Single-Cell RNA-Seq Reveals LRRC75A-Expressing Cell Population Involved in VEGF Secretion of Multipotent Mesenchymal Stromal/Stem Cells Under Ischemia
Abstract Human multipotent mesenchymal stromal/stem cells (MSCs) have been utilized in cell therapy for various diseases and their clinical applications are expected to increase in the future. However, the variation in MSC-based product quality due to the MSC heterogeneity has resulted in significan...
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| Veröffentlicht in: | Stem cells translational medicine 2023-06, Vol.12 (6), p.379-390 |
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| creator | Miura, Takumi Kouno, Tsukasa Takano, Megumi Kuroda, Takuya Yamamoto, Yumiko Kusakawa, Shinji Morioka, Masaki Suimye Sugawara, Tohru Hirai, Takamasa Yasuda, Satoshi Sawada, Rumi Matsuyama, Satoko Kawaji, Hideya Kasukawa, Takeya Itoh, Masayoshi Matsuyama, Akifumi Shin, Jay W Umezawa, Akihiro Kawai, Jun Sato, Yoji |
| description | Abstract
Human multipotent mesenchymal stromal/stem cells (MSCs) have been utilized in cell therapy for various diseases and their clinical applications are expected to increase in the future. However, the variation in MSC-based product quality due to the MSC heterogeneity has resulted in significant constraints in the clinical utility of MSCs. Therefore, we hypothesized that it might be important to identify and ensure/enrich suitable cell subpopulations for therapies using MSC-based products. In this study, we aimed to identify functional cell subpopulations to predict the efficacy of angiogenic therapy using bone marrow-derived MSCs (BM-MSCs). To assess its angiogenic potency, we observed various levels of vascular endothelial growth factor (VEGF) secretion among 11 donor-derived BM-MSC lines under in vitro ischemic culture conditions. Next, by clarifying the heterogeneity of BM-MSCs using single-cell RNA-sequencing analysis, we identified a functional cell subpopulation that contributed to the overall VEGF production in BM-MSC lines under ischemic conditions. We also found that leucine-rich repeat-containing 75A (LRRC75A) was more highly expressed in this cell subpopulation than in the others. Importantly, knockdown of LRRC75A using small interfering RNA resulted in significant inhibition of VEGF secretion in ischemic BM-MSCs, indicating that LRRC75A regulates VEGF secretion under ischemic conditions. Therefore, LRRC75A may be a useful biomarker to identify cell subpopulations that contribute to the angiogenic effects of BM-MSCs. Our work provides evidence that a strategy based on single-cell transcriptome profiles is effective for identifying functional cell subpopulations in heterogeneous MSC-based products.
Graphical Abstract
We identified a cell subpopulation associated with VEGF secretion in human multipotent mesenchymal stromal/stem cells under ischemia using single-cell transcriptome analysis and highlighted the potential contribution of LRRC75A on inducing VEGF secretion under ischemia. |
| doi_str_mv | 10.1093/stcltm/szad029 |
| format | Article |
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Human multipotent mesenchymal stromal/stem cells (MSCs) have been utilized in cell therapy for various diseases and their clinical applications are expected to increase in the future. However, the variation in MSC-based product quality due to the MSC heterogeneity has resulted in significant constraints in the clinical utility of MSCs. Therefore, we hypothesized that it might be important to identify and ensure/enrich suitable cell subpopulations for therapies using MSC-based products. In this study, we aimed to identify functional cell subpopulations to predict the efficacy of angiogenic therapy using bone marrow-derived MSCs (BM-MSCs). To assess its angiogenic potency, we observed various levels of vascular endothelial growth factor (VEGF) secretion among 11 donor-derived BM-MSC lines under in vitro ischemic culture conditions. Next, by clarifying the heterogeneity of BM-MSCs using single-cell RNA-sequencing analysis, we identified a functional cell subpopulation that contributed to the overall VEGF production in BM-MSC lines under ischemic conditions. We also found that leucine-rich repeat-containing 75A (LRRC75A) was more highly expressed in this cell subpopulation than in the others. Importantly, knockdown of LRRC75A using small interfering RNA resulted in significant inhibition of VEGF secretion in ischemic BM-MSCs, indicating that LRRC75A regulates VEGF secretion under ischemic conditions. Therefore, LRRC75A may be a useful biomarker to identify cell subpopulations that contribute to the angiogenic effects of BM-MSCs. Our work provides evidence that a strategy based on single-cell transcriptome profiles is effective for identifying functional cell subpopulations in heterogeneous MSC-based products.
