Mechanistic insights on the mode of action of an antiproliferative thiosemicarbazone-nickel complex revealed by an integrated chemogenomic profiling study.
Identifieur interne : 000048 ( Main/Exploration ); précédent : 000047; suivant : 000049Mechanistic insights on the mode of action of an antiproliferative thiosemicarbazone-nickel complex revealed by an integrated chemogenomic profiling study.
Auteurs : Enrico Baruffini [Italie] ; Roberta Ruotolo [Italie] ; Franco Bisceglie [Italie] ; Serena Montalbano [Italie] ; Simone Ottonello [Italie] ; Giorgio Pelosi [Italie] ; Annamaria Buschini [Italie] ; Tiziana Lodi [Italie]Source :
- Scientific reports [ 2045-2322 ] ; 2020.
Abstract
Thiosemicarbazones (TSC) and their metal complexes display diverse biological activities and are active against multiple pathological conditions ranging from microbial infections to abnormal cell proliferation. Ribonucleotide reductase (RNR) is considered one of the main targets of TSCs, yet, the existence of additional targets, differently responsible for the multifaceted activities of TSCs and their metal complexes has been proposed. To set the basis for a more comprehensive delineation of their mode of action, we chemogenomically profiled the cellular effects of bis(citronellalthiosemicarbazonato)nickel(II) [Ni(S-tcitr)2] using the unicellular eukaryote Saccharomyces cerevisiae as a model organism. Two complementary genomic phenotyping screens led to the identification of 269 sensitive and 56 tolerant deletion mutant strains and of 14 genes that when overexpressed make yeast cells resistant to an otherwise lethal concentration of Ni(S-tcitr)2. Chromatin remodeling, cytoskeleton organization, mitochondrial function and iron metabolism were identified as lead cellular processes responsible for Ni(S-tcitr)2 toxicity. The latter process, and particularly glutaredoxin-mediated iron loading of RNR, was found to be affected by Ni(S-tcitr)2. Given the multiple pathways regulated by glutaredoxins, targeting of these proteins by Ni(S-tcitr)2 can negatively affect various core cellular processes that may critically contribute to Ni(S-tcitr)2 cytotoxicity.
DOI: 10.1038/s41598-020-67439-y
PubMed: 32601343
PubMed Central: PMC7324377
Affiliations:
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first="Roberta" last="Ruotolo">Roberta Ruotolo</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author><author><name sortKey="Bisceglie, Franco" sort="Bisceglie, Franco" uniqKey="Bisceglie F" first="Franco" last="Bisceglie">Franco Bisceglie</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author><author><name sortKey="Montalbano, Serena" sort="Montalbano, Serena" uniqKey="Montalbano S" first="Serena" last="Montalbano">Serena Montalbano</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author><author><name sortKey="Ottonello, Simone" sort="Ottonello, Simone" uniqKey="Ottonello S" first="Simone" last="Ottonello">Simone Ottonello</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author><author><name sortKey="Pelosi, Giorgio" sort="Pelosi, Giorgio" uniqKey="Pelosi G" first="Giorgio" last="Pelosi">Giorgio Pelosi</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author><author><name sortKey="Buschini, Annamaria" sort="Buschini, Annamaria" uniqKey="Buschini A" first="Annamaria" last="Buschini">Annamaria Buschini</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy. annamaria.buschini@unipr.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author><author><name sortKey="Lodi, Tiziana" sort="Lodi, Tiziana" uniqKey="Lodi T" first="Tiziana" last="Lodi">Tiziana Lodi</name><affiliation wicri:level="1"><nlm:affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy. tiziana.lodi@unipr.it.</nlm:affiliation><country xml:lang="fr">Italie</country><wicri:regionArea>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma</wicri:regionArea><wicri:noRegion>Parma</wicri:noRegion></affiliation></author></analytic><series><title level="j">Scientific reports</title><idno type="eISSN">2045-2322</idno><imprint><date when="2020" type="published">2020</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Thiosemicarbazones (TSC) and their metal complexes display diverse biological activities and are active against multiple pathological conditions ranging from microbial infections to abnormal cell proliferation. Ribonucleotide reductase (RNR) is considered one of the main targets of TSCs, yet, the existence of additional targets, differently responsible for the multifaceted activities of TSCs and their metal complexes has been proposed. To set the basis for a more comprehensive delineation of their mode of action, we chemogenomically profiled the cellular effects of bis(citronellalthiosemicarbazonato)nickel(II) [Ni(S-tcitr)<sub>2</sub>] using the unicellular eukaryote Saccharomyces cerevisiae as a model organism. Two complementary genomic phenotyping screens led to the identification of 269 sensitive and 56 tolerant deletion mutant strains and of 14 genes that when overexpressed make yeast cells resistant to an otherwise lethal concentration of Ni(S-tcitr)<sub>2</sub>. Chromatin remodeling, cytoskeleton organization, mitochondrial function and iron metabolism were identified as lead cellular processes responsible for Ni(S-tcitr)<sub>2</sub> toxicity. The latter process, and particularly glutaredoxin-mediated iron loading of RNR, was found to be affected by Ni(S-tcitr)<sub>2</sub>. Given the multiple pathways regulated by glutaredoxins, targeting of these proteins by Ni(S-tcitr)<sub>2</sub> can negatively affect various core cellular processes that may critically contribute to Ni(S-tcitr)<sub>2</sub> cytotoxicity.