Skip to main content
SpringerLink
Log in

Adult-repopulating lymphoid potential of yolk sac blood vessels is not confined to arterial endothelial cells

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

During embryogenesis, hematopoietic stem progenitor cells (HSPCs) are believed to be derived from hemogenic endothelial cells (HECs). Moreover, arterial feature is proposed to be a prerequisite for HECs to generate HSPCs with lymphoid potential. Although the molecular basis of hematopoietic stem cell-competent HECs has been delicately elucidated within the embryo proper, the functional and molecular characteristics of HECs in the extraembryonic yolk sac (YS) remain largely unresolved. In this study, we initially identified six molecularly different endothelial populations in the midgestational YS through integrated analysis of several single-cell RNA sequencing (scRNA-seq) datasets and validated the arterial vasculature distribution of Gja5+ ECs using a Gja5-EGFP reporter mouse model. Further, we explored the hemogenic potential of different EC populations based on their Gja5-EGFP and CD44 expression levels. The hemogenic potential was ubiquitously detected in spatiotemporally different vascular beds on embryonic days (E)8.5–E9.5 and gradually concentrated in CD44-positive ECs from E10.0. Unexpectedly, B-lymphoid potential was detected in the YS ECs as early as E8.5 regardless of their arterial features. Furthermore, the capacity for generating hematopoietic progenitors with in vivo lymphoid potential was found in nonarterial as well as arterial YS ECs on E10.0–E10.5. Importantly, the distinct identities of E10.0–E10.5 HECs between YS and intraembryonic caudal region were revealed by further scRNA-seq analysis. Cumulatively, these findings extend our knowledge regarding the hemogenic potential of ECs from anatomically and molecularly different vascular beds, providing a theoretical basis for better understanding the sources of HSPCs during mammalian development.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahmed, M.S., Byeon, S.E., Jeong, Y., Miah, M.A., Salahuddin, M., Lee, Y., Park, S.S., and Bae, Y.S. (2015). Dab2, a negative regulator of DC immunogenicity, is an attractive molecular target for DC-based immunotherapy. Oncoimmunology 4, e984550.

    Article  PubMed  PubMed Central  Google Scholar 

  • Anders, S., Pyl, P.T., and Huber, W. (2015). HTSeq—a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166–169.

    Article  CAS  PubMed  Google Scholar 

  • Aneja, K., Jalagadugula, G., Mao, G., Singh, A., and Rao, A.K. (2011). Mechanism of platelet factor 4 (PF4) deficiency with RUNX1 haplodeficiency: RUNX1 is a transcriptional regulator of PF4. J Thromb Haemost 9, 383–391.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Artuz, C.M., Knights, A.J., Funnell, A.P.W., Gonda, T.J., Ravid, K., Pearson, R.C.M., Quinlan, K.G.R., and Crossley, M. (2018). Partial reprogramming of heterologous cells by defined factors to generate megakaryocyte lineage-restricted biomolecules. Biotech Rep 20, e00285.

    Article  Google Scholar 

  • Baron, C.S., Kester, L., Klaus, A., Boisset, J.C., Thambyrajah, R., Yvernogeau, L., Kouskoff, V., Lacaud, G., van Oudenaarden, A., and Robin, C. (2018). Single-cell transcriptomics reveal the dynamic of haematopoietic stem cell production in the aorta. Nat Commun 9, 2517.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bennett, M.L., and Bennett, F.C. (2020). The influence of environment and origin on brain resident macrophages and implications for therapy. Nat Neurosci 23, 157–166.

    Article  CAS  PubMed  Google Scholar 

  • Bertrand, J.Y., Jalil, A., Klaine, M., Jung, S., Cumano, A., and Godin, I. (2005). Three pathways to mature macrophages in the early mouse yolk sac. Blood 106, 3004–3011.

