Human T-lymphoid progenitors generated in a feeder-cell-free delta-like-4 culture system promote T-cell reconstitution in NOD/SCID/γc-/- mice

Stem Cells

Volumn 30, Issue 8, 2012, Pages 1771-1780

  Reimann, Christian ^a,b,c   Six, Emmanuelle ^a,b   Dal Cortivo, Liliane ^d   Schiavo, Andrea ^a,b   Appourchaux, Kevin ^a,b   Lagresle Peyrou, Chantal ^b,e   De Chappedelaine, Corinne ^a,b   Ternaux, Brigitte ^d   Coulombel, Laure ^f   Beldjord, Kheira ^g   Cavazzana Calvo, Marina ^a,b,d,e   Andre Schmutz, Isabelle ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b IMAGINE INSTITUTE   (France)

^c UNIVERSITY OF FREIBURG   (Germany)

^d HÔPITAL NECKER ENFANTS MALADES   (France)

^e INSERM   (France)

^f Centre National de la Recherche Scientifique   (France)

^g Laboratoire Central d'Hematologie   (France)

Author keywords

DLL4 protein; Hematopoietic stem cell transplantation; Immunotherapy; Notch1; T lymphoid precursor cells

Indexed keywords

CD34 ANTIGEN; DELTA LIKE 4 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; FEEDER CELL; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOPHENOTYPING; LYMPHOCYTE CULTURE; LYMPHOCYTE MIGRATION; LYMPHOCYTE TRANSFER; MOUSE; NONHUMAN; NONOBESE DIABETIC MOUSE; PRE T LYMPHOCYTE; SCID MOUSE;

ANIMALS; CELL DIFFERENTIATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; IMMUNOTHERAPY; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LYMPHOPOIESIS; MICE; MICE, INBRED NOD; MICE, SCID; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

MUS;

EID: 84864326863     PISSN: 10665099     EISSN: None     Source Type: Journal    
DOI: 10.1002/stem.1145     Document Type: Article

References (50)

