Neuromyotonia and limbic encephalitis sera target mature Shaker-type K + channels: Subunit specificity correlates with clinical manifestations

Brain

Volumn 129, Issue 6, 2006, Pages 1570-1584

  Kleopa, Kleopas A ^a   Elman, Lauren B ^b   Lang, Bethan ^c   Vincent, Angela ^c   Scherer, Steven S ^b  

^a CYPRUS INSTITUTE OF NEUROLOGY AND GENETICS   (Cyprus)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

Hippocampus; Ion channels; Juxtaparanodes; Morvan's syndrome; Myokymia

Indexed keywords

POTASSIUM CHANNEL; POTASSIUM CHANNEL SUBUNIT KV1; POTASSIUM CHANNEL SUBUNIT KV1.1; POTASSIUM CHANNEL SUBUNIT KV1.2; POTASSIUM CHANNEL SUBUNIT KV1.6; UNCLASSIFIED DRUG; AUTOANTIBODY; BIOLOGICAL MARKER; KCNA6 PROTEIN, HUMAN; POTASSIUM CHANNEL KV1.1; POTASSIUM CHANNEL KV1.2; SHAKER POTASSIUM CHANNEL;

ADULT; AGED; ANIMAL TISSUE; ARTICLE; CEREBELLUM; CLINICAL ARTICLE; CONTROLLED STUDY; FEMALE; HELA CELL; HIPPOCAMPUS; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; MYOKYMIA; NONHUMAN; PARANEOPLASTIC NEUROPATHY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCIATIC NERVE; SERUM; SPINAL CORD; ADOLESCENT; ANIMAL; ANTIBODY SPECIFICITY; AUTOIMMUNE DISEASE; BLOOD; BRAIN; GENETIC TRANSFECTION; IMMUNOLOGY; MIDDLE AGED; PERIPHERAL NERVE; SYNAPTOSOME; SYRINGOMYELIA;

ADOLESCENT; ADULT; AGED; ANIMALS; ANTIBODY SPECIFICITY; AUTOANTIBODIES; AUTOIMMUNE DISEASES; BIOLOGICAL MARKERS; BRAIN; FEMALE; HELA CELLS; HIPPOCAMPUS; HUMANS; ISAACS SYNDROME; KV1.1 POTASSIUM CHANNEL; KV1.2 POTASSIUM CHANNEL; LIMBIC ENCEPHALITIS; MALE; MICE; MIDDLE AGED; PERIPHERAL NERVES; PRESYNAPTIC TERMINALS; SHAKER SUPERFAMILY OF POTASSIUM CHANNELS; SPINAL CORD; SYRINGOMYELIA; TRANSFECTION;

EID: 33745105091     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awl084     Document Type: Article

References (61)

