Ceramide Glycosylation by Glucosylceramide Synthase Selectively Maintains the Properties of Breast Cancer Stem Cells
Cancer stem cells are distinguished from normal adult stem cells by their stemness without tissue homeostasis control. Glycosphingolipids (GSLs), particularly globo-series GSLs, are important markers of undifferentiated embryonic stem cells, but little is known about whether or not ceramide glycosyl...
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| Veröffentlicht in: | The Journal of biological chemistry 2012-10, Vol.287 (44), p.37195-37205 |
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| creator | Gupta, Vineet Bhinge, Kaustubh N. Hosain, Salman B. Xiong, Katherine Gu, Xin Shi, Runhua Ho, Ming-Yi Khoo, Kay-Hooi Li, Su-Chen Li, Yu-Teh Ambudkar, Suresh V. Jazwinski, S.Michal Liu, Yong-Yu |
| description | Cancer stem cells are distinguished from normal adult stem cells by their stemness without tissue homeostasis control. Glycosphingolipids (GSLs), particularly globo-series GSLs, are important markers of undifferentiated embryonic stem cells, but little is known about whether or not ceramide glycosylation, which controls glycosphingolipid synthesis, plays a role in modulating stem cells. Here, we report that ceramide glycosylation catalyzed by glucosylceramide synthase, which is enhanced in breast cancer stem cells (BCSCs) but not in normal mammary epithelial stem cells, maintains tumorous pluripotency of BCSCs. Enhanced ceramide glycosylation and globotriosylceramide (Gb3) correlate well with the numbers of BCSCs in breast cancer cell lines. In BCSCs sorted with CD44+/ESA+/CD24− markers, Gb3 activates c-Src/β-catenin signaling and up-regulates the expression of FGF-2, CD44, and Oct-4 enriching tumorigenesis. Conversely, silencing glucosylceramide synthase expression disrupts Gb3 synthesis and selectively kills BCSCs through deactivation of c-Src/β-catenin signaling. These findings highlight the unexploited role of ceramide glycosylation in selectively maintaining the tumorous pluripotency of cancer stem cells. It speculates that disruption of ceramide glycosylation or globo-series GSL is a useful approach to specifically target BCSCs specifically.
Background: Glucosylceramide synthase catalyzes ceramide glycosylation that regulates the synthesis of glycosphingolipids.
Results: Increased globo-series glycosphingolipids in breast cancer stem cells activate c-Src signaling and β-catenin-mediated transcription up-regulating stem cell factors.
Conclusion: Ceramide glycosylation maintains the stemness of cancer stem cells.
Significance: Glycosphingolipids in cell membrane actively participate in maintaining cancer stem cells. |
| doi_str_mv | 10.1074/jbc.M112.396390 |
| format | Article |
| fullrecord | <record><control><sourceid>pubmed_cross</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_3481319</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0021925820625194</els_id><sourcerecordid>22936806</sourcerecordid><originalsourceid>FETCH-LOGICAL-c443t-a3bfaa235b6a641244a33c3290fb5ce0bcc66791594351b7dcb7dd68f3c775cc3</originalsourceid><addsrcrecordid>eNp1UU1LAzEQDaJo_Th7k_yBbZNN9iMXQRetQkWhCt5CNjtrI9vdkqSF_femri16MDBkmHnzhnkPoUtKxpRkfPJZ6vETpfGYiZQJcoBGlOQsYgl9P0QjQmIaiTjJT9Cpc58kPC7oMTqJY8HSnKQj5AuwamkqwNOm153rG-VN1-KyD4X1d0HvEPO-9QvlQgINaG820PT4SZnWh3DYLwC_2G4F1htwuKvxrQXlPC5UGzjw3MMSF9A07hwd1apxcPHzn6G3-7vX4iGaPU8fi5tZpDlnPlKsrJWKWVKmKuU05lwxplksSF0mGkipdZpmgiaCh4PLrNIhqjSvmc6yRGt2hq4H3tW6XEKlofVWNXJlzVLZXnbKyL-d1izkR7eRjOeUUREIJgOBtp1zFur9LCVya4AMBsitAXIwIExc_V65x-8UDwAxACAcvjFgpdMGgkCVsUFUWXXmX_IvgaWY6w</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>Ceramide Glycosylation by Glucosylceramide Synthase Selectively Maintains the Properties of Breast Cancer Stem Cells</title><source>MEDLINE</source><source>EZB-FREE-00999 freely available EZB journals</source><source>PubMed Central</source><source>Alma/SFX Local