    Article  CAS  PubMed  Google Scholar 

  • Bian, Z., Gong, Y., Huang, T., Lee, C.Z.W., Bian, L., Bai, Z., Shi, H., Zeng, Y., Liu, C., He, J., et al. (2020). Deciphering human macrophage development at single-cell resolution. Nature 582, 571–576.

    Article  CAS  PubMed  Google Scholar 

  • Böiers, C., Carrelha, J., Lutteropp, M., Luc, S., Green, J.C.A., Azzoni, E., Woll, P.S., Mead, A.J., Hultquist, A., Swiers, G., et al. (2013). Lymphomyeloid contribution of an immune-restricted progenitor emerging prior to definitive hematopoietic stem cells. Cell Stem Cell 13, 535–548.

    Article  PubMed  Google Scholar 

  • Boisset, J.C., van Cappellen, W., Andrieu-Soler, C., Galjart, N., Dzierzak, E., and Robin, C. (2010). In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464, 116–120.

    Article  CAS  PubMed  Google Scholar 

  • Cumano, A., Dieterlen-Lievre, F., and Godin, I. (1996). Lymphoid potential, probed before circulation in mouse, is restricted to caudal intraembryonic splanchnopleura. Cell 86, 907–916.

    Article  CAS  PubMed  Google Scholar 

  • Cumano, A., Ferraz, J.C., Klaine, M., Di Santo, J.P., and Godin, I. (2001). Intraembryonic, but not yolk sac hematopoietic precursors, isolated before circulation, provide long-term multilineage reconstitution. Immunity 15, 477–485.

    Article  CAS  PubMed  Google Scholar 

  • Cumano, A., and Godin, I. (2007). Ontogeny of the hematopoietic system. Annu Rev Immunol 25, 745–785.

    Article  CAS  PubMed  Google Scholar 

  • de Bruijn, M.F., Speck, N.A., Peeters, M.C., and Dzierzak, E. (2000). Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J 19, 2465–2474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • de Bruijn, M.F., Ma, X., Robin, C., Ottersbach, K., Sanchez, M.J., and Dzierzak, E. (2002). Hematopoietic stem cells localize to the endothelial cell layer in the midgestation mouse aorta. Immunity 16, 673–683.

    Article  CAS  PubMed  Google Scholar 

  • den Hartogh, S.C., Wolstencroft, K., Mummery, C.L., and Passier, R. (2016). A comprehensive gene expression analysis at sequential stages of in vitro cardiac differentiation from isolated MESP1-expressing-mesoderm progenitors. Sci Rep 6, 19386.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Drake, C.J., and Fleming, P.A. (2000). Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95, 1671–1679.

    Article  CAS  PubMed  Google Scholar 

  • Dzierzak, E., and Bigas, A. (2018). Blood development: hematopoietic stem cell dependence and independence. Cell Stem Cell 22, 639–651.

    Article  CAS  PubMed  Google Scholar 

  • Eilken, H.M., Nishikawa, S.I., and Schroeder, T. (2009). Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457, 896–900.

    Article  CAS  PubMed  Google Scholar 

  • Frame, J.M., Fegan, K.H., Conway, S.J., McGrath, K.E., and Palis, J. (2016). Definitive hematopoiesis in the yolk sac emerges from Wntresponsive hemogenic endothelium independently of circulation and arterial identity. Stem Cells 34, 431–444.

    Article  CAS  PubMed  Google Scholar 

  • Ganuza, M., Chabot, A., Tang, X., Bi, W., Natarajan, S., Carter, R., Gawad, C., Kang, G., Cheng, Y., and McKinney-Freeman, S. (2018). Murine hematopoietic stem cell activity is derived from pre-circulation embryos but not yolk sacs. Nat Commun 9, 5405.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gao, L., Tober, J., Gao, P., Chen, C., Tan, K., and Speck, N.A. (2018). RUNX1 and the endothelial origin of blood. Exp Hematol 68, 2–9.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaudet, P., Livstone, M.S., Lewis, S.E., and Thomas, P.D. (2011). Phylogenetic-based propagation of functional annotations within the Gene Ontology consortium. Brief Bioinf 12, 449–462.

