Mg2+ Block of Drosophila NMDA Receptors Is Required for Long-Term Memory Formation and CREB-Dependent Gene Expression

Miyashita, Tomoyuki; Oda, Y.; Horiuchi, Junjiro; Yin, Jingyi; Morimoto, Takako; Saitoe, Minoru

doi:10.1016/j.neuron.2012.03.039

Cited by 96 publications

(102 citation statements)

References 54 publications

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“…The role of NMDARs in learning and memory processes was also demonstrated in several other invertebrates (Müssig et al 2010;Amano and Maruyama 2011;Miyashita et al 2012;Hepp et al 2013). In our laboratory, research performed in the crab Neohelice granulata (formerly Chasmagnathus granulatus) using context associative learning (context signal memory, CSM) has indicated that NMDA-like receptors are involved in consolidation and reconsolidation (Pedreira et al 2002;Troncoso and Maldonado 2002).…”

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confidence: 82%

Surface expression of NMDA receptor changes during memory consolidation in the crabNeohelice granulata

et al. 2016

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The aim of the present study was to analyze the surface expression of the NMDA-like receptors during the consolidation of contextual learning in the crab Neohelice granulata. Memory storage is based on alterations in the strength of synaptic connections between neurons. The glutamatergic synapses undergo various forms of N-methyl-D aspartate receptor (NMDAR)-dependent changes in strength, a process that affects the abundance of other receptors at the synapse and underlies some forms of learning and memory. Here we propose a direct regulation of the NMDAR. Changes in NMDAR's functionality might be induced by the modification of the subunit's expression or cellular trafficking. This trafficking does not only include NMDAR's movement between synaptic and extra-synaptic localizations but also the cycling between intracellular compartments and the plasma membrane, a process called surface expression. Consolidation of contextual learning affects the surface expression of the receptor without affecting its general expression. The surface expression of the GluN1 subunit of the NMDAR is down-regulated immediately after training, up-regulated 3 h after training and returns to naïve and control levels 24 h after training. The changes in NMDAR surface expression observed in the central brain are not seen in the thoracic ganglion. A similar increment in surface expression of GluN1 in the central brain is observed 3 h after administration of the competitive GABA A receptor antagonist, bicuculline. These consolidation changes are part of a plasticity event that first, during the down-regulation, stabilizes the trace and later, at 3-h post-training, changes the threshold for synapse activation.

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confidence: 82%

Surface expression of NMDA receptor changes during memory consolidation in the crabNeohelice granulata

et al. 2016

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“…The amount of CG9134 transcript was normalized to that of a housekeeping gene, Glyceraldehyde 3 phosphate dehydrogenase 1 (Gapdh1) (Miyashita et al 2012). The primers used to amplify CG9134 were 59-GGA GAGTGACTGCGATTGGTTTG-39 and 59-TGTTGCTGCTTT TCGGTCCTG-39.…”