Graphical Abstract
We identified a cell subpopulation associated with VEGF secretion in human multipotent mesenchymal stromal/stem cells under ischemia using single-cell transcriptome analysis and highlighted the potential contribution of LRRC75A on inducing VEGF secretion under ischemia.</description><identifier>ISSN: 2157-6564</identifier><identifier>EISSN: 2157-6580</identifier><identifier>DOI: 10.1093/stcltm/szad029</identifier><identifier>PMID: 37263619</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Bone Marrow Cells ; Cell Differentiation ; Cell Proliferation ; Humans ; Ischemia - genetics ; Ischemia - metabolism ; Ischemia - therapy ; Manufacturing for Regenerative Medicine ; Mesenchymal Stem Cells ; Single-Cell Gene Expression Analysis ; Stem Cells ; Vascular Endothelial Growth Factor A - genetics ; Vascular Endothelial Growth Factor A - metabolism ; Vascular Endothelial Growth Factors - metabolism ; Vascular Endothelial Growth Factors - pharmacology</subject><ispartof>Stem cells translational medicine, 2023-06, Vol.12 (6), p.379-390</ispartof><rights>The Author(s) 2023. Published by Oxford University Press. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c425t-bd215fbafc6408ad6d9d8e12ef2f3e2f3bbbb6ecddfbe1b23fc576a5efbc32b73</citedby><cites>FETCH-LOGICAL-c425t-bd215fbafc6408ad6d9d8e12ef2f3e2f3bbbb6ecddfbe1b23fc576a5efbc32b73</cites><orcidid>0000-0001-5085-0802 ; 0000-0002-9889-1272</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/PMC10267575/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10267575/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,1598,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37263619$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Miura, Takumi</creatorcontrib><creatorcontrib>Kouno, Tsukasa</creatorcontrib><creatorcontrib>Takano, Megumi</creatorcontrib><creatorcontrib>Kuroda, Takuya</creatorcontrib><creatorcontrib>Yamamoto, Yumiko</creatorcontrib><creatorcontrib>Kusakawa, Shinji</creatorcontrib><creatorcontrib>Morioka, Masaki Suimye</creatorcontrib><creatorcontrib>Sugawara, Tohru</creatorcontrib><creatorcontrib>Hirai, Takamasa</creatorcontrib><creatorcontrib>Yasuda, Satoshi</creatorcontrib><creatorcontrib>Sawada, Rumi</creatorcontrib><creatorcontrib>Matsuyama, Satoko</creatorcontrib><creatorcontrib>Kawaji, Hideya</creatorcontrib><creatorcontrib>Kasukawa, Takeya</creatorcontrib><creatorcontrib>Itoh, Masayoshi</creatorcontrib><creatorcontrib>Matsuyama, Akifumi</creatorcontrib><creatorcontrib>Shin, Jay W</creatorcontrib><creatorcontrib>Umezawa, Akihiro</creatorcontrib><creatorcontrib>Kawai, Jun</creatorcontrib><creatorcontrib>Sato, Yoji</creatorcontrib><title>Single-Cell RNA-Seq Reveals LRRC75A-Expressing Cell Population Involved in VEGF Secretion of Multipotent Mesenchymal Stromal/Stem Cells Under Ischemia</title><title>Stem cells translational medicine</title><addtitle>Stem Cells Transl Med</addtitle><description>Abstract
Human multipotent mesenchymal stromal/stem cells (MSCs) have been utilized in cell therapy for various diseases and their clinical applications are expected to increase in the future. However, the variation in MSC-based product quality due to the MSC heterogeneity has resulted in significant constraints in the clinical utility of MSCs. Therefore, we hypothesized that it might be important to identify and ensure/enrich suitable cell subpopulations for therapies using MSC-based products. In this study, we aimed to identify functional cell subpopulations to