    Article  Google Scholar 

  • Getman, M., England, S.J., Malik, J., Peterson, K., Palis, J., and Steiner, L. A. (2014). Extensively self-renewing erythroblasts derived from transgenic β-yac mice is a novel model system for studying globin switching and erythroid maturation. Exp Hematol 42, 536–546.e8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Godin, I.E., Garcia-Porrero, J.A., Coutinho, A., Dieterlen-Lièvre, F., and Marcos, M.A.R. (1993). Para-aortic splanchnopleura from early mouse embryos contains B1a cell progenitors. Nature 364, 67–70.

    Article  CAS  PubMed  Google Scholar 

  • Guo, R., Hu, F., Weng, Q., Lv, C., Wu, H., Liu, L., Li, Z., Zeng, Y., Bai, Z., Zhang, M., et al. (2020). Guiding T lymphopoiesis from pluripotent stem cells by defined transcription factors. Cell Res 30, 21–33.

    Article  CAS  PubMed  Google Scholar 

  • Harris, N., Super, M., Rits, M., Chang, G., and Ezekowitz, R.A. (1992). Characterization of the murine macrophage mannose receptor: demonstration that the downregulation of receptor expression mediated by interferon-gamma occurs at the level of transcription. Blood 80, 2363–2373.

    Article  CAS  PubMed  Google Scholar 

  • Hirose, Y., Saijou, E., Sugano, Y., Takeshita, F., Nishimura, S., Nonaka, H., Chen, Y.R., Sekine, K., Kido, T., Nakamura, T., et al. (2012). Inhibition of Stabilin-2 elevates circulating hyaluronic acid levels and prevents tumor metastasis. Proc Natl Acad Sci USA 109, 4263–4268.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoeffel, G., Chen, J., Lavin, Y., Low, D., Almeida, F.F., See, P., Beaudin, A.E., Lum, J., Low, I., Forsberg, E.C., et al. (2015). c-Myb+ erythromyeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42, 665–678.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Holmes, W.B., and Moncman, C.L. (2008). Nebulette interacts with filamin C. Cell Motil Cytoskeleton 65, 130–142.

    Article  CAS  PubMed  Google Scholar 

  • Hou, S., Li, Z., Zheng, X., Gao, Y., Dong, J., Ni, Y., Wang, X., Li, Y., Ding, X., Chang, Z., et al. (2020). Embryonic endothelial evolution towards first hematopoietic stem cells revealed by single-cell transcriptomic and functional analyses. Cell Res 30, 376–392.

    Article  PubMed  PubMed Central  Google Scholar 

  • Houle, F., Rousseau, S., Morrice, N., Luc, M., Mongrain, S., Turner, C.E., Tanaka, S., Moreau, P., and Huot, J. (2003). Extracellular signalregulated kinase mediates phosphorylation of tropomyosin-1 to promote cytoskeleton remodeling in response to oxidative stress: impact on membrane blebbing. Mol Biol Cell 14, 1418–1432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ivanovs, A., Rybtsov, S., Welch, L., Anderson, R.A., Turner, M.L., and Medvinsky, A. (2011). Highly potent human hematopoietic stem cells first emerge in the intraembryonic aorta-gonad-mesonephros region. J Exp Med 208, 2417–2427.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kallianpur, A.R., Jordan, J.E., and Brandt, S.J. (1994). The SCL/TAL-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 83, 1200–1208.

    Article  CAS  PubMed  Google Scholar 

  • Kalucka, J., de Rooij, L.P.M.H., Goveia, J., Rohlenova, K., Dumas, S.J., Meta, E., Conchinha, N.V., Taverna, F., Teuwen, L.A., Veys, K., et al. (2020). Single-cell transcriptome atlas of murine endothelial cells. Cell 180, 764–779.e20.

