Real-time monitoring of cellular superoxide anion release in THP-1 cells using a catalytically amplified superoxide dismutase–based microbiosensor
Reactive oxygen species (ROS) including the superoxide anion (O 2 •− ) are typically studied in cell cultures using fluorescent dyes, which provide only discrete single-point measurements. These methods lack the capabilities for assessing O 2 •− kinetics and release in a quantitative manner over lon...
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| Veröffentlicht in: | Analytical and bioanalytical chemistry 2024-09, Vol.416 (21), p.4727-4737 |
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| creator | Deshpande, Aaditya S. Bechard, Tyler DeVoe, Emily Morse, Jared Khan, Reem Leung, Ka Ho Andreescu, Silvana |
| description | Reactive oxygen species (ROS) including the superoxide anion (O
2
•−
) are typically studied in cell cultures using fluorescent dyes, which provide only discrete single-point measurements. These methods lack the capabilities for assessing O
2
•−
kinetics and release in a quantitative manner over long monitoring times. Herein, we present the fabrication and application of an electrochemical biosensor that enables real-time continuous monitoring of O
2
•−
release in cell cultures for extended periods (> 8 h) using an O
2
•−
specific microelectrode. To achieve the sensitivity and selectivity requirements for cellular sensing, we developed a biohybrid system consisting of superoxide dismutase (SOD) and Ti
3
C
2
T
x
MXenes, deposited on a gold microwire electrode (AuME) as O
2
•−
specific materials with catalytic amplification through the synergistic action of the enzyme and the biomimetic MXenes-based structure. The biosensor demonstrated a sensitivity of 18.35 nA/μM with a linear range from 147 to 930 nM in a cell culture medium. To demonstrate its robustness and practicality, we applied the biosensor to monitor O
2
•−
levels in human leukemia monocytic THP-1 cells upon stimulation with lipopolysaccharide (LPS). Using this strategy, we successfully monitored LPS-induced O
2
•−
in THP-1 cells, as well as the quenching effect induced by the ROS scavenger N-acetyl-
l
-cysteine (NAC). The biosensor is generally useful for exploring the role of oxidative stress and longitudinally monitoring O
2
•−
release in cell cultures, enabling studies of biochemical processes and associated oxidative stress mechanisms in cellular and other biological environments.
Graphical Abstract |
| doi_str_mv | 10.1007/s00216-024-05437-z |
| format | Article |
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2
•−
) are typically studied in cell cultures using fluorescent dyes, which provide only discrete single-point measurements. These methods lack the capabilities for assessing O
2
•−
kinetics and release in a quantitative manner over long monitoring times. Herein, we present the fabrication and application of an electrochemical biosensor that enables real-time continuous monitoring of O
2
•−
release in cell cultures for extended periods (> 8 h) using an O
2
•−
specific microelectrode. To achieve the sensitivity and selectivity requirements for cellular sensing, we developed a biohybrid system consisting of superoxide dismutase (SOD) and Ti
3
C
2
T
x
MXenes, deposited on a gold microwire electrode (AuME) as O
2
•−
specific materials with catalytic amplification through the synergistic action of the enzyme and the biomimetic MXenes-based structure. The biosensor demonstrated a sensitivity of 18.35 nA/μM with a linear range from 147 to 930 nM in a cell culture medium. To demonstrate its robustness and practicality, we applied the biosensor to monitor O
2
•−
levels in human leukemia monocytic THP-1 cells upon stimulation with lipopolysaccharide (LPS). Using this strategy, we successfully monitored LPS-induced O
2
•−
in THP-1 cells, as well as the quenching effect induced by the ROS scavenger N-acetyl-
l
-cysteine (NAC). The biosensor is generally useful for exploring the role of oxidative stress and longitudinally monitoring O
2
•−
release in cell cultures, enabling studies of biochemical processes and associated oxidative stress mechanisms in cellular and other biological environments.
