Potential effect of matrix stiffness on the enrichment of tumor initiating cells under three-dimensional culture conditions
Cancer stem cell (CSC) or tumor initiating cell (TIC) plays an important role in tumor progression and metastasis. Biophysical forces in tumor microenvironment have an important effect on tumor formation and development. In this study, the potential effect of matrix stiffness on the biological chara...
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| Veröffentlicht in: | Experimental cell research 2015-01, Vol.330 (1), p.123-134 |
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| creator | Liu, Chang Liu, Yang Xu, Xiao-xi Wu, Hao Xie, Hong-guo Chen, Li Lu, Ting Yang, Li Guo, Xin Sun, Guang-wei Wang, Wei Ma, Xiao-jun He, Xin |
| description | Cancer stem cell (CSC) or tumor initiating cell (TIC) plays an important role in tumor progression and metastasis. Biophysical forces in tumor microenvironment have an important effect on tumor formation and development. In this study, the potential effect of matrix stiffness on the biological characteristics of human head and neck squamous cell carcinoma (HNSCC) TICs, especially the enrichment of HNSCC TICs, was investigated under three-dimensional (3D) culture conditions by means of alginate gel (ALG) beads with different matrix stiffnesses. ALG beads with soft (21kPa), moderate (70kPa) and hard (105kPa) stiffness were generated by changing alginate concentration. It was found that significant HNSCC TIC enrichment was achieved in the ALG beads with moderate matrix stiffness (70kPa). The gene expression of stemness markers Oct3/4 and Nanog, TIC markers CD44 and ABCG2 was enhanced in cells under this moderate (70kPa) stiffness. HNSCC TIC proportion was also highly enriched under moderate matrix stiffness, accompanying with higher tumorigenicity, metastatic ability and drug resistance. And it was also found that the possible molecular mechanism underlying the regulated TIC properties by matrix stiffness under 3D culture conditions was significantly different from 2D culture condition. Therefore, the results achieved in this study indicated that 3D biophysical microenvironment had an important effect on TIC characteristics and alginate-based biomimetic scaffolds could be utilized as a proper platform to investigate the interaction between tumor cells and 3D microenvironment.
•Effect of matrix stiffness on TIC characteristics in 3D system was investigated.•Matrix stiffness played an important role in regulating HNSCC TIC characteristics.•The underlying mechanism between matrix stiffness and TICs was also explored. |
| doi_str_mv | 10.1016/j.yexcr.2014.07.036 |
| format | Article |
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•Effect of matrix stiffness on TIC characteristics in 3D system was investigated.•Matrix stiffness played an important role in regulating HNSCC TIC characteristics.•The underlying mechanism between matrix stiffness and TICs was also explored.</description><identifier>ISSN: 0014-4827</identifier><identifier>EISSN: 1090-2422</identifier><identifier>DOI: 10.1016/j.yexcr.2014.07.036</identifier><identifier>PMID: 25108138</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>3-D technology ; Alginate gel beads ; Alginates - pharmacology ; ATP Binding Cassette Transporter, Sub-Family G, Member 2 ; ATP-Binding Cassette Transporters - genetics ; ATP-Binding Cassette Transporters - metabolism ; Carcinoma, Squamous Cell - metabolism ; Cell culture ; Cell Line, Tumor ; Extracellular Matrix - chemistry ; Extracellular Matrix - metabolism ; Gene expression ; Head & neck cancer ; Head and Neck Neoplasms - metabolism ; Homeodomain Proteins - genetics ; Homeodomain Proteins - metabolism ; Humans ; Hyaluronan Receptors - genetics ; Hyaluronan Receptors - metabolism ; Matrix stiffness ; Metastasis ; Nanog Homeobox Protein ; Neoplasm Proteins - genetics ; Neoplasm Proteins - metabolism ; Neoplastic Stem Cells - drug effects ; Neoplastic Stem Cells - metabolism ; Octamer Transcription Factor-3 - genetics ; Octamer Transcription Factor-3 - metabolism ; Three-dimensional culture ; Tumor initiating cells ; Tumor Microenvironment ; Tumorigenesis</subject><ispartof>Experimental cell research, 2015-01, Vol.330 (1), p.123-134</ispartof><rights>2014 Elsevier Inc.