Systemic RNA interference for the study of learning and memory in an insect

Takahashi, Tamiko; Hamada, Atsuko; Miyawaki, Katsuyuki; Matsumoto, Y.; Mito, Taro; Noji, Sumihare; Mizunami, Makoto

doi:10.1016/j.jneumeth.2009.01.002

Cited by 45 publications

(38 citation statements)

References 48 publications

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“…In fruit-flies, the participation of Kenyon cells of the mushroom body in LTM formation is well established [8], and this most likely applies to crickets, because we observed that mRNA of NO synthase (NOS) and soluble guanylyl cyclase (sGC), key molecules for LTM formation in crickets, are densely distributed in outer and inner Kenyon cells, respectively [45]. It has also been reported that enzymatic activity of CaMKII is enriched in Kenyon cells in fruit-flies [18], [46], honey bees [47], [48] and cockroaches [21].…”

Section: Discussionmentioning

confidence: 84%

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

et al. 2014

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Ca2+/calmodulin (CaM)-dependent protein kinase II (CaMKII) is a key molecule in many systems of learning and memory in vertebrates, but roles of CaMKII in invertebrates have not been characterized in detail. We have suggested that serial activation of NO/cGMP signaling, cyclic nucleotide-gated channel, Ca2+/CaM and cAMP signaling participates in long-term memory (LTM) formation in olfactory conditioning in crickets, and here we show participation of CaMKII in LTM formation and propose its site of action in the biochemical cascades. Crickets subjected to 3-trial conditioning to associate an odor with reward exhibited memory that lasts for a few days, which is characterized as protein synthesis-dependent LTM. In contrast, animals subjected to 1-trial conditioning exhibited memory that lasts for only several hours (mid-term memory, MTM). Injection of a CaMKII inhibitor prior to 3-trial conditioning impaired 1-day memory retention but not 1-hour memory retention, suggesting that CaMKII participates in LTM formation but not in MTM formation. Animals injected with a cGMP analogue, calcium ionophore or cAMP analogue prior to 1-trial conditioning exhibited 1-day retention, and co-injection of a CaMKII inhibitor impaired induction of LTM by the cGMP analogue or that by the calcium ionophore but not that by the cAMP analogue, suggesting that CaMKII is downstream of cGMP production and Ca2+ influx and upstream of cAMP production in biochemical cascades for LTM formation. Animals injected with an adenylyl cyclase (AC) activator prior to 1-trial conditioning exhibited 1-day retention. Interestingly, a CaMKII inhibitor impaired LTM induction by the AC activator, although AC is expected to be a downstream target of CaMKII. The results suggest that CaMKII interacts with AC to facilitate cAMP production for LTM formation. We propose that CaMKII serves as a key molecule for interplay between Ca2+ signaling and cAMP signaling for LTM formation, a new role of CaMKII in learning and memory.

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Section: Discussionmentioning

confidence: 84%

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

et al. 2014

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“…Through this simple histochemical reaction, NOS-like enzymes have been identified in the neurons of a number of vertebrate and invertebrate taxa and NO was recognized as one of the most ancient signaling molecules which is widespread in all animal phyla (see González-Domenech and Muñoz-Chápuli, 2010;Andreakis et al, 2011, for phylogenetic analyses of metazoan NOS). The molecular characteristics of invertebrate NOSs have been identified in some taxa: cnidarians (Panchin et al, 2002), arthropods (Regulski and Tully, 1995;Yuda et al, 1996;Nighorn et al, 1998;Imamura et al, 2002;Watanabe et al, 2005;Takahashi et al, 2009), molluscs (Scheinker et al, 2005), and amphioxus (Panchin et al, 2003). Most invertebrate NOSs appear to be similar to the constitutive neuronal NOS of mammals, except for their N-termini, which lack a PSD-95/discs-large/ZO-1 (PDZ) domain.…”

Section: Indexing Terms: Nos; Stramonita Haemastoma; Nadph Diaphorasementioning

confidence: 99%

Cellular, biochemical, and molecular characterization of nitric oxide synthase expressed in the nervous system of the prosobranch Stramonita haemastoma (Gastropoda, Neogastropoda)

