Deletion of the ryanodine receptor type 3 (RyR3) impairs forms of synaptic plasticity and spatial learning

EMBO Journal

Volumn 18, Issue 19, 1999, Pages 5264-5273

  Balschun, Detlef ^a   Wolfer, David P ^c   Bertocchini, Federica ^b   Barone, Virginia ^b   Conti, Antonio ^b   Zuschratter, Werner ^a   Missiaen, Ludwig ^c   Lipp, Hans Peter ^c   Frey, J Uwe ^a   Sorrentino, Vincenzo ^b  

^a LEIBNIZ INSTITUTE FOR NEUROBIOLOGY   (Germany)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c NONE

Author keywords

Behavior; Calcium release channe s; Ryanodine receptor type 3; Spatial learning; Synaptic plasticity

Indexed keywords

BRAIN RECEPTOR; CALCIUM ION; RECEPTOR SUBTYPE; RYANODINE RECEPTOR; RYANODINE RECEPTOR 3; UNCLASSIFIED DRUG;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CALCIUM TRANSPORT; CELL STRUCTURE; CONTROLLED STUDY; DENTATE GYRUS; EXPLORATORY BEHAVIOR; GENE DELETION; HABITUATION; HIPPOCAMPUS; IMMUNOBLOTTING; KNOCKOUT MOUSE; LEARNING; LOCOMOTION; LONG TERM POTENTIATION; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NEWBORN; NONHUMAN; PRIORITY JOURNAL; RUNNING; SYNAPTIC TRANSMISSION;

ANIMALS; BEHAVIOR, ANIMAL; DENTATE GYRUS; GENE DELETION; LEARNING; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SYNAPSES;

ANIMALIA; HIPPOCAMPUS HIPPOCAMPUS;

EID: 0033214757     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.19.5264     Document Type: Article

References (57)

