C-type lectin-like receptor 2 specifies a functionally distinct subpopulation within phenotypically defined hematopoietic stem cell population that contribute to emergent megakaryopoiesis
C-type lectin-like receptor 2 (CLEC-2) expressed on megakaryocytes plays important roles in megakaryopoiesis. We found that CLEC-2 was expressed in about 20% of phenotypical long-term hematopoietic stem cells (LT-HSCs), which expressed lower levels of HSC-specific genes and produced larger amounts o...
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| Veröffentlicht in: | International journal of hematology 2022-03, Vol.115 (3), p.310-321 |
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| creator | Kumode, Takahiro Tanaka, Hirokazu Esipinoza, Jorge Luis Rai, Shinya Taniguchi, Yasuhiro Fujiwara, Ryosuke Sano, Keigo Serizawa, Kentaro Iwata, Yoshio Morita, Yasuyoshi Matsumura, Itaru |
| description | C-type lectin-like receptor 2 (CLEC-2) expressed on megakaryocytes plays important roles in megakaryopoiesis. We found that CLEC-2 was expressed in about 20% of phenotypical long-term hematopoietic stem cells (LT-HSCs), which expressed lower levels of HSC-specific genes and produced larger amounts of megakaryocyte-related molecules than CLEC-2
low
LT-HSCs. Although CLEC-2
high
LT-HSCs had immature clonogenic activity, cultured CLEC-2
high
LT-HSCs preferentially differentiated into megakaryocytes. CLEC-2
high
HSCs yielded 6.8 times more megakaryocyte progenitors (MkPs) and 6.0 times more platelets 2 weeks and 1 week after transplantation compared with CLEC-2
low
LT-HSCs. However, platelet yield from CLEC-2
high
HSCs gradually declined with the loss of MkPs, while CLEC-2
low
HSCs self-renewed long-term, indicating that CLEC-2
high
LT-HSCs mainly contribute to early megakaryopoiesis. Treatment with pI:C and LPS increased the proportion of CLEC-2
high
LT-HSCs within LT-HSCs. Almost all CLEC-2
low
LT-HSCs were in the G0 phase and barely responded to pI:C. In contrast, 54% of CLEC-2
high
LT-HSCs were in G0, and pI:C treatment obliged CLEC-2
high
LT-HSCs to enter the cell cycle and differentiate into megakaryocytes, indicating that CLEC-2
high
LT-HSCs are primed for cell cycle entry and rapidly yield platelets in response to inflammatory stress. In conclusion, CLEC-2
high
LT-HSCs appear to act as a reserve for emergent platelet production under stress conditions. |
| doi_str_mv | 10.1007/s12185-021-03220-9 |
| format | Article |
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low
LT-HSCs. Although CLEC-2
high
LT-HSCs had immature clonogenic activity, cultured CLEC-2
high
LT-HSCs preferentially differentiated into megakaryocytes. CLEC-2
high
HSCs yielded 6.8 times more megakaryocyte progenitors (MkPs) and 6.0 times more platelets 2 weeks and 1 week after transplantation compared with CLEC-2
low
LT-HSCs. However, platelet yield from CLEC-2
high
HSCs gradually declined with the loss of MkPs, while CLEC-2
low
HSCs self-renewed long-term, indicating that CLEC-2
high
LT-HSCs mainly contribute to early megakaryopoiesis. Treatment with pI:C and LPS increased the proportion of CLEC-2
high
LT-HSCs within LT-HSCs. Almost all CLEC-2
low
LT-HSCs were in the G0 phase and barely responded to pI:C. In contrast, 54% of CLEC-2
high
LT-HSCs were in G0, and pI:C treatment obliged CLEC-2
high
LT-HSCs to enter the cell cycle and differentiate into megakaryocytes, indicating that CLEC-2
high
LT-HSCs are primed for cell cycle entry and rapidly yield platelets in response to inflammatory stress. In conclusion, CLEC-2
high
