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Three‐dimensional collagenous niche and azacytidine selectively promote time‐dependent cardiomyogenesis from human bone marrow‐derived MSC spheroids
Endogenous adult cardiac regenerative machinery is not capable of replacing the lost cells following myocardial infarction, often leading to permanent alterations in structure‐function‐mechanical properties. Regenerative therapies based on delivering autologous stem cells within an appropriate 3D mi...
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| Published in: | Biotechnology and bioengineering 2018-08, Vol.115 (8), p.2013-2026 |
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| container_issue | 8 |
| container_start_page | 2013 |
| container_title | Biotechnology and bioengineering |
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| creator | Joshi, Jyotsna Mahajan, Gautam Kothapalli, Chandrasekhar R. |
| description | Endogenous adult cardiac regenerative machinery is not capable of replacing the lost cells following myocardial infarction, often leading to permanent alterations in structure‐function‐mechanical properties. Regenerative therapies based on delivering autologous stem cells within an appropriate 3D milieu could meet such demand, by enabling homing and directed differentiation of the transplanted cells into lost specialized cell populations. Since type I collagen is the predominant cardiac tissue matrix protein, we here optimized the 3D niche which could promote time‐dependent evolution of cardiomyogenesis from human bone marrow‐derived mesenchymal stem cells (BM‐MSC). 3D collagen gel physical and mechanical characteristics were assessed using SEM and AFM, respectively, while the standalone and combined effects of collagen concentration, culture duration, and 5‐azacytidine (aza) dose on the phenotype and genotype of MSC spheroids were quantified using immunofluorescence labeling and RT‐PCR analysis. Increasing collagen concentration led to a significant increase in Young's modulus (p |
| doi_str_mv | 10.1002/bit.26714 |
| format | article |
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In this study, we evaluated the standalone and combined effects of collagen gel concentration, azacytidine dosage, and culture duration on the differentiation and maturation of adult human bone marrow‐derived MSC spheroids into cardiomyocytes. The role of canonical Wnt/b‐catenin signaling pathway was assessed. Results suggest that 2 mg/mL collagen gels and 10 uM aza offer optimal environment for time‐dependent evolution of cardiomyogenesis from MSCs, with significant applications in cardiac tissue engineering and stem cell transplantation for regenerating lost cardiac tissue.</description><identifier>ISSN: 0006-3592</identifier><identifier>EISSN: 1097-0290</identifier><identifier>DOI: 10.1002/bit.26714</identifier><identifier>PMID: 29665002</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>5‐azacytidine ; atomic force microscopy ; Autografts ; Azacytidine ; Bone marrow ; Cell culture ; Cell interactions ; Collagen ; Collagen (type I) ; collagen gels ; Differentiation ; Evolution ; Gels ; Genotypes ; Homing ; human bone marrow‐derived MSCs ; Immunofluorescence ; Matrix protein ; Mechanical properties ; Mesenchyme ; Modulus of elasticity ; Myocardial infarction ; Phenotypes ; Pore size ; Porosity ; Proteins ; Signal transduction ; Signaling ; Spheroids ; Stem cell transplantation ; Stem cells ; Stiffness ; Structure-function relationships ; Time dependence ; Tissue engineering ; Transplantation ; Wnt protein ; Wnt signaling</subject><ispartof>Biotechnology and bioengineering, 2018-08, Vol.115 (8), p.2013-2026</ispartof><rights>2018 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3904-3488111db63dc1004ccfb31e46fbb5714411a937e2f4fd2e1bb2c3fb88771f1d3</citedby><cites>FETCH-LOGICAL-c3904-3488111db63dc1004ccfb31e46fbb5714411a937e2f4fd2e1bb2c3fb88771f1d3</cites><orcidid>0000-0001-8450-0640</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29665002$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Joshi, Jyotsna</creatorcontrib><creatorcontrib>Mahajan, Gautam</creatorcontrib><creatorcontrib>Kothapalli, Chandrasekhar R.