Insight into the antitumor activity of carbosilane Cu()-metallodendrimers through their interaction with biological membrane models
Current cancer therapies present serious drawbacks including severe side-effects and development of drug resistance. Strategies based on nanosized metallodrugs combine the structural diversity and non-classical modes of action of metal complexes with the selectivity arising from the unique interacti...
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| Veröffentlicht in: | Nanoscale 2019-07, Vol.11 (28), p.1333-13342 |
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| creator | Sanz del Olmo, Natalia Carloni, Riccardo Bajo, Ana M Ortega, Paula Fattori, Alberto Gómez, Rafael Ottaviani, Maria Francesca García-Gallego, Sandra Cangiotti, Michela de la Mata, F. Javier |
| description | Current cancer therapies present serious drawbacks including severe side-effects and development of drug resistance. Strategies based on nanosized metallodrugs combine the structural diversity and non-classical modes of action of metal complexes with the selectivity arising from the unique interaction of nanoparticles with biological membranes. A new family of water-soluble copper(
ii
) carbosilane metallodendrimers was synthesized and characterized as a nanotechnological alternative to current therapies. The interactions occurring over time between the dendrimers, at different generations (G
0
to G
2
) and with different Cu(
ii
) counter-ions (nitrate
vs.
chloride), and cell-membrane models (cethyl-trimethylammonium bromide (CTAB) micelles and lecithin liposomes) were investigated using a computer-aided analysis of the electron paramagnetic resonance (EPR) spectra. The EPR analysis provided structural and dynamical information on the systems indicating that the increase in generation and the change of the Cu(
ii
) contra-ion - from nitrate to chloride - produce an increased relative amount and strength of interaction of the dendrimer with the model membranes. Interestingly, the stabilization effect produced a lower toxicity towards cancer cells. The cytotoxic effect of Cu(
ii
) metallodendrimers was verified by an
in vitro
screening in a selection of tumor cell lines, revealing the impact of multivalency on the effectivity and selectivity of the metallodrugs. As a proof-of-concept, first-generation dendrimer G
1
-Cu(ONO
2
)
2
was selected for in-depth
in vitro
and
in vivo
antitumor evaluation towards resistant prostate cancer. The Cu(
ii
)-metallodendrimers produced a significant tumor size reduction with no signs of toxicity during the experiment, confirming their promising potential as anticancer metallodrugs.
We present a new family of water-soluble copper(
ii
) carbosilane metallodendrimers. The combined experimental and theoretical analysis reveals that they display different interactions with model membranes, which also dictate their antitumor behavior. |
| doi_str_mv | 10.1039/c9nr03313k |
| format | Article |
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ii
) carbosilane metallodendrimers was synthesized and characterized as a nanotechnological alternative to current therapies. The interactions occurring over time between the dendrimers, at different generations (G
0
to G
2
) and with different Cu(
ii
) counter-ions (nitrate
vs.
chloride), and cell-membrane models (cethyl-trimethylammonium bromide (CTAB) micelles and lecithin liposomes) were investigated using a computer-aided analysis of the electron paramagnetic resonance (EPR) spectra. The EPR analysis provided structural and dynamical information on the systems indicating that the increase in generation and the change of the Cu(
ii
) contra-ion - from nitrate to chloride - produce an increased relative amount and strength of interaction of the dendrimer with the model membranes. Interestingly, the stabilization effect produced a lower toxicity towards cancer cells. The cytotoxic effect of Cu(
ii
) metallodendrimers was verified by an
in vitro
screening in a selection of tumor cell lines, revealing the impact of multivalency on the effectivity and selectivity of the metallodrugs. As a proof-of-concept, first-generation dendrimer G
1
-Cu(ONO
2
)
2
was selected for in-depth
in vitro
and
in vivo
antitumor evaluation towards resistant prostate cancer. The Cu(
ii
)-metallodendrimers produced a significant tumor size reduction with no signs of toxicity during the experiment, confirming their promising potential as anticancer metallodrugs.
