Lambert-eaton antibodies inhibit Ca2+ currents but paradoxically increase exocytosis during stimulus trains in bovine adrenal chromaffin cells

Journal of Neuroscience

Volumn 19, Issue 9, 1999, Pages 3384-3395

  Engisch, Kathrin L ^a,c   Rich, Mark M ^b,c   Cook, Noah ^a   Nowycky, Martha C ^a,d  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Ca2+ secretion coupling; Capacitance detection; Chromaffin cell; Exocytosis; Facilitation; Lambert Eaton myasthenic syndrome

Indexed keywords

AUTOANTIBODY; CALCIUM ION; IMMUNOGLOBULIN G;

ADULT; AGED; ANIMAL CELL; ARTICLE; AUTOIMMUNE DISEASE; CALCIUM CURRENT; CATTLE; CHROMAFFIN CELL; CLINICAL ARTICLE; CONTROLLED STUDY; EATON LAMBERT SYNDROME; EXOCYTOSIS; FEMALE; HUMAN; ION CURRENT; MALE; MYASTHENIA; NEUROMUSCULAR TRANSMISSION; NONHUMAN; PRIORITY JOURNAL;

EID: 0033135521     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.19-09-03384.1999     Document Type: Article

References (66)

1. Artalejo CR, Ariano MA, Perlman RL, Fox AP (1990) Activation of facilitation calcium channels in chromaffin cells by D1 dopamine receptors through a cAMP/protein kinase A-dependent mechanism. Nature 348:239-242.
2. Artalejo CR, Dahmer MK, Perlman RL, Fox AP (1991a) Two types of Ca2f currents are found in bovine chromaffin cells: facilitation is due to the recruitment of one type. J Physiol (Lond) 432:681-707.
3. 2+ channels: facilitation increases the opening probability of a 27 pS channel. J Physiol (Lond) 444:213-240.
4. Blandino JK, Kim YI (1993) Lambert-Eaton syndrome IgG inhibits dihydropyridine-sensitive, slowly inactivating calcium channels in bovine adrenal chromaffin cells. Ann NY Acad Sci 681:394-397.
5. Blandino JKW, Viglione MP, Bradley WA, Oie HK, Kim YI (1995) Voltage-dependent sodium channels in human small-cell lung cancer cells: role in action potentials and inhibition by Lambert-Eaton syndrome IgG. J Membr Biol 143:153-163.
6. Burgoyne RD, Morgan A (1998) Analysis of regulated exocytosis in adrenal chromaffin cells: insights into NSF/SNAP/SNARE function. BioEssays 20:328-335.
7. 1A subunit of the P/Q-type calcium channel. EMBO J 16:4591-4596.
8. Chow RH, Klingauf J, Heinemann C, Zucker RS, Neher E (1996) Mechanisms determining the time course of secretion in neuroendocrine cells. Neuron 16:369-376.
9. Cooke JD, Okamoto K, Quastel DMJ (1973) The role of calcium in depolarization secretion coupling at the motor nerve terminal. J Physiol (Lond) 228:459-497.
10. Cull-Candy SO, Lundh H, Thesleff S (1976) Effects of botulinum toxin on neuromuscular transmission in the rat. J Physiol (Lond) 260:177-203.
11. Cull-Candy SG, Miledi R, Trautmann A, Uchitel OD (1980) On the release of transmitter at normal, myasthenia gravis and myasthenic syndrome affected human end-plates. J Physiol (Lond) 299:621-638.
12. Del Castillo J, Katz B (1954) The effect of magnesium on the activity of motor nerve endings. J Physiol (Lond) 124:553-559.
13. Dodge FA, Rahamimoff R (1967) Cooperative action of calcium ions in transmitter release at the neuromuscular junction. J Physiol (Lond) 193:419-433.
14. Elhamdani A, Zhou Z, Artalejo CR (1998) Timing of dense-core vesicle exocytosis depends on the facilitation L-type Ca channel in adrenal chromaffin cells. J Neurosci 18:6230-6240.
15. Elmqvist D, Lambert EH (1968) Detailed analysis of neuromuscular transmission in a patient with myasthenic syndrome sometimes associated with bronchogenic carcinoma. Mayo Clin Proc 43:689-713.
16. Elmqvist D, Quastel DMJ (1965) A quantitative study of end-plate potentials in isolated human muscle. J Physiol (Lond) 178:505-529.
17. Engel AG (1991) Review of evidence for loss of motor nerve terminal calcium channels in Lambert-Eaton myasthenic syndrome. Ann NY Acad Sci 635:246-258.
18. Engisch KL, Nowycky MC (1996) Calcium dependence of large dense-cored vesicle exocytosis evoked by calcium influx in bovine adrenal chromaffin cells. J Neurosci 16:1359-1369.
