Elevated antibody binding to striatal cholinergic interneurons in patients with pediatric acute-onset neuropsychiatric syndrome

Brain Behav Immun. 2024 Nov:122:241-255. doi: 10.1016/j.bbi.2024.07.044. Epub 2024 Jul 30.

Abstract

Pediatric Acute-onset Neuropsychiatric Syndrome (PANS) is characterized by the abrupt onset of significant obsessive-compulsive symptoms (OCS) and/or severe food restriction, together with other neuropsychiatric manifestations. An autoimmune pathogenesis triggered by infection has been proposed for at least a subset of PANS. The older diagnosis of Pediatric Autoimmune Neuropsychiatric Disorder Associated with Streptococcus (PANDAS) describes rapid onset of OCD and/or tics associated with infection with Group A Streptococcus. The pathophysiology of PANS and PANDAS remains incompletely understood. We recently found serum antibodies from children with rigorously defined PANDAS to selectively bind to cholinergic interneurons (CINs) in the striatum. Here we examine this binding in children with relapsing and remitting PANS, a more heterogeneous condition, collected in a distinct clinical context from those examined in our previous work, from children with a clinical history of Streptococcus infection. IgG from PANS cases showed elevated binding to striatal CINs in both mouse and human brain. Patient plasma collected during symptom flare decreased a molecular marker of CIN activity, phospho-riboprotein S6, in ex vivo brain slices; control plasma did not. Neither elevated antibody binding to CINs nor diminished CIN activity was seen with plasma collected from the same children during remission. These findings replicate what we have seen previously in PANDAS and support the hypothesis that at least a subset of PANS cases have a neuroimmune pathogenesis. Given the critical role of CINs in modulating basal ganglia function, these findings confirm striatal CINs as a locus of interest in the pathophysiology of both PANS and PANDAS.

Keywords: Antibody binding; Cholinergic interneurons; Dorsal striatum; Neuronal activity; OCD; PANDAS; PANS; Phospho-rpS6; Plasma autoantibodies.

MeSH terms

  • Adolescent
  • Animals
  • Autoantibodies / immunology
  • Autoantibodies / metabolism
  • Autoimmune Diseases / immunology
  • Autoimmune Diseases / metabolism
  • Child
  • Child, Preschool
  • Cholinergic Neurons / metabolism
  • Corpus Striatum* / metabolism
  • Female
  • Humans
  • Immunoglobulin G / metabolism
  • Interneurons* / immunology
  • Interneurons* / metabolism
  • Male
  • Mice
  • Obsessive-Compulsive Disorder* / immunology
  • Obsessive-Compulsive Disorder* / metabolism
  • Streptococcal Infections* / immunology
  • Streptococcal Infections* / metabolism

Substances

  • Immunoglobulin G
  • Autoantibodies

Supplementary concepts

  • Pediatric acute-onset neuropsychiatric syndrome
  • Pediatric Autoimmune Neuropsychiatric Disorders Associated with Streptococcal infections