-Hadidi ES, Hewedi DH, Abdou MM. Oxidative stress in Egyptian children with autism: relation to autoimmunity. J Neuroimmunol. 2010;219(1–2):114–8.PubMedGoogle Scholar
  90. Murakami M, Kudo I. Phospholipase A2. J Biochem. 2002;131(3):285–92.PubMedGoogle Scholar
  91. O'Neill GP, Ford-Hutchinson AW. Expression of mRNA for cyclooxygenase-1 and cyclooxygenase-2 in human tissues. FEBS Lett. 1993;330(2):156–60.PubMedGoogle Scholar
  92. Ono H, Sakamoto A, Sakura N. Plasma total glutathione concentrations in healthy pediatric and adult subjects. Clin Chim Acta. 2001;312(1–2):227–9.PubMedGoogle Scholar
  93. Oshima H, Oshima M. Mouse models of gastric tumors: Wnt activation and PGE2 induction. Pathol Int. 2010;60(9):599–607.PubMedGoogle Scholar
  94. Oshima H, Oguma K, Du YC, Oshima M. Prostaglandin E2, Wnt, and BMP in gastric tumor mouse models. Cancer Sci. 2009;100(10):1779–85.PubMedGoogle Scholar
  95. Patrick L, Salik R. The effect of essential fatty acid supplementation on language development and learning skills in autism and Asperger’s syndrome. Autism Asperger’s Digest. 2005; Jan–Feb:36–7.Google Scholar
  96. Pepicelli O, Fedele E, Berardi M, et al. Cyclo-oxygenase-1 and -2 differently contribute to prostaglandin E2 synthesis and lipid peroxidation after in vivo activation of N-methyl-D-aspartate receptors in rat hippocampus. J Neurochem. 2005;93(6):1561–7.PubMedGoogle Scholar
  97. Politi P, Cena H, Comelli M, et al. Behavioral effects of omega-3 fatty acid supplementation in young adults with severe autism: an open label study. Arch Med Res. 2008;39(7):682–5.PubMedGoogle Scholar
  98. Ponzio NM, Servatius R, Beck K, Marzouk A, Kreider T. Cytokine levels during pregnancy influence immunological profiles and neurobehavioral patterns of the offspring. Ann N Y Acad Sci. 2007;1107:118–28.PubMedGoogle Scholar
  99. Pratico D, Lawson JA, Rokach J, FitzGerald GA. The isoprostanes in biology and medicine. Trends Endocrinol Metab. 2001;12(6):243–7.PubMedGoogle Scholar
  100. Ricciotti E, FitzGerald GA. Prostaglandins and inflammation. Arterioscler Thromb Vasc Biol. 2011;31(5):986–1000.PubMedGoogle Scholar
  101. Rice D, Barone Jr S. Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ Health Perspect. 2000;108 Suppl 3:511–33.PubMedGoogle Scholar
  102. Rothwell NJ, Hopkins SJ. Cytokines and the nervous system. I: expression and recognition. Trends Neurosci. 1995;18(2):83–8.PubMedGoogle Scholar
  103. Russo I, Amornphimoltham P, Weigert R, Barlati S, Bosetti F. Cyclooxygenase-1 is involved in the inhibition of hippocampal neurogenesis after lipopolysaccharide-induced neuroinflammation. Cell Cycle. 2011;10(15):2568–73.PubMedGoogle Scholar
  104. Sahores M, Salinas PC. Activity-mediated synapse formation a role for Wnt-Fz signaling. Curr Top Dev Biol. 2011;97:119–36.PubMedGoogle Scholar
  105. Saint-Dizier M, Guyader-Joly C, Charpigny G, Grimard B, Humblot P, Ponter AA. Expression of enzymes involved in the synthesis of prostaglandin E2 in bovine in vitro-produced embryos. Zygote. 2011;19(3):277–83.PubMedGoogle Scholar
  106. Sang N, Chen C. Lipid signaling and synaptic plasticity. Neuroscientist. 2006;12(5):425–34.PubMedGoogle Scholar
  107. Sastry PS. Lipids of nervous tissue: composition and metabolism. Prog Lipid Res. 1985;24(2):69–176.PubMedGoogle Scholar
  108. Schultz ST, Klonoff-Cohen HS, Wingard DL, et al. Breastfeeding, infant formula supplementation, and autistic disorder: the results of a parent survey. Int Breastfeed J. 2006;1:16.PubMedGoogle Scholar
  109. Sedel F, Bechade C, Vyas S, Triller A. Macrophage-derived tumor necrosis factor alpha, an early developmental signal for motoneuron death. J Neurosci. 2004;24(9):2236–46.PubMedGoogle Scholar
  110. Shi L, Fatemi SH, Sidwell RW, Patterson PH. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci. 2003;23(1):297–302.PubMedGoogle Scholar
  111. Shi L, Smith SE, Malkova N, Tse D, Su Y, Patterson PH. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav Immun. 2009;23(1):116–23.PubMedGoogle Scholar
