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Here, we generate patient-derived monoclonal antibodies (mAbs) against LGI1. We explore their sequences and binding characteristics, plus their pathogenic potential using transfected HEK293T cells, rodent neuronal preparations, and behavioural and electrophysiological assessments in vivo after mAb injections into the rodent hippocampus. In live cell-based assays, LGI1 epitope recognition was examined with patient sera (n\u2009=\u200931), CSFs (n\u2009=\u200911), longitudinal serum samples (n\u2009=\u200915), and using mAbs (n\u2009=\u200914) generated from peripheral B cells of two patients. All sera and 9\/11 CSFs bound both the leucine-rich repeat (LRR) and the epitempin repeat (EPTP) domains of LGI1, with stable ratios of LRR:EPTP antibody levels over time. By contrast, the mAbs derived from both patients recognized either the LRR or EPTP domain. mAbs against both domain specificities showed varied binding strengths, and marked genetic heterogeneity, with high mutation frequencies. LRR-specific mAbs recognized LGI1 docked to its interaction partners, ADAM22 and ADAM23, bound to rodent brain sections, and induced internalization of the LGI1-ADAM22\/23 complex in both HEK293T cells and live hippocampal neurons. By contrast, few EPTP-specific mAbs bound to rodent brain sections or ADAM22\/23-docked LGI1, but all inhibited the docking of LGI1 to ADAM22\/23. After intrahippocampal injection, and by contrast to the LRR-directed mAbs, the EPTP-directed mAbs showed far less avid binding to brain tissue and were consistently detected in the serum. Post-injection, both domain-specific mAbs abrogated long-term potentiation induction, and LRR-directed antibodies with higher binding strengths induced memory impairment. Taken together, two largely dichotomous populations of LGI1 mAbs with distinct domain binding characteristics exist in the affinity matured peripheral autoantigen-specific memory pools of individuals, both of which have pathogenic potential. In human autoantibody-mediated diseases, the detailed characterization of patient mAbs provides a valuable method to dissect the molecular mechanisms within polyclonal populations.<\/jats:p>","DOI":"10.1093\/brain\/awaa104","type":"journal-article","created":{"date-parts":[[2020,3,16]],"date-time":"2020-03-16T16:33:04Z","timestamp":1584376384000},"page":"1731-1745","source":"Crossref","is-referenced-by-count":138,"title":["Distinctive binding properties of human monoclonal LGI1 autoantibodies determine pathogenic mechanisms"],"prefix":"10.1093","volume":"143","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-3082-6906","authenticated-orcid":false,"given":"Melanie","family":"Ramberger","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Berretta","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jeanne M M","family":"Tan","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"},{"name":"Department of Neurology, John Radcliffe Hospital, Oxford University Hospitals, Oxford, UK"},{"name":"Department of Neurology, National Neuroscience Institute, 11 Jalan Tan Tock Seng, Singapore 308433, Singapore"},{"name":"Experimental Neuropathology Group, Department of Pharmacology, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Bo","family":"Sun","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"},{"name":"Department of Neurology, John Radcliffe Hospital, Oxford University Hospitals, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sophia","family":"Michael","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"},{"name":"Department of Neurology, John Radcliffe Hospital, Oxford University Hospitals, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tianrong","family":"Yeo","sequence":"first","affiliation":[{"name":"Department of Neurology, National Neuroscience Institute, 11 Jalan Tan Tock Seng, Singapore 308433, Singapore"},{"name":"Experimental Neuropathology Group, Department of Pharmacology, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8752-3151","authenticated-orcid":false,"given":"Jakob","family":"Theorell","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rachael","family":"Bashford-Rogers","sequence":"first","affiliation":[{"name":"Wellcome Centre for Human Genetics, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sofija","family":"Paneva","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Victoria","family":"O\u2019Dowd","sequence":"first","affiliation":[{"name":"UCB Pharma, 208-216 Bath Road, Berkshire, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Neesha","family":"Dedi","sequence":"first","affiliation":[{"name":"UCB Pharma, 208-216 Bath Road, Berkshire, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarfaraj","family":"Topia","sequence":"first","affiliation":[{"name":"UCB Pharma, 208-216 Bath