Direct analysis of the actin-filament formation effect in photodynamic therapy

Photodynamic therapy (PDT) is a method in which a photosensitizer is administered in vivo and irradiated with light to generate reactive oxygen species (ROS), thereby causing the selective death of cancer cells. Since PDT is a noninvasive cancer treatment method with few adverse effects, it has attr...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:RSC advances 2022-02, Vol.12 (1), p.5878-5889
Hauptverfasser: Taninaka, Atsushi, Ugajin, Shunta, Kurokawa, Hiromi, Nagoshi, Yu, Kamiyanagi, Mayuka, Takeuchi, Osamu, Matsui, Hirofumi, Shigekawa, Hidemi
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 5889
container_issue 1
container_start_page 5878
container_title RSC advances
container_volume 12
creator Taninaka, Atsushi
Ugajin, Shunta
Kurokawa, Hiromi
Nagoshi, Yu
Kamiyanagi, Mayuka
Takeuchi, Osamu
Matsui, Hirofumi
Shigekawa, Hidemi
description Photodynamic therapy (PDT) is a method in which a photosensitizer is administered in vivo and irradiated with light to generate reactive oxygen species (ROS), thereby causing the selective death of cancer cells. Since PDT is a noninvasive cancer treatment method with few adverse effects, it has attracted considerable attention and is increasingly used. In PDT, there are two dominant processes based on the actin filament (A-filament) formation effect: the destruction of cells by necrosis and vascular shutdown. Despite the importance of its fine control, the mechanism of the reaction process from the generation of reactive oxygen by photoinduction inducing the formation of A-filament and its polymerization to form stress fibers (S-fibers) has not yet been clarified because, for example, it has been difficult to directly observe and quantify such processes in living cells by conventional methods. Here, we have combined atomic force microscopy (AFM) with other techniques to reveal the mechanism of the A-filament and S-fiber formation processes that underlie the cell death process due to PDT. First, it was confirmed that activation of the small G protein RhoA, which is a signal that induces an increase in A-filament production, begins immediately after PDT treatment. The production of A-filament did not increase with increasing light intensity when the amount of light was large. Namely, the activation of RhoA reached an equilibrium state in about 1 min: however, the production of A-filament and its polymerization continued. The observed process corresponds well with the change in the amount of phosphorylated myosin-light chains, which induce A-filament polymerization. The increase in the elastic modulus of cells following the formation of S-fiber was confirmed by AFM for the first time. The distribution of generated A-filament and S-fiber was consistent with the photosensitizer distribution. PDT increases A-filament production, and when the ROS concentration is high, blebbing occurs and cells die, but when it is low, cell death does not occur and S-fiber is formed. That is, it is expected that vascular shutdown can be controlled efficiently by adjusting the amount of photosensitizer and the light intensity. We have combined atomic force microscopy with other techniques to reveal the mechanism of the actin filament and stress fibers formation processes that underlies the cell death process due to photodynamic therapy.
doi_str_mv 10.1039/d1ra09291j
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_crossref_primary_10_1039_D1RA09291J</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>2635492627</sourcerecordid><originalsourceid>FETCH-LOGICAL-c494t-78e8d2140d12fc66da0fe48fe0291357253ed8b2ef6529086056191b05690abd3</originalsourceid><addsrcrecordid>eNpdkc9LwzAcxYMobsxdvCsFLyJUk7TJkoswNn8yFETPIUsTl9E2M-mE_fembs5pLt_A95PHy3sAHCN4iWDGrwrkJeSYo_ke6GKY0xRDyvd37h3QD2EO46EEYYoOQScjOc4JybrgaWy9Vk0ia1mugg2JM0kz04lUja1TY0tZ6bpJjPOVbKyrE21My9s6Wcxc44pVLSur2jdeLlZH4MDIMuj-ZvbA2-3N6-g-nTzfPYyGk1TlPG_SAdOswCiHBcJGUVpIaHTOjIbxIxkZYJLpgk2xNpRgDhmFhCKOpnFwKKdF1gPXa93FclrpQkWPXpZi4W0l_Uo4acXfTW1n4t19CsYZIhhFgfONgHcfSx0aUdmgdFnKWrtlEDhmRRnDfBDRs3_o3C19zKulYpIcU9xSF2tKeReC12ZrBkHRNiXG6GX43dRjhE937W_Rn14icLIGfFDb7W_V2RdpEJf1</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2635492627</pqid></control><display><type>article</type><title>Direct analysis of the actin-filament formation effect in photodynamic therapy</title><source>DOAJ Directory of Open Access Journals</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>PubMed Central Open Access</source><source>PubMed Central</source><creator>Taninaka, Atsushi ; Ugajin, Shunta ; Kurokawa, Hiromi ; Nagoshi, Yu ; Kamiyanagi, Mayuka ; Takeuchi, Osamu ; Matsui, Hirofumi ; Shigekawa, Hidemi</creator><creatorcontrib>Taninaka, Atsushi ; Ugajin, Shunta ; Kurokawa, Hiromi ; Nagoshi, Yu ; Kamiyanagi, Mayuka ; Takeuchi, Osamu ; Matsui, Hirofumi ; Shigekawa, Hidemi</creatorcontrib><description>Photodynamic therapy (PDT) is a method in which a photosensitizer is administered in vivo and irradiated with light to generate reactive oxygen species (ROS), thereby causing the selective death of cancer cells. Since PDT is a noninvasive cancer treatment method with few adverse effects, it has attracted considerable attention and is increasingly used. In PDT, there are two dominant processes based on the actin filament (A-filament) formation effect: the destruction of cells by necrosis and vascular shutdown. Despite the importance of its fine control, the mechanism of the reaction process from the generation of reactive oxygen by photoinduction inducing the formation of A-filament and its polymerization to form stress fibers (S-fibers) has not yet been clarified because, for example, it has been difficult to directly observe and quantify such processes in living cells by conventional methods. Here, we have combined atomic force microscopy (AFM) with other techniques to reveal the mechanism of the A-filament and S-fiber formation processes that underlie the cell death process due to PDT. First, it was confirmed that activation of the small G protein RhoA, which is a signal that induces an increase in A-filament production, begins immediately after PDT treatment. The production of A-filament did not increase with increasing light intensity when the amount of light was large. Namely, the activation of RhoA reached an equilibrium state in about 1 min: however, the production of A-filament and its polymerization continued. The observed process corresponds well with the change in the amount of phosphorylated myosin-light chains, which induce A-filament polymerization. The increase in the elastic modulus of cells following the formation of S-fiber was confirmed by AFM for the first time. The distribution of generated A-filament and S-fiber was consistent with the photosensitizer distribution. PDT increases A-filament production, and when the ROS concentration is high, blebbing occurs and cells die, but when it is low, cell death does not occur and S-fiber is formed. That is, it is expected that vascular shutdown can be controlled efficiently by adjusting the amount of photosensitizer and the light intensity. We have combined atomic force microscopy with other techniques to reveal the mechanism of the actin filament and stress fibers formation processes that underlies the cell death process due to photodynamic therapy.</description><identifier>ISSN: 2046-2069</identifier><identifier>EISSN: 2046-2069</identifier><identifier>DOI: 10.1039/d1ra09291j</identifier><identifier>PMID: 35424553</identifier><language>eng</language><publisher>England: Royal Society of Chemistry</publisher><subject>Apoptosis ; Atomic force microscopy ; Cancer ; Cell death ; Chemistry ; In vivo methods and tests ; Luminous intensity ; Modulus of elasticity ; Myosin ; Necrosis ; Photodynamic therapy ; Polymerization ; Shutdowns</subject><ispartof>RSC advances, 2022-02, Vol.12 (1), p.5878-5889</ispartof><rights>This journal is © The Royal Society of Chemistry.</rights><rights>Copyright Royal Society of Chemistry 2022</rights><rights>This journal is © The Royal Society of Chemistry 2022 The Royal Society of Chemistry</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c494t-78e8d2140d12fc66da0fe48fe0291357253ed8b2ef6529086056191b05690abd3</citedby><cites>FETCH-LOGICAL-c494t-78e8d2140d12fc66da0fe48fe0291357253ed8b2ef6529086056191b05690abd3</cites><orcidid>0000-0001-9550-5148</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8981521/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8981521/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,27923,27924,53790,53792</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35424553$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Taninaka, Atsushi</creatorcontrib><creatorcontrib>Ugajin, Shunta</creatorcontrib><creatorcontrib>Kurokawa, Hiromi</creatorcontrib><creatorcontrib>Nagoshi, Yu</creatorcontrib><creatorcontrib>Kamiyanagi, Mayuka</creatorcontrib><creatorcontrib>Takeuchi, Osamu</creatorcontrib><creatorcontrib>Matsui, Hirofumi</creatorcontrib><creatorcontrib>Shigekawa, Hidemi</creatorcontrib><title>Direct analysis of the actin-filament formation effect in photodynamic therapy</title><title>RSC advances</title><addtitle>RSC Adv</addtitle><description>Photodynamic therapy (PDT) is a method in which a photosensitizer is administered in vivo and irradiated with light to generate reactive oxygen species (ROS), thereby causing the selective death of cancer cells. Since PDT is a noninvasive cancer treatment method with few adverse effects, it has attracted considerable attention and is increasingly