Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry

Moroz, Leonid L.; Edwards, John; Puthanveettil, Sathyanarayanan V.; Kohn, Andrea B.; Ha, Thomas; Heyland, Andreas; Knudsen, Bjarne; Sahni, Anuj; Yu, Fahong; Liu, Li; Jezzini, Sami H.; Lovell, Peter V.; Iannucculli, William; Chen, Minchen; Nguyen, Tan Van; Sheng, Huitao; Shaw, Regina; Kalachikov, Sergey; Panchin, Yu. V.; Farmerie, William G.; Russo, James J.; Ju, Jingyue; Kandel, Eric R.

doi:10.1016/j.cell.2006.09.052

Cited by 300 publications

(302 citation statements)

References 62 publications

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“…Table 1. Comparison of the amino acid sequence recognized by the applied rat anti-nNOS antibody and the equivalent NOS amino acid sequences identified in Drosophila (Stasiv, et al, 2001) and some mollusks (Aplysia [Moroz, et al, 2006]; Lymnaea [Korneev et al, 1998[Korneev et al, , 2005). Identical sequences are highlighted.…”

Section: Possible Functional Consequences Of the Distribution Of Nadpmentioning

confidence: 99%

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Nacsa

Elekes

Serfözö

2015

Micron

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This manuscript is contextually identical with the following published paper:For the first time, we have shown that NADPH-diaphorase reactivity and NOS immunoreactivity are bound to transmitter vesicle membranes in varicosities of ganglionic neuropil of an invertebrate. The presence of NOS in certain synaptic configurations of the snail CNS suggests a role of NO in fast and target specific interneuronal signaling processes. 3 ABSTRACTComparative studies on the nervous system revealed that nitric oxide (NO) retains its function through the evolution. In vertebrates NO can act in different ways: it is released solely or as a co-transmitter, released from presynaptic or postsynaptic site, spreads as a volumetric signal or targets synaptic proteins. In invertebrates, however, the possible sites of NO release have not yet been identified. Therefore, in the present study, the subcellular distribution of the NO synthase (NOS) was examined in the central nervous system (CNS) of two gastropod species, the terrestrial snail, Helix pomatia and the pond snail, Lymnaea stagnalis, which are model species in comparative neurobiology. For the visualization of NOS NADPH-diaphorase histochemistry and an immunohistochemical procedure using a universal anti-NOS antibody were applied. At light microscopic level both techniques labeled identical structures in sensory tracts ramifying in the neuropils of central ganglia and cell bodies of the Lymnaea and Helix CNS. At ultrastructural level NADPH-d reactive/NOS-immunoreactive materials were localized on the nuclear envelope and membrane segments of the rough and smooth endoplasmic reticulum, as well as the cell membrane and axolemma of positive perikarya. NADPH-d reactive and NOS-immunoreactive varicosities connected to neighboring neurons with both unspecialized and specialized synaptic contacts. In the varicosities, the majority of the NADPH-d reactive/NOS-immunoreactive membrane segments were detected in round and pleomorph agranular vesicles of small size (50-200 nm). However, only a small portion (16%) of the vesicles displayed the NADPH-d reactivity/NOSimmunoreactivity. No evidence for the postsynaptic location of NOS was found. Our results suggest that the localization of NADPH-diaphorase and NOS is identical in the snail nervous system. In contrast to vertebrates, however, NO seems to act exclusively in an anterograde way possibly released from membrane segments of the presynaptic transmitter vesicle surface. Based on the subcellular distribution of NOS, NO could be both a volume and a synaptic mediator, in addition NO may function as a co-transmitter.

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Section: Possible Functional Consequences Of the Distribution Of Nadpmentioning

confidence: 99%

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Nacsa

Elekes

Serfözö

2015

Micron

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“…The methods for cloning and sequencing (71), in situ hybridization (40), and behavior and electrophysiology (28-30, 37, 43) were generally the same as described previously. See SI Appendix for details.…”

Section: Methodsmentioning

confidence: 99%

Hyperpolarization-activated, cyclic nucleotide-gated cation channels in Aplysia : Contribution to classical conditioning