1. Alcazar, A, Martin de la Vega, C., Bazan, E., Fando, J.L. and Salinas, M. (1997) Calcium mobilization by ryanodine promotes the phosphorylation of initiation factor 2α subunit and inhibits protein synthesis in cultured neurons. J. Neurochem., 69, 1703-1708.
2. + channel cascade. Trends Neurosci., 21, 529-537.
3. Anderson, P. (1960) Interhippocampal impulses. Acta Physiol. Scand., 48, 178-480.
4. Artola, A. and Singer, W. (1993) Long-term depression of excitatory synaptic transmission and its relationship to long-term potentiation. Trends Neurosci., 16, 480-487.
5. Barrionuevo, G., Schottler, F. and Lynch, G. (1980) The effects of repetitive low frequency stimulation on control and 'potentiated' synaptic responses in the hippocampus. Life Sci., 27, 2385-2391.
6. Berridge, M.J. (1998) Neuronal calcium signaling. Neuron, 21, 13-26.
7. Bertocchini, F., Ovitt, C., Conti, A., Barone, V., Scholer, H.R., Reggiani, C. and Sorrentino, V. (1997) Requirement of the ryanodine receptor type 3 for efficient contraction in neonatal skeletal muscles. EMBO J., 16, 6956-6963.
8. Bliss, T.V.P. and Collingridge, G.L. (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature, 361, 31-39.
9. Bootman, M.D. and Berridge, M.J. (1995) The elemental principles of calcium signaling. Cell, 83, 675-678.
10. Chavis, P., Fagni, L., Lansman, J.B. and Bockaert, J. (1996) Functional coupling between ryanodine receptors and L-type calcium channels in neurons. Nature, 382, 719-722.
11. 2+ release channel (ryanodine receptor) expressed in HEK293 Cells. J. Biol. Chem., 272, 24234-24246.
12. Conti, A., Gorza, L. and Sorrentino, V. (1996) Differential distribution of ryanodine receptor type 3 (RyR3) gene product in mammalian skeletal muscles. Biochem. J., 316, 19-23.
13. 2+ signaling requirements for long-term depression in the hippocampus. Neuron, 16, 825-833.
14. Curtis, D.R. and Eccles, J.C. (1960). Synaptic action during and after repetitive stimulation. J. Physiol. (Lond.), 183, 341-359.
15. Davis, H.P. and Squire, L.R. (1984) Protein synthesis and memory. Psychol. Bull., 96, 518-559.
16. Doyere, V., Srebro, B. and Laroche, S. (1997) Heterosynaptic LTD and depotentiation in the medial perforant path of the dentate gyrus in the freely moving rat. J. Neurophysiol., 77, 571-578.
17. Flucher, B.E., Conti, A., Takeshima, H. and Sorrentino, V. (1999) Type 3 and Type 1 ryanodine receptors are localized in triads of the same mammalian skeletal muscle fibers. J. Cell Biol., 146, 621-630.
18. 2+ stores and hippocampal synaptic plasticity. Semin. Neurosci., 8, 301-309.
19. Frey, U. and Morris, R.G.M. (1997) Synaptic tagging and long-term potentiation. Nature, 385, 533-536.
20. Frey, U., Krug, M., Reymann, K.G. and Matthies, H. (1988) Anisomycin, an inhibitor of protein synthesis, blocks late phases of LTP phenomena in the hippocampal CA1 region in vitro. Brain Res., 452, 57-65.
21. Frey, U., Müller, M. and Kuhl, D. (1996) A different form of long-lasting potentiation revealed in tissue plasminogen activator mutant mice. J. Neurosci., 16, 2057-2063.
22. 2+ release channels are differentially expressed in rabbit brain. J. Neurosci., 14, 4794-4805.
23. Gallagher, M., Burwell, R. and Burchinal, M. (1993) Severity of spatial learning impairment in aging: development of a learning index for performance in the Morris water maze. Behav. Neurosci., 107, 618-626.
24. Giannini, G., Conti, A., Mammarella, S., Scrobogna, M. and Sorrentino, V. (1995) The ryanodine receptor/calcium channel genes are widely and differentially expressed in murine brain and peripheral tissues. J. Cell Biol., 128, 893-904.
25. Goelet, P., Castellucci, V.F., Schacher, S. and Kandel, E.R. (1986) The long and the short of long-term memory - a molecular framework. Nature, 322, 419-422.
26. Grover, L.M. and Teyler, T.J. (1990) Two components of long-term potentiation induced by different patterns of activation. Nature, 347, 477-479.
27. Grover, L.M. and Teyler, T.J. (1994) Activation of NMDA receptors by low and high frequency orthodromic stimulation and their contribution to induction of long-term potentiation. Synapse, 16, 66-75.
28. 2+ stores, is required for the induction of LTD in cultured cerebellar Purkinje cells. J. Neurophysiol., 74, 2184-2188.
29. Lisman, J. (1989) A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc. Natl Acad. Sci. USA, 86, 9574-9578.
