Cellular Barcoding Links B-1a B Cell Potential to a Fetal Hematopoietic Stem Cell State at the Single-Cell Level

Immunity

Volumn 45, Issue 2, 2016, Pages 346-357

  Kristiansen, Trine A ^a   Jaensson Gyllenbäck, Elin ^a   Zriwil, Alya ^a   Björklund, Tomas ^b   Daniel, Jeremy A ^c   Sitnicka, Ewa ^a   Soneji, Shamit ^a   Bryder, David ^a   Yuan, Joan ^a  

^a LUND UNIVERSITY   (Sweden)

^b LUND UNIVERSITY   (Sweden)

^c University of Copenhagen   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

RNA BINDING PROTEIN; RNA BINDING PROTEIN LIN28B; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; LIN28B PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; CELL FATE; CELL FUNCTION; CELL LINEAGE; CELL PLASTICITY; CELL SELF-RENEWAL; CONTROLLED STUDY; DNA BARCODING; ECTOPIC EXPRESSION; FEMALE; FETUS; FETUS CELL; FETUS LIVER; GENE EXPRESSION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; ANIMAL; C57BL MOUSE; CELL CLONE; CELL DIFFERENTIATION; GENETICS; IMMUNOPHENOTYPING; LIVER; LYMPHOCYTE SUBPOPULATION; METABOLISM; PHYSIOLOGY; SINGLE CELL ANALYSIS; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; B-LYMPHOCYTES; CELL DIFFERENTIATION; CELL PLASTICITY; CELL SELF RENEWAL; CLONE CELLS; DNA-BINDING PROTEINS; FEMALE; HEMATOPOIESIS; HEMATOPOIETIC STEM CELLS; IMMUNOPHENOTYPING; LIVER; LYMPHOCYTE SUBSETS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; SINGLE-CELL ANALYSIS;

EID: 85002548279     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2016.07.014     Document Type: Article

References (56)