Yang

Kuzyk

Antonov

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Hyperpolarization-activated, cyclic nucleotide-gated cation (HCN) channels are critical regulators of neuronal excitability, but less is known about their possible roles in synaptic plasticity and memory circuits. Here, we characterized the HCN gene organization, channel properties, distribution, and involvement in associative and nonassociative forms of learning in Aplysia californica. Aplysia has only one HCN gene, which codes for a channel that has many similarities to the mammalian HCN channel. The cloned acHCN gene was expressed in Xenopus oocytes, which displayed a hyperpolarization-induced inward current that was enhanced by cGMP as well as cAMP. Similarly to its homologs in other animals, acHCN is permeable to K + and Na + ions, and is selectively blocked by Cs + and ZD7288. We found that acHCN is predominantly expressed in inter-and motor neurons, including LFS siphon motor neurons, and therefore tested whether HCN channels are involved in simple forms of learning of the siphon-withdrawal reflex in a semiintact preparation. ZD7288 (100 μM) significantly reduced an associative form of learning (classical conditioning) but had no effect on two nonassociative forms of learning (intermediate-term sensitization and unpaired training) or baseline responses. The HCN current is enhanced by nitric oxide (NO), which may explain the postsynaptic role of NO during conditioning. HCN current in turn enhances the NMDA-like current in the motor neurons, suggesting that HCN channels contribute to conditioning through this pathway.HCN channels | learning and memory | NMDA | nitric oxide | Aplysia H yperpolarization-activated, cyclic nucleotide-gated (HCN), cation nonselective ion channels generate hyperpolarization-activated inward currents (I h ) and thus tend to stabilize membrane potential (1-3). In addition, binding of cyclic nucleotides (cAMP and cGMP) to the C-terminal cyclic nucleotide binding domain (CNBD) enhances I h and thus couples membrane excitability with intracellular signaling pathways (2, 4). HCN channels are widely important for numerous systemic functions such as hormonal regulation, heart contractility, epilepsy, pain, central pattern generation, sensory perception (4-15), and learning and memory (16-24).However, in previous studies it has been difficult to relate the cellular effects of HCN channels directly to their behavioral effects, because of the immense complexity of the mammalian brain. We have therefore investigated the role of HCN channels in Aplysia, which has a numerically simpler nervous system (25). We first identified and characterized an HCN gene in Aplysia, and showed that it codes for a channel that has many similarities to the mammalian HCN channel. We found that the Aplysia HCN channel is predominantly expressed in motor neurons including LFS neurons in the siphon withdrawal reflex circuit (26, 27). We therefore investigated simple forms of learning of that reflex in a semiintact preparation (28-30) and found that HCN current is involved in classical conditioning and enhances the ...

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“…Second, A. californica possess a well-identified CNS and reproductive axis (Kandel, 1979) that should greatly facilitate our understanding of neural and reproductive roles of GnRH. Lastly, the recent publication of A. californica CNS transcriptome (Moroz et al, 2006) is a tremendous resource that aids in the search for vertebrate neuropeptide homologues in mollusks. With the help of the CNS transcriptome database, we cloned the first gastropod GnRH-like molecule (apGnRH) in A. californica.…”

Section: Introductionmentioning

confidence: 99%

Molecular cloning, expression pattern, and immunocytochemical localization of a gonadotropin-releasing hormone-like molecule in the gastropod mollusk, Aplysia californica

Zhang

Tello

Zhang

et al. 2008

General and Comparative Endocrinology

105

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Successful reproduction in vertebrates depends upon the actions of gonadotropin-releasing hormone (GnRH). Despite the wide presence of GnRH in Phylum Chordata, GnRH has not been isolated in protostomes other than the common octopus. To provide information on the evolution of this critical hormone, we isolated the full-length cDNA of a GnRH-like molecule from the central nervous system of a gastropod mollusk, the sea hare Aplysia californica. The open reading frame of this cDNA encodes a protein of 147 amino acids. The molecular architecture of the deduced protein is highly homologous to that reported for the prepro-octopus GnRH (oct-GnRH) and consists of a putative signal peptide, a GnRH dodecapeptide, a downstream processing site, and a GnRH-associated peptide (GAP). The deduced amino acid sequence of the Aplysia GnRH (ap-GnRH) is QNYHFSNGWYAG and differs from oct-GnRH by only two amino acids. The transcript for ap-GnRH is widely expressed in the central nervous system (CNS), the ovotestis, and the atrial gland, an exocrine gland. Immunocytochemistry (ICC) using an antiserum against oct-GnRH detected immunoreactive neurons in all CNS ganglia examined, and the staining was abolished by the preadsorption of the antiserum with synthetic ap-GnRH. In sum, ap-GnRH sequence is the first gastropod GnRH-like molecule to be elucidated. Further, it represents one of the only two GnRH-like molecules found outside Phylum Chordata. These data refute the possibility that oct-GnRH arose singly in cephalopods by convergent evolution and provide valuable support for an ancient origin of GnRH during metazoan evolution.

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Neuronal Transcriptome of Aplysia: Neuronal Compartments and Circuitry

Cited by 300 publications

References 62 publications

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Ultrastructural localization of NADPH diaphorase and nitric oxide synthase in the neuropils of the snail CNS

Hyperpolarization-activated, cyclic nucleotide-gated cation channels in Aplysia : Contribution to classical conditioning

Molecular cloning, expression pattern, and immunocytochemical localization of a gonadotropin-releasing hormone-like molecule in the gastropod mollusk, Aplysia californica

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