    Article  CAS  PubMed  Google Scholar 

  • Kim, D., Langmead, B., and Salzberg, S.L. (2015). HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12, 357–360.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kissa, K., and Herbomel, P. (2010). Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112–115.

    Article  CAS  PubMed  Google Scholar 

  • Lam, E.Y.N., Hall, C.J., Crosier, P.S., Crosier, K.E., and Flores, M.V. (2010). Live imaging of Runx1 expression in the dorsal aorta tracks the emergence of blood progenitors from endothelial cells. Blood 116, 909–914.

    Article  CAS  PubMed  Google Scholar 

  • Lee, L.K., Ghorbanian, Y., Wang, W., Wang, Y., Kim, Y.J., Weissman, I.L., Inlay, M.A., and Mikkola, H.K.A. (2016). LYVE1 marks the divergence of yolk sac definitive hemogenic endothelium from the primitive erythroid lineage. Cell Rep 17, 2286–2298.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, L., Dong, J., Yan, L., Yong, J., Liu, X., Hu, Y., Fan, X., Wu, X., Guo, H., Wang, X., et al. (2017). Single-cell RNA-seq analysis maps development of human germline cells and gonadal niche interactions. Cell Stem Cell 20, 891–892.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z., Lan, Y., He, W., Chen, D., Wang, J., Zhou, F., Wang, Y., Sun, H., Chen, X., Xu, C., et al. (2012). Mouse embryonic head as a site for hematopoietic stem cell development. Cell Stem Cell 11, 663–675.

    Article  CAS  PubMed  Google Scholar 

  • Lin, Y., Yoder, M.C., and Yoshimoto, M. (2014). Lymphoid progenitor emergence in the murine embryo and yolk sac precedes stem cell detection. Stem Cells Dev 23, 1168–1177.

    Article  PubMed  PubMed Central  Google Scholar 

  • Macosko, E.Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A.R., Kamitaki, N., Martersteck, E.M., et al. (2015). Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets. Cell 161, 1202–1214.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matsuoka, S., Tsuji, K., Hisakawa, H., Xu, M., Ebihara, Y., Ishii, T., Sugiyama, D., Manabe, A., Tanaka, R., Ikeda, Y., et al. (2001). Generation of definitive hematopoietic stem cells from murine early yolk sac and paraaortic splanchnopleures by aorta-gonad-mesonephros region-derived stromal cells. Blood 98, 6–12.

    Article  CAS  PubMed  Google Scholar 

  • McGrath, K.E., Frame, J.M., Fegan, K.H., Bowen, J.R., Conway, S.J., Catherman, S.C., Kingsley, P.D., Koniski, A.D., and Palis, J. (2015). Distinct sources of hematopoietic progenitors emerge before HSCs and provide functional blood cells in the mammalian embryo. Cell Rep 11, 1892–1904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Medvinsky, A., and Dzierzak, E. (1996). Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897–906.

    Article  CAS  PubMed  Google Scholar 

  • Medvinsky, A., Rybtsov, S., and Taoudi, S. (2011). Embryonic origin of the adult hematopoietic system: advances and questions. Development 138, 1017–1031.

    Article  CAS  PubMed  Google Scholar 

  • Mikkola, H.K.A., Gekas, C., Orkin, S.H., and Dieterlen-Lievre, F. (2005). Placenta as a site for hematopoietic stem cell development. Exp Hematol 33, 1048–1054.

    Article  CAS  PubMed  Google Scholar 

  • Miquerol, L., Meysen, S., Mangoni, M., Bois, P., van Rijen, H.V.M., Abran, P., Jongsma, H., Nargeot, J., and Gros, D. (2004). Architectural and functional asymmetry of the His-Purkinje system of the murine heart. Cardiovasc Res 63, 77–86.

    Article  CAS  PubMed  Google Scholar 

  • Müller, A.M., Medvinsky, A., Strouboulis, J., Grosveld, F., and Dzierzakt, E. (1994). Development of hematopoietic stem cell activity in the mouse embryo. Immunity 1, 291–301.

