Endowing Pt(IV) with Perfluorocarbon Chains and Human Serum Albumin Encapsulation for Highly Effective Antitumor Chemoimmunotherapy
Tumor metastases and reoccurrence are considered the leading causes of cancer-associated deaths. As an emerging therapeutic method, increasing research efforts have been devoted to immunogenic cell death (ICD)-inducing compounds to solve the challenge. The clinically approved chemotherapeutic Pt com...
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description | Tumor metastases and reoccurrence are considered the leading causes of cancer-associated deaths. As an emerging therapeutic method, increasing research efforts have been devoted to immunogenic cell death (ICD)-inducing compounds to solve the challenge. The clinically approved chemotherapeutic Pt complexes are not or are only poorly able to trigger ICD. Herein, the axial functionalization of the Pt(II) complex cisplatin with perfluorocarbon chains into ICD-inducing Pt(IV) prodrugs is reported. Strikingly, while the Pt(II) complex as well as the perfluorocarbon ligands did not induce ICD, the Pt(IV) prodrug demonstrated unexpectantly the induction of ICD through accumulation in the endoplasmic reticulum and generation of reactive oxygen species in this organelle. To enhance the pharmacological properties, the compound was encapsulated with human serum albumin into nanoparticles. While selectively accumulating in the tumorous tissue, the nanoparticles demonstrated a strong tumor growth inhibitory effect against osteosarcoma inside a mouse model. In vivo tumor vaccine analysis also demonstrated the ability of Pt(IV) to be an ideal ICD inducer. Overall, this study reports on axially perfluorocarbon chain-modified Pt(IV) complexes for ICD induction and chemoimmunotherapy in osteosarcoma. |
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As an emerging therapeutic method, increasing research efforts have been devoted to immunogenic cell death (ICD)-inducing compounds to solve the challenge. The clinically approved chemotherapeutic Pt complexes are not or are only poorly able to trigger ICD. Herein, the axial functionalization of the Pt(II) complex cisplatin with perfluorocarbon chains into ICD-inducing Pt(IV) prodrugs is reported. Strikingly, while the Pt(II) complex as well as the perfluorocarbon ligands did not induce ICD, the Pt(IV) prodrug demonstrated unexpectantly the induction of ICD through accumulation in the endoplasmic reticulum and generation of reactive oxygen species in this organelle. To enhance the pharmacological properties, the compound was encapsulated with human serum albumin into nanoparticles. While selectively accumulating in the tumorous tissue, the nanoparticles demonstrated a strong tumor growth inhibitory effect against osteosarcoma inside a mouse model. In vivo tumor vaccine analysis also demonstrated the ability of Pt(IV) to be an ideal ICD inducer. Overall, this study reports on axially perfluorocarbon chain-modified Pt(IV) complexes for ICD induction and chemoimmunotherapy in osteosarcoma.</description><identifier>ISSN: 1936-0851</identifier><identifier>EISSN: 1936-086X</identifier><identifier>DOI: 10.1021/acsnano.4c01352</identifier><identifier>PMID: 38749906</identifier><language>eng</language><publisher>United States: American Chemical Society</publisher><subject>Animals ; Antineoplastic Agents - chemistry ; Antineoplastic Agents - pharmacology ; Cell Line, Tumor ; Cell Proliferation - drug effects ; Cisplatin - chemistry ; Cisplatin - pharmacology ; Fluorocarbons - chemistry ; Fluorocarbons - pharmacology ; Humans ; Immunogenic Cell Death - drug effects ; Immunotherapy ; Mice ; Mice, Inbred BALB C ; Nanoparticles - chemistry ; Platinum - chemistry ; Platinum - pharmacology ; Prodrugs - chemistry ; Prodrugs - pharmacology ; Serum Albumin, Human - chemistry</subject><ispartof>ACS nano, 2024-05, Vol.18 (21), p.13683-13695</ispartof><rights>2024 American Chemical Society</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-a287t-de0768f553b296f165b9acaee515834b2b1b8b39cda1049bf4e69637fe7a32ee3</cites><orcidid>0000-0001-7622-4674 ; 0000-0001-8159-8187 ; 