PpIX-enabled fluorescence-based detection and photodynamic priming of platinum-resistant ovarian cancer cells under fluid shear stress
Over 75% percent of ovarian cancer patients are diagnosed with advanced-stage disease characterized by unresectable intraperitoneal dissemination and the presence of ascites, or excessive fluid build-up within the abdomen. Conventional treatments include cytoreductive surgery followed by multi-line...
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| Veröffentlicht in: | Photochemistry and photobiology 2024-11, Vol.100 (6), p.1603-1621 |
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| creator | Ruhi, Mustafa Kemal Rickard, Brittany P Overchuk, Marta Sinawang, Prima Dewi Stanley, Elizabeth Mansi, Matthew Sierra, Raymond G Hayes, Brandon Tan, Xianming Akin, Demir Chen, Bin Demirci, Utkan Rizvi, Imran |
| description | Over 75% percent of ovarian cancer patients are diagnosed with advanced-stage disease characterized by unresectable intraperitoneal dissemination and the presence of ascites, or excessive fluid build-up within the abdomen. Conventional treatments include cytoreductive surgery followed by multi-line platinum and taxane chemotherapy regimens. Despite an initial response to treatment, over 75% of patients with advanced-stage ovarian cancer will relapse and succumb to platinum-resistant disease. Recent evidence suggests that fluid shear stress (FSS), which results from the movement of fluid such as ascites, induces epithelial-to-mesenchymal transition and confers resistance to carboplatin in ovarian cancer cells. This study demonstrates, for the first time, that FSS-induced platinum resistance correlates with increased cellular protoporphyrin IX (PpIX), the penultimate downstream product of heme biosynthesis, the production of which can be enhanced using the clinically approved pro-drug aminolevulinic acid (ALA). These data suggest that, with further investigation, PpIX could serve as a fluorescence-based biomarker of FSS-induced platinum resistance. Additionally, this study investigates the efficacy of PpIX-enabled photodynamic therapy (PDT) and the secretion of extracellular vesicles under static and FSS conditions in Caov-3 and NIH:OVCAR-3 cells, two representative cell lines for high-grade serous ovarian carcinoma (HGSOC), the most lethal form of the disease. FSS induces resistance to ALA-PpIX-mediated PDT, along with a significant increase in the number of EVs. Finally, the ability of PpIX-mediated photodynamic priming (PDP) to enhance carboplatin efficacy under FSS conditions is quantified. These preliminary findings in monolayer cultures necessitate additional studies to determine the feasibility of PpIX as a fluorescence-based indicator, and mediator of PDP, to target chemoresistance in the context of FSS. |
| doi_str_mv | 10.1111/php.14014 |
| format | Article |
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Conventional treatments include cytoreductive surgery followed by multi-line platinum and taxane chemotherapy regimens. Despite an initial response to treatment, over 75% of patients with advanced-stage ovarian cancer will relapse and succumb to platinum-resistant disease. Recent evidence suggests that fluid shear stress (FSS), which results from the movement of fluid such as ascites, induces epithelial-to-mesenchymal transition and confers resistance to carboplatin in ovarian cancer cells. This study demonstrates, for the first time, that FSS-induced platinum resistance correlates with increased cellular protoporphyrin IX (PpIX), the penultimate downstream product of heme biosynthesis, the production of which can be enhanced using the clinically approved pro-drug aminolevulinic acid (ALA). These data suggest that, with further investigation, PpIX could