Transition of signal requirement in hematopoietic stem cell development from hemogenic endothelial cells
Hematopoietic stem cells (HSCs) develop from hemogenic endothelial cells (HECs) in vivo during mouse embryogenesis. When cultured in vitro, cells from the embryo phenotypically defined as pre-HSC-I and pre-HSC-II have the potential to differentiate into HSCs. However, minimal factors required for HS...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2024-07, Vol.121 (31), p.e2404193121 |
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| creator | Morino-Koga, Saori Tsuruda, Mariko Zhao, Xueyu Oshiro, Shogo Yokomizo, Tomomasa Yamane, Mariko Tanigawa, Shunsuke Miike, Koichiro Usuki, Shingo Yasunaga, Kei-Ichiro Nishinakamura, Ryuichi Suda, Toshio Ogawa, Minetaro |
| description | Hematopoietic stem cells (HSCs) develop from hemogenic endothelial cells (HECs) in vivo during mouse embryogenesis. When cultured in vitro, cells from the embryo phenotypically defined as pre-HSC-I and pre-HSC-II have the potential to differentiate into HSCs. However, minimal factors required for HSC induction from HECs have not yet been determined. In this study, we demonstrated that stem cell factor (SCF) and thrombopoietin (TPO) induced engrafting HSCs from embryonic day (E) 11.5 pre-HSC-I in a serum-free and feeder-free culture condition. In contrast, E10.5 pre-HSC-I and HECs required an endothelial cell layer in addition to SCF and TPO to differentiate into HSCs. A single-cell RNA sequencing analysis of E10.5 to 11.5 dorsal aortae with surrounding tissues and fetal livers detected TPO expression confined in hepatoblasts, while SCF was expressed in various tissues, including endothelial cells and hepatoblasts. Our results suggest a transition of signal requirement during HSC development from HECs. The differentiation of E10.5 HECs to E11.5 pre-HSC-I in the aorta-gonad-mesonephros region depends on SCF and endothelial cell-derived factors. Subsequently, SCF and TPO drive the differentiation of E11.5 pre-HSC-I to pre-HSC-II/HSCs in the fetal liver. The culture system established in this study provides a beneficial tool for exploring the molecular mechanisms underlying the development of HSCs from HECs. |
| doi_str_mv | 10.1073/pnas.2404193121 |
| format | Article |
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When cultured in vitro, cells from the embryo phenotypically defined as pre-HSC-I and pre-HSC-II have the potential to differentiate into HSCs. However, minimal factors required for HSC induction from HECs have not yet been determined. In this study, we demonstrated that stem cell factor (SCF) and thrombopoietin (TPO) induced engrafting HSCs from embryonic day (E) 11.5 pre-HSC-I in a serum-free and feeder-free culture condition. In contrast, E10.5 pre-HSC-I and HECs required an endothelial cell layer in addition to SCF and TPO to differentiate into HSCs. A single-cell RNA sequencing analysis of E10.5 to 11.5 dorsal aortae with surrounding tissues and fetal livers detected TPO expression confined in hepatoblasts, while SCF was expressed in various tissues, including endothelial cells and hepatoblasts. Our results suggest a transition of signal requirement during HSC development from HECs. The differentiation of E10.5 HECs to E11.5 pre-HSC-I in the aorta-gonad-mesonephros region depends on SCF and endothelial cell-derived factors. Subsequently, SCF and TPO drive the differentiation of E11.5 pre-HSC-I to pre-HSC-II/HSCs in the fetal liver. The culture system established in this study provides a beneficial tool for exploring the molecular mechanisms underlying the development of HSCs from HECs.