Activity-dependent initiation of a prolonged depolarization in Aplysia bag cell neurons: Role for a cation channel

Journal of Neurophysiology

Volumn 97, Issue 3, 2007, Pages 2465-2479

  Hung, Anne Y ^a   Magoski, Neil S ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; CALCIUM ION; CALMODULIN KINASE; CATION CHANNEL; FLUFENAMIC ACID; GADOLINIUM; N (2 PHENYLCYCLOPENTYL)AZACYCLOTRIDECAN 2 IMINE; PHOSPHOTRANSFERASE; POTASSIUM ION; SODIUM ION; TETRODOTOXIN; TETRYLAMMONIUM; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL CELL; APLYSIA; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CELL ACTIVITY; CELL CULTURE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; CORRELATION ANALYSIS; ENZYME INHIBITION; EVOKED RESPONSE; MEMBRANE POTENTIAL; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION;

1-(5-ISOQUINOLINESULFONYL)-2-METHYLPIPERAZINE; ANIMALS; APLYSIA; CALMODULIN-BINDING PROTEINS; CATIONS; CELLS, CULTURED; CHELATING AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DOSE-RESPONSE RELATIONSHIP, RADIATION; EGTAZIC ACID; ELECTRIC STIMULATION; ENZYME INHIBITORS; ION CHANNELS; MEMBRANE POTENTIALS; MEMBRANE TRANSPORT MODULATORS; NEURONS; PATCH-CLAMP TECHNIQUES; POTASSIUM CHANNEL BLOCKERS; TETRAETHYLAMMONIUM; TIME FACTORS;

EID: 33947102512     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00941.2006     Document Type: Article

References (114)

1. Andrew RD, Dudek FE. Burst discharge in mammalian neuroendocrine cells involves an intrinsic regenerative mechanism. Science 221: 1050-1052, 1983.
2. Aracri P, Colombo E, Mantegazza M, Scalmani P, Curia G, Avanzini G, Franceschetti S. Layer-specific properties of the persistent sodium current in sensorimotor cortex. J Neurophysiol 95: 3460-3468, 2006.
3. 2+ entry in cultured neurons and astrocytes. Biochem Biophys Res Commun 279: 354-357, 2000.
4. Arch S. Biosynthesis of the egg-laying hormone (ELH) in the bag cell neurons of Aplysia californica. J Gen Physiol 60: 102-119, 1972.
5. 2+ entry: implications in synaptic plasticity J Neurosci 23: 7737-7741, 2003.
6. Bengtson CP, Tozzi A, Bernardi G, Mercuri NB. Transient receptor potential-like channels mediate metabotropic glutamate receptor EPSCs in rat dopamine neurones. J Physiol 555: 323-330, 2004.
7. Blankenship JE, Haskins JT. Electrotonic coupling among neuroendocrine cells in Aplysia. J Neurophysiol 42: 347-355, 1979.
8. Bouillon M, Audette M. Retinoic acid-stimulated intercellular adhesion molecule-1 expression on SK-N-SH cells: calcium/calmodulin-dependent pathway. Cancer Res 54: 4144-4149, 1994.
9. Brown CH, Bourque CW. Autocrine feedback inhibition of plateau potentials terminates phasic bursts in magnocellular neurosecretory cells of the rat supraoptic nucleus. J Physiol 557: 949-960, 2004.
10. Brown RO, Mayeri E. Positive feedback by autoexcitatory neuropeptides in neuroendocrine bag cells of Aplysia. J Neurosci 9: 1443-1451, 1989.
11. 2+ release from internal stores in vascular endothelial cells. Biochem J 295: 357-366, 1993.
12. Chakfe Y, Bourque CW. Excitatory peptides and osmotic pressure modulate mechanosensitive cation channels in concert. Nat Neurosci 3: 572-579, 2000.
