The cytotoxicity of gallium maltolate in glioblastoma cells is enhanced by metformin through combined action on mitochondrial complex 1.
Identifieur interne : 000019 ( Main/Exploration ); précédent : 000018; suivant : 000020The cytotoxicity of gallium maltolate in glioblastoma cells is enhanced by metformin through combined action on mitochondrial complex 1.
Auteurs : Hisham S. Alhajala [États-Unis] ; John L. Markley [États-Unis] ; Jin Hae Kim [États-Unis] ; Mona M. Al-Gizawiy [États-Unis] ; Kathleen M. Schmainda [États-Unis] ; John S. Kuo [États-Unis] ; Christopher R. Chitambar [États-Unis]Source :
- Oncotarget [ 1949-2553 ] ; 2020.
Abstract
New drugs are needed for glioblastoma, an aggressive brain tumor with a dismal prognosis. We recently reported that gallium maltolate (GaM) retards the growth of glioblastoma in a rat orthotopic brain tumor model by inhibiting mitochondrial function and iron-dependent ribonucleotide reductase (RR). However, GaM's mechanism of action at the mitochondrial level is not known. Given the interaction between gallium and iron metabolism, we hypothesized that gallium might target iron-sulfur (Fe-S) cluster-containing mitochondrial proteins. Using Extracellular Flux Analyzer technology, we confirmed that after a 24-h incubation, GaM 50 μmol/L inhibited glioblastoma cell growth by <10% but inhibited cellular oxygen consumption rate by 44% and abrogated mitochondrial reserve capacity. GaM blocked mitochondrial complex I activity and produced a 2.9-fold increase in cellular ROS. NMR spectroscopy revealed that gallium binds to IscU, the bacterial scaffold protein for Fe-S cluster assembly and stabilizes its folded state. Gallium inhibited the rate of in vitro cluster assembly catalyzed by bacterial cysteine desulfurase in a reaction mixture containing IscU, Fe (II), DTT, and L-cysteine. Metformin, a complex I inhibitor, enhanced GaM's inhibition of complex I, further increased cellular ROS levels, and synergistically enhanced GaM's cytotoxicity in glioblastoma cells in 2-D and 3-D cultures. Metformin did not affect GaM action on cellular iron uptake or transferrin receptor1 expression nor did it enhance the cytotoxicity of the RR inhibitor Didox. Our results show that GaM inhibits complex I by disrupting iron-sulfur cluster assembly and that its cytotoxicity can be synergistically enhanced by metformin through combined action on complex I.
DOI: 10.18632/oncotarget.27567
PubMed: 32391122
PubMed Central: PMC7197450
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Alhajala</name><affiliation wicri:level="2"><nlm:affiliation>Division of Hematology and Oncology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Hematology and Oncology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Markley, John L" sort="Markley, John L" uniqKey="Markley J" first="John L" last="Markley">John L. Markley</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Kim, Jin Hae" sort="Kim, Jin Hae" uniqKey="Kim J" first="Jin Hae" last="Kim">Jin Hae Kim</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Al Gizawiy, Mona M" sort="Al Gizawiy, Mona M" uniqKey="Al Gizawiy M" first="Mona M" last="Al-Gizawiy">Mona M. Al-Gizawiy</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Schmainda, Kathleen M" sort="Schmainda, Kathleen M" uniqKey="Schmainda K" first="Kathleen M" last="Schmainda">Kathleen M. Schmainda</name><affiliation wicri:level="2"><nlm:affiliation>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author><author><name sortKey="Kuo, John S" sort="Kuo, John S" uniqKey="Kuo J" first="John S" last="Kuo">John S. Kuo</name><affiliation wicri:level="2"><nlm:affiliation>Department of Neurosurgery and Mulva Clinic for the Neurosciences, Dell Medical School, Austin, Texas, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Neurosurgery and Mulva Clinic for the Neurosciences, Dell Medical School, Austin, Texas</wicri:regionArea><placeName><region type="state">Texas</region></placeName></affiliation></author><author><name sortKey="Chitambar, Christopher R" sort="Chitambar, Christopher R" uniqKey="Chitambar C" first="Christopher R" last="Chitambar">Christopher R. Chitambar</name><affiliation wicri:level="2"><nlm:affiliation>Division of Hematology and Oncology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Division of Hematology and Oncology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation><affiliation wicri:level="2"><nlm:affiliation>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</nlm:affiliation><country