The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro
Several lines of evidence have clearly demonstrated the role of the tumor microenvironment in favoring the drug resistance of melanoma cells, as well as the progression of this cancer type. Since our previous studies proved that the accumulation of prednisolone disodium phosphate (PLP) in melanoma t...
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description | Several lines of evidence have clearly demonstrated the role of the tumor microenvironment in favoring the drug resistance of melanoma cells, as well as the progression of this cancer type. Since our previous studies proved that the accumulation of prednisolone disodium phosphate (PLP) in melanoma tissue inhibited tumor growth by exerting anti‑angiogenic effects on the most abundant cells of the tumor microenvironment, tumor‑associated macrophages (TAMs), the present study investigated whether PLP could enhance the cytotoxic effects of doxorubicin (DOX) on B16.F10 murine melanoma cells. To assess the antitumor efficacy of the combined therapeutic approach based on PLP and DOX, we used a co‑culture system composed of bone marrow‑derived macrophages (BMDMs) and B16.F10 murine melanoma cells at a cell density ratio that approximates the melanoma microenvironment in vivo, ensuring the polarization of the BMDMs into TAMs. Thus, we assessed the combined therapeutic effects of PLP and DOX on melanoma cell proliferation and apoptosis, as well as on supportive processes for tumor growth, such as oxidative stress as well as the angiogenic and inflammatory capacity of the cell co‑culture. Our data demonstrated that the cytotoxicity of DOX was potentiated mainly via the anti‑angiogenic activity of PLP in the melanoma microenvironment in vitro. Moreover, the amplitude of the cytotoxicity of the combined treatments may be linked to the degree of the suppression of the pro‑angiogenic function of TAMs. Thus, the potent decrease in the expression of the majority of the angiogenic and inflammatory proteins in TAMs following the concomitant administration of PLP and DOX may be associated with their anti‑proliferative, as well as pro‑apoptotic effects on B16.F10 melanoma cells. However, the combination therapy tested did not affect the immunosuppressive phenotype of the TAMs, as the levels of two important markers of the M2‑like phenotype of macrophages (IL‑10 and Arg‑1) were not reduced or even increased following these treatments. On the whole, the findings of this study indicated that PLP improved the therapeutic outcome of DOX in the melanoma microenvironment via the inhibition of the pro‑angiogenic function of TAMs. |
doi_str_mv | 10.3892/or.2019.7346 |
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Since our previous studies proved that the accumulation of prednisolone disodium phosphate (PLP) in melanoma tissue inhibited tumor growth by exerting anti‑angiogenic effects on the most abundant cells of the tumor microenvironment, tumor‑associated macrophages (TAMs), the present study investigated whether PLP could enhance the cytotoxic effects of doxorubicin (DOX) on B16.F10 murine melanoma cells. To assess the antitumor efficacy of the combined therapeutic approach based on PLP and DOX, we used a co‑culture system composed of bone marrow‑derived macrophages (BMDMs) and B16.F10 murine melanoma cells at a cell density ratio that approximates the melanoma microenvironment in vivo, ensuring the polarization of the BMDMs into TAMs. Thus, we assessed the combined therapeutic effects of PLP and DOX on melanoma cell proliferation and apoptosis, as well as on supportive processes for tumor growth, such as oxidative stress as well as the angiogenic and inflammatory capacity of the cell co‑culture. Our data demonstrated that the cytotoxicity of DOX was potentiated mainly via the anti‑angiogenic activity of PLP in the melanoma microenvironment in vitro. Moreover, the amplitude of the cytotoxicity of the combined treatments may be linked to the degree of the suppression of the pro‑angiogenic function of TAMs. Thus, the potent decrease in the expression of the majority of the angiogenic and inflammatory proteins in TAMs following the concomitant administration of PLP and DOX may be associated with their anti‑proliferative, as well as pro‑apoptotic effects on B16.F10 melanoma cells. However, the combination therapy tested did not affect the immunosuppressive phenotype of the TAMs, as the levels of two important markers of the M2‑like phenotype of macrophages (IL‑10 and Arg‑1) were not reduced or even increased following these treatments. On the whole, the findings of this study indicated that PLP improved the therapeutic outcome of DOX in the melanoma microenvironment via the inhibition of the pro‑angiogenic function of TAMs.