Impaired cerebellar long-term potentiation in type I adenylyl cyclase mutant mice

Neuron

Volumn 20, Issue 6, 1998, Pages 1199-1210

  Storm, Daniel R ^a   Hansel, Christian ^b   Hacker, Beth ^a   Parent, Angèle ^b   Linden, David J ^b  

^a UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; CALCIMYCIN; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DERIVATIVE; MESSENGER RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CEREBELLUM; CONTROLLED STUDY; ENZYME ACTIVITY; GENE; GRANULE CELL; LONG TERM POTENTIATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL;

EID: 17644438421     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80500-0     Document Type: Article

References (66)

1. Banbury Conference on Genetic Background in Mice. (1997). Mutant mice and neuroscience: recommendations concerning genetic background. Neuron 19, 755-759.
2. Bradley, J., Zhang, Y., Baskin, R., Lester, H.A., Ronnett, G.V., and Zinn, K. (1997). Functional expression of the heteromeric "olfactory" cyclic nucleotide-gated channel in the hippocampus: a potential effector of synaptic plasticity in brain neurons. J. Neurosci. 17, 1993-2005.
3. Byrne, J.H., and Kandel, E.R. (1996). Presynaptic facilitation revisited: state and time dependence. J. Neurosci. 16, 425-435.
4. 2+/calmodulin stimulated enzyme expressed in discrete regions of rat brain. J. Biol. Chem. 269, 12190-12196.
5. Castillo, P.E., Janz, R., Südhof, T.C., Tzounopoulos, T., Malenka, R.C., and Nicoll, R.A. (1997). Rab3A is essential for mossy fibre long-term potentiation in the hippocampus. Nature 388, 590-593.
6. Chavis, P., Mollard, P., Bockaert, J., and Manzoni, O. (1998). Visualization of cyclic AMP-regulated presynaptic activity at cerebellar granule cells. Neuron 20, 773-781.
7. Chen, C., and Tonegawa, S. (1997). Molecular genetic analysis of synaptic plasticity, activity-dependent neural development, learning and memory in the mammalian brain. Annu. Rev. Neurosci. 20, 157-184.
8. Choi, E.J., Wong, S.T., Hinds, T.R., and Storm, D.R. (1992a). Calcium and muscarinic agonist stimulation of type I adenylyl cyclase in whole cells. J. Biol. Chem. 267, 12440-12442.
9. Choi, E.J., Xia, Z., and Storm, D.R. (1992b). Stimulation of the type III olfactory adenylyl cyclase by calcium and calmodulin. Biochemistry 31, 6492-6498.
10. Crepel, F., and Jaillard, D. (1991). Pairing of pre-and postsynaptic activities in cerebellar Purkinje cells induces long-term changes in synaptic efficacy in vitro. J. Physiol. 432, 123-141.
11. Davis, R.L. (1996). Physiology and biochemistry of Drosophila learning mutants. Physiol. Rev. 76, 299-317.
12. De Zeeuw, C.I., Hansel, C., Bian, F., Koekkoek, S.K.E., van Alphen, A.M., Linden, D.J., and Oberdick, J. (1998). Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar long-term depression and adaptation of the vestibulo-ocular reflex. Neuron 20, 495-508.
13. Dixon, D., and Atwood, H.L. (1989). Adenylate cyclase system is essential for long-term facilitation at the crayfish neuromuscular junction. J. Neurosci. 9, 4246-4252.
14. El-Husseini, A.E.-D., Bladen, C., and Vincent, S.R. (1995). Expression of the olfactory cyclic-nucleotide gated channel (cng1) in the rat-brain. NeuroReport 6, 1459-1463.
15. Frey, U., Huang, Y.-Y., and Kandel, E.R. (1993). Effects of cAMP simulate a late stage of LTP in hippocampal CA1 neurons. Science 260, 1661-1664.
16. Gerlai, R. (1996). Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci. 19, 177-181.
17. Goodwin, S.F., DelVecchio, M., Velinzon, K., Hogel, C., Russell, S.R.H., Tully, T., and Kaiser, K. (1997). Defective learning in mutants of the Drosophila gene for a regulatory subunit of cAMP-dependent protein kinase. J. Neurosci. 17, 8817-8827.
18. Harris, D.M., Asaad, M.M., Phillips, M.B., Goldenberg, H.J., and Antonaccio, M.J. (1979). Inhibition of adenylate cyclase in human blood platelets by 9-substituted adenine derivatives. J. Cyc. Nucleotide Res. 5, 125-134.