1. Ances BM, Vitaliani R, Taylor RA, Liebeskind DS, Voloschin A, Houghton DJ, et al. Treatment-responsive limbic encephalitis identified by neuropil antibodies: MRI and PET correlates. Brain 2005; 128: 1764-77.
2. Antozzi C, Frassoni C, Vincent A, Regondi MC, Andreetta F, Bernasconi P, et al. Sequential antibodies to potassium channels and glutamic acid decarboxylase in neuromyotonia. Neurology 2005; 64: 1290-3.
3. Arimura K, Watanabe O, Kitajima I, Suehara M, Minato S, Sonoda Y, et al. Antibodies to potassium channels of PC12 in serum of Isaacs' syndrome: western blot and immunohistochemical studies. Muscle Nerve 1997; 20: 299-305.
4. Arimura K, Arimura Y, Ng A, Uehara A, Nakae M, Osame M, et al. The origin of spontaneous discharges in acquired neuromyotonia. A macro EMG study. Clin Neurophysiol 2005; 116: 1835-9.
5. Arroyo EJ, Xu YT, Zhou L, Messing A, Peles E, Chiu SY, et al. Myelinating Schwann cells determine the internodal localization of Kv1.1, Kv1.2, Kvβ2, and Caspr. J Neurocytol 1999; 28: 333-47.
6. Auger RG. AAEM minimonograph no. 44: diseases associated with excess motor unit activity. Muscle Nerve 1994; 17: 1250-63.
7. Browne DL, Gancher ST, Nutt JG, Brunt ER, Smith EA, Kramer P, et al. Episodic ataxia/myokymia syndrome is associated with point mutations in the human potassium channel gene, KCNA1. Nat Genet 1994; 8: 136-40.
8. Buckley C, Oger J, Clover L, Tuzun E, Carpenter K, Jackson M, et al. Potassium channel antibodies in two patients with reversible limbic encephalitis. Ann Neurol 2001; 50: 73-8.
9. Campomanes CR, Carroll KI, Manganas LN, Hershberger ME, Gong B, Antonucci D, et al. Kv beta subunit oxidoreductase activity and Kv1 potassium channel trafficking. J Biol Chem 2002; 277: 8298-305.
10. Chiu SY, Zhou L, Zhang CL, Messing A. Analysis of potassium channel functions in mammalian axons by gene knockouts. J Neurocytol 1999; 28: 349-64.
11. Chung YH, Shin C, Kim MJ, Lee BK, Cha CI. Immunohistochemical study on the distribution of six members of the Kv1 channel subunits in the rat cerebellum. Brain Res 2001; 895: 173-7.
12. Chung YH, Joo KM, Nam RH, Kim YS, Lee WB, Cha CI. Immunohistochemical study on the distribution of the voltage-gated potassium channels in the gerbil cerebellum. Neurosci Lett 2005; 374: 58-62.
13. Corrette BJ, Repp H, Dreyer F, Schwarz JR. Two types of fast K+ channels in rat myelinated fibres and their sensitivity to dendrotoxin. Pflugers Arch 1991; 418: 408-16.
14. Dalmau J, Furneaux HM, Gralla RJ, Kris MG, Posner JB. Detection of the anti-Hu antibody in the serum of patients with small cell lung cancer-A quantitative western blot analysis. Ann Neurol 1990; 27: 544-52.
15. Devaux J, Alcaraz G, Grinspan J, Bennett V, Joho R, Crest M, et al. Kv3.1b is a novel component of CNS nodes. J Neurosci 2003; 23: 4509-18.
16. Devaux JJ, Kleopa KA, Cooper EC, Scherer SS. KCNQ2 is a nodal K+ channel. J Neurosci 2004; 24: 1236-44.
17. Eunson LH, Rea R, Zuberi SM, Youroukos S, Panayiotopoulos CP, Liguori R, et al. Clinical, genetic, and expression studies of mutations in the potassium channel gene KCNA1 reveal new phenotypic variability. Ann Neurol 2000; 48: 647-56.
18. Hart IK, Waters C, Vincent A, Newland C, Beeson D, Pongs O, et al. Autoantibodies detected to expressed K+ channels are implicated in neuromyotonia. Ann Neurol 1997; 41: 238-46.
19. Hart IK, Maddison P, Newsom-Davis J, Vincent A, Mills KR. Phenotypic variants of autoimmune peripheral nerve hyperexcitability. Brain 2002; 125: 1887-95.
20. Isaacs H. A syndrome of continuous muscle-fibre activity. J Neurol Neurosurg Psychiatry 1961; 24: 319-25.
