Autoimmune synaptopathies

Nature Reviews Neuroscience

Volumn 17, Issue 2, 2016, Pages 103-117

  Crisp, Sarah J ^a   Kullmann, Dimitri M ^a   Vincent, Angela ^b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOANTIBODY; CHOLINERGIC RECEPTOR ANTIBODY; COMPLEMENT; GLYCINE RECEPTOR; IMMUNOGLOBULIN ANTIBODY; IMMUNOGLOBULIN G4 ANTIBODY; LGI1 AUTOANTIBODY; UNCLASSIFIED DRUG;

AUTOIMMUNE DISEASE; BLOOD BRAIN BARRIER; CENTRAL NERVOUS SYSTEM DISEASE; CYTOLOGY; EATON LAMBERT SYNDROME; GENE MUTATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MENTAL DISEASE; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; MYOKYMIA; NEUROMUSCULAR JUNCTION DISORDER; NONHUMAN; PRIORITY JOURNAL; REVIEW; ANIMAL; IMMUNOLOGY; METABOLISM; NERVOUS SYSTEM; PATHOLOGY; SYNAPSE; SYNAPTIC TRANSMISSION;

ANIMALS; AUTOANTIBODIES; AUTOIMMUNE DISEASES; HUMANS; NERVOUS SYSTEM; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84955565510     PISSN: 1471003X     EISSN: 14710048     Source Type: Journal    
DOI: 10.1038/nrn.2015.27     Document Type: Review

References (196)

1. Berrih-Aknin S, & Le Panse R. Myasthenia gravis: a comprehensive review of immune dysregulation and etiological mechanisms. J. Autoimmun. 52, 90-100 (2014).
2. Keir G, & Thompson E. J. Proteins as parameters in the discrimination between different blood-CSF barriers. J. Neurol. Sci. 75, 245-253 (1986).
3. Vincent A. Autoimmune channelopathies: new antibody-mediated disorders of the central nervous system. F1000 Biol. Rep. 1, 61 (2009).
4. Hladky S. B, & Barrand M. A. Mechanisms of fluid movement into, through and out of the brain: evaluation of the evidence. Fluids Barriers CNS. 11, 26 (2014).
5. Busse S, et al. Seroprevalence of N methyl-d aspartate glutamate receptor (NMDA R) autoantibodies in aging subjects without neuropsychiatric disorders and in dementia patients. Eur. Arch. Psychiatry Clin. Neurosci. 264, 545-550 (2014).
6. Gold M, Pul R, Bach J. P, Stangel M, & Dodel R. Pathogenic and physiological autoantibodies in the central nervous system. Immunol. Rev. 248, 68-86 (2012).
7. Rose N. R, & Bona C. Defining criteria for autoimmune diseases (Witebsky's postulates revisited). Immunol. Today. 14, 426-430 (1993).
8. Toyka K. V, Brachman D. B, Pestronk A, & Kao I. Myasthenia gravis: passive transfer from man to mouse. Science. 190, 397-399 (1975).
9. Plomp J. J, Morsch M, Phillips W. D, & Verschuuren J. J. Electrophysiological analysis of neuromuscular synaptic function in myasthenia gravis patients and animal models. Exp. Neurol. 270, 41-54 (2015).
10. Patrick J, & Lindstrom J. Autoimmune response to acetylcholine receptor. Science. 180, 871-872 (1973).
11. Leite M. I, et al. IgG1 antibodies to acetylcholine receptors in 'seronegative' myasthenia gravis. Brain. 131, 1940-1952 (2008).
12. Newsom-Davis J, Pinching A. J, Vincent A, & Wilson S. G. Function of circulating antibody to acetylcholine receptor in myasthenia gravis: investigation by plasma exchange. Neurology. 28, 266-272 (1978).
13. Fambrough D. M, Drachman D. B, & Satyamurti S. Neuromuscular junction in myasthenia gravis: decreased acetylcholine receptors. Science. 182, 293-295 (1973).
14. Albuquerque E. X, Rash J. E, Mayer R. F, & Satterfield J. R. An electrophysiological and morphological study of the neuromuscular junction in patients with myasthenia gravis. Exp. Neurol. 51, 536-563 (1976).
15. Engel A. G, & Arahata K. The membrane attack complex of complement at the endplate in myasthenia gravis. Ann. NY Acad. Sci. 505, 326-332 (1987).
16. Woolf A. L. Morphology of the myasthenic neuromuscular junction. Ann. NY Acad. Sci. 135, 35-59 (1966).
17. Zacks S. I, Bauer W. C, & Blumberg J. M. The fine structure of the myasthenic neuromuscular junction. J. Neuropathol. Exp. Neurol. 21, 335-347 (1962).
18. Tuzun E, & Christadoss P. Complement associated pathogenic mechanisms in myasthenia gravis. Autoimmun. Rev. 12, 904-911 (2013).
19. De Baets M. H, Verschuuren J, Daha M. R, & van Breda Vriesman P. J. Effects of the rate of acetylcholine receptor synthesis on the severity of experimental autoimmune myasthenia gravis. Immunol. Res. 7, 200-211 (1988).
