Are There Lipid Membrane-Domain Subtypes in Neurons with Different Roles in Calcium Signaling?
Abstract
:1. Lipid Membrane Nanodomains Organization in the Neuronal Plasma Membrane
2. Properties of Caveolin-, Flotillin- or Ganglioside-Containing Lipid Membrane Domains
2.1. Caveolin-Enriched Lipid Membrane Domains in Neurons
2.2. Histological and Cytological Distribution of Caveolin-Enriched Lipid Membrane Domains in Neurons and Their Function in Calcium Signaling
2.3. Flotillin and Neuronal Lipid Membrane Domains
2.4. Histological Cytological Distribution of Flotillin-Enriched Lipid Membrane Domains in Neurons and Function Calcium Signaling
2.5. Gangliosides as a Lipid Membrane-Domain Biomarkers for Some Caveolin- and Flotillin-Enriched Lipid Membrane Domains
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- Type 1 GBD, or GBD-1, comprises any membrane protein ganglioside-binding domain able to form a stoichiometric (1:1, mol:mol) complex with a single ganglioside molecule [247]. GBD-1 is generally present at the flexible juxta membrane region interacting with transmembrane glycoproteins [113]. The serotonin 5-HT1A receptor, the tumor stem cell marker CD133 are candidates the EGF and PDGF receptors and ion transporters [247]. These membrane proteins are expected to reside at the edge of a lipid raft.
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- Type 2 GBD, or GBD-2 are represented by protein dimeric structures resembling a flower chalice or the open wings of a butterfly [250,251]. The typical protein insertion processes have been associated with these domains in which proteins with a hairpin loop interact with the ganglioside, leading to a conformational change that implicates a deep interaction with the ganglioside [251]. This type of ganglioside-dependent insertion process accounts at the edge of a lipid raft or at the periphery since they need to have sufficient conformational flexibility to accommodate the loop [251]. Chalice-shaped ganglioside dimers are required for HIV fusion with host cell membranes [247,252] and the formation of oligomeric calcium permeable amyloid pores [247,253].
2.6. Histological Cytological Distribution of Gangliosides-Enriched Lipid Membrane Domains in Neurons and Function Calcium Signaling
3. The Summary of the Distribution Map
4. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
Abbreviations
References
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Type | Subunit | Neuronal Type | Associated with Raft Component | Main Distribution in Brain and Subcellular Location | Function |
---|---|---|---|---|---|
L-type | Cav1.2 | Primary culture of cerebellar granule neurons and Purkinje cells [30,279] | Cav-1 and GM1 [30], GM1 [279] | Neuronal calcium transients in cell bodies and dendrites, regulation of enzyme activity, regulation of transcription [125] | |
P/Q-type | Cav2.1 | Cerebellar Purkinje neurons (tissue [175]; primary culture [284]; brain synaptosomal fraction [225]) | Flot-1 [175], GM1 [225,284] | Hippocampus [285], dorsal root ganglion neurons [286], presynaptic areas [225,286] | Neurotransmitter release, dendritic calcium transients [125] |
L/P/Q/N-type | α2δ-2, α2δ-3 [226] | Hippocampal neurons (raft isolation and microscopy) [226] | Flot-1 [226] | GPI-enriched areas [226] | |
NMDA | NR1 | Primary cultures of hippocampal neurons [206]; ganglion cells in rat retina (tissue) [287,288]; ventral part of lamina III and in laminae III and IV [289] | Flot-1 [206]; GM1 [287,288,289] | Small uniform puncta throughout the neuron, pre and postsynapse [206,289]; ganglion cell dendrites [287], extrasynaptic plasma membrane [288] | Signaling complexes in the postsynaptic density [290], glutamatergic signaling, synaptic plasticity, excitotoxicity, and memory [132], neurite outgrowth and axonal growth cone motility [291,292] |