serve as a fluorescence-based biomarker of FSS-induced platinum resistance. Additionally, this study investigates the efficacy of PpIX-enabled photodynamic therapy (PDT) and the secretion of extracellular vesicles under static and FSS conditions in Caov-3 and NIH:OVCAR-3 cells, two representative cell lines for high-grade serous ovarian carcinoma (HGSOC), the most lethal form of the disease. FSS induces resistance to ALA-PpIX-mediated PDT, along with a significant increase in the number of EVs. Finally, the ability of PpIX-mediated photodynamic priming (PDP) to enhance carboplatin efficacy under FSS conditions is quantified. These preliminary findings in monolayer cultures necessitate additional studies to determine the feasibility of PpIX as a fluorescence-based indicator, and mediator of PDP, to target chemoresistance in the context of FSS.</description><identifier>ISSN: 0031-8655</identifier><identifier>ISSN: 1751-1097</identifier><identifier>EISSN: 1751-1097</identifier><identifier>DOI: 10.1111/php.14014</identifier><identifier>PMID: 39189505</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Aminolevulinic acid ; Aminolevulinic Acid - pharmacology ; Aminolevulinic Acid - therapeutic use ; Antineoplastic Agents - pharmacology ; Ascites ; Biomarkers ; Biosynthesis ; Cancer ; Cancer therapies ; Carboplatin ; Carboplatin - pharmacology ; Cell Line, Tumor ; Cell migration ; Chemoresistance ; Chemotherapy ; Disease resistance ; Drug Resistance, Neoplasm ; Effectiveness ; Feasibility studies ; Female ; Fluid flow ; Fluorescence ; Humans ; Mechanical stimuli ; Ovarian cancer ; Ovarian carcinoma ; Ovarian Neoplasms - drug therapy ; Ovarian Neoplasms - metabolism ; Ovarian Neoplasms - pathology ; Patients ; Photochemotherapy - methods ; Photodynamic therapy ; Photosensitizing Agents - pharmacology ; Photosensitizing Agents - therapeutic use ; Platinum ; Platinum - pharmacology ; Platinum - therapeutic use ; Priming ; Protoporphyrin ; Protoporphyrin IX ; Protoporphyrins - metabolism ; Shear stress ; Stress, Mechanical ; Tumor cell lines</subject><ispartof>Photochemistry and photobiology, 2024-11, Vol.100 (6), p.1603-1621</ispartof><rights>2024 The Author(s). 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Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c238t-200d905cda60cd34fe0478f97b4e5bcc2085d07c40555b18334295f3976caeac3</cites><orcidid>0000-0001-8460-3260 ; 0000-0002-8203-0427 ; 0000-0002-6112-1290 ; 0000-0002-7736-4158 ; 0000-0001-9673-4700</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39189505$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ruhi, Mustafa Kemal</creatorcontrib><creatorcontrib>Rickard, Brittany P</creatorcontrib><creatorcontrib>Overchuk, Marta</creatorcontrib><creatorcontrib>Sinawang, Prima Dewi</creatorcontrib><creatorcontrib>Stanley, Elizabeth</creatorcontrib><creatorcontrib>Mansi, Matthew</creatorcontrib><creatorcontrib>Sierra, Raymond G</creatorcontrib><creatorcontrib>Hayes, Brandon</creatorcontrib><creatorcontrib>Tan, Xianming</creatorcontrib><creatorcontrib>Akin, Demir</creatorcontrib><creatorcontrib>Chen, Bin</creatorcontrib><creatorcontrib>Demirci, Utkan</creatorcontrib><creatorcontrib>Rizvi, Imran</creatorcontrib><title>PpIX-enabled fluorescence-based detection and photodynamic priming of platinum-resistant ovarian cancer cells under fluid shear stress</title><title>Photochemistry and photobiology</title><addtitle>Photochem Photobiol</addtitle><description>Over 75% percent of ovarian cancer patients are diagnosed with advanced-stage disease characterized by unresectable intraperitoneal dissemination and the presence of ascites, or excessive fluid build-up within the abdomen. Conventional treatments include cytoreductive surgery followed by multi-line platinum and taxane chemotherapy