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Maternal neuronal antibodies associated with autism and a language disorder
Open accessAbstract
Neurodevelopmental disorders could be caused by maternal antibodies or other serum factors. We detected serum antibodies binding to rodent Purkinje cells and other neurons in a mother of three children: the first normal, the second with autism, and the third with a severe specific language disorder. We injected the serum (0.5–1.0ml/day) into pregnant mice during gestation and found altered exploration and motor coordination and changes in cerebellar magnetic resonance spectroscopy in the mouse offspring, comparing with offspring of mice injected with sera from mothers of healthy children. This evidence supports a role for maternal antibodies in some forms of neurodevelopmental disorder. Ann Neurol 2003;53:533–537
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“animal models have yielded many intriguing insights into the effects and mechanisms of inflammation and immune activation, as well as the role of toxic agents, in inducing autism-like behaviors in rodent and other species [103, 104, 112–115, 207].”
From The contribution of environmental exposure to the etiology of autism spectrum disorder (2019) · cites this paper as [112]
In the citing paper
“investigators injected maternal serum containing anti-brain antibodies into pregnant mice daily between E10 and E17, and observed reduced exploration and motor control in their offspring as compared with the offspring of untreated dams”
From The Role of the Immune System in Autism Spectrum Disorder (2017) · cites this paper as Dalton et al, 2003
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“Maternal autoantibodies may also aVect fetal brain development during critical periods of neurodevelopment in a subset of children with ASD (Ashwood and Van de Water 2004; Dalton et al. 2003; Singer et al. 2006).”
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Vincent, A. C., Dalton, P., Clover, L. M., Palace, J. A., & Lang, B. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb03137.x · Cited by 30
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“In a case-report, serum antibodies from a mother (Aut-M) of three children (eldest normal, second autistic and the third with severe language disorder) targeted the Purkinje neurons in rodent brains and when injected into pregnant mice caused altered exploration, motor coordination and cerebellar magnetic resonance sp…”
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Hoffmann, C., Zong, S., Mané-Damas, M., Molenaar, P. C., Losen, M. H., & Martínez‐Martínez, P. (2016) · Antibodies · doi:10.3390/antib5020009 · Cited by 30
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Mazón-Cabrera, R., Vandormael, P., & Somers, V. A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01474 · Cited by 29
“A direct functional role for these antibodies was also suggested, as passive transfer of serum of this mother in pregnant mice led to altered exploratory behavior in the pups (30).”
BackgroundAria, F., Bonini, S. A., Cattaneo, V., Premoli, M., Mastinu, A., Maccarinelli, G., & Memo, M. (2020) · Brain Sciences · doi:10.3390/brainsci10090620 · Cited by 28
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“In addition, both mice and monkeys exposed to antibodies from mothers of children with autism have demonstrated abnormal behavior suggesting a pathogenic nature for these antibodies [60–62].”
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“The serum contained antibodies that bound to fetal cerebellar neurons in rat tissue sections and impaired motor behavior in the adult mouse offspring of injected dams (117).”
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“[18] explored a maternal-fetal passive transfer model, administering serum from a mother of a child with ASD or pooled sera from mothers of a typically developed child into pregnant mice starting at gestational age E10.”
BackgroundTranslational Neuroscience Approaches to Understanding Autism
Veenstra-VanderWeele, J. M., O’Reilly, K. C., Dennis, M. Y., Uribe‐Salazar, J. M., & Amaral, D. G. (2023) · American Journal of Psychiatry · doi:10.1176/appi.ajp.20230153 · Cited by 25
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Maternal Antibody and ASD: Clinical Data and Animal Models
Gata-Garcia, A., & Diamond, B. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01129 · Cited by 22
“(79) showed that, when injected into pregnant mice, brain-reactive serum from a mother of a child with autism and a child with severe specific language disorder led to decreased exploration, deficient motor coordination, and altered cerebellar metabolites in the offspring compared to the offspring of mice given sera f…”
BackgroundNeuroimaging in Disorders of Social and Emotional Functioning: What Is the Question?
Herbert, M. R. (2004) · Journal of Child Neurology · doi:10.1177/08830738040190100701 · Cited by 21
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“We did not find differences in maternal or newborn specimens comparing children with DD to controls.”
ResultMartínez‐Martínez, P., Molenaar, P. C., Losen, M. H., Stevens, J., Baets, M. H. D., Szöke, A., Honnorat, J., Tamouza, R., Leboyer, M., van Os, J., et al. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00181 · Cited by 19
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“Recently, a strong association between maternal IgG antibodies reactive against proteins in fetal brain (MAU) and an outcome of autism in the child, has been independently identified by several groups [10, 11].”