Section: Real-time Pcrmentioning

confidence: 99%

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development inDrosophila

et al. 2015

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The class I myosin genes are conserved in diverse organisms, and their gene products are involved in actin dynamics, endocytosis, and signal transduction. Drosophila melanogaster has three class I myosin genes, Myosin 31DF (Myo31DF), Myosin 61F (Myo61F), and Myosin 95E (Myo95E). Myo31DF, Myo61F, and Myo95E belong to the Myosin ID, Myosin IC, and Myosin IB families, respectively. Previous loss-of-function analyses of Myo31DF and Myo61F revealed important roles in left-right (LR) asymmetric development and enterocyte maintenance, respectively. However, it was difficult to elucidate their roles in vivo, because of potential redundant activities. Here we generated class I myosin double and triple mutants to address this issue. We found that the triple mutant was viable and fertile, indicating that all three class I myosins were dispensable for survival. A loss-of-function analysis revealed further that Myo31DF and Myo61F, but not Myo95E, had redundant functions in promoting the dextral LR asymmetric development of the male genitalia. Myo61F overexpression is known to antagonize the dextral activity of Myo31DF in various Drosophila organs. Thus, the LR-reversing activity of overexpressed Myo61F may not reflect its physiological function. The endogenous activity of Myo61F in promoting dextral LR asymmetric development was observed in the male genitalia, but not the embryonic gut, another LR asymmetric organ. Thus, Myo61F and Myo31DF, but not Myo95E, play tissue-specific, redundant roles in LR asymmetric development. Our studies also revealed differential colocalization of the class I myosins with filamentous (F)-actin in the brush border of intestinal enterocytes.KEYWORDS myosin I; Myosin 31DF; Myosin 61F; Myosin 95E; left-right asymmetry T HE class I myosin genes encode myosin heavy chains, which are conserved in phylogenetically diverse organisms (Sellers 2000;Krendel and Mooseker 2005). The class I myosins are nonfilamentous, actin-based motor proteins and were the first discovered unconventional myosin proteins. These myosins are involved in a variety of cellular processes, such as cell migration, cell adhesion, and cell growth, through their regulation of actin dynamics, endocytosis, and signal transduction (Osherov and May 2000;Krendel and Mooseker 2005;Kim and Flavell 2008;McConnell and Tyska 2010).The structure of the myosin I heavy chains is evolutionarily conserved and composed of head (or motor), neck, and tail domains ( Figure 1A) (Coluccio 1997;Barylko et al. 2000). The head domain binds to filamentous (F)-actin and adenosine triphosphate (ATP), a common feature of myosin proteins ( Figure 1A) (Mermall et al. 1998); the neck domain possesses one or more IQ motifs, which directly interact with calmodulin or calmodulin-related myosin light chains (Coluccio 1997;Barylko et al. 2000), and the tail domains are divided into short and long types. Short tails contain a single tail homology 1 (TH1) domain, which is rich in basic residues and thought to interact with plasma membranes (Coluccio 1997;Barylko...

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“…As a possible molecular mechanism underlying the memory, the cAMP response element binding protein (Ci-CREB) is important for memory formation in the larval neurons of some animals (Chen et al, 2010;Imai et al, 2004;Kandel, 2004;Miyashita et al, 2012;Yamada et al, 2003). Nitric oxide synthase expressed in the central nervous system (CNS) is another candidate, as it is involved in synaptic potentiation to form memory in mice (Comes et al, 2007;Lange et al, 2012).…”

Section: Larvae Can Remember the Experience Of Adhesionmentioning

confidence: 99%

Time course for tail regression during metamorphosis of the ascidian Ciona intestinalis

Matsunobu

Sasakura

2015

Developmental Biology

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In most ascidians, the tadpole-like swimming larvae dramatically change their body-plans during metamorphosis and develop into sessile adults. The mechanisms of ascidian metamorphosis have been researched and debated for many years. Until now information on the detailed time course of the initiation and completion of each metamorphic event has not been described. One dramatic and important event in ascidian metamorphosis is tail regression, in which ascidian larvae lose their tails to adjust themselves to sessile life. In the present study, we measured the time associated with tail regression in the ascidian Ciona intestinalis. Larvae are thought to acquire competency for each metamorphic event in certain developmental periods. We show that the timing with which the competence for tail regression is acquired is determined by the time since hatching, and this timing is not affected by the timing of post-hatching events such as adhesion. Because larvae need to adhere to substrates with their papillae to induce tail regression, we measured the duration for which larvae need to remain adhered in order to initiate tail regression and the time needed for the tail to regress. Larvae acquire the ability to adhere to substrates before they acquire tail regression competence. We found that when larvae adhered before they acquired tail regression competence, they were able to remember the experience of adhesion until they acquired the ability to undergo tail regression. The time course of the events associated with tail regression provides a valuable reference, upon which the cellular and molecular mechanisms of ascidian metamorphosis can be elucidated.

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Mg2+ Block of Drosophila NMDA Receptors Is Required for Long-Term Memory Formation and CREB-Dependent Gene Expression

Cited by 96 publications

References 54 publications

Surface expression of NMDA receptor changes during memory consolidation in the crabNeohelice granulata

Surface expression of NMDA receptor changes during memory consolidation in the crabNeohelice granulata

Class I Myosins Have Overlapping and Specialized Functions in Left-Right Asymmetric Development inDrosophila

Time course for tail regression during metamorphosis of the ascidian Ciona intestinalis

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