Functional differences between transplantable human hematopoietic stem cells from fetal liver, cord blood, and adult marrow

Experimental Hematology

Volumn 27, Issue 9, 1999, Pages 1418-1427

  Holyoake, Tessa L ^a   Nicolini, Franck E ^a   Eaves, Connie J ^a  

^a BRITISH COLUMBIA CANCER AGENCY   (Canada)

Author keywords

Human competitive repopulating unit; LTC IC; NOD SCID mice; Ontogeny; Self renewal

Indexed keywords

CD15 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CD45 ANTIGEN; CD71 ANTIGEN;

ANIMAL CELL; ARTICLE; BONE MARROW; CONTROLLED STUDY; FETUS; FETUS LIVER; FLOW CYTOMETRY; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; IMMUNOPHENOTYPING; MOUSE; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; UMBILICAL CORD BLOOD;

ADULT; ANIMALS; BLOOD CELLS; BONE MARROW EXAMINATION; BONE MARROW TRANSPLANTATION; CELL COUNT; COLONY-FORMING UNITS ASSAY; FETAL BLOOD; FLOW CYTOMETRY; GRAFT SURVIVAL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HEMATOPOIETIC STEM CELLS; HUMANS; INFANT, NEWBORN; LIVER; MICE; MICE, INBRED NOD; MICE, SCID; ORGAN SPECIFICITY; RADIATION CHIMERA; TRANSPLANTATION, HETEROLOGOUS;

ANIMALIA;

EID: 0032875612     PISSN: 0301472X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0301-472X(99)00078-8     Document Type: Article

References (44)