13. Chandler WK, Meves H. Voltage clamp experiments on internally perfused giant axons. J Physiol 180: 788-820, 1965.
14. Chiu AY, Hunkapiller MW, Heller E, Stuart DK, Hood LE, Strumwasser F. Purification and primary structure of the neuropeptide egg-laying hormone of Aplysia californica. Proc Natl Acad Sci USA 76: 6656-6660, 1979.
15. Conn PJ, Kaczmarek LK. The bag cell neurons of Aplysia. A model for the study of the molecular mechanisms involved in the control of prolonged animal behaviors. Mol Neurobiol 3: 237-273, 1989.
16. Connor CG, Brady RC, Brownstein BL. Trifluoperazine inhibits spreading and migration of cells in culture. J Cell Physiol 108: 299-307, 1981.
17. Cordova D, Delpech VR, Satelle DB, Rauh JJ. Spatiotemporal calcium signaling in a Drosophila melanogaster cell line stably expressing a Drosophila muscarinic acetylcholine receptor. Invert Neurosci 5: 19-28, 2003.
18. Cornwell MM, Juliano RL, Davies PJ. Inhibition of the adhesion of Chinese hamster ovary cells by the naphthylsulfonamides dansylcadaverine and N-(6-aminohexyl)-5-chloro-1-naphthylenesulfonamide (W7). Biochim Biophys Acta 762: 414-419, 1983.
19. Daly JW, Leuders J, Padgett WL, Shin Y, Gusovsky F. Malotoxin-elicited calcium influx in cultured cells. Biochem Pharmacol 50: 1187-1197, 1995.
20. Dembrow NC, Jing J, Brezina V, Weiss KR. A specific synaptic pathway activates a conditional plateau potential underlying protraction phase in the Aplysia feeding central pattern generator. J Neurosci 24: 5230-5238, 2004.
21. DeRiemer SA, Kaczmarek LK, Lai Y, McGuinness TL, Greengard P. Calcium/calmodulin-dependent protein phosphorylation in the nervous system of Aplysia. J Neurosci 4: 1618-1625, 1984.
22. DeRiemer SA, Schweitzer B, Kaczmarek LK. Inhibitors of calcium-dependent enzymes prevent the onset of afterdischarge in the peptidergic bag cell neurons of Aplysia. Brain Res 340: 175-180, 1985.
23. Derjean D, Bertrand S, Nagy F, Shefchyk SJ. Plateau potentials and membrane oscillations in parasympathetic preganglionic neurons and intermediolateral neurons in the rat lumbosacral spinal cord. J Physiol 563: 583-596, 2005.
24. Dudek FE, Cobbs JS, Pinsker HM. Bag cell electrical activity underlying spontaneous egg laying in freely behaving Aplysia brasiliana. J Neurophysiol 42: 804-817, 1979.
25. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA. Graded persistent activity in entorhinal cortex neurons. Nature 420: 173-178, 2002.
26. Eyzaguirre C, Kuffler SW. Further study of soma, dendrite, and axon excitation in single neurons. J Gen Physiol 39: 121-153, 1955.
27. Fisher TE, Levy S, Kaczmarek LK. Transient changes in intracellular calcium associated with a prolonged increase in excitability in neurons of Aplysia californica. J Neurophysiol 71: 1254-1257, 1994.
28. 2+ can affect the pattern of discharge in rat thalamic neurons. J Physiol 535: 33-45, 2001.
29. Franco A Jr, Lansman JB. Stretch-sensitive channels in developing muscle cells from a mouse cell line. J Physiol 427: 361-380, 1990.
30. Fraser DD, MacVicar BA. Cholinergic-dependent plateau potential in hippocampal CA1 pyramidal neurons. J Neurosci 16: 4113-4128, 1996.
31. Gee CE, Benquet P, Gerber U. Group I metabotropic glutamate receptors activate a calcium-sensitive transient receptor potential-like conductance in rat hippocampus. J Physiol 546: 655-664, 2003.
32. Ghamari-Langroudi M, Bourque CW. Flufenamic acid blocks depolarizing afterpotentials and phasic firing in rat supraoptic neurons. J Physiol 545: 537-542, 2002.
