Advertisement

Antibody-mediated neuronal cell signaling in behavior and movement disorders

  • Christine A. Kirvan
    Affiliations
    Department of Biological Sciences, California State University, Sacramento, 6000 J Street, Sacramento, CA 95618-6077, USA
    Search for articles by this author
  • Susan E. Swedo
    Affiliations
    Pediatrics and Developmental Neuropsychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, 35 Convent Dr., BG 35 MSC 3710, Bethesda, MD 20814, USA
    Search for articles by this author
  • Lisa A. Snider
    Affiliations
    Pediatrics and Developmental Neuropsychiatry Branch, National Institute of Mental Health, National Institutes of Health, Department of Health and Human Services, 35 Convent Dr., BG 35 MSC 3710, Bethesda, MD 20814, USA
    Search for articles by this author
  • Author Footnotes
    1 Financial support: M.W.C holds grants from the National Heart, Lung, and Blood Institute (HL35280 and HL56267) and the Oklahoma Center for the Advancement of Science and Technology.
    Madeleine W. Cunningham
    Correspondence
    Corresponding author. Tel.: +1 405 271 3128; fax: +1 405 271 2217.
    Footnotes
    1 Financial support: M.W.C holds grants from the National Heart, Lung, and Blood Institute (HL35280 and HL56267) and the Oklahoma Center for the Advancement of Science and Technology.
    Affiliations
    Department of Microbiology and Immunology, University of Oklahoma, HSC, 975 N. E. 10th Street, Biomedical Research Center Room 217, Oklahoma City, OK 73104, USA
    Search for articles by this author
  • Author Footnotes
    1 Financial support: M.W.C holds grants from the National Heart, Lung, and Blood Institute (HL35280 and HL56267) and the Oklahoma Center for the Advancement of Science and Technology.

      Abstract

      Behavioral and movement disorders may have antibody responses where mimicry and signal transduction may lead to neuropsychiatric abnormalities. In our study, antibodies in pediatric autoimmune neuropsychiatric disorders associated with streptococci (PANDAS) reacted with the neuronal cell surface and caudate–putamen and induced calcium–calmodulin dependent protein (CaM) kinase II activity in neuronal cells. Depletion of serum IgG abrogated CaM kinase II cell signaling and reactivity of CSF was blocked by streptococcal antigen N-acetyl-beta-d-glucosamine (GlcNAc). Antibodies against GlcNAc in PANDAS sera were inhibited by lysoganglioside GM1. Results suggest that antibodies from an infection may signal neuronal cells in some behavioral and movement disorders.

