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EZH2 Regulates Neuronal Differentiation of Mesenchymal Stem Cells through PIP5K1C-dependent Calcium Signaling
Enhancer of zeste homolog 2 (EZH2) regulates stem cells renewal, maintenance, and differentiation into different cell lineages including neuron. Changes in intracellular Ca2+ concentration play a critical role in the differentiation of neurons. However, whether EZH2 modulates intracellular Ca2+ sign...
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Published in: | The Journal of biological chemistry 2011-03, Vol.286 (11), p.9657-9667 |
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creator | Yu, Yung-Luen Chou, Ruey-Hwang Chen, Ling-Tzu Shyu, Woei-Cherng Hsieh, Su-Ching Wu, Chen-Shiou Zeng, Hong-Jie Yeh, Su-Peng Yang, De-Ming Hung, Shih-Chieh Hung, Mien-Chie |
description | Enhancer of zeste homolog 2 (EZH2) regulates stem cells renewal, maintenance, and differentiation into different cell lineages including neuron. Changes in intracellular Ca2+ concentration play a critical role in the differentiation of neurons. However, whether EZH2 modulates intracellular Ca2+ signaling in regulating neuronal differentiation from human mesenchymal stem cells (hMSCs) still remains unclear. When hMSCs were treated with a Ca2+ chelator or a PLC inhibitor to block IP3-mediated Ca2+ signaling, neuronal differentiation was disrupted. EZH2 bound to the promoter region of PIP5K1C to suppress its transcription in proliferating hMSCs. Interestingly, knockdown of EZH2 enhanced the expression of PIP5K1C, which in turn increased the amount of PI(4,5)P2, a precursor of IP3, and resulted in increasing the intracellular Ca2+ level, suggesting that EZH2 negatively regulates intracellular Ca2+ through suppression of PIP5K1C. Knockdown of EZH2 also enhanced hMSCs differentiation into functional neuron both in vitro and in vivo. In contrast, knockdown of PIP5K1C significantly reduced PI(4,5)P2 contents and intracellular Ca2+ release in EZH2-silenced cells and resulted in the disruption of neuronal differentiation from hMSCs. Here, we provide the first evidence to demonstrate that after induction to neuronal differentiation, decreased EZH2 activates the expression of PIP5K1C to evoke intracellular Ca2+ signaling, which leads hMSCs to differentiate into functional neuron lineage. Activation of intracellular Ca2+ signaling by repressing or knocking down EZH2 might be a potential strategy to promote neuronal differentiation from hMSCs for application to neurological dysfunction diseases. |
doi_str_mv | 10.1074/jbc.M110.185124 |
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Changes in intracellular Ca2+ concentration play a critical role in the differentiation of neurons. However, whether EZH2 modulates intracellular Ca2+ signaling in regulating neuronal differentiation from human mesenchymal stem cells (hMSCs) still remains unclear. When hMSCs were treated with a Ca2+ chelator or a PLC inhibitor to block IP3-mediated Ca2+ signaling, neuronal differentiation was disrupted. EZH2 bound to the promoter region of PIP5K1C to suppress its transcription in proliferating hMSCs. Interestingly, knockdown of EZH2 enhanced the expression of PIP5K1C, which in turn increased the amount of PI(4,5)P2, a precursor of IP3, and resulted in increasing the intracellular Ca2+ level, suggesting that EZH2 negatively regulates intracellular Ca2+ through suppression of PIP5K1C. Knockdown of EZH2 also enhanced hMSCs differentiation into functional neuron both in vitro and in vivo. In contrast, knockdown of PIP5K1C significantly reduced PI(4,5)P2 contents and intracellular Ca2+ release in EZH2-silenced cells and resulted in the disruption of neuronal differentiation from hMSCs. Here, we provide the first evidence to demonstrate that after induction to neuronal differentiation, decreased EZH2 activates the expression of PIP5K1C to evoke intracellular Ca2+ signaling, which leads hMSCs to differentiate into functional neuron lineage. Activation of intracellular Ca2+ signaling by repressing or knocking down EZH2 might be a potential strategy to promote neuronal differentiation from hMSCs for application to neurological dysfunction diseases.