</creatorcontrib><title>Three‐dimensional collagenous niche and azacytidine selectively promote time‐dependent cardiomyogenesis from human bone marrow‐derived MSC spheroids</title><title>Biotechnology and bioengineering</title><addtitle>Biotechnol Bioeng</addtitle><description>Endogenous adult cardiac regenerative machinery is not capable of replacing the lost cells following myocardial infarction, often leading to permanent alterations in structure‐function‐mechanical properties. Regenerative therapies based on delivering autologous stem cells within an appropriate 3D milieu could meet such demand, by enabling homing and directed differentiation of the transplanted cells into lost specialized cell populations. Since type I collagen is the predominant cardiac tissue matrix protein, we here optimized the 3D niche which could promote time‐dependent evolution of cardiomyogenesis from human bone marrow‐derived mesenchymal stem cells (BM‐MSC). 3D collagen gel physical and mechanical characteristics were assessed using SEM and AFM, respectively, while the standalone and combined effects of collagen concentration, culture duration, and 5‐azacytidine (aza) dose on the phenotype and genotype of MSC spheroids were quantified using immunofluorescence labeling and RT‐PCR analysis. Increasing collagen concentration led to a significant increase in Young's modulus (p < 0.01) but simultaneous decrease in the mean pore size, resulting in stiffer gels. Spheroid formation significantly modulated MSC differentiation and genotype, mostly due to better cell–cell interactions. Among the aza dosages tested, 10 μM appears to be optimal, while 3 mg/ml gels resulted in significantly lower cell viability compared to 1 or 2 mg/ml gels. Stiffer gels (2 and 3 mg/ml) and exposure to 10 μM aza upregulated early and late cardiac marker expressions in a time‐dependent fashion. On the other hand, cell–cell signaling within the MSC spheroids seem to have a strong role in influencing mature cardiac markers expression, since neither aza nor gel stiffness seem to significantly improve their expression. Western blot analysis suggested that canonical Wnt/β‐catenin signaling pathway might be primarily mediating the observed benefits of aza on cardiac differentiation of MSC spheroids. In conclusion, 2 mg/ml collagen and 10 μM aza appears to offer optimal 3D microenvironment in terms of cell viability and time‐dependent evolution of cardiomyogenesis from human BM‐MSCs, with significant applications in cardiac tissue engineering and stem cell transplantation for regenerating lost cardiac tissue.
In this study, we evaluated the standalone and combined effects of collagen gel concentration, azacytidine dosage, and culture duration on the differentiation and maturation of adult human bone marrow‐derived MSC spheroids into cardiomyocytes. The role of canonical Wnt/b‐catenin signaling pathway was assessed. Results suggest that 2 mg/mL collagen gels and 10 uM aza offer optimal environment for time‐dependent evolution of cardiomyogenesis from MSCs, with significant applications in cardiac tissue engineering and stem cell transplantation for regenerating lost cardiac tissue.</description><subject>5‐azacytidine</subject><subject>atomic force microscopy</subject><subject>Autografts</subject><subject>Azacytidine</subject><subject>Bone marrow</subject><subject>Cell culture</subject><subject>Cell interactions</subject><subject>Collagen</subject><subject>Collagen (type I)</subject><subject>collagen gels</subject><subject>Differentiation</subject><subject>Evolution</subject><subject>Gels</subject><subject>Genotypes</subject><subject>Homing</subject><subject>human bone marrow‐derived MSCs</subject><subject>Immunofluorescence</subject><subject>Matrix protein</subject><subject>Mechanical properties</subject><subject>Mesenchyme</subject><subject>Modulus of elasticity</subject><subject>Myocardial infarction</subject><subject>Phenotypes</subject><subject>Pore