    Article  PubMed  Google Scholar 

  • Nonaka, H., Tanaka, M., Suzuki, K., and Miyajima, A. (2007). Development of murine hepatic sinusoidal endothelial cells characterized by the expression of hyaluronan receptors. Dev Dyn 236, 2258–2267.

    Article  CAS  PubMed  Google Scholar 

  • Novershtern, N., Subramanian, A., Lawton, L.N., Mak, R.H., Haining, W. N., McConkey, M.E., Habib, N., Yosef, N., Chang, C.Y., Shay, T., et al. (2011). Densely interconnected transcriptional circuits control cell states in human hematopoiesis. Cell 144, 296–309.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palis, J., Robertson, S., Kennedy, M., Wall, C., and Keller, G. (1999). Development of erythroid and myeloid progenitors in the yolk sac and embryo proper of the mouse. Development 126, 5073–5084.

    Article  CAS  PubMed  Google Scholar 

  • Pi, J., Cheng, Y., Sun, H., Chen, X., Zhuang, T., Liu, J., Li, Y., Chang, H., Zhang, L., Zhang, Y.Z., et al. (2017). Apln-CreERT:mT/mG reporter mice as a tool for sprouting angiogenesis study. BMC Ophthalmol 17, 163.

    Article  PubMed  PubMed Central  Google Scholar 

  • Picelli, S., Björklund, Å.K., Faridani, O.R., Sagasser, S., Winberg, G., and Sandberg, R. (2013). Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat Methods 10, 1096–1098.

    Article  CAS  PubMed  Google Scholar 

  • Pijuan-Sala, B., Griffiths, J.A., Guibentif, C., Hiscock, T.W., Jawaid, W., Calero-Nieto, F.J., Mulas, C., Ibarra-Soria, X., Tyser, R.C.V., Ho, D.L. L., et al. (2019). A single-cell molecular map of mouse gastrulation and early organogenesis. Nature 566, 490–495.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Popson, S.A., Ziegler, M.E., Chen, X., Holderfield, M.T., Shaaban, C.I., Fong, A.H., Welch-Reardon, K.M., Papkoff, J., and Hughes, C.C.W. (2014). Interferon-induced transmembrane protein 1 regulates endothelial lumen formation during angiogenesis. Arterioscler Thromb Vasc Biol 34, 1011–1019.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Prevo, R., Banerji, S., Ferguson, D.J.P., Clasper, S., and Jackson, D.G. (2001). Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium. J Biol Chem 276, 19420–19430.

    Article  CAS  PubMed  Google Scholar 

  • Robin, C., Ottersbach, K., Durand, C., Peeters, M., Vanes, L., Tybulewicz, V., and Dzierzak, E. (2006). An unexpected role for IL-3 in the embryonic development of hematopoietic stem cells. Dev Cell 11, 171–180.

    Article  CAS  PubMed  Google Scholar 

  • Samokhvalov, I.M., Samokhvalova, N.I., and Nishikawa, S.I. (2007). Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446, 1056–1061.

    Article  CAS  PubMed  Google Scholar 

  • Sayeed, S., Asano, E., Ito, S., Ohno, K., Hamaguchi, M., and Senga, T. (2013). S100A10 is required for the organization of actin stress fibers and promotion of cell spreading. Mol Cell Biochem 374, 105–111.

    Article  CAS  PubMed  Google Scholar 

  • Solaimani Kartalaei, P., Yamada-Inagawa, T., Vink, C.S., de Pater, E., van der Linden, R., Marks-Bluth, J., van der Sloot, A., van den Hout, M., Yokomizo, T., van Schaick-Solernó, M.L., et al. (2015). Wholetranscriptome analysis of endothelial to hematopoietic stem cell transition reveals a requirement for Gpr56 in HSC generation. J Exp Med 212, 93–106.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tang, J., Zhang, H., He, L., Huang, X., Li, Y., Pu, W., Yu, W., Zhang, L., Cai, D., Lui, K.O., et al. (2018). Genetic fate mapping defines the vascular potential of endocardial cells in the adult heart. Circ Res 122, 984–993.