</rights><rights>Copyright © 2014 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c523t-9405a1a2f1efbf9dc2dd60875f841675703b194468c8f2c317049bdc027bb203</citedby><cites>FETCH-LOGICAL-c523t-9405a1a2f1efbf9dc2dd60875f841675703b194468c8f2c317049bdc027bb203</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.yexcr.2014.07.036$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3548,27923,27924,45994</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25108138$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Chang</creatorcontrib><creatorcontrib>Liu, Yang</creatorcontrib><creatorcontrib>Xu, Xiao-xi</creatorcontrib><creatorcontrib>Wu, Hao</creatorcontrib><creatorcontrib>Xie, Hong-guo</creatorcontrib><creatorcontrib>Chen, Li</creatorcontrib><creatorcontrib>Lu, Ting</creatorcontrib><creatorcontrib>Yang, Li</creatorcontrib><creatorcontrib>Guo, Xin</creatorcontrib><creatorcontrib>Sun, Guang-wei</creatorcontrib><creatorcontrib>Wang, Wei</creatorcontrib><creatorcontrib>Ma, Xiao-jun</creatorcontrib><creatorcontrib>He, Xin</creatorcontrib><title>Potential effect of matrix stiffness on the enrichment of tumor initiating cells under three-dimensional culture conditions</title><title>Experimental cell research</title><addtitle>Exp Cell Res</addtitle><description>Cancer stem cell (CSC) or tumor initiating cell (TIC) plays an important role in tumor progression and metastasis. Biophysical forces in tumor microenvironment have an important effect on tumor formation and development. In this study, the potential effect of matrix stiffness on the biological characteristics of human head and neck squamous cell carcinoma (HNSCC) TICs, especially the enrichment of HNSCC TICs, was investigated under three-dimensional (3D) culture conditions by means of alginate gel (ALG) beads with different matrix stiffnesses. ALG beads with soft (21kPa), moderate (70kPa) and hard (105kPa) stiffness were generated by changing alginate concentration. It was found that significant HNSCC TIC enrichment was achieved in the ALG beads with moderate matrix stiffness (70kPa). The gene expression of stemness markers Oct3/4 and Nanog, TIC markers CD44 and ABCG2 was enhanced in cells under this moderate (70kPa) stiffness. HNSCC TIC proportion was also highly enriched under moderate matrix stiffness, accompanying with higher tumorigenicity, metastatic ability and drug resistance. And it was also found that the possible molecular mechanism underlying the regulated TIC properties by matrix stiffness under 3D culture conditions was significantly different from 2D culture condition. Therefore, the results achieved in this study indicated that 3D biophysical microenvironment had an important effect on TIC characteristics and alginate-based biomimetic scaffolds could be utilized as a proper platform to investigate the interaction between tumor cells and 3D microenvironment.
•Effect of matrix stiffness on TIC characteristics in 3D system was investigated.•Matrix stiffness played an important role in regulating HNSCC TIC characteristics.•The underlying mechanism between matrix stiffness and TICs was also explored.</description><subject>3-D technology</subject><subject>Alginate gel beads</subject><subject>Alginates - pharmacology</subject><subject>ATP Binding Cassette Transporter, Sub-Family G, Member 2</subject><subject>ATP-Binding Cassette Transporters - genetics</subject><subject>ATP-Binding Cassette Transporters - metabolism</subject><subject>Carcinoma, Squamous Cell - metabolism</subject><subject>Cell culture</subject><subject>Cell Line, Tumor</subject><subject>Extracellular Matrix - chemistry</subject><subject>Extracellular Matrix - metabolism</subject><subject>Gene expression</subject><subject>Head & neck cancer</subject><subject>Head and Neck Neoplasms - metabolism</subject><subject>Homeodomain Proteins - genetics</subject><subject>Homeodomain Proteins - metabolism</subject><subject>Humans</subject><subject>Hyaluronan