20. Howard J. F. Jr et al A randomized, double-blind, placebo-controlled phase II study of eculizumab in patients with refractory generalized myasthenia gravis. Muscle Nerve. 48, 76-84 (2013).
21. Heinemann S, Bevan S, Kullberg R, Lindstrom J, & Rice J. Modulation of acetylcholine receptor by antibody against the receptor. Proc. Natl Acad. Sci. USA. 74, 3090-3094 (1977).
22. Drachman D. B, Angus C. W, Adams R. N, Michelson J. D, & Hoffman G. J. Myasthenic antibodies cross-link acetylcholine receptors to accelerate degradation. N. Engl. J. Med. 298, 1116-1122 (1978).
23. Toyka K. V, et al. Passively transferred myasthenia gravis: protection of mouse endplates by Fab fragments from human myasthenic IgG. J. Neurol. Neurosurg. Psychiatry. 43, 836-842 (1980).
24. Drachman D. B, Adams R. N, Josifek L. F, & Self S. G. Functional activities of autoantibodies to acetylcholine receptors and the clinical severity of myasthenia gravis. N. Engl. J. Med. 307, 769-775 (1982).
25. Bufler J, Pitz R, Czep M, Wick M, & Franke C. Purified IgG from seropositive and seronegative patients with mysasthenia gravis reversibly blocks currents through nicotinic acetylcholine receptor channels. Ann. Neurol. 43, 458-464 (1998).
26. Hoch W, et al. Auto-Antibodies to the receptor tyrosine kinase MuSK in patients with myasthenia gravis without acetylcholine receptor antibodies. Nat. Med. 7, 365-368 (2001).
27. Kim N, et al. Lrp4 is a receptor for Agrin and forms a complex with MuSK. Cell. 135, 334-342 (2008).
28. Zhang B, et al. LRP4 serves as a coreceptor of agrin. Neuron. 60, 285-297 (2008).
29. Messeant J, et al. MuSK frizzled-like domain is critical for mammalian neuromuscular junction formation and maintenance. J. Neurosci. 35, 4926-4941 (2015).
30. Barik A, et al. LRP4 is critical for neuromuscular junction maintenance. J. Neurosci. 34, 13892-13905 (2014).
31. Zhou L, et al. Clinical comparison of muscle-specific tyrosine kinase (MuSK) antibody-positive and -negative myasthenic patients. Muscle Nerve. 30, 55-60 (2004).
32. McConville J, et al. Detection and characterization of MuSK antibodies in seronegative myasthenia gravis. Ann. Neurol. 55, 580-584 (2004).
33. Reddel S. W, Morsch M, & Phillips W. D. Clinical and scientific aspects of muscle-specific tyrosine kinase-related myasthenia gravis. Curr. Opin. Neurol. 27, 558-565 (2014).
34. Feinstein A, Richardson N, & Taussig M. I. Immunoglobulin flexibility in complement activation. Immunol. Today. 7, 169-174 (1986).
35. Bruggemann M, et al. Comparison of the effector functions of human immunoglobulins using a matched set of chimeric antibodies. J. Exp. Med. 166, 1351-1361 (1987).
36. van der Neut Kolfschoten M, et al. Anti-inflammatory activity of human IgG4 antibodies by dynamic Fab arm exchange. Science. 317, 1554-1557 (2007).
37. Huijbers M. G, et al. MuSK IgG4 autoantibodies cause myasthenia gravis by inhibiting binding between MuSK and Lrp4. Proc. Natl Acad. Sci. USA. 110, 20783-20788 (2013).
38. Koneczny I, Cossins J, Waters P, Beeson D, & Vincent A. MuSK myasthenia gravis IgG4 disrupts the interaction of LRP4 with MuSK but both IgG4 and IgG1 3 can disperse preformed agrin-independent AChR clusters. PLoS ONE. 8, e80695 (2013).
39. Klooster R, et al. Muscle-specific kinase myasthenia gravis IgG4 autoantibodies cause severe neuromuscular junction dysfunction in mice. Brain. 135, 1081-1101 (2012).
40. Higuchi O, Hamuro J, Motomura M, & Yamanashi Y. Autoantibodies to low-density lipoprotein receptor-related protein 4 in myasthenia gravis. Ann. Neurol. 69, 418-422 (2011).
41. Plomp J. J, et al. Acetylcholine release in myasthenia gravis: regulation at single end-plate level. Ann. Neurol. 37, 627-636 (1995).
42. Mori S, et al. Antibodies against muscle-specific kinase impair both presynaptic and postsynaptic functions in a murine model of myasthenia gravis. Am. J. Pathol. 180, 798-810 (2012).
43. Viegas S, et al. Passive and active immunization models of MuSK Ab positive myasthenia: electrophysiological evidence for pre and postsynaptic defects. Exp. Neurol. 234, 506-512 (2012).