1. Zanjani E.D., Flake A.W., Rice H., Hedrick M., Tavassoli M. Long-term repopulating ability of xenogeneic transplanted human fetal liver hematopoietic stem cells in sheep. J Clin Invest. 93:1994;1051.
2. Zanjani E.D., Pallavicini M.G., Ascensao J.L., Flake A.W., Langlois R.G., Reitsma M., MacKintosh F.R., Stutes D., Harrison M.R., Tavassoli M. Engraftment and long-term expression of human fetal hemopoietic stem cells in sheep following transplantation in utero. J Clin Invest. 89:1992;1178.
3. Kamel-Reid S., Dick J.E. Engraftment of immune-deficient mice with human hematopoietic stem cells. Science. 242:1988;1706.
4. Lapidot T., Pflumio F., Doedens M., Murdoch B., Williams D.E., Dick J.E. Cytokine stimulation of multilineage hematopoiesis from immature human cells engrafted in SCID mice. Science. 255:1992;1137.
5. Pflumio F., Izac B., Katz A., Shultz L.D., Vainchenker W., Coulombel L. Phenotype and function of human hematopoietic cells engrafting immune-deficient CB17-severe combined immunodeficiency mice and nonobese diabetic-severe combined immunodeficiency mice after transplantation of human cord blood mononuclear cells. Blood. 88:1996;3731.
6. Cashman J.D., Lapidot T., Wang J.C.Y., Doedens M., Shultz L.D., Lansdorp P., Dick J.E., Eaves C.J. Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice. Blood. 89:1997;4307.
7. Larochelle A., Vormoor J., Hanenberg H., Wang J.C.Y., Bhatia M., Lapidot T., Moritz T., Murdoch B., Xiao X.L., Kato I., Williams D.A., Dick J.E. Identification of primitive human hematopoietic cells capable of repopulating NOD/SCID mouse bone marrow. implications for gene therapy Nature Med. 2:1996;1329.
8. Cashman J., Bockhold K., Hogge D.E., Eaves A.C., Eaves C.J. Sustained proliferation, multi-lineage differentiation and maintenance of primitive human haematopoietic cells in NOD/SCID mice transplanted with human cord blood. Br J Haematol. 98:1997;1026.
9. Conneally E., Cashman J., Petzer A., Eaves C. Expansion in vitro of transplantable human cord blood stem cells demonstrated using a quantitative assay of their lympho-myeloid repopulating activity in nonobese diabetic-scid/scid mice. Proc Natl Acad Sci U S A. 94:1997;9836.
10. Szilvassy S.J., Humphries R.K., Lansdorp P.M., Eaves A.C., Eaves C.J. Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulation strategy. Proc Natl Acad Sci U S A. 87:1990;8736.
11. Miller C.L., Eaves C.J. Expansion in vitro of adult murine hematopoietic stem cells with transplantable lympho-myeloid reconstituting ability. Proc Natl Acad Sci U S A. 94:1997;13648.
12. Bhatia M., Wang J.C.Y., Kapp U., Bonnet D., Dick J.E. Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A. 94:1997;5320.
13. +-enriched cells from umbilical cord blood in NOD/LtSz-scid/scid mice. Blood. 90:1997;85.
14. + human hematopoietic progenitor cells. Exp Hematol. 24:1996;875.
15. Unkeless J.C. Characterization of a monoclonal antibody directed against mouse macrophage and lymphocyte Fc receptors. J Exp Med. 150:1979;580.
16. Schmitt C., Eaves C.J., Lansdorp P.M. Expression of CD34 on human B cell precursors. Clin Exp Immunol. 85:1991;168.
17. Hogge D., Fanning S., Bockhold K., Petzer A., Lambie K., Lansdorp P., Eaves A., Eaves C. Quantitation and characterization of human megakaryocyte colony-forming cells using a standardized serum-free agarose assay. Br J Haematol. 96:1997;790.
18. Holyoake T.L., Cameron G., Horrocks C., Thomas T., Eaves C., Eaves A. Development of immunomagnetic negative depletion procedures for obtaining enriched populations of primitive cells from CML blood samples or their progeny regenerated in NOD/SCID mice. Exp Hematol. 26:1998;757. (abstr).
19. Hogge D.E., Lansdorp P.M., Reid D., Gerhard B., Eaves C.J. Enhanced detection, maintenance and differentiation of primitive human hematopoietic cells in cultures containing murine fibroblasts engineered to produce human Steel factor, interleukin-3 and granulocyte colony-stimulating factor. Blood. 88:1996;3765.
20. Nicolini FE, Holyoake TL, Cashman JD, Chu PPY, Lambie K, Eaves CJ. Unique differentiation programs of human fetal liver stem cells revealed both in vitro and in vivo in NOD/SCID mice. Blood (in press).
21. Boggs D.R. The total marrow mass of the mouse. a simplified method of measurement Am J Hematol. 16:1984;277.
22. Cashman J.D., Eaves C.J. Human growth factor-enhanced regeneration of transplantable human hematopoietic stem cells in nonobese diabetic/severe combined immunodeficient mice. Blood. 93:1999;481.
