From molecules to neural morphology: Understanding neuroinflammation in autism spectrum condition

Molecular Autism

Volumn 7, Issue 1, 2016, Pages

  Young, Adam M H ^a,b   Chakrabarti, Bhismadev ^a,c   Roberts, David ^b   Lai, Meng Chuan ^a,d,e   Suckling, John ^f,g   Baron Cohen, Simon ^a,h  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

^d UNIVERSITY OF TORONTO   (Canada)

^e NATIONAL TAIWAN UNIVERSITY HOSPITAL   (Taiwan)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^g UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^h CAMBRIDGESHIRE AND PETERBOROUGH NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

Autism; Brain; Inflammation; NF B

Indexed keywords

COLLAPSIN RESPONSE MEDIATOR PROTEIN 1; COLLAPSIN RESPONSE MEDIATOR PROTEIN 2; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN G; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 8; LACTATE DEHYDROGENASE; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 3; MEMBRANE PROTEIN; MONOCYTE CHEMOTACTIC PROTEIN 1; POLYINOSINIC POLYCYTIDYLIC ACID; PROTEIN P52; STRESS INDUCED PHOSPHOPROTEIN 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 9; TRANSCRIPTION FACTOR RELA; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; UNINDEXED DRUG; Y BOX BINDING PROTEIN 1; AUTACOID; AUTOANTIBODY; CHEMOKINE; CYTOKINE; GLUTAMIC ACID; HLA ANTIGEN; LIPOPOLYSACCHARIDE; MEMBRANE ANTIGEN; NERVE PROTEIN;

AUTISM; BRAIN SIZE; CELL ACTIVATION; CELL STRUCTURE; FETOMATERNAL TRANSFUSION; GENE LOCUS; GENE MUTATION; GENE STRUCTURE; GENETIC ASSOCIATION; GENETIC RISK; HEREDITY; HUMAN; MAJOR HISTOCOMPATIBILITY COMPLEX; MICROGLIA; NERVOUS SYSTEM INFLAMMATION; NEUROIMAGING; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; AMNION FLUID; ANIMAL; BLOOD; BODY FLUID; BRAIN; BRAIN CHEMISTRY; CHEMISTRY; EMBRYOLOGY; FEMALE; GENETICS; GLIA; HAPLORHINI; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOUSE; PASSIVE IMMUNIZATION; PATHOLOGY; PHYSIOLOGY; PREGNANCY; PREGNANCY COMPLICATION; PRENATAL EXPOSURE; SIGNAL TRANSDUCTION;

AMNIOTIC FLUID; ANIMALS; ANTIGENS, SURFACE; AUTISM SPECTRUM DISORDER; AUTOANTIBODIES; BODY FLUIDS; BRAIN; BRAIN CHEMISTRY; CHEMOKINES; CYTOKINES; FEMALE; GLUTAMIC ACID; HAPLORHINI; HLA ANTIGENS; HUMANS; IMMUNITY, MATERNALLY-ACQUIRED; INFLAMMATION; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MATERNAL-FETAL EXCHANGE; MICE; NERVE TISSUE PROTEINS; NEUROGLIA; NEUROIMAGING; PREGNANCY; PREGNANCY COMPLICATIONS, INFECTIOUS; PRENATAL EXPOSURE DELAYED EFFECTS; SIGNAL TRANSDUCTION;

EID: 84955296337     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/s13229-016-0068-x     Document Type: Review

References (110)