33. Giannone G, Takeda K, Kleschyov AL. Novel activation of non-selective cationic channels by dinitrosyl iron-thiosulfate in PC12 cells. J Physiol 529: 735-745, 2000.
34. Hagiwara S, Saito N. Voltage-current relations in nerve cell membrane of Onchidium verruculatum. J Physiol 148: 161-179, 1959.
35. Haj-Damane S, Andrade R. Calcium-activated cation nonselective current contributes to the fast afterdepolarization in rat prefrontal cortex neurons. J Neurophysiol 78: 1983-1989, 1997.
36. Haj-Damane S, Andrade R. Muscarinic receptors regulate two different calcium-dependent non-selective cation currents in rat prefrontal cortex. Eur J Neurosci 11: 1973-1980, 1999.
37. 2+/calmodulin- dependent protein kinases. Annu Rev Biochem 61: 559-601, 1992.
38. Hasuo H, Phelan KD, Twery MJ, Gallagher JP. A calcium-dependent slow afterdepolarization recorded in rat dorsolateral septal nucleus neurons in vitro. J Neurophysiol 64: 1838-1846, 1990.
39. Hill AJ, Hinton JM, Cheng H, Gao Z, Bates DO, Hancox JC, Langton PD, James AF. A TRPC-like non-selective cation current activated by alpha1-adrenoceptors in rat mesenteric artery smooth muscle cells. Cell Calcium 40: 29-40, 2006.
40. Hille B. Ionic Channels of Excitable Membranes. Sunderland, MA: Sinauer Associates, 2001.
41. 2+ influx pathway in the bag cell neurons of Aplysia. J Neurophysiol 96: 2688-2698, 2006.
42. Kaczmarek LK, Finbow M, Revel JP, Strumwasser F. The morphology and coupling of Aplysia bag cells within the abdominal ganglion and in cell culture. J Neurobiol 10: 535-550, 1979.
43. Kaczmarek LK, Jennings KR, Strumwasser F. An early sodium and a late calcium phase in the afterdischarge of peptide-secreting neurons of Aplysia. Brain Res 238: 105-115, 1982.
44. Kim SJ, Kim YS, Yuan JP, Petralia RS, Worley PF, Linden DJ. Activation of the TRPC1 cation channel by metabotropic glutamate receptor mGluR1. Nature 426: 285-291, 2003.
45. 2+ current: mechanism for behavioral sensitization in Aplysia californica. Proc Natl Acad Sci USA 75: 3512-3516, 1978.
46. 2+ release in peptidergic neurons of Aplysia californica. J Physiol 494: 627-639, 1996.
47. Kramer RH, Zucker RS. Calcium-dependent inward current in Aplysia bursting pace-maker neurons. J Physiol 362: 107-130, 1985.
48. Kupfermann I. Stimulation of egg laying: possible neuroendocrine function of bag cells of abdominal ganglion of Aplysia californica. Nature 216: 814-815, 1967.
49. Kupfermann I. Stimulation of egg laying by extracts of neuroendocrine cells (bag cells) of abdominal ganglion of Aplysia. J Neurophysiol 33: 877-881, 1970.
50. Kupfermann I, Kandel ER. Electrophysiological properties and functional interconnections of two symmetrical neurosecretory clusters (bag cells) in abdominal ganglion of Aplysia. J Neurophysiol 33: 865-876, 1970.
51. Lapetina EG, Reep B, Read NG, Moncada S. Adhesion of human platelets to collagen in the presence of prostacyclin, indomethacin and compound BW 755C. Thromb Res 41: 325-335, 1986.
52. Levitan IB. It is calmodulin after all! Mediator of the calcium modulation of multiple ion channels. Neuron 22: 645-648, 1999.
53. 2+ stores in rat supraoptic neurons: involvement in histamine-induced enhancement of depolarizing afterpotentials. Neuroscience 93: 667-674, 1999.
54. Liu J, Chen T, Yu B, Xu Q. Ruscogenin glycoside (Lm-3) isolated from Liriope muscari inhibits lymphocyte adhesion to extracellular matrix. J Pharm Pharmacol 54: 959-965, 2002.
