Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli
The tendon is highly prone to injury, overuse, or age-related degeneration in both humans and horses. Natural healing of injured tendon is poor, and cell-based therapeutic treatment is still a significant clinical challenge. In this study, we extensively investigated the expression of tenogenic gene...
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| description | The tendon is highly prone to injury, overuse, or age-related degeneration in both humans and horses. Natural healing of injured tendon is poor, and cell-based therapeutic treatment is still a significant clinical challenge. In this study, we extensively investigated the expression of tenogenic genes in equine bone marrow mesenchymal stem cells (BMSCs) and tenocyte-derived induced pluripotent stem cells (teno-iPSCs) stimulated by growth factors (TGF-β3 and BMP12) combined with ectopic expression of tenogenic transcription factor MKX or cyclic uniaxial mechanical stretch. Western blotting revealed that TGF-β3 and BMP12 increased the expression of transcription factors SCX and MKX in both cells, but the tenocyte marker tenomodulin (TNMD) was detected only in BMSCs and upregulated by either inducer. On the other hand, quantitative real-time PCR showed that TGF-β3 increased the expression of EGR1, COL1A2, FMOD, and TNC in BMSCs and SCX, COL1A2, DCN, FMOD, and TNC in teno-iPSCs. BMP12 treatment elevated SCX, MKX, DCN, FMOD, and TNC in teno-iPSCs. Overexpression of MKX increased SCX, DCN, FMOD, and TNC in BMSCs and EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 further enhanced TNC in BMSCs. Moreover, mechanical stretch increased SCX, EGR1, DCN, ELN, and TNC in BMSCs and SCX, MKX, EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 tended to further elevate SCX, ELN, and TNC in BMSCs and SCX, MKX, COL1A2, DCN, and TNC in teno-iPSCs, while BMP12 further uptrended the expression of SCX and DCN in BMSCs and DCN in teno-iPSCs. Additionally, the aforementioned tenogenic inducers also affected the expression of signaling regulators SMAD7, ETV4, and SIRT1 in BMSCs and teno-iPSCs. Taken together, our data demonstrate that, in respect to the tenocyte-lineage-specific gene expression, BMSCs and teno-iPSCs respond differently to the tenogenic stimuli, which may affect the outcome of their application in tendon repair or regeneration. |
| doi_str_mv | 10.1155/2021/8835576 |
| format | Article |
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Natural healing of injured tendon is poor, and cell-based therapeutic treatment is still a significant clinical challenge. In this study, we extensively investigated the expression of tenogenic genes in equine bone marrow mesenchymal stem cells (BMSCs) and tenocyte-derived induced pluripotent stem cells (teno-iPSCs) stimulated by growth factors (TGF-β3 and BMP12) combined with ectopic expression of tenogenic transcription factor MKX or cyclic uniaxial mechanical stretch. Western blotting revealed that TGF-β3 and BMP12 increased the expression of transcription factors SCX and MKX in both cells, but the tenocyte marker tenomodulin (TNMD) was detected only in BMSCs and upregulated by either inducer. On the other hand, quantitative real-time PCR showed that TGF-β3 increased the expression of EGR1, COL1A2, FMOD, and TNC in BMSCs and SCX, COL1A2, DCN, FMOD, and TNC in teno-iPSCs. BMP12 treatment elevated SCX, MKX, DCN, FMOD, and TNC in teno-iPSCs. Overexpression of MKX increased SCX, DCN, FMOD, and TNC in BMSCs and EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 further enhanced TNC in BMSCs. Moreover, mechanical stretch increased SCX, EGR1, DCN, ELN, and TNC in BMSCs and SCX, MKX, EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 tended to further elevate SCX, ELN, and TNC in BMSCs and SCX, MKX, COL1A2, DCN, and TNC in teno-iPSCs, while BMP12 further uptrended the expression of SCX and DCN in BMSCs and DCN in teno-iPSCs. Additionally, the aforementioned tenogenic inducers also affected the expression of signaling regulators SMAD7, ETV4, and SIRT1 in BMSCs and teno-iPSCs. Taken together, our data demonstrate that, in respect to the tenocyte-lineage-specific gene expression, BMSCs and teno-iPSCs respond differently to the tenogenic stimuli, which may affect the outcome of their application in tendon repair or regeneration.