44. Yumoto N, Kim N, & Burden S. J. Lrp4 is a retrograde signal for presynaptic differentiation at neuromuscular synapses. Nature. 489, 438-442 (2012).
45. Lambert E. H, & Elmqvist D. Quantal components of end-plate potentials in the myasthenic syndrome. Ann. NY Acad. Sci. 183, 183-199 (1971).
46. Lang B, Newsom-Davis J, Wray D, Vincent A, & Murray N. Autoimmune aetiology for myasthenic (Eaton-Lambert) syndrome. Lancet. 2, 224-226 (1981).
47. Lang B, Newsom-Davis J, Peers C, Prior C, & Wray D. W. The effect of myasthenic syndrome antibody on presynaptic calcium channels in the mouse. J. Physiol. 390, 257-270 (1987).
48. Nagel A, Engel A. G, Lang B, Newsom-Davis J, & Fukuoka T. Lambert-Eaton myasthenic syndrome IgG depletes presynaptic membrane active zone particles by antigenic modulation. Ann. Neurol. 24, 552-558 (1988).
49. Prior C, Lang B, Wray D, & Newsom-Davis J. Action of Lambert-Eaton myasthenic syndrome IgG at mouse motor nerve terminals. Ann. Neurol. 17, 587-592 (1985).
50. Lennon V. A, et al. Calcium-channel antibodies in the Lambert-Eaton syndrome and other paraneoplastic syndromes. N. Engl. J. Med. 332, 1467-1474 (1995).
51. Motomura M, et al. Incidence of serum anti P/O type and anti N type calcium channel autoantibodies in the Lambert-Eaton myasthenic syndrome. J. Neurol. Sci. 147, 35-42 (1997).
52. Pinto A, Iwasa K, Newland C, Newsom-Davis J, & Lang B. The action of Lambert-Eaton myasthenic syndrome immunoglobulin G on cloned human voltage-gated calcium channels. Muscle Nerve. 25, 715-724 (2002).
53. Spillane J, et al. Lambert-Eaton syndrome IgG inhibits transmitter release via P/Q Ca2+ channels. Neurology. 84, 575-579 (2015).
54. O'Neill J. H, Murray N. M, & Newsom-Davis J. The Lambert-Eaton myasthenic syndrome A review of 50 cases. Brain. 111, 577-596 (1988).
55. Meriney S. D, Hulsizer S. C, Lennon V. A, & Grinnell A. D. Lambert-Eaton myasthenic syndrome immunoglobulins react with multiple types of calcium channels in small-cell lung carcinoma. Ann. Neurol. 40, 739-749 (1996).
56. Isaacs H. A. Syndrome of continuous muscle-fibre activity. J. Neurol. Neurosurg. Psychiatry. 24, 319-325 (1961).
57. Newsom-Davis J, & Mills K. R. Immunological associations of acquired neuromyotonia (Isaacs' syndrome). Report of five cases and literature review. Brain. 116, 453-469 (1993).
58. Sinha S, et al. Autoimmune aetiology for acquired neuromyotonia (Isaacs' syndrome). Lancet. 338, 75-77 (1991).
59. Shillito P, et al. Acquired neuromyotonia: evidence for autoantibodies directed against K+ channels of peripheral nerves. Ann. Neurol. 38, 714-722 (1995).
60. Sonoda Y, et al. Serum of Isaacs' syndrome suppresses potassium channels in PC 12 cell lines. Muscle Nerve. 19, 1439-1446 (1996).
61. Nagado T, et al. Potassium current suppression in patients with peripheral nerve hyperexcitability. Brain. 122, 2057-2066 (1999).
62. Buckley C, et al. Potassium channel antibodies in two patients with reversible limbic encephalitis. Ann. Neurol. 50, 73-78 (2001).
63. Vincent A, et al. Potassium channel antibody-Associated encephalopathy: a potentially immunotherapy-responsive form of limbic encephalitis. Brain. 127, 701-712 (2004).
64. Bataller L, et al. Autoimmune limbic encephalitis in 39 patients: immunophenotypes and outcomes. J. Neurol. Neurosurg. Psychiatry. 78, 381-385 (2007).
65. Irani S. R, et al. Antibodies to Kv1 potassium channel complex proteins leucine-rich, glioma inactivated 1 protein and contactin-Associated protein 2 in limbic encephalitis, Morvan's syndrome and acquired neuromyotonia. Brain. 133, 2734-2748 (2010).
66. Lai M, et al. Investigation of LGI1 as the antigen in limbic encephalitis previously attributed to potassium channels: a case series. Lancet Neurol. 9, 776-785 (2010).
67. Poliak S, et al. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG 1. J. Cell Biol. 162, 1149-1160 (2003).
68. Penagarikano O, et al. Absence of CNTNAP2 leads to epilepsy, neuronal migration abnormalities, and core autism-related deficits. Cell. 147, 235-246 (2011).
69. Anderson G. R, et al. Candidate autism gene screen identifies critical role for cell-Adhesion molecule CASPR2 in dendritic arborization and spine development. Proc. Natl Acad. Sci. USA. 109, 18120-18125 (2012).