</description><identifier>ISSN: 0027-8424</identifier><identifier>ISSN: 1091-6490</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.2404193121</identifier><identifier>PMID: 39042698</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Animals ; Aorta ; Cell culture ; Cell Differentiation ; Differentiation ; Embryo, Mammalian - cytology ; Embryo, Mammalian - metabolism ; Embryogenesis ; Embryonic Development ; Embryonic growth stage ; Endothelial cells ; Endothelial Cells - cytology ; Endothelial Cells - metabolism ; Fetuses ; Gene expression ; Gene sequencing ; Hemangioblasts - cytology ; Hemangioblasts - metabolism ; Hematopoiesis - physiology ; Hematopoietic stem cells ; Hematopoietic Stem Cells - cytology ; Hematopoietic Stem Cells - metabolism ; In vivo methods and tests ; Liver - cytology ; Liver - embryology ; Liver - metabolism ; Mice ; Molecular modelling ; Sequence analysis ; Signal Transduction ; Stem cell factor ; Stem Cell Factor - metabolism ; Stem cells ; Thrombopoietin ; Thrombopoietin - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2024-07, Vol.121 (31), p.e2404193121</ispartof><rights>Copyright National Academy of Sciences Jul 30, 2024</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1248-8d1c01f879d8f500cfa35a6759a5266d7f80cd20f1eacc22fcf253d4f03fd913</cites><orcidid>0009-0000-8618-0687 ; 0000-0002-4104-8911 ; 0000-0001-8354-174X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>315,782,786,27933,27934</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39042698$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Morino-Koga, Saori</creatorcontrib><creatorcontrib>Tsuruda, Mariko</creatorcontrib><creatorcontrib>Zhao, Xueyu</creatorcontrib><creatorcontrib>Oshiro, Shogo</creatorcontrib><creatorcontrib>Yokomizo, Tomomasa</creatorcontrib><creatorcontrib>Yamane, Mariko</creatorcontrib><creatorcontrib>Tanigawa, Shunsuke</creatorcontrib><creatorcontrib>Miike, Koichiro</creatorcontrib><creatorcontrib>Usuki, Shingo</creatorcontrib><creatorcontrib>Yasunaga, Kei-Ichiro</creatorcontrib><creatorcontrib>Nishinakamura, Ryuichi</creatorcontrib><creatorcontrib>Suda, Toshio</creatorcontrib><creatorcontrib>Ogawa, Minetaro</creatorcontrib><title>Transition of signal requirement in hematopoietic stem cell development from hemogenic endothelial cells</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>Hematopoietic stem cells (HSCs) develop from hemogenic endothelial cells (HECs) in vivo during mouse embryogenesis. When cultured in vitro, cells from the embryo phenotypically defined as pre-HSC-I and pre-HSC-II have the potential to differentiate into HSCs. However, minimal factors required for HSC induction from HECs have not yet been determined. In this study, we demonstrated that stem cell factor (SCF) and thrombopoietin (TPO) induced engrafting HSCs from embryonic day (E) 11.5 pre-HSC-I in a serum-free and feeder-free culture condition. In contrast, E10.5 pre-HSC-I and HECs required an endothelial cell layer in addition to SCF and TPO to differentiate into HSCs. A single-cell RNA sequencing analysis of E10.5 to 11.5 dorsal aortae with surrounding tissues and fetal livers detected TPO expression confined in hepatoblasts, while SCF was expressed in various tissues, including endothelial cells and hepatoblasts. Our results suggest a transition of signal requirement during HSC development from HECs. The differentiation of E10.5 HECs to E11.5 pre-HSC-I in the aorta-gonad-mesonephros region depends on SCF and endothelial cell-derived factors. Subsequently, SCF and TPO drive the differentiation of E11.5 pre-HSC-I to pre-HSC-II/HSCs in the fetal liver. The culture system established in this study provides a beneficial tool for exploring the molecular mechanisms underlying the development of HSCs from HECs.</description><subject>Animals</subject><subject>Aorta</subject><subject>Cell culture</subject><subject>Cell Differentiation</subject><subject>Differentiation</subject><subject>Embryo, Mammalian - cytology</subject><subject>Embryo, Mammalian - metabolism</subject><subject>Embryogenesis</subject><subject>Embryonic Development</subject><subject>Embryonic growth stage</subject><subject>Endothelial cells</subject><subject>Endothelial Cells - cytology</subject><subject>Endothelial Cells - metabolism</subject><subject>Fetuses</subject><subject>Gene expression</subject><subject>Gene sequencing</subject><subject>Hemangioblasts - cytology</subject><subject>Hemangioblasts - metabolism</subject><subject>Hematopoiesis - physiology</subject><subject>Hematopoietic stem cells</subject><subject>Hematopoietic Stem Cells - cytology</subject><subject>Hematopoietic Stem Cells - metabolism</subject><subject>In vivo methods and tests</subject><subject>Liver - cytology</subject><subject>Liver - embryology</subject><subject>Liver - metabolism</subject><subject>Mice</subject><subject>Molecular modelling</subject><subject>Sequence analysis</subject><subject>Signal