Skip to main content
SpringerLink
Log in

Historical Roots

  • Chapter
  • First Online:
Biology of Stem Cells and the Molecular Basis of the Stem State

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

  • 1093 Accesses

Abstract

The monograph is aimed at re-assessing stem cell notions and eventually, suggesting an alternative view of stemness. The history of discovery of the prototypic stem cells, the hemopoietic stem cells (HSCs), is described. This provides a first, basic definition of stemness: HSCs are rare cells, capable of giving rise to all mature blood cells, but not to cell types of other tissues and organs, and are capable of migration and engraftment following transplantation. HSC maintenance and quiescence strictly depend upon their residence in specific bone marrow niches. Within these niches HSCs seem to be capable of asymmetric cell divisions and self-renewal, while maintaining their multipotency, i.e. ability to differentiate into a variety of mature hemopoietic cell lineages. The first stage of differentiation entails the generation of committed progenitors. These cells are extensively proliferating but only in a transient manner until they differentiate terminally.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Jacobson, L.O., Marks, E.K., Gaston, E.O., Robson, M. & Zirkle, R.E. (1949) The role of the spleen in radiation injury. Proc Soc Exp Biol Med, 70, 740–742.

    PubMed  CAS  Google Scholar 

  • Jacobson, L.O., Marks, E.K. & Gaston, E.O. (1955) Observations on the Effect of Spleen Shielding and the Injection of Cell Suspensions on Survival Following Irradiation. Butterworths, London.

    Google Scholar 

  • McCulloch, E.A. & Till, J.E. (1960) The radiation sensitivity of normal mouse bone marrow cells, determined by quantitative marrow transplantation into irradiated mice. Radiat Res, 13, 115–125.

    PubMed  CAS  Google Scholar 

  • Till, J.E. & McCulloch, E.A. (1961) A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat Res, 14, 213–222.

    PubMed  CAS  Google Scholar 

  • Goldwasser, E., White, W.F. & Taylor, K.B. (1962) Further purification of sheep plasma erythropoietin. Biochim Biophys Acta, 64, 487–496.

    PubMed  CAS  Google Scholar 

  • Becker, A.J., Mc, C.E. & Till, J.E. (1963) Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature, 197, 452–454.

    PubMed  CAS  Google Scholar 

  • Siminovitch, L., McCulloch, E.A. & Till, J.E. (1963) The distribution of colony-forming cells among spleen colonies. J Cell Physiol, 62, 327–336.

    PubMed  CAS  Google Scholar 

  • McCulloch, E.A., Siminovitch, L. & Till, J.E. (1964) Spleen-colony formation in anemic mice of genotype Ww. Science, 144, 844–846.

    PubMed  CAS  Google Scholar 

  • Pluznik, D.H. & Sachs, L. (1965) The cloning of normal “mast” cells in tissue culture. J Cell Physiol, 66, 319–324.

    PubMed  CAS  Google Scholar 

  • Weiss, L. (1965) The structure of the bone marrow: Functional interrelationships of vascular and hematopoietic compartments in experimental hemolytic anemia: an electorn microscope study. J Morph, 117, 467–538.

    PubMed  CAS  Google Scholar 

  • Bradley, T.R. & Metcalf, D. (1966) The growth of mouse bone marrow cells in vitro. Aust J Exp Biol Med Sci, 44, 287–299.

    PubMed  CAS  Google Scholar 

  • Micklem, H.S., Ford, C.E., Evans, E.P. & Gray, J. (1966) Interrelationships of myeloid and lymphoid cells: studies with chromosome-marked cells transfused into lethally irradiated mice. Proc R Soc Lond B Biol Sci, 165, 78–102.

    PubMed  CAS  Google Scholar 

  • Pluznik, D.H. & Sachs, L. (1966) The induction of clones of normal mast cells by a substance from conditioned medium. Exp Cell Res, 43, 553–563.

    PubMed  CAS  Google Scholar 

  • Van Bekkum, D.W. & De Vries, M.J. (1967) Radiation Chimaeras. Logos Press Academic Press, London.

    Google Scholar 

  • Bradley, T.R. & Sumner, M.A. (1968) Stimulation of mouse bone marrow colony growth in vitro by conditioned medium. Aust J Exp Biol Med Sci, 46, 607–618.

    PubMed  CAS  Google Scholar 

  • Wu, A.M., Till, J.E., Siminovitch, L. & McCulloch, E.A. (1968) Cytological evidence for a relationship between normal hemotopoietic colony-forming cells and cells of the lymphoid system. J Exp Med, 127, 455–464.

    PubMed  CAS  Google Scholar 

  • Dicke, K.A., Tridente, G. & van Bekkum, D.W. (1969) The selective elimination of immunologically competent cells from bone marrow and lymphocyte cell mixtures. 3. In vitro test for detection of immunocompetent cells in fractionated mouse spleen cell suspensions and primate bone marrow suspensions. Transplantation, 8, 422–434.

    PubMed  CAS  Google Scholar 

  • Miller, R.G. & Phillips, R.A. (1969) Separation of cells by velocity sedimentation. J Cell Physiol, 73, 191–201.

    PubMed  CAS  Google Scholar 

  • Friedenstein, A.J., Chailakhjan, R.K. & Lalykina, K.S. (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet, 3, 393–403.