      Keywords

      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Journal of Neuroimmunology
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Asbahr F.R.
        • Negrao A.B.
        • Gentil V.
        • Zanetta D.M.
        • da Paz J.A.
        • Marques-Dias M.J.
        • Kiss M.H.
        Obsessive–compulsive and related symptoms in children and adolescents with rheumatic fever with and without chorea: a prospective 6-month study.
        Am. J. Psychiatry. 1998; 155: 1122-1124
        • Asbahr F.R.
        • Ramos R.T.
        • Negrao A.B.
        • Gentil V.
        Case series: increased vulnerability to obsessive–compulsive symptoms with repeated episodes of Sydenham chorea.
        J. Am. Acad. Child Adolesc. Psych. 1999; 38: 1522-1525
        • Bejar R.
        • Yasuda R.
        • Krugers H.
        • Hood K.
        • Mayford M.
        Transgenic calmodulin-dependent protein kinase II activation: dose-dependent effects on synaptic plasticity, learning, and memory.
        J. Neurosci. 2002; 22: 5719-5726
        • Bronze M.S.
        • Dale J.B.
        Epitopes of streptococcal M protein that evoke antibodies that cross-react with human brain.
        J. Immunol. 1993; 151: 2820-2828
        • Chakrabarty K.
        • Bhattacharyya S.
        • Christopher R.
        • Khanna S.
        Glutamatergic dysfunction in OCD.
        Neuropsychopharmacology. 2005;
        • Cunningham M.W.
        Pathogenesis of group A streptococcal infections.
        Clin. Microbiol. Rev. 2000; 13: 470-511
        • De Koninck P.
        • Schulman H.
        Sensitivity of CaM kinase II to the frequency of Ca2+ oscillations.
        Science. 1998; 279: 227-230
        • Galvin J.E.
        • Hemric M.E.
        • Ward K.
        • Cunningham M.W.
        Cytotoxic mAb from rheumatic carditis recognizes heart valves and laminin.
        J. Clin. Invest. 2000; 106: 217-224
        • Garvey M.A.
        • Giedd J.
        • Swedo S.E.
        PANDAS: the search for environmental triggers of pediatric neuropsychiatric disorders. Lessons from rheumatic fever.
        J. Child Neurol. 1998; 13: 413-423
        • Garvey M.A.
        • Snider L.A.
        • Leitman S.F.
        • Werden R.
        • Swedo S.E.
        Treatment of Sydenham's chorea with intravenous immunoglobulin, plasma exchange, or prednisone.
        J. Child Neurol. 2005; 20: 424-429
        • Giedd J.N.
        • Rapoport J.L.
        • Kruesi M.J.P.
        • Parker C.
        • Schapiro M.B.
        • Allen A.J.
        • Leonard H.L.
        • Kaysen D.
        • Dickstein D.P.
        • Marsh W.L.
        • Kozuch P.L.
        • Vaituzis A.C.
        • Hamburger S.D.
        • Swedo S.E.
        Sydenham's chorea: magnetic resonance imaging of the basal ganglia.
        Neurology. 1995; 45: 2199-2202
        • Giedd J.N.
        • Rapoport J.L.
        • Leonard H.L.
        • Richter D.
        • Swedo S.E.
        Case study: acute basal ganglia enlargement and obsessive–compulsive symptoms in an adolescent boy.
        J. Am. Acad. Child Adolesc. Psych. 1996; 35: 913-915
        • Greengard P.
        • Valtorta F.
        • Czernik A.J.
        • Benfenati F.
        Synaptic vesicle phosphoproteins and regulation of synaptic function.
        Science. 1993; 259: 780-785
        • Griffith L.C.
        • Schulman H.
        The multifunctional Ca2+/calmodulin-dependent protein kinase mediates Ca2+-dependent phosphorylation of tyrosine hydroxylase.
        J. Biol. Chem. 1988; 263: 9542-9549
        • Huerta P.T.
        • Kowal C.
        • DeGiogio L.A.
        • Volpe B.T.
        • Diamond B.
        Immunity and behavior: antibodies alter emotion.
        Proc. Natl. Acad. Sci. U. S. A. 2006; 103: 678-683
        • Husby G.I.
        • Rijn v.d.
        • Zabriskie J.B.
        • Abdin A.H.
        • Williams R.C.
        Antibodies reacting with cytoplasm of subthalamic and caudate nuclei neurons in chorea and acute rheumatic fever.
        J. Exp. Med. 1976; 144: 1094-1110
        • Kirvan C.A.
        • Swedo S.E.
        • Heuser J.S.
        • Cunningham M.W.
        Mimicry and autoantibody-mediated neuronal cell signaling in Sydenham chorea.
        Nat. Med. 2003; 9: 914-920
        • Kurlan R.
        • Kaplan E.L.
