Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation

Strategies to increase the proportion of neural stem cells that differentiate into neurons are vital for therapy of neurodegenerative disorders. In vitro, the extracellular matrix composition and topography have been found to be important factors in stem cell differentiation. We have developed a nov...

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Main Authors: Seunghyun Jung, Nathaniel Harris, Isabelle I. Niyonshuti, Samir V. Jenkins, Abdallah M. Hayar, Fumiya Watanabe, Azemat Jamshidi-Parsian, Jingyi Chen, Michael J. Borrelli, Robert J. Griffin
Format: Article
Language:English
Published: MDPI AG 2021-05-01
Series:Nanomaterials
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Online Access:https://www.mdpi.com/2079-4991/11/5/1216
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author Seunghyun Jung
Nathaniel Harris
Isabelle I. Niyonshuti
Samir V. Jenkins
Abdallah M. Hayar
Fumiya Watanabe
Azemat Jamshidi-Parsian
Jingyi Chen
Michael J. Borrelli
Robert J. Griffin
author_facet Seunghyun Jung
Nathaniel Harris
Isabelle I. Niyonshuti
Samir V. Jenkins
Abdallah M. Hayar
Fumiya Watanabe
Azemat Jamshidi-Parsian
Jingyi Chen
Michael J. Borrelli
Robert J. Griffin
author_sort Seunghyun Jung
collection DOAJ
description Strategies to increase the proportion of neural stem cells that differentiate into neurons are vital for therapy of neurodegenerative disorders. In vitro, the extracellular matrix composition and topography have been found to be important factors in stem cell differentiation. We have developed a novel artificial extracellular matrix (aECM) formed by attaching gold nanocages (AuNCs) to glass coverslips. After culturing rat neural stem cells (rNSCs) on these gold nanocage-coated surfaces (AuNC-aECMs), we observed that 44.6% of rNSCs differentiated into neurons compared to only 27.9% for cells grown on laminin-coated glass coverslips. We applied laser irradiation to the AuNC-aECMs to introduce precise amounts of photothermally induced heat shock in cells. Our results showed that laser-induced thermal stimulation of AuNC-aECMs further enhanced neuronal differentiation (56%) depending on the laser intensity used. Response to these photothermal effects increased the expression of heat shock protein 27, 70, and 90α in rNSCs. Analysis of dendritic complexity showed that this thermal stimulation promoted neuronal maturation by increasing dendrite length as thermal dose was increased. In addition, we found that cells growing on AuNC-aECMs post laser irradiation exhibited action potentials and increased the expression of voltage-gated Na+ channels compared to laminin-coated glass coverslips. These results indicate that the photothermal response induced in cells growing on AuNC-aECMs can be used to produce large quantities of functional neurons, with improved electrochemical properties, that can potentially be transplanted into a damaged central nervous system to provide replacement neurons and restore lost function.
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spelling doaj.art-9ba3124d3f3948978fd947c4e2280f612023-11-21T18:21:38ZengMDPI AGNanomaterials2079-49912021-05-01115121610.3390/nano11051216Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell DifferentiationSeunghyun Jung0Nathaniel Harris1Isabelle I. Niyonshuti2Samir V. Jenkins3Abdallah M. Hayar4Fumiya Watanabe5Azemat Jamshidi-Parsian6Jingyi Chen7Michael J. Borrelli8Robert J. Griffin9Department of Physiology and Cell Biology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USAMechanical Engineering, University of Arkansas, Fayetteville, AR 72701, USADepartment of Chemistry and Biochemistry, University of Arkansas, Fayetteville, AR 72701, USADepartment of Radiation Oncology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USADepartment of Neurobiology and Developmental Sciences, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USACenter for Integrative Nanotechnology Sciences, University of Arkansas, Little Rock, AR 72204, USADepartment of Radiation Oncology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USADepartment of Chemistry and Biochemistry, University of Arkansas, Fayetteville, AR 72701, USADepartment of Physiology and Cell Biology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USADepartment of Radiation Oncology, University of Arkansas for Medical Sciences, Little Rock, AR 72205, USAStrategies to increase the proportion of neural stem cells that differentiate into neurons are vital for therapy of neurodegenerative disorders. In vitro, the extracellular matrix composition and topography have been found to be important factors in stem cell differentiation. We have developed a novel artificial extracellular matrix (aECM) formed by attaching gold nanocages (AuNCs) to glass coverslips. After culturing rat neural stem cells (rNSCs) on these gold nanocage-coated surfaces (AuNC-aECMs), we observed that 44.6% of rNSCs differentiated into neurons compared to only 27.9% for cells grown on laminin-coated glass coverslips. We applied laser irradiation to the AuNC-aECMs to introduce precise amounts of photothermally induced heat shock in cells. Our results showed that laser-induced thermal stimulation of AuNC-aECMs further enhanced neuronal differentiation (56%) depending on the laser intensity used. Response to these photothermal effects increased the expression of heat shock protein 27, 70, and 90α in rNSCs. Analysis of dendritic complexity showed that this thermal stimulation promoted neuronal maturation by increasing dendrite length as thermal dose was increased. In addition, we found that cells growing on AuNC-aECMs post laser irradiation exhibited action potentials and increased the expression of voltage-gated Na+ channels compared to laminin-coated glass coverslips. These results indicate that the photothermal response induced in cells growing on AuNC-aECMs can be used to produce large quantities of functional neurons, with improved electrochemical properties, that can potentially be transplanted into a damaged central nervous system to provide replacement neurons and restore lost function.https://www.mdpi.com/2079-4991/11/5/1216gold nanocagesartificial extracellular matrixphotothermalneuronal differentiationneuronal maturation
spellingShingle Seunghyun Jung
Nathaniel Harris
Isabelle I. Niyonshuti
Samir V. Jenkins
Abdallah M. Hayar
Fumiya Watanabe
Azemat Jamshidi-Parsian
Jingyi Chen
Michael J. Borrelli
Robert J. Griffin
Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation
Nanomaterials
gold nanocages
artificial extracellular matrix
photothermal
neuronal differentiation
neuronal maturation
title Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation
title_full Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation
title_fullStr Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation
title_full_unstemmed Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation
title_short Photothermal Response Induced by Nanocage-Coated Artificial Extracellular Matrix Promotes Neural Stem Cell Differentiation
title_sort photothermal response induced by nanocage coated artificial extracellular matrix promotes neural stem cell differentiation
topic gold nanocages
artificial extracellular matrix
photothermal
neuronal differentiation
neuronal maturation
url https://www.mdpi.com/2079-4991/11/5/1216
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