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March 2023; 10 (2) Research ArticleOpen Access

Anti-LGI4 Antibody Is a Novel Juxtaparanodal Autoantibody for Chronic Inflammatory Demyelinating Polyneuropathy

Xu Zhang, Jun-Ichi Kira, Hidenori Ogata, Tomohiro Imamura, Mikio Mitsuishi, Takayuki Fujii, Masaki Kobayashi, Kazuo Kitagawa, Yukihiro Namihira, Yusuke Ohya, Guzailiayi Maimaitijiang, Ryo Yamasaki, Yuko Fukata, Masaki Fukata, Noriko Isobe, Yuri Nakamura
First published January 11, 2023, DOI: https://doi.org/10.1212/NXI.0000000000200081
Xu Zhang
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Jun-Ichi Kira
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Hidenori Ogata
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Tomohiro Imamura
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Mikio Mitsuishi
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Takayuki Fujii
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Masaki Kobayashi
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Kazuo Kitagawa
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Yukihiro Namihira
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Yusuke Ohya
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Guzailiayi Maimaitijiang
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Ryo Yamasaki
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Yuko Fukata
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Masaki Fukata
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Noriko Isobe
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Yuri Nakamura
From the Translational Neuroscience Center (X.Z., J.K., T.I., M.M., G.M., Y. Nakamura), Graduate School of Medicine, International University of Health and Welfare, Okawa; School of Pharmacy at Fukuoka (J.K., T.I., Y. Nakamura), International University of Health and Welfare, Okawa; Department of Neurology (J.K., Y. Nakamura), Brain and Nerve Center, Fukuoka Central Hospital, International University of Health and Welfare, Fukuoka; Department of Neurology (H.O., T.F., R.Y., N.I.), Neurological Institute, Graduate School of Medical Sciences, Kyushu University, Fukuoka; Department of Neurology (M.K., K.K.), Tokyo Women's Medical University Hospital, Tokyo; Department of Cardiovascular Medicine (Y. Namihira, Y.O.), Nephrology, and Neurology, Graduate School of Medicine, University of Ryukyus, Okinawa; and Division of Membrane Physiology (Y.F., M.F.), National Institute for Physiological Sciences, Okazaki, Japan.
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Citation
Anti-LGI4 Antibody Is a Novel Juxtaparanodal Autoantibody for Chronic Inflammatory Demyelinating Polyneuropathy
Xu Zhang, Jun-Ichi Kira, Hidenori Ogata, Tomohiro Imamura, Mikio Mitsuishi, Takayuki Fujii, Masaki Kobayashi, Kazuo Kitagawa, Yukihiro Namihira, Yusuke Ohya, Guzailiayi Maimaitijiang, Ryo Yamasaki, Yuko Fukata, Masaki Fukata, Noriko Isobe, Yuri Nakamura
Neurol Neuroimmunol Neuroinflamm Mar 2023, 10 (2) e200081; DOI: 10.1212/NXI.0000000000200081

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    Figure 1 Screening for Autoantibodies in Anti-neurofascin155 and Anti-contactin1 Antibody-Negative Patients With CIDP Using Mouse Sciatic Nerves and DRG

    (A) Double immunostaining of a mouse teased sciatic nerve with a patient's serum and anti-Kv1.2 antibody shows colocalization of the patient's IgG with Kv1.2, a marker of juxtaparanodes. (B) IgG from 4 patients with CIDP, but not from a healthy control, demonstrates a circle-like staining pattern around the ganglion cells (see the magnified images). For case 1, immunostaining of mouse DRG by serum samples obtained before and 16 years after the first IVIg treatment is shown. Scale bar: 50 μm. Kv = potassium channel; CIDP = chronic inflammatory demyelinating polyneuropathy; DRG = dorsal root ganglia; IFA = immunofluorescence assay; IVIg = IV immunoglobulin.