    PubMed  CAS  Google Scholar 

  • Gordon, A.S. (1970) Regulation of Hematopoiesis. Appleton-Century-Crofts, New York.

    Google Scholar 

  • McCulloch, E.A. (1970) Control of Hematopoiesis at the cellular level. In: Regulation of Hematopoiesis (ed. by Gordon, A.S.), Vol. 1, pp. 133–159. Appleton-Century-Crofts, New York.

    Google Scholar 

  • Moore, M.A. & Metcalf, D. (1970) Ontogeny of the haemopoietic system: yolk sac origin of in vivo and in vitro colony forming cells in the developing mouse embryo. Br J Haematol, 18, 279–296.

    PubMed  CAS  Google Scholar 

  • Sachs, L. (1970) In-vitro control of growth and development of hematopoietic cell clones. In: Regulation of Hematopoiesis (ed. by Gordon, A.S.), Vol. 1, pp. 217–233. Appleton-Century-Crofts, New York.

    Google Scholar 

  • Trentin, J.J. (1970) Influence of hematopoietic organ stroma (hemopoietic inductive microenvironment) on stem cell differentiation. In: Regulation of Hemopoiesis (ed. by Gordon, A.S.), Vol. 1, pp. 161–186. Appleton-Century-Crofts, New York.

    Google Scholar 

  • Metcalf, D. & Moore, M.A.S. (1971) Haemopoietic Cells. North-Holland Publishing Compary, Amsterdam, London.

    Google Scholar 

  • Friedenstein, A.J., Chailakhyan, R.K., Latsinik, N.V., Panasyuk, A.F. & Keiliss-Borok, I.V. (1974a) Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues. Cloning in vitro and retransplantation in vivo. Transplantation, 17, 331–340.

    PubMed  CAS  Google Scholar 

  • Friedenstein, A.J., Deriglasova, U.F., Kulagina, N.N., Panasuk, A.F., Rudakowa, S.F., Luria, E.A. & Ruadkow, I.A. (1974b) Precursors for fibroblasts in different populations of hematopoietic cells as detected by the in vitro colony assay method. Exp Hematol, 2, 83–92.

    PubMed  CAS  Google Scholar 

  • Dieterlen-Lievre, F. (1975) On the origin of haemopoietic stem cells in the avian embryo: an experimental approach. J Embryol Exp Morphol, 33, 607–619.

    PubMed  CAS  Google Scholar 

  • Gregory, C.J., McCulloch, E.A. & Till, J.E. (1975) The cellular basis for the defect in haemopoiesis in flexed-tailed mice. III. Restriction of the defect to erythropoietic progenitors capable of transient colony formation in vivo. Br J Haematol, 30, 401–410.

    PubMed  CAS  Google Scholar 

  • Lord, B.I., Testa, N.G. & Hendry, J.H. (1975) The relative spatial distributions of CFUs and CFUc in the normal mouse femur. Blood, 46, 65–72.

    PubMed  CAS  Google Scholar 

  • Rozenszajn, L.A., Shoham, D. & Kalechman, I. (1975) Clonal proliferation of PHA-stimulated human lymphocytes in soft agar culture. Immunology, 29, 1041–1055.

    PubMed  CAS  Google Scholar 

  • Sredni, B., Kalechman, Y., Michlin, H. & Rozenszajn, L.A. (1976) Development of colonies in vitro of mitogen-stimulated mouse T lymphocytes. Nature, 259, 130–132.

    PubMed  CAS  Google Scholar 

  • Abramson, S., Miller, R.G. & Phillips, R.A. (1977) The identification in adult bone marrow of pluripotent and restricted stem cells of the myeloid and lymphoid systems. J Exp Med, 145, 1567–1579.

    PubMed  CAS  Google Scholar 

  • Dexter, T.M., Allen, T.D. & Lajtha, L.G. (1977) Conditions controlling the proliferation of haemopoietic stem cells in vitro. J Cell Physiol, 91, 335–344.

    PubMed  CAS  Google Scholar 

  • Schofield, R. (1978) The relationship between the spleen colony-forming cell and the haemopoietic stem cell. Blood Cells, 4, 7–25.

    PubMed  CAS  Google Scholar 

  • Botnick, L.E., Hannon, E.C. & Hellman, S. (1979) Nature of the hemopoietic stem cell compartment and its proliferative potential. Blood Cells, 5, 195–210.

    PubMed  CAS  Google Scholar 

  • Fauser, A.A. & Messner, H.A. (1979) Proliferative state of human pluripotent hemopoietic progenitors (CFU-GEMM) in normal individuals and under regenerative conditions after bone marrow transplantation. Blood, 54, 1197–1200.

    PubMed  CAS  Google Scholar 

  • Nicola, N.A., Metcalf, D., Johnson, G.R. & Burgess, A.W. (1979) Separation of functionally distinct human granulocyte-macrophage colony-stimulating factors. Blood, 54, 614–627.

    PubMed  CAS  Google Scholar 

  • Harrison, D.E. (1980) Competitive repopulation: a new assay for long-term stem cell functional capacity. Blood, 55, 77–81.

    PubMed  CAS  Google Scholar 

  • Zipori, D. & Sasson, T. (1980) Adherent cells from mouse bone marrow inhibit the formation of colony stimulating factor (CSF) induced myeloid colonies. Exp Hematol, 8, 816–817.

