T-cell potential and development in vitro: the OP9-DL1 approach

Current Opinion in Immunology

Volumn 19, Issue 2, 2007, Pages 163-168

  de Pooter, Renée ^a   Zúñiga Pflücker, Juan Carlos ^a  

^a Sunnybrook Health Sciences Centre   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; B LYMPHOCYTE; BONE MARROW CELL; CELL COMPARTMENTALIZATION; CELL SURVIVAL; DENDRITIC CELL; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMUS;

ANIMALS; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; LYMPHOPOIESIS; T-LYMPHOCYTES; THYMUS GLAND;

EID: 33847656103     PISSN: 09527915     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.coi.2007.02.011     Document Type: Review

References (62)

1. Hare K.J., Jenkinson E.J., and Anderson G. In vitro models of T cell development. Semin Immunol 11 (1999) 3-12
2. Jenkinson E.J., Franchi L.L., Kingston R., and Owen J.J. Effect of deoxyguanosine on lymphopoiesis in the developing thymus rudiment in vitro: application in the production of chimeric thymus rudiments. Eur J Immunol 12 (1982) 583-587
3. Anderson G., Jenkinson E.J., Moore N.C., and Owen J.J. MHC class II-positive epithelium and mesenchyme cells are both required for T-cell development in the thymus. Nature 362 (1993) 70-73
4. de Pooter R.F., Cho S.K., Carlyle J.R., and Zuniga-Pflucker J.C. In vitro generation of T lymphocytes from embryonic stem cell-derived prehematopoietic progenitors. Blood 102 (2003) 1649-1653
5. Schmitt T.M., and Zuniga-Pflucker J.C. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17 (2002) 749-756
6. Nakano T., Kodama H., and Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science 265 (1994) 1098-1101
7. Cho S.K., Webber T.D., Carlyle J.R., Nakano T., Lewis S.M., and Zuniga-Pflucker J.C. Functional characterization of B lymphocytes generated in vitro from embryonic stem cells. Proc Natl Acad Sci USA 96 (1999) 9797-9802
8. Felli M.P., Maroder M., Mitsiadis T.A., Campese A.F., Bellavia D., Vacca A., Mann R.S., Frati L., Lendahl U., Gulino A., et al. Expression pattern of notch1, 2 and 3 and Jagged1 and 2 in lymphoid and stromal thymus components: distinct ligand-receptor interactions in intrathymic T cell development. Int Immunol 11 (1999) 1017-1025
9. Kaneta M., Osawa M., Sudo K., Nakauchi H., Farr A.G., and Takahama Y. A role for pref-1 and HES-1 in thymocyte development. J Immunol 164 (2000) 256-264
10. Radtke F., Wilson A., and MacDonald H.R. Notch signaling in T- and B-cell development. Curr Opin Immunol 16 (2004) 174-179
11. Schmitt T.M., de Pooter R.F., Gronski M.A., Cho S.K., Ohashi P.S., and Zuniga-Pflucker J.C. Induction of T cell development and establishment of T cell competence from embryonic stem cells differentiated in vitro. Nat Immunol 5 (2004) 410-417
12. de Pooter R.F., Schmitt T.M., de la Pompa J.L., Fujiwara Y., Orkin S.H., and Zuniga-Pflucker J.C. Notch signaling requires GATA-2 to inhibit myelopoiesis from embryonic stem cells and primary hemopoietic progenitors. J Immunol 176 (2006) 5267-5275
13. La Motte-Mohs R.N., Herer E., and Zuniga-Pflucker J.C. Induction of T-cell development from human cord blood hematopoietic stem cells by Delta-like 1 in vitro. Blood 105 (2005) 1431-1439
14. + progenitor cells mature to T cells on OP9-DL1 stromal cell line without thymus microenvironment. Blood Cells Mol Dis 33 (2004) 227-232
15. Lehar S.M., Dooley J., Farr A.G., and Bevan M.J. Notch ligands Delta 1 and Jagged1 transmit distinct signals to T-cell precursors. Blood 105 (2005) 1440-1447
16. Jaleco A.C., Neves H., Hooijberg E., Gameiro P., Clode N., Haury M., Henrique D., and Parreira L. Differential effects of Notch ligands Delta-1 and Jagged-1 in human lymphoid differentiation. J Exp Med 194 (2001) 991-1002
17. Hoflinger S., Kesavan K., Fuxa M., Hutter C., Heavey B., Radtke F., and Busslinger M. Analysis of Notch1 function by in vitro T cell differentiation of Pax5 mutant lymphoid progenitors. J Immunol 173 (2004) 3935-3944
18. + cells, responded to OP9-DL1 cells by adopting a T fate.
19. + lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121 (2005) 295-306. This study rigorously characterized BM progenitors that diverged from the conventional paradigm of CMP versus CLP hematopoietic differentiation as they possessed myeloid and lymphoid but very little detectable erythro-megakaryocyte potential. The OP9/OP9-DL1 was used to examine the lymphoid potential of this population at the single-cell level.