70. Rodenas-Cuadrado P, Ho J, & Vernes S. C. Shining a light on CNTNAP2: complex functions to complex disorders. Eur. J. Hum. Genet. 22, 171-178 (2014).
71. Senechal K. R, Thaller C, & Noebels J. L. ADPEAF mutations reduce levels of secreted LGI1, a putative tumor suppressor protein linked to epilepsy. Hum. Mol. Genet. 14, 1613-1620 (2005).
72. Tuzun E, & Dalmau J. Limbic encephalitis and variants: classification, diagnosis and treatment. Neurologist. 13, 261-271 (2007).
73. Irani S. R, et al. Faciobrachial dystonic seizures precede Lgi1 antibody limbic encephalitis. Ann. Neurol. 69, 892-900 (2011).
74. Thieben M. J, et al. Potentially reversible autoimmune limbic encephalitis with neuronal potassium channel antibody. Neurology. 62, 1177-1182 (2004).
75. Gultekin S. H, et al. Paraneoplastic limbic encephalitis: neurological symptoms, immunological findings and tumour association in 50 patients. Brain. 123, 1481-1494 (2000).
76. Bernal F, et al. Immunohistochemical analysis of anti Hu associated paraneoplastic encephalomyelitis. Acta Neuropathol. 103, 509-515 (2002).
77. Morante-Redolat J. M, et al. Mutations in the LGI1/.Epitempin gene on 10q24 cause autosomal dominant lateral temporal epilepsy. Hum. Mol. Genet. 11, 1119-1128 (2002).
78. Hawrylycz M. J, et al. An anatomically comprehensive atlas of the adult human brain transcriptome. Nature. 489, 391-399 (2012).
79. Fukata Y, et al. Epilepsy-related ligand/receptor complex LGI1 and ADAM22 regulate synaptic transmission. Science. 313, 1792-1795 (2006).
80. Fukata Y, et al. Disruption of LGI1 linked synaptic complex causes abnormal synaptic transmission and epilepsy. Proc. Natl Acad. Sci. USA. 107, 3799-3804 (2010).
81. Owuor K, et al. LGI1 associated epilepsy through altered ADAM23 dependent neuronal morphology. Mol. Cell Neurosci. 42, 448-457 (2009).
82. Schulte U, et al. The epilepsy-linked Lgi1 protein assembles into presynaptic Kv1 channels and inhibits inactivation by Kvbeta1. Neuron. 49, 697-706 (2006).
83. Chernova O. B, Somerville R. P, & Cowell J. K A novel gene, LGI1, from 10q24 is rearranged and downregulated in malignant brain tumors. Oncogene. 17, 2873-2881 (1998).
84. Ohkawa T, et al. Autoantibodies to epilepsy-related LGI1 in limbic encephalitis neutralize LGI1 ADAM22 interaction and reduce synaptic AMPA receptors. J. Neurosci. 33, 18161-18174 (2013).
85. Lalic T, Pettingill P, Vincent A, & Capogna M. Human limbic encephalitis serum enhances hippocampal mossy fiber CA3 pyramidal cell synaptic transmission. Epilepsia. 52, 121-131 (2011).
86. Irani S. R, et al. Morvan syndrome: clinical and serological observations in 29 cases. Ann. Neurol. 72, 241-255 (2012).
87. Bien C. G, et al. Immunopathology of autoantibody-Associated encephalitides: clues for pathogenesis. Brain. 135, 1622-1638 (2012).
88. Malter M. P, et al. Outcome of limbic encephalitis with VGKC-complex antibodies: relation to antigenic specificity. J. Neurol. 261, 1695-1705 (2014).
89. Butler C. R, et al. Persistent anterograde amnesia following limbic encephalitis associated with antibodies to the voltage-gated potassium channel complex. J. Neurol. Neurosurg. Psychiatry. 85, 387-391 (2014).
90. Klang A, et al. IgG and complement deposition and neuronal loss in cats and humans with epilepsy and voltage-gated potassium channel complex antibodies. J. Neuropathol. Exp. Neurol. 73, 403-413 (2014).
91. Kalachikov S, et al. Mutations in LGI1 cause autosomal-dominant partial epilepsy with auditory features. Nat. Genet. 30, 335-341 (2002).
92. Tessa C, et al. Structural anomaly of left lateral temporal lobe in epilepsy due to mutated LGI1. Neurology. 69, 1298-1300 (2007).
93. Kobayashi E, et al. Magnetic resonance imaging abnormalities in familial temporal lobe epilepsy with auditory auras. Arch. Neurol. 60, 1546-1551 (2003).
94. Chabrol E, et al. Electroclinical characterization of epileptic seizures in leucine-rich, glioma-inactivated 1 deficient mice. Brain. 133, 2749-2762 (2010).
95. Silva J, Sharma S, & Cowell J. K. Homozygous deletion of the LGI1 gene in mice leads to developmental abnormalities resulting in cortical dysplasia. Brain Pathol. 25, 587-597 (2014).