    PubMed  CAS  Google Scholar 

  • Stanley, E.R. & Guilbert, L.J. (1981) Methods for the purification, assay, characterization and target cell binding of a colony stimulating factor (CSF-1). J Immunol Methods, 42, 253–284.

    PubMed  CAS  Google Scholar 

  • Zipori, D. (1981) Cell interactions in the bone marrow microenvironment: role of endogenous colony-stimulating activity. J Supramol Struct Cell Biochem, 17, 347–357.

    PubMed  CAS  Google Scholar 

  • Zipori, D. & Sasson, T. (1981) Myelopoiesis in the presence of stromal cells from mouse bone marrow: II. Mechanism of glucose dependent colony formation. Exp Hematol, 9, 663–674.

    PubMed  CAS  Google Scholar 

  • Zipori, D., Sasson, T. & Frenkel, A. (1981) Myelopoiesis in the presence of stromal cells from mouse bone marrow: I. Monosaccharides regulate colony formation. Exp Hematol, 9, 656–663.

    PubMed  CAS  Google Scholar 

  • Allen, T.D. & Dexter, T.M. (1982) Ultrastructural aspects of erythropoietic differentiation in long-term bone marrow culture. Differentiation, 21, 86–94.

    PubMed  CAS  Google Scholar 

  • Jenkinson, E.J., Franchi, L.L., Kingston, R. & Owen, J.J. (1982) Effect of deoxyguanosine on lymphopoiesis in the developing thymus rudiment in vitro: application in the production of chimeric thymus rudiments. Eur J Immunol, 12, 583–587.

    PubMed  CAS  Google Scholar 

  • Magli, M.C., Iscove, N.N. & Odartchenko, N. (1982) Transient nature of early haematopoietic spleen colonies. Nature, 295, 527–529.

    PubMed  CAS  Google Scholar 

  • Whitlock, C.A. & Witte, O.N. (1982) Long-term culture of B lymphocytes and their precursors from murine bone marrow. Proc Natl Acad Sci U S A, 79, 3608–3612.

    PubMed  CAS  Google Scholar 

  • Baines, P. & Visser, J.W. (1983) Analysis and separation of murine bone marrow stem cells by H33342 fluorescence-activated cell sorting. Exp Hematol, 11, 701–708.

    PubMed  CAS  Google Scholar 

  • Smith, L.J., Curtis, J.E., Messner, H.A., Senn, J.S., Furthmayr, H. & McCulloch, E.A. (1983) Lineage infidelity in acute leukemia. Blood, 61, 1138–1145.

    PubMed  CAS  Google Scholar 

  • Suda, T., Suda, J. & Ogawa, M. (1983) Proliferative kinetics and differentiation of murine blast cell colonies in culture: evidence for variable G0 periods and constant doubling rates of early pluripotent hemopoietic progenitors. J Cell Physiol, 117, 308–318.

    PubMed  CAS  Google Scholar 

  • Lambertsen, R.H. & Weiss, L. (1984) A model of intramedullary hematopoietic microenvironments based on stereologic study of the distribution of endocloned marrow colonies. Blood, 63, 287–297.

    PubMed  CAS  Google Scholar 

  • Bertoncello, I., Hodgson, G.S. & Bradley, T.R. (1985) Multiparameter analysis of transplantable hemopoietic stem cells: I. The separation and enrichment of stem cells homing to marrow and spleen on the basis of rhodamine-123 fluorescence. Exp Hematol, 13, 999–1006.

    PubMed  CAS  Google Scholar 

  • Dick, J.E., Magli, M.C., Huszar, D., Phillips, R.A. & Bernstein, A. (1985) Introduction of a selectable gene into primitive stem cells capable of long-term reconstitution of the hemopoietic system of W/Wv mice. Cell, 42, 71–79.

    PubMed  CAS  Google Scholar 

  • Hirokawa, K., Sado, T., Kubo, S., Kamisaku, H., Hitomi, K. & Utsuyama, M. (1985) Intrathymic T cell differentiation in radiation bone marrow chimeras and its role in T cell emigration to the spleen. An immunohistochemical study. J Immunol, 134, 3615–3624.

    PubMed  CAS  Google Scholar 

  • Keller, G., Paige, C., Gilboa, E. & Wagner, E.F. (1985) Expression of a foreign gene in myeloid and lymphoid cells derived from multipotent haematopoietic precursors. Nature, 318, 149–154.

    PubMed  CAS  Google Scholar 

  • Greaves, M.F., Chan, L.C., Furley, A.J., Watt, S.M. & Molgaard, H.V. (1986) Lineage promiscuity in hemopoietic differentiation and leukemia. Blood, 67, 1–11.

    PubMed  CAS  Google Scholar 

  • Lemischka, I.R., Raulet, D.H. & Mulligan, R.C. (1986) Developmental potential and dynamic behavior of hematopoietic stem cells. Cell, 45, 917–927.

    PubMed  CAS  Google Scholar 

  • Zipori, D., Tamir, M., Toledo, J. & Oren, T. (1986) Differentiation stage and lineage-specific inhibitor from the stroma of mouse bone marrow that restricts lymphoma cell growth. Proc Natl Acad Sci U S A, 83, 4547–4551.