</description><identifier>ISSN: 1687-966X</identifier><identifier>ISSN: 1687-9678</identifier><identifier>EISSN: 1687-9678</identifier><identifier>DOI: 10.1155/2021/8835576</identifier><identifier>PMID: 33510795</identifier><language>eng</language><publisher>United States: Hindawi</publisher><subject>Age ; Biomechanics ; Bone marrow ; Comparative analysis ; Degeneration ; DNA binding proteins ; Ectopic expression ; EGR-1 protein ; Ethylenediaminetetraacetic acid ; Gene expression ; Genes ; Genetic research ; Growth factors ; Horses ; Infections ; Laboratories ; Mesenchymal stem cells ; Pluripotency ; Regeneration ; Repair & maintenance ; SIRT1 protein ; Smad7 protein ; Stem cells ; Stimuli ; Tendons ; Transcription factors ; Transforming growth factors ; Western blotting ; Wound healing</subject><ispartof>Stem cells international, 2021, Vol.2021, p.8835576-18</ispartof><rights>Copyright © 2021 Feikun Yang and Dean W. Richardson.</rights><rights>COPYRIGHT 2021 John Wiley & Sons, Inc.</rights><rights>Copyright © 2021 Feikun Yang and Dean W. Richardson. This is an open access article distributed under the Creative Commons Attribution License (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. https://creativecommons.org/licenses/by/4.0</rights><rights>Copyright © 2021 Feikun Yang and Dean W. Richardson. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c710t-d12802cb7d69ec800e757c73eb72c3675344c35d33c46d0ac79460cb172924993</citedby><cites>FETCH-LOGICAL-c710t-d12802cb7d69ec800e757c73eb72c3675344c35d33c46d0ac79460cb172924993</cites><orcidid>0000-0002-7295-0553 ; 0000-0003-1504-1537</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/PMC7825360/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC7825360/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,877,885,2102,4024,27923,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33510795$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Jiang, Yangzi</contributor><contributor>Yangzi Jiang</contributor><creatorcontrib>Yang, Feikun</creatorcontrib><creatorcontrib>Richardson, Dean W.</creatorcontrib><title>Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli</title><title>Stem cells international</title><addtitle>Stem Cells Int</addtitle><description>The tendon is highly prone to injury, overuse, or age-related degeneration in both humans and horses. Natural healing of injured tendon is poor, and cell-based therapeutic treatment is still a significant clinical challenge. In this study, we extensively investigated the expression of tenogenic genes in equine bone marrow mesenchymal stem cells (BMSCs) and tenocyte-derived induced pluripotent stem cells (teno-iPSCs) stimulated by growth factors (TGF-β3 and BMP12) combined with ectopic expression of tenogenic transcription factor MKX or cyclic uniaxial mechanical stretch. Western blotting revealed that TGF-β3 and BMP12 increased the expression of transcription factors SCX and MKX in both cells, but the tenocyte marker tenomodulin (TNMD) was detected only in BMSCs and upregulated by either inducer. On the other hand, quantitative real-time PCR showed that TGF-β3 increased the expression of EGR1, COL1A2, FMOD, and TNC in BMSCs and SCX, COL1A2, DCN, FMOD, and TNC in teno-iPSCs. BMP12 treatment elevated SCX, MKX, DCN, FMOD, and TNC in teno-iPSCs. Overexpression of MKX increased SCX, DCN, FMOD, and TNC in BMSCs and EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 further enhanced TNC in BMSCs. Moreover, mechanical stretch increased SCX, EGR1, DCN, ELN, and TNC in BMSCs and SCX, MKX, EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 tended to further elevate SCX, ELN, and TNC in BMSCs and SCX, MKX, COL1A2, DCN, and TNC in teno-iPSCs, while BMP12 further uptrended the expression of SCX and DCN in BMSCs and DCN in teno-iPSCs. Additionally, the aforementioned tenogenic inducers also affected the expression of signaling regulators SMAD7, ETV4, and SIRT1 in BMSCs and teno-iPSCs. Taken together, our data demonstrate that, in respect to the tenocyte-lineage-specific gene expression, BMSCs and teno-iPSCs respond differently to the tenogenic stimuli, which may affect the outcome of their application in tendon repair or regeneration.