        The pediatric autoimmune neuropsychiatric disorders associated with streptococcal infection (PANDAS) etiology for tics and obsessive–compulsive symptoms: hypothesis or entity? Practical considerations for the clinician.
        Pediatrics. 2004; 113: 883-886
        • Marques-Dias M.J.
        • Mercadante M.T.
        • Tucker D.
        • Lombroso P.
        Sydenham's chorea.
        in: Neuropsychiatry of the Basal Ganglia. vol. 20. 1997: 809
        • Menegon A.
        • Verderio C.
        • Leoni C.
        • Benfenati F.
        • Czernik A.J.
        • Greengard P.
        • Matteoli M.
        • Valtorta F.
        Spatial and temporal regulation of Ca2+/calmodulin-dependent protein kinase II activity in developing neurons.
        J. Neurosci. 2002; 22: 7016-7026
        • Mercadante M.T.
        • Busatto G.F.
        • Lombroso P.J.
        • Prado L.
        • Rosario-Campos M.C.
        • do Valle R.
        • Marques-Dias M.J.
        • Kiss M.H.
        • Leckman J.F.
        • Miguel E.C.
        The psychiatric symptoms of rheumatic fever.
        Am. J. Psychiatry. 2000; 157: 2036-2038
        • Perlmutter S.J.
        • Leitman S.F.
        • Garvey M.A.
        • Hamburger S.
        • Feldman E.
        • Leonard H.L.
        • Swedo S.E.
        Therapeutic plasma exchange and intravenous immunoglobulin for obsessive–compulsive disorder and tic disorders in childhood.
        Lancet. 1999; 354: 1153-1158
        • Shikhman A.R.
        • Greenspan N.S.
        • Cunningham M.W.
        A subset of mouse monoclonal antibodies cross-reactive with cytoskeletal proteins and group A streptococcal M proteins recognizes N-acetyl-beta-d-glucosamine.
        J. Immunol. 1993; 151: 3902-3913
        • Soderling T.R.
        • Chang B.
        • Brickey D.
        Cellular signaling through multifunctional Ca2+/calmodulin-dependent protein kinase II.
        J. Biol. Chem. 2001; 276: 3719-3722
        • Stollerman G.H.
        Rheumatic fever in the 21st century.
        Clin. Infect. Dis. 2001; 33: 806-814
        • Swedo S.E.
        Sydenham's chorea: a model of childhood autoimmune neuropsychiatric disorders.
        JAMA. 1994; 272: 1788-1791
        • Swedo S.E.
        • Rapoport J.L.
        • Cheslow D.L.
        • Leonard H.L.
        • Ayoub E.M.
        • Hosier D.M.
        • Wald E.R.
        High prevalence of obsessive–compulsive symptoms in patients with Sydenham's chorea.
        Am. J. Psychiatry. 1989; 146: 246
        • Swedo S.E.
        • Leonard H.L.
        • Schapiro M.B.
        • Casey B.J.
        • Mannheim G.B.
        • Lenane M.C.
        • Rettew D.C.
        Sydenham's chorea: physical and psychological symptoms of St Vitus dance.
        Pediatrics. 1993; 91: 706-713
        • Swedo S.E.
        • Leonard H.L.
        • Garvey M.
        • Mittleman B.
        • Allen A.J.
        • Perlmutter S.
        • Lougee L.
        • Dow S.
        • Zamkoff J.
        • Dubbert B.K.
        Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases.
        Am. J. Psychiatry. 1998; 155: 264-271
        • Swedo S.E.
        • Leonard H.L.
        • Garvey M.
        • Mittleman B.
        • Allen A.J.
        • Perlmutter S.
        • Lougee L.
        • Dow S.
        • Zamkoff J.
        • Dubbert B.K.
        Pediatric autoimmune neuropsychiatric disorders associated with streptococcal infections: clinical description of the first 50 cases.
        Am. J. Psychiatry. 1998; 155: 264-271
        • Taranta A.
        Relation of isolated recurrences of Sydenham's chorea to preceding streptococcal infections.
        N. Engl. J. Med. 1959; 260: 1204-1210
        • Taranta A.
        • Stollerman G.H.
        The relationship of Sydenham's chorea to infection with group A streptococci.
        Am. J. Med. 1956; 20: 170-175
        • Tsui J.
        • Inagaki M.
        • Schulman H.
        Calcium/calmodulin-dependent protein kinase II (CaMKII) localization acts in concert with substrate targeting to create spatial restriction for phosphorylation.
        J. Biol. Chem. 2005; 280: 9210-9216
        • Zhu G.
        • Okada M.
        • Yoshida S.
        • Hirose S.
        • Kaneko S.
        Pharmacological discrimination of protein kinase associated exocytosis mechanisms between dopamine and 3,4-dihydroxyphenylalanine in rat striatum using in vivo microdialysis.
        Neurosci. Lett. 2004; 363: 120-124