    PubMed  CAS  Google Scholar 

  • Lang, R.A., Metcalf, D., Cuthbertson, R.A., Lyons, I., Stanley, E., Kelso, A., Kannourakis, G., Williamson, D.J., Klintworth, G.K., Gonda, T.J. & et al. (1987) Transgenic mice expressing a hemopoietic growth factor gene (GM-CSF) develop accumulations of macrophages, blindness, and a fatal syndrome of tissue damage. Cell, 51, 675–686.

    PubMed  CAS  Google Scholar 

  • Mulder, A.H. & Visser, J.W. (1987) Separation and functional analysis of bone marrow cells separated by rhodamine-123 fluorescence. Exp Hematol, 15, 99–104.

    PubMed  CAS  Google Scholar 

  • Whitlock, C.A., Tidmarsh, G.F., Muller-Sieburg, C. & Weissman, I.L. (1987) Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasia-associated molecule. Cell, 48, 1009–1021.

    PubMed  CAS  Google Scholar 

  • Williams, D.E., Straneva, J.E., Shen, R.N. & Broxmeyer, H.E. (1987) Purification of murine bone-marrow-derived granulocyte-macrophage colony-forming cells. Exp Hematol, 15, 243–250.

    PubMed  CAS  Google Scholar 

  • Berenson, R.J., Andrews, R.G., Bensinger, W.I., Kalamasz, D., Knitter, G., Buckner, C.D. & Bernstein, I.D. (1988) Antigen CD34+ marrow cells engraft lethally irradiated baboons. J Clin Invest, 81, 951–955.

    PubMed  CAS  Google Scholar 

  • Ploemacher, R.E. & Brons, N.H. (1988) Cells with marrow and spleen repopulating ability and forming spleen colonies on day 16, 12, and 8 are sequentially ordered on the basis of increasing rhodamine 123 retention. J Cell Physiol, 136, 531–536.

    PubMed  CAS  Google Scholar 

  • Spangrude, G.J., Heimfeld, S. & Weissman, I.L. (1988) Purification and characterization of mouse hematopoietic stem cells. Science, 241, 58–62.

    PubMed  CAS  Google Scholar 

  • Capel, B., Hawley, R., Covarrubias, L., Hawley, T. & Mintz, B. (1989) Clonal contributions of small numbers of retrovirally marked hematopoietic stem cells engrafted in unirradiated neonatal W/Wv mice. Proc Natl Acad Sci U S A, 86, 4564–4568.

    PubMed  CAS  Google Scholar 

  • Jones, R.J., Celano, P., Sharkis, S.J. & Sensenbrenner, L.L. (1989) Two phases of engraftment established by serial bone marrow transplantation in mice. Blood, 73, 397–401.

    PubMed  CAS  Google Scholar 

  • Tamir, M., Harris, N., Trainin, N., Toledo, J. & Zipori, D. (1989) Multilineage hemopoiesis induced by cloned stromal cells. Int J Cell Cloning, 7, 373–384.

    PubMed  CAS  Google Scholar 

  • Jones, R.J., Wagner, J.E., Celano, P., Zicha, M.S. & Sharkis, S.J. (1990) Separation of pluripotent haematopoietic stem cells from spleen colony-forming cells. Nature, 347, 188–189.

    PubMed  CAS  Google Scholar 

  • Jordan, C.T., McKearn, J.P. & Lemischka, I.R. (1990) Cellular and developmental properties of fetal hematopoietic stem cells. Cell, 61, 953–963.

    PubMed  CAS  Google Scholar 

  • McAlister, I., Wolf, N.S., Pietrzyk, M.E., Rabinovitch, P.S., Priestley, G. & Jaeger, B. (1990) Transplantation of hematopoietic stem cells obtained by a combined dye method fractionation of murine bone marrow. Blood, 75, 1240–1246.

    PubMed  CAS  Google Scholar 

  • Tamir, M., Eren, R., Globerson, A., Kedar, E., Epstein, E., Trainin, N. & Zipori, D. (1990) Selective accumulation of lymphocyte precursor cells mediated by stromal cells of hemopoietic origin. Exp Hematol, 18, 322–340.

    PubMed  CAS  Google Scholar 

  • Zipori, D. (1990a) Regulation of hemopoiesis by cytokines that restrict options for growth and differentiation. Cancer Cells, 2, 205–211.

    PubMed  CAS  Google Scholar 

  • Zipori, D. (1990b) Role of stromal cell factors (restrictins) in microorganization of hemopoietic tissues. Prog Clin Biol Res, 352, 115–122.

    PubMed  CAS  Google Scholar 

  • Ogawa, M., Matsuzaki, Y., Nishikawa, S., Hayashi, S., Kunisada, T., Sudo, T., Kina, T. & Nakauchi, H. (1991) Expression and function of c-kit in hemopoietic progenitor cells. J Exp Med, 174, 63–71.

    PubMed  CAS  Google Scholar 

  • Testa, N.G. & Dexter, T.M. (1991) The biology of long-term bone marrow cultures and its application to bone marrow transplantation. Curr Opin Oncol, 3, 272–278.

    PubMed  CAS  Google Scholar 

  • Briddell, R.A., Broudy, V.C., Bruno, E., Brandt, J.E., Srour, E.F. & Hoffman, R. (1992) Further phenotypic characterization and isolation of human hematopoietic progenitor cells using a monoclonal antibody to the c-kit receptor. Blood, 79, 3159–3167.