  112. Shukuri M, Takashima-Hirano M, Tokuda K, et al. In vivo expression of cyclooxygenase-1 in activated microglia and macrophages during neuroinflammation visualized by PET with 11C-ketoprofen methyl ester. J Nucl Med. 2011;52(7):1094–101.PubMedGoogle Scholar
  113. Shulman RG, Rothman DL, Behar KL, Hyder F. Energetic basis of brain activity: implications for neuroimaging. Trends Neurosci. 2004;27(8):489–95.PubMedGoogle Scholar
  114. Shultz SR, Macfabe DF, Martin S, et al. Intracerebroventricular injections of the enteric bacterial metabolic product propionic acid impair cognition and sensorimotor ability in the Long-Evans rat: further development of a rodent model of autism. Behav Brain Res. 2009;200(1):33–41.PubMedGoogle Scholar
  115. Sies H. Oxidative stress: oxidants and antioxidants. Exp Physiol. 1997;82(2):291–5.PubMedGoogle Scholar
  116. Sikora DM, Pettit-Kekel K, Penfield J, Merkens LS, Steiner RD. The near universal presence of autism spectrum disorders in children with Smith-Lemli-Opitz syndrome. Am J Med Genet A. 2006;140(14):1511–8.PubMedGoogle Scholar
  117. Sliwinski S, Croonenberghs J, Christophe A, Deboutte D, Maes M. Polyunsaturated fatty acids: do they have a role in the pathophysiology of autism? Neuro Endocrinol Lett. 2006;27(4):465–71.PubMedGoogle Scholar
  118. Soleymaninejadian E, Pramanik K, Samadian E. Immunomodulatory properties of mesenchymal stem cells: cytokines and factors. Am J Reprod Immunol. 2012;67(1):1–8.PubMedGoogle Scholar
  119. Stolp H, Neuhaus A, Sundramoorthi R, Molnar Z. The long and the short of it: gene and environment interactions during early cortical development and consequences for long-term neurological disease. Front Psychiatry. 2012;3:50.PubMedGoogle Scholar
  120. Su HM. Mechanisms of n-3 fatty acid-mediated development and maintenance of learning memory performance. J Nutr Biochem. 2010;21(5):364–73.PubMedGoogle Scholar
  121. Sugimoto Y, Narumiya S. Prostaglandin E receptors. J Biol Chem. 2007;282(16):11613–7.PubMedGoogle Scholar
  122. Tallberg T, Dabek J, Hallamaa R, Atroshi F. Lipidomics: the function of vital lipids in embryogenesis preventing autism spectrum disorders, treating sterile inflammatory diatheses with a lymphopoietic central nervous system component. J lipids. 2011;2011:137175.PubMedGoogle Scholar
  123. Tamiji J, Crawford DA. Misoprostol elevates intracellular calcium in neuro-2a cells via protein kinase a. Biochem Biophys Res Commun. 2010a;399(4):565–70.PubMedGoogle Scholar
  124. Tamiji J, Crawford DA. Prostaglandin E(2) and misoprostol induce neurite retraction in neuro-2a cells. Biochem Biophys Res Commun. 2010b;398(3):450–6.PubMedGoogle Scholar
  125. Tamiji J, Crawford DA. The neurobiology of lipid metabolism in autism spectrum disorders. Neurosignals. 2010c;18(2):98–112.PubMedGoogle Scholar
  126. Tassoni D, Kaur G, Weisinger RS, Sinclair AJ. The role of eicosanoids in the brain. Asia Pac J Clin Nutr. 2008;17 Suppl 1:220–8.PubMedGoogle Scholar
  127. Thomas RH, Foley KA, Mepham JR, Tichenoff LJ, Possmayer F, MacFabe DF. Altered brain phospholipid and acylcarnitine profiles in propionic acid infused rodents: further development of a potential model of autism spectrum disorders. J Neurochem. 2010;113(2):515–29.PubMedGoogle Scholar
  128. Tierney E, Bukelis I, Thompson RE, et al. Abnormalities of cholesterol metabolism in autism spectrum disorders. Am J Med Genet B Neuropsychiatr Genet. 2006;141B(6):666–8.PubMedGoogle Scholar
  129. Vancassel S, Durand G, Barthelemy C, et al. Plasma fatty acid levels in autistic children. Prostaglandins Leukot Essent Fatty Acids. 2001;65(1):1–7.PubMedGoogle Scholar
  130. Vane JR. Inhibition of prostaglandin synthesis as a mechanism of action for aspirin-like drugs. Nat New Biol. 1971;231(25):232–5.PubMedGoogle Scholar
  131. Wall R, Ross RP, Fitzgerald GF, Stanton C. Fatty acids from fish: the anti-inflammatory potential of long-chain omega-3 fatty acids. Nutr Rev. 2010;68(5):280–9.PubMedGoogle Scholar