1. Adolfsson, J., Månsson, R., Buza-Vidas, N., Hultquist, A., Liuba, K., Jensen, C.T., Bryder, D., Yang, L., Borge, O.-J., Thoren, L.A.M., et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121 (2005), 295–306.
2. 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.
3. Basu, S., Hodgson, G., Katz, M., Dunn, A.R., Evaluation of role of G-CSF in the production, survival, and release of neutrophils from bone marrow into circulation. Blood 100 (2002), 854–861.
4. Benedict, C.L., Kearney, J.F., Increased junctional diversity in fetal B cells results in a loss of protective anti-phosphorylcholine antibodies in adult mice. Immunity 10 (1999), 607–617.
5. 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.
6. Berland, R., Wortis, H.H., Origins and functions of B-1 cells with notes on the role of CD5. Annu. Rev. Immunol. 20 (2002), 253–300.
7. 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.
8. Briles, D.E., Forman, C., Hudak, S., Claflin, J.L., Anti-phosphorylcholine antibodies of the T15 idiotype are optimally protective against Streptococcus pneumoniae. J. Exp. Med. 156 (1982), 1177–1185.
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. Bystrykh, L.V., Verovskaya, E., Zwart, E., Broekhuis, M., de Haan, G., Counting stem cells: methodological constraints. Nat. Methods 9 (2012), 567–574.
11. Casola, S., Otipoby, K.L., Alimzhanov, M., Humme, S., Uyttersprot, N., Kutok, J.L., Carroll, M.C., Rajewsky, K., B cell receptor signal strength determines B cell fate. Nat. Immunol. 5 (2004), 317–327.
12. Celso, C., Scadden, D., Isolation and transplantation of hematopoietic stem cells (HSCs). J. Vis. Exp., 9, 2007, 157.
13. Copley, M.R., Beer, P.A., Eaves, C.J., Hematopoietic stem cell heterogeneity takes center stage. Cell Stem Cell 10 (2012), 690–697.
14. Copley, M.R., Babovic, S., Benz, C., Knapp, D.J.H.F., Beer, P.A., Kent, D.G., Wohrer, S., Treloar, D.Q., Day, C., Rowe, K., et al. The Lin28b-let-7-Hmga2 axis determines the higher self-renewal potential of fetal haematopoietic stem cells. Nat. Cell Biol. 15 (2013), 916–925.
15. Cumano, A., Paige, C.J., Iscove, N.N., Brady, G., Bipotential precursors of B cells and macrophages in murine fetal liver. Nature 356 (1992), 612–615.
16. Etzrodt, M., Endele, M., Schroeder, T., Quantitative single-cell approaches to stem cell research. Cell Stem Cell 15 (2014), 546–558.
17. Gerlach, C., Rohr, J.C., Perié, L., van Rooij, N., van Heijst, J.W.J., Velds, A., Urbanus, J., Naik, S.H., Jacobs, H., Beltman, J.B., et al. Heterogeneous differentiation patterns of individual CD8+ T cells. Science 340 (2013), 635–639.
18. Gerrits, A., Dykstra, B., Kalmykowa, O.J., Klauke, K., Verovskaya, E., Broekhuis, M.J.C., de Haan, G., Bystrykh, L.V., Cellular barcoding tool for clonal analysis in the hematopoietic system. Blood 115 (2010), 2610–2618.
19. Ghosn, E.E.B., Yang, Y., Hematopoietic stem cell-independent B-1a lineage. Ann. N Y Acad. Sci. 1362 (2015), 23–38.
20. Ghosn, E.E.B., 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.
21. Ghosn, E.E.B., 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.
22. Hardy, R.R., Hayakawa, K., A developmental switch in B lymphopoiesis. Proc. Natl. Acad. Sci. USA 88 (1991), 11550–11554.
23. Haughton, G., Arnold, L.W., Whitmore, A.C., Clarke, S.H., B-1 cells are made, not born. Immunol. Today 14 (1993), 84–87.
24. Hayakawa, K., Hardy, R.R., Herzenberg, L.A., Herzenberg, L.A., Progenitors for Ly-1 B cells are distinct from progenitors for other B cells. J. Exp. Med. 161 (1985), 1554–1568.
25. He, S., Kim, I., Lim, M.S., Morrison, S.J., Sox17 expression confers self-renewal potential and fetal stem cell characteristics upon adult hematopoietic progenitors. Genes Dev. 25 (2011), 1613–1627.
26. Hochedlinger, K., Yamada, Y., Beard, C., Jaenisch, R., Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121 (2005), 465–477.
27. Ikuta, K., Weissman, I.L., The junctional modifications of a T cell receptor gamma chain are determined at the level of thymic precursors. J. Exp. Med. 174 (1991), 1279–1282.
28. Kantor, A.B., Herzenberg, L.A., Origin of murine B cell lineages. Annu. Rev. Immunol. 11 (1993), 501–538.
29. Kantor, A.B., Stall, A.M., Adams, S., Watanabe, K., Herzenberg, L.A., De novo development and self-replenishment of B cells. Int. Immunol. 7 (1995), 55–68.
30. Kikuchi, K., Kondo, M., Developmental switch of mouse hematopoietic stem cells from fetal to adult type occurs in bone marrow after birth. Proc. Natl. Acad. Sci. USA 103 (2006), 17852–17857.
31. Kim, I., Saunders, T.L., Morrison, S.J., Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 130 (2007), 470–483.