Graphical Abstract</description><identifier>ISSN: 1618-2642</identifier><identifier>ISSN: 1618-2650</identifier><identifier>EISSN: 1618-2650</identifier><identifier>DOI: 10.1007/s00216-024-05437-z</identifier><identifier>PMID: 39014219</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>Acetylcysteine ; Amplification ; Analytical Chemistry ; Anions ; Biochemistry ; Biological activity ; Biomimetic materials ; Biomimetics ; Biomonitoring ; Biosensing Techniques - methods ; Biosensors ; Cell culture ; Cellular structure ; Characterization and Evaluation of Materials ; Chemistry ; Chemistry and Materials Science ; Electrochemical Techniques - instrumentation ; Electrochemical Techniques - methods ; Electrochemistry ; Emerging Trends in Electrochemical Analysis ; Fabrication ; Fluorescent dyes ; Fluorescent indicators ; Food Science ; Humans ; Laboratory Medicine ; Leukemia ; Limit of Detection ; Lipopolysaccharides ; Lipopolysaccharides - pharmacology ; Microelectrodes ; Monitoring/Environmental Analysis ; Monocytes ; MXenes ; Oxidative stress ; Paper in Forefront ; Reactive oxygen species ; Real time ; Superoxide anions ; Superoxide dismutase ; Superoxide Dismutase - metabolism ; Superoxides - analysis ; Superoxides - metabolism ; THP-1 Cells</subject><ispartof>Analytical and bioanalytical chemistry, 2024-09, Vol.416 (21), p.4727-4737</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2024. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><rights>2024. The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c256t-3b1b93aab04b87c21ffdaf428f93cb4371207dccceb378f627d6bb28e46392533</cites><orcidid>0000-0003-3382-7939</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00216-024-05437-z$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00216-024-05437-z$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39014219$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Deshpande, Aaditya S.</creatorcontrib><creatorcontrib>Bechard, Tyler</creatorcontrib><creatorcontrib>DeVoe, Emily</creatorcontrib><creatorcontrib>Morse, Jared</creatorcontrib><creatorcontrib>Khan, Reem</creatorcontrib><creatorcontrib>Leung, Ka Ho</creatorcontrib><creatorcontrib>Andreescu, Silvana</creatorcontrib><title>Real-time monitoring of cellular superoxide anion release in THP-1 cells using a catalytically amplified superoxide dismutase–based microbiosensor</title><title>Analytical and bioanalytical chemistry</title><addtitle>Anal Bioanal Chem</addtitle><addtitle>Anal Bioanal Chem</addtitle><description>Reactive oxygen species (ROS) including the superoxide anion (O
2
•−
) are typically studied in cell cultures using fluorescent dyes, which provide only discrete single-point measurements. These methods lack the capabilities for assessing O
2
•−
kinetics and release in a quantitative manner over long monitoring times. Herein, we present the fabrication and application of an electrochemical biosensor that enables real-time continuous monitoring of O
2
•−
release in cell cultures for extended periods (> 8 h) using an O
2
•−
specific microelectrode. To achieve the sensitivity and selectivity requirements for cellular sensing, we developed a biohybrid system consisting of superoxide dismutase (SOD) and Ti
3
C
2
T
x
MXenes, deposited on a gold microwire electrode (AuME) as O
2
•−
specific materials with catalytic amplification through the synergistic action of the enzyme and the biomimetic MXenes-based structure. The biosensor demonstrated a sensitivity of 18.35 nA/μM with a linear range from 147 to 930 nM in a cell culture medium. To demonstrate its robustness and practicality, we applied the biosensor to monitor O
2
•−
levels in human leukemia monocytic THP-1 cells upon stimulation with lipopolysaccharide (LPS). Using this strategy, we successfully monitored LPS-induced O
2
•−
in THP-1 cells, as well as the quenching effect induced by the ROS scavenger N-acetyl-
l
-cysteine (NAC). The biosensor is generally useful for exploring the role of oxidative stress and longitudinally monitoring O
2
•−
release in cell cultures, enabling studies of biochemical processes and associated oxidative stress mechanisms in cellular and other biological environments.