21. Johnston D, Hoffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, et al. Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol 2000; 525: 75-81.
22. Koch RO, Wanner SG, Koschak A, Hanner M, Schwarzer C, Kaczorowski GJ, et al. Complex subunit assembly of neuronal voltage-gated K+ channels. Basis for high-affinity toxin interactions and pharmacology. J Biol Chem 1997; 272: 27577-81.
23. Laube G, Roper J, Pitt JC, Sewing S, Kistner U, Garner CC, et al. Ultrastructural localization of Shaker-related potassium channel subunits and synapse-associated protein 90 to septate-like junctions in rat cerebellar cortex. Brain Res Mol Brain Res 1996; 42: 51-61.
24. Lee EK, Maselli RA, Ellis WG, Agius MA. Morvan's fibrillary chorea: a paraneoplastic manifestation of thymoma. J Neurol Neurosurg Psychiatry 1998; 65: 857-62.
25. Liguori R, Vincent A, Clover L, Avoni P, Plazzi G, Cortelli P, et al. Morvan's syndrome: peripheral and central nervous system and cardiac involvement with antibodies to voltage-gated potassium channels. Brain 2001; 124: 2417-26.
26. Manganas LN, Trimmer JS. Subunit composition determines Kv1 potassium channel surface expression. J Biol Chem 2000; 275: 29685-93.
27. Mason WP, Graus F, Lang B, Honnorat J, Delattre JY, Valldeoriola F, et al. Small-cell lung cancer, paraneoplastic cerebellar degeneration and the Lambert-Eaton myasthenic syndrome. Brain 1997; 120: 1279-300.
28. Matus-Leibovitch N, Vogel Z, Ezra-Macabee V, Etkin S, Nevo I, Attali B. Chronic morphine administration enhances the expression of Kv1.5 and Kv1.6 voltage-gated K+ channels in rat spinal cord. Brain Res Mol Brain Res 1996; 40: 261-70.
29. + channel containing the α subunit Kv1.2 in the basket cell nerve terminals of rat cerebellum. Neuroscience 1993; 57: 1039-45.
30. McNamara JO, Whitney KD, Andrews PI, He XP, Janumpalli S, Patel MN. Evidence for glutamate receptor autoimmunity in the pathogenesis of Rasmussen encephalitis. Adv Neurol 1999; 79: 543-50.
31. Monaghan MM, Trimmer JS, Rhodes KJ. Experimental localization of Kv1 family voltage-gated K+ channel alpha and beta subunits in rat hippocampal formation. J Neurosci 2001; 21: 5973-83.
32. Nagado T, Arimura K, Sonoda Y, Kurono A, Horikiri Y, Kameyama A, et al. Potassium current suppression in patients with peripheral nerve hyperexcitability. Brain 1999; 122: 2057-66.
33. Newsom-Davis J. Autoimmune neuromyotonia (Isaac's syndrome): an antibody-mediated potassium channelopathy. Ann N Y Acad Sci 1997; 835: 111-9.
34. Newsom-Davis J, Mills KR. Immunological associations of acquired neuromyotonia (Isaacs' syndrome). Report of five cases and literature review. Brain 1993; 116: 453-69.
35. Newsom-Davis J, Buckley C, Clover L, Hart I, Maddison P, Tuzum E, et al. Autoimmune disorders of neuronal potassium channels. Ann N Y Acad Sci 2003; 998: 202-10.
36. Poliak S, Salomon D, Elhanany H, Sabanay H, Kiernan B, Pevny L, et al. Juxtaparanodal clustering of Shaker-like K+ channels in myelinated axons depends on Caspr2 and TAG-1. J Cell Biol 2003; 162: 1149-60.
37. Rasband MN, Trimmer JS, Schwarz TL, Levinson SR, Ellisman MH, Schachner M, et al. Potassium channel distribution, clustering, and function in remyelinating rat axons. J Neurosci 1998; 18: 36-47.
38. + channel distribution and clustering in developing and hypomyelinated axons of the optic nerve. J Neurocytol 1999; 28: 319-31.
39. Reid G, Scholz A, Bostock H, Vogel W. Human axons contain at least five types of voltage-dependent potassium channel. J Physiol 1999; 518: 681-96.
40. + channel complexes. J Neurosci 1997; 17: 8246-258.
41. Roper J, Schwarz JR. Heterogeneous distribution of fast and slow potassium channels in myelinated rat nerve fibres. J Physiol 1989; 416: 93-110.