32. Kobayashi, M., Shelley, W.C., Seo, W., Vemula, S., Lin, Y., Liu, Y., Kapur, R., Taniuchi, I., Yoshimoto, M., Functional B-1 progenitor cells are present in the hematopoietic stem cell-deficient embryo and depend on Cbfβ for their development. Proc. Natl. Acad. Sci. USA 111 (2014), 12151–12156.
33. Lu, R., Neff, N.F., Quake, S.R., Weissman, I.L., Tracking single hematopoietic stem cells in vivo using high-throughput sequencing in conjunction with viral genetic barcoding. Nat. Biotechnol. 29 (2011), 928–933.
34. Magee, J.A., Ikenoue, T., Nakada, D., Lee, J.Y., Guan, K.-L., Morrison, S.J., Temporal changes in PTEN and mTORC2 regulation of hematopoietic stem cell self-renewal and leukemia suppression. Cell Stem Cell 11 (2012), 415–428.
35. McHeyzer-Williams, L.J., Milpied, P.J., Okitsu, S.L., McHeyzer-Williams, M.G., Class-switched memory B cells remodel BCRs within secondary germinal centers. Nat. Immunol. 16 (2015), 296–305.
36. Merriman, B., Rothberg, J.M., Ion Torrent R&D Team. Progress in ion torrent semiconductor chip based sequencing. Electrophoresis 33 (2012), 3397–3417.
37. Montecino-Rodriguez, E., Dorshkind, K., B-1 B cell development in the fetus and adult. Immunity 36 (2012), 13–21.
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. Naik, S.H., Perié, L., Swart, E., Gerlach, C., van Rooij, N., de Boer, R.J., Schumacher, T.N., Diverse and heritable lineage imprinting of early haematopoietic progenitors. Nature 496 (2013), 229–232.
40. Naik, S.H., Schumacher, T.N., Perié, L., Cellular barcoding: a technical appraisal. Exp. Hematol. 42 (2014), 598–608.
41. Osawa, M., Hanada, K., Hamada, H., Nakauchi, H., Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273 (1996), 242–245.
42. Paul, F., Arkin, Y., Giladi, A., Jaitin, D.A., Kenigsberg, E., Keren-Shaul, H., Winter, D., Lara-Astiaso, D., Gury, M., Weiner, A., et al. Transcriptional heterogeneity and lineage commitment in myeloid progenitors. Cell 163 (2015), 1663–1677.
43. Pawliuk, R., Eaves, C., Humphries, R.K., Evidence of both ontogeny and transplant dose-regulated expansion of hematopoietic stem cells in vivo. Blood 88 (1996), 2852–2858.
44. Pina, C., Fugazza, C., Tipping, A.J., Brown, J., Soneji, S., Teles, J., Peterson, C., Enver, T., Inferring rules of lineage commitment in haematopoiesis. Nat. Cell Biol. 14 (2012), 287–294.
45. Rajewsky, K., The Herzenberg lecture: how to make a B-1 cell?. Ann. N Y Acad. Sci. 1362 (2015), 6–7, 10.1111/nyas.12767.
46. Rebel, V.I., Miller, C.L., Eaves, C.J., Lansdorp, P.M., The repopulation potential of fetal liver hematopoietic stem cells in mice exceeds that of their liver adult bone marrow counterparts. Blood 87 (1996), 3500–3507.
47. Sudo, K., Ema, H., Morita, Y., Nakauchi, H., Age-associated characteristics of murine hematopoietic stem cells. J. Exp. Med. 192 (2000), 1273–1280.
48. Sun, J., Ramos, A., Chapman, B., Johnnidis, J.B., Le, L., Ho, Y.-J., Klein, A., Hofmann, O., Camargo, F.D., Clonal dynamics of native haematopoiesis. Nature 514 (2014), 322–327.
49. Verovskaya, E., Broekhuis, M.J.C., Zwart, E., Ritsema, M., van Os, R., de Haan, G., Bystrykh, L.V., Heterogeneity of young and aged murine hematopoietic stem cells revealed by quantitative clonal analysis using cellular barcoding. Blood 122 (2013), 523–532.
50. Xie, H., Xu, J., Hsu, J.H., Nguyen, M., Fujiwara, Y., Peng, C., Orkin, S.H., Polycomb repressive complex 2 regulates normal hematopoietic stem cell function in a developmental-stage-specific manner. Cell Stem Cell 14 (2014), 68–80.
51. Yoshimoto, M., The first wave of B lymphopoiesis develops independently of stem cells in the murine embryo. Ann. N Y Acad. Sci. 1362 (2015), 16–22.
52. Yoshimoto, M., Montecino-Rodriguez, E., Ferkowicz, M.J., Porayette, P., Shelley, W.C., Conway, S.J., Dorshkind, K., Yoder, M.C., 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 (2011), 1468–1473.
53. Yuan, J., Nguyen, C.K., Liu, X., Kanellopoulou, C., Muljo, S.A., Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Science 335 (2012), 1195–1200.
54. Zhou, Y., Li, Y.S., Bandi, S.R., Tang, L., Shinton, S.A., Hayakawa, K., Hardy, R.R., Lin28b promotes fetal B lymphopoiesis through the transcription factor Arid3a. J. Exp. Med. 212 (2015), 569–580.
55. Zhu, H., Shyh-Chang, N., Segrè, A.V., Shinoda, G., Shah, S.P., Einhorn, W.S., Takeuchi, A., Engreitz, J.M., Hagan, J.P., Kharas, M.G., et al. DIAGRAM Consortium, MAGIC Investigators. The Lin28/let-7 axis regulates glucose metabolism. Cell 147 (2011), 81–94.
56. Zorita, E., Cuscó, P., Filion, G.J., Starcode: sequence clustering based on all-pairs search. Bioinformatics 31 (2015), 1913–1919.