</description><identifier>ISSN: 1021-335X</identifier><identifier>EISSN: 1791-2431</identifier><identifier>DOI: 10.3892/or.2019.7346</identifier><identifier>PMID: 31578578</identifier><language>eng</language><publisher>Greece: Spandidos Publications</publisher><subject>Analysis ; Angiogenesis ; Angiogenesis Inhibitors - pharmacology ; Animals ; Anthracyclines ; Antineoplastic agents ; Apoptosis - drug effects ; Bone marrow ; Cancer ; Cancer prevention ; Cancer research ; Cancer therapies ; Cancer treatment ; Cell growth ; Cell Line, Tumor ; Cell Proliferation - drug effects ; Cytotoxicity ; Development and progression ; Doxorubicin - pharmacology ; Drug Delivery Systems ; Drug resistance ; Glucocorticoids ; Health aspects ; Humans ; Inflammation ; Liposomes - pharmacology ; Macrophages ; Macrophages - drug effects ; Macrophages - pathology ; Melanoma ; Melanoma, Experimental - drug therapy ; Melanoma, Experimental - pathology ; Metastasis ; Mice ; Neovascularization, Pathologic - drug therapy ; Neovascularization, Pathologic - pathology ; Oxidative stress ; Phosphates ; Prednisolone ; Prednisolone - analogs & derivatives ; Prednisolone - pharmacology ; Proteins ; Tumor Microenvironment - drug effects ; Tumors ; Vascular endothelial growth factor</subject><ispartof>Oncology reports, 2019-12, Vol.42 (6), p.2694-2705</ispartof><rights>COPYRIGHT 2019 Spandidos Publications</rights><rights>Copyright Spandidos Publications UK Ltd. 2019</rights><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c455t-772bfdce2993500575c75e39fec0f95894e7fb50651bb8058a7c0c1a2cabbe883</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,781,785,27929,27930</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31578578$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Licarete, Emilia</creatorcontrib><creatorcontrib>Rauca, Valentin Florian</creatorcontrib><creatorcontrib>Luput, Lavinia</creatorcontrib><creatorcontrib>Patras, Laura</creatorcontrib><creatorcontrib>Sesarman, Alina</creatorcontrib><creatorcontrib>Banciu, Manuela</creatorcontrib><title>The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro</title><title>Oncology reports</title><addtitle>Oncol Rep</addtitle><description>Several lines of evidence have clearly demonstrated the role of the tumor microenvironment in favoring the drug resistance of melanoma cells, as well as the progression of this cancer type. Since our previous studies proved that the accumulation of prednisolone disodium phosphate (PLP) in melanoma tissue inhibited tumor growth by exerting anti‑angiogenic effects on the most abundant cells of the tumor microenvironment, tumor‑associated macrophages (TAMs), the present study investigated whether PLP could enhance the cytotoxic effects of doxorubicin (DOX) on B16.F10 murine melanoma cells. To assess the antitumor efficacy of the combined therapeutic approach based on PLP and DOX, we used a co‑culture system composed of bone marrow‑derived macrophages (BMDMs) and B16.F10 murine melanoma cells at a cell density ratio that approximates the melanoma microenvironment in vivo, ensuring the polarization of the BMDMs into TAMs. Thus, we assessed the combined therapeutic effects of PLP and DOX on melanoma cell proliferation and apoptosis, as well as on supportive processes for tumor growth, such as oxidative stress as well as the angiogenic and inflammatory capacity of the cell co‑culture. Our data demonstrated that the cytotoxicity of DOX was potentiated mainly via the anti‑angiogenic activity of PLP in the melanoma microenvironment in vitro. Moreover, the amplitude of the cytotoxicity of the combined treatments may be linked to the degree of the suppression of the pro‑angiogenic function of TAMs. Thus, the potent decrease in the expression of the majority of the angiogenic and inflammatory proteins in TAMs following the concomitant administration of PLP and DOX may be associated with their anti‑proliferative, as well as pro‑apoptotic effects on B16.F10 melanoma cells. However, the combination therapy tested did not affect the immunosuppressive phenotype of the TAMs, as the levels of two important markers of the M2‑like phenotype of macrophages (IL‑10 and Arg‑1) were not reduced or even increased following these treatments. On the whole, the findings of this study indicated that PLP improved the therapeutic outcome of DOX in the melanoma microenvironment via the inhibition of the pro‑angiogenic function of TAMs.