Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons

Taurine is a sulfur-containing amino acid that is widely expressed throughout the human brain, heart, retina, and muscle tissues. Taurine deficiency is associated with cardiomyopathy, renal dysfunction, abnormalities of the developing nervous system, and epilepsy which suggests a role specific to ex...

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Main Authors: Brittany Mersman, Wali Zaidi, Naweed I. Syed, Fenglian Xu
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-07-01
Series:Frontiers in Synaptic Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fnsyn.2020.00029/full
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spelling doaj-62067479426546179510e5031420b3a72020-11-25T03:26:23ZengFrontiers Media S.A.Frontiers in Synaptic Neuroscience1663-35632020-07-011210.3389/fnsyn.2020.00029548210Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central NeuronsBrittany Mersman0Brittany Mersman1Wali Zaidi2Naweed I. Syed3Fenglian Xu4Fenglian Xu5Department of Biology, College of Arts and Sciences, Saint Louis University, St. Louis, MO, United StatesHenry and Amelia Nasrallah Center for Neuroscience, Saint Louis University, St. Louis, MO, United StatesDepartment of Cell Biology and Anatomy, Hotchkiss Brain Institute and Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, AB, CanadaDepartment of Cell Biology and Anatomy, Hotchkiss Brain Institute and Alberta Children’s Hospital Research Institute, University of Calgary, Calgary, AB, CanadaDepartment of Biology, College of Arts and Sciences, Saint Louis University, St. Louis, MO, United StatesHenry and Amelia Nasrallah Center for Neuroscience, Saint Louis University, St. Louis, MO, United StatesTaurine is a sulfur-containing amino acid that is widely expressed throughout the human brain, heart, retina, and muscle tissues. Taurine deficiency is associated with cardiomyopathy, renal dysfunction, abnormalities of the developing nervous system, and epilepsy which suggests a role specific to excitable tissues. Like vertebrates, invertebrates maintain high levels of taurine during embryonic and larval development, which decline during aging, indicating a potential developmental role. Notwithstanding its extensive presence throughout, taurine’s precise role/s during early brain development, function, and repair remains largely unknown in both vertebrate and invertebrate. Here, we investigated whether taurine affects neurite outgrowth, synapse formation, and synaptic transmission between postnatal day 0 rat cortical neurons in vitro, whereas its synaptogenic role was tested more directly using the Lymnaea soma-soma synapse model. We provide direct evidence that when applied at physiological concentrations, taurine exerts a significant neurotrophic effect on neuritic outgrowth and thickness of neurites as well as the expression of synaptic puncta as revealed by immunostaining of presynaptic synaptophysin and postsynaptic PSD95 proteins in rat cortical neurons, indicating direct involvement in synapse development. To demonstrate taurine’s direct effects on neurons in the absence of glia and other confounding factors, we next exploited individually identified pre- and postsynaptic neurons from the mollusk Lymnaea stagnalis. We found that taurine increased both the incidence of synapse formation (percent of cells that form synapses) and the efficacy of synaptic transmission between the paired neurons. This effect was comparable, but not additive, to Lymnaea trophic factor-induced synaptogenesis. This study thus provides direct morphological and functional evidence that taurine plays an important role in neurite outgrowth, synaptogenesis, and synaptic transmission during the early stages of brain development and that this role is conserved across both vertebrate and invertebrate species.https://www.frontiersin.org/article/10.3389/fnsyn.2020.00029/fulltaurineneural developmentsynapsevertebrateinvertebratemolluska
collection DOAJ
language English
format Article
sources DOAJ
author Brittany Mersman
Brittany Mersman
Wali Zaidi
Naweed I. Syed
Fenglian Xu
Fenglian Xu
spellingShingle Brittany Mersman
Brittany Mersman
Wali Zaidi
Naweed I. Syed
Fenglian Xu
Fenglian Xu
Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
Frontiers in Synaptic Neuroscience
taurine
neural development
synapse
vertebrate
invertebrate
molluska
author_facet Brittany Mersman
Brittany Mersman
Wali Zaidi
Naweed I. Syed
Fenglian Xu
Fenglian Xu
author_sort Brittany Mersman
title Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
title_short Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
title_full Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
title_fullStr Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
title_full_unstemmed Taurine Promotes Neurite Outgrowth and Synapse Development of Both Vertebrate and Invertebrate Central Neurons
title_sort taurine promotes neurite outgrowth and synapse development of both vertebrate and invertebrate central neurons
publisher Frontiers Media S.A.
series Frontiers in Synaptic Neuroscience
issn 1663-3563
publishDate 2020-07-01
description Taurine is a sulfur-containing amino acid that is widely expressed throughout the human brain, heart, retina, and muscle tissues. Taurine deficiency is associated with cardiomyopathy, renal dysfunction, abnormalities of the developing nervous system, and epilepsy which suggests a role specific to excitable tissues. Like vertebrates, invertebrates maintain high levels of taurine during embryonic and larval development, which decline during aging, indicating a potential developmental role. Notwithstanding its extensive presence throughout, taurine’s precise role/s during early brain development, function, and repair remains largely unknown in both vertebrate and invertebrate. Here, we investigated whether taurine affects neurite outgrowth, synapse formation, and synaptic transmission between postnatal day 0 rat cortical neurons in vitro, whereas its synaptogenic role was tested more directly using the Lymnaea soma-soma synapse model. We provide direct evidence that when applied at physiological concentrations, taurine exerts a significant neurotrophic effect on neuritic outgrowth and thickness of neurites as well as the expression of synaptic puncta as revealed by immunostaining of presynaptic synaptophysin and postsynaptic PSD95 proteins in rat cortical neurons, indicating direct involvement in synapse development. To demonstrate taurine’s direct effects on neurons in the absence of glia and other confounding factors, we next exploited individually identified pre- and postsynaptic neurons from the mollusk Lymnaea stagnalis. We found that taurine increased both the incidence of synapse formation (percent of cells that form synapses) and the efficacy of synaptic transmission between the paired neurons. This effect was comparable, but not additive, to Lymnaea trophic factor-induced synaptogenesis. This study thus provides direct morphological and functional evidence that taurine plays an important role in neurite outgrowth, synaptogenesis, and synaptic transmission during the early stages of brain development and that this role is conserved across both vertebrate and invertebrate species.
topic taurine
neural development
synapse
vertebrate
invertebrate
molluska
url https://www.frontiersin.org/article/10.3389/fnsyn.2020.00029/full
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