Transduction</subject><subject>Stem cell factor</subject><subject>Stem Cell Factor - metabolism</subject><subject>Stem cells</subject><subject>Thrombopoietin</subject><subject>Thrombopoietin - metabolism</subject><issn>0027-8424</issn><issn>1091-6490</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpd0UtLxTAQBeAgil4fa3dScOOmOnm0TZYivkBwc_clJhNvpE1q0gr-e1uf4CqbL4eZOYQcUzin0PCLIeh8zgQIqjhldIusKCha1kLBNlkBsKaUgok9sp_zCwCoSsIu2eMKBKuVXJHNOumQ_ehjKKIrsn8OuisSvk4-YY9hLHwoNtjrMQ7R4-hNkUfsC4NdV1h8wy4On8yl2C8wPmOYEQYbxw12fk5bbD4kO053GY--3wOyvrleX92VD4-391eXD6WhTMhSWmqAOtkoK10FYJzmla6bSumK1bVtnARjGTiK2hjGnHGs4lY44M4qyg_I2VfskOLrhHlse5-XAXTAOOWWgxTAJNBmpqf_6Euc0rz-p2q4VErwWV18KZNizgldOyTf6_TeUmiXDtqlg_avg_nHyXfu9NSj_fU_R-cfFnmECg</recordid><startdate>20240730</startdate><enddate>20240730</enddate><creator>Morino-Koga, Saori</creator><creator>Tsuruda, Mariko</creator><creator>Zhao, Xueyu</creator><creator>Oshiro, Shogo</creator><creator>Yokomizo, Tomomasa</creator><creator>Yamane, Mariko</creator><creator>Tanigawa, Shunsuke</creator><creator>Miike, Koichiro</creator><creator>Usuki, Shingo</creator><creator>Yasunaga, Kei-Ichiro</creator><creator>Nishinakamura, Ryuichi</creator><creator>Suda, Toshio</creator><creator>Ogawa, Minetaro</creator><general>National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0009-0000-8618-0687</orcidid><orcidid>https://orcid.org/0000-0002-4104-8911</orcidid><orcidid>https://orcid.org/0000-0001-8354-174X</orcidid></search><sort><creationdate>20240730</creationdate><title>Transition of signal requirement in hematopoietic stem cell development from hemogenic endothelial cells</title><author>Morino-Koga, Saori ; 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When cultured in vitro, cells from the embryo phenotypically defined as pre-HSC-I and pre-HSC-II have the potential to differentiate into HSCs. However, minimal factors required for HSC induction from HECs have not yet been determined. In this study, we demonstrated that stem cell factor (SCF) and thrombopoietin (TPO) induced engrafting HSCs from embryonic day (E) 11.5 pre-HSC-I in a serum-free and feeder-free culture condition. In contrast, E10.5 pre-HSC-I and HECs required an endothelial cell layer in addition to SCF and TPO to differentiate into HSCs. A single-cell RNA sequencing analysis of E10.5 to 11.5 dorsal aortae with surrounding tissues and fetal livers detected TPO expression confined in hepatoblasts, while SCF was expressed in various tissues, including endothelial cells and hepatoblasts. Our results suggest a transition of signal requirement during HSC development from HECs. The differentiation of E10.5 HECs to E11.5 pre-HSC-I in the aorta-gonad-mesonephros region depends on SCF and endothelial cell-derived factors. Subsequently, SCF and TPO drive the differentiation of E11.5 pre-HSC-I to pre-HSC-II/HSCs in the fetal liver. The culture system established in this study provides a beneficial tool for exploring the molecular mechanisms underlying the development of HSCs from HECs.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>39042698</pmid><doi>10.1073/pnas.2404193121</doi><orcidid>https://orcid.org/0009-0000-8618-0687</orcidid><orcidid>https://orcid.org/0000-0002-4104-8911</orcidid><orcidid>https://orcid.org/0000-0001-8354-174X</orcidid></addata></record> |
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| subjects | Animals Aorta Cell culture Cell Differentiation Differentiation Embryo, Mammalian - cytology Embryo, Mammalian - metabolism Embryogenesis Embryonic Development Embryonic growth stage Endothelial cells Endothelial Cells - cytology Endothelial Cells - metabolism Fetuses Gene expression Gene sequencing Hemangioblasts - cytology Hemangioblasts - metabolism Hematopoiesis - physiology Hematopoietic stem cells Hematopoietic Stem Cells - cytology Hematopoietic Stem Cells - metabolism In vivo methods and tests Liver - cytology Liver - embryology Liver - metabolism Mice Molecular modelling Sequence analysis Signal Transduction Stem cell factor Stem Cell Factor - metabolism Stem cells Thrombopoietin Thrombopoietin - metabolism |
| title | Transition of signal requirement in hematopoietic stem cell development from hemogenic endothelial cells |
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