</div></front></TEI><pubmed><MedlineCitation Status="In-Process" Owner="NLM"><PMID Version="1">32601343</PMID><DateRevised><Year>2020</Year><Month>10</Month><Day>15</Day></DateRevised><Article PubModel="Electronic"><Journal><ISSN IssnType="Electronic">2045-2322</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>1</Issue><PubDate><Year>2020</Year><Month>06</Month><Day>29</Day></PubDate></JournalIssue><Title>Scientific reports</Title><ISOAbbreviation>Sci Rep</ISOAbbreviation></Journal><ArticleTitle>Mechanistic insights on the mode of action of an antiproliferative thiosemicarbazone-nickel complex revealed by an integrated chemogenomic profiling study.</ArticleTitle><Pagination><MedlinePgn>10524</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.1038/s41598-020-67439-y</ELocationID><Abstract><AbstractText>Thiosemicarbazones (TSC) and their metal complexes display diverse biological activities and are active against multiple pathological conditions ranging from microbial infections to abnormal cell proliferation. Ribonucleotide reductase (RNR) is considered one of the main targets of TSCs, yet, the existence of additional targets, differently responsible for the multifaceted activities of TSCs and their metal complexes has been proposed. To set the basis for a more comprehensive delineation of their mode of action, we chemogenomically profiled the cellular effects of bis(citronellalthiosemicarbazonato)nickel(II) [Ni(S-tcitr)<sub>2</sub>] using the unicellular eukaryote Saccharomyces cerevisiae as a model organism. Two complementary genomic phenotyping screens led to the identification of 269 sensitive and 56 tolerant deletion mutant strains and of 14 genes that when overexpressed make yeast cells resistant to an otherwise lethal concentration of Ni(S-tcitr)<sub>2</sub>. Chromatin remodeling, cytoskeleton organization, mitochondrial function and iron metabolism were identified as lead cellular processes responsible for Ni(S-tcitr)<sub>2</sub> toxicity. The latter process, and particularly glutaredoxin-mediated iron loading of RNR, was found to be affected by Ni(S-tcitr)<sub>2</sub>. Given the multiple pathways regulated by glutaredoxins, targeting of these proteins by Ni(S-tcitr)<sub>2</sub> can negatively affect various core cellular processes that may critically contribute to Ni(S-tcitr)<sub>2</sub> cytotoxicity.</AbstractText></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Baruffini</LastName><ForeName>Enrico</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ruotolo</LastName><ForeName>Roberta</ForeName><Initials>R</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Bisceglie</LastName><ForeName>Franco</ForeName><Initials>F</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Montalbano</LastName><ForeName>Serena</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Ottonello</LastName><ForeName>Simone</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Pelosi</LastName><ForeName>Giorgio</ForeName><Initials>G</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Buschini</LastName><ForeName>Annamaria</ForeName><Initials>A</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy. annamaria.buschini@unipr.it.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Lodi</LastName><ForeName>Tiziana</ForeName><Initials>T</Initials><AffiliationInfo><Affiliation>Department of Chemistry, Life Sciences and Environmental Sustainability, University of Parma, Parco Area Delle Scienze, 11/A, 43124, Parma, Italy. tiziana.lodi@unipr.it.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType><PublicationType UI="D013485">Research Support, Non-U.S. Gov't</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>06</Month><Day>29</Day></ArticleDate></Article><MedlineJournalInfo><Country>England</Country><MedlineTA>Sci Rep</MedlineTA><NlmUniqueID>101563288</NlmUniqueID><ISSNLinking>2045-2322</ISSNLinking></MedlineJournalInfo><CitationSubset>IM</CitationSubset></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>01</Month><Day>15</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>06</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>7</Month><Day>1</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate 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sortKey="Bisceglie, Franco" sort="Bisceglie, Franco" uniqKey="Bisceglie F" first="Franco" last="Bisceglie">Franco Bisceglie</name><name sortKey="Buschini, Annamaria" sort="Buschini, Annamaria" uniqKey="Buschini A" first="Annamaria" last="Buschini">Annamaria Buschini</name><name sortKey="Lodi, Tiziana" sort="Lodi, Tiziana" uniqKey="Lodi T" first="Tiziana" last="Lodi">Tiziana Lodi</name><name sortKey="Montalbano, Serena" sort="Montalbano, Serena" uniqKey="Montalbano S" first="Serena" last="Montalbano">Serena Montalbano</name><name sortKey="Ottonello, Simone" sort="Ottonello, Simone" uniqKey="Ottonello S" first="Simone" last="Ottonello">Simone Ottonello</name><name sortKey="Pelosi, Giorgio" sort="Pelosi, Giorgio" uniqKey="Pelosi G" first="Giorgio" last="Pelosi">Giorgio Pelosi</name><name sortKey="Ruotolo, Roberta" sort="Ruotolo, Roberta" uniqKey="Ruotolo R" first="Roberta" last="Ruotolo">Roberta Ruotolo</name></country></tree></affiliations></record>Pour manipuler ce document sous Unix 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