Autophagy inhibition upregulates CD4+ tumor infiltrating lymphocyte expression via miR-155 regulation and TRAIL activation.
Identifieur interne : 000193 ( PubMed/Corpus ); précédent : 000192; suivant : 000194Autophagy inhibition upregulates CD4+ tumor infiltrating lymphocyte expression via miR-155 regulation and TRAIL activation.
Auteurs : Paul Zarogoulidis ; Savvas Petanidis ; Kalliopi Domvri ; Efrosini Kioseoglou ; Doxakis Anestakis ; Lutz Freitag ; Konstantinos Zarogoulidis ; Wolfgang Hohenforst-Schmidt ; Wilfried EberhardtSource :
- Molecular oncology [ 1878-0261 ] ; 2016.
English descriptors
- KwdEn :
- Adult, Aged, Aged, 80 and over, Antineoplastic Agents (pharmacology), Antineoplastic Agents (therapeutic use), Antirheumatic Agents (pharmacology), Antirheumatic Agents (therapeutic use), Apoptosis (drug effects), Autophagy (drug effects), CD4-Positive T-Lymphocytes (drug effects), CD4-Positive T-Lymphocytes (immunology), CD4-Positive T-Lymphocytes (pathology), Carboplatin (pharmacology), Carboplatin (therapeutic use), Carcinoma, Non-Small-Cell Lung (drug therapy), Carcinoma, Non-Small-Cell Lung (immunology), Carcinoma, Non-Small-Cell Lung (pathology), Carcinoma, Non-Small-Cell Lung (secondary), Chloroquine (pharmacology), Chloroquine (therapeutic use), Drug Resistance, Neoplasm (drug effects), Gene Expression Regulation, Neoplastic (drug effects), Humans, Lung (drug effects), Lung (immunology), Lung (pathology), Lung Neoplasms (drug therapy), Lung Neoplasms (immunology), Lung Neoplasms (pathology), Lung Neoplasms (secondary), Lymphocytes, Tumor-Infiltrating (drug effects), Lymphocytes, Tumor-Infiltrating (immunology), Lymphocytes, Tumor-Infiltrating (pathology), MicroRNAs (genetics), MicroRNAs (immunology), Middle Aged, TNF-Related Apoptosis-Inducing Ligand (immunology).
- MESH :
- chemical , genetics : MicroRNAs.
- chemical , immunology : MicroRNAs, TNF-Related Apoptosis-Inducing Ligand.
- chemical , pharmacology : Antineoplastic Agents, Antirheumatic Agents, Carboplatin, Chloroquine.
- chemical , therapeutic use : Antineoplastic Agents, Antirheumatic Agents, Carboplatin, Chloroquine.
- drug effects : Apoptosis, Autophagy, CD4-Positive T-Lymphocytes, Drug Resistance, Neoplasm, Gene Expression Regulation, Neoplastic, Lung, Lymphocytes, Tumor-Infiltrating.
- drug therapy : Carcinoma, Non-Small-Cell Lung, Lung Neoplasms.
- immunology : CD4-Positive T-Lymphocytes, Carcinoma, Non-Small-Cell Lung, Lung, Lung Neoplasms, Lymphocytes, Tumor-Infiltrating.
- pathology : CD4-Positive T-Lymphocytes, Carcinoma, Non-Small-Cell Lung, Lung, Lung Neoplasms, Lymphocytes, Tumor-Infiltrating.
- secondary : Carcinoma, Non-Small-Cell Lung, Lung Neoplasms.
- Adult, Aged, Aged, 80 and over, Humans, Middle Aged.
Abstract
Chemoresistance is a major challenge in lung cancer treatment. Recent findings have revealed that autophagic mechanism contributes significantly to immunosuppressive related chemoresistance. For that reason, targeting autophagy-related immunosuppression is an important approach to reverse tumor drug resistance. In this study, we report for the first time that autophagy inhibition triggers upregulation of CD4+, Foxp3+ tumor infiltrating lymphocytes in late metastatic lung cancer tissues. Furthermore, autophagy blockage induces chemosensitization to carboplatin, immune activation and cell cycle arrest. This induction correlated with reduction in expression of drug resistance genes MDR1, MRP1, ABCG2 and ABCC2 along with decreased expression of PD-L1 which is associated with severe dysfunction of tumor specific CD8+ T cells. Furthermore, experiments revealed that co-treatment of carboplatin and autophagy inhibitor chloroquine increased lung tissue infiltration by CD4+, FoxP3+ lymphocytes and antigen-specific immune activation. Subsequent ex vivo experiments showed the activation of carboplatin related TRAIL-dependent apoptosis through caspase 8 and a synergistic role of miR-155 in lung tissue infiltration by CD4+, and FoxP3+ lymphocytes. Overall, our results indicate that autophagy blockage increases lung cancer chemosensitivity to carboplatin, but also reveal that miR-155 functions as a novel immune system activator by promoting TILs infiltration. These results indicate that targeting of autophagy can prevent cancer related immunosuppression and elucidate immune cell infiltration in tumor microenvironment thus representing a potential therapeutic strategy to inhibit lung cancer progression and metastasis.