  132. Wayman GA, Impey S, Marks D, et al. Activity-dependent dendritic arborization mediated by CaM-kinase I activation and enhanced CREB-dependent transcription of Wnt-2. Neuron. 2006;50(6):897–909.PubMedGoogle Scholar
  133. Wegiel J, Kuchna I, Nowicki K, et al. The neuropathology of autism: defects of neurogenesis and neuronal migration, and dysplastic changes. Acta Neuropathol. 2010;119(6):755–70.PubMedGoogle Scholar
  134. Wiest MM, German JB, Harvey DJ, Watkins SM, Hertz-Picciotto I. Plasma fatty acid profiles in autism: a case–control study. Prostaglandins Leukot Essent Fatty Acids. 2009;80(4):221–7.PubMedGoogle Scholar
  135. Willatts P, Forsyth JS, DiModugno MK, Varma S, Colvin M. Effect of long-chain polyunsaturated fatty acids in infant formula on problem solving at 10 months of age. Lancet. 1998;352(9129):688–91.PubMedGoogle Scholar
  136. Williams TA, Mars AE, Buyske SG, et al. Risk of autistic disorder in affected offspring of mothers with a glutathione S-transferase P1 haplotype. Arch Pediatr Adolesc Med. 2007;161(4):356–61.PubMedGoogle Scholar
  137. Wong C, Li H, Crawford DA. The role of prostaglandin E2 signaling pathway in neuroectodermal stem cell function. Poster# 151.08/V6. Society for Neuroscience – Annual Meeting; Sunday, 13 Nov 2011; 2011. Washington, DC.Google Scholar
  138. Wong C, Li H, Crawford DA. The implications of prostaglandin E2-wnt signaling pathway interaction in autism. Poster# 108.128. International meeting for autism research; Thursday, 17 May 2012; 2012, Toronto, Ontario, Canada.Google Scholar
  139. Wu A, Ying Z, Gomez-Pinilla F. Docosahexaenoic acid dietary supplementation enhances the effects of exercise on synaptic plasticity and cognition. Neuroscience. 2008;155(3):751–9.PubMedGoogle Scholar
  140. Yamagata K, Andreasson KI, Kaufmann WE, Barnes CA, Worley PF. Expression of a mitogen-inducible cyclooxygenase in brain neurons: regulation by synaptic activity and glucocorticoids. Neuron. 1993;11(2):371–86.PubMedGoogle Scholar
  141. Yao Y, Walsh WJ, McGinnis WR, Pratico D. Altered vascular phenotype in autism: correlation with oxidative stress. Arch Neurol. 2006;63(8):1161–4.PubMedGoogle Scholar
  142. Yehuda S, Rabinovitz S, Mostofsky DI. Essential fatty acids are mediators of brain biochemistry and cognitive functions. J Neurosci Res. 1999;56(6):565–70.PubMedGoogle Scholar
  143. Yoo HJ, Cho IH, Park M, et al. Association between PTGS2 polymorphism and autism spectrum disorders in Korean trios. Neurosci Res. 2008;62(1):66–9.PubMedGoogle Scholar
  144. Zerbo O, Iosif AM, Walker C, Ozonoff S, Hansen RL, Hertz-Picciotto I. Is Maternal Influenza or Fever During Pregnancy Associated with Autism or Developmental Delays? Results from the CHARGE (CHildhood Autism Risks from Genetics and Environment) Study. J Autism Dev Disord. Jan 2013;43(1):25–33.PubMedGoogle Scholar
  145. Zhang J, Rivest S. Anti-inflammatory effects of prostaglandin E2 in the central nervous system in response to brain injury and circulating lipopolysaccharide. J Neurochem. 2001;76(3):855–64.PubMedGoogle Scholar
  146. Zhou CJ, Zhao C, Pleasure SJ. Wnt signaling mutants have decreased dentate granule cell production and radial glial scaffolding abnormalities. J Neurosci. 2004;24(1):121–6.PubMedGoogle Scholar
  147. Zhou CJ, Borello U, Rubenstein JL, Pleasure SJ. Neuronal production and precursor proliferation defects in the neocortex of mice with loss of function in the canonical Wnt signaling pathway. Neuroscience. 2006;142(4):1119–31.PubMedGoogle Scholar
  148. Zhu Y, Yu T, Zhang XC, Nagasawa T, Wu JY, Rao Y. Role of the chemokine SDF-1 as the meningeal attractant for embryonic cerebellar neurons. Nat Neurosci. 2002;5(8):719–20.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Department of BiologyYork University, Faculty of HealthTorontoCanada
  2. 2.School of Kinesiology and Health Science, Neuroscience Diploma ProgramFaculty of Health, York UniversityTorontoCanada

Personalised recommendations