1. Ruggeri A, Peffault de Latour R, Carmagnat M et al. Outcomes, infections, and immune reconstitution after double cord blood transplantation in patients with high-risk hematological diseases. Transpl Infect Dis 2011;13:456-465.
2. Storek J, Geddes M, Khan F et al. Reconstitution of the immune system after hematopoietic stem cell transplantation in humans. Semin Immunopathol 2008;30:425-437.
3. Komanduri KV, St John LS, de Lima M et al. Delayed immune reconstitution after cord blood transplantation is characterized by impaired thymopoiesis and late memory T-cell skewing. Blood 2007;110:4543-4551. (Pubitemid 351377822)
4. Jacobson CA, Turki AT, McDonough SM et al. Immune Reconstitution after double umbilical cord blood stem cell transplantation: Comparison with unrelated peripheral blood stem cell transplantation. Biol Blood Marrow Transplant 2012;18:565-574.
5. Thomson BG, Robertson KA, Gowan D et al. Analysis of engraftment, graft-versus-host disease, and immune recovery following unrelated donor cord blood transplantation. Blood 2000;96:2703-2711.
6. Parkman R, Weinberg KI. Immunological reconstitution following bone marrow transplantation. Immunol Rev 1997;157:73-78. (Pubitemid 27303122)
7. Zlotoff DA, Zhang SL, De Obaldia ME et al. Delivery of progenitors to the thymus limits T-lineage reconstitution after bone marrow transplantation. Blood 2011;118:1962-1970.
8. Krenger W, Blazar BR, Hollander GA. Thymic T-cell development in allogeneic stem cell transplantation. Blood 2011;117:6768-6776.
9. Pui JC, Allman D, Xu L et al. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 1999;11: 299-308. (Pubitemid 29463238)
10. Yashiro-Ohtani Y, Ohtani T, Pear WS. Notch regulation of early thymocyte development. Semin Immunol 2010;22:261-269.
11. Radtke F, Wilson A, Mancini SJ et al. Notch regulation of lymphocyte development and function. Nat Immunol 2004;5:247-253. (Pubitemid 38332121)
12. Awong G, Herer E, Surh CD et al. Characterization in vitro and engraftment potential in vivo of human progenitor T cells generated from hematopoietic stem cells. Blood 2009;114:972-982.
13. Meek B, Cloosen S, Borsotti C et al. In vitro-differentiated T/natural killer-cell progenitors derived from human CD34+ cells mature in the thymus. Blood 2009;115:261-264.
14. Eyrich M, Schreiber SC, Wollny G et al. Predifferentiated human committed T-lymphoid progenitors promote peripheral T-cell reconstitution after stem cell transplantation in immunodeficient mice. Eur J Immunol 2011;41:3596-3603.
15. Zakrzewski JL, Kochman AA, Lu SX et al. Adoptive transfer of T-cell precursors enhances T-cell reconstitution after allogeneic hematopoietic stem cell transplantation. Nat Med 2006;12:1039-1047. (Pubitemid 44353385)
16. Zakrzewski JL, Suh D, Markley JC et al. Tumor immunotherapy across MHC barriers using allogeneic T-cell precursors. Nat Biotechnol 2008;26:453-461. (Pubitemid 351501816)
17. Ohishi K, Varnum-Finney B, Bernstein ID. Delta-1 enhances marrow and thymus repopulating ability of human CD34(+)CD38(-) cord blood cells. J Clin Invest 2002;110:1165-1174. (Pubitemid 35215897)
18. Delaney C, Heimfeld S, Brashem-Stein C et al. Notch-mediated expansion of human cord blood progenitor cells capable of rapid myeloid reconstitution. Nat Med 2010;16:232-236.
19. Koch U, Fiorini E, Benedito R et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J Exp Med 2008;205:2515-2523.
20. Besseyrias V, Fiorini E, Strobl LJ et al. Hierarchy of Notch-Delta interactions promoting T cell lineage commitment and maturation. J Exp Med 2007;204:331-343. (Pubitemid 46294549)
21. Hozumi K, Mailhos C, Negishi N et al. Delta-like 4 is indispensable in thymic environment specific for T cell development. J Exp Med 2008;205:2507-2513.
22. Lefort N, Benne C, Lelievre JD et al. Short exposure to Notch ligand Delta-4 is sufficient to induce T-cell differentiation program and to increase the T cell potential of primary human CD34+ cells. Exp Hematol 2006;34:1720-1729. (Pubitemid 44839011)
23. Six EM, Bonhomme D, Monteiro M et al. A human postnatal lymphoid progenitor capable of circulating and seeding the thymus. J Exp Med 2007;204:3085-3093.
24. Six EM, Benjelloun F, Garrigue A et al. Cytokines and culture medium have a major impact on human in vitro T-cell differentiation. Blood Cells Mol Dis 2011;47:72-78.
25. van Dongen JJ, Langerak AW, Bruggemann M et al. Design and standardization of PCR primers and protocols for detection of clonal immunoglobulin and T-cell receptor gene recombinations in suspect lymphoproliferations: Report of the BIOMED-2 concerted action BMH4-CT98-3936. Leukemia 2003;17:2257-2317. (Pubitemid 38072572)