    PubMed  CAS  Google Scholar 

  • Ikuta, K. & Weissman, I.L. (1992) Evidence that hematopoietic stem cells express mouse c-kit but do not depend on steel factor for their generation. Proc Natl Acad Sci U S A, 89, 1502–1506.

    PubMed  CAS  Google Scholar 

  • Jacobsen, S.E., Ruscetti, F.W., Dubois, C.M., Wine, J. & Keller, J.R. (1992) Induction of colony-stimulating factor receptor expression on hematopoietic progenitor cells: proposed mechanism for growth factor synergism. Blood, 80, 678–687.

    PubMed  CAS  Google Scholar 

  • Okada, S., Nakauchi, H., Nagayoshi, K., Nishikawa, S., Miura, Y. & Suda, T. (1992) In vivo and in vitro stem cell function of c-kit- and Sca-1-positive murine hematopoietic cells. Blood, 80, 3044–3050.

    PubMed  CAS  Google Scholar 

  • Uchida, N. & Weissman, I.L. (1992) Searching for hematopoietic stem cells: evidence that Thy-1.1lo Lin- Sca-1+ cells are the only stem cells in C57BL/Ka-Thy-1.1 bone marrow. J Exp Med, 175, 175–184.

    PubMed  CAS  Google Scholar 

  • Zipori, D. (1992) The renewal and differentiation of hemopoietic stem cells. Faseb J, 6, 2691–2697.

    PubMed  CAS  Google Scholar 

  • Brosh, N., Sternberg, D., Honigwachs-Sha’anani, J., Lee, B.C., Shav-Tal, Y., Tzehoval, E., Shulman, L.M., Toledo, J., Hacham, Y., Carmi, P. & et al. (1995) The plasmacytoma growth inhibitor restrictin-P is an antagonist of interleukin 6 and interleukin 11. Identification as a stroma-derived activin A. J Biol Chem, 270, 29594–29600.

    PubMed  CAS  Google Scholar 

  • Sternberg, D., Honigwachs-sha’anani, J., Brosh, N., Malik, Z., Burstein, Y. & Zipori, D. (1995) Restrictin-P/stromal activin A, kills its target cells via an apoptotic mechanism. Growth Factors, 12, 277–287.

    PubMed  CAS  Google Scholar 

  • Civin, C.I., Trischmann, T., Kadan, N.S., Davis, J., Noga, S., Cohen, K., Duffy, B., Groenewegen, I., Wiley, J., Law, P., Hardwick, A., Oldham, F. & Gee, A. (1996) Highly purified CD34-positive cells reconstitute hematopoiesis. J Clin Oncol, 14, 2224–2233.

    PubMed  CAS  Google Scholar 

  • Goodell, M.A., Brose, K., Paradis, G., Conner, A.S. & Mulligan, R.C. (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med, 183, 1797–1806.

    PubMed  CAS  Google Scholar 

  • Leemhuis, T., Yoder, M.C., Grigsby, S., Aguero, B., Eder, P. & Srour, E.F. (1996) Isolation of primitive human bone marrow hematopoietic progenitor cells using Hoechst 33342 and Rhodamine 123. Exp Hematol, 24, 1215–1224.

    PubMed  CAS  Google Scholar 

  • Medvinsky, A. & Dzierzak, E. (1996) Definitive hematopoiesis is autonomously initiated by the AGM region. Cell, 86, 897–906.

    PubMed  CAS  Google Scholar 

  • Osawa, M., Hanada, K., Hamada, H. & Nakauchi, H. (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science, 273, 242–245.

    PubMed  CAS  Google Scholar 

  • Sternberg, D., Peled, A., Shezen, E., Abramsky, O., Jiang, W., Bertolero, F. & Zipori, D. (1996) Control of stroma-dependent hematopoiesis by basic fibroblast growth factor: stromal phenotypic plasticity and modified myelopoietic functions. Cytokines Mol Ther, 2, 29–38.

    PubMed  CAS  Google Scholar 

  • Cashman, J.D., Lapidot, T., Wang, J.C., Doedens, M., Shultz, L.D., Lansdorp, P., Dick, J.E. & Eaves, C.J. (1997) Kinetic evidence of the regeneration of multilineage hematopoiesis from primitive cells in normal human bone marrow transplanted into immunodeficient mice. Blood, 89, 4307–4316.

    PubMed  CAS  Google Scholar 

  • Christianson, S.W., Greiner, D.L., Hesselton, R.A., Leif, J.H., Wagar, E.J., Schweitzer, I.B., Rajan, T.V., Gott, B., Roopenian, D.C. & Shultz, L.D. (1997) Enhanced human CD4+ T cell engraftment in beta2-microglobulin-deficient NOD-scid mice. J Immunol, 158, 3578–3586.

    PubMed  CAS  Google Scholar 

  • Habibian, H.K., Peters, S.O., Hsieh, C.C., Wuu, J., Vergilis, K., Grimaldi, C.I., Reilly, J., Carlson, J.E., Frimberger, A.E., Stewart, F.M. & Quesenberry, P.J. (1998) The fluctuating phenotype of the lymphohematopoietic stem cell with cell cycle transit. J Exp Med, 188, 393–398.

