A Transient Developmental Hematopoietic Stem Cell Gives Rise to Innate-like B and T Cells

Cell Stem Cell

Volumn 19, Issue 6, 2016, Pages 768-783

  Beaudin, Anna E ^a,c   Boyer, Scott W ^a   Perez Cunningham, Jessica ^a   Hernandez, Gloria E ^a   Derderian, S Christopher ^b   Jujjavarapu, Chethan ^a   Aaserude, Eric ^a   MacKenzie, Tippi ^b   Forsberg, E Camilla ^a  

^a University of California Santa Cruz   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

development; hematopoiesis; hematopoietic stem cell; immune cells; innate like B and T lymphocytes; lineage potential; lineage tracing; self renewal; tissue resident; transplantation

Indexed keywords

CD150 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; FIBRINOGEN RECEPTOR; STEM CELL ANTIGEN 1; T LYMPHOCYTE RECEPTOR; GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL EXPERIMENT; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CELL SURVIVAL; FETUS DEVELOPMENT; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IN VIVO STUDY; INNATE IMMUNITY; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RNA SEQUENCE; T LYMPHOCYTE; ANIMAL; CELL AGING; CELL LINEAGE; CYTOLOGY; EMBRYOLOGY; IMMUNOLOGY; LIVER; METABOLISM; SEQUENCE ANALYSIS; THYMUS; TUMOR MICROENVIRONMENT;

ANIMALS; B-LYMPHOCYTES; CELL AGING; CELL LINEAGE; CELLULAR MICROENVIRONMENT; FETAL DEVELOPMENT; GREEN FLUORESCENT PROTEINS; HEMATOPOIETIC STEM CELLS; IMMUNITY, INNATE; LIVER; MICE; SEQUENCE ANALYSIS, RNA; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84994517460     PISSN: 19345909     EISSN: 18759777     Source Type: Journal    
DOI: 10.1016/j.stem.2016.08.013     Document Type: Article

References (46)