xml:lang="fr">États-Unis</country><wicri:regionArea>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin</wicri:regionArea><placeName><region type="state">Wisconsin</region></placeName></affiliation></author></analytic><series><title level="j">Oncotarget</title><idno type="eISSN">1949-2553</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">New drugs are needed for glioblastoma, an aggressive brain tumor with a dismal prognosis. We recently reported that gallium maltolate (GaM) retards the growth of glioblastoma in a rat orthotopic brain tumor model by inhibiting mitochondrial function and iron-dependent ribonucleotide reductase (RR). However, GaM's mechanism of action at the mitochondrial level is not known. Given the interaction between gallium and iron metabolism, we hypothesized that gallium might target iron-sulfur (Fe-S) cluster-containing mitochondrial proteins. Using Extracellular Flux Analyzer technology, we confirmed that after a 24-h incubation, GaM 50 μmol/L inhibited glioblastoma cell growth by <10% but inhibited cellular oxygen consumption rate by 44% and abrogated mitochondrial reserve capacity. GaM blocked mitochondrial complex I activity and produced a 2.9-fold increase in cellular ROS. NMR spectroscopy revealed that gallium binds to IscU, the bacterial scaffold protein for Fe-S cluster assembly and stabilizes its folded state. Gallium inhibited the rate of <i>in vitro</i> cluster assembly catalyzed by bacterial cysteine desulfurase in a reaction mixture containing IscU, Fe (II), DTT, and L-cysteine. Metformin, a complex I inhibitor, enhanced GaM's inhibition of complex I, further increased cellular ROS levels, and synergistically enhanced GaM's cytotoxicity in glioblastoma cells in 2-D and 3-D cultures. Metformin did not affect GaM action on cellular iron uptake or transferrin receptor1 expression nor did it enhance the cytotoxicity of the RR inhibitor Didox. Our results show that GaM inhibits complex I by disrupting iron-sulfur cluster assembly and that its cytotoxicity can be synergistically enhanced by metformin through combined action on complex I.</div></front></TEI><pubmed><MedlineCitation Status="PubMed-not-MEDLINE" Owner="NLM"><PMID Version="1">32391122</PMID><DateRevised><Year>2020</Year><Month>05</Month><Day>15</Day></DateRevised><Article PubModel="Electronic-eCollection"><Journal><ISSN IssnType="Electronic">1949-2553</ISSN><JournalIssue CitedMedium="Internet"><Volume>11</Volume><Issue>17</Issue><PubDate><Year>2020</Year><Month>Apr</Month><Day>28</Day></PubDate></JournalIssue><Title>Oncotarget</Title><ISOAbbreviation>Oncotarget</ISOAbbreviation></Journal><ArticleTitle>The cytotoxicity of gallium maltolate in glioblastoma cells is enhanced by metformin through combined action on mitochondrial complex 1.</ArticleTitle><Pagination><MedlinePgn>1531-1544</MedlinePgn></Pagination><ELocationID EIdType="doi" ValidYN="Y">10.18632/oncotarget.27567</ELocationID><Abstract><AbstractText>New drugs are needed for glioblastoma, an aggressive brain tumor with a dismal prognosis. We recently reported that gallium maltolate (GaM) retards the growth of glioblastoma in a rat orthotopic brain tumor model by inhibiting mitochondrial function and iron-dependent ribonucleotide reductase (RR). However, GaM's mechanism of action at the mitochondrial level is not known. Given the interaction between gallium and iron metabolism, we hypothesized that gallium might target iron-sulfur (Fe-S) cluster-containing mitochondrial proteins. Using Extracellular Flux Analyzer technology, we confirmed that after a 24-h incubation, GaM 50 μmol/L inhibited glioblastoma cell growth by <10% but inhibited cellular oxygen consumption rate by 44% and abrogated mitochondrial reserve capacity. GaM blocked mitochondrial complex I activity and produced a 2.9-fold increase in cellular ROS. NMR spectroscopy revealed that gallium binds to IscU, the bacterial scaffold protein for Fe-S cluster assembly and stabilizes its folded state. Gallium inhibited the rate of <i>in vitro</i> cluster assembly catalyzed by bacterial cysteine desulfurase in a reaction mixture containing IscU, Fe (II), DTT, and L-cysteine. Metformin, a complex I inhibitor, enhanced GaM's inhibition of complex I, further increased cellular ROS levels, and synergistically enhanced GaM's cytotoxicity in glioblastoma cells in 2-D and 3-D cultures. Metformin did not affect GaM action on cellular iron uptake or transferrin receptor1 expression nor did it enhance the cytotoxicity of the RR inhibitor Didox. Our results show that GaM inhibits complex I by disrupting iron-sulfur cluster assembly and that its cytotoxicity can be synergistically enhanced by metformin through combined action on complex I.