96. Boillot M, et al. Glutamatergic neuron-Targeted loss of LGI1 epilepsy gene results in seizures. Brain. 137, 2984-2996 (2014).
97. Zhou Y. D, et al. Epilepsy gene LGI1 regulates postnatal developmental remodeling of retinogeniculate synapses. J. Neurosci. 32, 903-910 (2012).
98. Boesebeck F, et al. Faciobrachial dystonic seizures arise from cortico-subcortical abnormal brain areas. J. Neurol. 260, 1684-1686 (2013).
99. Plantone D, Renna R, Grossi D, Plantone F, & Iorio R. Teaching NeuroImages: basal ganglia involvement in facio-brachial dystonic seizures associated with LGI1 antibodies. Neurology. 80, e183-e184 (2013).
100. Titulaer M. J, et al. Treatment and prognostic factors for long-Term outcome in patients with anti-NMDA receptor encephalitis: an observational cohort study. Lancet Neurol. 12, 157-165 (2013).
101. Dalmau J, et al. Anti-NMDA-receptor encephalitis: case series and analysis of the effects of antibodies. Lancet Neurol. 7, 1091-1098 (2008).
102. Irani S. R, et al. N methyl-d aspartate antibody encephalitis: temporal progression of clinical and paraclinical observations in a predominantly non-paraneoplastic disorder of both sexes. Brain. 133, 1655-1667 (2010).
103. Dalmau J, Lancaster E, Martinez-Hernandez E, Rosenfeld M. R, & Balice-Gordon R. Clinical experience and laboratory investigations in patients with anti-NMDAR encephalitis. Lancet Neurol. 10, 63-74 (2011).
104. Tuzun E, et al. Evidence for antibody-mediated pathogenesis in anti-NMDAR encephalitis associated with ovarian teratoma. Acta Neuropathol. 118, 737-743 (2009).
105. Vitaliani R, et al. Paraneoplastic encephalitis, psychiatric symptoms, and hypoventilation in ovarian teratoma. Ann. Neurol. 58, 594-604 (2005).
106. Dalmau J, et al. Paraneoplastic anti N methyl-d aspartate receptor encephalitis associated with ovarian teratoma. Ann. Neurol. 61, 25-36 (2007).
107. Day G. S, Laiq S, Tang-Wai D. F, & Munoz D. G. Abnormal neurons in teratomas in NMDAR encephalitis. JAMA Neurol. 71, 717-724 (2014).
108. Hacohen Y, et al. N methyl-d aspartate receptor antibodies in post-herpes simplex virus encephalitis neurological relapse. Mov. Disord. 29, 90-96 (2014).
109. Armangue T, et al. Pediatric anti N methyl-d aspartate receptor encephalitis-clinical analysis and novel findings in a series of 20 patients. J. Pediatr. 162, 850-856.e2 (2013).
110. Mohammad S. S, et al. Herpes simplex encephalitis relapse with chorea is associated with autoantibodies to N methyl-d aspartate receptor or dopamine 2 receptor. Mov. Disord. 29, 117-122 (2014).
111. Armangue T, et al. Herpes simplex virus encephalitis is a trigger of brain autoimmunity. Ann. Neurol. 75, 317-323 (2014).
112. Gleichman A. J, Spruce L. A, Dalmau J, Seeholzer S. H, & Lynch D. R. Anti-NMDA receptor encephalitis antibody binding is dependent on amino acid identity of a small region within the GluN1 amino terminal domain. J. Neurosci. 32, 11082-11094 (2012).
113. Hughes E. G, et al. Cellular and synaptic mechanisms of anti-NMDA receptor encephalitis. J. Neurosci. 30, 5866-5875 (2010).
114. Moscato E. H, et al. Acute mechanisms underlying antibody effects in anti N methyl-d aspartate receptor encephalitis. Ann. Neurol. 76, 108-119 (2014).
115. Mikasova L, et al. Disrupted surface cross-Talk between NMDA and Ephrin B2 receptors in anti-NMDA encephalitis. Brain. 135, 1606-1621 (2012).
116. Nolt M. J, et al. EphB controls NMDA receptor function and synaptic targeting in a subunit-specific manner. J. Neurosci. 31, 5353-5364 (2011).
117. Zhang Q, et al. Suppression of synaptic plasticity by cerebrospinal fluid from anti-NMDA receptor encephalitis patients. Neurobiol. Dis. 45, 610-615 (2012).
118. Manto M, Dalmau J, Didelot A, Rogemond V, & Honnorat J. In vivo effects of antibodies from patients with anti-NMDA receptor encephalitis: further evidence of synaptic glutamatergic dysfunction. Orphanet J. Rare Dis. 5, 31 (2010).
119. Manto M, Dalmau J, Didelot A, Rogemond V, & Honnorat J. Afferent facilitation of corticomotor responses is increased by IgGs of patients with NMDA-receptor antibodies. J. Neurol. 258, 27-33 (2011).
