Dynamic color-coded fluorescence imaging of the cell-cycle phase, mitosis, and apoptosis demonstrates how caffeine modulates cisplatinum efficacy
ABSTRACT Caffeine enhances the effect of certain anticancer drugs, but the mechanism of modulation is poorly understood. In this study, modulation of cisplatinum efficacy induced by caffeine was visualized at the subcellular level by real‐time fluorescent‐protein imaging. Mitotic and apoptotic chang...
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| Veröffentlicht in: | Journal of cellular biochemistry 2013-11, Vol.114 (11), p.2454-2460 |
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| creator | Miwa, Shinji Yano, Shuya Tome, Yasunori Sugimoto, Naotoshi Hiroshima, Yukihiko Uehara, Fuminari Mii, Sumiyuki Kimura, Hiroaki Hayashi, Katsuhiro Efimova, Elena V. Fujiwara, Toshiyoshi Tsuchiya, Hiroyuki Hoffman, Robert M. |
| description | ABSTRACT
Caffeine enhances the effect of certain anticancer drugs, but the mechanism of modulation is poorly understood. In this study, modulation of cisplatinum efficacy induced by caffeine was visualized at the subcellular level by real‐time fluorescent‐protein imaging. Mitotic and apoptotic changes were observed by imaging 143B human osteosarcoma dual‐color cells, in which GFP is expressed in the nucleus and RFP is expressed in the cytoplasm. Modulation of the cell cycle was imaged using time‐lapse imaging of HeLa cells expressing a fluorescent ubiquitination‐based cell cycle indicator (FUCCI) in the nucleus. Clonogenic assays showed that caffeine increased the inhibition by cisplatinum on cell proliferation. Subcellular imaging demonstrated that cisplatinum decreased mitosis and induced apoptosis in 143B cells. The combination of cisplatinum and caffeine enhanced mitosis and subsequently increased apoptosis. Time‐lapse imaging showed that cisplatinum strongly induced cell‐cycle arrest in the S/G2 phase in HeLa‐FUCCI cells. Caffeine overcame the cell‐cycle arrest induced by cisplatinum, thereby increasing its efficacy, since cisplatinum is ineffective against quiescent cells. The data in this report indicate that caffeine modulates the cell cycle in cancer cells, thereby enhancing efficacy of cell‐cycle‐dependent anticancer drugs such as cisplatinum. J. Cell. Biochem. 114: 2454–2460, 2013. © 2013 Wiley Periodicals, Inc. |
| doi_str_mv | 10.1002/jcb.24593 |
| format | Article |
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Caffeine enhances the effect of certain anticancer drugs, but the mechanism of modulation is poorly understood. In this study, modulation of cisplatinum efficacy induced by caffeine was visualized at the subcellular level by real‐time fluorescent‐protein imaging. Mitotic and apoptotic changes were observed by imaging 143B human osteosarcoma dual‐color cells, in which GFP is expressed in the nucleus and RFP is expressed in the cytoplasm. Modulation of the cell cycle was imaged using time‐lapse imaging of HeLa cells expressing a fluorescent ubiquitination‐based cell cycle indicator (FUCCI) in the nucleus. Clonogenic assays showed that caffeine increased the inhibition by cisplatinum on cell proliferation. Subcellular imaging demonstrated that cisplatinum decreased mitosis and induced apoptosis in 143B cells. The combination of cisplatinum and caffeine enhanced mitosis and subsequently increased apoptosis. Time‐lapse imaging showed that cisplatinum strongly induced cell‐cycle arrest in the S/G2 phase in HeLa‐FUCCI cells. Caffeine overcame the cell‐cycle arrest induced by cisplatinum, thereby increasing its efficacy, since cisplatinum is ineffective against quiescent cells. The data in this report indicate that caffeine modulates the cell cycle in cancer cells, thereby enhancing efficacy of cell‐cycle‐dependent anticancer drugs such as cisplatinum. J. Cell. Biochem. 