</description><subject>Age</subject><subject>Biomechanics</subject><subject>Bone marrow</subject><subject>Comparative analysis</subject><subject>Degeneration</subject><subject>DNA binding proteins</subject><subject>Ectopic expression</subject><subject>EGR-1 protein</subject><subject>Ethylenediaminetetraacetic acid</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Genetic research</subject><subject>Growth factors</subject><subject>Horses</subject><subject>Infections</subject><subject>Laboratories</subject><subject>Mesenchymal stem cells</subject><subject>Pluripotency</subject><subject>Regeneration</subject><subject>Repair & maintenance</subject><subject>SIRT1 protein</subject><subject>Smad7 protein</subject><subject>Stem cells</subject><subject>Stimuli</subject><subject>Tendons</subject><subject>Transcription factors</subject><subject>Transforming growth factors</subject><subject>Western blotting</subject><subject>Wound healing</subject><issn>1687-966X</issn><issn>1687-9678</issn><issn>1687-9678</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>RHX</sourceid><sourceid>8G5</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>GUQSH</sourceid><sourceid>M2O</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99v0zAQgCMEYtPYG8_IEhJCgm7-Ecf2C1JXxpi0CcSGxFvkOpfGU2IXO9nof8ifhduO0iI0kTw4sr_7TvHdZdlzgo8I4fyYYkqOpWSci-JRtk8KKUaqEPLx5rv4tpcdxniD08MUzjF9mu0xxgkWiu9nPye-m-uge3sLaOx0u4g2Il-ja3B-Bs4adAYO0OmPeYAYrXfIutWhWfQweg8hBVbo3FWDSevndgh27ntwPbrqoUMTaNuItKvQiU-aSx2Cv9uEXUIEZ5pFp9ttPGX4AnHuXQTUe3RivWmgsyZRK5P1HZhGu9XOVW-7obXPsie1biMc3q8H2dcPp9eTj6OLT2fnk_HFyAiC-1FFqMTUTEVVKDASYxBcGMFgKqhhheAszw3jFWMmLyqsjVB5gc2UCKporhQ7yM7X3srrm3IebKfDovTalqsNH2alDr01LZSyULmgsqoFh5xgrOskJ0LpSoIkmCXXu7VrPkw7qEy6taDbHenuibNNOfO3pZCUswInwet7QfDfB4h92dlo0h1qB36IJc0lk4Tniib05V_ojR9CKviKwoRyxdQfaqbTD1hX-5TXLKXluEiNRQup-MNUakYmpJKJOvoHld5qWcvUDbVN-zva_wvYyvBqK6AB3fZN9O3QpzaNu-aHwS3j2zVogo8xQL0pBsHlcuLK5cSV9xOX8BfbBdzAv-crAW_WQGNdpe_sw7pf_1cwRg</recordid><startdate>2021</startdate><enddate>2021</enddate><creator>Yang, Feikun</creator><creator>Richardson, Dean W.</creator><general>Hindawi</general><general>John Wiley & Sons, Inc</general><general>Hindawi Limited</general><scope>RHU</scope><scope>RHW</scope><scope>RHX</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7QO</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>8AO</scope><scope>8FD</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>H94</scope><scope>K9.</scope><scope>M0S</scope><scope>M2O</scope><scope>MBDVC</scope><scope>P64</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0002-7295-0553</orcidid><orcidid>https://orcid.org/0000-0003-1504-1537</orcidid></search><sort><creationdate>2021</creationdate><title>Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli</title><author>Yang, Feikun ; Richardson, Dean W.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c710t-d12802cb7d69ec800e757c73eb72c3675344c35d33c46d0ac79460cb172924993</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Age</topic><topic>Biomechanics</topic><topic>Bone marrow</topic><topic>Comparative analysis</topic><topic>Degeneration</topic><topic>DNA binding proteins</topic><topic>Ectopic expression</topic><topic>EGR-1 protein</topic><topic>Ethylenediaminetetraacetic acid</topic><topic>Gene expression</topic><topic>Genes</topic><topic>Genetic research</topic><topic>Growth factors</topic><topic>Horses</topic><topic>Infections</topic><topic>Laboratories</topic><topic>Mesenchymal stem cells</topic><topic>Pluripotency</topic><topic>Regeneration</topic><topic>Repair & maintenance</topic><topic>SIRT1 protein</topic><topic>Smad7 protein</topic><topic>Stem cells</topic><topic>Stimuli</topic><topic>Tendons</topic><topic>Transcription factors</topic><topic>Transforming growth factors</topic><topic>Western blotting</topic><topic>Wound healing</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Yang, Feikun</creatorcontrib><creatorcontrib>Richardson, Dean W.