predict the efficacy of angiogenic therapy using bone marrow-derived MSCs (BM-MSCs). To assess its angiogenic potency, we observed various levels of vascular endothelial growth factor (VEGF) secretion among 11 donor-derived BM-MSC lines under in vitro ischemic culture conditions. Next, by clarifying the heterogeneity of BM-MSCs using single-cell RNA-sequencing analysis, we identified a functional cell subpopulation that contributed to the overall VEGF production in BM-MSC lines under ischemic conditions. We also found that leucine-rich repeat-containing 75A (LRRC75A) was more highly expressed in this cell subpopulation than in the others. Importantly, knockdown of LRRC75A using small interfering RNA resulted in significant inhibition of VEGF secretion in ischemic BM-MSCs, indicating that LRRC75A regulates VEGF secretion under ischemic conditions. Therefore, LRRC75A may be a useful biomarker to identify cell subpopulations that contribute to the angiogenic effects of BM-MSCs. Our work provides evidence that a strategy based on single-cell transcriptome profiles is effective for identifying functional cell subpopulations in heterogeneous MSC-based products.
Graphical Abstract
We identified a cell subpopulation associated with VEGF secretion in human multipotent mesenchymal stromal/stem cells under ischemia using single-cell transcriptome analysis and highlighted the potential contribution of LRRC75A on inducing VEGF secretion under ischemia.</description><subject>Bone Marrow Cells</subject><subject>Cell Differentiation</subject><subject>Cell Proliferation</subject><subject>Humans</subject><subject>Ischemia - genetics</subject><subject>Ischemia - metabolism</subject><subject>Ischemia - therapy</subject><subject>Manufacturing for Regenerative Medicine</subject><subject>Mesenchymal Stem Cells</subject><subject>Single-Cell Gene Expression Analysis</subject><subject>Stem Cells</subject><subject>Vascular Endothelial Growth Factor A - genetics</subject><subject>Vascular Endothelial Growth Factor A - metabolism</subject><subject>Vascular Endothelial Growth Factors - metabolism</subject><subject>Vascular Endothelial Growth Factors - pharmacology</subject><issn>2157-6564</issn><issn>2157-6580</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>TOX</sourceid><sourceid>EIF</sourceid><recordid>eNqFkcFr2zAUxs1YaUvba49Dx-3gxpJj2T6NENI2kG4jXncVsvTUeMiSK8lh3R_Sv3dakoXttAfiCd5Pn77HlyTXOLvBWZ1PfBA69BP_k8uM1G-Sc4KLMqVFlb093un0LLny_nsWi9a0JtlpcpaXhOYU1-fJa9OZJw3pHLRG60-ztIFntIYtcO3Rar2el8UsXfwYHHgfSbTjvthh1Dx01qCl2Vq9BYk6g74t7m5RA8LBbmQVehh16AYbwAT0AB6M2Lz0XKMmOBv7pAnQ7yQ9ejQSHFp6sYG-45fJiYoO4OrQL5LH28XX-X26-ny3nM9WqZiSIqStjFuqlitBp1nFJZW1rAATUETlEE8bi4KQUrWAW5IrUZSUF6BakZO2zC-Sj3vdYWx7kCIadVyzwXU9dy_M8o79OzHdhj3ZLcMZoWVRFlHh_UHB2ecRfGB950VciRuwo2ekIiQvq7zGEb3Zo8JZ7x2o4z84Y78DZftA2SHQ-ODd3-6O-J_4IvBhD9hx-J_YLwKWsYQ</recordid><startdate>20230615</startdate><enddate>20230615</enddate><creator>Miura, Takumi</creator><creator>Kouno, Tsukasa</creator><creator>Takano, Megumi</creator><creator>Kuroda, Takuya</creator><creator>Yamamoto, Yumiko</creator><creator>Kusakawa, Shinji</creator><creator>Morioka, Masaki Suimye</creator><creator>Sugawara, Tohru</creator><creator>Hirai, Takamasa</creator><creator>Yasuda, Satoshi</creator><creator>Sawada, Rumi</creator><creator>Matsuyama, Satoko</creator><creator>Kawaji, Hideya</creator><creator>Kasukawa, Takeya</creator><creator>Itoh, Masayoshi</creator><creator>Matsuyama, Akifumi</creator><creator>Shin, Jay