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March 28, 2017; 88 (13) Article

Netrin-1 receptor antibodies in thymoma-associated neuromyotonia with myasthenia gravis

Estefanía Torres-Vega, Nuria Mancheño, Arantxa Cebrián-Silla, Vicente Herranz-Pérez, María J. Chumillas, Germán Moris, Bastien Joubert, Jérôme Honnorat, Teresa Sevilla, Juan J. Vílchez, Josep Dalmau, Francesc Graus, José Manuel García-Verdugo, Luis Bataller
First published March 1, 2017, DOI: https://doi.org/10.1212/WNL.0000000000003778
Estefanía Torres-Vega
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Nuria Mancheño
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Arantxa Cebrián-Silla
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Vicente Herranz-Pérez
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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María J. Chumillas
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Germán Moris
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Bastien Joubert
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Jérôme Honnorat
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Teresa Sevilla
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Juan J. Vílchez
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Josep Dalmau
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Francesc Graus
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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José Manuel García-Verdugo
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Luis Bataller
From the Laboratorio de Neurología (E.T.-V., T.S., J.J.V., L.B.), Instituto de Investigación Sanitaria La Fe, Hospital Universitario y Politécnico La Fe, CIBERER, Valencia; Servicio de Anatomía Patológica (N.M.), Servicio de Neurofisiología Clínica (M.J.C.), and Servicio de Neurología (T.S., J.J.V., L.B.), Hospital Universitario y Politécnico La Fe, Valencia; Laboratorio de Neurobiología Comparada (A.C.-S., V.H.-P., J.M.G.-V.), Instituto Cavanilles, Universidad de Valencia, CIBERNED; Servicio de Neurología (G.M.), Hospital Central de Asturias, Oviedo, Spain; French Reference Center on Paraneoplastic Neurological Syndrome (B.J., J.H.), Hospices Civils de Lyon, Hôpital Neurologique, Bron, and Institut NeuroMyoGene INSERM U1217/CNRS UMR 5310, Université de Lyon–Université Claude Bernard Lyon 1, France; Laboratori de Neurologia (J.D., F.G.), Institut d´Investigacions Biomèdiques August Pi I Sunyer, CIBERER, Barcelona, Spain; and Department of Neurology (J.D.), University of Pennsylvania, Philadelphia, and Institució Catalana de Recerca i Estudis Avançats, Barcelona, Spain.
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Citation
Netrin-1 receptor antibodies in thymoma-associated neuromyotonia with myasthenia gravis
Estefanía Torres-Vega, Nuria Mancheño, Arantxa Cebrián-Silla, Vicente Herranz-Pérez, María J. Chumillas, Germán Moris, Bastien Joubert, Jérôme Honnorat, Teresa Sevilla, Juan J. Vílchez, Josep Dalmau, Francesc Graus, José Manuel García-Verdugo, Luis Bataller
Neurology Mar 2017, 88 (13) 1235-1242; DOI: 10.1212/WNL.0000000000003778

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Abstract

Objective: To identify cell-surface antibodies in patients with neuromyotonia and to describe the main clinical implications.

Methods: Sera of 3 patients with thymoma-associated neuromyotonia and myasthenia gravis were used to immunoprecipitate and characterize neuronal cell-surface antigens using reported techniques. The clinical significance of antibodies against precipitated proteins was assessed with sera of 98 patients (neuromyotonia 46, myasthenia gravis 52, thymoma 42; 33 of them with overlapping syndromes) and 219 controls (other neurologic diseases, cancer, and healthy volunteers).

Results: Immunoprecipitation studies identified 3 targets, including the Netrin-1 receptors DCC (deleted in colorectal carcinoma) and UNC5A (uncoordinated-5A) as well as Caspr2 (contactin-associated protein-like 2). Cell-based assays with these antigens showed that among the indicated patients, 9 had antibodies against Netrin-1 receptors (7 with additional Caspr2 antibodies) and 5 had isolated Caspr2 antibodies. Only one of the 219 controls had isolated Caspr2 antibodies with relapsing myelitis episodes. Among patients with neuromyotonia and/or myasthenia gravis, the presence of Netrin-1 receptor or Caspr2 antibodies predicted thymoma (p < 0.05). Coexisting Caspr2 and Netrin-1 receptor antibodies were associated with concurrent thymoma, myasthenia gravis, and neuromyotonia, often with Morvan syndrome (p = 0.009). Expression of DCC, UNC5A, and Caspr2 proteins was demonstrated in paraffin-embedded thymoma samples (3) and normal thymus.

Conclusions: Antibodies against Netrin-1 receptors (DCC and UNC5a) and Caspr2 often coexist and associate with thymoma in patients with neuromyotonia and myasthenia gravis.

Classification of evidence: This study provides Class III evidence that antibodies against Netrin-1 receptors can identify patients with thymoma (sensitivity 21.4%, specificity 100%).

GLOSSARY

Caspr2=
contactin-associated protein-like 2;
DCC=
deleted in colorectal carcinoma;
OR=
odds ratio;
PPV=
positive predictive value;
UNC5A=
uncoordinated-5A

Footnotes

  • Go to Neurology.org for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Supplemental data at Neurology.org

  • Received September 27, 2016.
  • Accepted in final form January 4, 2017.
  • © 2017 American Academy of Neurology
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