</creatorcontrib><collection>Hindawi Publishing Complete</collection><collection>Hindawi Publishing Subscription Journals</collection><collection>Hindawi Publishing Open Access Journals</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Biotechnology Research Abstracts</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Research Library</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</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>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>Stem cells international</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yang, Feikun</au><au>Richardson, Dean W.</au><au>Jiang, Yangzi</au><au>Yangzi Jiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli</atitle><jtitle>Stem cells international</jtitle><addtitle>Stem Cells Int</addtitle><date>2021</date><risdate>2021</risdate><volume>2021</volume><spage>8835576</spage><epage>18</epage><pages>8835576-18</pages><issn>1687-966X</issn><issn>1687-9678</issn><eissn>1687-9678</eissn><abstract>The tendon is highly prone to injury, overuse, or age-related degeneration in both humans and horses. Natural healing of injured tendon is poor, and cell-based therapeutic treatment is still a significant clinical challenge. In this study, we extensively investigated the expression of tenogenic genes in equine bone marrow mesenchymal stem cells (BMSCs) and tenocyte-derived induced pluripotent stem cells (teno-iPSCs) stimulated by growth factors (TGF-β3 and BMP12) combined with ectopic expression of tenogenic transcription factor MKX or cyclic uniaxial mechanical stretch. Western blotting revealed that TGF-β3 and BMP12 increased the expression of transcription factors SCX and MKX in both cells, but the tenocyte marker tenomodulin (TNMD) was detected only in BMSCs and upregulated by either inducer. On the other hand, quantitative real-time PCR showed that TGF-β3 increased the expression of EGR1, COL1A2, FMOD, and TNC in BMSCs and SCX, COL1A2, DCN, FMOD, and TNC in teno-iPSCs. BMP12 treatment elevated SCX, MKX, DCN, FMOD, and TNC in teno-iPSCs. Overexpression of MKX increased SCX, DCN, FMOD, and TNC in BMSCs and EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 further enhanced TNC in BMSCs. Moreover, mechanical stretch increased SCX, EGR1, DCN, ELN, and TNC in BMSCs and SCX, MKX, EGR1, COL1A2, DCN, FMOD, and TNC in teno-iPSCs; TGF-β3 tended to further elevate SCX, ELN, and TNC in BMSCs and SCX, MKX, COL1A2, DCN, and TNC in teno-iPSCs, while BMP12 further uptrended the expression of SCX and DCN in BMSCs and DCN in teno-iPSCs. Additionally, the aforementioned tenogenic inducers also affected the expression of signaling regulators SMAD7, ETV4, and SIRT1 in BMSCs and teno-iPSCs. Taken together, our data demonstrate that, in respect to the tenocyte-lineage-specific gene expression, BMSCs and teno-iPSCs respond differently to the tenogenic stimuli, which may affect the outcome of their application in tendon repair or regeneration.</abstract><cop>United States</cop><pub>Hindawi</pub><pmid>33510795</pmid><doi>10.1155/2021/8835576</doi><tpages>18</tpages><orcidid>https://orcid.org/0000-0002-7295-0553</orcidid><orcidid>https://orcid.org/0000-0003-1504-1537</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Age Biomechanics Bone marrow Comparative analysis Degeneration DNA binding proteins Ectopic expression EGR-1 protein Ethylenediaminetetraacetic acid Gene expression Genes Genetic research Growth factors Horses Infections Laboratories Mesenchymal stem cells Pluripotency Regeneration Repair & maintenance SIRT1 protein Smad7 protein Stem cells Stimuli Tendons Transcription factors Transforming growth factors Western blotting Wound healing |
| title | Comparative Analysis of Tenogenic Gene Expression in Tenocyte-Derived Induced Pluripotent Stem Cells and Bone Marrow-Derived Mesenchymal Stem Cells in Response to Biochemical and Biomechanical Stimuli |
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