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    Figure 2 Identification of Anti-LGI4 Antibodies in Sera From Tissue-Based IFA-Positive Patients With CIDP by DRG-Based IFAs

    Double immunostaining of mouse DRG with serum from a tissue-based IFA-positive patient with CIDP (case 1 in Table 1) and different commercial antibodies. (A) Immunostaining of glutamine synthetase (red), a specific satellite glial cell marker, colocalized with patient IgG binding (green). (B) Immunostaining of S100β (red), a marker of large DRG neurons and satellite glial cells, partly colocalized with patient IgG binding (green). (C) IgG binding of the patient's serum (green) colocalized with that of the commercial anti-LGI4 antibody (LGI4; red). (D) immunostaining of CASPR1 (red), a paranode marker, which mainly stained sensory neuron somata, barely colocalized with patient IgG binding (green). Scale bar: 50 µm. CIDP = chronic inflammatory demyelinating polyneuropathy; CASPR1 = contactin-associated protein 1; DRG = dorsal root ganglia; IFA = immunofluorescence assay; LGI4 = leucine-rich repeat LGI family member 4.

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    Figure 3 Cell-Based IFA Using Rat Schwann Cells With Patients' IgG and a Commercial Anti-LGI4 Antibody

    Serum samples from 4 seropositive patients with CIDP and a commercial anti-LGI4 antibody all demonstrate the same immunostaining pattern on rat Schwann cells, while a healthy control shows no immunoreactivity. Scale bars: 20 µm. CIDP = chronic inflammatory demyelinating polyneuropathy; IFA = immunofluorescence assay; LGI4 = leucine-rich repeat LGI family member 4.

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    Figure 4 Cell-Based IFAs Using Commercial Anti-LGI4 Antibodies and Sera of Seropositive Patient With CIDP

    (A) LGI4-Flag–cotransfected and ADAM22-HA–cotransfected HEK293T cells stained with anti-Flag and commercial anti-LGI4 antibodies. (B) LGI4-Flag–cotransfected and ADAM22-HA–cotransfected HEK293T cells stained with anti-Flag antibodies and IgG from seropositive patients with CIDP (cases 1 and 4) showed cell surface staining. Scale bar: 50 μm. ADAM22 = a disintegrin and metalloprotease domain–containing protein 22, CIDP = chronic inflammatory demyelinating polyneuropathy; HEK = human embryonic kidney; IFA = immunofluorescence assay; LGI4 = leucine-rich repeat LGI family member 4.

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    Figure 5 Confirmation of the Autoantibody Specificity for LGI4 Using a Genetic Strategy With Rat Schwann Cells

    (A) Assessment of the effect of Lgi4 siRNA transfection on Lgi4 mRNA levels in rat Schwann cells by quantitative real-time PCR. The results are expressed as mean ± SEM. The expression of glyceraldehyde-3-phosphate dehydrogenase was determined as a housekeeping gene. *p = 0.0213. (B) WB analysis of LGI4 protein using rat Schwann cells after Lgi4 siRNA or scrambled siRNA treatment. IgG from 1 representative seropositive patient with CIDP (case 2) and a commercial anti-LGI4 antibody showed decreased signals after Lgi4 siRNA treatment compared with the scrambled siRNA in rat Schwann cells. (C) Cell-based IFA using Lgi4 siRNA or scrambled siRNA-treated rat Schwann cells. Signals in rat Schwann cells from the serum of case 2 and the anti-LGI4 antibody were significantly decreased after Lgi4 siRNA treatment compared with those after scrambled siRNA treatment. (D) Comparison of the MFI from a CIDP patient's IgG between Lgi4 siRNA and scrambled siRNA-treated rat Schwann cells. Nuclei are counterstained with DAPI (blue). The results are expressed as the mean ± SEM. *p = 0.0241. Scale bars: (C) 30 μm. AU = arbitrary units; CIDP = chronic inflammatory demyelinating polyneuropathy; DAPI = 4′,6-diamidino-2-phenylindole; IFA = immunofluorescence assay; LGI4 = leucine-rich repeat LGI family member 4; MFI = mean fluorescence intensity; WB = Western blotting.

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    Figure 6 Effects of Sera From Anti-LGI4 Antibody-Seropositive Patients With CIDP and Controls on Schwann Cells

    Quantitative real-time PCR assessment of Krox20 (A) and Periaxin (B) expression in rat Schwann cells. The results are expressed as the mean ± SEM. *p = 0.03, **p = 0.0045. CIDP = chronic inflammatory demyelinating polyneuropathy; LGI4 = leucine-rich repeat LGI family member 4.

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Neurology: Neuroimmunology & Neuroinflammation
Online ISSN: 2332-7812

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