We present a new family of water-soluble copper(
ii
) carbosilane metallodendrimers. The combined experimental and theoretical analysis reveals that they display different interactions with model membranes, which also dictate their antitumor behavior.</description><identifier>ISSN: 2040-3364</identifier><identifier>EISSN: 2040-3372</identifier><identifier>DOI: 10.1039/c9nr03313k</identifier><identifier>PMID: 31271405</identifier><language>eng</language><publisher>England: Royal Society of Chemistry</publisher><subject>Animals ; Anticancer properties ; Antineoplastic Agents ; Biocompatibility ; Cancer ; Cell Membrane - metabolism ; Cell Membrane - pathology ; Cetyltrimethylammonium bromide ; Coordination compounds ; Copper ; Copper - chemistry ; Copper - pharmacology ; Copper compounds ; Cytotoxins - chemistry ; Cytotoxins - pharmacology ; Dendrimers ; Dendrimers - chemistry ; Dendrimers - pharmacology ; Electron paramagnetic resonance ; Humans ; Lecithin ; Liposomes ; Male ; MCF-7 Cells ; Membranes ; Mice ; Mice, Nude ; Micelles ; Models, Biological ; Nanoparticles ; Neoplasms, Experimental - drug therapy ; Neoplasms, Experimental - metabolism ; Neoplasms, Experimental - pathology ; PC-3 Cells ; Prostate ; Selectivity ; Silanes - chemistry ; Silanes - pharmacology ; Size reduction ; Toxicity ; Tumors ; Xenograft Model Antitumor Assays</subject><ispartof>Nanoscale, 2019-07, Vol.11 (28), p.1333-13342</ispartof><rights>Copyright Royal Society of Chemistry 2019</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c400t-31bf73c319e000db8d95abe9f2cc22cbd4fa8b3e4e7444445a12b85be54e11c93</citedby><cites>FETCH-LOGICAL-c400t-31bf73c319e000db8d95abe9f2cc22cbd4fa8b3e4e7444445a12b85be54e11c93</cites><orcidid>0000-0001-8052-213X ; 0000-0003-0377-5429 ; 0000-0001-6112-0450 ; 0000-0003-0418-3935 ; 0000-0001-6448-2414 ; 0000-0001-9946-8073</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,777,781,27905,27906</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31271405$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Sanz del Olmo, Natalia</creatorcontrib><creatorcontrib>Carloni, Riccardo</creatorcontrib><creatorcontrib>Bajo, Ana M</creatorcontrib><creatorcontrib>Ortega, Paula</creatorcontrib><creatorcontrib>Fattori, Alberto</creatorcontrib><creatorcontrib>Gómez, Rafael</creatorcontrib><creatorcontrib>Ottaviani, Maria Francesca</creatorcontrib><creatorcontrib>García-Gallego, Sandra</creatorcontrib><creatorcontrib>Cangiotti, Michela</creatorcontrib><creatorcontrib>de la Mata, F. Javier</creatorcontrib><title>Insight into the antitumor activity of carbosilane Cu()-metallodendrimers through their interaction with biological membrane models</title><title>Nanoscale</title><addtitle>Nanoscale</addtitle><description>Current cancer therapies present serious drawbacks including severe side-effects and development of drug resistance. Strategies based on nanosized metallodrugs combine the structural diversity and non-classical modes of action of metal complexes with the selectivity arising from the unique interaction of nanoparticles with biological membranes. A new family of water-soluble copper(
ii
) carbosilane metallodendrimers was synthesized and characterized as a nanotechnological alternative to current therapies. The interactions occurring over time between the dendrimers, at different generations (G
0
to G
2
) and with different Cu(
ii
) counter-ions (nitrate
vs.
