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Serotonin Stimulation of Camp-Dependent Plasticity in Aplysia Sensory Neurons Is Mediated by Calmodulin- Sensitive Adenylyl Cyclase

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Serotonin Stimulation of Camp-Dependent Plasticity in Aplysia Sensory Neurons Is Mediated by Calmodulin- Sensitive Adenylyl Cyclase Serotonin stimulation of cAMP-dependent plasticity in Aplysia sensory neurons is mediated by calmodulin- sensitive adenylyl cyclase Allison H. Lina, Jonathan E. Cohena, Qin Wana, Katelyn Niub, Pragya Shresthaa, Steven L. Bernsteinc, and Thomas W. Abramsa,b,1 aDepartment of Pharmacology, bProgram in Neuroscience, and cDepartment of Ophthalmology, University of Maryland School of Medicine, Baltimore, MD 21201-1559 Edited* by Eric Richard Kandel, Columbia University, New York, NY, and approved July 13, 2010 (received for review April 2, 2010) Calmodulin (CaM)-sensitive adenylyl cyclase (AC) in sensory neu- SNs. In these studies, we focused on the biochemical properties and rons (SNs) in Aplysia has been proposed as a molecular coincidence regulation of the two AC isoforms that are expressed in Aplysia detector during conditioning. We identified four putative ACs in SNs. One of these isoforms, AC-AplA, is stimulated by Ca2+/CaM, Aplysia CNS. CaM binds to a sequence in the C1b region of AC- whereas the second, AC-AplC, is directly inhibited by Ca2+. AplA that resembles the CaM-binding sequence in the C1b region Knockdown experiments revealed that the Ca2+/CaM-sensitive of AC1 in mammals. Recombinant AC-AplA was stimulated by Ca2+/ isoform is responsible for the great majority of 5-HT-induced CaM. AC-AplC is most similar to the Ca2+-inhibited AC5 and AC6 cAMP-mediated plasticity in SN somata. This demonstrates that the in mammals. Recombinant AC-AplC was directly inhibited by Ca2+, CaM-sensitive AC is indeed dually regulated in those neurons where independent of CaM. AC-AplA and AC-AplC are expressed in SNs, it has been hypothesized to function as an associative integrator. whereas AC-AplB and AC-AplD are not. Knockdown of AC-AplA demonstrated that serotonin stimulation of cAMP-dependent plas- Results ticity in SNs is predominantly mediated by this CaM-sensitive AC. In an initial effort to identify AC isoforms expressed in Aplysia We propose that the coexpression of a Ca2+-inhibited AC in SNs, CNS, we used degenerate primers corresponding to sequences NEUROSCIENCE together with a Ca2+/CaM-stimulated AC, would enhance the as- within the two cytoplasmic regions that are highly conserved 2+ sociative requirement for coincident Ca influx and serotonin for among transmembrane ACs in metazoans, the C1a and C2a re- effective stimulation of cAMP levels and initiation of plasticity me- gions (19, 20). We isolated cDNA clones from Aplysia CNS that diated by AC-AplA. corresponded to three distinct sequences based on restriction map analysis and sequencing. Full-length sequences of these coincidence detector | associative learning | synaptic plasticity | classical putative AC transcripts, AC-AplA, AC-AplB, and AC-AplC, were conditioning | calcium generated by 5′ and 3′ rapid amplification of cDNA ends (RACE) (GenBank accession nos. AY843025, AY843026, and hree decades ago, early experimental evidence from two sim- AY843027). The membrane-associated ACs of multicellular Tple invertebrates, Aplysia and Drosophila (1, 2), demonstrated animals have two transmembrane domains, each with approxi- that cAMP plays an important role in learning. Based on studies mately six membrane-spanning α-helices, separated by a cyto- of classical conditioning in Aplysia, calmodulin (CaM)-sensitive plasmic C1 domain. A second cytoplasmic domain, C2, is located adenylyl cyclase (AC) was proposed to play an associative role in at the C terminus and a third, relatively short cytoplasmic se- learning (3–5). CaM-sensitive AC was similarly implicated in quence is at the N terminus (21). Analysis of these putative conditioning in Drosophila (6, 7). Subsequently, CaM-sensitive AC Aplysia AC isoforms indicated a similar structure, with two hy- was also found to be important in learning in mammals; mouse drophobic domains containing five to seven membrane-spanning mutants that lack CaM-sensitive ACs 1 and 8 displayed deficits in α-helices per domain, similar to predictions for mammalian ACs memory (8, 9), and overexpression of AC1 in mice improved (Fig. S1). Because in transmembrane ACs the C1a and C2a cy- memory (10). toplasmic regions interact to create the nucleotide binding site The CaM-sensitive AC in Aplysia was hypothesized to serve required for catalytic activity, we predict there is an even number as an associative coincidence detector that integrates two signals of membrane crossings, namely six. A fourth putative AC, AC- 2+ during classical conditioning: (i)Ca influx during sensory AplD, was identified through a search of the Aplysia EST data- neuron (SN) activity triggered by the conditioned stimulus and (ii) base (22) and a full-length