</description><identifier>ISSN: 0021-9258</identifier><identifier>EISSN: 1083-351X</identifier><identifier>DOI: 10.1074/jbc.M110.185124</identifier><identifier>PMID: 21216957</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Calcium ; Calcium - metabolism ; Calcium Signaling - drug effects ; Calcium Signaling - physiology ; Cell Biology ; Cell Differentiation - drug effects ; Cell Differentiation - physiology ; Cells, Cultured ; Chelating Agents - pharmacology ; Differentiation ; DNA-Binding Proteins - genetics ; DNA-Binding Proteins - metabolism ; Enhancer of Zeste Homolog 2 Protein ; EZH2 ; Gene Expression ; Gene Expression Regulation, Enzymologic - drug effects ; Gene Expression Regulation, Enzymologic - physiology ; Gene Knockdown Techniques ; Gene Regulation ; Humans ; Intracellular Calcium ; Mesenchymal Stem Cells ; Mesenchymal Stem Cells - cytology ; Mesenchymal Stem Cells - metabolism ; Nervous System Diseases - genetics ; Nervous System Diseases - metabolism ; Nervous System Diseases - therapy ; Neuron ; Neuronal Differentiation ; Neurons - cytology ; Neurons - metabolism ; Phosphotransferases (Alcohol Group Acceptor) - biosynthesis ; Phosphotransferases (Alcohol Group Acceptor) - genetics ; PIP5K1C ; Polycomb Repressive Complex 2 ; Promoter Regions, Genetic - drug effects ; Promoter Regions, Genetic - physiology ; Transcription Factors - genetics ; Transcription Factors - metabolism</subject><ispartof>The Journal of biological chemistry, 2011-03, Vol.286 (11), p.9657-9667</ispartof><rights>2011 © 2011 ASBMB. Currently published by Elsevier Inc; originally published by American Society for Biochemistry and Molecular Biology.</rights><rights>2011 by The American Society for Biochemistry and Molecular Biology, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c512t-2ba5873617fc85ac494577ff76c33e09710ef7686d75c1f1545223ef445f28373</citedby><cites>FETCH-LOGICAL-c512t-2ba5873617fc85ac494577ff76c33e09710ef7686d75c1f1545223ef445f28373</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/PMC3059014/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0021925820518504$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,3549,27924,27925,45780,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/21216957$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yu, Yung-Luen</creatorcontrib><creatorcontrib>Chou, Ruey-Hwang</creatorcontrib><creatorcontrib>Chen, Ling-Tzu</creatorcontrib><creatorcontrib>Shyu, Woei-Cherng</creatorcontrib><creatorcontrib>Hsieh, Su-Ching</creatorcontrib><creatorcontrib>Wu, Chen-Shiou</creatorcontrib><creatorcontrib>Zeng, Hong-Jie</creatorcontrib><creatorcontrib>Yeh, Su-Peng</creatorcontrib><creatorcontrib>Yang, De-Ming</creatorcontrib><creatorcontrib>Hung, Shih-Chieh</creatorcontrib><creatorcontrib>Hung, Mien-Chie</creatorcontrib><title>EZH2 Regulates Neuronal Differentiation of Mesenchymal Stem Cells through PIP5K1C-dependent Calcium Signaling</title><title>The Journal of biological chemistry</title><addtitle>J Biol Chem</addtitle><description>Enhancer of zeste homolog 2 (EZH2) regulates stem cells renewal, maintenance, and differentiation into different cell lineages including neuron. Changes in intracellular Ca2+ concentration play a critical role in the differentiation of neurons. However, whether