19. 2+-exocytosis relationship during repetitive pulse protocols in bovine adrenal chromaffin cells. J Neurosci 17:9010-9025.
20. Fidler N, Fernandez JM (1989) Phase tracking: an improved phase detection technique for cell membrane capacitance measurements. Biophys J 56:1153-1162.
21. Fukunaga H, Engel AG, Osame M, Lambert EH (1982) Paucity and disorganization of presynaptic membrane active zones in the Lambert-Eaton myasthenic syndrome. Muscle Nerve 5:686-697.
22. Garcia KD, Beam KG (1996) Reduction of calcium currents by Lambert-Eaton syndrome sera: motoneurons are preferentially affected, and L-type currents are spared. J Neurosci 16:4903-4913.
23. Garcia KD, Mynlieff M, Sanders DB, Beam KG, Walrond JP (1996) Lambert-Eaton sera reduce low-voltage and high-voltage activated Ca2+ currents in murinc dorsal root ganglion neurons. Proc Natl Acad Sci USA 93:9264-9269.
24. 2+ channels of human neuroblastoma IMR32 cells by Lambert-Eaton myasthenic syndrome (LEMS) IgGs. Neurosci Lett 181:50-56.
25. Hajela RK, Atchison WD (1995) The proteins synaptotagmin and syntaxin are not general targets of Lambert-Eaton myasthenic syndrome autoantibody. J Neurochem 64:1245-1251.
26. Horrigan FT, Bookman RJ (1993) Na channel gating charge movement is responsible for the transient capacitance increase evoked by depolarization in rat adrenal chromaffin cells. Biophys J 64:A101.
27. Hubbard JI, Jones SF, Landau EM (1968) On the mechanism by which calcium and magnesium affect the release of transmitter by nerve impulses. J Physiol (Lond) 196:75-86.
28. Johnston l, Lang B, Leys K, Newsom-Davis J (1994) Heterogeneity of calcium channel autoantibodies detected using a small-cell lung cancer line derived from a Lambert-Eaton myasthenic syndrome patient. Neurology 44:334-338.
29. Joshi C, Fernandez JM (1988) Capacitance measurements. An analysis of the phase detector technique used to study exocytosis and endocytosis. Biophys J 53:885-892.
30. 2+ and short-term synaptic plasticity. Nature 371:603-606.
31. Katz B, Miledi R (1968) The role of calcium in neuromuscular facilitation. J Physiol (Lond) 195:481-492.
32. Katz JS, Wolfe GI, Bryan WW, Tintner R, Barohn RJ (1998) Acetylcholine receptor antibodies in the Lambert-Eaton myasthenic syndrome. Neurology 50:470-475.
33. Kim YI, Neher E (1988) IgG from patients with Lambert-Eaton syndrome blocks voltage-dependent calcium channels. Science 239: 405-408.
34. Kimura J (1989) Electrodiagnosis. In: Diseases of nerve and muscle: principles and practice, p 107. Philadelphia: F. A. Davis.
35. Lambert EH, Elmqvist D (1971) Quantal components of end-plate potentials in the myasthenic syndrome. Ann NY Acad Sci 183:183-199.
36. Lang B, Newsom-Davis J, Peers C, Prior C, Wray DW (1987) The effect of myasthenic syndrome antibody on presynaptic calcium channels in the mouse. J Physiol (Lond) 390:257-270.
37. Lennon VA, Kryzer TJ, Griesmann GE, O'Suilleabhain PE, Windebank AJ, Woppmann A, Miljanich GP, Lambert EH (1995) Calcium-channel antibodies in the Lambert-Eaton syndrome and other paraneoplastic syndromes. N Engl J Med 332:1467-1474.
38. Leveque C, Hoshino T, David P, Shoji-Kasi Y, Leys K, Omori A, Lang B, El Far O, Sato K, Martin-Moutot N, Newsom-Davis J, Takahashi M, Seagar MJ (1992) The synaptic vesicle protein synaptotagmin associates with calcium channels and is a putative Lambert-Eaton myasthenic syndrome antigen. Proc Natl Acad Sci USA 89:3625-3629.
39. Maddison P, Newsom-Davis J, Mills KR (1998) Decay of postexercise augmentation in the Lambert-Eaton myasthenic syndrome: effect of cooling. Neurology 50:1083-1087.
40. Magelby K (1987) Short-term changes in synaptic efficacy. In: Synaptic function (Edelman GM, Gall WE, Cowan WM, eds), pp. 21-56. New York: Wiley.
41. 2+ channels by Lambert-Eaton myasthenic syndrome (LEMS) antibodies in rat insulinoma RINm5F cells. FEBS Lett 387:47-52.
42. Meriney SD, Hulsizer SC, Lennon VA, Grinnell AD (1996) Lambert-Eaton myasthenic syndrome immunoglobulins react with multiple types of calcium channels in small-cell lung carcinoma. Ann Neurol 40:739-749.
