High ploidy large cytoplasmic megakaryocytes are hematopoietic stem cells regulators and essential for platelet production

Shen Y. Heazlewood, Tanveer Ahmad, Benjamin Cao, Huimin Cao, Melanie Domingues, Xuan Sun, Chad K. Heazlewood, Songhui Li, Brenda Williams, Madeline Fulton, Jacinta F. White, Tom Nebl, Christian M. Nefzger, Jose M. Polo, Benjamin T. Kile, Felix Kraus, Michael T. Ryan, Yu B. Sun, Peter F.M. Choong, Sarah L. EllisMinna Liisa Anko, Susan K. Nilsson

    Research output: Contribution to journalArticleScientificpeer-review

    13 Citations (Scopus)
    8 Downloads (Pure)

    Abstract

    Megakaryocytes (MK) generate platelets. Recently, we and others, have reported MK also regulate hematopoietic stem cells (HSC). Here we show high ploidy large cytoplasmic megakaryocytes (LCM) are critical negative regulators of HSC and critical for platelet formation. Using a mouse knockout model (Pf4-Srsf3Δ/Δ) with normal MK numbers, but essentially devoid of LCM, we demonstrate a pronounced increase in BM HSC concurrent with endogenous mobilization and extramedullary hematopoiesis. Severe thrombocytopenia is observed in animals with diminished LCM, although there is no change in MK ploidy distribution, uncoupling endoreduplication and platelet production. When HSC isolated from a microenvironment essentially devoid of LCM reconstitute hematopoiesis in lethally irradiated mice, the absence of LCM increases HSC in BM, blood and spleen, and the recapitulation of thrombocytopenia. In contrast, following a competitive transplant using minimal numbers of WT HSC together with HSC from a microenvironment with diminished LCM, sufficient WT HSC-generated LCM regulates a normal HSC pool and prevents thrombocytopenia. Importantly, LCM are conserved in humans.
    Original languageEnglish
    Article number2099
    Number of pages18
    JournalNature Communications
    Volume14
    Issue number1
    DOIs
    Publication statusPublished - 13 Apr 2023
    Publication typeA1 Journal article-refereed

    Publication forum classification

    • Publication forum level 3

    ASJC Scopus subject areas

    • General Chemistry
    • General Biochemistry,Genetics and Molecular Biology
    • General
    • General Physics and Astronomy

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