size</subject><subject>Porosity</subject><subject>Proteins</subject><subject>Signal transduction</subject><subject>Signaling</subject><subject>Spheroids</subject><subject>Stem cell transplantation</subject><subject>Stem cells</subject><subject>Stiffness</subject><subject>Structure-function relationships</subject><subject>Time dependence</subject><subject>Tissue engineering</subject><subject>Transplantation</subject><subject>Wnt protein</subject><subject>Wnt signaling</subject><issn>0006-3592</issn><issn>1097-0290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNp1kctu1DAUhi0EokNhwQsgS2xgkdaXjJ0s6YhLpSIWDOvIlxPGVWIPdkIVVjwCax6PJ-FMp7BAYnV0pO980vl_Qp5ydsYZE-c2TGdCaV7fIyvOWl0x0bL7ZMUYU5Vct-KEPCrlGlfdKPWQnIhWqTVersjP7S4D_Pr-w4cRYgkpmoG6NAzmM8Q0FxqD2wE10VPzzbhlCj5EoAUGcFP4CsNC9zmNaQI6oeEggj1ED3GizmQf0rgkVEEJhfZI0t08mkhtQstock43tzcZXZ6-_7ihZb-DnIIvj8mD3gwFntzNU_Lpzevt5l119eHt5ebVVeVky-pK1k3DOfdWSe8wjtq53koOteqtXWMoNeemlRpEX_deALdWONnbptGa99zLU_Li6MVHvsxQpm4MxQFGEAET6AQTmmkm2xrR5_-g12nOGNmBUo2WupYKqZdHyuVUSoa-2-eAvy4dZ92hsA4L624LQ_bZnXG2I_i_5J-GEDg_AjdhgOX_pu7icntU_gbCQ6Xf</recordid><startdate>201808</startdate><enddate>201808</enddate><creator>Joshi, Jyotsna</creator><creator>Mahajan, Gautam</creator><creator>Kothapalli, Chandrasekhar R.</creator><general>Wiley Subscription Services, Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QF</scope><scope>7QO</scope><scope>7QQ</scope><scope>7SC</scope><scope>7SE</scope><scope>7SP</scope><scope>7SR</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7U5</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>JG9</scope><scope>JQ2</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>P64</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-8450-0640</orcidid></search><sort><creationdate>201808</creationdate><title>Three‐dimensional collagenous niche and azacytidine selectively promote time‐dependent cardiomyogenesis from human bone marrow‐derived MSC spheroids</title><author>Joshi, Jyotsna ; Mahajan, Gautam ; Kothapalli, Chandrasekhar R.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3904-3488111db63dc1004ccfb31e46fbb5714411a937e2f4fd2e1bb2c3fb88771f1d3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>5‐azacytidine</topic><topic>atomic force microscopy</topic><topic>Autografts</topic><topic>Azacytidine</topic><topic>Bone marrow</topic><topic>Cell culture</topic><topic>Cell interactions</topic><topic>Collagen</topic><topic>Collagen (type I)</topic><topic>collagen gels</topic><topic>Differentiation</topic><topic>Evolution</topic><topic>Gels</topic><topic>Genotypes</topic><topic>Homing</topic><topic>human bone marrow‐derived MSCs</topic><topic>Immunofluorescence</topic><topic>Matrix protein</topic><topic>Mechanical properties</topic><topic>Mesenchyme</topic><topic>Modulus of elasticity</topic><topic>Myocardial infarction</topic><topic>Phenotypes</topic><topic>Pore size</topic><topic>Porosity</topic><topic>Proteins</topic><topic>Signal transduction</topic><topic>Signaling</topic><topic>Spheroids</topic><topic>Stem cell transplantation</topic><topic>Stem cells</topic><topic>Stiffness</topic><topic>Structure-function relationships</topic><topic>Time dependence</topic><topic>Tissue engineering</topic><topic>Transplantation</topic><topic>Wnt protein</topic><topic>Wnt signaling</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Joshi, Jyotsna</creatorcontrib><creatorcontrib>Mahajan, Gautam</creatorcontrib><creatorcontrib>Kothapalli, Chandrasekhar R.</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Biotechnology Research Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Biotechnology and bioengineering</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Joshi, Jyotsna</au><au>Mahajan, Gautam</au><au>Kothapalli, Chandrasekhar R.