19. Hirano, T. (1990). Depression and potentiation of the synaptic transmission between a granule cell and a Purkinje cell in rat cerebellar culture. Neurosci. Lett. 119, 141-144.
20. Hirano, T. (1991). Differential pre-and postsynaptic mechanisms for synaptic potentiation and depression between a granule cell and a Purkinje cell in rat cerebellar culture. Synapse 7, 321-323.
21. Hopkins, W.F., and Johnston, D. (1984). Frequency-dependent nor-adrenergic modulation of long-term potentiation in the hippocampus. Science 226, 350-352.
22. + channels is independent of adenylate cyclase activation. Science 240, 1652-1655.
23. Huang, Y.-Y., and Kandel, E.R. (1995). D1/D5 receptor agonists induce a protein synthesis-dependent late potentiation in the CA1 region of hippocampus. Proc. Natl. Acad. Sci. USA 92, 2446-2450.
24. Huang, Y.Y., and Kandel, R. (1996). Modulation of both the early and the late phase of mossy fiber LTP by the activation of β-adrenergic receptors. Neuron 16, 611-617.
25. Huang, Y.Y., Li, X.C., and Kandel, E.R. (1994). cAMP contributes to mossy fiber LTP by initiating both a covalently mediated early phase and macromolecular synthesis-dependent late phase. Cell 79, 69-79.
26. Ito, M. (1984). The Cerebellum and Neural Control (New York: Raven). Johnston, D., Williams, S., Jaffe, D., and Gray, R. (1992). NMDA-receptor-independent long-term potentiation. Annu. Rev. Physiol. 54, 489-505.
27. γ mutant mice. Cell 83, 1223-1231.
28. Kingston, P.A., Zufall, F., and Barnstable, C.J. (1996). Rat hippocampal neurons express genes for both rod retinal and olfactory cyclic nucleotide-gated channels: novel targets for cAMP/cGMP function. Proc. Natl. Acad. Sci. USA 93, 10440-10445.
29. Kramer, R.H., and Tibbs, G.R. (1996). Antagonists of cyclic nucleotide-gated channels and molecular mapping of their site of action. J. Neurosci. 16, 1285-1293.
30. Lalonde, R., Botez, M.I., Joyal, C.C., and Caumartin, M. (1992). Motor abnormalities in lurcher mutant mice. Physiol. Behav. 51, 523-525.
31. Linden, D.J. (1996). Cerebellar long-term depression as investigated in a cell culture preparation. Behav. Brain Sci. 19, 339-346 and 482-487.
32. Linden, D.J. (1997). Long-term potentiation of glial synaptic currents in cerebellar culture. Neuron 18, 983-994.
33. Linden, D.J. (1998). Synaptically-evoked glutamate transport currents may be used to detect the expression of long-term potentiation in cerebellar culture. J. Neurophys. 79, 3151-3156.
34. Linden, D.J., and Connor, J.A. (1995). Long-term synaptic depression. Annu. Rev. Neurosci. 18, 319-357.
35. Linden, D.J., Dickinson, M.H., Smeyne, M., and Connor, J.A. (1991). A long-term depression of AMPA currents in cultured cerebellar Purkinje neurons. Neuron 7, 81-91.
36. Llinás, R., Lang, E.J., and Welsh, J.P. (1997). The cerebellum, LTD, and memory: alternative views. Learning and Memory 3, 445-455.
37. Matthies, H., and Reymann, K.G. (1993). Protein kinase A inhibitors prevent the maintenance of hippocampal long-term potentiation. NeuroReport 4, 712-714.
38. Mauk, M.D., Garcia, K.S., Medina, J.F., and Steele, P.M. (1998). Does cerebellar LTD mediate motor learning? Toward resolution without a smoking gun. Neuron 20, 359-362.
39. Narasimhan, K., and Linden, D.J. (1996). Defining a minimal computational unit for cerebellar long-term depression. Neuron 17, 333-341.
40. i-coupled receptors in vivo. J. Biol. Chem. 271, 33308-33316.
41. Olwin, B.B., and Storm, D.R. (1985). Binding of calcium to calmodulin-protein complexes. Biochemistry 24, 8081-8086.
42. Otmakhova, N.A., and Lisman, J.E. (1996). D1/D5 dopamine receptor activation increases the magnitude of long-term potentiation at CA1 hippocampal synapses. J. Neurosci. 16, 7478-7486.
43. Parent, A., Schrader, K., Munger, S.D., Reed, R.R., Linden, D.J., and Ronnett, G.V. (1998). Synaptic transmission and hippocampal long-term potentiation in an olfactory cyclic nucleotide-gated channel type 1 (OCNC1) null mouse. J. Neurophys. 79, 3295-3301.