1. Abdallah MW, Larsen N, Grove J, Bonefeld-Jørgensen EC, Nørgaard-Pedersen B, Hougaard DM, et al. Neonatal chemokine levels and risk of autism spectrum disorders: findings from a Danish historic birth cohort follow-up study. Cytokine. 2013;61(2):370-6. doi: 10.1016/j.cyto.2012.11.015.
2. Anderson AA, Ushakov DS, Ferenczi MA, Mori R, Martin P, Saffell JL. Morphoregulation by acetylcholinesterase in fibroblasts and astrocytes. J Cell Physiol. 2008;215(1):82-100.
3. Ashwood P, Enstrom A, Krakowiak P, Hertz-Picciotto I, Hansen RL, Croen LA, et al. Decreased transforming growth factor beta1 in autism: a potential link between immune dysregulation and impairment in clinical behavioral outcomes. J Neuroimmunol. 2008;204(1-2):149-53.
4. Balosso S, Ravizza T, Pierucci M, Calcagno E, Invernizzi R, Di Giovanni G, et al. Molecular and functional interactions between tumor necrosis factor-alpha receptors and the glutamatergic system in the mouse hippocampus: implications for seizure susceptibility. Neuroscience. 2009;161(1):293-300.
5. Baron-Cohen S. The extreme male brain theory of autism. Trends Cogn Sci. 2002;6(6):248-54.
6. Baron-Cohen S, Leslie AM, Frith U. Does the autistic child have a "theory of mind"? Cognition. 1985;21(1):37-46.
7. Bauman MD, Iosif AM, Ashwood P, Braunschweig D, Lee A, Schumann CM, et al. Maternal antibodies from mothers of children with autism alter brain growth and social behavior development in the rhesus monkey. Transl Psychiatry. 2013;3:e278. doi: 10.1038/tp.2013.47.
8. Becker KG. Autism, asthma, inflammation, and the hygiene hypothesis. Med Hypotheses. 2007;69(4):731-40.
9. Beart PM, O'Shea RD. Transporters for L-glutamate: an update on their molecular pharmacology and pathological involvement. Br J Pharmacol. 2007;150(1):5-17.
10. Bernardi S, Anagnostou E, Shen J, Kolevzon A, Buxbaum JD, Hollander E, et al. In vivo 1H-magnetic resonance spectroscopy study of the attentional networks in autism. Brain Res. 2011;1380:198-205.
11. Braunschweig D, Krakowiak P, Duncanson P, Boyce R, Hansen RL, Ashwood P, et al. Autism-specific maternal autoantibodies recognize critical proteins in developing brain. Transl Psychiatry. 2013;3:e277.
12. Braunschweig D, Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Croen LA, et al. Autism: maternally derived antibodies specific for fetal brain proteins. Neurotoxicology. 2008;29(2):226-31.
13. Brimberg L, Sadiq A, Gregersen PK, Diamond B. Brain-reactive IgG correlates with autoimmunity in mothers of a child with an autism spectrum disorder. Mol Psychiatry. 2013;18(11):1171-7.
14. Buehler MR. A proposed mechanism for autism: an aberrant neuroimmune response manifested as a psychiatric disorder. Med Hypotheses. 2011;76(6):863-70.
15. Camacho J, Jones K, Miller E, Ariza J, Noctor S, Van de Water J, et al. Embryonic intraventricular exposure to autism-specific maternal autoantibodies produces alterations in autistic-like stereotypical behaviors in offspring mice. Behav Brain Res. 2014;266:46-51. doi: 10.1016/j.bbr.2014.02.045.
16. Castedo M, Perfettini JL, Roumier T, Kroemer G. Cyclin-dependent kinase-1: linking apoptosis to cell cycle and mitotic catastrophe. Cell Death Differ. 2002;9(12):1287-93.
17. Chawarska K, Shic F, Macari S, Campbell DJ, Brian J, Landa R, et al. 18-month predictors of later outcomes in younger siblings of children with autism spectrum disorder: a baby siblings research consortium study. J Am Acad Child Adolesc Psychiatry. 2014;53(12):1317-27.
18. Chen JA, Peñagarikano O, Belgard TG, Swarup V, Geschwind DH. The emerging picture of autism spectrum disorder: genetics and pathology. Annu Rev Pathol. 2015;10:111-44.
19. Chien YL, Wu YY, Chen CH, Gau SS, Huang YS, Chien WH, et al. Association of HLA-DRB1 alleles and neuropsychological function in autism. Psychiatr Genet. 2012;22(1):46-9.
