Differential effects of interleukin-3, interleukin-7, interleukin 15, and granulocyte-macrophage colony-stimulating factor in the generation of natural killer and B cells from primitive human fetal liver progenitors

Experimental Hematology

Volumn 28, Issue 8, 2000, Pages 961-973

  Muench, Marcus O ^a   Humeau, Laurent ^a   Paek, Bettina ^a   Ohkubo, Tatsuo ^a   Lanier, Lewis L ^a   Albanese, Craig T ^a   Bárcena, Alicia ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

B lymphocytes; Hematopoiesis; Natural killer cells; Ontogeny; Stem cells

Indexed keywords

CD16 ANTIGEN; CD19 ANTIGEN; CD2 ANTIGEN; CD20 ANTIGEN; CD3 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CD56 ANTIGEN; CD8 ANTIGEN; CD94 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; FLT3 LIGAND; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HLA DQ ANTIGEN; HLA DR ANTIGEN; IMMUNOGLOBULIN M; INTERLEUKIN 15; INTERLEUKIN 3; INTERLEUKIN 7; STEM CELL FACTOR;

ANTIGEN EXPRESSION; ARTICLE; B LYMPHOCYTE; CELL CULTURE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFECT; FETUS LIVER; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOGLOBULIN PRODUCTION; IMMUNOPHENOTYPING; LYMPHOPOIESIS; NATURAL KILLER CELL; ONTOGENY; PRIORITY JOURNAL; REGULATORY MECHANISM; STEM CELL;

ADP-RIBOSYL CYCLASE; ANTIGENS, CD; ANTIGENS, CD19; ANTIGENS, CD3; ANTIGENS, CD34; ANTIGENS, CD38; ANTIGENS, CD56; ANTIGENS, DIFFERENTIATION; B-LYMPHOCYTES; CELL DIFFERENTIATION; CULTURE MEDIA, SERUM-FREE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HEMATOPOIETIC STEM CELLS; HUMANS; INTERLEUKIN-15; INTERLEUKIN-3; INTERLEUKIN-7; INTERLEUKINS; KILLER CELLS, NATURAL; LIVER; MEMBRANE GLYCOPROTEINS; MEMBRANE PROTEINS; NAD+ NUCLEOSIDASE; PHENOTYPE; STEM CELL FACTOR;

EID: 0033827910     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-472X(00)00490-2     Document Type: Article

References (64)