used. In PDT, there are two dominant processes based on the actin filament (A-filament) formation effect: the destruction of cells by necrosis and vascular shutdown. Despite the importance of its fine control, the mechanism of the reaction process from the generation of reactive oxygen by photoinduction inducing the formation of A-filament and its polymerization to form stress fibers (S-fibers) has not yet been clarified because, for example, it has been difficult to directly observe and quantify such processes in living cells by conventional methods. Here, we have combined atomic force microscopy (AFM) with other techniques to reveal the mechanism of the A-filament and S-fiber formation processes that underlie the cell death process due to PDT. First, it was confirmed that activation of the small G protein RhoA, which is a signal that induces an increase in A-filament production, begins immediately after PDT treatment. The production of A-filament did not increase with increasing light intensity when the amount of light was large. Namely, the activation of RhoA reached an equilibrium state in about 1 min: however, the production of A-filament and its polymerization continued. The observed process corresponds well with the change in the amount of phosphorylated myosin-light chains, which induce A-filament polymerization. The increase in the elastic modulus of cells following the formation of S-fiber was confirmed by AFM for the first time. The distribution of generated A-filament and S-fiber was consistent with the photosensitizer distribution. PDT increases A-filament production, and when the ROS concentration is high, blebbing occurs and cells die, but when it is low, cell death does not occur and S-fiber is formed. That is, it is expected that vascular shutdown can be controlled efficiently by adjusting the amount of photosensitizer and the light intensity. We have combined atomic force microscopy with other techniques to reveal the mechanism of the actin filament and stress fibers formation processes that underlies the cell death process due to photodynamic therapy.</description><subject>Apoptosis</subject><subject>Atomic force microscopy</subject><subject>Cancer</subject><subject>Cell death</subject><subject>Chemistry</subject><subject>In vivo methods and tests</subject><subject>Luminous intensity</subject><subject>Modulus of elasticity</subject><subject>Myosin</subject><subject>Necrosis</subject><subject>Photodynamic therapy</subject><subject>Polymerization</subject><subject>Shutdowns</subject><issn>2046-2069</issn><issn>2046-2069</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNpdkc9LwzAcxYMobsxdvCsFLyJUk7TJkoswNn8yFETPIUsTl9E2M-mE_fembs5pLt_A95PHy3sAHCN4iWDGrwrkJeSYo_ke6GKY0xRDyvd37h3QD2EO46EEYYoOQScjOc4JybrgaWy9Vk0ia1mugg2JM0kz04lUja1TY0tZ6bpJjPOVbKyrE21My9s6Wcxc44pVLSur2jdeLlZH4MDIMuj-ZvbA2-3N6-g-nTzfPYyGk1TlPG_SAdOswCiHBcJGUVpIaHTOjIbxIxkZYJLpgk2xNpRgDhmFhCKOpnFwKKdF1gPXa93FclrpQkWPXpZi4W0l_Uo4acXfTW1n4t19CsYZIhhFgfONgHcfSx0aUdmgdFnKWrtlEDhmRRnDfBDRs3_o3C19zKulYpIcU9xSF2tKeReC12ZrBkHRNiXG6GX43dRjhE937W_Rn14icLIGfFDb7W_V2RdpEJf1</recordid><startdate>20220216</startdate><enddate>20220216</enddate><creator>Taninaka, Atsushi</creator><creator>Ugajin, Shunta</creator><creator>Kurokawa, Hiromi</creator><creator>Nagoshi, Yu</creator><creator>Kamiyanagi, Mayuka</creator><creator>Takeuchi, Osamu</creator><creator>Matsui, Hirofumi</creator><creator>Shigekawa, Hidemi</creator><general>Royal Society of Chemistry</general><general>The Royal Society of Chemistry</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SR</scope><scope>8BQ</scope><scope>8FD</scope><scope>JG9</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9550-5148</orcidid></search><sort><creationdate>20220216</creationdate><title>Direct analysis of the actin-filament formation effect in photodynamic therapy</title><author>Taninaka, Atsushi ; Ugajin, Shunta ; Kurokawa, Hiromi ; Nagoshi, Yu ; Kamiyanagi, Mayuka ; Takeuchi, Osamu ; Matsui, Hirofumi ; Shigekawa, Hidemi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c494t-78e8d2140d12fc66da0fe48fe0291357253ed8b2ef6529086056191b05690abd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Apoptosis</topic><topic>Atomic force microscopy</topic><topic>Cancer</topic><topic>Cell death</topic><topic>Chemistry</topic><topic>In vivo methods and tests</topic><topic>Luminous intensity</topic><topic>Modulus of elasticity</topic><topic>Myosin</topic><topic>Necrosis</topic><topic>Photodynamic therapy</topic><topic>Polymerization</topic><topic>Shutdowns</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Taninaka, Atsushi</creatorcontrib><creatorcontrib>Ugajin, Shunta</creatorcontrib><creatorcontrib>Kurokawa, Hiromi</creatorcontrib><creatorcontrib>Nagoshi, Yu</creatorcontrib><creatorcontrib>Kamiyanagi, Mayuka</creatorcontrib><creatorcontrib>Takeuchi, Osamu</creatorcontrib><creatorcontrib>Matsui, Hirofumi</creatorcontrib><creatorcontrib>Shigekawa, Hidemi</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Engineered