DOI: 10.1016/j.molonc.2016.08.005
PubMed: 27692344
Links to Exploration step
pubmed:27692344Le document en format XML
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Papanikolaou" General Hospital, Aristotle University of Thessaloniki, Thessaloniki, 57010, Greece.</nlm:affiliation></affiliation></author><author><name sortKey="Petanidis, Savvas" sort="Petanidis, Savvas" uniqKey="Petanidis S" first="Savvas" last="Petanidis">Savvas Petanidis</name><affiliation><nlm:affiliation>Department of Chemical Engineering, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece. Electronic address: spetanid@auth.gr.</nlm:affiliation></affiliation></author><author><name sortKey="Domvri, Kalliopi" sort="Domvri, Kalliopi" uniqKey="Domvri K" first="Kalliopi" last="Domvri">Kalliopi Domvri</name><affiliation><nlm:affiliation>Pulmonary Department-Oncology Unit, "G. Papanikolaou" General Hospital, Aristotle University of Thessaloniki, Thessaloniki, 57010, Greece.</nlm:affiliation></affiliation></author><author><name sortKey="Kioseoglou, Efrosini" sort="Kioseoglou, Efrosini" uniqKey="Kioseoglou E" first="Efrosini" last="Kioseoglou">Efrosini Kioseoglou</name><affiliation><nlm:affiliation>Department of Chemical Engineering, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece.</nlm:affiliation></affiliation></author><author><name sortKey="Anestakis, Doxakis" sort="Anestakis, Doxakis" uniqKey="Anestakis D" first="Doxakis" last="Anestakis">Doxakis Anestakis</name><affiliation><nlm:affiliation>Department of Medicine, Laboratory of General Biology, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece; Department of Medicine, Laboratory of Forensic Medicine and Toxicology, Aristotle University of Thessaloniki, 54124, Greece.</nlm:affiliation></affiliation></author><author><name sortKey="Freitag, Lutz" sort="Freitag, Lutz" uniqKey="Freitag L" first="Lutz" last="Freitag">Lutz Freitag</name><affiliation><nlm:affiliation>Department of Interventional Pneumology, Ruhrlandklinik, University Hospital Essen, University of Essen-Duisburg, Tueschener Weg 40, 45239, Essen, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Zarogoulidis, Konstantinos" sort="Zarogoulidis, Konstantinos" uniqKey="Zarogoulidis K" first="Konstantinos" last="Zarogoulidis">Konstantinos Zarogoulidis</name><affiliation><nlm:affiliation>Pulmonary Department-Oncology Unit, "G. Papanikolaou" General Hospital, Aristotle University of Thessaloniki, Thessaloniki, 57010, Greece.</nlm:affiliation></affiliation></author><author><name sortKey="Hohenforst Schmidt, Wolfgang" sort="Hohenforst Schmidt, Wolfgang" uniqKey="Hohenforst Schmidt W" first="Wolfgang" last="Hohenforst-Schmidt">Wolfgang Hohenforst-Schmidt</name><affiliation><nlm:affiliation>Medical Clinic I, "Fuerth" Hospital, University of Erlangen, 91054, Fuerth, Germany.</nlm:affiliation></affiliation></author><author><name sortKey="Eberhardt, Wilfried" sort="Eberhardt, Wilfried" uniqKey="Eberhardt W" first="Wilfried" last="Eberhardt">Wilfried Eberhardt</name><affiliation><nlm:affiliation>Division of Thoracic Oncology, Department of Medical Oncology, West German Cancer Center, University Hospital Essen, University Duisburg-Essen, 45122, Essen, Germany.</nlm:affiliation></affiliation></author></analytic><series><title level="j">Molecular oncology</title><idno type="eISSN">1878-0261</idno><imprint><date when="2016" type="published">2016</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adult</term><term>Aged</term><term>Aged, 80 and over</term><term>Antineoplastic Agents (pharmacology)</term><term>Antineoplastic Agents (therapeutic use)</term><term>Antirheumatic Agents (pharmacology)</term><term>Antirheumatic Agents (therapeutic use)</term><term>Apoptosis (drug effects)</term><term>Autophagy (drug effects)</term><term>CD4-Positive T-Lymphocytes (drug effects)</term><term>CD4-Positive T-Lymphocytes (immunology)</term><term>CD4-Positive T-Lymphocytes (pathology)</term><term>Carboplatin (pharmacology)</term><term>Carboplatin (therapeutic use)</term><term>Carcinoma, Non-Small-Cell Lung (drug therapy)</term><term>Carcinoma, Non-Small-Cell Lung (immunology)</term><term>Carcinoma, Non-Small-Cell Lung (pathology)</term><term>Carcinoma, Non-Small-Cell Lung (secondary)</term><term>Chloroquine (pharmacology)</term><term>Chloroquine (therapeutic use)</term><term>Drug Resistance, Neoplasm (drug effects)</term><term>Gene Expression Regulation, Neoplastic (drug effects)</term><term>Humans</term><term>Lung (drug effects)</term><term>Lung (immunology)</term><term>Lung (pathology)</term><term>Lung Neoplasms (drug therapy)</term><term>Lung Neoplasms (immunology)</term><term>Lung Neoplasms (pathology)</term><term>Lung Neoplasms (secondary)</term><term>Lymphocytes, Tumor-Infiltrating (drug effects)</term><term>Lymphocytes, Tumor-Infiltrating (immunology)</term><term>Lymphocytes, Tumor-Infiltrating (pathology)</term><term>MicroRNAs (genetics)</term><term>MicroRNAs (immunology)</term><term>Middle Aged</term><term>TNF-Related Apoptosis-Inducing Ligand (immunology)</term></keywords><keywords scheme="MESH" type="chemical" qualifier="genetics" xml:lang="en"><term>MicroRNAs</term></keywords><keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en"><term>MicroRNAs</term><term>TNF-Related Apoptosis-Inducing Ligand</term></keywords><keywords scheme="MESH" type="chemical" qualifier="pharmacology" xml:lang="en"><term>Antineoplastic Agents</term><term>Antirheumatic Agents</term><term>Carboplatin</term><term>Chloroquine</term></keywords><keywords scheme="MESH" type="chemical" qualifier="therapeutic use" xml:lang="en"><term>Antineoplastic Agents</term><term>Antirheumatic Agents</term><term>Carboplatin</term><term>Chloroquine</term></keywords><keywords scheme="MESH" qualifier="drug effects" xml:lang="en"><term>Apoptosis</term><term>Autophagy</term><term>CD4-Positive T-Lymphocytes</term><term>Drug Resistance, Neoplasm</term><term>Gene Expression Regulation, Neoplastic</term><term>Lung</term><term>Lymphocytes, Tumor-Infiltrating</term></keywords><keywords scheme="MESH" qualifier="drug therapy" xml:lang="en"><term>Carcinoma, Non-Small-Cell Lung</term><term>Lung Neoplasms</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>CD4-Positive T-Lymphocytes</term><term>Carcinoma, Non-Small-Cell Lung</term><term>Lung</term><term>Lung Neoplasms</term><term>Lymphocytes, Tumor-Infiltrating</term></keywords><keywords scheme="MESH" qualifier="pathology" xml:lang="en"><term>CD4-Positive T-Lymphocytes</term><term>Carcinoma, Non-Small-Cell Lung</term><term>Lung</term><term>Lung Neoplasms</term><term>Lymphocytes, Tumor-Infiltrating</term></keywords><keywords scheme="MESH" qualifier="secondary" xml:lang="en"><term>Carcinoma, Non-Small-Cell Lung</term><term>Lung Neoplasms</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Adult</term><term>Aged</term><term>Aged, 80 and over</term><term>Humans</term><term>Middle Aged</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en">Chemoresistance is a major challenge in lung cancer treatment. Recent findings have revealed that autophagic mechanism contributes significantly to immunosuppressive related chemoresistance. For that reason, targeting autophagy-related immunosuppression is an important approach to reverse tumor drug resistance. In this study, we report for the first time that autophagy inhibition triggers upregulation of CD4<sup>+</sup>, Foxp3<sup>+</sup> tumor infiltrating lymphocytes in late metastatic lung cancer tissues. Furthermore, autophagy blockage induces chemosensitization to carboplatin, immune activation and cell cycle arrest. This induction correlated with reduction in expression of drug resistance genes MDR1, MRP1, ABCG2 and ABCC2 along with decreased expression of PD-L1 which is associated with severe dysfunction of tumor specific CD8<sup>+</sup> T cells. Furthermore, experiments revealed that co-treatment of carboplatin and autophagy inhibitor chloroquine increased lung tissue infiltration by CD4<sup>+</sup>, FoxP3<sup>+</sup> lymphocytes and antigen-specific immune activation. Subsequent ex vivo experiments showed the activation of carboplatin related TRAIL-dependent apoptosis through caspase 8 and a synergistic role of miR-155 in lung tissue infiltration by CD4<sup>+</sup>, and FoxP3<sup>+</sup> lymphocytes. Overall, our results indicate that autophagy blockage increases lung cancer chemosensitivity to carboplatin, but also reveal that miR-155 functions as a novel immune system activator by promoting TILs infiltration. These results indicate that targeting of autophagy can prevent cancer related immunosuppression and elucidate immune cell infiltration in tumor microenvironment thus representing a potential therapeutic strategy to inhibit lung cancer progression and metastasis.