114: 2454–2460, 2013. © 2013 Wiley Periodicals, Inc.</description><identifier>ISSN: 0730-2312</identifier><identifier>EISSN: 1097-4644</identifier><identifier>DOI: 10.1002/jcb.24593</identifier><identifier>PMID: 23696238</identifier><language>eng</language><publisher>United States: Blackwell Publishing Ltd</publisher><subject>Antitumor agents ; APOPTOSIS ; Apoptosis - drug effects ; CAFFEINE ; Caffeine - pharmacology ; CELL CYCLE ; Cell Cycle - drug effects ; Cell Line, Tumor ; Cisplatin - pharmacology ; CISPLATINUM ; DNA Damage - drug effects ; Drug Interactions ; FLUORESCENCE IMAGING ; FUCCI ; GFP ; Humans ; Microscopy, Confocal ; MITOSIS ; Mitosis - drug effects ; MODULATION ; OSTEOSARCOMA ; RFP</subject><ispartof>Journal of cellular biochemistry, 2013-11, Vol.114 (11), p.2454-2460</ispartof><rights>2013 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4563-bde2e739586ed05805f14bdbf5f23b222f0a796439941deb16755d38cde6b26f3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1002%2Fjcb.24593$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1002%2Fjcb.24593$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,780,784,1417,27924,27925,45574,45575</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23696238$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miwa, Shinji</creatorcontrib><creatorcontrib>Yano, Shuya</creatorcontrib><creatorcontrib>Tome, Yasunori</creatorcontrib><creatorcontrib>Sugimoto, Naotoshi</creatorcontrib><creatorcontrib>Hiroshima, Yukihiko</creatorcontrib><creatorcontrib>Uehara, Fuminari</creatorcontrib><creatorcontrib>Mii, Sumiyuki</creatorcontrib><creatorcontrib>Kimura, Hiroaki</creatorcontrib><creatorcontrib>Hayashi, Katsuhiro</creatorcontrib><creatorcontrib>Efimova, Elena V.</creatorcontrib><creatorcontrib>Fujiwara, Toshiyoshi</creatorcontrib><creatorcontrib>Tsuchiya, Hiroyuki</creatorcontrib><creatorcontrib>Hoffman, Robert M.</creatorcontrib><title>Dynamic color-coded fluorescence imaging of the cell-cycle phase, mitosis, and apoptosis demonstrates how caffeine modulates cisplatinum efficacy</title><title>Journal of cellular biochemistry</title><addtitle>J. Cell. Biochem</addtitle><description>ABSTRACT
Caffeine enhances the effect of certain anticancer drugs, but the mechanism of modulation is poorly understood. In this study, modulation of cisplatinum efficacy induced by caffeine was visualized at the subcellular level by real‐time fluorescent‐protein imaging. Mitotic and apoptotic changes were observed by imaging 143B human osteosarcoma dual‐color cells, in which GFP is expressed in the nucleus and RFP is expressed in the cytoplasm. Modulation of the cell cycle was imaged using time‐lapse imaging of HeLa cells expressing a fluorescent ubiquitination‐based cell cycle indicator (FUCCI) in the nucleus. Clonogenic assays showed that caffeine increased the inhibition by cisplatinum on cell proliferation. Subcellular imaging demonstrated that cisplatinum decreased mitosis and induced apoptosis in 143B cells. The combination of cisplatinum and caffeine enhanced mitosis and subsequently increased apoptosis. Time‐lapse imaging showed that cisplatinum strongly induced cell‐cycle arrest in the S/G2 phase in HeLa‐FUCCI cells. Caffeine overcame the cell‐cycle arrest induced by cisplatinum, thereby increasing its efficacy, since cisplatinum is ineffective against quiescent cells. The data in this report indicate that caffeine modulates the cell cycle in cancer cells, thereby enhancing efficacy of cell‐cycle‐dependent anticancer drugs such as cisplatinum. J. Cell. Biochem. 114: 2454–2460, 2013. © 2013 Wiley Periodicals, Inc.