Tamoxifen resistance alters sensitivity to 5-fluorouracil in a subset of estrogen receptor-positive breast cancer
Sequential treatment with endocrine or chemotherapy is generally used in the treatment of estrogen receptor (ER)-positive recurrent breast cancer. To date, few studies have investigated the effect of long-term endocrine therapy on the response to subsequent chemotherapy in ER-positive breast cancer....
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| creator | Watanabe, Takayuki Oba, Takaaki Tanimoto, Keiji Shibata, Tomohiro Kamijo, Shinobu Ito, Ken-Ichi |
| description | Sequential treatment with endocrine or chemotherapy is generally used in the treatment of estrogen receptor (ER)-positive recurrent breast cancer. To date, few studies have investigated the effect of long-term endocrine therapy on the response to subsequent chemotherapy in ER-positive breast cancer. We examined whether a preceding endocrine therapy affects the sensitivity to subsequent chemotherapy in ER-positive breast cancer cells. Three ER-positive breast cancer cell lines (T47D, MCF7, BT474) and tamoxifen-resistant sublines (T47D/T, MCF7/T, BT474/T) were analyzed for sensitivity to 5-fluorouracil, paclitaxel, and doxorubicin. The mRNA levels of factors related to drug sensitivity were analyzed by RT-PCR. MCF7/T cells became more sensitive to 5-fluorouracil than wild-type (wt)-MCF7 cells. In addition, the apoptosis induced by 5-fluorouracil was significantly increased in MCF7/T cells. However, no difference in sensitivity to chemotherapeutic agents was observed in T47D/T and BT474/T cells compared with their wt cells. Dihydropyrimidine dehydrogenase (DPYD) mRNA expression was significantly decreased in MCF7/T cells compared with wt-MCF7 cells. The expression of DPYD mRNA was restored with 5-azacytidine treatment in MCF7/T cells. In addition, DPYD 3'-UTR luciferase activity was significantly reduced in MCF7/T cells. These data indicated that the expression of DPYD mRNA was repressed by methylation of the DPYD promoter region and post-transcriptional regulation by miRNA in MCF7/T cells. In the mouse xenograft model, capecitabine significantly reduced the tumor volume in MCF7/T compared with MCF7. The results of this study indicate that endocrine therapy could alter the sensitivity to chemotherapeutic agents in a subset of breast cancers, and 5-fluorouracil may be effective in tamoxifen-resistant breast cancers. |
| doi_str_mv | 10.1371/journal.pone.0252822 |
| format | Article |
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To date, few studies have investigated the effect of long-term endocrine therapy on the response to subsequent chemotherapy in ER-positive breast cancer. We examined whether a preceding endocrine therapy affects the sensitivity to subsequent chemotherapy in ER-positive breast cancer cells. Three ER-positive breast cancer cell lines (T47D, MCF7, BT474) and tamoxifen-resistant sublines (T47D/T, MCF7/T, BT474/T) were analyzed for sensitivity to 5-fluorouracil, paclitaxel, and doxorubicin. The mRNA levels of factors related to drug sensitivity were analyzed by RT-PCR. MCF7/T cells became more sensitive to 5-fluorouracil than wild-type (wt)-MCF7 cells. In addition, the apoptosis induced by 5-fluorouracil was significantly increased in MCF7/T cells. However, no difference in sensitivity to chemotherapeutic agents was observed in T47D/T and BT474/T cells compared with their wt cells. Dihydropyrimidine dehydrogenase (DPYD) mRNA expression was significantly decreased in MCF7/T cells compared with wt-MCF7 cells. The expression of DPYD mRNA was restored with 5-azacytidine treatment in MCF7/T cells. In addition, DPYD 3'-UTR luciferase activity was significantly reduced in MCF7/T cells. These data indicated that the expression of DPYD mRNA was repressed by methylation of the DPYD promoter region and post-transcriptional regulation by miRNA in MCF7/T cells. In the mouse xenograft model, capecitabine significantly reduced the tumor volume in MCF7/T compared with MCF7. The results of this study indicate that endocrine therapy could alter the sensitivity to chemotherapeutic agents in a subset of breast cancers, and 5-fluorouracil may be effective in tamoxifen-resistant breast cancers.