43. Morgan A, Burgoyne RD (1997) Common mechanisms for regulated exocytosis in the chromaffin cell and the synapse. Semin Cell Dev Biol 8:141-149.
44. Motomura M, Lang B, Johnston I, Palace J, Vincent A, Newsom-Davis J (1997) Incidence of serum anti-P/Q-type and anti-N-type calcium channel autoantibodies in the Lambert-Eaton myasthenic syndrome. J Neurol Sci 147:35-42.
45. Neher E, Marty A (1982) Discrete changes of cell membrane capacitance observed under conditions of enhanced secretion in bovine adrenal chromaffin cells. Proc Natl Acad Sci USA 79:6712-6716.
46. 1A calcium channel subunit reduce both P-type and Q-type calcium currents in cerebellar neurons. Proc Natl Acad Sci USA 95:8328-8333.
47. Protti DA, Reisin R, Angelillo Mackinley T, Uchitel OD (1996) Calcium channel blockers and transmitter release at the normal human neuromuscular junction. Neurology 46:1391-1396.
48. 2+-channel diversity: is it time for T? J Membr Biol 161:207-213.
49. Seward EP, Nowycky MC (1996) Kinetics of stimulus-coupled secretion in dialyzed bovine chromaffin cells in response to trains of depolarizing pulses. J Neurosci 16:553-562.
50. Sher E, Carbone E, Clementi F (1993) Neuronal calcium channels as target for Lambert-Eaton myasthenic syndrome autoantibodies. Ann NY Acad Sci 681:373-381.
51. Smith DO, Conklin MW, Jensen PJ, Atchison WD (1995) Decreased calcium currents in motor nerve terminals of mice with Lambert-Eaton myasthenic syndrome. J Physiol (Lond) 487:115-123.
52. 2+/calmodulin-dependent protein kinase II phosphorylate a novel 58-kDa protein in synaptic vesicles. Brain Res 551:279-292.
53. Takamori M, Hamada T, Komai K, Takahashi M, Yoshida A (1994) Synaptotagmin can cause an immune-mediated model of Lambert-Eaton myasthenic syndrome in rats. Ann Neurol 35:74-80.
54. Takamori M, Takahashi M, Yasukawa Y, Iwasa K, Nemoto Y, Suenaga A, Nagataki S, Nakamura T (1995) Antibodies to recombinant synaptotagmin and calcium channel subtypes in Lambert-Eaton myasthenic syndrome. J Neurol Sci 133:95-101.
55. 1A subunit of the voltage-gated calcium channel in Lambert-Eaton myasthenic syndrome. Neurology 48:1261-1265.
56. Thies RE (1965) Neuromuscular depression and the apparent depletion of transmitter in mammalian muscle. J Neurophysiol 28:427-442.
57. Tim RW, Sanders DB (1994) Repetitive nerve stimulation studies in the Lambert-Eaton myasthenic syndrome. Muscle Nerve 17:995-1001.
58. Trifaro JM, Vitale ML, Rodriguez Del Castillo A (1993) Scinderin and chromaffin cell actin network dynamics during neurotransmitter release. J Physiol (Paris) 87:89-106.
59. Verschuuren JJ, Dalmau J, Tunkel R, Lang B, Graus F, Schramm L, Posner JB, Newsom-Davis J, Rosenfeld MR (1998) Antibodies against the calcium channel β-subunit in Lambert-Eaton myasthenic syndrome. Neurology 50:475-479.
60. Viglione MP, Creutz CE, Kim YI (1992) Lambert-Eaton syndrome: antigen-antibody interaction and calcium current inhibition in chromaffin cells. Muscle Nerve 15:1325-1333.
61. Viglione MP, O'Shaughnessy TJ, Kim YI (1995) Inhibition of calcium currents and exocytosis by Lambert-Eaton syndrome antibodies in human lung cancer cells. J Physiol (Lond) 488:303-317.
62. Vincent A, Lang B, Newsom-Davis J (1989) Autoimmunity to the voltage-gated calcium channel underlies the Lambert-Eaton myasthenic syndrome, a paraneoplastic disorder. Trends Neurosci 12:496-502.
63. Vitale M, Rodriguez del Castillo A, Tchakarov L, Trifaro J-M (1991) Cortical filamentous actin disassembly and scinderin redistribution during chromaffin cell stimulation precede exocytosis, a phenomenon not exhibited by gelsolin. J Cell Biol 113:1057-1067.
64. Yoshida A, Oho C, Omori A, Kuwahara R, Ito T, Takahashi M (1992) HPC-1 is associated with synaptotagmin and ω-conotoxin receptor. J Biol Chem 267:24925-24928.
65. Zucker RS (1989) Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.
66. Zucker RS (1996) Exocytosis: a molecular and physiological perspective. Neuron 17:1049-1055.