20. Arcangeli M.L., Lancrin C., Lambolez F., Cordier C., Schneider E., Rocha B., and Ezine S. Extrathymic hemopoietic progenitors committed to T cell differentiation in the adult mouse. J Immunol 174 (2005) 1980-1988
21. - hematopoietic progenitor with potent lymphoid and myeloid developmental potential. Eur J Immunol 35 (2005) 2019-2030
22. Terra R., Louis I., Le Blanc R., Ouellet S., Zuniga-Pflucker J.C., and Perreault C. T-cell generation by lymph node resident progenitor cells. Blood 106 (2005) 193-200
23. Yokota T., Huang J., Tavian M., Nagai Y., Hirose J., Zuniga-Pflucker J.C., Peault B., and Kincade P.W. Tracing the first waves of lymphopoiesis in mice. Development 133 (2006) 2041-2051
24. Yoshida T., Ng S.Y., Zuniga-Pflucker J.C., and Georgopoulos K. Early hematopoietic lineage restrictions directed by Ikaros. Nat Immunol 7 (2006) 382-391
25. Benz C., and Bleul C.C. A multipotent precursor in the thymus maps to the branching point of the T versus B lineage decision. J Exp Med 202 (2005) 21-31. This work defined a population that is present in the BM, blood and thymus that expresses a chemokine receptor, which can be detected by a GFP reporter. Cells of this phenotype have T, B and DC potential at the single cell level in the BM and blood, but quickly loose B potential following entry into the thymus.
26. Krueger A., Garbe A.I., and von Boehmer H. Phenotypic plasticity of T cell progenitors upon exposure to Notch ligands. J Exp Med 203 (2006) 1977-1984
27. Porritt H.E., Rumfelt L.L., Tabrizifard S., Schmitt T.M., Zuniga-Pflucker J.C., and Petrie H.T. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20 (2004) 735-745
28. Schmitt T.M., Ciofani M., Petrie H.T., and Zuniga-Pflucker J.C. Maintenance of T cell specification and differentiation requires recurrent notch receptor-ligand interactions. J Exp Med 200 (2004) 469-479
29. + cells in the thymus, but not the blood, required Notch signals to arise.
30. Taghon T.N., David E.S., Zuniga-Pflucker J.C., and Rothenberg E.V. Delayed, asynchronous, and reversible T-lineage specification induced by Notch/Delta signaling. Genes Dev 19 (2005) 965-978
31. Garcia-Peydro M., de Yebenes V.G., and Toribio M.L. Notch1 and IL-7 receptor interplay maintains proliferation of human thymic progenitors while suppressing non-T cell fates. J Immunol 177 (2006) 3711-3720
32. Weerkamp F., Baert M.R., Brugman M.H., Dik W.A., de Haas E.F., Visser T.P., de Groot C.J., Wagemaker G., van Dongen J.J., and Staal F.J. Human thymus contains multipotent progenitors with T/B lymphoid, myeloid, and erythroid lineage potential. Blood 107 (2006) 3131-3137
33. Balciunaite G., Ceredig R., Fehling H.J., Zuniga-Pflucker J.C., and Rolink A.G. The role of Notch and IL-7 signaling in early thymocyte proliferation and differentiation. Eur J Immunol 35 (2005) 1292-1300
34. Huang J., Garrett K.P., Pelayo R., Zuniga-Pflucker J.C., Petrie H.T., and Kincade P.W. Propensity of adult lymphoid progenitors to progress to DN2/3 stage thymocytes with Notch receptor ligation. J Immunol 175 (2005) 4858-4865
35. Kawazu M., Asai T., Ichikawa M., Yamamoto G., Saito T., Goyama S., Mitani K., Miyazono K., Chiba S., Ogawa S., et al. Functional domains of Runx1 are differentially required for CD4 repression, TCRbeta expression, and CD4/8 double-negative to CD4/8 double-positive transition in thymocyte development. J Immunol 174 (2005) 3526-3533
36. El Andaloussi A., Graves S., Meng F., Mandal M., Mashayekhi M., and Aifantis I. Hedgehog signaling controls thymocyte progenitor homeostasis and differentiation in the thymus. Nat Immunol 7 (2006) 418-426
37. Lehar S.M., and Bevan M.J. T cells develop normally in the absence of both Deltex1 and Deltex2. Mol Cell Biol 26 (2006) 7358-7371
38. Visan I., Yuan J.S., Tan J.B., Cretegny K., and Guidos C.J. Regulation of intrathymic T-cell development by Lunatic Fringe-Notch1 interactions. Immunol Rev 209 (2006) 76-94
39. Wang D., Claus C.L., Vaccarelli G., Braunstein M., Schmitt T.M., Zuniga-Pflucker J.C., Rothenberg E.V., and Anderson M.K. The basic helix-loop-helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J Immunol 177 (2006) 109-119
40. Ciofani M., Schmitt T.M., Ciofani A., Michie A.M., Cuburu N., Aublin A., Maryanski J.L., and Zuniga-Pflucker J.C. Obligatory role for cooperative signaling by pre-TCR and Notch during thymocyte differentiation. J Immunol 172 (2004) 5230-5239