Cioni¹,

Patti²,

Venturini³

et al. 2011

J of Comparative Neurology

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Nitric oxide synthase (NOS) has been characterized in several opistobranchs and pulmonates but it was much less investigated in prosobranchs, which include more than 20,000 species and account for most of the gastropod diversity. Therefore, new data from this large group are needed for a better knowledge of the molecular evolution of NOS enzymes in molluscs. This study focused on NOS expressed in the nervous system of the prosobranch neogastropod Stramonita haemastoma. In this study we report compelling evidence on the expression of a constitutive Ca(2+) /CaM-dependent neuronal NOS in the central and peripheral nervous system. The prevailing neuronal localization of NADPHd activity was demonstrated by NADPHd histochemistry in both central and peripheral nervous system structures. L-arginine/citrulline assays suggested that Stramonita NOS is a constitutive enzyme which is both cytosolic and membrane-bound. Molecular cloning of the full-length Stramonita NOS (Sh-NOS) by reverse-transcription polymerase chain reaction (RT-PCR) followed by 5' and 3' RACE showed that Sh-NOS is a protein of 1,517 amino acids, containing a PDZ domain at the N-terminus and sharing similar regulatory domains to the mammalian neuronal NOS (nNOS). Regional expression of the Sh-NOS gene was evaluated by RT-PCR. This analysis showed different expression levels in the nerve ring, the osphradium, the cephalic tentacles, the buccal tissues, and the foot, whereas NOS expression was not found in the salivary glands and the gland of Leiblein. The present data provide a solid background for further studies addressing the specific functions of NO in neogastropods.

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“…Cayre et al (2005) first showed that NOS mRNA is expressed in the cell bodies of the large Kenyon cells in A. domesticus. Later, Takahashi et al (2009) showed that silencing of NOS expression by systemic RNAi impairs long-term memory formation in the cricket G. bimaculatus. Using NADPH diaphorase staining and anti-citrulline immunoreactivity, Cayre et al (2005) demonstrated that NOS was highly expressed in the calyx zona externa as well as in the large cells over the posterior calyx.…”

Section: Discussionmentioning

confidence: 99%

Nitric oxide/cGMP/PKG signaling pathway activated by M₁-type muscarinic acetylcholine receptor cascade inhibits Na⁺-activated K⁺currents in Kenyon cells

Hasebe

Yamada

2016

Journal of Neurophysiology

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activity in Kenyon cells of crickets (Gryllus bimaculatus). We found that two different NO donors, S-nitrosoglutathione (GSNO) and S-nitroso-N-acetyl-DL-penicillamine(SNAP), strongly suppressed K Na channel currents. Additionally, this inhibitory effect of GSNO on K Na channel activity was diminished by 1H-[1,2,4]oxadiazolo[4,3-a]quinoxalin-1-one (ODQ), an inhibitor of soluble guanylate cyclase (sGC), and KT5823, an inhibitor of protein kinase G (PKG). Next, we analyzed the role of ACh in the NO signaling cascade. ACh strongly suppressed K Na channel currents, similar to NO donors. Furthermore, this inhibitory effect of ACh was blocked by pirenzepine, an M 1 muscarinic ACh receptor antagonist, but not by 1,1-dimethyl-4-diphenylacetoxypiperidinium iodide (4-DAMP) and mecamylamine, an M 3 muscarinic ACh receptor antagonist and a nicotinic ACh receptor antagonist, respectively. The ACh-induced inhibition of K Na channel currents was also diminished by the PLC inhibitor U73122 and the calmodulin antagonist W-7. Finally, we found that ACh inhibition was blocked by the nitric oxide synthase (NOS) inhibitor N G -nitro-L-arginine methyl ester (L-NAME). These results suggested that the ACh signaling cascade promotes NO production by activating NOS and NO inhibits K Na channel currents via the sGC/cGMP/PKG signaling cascade in Kenyon cells.

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Systemic RNA interference for the study of learning and memory in an insect

Cited by 45 publications

References 48 publications

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

Cellular, biochemical, and molecular characterization of nitric oxide synthase expressed in the nervous system of the prosobranch Stramonita haemastoma (Gastropoda, Neogastropoda)

Nitric oxide/cGMP/PKG signaling pathway activated by M₁-type muscarinic acetylcholine receptor cascade inhibits Na⁺-activated K⁺currents in Kenyon cells

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Systemic RNA interference for the study of learning and memory in an insect

Cited by 45 publications

References 48 publications

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

Roles of Calcium/Calmodulin-Dependent Kinase II in Long-Term Memory Formation in Crickets

Cellular, biochemical, and molecular characterization of nitric oxide synthase expressed in the nervous system of the prosobranch Stramonita haemastoma (Gastropoda, Neogastropoda)

Nitric oxide/cGMP/PKG signaling pathway activated by M1-type muscarinic acetylcholine receptor cascade inhibits Na+-activated K+currents in Kenyon cells

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Nitric oxide/cGMP/PKG signaling pathway activated by M₁-type muscarinic acetylcholine receptor cascade inhibits Na⁺-activated K⁺currents in Kenyon cells