chloride), and cell-membrane models (cethyl-trimethylammonium bromide (CTAB) micelles and lecithin liposomes) were investigated using a computer-aided analysis of the electron paramagnetic resonance (EPR) spectra. The EPR analysis provided structural and dynamical information on the systems indicating that the increase in generation and the change of the Cu(
ii
) contra-ion - from nitrate to chloride - produce an increased relative amount and strength of interaction of the dendrimer with the model membranes. Interestingly, the stabilization effect produced a lower toxicity towards cancer cells. The cytotoxic effect of Cu(
ii
) metallodendrimers was verified by an
in vitro
screening in a selection of tumor cell lines, revealing the impact of multivalency on the effectivity and selectivity of the metallodrugs. As a proof-of-concept, first-generation dendrimer G
1
-Cu(ONO
2
)
2
was selected for in-depth
in vitro
and
in vivo
antitumor evaluation towards resistant prostate cancer. The Cu(
ii
)-metallodendrimers produced a significant tumor size reduction with no signs of toxicity during the experiment, confirming their promising potential as anticancer metallodrugs.
We present a new family of water-soluble copper(
ii
) carbosilane metallodendrimers. The combined experimental and theoretical analysis reveals that they display different interactions with model membranes, which also dictate their antitumor behavior.</description><subject>Animals</subject><subject>Anticancer properties</subject><subject>Antineoplastic Agents</subject><subject>Biocompatibility</subject><subject>Cancer</subject><subject>Cell Membrane - metabolism</subject><subject>Cell Membrane - pathology</subject><subject>Cetyltrimethylammonium bromide</subject><subject>Coordination compounds</subject><subject>Copper</subject><subject>Copper - chemistry</subject><subject>Copper - pharmacology</subject><subject>Copper compounds</subject><subject>Cytotoxins - chemistry</subject><subject>Cytotoxins - pharmacology</subject><subject>Dendrimers</subject><subject>Dendrimers - chemistry</subject><subject>Dendrimers - pharmacology</subject><subject>Electron paramagnetic resonance</subject><subject>Humans</subject><subject>Lecithin</subject><subject>Liposomes</subject><subject>Male</subject><subject>MCF-7 Cells</subject><subject>Membranes</subject><subject>Mice</subject><subject>Mice, Nude</subject><subject>Micelles</subject><subject>Models, Biological</subject><subject>Nanoparticles</subject><subject>Neoplasms, Experimental - drug therapy</subject><subject>Neoplasms, Experimental - metabolism</subject><subject>Neoplasms, Experimental - pathology</subject><subject>PC-3 Cells</subject><subject>Prostate</subject><subject>Selectivity</subject><subject>Silanes - chemistry</subject><subject>Silanes - pharmacology</subject><subject>Size reduction</subject><subject>Toxicity</subject><subject>Tumors</subject><subject>Xenograft Model Antitumor Assays</subject><issn>2040-3364</issn><issn>2040-3372</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kc1LwzAYh4MoOj8u3pWIFxWq-WjX5SjFj-FQED2XJH27ZbbNTFLFs_-4rdN5M5cEfs_7hPyC0D4l55RwcaFF4wjnlL-soQEjMYk4T9n66jyMt9C293NChoIP-Sba4pSlNCbJAH2OG2-ms4BNEywOM8CyCSa0tXVY6mDeTPjAtsRaOmW9qWQDOGtPTqMagqwqW0BTOFOD892ws-101kuM633geoNt8LsJM6yMrezUaFnhGmrlelPdzVd-F22UsvKw97PvoOfrq6fsNpo83Iyzy0mkY0JCxKkqU645FUAIKdSoEIlUIEqmNWNaFXEpR4pDDGncr0RSpkaJgiQGSrXgO-h46V04-9qCD_nctq7prswZSwRLUp6SjjpbUtpZ7x2U-aJ7oHQfOSV533eeifvH777vOvjwR9mqGooV-ltwBxwsAef1Kv37sC4_-i_PF0XJvwBI-pNq</recordid><startdate>20190728</startdate><enddate>20190728</enddate><creator>Sanz del Olmo, Natalia</creator><creator>Carloni, Riccardo</creator><creator>Bajo, Ana M</creator><creator>Ortega, Paula</creator><creator>Fattori, Alberto</creator><creator>Gómez, Rafael</creator><creator>Ottaviani, Maria Francesca</creator><creator>García-Gallego, Sandra</creator><creator>Cangiotti, Michela</creator><creator>de la Mata, F. Javier</creator><general>Royal Society of Chemistry</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>7SR</scope><scope>7U5</scope><scope>8BQ</scope><scope>8FD</scope><scope>F28</scope><scope>FR3</scope><scope>JG9</scope><scope>L7M</scope><orcidid>https://orcid.org/0000-0001-8052-213X</orcidid><orcidid>https://orcid.org/0000-0003-0377-5429</orcidid><orcidid>https://orcid.org/0000-0001-6112-0450</orcidid><orcidid>https://orcid.org/0000-0003-0418-3935</orcidid><orcidid>https://orcid.org/0000-0001-6448-2414</orcidid><orcidid>https://orcid.org/0000-0001-9946-8073</orcidid></search><sort><creationdate>20190728</creationdate><title>Insight