    PubMed  CAS  Google Scholar 

  • Rachamim, N., Gan, J., Segall, H., Krauthgamer, R., Marcus, H., Berrebi, A., Martelli, M. & Reisner, Y. (1998) Tolerance induction by “megadose” hematopoietic transplants: donor-type human CD34 stem cells induce potent specific reduction of host anti-donor cytotoxic T lymphocyte precursors in mixed lymphocyte culture. Transplantation, 65, 1386–1393.

    PubMed  CAS  Google Scholar 

  • Persons, D.A., Allay, J.A., Allay, E.R., Ashmun, R.A., Orlic, D., Jane, S.M., Cunningham, J.M. & Nienhuis, A.W. (1999) Enforced expression of the GATA-2 transcription factor blocks normal hematopoiesis. Blood, 93, 488–499.

    PubMed  CAS  Google Scholar 

  • Ziegler, B.L., Valtieri, M., Porada, G.A., De Maria, R., Muller, R., Masella, B., Gabbianelli, M., Casella, I., Pelosi, E., Bock, T., Zanjani, E.D. & Peschle, C. (1999) KDR receptor: a key marker defining hematopoietic stem cells. Science, 285, 1553–1558.

    PubMed  CAS  Google Scholar 

  • de Bruijn, M.F., Speck, N.A., Peeters, M.C. & Dzierzak, E. (2000) Definitive hematopoietic stem cells first develop within the major arterial regions of the mouse embryo. Embo J, 19, 2465–2474.

    PubMed  Google Scholar 

  • Rosu-Myles, M., Gallacher, L., Murdoch, B., Hess, D.A., Keeney, M., Kelvin, D., Dale, L., Ferguson, S.S., Wu, D., Fellows, F. & Bhatia, M. (2000) The human hematopoietic stem cell compartment is heterogeneous for CXCR4 expression. Proc Natl Acad Sci U S A, 97, 14626–14631.

    PubMed  CAS  Google Scholar 

  • Shoham, T., Sternberg, D., Brosh, N., Krupsky, M., Barda-Saad, M. & Zipori, D. (2001) The promotion of plasmacytoma tumor growth by mesenchymal stroma is antagonized by basic fibroblast growth factor induced activin A. Leukemia, 15, 1102–1110.

    PubMed  CAS  Google Scholar 

  • Zipori, D. & Barda-Saad, M. (2001) Role of activin A in negative regulation of normal and tumor B lymphocytes. J Leukoc Biol, 69, 867–873.

    PubMed  CAS  Google Scholar 

  • Chen, C.Z., Li, M., de Graaf, D., Monti, S., Gottgens, B., Sanchez, M.J., Lander, E.S., Golub, T.R., Green, A.R. & Lodish, H.F. (2002) Identification of endoglin as a functional marker that defines long-term repopulating hematopoietic stem cells. Proc Natl Acad Sci U S A, 99, 15468–15473.

    PubMed  CAS  Google Scholar 

  • Ito, M., Hiramatsu, H., Kobayashi, K., Suzue, K., Kawahata, M., Hioki, K., Ueyama, Y., Koyanagi, Y., Sugamura, K., Tsuji, K., Heike, T. & Nakahata, T. (2002) NOD/SCID/gamma(c)(null) mouse: an excellent recipient mouse model for engraftment of human cells. Blood, 100, 3175–3182.

    PubMed  CAS  Google Scholar 

  • Lancrin, C., Schneider, E., Lambolez, F., Arcangeli, M.L., Garcia-Cordier, C., Rocha, B. & Ezine, S. (2002) Major T cell progenitor activity in bone marrow-derived spleen colonies. J Exp Med, 195, 919–929.

    PubMed  CAS  Google Scholar 

  • Goolsby, J., Marty, M.C., Heletz, D., Chiappelli, J., Tashko, G., Yarnell, D., Fishman, P.S., Dhib-Jalbut, S., Bever, C.T., Jr., Pessac, B. & Trisler, D. (2003) Hematopoietic progenitors express neural genes. Proc Natl Acad Sci U S A, 100, 14926–14931. Epub 12003 Nov 14921.

    PubMed  CAS  Google Scholar 

  • Horn, P.A., Thomasson, B.M., Wood, B.L., Andrews, R.G., Morris, J.C. & Kiem, H.P. (2003) Distinct hematopoietic stem/progenitor cell populations are responsible for repopulating NOD/SCID mice compared with nonhuman primates. Blood, 102, 4329–4335.

    PubMed  CAS  Google Scholar 

  • Lambert, J.F., Liu, M., Colvin, G.A., Dooner, M., McAuliffe, C.I., Becker, P.S., Forget, B.G., Weissman, S.M. & Quesenberry, P.J. (2003) Marrow stem cells shift gene expression and engraftment phenotype with cell cycle transit. J Exp Med, 197, 1563–1572.

    PubMed  CAS  Google Scholar 

  • Mazurier, F., Doedens, M., Gan, O.I. & Dick, J.E. (2003) Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med, 9, 959–963.

    PubMed  CAS  Google Scholar 

  • Wang, X., Rosol, M., Ge, S., Peterson, D., McNamara, G., Pollack, H., Kohn, D.B., Nelson, M.D. & Crooks, G.M. (2003) Dynamic tracking of human hematopoietic stem cell engraftment using in vivo bioluminescence imaging. Blood, 102, 3478–3482.

