Antibodies From Children With PANDAS Bind Specifically to Striatal Cholinergic Interneurons and Alter Their Activity
Objective:Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections, or PANDAS, describes such a situation after infection with Streptococcus pyogenes. PA...
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| Published in | The American journal of psychiatry Vol. 178; no. 1; pp. 48 - 64 |
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| Main Authors | , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
American Psychiatric Association
01.01.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | Objective:Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections, or PANDAS, describes such a situation after infection with Streptococcus pyogenes. PANDAS may result from induced autoimmunity against brain antigens, although this remains unproven. Pilot work suggests that IgG antibodies from children with PANDAS bind to cholinergic interneurons (CINs) in the striatum. CIN deficiency has been independently associated with tics in humans and with repetitive behavioral pathology in mice, making it a plausible locus of pathology. The authors sought to replicate and extend earlier work and to investigate the cellular effects of PANDAS antibodies on cholinergic interneurons.Methods:Binding of IgG to specific neurons in human and mouse brain slices was evaluated ex vivo after incubation with serum from 27 children with rigorously characterized PANDAS, both at baseline and after intravenous immunoglobulin (IVIG) treatment, and 23 matched control subjects. Binding was correlated with symptom measures. Neural activity after serum incubation was assessed in mouse slices using molecular markers and electrophysiological recording.Results:IgG from children with PANDAS bound to CINs, but not to several other neuron types, more than IgG from control subjects, in three independent cohorts of patients. Post-IVIG serum had reduced IgG binding to CINs, and this reduction correlated with symptom improvement. Baseline PANDAS sera decreased activity of striatal CINs, but not of parvalbumin-expressing GABAergic interneurons, and altered their electrophysiological responses, in acute mouse brain slices. Post-IVIG PANDAS sera and IgG-depleted baseline sera did not alter the activity of striatal CINs.Conclusions:These findings provide strong evidence for striatal CINs as a critical cellular target that may contribute to pathophysiology in children with rapid-onset OCD symptoms, and perhaps in other conditions. |
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| AbstractList | Objective:Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections, or PANDAS, describes such a situation after infection with Streptococcus pyogenes. PANDAS may result from induced autoimmunity against brain antigens, although this remains unproven. Pilot work suggests that IgG antibodies from children with PANDAS bind to cholinergic interneurons (CINs) in the striatum. CIN deficiency has been independently associated with tics in humans and with repetitive behavioral pathology in mice, making it a plausible locus of pathology. The authors sought to replicate and extend earlier work and to investigate the cellular effects of PANDAS antibodies on cholinergic interneurons.Methods:Binding of IgG to specific neurons in human and mouse brain slices was evaluated ex vivo after incubation with serum from 27 children with rigorously characterized PANDAS, both at baseline and after intravenous immunoglobulin (IVIG) treatment, and 23 matched control subjects. Binding was correlated with symptom measures. Neural activity after serum incubation was assessed in mouse slices using molecular markers and electrophysiological recording.Results:IgG from children with PANDAS bound to CINs, but not to several other neuron types, more than IgG from control subjects, in three independent cohorts of patients. Post-IVIG serum had reduced IgG binding to CINs, and this reduction correlated with symptom improvement. Baseline PANDAS sera decreased activity of striatal CINs, but not of parvalbumin-expressing GABAergic interneurons, and altered their electrophysiological responses, in acute mouse brain slices. Post-IVIG PANDAS sera and IgG-depleted baseline sera did not alter the activity of striatal CINs.Conclusions:These findings provide strong evidence for striatal CINs as a critical cellular target that may contribute to pathophysiology in children with rapid-onset OCD symptoms, and perhaps in other conditions. Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections, or PANDAS, describes such a situation after infection with Streptococcus pyogenes. PANDAS may result from induced autoimmunity against brain antigens, although this remains unproven. Pilot work suggests that IgG antibodies from children with PANDAS bind to cholinergic interneurons (CINs) in the striatum. CIN deficiency has been independently associated with tics in humans and with repetitive behavioral pathology in mice, making it a plausible locus of pathology. The authors sought to replicate and extend earlier work and to investigate the cellular effects of PANDAS antibodies on cholinergic interneurons.OBJECTIVEPediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections, or PANDAS, describes such a situation after infection with Streptococcus pyogenes. PANDAS may result from induced autoimmunity against brain antigens, although this remains unproven. Pilot work suggests that IgG antibodies from children with PANDAS bind to cholinergic interneurons (CINs) in the striatum. CIN deficiency has been independently associated with tics in humans and with repetitive behavioral pathology in mice, making it a plausible locus of pathology. The authors sought to replicate and extend earlier work and to investigate the cellular effects of PANDAS antibodies on cholinergic interneurons.Binding of IgG to specific neurons in human and mouse brain slices was evaluated ex vivo after incubation with serum from 27 children with rigorously characterized PANDAS, both at baseline and after intravenous immunoglobulin (IVIG) treatment, and 23 matched control subjects. Binding was correlated with symptom measures. Neural activity after serum incubation was assessed in mouse slices using molecular markers and electrophysiological recording.METHODSBinding of IgG to specific neurons in human and mouse brain slices was evaluated ex vivo after incubation with serum from 27 children with rigorously characterized PANDAS, both at baseline and after intravenous immunoglobulin (IVIG) treatment, and 23 matched control subjects. Binding was correlated with symptom measures. Neural activity after serum incubation was assessed in mouse slices using molecular markers and electrophysiological recording.IgG from children with PANDAS bound to CINs, but not to several other neuron types, more than IgG from control subjects, in three independent cohorts of patients. Post-IVIG serum had reduced IgG binding to CINs, and this reduction correlated with symptom improvement. Baseline PANDAS sera decreased activity of striatal CINs, but not of parvalbumin-expressing GABAergic interneurons, and altered their electrophysiological responses, in acute mouse brain slices. Post-IVIG PANDAS sera and IgG-depleted baseline sera did not alter the activity of striatal CINs.RESULTSIgG from children with PANDAS bound to CINs, but not to several other neuron types, more than IgG from control subjects, in three independent cohorts of patients. Post-IVIG serum had reduced IgG binding to CINs, and this reduction correlated with symptom improvement. Baseline PANDAS sera decreased activity of striatal CINs, but not of parvalbumin-expressing GABAergic interneurons, and altered their electrophysiological responses, in acute mouse brain slices. Post-IVIG PANDAS sera and IgG-depleted baseline sera did not alter the activity of striatal CINs.These findings provide strong evidence for striatal CINs as a critical cellular target that may contribute to pathophysiology in children with rapid-onset OCD symptoms, and perhaps in other conditions.CONCLUSIONSThese findings provide strong evidence for striatal CINs as a critical cellular target that may contribute to pathophysiology in children with rapid-onset OCD symptoms, and perhaps in other conditions. Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections, or PANDAS, describes such a situation after infection with . PANDAS may result from induced autoimmunity against brain antigens, although this remains unproven. Pilot work suggests that IgG antibodies from children with PANDAS bind to cholinergic interneurons (CINs) in the striatum. CIN deficiency has been independently associated with tics in humans and with repetitive behavioral pathology in mice, making it a plausible locus of pathology. The authors sought to replicate and extend earlier work and to investigate the cellular effects of PANDAS antibodies on cholinergic interneurons. Binding of IgG to specific neurons in human and mouse brain slices was evaluated ex vivo after incubation with serum from 27 children with rigorously characterized PANDAS, both at baseline and after intravenous immunoglobulin (IVIG) treatment, and 23 matched control subjects. Binding was correlated with symptom measures. Neural activity after serum incubation was assessed in mouse slices using molecular markers and electrophysiological recording. IgG from children with PANDAS bound to CINs, but not to several other neuron types, more than IgG from control subjects, in three independent cohorts of patients. Post-IVIG serum had reduced IgG binding to CINs, and this reduction correlated with symptom improvement. Baseline PANDAS sera decreased activity of striatal CINs, but not of parvalbumin-expressing GABAergic interneurons, and altered their electrophysiological responses, in acute mouse brain slices. Post-IVIG PANDAS sera and IgG-depleted baseline sera did not alter the activity of striatal CINs. These findings provide strong evidence for striatal CINs as a critical cellular target that may contribute to pathophysiology in children with rapid-onset OCD symptoms, and perhaps in other conditions. |