</description><subject>Analysis</subject><subject>Angiogenesis</subject><subject>Angiogenesis Inhibitors - pharmacology</subject><subject>Animals</subject><subject>Anthracyclines</subject><subject>Antineoplastic agents</subject><subject>Apoptosis - drug effects</subject><subject>Bone marrow</subject><subject>Cancer</subject><subject>Cancer prevention</subject><subject>Cancer research</subject><subject>Cancer therapies</subject><subject>Cancer treatment</subject><subject>Cell growth</subject><subject>Cell Line, Tumor</subject><subject>Cell Proliferation - drug effects</subject><subject>Cytotoxicity</subject><subject>Development and progression</subject><subject>Doxorubicin - pharmacology</subject><subject>Drug Delivery Systems</subject><subject>Drug resistance</subject><subject>Glucocorticoids</subject><subject>Health aspects</subject><subject>Humans</subject><subject>Inflammation</subject><subject>Liposomes - pharmacology</subject><subject>Macrophages</subject><subject>Macrophages - drug effects</subject><subject>Macrophages - pathology</subject><subject>Melanoma</subject><subject>Melanoma, Experimental - drug therapy</subject><subject>Melanoma, Experimental - pathology</subject><subject>Metastasis</subject><subject>Mice</subject><subject>Neovascularization, Pathologic - drug therapy</subject><subject>Neovascularization, Pathologic - pathology</subject><subject>Oxidative stress</subject><subject>Phosphates</subject><subject>Prednisolone</subject><subject>Prednisolone - analogs & derivatives</subject><subject>Prednisolone - pharmacology</subject><subject>Proteins</subject><subject>Tumor Microenvironment - drug effects</subject><subject>Tumors</subject><subject>Vascular endothelial growth factor</subject><issn>1021-335X</issn><issn>1791-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNptkk1u1TAQgCMEoqWwY40sISEWvId_4jhZlooCUiU2RWIXOc74xVViBzuuYMcVuAFnYcFBOAkTXgsUIVuynXzzeayZonjI6FbUDX8e4pZT1myVKKtbxSFTDdvwUrDbuKecbYSQ7w-KeyldUMoVrZq7xYFgUtU4D4vv5wOQOULvXQpj8HgYQpoHvcCPz1-c77OBnqQ8I5OSC54ESxaM0X7nwg68M8Rmb5brX3kKESN1SsE4tPRk0iYGNO4gEfCD9gY3e8XifvEErAWzpFXQh48h5s4Zhz5PXrBqe8oomXJ0mNwEo_Zh0sTAOCbi_Levl26J4X5xx-oxwYOr9ah4d_ry_OT15uztqzcnx2cbU0q5bJTine0N8KYRklKppFESRIO3U9vIuilB2U7SSrKuq6mstTLUMM2N7jqoa3FUPN175xg-ZEhLO7m05qI9hJxaLtDa1LUSiD7-B70IOXrMDimmpGSykn-onR6hdd6GJWqzStvjiqqal5Svru1_KBw9TM5g1azD7zcCnvwVMIAelwHrm9cypZvgsz2INUopgm3n6CYdP7WMtmt_tSG2a3-1a38h_ujqUbmboP8NXzeU-AluPdA7</recordid><startdate>20191201</startdate><enddate>20191201</enddate><creator>Licarete, Emilia</creator><creator>Rauca, Valentin Florian</creator><creator>Luput, Lavinia</creator><creator>Patras, Laura</creator><creator>Sesarman, Alina</creator><creator>Banciu, Manuela</creator><general>Spandidos Publications</general><general>Spandidos Publications UK Ltd</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AN0</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope></search><sort><creationdate>20191201</creationdate><title>The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro</title><author>Licarete, Emilia ; Rauca, Valentin Florian ; Luput, Lavinia ; Patras, Laura ; Sesarman, Alina ; Banciu, Manuela</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c455t-772bfdce2993500575c75e39fec0f95894e7fb50651bb8058a7c0c1a2cabbe883</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Analysis</topic><topic>Angiogenesis</topic><topic>Angiogenesis Inhibitors - pharmacology</topic><topic>Animals</topic><topic>Anthracyclines</topic><topic>Antineoplastic agents</topic><topic>Apoptosis - drug effects</topic><topic>Bone marrow</topic><topic>Cancer</topic><topic>Cancer prevention</topic><topic>Cancer research</topic><topic>Cancer therapies</topic><topic>Cancer treatment</topic><topic>Cell growth</topic><topic>Cell Line, Tumor</topic><topic>Cell Proliferation - drug effects</topic><topic>Cytotoxicity</topic><topic>Development and progression</topic><topic>Doxorubicin - pharmacology</topic><topic>Drug Delivery Systems</topic><topic>Drug resistance</topic><topic>Glucocorticoids</topic><topic>Health aspects</topic><topic>Humans</topic><topic>Inflammation</topic><topic>Liposomes - pharmacology</topic><topic>Macrophages</topic><topic>Macrophages - drug effects</topic><topic>Macrophages - pathology</topic><topic>Melanoma</topic><topic>Melanoma, Experimental - drug therapy</topic><topic>Melanoma, Experimental - pathology</topic><topic>Metastasis</topic><topic>Mice</topic><topic>Neovascularization, Pathologic - drug therapy</topic><topic>Neovascularization, Pathologic - pathology</topic><topic>Oxidative stress</topic><topic>Phosphates</topic><topic>Prednisolone</topic><topic>Prednisolone - analogs & derivatives</topic><topic>Prednisolone - pharmacology</topic><topic>Proteins</topic><topic>Tumor Microenvironment - drug effects</topic><topic>Tumors</topic><topic>Vascular endothelial growth