LT-HSCs appear to act as a reserve for emergent platelet production under stress conditions.</description><identifier>ISSN: 0925-5710</identifier><identifier>EISSN: 1865-3774</identifier><identifier>DOI: 10.1007/s12185-021-03220-9</identifier><identifier>PMID: 35106701</identifier><language>eng</language><publisher>Singapore: Springer Singapore</publisher><subject>Animals ; Blood Platelets ; Cell Cycle ; Cell differentiation ; Cell Differentiation - genetics ; Gene Expression ; Hematology ; Hematopoietic stem cells ; Hematopoietic Stem Cells - metabolism ; Hematopoietic Stem Cells - physiology ; Inflammation ; Lectins, C-Type - genetics ; Lectins, C-Type - metabolism ; Lectins, C-Type - physiology ; Lipopolysaccharides ; Medicine ; Medicine & Public Health ; Megakaryocytes ; Megakaryocytes - metabolism ; Mice ; Mice, Inbred C57BL ; Oncology ; Original Article ; Phenotype ; Platelets ; Progenitor cells ; Receptors ; Stem cells ; Thrombopoiesis - genetics ; Thrombopoiesis - physiology ; Transplantation</subject><ispartof>International journal of hematology, 2022-03, Vol.115 (3), p.310-321</ispartof><rights>Japanese Society of Hematology 2022</rights><rights>2022. Japanese Society of Hematology.</rights><rights>Japanese Society of Hematology 2022.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c399t-9525dfc3b4e6d096dd01fecfbfe5eb71e8f9bb1f6da2aa6c16b015723eefe823</citedby><cites>FETCH-LOGICAL-c399t-9525dfc3b4e6d096dd01fecfbfe5eb71e8f9bb1f6da2aa6c16b015723eefe823</cites><orcidid>0000-0002-7192-525X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s12185-021-03220-9$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s12185-021-03220-9$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,780,784,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/35106701$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kumode, Takahiro</creatorcontrib><creatorcontrib>Tanaka, Hirokazu</creatorcontrib><creatorcontrib>Esipinoza, Jorge Luis</creatorcontrib><creatorcontrib>Rai, Shinya</creatorcontrib><creatorcontrib>Taniguchi, Yasuhiro</creatorcontrib><creatorcontrib>Fujiwara, Ryosuke</creatorcontrib><creatorcontrib>Sano, Keigo</creatorcontrib><creatorcontrib>Serizawa, Kentaro</creatorcontrib><creatorcontrib>Iwata, Yoshio</creatorcontrib><creatorcontrib>Morita, Yasuyoshi</creatorcontrib><creatorcontrib>Matsumura, Itaru</creatorcontrib><title>C-type lectin-like receptor 2 specifies a functionally distinct subpopulation within phenotypically defined hematopoietic stem cell population that contribute to emergent megakaryopoiesis</title><title>International journal of hematology</title><addtitle>Int J Hematol</addtitle><addtitle>Int J Hematol</addtitle><description>C-type lectin-like receptor 2 (CLEC-2) expressed on megakaryocytes plays important roles in megakaryopoiesis. We found that CLEC-2 was expressed in about 20% of phenotypical long-term hematopoietic stem cells (LT-HSCs), which expressed lower levels of HSC-specific genes and produced larger amounts of megakaryocyte-related molecules than CLEC-2
low
LT-HSCs. Although CLEC-2
high
LT-HSCs had immature clonogenic activity, cultured CLEC-2
high
LT-HSCs preferentially differentiated into megakaryocytes. CLEC-2
high
HSCs yielded 6.8 times more megakaryocyte progenitors (MkPs) and 6.0 times more platelets 2 weeks and 1 week after transplantation compared with CLEC-2
low
LT-HSCs. However, platelet yield from CLEC-2
high
HSCs gradually declined with the loss of MkPs, while CLEC-2
low
HSCs self-renewed long-term, indicating that CLEC-2
high
LT-HSCs mainly contribute to early megakaryopoiesis. Treatment with pI:C and LPS increased the proportion of CLEC-2
high
LT-HSCs within LT-HSCs. Almost all CLEC-2
low
LT-HSCs were in the G0 phase and barely responded to pI:C. In contrast, 54% of CLEC-2
high
LT-HSCs were in G0, and pI:C treatment obliged CLEC-2
high
LT-HSCs to enter the cell cycle and differentiate into megakaryocytes, indicating that CLEC-2
high
LT-HSCs are primed for cell cycle entry and rapidly yield platelets in response to inflammatory stress. In conclusion, CLEC-2
high
LT-HSCs appear to act as a reserve for emergent platelet production under stress conditions.