55. Lo FS, Erzurumlu RS. L-type calcium channel-mediated plateau potentials in barrelette cells during structural plasticity. J Neurophysiol 88: 794-801, 2002.
56. 2+-dependent regulation of a non-selective cation channel from Aplysia bag cell neurones. J Physiol 575: 491-508, 2006.
57. Magoski NS. Regulation of an Aplysia bag-cell neuron cation channel by closely associated protein kinase A and a protein phosphatase. J Neurosci 24: 6833-6841, 2004.
58. Magoski NS, Kaczmarek LK. Association/dissociation of a channel-kinase complex underlies state-dependent modulation. J Neurosci 25: 8037-8047, 2005.
59. 2+ release in Aplysia bag cell neurones. J Physiol 522: 271-283, 2000.
60. Magoski NS, Wilson GF, Kaczmarek LK. Protein kinase modulation of a neuronal cation channel requires protein-protein interactions mediated by an Src homology 3 domain. J Neurosci 22: 1-9, 2002.
61. Mayeri E, Brownell P, Branton WD. Multiple, prolonged actions of neuroendocrine bag cells on neurons in Aplysia. II. Effects on beating pacemaker and silent neurons. J Neurophysiol 42: 1185-1197, 1979b.
62. Mayeri E, Brownell P, Branton WD, Simon SB. Multiple, prolonged actions of neuroendocrine bag cells on neurons in Aplysia. I. Effects on bursting pacemaker neurons. J Neurophysiol 42: 1165-1184, 1979a.
63. Mercer AR, Kloppenburg P, Hildebrand JG. Plateau potentials in developing antennal-lobe neurons of the moth, Manduca sexta. J Neurophysiol 93: 1949-1958, 2005.
64. Merritt JE, Armstrong WP, Benham CD, Hallam TJ, Jacob R, Jaxa-Chamiec A, Leigh BK, McCarthy SA, Moorees KE, Rink TJ. SK&F 96365, a novel inhibitor of receptor-mediated calcium entry. Biochem J 271: 515-522, 1990.
65. Mohri T, Kameshita I, Suzuki S, Hioki K, Tokunaga R, Takatani S. Rapid adhesion and spread of non-adherent colon cancer Colo201 cells induced by the protein kinase inhibitors, K252a and KT5720 and suppression of the adhesion by the immunosuppressants FK506 and cyclosporin A. Cell Struct Funct 23: 255-264, 1998.
66. Morisset V, Nagy F. Ionic basis for plateau potentials in deep dorsal horn neurons of the rat spinal cord. J Neurosci 17: 7309-7316, 1999.
67. Nakanishi K, Zhang F, Baxter DA, Eskin A, Byrne JH. Role of calcium-calmodulin-dependent protein kinase II in modulation of sensorimotor synapses in Aplysia. J Neurophysiol 78: 409-416, 1997.
68. 2+] at the mouth of a calcium channel. J Neurosci 17: 6961-6973, 1997.
69. Narahashi T, Moore JW, Scott WR. Tetrodotoxin blockage of sodium conductance increase in lobster giant axons. J Gen Physiol 47: 965-974, 1964.
70. Ohki G, Miyoshi T, Murata M, Ishibashi K, Imai M, Suzuki M. A calcium-activated cation current by an alternatively spliced form of Trp3 in the heart. J Biol Chem 275: 39055-39060, 2000.
71. Partridge LD, Swandulla D. Calcium-activated non-specific cation channels. Trends Neurosci 11: 69-72, 1988.
72. Partridge LD, Valenzuela CF. Block of hippocampal CAN channels by flufenamate. Brain Res 867: 143-148, 2000.
73. Payne ME, Fong YL, Ono T, Colbran RJ, Kemp BE, Soderling TR, Means AR. Calcium/calmodulin-dependent protein kinase II. Characterization of distinct calmodulin binding and inhibitory domains. J Biol Chem 263: 7190-7195, 1988.