42. Safronov BV, Kampe K, Vogel W. Single voltage-dependent potassium channels in rat peripheral nerve membrane. J Physiol 1993; 460: 675-91.
43. Sheng M, Liao YJ, Jan YN, Jan LY. Presynaptic A-current based on heteromultimeric K+ channels detected in vivo. Nature 1993; 365: 72-5.
44. Sheng M, Tsaur ML, Jan YN, Jan LY. Contrasting subcellular localization of the Kv1.2 K+ channel subunit in different neurons of rat brain. J Neurosci 1994; 14: 2408-17.
45. Shi G, Nakahira K, Hammond S, Rhodes KJ, Schechter LE, Trimmer JS. Beta subunits promote K+ channel surface expression through effects early in biosynthesis. Neuron 1996; 16: 843-52.
46. Shillito P, Molenaar PC, Vincent A, Leys K, Zheng W, van den Berg RJ, et al. Acquired neuromyotonia: evidence for autoantibodies directed against K+ channels of peripheral nerves. Ann Neurol 1995; 38: 714-22.
47. Smart SL, Lopantsev V, Zhang CL, Robbins CA, Wang H, Chiu SY, et al. Deletion of the Kv1.1 potassium channel causes epilepsy in mice. Neuron 1998; 20: 809-19.
48. Sonoda Y, Arimura K, Kurono A, Suehara M, Kameyama M, Minato S, et al. Serum of Isaacs' syndrome suppresses potassium channels in PC-12 cell lines. Muscle Nerve 1996; 19: 1439-46.
49. Southan AP, Owen DG. The contrasting effects of dendrotoxins and other potassium channel blockers in the CA1 and dentate gyrus regions of rat hippocampal slices. Br J Pharmacol 1997; 122: 335-43.
50. Stuhmer W, Ruppersberg JP, Schroter KH, Sakmann B, Stocker M, Giese KP, et al. Molecular basis of functional diversity of voltage-gated potassium channels in mammalian brain. EMBO J 1989; 8: 3235-44.
51. Sutton I, Winer J, Rowlands D, Dalmau J. Limbic encephalitis and antibodies to Ma2: a paraneoplastic presentation of breast cancer. J Neurol Neurosurg Psychiatry 2000; 69: 266-8.
52. Thieben MJ, Lennon VA, Boeve BF, Aksamit AJ, Keegan M, Vernino S. Potentially reversible autoimmune limbic encephalitis with neuronal potassium channel antibody. Neurology 2004; 62: 1177-82.
53. Tomimitsu H, Arimura K, Nagado T, Watanabe O, Otsuka R, Kurono A, et al. Mechanism of action of voltage-gated K+ channel antibodies in acquired neuromyotonia. Ann Neurol 2004; 56: 440-4.
54. Traka M, Goutebroze L, Denisenko N, Bessa M, Nifli A, Havaki S, et al. Association of TAG-1 with Caspr2 is essential for the molecular organization of juxtaparanodal regions of myelinated fibers. J Cell Biol 2003; 162: 1161-72.
55. Vabnick I, Trimmer JS, Schwarz TL, Levinson SR, Risal D, Shrager P. Dynamic potassium channel distributions during axonal development prevent aberrant firing patterns. J Neurosci 1999; 19: 747-58.
56. Vincent A. Understanding neuromyotonia. Muscle Nerve 2000; 23: 655-7.
57. Vincent A, Buckley C, Schott JM, Baker I, Dewar BK, Detert N, et al. Potassium channel antibody-associated encephalopathy: a potentially immunotherapy-responsive form of limbic encephalitis. Brain 2004; 127: 701-12.
58. Wang H, Kunkel DD, Martin TM, Schwartkroin PA, Tempel BL. Heteromultimeric K+ channels in terminal and juxtaparanodal regions of neurons. Nature 1993; 365: 75-9.
59. Wang H, Kunkel DD, Schwartzkroin PA, Tempel BL. Localization of Kv1.1 and Kv1.2, two K channel proteins, to synaptic terminals, somata, and dendrites in the mouse brain. J Neurosci 1994; 14: 4588-99.
60. Zerr P, Adelman JP, Maylie J. Episodic ataxia mutations in Kv1.1 alter potassium channel function by dominant negative effects or haploinsufficiency. J Neurosci 1998; 18: 2842-8.
61. Zhou L, Zhang CL, Messing A, Chiu SY. Temperature-sensitive neuromuscular transmission in Kv1.1 null mice: role of potassium channels under the myelin sheath in young nerves. J Neurosci 1998; 18: 7200-15.