1. Phillips J.H., Hori T., Nagler A., Bhat N., Spits H., Lanier L.L. Ontogeny of human natural killer (NK) cells. fetal NK cells mediate cytolytic function and express cytoplasmic CD3 epsilon, delta proteins J Exp Med. 175:1992;1055.
2. Thilaganathn B., Abbas A., Nicolaides K.H. Fetal blood natural killer cells in human pregnancy. Fetal Diagn Ther. 8:1993;149.
3. + NK progenitor Blood. 83:1994;2594.
4. Mrozek E., Anderson P., Caligiuri M.A. Role of interleukin-15 in the development of human CD56+ natural killer cells from CD34+ hematopoietic progenitor cells. Blood. 87:1996;2632.
5. Silva M.R.G., Hoffman R., Srour E.F., Ascensao J.A. Generation of human natural killer cells from immature progenitors does not require marrow stromal cells. Blood. 84:1994;841.
6. Cavazzana-Calvo M., Hacein-Bey S., de Saint Basile G., De Coene C., Selz F., Le Deist F., Fischer A. Role of interleukin-2 (IL-2), IL-7, and IL-15 in natural killer cell differentiation from cord blood hematopoietic progenitor cells and from gamma c transduced severe combined immunodeficiency X1 bone marrow cells. Blood. 88:1996;3901.
7. Carayol G., Robin C., Bourhis J.H., Bennaceur-Griscelli A., Chouaib S., Coulombel L., Caignard A. NK cells differentiated from bone marrow, cord blood and peripheral blood stem cells exhibit similar phenotype and functions. Eur J Immunol. 28:1998;1991.
8. Suzuki H., Duncan G.S., Takimoto H., Mak T.W. Abnormal development of intestinal intraepithelial lymphocytes and peripheral natural killer cells in mice lacking the IL-2 receptor beta chain. J Exp Med. 185:1997;499.
9. DiSanto J.P., Muller W., Guy-Grand D., Fischer A., Rajewsky K. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc Natl Acad Sci USA. 92:1995;377.
10. Cao X., Shores E.W., Hu-Li J., Anver M.R., Kelsall B.L., Russell S.M., Drago J., Noguchi M., Grinberg A., Bloom E.T.et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity. 2:1995;223.
11. Williams N.S., Klem J., Puzanov I.J., Sivakumar P.V., Schatzle J.D., Bennett M., Kumar V. Natural killer cell differentiation. insights from knockout and transgenic mouse models and in vitro systems Immunol Rev. 165:1998;47.
12. Punnonen J., Aversa G.G., Vandekerckhove B., Roncarolo M.G., de Vries J.E. Induction of isotype switching and Ig production by CD5+ and CD10+ human fetal B cells. J Immunol. 148:1992;3398.
13. Charbord P., Tavian M., Humeau L., Peault B. Early ontogeny of the human marrow from long bones. an immunohistochemical study of hematopoiesis and its microenvironment Blood. 87:1996;4109.
14. Gathings W.E., Kubagawa H., Cooper M.D. A distinctive pattern of B cell immaturity in perinatal humans. Immunol Rev. 5:1981;107.
15. - progenitor cells from human cord blood generate B lymphocytes and granulocytes. Blood. 89:1997;3554.
16. - cells with both lymphoid and myeloid potential. Blood. 91:1998;4145.
17. - progenitors give rise to natural killer cells, B-cell lineage cells dendritic cells, and myeloid cells. Blood. 93:1999;96.
18. Namikawa R., Muench M.O., de Vries J.E., Roncarolo M.-G. The FLK2/FLT3 ligand synergizes with interleukin-7 in promoting stromal-cell-independent expansion and differentiation of human fetal pro-B cells in vitro. Blood. 87:1996;1881.
19. Muench M.O., Cupp J., Polakoff J., Roncarolo M.G. Characterization of CD33, CD38 and HLA-DR expression on human fetal liver progenitors with a high proliferative potential. Blood. 83:1994;3170.
20. - fetal liver cells. Exp Hematol. 27:1999;1428.
21. Muench M.O., Roncarolo M.G., Menon S., Xu Y., Kastelein R., Zurawski S., Hannum C.H., Culpepper J., Lee F., Namikawa R. FLK-2/FLT-3 ligand (FL) regulates the growth of early myeloid progenitors isolated from human fetal liver. Blood. 85:1995;963.
22. +/++ cells for transplantation. Bone Marrow Transplant. 24:1999;451.
