Long-lasting hyperexcitability induced by depolarization in the absence of detectable Ca2+ signals

Journal of Neurophysiology

Volumn 101, Issue 3, 2009, Pages 1351-1360

  Kunjilwar, Kumud K ^a   Fishman, Harvey M ^a   Englot, Dario J ^a,b   O'Neil, Roger G ^a   Walters, Edgar T ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; THAPSIGARGIN; 1,2 BIS(2 AMINOPHENOXY)ETHANE N,N,N',N' TETRAACETIC ACID ACETOXYMETHYL ESTER; 1,2-BIS(2-AMINOPHENOXY)ETHANE N,N,N',N'-TETRAACETIC ACID ACETOXYMETHYL ESTER; CALCIMYCIN; CHELATING AGENT; DRUG DERIVATIVE; EGTAZIC ACID; IONOPHORE; POTASSIUM CHLORIDE;

APLYSIA; ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DEPOLARIZATION; EXTRACELLULAR CALCIUM; GANGLION; NERVE CELL CULTURE; NERVE EXCITABILITY; NERVE FIBER; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; SENSORY NERVE CELL; ACTION POTENTIAL; ANALYSIS OF VARIANCE; ANIMAL; BIOPHYSICS; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; DRUG INTERACTION; ELECTROSTIMULATION; IN VITRO STUDY; LONG TERM DEPRESSION; METABOLISM; METHODOLOGY; PHYSIOLOGY; SENSORY RECEPTOR; TIME;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; APLYSIA; AXONS; BIOPHYSICS; CALCIMYCIN; CALCIUM; CHELATING AGENTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EGTAZIC ACID; ELECTRIC STIMULATION; GANGLIA, INVERTEBRATE; IONOPHORES; LONG-TERM SYNAPTIC DEPRESSION; POTASSIUM CHLORIDE; SENSORY RECEPTOR CELLS; TIME FACTORS;

EID: 64749102391     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.91012.2008     Document Type: Article

References (67)