23. Vormoor J., Lapidot T., Pflumio F., Risdon G., Patterson B., Broxmeyer H.E., Dick J.E. Immature human cord blood progenitors engraft and proliferate to high levels in severe combined immunodeficient mice. Blood. 83:1994;2489.
24. Xu M., Tsuji K., Ueda T., Mukouyama Y., Hara T., Yang F.-C., Ebihara Y., Matsuoka S., Manabe A., Kikuchi A., Ito M., Miyajima A., Nakahata T. Stimulation of mouse and human primitive hematopoiesis by murine embryonic aorta-gonad-mesonephros-derived stromal cell lines. Blood. 92:1998;2032.
25. Baum C.M., Weissman I.L., Tsukamoto A.S., Buckle A.M., Péault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A. 89:1992;2804.
26. Sutherland H.J., Eaves C.J., Lansdorp P.M., Thacker J.D., Hogge D.E. Differential regulation of primitive human hematopoietic cells in long-term cultures maintained on genetically engineered murine stromal cells. Blood. 78:1991;666.
27. ++/CD38 progenitor cells in long-term cultures and semisolid assays. Blood. 81:1993;2916.
28. +CD38 progenitors to maintain primitive function and immunophenotype in vitro. Exp Hematol. 26:1998;612.
29. Martin F.H., Suggs S.V., Langley K.E., Lu H.S., Ting J., Okino K.H., Morris C.F., McNiece I.K., Jacobsen F.W., Mendiaz E.A., Birkett N.C., Smith K.A.et al. Primary structure and functional expression of rat and human stem cell factor DNAs. Cell. 63:1990;203.
30. Lyman S.D., James L., Vanden Bos T., de Vries P., Brasel K., Gliniak B., Hollingsworth L.T., Picha K.S., McKenna H.J., Splett R.R., Fletcher F.A., Maraskovsky E.et al. Molecular cloning of a ligand for the flt3/flk-2 tyrosine kinase receptor. a proliferative factor for primitive hematopoietic cells Cell. 75:1993;1157.
31. Wendling F., Maraskovsky E., Debili N., Florindo C., Teepe M., Titeux M., Methia N., Breton-Gorius J., Cosman D., Vainchenker W. c-Mpl ligand is a humoral regulator of megakaryocytopoiesis. Nature. 369:1994;571.
32. Jordan C.T., Lemischka I.R. Clonal and systemic analysis of long-term hematopoiesis in the mouse. Genes Dev. 4:1990;220.
33. Civin C.I., Almeida-Porada G., Lee M., Olweus J., Terstappen L.W.M.M., Zanjani E.D. Sustained, retransplantable, multilineage engraftment of highly purified adult human bone marrow stem cells in vivo. Blood. 88:1996;4102.
34. Prosper F., Stroncek D., Verfaillie C.M. Phenotypic and functional characterization of long-term culture-initiating cells present in peripheral blood progenitor collections of normal donors treated with granulocyte colony-stimulating factor. Blood. 88:1996;2033.
35. Hao Q.L., Thiemann F.T., Petersen D., Smogorzewska E.M., Crooks G.M. Extended long-term culture reveals a highly quiescent and primitive human hematopoietic progentior population. Blood. 88:1996;3306.
36. Rich I.N., Kubanek B. Erythroid colony formation (CFU-e) in fetal liver and adult bone marrow and spleen from the mouse. Blut. 33:1976;171.
37. Peschle C., Migliaccio A.R., Migliaccio G., Ciccariello R., Lettieri F., Quattrin S., Russo G., Mastroberardino G. Identification and characterization of three classes of erythroid progenitors in human fetal liver. Blood. 58:1981;565.
38. + human hematopoietic progenitors from fetal liver, cord blood, and adult bone marrow respond differently to hematopoietic cytokines depending on the ontogenic source. Exp Hematol. 26:1998;1034.
39. Micklem H.S., Ford C.E., Evans E.P., Ogden D.A., Papworth D.S. Competitive in vivo proliferation of foetal and adult haematopoietic cells in lethally irradiated mice. J Cell Physiol. 79:1972;293.
40. 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 adult bone marrow counterparts. Blood. 87:1996;3500.
41. Brenner M.K., Rill D.R., Holladay M.S., Heslop H.E., Moen R.C., Buschle M., Krance R.A., Santana V.M., Anderson W.F., Ihle J.N. Gene marking to determine whether autologous marrow infusion restores long-term haemopoiesis in cancer patients. Lancet. 342:1993;1134.
42. Cashman J.D., Clark-Lewis I., Eaves A., Eaves C.J. Differentiation stage-specific regulation of primitive human hematopoietic progenitor cycling by exogenous and endogenous inhibitors in an in vivo model. Blood. in press:1998.
43. Sauvageau G., Thorsteinsdottir U., Eaves C.J., Lawrence H.J., Largman C., Lansdorp P.M., Humphries R.K. Overexpression of HOXB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev. 9:1995;1753.
44. 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.