Road, Berkshire, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Robert","family":"Griffin","sequence":"first","affiliation":[{"name":"UCB Pharma, 208-216 Bath Road, Berkshire, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jorge","family":"Ramirez-Franco","sequence":"first","affiliation":[{"name":"Unit\u00e9 de Neurobiologie des Canaux Ioniques et de la Synapse, INSERM UMR_S 1072, Aix Marseille Universit\u00e9, Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Oussama","family":"El Far","sequence":"first","affiliation":[{"name":"Unit\u00e9 de Neurobiologie des Canaux Ioniques et de la Synapse, INSERM UMR_S 1072, Aix Marseille Universit\u00e9, Marseille, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"St\u00e9phanie","family":"Baulac","sequence":"first","affiliation":[{"name":"Sorbonne Universit\u00e9, UPMC Univ Paris 06, UMR S 1127, INSERM, U1127, CNRS, UMR 7225, Institut du Cerveau et de la Moelle \u00e9pini\u00e8re (ICM), H\u00f4pital Piti\u00e9-Salp\u00eatri\u00e8re, Paris, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria I","family":"Leite","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"},{"name":"Department of Neurology, John Radcliffe Hospital, Oxford University Hospitals, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Arjune","family":"Sen","sequence":"first","affiliation":[{"name":"Oxford Autoimmune Neurology Group, Nuffield Department of Clinical Neurosciences, University of Oxford, Oxford, UK"},{"name":"Department of Neurology, John Radcliffe Hospital, Oxford University Hospitals, Oxford, UK"},{"name":"Oxford Epilepsy Research Group, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Alexander","family":"Jeans","sequence":"first","affiliation":[{"name":"Experimental Neuropathology Group, Department of Pharmacology, University of Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David","family":"McMillan","sequence":"first","affiliation":[{"name":"UCB Pharma, 208-216 Bath Road, Berkshire, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Diane","family":"Marshall","sequence":"first","affiliation":[{"name":"UCB Pharma, 208-216 Bath Road, Berkshire, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel","family":"Anthony","sequence":"first","affiliation":[{"name":"Experimental Neuropathology Group, Department of Pharmacology, University of Oxford, Oxford, 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Oxford, Oxford, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,5,21]]},"reference":[{"key":"2020061607534796500_OP-B1","doi-asserted-by":"crossref","DOI":"10.1093\/brain\/awy109","article-title":"Distinct HLA associations of LGI1 and CASPR2-antibody diseases","volume":":","author":"Binks","year":"2018","journal-title":"Brain"},{"key":"2020061607534796500_OP-B2","doi-asserted-by":"crossref","first-page":"2749","DOI":"10.1093\/brain\/awq171","article-title":"Electroclinical characterization of epileptic seizures in leucine-rich, glioma-inactivated 1-deficient mice","volume":"133","author":"Chabrol","year":"2010","journal-title":"Brain"},{"key":"2020061607534796500_OP-B3","doi-asserted-by":"crossref","first-page":"143","DOI":"10.4161\/mabs.27044","article-title":"The rapid generation of recombinant functional monoclonal antibodies from individual, antigenspecific bone marrow-derived plasma cells isolated using a novel 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patients","volume":"82","author":"Gadoth","year":"2017","journal-title":"Ann Neurol"},{"key":"2020061607534796500_OP-B8090189","doi-asserted-by":"crossref","first-page":"388\u2013403.e12.\u00a0","DOI":"10.1016\/j.immuni.2020.01.001","article-title":"Analysis of a Therapeutic Antibody Cocktail Reveals Determinants for Cooperative and Broad Ebolavirus Neutralization","volume":"52","author":"Gilchuk","year":"2020","journal-title":"Immunity"},{"key":"2020061607534796500_OP-B7","doi-asserted-by":"crossref","first-page":"3610","DOI":"10.1128\/JVI.03099-14","article-title":"Broadly neutralizing anti-influenza virus antibodies: enhancement of neutralizing potency in polyclonal mixtures and IgA backbones","volume":"89","author":"He","year":"2015","journal-title":"J Virol"},{"key":"2020061607534796500_OP-B9","doi-asserted-by":"crossref","first-page":"5866","DOI":"10.1523\/JNEUROSCI.0167-10.2010","article-title":"Cellular and synaptic mechanisms of anti-NMDA receptor 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Neurosci"},{"key":"2020061607534796500_OP-B10","doi-asserted-by":"crossref","first-page":"2734","DOI":"10.1093\/brain\/awq213","article-title":"Antibodies to Kv1 potassium channel-complex proteins leucine-rich, glioma inactivated 1 protein and contactin-associated protein-2 in limbic encephalitis, Morvan\u2019s syndrome and acquired