    PubMed  CAS  Google Scholar 

  • Yahata, T., Ando, K., Sato, T., Miyatake, H., Nakamura, Y., Muguruma, Y., Kato, S. & Hotta, T. (2003) A highly sensitive strategy for SCID-repopulating cell assay by direct injection of primitive human hematopoietic cells into NOD/SCID mice bone marrow. Blood, 101, 2905–2913.

    PubMed  CAS  Google Scholar 

  • Colvin, G.A., Lambert, J.F., Moore, B.E., Carlson, J.E., Dooner, M.S., Abedi, M., Cerny, J. & Quesenberry, P.J. (2004) Intrinsic hematopoietic stem cell/progenitor plasticity: Inversions. J Cell Physiol, 199, 20–31.

    PubMed  CAS  Google Scholar 

  • Jamieson, C.H., Ailles, L.E., Dylla, S.J., Muijtjens, M., Jones, C., Zehnder, J.L., Gotlib, J., Li, K., Manz, M.G., Keating, A., Sawyers, C.L. & Weissman, I.L. (2004) Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N Engl J Med, 351, 657–667.

    PubMed  CAS  Google Scholar 

  • Matsuzaki, Y., Kinjo, K., Mulligan, R.C. & Okano, H. (2004) Unexpectedly efficient homing capacity of purified murine hematopoietic stem cells. Immunity, 20, 87–93.

    PubMed  CAS  Google Scholar 

  • Muller-Sieburg, C.E., Cho, R.H., Karlsson, L., Huang, J.F. & Sieburg, H.B. (2004) Myeloid-biased hematopoietic stem cells have extensive self-renewal capacity but generate diminished lymphoid progeny with impaired IL-7 responsiveness. Blood, 19, 19.

    Google Scholar 

  • Gekas, C., Dieterlen-Lievre, F., Orkin, S.H. & Mikkola, H.K. (2005) The placenta is a niche for hematopoietic stem cells. Dev Cell, 8, 365–375.

    PubMed  CAS  Google Scholar 

  • Gothert, J.R., Gustin, S.E., Hall, M.A., Green, A.R., Gottgens, B., Izon, D.J. & Begley, C.G. (2005) In vivo fate-tracing studies using the Scl stem cell enhancer: embryonic hematopoietic stem cells significantly contribute to adult hematopoiesis. Blood, 105, 2724–2732.

    PubMed  Google Scholar 

  • Mikkola, H.K., Gekas, C., Orkin, S.H. & Dieterlen-Lievre, F. (2005) Placenta as a site for hematopoietic stem cell development. Exp Hematol, 33, 1048–1054.

    PubMed  CAS  Google Scholar 

  • Ottersbach, K. & Dzierzak, E. (2005) The murine placenta contains hematopoietic stem cells within the vascular labyrinth region. Dev Cell, 8, 377–387.

    PubMed  CAS  Google Scholar 

  • Taussig, D.C., Pearce, D.J., Simpson, C., Rohatiner, A.Z., Lister, T.A., Kelly, G., Luongo, J.L., Danet-Desnoyers, G.A. & Bonnet, D. (2005) Hematopoietic stem cells express multiple myeloid markers: implications for the origin and targeted therapy of acute myeloid leukemia. Blood, 106, 4086–4092.

    PubMed  CAS  Google Scholar 

  • Bajenoff, M., Egen, J.G., Koo, L.Y., Laugier, J.P., Brau, F., Glaichenhaus, N. & Germain, R.N. (2006) Stromal cell networks regulate lymphocyte entry, migration, and territoriality in lymph nodes. Immunity, 25, 989–1001.

    PubMed  CAS  Google Scholar 

  • Balazs, A.B., Fabian, A.J., Esmon, C.T. & Mulligan, R.C. (2006) Endothelial protein C receptor (CD201) explicitly identifies hematopoietic stem cells in murine bone marrow. Blood, 107, 2317–2321.

    PubMed  CAS  Google Scholar 

  • Giebel, B., Zhang, T., Beckmann, J., Spanholtz, J., Wernet, P., Ho, A.D. & Punzel, M. (2006) Primitive human hematopoietic cells give rise to differentially specified daughter cells upon their initial cell division. Blood, 107, 2146–2152.

    PubMed  CAS  Google Scholar 

  • Kirkland, M.A., Quesenberry, P.J. & Roeder, I. (2006) Discrete stem cells: subsets or a continuum? Blood, 108, 3949; author reply 3950.

    PubMed  CAS  Google Scholar 

  • Lai, A.Y. & Kondo, M. (2006) Asymmetrical lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. J Exp Med, 203, 1867–1873.

    PubMed  CAS  Google Scholar 

  • Laslo, P., Spooner, C.J., Warmflash, A., Lancki, D.W., Lee, H.J., Sciammas, R., Gantner, B.N., Dinner, A.R. & Singh, H. (2006) Multilineage transcriptional priming and determination of alternate hematopoietic cell fates. Cell, 126, 755–766.

    PubMed  CAS  Google Scholar 

  • McKenzie, J.L., Gan, O.I., Doedens, M., Wang, J.C. & Dick, J.E. (2006) Individual stem cells with highly variable proliferation and self-renewal properties comprise the human hematopoietic stem cell compartment. Nat Immunol, 7, 1225–1233.

