Tyrosyl-tRNA synthetase stimulates thrombopoietin-independent hematopoiesis accelerating recovery from thrombocytopenia
New mechanisms behind blood cell formation continue to be uncovered, with therapeutic approaches for hematological diseases being of great interest. Here we report an enzyme in protein synthesis, known for cell-based activities beyond translation, is a factor inducing megakaryocyte-biased hematopoie...
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| Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 2018-08, Vol.115 (35), p.E8228-E8235 |
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| creator | Kanaji, Taisuke Vo, My-Nuong Kanaji, Sachiko Zarpellon, Alessandro Shapiro, Ryan Morodomi, Yosuke Yuzuriha, Akinori Eto, Koji Belani, Rajesh Do, Minh-Ha Yang, Xiang-Lei Ruggeri, Zaverio M. Schimmel, Paul |
| description | New mechanisms behind blood cell formation continue to be uncovered, with therapeutic approaches for hematological diseases being of great interest. Here we report an enzyme in protein synthesis, known for cell-based activities beyond translation, is a factor inducing megakaryocyte-biased hematopoiesis, most likely under stress conditions. We show an activated form of tyrosyl-tRNA synthetase (YRSACT), prepared either by rationally designed mutagenesis or alternative splicing, induces expansion of a previously unrecognized high-ploidy Sca-1⁺ megakaryocyte population capable of accelerating platelet replenishment after depletion. Moreover, YRSACT targets monocytic cells to induce secretion of transacting cytokines that enhance megakaryocyte expansion stimulating the Toll-like receptor/MyD88 pathway. Platelet replenishment by YRSACT is independent of thrombopoietin (TPO), as evidenced by expansion of the megakaryocytes from induced pluripotent stem cell-derived hematopoietic stem cells from a patient deficient in TPO signaling. We suggest megakaryocyte-biased hematopoiesis induced by YRSACT offers new approaches for treating thrombocytopenia, boosting yields from cell-culture production of platelet concentrates for transfusion, and bridging therapy for hematopoietic stem cell transplantation. |
| doi_str_mv | 10.1073/pnas.1807000115 |
| format | Article |
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Here we report an enzyme in protein synthesis, known for cell-based activities beyond translation, is a factor inducing megakaryocyte-biased hematopoiesis, most likely under stress conditions. We show an activated form of tyrosyl-tRNA synthetase (YRSACT), prepared either by rationally designed mutagenesis or alternative splicing, induces expansion of a previously unrecognized high-ploidy Sca-1⁺ megakaryocyte population capable of accelerating platelet replenishment after depletion. Moreover, YRSACT targets monocytic cells to induce secretion of transacting cytokines that enhance megakaryocyte expansion stimulating the Toll-like receptor/MyD88 pathway. Platelet replenishment by YRSACT is independent of thrombopoietin (TPO), as evidenced by expansion of the megakaryocytes from induced pluripotent stem cell-derived hematopoietic stem cells from a patient deficient in TPO signaling. We suggest megakaryocyte-biased hematopoiesis induced by YRSACT offers new approaches for treating thrombocytopenia, boosting yields from cell-culture production of platelet concentrates for transfusion, and bridging therapy for hematopoietic stem cell transplantation.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1807000115</identifier><identifier>PMID: 30104364</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>Alternative splicing ; Biological Sciences ; Blood cells ; Blood Platelets - metabolism ; Blood Platelets - pathology ; Cell culture ; Cell Culture Techniques ; Cells ; Cells, Cultured ; Cytokines ; Enzymes ; Expansion ; Female ; Hematological diseases ; Hematology ; Hematopoiesis ; Hematopoietic stem cells ; Hematopoietic Stem Cells - metabolism ; Hematopoietic Stem Cells - pathology ; Humans ; Immune system ; Induced Pluripotent Stem Cells - metabolism ; Induced Pluripotent Stem Cells - pathology ; Male ; Megakaryocytes ; Megakaryocytes - metabolism ; Megakaryocytes - pathology ; Monocytes ; Mutagenesis ; MyD88 protein ; Platelets ; Ploidy ; Pluripotency ; PNAS Plus ; Polyploidy ; Protein biosynthesis ; Protein synthesis ; Proteins ; Replenishment ; Signal Transduction ; Splicing ; Stem cell transplantation ; Stem cells ; Thrombocytopenia ; Thrombocytopenia - metabolism ; Thrombocytopenia - pathology ; Thrombopoietin ; Thrombopoietin - metabolism ; Toll-like receptors ; Transfusion ; Transplantation ; tRNA ; Tyrosine-tRNA ligase ; Tyrosine-tRNA Ligase - metabolism</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2018-08, Vol.115 (35), p.E8228-E8235</ispartof><rights>Volumes 1–89 and 106–115, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright © 2018 the Author(s). Published by PNAS.</rights><rights>Copyright National Academy of Sciences Aug 28, 2018</rights><rights>Copyright © 2018 the Author(s). Published by PNAS. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c509t-8cc6876c88b5a3f2c21814f04b1e68c59fe105ceac0b3c22ce355799354bc0ef3</citedby><cites>FETCH-LOGICAL-c509t-8cc6876c88b5a3f2c21814f04b1e68c59fe105ceac0b3c22ce355799354bc0ef3</cites><orcidid>0000-0003-0807-1295</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26530346$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26530346$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30104364$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Kanaji, Taisuke</creatorcontrib><creatorcontrib>Vo, My-Nuong</creatorcontrib><creatorcontrib>Kanaji, Sachiko</creatorcontrib><creatorcontrib>Zarpellon, Alessandro</creatorcontrib><creatorcontrib>Shapiro, Ryan</creatorcontrib><creatorcontrib>Morodomi, Yosuke</creatorcontrib><creatorcontrib>Yuzuriha, Akinori</creatorcontrib><creatorcontrib>Eto, Koji</creatorcontrib><creatorcontrib>Belani, Rajesh</creatorcontrib><creatorcontrib>Do, Minh-Ha</creatorcontrib><creatorcontrib>Yang, Xiang-Lei</creatorcontrib><creatorcontrib>Ruggeri, Zaverio M.</creatorcontrib><creatorcontrib>Schimmel, Paul</creatorcontrib><title>Tyrosyl-tRNA synthetase stimulates thrombopoietin-independent hematopoiesis accelerating recovery from thrombocytopenia</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>New mechanisms behind blood cell formation continue to be uncovered, with therapeutic approaches for hematological diseases being of great interest. Here we report an enzyme in protein synthesis, known for cell-based activities beyond translation, is a factor inducing megakaryocyte-biased hematopoiesis, most likely under stress conditions. We show an activated form of tyrosyl-tRNA synthetase (YRSACT), prepared either by rationally designed mutagenesis or alternative splicing, induces expansion of a previously unrecognized high-ploidy Sca-1⁺ megakaryocyte population capable of accelerating platelet replenishment after depletion. Moreover, YRSACT targets monocytic cells to induce secretion of transacting cytokines that enhance megakaryocyte expansion stimulating the Toll-like receptor/MyD88 pathway. Platelet replenishment by YRSACT is independent of thrombopoietin (TPO), as evidenced by expansion of the megakaryocytes from induced pluripotent stem cell-derived hematopoietic stem cells from a patient deficient in TPO signaling. We suggest megakaryocyte-biased hematopoiesis induced by YRSACT offers new approaches for treating thrombocytopenia, boosting yields from cell-culture production of platelet concentrates for transfusion, and bridging therapy for hematopoietic stem cell transplantation.