</div></front></TEI><pubmed><MedlineCitation Status="MEDLINE" Owner="NLM"><PMID Version="1">27692344</PMID><DateCompleted><Year>2017</Year><Month>09</Month><Day>25</Day></DateCompleted><DateRevised><Year>2020</Year><Month>03</Month><Day>06</Day></DateRevised><Article PubModel="Print-Electronic"><Journal><ISSN IssnType="Electronic">1878-0261</ISSN><JournalIssue CitedMedium="Internet"><Volume>10</Volume><Issue>10</Issue><PubDate><Year>2016</Year><Month>12</Month></PubDate></JournalIssue><Title>Molecular oncology</Title><ISOAbbreviation>Mol Oncol</ISOAbbreviation></Journal><ArticleTitle>Autophagy inhibition upregulates CD4<sup>+</sup> tumor infiltrating lymphocyte expression via miR-155 regulation and TRAIL activation.</ArticleTitle><Pagination><MedlinePgn>1516-1531</MedlinePgn></Pagination><ELocationID EIdType="pii" ValidYN="Y">S1574-7891(16)30086-2</ELocationID><ELocationID EIdType="doi" ValidYN="Y">10.1016/j.molonc.2016.08.005</ELocationID><Abstract><AbstractText>Chemoresistance is a major challenge in lung cancer treatment. Recent findings have revealed that autophagic mechanism contributes significantly to immunosuppressive related chemoresistance. For that reason, targeting autophagy-related immunosuppression is an important approach to reverse tumor drug resistance. In this study, we report for the first time that autophagy inhibition triggers upregulation of CD4<sup>+</sup>, Foxp3<sup>+</sup> tumor infiltrating lymphocytes in late metastatic lung cancer tissues. Furthermore, autophagy blockage induces chemosensitization to carboplatin, immune activation and cell cycle arrest. This induction correlated with reduction in expression of drug resistance genes MDR1, MRP1, ABCG2 and ABCC2 along with decreased expression of PD-L1 which is associated with severe dysfunction of tumor specific CD8<sup>+</sup> T cells. Furthermore, experiments revealed that co-treatment of carboplatin and autophagy inhibitor chloroquine increased lung tissue infiltration by CD4<sup>+</sup>, FoxP3<sup>+</sup> lymphocytes and antigen-specific immune activation. Subsequent ex vivo experiments showed the activation of carboplatin related TRAIL-dependent apoptosis through caspase 8 and a synergistic role of miR-155 in lung tissue infiltration by CD4<sup>+</sup>, and FoxP3<sup>+</sup> lymphocytes. Overall, our results indicate that autophagy blockage increases lung cancer chemosensitivity to carboplatin, but also reveal that miR-155 functions as a novel immune system activator by promoting TILs infiltration. These results indicate that targeting of autophagy can prevent cancer related immunosuppression and elucidate immune cell infiltration in tumor microenvironment thus representing a potential therapeutic strategy to inhibit lung cancer progression and metastasis.</AbstractText><CopyrightInformation>Copyright © 2016 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.</CopyrightInformation></Abstract><AuthorList CompleteYN="Y"><Author ValidYN="Y"><LastName>Zarogoulidis</LastName><ForeName>Paul</ForeName><Initials>P</Initials><AffiliationInfo><Affiliation>Pulmonary Department-Oncology Unit, "G. Papanikolaou" General Hospital, Aristotle University of Thessaloniki, Thessaloniki, 57010, Greece.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Petanidis</LastName><ForeName>Savvas</ForeName><Initials>S</Initials><AffiliationInfo><Affiliation>Department of Chemical Engineering, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece. Electronic address: spetanid@auth.gr.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Domvri</LastName><ForeName>Kalliopi</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Pulmonary Department-Oncology Unit, "G. Papanikolaou" General Hospital, Aristotle University of Thessaloniki, Thessaloniki, 57010, Greece.