74. 2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L-type calcium current. J Neurophysiol 89: 954-959, 2003.
75. Pierson PM, Liu X, Raggenbass M. Suppression of potassium channels elicits calcium-dependent plateau potentials in suprachiasmatic neurons of the rat. Brain Res 1036: 50-59, 2005.
76. Pinsker HM, Dudek FE. Bag cell control of egg-laying in freely moving Aplysia. Science 197: 490-493, 1977.
77. Popp R, Englert HC, Lang HJ, Gogelein H. Inhibitors of nonselective cation channels in cells of the blood-brain barrier. EXS 66: 213-218, 1993.
78. 2+ channels by 2-aminoethyldiphenyl borate (2-APB) occurs independently of IP3 receptors. J Physiol 536: 3-19, 2001.
79. Quattrocki EA, Marshall J, Kaczmarek LK. A Shab potassium channel contributes to action potential broadening in peptidergic neurons. Neuron 12: 73-86, 1994.
80. Rekling JC, Feldman JL. Calcium-dependent plateau potentials in rostral ambiguous neurons in the newborn mouse brain stem in vitro. J Neurophysiol 78: 2483-2492, 1997.
81. Rothman BS, Weir G, Dudek FE. Egg-laying hormone: direct action on the ovitestis of Aplysia. Gen Comp Endocrinol 52: 134-141, 1983.
82. Russell DF, Hartline DK. Slow active potentials and bursting motor patterns in pyloric network of the lobster, Panulirus interruptus. J Neurophysiol 48: 914-937, 1982.
83. Russo RE, Hounsgaard J. Burst-generating neurones in the dorsal horn in an in vitro preparation of the turtle spinal cord. J Physiol 493: 39-54, 1996.
84. Saimi Y, Kung C. Ion channel regulation by calmodulin binding. FEBS Lett 350: 155-158, 1994.
85. Scheller RH, Jackson JF, McAllister LB, Schwartz JH, Kandel ER, Axel R. A family of genes that codes for ELH, a neuropeptide eliciting a stereotyped pattern of behaviour in Aplysia. Cell 28: 707-719, 1982.
86. 2+-activated channels in neurons. Neurosci Lett 190: 121-124, 1995.
87. Siegel BW, Wiech NL. RMI 12330A: an inhibitor of cholera toxin induced intestinal hypersecretion which also inhibits adenylate cyclase activity. Gastroenterology 70: 937-945, 1976.
88. Sierra F, Comas V, Buno W, Macadar O. Sodium-dependent plateau potentials in electrocytes of the electric fish Gymnotus carapo. J Comp Physiol A Sens Neural Behav Physiol 191: 1-11, 2005.
89. Sigvardt KA, Rothman BS, Brown RO, Mayeri E. The bag cells of Aplysia as a multitransmitter system: identification of alpha bag cell peptide as a second neurotransmitter. J Neurosci 6: 803-813, 1986.
90. Sinohara Y, Nakajima Y, Nakanishi S. Glutamate induces focal adhesion kinase tyrosine phosphorylation and actin rearrangement in heterologous mGluR1-expressing CHO cells via calcium/calmodulin signalling. J Neurochem 78: 365-373, 2001.
91. Smith SM, Bergsman JB, Harata NC, Scheller RH, Tsien RW. Recordings from single neocortical nerve terminals reveal a nonselective cation channel activated by decreases in extracellular calcium. Neuron 41: 243-256, 2004.
92. Soong HK, Cintron C. Different corneal epithelial healing mechanisms in rat and rabbit: role of actin and calmodulin. Invest Ophthalmol Vis Sci 26: 838-848, 1985.
93. Stuart DK, Chiu AY, Strumwasser F. Neurosecretion of egg-laying hormone and other peptides from electrically active bag cell neurons of Aplysia. J Neurophysiol 43: 488-498, 1980.
94. Stuart DK, Strumwasser F. Neuronal sites of action of a neurosecretory peptide, egg-laying hormone in Aplysia californica. J Neurophysiol 43: 499-519, 1980.