120. Finke C, et al. Cognitive deficits following anti-NMDA receptor encephalitis. J. Neurol. Neurosurg. Psychiatry. 83, 195-198 (2012).
121. Finke C, et al. Structural hippocampal damage following anti N methyl-d aspartate receptor encephalitis. Biol. Psychiatry http://dx.doi.org/.10.1016/j.biopsych.2015.02.024 (2015).
122. Planaguma J, et al. Human N methyl d aspartate receptor antibodies alter memory and behaviour in mice. Brain. 138, 94-109 (2015).
123. Wright S, et al. Epileptogenic effects of NMDAR antibodies in a passive transfer mouse model. Brain. 138, 3159-3167 (2015).
124. Ohba C, et al. GRIN1 mutations cause encephalopathy with infantile-onset epilepsy, and hyperkinetic and stereotyped movement disorders. Epilepsia. 56, 841-848 (2015).
125. Redin C, et al. Efficient strategy for the molecular diagnosis of intellectual disability using targeted high-Throughput sequencing. J. Med. Genet. 51, 724-736 (2014).
126. Epi K. C, et al. De novo mutations in epileptic encephalopathies. Nature. 501, 217-221 (2013).
127. Lodge D, & Mercier M. S. Ketamine and phencyclidine: the good, the bad and the unexpected. Br. J. Pharmacol. 172, 4254-4276 (2015).
128. Meinck H. M, & Thompson P. D. Stiff man syndrome and related conditions. Mov. Disord. 17, 853-866 (2002).
129. Brown P, & Marsden C. D. The stiff man and stiff man plus syndromes. J. Neurol. 246, 648-652 (1999).
130. Carvajal-Gonzalez A, et al. Glycine receptor antibodies in PERM and related syndromes: characteristics, clinical features and outcomes. Brain. 137, 2178-2192 (2014).
131. Durisic N, et al. Stoichiometry of the human glycine receptor revealed by direct subunit counting. J. Neurosci. 32, 12915-12920 (2012).
132. Malosio M. L, Marqueze-Pouey B, Kuhse J, & Betz H. Widespread expression of glycine receptor subunit mRNAs in the adult and developing rat brain. EMBO J. 10, 2401-2409 (1991).
133. Sato K, Kiyama H, & Tohyama M. Regional distribution of cells expressing glycine receptor alpha 2 subunit mRNA in the rat brain. Brain Res. 590, 95-108 (1992).
134. Dreissen Y. E, & Tijssen M. A. The startle syndromes: physiology and treatment. Epilepsia 53 (Suppl. 7), 3-11 (2012).
135. Peeters E, et al. Supranuclear gaze palsy in glycine receptor antibody-positive progressive encephalomyelitis with rigidity and myoclonus. Mov. Disord. 27, 1830-1832 (2012).
136. Clerinx K, et al. Progressive encephalomyelitis with rigidity and myoclonus: resolution after thymectomy. Neurology. 76, 303-304 (2011).
137. Ahmadi S, Lippross S, Neuhuber W. L, & Zeilhofer H. U. PGE2 selectively blocks inhibitory glycinergic neurotransmission onto rat superficial dorsal horn neurons. Nat. Neurosci. 5, 34-40 (2002).
138. Foster E, et al. Targeted ablation, silencing, and activation establish glycinergic dorsal horn neurons as key components of a spinal gate for pain and itch. Neuron. 85, 1289-1304 (2015).
139. Horn A. K, Buttner-Ennever J. A, Wahle P, & Reichenberger I. Neurotransmitter profile of saccadic omnipause neurons in nucleus raphe interpositus. J. Neurosci. 14, 2032-2046 (1994).
140. Iwamoto Y, Kaneko H, Yoshida K, & Shimazu H. Role of glycinergic inhibition in shaping activity of saccadic burst neurons. J. Neurophysiol. 101, 3063-3074 (2009).
141. Waldvogel H. J, et al. Differential localization of gamma-Aminobutyric acid type A and glycine receptor subunits and gephyrin in the human pons, medulla oblongata and uppermost cervical segment of the spinal cord: an immunohistochemical study. J. Comp. Neurol. 518, 305-328 (2010).
142. Lynch J. W. Native glycine receptor subtypes and their physiological roles. Neuropharmacology. 56, 303-309 (2009).
143. Meinck H. M. Startle and its disorders. Neurophysiol. Clin. 36, 357-364 (2006).
144. Becker C. M, Hoch W, & Betz H. Glycine receptor heterogeneity in rat spinal cord during postnatal development. EMBO J. 7, 3717-3726 (1988).
145. Jonsson S, et al. Changes in glycine receptor subunit expression in forebrain regions of the Wistar rat over development. Brain Res. 1446, 12-21 (2012).
146. Liu Q, & Wong-Riley M. T. Postnatal development of glycine receptor subunits a1, a2, a3, and β immunoreactivity in multiple brain stem respiratory-related nuclear groups of the rat. Brain Res. 1538, 1-16 (2013).