| Author | Leckman, James Fahey, Shaylyn Xu, Jian Frick, Luciana Liu, Rong-Jian Vaccarino, Flora Swedo, Susan Duman, Ronald S Williams, Kyle Pittenger, Christopher |
| AuthorAffiliation | 4 Department of Pediatrics, Yale University School of Medicine 2 Current address: Hunter James Kelly Research Institute, University at Buffalo 1 Department of Psychiatry, Yale University School of Medicine, 34 Park Street, New Haven, CT 06519 6 Current address: Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School 7 Pediatrics and Developmental Neuroscience Branch, National Institute of Mental Health 8 PANDAS Physicians Network 3 Child Study Center, Yale University School of Medicine 9 Interdepartmental Neuroscience Program, Yale University 5 Department of Neuroscience, Yale University School of Medicine |
| AuthorAffiliation_xml | – name: 4 Department of Pediatrics, Yale University School of Medicine – name: 1 Department of Psychiatry, Yale University School of Medicine, 34 Park Street, New Haven, CT 06519 – name: 9 Interdepartmental Neuroscience Program, Yale University – name: 2 Current address: Hunter James Kelly Research Institute, University at Buffalo – name: 7 Pediatrics and Developmental Neuroscience Branch, National Institute of Mental Health – name: 8 PANDAS Physicians Network – name: 6 Current address: Department of Psychiatry, Massachusetts General Hospital and Harvard Medical School – name: 3 Child Study Center, Yale University School of Medicine – name: 5 Department of Neuroscience, Yale University School of Medicine |
| Author_xml | – sequence: 1 givenname: Jian surname: Xu fullname: Xu, Jian email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 2 givenname: Rong-Jian surname: Liu fullname: Liu, Rong-Jian email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 3 givenname: Shaylyn surname: Fahey fullname: Fahey, Shaylyn email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 4 givenname: Luciana surname: Frick fullname: Frick, Luciana email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 5 givenname: James surname: Leckman fullname: Leckman, James email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 6 givenname: Flora surname: Vaccarino fullname: Vaccarino, Flora email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 7 givenname: Ronald S surname: Duman fullname: Duman, Ronald S email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 8 givenname: Kyle surname: Williams fullname: Williams, Kyle email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 9 givenname: Susan surname: Swedo fullname: Swedo, Susan email: christopher.pittenger@yale.edu, jian.xu@yale.edu – sequence: 10 givenname: Christopher surname: Pittenger fullname: Pittenger, Christopher email: christopher.pittenger@yale.edu, jian.xu@yale.edu |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32539528$$D View this record in MEDLINE/PubMed |
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| Keywords | PANS Basal Ganglia Obsessive-Compulsive Disorder PANDAS Cholinergic Interneuron Interneuron |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Author Contributions JX conducted immunohistochemistry, biochemistry, and image processing and performed data analysis, with support from SF; KW and SS provided serum samples; RJL performed electrophysiological experiments and analyzed electrophysiological data; FV provided human post-mortem tissue sections; RSD and LRF provided key intellectual contributions; CP supervised the study; JX and CP led manuscript writing; all authors contributed to data interpretation and manuscript preparation. |
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| Snippet | Objective:Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune... Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune neuropsychiatric... Objective: Pediatric obsessive-compulsive disorder (OCD) sometimes appears rapidly, even overnight, often after an infection. Pediatric autoimmune... |
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| SubjectTerms | Animals Antibodies Antigens Autoantibodies - immunology Autoimmune diseases Autoimmune Diseases - complications Autoimmune Diseases - immunology Brain Case-Control Studies Child Child, Preschool Children & youth Cholinergic Neurons - immunology Cholinergic Neurons - physiology Corpus Striatum - immunology Corpus Striatum - physiopathology Female Humans Immunoglobulin G - immunology Male Mice Mice, Inbred C57BL Mice, Transgenic Obsessive compulsive disorder Obsessive-Compulsive Disorder - complications Obsessive-Compulsive Disorder - etiology Obsessive-Compulsive Disorder - immunology Streptococcal Infections - complications Streptococcal Infections - immunology Streptococcus infections |
| Title | Antibodies From Children With PANDAS Bind Specifically to Striatal Cholinergic Interneurons and Alter Their Activity |
| URI | http://dx.doi.org/10.1176/appi.ajp.2020.19070698 https://www.ncbi.nlm.nih.gov/pubmed/32539528 https://www.proquest.com/docview/2485545117 https://www.proquest.com/docview/2413994690 https://pubmed.ncbi.nlm.nih.gov/PMC8573771 |
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