20. Clifford S, Dissanayake C, Bui QM, Huggins R, Taylor AK, Loesch DZ. Autism spectrum phenotype in males and females with fragile X full mutation and premutation. J Autism Dev Disord. 2007;37(4):738-47.
21. Courchesne E, Campbell K, Solso S. Brain growth across the life span in autism: age-specific changes in anatomical pathology. Brain Res. 2011;1380:138-45.
22. Courchesne E, Mouton PR, Calhoun ME, Semendeferi K, Ahrens-Barbeau C, Hallet MJ, et al. Neuron number and size in prefrontal cortex of children with autism. JAMA. 2011;306(18):2001-10.
23. Croen LA, Goines P, Braunschweig D, Yolken R, Yoshida CK, Grether JK, et al. Brain-derived neurotrophic factor and autism: maternal and infant peripheral blood levels in the Early Markers for Autism (EMA) Study. Autism Res. 2008;1(2):130-7.
24. Croen LA, Braunschweig D, Haapanen L, Yoshida CK, Fireman B, Grether JK, et al. Maternal mid-pregnancy autoantibodies to fetal brain protein: the early markers for autism study. Biol Psychiatry. 2008;64(7):583-8.
25. Cusco I, Medrano A, Gener B, Vilardell M, Gallastegui F, Villa O, et al. Autism-specific copy number variants further implicate the phosphatidylinositol signaling pathway and the glutamatergic synapse in the etiology of the disorder. Hum Mol Genet. 2009;18(10):1795-804.
26. Deitmer JW, Broer A, Broer S. Glutamine efflux from astrocytes is mediated by multiple pathways. J Neurochem. 2003;87(1):127-35.
27. Deverman BE, Patterson PH. Cytokines and CNS development. Neuron. 2009;64(1):61-78.
28. DeVito TJ, Drost DJ, Neufeld RW, Rajakumar N, Pavlosky W, Williamson P, et al. Evidence for cortical dysfunction in autism: a proton magnetic resonance spectroscopic imaging study. Biol Psychiatry. 2007;61(4):465-73.
29. DSM-IV® Sourcebook (1994) American Psychiatric Association. ISBN 978-0-89042-025-6.
30. DSM-V® Sourcebook (2013) American Psychiatric Association. ISBN 978-0-89042-065-2
31. Doshi-Velez F, Ge Y, Kohane I. Comorbidity clusters in autism spectrum disorders: an electronic health record time-series analysis. Pediatrics. 2014;133(1):e54-63. doi: 10.1542/peds.2013-0819.
32. Engstrom M, Karlsson R, Jonsson JI. Inactivation of the forkhead transcription factor FoxO3 is essential for PKB-mediated survival of hematopoietic progenitor cells by kit ligand. Exp Hematol. 2003;31(4):316-23.
33. Enstrom AM, Onore CE, Van de Water JA, Ashwood P. Differential monocyte responses to TLR ligands in children with autism spectrum disorders. Brain Behav Immun. 2010;24(1):64-71.
34. Fatemi SH, Stary JM, Halt AR, Realmuto GR. Dysregulation of Reelin and Bcl-2 proteins in autistic cerebellum. J Autism Dev Disord. 2001;31(6):529-35.
35. Frith U. A new look at language and communication in autism. Br J Disord Commun. 1989;24(2):123-50.
36. Fujii E, Mori K, Miyazaki M, Hashimoto T, Harada M, Kagami S. Function of the frontal lobe in autistic individuals: a proton magnetic resonance spectroscopic study. J Med Invest. 2010;57(1-2):35-44.
37. Gabis L, Wei H, Azizian A, DeVincent C, Tudorica A, Kesner-Baruch Y, et al. 1H-magnetic resonance spectroscopy markers of cognitive and language ability in clinical subtypes of autism spectrum disorders. J Child Neurol. 2008;23(7):766-74.
38. Gao YX, Cai FC. Experimental study on the therapeutic mechanism of high dose intravenous immunoglobulin in treatment of immune-mediated peripheral neuropathy. Zhonghua Er Ke Za Zhi. 2003;41(9):684-7.
39. Garty BZ, Ludomirsky A, Danon YL, Peter JB, Douglas SD. Placental transfer of immunoglobulin G subclasses. Clin Diagn Lab Immunol. 1994;1(6):667-9.
40. Gaugler T, Klei L, Sanders SJ, Bodea CA, Goldberg AP, Lee AB, et al. Most genetic risk for autism resides with common variation. Nat Genet. 2014;46(8):881-5.
41. Geschwind DH, Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol. 2007;17(1):103-11.
