Effects of the mono- and tetrasialogangliosides GM1 and GQ1b on ATP-induced long-term potentiation in hippocampal CA1 neurons

Fujii, Satoshi; Igarashi, Kotaro; Sasaki, Hiroshi; Furuse, Hidekazu; Ito, Kenichi; Kaneko, Kenya; Katô, Hiroshi; Inokuchi, Jin-ichi; Waki, Hatsue; Ando, Susumu

doi:10.1093/glycob/12.5.339

Cited by 42 publications

(25 citation statements)

References 26 publications

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“…Since activation of CaMKII due to Ca 2+ influx through NMDA receptors is involved in the mechanism of LTP in hippocampal CA1 neurons, but not in the mechanism of LTD, it is possible that inhibition of de novo synthesis of b-pathway gangliosides in d-PDMP-treated mice decreases CaMKII activity and attenuates LTP induction in hippocampal neurons, but does not affect LTD formation. Jung et al (16) reported that GQ1b-treated rats show a marked increase in memory performance in the Y maze test and Morris water maze test (23), suggesting a positive effect of GQ1b on LTP induction in hippocampal CA1 neurons (9,12). In the present study, the d-PDMP-treated mice exhibited both impairment of LTP induction in hippocampal CA1 neurons (Fig.…”

Section: Referencessupporting

confidence: 62%

“…A possible explanation for the different effects of gangliosides on LTP induction and LTD formation might be that b-pathway gangliosides are more effective than a-pathway gangliosides in activating CaMKII in hippocampal neurons (11). In our previous studies, we suggested that it was possible that ganglioside-Ca 2+ complexes may facilitate Ca 2+ influx through NMDA receptors by acting as Ca 2+ donors (9,12). Other studies have suggested the possibility that gangliosides GD1b and GT1b activate CaMKII in hippocampal neurons (7,11).…”

Section: Referencesmentioning

confidence: 85%

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Impairment of hippocampal long-term potentiation and failure of learning in mice treated with d-threo-1-phenyl-2-decanoylamino-3-morpholino-1-propanol

et al. 2012

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Gangliosides (sialic acid-containing glycosphingolipids) play important roles in many physiological functions, including synaptic plasticity in the hippocampus, which has been suggested as the basal cellular process of learning and memory in the brain. In the present study, long-term potentiation (LTP) and long-term depression (LTD) in CA1 hippocampal neurons and learning behavior were examined in mice treated with d-threo-1-phenyl-2-decanoylamino-3-morpholino-1-propanol (d-PDMP), an inhibitor of ganglioside biosynthesis. Mice treated with d-PDMP, but not those treated with l-PDMP, showed impairment of LTP induction in hippocampal CA1 neurons without any significant change in LTD formation and also showed a failure of learning in the 4-pellet taking test. These results indicate that de novo synthesis of gangliosides in the brain is involved in synaptic plasticity of LTP in mouse hippocampal CA1 neurons and plays important roles in learning and memory.In rodent CA1 hippocampal neurons, long-term potentiation (LTP) and long-term depression (LTD) are two types of synaptic plasticity, considered to be the cellular basis of learning and memory in the brain (6,21). LTP is a state of persistent synaptic enhancement induced by a brief period of high frequency electrical stimulation (HFS) of afferents (4, 5), while LTD is another activity-dependent synaptic phenomenon in which low-frequency afferent stimulation (LFS) depresses a synaptic response in a naive pathway (8,19). Gangliosides (sialic acid-containing glycosphingolipids) are abundant in the plasma membrane, especially in the termini and synapses of neural tissue (1). Ganglioside biosynthesis occurs by sequential glycosylation reactions via two major pathways designated the "a-pathway" (GM2, GM1a, and GD1a) and "b-pathway" (GD3, GD2, GD1b, GT1b, and GQ1b), with a common precursor, GM3. The analogous steps in the two pathways are catalyzed by the same glycosyltransferases (13,17). We previously studied the effects of GM1 and GQ1b on induction of LTP in CA1 neurons in rat hippocampal slices and showed that LTP is enhanced by bath application of either ganglioside, with GQ1b having a significantly greater effect than GM1 (12). In our recent study (14), we investigated LTP and LTD in the field excitatory post-synaptic potential (EPSP) in CA1 hippocampal neurons and learning behavior in β1,4-N-acetylgalactosaminyltransferase (β1,4 GalNAc-T; GM2/GD2 synthase) gene transgenic (TG) mice (10), which showed a significant decrease in levels of b-pathway gangliosides (GQ1b, GT1b, and GD1b) and a significant increase in lev-

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Section: Referencessupporting

confidence: 62%

Section: Referencesmentioning

confidence: 85%

Impairment of hippocampal long-term potentiation and failure of learning in mice treated with d-threo-1-phenyl-2-decanoylamino-3-morpholino-1-propanol

et al. 2012

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“…At Schaffer collateral-CA1 synapses, the tetra-sialoganglioside GQ1b increased the magnitude of LTP much more than did the mono-sialoganglioside GM1 [4, 33–35]. Removal of PSA with endo-N, an endosialidase that specifically cleaves α2,8-linked sialic acid, causes impairment of long-term depression as well as LTP.…”