147. Lall D, Armbruster A, Ruffert K, Betz H, & Eulenburg V. Transport activities and expression patterns of glycine transporters 1 and 2 in the developing murine brain stem and spinal cord. Biochem. Biophys. Res. Commun. 423, 661-666 (2012).
148. Graham B. A, Schofield P. R, Sah P, Margrie T. W, & Callister R. J. Distinct physiological mechanisms underlie altered glycinergic synaptic transmission in the murine mutants spastic, spasmodic, and oscillator. J. Neurosci. 26, 4880-4890 (2006).
149. Stephenson J. B. Vigabatrin for startle-disease with altered cerebrospinal-fluid free gamma-Aminobutyric acid. Lancet. 340, 430-431 (1992).
150. Piotrowicz A, Thumen A, Leite M. I, Vincent A, & Moser A A case of glycine-receptor antibody-Associated encephalomyelitis with rigidity and myoclonus (PERM): clinical course, treatment and CSF findings. J. Neurol. 258, 2268-2270 (2011).
151. Liguori R, et al. Morvan's syndrome: peripheral and central nervous system and cardiac involvement with antibodies to voltage-gated potassium channels. Brain. 124, 2417-2426 (2001).
152. Garty B. Z, Ludomirsky A, Danon Y. L, Peter J. B, & Douglas S. D. Placental transfer of immunoglobulin G subclasses. Clin. Diagn. Lab Immunol. 1, 667-669 (1994).
153. Firan M, et al. The MHC class I related receptor, FcRn, plays an essential role in the maternofetal transfer of gamma-globulin in humans. Int. Immunol. 13, 993-1002 (2001).
154. Vernet-der Garabedian B, et al. Association of neonatal myasthenia gravis with antibodies against the fetal acetylcholine receptor. J. Clin. Invest. 94, 555-559 (1994).
155. Jacobson L, Polizzi A, Morriss-Kay G, & Vincent A. Plasma from human mothers of fetuses with severe arthrogryposis multiplex congenita causes deformities in mice. J. Clin. Invest. 103, 1031-1038 (1999).
156. Riemersma S, et al. Association of arthrogryposis multiplex congenita with maternal antibodies inhibiting fetal acetylcholine receptor function. J. Clin. Invest. 98, 2358-2363 (1996).
157. Hesselmans L. F, Jennekens F. G, Van den Oord C. J, Veldman H, & Vincent A. Development of innervation of skeletal muscle fibers in man: relation to acetylcholine receptors. Anat. Rec. 236, 553-562 (1993).
158. Yashiro K, & Philpot B. D. Regulation of NMDA receptor subunit expression and its implications for LTD, LTP, and metaplasticity. Neuropharmacology. 55, 1081-1094 (2008).
159. Olsen R. W, & Sieghart W. G.A.B. A A receptors: subtypes provide diversity of function and pharmacology. Neuropharmacology. 56, 141-148 (2009).
160. Moody W. J, & Bosma M. M. Ion channel development, spontaneous activity, and activity-dependent development in nerve and muscle cells. Physiol. Rev. 85, 883-941 (2005).
161. Luhmann H. J, Fukuda A, & Kilb W. Control of cortical neuronal migration by glutamate and GABA. Front. Cell Neurosci. 9, 4 (2015).
162. Komuro H, & Rakic P. Orchestration of neuronal migration by activity of ion channels, neurotransmitter receptors, and intracellular Ca2+ fluctuations. J. Neurobiol. 37, 110-130 (1998).
163. Lee J. Y, et al. Neurotoxic autoantibodies mediate congenital cortical impairment of offspring in maternal lupus. Nat. Med. 15, 91-96 (2009).
164. Kayser M. S, Titulaer M. J, Gresa-Arribas N, & Dalmau J. Frequency and characteristics of isolated psychiatric episodes in anti N methyl-d aspartate receptor encephalitis. JAMA Neurol. 70, 1133-1139 (2013).
165. Zandi M. S, et al. Immunotherapy for patients with acute psychosis and serum N methyl d aspartate receptor (NMDAR) antibodies: a description of a treated case series. Schizophr. Res. 160, 193-195 (2014).
166. Steiner J, et al. Increased prevalence of diverse N methyl-d aspartate glutamate receptor antibodies in patients with an initial diagnosis of schizophrenia: specific relevance of IgG NR1a antibodies for distinction from N methyl-d aspartate glutamate receptor encephalitis. JAMA Psychiatry. 70, 271-278 (2013).
167. de Witte L. D, et al. Absence of N methyl-d aspartate receptor IgG autoantibodies in schizophrenia: the importance of cross-validation studies. JAMA Psychiatry. 72, 731-733 (2015).
168. Brenner T, et al. Prevalence of neurologic autoantibodies in cohorts of patients with new and established epilepsy. Epilepsia. 54, 1028-1035 (2013).
169. Suleiman J, Brilot F, Lang B, Vincent A, & Dale R. C. Autoimmune epilepsy in children: case series and proposed guidelines for identification. Epilepsia. 54, 1036-1045 (2013).