1. 2+/calmodulin and transmitter. J Neurosci 11: 2655-2665, 1991.
2. 2+ store in the plasticity of central neurons. Trends Pharmacol Sci 27: 78-84, 2006.
3. Ben-Chaim Y, Chanda B, Dascal N, Bezanilla F, Parnas I, Parnas H. Movement of "gating charge" is coupled to ligand binding in a G-protein-coupled receptor. Nature 444: 106-109, 2006.
4. Berdan RC, Easaw JC, Wang R. Alterations in membrane potential after axotomy at different distances from the soma of an identified neuron and the effect of depolarization on neurite outgrowth and calcium channel expression. J Neurophysiol 69: 151-164, 1993. (Pubitemid 23071092)
5. Bernath S. Calcium-independent release of amino acid neurotransmitters: fact or artifact? Prog Neurobiol 38: 57-91, 1992.
6. Bozyczko-Coyne D, McKenna BW, Connors TJ, Neff NT. A rapid fluorometric assay to measure neuronal survival in vitro. J Neurosci Methods 50: 205-216, 1993. (Pubitemid 24013807)
7. Brager DH, Johnston D. Plasticity of intrinsic excitability during long-term depression is mediated through mGluR-dependent changes in Ih in hippocampal CA1 pyramidal neurons. J Neurosci 27: 13926-13937, 2007.
8. Brown TH, Chapman PF, Kairiss EW, Keenan CL. Long-term synaptic potentiation. Science 242: 724-728, 1988. (Pubitemid 18276494)
9. 2+ signalling. Nat Rev Neurosci 8: 182-193, 2007.
10. Casadio A, Martin KC, Giustetto M, Zhu H, Chen M, Bartsch D, Bailey CH, Kandel ER. A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99: 221-237, 1999. (Pubitemid 29491788)
11. Case RM, Eisner D, Gurney A, Jones O, Muallem S, Verkhratsky A. Evolution of calcium homeostasis: from birth of the first cell to an omnipresent signalling system. Cell Calcium 42: 345-350, 2007. (Pubitemid 47264007)
12. de Curtis M, Avanzini G. Interictal spikes in focal epileptogenesis. Prog Neurobiol 63: 541-567, 2001. (Pubitemid 32115432)
13. Deng PY, Lei S. Long-term depression in identified stellate neurons of juvenile rat entorhinal cortex. J Neurophysiol 97: 727-737, 2007. (Pubitemid 46150791)
14. Destexhe A, Rudolph M, Paré D. The high-conductance state of neocortical neurons in vivo. Nat Rev Neurosci 4: 739-751, 2003. (Pubitemid 37280153)
15. Dong C, Upadhya SC, Ding L, Smith TK, Hegde AN. Proteasome inhibition enhances the induction and impairs the maintenance of late-phase long-term potentiation. Learn Mem 15: 335-347, 2008.
16. Eccles JC. Calcium in long-term potentiation as a model for memory. Neuroscience 10: 1071-1081, 1983.
17. h. Nat Neurosci 8: 1542-1551, 2005.
18. Fishman HM, Bittner GD. Vesicle-mediated restoration of a plasmalemmal barrier in severed axons. News Physiol Sci 18: 115-118, 2003. (Pubitemid 36782801)
19. Fitzjohn SM, Collingridge GL. Calcium stores and synaptic plasticity. Cell Calcium 32: 405-411, 2002. (Pubitemid 36175760)
20. Glanzman DL. New tricks for an old slug: the critical role of postsynaptic mechanisms in learning and memory in Aplysia. Prog Brain Res 169C: 277-292, 2008.
21. Gorman AL, Hermann A, Thomas MV. Ionic requirements for membrane oscillations and their dependence on the calcium concentration in a molluscan pace-maker neurone. J Physiol 327: 185-217, 1982. (Pubitemid 12086446)
22. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
23. Hawkins RD, Abrams TW, Carew TJ, Kandel ER. A cellular mechanism of classical conditioning in Aplysia: activity-dependent amplification of presynaptic facilitation. Science 219: 400-405, 1983. (Pubitemid 13176267)
24. + channels. Proc Natl Acad Sci USA 103: 2886-2891, 2006.
25. Hille B. Ion Channels of Excitable Membranes (3rd ed.). Sunderland, MA: Sinauer, 2001, p. xviii.
26. Hochner B, Parnas H, Parnas I. Membrane depolarization evokes neurotransmitter release in the absence of calcium entry. Nature 342: 433-435, 1989. (Pubitemid 19277518)
27. Hu JY, Glickman L, Wu F, Schacher S. Serotonin regulates the secretion and autocrine action of a neuropeptide to activate MAPK required for long-term facilitation in Aplysia. Neuron 43: 373-385, 2004. (Pubitemid 39061129)
28. Ibata K, Sun Q, Turrigiano GG. Rapid synaptic scaling induced by changes in postsynaptic firing. Neuron 57: 819-826, 2008.
29. Iwasaki H, Murata Y, Kim Y, Hossain MI, Worby CA, Dixon JE, McCormack T, Sasaki T, Okamura Y. A voltage-sensing phosphatase, Ci-VSP, which shares sequence identity with PTEN, dephosphorylates phosphatidylinositol 4,5-bisphosphate. Proc Natl Acad Sci USA 105: 7970-7975, 2008.
30. Kachoei BA, Knox RJ, Uthuza D, Levy S, Kaczmarek LK, Magoski NS. A store-operated Ca(2+) influx pathway in the bag cell neurons of Aplysia. J Neurophysiol 96: 2688-2698, 2006.
31. Kaczmarek LK. Non-conducting functions of voltage-gated ion channels. Nat Rev Neurosci 7: 761-771, 2006.
32. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038, 2001.
33. Kehoe J. Synaptic block of a calcium-activated potassium conductance in Aplysia neurones. J Physiol 369: 439-474, 1985. (Pubitemid 16176886)
34. Kingsbury TJ, Bambrick LL, Roby CD, Krueger BK. Calcineurin activity is required for depolarization-induced, CREB-dependent gene transcription in cortical neurons. J Neurochem 103: 761-770, 2007.