into the antitumor activity of carbosilane Cu()-metallodendrimers through their interaction with biological membrane models</title><author>Sanz del Olmo, Natalia ; Carloni, Riccardo ; Bajo, Ana M ; Ortega, Paula ; Fattori, Alberto ; Gómez, Rafael ; Ottaviani, Maria Francesca ; García-Gallego, Sandra ; Cangiotti, Michela ; de la Mata, F. Javier</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c400t-31bf73c319e000db8d95abe9f2cc22cbd4fa8b3e4e7444445a12b85be54e11c93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Animals</topic><topic>Anticancer properties</topic><topic>Antineoplastic Agents</topic><topic>Biocompatibility</topic><topic>Cancer</topic><topic>Cell Membrane - metabolism</topic><topic>Cell Membrane - pathology</topic><topic>Cetyltrimethylammonium bromide</topic><topic>Coordination compounds</topic><topic>Copper</topic><topic>Copper - chemistry</topic><topic>Copper - pharmacology</topic><topic>Copper compounds</topic><topic>Cytotoxins - chemistry</topic><topic>Cytotoxins - pharmacology</topic><topic>Dendrimers</topic><topic>Dendrimers - chemistry</topic><topic>Dendrimers - pharmacology</topic><topic>Electron paramagnetic resonance</topic><topic>Humans</topic><topic>Lecithin</topic><topic>Liposomes</topic><topic>Male</topic><topic>MCF-7 Cells</topic><topic>Membranes</topic><topic>Mice</topic><topic>Mice, Nude</topic><topic>Micelles</topic><topic>Models, Biological</topic><topic>Nanoparticles</topic><topic>Neoplasms, Experimental - drug therapy</topic><topic>Neoplasms, Experimental - metabolism</topic><topic>Neoplasms, Experimental - pathology</topic><topic>PC-3 Cells</topic><topic>Prostate</topic><topic>Selectivity</topic><topic>Silanes - chemistry</topic><topic>Silanes - pharmacology</topic><topic>Size reduction</topic><topic>Toxicity</topic><topic>Tumors</topic><topic>Xenograft Model Antitumor Assays</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Sanz del Olmo, Natalia</creatorcontrib><creatorcontrib>Carloni, Riccardo</creatorcontrib><creatorcontrib>Bajo, Ana M</creatorcontrib><creatorcontrib>Ortega, Paula</creatorcontrib><creatorcontrib>Fattori, Alberto</creatorcontrib><creatorcontrib>Gómez, Rafael</creatorcontrib><creatorcontrib>Ottaviani, Maria Francesca</creatorcontrib><creatorcontrib>García-Gallego, Sandra</creatorcontrib><creatorcontrib>Cangiotti, Michela</creatorcontrib><creatorcontrib>de la Mata, F. Javier</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Engineered Materials Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Materials Research Database</collection><collection>Advanced Technologies Database with Aerospace</collection><jtitle>Nanoscale</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Sanz del Olmo, Natalia</au><au>Carloni, Riccardo</au><au>Bajo, Ana M</au><au>Ortega, Paula</au><au>Fattori, Alberto</au><au>Gómez, Rafael</au><au>Ottaviani, Maria Francesca</au><au>García-Gallego, Sandra</au><au>Cangiotti, Michela</au><au>de la Mata, F. Javier</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Insight into the antitumor activity of carbosilane Cu()-metallodendrimers through their interaction with biological membrane models</atitle><jtitle>Nanoscale</jtitle><addtitle>Nanoscale</addtitle><date>2019-07-28</date><risdate>2019</risdate><volume>11</volume><issue>28</issue><spage>1333</spage><epage>13342</epage><pages>1333-13342</pages><issn>2040-3364</issn><eissn>2040-3372</eissn><abstract>Current cancer therapies present serious drawbacks including severe side-effects and development of drug resistance. Strategies based on nanosized metallodrugs combine the structural diversity and non-classical modes of action of metal complexes with the selectivity arising from the unique interaction of nanoparticles with biological membranes. A new family of water-soluble copper(
ii
) carbosilane metallodendrimers was synthesized and characterized as a nanotechnological alternative to current therapies. The interactions occurring over time between the dendrimers, at different generations (G
0
to G
2
) and with different Cu(
ii
) counter-ions (nitrate
vs.