sequence was obtained by RACE serotonin (5-hydroxytryptamine; 5-HT), released by modulatory (GenBank accession no. HM030824). Analysis of this transcript interneurons during the unconditioned stimulus. This coincidence indicated a similar topology (Fig. S1D). The predicted C2 do- detector concept was based on cellular electrophysiology and main of AC-AplA is nearly three times the length of the other C2 – biochemical assays (5, 11 14). Evidence suggesting that CaM- domains (Table S1). All metazoan transmembrane ACs contain sensitive AC may function as a coincidence detector has also been highly conserved sequences in the C1a and C2a regions that obtained in Drosophila (15) and in studies of the mammalian AC1 (16). Nevertheless, the proposed role of CaM-sensitive AC as a coincidence detector during learning has not been directly Author contributions: A.H.L., J.E.C., S.L.B., and T.W.A. designed research; A.H.L., J.E.C., tested in Aplysia or any other system. Q.W., K.N., P.S., and T.W.A. performed research; A.H.L., J.E.C., Q.W., P.S., and T.W.A. Although CaM-sensitive AC was implicated in synaptic plasticity analyzed data; and A.H.L., J.E.C., K.N., S.L.B., and T.W.A. wrote the paper. during learning in Aplysia more than 25 years ago, this enzyme from The authors declare no conflict of interest. Aplysia had not been characterized at the molecular level. Recent *This Direct Submission article had a prearranged editor. studies have raised questions about the role of the cAMP cascade Data deposition: The sequences reported in this paper have been deposited in the Gen- in associative facilitation at Aplysia SN-to-motor neuron (MN) Bank database (accession nos. AY843025, AY843026, AY843027, and HM030824). synapses (17, 18). We have investigated which AC isoforms are 1To whom correspondence should be addressed. E-mail: [email protected]. expressed in Aplysia CNS and in SNs in particular, and determined This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. whether a CaM-sensitive AC is coupled to 5-HT receptors in the 1073/pnas.1004451107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1004451107 PNAS Early Edition | 1of6 Downloaded by guest on September 28, 2021 together form the ATP-binding pocket in the catalytic core the other cytoplasmic domains (Fig. S5). The C1b region of AC- (Fig. S2) (23–25). The four putative Aplysia ACs share this AplA contains a sequence with similarity to the CaM-binding conserved pattern of residues (Fig. S2). All four C1a regions region of mammalian AC1 (28) (Fig. 1). CaM-binding motifs are contain the characteristic GDCYYC sequence (19, 20), which is relatively diverse, and include the 1-8-14 pattern of hydrophobic conserved in all transmembrane ACs in metazoans that we have residues (35, 36). AC1 contains a 1-8 motif, where the 1 and 8 examined, including Trichoplax (Fig. S2C). Moreover, in the residues are both required for CaM binding (28). Both AC-AplA purine-binding pocket of the C2a region, all four predicted and rutabaga AC contain a 1-8-15 pattern of hydrophobic resi- sequences contain the lysine and aspartate residues that typify dues within the C1b region (37). A 25-aa peptide from AC-AplA ACs, in contrast to guanylyl cyclases (24, 26). containing this 1-8-15 sequence bound CaM. To determine which AC-AplA and AC-AplC Resemble AC Isoforms That Are Regulated by hydrophobic amino acids mediated CaM binding, we mutated the Ca2+. To identify the CaM-sensitive AC in Aplysia, which had been motif in the AC-AplA C1 domain at positions 1 and 8 (F498S/ proposed to play an associative role in classical conditioning, V505D), positions 8 and 15 (V505D/V512D), or positions 15 we compared the four Aplysia sequences with the C1a and C2a alone (V512D). CaM binding was eliminated in both the F498S/ regions of all nine mammalian and four of the Drosophila transmembrane ACs. In mammals, AC1 and AC8 are stimulated by Ca2+/CaM (27–29). ACs 5 and 6 are highly similar isoforms that are directly inhibited by Ca2+ (30). ACs 2, 4, and 7 are closely related, Ca2+-independent ACs. AC3 is inhibited by CaM kinase II (31). AC9 is regulated by CaM kinase II, PKC, and calcineurin (32, 33). The C1a region of AC-AplA is particularly similar (72%) to rutabaga, the Ca2+/CaM-sensitive AC in Drosophila (34) (Fig. S3), which suggested that AC-AplA may be the Ca2+/CaM-sensitive AC in Aplysia CNS (Fig. S4). AC-AplA is also similar to ACs 1, 5, and 6, as is rutabaga AC. However, AC-AplC is the Aplysia isoform most similar to AC5 and AC6 (Fig. S4). Based on this analysis, we predicted that AC-AplA might be stimulated by Ca2+/CaM and that AC-AplCmightbeCa2+-inhibited. The C1a region of AC-AplBis not highly similar to any single group of ACs, whereas the C2a do- main of AC-AplB is most similar to members of the AC2/4/7 group (Figs. S3 and S4). AC-AplD has a relatively low similarity to all of the mammalian ACs; however, it is most similar to AC9 and to Dro- sophila AC 35C, the Drosophila homolog of AC9 (19) (Fig.
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