Section: Discussionmentioning

confidence: 99%

“…Many neural functions including memory processing depend on sialic acid in glycoproteins and gangliosides [1–3]. Sialic acid contained in gangliosides such as the tetra-sialoganglioside GQ1b is crucial for synaptic plasticity and hippocampal memory [4, 5]. The sialic acid polymer (poly sialic acid, PSA), having a large negative charge, attached to neural cell adhesion molecules (NCAM) regulates neural circuit formation in memory and brain development [6, 7].…”

Section: Introductionmentioning

confidence: 99%

Role of Sialidase in Long-Term Potentiation at Mossy Fiber-CA3 Synapses and Hippocampus-Dependent Spatial Memory

et al. 2016

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Sialic acid bound to glycans in glycolipids and glycoproteins is essential for synaptic plasticity and memory. Sialidase (EC 3.2.1.18), which has 4 isozymes including Neu1, Neu2, Neu3 and Neu4, regulates the sialylation level of glycans by removing sialic acid from sialylglycoconjugate. In the present study, we investigated the distribution of sialidase activity in rat hippocampus and the role of sialidase in hippocampal memory processing. We previously developed a highly sensitive histochemical imaging probe for sialidase activity, BTP3-Neu5Ac. BTP3-Neu5Ac was cleaved efficiently by rat Neu2 and Neu4 at pH 7.3 and by Neu1 and Neu3 at pH 4.6. When a rat hippocampal acute slice was stained with BTP3-Neu5Ac at pH 7.3, mossy fiber terminal fields showed relatively intense sialidase activity. Thus, the role of sialidase in the synaptic plasticity was investigated at mossy fiber terminal fields. The long-term potentiation (LTP) at mossy fiber-CA3 pyramidal cell synapses was impaired by 2,3-dehydro-2-deoxy-N-acetylneuraminic acid (DANA), a sialidase inhibitor. DANA also failed to decrease paired-pulse facilitation after LTP induction. We also investigated the role of sialidase in hippocampus-dependent spatial memory by using the Morris water maze. The escape latency time to reach the platform was prolonged by DANA injection into the hippocampal CA3 region or by knockdown of Neu4 without affecting motility. The results show that the regulation of sialyl signaling by Neu4 is involved in hippocampal memory processing.

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“…Ganglioside treatments increased the magnitude of LTP. This increment of LTP was much greater in the case of tetrasialoganglioside GQ1b treatment than in the case of monosialoganglioside GM1 treatment (55)(56)(57)(58). Injection of GQ1b into the rat lateral ventricle improves spatial learning and memory as estimated by the Y-maze and the Morris water maze tests (59).…”

Section: D-4 Role Of Sialidase In Learning and Memorymentioning

confidence: 90%

Distribution of Sialidase Activity and the Role of Sialidase in the Brain

Minami¹,

Suzuki²

2012

TIGG

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Sialic acid is an acidic monosaccaride and plays crucial roles in various membrane functions in mammalian central nervous systems. Sialidase removes sialic acid from sialoglycoconjugates and also plays crucial roles in many neural functions, including differentiation and maturation of neurons and learning and memory. Recently, we visualized extracellular sialidase activity on the membrane surface in the rat brain by using a highly sensitive fluorescent histochemical method. Myelin-abundant regions showed intense fluorescence in the rat brain. Although the hippocampus showed weak fluorescence in the brain, mossy fiber terminals in the hippocampus showed relatively intense fluorescence. In this review, we describe the distribution of sialidase activity in the brain and discuss the role of sialidase in myelin and the hippocampus. A. Introduction S i a l i d a s e r e m o v e s s i a l i c a c i d r e s i d u e s f r o m sialoglycoconjugates, such as glycoproteins and glycolipids.Four types of mammalian sialidase (Neu1, Neu2, Neu3 and Neu4) have been identified in mammalian tissues by their localization and enzymatic properties. These four types of sialidase were reported to be expressed in mammalian brains (1). Since sialidase extracellularly applied to the rat hippocampus influences many neural functions including memory, synaptic plasticity, axon outgrowth and neural differentiation, activities of endogenous sialidases on the extracellular membrane surface would also affect neural functions (2-5). Neu1, Neu2 and Neu3 show enzyme activity on the extracellular membrane surface. Neu1 specifically acts on low-molecular-weight substrates, including 4MU-Neu5Ac, oligosaccharides and glycopeptides (6,7). Neu1 is mainly located at lysosomes. Neu1 is relocalized from the lysosome to the cell surface with activation of T cells and differentiation of monocytes (8,9). Neu2 hydrolyzes gangliosides and glycoproteins at neutral pH. Neu2 is located mainly in the cytoplasm but also in plasma membranes in the mouse

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Effects of the mono- and tetrasialogangliosides GM1 and GQ1b on ATP-induced long-term potentiation in hippocampal CA1 neurons

Cited by 42 publications

References 26 publications

Impairment of hippocampal long-term potentiation and failure of learning in mice treated with d-threo-1-phenyl-2-decanoylamino-3-morpholino-1-propanol

Impairment of hippocampal long-term potentiation and failure of learning in mice treated with d-threo-1-phenyl-2-decanoylamino-3-morpholino-1-propanol

Role of Sialidase in Long-Term Potentiation at Mossy Fiber-CA3 Synapses and Hippocampus-Dependent Spatial Memory

Distribution of Sialidase Activity and the Role of Sialidase in the Brain

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