BackgroundTrifonova, E. A., Мустафин, З. С., Lashin, S. A., & Kochetov, A. V. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23020967 · Cited by 19
“Injecting serum from a mother of an ASD child to pregnant mice resulted in offspring with altered cognitive abilities and motor coordination [25].”
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“(2003) [16] Plasma from a mother of an autistic child and a child with a severe specific language disorder injected into pregnant mouse dams: offspring displayed a slowed righting reflex, decreased exploration and decreased performance on the multiple static rods test.”
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“Western blot analysis and immunohistochemical studies have found evidence for the presence of antibodies in the plasma of some children with ASD that bind brain tissue (Cabanlit et al. 2007; Connolly et al. 1999; Dalton et al. 2003; Singer et al. 2006; Singh et al. 1997; Wills et al. 2009).”
Therapeutic properties of mesenchymal stem cells for autism spectrum disorders
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BackgroundMaternal Immune Activation, Cytokines and Autism
Patterson, P. H., Xu, W., Smith, S. E. P., & Devarman, B. E. (2008) · Humana Press eBooks · doi:10.1007/978-1-60327-489-0_13 · Cited by 17
“Interleukin-6 could also enhance the production of maternal antibodies, which could cross-react with the fetal brain, as has been proposed for autism [ 62 ] (see chapters by Singer and Van de Water).”
BackgroundPilot Study of Maternal Autoantibody–Related Autism
Angkustsiri, K., Fussell, J. J., Bennett, A., Schauer, J. D., Ramirez-Celis, A., Hansen, R. L., & de Water, J. V. (2022) · Journal of Developmental & Behavioral Pediatrics · doi:10.1097/dbp.0000000000001100 · Cited by 16
Childhood Serum Anti-Fetal Brain Antibodies Do Not Predict Autism
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“4 frontal cortex, cingulate gyrus, and cerebellum) [6-9], as well as behavioral changes in rodents after exposure to anti-Purkinje cell antibodies from the mother of an autistic child [10].”
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Self-citationImmunity and autoantibodies of a mouse strain with autistic-like behavior
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“ASD patients have higher levels of total IgG and brain Ag-specific autoAbs (Dalton et al., 2003; Wills et al., 2007).”
BackgroundOxidative stress and neuroimmune proteins in a mouse model of autism
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Pathogenesis of Autism: A Patchwork of Genetic Causes
Grigorenko, E. L. (2009) · Future Neurology · doi:10.2217/fnl.09.29 · Cited by 14
Autoantibodies in CNS Trauma and Neuropsychiatric Disorders: A New Generation of Biomarkers
Kobeissy, F. H. (2015) · CRC Press eBooks · doi:10.1201/b18126-36 · Cited by 14
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“Most of these antibodies are possibly directed at neuronal tissue [14].”
BackgroundIs ‘bench-to-bedside’ realistic for autism? An integrative neuroscience approach
Bauman, M. D., & Schumann, C. M. (2013) · Neuropsychiatry · doi:10.2217/npy.13.18 · Cited by 13
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TWO HYPOTHESES ON THE CAUSES OF MALE HOMOSEXUALITY AND PAEDOPHILIA
James, W. H. (2005) · Journal of Biosocial Science · doi:10.1017/s0021932005027173 · Cited by 12
Pre-autism: What a paediatrician should know about early diagnosis of autism
Al‐Beltagi, M. (2023) · World Journal of Clinical Pediatrics · doi:10.5409/wjcp.v12.i5.273 · Cited by 13
Autoimmune channelopathies: John Newsom-Davis's work and legacy
Vincent, A. C. (2008) · Journal of Neuroimmunology · doi:10.1016/j.jneuroim.2008.07.007 · Cited by 11
Self-citationAnimal Models of Autism Spectrum Disorder
Erdoğan, H. (2017) · Journal of Neurology & Stroke · doi:10.15406/jnsk.2017.06.00209 · Cited by 11
“It has been proposed that one cause of the disease is exposure of the fetal brain to maternal autoantibodies during pregnancy [62].”
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Therapeutic potential of CBD in Autism Spectrum Disorder
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Schlickmann, E., & Fortunato, J. J. (2013) · Jornal Brasileiro de Psiquiatria · doi:10.1590/s0047-20852013000200009 · Cited by 7
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“One proposed cause of ASDs is exposure of the fetal brain to maternal autoantibodies during pregnancy.(6) An etiologic role of maternal antibodies in ASDs is plausible due to the dynamics of the gestational transfer of maternal immunoglobulin G (IgG) during pregnancy.”
BackgroundLack of serum antineuronal antibodies in children with autism
Bayram, A. K., Kardaş, F., Demi̇rci̇, E., Gökahmetoğlu, S., Özmen, S., Canpolat, M., Öztop, D. B., Kumandaş, S., Gümüş, H., & Per, H. (2016) · Bratislavské lekárske listy/Bratislava medical journal · doi:10.4149/bll_2016_015 · Cited by 7
“Glutamic acid decarboxylase (GAD) enzyme is a catalyser in the conversion of L-glutamic acid to γ-amino butyric acid (GABA), which is an inhibitory neurotransmitter (5).”