0000-0001-5258-0260</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://pubs.acs.org/doi/pdf/10.1021/acsnano.4c01352$$EPDF$$P50$$Gacs$$H</linktopdf><linktohtml>$$Uhttps://pubs.acs.org/doi/10.1021/acsnano.4c01352$$EHTML$$P50$$Gacs$$H</linktohtml><link.rule.ids>314,776,780,2752,27053,27901,27902,56713,56763</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38749906$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xie, Peng</creatorcontrib><creatorcontrib>Jin, Qiao</creatorcontrib><creatorcontrib>Zhang, Lingpu</creatorcontrib><creatorcontrib>Zhang, Hanchen</creatorcontrib><creatorcontrib>Montesdeoca, Nicolás</creatorcontrib><creatorcontrib>Karges, Johannes</creatorcontrib><creatorcontrib>Xiao, Haihua</creatorcontrib><creatorcontrib>Mao, Xinzhan</creatorcontrib><creatorcontrib>Song, Haiqin</creatorcontrib><creatorcontrib>Shang, Kun</creatorcontrib><title>Endowing Pt(IV) with Perfluorocarbon Chains and Human Serum Albumin Encapsulation for Highly Effective Antitumor Chemoimmunotherapy</title><title>ACS nano</title><addtitle>ACS Nano</addtitle><description>Tumor metastases and reoccurrence are considered the leading causes of cancer-associated deaths. As an emerging therapeutic method, increasing research efforts have been devoted to immunogenic cell death (ICD)-inducing compounds to solve the challenge. The clinically approved chemotherapeutic Pt complexes are not or are only poorly able to trigger ICD. Herein, the axial functionalization of the Pt(II) complex cisplatin with perfluorocarbon chains into ICD-inducing Pt(IV) prodrugs is reported. Strikingly, while the Pt(II) complex as well as the perfluorocarbon ligands did not induce ICD, the Pt(IV) prodrug demonstrated unexpectantly the induction of ICD through accumulation in the endoplasmic reticulum and generation of reactive oxygen species in this organelle. To enhance the pharmacological properties, the compound was encapsulated with human serum albumin into nanoparticles. While selectively accumulating in the tumorous tissue, the nanoparticles demonstrated a strong tumor growth inhibitory effect against osteosarcoma inside a mouse model. In vivo tumor vaccine analysis also demonstrated the ability of Pt(IV) to be an ideal ICD inducer. Overall, this study reports on axially perfluorocarbon chain-modified Pt(IV) complexes for ICD induction and chemoimmunotherapy in osteosarcoma.</description><subject>Animals</subject><subject>Antineoplastic Agents - chemistry</subject><subject>Antineoplastic Agents - pharmacology</subject><subject>Cell Line, Tumor</subject><subject>Cell Proliferation - drug effects</subject><subject>Cisplatin - chemistry</subject><subject>Cisplatin - pharmacology</subject><subject>Fluorocarbons - chemistry</subject><subject>Fluorocarbons - pharmacology</subject><subject>Humans</subject><subject>Immunogenic Cell Death - drug effects</subject><subject>Immunotherapy</subject><subject>Mice</subject><subject>Mice, Inbred BALB C</subject><subject>Nanoparticles - chemistry</subject><subject>Platinum - chemistry</subject><subject>Platinum - pharmacology</subject><subject>Prodrugs - chemistry</subject><subject>Prodrugs - pharmacology</subject><subject>Serum Albumin, Human - chemistry</subject><issn>1936-0851</issn><issn>1936-086X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kM9rFDEUx4MotlbP3iTHimybTCaZyXFZVrdQsOAPvA1J5qWTMknW_LDs2X_ckV178_QevM_3C--D0FtKrihp6LUyOagQr1pDKOPNM3ROJRMr0osfz592Ts_Qq5wfCOFd34mX6Iz1XSslEefo9zaM8dGFe3xXLm--v8ePrkz4DpKda0zRqKRjwJtJuZCxCiPeVa8C_gKperyedfUu4G0wap_rrIpbYBsT3rn7aT7grbVgivsFeB2KK9Uvp80EPjrva4hlgqT2h9fohVVzhjeneYG-fdx-3exWt58_3WzWtyvV9F1ZjUA60VvOmW6ksFRwLZVRAJzynrW60VT3mkkzKkpaqW0LQgrWWegUawDYBbo89u5T_Fkhl8G7bGCeVYBY88AI571ksmkW9PqImhRzTmCHfXJepcNAyfDX_HAyP5zML4l3p_KqPYxP_D_VC_DhCCzJ4SHWFJZf_1v3B0Oakbo</recordid><startdate>20240528</startdate><enddate>20240528</enddate><creator>Xie, Peng</creator><creator>Jin, Qiao</creator><creator>Zhang, Lingpu</creator><creator>Zhang, Hanchen</creator><creator>Montesdeoca, Nicolás</creator><creator>Karges, Johannes</creator><creator>Xiao, Haihua</creator><creator>Mao, Xinzhan</creator><creator>Song, Haiqin</creator><creator>Shang, Kun</creator><general>American Chemical Society</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>7X8</scope><orcidid>https://orcid.org/0000-0001-7622-4674</orcidid><orcidid>https://orcid.org/0000-0001-8159-8187</orcidid><orcidid>https://orcid.org/0000-0001-5258-0260</orcidid></search><sort><creationdate>20240528</creationdate><title>Endowing