44. Pekhletski, R., Gerlai, R., Overstreet, L., Huang, X.-P., Agopyan, N., Slater, N.T., Abramow-Newerly, W., Roder, J.C., and Hampson, D.R. (1996). Impaired cerebellar synaptic plasticity and motor performance in mice lacking the mGluR4 subtype of metabotropic glutamate receptor. J. Neurosci. 16, 6364-6373.
45. Perrett, S.P., and Mauk, M.D. (1995). Extinction of conditioned eyelid responses requires the anterior lobe of cerebellar cortex. J. Neurosci. 15, 2074-2080.
46. Raymond, J.L., Lisberger, S.G., and Mauk, M.D. (1996). The cerebellum: a neuronal learning machine? Science 272, 1126-1131.
47. Reddy, R., Smith, D., Wayman, G., Wu, Z., Villacres, E.C., and Storm, D.R. (1995). Voltage-sensitive adenylyl cyclase activity in cultured neurons. A calcium-independent phenomenon. J. Biol. Chem. 270, 14340-14346.
48. Sakurai, M. (1987). Synaptic modification of parallel fiber-Purkinje cell transmission in in vitro guinea-pig cerebellar slices. J. Physiol. 394, 463-480.
49. Sakurai, M. (1990). Calcium is an intracellular mediator of the climbing fiber in induction of cerebellar long-term depression. Proc. Natl. Acad. Sci. USA 87, 3383-3385.
50. Salin, P.A., Malenka, R.C., and Nicoll, R.A. (1996). cAMP mediates a presynaptic form of LTP at cerebellar parallel fiber synapses. Neuron 16, 797-803.
51. 2+ activity. NeuroReport 3, 231-234.
52. Tang, W.J., Krupinski, J., and Gilman, A.G. (1991). Expression and characterization of calmodulin activated (type I) adenylyl cyclase. J. Biol. Chem. 266, 8595-8603.
53. Thomas, M.J., Moody, T.D., Makhinson, M., and O'Dell, T.J. (1996). Activity-dependent β-adrenergic modulation of low-frequency stimulation induced LTP in the hippocampal CA1 region. Neuron 17, 475-482.
54. Thompson, R.F. (1986). The neurobiology of learning and memory. Science 233, 941-947.
55. Trudeau, L.E., Emery, D.G., and Haydon, P.G. (1996). Direct modulation of the secretory machinery underlies PKA-dependent synaptic facilitation in hippocampal neurons. Neuron 17, 789-797.
56. 2+-sensitive adenylyl cyclase activity is disrupted in the brains of type I adenylyl cyclase mutant mice. J. Biol. Chem. 270, 14352-14357.
57. Villacres, E.C., Wong, S.T., Chavkin, C., and Storm, D.R. (1998). Type I adenylyl cyclase mutant mice have impaired mossy fiber long-term potentiation. J. Neurosci. 18, 3186-3194.
58. Wang, J.-H., and Kelly, P.T. (1997). Attenuation of paired-pulse facilitation associated with synaptic potentiation mediated by postsynaptic mechanisms. J. Neurophys. 78, 2707-2716.
59. s-coupled receptors in vivo. J. Biol. Chem. 269, 25400-25405.
60. Wei, J.Y., Cohen, E.D., and Barnstable, C.J. (1997). Direct blockade of both cloned rat rod photoreceptor cyclic nucleotide-gated non-selective cation (CNG) channel alpha-subunit and native CNG channels from Xenopus rod outer segments by H-8, a non-specific cyclic nucleotide-dependent protein kinase inhibitor. Neurosci. Lett. 233, 37-40.
61. Weisskopf, M.G., Castillo, P.E., Zalutsky, R.A., and Nicoll, R.A. (1994). Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 23, 1878-1882.
62. Wu, Z.L., Thomas, S.A., Villacres, E.C., Xia, Z., Simmons, M.L., Chavkin, C., Palmiter, R.D., and Storm, D.R. (1995a). Altered behavior and long-term potentiation in type I adenylyl cyclase mutant mice. Proc. Natl. Acad. Sci. USA 92, 220-224.
63. Wu, Z., Wong, S.T., and Storm, D.R. (1995b). Modification of the calcium and calmodulin sensitivity of the type I adenylyl cyclase by mutagenesis of its calmodulin binding domain. J. Biol. Chem. 268, 23766-23768.
64. Xia, Z.G., Refsdal, C.D., Merchant, K.M., Dorsa, D.M., and Storm, D.R. (1991). Distribution of mRNA for the calmodulin-sensitive adenylate cyclase in rat brain: expression in areas associated with learning and memory. Neuron 6, 431-443.
65. 2+ channel blocker-like action in rat cerebellar granule cells. Eur. J. Pharm. 303, 101-108.
66. Zucker, R.S. (1996). Exocytosis: a molecular and physiological perspective. Neuron 17, 1049-1055.