</description><subject>Antitumor agents</subject><subject>APOPTOSIS</subject><subject>Apoptosis - drug effects</subject><subject>CAFFEINE</subject><subject>Caffeine - pharmacology</subject><subject>CELL CYCLE</subject><subject>Cell Cycle - drug effects</subject><subject>Cell Line, Tumor</subject><subject>Cisplatin - pharmacology</subject><subject>CISPLATINUM</subject><subject>DNA Damage - drug effects</subject><subject>Drug Interactions</subject><subject>FLUORESCENCE IMAGING</subject><subject>FUCCI</subject><subject>GFP</subject><subject>Humans</subject><subject>Microscopy, Confocal</subject><subject>MITOSIS</subject><subject>Mitosis - drug effects</subject><subject>MODULATION</subject><subject>OSTEOSARCOMA</subject><subject>RFP</subject><issn>0730-2312</issn><issn>1097-4644</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkctu1DAUhi0EokNhwQsgS2y6aFrfkyxheoGqAqkCwc5y7OOOhyQOcaKSx-gbk8mULrpidW7ff6RzfoTeUnJCCWGnW1udMCFL_gytKCnzTCghnqMVyTnJGKfsAL1KaUsIKUvOXqIDxlWpGC9W6P5sak0TLLaxjn1mowOHfT3GHpKF1gIOjbkN7S2OHg8bwBbqOrOTrQF3G5PgGDdhiCmkY2xah00Xu6XEDprYpqE3AyS8iXfYGu8htICb6MZ6aduQujkL7dhg8D5YY6fX6IU3dYI3D_EQfb84_7b-lF1_vfy8_nCdWSEVzyoHDHJeykKBI7Ig0lNRucpLz3jFGPPE5KUSvCwFdVBRlUvpeGEdqIopzw_R0X5v18ffI6RBNyHtrjMtxDFpOksZI0qS_0GZolIU-Yy-f4Ju49i38yELRZgq6I5690CNVQNOd_385X7S_3yZgdM9cBdqmB7nlOid4Xo2XC-G66v1xyWZFdleEdIAfx4Vpv-lVc5zqX98udT8pzpjQt3oG_4XlvqtVg</recordid><startdate>201311</startdate><enddate>201311</enddate><creator>Miwa, Shinji</creator><creator>Yano, Shuya</creator><creator>Tome, Yasunori</creator><creator>Sugimoto, Naotoshi</creator><creator>Hiroshima, Yukihiko</creator><creator>Uehara, Fuminari</creator><creator>Mii, Sumiyuki</creator><creator>Kimura, Hiroaki</creator><creator>Hayashi, Katsuhiro</creator><creator>Efimova, Elena V.</creator><creator>Fujiwara, Toshiyoshi</creator><creator>Tsuchiya, Hiroyuki</creator><creator>Hoffman, Robert M.</creator><general>Blackwell Publishing Ltd</general><general>Wiley Subscription Services, Inc</general><scope>BSCLL</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7T7</scope><scope>7TK</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>K9.</scope><scope>M7N</scope><scope>P64</scope><scope>7X8</scope><scope>RC3</scope></search><sort><creationdate>201311</creationdate><title>Dynamic color-coded fluorescence imaging of the cell-cycle phase, mitosis, and apoptosis demonstrates how caffeine modulates cisplatinum efficacy</title><author>Miwa, Shinji ; Yano, Shuya ; Tome, Yasunori ; Sugimoto, Naotoshi ; Hiroshima, Yukihiko ; Uehara, Fuminari ; Mii, Sumiyuki ; Kimura, Hiroaki ; Hayashi, Katsuhiro ; Efimova, Elena V. ; Fujiwara, Toshiyoshi ; Tsuchiya, Hiroyuki ; Hoffman, Robert M.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4563-bde2e739586ed05805f14bdbf5f23b222f0a796439941deb16755d38cde6b26f3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Antitumor agents</topic><topic>APOPTOSIS</topic><topic>Apoptosis - drug effects</topic><topic>CAFFEINE</topic><topic>Caffeine - pharmacology</topic><topic>CELL CYCLE</topic><topic>Cell Cycle - drug effects</topic><topic>Cell Line, Tumor</topic><topic>Cisplatin - pharmacology</topic><topic>CISPLATINUM</topic><topic>DNA Damage - drug effects</topic><topic>Drug Interactions</topic><topic>FLUORESCENCE IMAGING</topic><topic>FUCCI</topic><topic>GFP</topic><topic>Humans</topic><topic>Microscopy, Confocal</topic><topic>MITOSIS</topic><topic>Mitosis - drug effects</topic><topic>MODULATION</topic><topic>OSTEOSARCOMA</topic><topic>RFP</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Miwa, Shinji</creatorcontrib><creatorcontrib>Yano, Shuya</creatorcontrib><creatorcontrib>Tome, Yasunori</creatorcontrib><creatorcontrib>Sugimoto, Naotoshi</creatorcontrib><creatorcontrib>Hiroshima, Yukihiko</creatorcontrib><creatorcontrib>Uehara, Fuminari</creatorcontrib><creatorcontrib>Mii, Sumiyuki</creatorcontrib><creatorcontrib>Kimura, Hiroaki</creatorcontrib><creatorcontrib>Hayashi, Katsuhiro</creatorcontrib><creatorcontrib>Efimova, Elena V.