Graphical Abstract</description><subject>Acetylcysteine</subject><subject>Amplification</subject><subject>Analytical Chemistry</subject><subject>Anions</subject><subject>Biochemistry</subject><subject>Biological activity</subject><subject>Biomimetic materials</subject><subject>Biomimetics</subject><subject>Biomonitoring</subject><subject>Biosensing Techniques - methods</subject><subject>Biosensors</subject><subject>Cell culture</subject><subject>Cellular structure</subject><subject>Characterization and Evaluation of Materials</subject><subject>Chemistry</subject><subject>Chemistry and Materials Science</subject><subject>Electrochemical Techniques - instrumentation</subject><subject>Electrochemical Techniques - methods</subject><subject>Electrochemistry</subject><subject>Emerging Trends in Electrochemical Analysis</subject><subject>Fabrication</subject><subject>Fluorescent dyes</subject><subject>Fluorescent indicators</subject><subject>Food Science</subject><subject>Humans</subject><subject>Laboratory Medicine</subject><subject>Leukemia</subject><subject>Limit of Detection</subject><subject>Lipopolysaccharides</subject><subject>Lipopolysaccharides - pharmacology</subject><subject>Microelectrodes</subject><subject>Monitoring/Environmental Analysis</subject><subject>Monocytes</subject><subject>MXenes</subject><subject>Oxidative stress</subject><subject>Paper in Forefront</subject><subject>Reactive oxygen species</subject><subject>Real time</subject><subject>Superoxide anions</subject><subject>Superoxide dismutase</subject><subject>Superoxide Dismutase - metabolism</subject><subject>Superoxides - analysis</subject><subject>Superoxides - metabolism</subject><subject>THP-1 Cells</subject><issn>1618-2642</issn><issn>1618-2650</issn><issn>1618-2650</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kbFu1jAURi1ERUvhBRiQJZYupr52EicjqlqKVAmEymzZzg1y5cTBTiT-TrwDPCFPgtO_FMTAdD2c79jXHyEvgL8GztVp5lxAw7ioGK8rqdjtI3IEDbRMNDV__HCuxCF5mvMN51C30Dwhh7LjUAnojsiPj2gCW_yIdIyTX2Ly02caB-owhDWYRPM6Y4pffY_UTD5ONGFAk5H6iV5ffmBwh2a65i1pqDOLCbvFOxPCjppxDn7w2P_t6X0e16U4fn77bsvo6ehditbHjFOO6Rk5GEzI-Px-HpNPF-fXZ5fs6v3bd2dvrpgTdbMwacF20hjLK9sqJ2AYejNUoh066Wz5EBBc9c45tFK1QyNU31grWqwa2YlaymNysvfOKX5ZMS969HnbxkwY16wlb0GpSnEo6Kt_0Ju4pqm8rlAdcGih24RiT5Vtck446Dn50aSdBq63zvS-M10603ed6dsSenmvXu2I_UPkd0kFkHsgz1s7mP7c_R_tL6A0plA</recordid><startdate>20240901</startdate><enddate>20240901</enddate><creator>Deshpande, Aaditya S.</creator><creator>Bechard, Tyler</creator><creator>DeVoe, Emily</creator><creator>Morse, Jared</creator><creator>Khan, Reem</creator><creator>Leung, Ka Ho</creator><creator>Andreescu, Silvana</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QO</scope><scope>7QQ</scope><scope>7SC</scope><scope>7SE</scope><scope>7SP</scope><scope>7SR</scope><scope>7TA</scope><scope>7TB</scope><scope>7U5</scope><scope>7U7</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0003-3382-7939</orcidid></search><sort><creationdate>20240901</creationdate><title>Real-time monitoring of cellular superoxide anion release in THP-1 cells using a catalytically amplified superoxide dismutase–based microbiosensor</title><author>Deshpande, Aaditya S. ; Bechard, Tyler ; DeVoe, Emily ; Morse, Jared ; Khan, Reem ; Leung, Ka Ho ; Andreescu, Silvana</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c256t-3b1b93aab04b87c21ffdaf428f93cb4371207dccceb378f627d6bb28e46392533</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Acetylcysteine</topic><topic>Amplification</topic><topic>Analytical Chemistry</topic><topic>Anions</topic><topic>Biochemistry</topic><topic>Biological activity</topic><topic>Biomimetic materials</topic><topic>Biomimetics</topic><topic>Biomonitoring</topic><topic>Biosensing Techniques - methods</topic><topic>Biosensors</topic><topic>Cell culture</topic><topic>Cellular structure</topic><topic>Characterization and Evaluation of Materials</topic><topic>Chemistry</topic><topic>Chemistry and Materials Science</topic><topic>Electrochemical Techniques - instrumentation</topic><topic>Electrochemical Techniques - methods</topic><topic>Electrochemistry</topic><topic>Emerging Trends in Electrochemical Analysis</topic><topic>Fabrication</topic><topic>Fluorescent dyes</topic><topic>Fluorescent indicators</topic><topic>Food Science</topic><topic>Humans</topic><topic>Laboratory Medicine</topic><topic>Leukemia</topic><topic>Limit of Detection</topic><topic>Lipopolysaccharides</topic><topic>Lipopolysaccharides - pharmacology</topic><topic>Microelectrodes</topic><topic>Monitoring/Environmental Analysis</topic><topic>Monocytes</topic><topic>MXenes</topic><topic>Oxidative stress</topic><topic>Paper in Forefront</topic><topic>Reactive oxygen species</topic><topic>Real time</topic><topic>Superoxide anions</topic><topic>Superoxide dismutase</topic><topic>Superoxide Dismutase - metabolism</topic><topic>Superoxides - analysis</topic><topic>Superoxides - metabolism</topic><topic>THP-1 Cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Deshpande, Aaditya S.