26. Pasqual N, Gallagher M, Aude-Garcia C et al. Quantitative and qualitative changes in V-J alpha rearrangements during mouse thymocytes differentiation: Implication for a limited T cell receptor alpha chain repertoire. J Exp Med 2002;196:1163-1173. (Pubitemid 35304183)
27. Haddad R, Guardiola P, Izac B et al. Molecular characterization of early human T/NK and B-lymphoid progenitor cells in umbilical cord blood. Blood 2004;104:3918-3926. (Pubitemid 39620139)
28. Haddad R, Guimiot F, Six E et al. Dynamics of thymus-colonizing cells during human development. Immunity 2006;24:217-230. (Pubitemid 43214590)
29. Hao QL, George AA, Zhu J et al. Human intrathymic lineage commitment is marked by differential CD7 expression: Identification of CD7-lympho-myeloid thymic progenitors. Blood 2008;111:1318-1326. (Pubitemid 351213418)
30. Hao QL, Zhu J, Price MA et al. Identification of a novel, human multilymphoid progenitor in cord blood. Blood 2001;97:3683-3690.
31. Taghon TN, David ES, Zuniga-Pflucker JC et al. Delayed, asynchronous, and reversible T-lineage specification induced by Notch/Delta signaling. Genes Dev 2005;19:965-978. (Pubitemid 40548064)
32. Dik WA, Pike-Overzet K, Weerkamp F et al. New insights on human T cell development by quantitative T cell receptor gene rearrangement studies and gene expression profiling. J Exp Med 2005;201: 1715-1723. (Pubitemid 41002890)
33. La Motte-Mohs RN, Herer E, Zuniga-Pflucker JC. Induction of T-cell development from human cord blood hematopoietic stem cells by Delta-like 1 in vitro. Blood 2005;105:1431-1439. (Pubitemid 40223658)
34. Janas ML, Varano G, Gudmundsson K et al. Thymic development beyond beta-selection requires phosphatidylinositol 3-kinase activation by CXCR4. J Exp Med 2010;207:247-261.
35. Ikawa T, Hirose S, Masuda K et al. An essential developmental checkpoint for production of the T cell lineage. Science 2010;329: 93-96.
36. Li L, Leid M, Rothenberg EV. An early T cell lineage commitment checkpoint dependent on the transcription factor Bcl11b. Science 2010;329:89-93.
37. Garcia-Peydro M, de Yebenes VG, Toribio ML. Notch1 and IL-7 receptor interplay maintains proliferation of human thymic progenitors while suppressing non-T cell fates. J Immunol 2006;177:3711-3720. (Pubitemid 44359903)
38. Gonzalez-Garcia S, Garcia-Peydro M, Martin-Gayo E et al. CSLMAML-dependent Notch1 signaling controls T lineage-specific IL-7R{alpha} gene expression in early human thymopoiesis and leukemia. J Exp Med 2009;206:779-791.
39. Li P, Burke S, Wang J et al. Reprogramming of T cells to natural killer-like cells upon Bcl11b deletion. Science 2010;329:85-89.
40. Janas ML, Turner M. Stromal cell-derived factor 1alpha and CXCR4: Newly defined requirements for efficient thymic beta-selection. Trends Immunol 2010;31:370-376.
41. Aoyama K, Delaney C, Varnum-Finney B et al. The interaction of the Wnt and Notch pathways modulates natural killer versus T cell differentiation. Stem Cells 2007;25:2488-2497. (Pubitemid 47582741)
42. Haraguchi K, Suzuki T, Koyama N et al. Notch activation induces the generation of functional NK cells from human cord blood CD34-positive cells devoid of IL-15. J Immunol 2009;182:6168-6178.
43. Varnum-Finney B, Halasz LM, Sun M et al. Notch2 governs the rate of generation of mouse long- and short-term repopulating stem cells. J Clin Invest 2010;121:1207-1216.
44. Van de Walle I, De Smet G, Gartner M et al. Jagged2 acts as a Delta-like Notch ligand during early hematopoietic cell fate decisions. Blood 2011;117:4449-4459.
45. Mohtashami M, Shah DK, Nakase H et al. Direct comparison of Dll1-and Dll4-mediated Notch activation levels shows differential lymphomyeloid lineage commitment outcomes. J Immunol 2010;185: 867-876.
46. Rucci F, Poliani PL, Caraffi S et al. Abnormalities of thymic stroma may contribute to immune dysregulation in murine models of leaky severe combined immunodeficiency. Front Immunol 2011;2:15.
47. Malacarne F, Benicchi T, Notarangelo LD et al. Reduced thymic output, increased spontaneous apoptosis and oligoclonal B cells in polyethylene glycol-adenosine deaminase-treated patients. Eur J Immunol 2005;35:3376-3386. (Pubitemid 41672541)
48. Hazra R, Mackall C. Thymic function in HIV infection. Curr HIV/AIDS Rep 2005;2:24-28.
49. Tanaskovic S, Fernandez S, French MA et al. Thymic tissue is not evident on high-resolution computed tomography and [(1)F]fluorodeoxy-glucose positron emission tomography scans of aviraemic HIV patients with poor recovery of CD4 T cells. AIDS 2011;25: 1235-1237.
50. Napolitano LA, Schmidt D, Gotway MB et al. Growth hormone enhances thymic function in HIV-1-infected adults. J Clin Invest 2008;118:1085-1098. (Pubitemid 351364616)