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Proplatelet formation releases into the bloodstream beads-on-a-string preplatelets, which undergo fission into mature platelets. For the first time, we show that preplatelet maturation is a third, tightly regulated, critical process akin to cytokinesis that regulates platelet count. We show that deficiency in cytokine receptor-like factor 3 (CRLF3) in mice leads to an isolated and sustained 25% to 48% reduction in the platelet count without any effect on other blood cell lineages. We show that Crlf3\u2212\/\u2212 preplatelets have increased microtubule stability, possibly because of increased microtubule glutamylation via the interaction of CRLF3 with key members of the Hippo pathway. Using a mouse model of JAK2 V617F essential thrombocythemia, we show that a lack of CRLF3 leads to long-term lineage-specific normalization of the platelet count. We thereby postulate that targeting CRLF3 has therapeutic potential for treatment of thrombocythemia.<\/jats:p>","DOI":"10.1182\/blood.2021013113","type":"journal-article","created":{"date-parts":[[2022,1,20]],"date-time":"2022-01-20T22:11:01Z","timestamp":1642716661000},"page":"2227-2239","update-policy":"https:\/\/doi.org\/10.1182\/blood.2019cm0000","source":"Crossref","is-referenced-by-count":23,"title":["CRLF3 plays a key role in the final stage of platelet genesis and is a potential therapeutic target for thrombocythemia"],"prefix":"10.1182","volume":"139","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-9796-9381","authenticated-orcid":false,"given":"Cavan","family":"Bennett","sequence":"first","affiliation":[{"name":"Department of Haematology, Cambridge Blood Centre, National Health Service Blood and Transplant, University of Cambridge, Cambridge, United 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