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0252822</identifier><identifier>PMID: 34101751</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>5-Fluorouracil ; Animals ; Anthracycline ; Antibodies ; Anticancer properties ; Antimetabolites, Antineoplastic - pharmacology ; Antineoplastic Agents, Hormonal - pharmacology ; Antitumor agents ; Apoptosis ; Apoptosis - drug effects ; Aromatase ; Auroral kilometric radiation ; Biology ; Biology and Life Sciences ; Biomarkers ; Breast cancer ; Breast Neoplasms - drug therapy ; Breast Neoplasms - genetics ; Breast Neoplasms - metabolism ; Cancer therapies ; Capecitabine - pharmacology ; Cell Line, Tumor ; Cell Proliferation - drug effects ; Chemical compounds ; Chemotherapy ; Complications and side effects ; Cyclin-dependent kinase 4 ; Cyclin-dependent kinases ; Dehydrogenases ; Drafting software ; Drug Resistance, Neoplasm - drug effects ; Drug Resistance, Neoplasm - genetics ; Drug therapy ; Editing ; Endocrine therapy ; Estradiol - pharmacology ; Estrogen receptors ; Estrogens ; Estrogens - pharmacology ; Experiments ; Female ; Fluorouracil ; Fluorouracil - pharmacology ; Gene expression ; Humans ; Inhibitors ; Kinases ; MCF-7 Cells ; Medical research ; Medicine ; Medicine and Health Sciences ; Metastases ; Metastasis ; Methodology ; Mice ; Mice, Inbred BALB C ; Mice, Nude ; Mutation ; Nuclear medicine ; Organs ; Patient outcomes ; Patients ; Pharmacology ; Physical Sciences ; Poly(ADP-ribose) polymerase ; Radiation ; Receptors, Estrogen - metabolism ; Research and analysis methods ; Ribose ; Sensitivity ; Surgery ; Tamoxifen ; Tamoxifen - pharmacology ; Tumors ; Xenograft Model Antitumor Assays - methods</subject><ispartof>PloS one, 2021-06, Vol.16 (6), p.e0252822</ispartof><rights>COPYRIGHT 2021 Public Library of Science</rights><rights>2021 Watanabe et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021 Watanabe et al 2021 Watanabe et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c719t-550e91aff4220db02d83270470976b8e88163cfe77afe375b28699822041a9e33</citedby><cites>FETCH-LOGICAL-c719t-550e91aff4220db02d83270470976b8e88163cfe77afe375b28699822041a9e33</cites><orcidid>0000-0002-6430-0307</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8186817/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8186817/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,860,881,2096,2915,23845,27901,27902,53766,53768,79569,79570</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34101751$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Watanabe, Takayuki</creatorcontrib><creatorcontrib>Oba, Takaaki</creatorcontrib><creatorcontrib>Tanimoto, Keiji</creatorcontrib><creatorcontrib>Shibata, Tomohiro</creatorcontrib><creatorcontrib>Kamijo, Shinobu</creatorcontrib><creatorcontrib>Ito, Ken-Ichi</creatorcontrib><title>Tamoxifen resistance alters sensitivity to 5-fluorouracil in a subset of estrogen receptor-positive breast cancer</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>Sequential treatment with endocrine or chemotherapy is generally used in the treatment of estrogen receptor (ER)-positive recurrent breast cancer. To date, few studies have investigated the effect of long-term endocrine therapy on the response to subsequent chemotherapy in ER-positive breast cancer. We examined whether a preceding endocrine therapy affects the sensitivity to subsequent chemotherapy in ER-positive breast cancer cells. Three ER-positive breast cancer cell lines (T47D, MCF7, BT474) and tamoxifen-resistant sublines (T47D/T, MCF7/T, BT474/T) were analyzed for sensitivity to 5-fluorouracil, paclitaxel, and doxorubicin. The mRNA levels of factors related to drug sensitivity were analyzed by RT-PCR. MCF7/T cells became more sensitive to 5-fluorouracil than wild-type (wt)-MCF7 cells. In addition, the apoptosis induced by 5-fluorouracil was significantly increased in MCF7/T cells. However, no difference in sensitivity to chemotherapeutic agents was observed in T47D/T and BT474/T cells compared with their wt cells. Dihydropyrimidine dehydrogenase (DPYD) mRNA expression was significantly decreased in MCF7/T cells compared with wt-MCF7 cells. The expression of DPYD mRNA was restored with 5-azacytidine treatment in MCF7/T cells. In addition, DPYD 3'-UTR luciferase activity was significantly reduced in MCF7/T cells. These data indicated that the expression of DPYD mRNA was repressed by methylation of the DPYD promoter region and post-transcriptional regulation by miRNA in MCF7/T cells. In the mouse xenograft model, capecitabine significantly reduced the tumor volume in MCF7/T compared with MCF7. The results of this study indicate that endocrine therapy could alter the sensitivity to chemotherapeutic agents in a subset of breast cancers, and 5-fluorouracil may be effective in tamoxifen-resistant breast cancers.