1. Barber, C.L., Montecino-Rodriguez, E., Dorshkind, K., Reduced production of B-1-specified common lymphoid progenitors results in diminished potential of adult marrow to generate B-1 cells. Proc. Natl. Acad. Sci. USA 108 (2011), 13700–13704.
2. Beaudin, A.E., Boyer, S.W., Forsberg, E.C., Flk2/Flt3 promotes both myeloid and lymphoid development by expanding non-self-renewing multipotent hematopoietic progenitor cells. Exp. Hematol. 42 (2014), 218–229.
3. Benlagha, K., Kyin, T., Beavis, A., Teyton, L., Bendelac, A., A thymic precursor to the NK T cell lineage. Science 296 (2002), 553–555.
4. Benz, C., Copley, M.R., Kent, D.G., Wohrer, S., Cortes, A., Aghaeepour, N., Ma, E., Mader, H., Rowe, K., Day, C., et al. Hematopoietic stem cell subtypes expand differentially during development and display distinct lymphopoietic programs. Cell Stem Cell 10 (2012), 273–283.
5. Bowie, M.B., Kent, D.G., Dykstra, B., McKnight, K.D., McCaffrey, L., Hoodless, P.A., Eaves, C.J., Identification of a new intrinsically timed developmental checkpoint that reprograms key hematopoietic stem cell properties. Proc. Natl. Acad. Sci. USA 104 (2007), 5878–5882.
6. Boyer, S.W., Schroeder, A.V., Smith-Berdan, S., Forsberg, E.C., All hematopoietic cells develop from hematopoietic stem cells through Flk2/Flt3-positive progenitor cells. Cell Stem Cell 9 (2011), 64–73.
7. Boyer, S.W., Beaudin, A.E., Forsberg, E.C., Mapping differentiation pathways from hematopoietic stem cells using Flk2/Flt3 lineage tracing. Cell Cycle 11 (2012), 3180–3188.
8. Burt, T.D., Fetal regulatory T cells and peripheral immune tolerance in utero: implications for development and disease. Am. J. Reprod. Immunol. 69 (2013), 346–358.
9. Busch, K., Klapproth, K., Barile, M., Flossdorf, M., Holland-Letz, T., Schlenner, S.M., Reth, M., Höfer, T., Rodewald, H.R., Fundamental properties of unperturbed haematopoiesis from stem cells in vivo. Nature 518 (2015), 542–546.
10. Buza-Vidas, N., Woll, P., Hultquist, A., Duarte, S., Lutteropp, M., Bouriez-Jones, T., Ferry, H., Luc, S., Jacobsen, S.E., FLT3 expression initiates in fully multipotent mouse hematopoietic progenitor cells. Blood 118 (2011), 1544–1548.
11. Carey, J.B., Moffatt-Blue, C.S., Watson, L.C., Gavin, A.L., Feeney, A.J., Repertoire-based selection into the marginal zone compartment during B cell development. J. Exp. Med. 205 (2008), 2043–2052.
12. Challen, G.A., Boles, N.C., Chambers, S.M., Goodell, M.A., Distinct hematopoietic stem cell subtypes are differentially regulated by TGF-beta1. Cell Stem Cell 6 (2010), 265–278.
13. Christensen, J.L., Weissman, I.L., Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc. Natl. Acad. Sci. USA 98 (2001), 14541–14546.
14. de Bruijn, M.F., Speck, N.A., Peeters, M.C., Dzierzak, E., Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. EMBO J. 19 (2000), 2465–2474.
15. Dzierzak, E., Speck, N.A., Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat. Immunol. 9 (2008), 129–136.
16. Epelman, S., Lavine, K.J., Beaudin, A.E., Sojka, D.K., Carrero, J.A., Calderon, B., Brija, T., Gautier, E.L., Ivanov, S., Satpathy, A.T., et al. Embryonic and adult-derived resident cardiac macrophages are maintained through distinct mechanisms at steady state and during inflammation. Immunity 40 (2014), 91–104.
17. Forsberg, E.C., Serwold, T., Kogan, S., Weissman, I.L., Passegué, E., New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell 126 (2006), 415–426.
18. Gapin, L., Matsuda, J.L., Surh, C.D., Kronenberg, M., NKT cells derive from double-positive thymocytes that are positively selected by CD1d. Nat. Immunol. 2 (2001), 971–978.
19. Ghosn, E.E., Yamamoto, R., Hamanaka, S., Yang, Y., Herzenberg, L.A., Nakauchi, H., Herzenberg, L.A., Distinct B-cell lineage commitment distinguishes adult bone marrow hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 109 (2012), 5394–5398.
20. Ghosn, E.E., Waters, J., Phillips, M., Yamamoto, R., Long, B.R., Yang, Y., Gerstein, R., Stoddart, C.A., Nakauchi, H., Herzenberg, L.A., Fetal hematopoietic stem cell transplantation fails to fully regenerate the B-lymphocyte compartment. Stem Cell Reports 6 (2016), 137–149.
21. Gomez Perdiguero, E., Klapproth, K., Schulz, C., Busch, K., Azzoni, E., Crozet, L., Garner, H., Trouillet, C., de Bruijn, M.F., Geissmann, F., Rodewald, H.R., Tissue-resident macrophages originate from yolk-sac-derived erythro-myeloid progenitors. Nature 518 (2015), 547–551.
22. Göthert, J.R., Gustin, S.E., Hall, M.A., Green, A.R., Göttgens, B., Izon, D.J., Begley, C.G., In vivo fate-tracing studies using the Scl stem cell enhancer: embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood 105 (2005), 2724–2732.