Collection</source><creator>Gupta, Vineet ; Bhinge, Kaustubh N. ; Hosain, Salman B. ; Xiong, Katherine ; Gu, Xin ; Shi, Runhua ; Ho, Ming-Yi ; Khoo, Kay-Hooi ; Li, Su-Chen ; Li, Yu-Teh ; Ambudkar, Suresh V. ; Jazwinski, S.Michal ; Liu, Yong-Yu</creator><creatorcontrib>Gupta, Vineet ; Bhinge, Kaustubh N. ; Hosain, Salman B. ; Xiong, Katherine ; Gu, Xin ; Shi, Runhua ; Ho, Ming-Yi ; Khoo, Kay-Hooi ; Li, Su-Chen ; Li, Yu-Teh ; Ambudkar, Suresh V. ; Jazwinski, S.Michal ; Liu, Yong-Yu</creatorcontrib><description>Cancer stem cells are distinguished from normal adult stem cells by their stemness without tissue homeostasis control. Glycosphingolipids (GSLs), particularly globo-series GSLs, are important markers of undifferentiated embryonic stem cells, but little is known about whether or not ceramide glycosylation, which controls glycosphingolipid synthesis, plays a role in modulating stem cells. Here, we report that ceramide glycosylation catalyzed by glucosylceramide synthase, which is enhanced in breast cancer stem cells (BCSCs) but not in normal mammary epithelial stem cells, maintains tumorous pluripotency of BCSCs. Enhanced ceramide glycosylation and globotriosylceramide (Gb3) correlate well with the numbers of BCSCs in breast cancer cell lines. In BCSCs sorted with CD44+/ESA+/CD24− markers, Gb3 activates c-Src/β-catenin signaling and up-regulates the expression of FGF-2, CD44, and Oct-4 enriching tumorigenesis. Conversely, silencing glucosylceramide synthase expression disrupts Gb3 synthesis and selectively kills BCSCs through deactivation of c-Src/β-catenin signaling. These findings highlight the unexploited role of ceramide glycosylation in selectively maintaining the tumorous pluripotency of cancer stem cells. It speculates that disruption of ceramide glycosylation or globo-series GSL is a useful approach to specifically target BCSCs specifically.
Background: Glucosylceramide synthase catalyzes ceramide glycosylation that regulates the synthesis of glycosphingolipids.
Results: Increased globo-series glycosphingolipids in breast cancer stem cells activate c-Src signaling and β-catenin-mediated transcription up-regulating stem cell factors.
Conclusion: Ceramide glycosylation maintains the stemness of cancer stem cells.
Significance: Glycosphingolipids in cell membrane actively participate in maintaining cancer stem cells.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M112.396390</identifier><identifier>PMID: 22936806</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Animals ; Antibiotics, Antineoplastic - pharmacology ; beta Catenin - metabolism ; Breast Neoplasms - enzymology ; Breast Neoplasms - pathology ; Cancer ; Catenin ; CD24 Antigen - metabolism ; Cell Biology ; Cell Separation ; Cell Survival - drug effects ; Cell Transformation, Neoplastic ; Ceramides - metabolism ; Doxorubicin - pharmacology ; Drug Resistance, Neoplasm ; Female ; Glucosylceramide Synthase ; Glucosyltransferases - metabolism ; Glycerosphingolipid ; Glycosylation ; Humans ; Hyaluronan Receptors - metabolism ; Immunomagnetic Separation ; MCF-7 Cells ; Mice ; Mice, Nude ; Neoplasm Transplantation ; Neoplastic Stem Cells - enzymology ; Neoplastic Stem Cells - metabolism ; Neoplastic Stem Cells - pathology ; Protein Processing, Post-Translational ; Signal Transduction ; Spheroids, Cellular - drug effects ; Src ; Stem Cells</subject><ispartof>The Journal of biological chemistry, 2012-10, Vol.287 (44), p.37195-37205</ispartof><rights>2012 © 2012 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2012 by The American Society for Biochemistry and Molecular Biology, Inc. 2012</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c443t-a3bfaa235b6a641244a33c3290fb5ce0bcc66791594351b7dcb7dd68f3c775cc3</citedby><cites>FETCH-LOGICAL-c443t-a3bfaa235b6a641244a33c3290fb5ce0bcc66791594351b7dcb7dd68f3c775cc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3481319/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3481319/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27922,27923,53789,53791</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/22936806$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gupta, Vineet</creatorcontrib><creatorcontrib>Bhinge, Kaustubh N.