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Kioseoglou</LastName><ForeName>Efrosini</ForeName><Initials>E</Initials><AffiliationInfo><Affiliation>Department of Chemical Engineering, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Anestakis</LastName><ForeName>Doxakis</ForeName><Initials>D</Initials><AffiliationInfo><Affiliation>Department of Medicine, Laboratory of General Biology, Aristotle University of Thessaloniki, Thessaloniki, 54124, Greece; Department of Medicine, Laboratory of Forensic Medicine and Toxicology, Aristotle University of Thessaloniki, 54124, Greece.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Freitag</LastName><ForeName>Lutz</ForeName><Initials>L</Initials><AffiliationInfo><Affiliation>Department of Interventional Pneumology, Ruhrlandklinik, University Hospital Essen, University of Essen-Duisburg, Tueschener Weg 40, 45239, Essen, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Zarogoulidis</LastName><ForeName>Konstantinos</ForeName><Initials>K</Initials><AffiliationInfo><Affiliation>Pulmonary Department-Oncology Unit, "G. Papanikolaou" General Hospital, Aristotle University of Thessaloniki, Thessaloniki, 57010, Greece.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Hohenforst-Schmidt</LastName><ForeName>Wolfgang</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Medical Clinic I, "Fuerth" Hospital, University of Erlangen, 91054, Fuerth, Germany.</Affiliation></AffiliationInfo></Author><Author ValidYN="Y"><LastName>Eberhardt</LastName><ForeName>Wilfried</ForeName><Initials>W</Initials><AffiliationInfo><Affiliation>Division of Thoracic Oncology, Department of Medical Oncology, West German Cancer Center, University Hospital Essen, University Duisburg-Essen, 45122, Essen, Germany.</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>2016</Year><Month>09</Month><Day>16</Day></ArticleDate></Article><MedlineJournalInfo><Country>United States</Country><MedlineTA>Mol Oncol</MedlineTA><NlmUniqueID>101308230</NlmUniqueID><ISSNLinking>1574-7891</ISSNLinking></MedlineJournalInfo><ChemicalList><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D000970">Antineoplastic Agents</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D018501">Antirheumatic Agents</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="C524942">MIRN155 microRNA, human</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D035683">MicroRNAs</NameOfSubstance></Chemical><Chemical><RegistryNumber>0</RegistryNumber><NameOfSubstance UI="D053221">TNF-Related Apoptosis-Inducing Ligand</NameOfSubstance></Chemical><Chemical><RegistryNumber>886U3H6UFF</RegistryNumber><NameOfSubstance UI="D002738">Chloroquine</NameOfSubstance></Chemical><Chemical><RegistryNumber>BG3F62OND5</RegistryNumber><NameOfSubstance UI="D016190">Carboplatin</NameOfSubstance></Chemical></ChemicalList><CitationSubset>IM</CitationSubset><MeshHeadingList><MeshHeading><DescriptorName UI="D000328" MajorTopicYN="N">Adult</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000368" MajorTopicYN="N">Aged</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000369" MajorTopicYN="N">Aged, 80 and over</DescriptorName></MeshHeading><MeshHeading><DescriptorName UI="D000970" MajorTopicYN="N">Antineoplastic Agents</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName><QualifierName UI="Q000627" MajorTopicYN="Y">therapeutic use</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D018501" MajorTopicYN="N">Antirheumatic Agents</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName><QualifierName UI="Q000627" MajorTopicYN="Y">therapeutic use</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D017209" MajorTopicYN="N">Apoptosis</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D001343" MajorTopicYN="N">Autophagy</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D015496" MajorTopicYN="N">CD4-Positive T-Lymphocytes</DescriptorName><QualifierName UI="Q000187" MajorTopicYN="N">drug effects</QualifierName><QualifierName UI="Q000276" MajorTopicYN="N">immunology</QualifierName><QualifierName UI="Q000473" MajorTopicYN="N">pathology</QualifierName></MeshHeading><MeshHeading><DescriptorName UI="D016190" MajorTopicYN="N">Carboplatin</DescriptorName><QualifierName UI="Q000494" MajorTopicYN="N">pharmacology</QualifierName><QualifierName UI="Q000627" MajorTopicYN="N">therapeutic 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