EZH2 modulates intracellular Ca2+ signaling in regulating neuronal differentiation from human mesenchymal stem cells (hMSCs) still remains unclear. When hMSCs were treated with a Ca2+ chelator or a PLC inhibitor to block IP3-mediated Ca2+ signaling, neuronal differentiation was disrupted. EZH2 bound to the promoter region of PIP5K1C to suppress its transcription in proliferating hMSCs. Interestingly, knockdown of EZH2 enhanced the expression of PIP5K1C, which in turn increased the amount of PI(4,5)P2, a precursor of IP3, and resulted in increasing the intracellular Ca2+ level, suggesting that EZH2 negatively regulates intracellular Ca2+ through suppression of PIP5K1C. Knockdown of EZH2 also enhanced hMSCs differentiation into functional neuron both in vitro and in vivo. In contrast, knockdown of PIP5K1C significantly reduced PI(4,5)P2 contents and intracellular Ca2+ release in EZH2-silenced cells and resulted in the disruption of neuronal differentiation from hMSCs. Here, we provide the first evidence to demonstrate that after induction to neuronal differentiation, decreased EZH2 activates the expression of PIP5K1C to evoke intracellular Ca2+ signaling, which leads hMSCs to differentiate into functional neuron lineage. Activation of intracellular Ca2+ signaling by repressing or knocking down EZH2 might be a potential strategy to promote neuronal differentiation from hMSCs for application to neurological dysfunction diseases.</description><subject>Calcium</subject><subject>Calcium - metabolism</subject><subject>Calcium Signaling - drug effects</subject><subject>Calcium Signaling - physiology</subject><subject>Cell Biology</subject><subject>Cell Differentiation - drug effects</subject><subject>Cell Differentiation - physiology</subject><subject>Cells, Cultured</subject><subject>Chelating Agents - pharmacology</subject><subject>Differentiation</subject><subject>DNA-Binding Proteins - genetics</subject><subject>DNA-Binding Proteins - metabolism</subject><subject>Enhancer of Zeste Homolog 2 Protein</subject><subject>EZH2</subject><subject>Gene Expression</subject><subject>Gene Expression Regulation, Enzymologic - drug effects</subject><subject>Gene Expression Regulation, Enzymologic - physiology</subject><subject>Gene Knockdown Techniques</subject><subject>Gene Regulation</subject><subject>Humans</subject><subject>Intracellular Calcium</subject><subject>Mesenchymal Stem Cells</subject><subject>Mesenchymal Stem Cells - cytology</subject><subject>Mesenchymal Stem Cells - metabolism</subject><subject>Nervous System Diseases - genetics</subject><subject>Nervous System Diseases - metabolism</subject><subject>Nervous System Diseases - therapy</subject><subject>Neuron</subject><subject>Neuronal Differentiation</subject><subject>Neurons - cytology</subject><subject>Neurons - metabolism</subject><subject>Phosphotransferases (Alcohol Group Acceptor) - biosynthesis</subject><subject>Phosphotransferases (Alcohol Group Acceptor) - genetics</subject><subject>PIP5K1C</subject><subject>Polycomb Repressive Complex 2</subject><subject>Promoter Regions, Genetic - drug effects</subject><subject>Promoter Regions, Genetic - physiology</subject><subject>Transcription Factors - genetics</subject><subject>Transcription Factors - metabolism</subject><issn>0021-9258</issn><issn>1083-351X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2011</creationdate><recordtype>article</recordtype><recordid>eNp1kEFv1DAQhS0EokvhzA38B9J67HidXJBQWmhFCxVLJcTF8jrjrKskXtlJpf57vAQqODCX0Wjee2N_hLwGdgJMlad3W3tyDYepksDLJ2QFrBKFkPD9KVkxxqGouayOyIuU7liusobn5IgDh3Ut1YoM5z8uOP2K3dybCRP9jHMMo-npmXcOI46TN5MPIw2OXmPC0e4ehrzeTDjQBvs-0WkXw9zt6M3ljfwETdHiHsc2O2ljeuvngW58lyP92L0kz5zpE7763Y_J7Yfzb81FcfXl42Xz_qqw-RdTwbdGVkqsQTlbSWPLupRKOafWVghktQKGeajWrZIWHMhSci7QlaV0vBJKHJN3S-5-3g7Y2vyYaHq9j34w8UEH4_W_m9HvdBfutWCyZlDmgNMlwMaQUkT36AWmD-R1Jq8P5PVCPjve_H3yUf8HdRa8XQTOBG266JO-3XAGgkEtof4VUS8KzGjuPUadrM_EsfUR7aTb4P97_ifsIpxc</recordid><startdate>20110318</startdate><enddate>20110318</enddate><creator>Yu, Yung-Luen</creator><creator>Chou, Ruey-Hwang</creator><creator>Chen, Ling-Tzu</creator><creator>Shyu, Woei-Cherng</creator><creator>Hsieh, Su-Ching</creator><creator>Wu, Chen-Shiou</creator><creator>Zeng, Hong-Jie</creator><creator>Yeh, Su-Peng</creator><creator>Yang, De-Ming</creator><creator>Hung, Shih-Chieh</creator><creator>Hung, Mien-Chie</creator><general>Elsevier Inc</general><general>American Society for Biochemistry and Molecular Biology</general><scope>6I.</scope><scope>AAFTH</scope><scope>FBQ</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>20110318</creationdate><title>EZH2 Regulates Neuronal Differentiation of Mesenchymal Stem Cells through PIP5K1C-dependent Calcium Signaling</title><author>Yu, Yung-Luen ; Chou, Ruey-Hwang ; Chen, Ling-Tzu ; Shyu, Woei-Cherng ; Hsieh, Su-Ching ; Wu, Chen-Shiou ; Zeng, Hong-Jie ; Yeh, Su-Peng ; Yang, De-Ming ; Hung, Shih-Chieh ; Hung, Mien-Chie</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c512t-2ba5873617fc85ac494577ff76c33e09710ef7686d75c1f1545223ef445f28373</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2011</creationdate><topic>Calcium</topic><topic>Calcium - metabolism</topic><topic>Calcium Signaling - drug effects</topic><topic>Calcium Signaling - physiology</topic><topic>Cell Biology</topic><topic>Cell Differentiation - drug effects</topic><topic>Cell Differentiation - physiology</topic><topic>Cells, Cultured</topic><topic>Chelating Agents - pharmacology</topic><topic>Differentiation</topic><topic>DNA-Binding Proteins - genetics</topic><topic>DNA-Binding Proteins - metabolism</topic><topic>Enhancer of Zeste Homolog 2 Protein</topic><topic>EZH2</topic><topic>Gene Expression</topic><topic>Gene Expression Regulation, Enzymologic - drug effects</topic><topic>Gene Expression Regulation, Enzymologic - physiology</topic><topic>Gene Knockdown Techniques</topic><topic>Gene Regulation</topic><topic>Humans</topic><topic>Intracellular Calcium</topic><topic>Mesenchymal Stem Cells</topic><topic>Mesenchymal Stem Cells - cytology</topic><topic>Mesenchymal Stem Cells - metabolism</topic><topic>Nervous System Diseases - genetics</topic><topic>Nervous System Diseases - metabolism</topic><topic>Nervous System Diseases - therapy</topic><topic>Neuron</topic><topic>Neuronal Differentiation</topic><topic>Neurons - cytology</topic><topic>Neurons - metabolism</topic><topic>Phosphotransferases (Alcohol Group Acceptor) - biosynthesis</topic><topic>Phosphotransferases (Alcohol Group Acceptor) - genetics</topic><topic>PIP5K1C</topic><topic>Polycomb Repressive Complex 2</topic><topic>Promoter Regions, Genetic - drug effects</topic><topic>Promoter Regions, Genetic - physiology</topic><topic>Transcription Factors - genetics</topic><topic>Transcription Factors - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yu, Yung-Luen</creatorcontrib><creatorcontrib>Chou, Ruey-Hwang</creatorcontrib><creatorcontrib>Chen, Ling-Tzu</creatorcontrib><creatorcontrib>Shyu, Woei-Cherng</creatorcontrib><creatorcontrib>Hsieh, Su-Ching</creatorcontrib><creatorcontrib>Wu, Chen-Shiou</creatorcontrib><creatorcontrib>Zeng, Hong-Jie</creatorcontrib><creatorcontrib>Yeh, Su-Peng</creatorcontrib><creatorcontrib>Yang, De-Ming</creatorcontrib><creatorcontrib>Hung, Shih-Chieh</creatorcontrib><creatorcontrib>Hung, Mien-Chie</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>AGRIS</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>Yu, Yung-Luen</au><au>Chou, Ruey-Hwang</au><au>Chen, Ling-Tzu</au><au>Shyu, Woei-Cherng</au><au>Hsieh, Su-Ching</au><au>Wu, Chen-Shiou</au><au>Zeng, Hong-Jie</au><au>Yeh, Su-Peng</au><au>Yang, De-Ming</au><au>Hung, Shih-Chieh</au><au>Hung, Mien-Chie</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>EZH2 