23. Lanier L.L., Chang C., Spits H., Phillips J.H. Expression of cytoplasmic CD3ε proteins in activated human adult killer (NK) cells and CD3γ,δ,ε complexes in fetal NK cells. J Immunol. 149:1992;1876.
24. + human natural killer progenitor that responds to interleukin-15. Blood. 92:1998;3647.
25. Bennett I.M., Zatsepina O., Zamai L., Azzoni L., Mikheeva T., Perussia B. Definition of a natural killer NKR-P1A+/CD56-/CD16- functionally immature human NK cell subset that differentiates in vitro in the presence of interleukin 12. J Exp Med. 184:1996;1845.
26. Lanier L.L., Corliss B., Phillips J.H. Arousal and inhibition of human NK cells. Immunol Rev. 155:1997;145.
27. Soderstrom K., Corliss B., Lanier L.L., Phillips J.H. CD94/NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J Immunol. 159:1997;1072.
28. Steffens U., Vyas Y., Dupont B., Selvakumar A. Nucleotide and aminoacid sequence alignment for human killer cell inhibitory receptors (KIR). Tissue Antigens. 51:1998;398.
29. Lanier L.L. NK cell receptors. Annu Rev Immunol. 16:1998;359.
30. Muench M.O., Roncarolo M.-G., Rosnet O., Birnbaum D., Namikawa R. Colony-forming cells expressing high levels of CD34 are the main targets for granulocyte colony-stimulating factor and macrophage colony-stimulating factor in the human fetal liver. Exp Hematol. 25:1997;27.
31. Miller J.S., Verfaillie C., McGlave P.B. The generation of human natural killer cells from CD34+/DR- primitive progenitors in long-term bone marrow culture. Blood. 80:1992;2182.
32. Dittel B.N., LeBien T.W. The growth response to IL-7 during normal human B cell ontogeny is restricted to B-lineage cells expressing CD34. J Immunol. 154:1995;58.
33. Namikawa R., Muench M.O., Roncarolo M.G. Regulatory roles of the ligand for Flk2/Flt3 tyrosine kinase receptor on human hematopoiesis. Stem Cells (Dayt). 14:1996;388.
34. Loken M.R., Shah V.O., Dattilio K.L., Civin C.I. Flow cytometric analysis of human bone marrow. II. Normal B lymphocyte development. Blood. 70:1987;1316.
35. Pontvert-Delucq S., Breton-Gorious J., Schmitt C., Baillou C., Guichard J., Najman A., Lemoine F.M. Characterization and functional analysis of adult human bone marrow cell subsets in relation to B-lymphoid development. Blood. 82:1993;417.
36. Sato T., Laver J.H., Aiba Y., Ogawa M. NK cell colony formation from human fetal thymocytes. Exp Hematol. 27:1999;726.
37. Res P., Martinez Caceres E., Cristina Jaleco A., Staal F., Noteboom E., Weijer K., Spits H. CD34+CD38dim cells in the human thymus can differentiate into T, natural killer, and dendritic cells but are distinct from pluripotent stem cells. Blood. 87:1996;5196.
38. Collins L.S., Dorshkind K. A stromal cell line from myeloid long-term cultures can support myelopoiesis and B lymphopoiesis. J Immunol. 138:1987;1082.
39. Rawlings D.L., Quan S., Hao Q.-L., Thiemann F.T., Smogorzewska M., Witte O.N., Crooks G.M. Differentiation of human CD34+CD38- cord blood stem cells into B cell progenitors in vitro. Exp Hematol. 25:1997;66.
40. Itoh K., Tezuka H., Sakoda H., Nagata K., Uchiyama T., Uchino H., Mori K.J. Reproducible establishment of hemopoietic supportive stromal cell lines from murine bone marrow. Exp Hematol. 17:1989;145.
41. Moore K.A., Ema H., Lemischka I.H. In vitro maintenance of highly purified, transplantable hematopoietic stem cells. Blood. 89:1997;4337.
42. Kurosaka D., LeBien T.W., Pribyl J.A. Comparative studies of different stromal cell microenvironments in support of human B-cell development. Exp Hematol. 27:1999;1271.
43. Bulfone-Paus S., Ungureanu D., Pohl T., Lindner G., Paus R., Rückert R., Krause H., Kunzendorf U. Itnerleukin-15 protects from lethal apoptosis in vivo. Nature Med. 3:1997;1124.
44. Bárcena A., Park S.W., Banapour B., Muench M.O., Mechetner E.B. Expression of Fas/CD95 and bcl-2 in primitive hematopoietic progenitors in the human fetal liver. Blood. 88:1996;2013.
