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Embryonic hematopoiesis in vertebrate somites gives rise to definitive hematopoietic stem cells
Juhui Qiu1,*, Xiaoying Fan2,3,4, Yixia Wang1, Hongbin Jin1, Yixiao Song1, Yang Han5, Shenghong Huang1, Yaping Meng1, Fuchou Tang2,3,4, and Anming Meng1,*
1State Key Laboratory of Membrane Biology, Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing 100084, China
2Biodynamic Optical Imaging Center, College of Life Sciences, Department of Obstetrics and Gynecology, Third Hospital, and Ministry of Education Key Laboratory of Cell Proliferation and Differentiation, Peking University, Beijing 100871, China
3Peking-Tsinghua Center for Life Sciences, Peking University, Beijing 100871, China
4Center for Molecular and Translational Medicine, Peking University Health Science Center, Beijing 100191, China
5College of Biological Sciences, China Agricultural University, Beijing 100083, China *Correspondence to:Anming Meng, E-mail: mengam@mail.tsinghua.edu.cn; Juhui Qiu, E-mail: jhqiu2008@126.com
J Mol Cell Biol, Volume 8, Issue 4, August 2016, Pages 288-301  https://doi.org/10.1093/jmcb/mjw024
Keyword: primitive hematopoiesis definitive hematopoiesis stem cells blood somite embryos zebrafish

Hematopoietic stem cells (HSCs) replenish all types of blood cells. It is debating whether HSCs in adults solely originate from the aorta-gonad-mesonephros (AGM) region, more specifically, the dorsal aorta, during embryogenesis. Here, we report that somite hematopoiesis, a previously unwitnessed hematopoiesis, can generate definitive HSCs (dHSCs) in zebrafish. By transgenic lineage tracing, we found that a subset of cells within the forming somites emigrate ventromedially and mix with lateral plate mesoderm-derived primitive hematopoietic cells before the blood circulation starts. These somite-derived hematopoietic precursors and stem cells (sHPSCs) subsequently enter the circulation and colonize the kidney of larvae and adults. RNA-seq analysis reveals that sHPSCs express hematopoietic genes with sustained expression of many muscle/skeletal genes. Embryonic sHPSCs transplanted into wild-type embryos expand during growth and survive for life time with differentiation into various hematopoietic lineages, indicating self-renewal and multipotency features. Therefore, the embryonic origin of dHSCs in adults is not restricted to the AGM.