95. 2+ elevation in bursting pacemaker neurons of Helix pomatia. J Neurophysiol 54: 1430-1443, 1985.
96. Tahvildari A, Egorov A, Klink R, Alonso A. Persistent activity in the entorhinal cortex neurons, TRP channels and intracellular calcium stores. Program No. 516.3. 2004 Abstract Viewer/Itinerary Planner. Washington, DC: Society for Neuroscience, 2004, Online.
97. + channels. Pfluegers Arch 451: 474-478, 2005.
98. + current and non-selective cation current in rat nucleus basalis neurons. Neuroscience 58: 553-561, 1994.
99. Thompson SH, Smith SJ. Depolarizing afterpotentials and burst production in molluscan pacemaker neurons. J Neurophysiol 39: 153-161, 1976.
100. 2+/calmodulin-dependent protein kinase II. J Biol Chem 265: 4315-4320, 1990.
101. Tozzi A, Bengtson CP, Longone P, Carignani C, Fusco FR, Bernardi G, Mercuri NB. Involvement of transient receptor potential-like channels in responses to mGluR-I activation in midbrain dopamine neurons. Eur J Neurosci 18: 2133-2145, 2003.
102. 2+ entry mediated by store depletion, S-nitrosylation, and TRP3 channels. Comparison of coupling and function. J Biol Chem 275: 28562-28568, 2000.
103. Warren EJ, Allen CN, Brown RL, Robinson DW. The light-activated signaling pathway in SCN-projecting rat retinal ganglion cells. Eur J Neurosci 23: 2477-2487, 2006.
104. Weissmann G, Azaroff L, Davidson S, Dunham P. Synergy between phorbol esters, 1-oleyl-2-acetylglycerol, urushiol, and calcium ionophore in eliciting aggregation of marine sponge cells. Proc Natl Acad Sci USA 83: 2914-2918, 1986.
105. Whim MD, Kaczmarek LK. Heterologous expression of the Kv3.1 potassium channel eliminates spike broadening and the induction of a depolarizing afterpotential in the peptidergic bag cell neurons. J Neurosci 18: 9171-9180, 1998.
106. Wilson GF, Magoski NS, Kaczmarek LK. Modulation of a calcium-sensitive nonspecific cation channel by closely associated protein kinase and phosphatase activities. Proc Natl Acad Sci USA 95: 10938-10943, 1998.
107. 2+-sensitive nonspecific cation channel underlying prolonged repetitive firing in Aplysia neurons. J Neurosci 16: 3661-3671, 1996.
108. Xiong ZG, Lu WY, MacDonald JF. Extracellular calcium sensed by a novel cation channel in hippocampal neurons. Proc Natl Acad Sci USA 94: 7012-7017, 1997.
109. Xu J, Kang N, Jiang L, Nedergaard M, Kang J. Activity-dependent long-term potentiation of intrinsic excitability in hippocampal CA1 pyramidal neurons. J Neurosci 25: 1750-1760, 2005.
110. Yang XC, Sachs F. Block of stretch-activated ion channels in Xenopus oocytes by gadolinium and calcium ions. Science 243: 1068-1071, 1989.
111. Zhang B, Woottoon JF, Harris-Warrick RM. Calcium-dependent plateau potentials in a crab somatogastric ganglion motor neuron. II. Calcium-activated slow inward current. J Neurophysiol 74: 1938 -1946, 1995.
112. Zhang W, Linden DJ. The other side of the engram: experience-driven changes in neuronal intrinsic excitability. Nat Rev Neurosci 4: 885-900, 2003.
113. + current contributes to the long-lasting refractory period of Aplysia bag cell neurons. J Neurosci 22: 10134-10141, 2002.
114. Zitt C, Obukhov AG, Strubing C, Zobel A, Kalkbrenner F, Luckhoff A, Schultz G. Expression of TRPC3 in Chinese hamster ovary cells results in calcium-activated cation currents not related to store depletion. J Cell Biol 138: 1333-1341, 1997.