</description><subject>Alternative splicing</subject><subject>Biological Sciences</subject><subject>Blood cells</subject><subject>Blood Platelets - metabolism</subject><subject>Blood Platelets - pathology</subject><subject>Cell culture</subject><subject>Cell Culture Techniques</subject><subject>Cells</subject><subject>Cells, Cultured</subject><subject>Cytokines</subject><subject>Enzymes</subject><subject>Expansion</subject><subject>Female</subject><subject>Hematological diseases</subject><subject>Hematology</subject><subject>Hematopoiesis</subject><subject>Hematopoietic stem cells</subject><subject>Hematopoietic Stem Cells - metabolism</subject><subject>Hematopoietic Stem Cells - pathology</subject><subject>Humans</subject><subject>Immune system</subject><subject>Induced Pluripotent Stem Cells - metabolism</subject><subject>Induced Pluripotent Stem Cells - pathology</subject><subject>Male</subject><subject>Megakaryocytes</subject><subject>Megakaryocytes - metabolism</subject><subject>Megakaryocytes - pathology</subject><subject>Monocytes</subject><subject>Mutagenesis</subject><subject>MyD88 protein</subject><subject>Platelets</subject><subject>Ploidy</subject><subject>Pluripotency</subject><subject>PNAS Plus</subject><subject>Polyploidy</subject><subject>Protein biosynthesis</subject><subject>Protein synthesis</subject><subject>Proteins</subject><subject>Replenishment</subject><subject>Signal Transduction</subject><subject>Splicing</subject><subject>Stem cell transplantation</subject><subject>Stem cells</subject><subject>Thrombocytopenia</subject><subject>Thrombocytopenia - metabolism</subject><subject>Thrombocytopenia - pathology</subject><subject>Thrombopoietin</subject><subject>Thrombopoietin - metabolism</subject><subject>Toll-like receptors</subject><subject>Transfusion</subject><subject>Transplantation</subject><subject>tRNA</subject><subject>Tyrosine-tRNA ligase</subject><subject>Tyrosine-tRNA Ligase - 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Here we report an enzyme in protein synthesis, known for cell-based activities beyond translation, is a factor inducing megakaryocyte-biased hematopoiesis, most likely under stress conditions. We show an activated form of tyrosyl-tRNA synthetase (YRSACT), prepared either by rationally designed mutagenesis or alternative splicing, induces expansion of a previously unrecognized high-ploidy Sca-1⁺ megakaryocyte population capable of accelerating platelet replenishment after depletion. Moreover, YRSACT targets monocytic cells to induce secretion of transacting cytokines that enhance megakaryocyte expansion stimulating the Toll-like receptor/MyD88 pathway. Platelet replenishment by YRSACT is independent of thrombopoietin (TPO), as evidenced by expansion of the megakaryocytes from induced pluripotent stem cell-derived hematopoietic stem cells from a patient deficient in TPO signaling. We suggest megakaryocyte-biased hematopoiesis induced by YRSACT offers new approaches for treating thrombocytopenia, boosting yields from cell-culture production of platelet concentrates for transfusion, and bridging therapy for hematopoietic stem cell transplantation.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>30104364</pmid><doi>10.1073/pnas.1807000115</doi><orcidid>https://orcid.org/0000-0003-0807-1295</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | Alternative splicing Biological Sciences Blood cells Blood Platelets - metabolism Blood Platelets - pathology Cell culture Cell Culture Techniques Cells Cells, Cultured Cytokines Enzymes Expansion Female Hematological diseases Hematology Hematopoiesis Hematopoietic stem cells Hematopoietic Stem Cells - metabolism Hematopoietic Stem Cells - pathology Humans Immune system Induced Pluripotent Stem Cells - metabolism Induced Pluripotent Stem Cells - pathology Male Megakaryocytes Megakaryocytes - metabolism Megakaryocytes - pathology Monocytes Mutagenesis MyD88 protein Platelets Ploidy Pluripotency PNAS Plus Polyploidy Protein biosynthesis Protein synthesis Proteins Replenishment Signal Transduction Splicing Stem cell transplantation Stem cells Thrombocytopenia Thrombocytopenia - metabolism Thrombocytopenia - pathology Thrombopoietin Thrombopoietin - metabolism Toll-like receptors Transfusion Transplantation tRNA Tyrosine-tRNA ligase Tyrosine-tRNA Ligase - metabolism |
| title | Tyrosyl-tRNA synthetase stimulates thrombopoietin-independent hematopoiesis accelerating recovery from thrombocytopenia |
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