</creatorcontrib><creatorcontrib>Hosain, Salman B.</creatorcontrib><creatorcontrib>Xiong, Katherine</creatorcontrib><creatorcontrib>Gu, Xin</creatorcontrib><creatorcontrib>Shi, Runhua</creatorcontrib><creatorcontrib>Ho, Ming-Yi</creatorcontrib><creatorcontrib>Khoo, Kay-Hooi</creatorcontrib><creatorcontrib>Li, Su-Chen</creatorcontrib><creatorcontrib>Li, Yu-Teh</creatorcontrib><creatorcontrib>Ambudkar, Suresh V.</creatorcontrib><creatorcontrib>Jazwinski, S.Michal</creatorcontrib><creatorcontrib>Liu, Yong-Yu</creatorcontrib><title>Ceramide Glycosylation by Glucosylceramide Synthase Selectively Maintains the Properties of Breast Cancer Stem Cells</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Cancer stem cells are distinguished from normal adult stem cells by their stemness without tissue homeostasis control. Glycosphingolipids (GSLs), particularly globo-series GSLs, are important markers of undifferentiated embryonic stem cells, but little is known about whether or not ceramide glycosylation, which controls glycosphingolipid synthesis, plays a role in modulating stem cells. Here, we report that ceramide glycosylation catalyzed by glucosylceramide synthase, which is enhanced in breast cancer stem cells (BCSCs) but not in normal mammary epithelial stem cells, maintains tumorous pluripotency of BCSCs. Enhanced ceramide glycosylation and globotriosylceramide (Gb3) correlate well with the numbers of BCSCs in breast cancer cell lines. In BCSCs sorted with CD44+/ESA+/CD24− markers, Gb3 activates c-Src/β-catenin signaling and up-regulates the expression of FGF-2, CD44, and Oct-4 enriching tumorigenesis. Conversely, silencing glucosylceramide synthase expression disrupts Gb3 synthesis and selectively kills BCSCs through deactivation of c-Src/β-catenin signaling. These findings highlight the unexploited role of ceramide glycosylation in selectively maintaining the tumorous pluripotency of cancer stem cells. It speculates that disruption of ceramide glycosylation or globo-series GSL is a useful approach to specifically target BCSCs specifically.
Background: Glucosylceramide synthase catalyzes ceramide glycosylation that regulates the synthesis of glycosphingolipids.
Results: Increased globo-series glycosphingolipids in breast cancer stem cells activate c-Src signaling and β-catenin-mediated transcription up-regulating stem cell factors.
Conclusion: Ceramide glycosylation maintains the stemness of cancer stem cells.
Significance: Glycosphingolipids in cell membrane actively participate in maintaining cancer stem cells.</description><subject>Animals</subject><subject>Antibiotics, Antineoplastic - pharmacology</subject><subject>beta Catenin - metabolism</subject><subject>Breast Neoplasms - enzymology</subject><subject>Breast Neoplasms - pathology</subject><subject>Cancer</subject><subject>Catenin</subject><subject>CD24 Antigen - metabolism</subject><subject>Cell Biology</subject><subject>Cell Separation</subject><subject>Cell Survival - drug effects</subject><subject>Cell Transformation, Neoplastic</subject><subject>Ceramides - metabolism</subject><subject>Doxorubicin - pharmacology</subject><subject>Drug Resistance, Neoplasm</subject><subject>Female</subject><subject>Glucosylceramide Synthase</subject><subject>Glucosyltransferases - metabolism</subject><subject>Glycerosphingolipid</subject><subject>Glycosylation</subject><subject>Humans</subject><subject>Hyaluronan Receptors - metabolism</subject><subject>Immunomagnetic Separation</subject><subject>MCF-7 Cells</subject><subject>Mice</subject><subject>Mice, Nude</subject><subject>Neoplasm Transplantation</subject><subject>Neoplastic Stem Cells - enzymology</subject><subject>Neoplastic Stem Cells - metabolism</subject><subject>Neoplastic Stem Cells - pathology</subject><subject>Protein Processing, Post-Translational</subject><subject>Signal Transduction</subject><subject>Spheroids, Cellular - drug effects</subject><subject>Src</subject><subject>Stem Cells</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1UU1LAzEQDaJo_Th7k_yBbZNN9iMXQRetQkWhCt5CNjtrI9vdkqSF_femri16MDBkmHnzhnkPoUtKxpRkfPJZ6vETpfGYiZQJcoBGlOQsYgl9P0QjQmIaiTjJT9Cpc58kPC7oMTqJY8HSnKQj5AuwamkqwNOm153rG-VN1-KyD4X1d0HvEPO-9QvlQgINaG820PT4SZnWh3DYLwC_2G4F1htwuKvxrQXlPC5UGzjw3MMSF9A07hwd1apxcPHzn6G3-7vX4iGaPU8fi5tZpDlnPlKsrJWKWVKmKuU05lwxplksSF0mGkipdZpmgiaCh4PLrNIhqjSvmc6yRGt2hq4H3tW6XEKlofVWNXJlzVLZXnbKyL-d1izkR7eRjOeUUREIJgOBtp1zFur9LCVya4AMBsitAXIwIExc_V65x-8UDwAxACAcvjFgpdMGgkCVsUFUWXXmX_IvgaWY6w</recordid><startdate>20121026</startdate><enddate>20121026</enddate><creator>Gupta, Vineet</creator><creator>Bhinge, Kaustubh N.</creator><creator>Hosain, Salman B.</creator><creator>Xiong, Katherine</creator><creator>Gu, Xin</creator><creator>Shi, Runhua</creator><creator>Ho, Ming-Yi</creator><creator>Khoo, Kay-Hooi</creator><creator>Li, Su-Chen</creator><creator>Li, Yu-Teh</creator><creator>Ambudkar, Suresh V.</creator><creator>Jazwinski, S.Michal</creator><creator>Liu, Yong-Yu</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><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>5PM</scope></search><sort><creationdate>20121026</creationdate><title>Ceramide Glycosylation by Glucosylceramide Synthase Selectively Maintains the Properties of Breast Cancer Stem Cells</title><author>Gupta, Vineet ; Bhinge, Kaustubh N. ; Hosain, Salman B. ; Xiong, Katherine ; Gu, Xin ; Shi, Runhua ; Ho, Ming-Yi ; Khoo, Kay-Hooi ; Li, Su-Chen ; Li, Yu-Teh ; Ambudkar, Suresh V. ; Jazwinski, S.Michal ; Liu, Yong-Yu</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c443t-a3bfaa235b6a641244a33c3290fb5ce0bcc66791594351b7dcb7dd68f3c775cc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Animals</topic><topic>Antibiotics, Antineoplastic - pharmacology</topic><topic>beta Catenin - metabolism</topic><topic>Breast Neoplasms - enzymology</topic><topic>Breast Neoplasms - pathology</topic><topic>Cancer</topic><topic>Catenin</topic><topic>CD24 Antigen - metabolism</topic><topic>Cell Biology</topic><topic>Cell Separation</topic><topic>Cell Survival - drug effects</topic><topic>Cell Transformation, Neoplastic</topic><topic>Ceramides - metabolism</topic><topic>Doxorubicin - pharmacology</topic><topic>Drug Resistance, Neoplasm</topic><topic>Female</topic><topic>Glucosylceramide Synthase</topic><topic>Glucosyltransferases - metabolism</topic><topic>Glycerosphingolipid</topic><topic>Glycosylation</topic><topic>Humans</topic><topic>Hyaluronan Receptors - metabolism</topic><topic>Immunomagnetic Separation</topic><topic>MCF-7 Cells</topic><topic>Mice</topic><topic>Mice, Nude</topic><topic>Neoplasm Transplantation</topic><topic>Neoplastic Stem Cells - enzymology</topic><topic>Neoplastic Stem Cells - metabolism</topic><topic>Neoplastic Stem Cells - pathology</topic><topic>Protein Processing, Post-Translational</topic><topic>Signal Transduction</topic><topic>Spheroids, Cellular - drug effects</topic><topic>Src</topic><topic>Stem Cells</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gupta, Vineet</creatorcontrib><creatorcontrib>Bhinge, Kaustubh N.</creatorcontrib><creatorcontrib>Hosain, Salman B.</creatorcontrib><creatorcontrib>Xiong, Katherine</creatorcontrib><creatorcontrib>Gu, Xin</creatorcontrib><creatorcontrib>Shi, Runhua</creatorcontrib><creatorcontrib>Ho, Ming-Yi</creatorcontrib><creatorcontrib>Khoo, Kay-Hooi</creatorcontrib><creatorcontrib>Li, Su-Chen</creatorcontrib><creatorcontrib>Li, Yu-Teh</creatorcontrib><creatorcontrib>Ambudkar, Suresh V.</creatorcontrib><creatorcontrib>Jazwinski, S.Michal</creatorcontrib><creatorcontrib>Liu, Yong-Yu</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of biological chemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gupta, Vineet</au><au>Bhinge, Kaustubh N.