42. Geschwind DH, State MW. Gene hunting in autism spectrum disorder: on the path to precision medicine. Lancet Neurol. 2015;16.
43. Ghosh S, Karin M. Missing pieces in the NF-kappaB puzzle. Cell. 2002;109(Suppl):S81-96.
44. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol. 1998;16:225-60.
45. Goines PE, Croen LA, Braunschweig D, Yoshida CK, Grether J, Hansen R, et al. Increased midgestational IFN-gamma, IL-4 and IL-5 in women bearing a child with autism: a case-control study. Mol Autism. 2011;2:13-2392-2-13.
46. Happé F, Frith U. The weak coherence account: detail-focused cognitive style in autism spectrum disorders. J Autism Dev Disord. 2006;36(1):5-25. Review.
47. Hay N, Sonenberg N. Upstream and downstream of mTOR. Genes Dev. 2004;18(16):1926-45.
48. Herman GE, Butter E, Enrile B, Pastore M, Prior TW, Sommer A. Increasing knowledge of PTEN germline mutations: two additional patients with autism and macrocephaly. Am J Med Genet A. 2007;143(6):589-93.
49. Herman GE, Henninger N, Ratliff-Schaub K, Pastore M, Fitzgerald S, McBride KL. Genetic testing in autism: how much is enough? Genet Med. 2007;9(5):268-74.
50. Hertz L. The astrocyte-neuron lactate shuttle: a challenge of a challenge. J Cereb Blood Flow Metab. 2004;24(11):1241-8.
51. 1H]MRS study. Transl Psychiatry. 2013;3:e279.
52. Hsiao EY, McBride SW, Hsien S, Sharon G, Hyde ER, McCue T, et al. Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell. 2013;155(7):1451-63.
53. Hu S, Sheng WS, Ehrlich LC, Peterson PK, Chao CC. Cytokine effects on glutamate uptake by human astrocytes. Neuroimmunomodulation. 2000;7(3):153-9.
54. Hu W, Zhang C, Wu R, Sun Y, Levine A, Feng Z. Glutaminase 2, a novel p53 target gene regulating energy metabolism and antioxidant function. Proc Natl Acad Sci U S A. 2010;107(16):7455-60.
55. Johnson WG, Buyske S, Mars AE, Sreenath M, Stenroos ES, Williams TA, et al. HLA-DR4 as a risk allele for autism acting in mothers of probands possibly during pregnancy. Arch Pediatr Adolesc Med. 2009;163(6):542-6.
56. Jyonouchi H, Sun S, Itokazu N. Innate immunity associated with inflammatory responses and cytokine production against common dietary proteins in patients with autism spectrum disorder. Neuropsychobiology. 2002;46(2):76-84.
57. Kern KL. The possible role of the cerebellum in autism/PDD: disruption of a multisensory feedback loop. Med Hypotheses. 2002;59(3):255-60.
58. Klauck SM. Genetics of autism spectrum disorder. Eur J Hum Genet. 2006;14(6):714-20.
59. Knuesel I, Chicha L, Britschgi M, Schobel SA, Bodmer M, Hellings JA, et al. Maternal immune activation and abnormal brain development across CNS disorders. Nat Rev Neurol. 2014;10(11):643-60.
60. Lai MC, Lombardo MV, Chakrabarti B, Baron-Cohen S. Subgrouping the autism "spectrum": reflections on DSM-5. PLoS Biol. 2013;11(4):e1001544.
61. Lee A, Pow DV. Astrocytes: glutamate transport and alternate splicing of transporters. Int J Biochem Cell Biol. 2010;42(12):1901-6.
62. Lee H, Brott BK, Kirkby LA, Adelson JD, Cheng S, Feller MB, et al. Synapse elimination and learning rules co-regulated by MHC class I H2-Db. Nature. 2014;509(7499):195-200.
63. Lin D, Smith MA, Champagne C, Elter J, Beck J, Offenbacher S. Porphyromonas gingivalis infection during pregnancy increases maternal tumor necrosis factor alpha, suppresses maternal interleukin-10, and enhances fetal growth restriction and resorption in mice. Infect Immun. 2003;71(9):5156-62.
64. Malik M, Tauqeer Z, Sheikh AM, Wen G, Nagori A, Yang K, et al. NF-κB signaling in the brain of autistic subjects. Mediators Inflamm. 2011;2011:785265. doi: 10.1155/2011/785265. Erratum in: Mediators Inflamm. 2013;2013:691975.
65. Martin LA, Ashwood P, Braunschweig D, Cabanlit M, Van de Water J, Amaral DG. Stereotypies and hyperactivity in rhesus monkeys exposed to IgG from mothers of children with autism. Brain Behav Immun. 2008;22(6):806-16.