chloride), and cell-membrane models (cethyl-trimethylammonium bromide (CTAB) micelles and lecithin liposomes) were investigated using a computer-aided analysis of the electron paramagnetic resonance (EPR) spectra. The EPR analysis provided structural and dynamical information on the systems indicating that the increase in generation and the change of the Cu(
ii
) contra-ion - from nitrate to chloride - produce an increased relative amount and strength of interaction of the dendrimer with the model membranes. Interestingly, the stabilization effect produced a lower toxicity towards cancer cells. The cytotoxic effect of Cu(
ii
) metallodendrimers was verified by an
in vitro
screening in a selection of tumor cell lines, revealing the impact of multivalency on the effectivity and selectivity of the metallodrugs. As a proof-of-concept, first-generation dendrimer G
1
-Cu(ONO
2
)
2
was selected for in-depth
in vitro
and
in vivo
antitumor evaluation towards resistant prostate cancer. The Cu(
ii
)-metallodendrimers produced a significant tumor size reduction with no signs of toxicity during the experiment, confirming their promising potential as anticancer metallodrugs.
We present a new family of water-soluble copper(
ii
) carbosilane metallodendrimers. The combined experimental and theoretical analysis reveals that they display different interactions with model membranes, which also dictate their antitumor behavior.</abstract><cop>England</cop><pub>Royal Society of Chemistry</pub><pmid>31271405</pmid><doi>10.1039/c9nr03313k</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0001-8052-213X</orcidid><orcidid>https://orcid.org/0000-0003-0377-5429</orcidid><orcidid>https://orcid.org/0000-0001-6112-0450</orcidid><orcidid>https://orcid.org/0000-0003-0418-3935</orcidid><orcidid>https://orcid.org/0000-0001-6448-2414</orcidid><orcidid>https://orcid.org/0000-0001-9946-8073</orcidid></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 2040-3364 |
| ispartof | Nanoscale, 2019-07, Vol.11 (28), p.1333-13342 |
| issn | 2040-3364 2040-3372 |
| language | eng |
| recordid | cdi_rsc_primary_c9nr03313k |
| source | MEDLINE; Royal Society Of Chemistry Journals 2008- |
| subjects | Animals Anticancer properties Antineoplastic Agents Biocompatibility Cancer Cell Membrane - metabolism Cell Membrane - pathology Cetyltrimethylammonium bromide Coordination compounds Copper Copper - chemistry Copper - pharmacology Copper compounds Cytotoxins - chemistry Cytotoxins - pharmacology Dendrimers Dendrimers - chemistry Dendrimers - pharmacology Electron paramagnetic resonance Humans Lecithin Liposomes Male MCF-7 Cells Membranes Mice Mice, Nude Micelles Models, Biological Nanoparticles Neoplasms, Experimental - drug therapy Neoplasms, Experimental - metabolism Neoplasms, Experimental - pathology PC-3 Cells Prostate Selectivity Silanes - chemistry Silanes - pharmacology Size reduction Toxicity Tumors Xenograft Model Antitumor Assays |
| title | Insight into the antitumor activity of carbosilane Cu()-metallodendrimers through their interaction with biological membrane models |
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