</creatorcontrib><creatorcontrib>Fujiwara, Toshiyoshi</creatorcontrib><creatorcontrib>Tsuchiya, Hiroyuki</creatorcontrib><creatorcontrib>Hoffman, Robert M.</creatorcontrib><collection>Istex</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Neurosciences Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Genetics Abstracts</collection><jtitle>Journal of cellular biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Miwa, Shinji</au><au>Yano, Shuya</au><au>Tome, Yasunori</au><au>Sugimoto, Naotoshi</au><au>Hiroshima, Yukihiko</au><au>Uehara, Fuminari</au><au>Mii, Sumiyuki</au><au>Kimura, Hiroaki</au><au>Hayashi, Katsuhiro</au><au>Efimova, Elena V.</au><au>Fujiwara, Toshiyoshi</au><au>Tsuchiya, Hiroyuki</au><au>Hoffman, Robert M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Dynamic color-coded fluorescence imaging of the cell-cycle phase, mitosis, and apoptosis demonstrates how caffeine modulates cisplatinum efficacy</atitle><jtitle>Journal of cellular biochemistry</jtitle><addtitle>J. Cell. Biochem</addtitle><date>2013-11</date><risdate>2013</risdate><volume>114</volume><issue>11</issue><spage>2454</spage><epage>2460</epage><pages>2454-2460</pages><issn>0730-2312</issn><eissn>1097-4644</eissn><abstract>ABSTRACT
Caffeine enhances the effect of certain anticancer drugs, but the mechanism of modulation is poorly understood. In this study, modulation of cisplatinum efficacy induced by caffeine was visualized at the subcellular level by real‐time fluorescent‐protein imaging. Mitotic and apoptotic changes were observed by imaging 143B human osteosarcoma dual‐color cells, in which GFP is expressed in the nucleus and RFP is expressed in the cytoplasm. Modulation of the cell cycle was imaged using time‐lapse imaging of HeLa cells expressing a fluorescent ubiquitination‐based cell cycle indicator (FUCCI) in the nucleus. Clonogenic assays showed that caffeine increased the inhibition by cisplatinum on cell proliferation. Subcellular imaging demonstrated that cisplatinum decreased mitosis and induced apoptosis in 143B cells. The combination of cisplatinum and caffeine enhanced mitosis and subsequently increased apoptosis. Time‐lapse imaging showed that cisplatinum strongly induced cell‐cycle arrest in the S/G2 phase in HeLa‐FUCCI cells. Caffeine overcame the cell‐cycle arrest induced by cisplatinum, thereby increasing its efficacy, since cisplatinum is ineffective against quiescent cells. The data in this report indicate that caffeine modulates the cell cycle in cancer cells, thereby enhancing efficacy of cell‐cycle‐dependent anticancer drugs such as cisplatinum. J. Cell. Biochem. 114: 2454–2460, 2013. © 2013 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>Blackwell Publishing Ltd</pub><pmid>23696238</pmid><doi>10.1002/jcb.24593</doi><tpages>7</tpages></addata></record> |
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| subjects | Antitumor agents APOPTOSIS Apoptosis - drug effects CAFFEINE Caffeine - pharmacology CELL CYCLE Cell Cycle - drug effects Cell Line, Tumor Cisplatin - pharmacology CISPLATINUM DNA Damage - drug effects Drug Interactions FLUORESCENCE IMAGING FUCCI GFP Humans Microscopy, Confocal MITOSIS Mitosis - drug effects MODULATION OSTEOSARCOMA RFP |
| title | Dynamic color-coded fluorescence imaging of the cell-cycle phase, mitosis, and apoptosis demonstrates how caffeine modulates cisplatinum efficacy |
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