W</creator><creator>Umezawa, Akihiro</creator><creator>Kawai, Jun</creator><creator>Sato, Yoji</creator><general>Oxford University Press</general><scope>TOX</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-5085-0802</orcidid><orcidid>https://orcid.org/0000-0002-9889-1272</orcidid></search><sort><creationdate>20230615</creationdate><title>Single-Cell RNA-Seq Reveals LRRC75A-Expressing Cell Population Involved in VEGF Secretion of Multipotent Mesenchymal Stromal/Stem Cells Under Ischemia</title><author>Miura, Takumi ; Kouno, Tsukasa ; Takano, Megumi ; Kuroda, Takuya ; Yamamoto, Yumiko ; Kusakawa, Shinji ; Morioka, Masaki Suimye ; Sugawara, Tohru ; Hirai, Takamasa ; Yasuda, Satoshi ; Sawada, Rumi ; Matsuyama, Satoko ; Kawaji, Hideya ; Kasukawa, Takeya ; Itoh, Masayoshi ; Matsuyama, Akifumi ; Shin, Jay W ; Umezawa, Akihiro ; Kawai, Jun ; Sato, Yoji</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c425t-bd215fbafc6408ad6d9d8e12ef2f3e2f3bbbb6ecddfbe1b23fc576a5efbc32b73</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Bone Marrow Cells</topic><topic>Cell Differentiation</topic><topic>Cell Proliferation</topic><topic>Humans</topic><topic>Ischemia - genetics</topic><topic>Ischemia - metabolism</topic><topic>Ischemia - therapy</topic><topic>Manufacturing for Regenerative Medicine</topic><topic>Mesenchymal Stem Cells</topic><topic>Single-Cell Gene Expression Analysis</topic><topic>Stem Cells</topic><topic>Vascular Endothelial Growth Factor A - genetics</topic><topic>Vascular Endothelial Growth Factor A - metabolism</topic><topic>Vascular Endothelial Growth Factors - metabolism</topic><topic>Vascular Endothelial Growth Factors - pharmacology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Miura, Takumi</creatorcontrib><creatorcontrib>Kouno, Tsukasa</creatorcontrib><creatorcontrib>Takano, Megumi</creatorcontrib><creatorcontrib>Kuroda, Takuya</creatorcontrib><creatorcontrib>Yamamoto, Yumiko</creatorcontrib><creatorcontrib>Kusakawa, Shinji</creatorcontrib><creatorcontrib>Morioka, Masaki Suimye</creatorcontrib><creatorcontrib>Sugawara, Tohru</creatorcontrib><creatorcontrib>Hirai, Takamasa</creatorcontrib><creatorcontrib>Yasuda, Satoshi</creatorcontrib><creatorcontrib>Sawada, Rumi</creatorcontrib><creatorcontrib>Matsuyama, Satoko</creatorcontrib><creatorcontrib>Kawaji, Hideya</creatorcontrib><creatorcontrib>Kasukawa, Takeya</creatorcontrib><creatorcontrib>Itoh, Masayoshi</creatorcontrib><creatorcontrib>Matsuyama, Akifumi</creatorcontrib><creatorcontrib>Shin, Jay W</creatorcontrib><creatorcontrib>Umezawa, Akihiro</creatorcontrib><creatorcontrib>Kawai, Jun</creatorcontrib><creatorcontrib>Sato, Yoji</creatorcontrib><collection>Oxford Academic Journals (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>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Stem cells translational medicine</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Miura, Takumi</au><au>Kouno, Tsukasa</au><au>Takano, Megumi</au><au>Kuroda, Takuya</au><au>Yamamoto, Yumiko</au><au>Kusakawa, Shinji</au><au>Morioka, Masaki Suimye</au><au>Sugawara, Tohru</au><au>Hirai, Takamasa</au><au>Yasuda, Satoshi</au><au>Sawada, Rumi</au><au>Matsuyama, Satoko</au><au>Kawaji, Hideya</au><au>Kasukawa, Takeya</au><au>Itoh, Masayoshi</au><au>Matsuyama, Akifumi</au><au>Shin, Jay W</au><au>Umezawa, Akihiro</au><au>Kawai, Jun</au><au>Sato, Yoji</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Single-Cell RNA-Seq Reveals LRRC75A-Expressing Cell Population Involved in VEGF Secretion of Multipotent Mesenchymal Stromal/Stem Cells Under Ischemia</atitle><jtitle>Stem cells translational medicine</jtitle><addtitle>Stem Cells Transl Med</addtitle><date>2023-06-15</date><risdate>2023</risdate><volume>12</volume><issue>6</issue><spage>379</spage><epage>390</epage><pages>379-390</pages><issn>2157-6564</issn><eissn>2157-6580</eissn><abstract>Abstract
