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September 2021; 8 (5) ArticleOpen Access

Argonaute Autoantibodies as Biomarkers in Autoimmune Neurologic Diseases

View ORCID ProfileLe-Duy Do, View ORCID ProfileChristian P. Moritz, View ORCID ProfileSergio Muñiz-Castrillo, Anne-Laurie Pinto, Yannick Tholance, Sabine Brugiere, View ORCID ProfileYohann Couté, View ORCID ProfileOda Stoevesandt, Michael J. Taussig, View ORCID ProfileVéronique Rogemond, View ORCID ProfileAlberto Vogrig, View ORCID ProfileBastien Joubert, Karine Ferraud, Jean-Philippe Camdessanché, Jean-Christophe Antoine, Jérôme Honnorat
First published July 28, 2021, DOI: https://doi.org/10.1212/NXI.0000000000001032
Le-Duy Do
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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  • For correspondence: le-duy.do@chu-lyon.fr
Christian P. Moritz
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Sergio Muñiz-Castrillo
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Anne-Laurie Pinto
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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  • For correspondence: anne-laurie.pinto@chu-lyon.fr
Yannick Tholance
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Sabine Brugiere
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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  • For correspondence: sabine.brugiere@cea.fr
Yohann Couté
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Oda Stoevesandt
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Michael J. Taussig
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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  • For correspondence: mike.taussig@cambridgeproteinarrays.com
Véronique Rogemond
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Alberto Vogrig
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Bastien Joubert
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Karine Ferraud
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Jean-Philippe Camdessanché
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Jean-Christophe Antoine
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Jérôme Honnorat
From French Reference Center on Paraneoplastic Neurological Syndrome (L.-D.D., S.M.-C., A.-L.P., V.R., A.V., B.J., J.-P.C., J.-C.A., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, France; Institute NeuroMyoGène (L.-D.D., C.P.M., S.M.-C., A.-L.P., Y.T., V.R., A.V., B.J., K.F., J.-P.C., J.-C.A., J.H.), INSERM U1217/CNRS UMR 5310, Université de Lyon, Université Claude Bernard Lyon 1, France; University Jean Monnet (C.P.M., Y.T., J.-P.C., J.-C.A.), Saint-Étienne, France; Department of Biochemistry (Y.T.), University Hospital of Saint-Etienne, France; University Grenoble Alpes (S.B., Y.C.), CEA, INSERM, IRIG, BGE, France; Cambridge Protein Arrays Ltd. (O.S., M.J.T.), Babraham Research Campus, United Kingdom; and Department of Neurology (K.F., J.-P.C., J.-C.A.), University Hospital of Saint-Etienne, France.
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Citation
Argonaute Autoantibodies as Biomarkers in Autoimmune Neurologic Diseases
Le-Duy Do, Christian P. Moritz, Sergio Muñiz-Castrillo, Anne-Laurie Pinto, Yannick Tholance, Sabine Brugiere, Yohann Couté, Oda Stoevesandt, Michael J. Taussig, Véronique Rogemond, Alberto Vogrig, Bastien Joubert, Karine Ferraud, Jean-Philippe Camdessanché, Jean-Christophe Antoine, Jérôme Honnorat
Neurol Neuroimmunol Neuroinflamm Sep 2021, 8 (5) e1032; DOI: 10.1212/NXI.0000000000001032

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    Figure 1 Identification of AGO-Abs

    (A) Immunostaining of the adult rat brain with CSF (1:10) of patient XI resulted in a strong reactivity with the stratum pyramidale of the hippocampus, granule cells of the cerebellum, and cerebral cortex. The scale bar is indicated for each magnification. (B) Immunoprecipitation of the antigens with patient XI's CSF. Note the specifically enriched band around 100 kDa (*) and the less intense band around 280 kDa (**) obtained after immunoprecipitation with patient XI's CSF (E+) compared with control CSF (E−). Protein bands were visualized via silver staining. (C) Quantified reactivities of 12 patients with SNN, 22 patients with ONPs, and 9 HCs with 7 AGO variants on protein microarrays. Red dots represent significantly positive samples (z-score > 4). AGO-Abs = antibodies against the Argonaute protein family; HC = healthy control; ONP = other peripheral neuropathy; SNN = sensory neuronopathy.

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    Figure 2 Confirmation of AGO-Abs Using Cell-Based Assay

    HEK293 cells were transfected with VP5-AGO1-4 or VP5-TNRC6B plasmid, for a transient overexpression. Fixed and permeabilized cells were then immunostained with anti-HA antibody (in green) and patient XI's CSF (1:10; in red). Only AGO-transfected cells (in green) reacted with patient XI's CSF. No reactivity was observed on TNRC6B-transfected cells or nontransfected cells. Scale bar = 50 μm. AGO-Abs = antibodies against the Argonaute protein family.

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    Figure 3 Neuroimaging Findings in 2 Patients With AGO2-Abs

    (A) Axial (top) and coronal (bottom) fluid-attenuated inversion recovery (FLAIR) brain MRI of patient XII with limbic encephalitis, showing bilateral swelling and hyperintensity of medial temporal lobes, extending also to a lesser degree to the lateral temporal cortex. (B) Axial FLAIR (top) brain MRI of patient XVII presenting with cerebellar ataxia, showing vermis atrophy and left cerebellar hemisphere hyperintensity. Pancerebellar atrophy is better demonstrated on the sagittal T2 brain MRI (bottom) of the same patient.

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