</description><subject>Animals</subject><subject>Blood Platelets</subject><subject>Cell Cycle</subject><subject>Cell differentiation</subject><subject>Cell Differentiation - genetics</subject><subject>Gene Expression</subject><subject>Hematology</subject><subject>Hematopoietic stem cells</subject><subject>Hematopoietic Stem Cells - metabolism</subject><subject>Hematopoietic Stem Cells - physiology</subject><subject>Inflammation</subject><subject>Lectins, C-Type - genetics</subject><subject>Lectins, C-Type - metabolism</subject><subject>Lectins, C-Type - physiology</subject><subject>Lipopolysaccharides</subject><subject>Medicine</subject><subject>Medicine & Public Health</subject><subject>Megakaryocytes</subject><subject>Megakaryocytes - metabolism</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Oncology</subject><subject>Original Article</subject><subject>Phenotype</subject><subject>Platelets</subject><subject>Progenitor cells</subject><subject>Receptors</subject><subject>Stem cells</subject><subject>Thrombopoiesis - genetics</subject><subject>Thrombopoiesis - physiology</subject><subject>Transplantation</subject><issn>0925-5710</issn><issn>1865-3774</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNp9kctu1TAQhi0Eooe2L8ACWWLDxuBLHCdLdAQUqVI33UeOMz7HbWIH2xE6z8bL1WnKRSy6msV8883YP0JvGf3IKFWfEuOskYRyRqjgnJL2BdqxppZEKFW9RDvackmkYvQMvUnpjlKmaKVeozMhGa0VZTv0a0_yaQY8gsnOk9HdA45gYM4hYo7TDMZZBwlrbBdfmOD1OJ7w4FLhTcZp6ecwL6NeW_iny0fn8XwEH4rXmQ0G6zwM-AiTzmEODrIzOGWYsIFxxP8I8lFnbILP0fVLBpwDhgniAXzGExz0vY6nR0Ny6QK9snpMcPlUz9Ht1y-3-ytyffPt-_7zNTGibTNpJZeDNaKvoB5oWw8DZRaM7S1I6BWDxrZ9z2w9aK51bVjdUyYVFwAWGi7O0YdNO8fwY4GUu8ml9W7tISyp4zWvyg7VVAV9_x96F5ZYfmylhJCqpmwV8o0yMaQUwXZzdFN5WMdotybbbcl2JdnuMdmuLUPvntRLP8HwZ-R3lAUQG5BKyx8g_t39jPYBQt610w</recordid><startdate>20220301</startdate><enddate>20220301</enddate><creator>Kumode, Takahiro</creator><creator>Tanaka, Hirokazu</creator><creator>Esipinoza, Jorge Luis</creator><creator>Rai, Shinya</creator><creator>Taniguchi, Yasuhiro</creator><creator>Fujiwara, Ryosuke</creator><creator>Sano, Keigo</creator><creator>Serizawa, Kentaro</creator><creator>Iwata, Yoshio</creator><creator>Morita, Yasuyoshi</creator><creator>Matsumura, Itaru</creator><general>Springer Singapore</general><general>Springer Nature B.V</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>3V.</scope><scope>7RV</scope><scope>7T5</scope><scope>7T7</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>C1K</scope><scope>CCPQU</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>H94</scope><scope>K9.</scope><scope>KB0</scope><scope>M0S</scope><scope>M1P</scope><scope>NAPCQ</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-7192-525X</orcidid></search><sort><creationdate>20220301</creationdate><title>C-type lectin-like receptor 2 specifies a functionally distinct subpopulation within phenotypically defined hematopoietic stem cell population that contribute to emergent megakaryopoiesis</title><author>Kumode, Takahiro ; Tanaka, Hirokazu ; Esipinoza, Jorge Luis ; Rai, Shinya ; Taniguchi, Yasuhiro ; Fujiwara, Ryosuke ; Sano, Keigo ; Serizawa, Kentaro ; Iwata, Yoshio ; Morita, Yasuyoshi ; Matsumura, Itaru</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c399t-9525dfc3b4e6d096dd01fecfbfe5eb71e8f9bb1f6da2aa6c16b015723eefe823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Animals</topic><topic>Blood Platelets</topic><topic>Cell Cycle</topic><topic>Cell differentiation</topic><topic>Cell Differentiation - genetics</topic><topic>Gene Expression</topic><topic>Hematology</topic><topic>Hematopoietic stem cells</topic><topic>Hematopoietic Stem Cells - metabolism</topic><topic>Hematopoietic Stem Cells - physiology</topic><topic>Inflammation</topic><topic>Lectins, C-Type - genetics</topic><topic>Lectins, C-Type - metabolism</topic><topic>Lectins, C-Type - physiology</topic><topic>Lipopolysaccharides</topic><topic>Medicine</topic><topic>Medicine & Public Health</topic><topic>Megakaryocytes</topic><topic>Megakaryocytes - metabolism</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Oncology</topic><topic>Original Article</topic><topic>Phenotype</topic><topic>Platelets</topic><topic>Progenitor cells</topic><topic>Receptors</topic><topic>Stem cells</topic><topic>Thrombopoiesis - genetics</topic><topic>Thrombopoiesis - physiology</topic><topic>Transplantation</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kumode, Takahiro</creatorcontrib><creatorcontrib>Tanaka, Hirokazu</creatorcontrib><creatorcontrib>Esipinoza, Jorge