</description><subject>5-Fluorouracil</subject><subject>Animals</subject><subject>Anthracycline</subject><subject>Antibodies</subject><subject>Anticancer properties</subject><subject>Antimetabolites, Antineoplastic - pharmacology</subject><subject>Antineoplastic Agents, Hormonal - pharmacology</subject><subject>Antitumor agents</subject><subject>Apoptosis</subject><subject>Apoptosis - drug effects</subject><subject>Aromatase</subject><subject>Auroral kilometric radiation</subject><subject>Biology</subject><subject>Biology and Life Sciences</subject><subject>Biomarkers</subject><subject>Breast cancer</subject><subject>Breast Neoplasms - drug therapy</subject><subject>Breast Neoplasms - genetics</subject><subject>Breast Neoplasms - metabolism</subject><subject>Cancer therapies</subject><subject>Capecitabine - 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Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Advanced Technologies & Aerospace Database</collection><collection>ProQuest Advanced Technologies & Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content 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>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Watanabe, Takayuki</au><au>Oba, Takaaki</au><au>Tanimoto, Keiji</au><au>Shibata, Tomohiro</au><au>Kamijo, Shinobu</au><au>Ito, Ken-Ichi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Tamoxifen resistance alters sensitivity to 5-fluorouracil in a subset of estrogen receptor-positive breast cancer</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2021-06-08</date><risdate>2021</risdate><volume>16</volume><issue>6</issue><spage>e0252822</spage><pages>e0252822-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Sequential treatment with endocrine or chemotherapy is generally used in the treatment of estrogen receptor (ER)-positive recurrent breast cancer. To date, few studies have investigated the effect of long-term endocrine therapy on the response to subsequent chemotherapy in ER-positive breast cancer. We examined whether a preceding endocrine therapy affects the sensitivity to subsequent chemotherapy in ER-positive breast cancer cells. Three ER-positive breast cancer cell lines (T47D, MCF7, BT474) and tamoxifen-resistant sublines (T47D/T, MCF7/T, BT474/T) were analyzed for sensitivity to 5-fluorouracil, paclitaxel, and doxorubicin. The mRNA levels of factors related to drug sensitivity were analyzed by RT-PCR. MCF7/T cells became more sensitive to 5-fluorouracil than wild-type (wt)-MCF7 cells. In addition, the apoptosis induced by 5-fluorouracil was significantly increased in MCF7/T cells. However, no difference in sensitivity to chemotherapeutic agents was observed in T47D/T and BT474/T cells compared with their wt cells. Dihydropyrimidine dehydrogenase (DPYD) mRNA expression was significantly decreased in MCF7/T cells compared with wt-MCF7 cells. The expression of DPYD mRNA was restored with 5-azacytidine treatment in MCF7/T cells. In addition, DPYD 3'-UTR luciferase activity was significantly reduced in MCF7/T cells. These data indicated that the expression of DPYD mRNA was repressed by methylation of the DPYD promoter region and post-transcriptional regulation by miRNA in MCF7/T cells. In the mouse xenograft model, capecitabine significantly reduced the tumor volume in MCF7/T compared with MCF7. The results of this study indicate that endocrine therapy could alter the sensitivity to chemotherapeutic agents in a subset of breast cancers, and 5-fluorouracil may be effective in tamoxifen-resistant breast cancers.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>34101751</pmid><doi>10.1371/journal.pone.0252822</doi><tpages>e0252822</tpages><orcidid>https://orcid.org/0000-0002-6430-0307</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2021-06, Vol.16 (6), p.e0252822 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_2539284861 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | 5-Fluorouracil Animals Anthracycline Antibodies Anticancer properties Antimetabolites, Antineoplastic - pharmacology Antineoplastic Agents, Hormonal - pharmacology Antitumor agents Apoptosis Apoptosis - drug effects Aromatase Auroral kilometric radiation Biology Biology and Life Sciences Biomarkers Breast cancer Breast Neoplasms - drug therapy Breast Neoplasms - genetics Breast Neoplasms - metabolism Cancer therapies Capecitabine - pharmacology Cell Line, Tumor Cell Proliferation - drug effects Chemical compounds Chemotherapy Complications and side effects Cyclin-dependent kinase 4 Cyclin-dependent kinases Dehydrogenases Drafting software Drug Resistance, Neoplasm - drug effects Drug Resistance, Neoplasm - genetics Drug therapy Editing Endocrine therapy Estradiol - pharmacology Estrogen receptors Estrogens Estrogens - pharmacology Experiments Female Fluorouracil Fluorouracil - pharmacology Gene expression Humans Inhibitors Kinases MCF-7 Cells Medical research Medicine Medicine and Health Sciences Metastases Metastasis Methodology Mice Mice, Inbred BALB C Mice, Nude Mutation Nuclear medicine Organs Patient outcomes Patients Pharmacology Physical Sciences Poly(ADP-ribose) polymerase Radiation Receptors, Estrogen - metabolism Research and analysis methods Ribose Sensitivity Surgery Tamoxifen Tamoxifen - pharmacology Tumors Xenograft Model Antitumor Assays - methods |
| title | Tamoxifen resistance alters sensitivity to 5-fluorouracil in a subset of estrogen receptor-positive breast cancer |
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