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Three‐dimensional collagenous niche and azacytidine selectively promote time‐dependent cardiomyogenesis from human bone marrow‐derived MSC spheroids</atitle><jtitle>Biotechnology and bioengineering</jtitle><addtitle>Biotechnol Bioeng</addtitle><date>2018-08</date><risdate>2018</risdate><volume>115</volume><issue>8</issue><spage>2013</spage><epage>2026</epage><pages>2013-2026</pages><issn>0006-3592</issn><eissn>1097-0290</eissn><abstract>Endogenous adult cardiac regenerative machinery is not capable of replacing the lost cells following myocardial infarction, often leading to permanent alterations in structure‐function‐mechanical properties. Regenerative therapies based on delivering autologous stem cells within an appropriate 3D milieu could meet such demand, by enabling homing and directed differentiation of the transplanted cells into lost specialized cell populations. Since type I collagen is the predominant cardiac tissue matrix protein, we here optimized the 3D niche which could promote time‐dependent evolution of cardiomyogenesis from human bone marrow‐derived mesenchymal stem cells (BM‐MSC). 3D collagen gel physical and mechanical characteristics were assessed using SEM and AFM, respectively, while the standalone and combined effects of collagen concentration, culture duration, and 5‐azacytidine (aza) dose on the phenotype and genotype of MSC spheroids were quantified using immunofluorescence labeling and RT‐PCR analysis. Increasing collagen concentration led to a significant increase in Young's modulus (p < 0.01) but simultaneous decrease in the mean pore size, resulting in stiffer gels. Spheroid formation significantly modulated MSC differentiation and genotype, mostly due to better cell–cell interactions. Among the aza dosages tested, 10 μM appears to be optimal, while 3 mg/ml gels resulted in significantly lower cell viability compared to 1 or 2 mg/ml gels. Stiffer gels (2 and 3 mg/ml) and exposure to 10 μM aza upregulated early and late cardiac marker expressions in a time‐dependent fashion. On the other hand, cell–cell signaling within the MSC spheroids seem to have a strong role in influencing mature cardiac markers expression, since neither aza nor gel stiffness seem to significantly improve their expression. Western blot analysis suggested that canonical Wnt/β‐catenin signaling pathway might be primarily mediating the observed benefits of aza on cardiac differentiation of MSC spheroids. In conclusion, 2 mg/ml collagen and 10 μM aza appears to offer optimal 3D microenvironment in terms of cell viability and time‐dependent evolution of cardiomyogenesis from human BM‐MSCs, with significant applications in cardiac tissue engineering and stem cell transplantation for regenerating lost cardiac tissue.
In this study, we evaluated the standalone and combined effects of collagen gel concentration, azacytidine dosage, and culture duration on the differentiation and maturation of adult human bone marrow‐derived MSC spheroids into cardiomyocytes. The role of canonical Wnt/b‐catenin signaling pathway was assessed. Results suggest that 2 mg/mL collagen gels and 10 uM aza offer optimal environment for time‐dependent evolution of cardiomyogenesis from MSCs, with significant applications in cardiac tissue engineering and stem cell transplantation for regenerating lost cardiac tissue.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>29665002</pmid><doi>10.1002/bit.26714</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0001-8450-0640</orcidid></addata></record> |
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| subjects | 5‐azacytidine atomic force microscopy Autografts Azacytidine Bone marrow Cell culture Cell interactions Collagen Collagen (type I) collagen gels Differentiation Evolution Gels Genotypes Homing human bone marrow‐derived MSCs Immunofluorescence Matrix protein Mechanical properties Mesenchyme Modulus of elasticity Myocardial infarction Phenotypes Pore size Porosity Proteins Signal transduction Signaling Spheroids Stem cell transplantation Stem cells Stiffness Structure-function relationships Time dependence Tissue engineering Transplantation Wnt protein Wnt signaling |
| title | Three‐dimensional collagenous niche and azacytidine selectively promote time‐dependent cardiomyogenesis from human bone marrow‐derived MSC spheroids |
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