neuromyotonia","volume":"133","author":"Irani","year":"2010","journal-title":"Brain"},{"key":"2020061607534796500_OP-B11","doi-asserted-by":"crossref","first-page":"892","DOI":"10.1002\/ana.22307","article-title":"Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis","volume":"69","author":"Irani","year":"2011","journal-title":"Ann Neurol"},{"key":"2020061607534796500_OP-B12","doi-asserted-by":"crossref","first-page":"3151","DOI":"10.1093\/brain\/awt212","article-title":"Faciobrachial dystonic seizures: the influence of immunotherapy on seizure control and prevention of cognitive impairment in a broadening phenotype","volume":"136","author":"Irani","year":"2013","journal-title":"Brain"},{"key":"2020061607534796500_OP-B13","doi-asserted-by":"crossref","first-page":"565","DOI":"10.1002\/ana.25552","article-title":"Human gestational N-methyl-d-aspartate receptor autoantibodies impair neonatal murine brain function","volume":"86","author":"Jurek","year":"2019","journal-title":"Ann. Neurol"},{"key":"2020061607534796500_OP-B14","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1002\/ana.24860","article-title":"Anti-LGI1 encephalitis is associated with unique HLA subtypes","volume":"81","author":"Kim","year":"2017","journal-title":"Ann Neurol"},{"key":"2020061607534796500_OP-B15","doi-asserted-by":"crossref","first-page":"1554","DOI":"10.1126\/science.1144603","article-title":"Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange","volume":"317","author":"Kolfschoten","year":"2007","journal-title":"Science"},{"key":"2020061607534796500_OP-B16","doi-asserted-by":"crossref","first-page":"405","DOI":"10.1002\/ana.25666","article-title":"Human CSF monoclonal LGI1 autoantibodies increase neuronal excitability","volume":"87","author":"Kornau","year":"2020","journal-title":"Ann Neurol"},{"key":"2020061607534796500_OP-B17","doi-asserted-by":"crossref","first-page":"2641","DOI":"10.1093\/brain\/aww208","article-title":"Human cerebrospinal fluid monoclonal N-methyl-D-aspartate receptor autoantibodies are sufficient for encephalitis pathogenesis","volume":"139","author":"Kreye","year":"2016","journal-title":"Brain"},{"key":"2020061607534796500_OP-B18","doi-asserted-by":"crossref","first-page":"776","DOI":"10.1016\/S1474-4422(10)70137-X","article-title":"Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series","volume":"9","author":"Lai","year":"2010","journal-title":"Lancet Neurol"},{"key":"2020061607534796500_OP-B1159519"},{"key":"2020061607534796500_OP-B19","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1002\/ana.25173","article-title":"N-methyl-D-aspartate receptor antibody production from germinal center reactions: therapeutic implications","volume":"83","author":"Makuch","year":"2018","journal-title":"Ann Neurol"},{"key":"2020061607534796500_OP-B0690779","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1093\/brain\/awx070","article-title":"Focal CA3 hippocampal subfield atrophy following LGI1 VGKC-complex antibody limbic encephalitis","volume":"140","author":"Miller","year":"2017","journal-title":"Brain"},{"key":"2020061607534796500_OP-B20","doi-asserted-by":"crossref","first-page":"863","DOI":"10.1002\/ana.25216","article-title":"Genetic predisposition in anti-LGI1 and anti-NMDA receptor encephalitis","volume":"83","author":"Mueller","year":"2018","journal-title":"Ann Neurol"},{"key":"2020061607534796500_OP-B21","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.neuron.2016.12.015","article-title":"A brief history of long-term potentiation","volume":"93","author":"Nicoll","year":"2017","journal-title":"Neuron"},{"key":"2020061607534796500_OP-B22","doi-asserted-by":"crossref","first-page":"18161","DOI":"10.1523\/JNEUROSCI.3506-13.2013","article-title":"Autoantibodies to epilepsy-related LGI1 in limbic encephalitis neutralize LGI1-ADAM22 interaction and reduce synaptic AMPA receptors","volume":"33","author":"Ohkawa","year":"2013","journal-title":"J. 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Commun"}],"container-title":["Brain"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/brain\/article-pdf\/143\/6\/1731\/33393265\/awaa104.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/brain\/article-pdf\/143\/6\/1731\/33393265\/awaa104.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,6,16]],"date-time":"2020-06-16T07:55:49Z","timestamp":1592294149000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/brain\/article\/143\/6\/1731\/5841730"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,5,21]]},"references-count":36,"journal-issue":{"issue":"6","published-online":{"date-parts":[[2020,5,21]]},"published-print":{"date-parts":[[2020,6,1]]}},"URL":"https:\/\/doi.org\/10.1093\/brain\/awaa104","relation":{},"ISSN":["0006-8950","1460-2156"],"issn-type":[{"value":"0006-8950","type":"print"},{"value":"1460-2156","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,6]]},"published":{"date-parts":[[2020,5,21]]}}}