66. Masi A, Quintana DS, Glozier N, Lloyd AR, Hickie IB, Guastella AJ. Cytokine aberrations in autism spectrum disorder: a systematic review and meta-analysis. Mol Psychiatry. 2015;20(4):440-6.
67. McAllister AK. Major histocompatibility complex I in brain development and schizophrenia. Biol Psychiatry. 2014;75(4):262-8.
68. Mondino A, Mueller DL. mTOR at the crossroads of T cell proliferation and tolerance. Semin Immunol. 2007;19(3):162-72.
69. Morgan JT, Chana G, Pardo CA, Achim C, Semendeferi K, Buckwalter J, et al. Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism. Biol Psychiatry. 2010;68(4):368-76.
70. Murdoch JD, State MW. Recent developments in the genetics of autism spectrum disorders. Curr Opin Genet Dev. 2013;23(3):310-5.
71. Naik US, Gangadharan C, Abbagani K, Nagalla B, Dasari N, Manna SK. A study of nuclear transcription factor-kappa B in childhood autism. PLoS ONE. 2011;6(5):e19488.
72. Neuhaus E, Beauchaine TP, Bernier R. Neurobiological correlates of social functioning in autism. Clin Psychol Rev. 2010;30(6):733-48.
73. Nordahl CW, Lange N, Li DD, Barnett LA, Lee A, Buonocore MH, et al. Brain enlargement is associated with regression in preschool-age boys with autism spectrum disorders. Proc Natl Acad Sci U S A. 2011;108(50):20195-200. doi: 10.1073/pnas.1107560108.
74. Nordahl CW, Scholz R, Yang X, Buonocore MH, Simon T, Rogers S, et al. Increased rate of amygdala growth in children aged 2 to 4 years with autism spectrum disorders: a longitudinal study. Arch Gen Psychiatry. 2012;69(1):53-61.
75. O'Dushlaine & The Network and Pathway Analysis Subgroup of the Psychiatric Genomics Consortium. Psychiatric genome-wide association study analyses implicate neuronal, immune and histone pathways. Nat Neurosci. 2015;18:199-209.
76. Ozonoff S, Rogers SJ, Farnham JM, Pennington BF. Can standard measures identify subclinical markers of autism? J Autism Dev Disord. 1993;23(3):429-41.
77. Pahl HL. Activators and target genes of Rel/NF-kappaB transcription factors. Oncogene. 1999;18(49):6853-66.
78. Paolicelli RC, Gross CT. Microglia in development: linking brain wiring to brain environment. Neuron Glia Biol. 2011;7(1):77-83.
79. Pardo CA, Vargas DL, Zimmerman AW. Immunity, neuroglia and neuroinflammation in autism. Int Rev Psychiatry. 2005;17(6):485-95.
80. Patterson PH. Immune involvement in schizophrenia and autism: etiology, pathology, and animal models. Behav Brain Res. 2008;12:121-8.
81. Perkins ND. NF-kappaB: tumor promoter or suppressor? Trends Cell Biol. 2004;14(2):64-9.
82. Plaisted K, O'Riordan M, Baron-Cohen S. Enhanced visual search for a conjunctive target in autism: a research note. J Child Psychol Psychiatry. 1998;39:777-83.
83. Plaisted K, O'Riordan M, Baron-Cohen S. Enhanced discrimination of novel, highly similar stimuli by adults with autism during a perceptual learning task. J Child Psychol Psychiatry. 1998;39:765-75.
84. Prabowo AS, Iyer AM, Anink JJ, Spliet WG, Rijen PC, Aronica E. Differential expression of major histocompatibility complex class I in developmental glioneuronal lesions. J Neuroinflammation. 2013;10:12.
85. Pramparo T, Pierce K, Lombardo MV, Carter Barnes C, Marinero S, Ahrens-Barbeau C, et al. Prediction of autism by translation and immune/inflammation coexpressed genes in toddlers from pediatric community practices. JAMA Psychiatry. 2015;72(4):386-94.
86. Sacco R, Militerni R, Frolli A, Bravaccio C, Gritti A, Elia M, et al. Clinical, morphological, and biochemical correlates of head circumference in autism. Biol Psychiatry. 2007;62(9):1038-47.
87. Sadiq FA, Slator L, Skuse D, Law J, Gillberg C, Minnis H. Social use of language in children with reactive attachment disorder and autism spectrum disorders. Eur Child Adolesc Psychiatry. 2012;21(5):267-76.