23. Hardy, R.R., Hayakawa, K., A developmental switch in B lymphopoiesis. Proc. Natl. Acad. Sci. USA 88 (1991), 11550–11554.
24. Hashimoto, D., Chow, A., Noizat, C., Teo, P., Beasley, M.B., Leboeuf, M., Becker, C.D., See, P., Price, J., Lucas, D., et al. Tissue-resident macrophages self-maintain locally throughout adult life with minimal contribution from circulating monocytes. Immunity 38 (2013), 792–804.
25. Havran, W.L., Allison, J.P., Developmentally ordered appearance of thymocytes expressing different T-cell antigen receptors. Nature 335 (1988), 443–445.
26. Hayashi, S., Abdulmalik, O., Peranteau, W.H., Ashizuka, S., Campagnoli, C., Chen, Q., Horiuchi, K., Asakura, T., Flake, A.W., Mixed chimerism following in utero hematopoietic stem cell transplantation in murine models of hemoglobinopathy. Exp. Hematol. 31 (2003), 176–184.
27. Herzenberg, L.A., Herzenberg, L.A., Toward a layered immune system. Cell 59 (1989), 953–954.
28. 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. C-Myb(+) erythro-myeloid progenitor-derived fetal monocytes give rise to adult tissue-resident macrophages. Immunity 42 (2015), 665–678.
29. Ikuta, K., Kina, T., MacNeil, I., Uchida, N., Peault, B., Chien, Y.H., Weissman, I.L., A developmental switch in thymic lymphocyte maturation potential occurs at the level of hematopoietic stem cells. Cell 62 (1990), 863–874.
30. Kim, I., He, S., Yilmaz, O.H., Kiel, M.J., Morrison, S.J., Enhanced purification of fetal liver hematopoietic stem cells using SLAM family receptors. Blood 108 (2006), 737–744.
31. Lemischka, I.R., Raulet, D.H., Mulligan, R.C., Developmental potential and dynamic behavior of hematopoietic stem cells. Cell 45 (1986), 917–927.
32. Matsuoka, S., Ebihara, Y., Xu, M., Ishii, T., Sugiyama, D., Yoshino, H., Ueda, T., Manabe, A., Tanaka, R., Ikeda, Y., et al. CD34 expression on long-term repopulating hematopoietic stem cells changes during developmental stages. Blood 97 (2001), 419–425.
33. McGrath, K.E., Palis, J., Hematopoiesis in the yolk sac: more than meets the eye. Exp. Hematol. 33 (2005), 1021–1028.
34. Medvinsky, A., Dzierzak, E., Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86 (1996), 897–906.
35. Mold, J.E., Venkatasubrahmanyam, S., Burt, T.D., Michaëlsson, J., Rivera, J.M., Galkina, S.A., Weinberg, K., Stoddart, C.A., McCune, J.M., Fetal and adult hematopoietic stem cells give rise to distinct T cell lineages in humans. Science 330 (2010), 1695–1699.
36. Montecino-Rodriguez, E., Dorshkind, K., B-1 B cell development in the fetus and adult. Immunity 36 (2012), 13–21.
37. Morita, Y., Ema, H., Nakauchi, H., Heterogeneity and hierarchy within the most primitive hematopoietic stem cell compartment. J. Exp. Med. 207 (2010), 1173–1182.
38. Morrison, S.J., Hemmati, H.D., Wandycz, A.M., Weissman, I.L., The purification and characterization of fetal liver hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 92 (1995), 10302–10306.
39. Nijagal, A., Le, T., Wegorzewska, M., Mackenzie, T.C., A mouse model of in utero transplantation. J. Vis. Exp.(47), 2011, 2303.
40. North, T.E., de Bruijn, M.F., Stacy, T., Talebian, L., Lind, E., Robin, C., Binder, M., Dzierzak, E., Speck, N.A., Runx1 expression marks long-term repopulating hematopoietic stem cells in the midgestation mouse embryo. Immunity 16 (2002), 661–672.
41. Perez-Cunningham, J., Boyer, S.W., Landon, M., Forsberg, E.C., Hematopoietic stem cell-specific GFP-expressing transgenic mice generated by genetic excision of a pan-hematopoietic reporter gene. Exp. Hematol. 44 (2016), 755–764.
42. Samokhvalov, I.M., Samokhvalova, N.I., Nishikawa, S., Cell tracing shows the contribution of the yolk sac to adult haematopoiesis. Nature 446 (2007), 1056–1061.
43. Sankaran, V.G., Xu, J., Orkin, S.H., Advances in the understanding of haemoglobin switching. Br. J. Haematol. 149 (2010), 181–194.
44. Smith-Berdan, S., Nguyen, A., Hassanein, D., Zimmer, M., Ugarte, F., Ciriza, J., Li, D., García-Ojeda, M.E., Hinck, L., Forsberg, E.C., Robo4 cooperates with CXCR4 to specify hematopoietic stem cell localization to bone marrow niches. Cell Stem Cell 8 (2011), 72–83.
45. Smith-Berdan, S., Nguyen, A., Hong, M.A., Forsberg, E.C., ROBO4-mediated vascular integrity regulates the directionality of hematopoietic stem cell trafficking. Stem Cell Reports 4 (2015), 255–268.
46. Ugarte, F., Sousae, R., Cinquin, B., Martin, E.W., Krietsch, J., Sanchez, G., Inman, M., Tsang, H., Warr, M., Passegué, E., et al. Progressive chromatin condensation and H3K9 methylation regulate the differentiation of embryonic and hematopoietic stem cells. Stem Cell Reports 5 (2015), 728–740.