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The Journal of Neuroscience, October 29, 2003, 23(30):9710-9718

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Cellular/Molecular
Type 8 Adenylyl Cyclase Is Targeted to Excitatory Synapses and Required for Mossy Fiber Long-Term Potentiation

Hongbing Wang,^1 * Victor V. Pineda,^1 * Guy C. K. Chan,¹ Scott T. Wong,¹ Louis J. Muglia,² and Daniel R. Storm¹

¹Department of Pharmacology, University of Washington, Seattle, Washington 98195-7280, and ²Departments of Pediatrics and Molecular Biology and Pharmacology, Washington University School of Medicine, St. Louis, Missouri 63130

Mossy fiber/CA3 long-term potentiation (LTP) is hypothesized to depend on cAMP signals generated by Ca²⁺-stimulated adenylyl cyclases AC1 or AC8. AC1 gene knock-out mice (AC1^–/–) show a partial reduction in mossy fiber LTP, suggesting that either AC8 activity is also critical for mossy fiber LTP or that there is a component of mossy fiber LTP that is independent of CaM-activated adenylyl cyclases. To address this issue, mossy fiber LTP was examined in hippocampal slices from AC8^–/– and AC1^–/– x AC8^–/– double knock-out mice (DKO). Despite the fact that AC8 contributes only a small fraction of the Ca²⁺-stimulated adenylyl cyclase activity in the hippocampus and is less sensitive to Ca²⁺ than AC1, AC8^–/– mice exhibited mossy fiber LTP defects comparable with AC1^–/– and DKO mice. Furthermore, short-term plasticity was disrupted in AC8^–/– mice but not in AC1^–/– mice. Because AC1 is not localized at the excitatory synapses in hippocampal neurons, we hypothesized that AC8 may be targeted to synapses, in which higher synaptic-specific Ca²⁺ increases occur. Here, we report that AC8 accumulates in puncta of dendrites and axons in hippocampal neurons and colocalizes with synaptic marker proteins. These data indicate that both synaptic and nonsynaptic cAMP signals, generated by different Ca²⁺-stimulated adenylyl cyclases, are required for mossy fiber LTP.

Key words: adenylyl cyclase; axon; calcium; calmodulin; dendrite; hippocampus; LTP; MDCK; mossy fiber; paired-pulse facilitation; synapse; targeting

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Received May 28, 2003; revised August 27, 2003; accepted September 3, 2003.

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