35. Kovacs KA, Steullet P, Steinmann M, Do KQ, Magistretti PJ, Halfon O, Cardinaux JR. TORC1 is a calcium- and cAMP-sensitive coincidence detector involved in hippocampal long-term synaptic plasticity. Proc Natl Acad Sci USA 104: 4700-4705, 2007. (Pubitemid 47186288)
36. Lan M, Shi Y, Sun L, Liu L, Guo X, Lu Y, Wang J, Liang J, Fan D. KCl depolarization increases HIF-1 transcriptional activity via the calcium-independent pathway in SGC7901 gastric cancer cells. Tumour Biol 28: 173-180, 2007. (Pubitemid 46976004)
37. + channel gene transcription and protein expression in pituitary cells. J Biol Chem 270: 6036-6041, 1995.
38. Malenka RC. The role of postsynaptic calcium in the induction of long-term potentiation. Mol Neurobiol 5: 289-295, 1991.
39. Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 44: 5-21, 2004. (Pubitemid 39348827)
40. Mattson MP. Calcium and neurodegeneration. Aging Cell 6: 337-350, 2007. (Pubitemid 46785139)
41. 2+. Synapse 1: 273-278, 1987.
42. McNeil PL, Terasaki M. Coping with the inevitable: how cells repair a torn surface membrane. Nat Cell Biol 3: E124-E129, 2001. (Pubitemid 32422077)
43. 2+-free solutions. Proc Natl Acad Sci USA 80: 315-319, 1983.
44. Montarolo PG, Goelet P, Castellucci VF, Morgan J, Kandel ER, Schacher S. A critical period for macromolecular synthesis in long-term heterosynaptic facilitation in Aplysia. Science 234: 1249-1254, 1986. (Pubitemid 17232366)
45. Okamura Y. Biodiversity of voltage sensor domain proteins. Pflügers Arch 454: 361-371, 2007. (Pubitemid 46742437)
46. Rao VR, Finkbeiner S. NMDA and AMPA receptors: old channels, new tricks. Trends Neurosci 30: 284-291, 2007. (Pubitemid 46802833)
47. Schacher S, Proshansky E. Neurite regeneration by Aplysia neurons in dissociated cell culture: modulation by Aplysia hemolymph and the presence of the initial axonal segment. J Neurosci 3: 2403-2413, 1983. (Pubitemid 14187118)
48. Scheetz AJ, Nairn AC, Constantine-Paton M. NMDA receptor-mediated control of protein synthesis at developing synapses. Nat Neurosci 3: 211-216, 2000. (Pubitemid 30140781)
49. Shaw NA. The neurophysiology of concussion. Prog Neurobiol 67: 281-344, 2002. (Pubitemid 35223130)
50. Turrigiano G, Abbott LF, Marder E. Activity-dependent changes in the intrinsic properties of cultured neurons. Science 264: 974-977, 1994. (Pubitemid 2099173)
51. 2+ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 11: 221-235, 1993.
52. + current in tail sensory neurons of Aplysia: role of serotonin and cAMP. J Neurophysiol 61: 32-44, 1989.
53. Walters ET, Bodnarova M, Billy AJ, Dulin MF, Diaz-Rios M, Miller MW, Moroz LL. Somatotopic organization and functional properties of mechanosensory neurons expressing sensorin-A mRNA in Aplysia californica. J Comp Neurol 471: 219-240, 2004. (Pubitemid 38325503)
54. Walters ET, Byrne JH. Associative conditioning of single sensory neurons suggests a cellular mechanism for learning. Science 219: 405-408, 1983. (Pubitemid 13176268)
55. Walters ET, Byrne JH, Carew TJ, Kandel ER. Mechanoafferent neurons innervating tail of Aplysia. I. Response properties and synaptic connections. J Neurophysiol 50: 1522-1542, 1983.
56. Weragoda RM, Ferrer E, Walters ET. Memory-like alterations in Aplysia axons after nerve injury or localized depolarization. J Neurosci 24: 10393-10401, 2004. (Pubitemid 39552624)
57. Weragoda RM, Walters ET. Serotonin induces memory-like, rapamycin-sensitive hyperexcitability in sensory axons of Aplysia that contributes to injury responses. J Neurophysiol 98: 1231-1239, 2007. (Pubitemid 47435877)
58. Wertz A, Rossler W, Obermayer M, Bickmeyer U. Functional neuroanatomy of the rhinophore of Aplysia punctata. Front Zool 3: Art. 6, 2006. (Pubitemid 44201891)
59. West AE, Chen WG, Dalva MB, Dolmetsch RE, Kornhauser JM, Shaywitz AJ, Takasu MA, Tao X, Greenberg ME. Calcium regulation of neuronal gene expression. Proc Natl Acad Sci USA 98: 11024-11031, 2001. (Pubitemid 32928677)
60. Williams RJ. The evolution of calcium biochemistry. Biochim Biophys Acta 1763: 1139-1146, 2006.
61. Wojtowicz JM, Atwood HL. Presynaptic long-term facilitation at the crayfish neuromuscular junction: voltage-dependent and ion-dependent phases. J Neurosci 8: 4667-4674, 1988.
62. Wu L, Gao X, Brown RC, Heller S, O'Neil RG. Dual role of the TRPV4 channel as a sensor of flow and osmolality in renal epithelial cells. Am J Physiol Renal Physiol 293: F1699-F1713, 2007. (Pubitemid 350086007)
63. Xu J, Kang J. The mechanisms and functions of activity-dependent long-term potentiation of intrinsic excitability. Rev Neurosci 16: 311-323, 2005. (Pubitemid 43185083)
64. + conductance TASK-3 via the calcineurin pathway. J Biol Chem 281: 28910-28918, 2006.
65. Zhang C, Zhou Z. Ca2+-independent but voltage-dependent secretion in mammalian dorsal root ganglion neurons. Nat Neurosci 5: 425-430, 2002. (Pubitemid 34454247)
66. 2+ following axotomy and throughout the recovery process of cultured Aplysia neurons. Eur J Neurosci 5: 657-668, 1993.
67. Zucker RS. Calcium- and activity-dependent synaptic plasticity. Curr Opin Neurobiol 9: 305-313, 1999. (Pubitemid 29267601)