Materials Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Materials Research Database</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>RSC advances</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Taninaka, Atsushi</au><au>Ugajin, Shunta</au><au>Kurokawa, Hiromi</au><au>Nagoshi, Yu</au><au>Kamiyanagi, Mayuka</au><au>Takeuchi, Osamu</au><au>Matsui, Hirofumi</au><au>Shigekawa, Hidemi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Direct analysis of the actin-filament formation effect in photodynamic therapy</atitle><jtitle>RSC advances</jtitle><addtitle>RSC Adv</addtitle><date>2022-02-16</date><risdate>2022</risdate><volume>12</volume><issue>1</issue><spage>5878</spage><epage>5889</epage><pages>5878-5889</pages><issn>2046-2069</issn><eissn>2046-2069</eissn><abstract>Photodynamic therapy (PDT) is a method in which a photosensitizer is administered in vivo and irradiated with light to generate reactive oxygen species (ROS), thereby causing the selective death of cancer cells. Since PDT is a noninvasive cancer treatment method with few adverse effects, it has attracted considerable attention and is increasingly used. In PDT, there are two dominant processes based on the actin filament (A-filament) formation effect: the destruction of cells by necrosis and vascular shutdown. Despite the importance of its fine control, the mechanism of the reaction process from the generation of reactive oxygen by photoinduction inducing the formation of A-filament and its polymerization to form stress fibers (S-fibers) has not yet been clarified because, for example, it has been difficult to directly observe and quantify such processes in living cells by conventional methods. Here, we have combined atomic force microscopy (AFM) with other techniques to reveal the mechanism of the A-filament and S-fiber formation processes that underlie the cell death process due to PDT. First, it was confirmed that activation of the small G protein RhoA, which is a signal that induces an increase in A-filament production, begins immediately after PDT treatment. The production of A-filament did not increase with increasing light intensity when the amount of light was large. Namely, the activation of RhoA reached an equilibrium state in about 1 min: however, the production of A-filament and its polymerization continued. The observed process corresponds well with the change in the amount of phosphorylated myosin-light chains, which induce A-filament polymerization. The increase in the elastic modulus of cells following the formation of S-fiber was confirmed by AFM for the first time. The distribution of generated A-filament and S-fiber was consistent with the photosensitizer distribution. PDT increases A-filament production, and when the ROS concentration is high, blebbing occurs and cells die, but when it is low, cell death does not occur and S-fiber is formed. That is, it is expected that vascular shutdown can be controlled efficiently by adjusting the amount of photosensitizer and the light intensity. We have combined atomic force microscopy with other techniques to reveal the mechanism of the actin filament and stress fibers formation processes that underlies the cell death process due to photodynamic therapy.</abstract><cop>England</cop><pub>Royal Society of Chemistry</pub><pmid>35424553</pmid><doi>10.1039/d1ra09291j</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-9550-5148</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 2046-2069
ispartof RSC advances, 2022-02, Vol.12 (1), p.5878-5889
issn 2046-2069
2046-2069
language eng
recordid cdi_crossref_primary_10_1039_D1RA09291J
source DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central Open Access; PubMed Central
subjects Apoptosis
Atomic force microscopy
Cancer
Cell death
Chemistry
In vivo methods and tests
Luminous intensity
Modulus of elasticity
Myosin
Necrosis
Photodynamic therapy
Polymerization
Shutdowns
title Direct analysis of the actin-filament formation effect in photodynamic therapy
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-08T07%3A28%3A12IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Direct%20analysis%20of%20the%20actin-filament%20formation%20effect%20in%20photodynamic%20therapy&rft.jtitle=RSC%20advances&rft.au=Taninaka,%20Atsushi&rft.date=2022-02-16&rft.volume=12&rft.issue=1&rft.spage=5878&rft.epage=5889&rft.pages=5878-5889&rft.issn=2046-2069&rft.eissn=2046-2069&rft_id=info:doi/10.1039/d1ra09291j&rft_dat=%3Cproquest_cross%3E2635492627%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2635492627&rft_id=info:pmid/35424553&rfr_iscdi=true