</au><au>Hosain, Salman B.</au><au>Xiong, Katherine</au><au>Gu, Xin</au><au>Shi, Runhua</au><au>Ho, Ming-Yi</au><au>Khoo, Kay-Hooi</au><au>Li, Su-Chen</au><au>Li, Yu-Teh</au><au>Ambudkar, Suresh V.</au><au>Jazwinski, S.Michal</au><au>Liu, Yong-Yu</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ceramide Glycosylation by Glucosylceramide Synthase Selectively Maintains the Properties of Breast Cancer Stem Cells</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2012-10-26</date><risdate>2012</risdate><volume>287</volume><issue>44</issue><spage>37195</spage><epage>37205</epage><pages>37195-37205</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Cancer stem cells are distinguished from normal adult stem cells by their stemness without tissue homeostasis control. Glycosphingolipids (GSLs), particularly globo-series GSLs, are important markers of undifferentiated embryonic stem cells, but little is known about whether or not ceramide glycosylation, which controls glycosphingolipid synthesis, plays a role in modulating stem cells. Here, we report that ceramide glycosylation catalyzed by glucosylceramide synthase, which is enhanced in breast cancer stem cells (BCSCs) but not in normal mammary epithelial stem cells, maintains tumorous pluripotency of BCSCs. Enhanced ceramide glycosylation and globotriosylceramide (Gb3) correlate well with the numbers of BCSCs in breast cancer cell lines. In BCSCs sorted with CD44+/ESA+/CD24− markers, Gb3 activates c-Src/β-catenin signaling and up-regulates the expression of FGF-2, CD44, and Oct-4 enriching tumorigenesis. Conversely, silencing glucosylceramide synthase expression disrupts Gb3 synthesis and selectively kills BCSCs through deactivation of c-Src/β-catenin signaling. These findings highlight the unexploited role of ceramide glycosylation in selectively maintaining the tumorous pluripotency of cancer stem cells. It speculates that disruption of ceramide glycosylation or globo-series GSL is a useful approach to specifically target BCSCs specifically.
Background: Glucosylceramide synthase catalyzes ceramide glycosylation that regulates the synthesis of glycosphingolipids.
Results: Increased globo-series glycosphingolipids in breast cancer stem cells activate c-Src signaling and β-catenin-mediated transcription up-regulating stem cell factors.
Conclusion: Ceramide glycosylation maintains the stemness of cancer stem cells.
Significance: Glycosphingolipids in cell membrane actively participate in maintaining cancer stem cells.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>22936806</pmid><doi>10.1074/jbc.M112.396390</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| ispartof | The Journal of biological chemistry, 2012-10, Vol.287 (44), p.37195-37205 |
| issn | 0021-9258 1083-351X |
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| subjects | Animals Antibiotics, Antineoplastic - pharmacology beta Catenin - metabolism Breast Neoplasms - enzymology Breast Neoplasms - pathology Cancer Catenin CD24 Antigen - metabolism Cell Biology Cell Separation Cell Survival - drug effects Cell Transformation, Neoplastic Ceramides - metabolism Doxorubicin - pharmacology Drug Resistance, Neoplasm Female Glucosylceramide Synthase Glucosyltransferases - metabolism Glycerosphingolipid Glycosylation Humans Hyaluronan Receptors - metabolism Immunomagnetic Separation MCF-7 Cells Mice Mice, Nude Neoplasm Transplantation Neoplastic Stem Cells - enzymology Neoplastic Stem Cells - metabolism Neoplastic Stem Cells - pathology Protein Processing, Post-Translational Signal Transduction Spheroids, Cellular - drug effects Src Stem Cells |
| title | Ceramide Glycosylation by Glucosylceramide Synthase Selectively Maintains the Properties of Breast Cancer Stem Cells |
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