45. Haynes B.F., Martin M.E., Kay H.H., Kurtzberg J. Early events in human T cell ontogeny. phenotypic characterization and immunohistological localization of T-cell precursors in early human fetal tissues J Exp Med. 168:1988;1061.
46. Shah A.J., Smogorzewska E.M., Hannum C., Crooks G.M. Flt3 ligand induces proliferation of quiescent human bone marrow CD34+CD38- cells and maintains progenitor cells in vitro. Blood. 87:1996;3563.
47. Vadhan-Raj S. PIXY321 (GM-CSF/IL-3 fusion protein). biology and early clinical development Stem Cells (Dayt). 12:1994;253.
48. Hirayama F., Clark S.C., Ogawa M. Negative regulation or early B lymphopoiesis by interleukin-3 and interleukin-1α Proc Natl Acad Sci USA. 91:1994;469.
49. Hirayama F., Ogawa M. Negative regulation or early T lymphopoiesis by interleukin-3 and interleukin-1α Blood. 86:1995;4527.
50. Aiba Y., Ogawa M. Development of natural killer cells, B lymphocytes, macrophages, and mast cells from single hematopoietic progenitors in culture of murine fetal liver cells. Blood. 90:1997;3923.
51. Nagler A., Lanier L.L., Cwirla S., Phillips J.H. Comparative studies of human FcRIII-positive and negative natural killer cells. J Immunol. 143:1989;3183.
52. Handgretinger R., Schafer H.J., Baur F., Frank D., Ottenlinger C., Buhring H.J., Niethammer D. Expression of an early myelopoietic antigen (CD33) on a subset of human umbilical cord blood-derived natural killer cells. Immunol Lett. 37:1993;223.
53. Matos M.E., Schnier G.S., Beecher M.S., Ashman L.K., William D.E., Caligiuri M.A. Expression of a functional c-kit receptor on a subset of natural killer cells. J Exp Med. 178:1993;1079.
54. Chang C., Rodríguez A., Carretero M., López-Botet M., Phillips J.H., Lanier L.L. Molecular characterization of CD94. a type II membrane glycoprotein related to the C-type lectin superfamily Eur J Immunol. 25:1995;2433.
55. Lanier L.L., Chang C., Phillips J.H. Human NKR-P1A. a disulphide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes J Immunol. 153:1994;2417.
56. Jaleco A.C., Blom B., Res P., Weijer K., Lanier L.L., Phillips J.H., Spits H. Fetal liver contains committed NK progenitors, but is not a site for development of CD34+ cells into T cells. J Immunol. 159:1997;694.
57. Mingari M.C., Vitale C., Cantoni C., Bellomo R., Ponte M., Schiavetti F., Bertone S., Moretta A., Moretta L. Interleukin-15-induced maturation of human natural killer cells from early thymic precursors. selective expression of CD94/NKG2-A as the only HLA class I-specific inhibitory receptor Eur J Immunol. 27:1997;1374.
58. Spits H., Blom B., Jaleco A.C., Weijer K., Verschuren M.C., van Dongen J.J., Heemskerk M.H., Res P.C. Early stages in the development of human T, natural killer and thymic dendritic cells. Immunol Rev. 165:1998;75.
59. Hirayama F., Shih J.P., Awgulewitsch A., Warr G.W., Clark S.C., Ogawa M. Clonal proliferation of murine lymphohemopoietic progenitors in culture. Proc Natl Acad Sci USA. 89:1992;5907.
60. Hirayama F., Lyman S.D., Clark S.C., Ogawa M. The flt3 ligand supports proliferation of lymphohematopoietic progenitors and early B-lymphoid progenitors. Blood. 85:1995;1762.
61. Lemieux M.E., Chappel S.M., Miller C.L., Eaves C.J. Differential ability of flt3-ligand, interleukin-11, and Steel factor to support the generation of B cell progenitors and myeloid cells from primitive murine fetal liver cells. Exp Hematol. 25:1997;951.
62. Hunte B.E., Hudak S., Campbell D., Xu Y., Rennick D. flk2/flt3 ligand is a potent cofactor for the growth of primitive B cell progenitors. J Immunol. 156:1996;489.
63. Pribyl J.A., LeBien T.W. Interleukin 7 independent development of human B cells. Proc Natl Acad Sci USA. 93:1996;10348.
64. Galy A., Travis M., Cen D., Chen B. Human T, B, natural killer and dendritic cells arise from a common bone marrow progenitor cell subset. Immunity. 3:1995;459.