Receptors - genetics</subject><subject>Hyaluronan Receptors - metabolism</subject><subject>Matrix stiffness</subject><subject>Metastasis</subject><subject>Nanog Homeobox Protein</subject><subject>Neoplasm Proteins - genetics</subject><subject>Neoplasm Proteins - metabolism</subject><subject>Neoplastic Stem Cells - drug effects</subject><subject>Neoplastic Stem Cells - metabolism</subject><subject>Octamer Transcription Factor-3 - genetics</subject><subject>Octamer Transcription Factor-3 - metabolism</subject><subject>Three-dimensional culture</subject><subject>Tumor initiating cells</subject><subject>Tumor Microenvironment</subject><subject>Tumorigenesis</subject><issn>0014-4827</issn><issn>1090-2422</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kT1v1TAUhi0EopeWX4CELLGwJBw7ie0MDKjiS6pEh-5WYh9TXyV2sR3Uqn8e397CwNDpDH7e9xz5IeQNg5YBEx_27R3emtRyYH0LsoVOPCM7BiM0vOf8OdlBfWl6xeUJeZXzHgCUYuIlOeEDA8U6tSP3l7FgKH5aKDqHptDo6DqV5G9pLt65gDnTGGi5RooheXO9Vv5AlW2Nifrga7r48JMaXJZMt2AxVTwhNtZXOPsYar3ZlrIlpCYGWyMx5DPywk1LxteP85Rcffl8df6tufjx9fv5p4vGDLwrzdjDMLGJO4ZudqM13FoBSg5O9UzIQUI3s7HvhTLKcdMxCf04WwNczjOH7pS8P9bepPhrw1z06vPh1ilg3LJmopODkGpgFX33H7qPW6rXP1BC8VGqsVLdkTIp5pzQ6Zvk1yndaQb6oEbv9YMafVCjQeqqpqbePnZv84r2X-aviwp8PAJY_-K3x6Sz8RgMWp-qGG2jf3LBH9lWol0</recordid><startdate>20150101</startdate><enddate>20150101</enddate><creator>Liu, Chang</creator><creator>Liu, Yang</creator><creator>Xu, Xiao-xi</creator><creator>Wu, Hao</creator><creator>Xie, Hong-guo</creator><creator>Chen, Li</creator><creator>Lu, Ting</creator><creator>Yang, Li</creator><creator>Guo, Xin</creator><creator>Sun, Guang-wei</creator><creator>Wang, Wei</creator><creator>Ma, Xiao-jun</creator><creator>He, Xin</creator><general>Elsevier Inc</general><general>Elsevier BV</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>7TK</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>20150101</creationdate><title>Potential effect of matrix stiffness on the enrichment of tumor initiating cells under three-dimensional culture conditions</title><author>Liu, Chang ; Liu, Yang ; Xu, Xiao-xi ; Wu, Hao ; Xie, Hong-guo ; Chen, Li ; Lu, Ting ; Yang, Li ; Guo, Xin ; Sun, Guang-wei ; Wang, Wei ; Ma, Xiao-jun ; He, Xin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c523t-9405a1a2f1efbf9dc2dd60875f841675703b194468c8f2c317049bdc027bb203</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>3-D technology</topic><topic>Alginate gel beads</topic><topic>Alginates - pharmacology</topic><topic>ATP Binding Cassette Transporter, Sub-Family G, Member 2</topic><topic>ATP-Binding Cassette Transporters - genetics</topic><topic>ATP-Binding Cassette Transporters - metabolism</topic><topic>Carcinoma, Squamous Cell - metabolism</topic><topic>Cell culture</topic><topic>Cell Line, Tumor</topic><topic>Extracellular Matrix - chemistry</topic><topic>Extracellular Matrix - metabolism</topic><topic>Gene expression</topic><topic>Head & neck cancer</topic><topic>Head and Neck Neoplasms - metabolism</topic><topic>Homeodomain Proteins - genetics</topic><topic>Homeodomain Proteins - metabolism</topic><topic>Humans</topic><topic>Hyaluronan Receptors - genetics</topic><topic>Hyaluronan Receptors - metabolism</topic><topic>Matrix stiffness</topic><topic>Metastasis</topic><topic>Nanog Homeobox Protein</topic><topic>Neoplasm Proteins - genetics</topic><topic>Neoplasm Proteins - metabolism</topic><topic>Neoplastic Stem Cells - drug effects</topic><topic>Neoplastic Stem Cells - metabolism</topic><topic>Octamer Transcription Factor-3 - genetics</topic><topic>Octamer Transcription Factor-3 - metabolism</topic><topic>Three-dimensional culture</topic><topic>Tumor initiating cells</topic><topic>Tumor Microenvironment</topic><topic>Tumorigenesis</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Chang</creatorcontrib><creatorcontrib>Liu, Yang</creatorcontrib><creatorcontrib>Xu, Xiao-xi</creatorcontrib><creatorcontrib>Wu, Hao</creatorcontrib><creatorcontrib>Xie, Hong-guo</creatorcontrib><creatorcontrib>Chen, Li</creatorcontrib><creatorcontrib>Lu, Ting</creatorcontrib><creatorcontrib>Yang, Li</creatorcontrib><creatorcontrib>Guo, Xin</creatorcontrib><creatorcontrib>Sun, Guang-wei</creatorcontrib><creatorcontrib>Wang, Wei</creatorcontrib><creatorcontrib>Ma, Xiao-jun</creatorcontrib><creatorcontrib>He, Xin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Experimental