Shao, W., Su, Y., Liu, J., Liu, Y., Zhao, J., & Fan, X. (2024) · Diabetes & Metabolism · doi:10.1016/j.diabet.2024.101543 · Cited by 6
“Research suggests that maternal autoimmune disease may increase the risk of ASD in offspring by affecting fetal neurodevelopment through inflammatory mediators and autoantibodies [121].”
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Lavrov, N. V., & Shabanov, P. D. (2018) · Reviews on Clinical Pharmacology and Drug Therapy · doi:10.17816/rcf16121-27 · Cited by 6
“модели аутизма, провоцируемого нарушениями развития в раннем онтогенезе Известно, что воздействие некоторых агентов в критические периоды во время беременности приводит к аутизму [28]: пренатальное введение этанола, вальпроевой кислоты (универсальное противо эпилептическое средство), талидомида (снотворное) и мизопрос…”
Inflammation and Neuroimmunity in the Pathogenesis of Autism
Pardo‐Villamizar, C., & Zimmerman, A. W. (2009) · CRC Press eBooks · doi:10.1201/9781420068870-c12 · Cited by 6
Heuer, L. S., Ashwood, P., & de Water, J. V. (2008) · Humana Press eBooks · doi:10.1007/978-1-60327-489-0_12 · Cited by 6
“In the original study by Dalton et al., the effects of such maternal antibodies on behavior were addressed in a mouse model [ 90 ].”
BackgroundInfluentialModeling Features of Autism in Animals
Patterson, P. H. (2006) · CRC Press eBooks · doi:10.1201/9781420004205-18 · Cited by 6
Relação entre hábito alimentar e síndrome do espectro autista
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“[31] hypothesize that, the maternal antibodies immunoglobulin G (IgG) in the mothers’ blood cross the placenta and enter into the fetus brain, react against fetal brain proteins and cause autism.”
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“…fetal brain antigens in the plasma samples of mothers with children diagnosed with autism has led to the hypothesis that maternal antibodies may contribute to the etiology (Bagnall-Moreau, Spielman, and Brimberg 2023; Braunschweig and Van De Water 2012; Croen et al. 2008; Dalton et al. 2003).”
Autoantibodies in CNS Trauma and Neuropsychiatric Disorders
Kobeissy, F. H., & Moshourab, R. A. (2015) · Cited by 4
Sobre o Autismo, Neuroinflamação e Modelos Animais para o Estudo de Autismo:
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“, 2008), and decreased orientation and exploratory behavior in rodents (Dalton et al., 2003).”
BackgroundNonhuman Primate Models for Autism Spectrum Disorders
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“Autoimmune attack to both mature and fetal cerebellar antigens has been described in several autoimmune diseases that affect humans, such as autism spectrum disorder [31, 32] and immune-mediated cerebellar ataxias [33].”
BackgroundImmune Involvement in Autism Spectrum Disorder as a Basis for Animal Models
Hsiao, E. Y. (2012) · Autism - Open Access · doi:10.4172/2165-7890.s1-003 · Cited by 2
Torr, J. J., & Lee, L. (2001) · Cambridge University Press eBooks · doi:10.1017/cbo9780511770715.007 · Cited by 2
Amaral, D. G., Rubenstein, J. L. R., & Rogers, S. J. (2008) · Wiley eBooks · doi:10.1002/9780470515167.ch23 · Cited by 2
Potential Autoepitope within the Extracellular Region of Contactin-Associated Protein-like 2 in Mice
Obregon, D. F., Zhu, Y., Bailey, A. R., Portis, S. M., Hou, H., Zeng, J., Stock, S. L., Murphy, T. K., Bengtson, M. A., & Tan, J. (2014) · Journal of Advances in Medicine and Medical Research · doi:10.9734/bjmmr/2014/6135 · Cited by 1
“Prior studies present compelling evidence of a role for the immune system in the pathogenesis of subsets of neurodevelopmental disorders [8-12,22,23,32-34].”
BackgroundCommon Sense - Its Development and Disorders 1
Smith, R. W. (2008) · Cited by 1
Immune Dysfunction in Autism Spectrum Disorder
Malkova, N. V., & Hsiao, E. Y. (2016) · Elsevier eBooks · doi:10.1016/b978-0-12-800109-7.00005-4 · Cited by 2
Kirsten, T. B. (2012) · Digital Library of Theses and Dissertations (Universidade de São Paulo) · doi:10.11606/t.10.2012.tde-25072013-142030 · Cited by 1
Bauman, M. D., Crawley, J. N., & Berman, R. F. (2019) · Wiley eBooks · doi:10.1002/9780470015902.a0022368.pub2 · Cited by 1
Is schizophrenia developmental adaptation to environmental menaces?