Luis</creatorcontrib><creatorcontrib>Rai, Shinya</creatorcontrib><creatorcontrib>Taniguchi, Yasuhiro</creatorcontrib><creatorcontrib>Fujiwara, Ryosuke</creatorcontrib><creatorcontrib>Sano, Keigo</creatorcontrib><creatorcontrib>Serizawa, Kentaro</creatorcontrib><creatorcontrib>Iwata, Yoshio</creatorcontrib><creatorcontrib>Morita, Yasuyoshi</creatorcontrib><creatorcontrib>Matsumura, Itaru</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing & Allied Health Database</collection><collection>Immunology Abstracts</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</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>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</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 China</collection><collection>MEDLINE - Academic</collection><jtitle>International journal of hematology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kumode, Takahiro</au><au>Tanaka, Hirokazu</au><au>Esipinoza, Jorge Luis</au><au>Rai, Shinya</au><au>Taniguchi, Yasuhiro</au><au>Fujiwara, Ryosuke</au><au>Sano, Keigo</au><au>Serizawa, Kentaro</au><au>Iwata, Yoshio</au><au>Morita, Yasuyoshi</au><au>Matsumura, Itaru</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>C-type lectin-like receptor 2 specifies a functionally distinct subpopulation within phenotypically defined hematopoietic stem cell population that contribute to emergent megakaryopoiesis</atitle><jtitle>International journal of hematology</jtitle><stitle>Int J Hematol</stitle><addtitle>Int J Hematol</addtitle><date>2022-03-01</date><risdate>2022</risdate><volume>115</volume><issue>3</issue><spage>310</spage><epage>321</epage><pages>310-321</pages><issn>0925-5710</issn><eissn>1865-3774</eissn><abstract>C-type lectin-like receptor 2 (CLEC-2) expressed on megakaryocytes plays important roles in megakaryopoiesis. We found that CLEC-2 was expressed in about 20% of phenotypical long-term hematopoietic stem cells (LT-HSCs), which expressed lower levels of HSC-specific genes and produced larger amounts of megakaryocyte-related molecules than CLEC-2
low
LT-HSCs. Although CLEC-2
high
LT-HSCs had immature clonogenic activity, cultured CLEC-2
high
LT-HSCs preferentially differentiated into megakaryocytes. CLEC-2
high
HSCs yielded 6.8 times more megakaryocyte progenitors (MkPs) and 6.0 times more platelets 2 weeks and 1 week after transplantation compared with CLEC-2
low
LT-HSCs. However, platelet yield from CLEC-2
high
HSCs gradually declined with the loss of MkPs, while CLEC-2
low
HSCs self-renewed long-term, indicating that CLEC-2
high
LT-HSCs mainly contribute to early megakaryopoiesis. Treatment with pI:C and LPS increased the proportion of CLEC-2
high
LT-HSCs within LT-HSCs. Almost all CLEC-2
low
LT-HSCs were in the G0 phase and barely responded to pI:C. In contrast, 54% of CLEC-2
high
LT-HSCs were in G0, and pI:C treatment obliged CLEC-2
high
LT-HSCs to enter the cell cycle and differentiate into megakaryocytes, indicating that CLEC-2
high
LT-HSCs are primed for cell cycle entry and rapidly yield platelets in response to inflammatory stress. In conclusion, CLEC-2
high
LT-HSCs appear to act as a reserve for emergent platelet production under stress conditions.</abstract><cop>Singapore</cop><pub>Springer Singapore</pub><pmid>35106701</pmid><doi>10.1007/s12185-021-03220-9</doi><tpages>12</tpages><orcidid>https://orcid.org/0000-0002-7192-525X</orcidid></addata></record> |
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| source | MEDLINE; SpringerNature Journals |
| subjects | Animals Blood Platelets Cell Cycle Cell differentiation Cell Differentiation - genetics Gene Expression Hematology Hematopoietic stem cells Hematopoietic Stem Cells - metabolism Hematopoietic Stem Cells - physiology Inflammation Lectins, C-Type - genetics Lectins, C-Type - metabolism Lectins, C-Type - physiology Lipopolysaccharides Medicine Medicine & Public Health Megakaryocytes Megakaryocytes - metabolism Mice Mice, Inbred C57BL Oncology Original Article Phenotype Platelets Progenitor cells Receptors Stem cells Thrombopoiesis - genetics Thrombopoiesis - physiology Transplantation |
| title | C-type lectin-like receptor 2 specifies a functionally distinct subpopulation within phenotypically defined hematopoietic stem cell population that contribute to emergent megakaryopoiesis |
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