    PubMed  CAS  Google Scholar 

  • Nagasawa, T. (2006) Microenvironmental niches in the bone marrow required for B-cell development. Nat Rev Immunol, 6, 107–116.

    PubMed  CAS  Google Scholar 

  • Ramos, C.A., Bowman, T.A., Boles, N.C., Merchant, A.A., Zheng, Y., Parra, I., Fuqua, S.A., Shaw, C.A. & Goodell, M.A. (2006) Evidence for diversity in transcriptional profiles of single hematopoietic stem cells. PLoS Genet, 2, e159.

    PubMed  Google Scholar 

  • Beckmann, J., Scheitza, S., Wernet, P., Fischer, J.C. & Giebel, B. (2007) Asymmetric cell division within the human hematopoietic stem and progenitor cell compartment: identification of asymmetrically segregating proteins. Blood, 109, 5494–5501.

    PubMed  CAS  Google Scholar 

  • Colvin, G.A., Dooner, M.S., Dooner, G.J., Sanchez-Guijo, F.M., Demers, D.A., Abedi, M., Ramanathan, M., Chung, S., Pascual, S. & Quesenberry, P.J. (2007) Stem cell continuum: directed differentiation hotspots. Exp Hematol, 35, 96–107.

    PubMed  CAS  Google Scholar 

  • Horn, P.A. & Blasczyk, R. (2007) Severe combined immunodeficiency-repopulating cell assay may overestimate long-term repopulation ability. Stem Cells, 25, 3271–3272.

    PubMed  Google Scholar 

  • Iwasaki, H. & Akashi, K. (2007) Myeloid lineage commitment from the hematopoietic stem cell. Immunity, 26, 726–740.

    PubMed  CAS  Google Scholar 

  • Kiel, M.J., He, S., Ashkenazi, R., Gentry, S.N., Teta, M., Kushner, J.A., Jackson, T.L. & Morrison, S.J. (2007) Haematopoietic stem cells do not asymmetrically segregate chromosomes or retain BrdU. Nature, 449, 238–242.

    PubMed  CAS  Google Scholar 

  • Mansson, R., Hultquist, A., Luc, S., Yang, L., Anderson, K., Kharazi, S., Al-Hashmi, S., Liuba, K., Thoren, L., Adolfsson, J., Buza-Vidas, N., Qian, H., Soneji, S., Enver, T., Sigvardsson, M. & Jacobsen, S.E. (2007) Molecular evidence for hierarchical transcriptional lineage priming in fetal and adult stem cells and multipotent progenitors. Immunity, 26, 407–419.

    PubMed  Google Scholar 

  • Dzierzak, E. & Speck, N.A. (2008) Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol, 9, 129–136.

    PubMed  CAS  Google Scholar 

  • Ichii, M., Oritani, K., Yokota, T., Nishida, M., Takahashi, I., Shirogane, T., Ezoe, S., Saitoh, N., Tanigawa, R., Kincade, P.W. & Kanakura, Y. (2008) Regulation of human B lymphopoiesis by the transforming growth factor-beta superfamily in a newly established coculture system using human mesenchymal stem cells as a supportive microenvironment. Exp Hematol, 36, 587–597.

    PubMed  CAS  Google Scholar 

  • Orkin, S.H. & Zon, L.I. (2008) Hematopoiesis: an evolving paradigm for stem cell biology. Cell, 132, 631–644.

    PubMed  CAS  Google Scholar 

  • Shi, M., Adachi, Y., Shigematsu, A., Koike-Kiriyama, N., Feng, W., Yanai, S., Yunze, C., Lian, Z.X., Li, J. & Ikehara, S. (2008) Intra-bone marrow injection of donor bone marrow cells suspended in collagen gel retains injected cells in bone marrow, resulting in rapid hemopoietic recovery in mice. Stem Cells, 26, 2211–2216.

    PubMed  Google Scholar 

  • Sugano, Y., Takeuchi, M., Hirata, A., Matsushita, H., Kitamura, T., Tanaka, M. & Miyajima, A. (2008) Junctional adhesion molecule-A, JAM-A, is a novel cell-surface marker for long-term repopulating hematopoietic stem cells. Blood, 111, 1167–1172.

    PubMed  CAS  Google Scholar 

  • Weissman, I.L. & Shizuru, J.A. (2008) The origins of the identification and isolation of hematopoietic stem cells, and their capability to induce donor-specific transplantation tolerance and treat autoimmune diseases. Blood, 112, 3543–3553.

    PubMed  CAS  Google Scholar 

  • Zhang, C.C. & Lodish, H.F. (2008) Cytokines regulating hematopoietic stem cell function. Curr Opin Hematol, 15, 307–311.

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Dept. Molecular Cell Biology, Weizmann Institute of Science, 76 100, Rehovot, Israel

    Dr Dov Zipori

Authors
  1. Dr Dov Zipori
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dov Zipori .

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Humana Press, a part of Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Zipori, D. (2009). Historical Roots. In: Biology of Stem Cells and the Molecular Basis of the Stem State. Stem Cell Biology and Regenerative Medicine. Humana Press. https://doi.org/10.1007/978-1-60761-130-1_1

Download citation

Publish with us

Policies and ethics

Search

Navigation