Regulates Neuronal Differentiation of Mesenchymal Stem Cells through PIP5K1C-dependent Calcium Signaling</atitle><jtitle>The Journal of biological chemistry</jtitle><addtitle>J Biol Chem</addtitle><date>2011-03-18</date><risdate>2011</risdate><volume>286</volume><issue>11</issue><spage>9657</spage><epage>9667</epage><pages>9657-9667</pages><issn>0021-9258</issn><eissn>1083-351X</eissn><abstract>Enhancer of zeste homolog 2 (EZH2) regulates stem cells renewal, maintenance, and differentiation into different cell lineages including neuron. Changes in intracellular Ca2+ concentration play a critical role in the differentiation of neurons. However, whether EZH2 modulates intracellular Ca2+ signaling in regulating neuronal differentiation from human mesenchymal stem cells (hMSCs) still remains unclear. When hMSCs were treated with a Ca2+ chelator or a PLC inhibitor to block IP3-mediated Ca2+ signaling, neuronal differentiation was disrupted. EZH2 bound to the promoter region of PIP5K1C to suppress its transcription in proliferating hMSCs. Interestingly, knockdown of EZH2 enhanced the expression of PIP5K1C, which in turn increased the amount of PI(4,5)P2, a precursor of IP3, and resulted in increasing the intracellular Ca2+ level, suggesting that EZH2 negatively regulates intracellular Ca2+ through suppression of PIP5K1C. Knockdown of EZH2 also enhanced hMSCs differentiation into functional neuron both in vitro and in vivo. In contrast, knockdown of PIP5K1C significantly reduced PI(4,5)P2 contents and intracellular Ca2+ release in EZH2-silenced cells and resulted in the disruption of neuronal differentiation from hMSCs. Here, we provide the first evidence to demonstrate that after induction to neuronal differentiation, decreased EZH2 activates the expression of PIP5K1C to evoke intracellular Ca2+ signaling, which leads hMSCs to differentiate into functional neuron lineage. Activation of intracellular Ca2+ signaling by repressing or knocking down EZH2 might be a potential strategy to promote neuronal differentiation from hMSCs for application to neurological dysfunction diseases.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>21216957</pmid><doi>10.1074/jbc.M110.185124</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Calcium Calcium - metabolism Calcium Signaling - drug effects Calcium Signaling - physiology Cell Biology Cell Differentiation - drug effects Cell Differentiation - physiology Cells, Cultured Chelating Agents - pharmacology Differentiation DNA-Binding Proteins - genetics DNA-Binding Proteins - metabolism Enhancer of Zeste Homolog 2 Protein EZH2 Gene Expression Gene Expression Regulation, Enzymologic - drug effects Gene Expression Regulation, Enzymologic - physiology Gene Knockdown Techniques Gene Regulation Humans Intracellular Calcium Mesenchymal Stem Cells Mesenchymal Stem Cells - cytology Mesenchymal Stem Cells - metabolism Nervous System Diseases - genetics Nervous System Diseases - metabolism Nervous System Diseases - therapy Neuron Neuronal Differentiation Neurons - cytology Neurons - metabolism Phosphotransferases (Alcohol Group Acceptor) - biosynthesis Phosphotransferases (Alcohol Group Acceptor) - genetics PIP5K1C Polycomb Repressive Complex 2 Promoter Regions, Genetic - drug effects Promoter Regions, Genetic - physiology Transcription Factors - genetics Transcription Factors - metabolism |
title | EZH2 Regulates Neuronal Differentiation of Mesenchymal Stem Cells through PIP5K1C-dependent Calcium Signaling |
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