30. Malenka, R.C., Kauer, J.A., Zucker, R.J. and Nicoll, R.J. (1988) Post-synaptic calcium is sufficient for potentiation of hippocampal synaptic transmission. Science, 242, 81-84.
31. Malenka, R.C., Lancaster, B. and Zucker, R.S. (1992) Temporal limits on the rise in postsynaptic calcium required for the induction of long-term potentiation. Neuron, 9, 121-128.
32. Matthies, H. (1989) In search of the cellular mechanisms of memory. Prog. Neurobiol., 32, 277-349.
33. McNaughton, B.L. (1982) Evidence for two physiologically distinct perforant pathways to the fascia dentata. Brain Res., 199, 1-19.
34. Morris, R.G.M. (1984) Developments of a water-maze procedure for studying spatial learning in the rat. J. Neurosci. Methods, 11, 47-60.
35. Murayama, T. and Ogawa, Y. (1996) Properties of RyR3 ryanodine receptor isoform in mammalian brain. J. Biol. Chem., 271, 5079-5084.
36. Murayama, T. and Ogawa, Y. (1997) Characterization of type 3 Ryanodine receptor (RyR3) in mammalian diaphragm muscle. J. Biol. Chem., 272, 24030-24037.
37. Neveau, D. and Zucker, R.S. (1996) Postsynaptic levels of calcium needed to trigger LTD and LTP. Neuron, 16, 619-629.
38. O'Mara, S.M, Rowan, M.J. and Anwyl, R. (1995) Dantrolene inhibits long-term depression and depotentiation of synaptic transmission in the rat dentate gyrus. Neuroscience, 68, 621-624.
39. 2+ from separate presynaptic and postsynaptic intracellular stores. J. Neurosci., 16, 5951-5960.
40. Reyes-Harde, M., Empson, R., Potter, B.V.L., Galione, A. and Stanton, P.K. (1999) Evidence of a role for cyclic ADP-ribose in long-term synaptic depression in hippocampus. Proc. Natl Acad. Sci. USA, 96, 4061-4066.
41. Rosenzweig, M.R. (1996) Aspects of the search for neural mechanisms of memory. Annu. Rev. Psychol., 47, 1-32.
42. Seidenbecher, T., Reymann, K.G. and Balschun, D. (1997) A post-tetanic time window for the reinforcement of long-term potentiation by appetitive and aversive stimuli. Proc. Natl Acad. Sci. USA, 94, 1494-1499.
43. 2+ release channels in rat brain. J. Neurosci., 13, 3051-3063.
44. 2+ release channel. EMBO J., 17, 2790-2798.
45. Sorrentino, V. and Reggiani, C. (1999) Expression of Ryanodine receptor type 3 in skeletal muscle: a new partner in excitation-contraction coupling? Trends Cardiovasc. Med., 9, 53-60.
46. Stäubli, U. and Chun, D. (1996) Factors regulating the reversibility of long-term potentiation. J. Neurosci., 16, 853-860.
47. Takeshima, H. et al. (1996) Generation and characterization of mutant mice lacking Ryanodine receptor type 3. J. Biol. Chem., 271, 19649-19652.
48. Tsumoto, J. and Yasuda, H. (1996) A switching role of postsynaptic calcium in the induction of long-term potentiation or long-term depression in visual cortex. Semin. Neurosci., 8, 311-319.
49. Wagner, J.J. and Alger, B.E. (1996) Homosynaptic LTD and depotentiation: do they differ in name only? Hippocampus, 6, 24-29.
50. Walther, T., Balschun, D., Voigt, J.-P., Fink, H., Zuschratter, W., Birchmeier, C., Ganten, D. and Bader, M. (1998) Sustained long-term potentiation and anxiety in mice lacking the Mas protooncogene. J. Biol. Chem., 19, 11867-11873.
51. Wang, Y., Wu, J., Rowan, M.J. and Anwyl, R. (1996) Ryanodine produces a low frequency stimulation-induced NMDA receptor-independent long-term potentiation in the rat dentate gyrus in vitro. J. Physiol., 495, 755-767.
52. 2+ from intracellular stores. J. Neurophysiol., 77, 812-825.
53. Wilsch, V.W., Behnisch, T., Jäger, T., Reymann, K.G. and Balschun, D. (1998) When are class I metabotropic glutamate receptors necessary for long-term potentiation? J. Neurosci., 18, 6071-6080.
54. Wolfer, D.P. and Lipp, H.-P. (1992) A new computer program for detailed off-line analysis of swimming navigation in the Morris water maze. J. Neurosci. Methods, 41, 65-74.
55. Wolfer, D.P., Mohajeri, H.M., Lipp, H.P. and Schachner, M. (1998) Increased flexibility and selectivity in spatial learning of transgenic mice ectopically expressing the neural cell adhesion molecule L1 in astrocytes. Eur. J. Neurosci., 10, 708-717.
56. Xu, L., Anwyl, R. and Rowan, M.J. (1998) Spatial exploration induces a persistent reversal of long-term potentiation in rat hippocampus. Nature, 394, 891-894.
57. Xu, Y.Z. and Krnjevic, K. (1990) Induction of long-term potentiation in isolated slices of Sprague-Dawley rat hippocampus is not blocked by dantrolene sodium. J. Physiol., 426, 50.