regimens. Despite an initial response to treatment, over 75% of patients with advanced-stage ovarian cancer will relapse and succumb to platinum-resistant disease. Recent evidence suggests that fluid shear stress (FSS), which results from the movement of fluid such as ascites, induces epithelial-to-mesenchymal transition and confers resistance to carboplatin in ovarian cancer cells. This study demonstrates, for the first time, that FSS-induced platinum resistance correlates with increased cellular protoporphyrin IX (PpIX), the penultimate downstream product of heme biosynthesis, the production of which can be enhanced using the clinically approved pro-drug aminolevulinic acid (ALA). These data suggest that, with further investigation, PpIX could serve as a fluorescence-based biomarker of FSS-induced platinum resistance. Additionally, this study investigates the efficacy of PpIX-enabled photodynamic therapy (PDT) and the secretion of extracellular vesicles under static and FSS conditions in Caov-3 and NIH:OVCAR-3 cells, two representative cell lines for high-grade serous ovarian carcinoma (HGSOC), the most lethal form of the disease. FSS induces resistance to ALA-PpIX-mediated PDT, along with a significant increase in the number of EVs. Finally, the ability of PpIX-mediated photodynamic priming (PDP) to enhance carboplatin efficacy under FSS conditions is quantified. These preliminary findings in monolayer cultures necessitate additional studies to determine the feasibility of PpIX as a fluorescence-based indicator, and mediator of PDP, to target chemoresistance in the context of FSS.</description><subject>Aminolevulinic acid</subject><subject>Aminolevulinic Acid - pharmacology</subject><subject>Aminolevulinic Acid - therapeutic use</subject><subject>Antineoplastic Agents - pharmacology</subject><subject>Ascites</subject><subject>Biomarkers</subject><subject>Biosynthesis</subject><subject>Cancer</subject><subject>Cancer therapies</subject><subject>Carboplatin</subject><subject>Carboplatin - pharmacology</subject><subject>Cell Line, Tumor</subject><subject>Cell migration</subject><subject>Chemoresistance</subject><subject>Chemotherapy</subject><subject>Disease resistance</subject><subject>Drug Resistance, Neoplasm</subject><subject>Effectiveness</subject><subject>Feasibility studies</subject><subject>Female</subject><subject>Fluid flow</subject><subject>Fluorescence</subject><subject>Humans</subject><subject>Mechanical stimuli</subject><subject>Ovarian cancer</subject><subject>Ovarian carcinoma</subject><subject>Ovarian Neoplasms - drug therapy</subject><subject>Ovarian Neoplasms - metabolism</subject><subject>Ovarian Neoplasms - pathology</subject><subject>Patients</subject><subject>Photochemotherapy - methods</subject><subject>Photodynamic therapy</subject><subject>Photosensitizing Agents - pharmacology</subject><subject>Photosensitizing Agents - therapeutic use</subject><subject>Platinum</subject><subject>Platinum - pharmacology</subject><subject>Platinum - therapeutic use</subject><subject>Priming</subject><subject>Protoporphyrin</subject><subject>Protoporphyrin IX</subject><subject>Protoporphyrins - metabolism</subject><subject>Shear stress</subject><subject>Stress, Mechanical</subject><subject>Tumor cell lines</subject><issn>0031-8655</issn><issn>1751-1097</issn><issn>1751-1097</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkc1u1TAQhS1ERS-FBS-ALLEpi7Tj2I7jJaooVKoEiyKxixx7wnWV2MF2kPoCfW586c-C2cxo9M2Z0RxC3jE4YzXO1_16xgQw8YLsmJKsYaDVS7ID4KzpOymPyeucb6ESWrFX5Jhr1msJckfuv69XPxsMZpzR0WneYsJsMVhsRpNry2FBW3wM1ARH130s0d0Fs3hL1-QXH37RONF1NsWHbWnqtM_FhELjH5O8CdSaKpaoxXnOdAuu1nWNdzTv0SSaSx3Jb8jRZOaMbx_zCflx-fnm4mtz_e3L1cWn68a2vC9NC-A0SOtMB9ZxMSEI1U9ajQLlaG0LvXSgrAAp5ch6zkWr5cS16qxBY_kJOX3QXVP8vWEuw-Lz4TQTMG554PVxQgvVsop--A-9jVsK9bqBs7bXAF2nKvXxgbIp5pxwGg5fMeluYDAczBmqOcM_cyr7_lFxGxd0z-STG_wvysGMCQ</recordid><startdate>202411</startdate><enddate>202411</enddate><creator>Ruhi, Mustafa