cell research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Chang</au><au>Liu, Yang</au><au>Xu, Xiao-xi</au><au>Wu, Hao</au><au>Xie, Hong-guo</au><au>Chen, Li</au><au>Lu, Ting</au><au>Yang, Li</au><au>Guo, Xin</au><au>Sun, Guang-wei</au><au>Wang, Wei</au><au>Ma, Xiao-jun</au><au>He, Xin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Potential effect of matrix stiffness on the enrichment of tumor initiating cells under three-dimensional culture conditions</atitle><jtitle>Experimental cell research</jtitle><addtitle>Exp Cell Res</addtitle><date>2015-01-01</date><risdate>2015</risdate><volume>330</volume><issue>1</issue><spage>123</spage><epage>134</epage><pages>123-134</pages><issn>0014-4827</issn><eissn>1090-2422</eissn><abstract>Cancer stem cell (CSC) or tumor initiating cell (TIC) plays an important role in tumor progression and metastasis. Biophysical forces in tumor microenvironment have an important effect on tumor formation and development. In this study, the potential effect of matrix stiffness on the biological characteristics of human head and neck squamous cell carcinoma (HNSCC) TICs, especially the enrichment of HNSCC TICs, was investigated under three-dimensional (3D) culture conditions by means of alginate gel (ALG) beads with different matrix stiffnesses. ALG beads with soft (21kPa), moderate (70kPa) and hard (105kPa) stiffness were generated by changing alginate concentration. It was found that significant HNSCC TIC enrichment was achieved in the ALG beads with moderate matrix stiffness (70kPa). The gene expression of stemness markers Oct3/4 and Nanog, TIC markers CD44 and ABCG2 was enhanced in cells under this moderate (70kPa) stiffness. HNSCC TIC proportion was also highly enriched under moderate matrix stiffness, accompanying with higher tumorigenicity, metastatic ability and drug resistance. And it was also found that the possible molecular mechanism underlying the regulated TIC properties by matrix stiffness under 3D culture conditions was significantly different from 2D culture condition. Therefore, the results achieved in this study indicated that 3D biophysical microenvironment had an important effect on TIC characteristics and alginate-based biomimetic scaffolds could be utilized as a proper platform to investigate the interaction between tumor cells and 3D microenvironment.
•Effect of matrix stiffness on TIC characteristics in 3D system was investigated.•Matrix stiffness played an important role in regulating HNSCC TIC characteristics.•The underlying mechanism between matrix stiffness and TICs was also explored.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25108138</pmid><doi>10.1016/j.yexcr.2014.07.036</doi><tpages>12</tpages></addata></record> |
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| subjects | 3-D technology Alginate gel beads Alginates - pharmacology ATP Binding Cassette Transporter, Sub-Family G, Member 2 ATP-Binding Cassette Transporters - genetics ATP-Binding Cassette Transporters - metabolism Carcinoma, Squamous Cell - metabolism Cell culture Cell Line, Tumor Extracellular Matrix - chemistry Extracellular Matrix - metabolism Gene expression Head & neck cancer Head and Neck Neoplasms - metabolism Homeodomain Proteins - genetics Homeodomain Proteins - metabolism Humans Hyaluronan Receptors - genetics Hyaluronan Receptors - metabolism Matrix stiffness Metastasis Nanog Homeobox Protein Neoplasm Proteins - genetics Neoplasm Proteins - metabolism Neoplastic Stem Cells - drug effects Neoplastic Stem Cells - metabolism Octamer Transcription Factor-3 - genetics Octamer Transcription Factor-3 - metabolism Three-dimensional culture Tumor initiating cells Tumor Microenvironment Tumorigenesis |
| title | Potential effect of matrix stiffness on the enrichment of tumor initiating cells under three-dimensional culture conditions |
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