</creatorcontrib><creatorcontrib>Bechard, Tyler</creatorcontrib><creatorcontrib>DeVoe, Emily</creatorcontrib><creatorcontrib>Morse, Jared</creatorcontrib><creatorcontrib>Khan, Reem</creatorcontrib><creatorcontrib>Leung, Ka Ho</creatorcontrib><creatorcontrib>Andreescu, Silvana</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Biotechnology Research Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Toxicology Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Analytical and bioanalytical chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Deshpande, Aaditya S.</au><au>Bechard, Tyler</au><au>DeVoe, Emily</au><au>Morse, Jared</au><au>Khan, Reem</au><au>Leung, Ka Ho</au><au>Andreescu, Silvana</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Real-time monitoring of cellular superoxide anion release in THP-1 cells using a catalytically amplified superoxide dismutase–based microbiosensor</atitle><jtitle>Analytical and bioanalytical chemistry</jtitle><stitle>Anal Bioanal Chem</stitle><addtitle>Anal Bioanal Chem</addtitle><date>2024-09-01</date><risdate>2024</risdate><volume>416</volume><issue>21</issue><spage>4727</spage><epage>4737</epage><pages>4727-4737</pages><issn>1618-2642</issn><issn>1618-2650</issn><eissn>1618-2650</eissn><abstract>Reactive oxygen species (ROS) including the superoxide anion (O
2
•−
) are typically studied in cell cultures using fluorescent dyes, which provide only discrete single-point measurements. These methods lack the capabilities for assessing O
2
•−
kinetics and release in a quantitative manner over long monitoring times. Herein, we present the fabrication and application of an electrochemical biosensor that enables real-time continuous monitoring of O
2
•−
release in cell cultures for extended periods (> 8 h) using an O
2
•−
specific microelectrode. To achieve the sensitivity and selectivity requirements for cellular sensing, we developed a biohybrid system consisting of superoxide dismutase (SOD) and Ti
3
C
2
T
x
MXenes, deposited on a gold microwire electrode (AuME) as O
2
•−
specific materials with catalytic amplification through the synergistic action of the enzyme and the biomimetic MXenes-based structure. The biosensor demonstrated a sensitivity of 18.35 nA/μM with a linear range from 147 to 930 nM in a cell culture medium. To demonstrate its robustness and practicality, we applied the biosensor to monitor O
2
•−
levels in human leukemia monocytic THP-1 cells upon stimulation with lipopolysaccharide (LPS). Using this strategy, we successfully monitored LPS-induced O
2
•−
in THP-1 cells, as well as the quenching effect induced by the ROS scavenger N-acetyl-
l
-cysteine (NAC). The biosensor is generally useful for exploring the role of oxidative stress and longitudinally monitoring O
2
•−
release in cell cultures, enabling studies of biochemical processes and associated oxidative stress mechanisms in cellular and other biological environments.
Graphical Abstract</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>39014219</pmid><doi>10.1007/s00216-024-05437-z</doi><tpages>11</tpages><orcidid>https://orcid.org/0000-0003-3382-7939</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1618-2642 |
| ispartof | Analytical and bioanalytical chemistry, 2024-09, Vol.416 (21), p.4727-4737 |
| issn | 1618-2642 1618-2650 1618-2650 |
| language | eng |
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| source | MEDLINE; SpringerNature Journals |
| subjects | Acetylcysteine Amplification Analytical Chemistry Anions Biochemistry Biological activity Biomimetic materials Biomimetics Biomonitoring Biosensing Techniques - methods Biosensors Cell culture Cellular structure Characterization and Evaluation of Materials Chemistry Chemistry and Materials Science Electrochemical Techniques - instrumentation Electrochemical Techniques - methods Electrochemistry Emerging Trends in Electrochemical Analysis Fabrication Fluorescent dyes Fluorescent indicators Food Science Humans Laboratory Medicine Leukemia Limit of Detection Lipopolysaccharides Lipopolysaccharides - pharmacology Microelectrodes Monitoring/Environmental Analysis Monocytes MXenes Oxidative stress Paper in Forefront Reactive oxygen species Real time Superoxide anions Superoxide dismutase Superoxide Dismutase - metabolism Superoxides - analysis Superoxides - metabolism THP-1 Cells |
| title | Real-time monitoring of cellular superoxide anion release in THP-1 cells using a catalytically amplified superoxide dismutase–based microbiosensor |
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