Pt(IV) with Perfluorocarbon Chains and Human Serum Albumin Encapsulation for Highly Effective Antitumor Chemoimmunotherapy</title><author>Xie, Peng ; Jin, Qiao ; Zhang, Lingpu ; Zhang, Hanchen ; Montesdeoca, Nicolás ; Karges, Johannes ; Xiao, Haihua ; Mao, Xinzhan ; Song, Haiqin ; Shang, Kun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-a287t-de0768f553b296f165b9acaee515834b2b1b8b39cda1049bf4e69637fe7a32ee3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Animals</topic><topic>Antineoplastic Agents - chemistry</topic><topic>Antineoplastic Agents - pharmacology</topic><topic>Cell Line, Tumor</topic><topic>Cell Proliferation - drug effects</topic><topic>Cisplatin - chemistry</topic><topic>Cisplatin - pharmacology</topic><topic>Fluorocarbons - chemistry</topic><topic>Fluorocarbons - pharmacology</topic><topic>Humans</topic><topic>Immunogenic Cell Death - drug effects</topic><topic>Immunotherapy</topic><topic>Mice</topic><topic>Mice, Inbred BALB C</topic><topic>Nanoparticles - chemistry</topic><topic>Platinum - chemistry</topic><topic>Platinum - pharmacology</topic><topic>Prodrugs - chemistry</topic><topic>Prodrugs - pharmacology</topic><topic>Serum Albumin, Human - chemistry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xie, Peng</creatorcontrib><creatorcontrib>Jin, Qiao</creatorcontrib><creatorcontrib>Zhang, Lingpu</creatorcontrib><creatorcontrib>Zhang, Hanchen</creatorcontrib><creatorcontrib>Montesdeoca, Nicolás</creatorcontrib><creatorcontrib>Karges, Johannes</creatorcontrib><creatorcontrib>Xiao, Haihua</creatorcontrib><creatorcontrib>Mao, Xinzhan</creatorcontrib><creatorcontrib>Song, Haiqin</creatorcontrib><creatorcontrib>Shang, Kun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>ACS nano</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xie, Peng</au><au>Jin, Qiao</au><au>Zhang, Lingpu</au><au>Zhang, Hanchen</au><au>Montesdeoca, Nicolás</au><au>Karges, Johannes</au><au>Xiao, Haihua</au><au>Mao, Xinzhan</au><au>Song, Haiqin</au><au>Shang, Kun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Endowing Pt(IV) with Perfluorocarbon Chains and Human Serum Albumin Encapsulation for Highly Effective Antitumor Chemoimmunotherapy</atitle><jtitle>ACS nano</jtitle><addtitle>ACS Nano</addtitle><date>2024-05-28</date><risdate>2024</risdate><volume>18</volume><issue>21</issue><spage>13683</spage><epage>13695</epage><pages>13683-13695</pages><issn>1936-0851</issn><eissn>1936-086X</eissn><abstract>Tumor metastases and reoccurrence are considered the leading causes of cancer-associated deaths. As an emerging therapeutic method, increasing research efforts have been devoted to immunogenic cell death (ICD)-inducing compounds to solve the challenge. The clinically approved chemotherapeutic Pt complexes are not or are only poorly able to trigger ICD. Herein, the axial functionalization of the Pt(II) complex cisplatin with perfluorocarbon chains into ICD-inducing Pt(IV) prodrugs is reported. Strikingly, while the Pt(II) complex as well as the perfluorocarbon ligands did not induce ICD, the Pt(IV) prodrug demonstrated unexpectantly the induction of ICD through accumulation in the endoplasmic reticulum and generation of reactive oxygen species in this organelle. To enhance the pharmacological properties, the compound was encapsulated with human serum albumin into nanoparticles. While selectively accumulating in the tumorous tissue, the nanoparticles demonstrated a strong tumor growth inhibitory effect against osteosarcoma inside a mouse model. 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subjects | Animals Antineoplastic Agents - chemistry Antineoplastic Agents - pharmacology Cell Line, Tumor Cell Proliferation - drug effects Cisplatin - chemistry Cisplatin - pharmacology Fluorocarbons - chemistry Fluorocarbons - pharmacology Humans Immunogenic Cell Death - drug effects Immunotherapy Mice Mice, Inbred BALB C Nanoparticles - chemistry Platinum - chemistry Platinum - pharmacology Prodrugs - chemistry Prodrugs - pharmacology Serum Albumin, Human - chemistry |
title | Endowing Pt(IV) with Perfluorocarbon Chains and Human Serum Albumin Encapsulation for Highly Effective Antitumor Chemoimmunotherapy |
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