</AbstractText><CopyrightInformation>Copyright: © 2020 Alhajala et al.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Alhajala</LastName><ForeName>Hisham S</ForeName><Initials>HS</Initials><AffiliationInfo><Affiliation>Division of Hematology and Oncology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Markley</LastName><ForeName>John L</ForeName><Initials>JL</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kim</LastName><ForeName>Jin Hae</ForeName><Initials>JH</Initials><AffiliationInfo><Affiliation>Department of Biochemistry, University of Wisconsin-Madison, Madison, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Al-Gizawiy</LastName><ForeName>Mona M</ForeName><Initials>MM</Initials><AffiliationInfo><Affiliation>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Schmainda</LastName><ForeName>Kathleen M</ForeName><Initials>KM</Initials><AffiliationInfo><Affiliation>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kuo</LastName><ForeName>John S</ForeName><Initials>JS</Initials><AffiliationInfo><Affiliation>Department of Neurosurgery and Mulva Clinic for the Neurosciences, Dell Medical School, Austin, Texas, USA.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Chitambar</LastName><ForeName>Christopher R</ForeName><Initials>CR</Initials><AffiliationInfo><Affiliation>Division of Hematology and Oncology, Department of Medicine, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</Affiliation></AffiliationInfo><AffiliationInfo><Affiliation>Department of Biophysics, Medical College of Wisconsin, Milwaukee, Wisconsin, USA.</Affiliation></AffiliationInfo></Author></AuthorList><Language>eng</Language><PublicationTypeList><PublicationType UI="D016428">Journal Article</PublicationType></PublicationTypeList><ArticleDate DateType="Electronic"><Year>2020</Year><Month>04</Month><Day>28</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Oncotarget</MedlineTA><NlmUniqueID>101532965</NlmUniqueID><ISSNLinking>1949-2553</ISSNLinking></MedlineJournalInfo><KeywordList Owner="NOTNLM"><Keyword MajorTopicYN="N">gallium</Keyword><Keyword MajorTopicYN="N">glioblastoma</Keyword><Keyword MajorTopicYN="N">iron</Keyword><Keyword MajorTopicYN="N">metformin</Keyword><Keyword MajorTopicYN="N">mitochondrial complex I</Keyword></KeywordList><CoiStatement>CONFLICTS OF INTEREST None.</CoiStatement></MedlineCitation><PubmedData><History><PubMedPubDate PubStatus="received"><Year>2020</Year><Month>02</Month><Day>01</Day></PubMedPubDate><PubMedPubDate PubStatus="accepted"><Year>2020</Year><Month>04</Month><Day>03</Day></PubMedPubDate><PubMedPubDate PubStatus="entrez"><Year>2020</Year><Month>5</Month><Day>12</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="pubmed"><Year>2020</Year><Month>5</Month><Day>12</Day><Hour>6</Hour><Minute>0</Minute></PubMedPubDate><PubMedPubDate PubStatus="medline"><Year>2020</Year><Month>5</Month><Day>12</Day><Hour>6</Hour><Minute>1</Minute></PubMedPubDate></History><PublicationStatus>epublish</PublicationStatus><ArticleIdList><ArticleId IdType="pubmed">32391122</ArticleId><ArticleId 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Alhajala</name></region><name sortKey="Al Gizawiy, Mona M" sort="Al Gizawiy, Mona M" uniqKey="Al Gizawiy M" first="Mona M" last="Al-Gizawiy">Mona M. Al-Gizawiy</name><name sortKey="Chitambar, Christopher R" sort="Chitambar, Christopher R" uniqKey="Chitambar C" first="Christopher R" last="Chitambar">Christopher R. Chitambar</name><name sortKey="Chitambar, Christopher R" sort="Chitambar, Christopher R" uniqKey="Chitambar C" first="Christopher R" last="Chitambar">Christopher R. Chitambar</name><name sortKey="Kim, Jin Hae" sort="Kim, Jin Hae" uniqKey="Kim J" first="Jin Hae" last="Kim">Jin Hae Kim</name><name sortKey="Kuo, John S" sort="Kuo, John S" uniqKey="Kuo J" first="John S" last="Kuo">John S. Kuo</name><name sortKey="Markley, John L" sort="Markley, John L" uniqKey="Markley J" first="John L" last="Markley">John L. Markley</name><name sortKey="Schmainda, Kathleen M" sort="Schmainda, Kathleen M" uniqKey="Schmainda K" first="Kathleen M" last="Schmainda">Kathleen M. 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