Surface Properties of Synaptosomes in the Presence of L-Glutamic and Kainic Acids: In Vitro Alteration of the ATPase and Acetylcholinesterase Activities.

Virjinia Doltchinkova,Nevena Mouleshkova,Victoria Vitkova

doi:10.3390/membranes11120987

Virjinia Doltchinkova, Nevena Mouleshkova + Show 1 more

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https://doi.org/10.3390/membranes11120987

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Abstract

Morphologically and functionally identical to brain synapses, the nerve ending particles synaptosomes are biochemically derived membrane structures responsible for the transmission of neural information. Their surface and mechanical properties, measured in vitro, provide useful information about the functional activity of synapses in the brain in vivo. Glutamate and kainic acid are of particular interest because of their role in brain pathology (including causing seizure, migraine, ischemic stroke, aneurysmal subarachnoid hemorrhage, intracerebral hematoma, traumatic brain injury and stroke). The effects of the excitatory neurotransmitter L-glutamic acid and its agonist kainic acid are tested on Na+, K+-ATPase and Mg2+-ATPase activities in synaptic membranes prepared from the cerebral cortex of rat brain tissue. The surface parameters of synaptosome preparations from the cerebral cortex in the presence of L-glutamic and kainic acids are studied by microelectrophoresis for the first time. The studied neurotransmitters promote a significant increase in the electrophoretic mobility and surface electrical charge of synaptosomes at 1–4 h after isolation. The measured decrease in the bending modulus of model bimolecular membranes composed of monounsaturated lipid 1-palmitoyl-2-oleoyl-sn-glycero-3-phosphocholine provides evidence for softer membranes in the presence of L-glutamate. Kainic acid does not affect membrane mechanical stability even at ten-fold higher concentrations. Both the L-glutamic and kainic acids reduce acetylcholinesterase activity and deviation from the normal functions of neurotransmission in synapses is presumed. The presented results regarding the modulation of the enzyme activity of synaptic membranes and surface properties of synaptosomes are expected by biochemical and biophysical studies to contribute to the elucidation of the molecular mechanisms of neurotransmitters/agonists’ action on membranes.

Highlights

The surface electrical charge and mechanical properties of synaptosomes predetermine their functional activity, altering the synapse physiological activity in the presence of neurotransmitters such as L-glutamic (L-Glu) or its agonists, kainic acids (KA)
The results from microelectrophoretic studies obtained on isolated synaptosomes from the cerebral cortex during in vitro aging consider circumstances that occur in the compartment in synapses in vivo
An increase in the surface electrical charge of synaptosomes treated with L-Glu or KA during in vitro aging is reported, which is related to the specific balance of their impact on processes affecting surface properties of synaptosomes

Summary

Introduction

The surface electrical charge and mechanical properties of synaptosomes predetermine their functional activity, altering the synapse physiological activity in the presence of neurotransmitters such as L-glutamic (L-Glu) or its agonists, kainic acids (KA). The synapse provides information communication between neurons, as well as between them and effector organs. It is the platform hosting the application sites of the action of drugs, and endogenous and exogenous factors [1,2]. The significance of elucidation of the role of exogenously added glutamate and kainic acid uptake in the surrounding medium of synaptic and of synaptosomal membranes presents a new biophysical event, underlying numerous pathologies, including pathological conditions such as seizure, migraine, traumatic brain injury and stroke [5,6] The enzymatic activities, and electrokinetic and mechanical properties of synaptosomes (“nerve-ending particles”, “nerve terminals”) are intimately related to the central nervous system (CNS) function.

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