Stiff person syndrome-associated autoantibodies to amphiphysin mediate reduced GABAergic inhibition

Synaptic inhibition is a central factor in the fine tuning of neuronal activity in the central nervous system. Symptoms consistent with reduced inhibition such as stiffness, spasms and anxiety occur in paraneoplastic stiff person syndrome with autoantibodies against the intracellular synaptic protei...

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Hauptverfasser: Geis, Christian (VerfasserIn) , Weishaupt, Andreas (VerfasserIn) , Hallermann, Stefan (VerfasserIn) , Grünewald, Benedikt (VerfasserIn) , Wessig, Carsten (VerfasserIn) , Wultsch, Thomas (VerfasserIn) , Reif, Andreas (VerfasserIn) , Byts, Nadiya (VerfasserIn) , Beck, Marcus (VerfasserIn) , Jablonka, Sibylle (VerfasserIn) , Boettger, Michael K. (VerfasserIn) , Üçeyler, Nurcan (VerfasserIn) , Fouquet, Wernher (VerfasserIn) , Gerlach, Manfred (VerfasserIn) , Meinck, Hans-Michael (VerfasserIn) , Sirén, Anna-Leena (VerfasserIn) , Sigrist, Stephan J. (VerfasserIn) , Toyka, Klaus Viktor (VerfasserIn) , Heckmann, Manfred (VerfasserIn) , Sommer, Claudia (VerfasserIn)
Dokumenttyp: Article (Journal)
Sprache:Englisch
Veröffentlicht: 30 September 2010
In: Brain
Year: 2010, Jahrgang: 133, Heft: 11, Pages: 3166-3180
ISSN:1460-2156
Online-Zugang: Volltext
Verfasserangaben:Christian Geis, Andreas Weishaupt, Stefan Hallermann, Benedikt Grünewald, Carsten Wessig, Thomas Wultsch, Andreas Reif, Nadiya Byts, Marcus Beck, Sibylle Jablonka, Michael K. Boettger, Nurcan Üçeyler, Wernher Fouquet, Manfred Gerlach, Hans-Michael Meinck, Anna-Leena Sirén, Stephan J. Sigrist, Klaus V. Toyka, Manfred Heckmann and Claudia Sommer

MARC

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245 1 0 |a Stiff person syndrome-associated autoantibodies to amphiphysin mediate reduced GABAergic inhibition  |c Christian Geis, Andreas Weishaupt, Stefan Hallermann, Benedikt Grünewald, Carsten Wessig, Thomas Wultsch, Andreas Reif, Nadiya Byts, Marcus Beck, Sibylle Jablonka, Michael K. Boettger, Nurcan Üçeyler, Wernher Fouquet, Manfred Gerlach, Hans-Michael Meinck, Anna-Leena Sirén, Stephan J. Sigrist, Klaus V. Toyka, Manfred Heckmann and Claudia Sommer 
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520 |a Synaptic inhibition is a central factor in the fine tuning of neuronal activity in the central nervous system. Symptoms consistent with reduced inhibition such as stiffness, spasms and anxiety occur in paraneoplastic stiff person syndrome with autoantibodies against the intracellular synaptic protein amphiphysin. Here we show that intrathecal application of purified anti-amphiphysin immunoglobulin G antibodies induces stiff person syndrome-like symptoms in rats, including stiffness and muscle spasms. Using in vivo recordings of Hoffmann reflexes and dorsal root potentials, we identified reduced presynaptic GABAergic inhibition as an underlying mechanism. Anti-amphiphysin immunoglobulin G was internalized into neurons by an epitope-specific mechanism and colocalized in vivo with presynaptic vesicular proteins, as shown by stimulation emission depletion microscopy. Neurons from amphiphysin deficient mice that did not internalize the immunoglobulin provided additional evidence of the specificity in antibody uptake. GABAergic synapses appeared more vulnerable than glutamatergic synapses to defective endocytosis induced by anti-amphiphysin immunoglobulin G, as shown by increased clustering of the endocytic protein AP180 and by defective loading of FM 1-43, a styryl dye used to label cell membranes. Incubation of cultured neurons with anti-amphiphysin immunoglobulin G reduced basal and stimulated release of γ-aminobutyric acid substantially more than that of glutamate. By whole-cell patch-clamp analysis of GABAergic inhibitory transmission in hippocampus granule cells we showed a faster, activity-dependent decrease of the amplitude of evoked inhibitory postsynaptic currents in brain slices treated with antibodies against amphiphysin. We suggest that these findings may explain the pathophysiology of the core signs of stiff person syndrome at the molecular level and show that autoantibodies can alter the function of inhibitory synapses in vivo upon binding to an intraneuronal key protein by disturbing vesicular endocytosis. 
650 4 |a Humans 
650 4 |a Aged 
650 4 |a Female 
650 4 |a Middle Aged 
650 4 |a Animals 
650 4 |a Mice 
650 4 |a Rats 
650 4 |a Cells, Cultured 
650 4 |a Mice, Knockout 
650 4 |a Autoantibodies 
650 4 |a Endocytosis 
650 4 |a gamma-Aminobutyric Acid 
650 4 |a Immunization, Passive 
650 4 |a Immunoglobulin G 
650 4 |a Inhibitory Postsynaptic Potentials 
650 4 |a Injections, Spinal 
650 4 |a Nerve Tissue Proteins 
650 4 |a Neural Inhibition 
650 4 |a Rats, Inbred Lew 
650 4 |a Stiff-Person Syndrome 
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