88. Sauer S, Bruno L, Hertweck A, Finlay D, Leleu M, Spivakov M, et al. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc Natl Acad Sci U S A. 2008;105(22):7797-802.
89. Schumann CM, Nordahl CW. Bridging the gap between MRI and postmortem research in autism. Brain Res. 2011;1380:175-86.
90. Schwarz E, Guest PC, Rahmoune H, Wang L, Levin Y, Ingudomnukul E, et al. Sex-specific serum biomarker patterns in adults with Asperger's syndrome. Mol Psychiatry. 2011;16(12):1213-20.
91. Shin JW, Nguyen KT, Pow DV, Knight T, Buljan V, Bennett MR, et al. Distribution of glutamate transporter GLAST in membranes of cultured astrocytes in the presence of glutamate transport substrates and ATP. Neurochem Res. 2009;34(10):1758-66.
92. Shatz CJ. MHC class I: an unexpected role in neuronal plasticity. Neuron. 2009;64(1):40-5.
93. Singer HS, Morris C, Gause C, Pollard M, Zimmerman AW, Pletnikov M. Prenatal exposure to antibodies from mothers of children with autism produces neurobehavioral alterations: a pregnant dam mouse model. J Neuroimmunol. 2009;211(1-2):39-48.
94. Singh B, Bera NK, De S, Nayak C, Chaudhuri TK. Study of HLA class I gene in Indian schizophrenic patients of Siliguri, West Bengal. Psychiatry Res. 2011;189(2):215-9.
95. Steeb H, Ramsey JM, Guest PC, Stocki P, Cooper JD, Rahmoune H, et al. Serum proteomic analysis identifies sex-specific differences in lipid metabolism and inflammation profiles in adults diagnosed with Asperger syndrome. Mol Autism. 2014;5(1):4. doi: 10.1186/2040-2392-5-4.
96. Stubbs EG, Budden SS, Jackson RH, Terdal LG, Ritvo ER. Effects of fenfluramine on eight outpatients with the syndrome of autism. Dev Med Child Neurol. 1986;28(2):229-35.
97. Stubbs EG, Ritvo ER, Mason-Brothers A. Autism and shared parental HLA antigens. J Am Acad Child Psychiatry. 1985;24(2):182-5.
98. Suzuki K, Matsuzaki H, Iwata K, Kameno Y, Shimmura C, Kawai S, et al. Plasma cytokine profiles in subjects with high-functioning autism spectrum disorders. PLoS ONE. 2011;6(5):e20470.
99. Tabuchi K, Blundell J, Etherton MR, Hammer RE, Liu X, Powell CM. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science. 2007;318:71-6.
100. Tincani A, Rebaioli CB, Frassi M, Taglietti M, Gorla R, Cavazzana I, et al. Pregnancy and autoimmunity: maternal treatment and maternal disease influence on pregnancy outcome. Autoimmun Rev. 2005;4(7):423-8.
101. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol. 2005;57(1):67-81.
102. Voineagu I, Wang X, Johnston P, Lowe JK, Tian Y, Horvath S, et al. Transcriptomic analysis of autistic brain reveals convergent molecular pathology. Nature. 2011;474(7351):380-4.
103. Voineagu I, Eapen V. Converging pathways in autism spectrum disorders: interplay between synaptic dysfunction and immune responses. Front Hum Neurosci. 2013;7:738.
104. Warren RP, Cole P, Odell JD, Pingree CB, Warren WL, White E, et al. Detection of maternal antibodies in infantile autism. J Am Acad Child Adolesc Psychiatry. 1990;29(6):873-7.
105. Williams PG, Hersh JH. Brief report: the association of neurofibromatosis type 1 and autism. J Autism Dev Disord. 1998;28(6):567-71.
106. Wiznitzer M. Autism and tuberous sclerosis. J Child Neurol. 2004;19(9):675-9.
107. Young AM, Campbell E, Lynch S, Suckling J, Powis SJ. Aberrant NF-kappaB expression in autism spectrum condition: a mechanism for neuroinflammation. Front Psychiatry. 2011;2:27.
108. Young AM, Campbell E, Lynch S, Dunn M, Powis SJ. TNF-α induction of murine brain inflammation via IKK/NF kappa B signalling: a potential model for autism. PLoS ONE. 2012;7(6):e39049.
109. Zimmerman AW, Connors SL, Matteson KJ, Lee LC, Singer HS, Castaneda JA, et al. Maternal antibrain antibodies in autism. Brain Behav Immun. 2007;21(3):351-7.
110. Zimmerman AW, Jyonouchi H, Comi AM, Connors SL, Milstien S, Varsou A, et al. Cerebrospinal fluid and serum markers of inflammation in autism. Pediatr Neurol. 2005;33(3):195-201.