41. Mandal M., Borowski C., Palomero T., Ferrando A.A., Oberdoerffer P., Meng F., Ruiz-Vela A., Ciofani M., Zuniga-Pflucker J.C., Screpanti I., et al. The BCL2A1 gene as a pre-T cell receptor-induced regulator of thymocyte survival. J Exp Med 201 (2005) 603-614
42. Ciofani M., and Zuniga-Pflucker J.C. Notch promotes survival of pre-T cells at the beta-selection checkpoint by regulating cellular metabolism. Nat Immunol 6 (2005) 881-888. This study used the OP9-DL1 system to demonstrate that Notch signals are required at the stage of β-selection to maintain the glucose metabolism of successful cells. This was shown to be mediated by maintenance of activation of the Akt pathway.
43. Dose M., Khan I., Guo Z., Kovalovsky D., Krueger A., von Boehmer H., Khazaie K., and Gounari F. c-Myc mediates pre-TCR-induced proliferation but not developmental progression. Blood 108 (2006) 2669-2677
44. Ciofani M., Knowles G.C., Wiest D.L., von Boehmer H., and Zuniga-Pflucker J.C. Stage-specific and differential notch dependency at the alphabeta and γδ T lineage bifurcation. Immunity 25 (2006) 105-116
45. Garbe A.I., Krueger A., Gounari F., Zuniga-Pflucker J.C., and von Boehmer H. Differential synergy of Notch and T cell receptor signaling determines αβ versus γδ lineage fate. J Exp Med 203 (2006) 1579-1590
46. Taghon T., Yui M.A., Pant R., Diamond R.A., and Rothenberg E.V. Developmental and molecular characterization of emerging β- and γδ-selected pre-T cells in the adult mouse thymus. Immunity 24 (2006) 53-64
47. Akashi K., Traver D., Miyamoto T., and Weissman I.L. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature 404 (2000) 193-197
48. Laiosa C.V., Stadtfeld M., and Graf T. Determinants of lymphoid-myeloid lineage diversification. Annu Rev Immunol 24 (2006) 705-738
49. Bhandoola A., and Sambandam A. From stem cell to T cell: one route or many?. Nat Rev Immunol 6 (2006) 117-126
50. Katsura Y. Redefinition of lymphoid progenitors. Nat Rev Immunol 2 (2002) 127-132
51. Kondo M., Weissman I.L., and Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91 (1997) 661-672
52. + lymphoid-restricted bone marrow cells with T precursor potential. Nat Immunol 4 (2003) 866-873
53. Wang H., Pierce L.J., and Spangrude G.J. Lymphoid potential of primitive bone marrow progenitors evaluated in vitro. Ann NY Acad Sci 1044 (2005) 210-219
54. Blom B., and Spits H. Development of human lymphoid cells. Annu Rev Immunol 24 (2006) 287-320
55. Perry S.S., Welner R.S., Kouro T., Kincade P.W., and Sun X.H. Primitive lymphoid progenitors in bone marrow with T lineage reconstituting potential. J Immunol 177 (2006) 2880-2887
56. Zakrzewski J.L., Kochman A.A., Lu S.X., Terwey T.H., Kim T.D., Hubbard V.M., Muriglan S.J., Suh D., Smith O.M., Grubin J., et al. Adoptive transfer of T-cell precursors enhances T-cell reconstitution after allogeneic hematopoietic stem cell transplantation. Nat Med 12 (2006) 1039-1047. The study used DN2/3 cells expanded in OP9-DL1 coculture in a mouse model of hematopoietic stem cell transplantation. In contrast to grafts containing only total bone marrow or HSC alone, those which also contained OP9-DL1-derived DN2/3 cells demonstrated improved T-cell chimerism, thymic cellularity, resistance to Listeria monocytogenes infection and anti-tumor immunity, without inducing graft-versus-host disease.
57. Clark R.A., Yamanaka K., Bai M., Dowgiert R., and Kupper T.S. Human skin cells support thymus-independent T cell development. J Clin Invest 115 (2005) 3239-3249
58. Mohtashami M., and Zuniga-Pflucker J.C. Three-dimensional architecture of the thymus is required to maintain delta-like expression necessary for inducing T cell development. J Immunol 176 (2006) 730-734
59. + cells. Exp Hematol 34 (2006) 1720-1729
60. Heinzel K., Benz C., Martins V.C., Haidl I.D., and Bleul C.C. Bone marrow-derived hemopoietic precursors commit to the T cell lineage only after arrival in the thymic microenvironment. J Immunol 178 (2007) 858-868
61. Krueger A., and von Boehmer H. Identification of a T lineage-committed progenitor in adult blood. Immunity 26 (2007) 105-116
62. Pipkin M.E., Ljutic B., Cruz-Guilloty F., Nouzova M., Rao A., Zuniga-Pflucker J.C., and Lichtenheld M.G. Chromosome transfer activates and delineates a locus control region for perforin. Immunity 26 (2007) 29-41