Kemal</creator><creator>Rickard, Brittany P</creator><creator>Overchuk, Marta</creator><creator>Sinawang, Prima Dewi</creator><creator>Stanley, Elizabeth</creator><creator>Mansi, Matthew</creator><creator>Sierra, Raymond G</creator><creator>Hayes, Brandon</creator><creator>Tan, Xianming</creator><creator>Akin, Demir</creator><creator>Chen, Bin</creator><creator>Demirci, Utkan</creator><creator>Rizvi, Imran</creator><general>Blackwell Publishing Ltd</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>4T-</scope><scope>7TM</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8460-3260</orcidid><orcidid>https://orcid.org/0000-0002-8203-0427</orcidid><orcidid>https://orcid.org/0000-0002-6112-1290</orcidid><orcidid>https://orcid.org/0000-0002-7736-4158</orcidid><orcidid>https://orcid.org/0000-0001-9673-4700</orcidid></search><sort><creationdate>202411</creationdate><title>PpIX-enabled fluorescence-based detection and photodynamic priming of platinum-resistant ovarian cancer cells under fluid shear stress</title><author>Ruhi, Mustafa Kemal ; Rickard, Brittany P ; Overchuk, Marta ; Sinawang, Prima Dewi ; Stanley, Elizabeth ; Mansi, Matthew ; Sierra, Raymond G ; Hayes, Brandon ; Tan, Xianming ; Akin, Demir ; Chen, Bin ; Demirci, Utkan ; Rizvi, Imran</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c238t-200d905cda60cd34fe0478f97b4e5bcc2085d07c40555b18334295f3976caeac3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Aminolevulinic acid</topic><topic>Aminolevulinic Acid - pharmacology</topic><topic>Aminolevulinic Acid - therapeutic use</topic><topic>Antineoplastic Agents - pharmacology</topic><topic>Ascites</topic><topic>Biomarkers</topic><topic>Biosynthesis</topic><topic>Cancer</topic><topic>Cancer therapies</topic><topic>Carboplatin</topic><topic>Carboplatin - pharmacology</topic><topic>Cell Line, Tumor</topic><topic>Cell migration</topic><topic>Chemoresistance</topic><topic>Chemotherapy</topic><topic>Disease resistance</topic><topic>Drug Resistance, Neoplasm</topic><topic>Effectiveness</topic><topic>Feasibility studies</topic><topic>Female</topic><topic>Fluid flow</topic><topic>Fluorescence</topic><topic>Humans</topic><topic>Mechanical stimuli</topic><topic>Ovarian cancer</topic><topic>Ovarian carcinoma</topic><topic>Ovarian Neoplasms - drug therapy</topic><topic>Ovarian Neoplasms - metabolism</topic><topic>Ovarian Neoplasms - pathology</topic><topic>Patients</topic><topic>Photochemotherapy - methods</topic><topic>Photodynamic therapy</topic><topic>Photosensitizing Agents - pharmacology</topic><topic>Photosensitizing Agents - therapeutic use</topic><topic>Platinum</topic><topic>Platinum - pharmacology</topic><topic>Platinum - therapeutic use</topic><topic>Priming</topic><topic>Protoporphyrin</topic><topic>Protoporphyrin IX</topic><topic>Protoporphyrins - metabolism</topic><topic>Shear stress</topic><topic>Stress, Mechanical</topic><topic>Tumor cell lines</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ruhi, Mustafa Kemal</creatorcontrib><creatorcontrib>Rickard, Brittany P</creatorcontrib><creatorcontrib>Overchuk, Marta</creatorcontrib><creatorcontrib>Sinawang, Prima Dewi</creatorcontrib><creatorcontrib>Stanley, Elizabeth</creatorcontrib><creatorcontrib>Mansi, Matthew</creatorcontrib><creatorcontrib>Sierra, Raymond G</creatorcontrib><creatorcontrib>Hayes, Brandon</creatorcontrib><creatorcontrib>Tan, Xianming</creatorcontrib><creatorcontrib>Akin, Demir</creatorcontrib><creatorcontrib>Chen, Bin</creatorcontrib><creatorcontrib>Demirci, Utkan</creatorcontrib><creatorcontrib>Rizvi, Imran</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>Nucleic