    Article  CAS  PubMed  Google Scholar 

  • Thambyrajah, R., Mazan, M., Patel, R., Moignard, V., Stefanska, M., Marinopoulou, E., Li, Y., Lancrin, C., Clapes, T., Möröy, T., et al. (2016). GFI1 proteins orchestrate the emergence of haematopoietic stem cells through recruitment of LSD1. Nat Cell Biol 18, 21–32.

    Article  CAS  PubMed  Google Scholar 

  • Tirosh, I., Izar, B., Prakadan, S.M., Wadsworth, M.H., Treacy, D., Trombetta, J.J., Rotem, A., Rodman, C., Lian, C., Murphy, G., et al. (2016). Dissecting the multicellular ecosystem of metastatic melanoma by single-cell RNA-seq. Science 352, 189–196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tober, J., Koniski, A., McGrath, K.E., Vemishetti, R., Emerson, R., de Mesy-Bentley, K.K.L., Waugh, R., and Palis, J. (2007). The megakaryocyte lineage originates from hemangioblast precursors and is an integral component both of primitive and of definitive hematopoiesis. Blood 109, 1433–1441.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uenishi, G.I., Jung, H.S., Kumar, A., Park, M.A., Hadland, B.K., McLeod, E., Raymond, M., Moskvin, O., Zimmerman, C.E., Theisen, D.J., et al. (2018). NOTCH signaling specifies arterial-type definitive hemogenic endothelium from human pluripotent stem cells. Nat Commun 9, 1828.

    Article  PubMed  PubMed Central  Google Scholar 

  • Walls, J.R., Coultas, L., Rossant, J., and Henkelman, R.M. (2008). Three-dimensional analysis of vascular development in the mouse embryo. PLoS ONE 3, e2853.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, H.U., Chen, Z.F., and Anderson, D.J. (1998). Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93, 741–753.

    Article  CAS  PubMed  Google Scholar 

  • Wareing, S., Eliades, A., Lacaud, G., and Kouskoff, V. (2012). ETV2 expression marks blood and endothelium precursors, including hemogenic endothelium, at the onset of blood development. Dev Dyn 241, 1454–1464.

    Article  CAS  PubMed  Google Scholar 

  • Yamada, Y., Pannell, R., Forster, A., and Rabbitts, T.H. (2000). The oncogenic LIM-only transcription factor Lmo2 regulates angiogenesis but not vasculogenesis in mice. Proc Natl Acad Sci USA 97, 320–324.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoder, M.C., Hiatt, K., Dutt, P., Mukherjee, P., Bodine, D.M., and Orlic, D. (1997a). Characterization of definitive lymphohematopoietic stem cells in the day 9 murine yolk sac. Immunity 7, 335–344.

    Article  CAS  PubMed  Google Scholar 

  • Yoder, M.C., Hiatt, K., and Mukherjee, P. (1997b). In vivo repopulating hematopoietic stem cells are present in the murine yolk sac at day 9.0 postcoitus. Proc Natl Acad Sci USA 94, 6776–6780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokota, T., Huang, J., Tavian, M., Nagai, Y., Hirose, J., Zuniga-Pflucker, J. C., Peault, B., and Kincade, P.W. (2006). Tracing the first waves of lymphopoiesis in mice. Development 133, 2041–2051.