NR2B | Anterior cingulate cortex neurons in tissue and cultured (microscopy and immunoprecipitation) [126]; neurons from normal rat cerebral cortex (raft isolation, microscopy and immunoprecipitation) [127]; primary culture of cortical neurons (microscopy and raft isolation) [132]; ganglion cells in rat retina (tissue) [287,288] | Cav-1 [126,127], Flot-1 [127]; GM1 [287,288] | Soma and postsynapses [126,127]; ganglion cell dendrites extrasynapses peri-synapses [287,288] | ||
NR2A [227] | Cultured hippocampal neurons (microscopy and raft isolation) [227] | Flot-1 and -2 [227] | Small uniform puncta throughout the neuron [227] | ||
AMPAR | GluA2 [130] | Primary culture of hippocampal neurons (microscopy, immunoprecipitation and raft preparation) [130] | Cav-1 [130], | Cell body and as puncta localized to areas of cellular outgrowth [130] | Postsynaptic currents mediated by the AMPA subtype of glutamate receptors in LTP [293]; long-term potentiation (LTP) induced GluA1 surface exposure [294] |
GluA1 [156,234] | Primary culture of hippocampal neurons (microscopy and raft isolation) [156,234] | Flot-1 and -2 [234], Cav-1 [129], GM1 [156] | Postsynapses [156], synapses and dendritic Spines [129] | ||
GluR2/3 [129] | Primary culture of hippocampal neurons (microscopy) [129], synaptosomes [271]; ganglion cells in rat retina (tissue) [287] | Cav-1 [129], GM1 [271,287] | Synapses and dendritic spines [129]; dendrites and somata [287] | ||
GluR4 | Ganglion cells in rat retina (tissue) [287] | GM1 [287] | Dendrites and somata [287] | ||
mGluR | mGluR1/5 | Primary hippocampal neurons (microscopy and immunoprecipitation) [128] | Cav-1 [128] | Soma and dendrites [128]; postsynaptic density late in development [295] | Synapse formation and plasticity [159] |
mGluR1a | Hippocampus, arcuate nucleus, hypothalamus [167] | Cav-1 [167] | Caveolin proteins act to functionally isolate distinct estrogen receptors and mGluRs, leading to activation of specific second messenger signaling cascades [167] | ||
mGluR1α | Synaptosomes from pig cerebellum | Cav-1 and Flot [173,248] | By application of MβCD, interaction of phosphorylated caveolin with the receptor decreased, and finally, internalization of the receptor was blocked [173] | ||
Pumps | PMCA isoform 4 | Synaptosomes from pig cerebellum (Brij96 extracts) [181] | ganglioside GM1 [181] | Discrete functional positions on the synaptic nerve terminals [181] | |
Purinergic receptors | P2X3 | Rat brain, cerebellar granule neurons in culture (microscopy, immunoprecipitation and raft preparation), dorsal root ganglion neurons in culture | Flot-2, Cav-1 | P2X3 subunit is expressed in cell bodies as well as in peripheral and central terminals of sensory neurons in dorsal root ganglia (DRG) [296,297] | Well-defined role in pain perception [298,299]. Cav-1 is required for basal and ligand-induced membrane delivery of the P2X3 receptor [187] |
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Samhan-Arias, A.K.; Poejo, J.; Marques-da-Silva, D.; Martínez-Costa, O.H.; Gutierrez-Merino, C. Are There Lipid Membrane-Domain Subtypes in Neurons with Different Roles in Calcium Signaling? Molecules 2023, 28, 7909. https://doi.org/10.3390/molecules28237909
Samhan-Arias AK, Poejo J, Marques-da-Silva D, Martínez-Costa OH, Gutierrez-Merino C. Are There Lipid Membrane-Domain Subtypes in Neurons with Different Roles in Calcium Signaling? Molecules. 2023; 28(23):7909. https://doi.org/10.3390/molecules28237909
Chicago/Turabian StyleSamhan-Arias, Alejandro K., Joana Poejo, Dorinda Marques-da-Silva, Oscar H. Martínez-Costa, and Carlos Gutierrez-Merino. 2023. "Are There Lipid Membrane-Domain Subtypes in Neurons with Different Roles in Calcium Signaling?" Molecules 28, no. 23: 7909. https://doi.org/10.3390/molecules28237909