Acids Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Photochemistry and photobiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ruhi, Mustafa Kemal</au><au>Rickard, Brittany P</au><au>Overchuk, Marta</au><au>Sinawang, Prima Dewi</au><au>Stanley, Elizabeth</au><au>Mansi, Matthew</au><au>Sierra, Raymond G</au><au>Hayes, Brandon</au><au>Tan, Xianming</au><au>Akin, Demir</au><au>Chen, Bin</au><au>Demirci, Utkan</au><au>Rizvi, Imran</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>PpIX-enabled fluorescence-based detection and photodynamic priming of platinum-resistant ovarian cancer cells under fluid shear stress</atitle><jtitle>Photochemistry and photobiology</jtitle><addtitle>Photochem Photobiol</addtitle><date>2024-11</date><risdate>2024</risdate><volume>100</volume><issue>6</issue><spage>1603</spage><epage>1621</epage><pages>1603-1621</pages><issn>0031-8655</issn><issn>1751-1097</issn><eissn>1751-1097</eissn><abstract>Over 75% percent of ovarian cancer patients are diagnosed with advanced-stage disease characterized by unresectable intraperitoneal dissemination and the presence of ascites, or excessive fluid build-up within the abdomen. Conventional treatments include cytoreductive surgery followed by multi-line platinum and taxane chemotherapy regimens. Despite an initial response to treatment, over 75% of patients with advanced-stage ovarian cancer will relapse and succumb to platinum-resistant disease. Recent evidence suggests that fluid shear stress (FSS), which results from the movement of fluid such as ascites, induces epithelial-to-mesenchymal transition and confers resistance to carboplatin in ovarian cancer cells. This study demonstrates, for the first time, that FSS-induced platinum resistance correlates with increased cellular protoporphyrin IX (PpIX), the penultimate downstream product of heme biosynthesis, the production of which can be enhanced using the clinically approved pro-drug aminolevulinic acid (ALA). These data suggest that, with further investigation, PpIX could serve as a fluorescence-based biomarker of FSS-induced platinum resistance. Additionally, this study investigates the efficacy of PpIX-enabled photodynamic therapy (PDT) and the secretion of extracellular vesicles under static and FSS conditions in Caov-3 and NIH:OVCAR-3 cells, two representative cell lines for high-grade serous ovarian carcinoma (HGSOC), the most lethal form of the disease. FSS induces resistance to ALA-PpIX-mediated PDT, along with a significant increase in the number of EVs. Finally, the ability of PpIX-mediated photodynamic priming (PDP) to enhance carboplatin efficacy under FSS conditions is quantified. 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| subjects | Aminolevulinic acid Aminolevulinic Acid - pharmacology Aminolevulinic Acid - therapeutic use Antineoplastic Agents - pharmacology Ascites Biomarkers Biosynthesis Cancer Cancer therapies Carboplatin Carboplatin - pharmacology Cell Line, Tumor Cell migration Chemoresistance Chemotherapy Disease resistance Drug Resistance, Neoplasm Effectiveness Feasibility studies Female Fluid flow Fluorescence Humans Mechanical stimuli Ovarian cancer Ovarian carcinoma Ovarian Neoplasms - drug therapy Ovarian Neoplasms - metabolism Ovarian Neoplasms - pathology Patients Photochemotherapy - methods Photodynamic therapy Photosensitizing Agents - pharmacology Photosensitizing Agents - therapeutic use Platinum Platinum - pharmacology Platinum - therapeutic use Priming Protoporphyrin Protoporphyrin IX Protoporphyrins - metabolism Shear stress Stress, Mechanical Tumor cell lines |
| title | PpIX-enabled fluorescence-based detection and photodynamic priming of platinum-resistant ovarian cancer cells under fluid shear stress |
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