factor</topic><toplevel>online_resources</toplevel><creatorcontrib>Licarete, Emilia</creatorcontrib><creatorcontrib>Rauca, Valentin Florian</creatorcontrib><creatorcontrib>Luput, Lavinia</creatorcontrib><creatorcontrib>Patras, Laura</creatorcontrib><creatorcontrib>Sesarman, Alina</creatorcontrib><creatorcontrib>Banciu, Manuela</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>British Nursing Database</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><jtitle>Oncology reports</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Licarete, Emilia</au><au>Rauca, Valentin Florian</au><au>Luput, Lavinia</au><au>Patras, Laura</au><au>Sesarman, Alina</au><au>Banciu, Manuela</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro</atitle><jtitle>Oncology reports</jtitle><addtitle>Oncol Rep</addtitle><date>2019-12-01</date><risdate>2019</risdate><volume>42</volume><issue>6</issue><spage>2694</spage><epage>2705</epage><pages>2694-2705</pages><issn>1021-335X</issn><eissn>1791-2431</eissn><abstract>Several lines of evidence have clearly demonstrated the role of the tumor microenvironment in favoring the drug resistance of melanoma cells, as well as the progression of this cancer type. Since our previous studies proved that the accumulation of prednisolone disodium phosphate (PLP) in melanoma tissue inhibited tumor growth by exerting anti‑angiogenic effects on the most abundant cells of the tumor microenvironment, tumor‑associated macrophages (TAMs), the present study investigated whether PLP could enhance the cytotoxic effects of doxorubicin (DOX) on B16.F10 murine melanoma cells. To assess the antitumor efficacy of the combined therapeutic approach based on PLP and DOX, we used a co‑culture system composed of bone marrow‑derived macrophages (BMDMs) and B16.F10 murine melanoma cells at a cell density ratio that approximates the melanoma microenvironment in vivo, ensuring the polarization of the BMDMs into TAMs. Thus, we assessed the combined therapeutic effects of PLP and DOX on melanoma cell proliferation and apoptosis, as well as on supportive processes for tumor growth, such as oxidative stress as well as the angiogenic and inflammatory capacity of the cell co‑culture. Our data demonstrated that the cytotoxicity of DOX was potentiated mainly via the anti‑angiogenic activity of PLP in the melanoma microenvironment in vitro. Moreover, the amplitude of the cytotoxicity of the combined treatments may be linked to the degree of the suppression of the pro‑angiogenic function of TAMs. Thus, the potent decrease in the expression of the majority of the angiogenic and inflammatory proteins in TAMs following the concomitant administration of PLP and DOX may be associated with their anti‑proliferative, as well as pro‑apoptotic effects on B16.F10 melanoma cells. However, the combination therapy tested did not affect the immunosuppressive phenotype of the TAMs, as the levels of two important markers of the M2‑like phenotype of macrophages (IL‑10 and Arg‑1) were not reduced or even increased following these treatments. On the whole, the findings of this study indicated that PLP improved the therapeutic outcome of DOX in the melanoma microenvironment via the inhibition of the pro‑angiogenic function of TAMs.</abstract><cop>Greece</cop><pub>Spandidos Publications</pub><pmid>31578578</pmid><doi>10.3892/or.2019.7346</doi><tpages>12</tpages><oa>free_for_read</oa></addata></record> |
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source | MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection |
subjects | Analysis Angiogenesis Angiogenesis Inhibitors - pharmacology Animals Anthracyclines Antineoplastic agents Apoptosis - drug effects Bone marrow Cancer Cancer prevention Cancer research Cancer therapies Cancer treatment Cell growth Cell Line, Tumor Cell Proliferation - drug effects Cytotoxicity Development and progression Doxorubicin - pharmacology Drug Delivery Systems Drug resistance Glucocorticoids Health aspects Humans Inflammation Liposomes - pharmacology Macrophages Macrophages - drug effects Macrophages - pathology Melanoma Melanoma, Experimental - drug therapy Melanoma, Experimental - pathology Metastasis Mice Neovascularization, Pathologic - drug therapy Neovascularization, Pathologic - pathology Oxidative stress Phosphates Prednisolone Prednisolone - analogs & derivatives Prednisolone - pharmacology Proteins Tumor Microenvironment - drug effects Tumors Vascular endothelial growth factor |
title | The prednisolone phosphate‑induced suppression of the angiogenic function of tumor‑associated macrophages enhances the antitumor effects of doxorubicin on B16.F10 murine melanoma cells in vitro |
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