Neuropathic pain and distinct CASPR2 autoantibody IgG subclasses drive neuronal hyperexcitability Article Swipe
Margarita Habib
,
Anna-Lena Wiessler
,
Patrik Greguletz
,
Michéle Niesner
,
Mareike Selcho
,
Ligia Abrante
,
Christian Werner
,
Annemarie Sodmann
,
M. H. J. Koch
,
Zare Abdelhossein
,
Harald Prüß
,
Justina Dargvainiene
,
Jan Lewerenz
,
Robert Handreka
,
Péter Körtvélyessy
,
Dirk Reinhold
,
Franziska Thaler
,
Kalliopi Pitarokoili
,
Robert J. Kittel
,
Michael Briese
,
Michael Sendtner
,
Heike L. Rittner
,
Frank Leypoldt
,
Claudia Sommer
,
Robert Blum
,
Kathrin Doppler
,
Carmen Villmann
·
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1101/2024.09.04.611282
YOU?
·
· 2024
· Open Access
·
· DOI: https://doi.org/10.1101/2024.09.04.611282
Patients with autoantibodies (aAbs) against the contactin-associated protein-like 2 (CASPR2) suffer from a variety of clinical syndromes including neuropathic pain, in some patients even as the only symptom. CASPR2 is an adhesion protein of the neurexin IV family and part of the voltage-gated potassium channel complex (VGKC) in neurons of dorsal root ganglia (DRG). The subsequent pathological mechanisms following the binding of CASPR2 aAbs and their association with pain are only partially understood. CASPR2 aAbs are mainly of the IgG4 subclass. Previous studies have neglected subclass-dependent effects. Here we investigated 49 subclassified patient serum samples positive for CASPR2 aAbs. To unravel underlying molecular mechanisms, we used a combination of super-resolution lattice structural illumination microscopy (SIM 2 ) and functional readouts by calcium imaging and electrophysiological recordings. CASPR2-positive patient sera subclassified in IgG4 together with at least one other IgG subclass (IgGX) and patients with only IgG4 were further subdivided into the pain and no pain group. Patient subclassification shed further light on the pathological mechanisms of CASPR2 aAbs. A decrease of CASPR2 expression after long-term exposure to CASPR2 aAbs was only observed for the patient group without pain. Upon withdrawal of the CASPR2 aAbs, CASPR2 expression returned to normal level. Structural alterations were obtained by increased distances between CASPR2 and associated potassium channels along DRG axons using high-resolution lattice SIM 2 microscopy but only following binding of CASPR2 aAbs from patients with pain. Similarly, CASPR2 aAbs of patients with pain significantly increased overall neuronal excitability of cultured DRG neurons as measured by calcium imaging. Patch-clamp recordings revealed significantly decreased current amplitudes of voltage-gated potassium (Kv) channels after incubation with all four CASPR2 aAbs subclassifications with the most prominent effect of serum samples harboring IgG4 aAbs. Notably, a patient serum sample lacking IgG4 did not alter Kv channel function. Withdrawal of aAbs rescued Kv channel function to normal levels suggesting that the affected potassium channel function is rather due to a functional block of the VGKC rather than altered structural integrity of the VGKC. Taken together, we found IgG4 aAbs to be a major modifier of potassium channel function. The increase in DRG excitability is primarily due to impaired Kv channel conductance as a consequence of CASPR2 aAbs binding but additional and so far unidentified signal pathways contribute to this process in patients with neuropathic pain.
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Metadata
- Type
- preprint
- Language
- en
- Landing Page
- http://doi.org/10.1101/2024.09.04.611282
- OA Status
- green
- References
- 47
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4402315394
All OpenAlex metadata
Raw OpenAlex JSON
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https://openalex.org/W4402315394Canonical identifier for this work in OpenAlex
- DOI
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https://doi.org/10.1101/2024.09.04.611282Digital Object Identifier
- Title
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Neuropathic pain and distinct CASPR2 autoantibody IgG subclasses drive neuronal hyperexcitabilityWork title
- Type
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preprintOpenAlex work type
- Language
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enPrimary language
- Publication year
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2024Year of publication
- Publication date
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2024-09-06Full publication date if available
- Authors
-
Margarita Habib, Anna-Lena Wiessler, Patrik Greguletz, Michéle Niesner, Mareike Selcho, Ligia Abrante, Christian Werner, Annemarie Sodmann, M. H. J. Koch, Zare Abdelhossein, Harald Prüß, Justina Dargvainiene, Jan Lewerenz, Robert Handreka, Péter Körtvélyessy, Dirk Reinhold, Franziska Thaler, Kalliopi Pitarokoili, Robert J. Kittel, Michael Briese, Michael Sendtner, Heike L. Rittner, Frank Leypoldt, Claudia Sommer, Robert Blum, Kathrin Doppler, Carmen VillmannList of authors in order
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https://doi.org/10.1101/2024.09.04.611282Publisher landing page
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YesWhether a free full text is available
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-
greenOpen access status per OpenAlex
- OA URL
-
https://doi.org/10.1101/2024.09.04.611282Direct OA link when available
- Concepts
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Neuropathic pain, Autoantibody, Neuroscience, Medicine, Immunology, Psychology, AntibodyTop concepts (fields/topics) attached by OpenAlex
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0Total citation count in OpenAlex
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47Number of works referenced by this work
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10Other works algorithmically related by OpenAlex
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