Human multipotent mesenchymal stromal/stem cells (MSCs) have been utilized in cell therapy for various diseases and their clinical applications are expected to increase in the future. However, the variation in MSC-based product quality due to the MSC heterogeneity has resulted in significant constraints in the clinical utility of MSCs. Therefore, we hypothesized that it might be important to identify and ensure/enrich suitable cell subpopulations for therapies using MSC-based products. In this study, we aimed to identify functional cell subpopulations to predict the efficacy of angiogenic therapy using bone marrow-derived MSCs (BM-MSCs). To assess its angiogenic potency, we observed various levels of vascular endothelial growth factor (VEGF) secretion among 11 donor-derived BM-MSC lines under in vitro ischemic culture conditions. Next, by clarifying the heterogeneity of BM-MSCs using single-cell RNA-sequencing analysis, we identified a functional cell subpopulation that contributed to the overall VEGF production in BM-MSC lines under ischemic conditions. We also found that leucine-rich repeat-containing 75A (LRRC75A) was more highly expressed in this cell subpopulation than in the others. Importantly, knockdown of LRRC75A using small interfering RNA resulted in significant inhibition of VEGF secretion in ischemic BM-MSCs, indicating that LRRC75A regulates VEGF secretion under ischemic conditions. Therefore, LRRC75A may be a useful biomarker to identify cell subpopulations that contribute to the angiogenic effects of BM-MSCs. Our work provides evidence that a strategy based on single-cell transcriptome profiles is effective for identifying functional cell subpopulations in heterogeneous MSC-based products.
Graphical Abstract
We identified a cell subpopulation associated with VEGF secretion in human multipotent mesenchymal stromal/stem cells under ischemia using single-cell transcriptome analysis and highlighted the potential contribution of LRRC75A on inducing VEGF secretion under ischemia.</abstract><cop>US</cop><pub>Oxford University Press</pub><pmid>37263619</pmid><doi>10.1093/stcltm/szad029</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0001-5085-0802</orcidid><orcidid>https://orcid.org/0000-0002-9889-1272</orcidid><oa>free_for_read</oa></addata></record> |
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| ispartof | Stem cells translational medicine, 2023-06, Vol.12 (6), p.379-390 |
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| subjects | Bone Marrow Cells Cell Differentiation Cell Proliferation Humans Ischemia - genetics Ischemia - metabolism Ischemia - therapy Manufacturing for Regenerative Medicine Mesenchymal Stem Cells Single-Cell Gene Expression Analysis Stem Cells Vascular Endothelial Growth Factor A - genetics Vascular Endothelial Growth Factor A - metabolism Vascular Endothelial Growth Factors - metabolism Vascular Endothelial Growth Factors - pharmacology |
| title | Single-Cell RNA-Seq Reveals LRRC75A-Expressing Cell Population Involved in VEGF Secretion of Multipotent Mesenchymal Stromal/Stem Cells Under Ischemia |
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