Goto, Y., & Lee, Y. (2011) · Medical Hypotheses · doi:10.1016/j.mehy.2011.07.031
“In addition, there have been studies confirming that transported maternal antibodies indeed reach to fetal forebrains in rodents [87,88].”
BackgroundAnticorps antineuronaux maternels et troubles spécifiques du développement
Chabrier, S. (2003) · Archives de Pédiatrie · doi:10.1016/j.arcped.2003.09.014
2006): Neuroimmunology of autism
Hu, Y.-Y., & Zhong, N. A. (2015)
The Gene-Environment Interaction in Asperger's Disorder
Johnson, M. E., Sanders, C., & Rausch, J. L. (2008) · Medical psychiatry · doi:10.3109/9780849383649.011
Maternal Autoantibodies in Autism Spectrum Disorder
Jones, K. L., & de Water, J. V. (2014) · WORLD SCIENTIFIC eBooks · doi:10.1142/9789814602167_0017
Maternal Brain-Reactive Antibodies and Autism Spectrum Disorder
Diamond, B. (2015)
Dhami, T., Jan, M., & Mohamed, A. (2021) · Undergraduate Research in Natural and Clinical Science and Technology (URNCST) Journal · doi:10.26685/urncst.214
“Between 1990 and 2008, only three new fetal medications had been licensed [15].”
BackgroundEyre, M., & Lim, M. J. (2021) · Brain Behavior and Immunity · doi:10.1016/j.bbi.2021.03.026
Is Autism Spectrum Disorder Related to Immune Dysfunction(s)?
Lejuste, F., Tamouza, R., & Leboyer, M. (2021) · Springer eBooks · doi:10.1007/978-3-030-71229-7_13
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Maternal Antibodies to Fetal Brain Neurons and Autism
Bagasra, O., Heggen, C., & Hossain, M. I. (2018) · Wiley eBooks · doi:10.1002/9781119042280.ch8
Krämer, P., & Bressan, P. (2017) · doi:10.31219/osf.io/k39mn
Autism, Gastrointestinal Disturbance, and Immune Dysfunction
Ashwood, P., Enstrom, A. M., & de Water, J. V. (2009) · CRC Press eBooks · doi:10.1201/9781420068870-c14 · Cited by 1
Glutamine in the cerebellum by magnetic resonance for the diagnosis of Autism
Sabrá, A., Filho, A. S., Sabrá, S., Bandeira, T. L., Mafra, I. C. B., & Werber-Bandeira, L. (2023) · GSC Advanced Research and Reviews · doi:10.30574/gscarr.2023.14.2.0366
“Cerebellar abnormalities are likely to contribute significantly to several of the clinical features of the autistic spectrum [24, 25].”
Metadata
- Authors
- Dalton, P., Deacon, R., Blamire, A., Pike, M., McKinlay, I., Stein, J., Styles, P., & Vincent, A.
- Affiliations
- University of Oxford (GB)
- John Radcliffe Hospital (GB)
- Venue
- Annals of Neurology
- Publisher
- Wiley
- Published
- 2003-03-24
- Volume
- 53
- Issue
- 4
- Pages
- 533-537
- ISSN
- 0364-5134 (ISSN-L)
- 1531-8249
- OpenAlex
- W2105371617
- Cited by
- 204
- References
- 20
- Citations by year
- 2025: 1 · 2024: 5 · 2023: 9 · 2022: 5 · 2021: 9 · 2020: 10 · 2019: 12 · 2018: 9 · 2017: 9 · 2016: 10 · 2015: 15 · 2014: 10 · 2013: 14 · 2012: 11
- FWCI
- 4.08
- Type
- journal article
- Language
- en
- Open access
- green
- doi.org
- Locations
- Annals of Neurology (publishedVersion)
- PubMed (publishedVersion)
- Newcastle University ePrints (Newcastle Univesity)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Autism Spectrum Disorder Research
- Health Sciences › Medicine › Clinical Neurology › Autoimmune Neurological Disorders and Treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- maternal antibodies, autism spectrum disorder, specific language impairment, Purkinje cells, cerebellum, neurodevelopmental disorders, mouse offspring, motor coordination, maternal-fetal immune transfer
- MeSH terms
- Adult, Animals, Autistic Disorder, Child, Dyslexia, Postural Balance, Female, Humans, Immunoglobulin G, Immunoglobulin M, Immunity, Maternally-Acquired, Magnetic Resonance Imaging, Male, Motor Activity, Magnetic Resonance Spectroscopy, Pregnancy, Purkinje Cells, Mice
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