170. Busse S, et al. N methyl-d aspartate glutamate receptor (NMDA R) antibodies in mild cognitive impairment and dementias. Neurosci. Res. 85, 58-64 (2014).
171. Doss S, et al. High prevalence of NMDA receptor IgA/.IgM antibodies in different dementia types. Ann. Clin. Transl. Neurol. 1, 822-832 (2014).
172. Hammer C, et al. Neuropsychiatric disease relevance of circulating anti-NMDA receptor autoantibodies depends on blood-brain barrier integrity. Mol. Psychiatry. 19, 1143-1149 (2014).
173. Zerche M, et al. Preexisting serum autoantibodies against the NMDAR subunit NR1 modulate evolution of lesion size in acute ischemic stroke. Stroke. 46, 1180-1186 (2015).
174. Edelman G. M, et al. The covalent structure of an entire gammaG immunoglobulin molecule. Proc. Natl Acad. Sci. USA. 63, 78-85 (1969).
175. Schroeder H. W. Jr & Cavacini L. Structure and function of immunoglobulins. J. Allergy Clin. Immunol. 125, S41-S552 (2010).
176. Vidarsson G, Dekkers G, & Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front. Immunol. 5, 520 (2014).
177. Davies A. M, & Sutton B. J. Human IgG4: a structural perspective. Immunol. Rev. 268, 139-159 (2015).
178. Andrew S. M, & Titus J. A. Fragmentation of immunoglobulin G. Curr. Protoc. Cell Biol. 17, 16.4.1-16.4.10 (2003).
179. Kortvelyessy P, et al. Complement-Associated neuronal loss in a patient with CASPR2 antibody-Associated encephalitis. Neurol. Neuroimmunol. Neuroinflamm. 2, e75 (2015).
180. Hoftberger R, et al. Encephalitis and AMPA receptor antibodies: novel findings in a case series of 22 patients. Neurology. 84, 2403-2412 (2015).
181. Joubert B, et al. Clinical spectrum of encephalitis associated with antibodies against the a-Amino 3 hydroxy 5 methyl 4 isoxazolepropionic acid receptor: case series and review of the literature. JAMA Neurol. 72, 1163-1169 (2015).
182. Lai M, et al. AMPA receptor antibodies in limbic encephalitis alter synaptic receptor location. Ann. Neurol. 65, 424-434 (2009).
183. Peng X, et al. Cellular plasticity induced by anti-A-Amino 3 hydroxy 5 methyl 4 isoxazolepropionic acid (AMPA) receptor encephalitis antibodies. Ann. Neurol. 77, 381-398 (2015).
184. Pettingill P, et al. Antibodies to GABAA receptor a1 and ?2 subunits: clinical and serologic characterization. Neurology. 84, 1233-1241 (2015).
185. Petit-Pedrol M, et al. Encephalitis with refractory seizures, status epilepticus, and antibodies to the GABAA receptor: a case series, characterisation of the antigen, and analysis of the effects of antibodies. Lancet Neurol. 13, 276-286 (2014).
186. Hoftberger R, et al. Encephalitis and GABAB receptor antibodies: novel findings in a new case series of 20 patients. Neurology. 81, 1500-1506 (2013).
187. Dogan Onugoren M, et al. Limbic encephalitis due to GABAB and AMPA receptor antibodies: a case series. J. Neurol. Neurosurg. Psychiatry. 86, 965-972 (2015).
188. Lancaster E, et al. Antibodies to the GABAB receptor in limbic encephalitis with seizures: case series and characterisation of the antigen. Lancet Neurol. 9, 67-76 (2010).
189. Boronat A, et al. Encephalitis and antibodies to dipeptidyl-peptidase-like protein 6, a subunit of Kv4.2 potassium channels. Ann. Neurol. 73, 120-128 (2013).
190. Balint B, et al. Progressive encephalomyelitis with rigidity and myoclonus: a new variant with DPPX antibodies. Neurology. 82, 1521-1528 (2014).
191. Piepgras J, et al. Anti-DPPX encephalitis: pathogenic effects of antibodies on gut and brain neurons. Neurology. 85, 890-897 (2015).
192. Dale R. C, et al. Antibodies to surface dopamine 2 receptor in autoimmune movement and psychiatric disorders. Brain. 135, 3453-3468 (2012).
193. Sabater L, et al A novel non-rapid-eye movement and rapid-eye-movement parasomnia with sleep breathing disorder associated with antibodies to IgLON5: a case series, characterisation of the antigen, and post-mortem study. Lancet Neurol. 13, 575-586 (2014).
194. Sillevis Smitt P, et al. Paraneoplastic cerebellar ataxia due to autoantibodies against a glutamate receptor. N. Engl. J. Med. 342, 21-27 (2000).
195. Coesmans M, et al. Mechanisms underlying cerebellar motor deficits due to mGluR1 autoantibodies. Ann. Neurol. 53, 325-336 (2003).
196. Lancaster E, et al. Antibodies to metabotropic glutamate receptor 5 in the Ophelia syndrome. Neurology. 77, 1698-1701 (2011).