    Article  CAS  PubMed  Google Scholar 

  • Yoshimoto, M., Porayette, P., and Yoder, M.C. (2008). Overcoming obstacles in the search for the site of hematopoietic stem cell emergence. Cell Stem Cell 3, 583–586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimoto, M., Montecino-Rodriguez, E., Ferkowicz, M.J., Porayette, P., Shelley, W.C., Conway, S.J., Dorshkind, K., and Yoder, M.C. (2011). Embryonic day 9 yolk sac and intra-embryonic hemogenic endothelium independently generate a B-1 and marginal zone progenitor lacking B-2 potential. Proc Natl Acad Sci USA 108, 1468–1473.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshimoto, M., Porayette, P., Glosson, N.L., Conway, S.J., Carlesso, N., Cardoso, A.A., Kaplan, M.H., and Yoder, M.C. (2012). Autonomous murine T-cell progenitor production in the extra-embryonic yolk sac before HSC emergence. Blood 119, 5706–5714.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu, G., Wang, L.G., Han, Y., and He, Q.Y. (2012). clusterProfiler: an R package for comparing biological themes among gene clusters. OMICS 16, 284–287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yzaguirre, A.D., and Speck, N.A. (2016). Insights into blood cell formation from hemogenic endothelium in lesser-known anatomic sites. Dev Dyn 245, 1011–1028.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng, Y., He, J., Bai, Z., Li, Z., Gong, Y., Liu, C., Ni, Y., Du, J., Ma, C., Bian, L., et al. (2019). Tracing the first hematopoietic stem cell generation in human embryo by single-cell RNA sequencing. Cell Res 29, 881–894.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou, F., Li, X., Wang, W., Zhu, P., Zhou, J., He, W., Ding, M., Xiong, F., Zheng, X., Li, Z., et al. (2016). Tracing haematopoietic stem cell formation at single-cell resolution. Nature 533, 487–492.

    Article  CAS  PubMed  Google Scholar 

  • Zovein, A.C., Turlo, K.A., Ponec, R.M., Lynch, M.R., Chen, K.C., Hofmann, J.J., Cox, T.C., Gasson, J.C., and Iruela-Arispe, M.L. (2010). Vascular remodeling of the vitelline artery initiates extravascular emergence of hematopoietic clusters. Blood 116, 3435–3444.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2020YFA0112402, 2017YFA0103401, and 2016YFA0100601), the National Natural Science Foundation of China (81890991, 31930054, 31871173, 82000111, and 81900115), the Program for Guangdong Introducing Innovative and Entrepreneurial Teams (2017ZT07S347), and the Key Research and Development Program of Guangdong Province (2019B020234002). The authors thank Lucile Miquerol and Bin Zhou for providing the Gja5EGFP/+ mice.

Author information

Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. Key Laboratory for Regenerative Medicine of Ministry of Education, Institute of Hematology, School of Medicine, Jinan University, Guangzhou, 510632, China

    Chaojie Wang, Siyuan Hou, Bing Liu & Yu Lan

  2. State Key Laboratory of Experimental Hematology, Institute of Hematology, Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China

    Yandong Gong, Zongcheng Li & Bing Liu

  3. State Key Laboratory of Proteomics, Academy of Military Medical Sciences, Academy of Military Sciences, Beijing, 100850, China

    Anbang Wei, Tao Huang & Junjie Du

  4. Integrated Chinese and Western Medicine Postdoctoral Research Station, Jinan University, Guangzhou, 510632, China

    Siyuan Hou

  5. Department of radiotherapy, Fifth Medical Center of Chinese PLA General Hospital, Beijing, 100071, China

    Junliang Wang

Authors
  1. Chaojie Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yandong Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anbang Wei
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tao Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Siyuan Hou
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Junjie Du
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zongcheng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Junliang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Yu Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Bing Liu or Yu Lan.

Ethics declarations

Compliance and ethics The author(s) declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, C., Gong, Y., Wei, A. et al. Adult-repopulating lymphoid potential of yolk sac blood vessels is not confined to arterial endothelial cells. Sci. China Life Sci. 64, 2073–2087 (2021). https://doi.org/10.1007/s11427-021-1935-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-021-1935-2

Keywords

Search

Navigation