Stem cells: Units of development, units of regeneration, and units in evolution

Cell

Volumn 100, Issue 1, 2000, Pages 157-168

  Weissman, Irving L ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL COUNT; CELL DIFFERENTIATION; CELL FATE; CELL LINEAGE; CELL MATURATION; CELL REGENERATION; EVOLUTION; GERM CELL; HEMATOPOIETIC STEM CELL; NATURAL SELECTION; NERVE CELL; NONHUMAN; ONTOGENY; PRIORITY JOURNAL; REVIEW; STEM CELL;

EID: 0034614576     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81692-X     Document Type: Review

References (110)

1. Akashi, K., Kondo, M., Cheshier, S., Shizuru, J., Gandy, K., Domen, J., Mebius, R., Traver, D., and Weissman, I. (1999). Lymphoid development from stem cells and the common lymphocyte progenitors. Cold Spring Harb. Symp. Quant. Biol., in press.
2. Allsopp, R.C., Chang, E., Kashefi-Aazam, M., Rogaev, E.I., Piatyszek, M.A., Shay, J.W., and Harley, C.B. (1995). Telomere shortening is associated with cell division in vitro and in vivo. Exp. Cell Res. 220, 194-200.
3. Altman, J., and Das, G.D. (1966). Autoradiographic and histological studies of postnatal neurogenesis. I. A longitudinal investigation of the kinetics, migration and transformation of cells incorporating tritiated thymidine in neonate rats, with special reference to postnatal neurogenesis in some brain regions. J. Comp. Neurol. 126, 337-389.
4. Archimbaud, E., Philip, I., Coiffier, B., Michallet, M., Salles, G., Sebban, C., Roubi, N., Lopez, F., Bessueille, L., Mazars, P., Gerard, C., et al. (1997). Selected autologous peripheral blood CD34+ Thy-1+ Lin- hematopoietic stem cell (HSC) transplantation and multiple myeloma: A European study. Blood 90, 394a.
5. Asahara, T., Murohara, T., Sullivan, A., Silver, M., van der Zee, R., Li, T., Witzenbichler, B., Schatteman, G., and Isner, J.M. (1997). Isolation of putative progenitor endothelial cells for angiogenesis. Science 275, 964-967.
6. Bancroft, F.W. (1903). Variation and fusion of colonies in compound ascidians. Calif. Acad. Sci. 31, 137-186.
7. Baroffio, A., Hamann, M., Bernheim, L., Bochaton-Piallat, M.L., Gabbiani, G., and Bader, C.R. (1996). Identification of self-renewing myoblasts in the progeny of single human muscle satellite cells. Differentiation 60, 47-57.
8. Baum, C.M., Weissman, I.L., Tsukamoto, A.S., Buckle, A.M., and Peault, B. (1992). Isolation of a candidate human hematopoietic stem-cell population. Proc. Natl. Acad. Sci. USA 89, 2804-2808.
9. Becker, A., McCulloch, E., and Till, J. (1963). Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 197, 452-454.
10. Berrill, N. (1941). Development of the bud in Botryllus. Biol. Bull. 80, 185-193.
11. Billingham, R., Brent, L., and Medawar, P.B. (1954). Quantitative studies on tissue transplantation immunity II: The origin, strength, and duration of actively and adoptively acquired immunity. Proc. R. Soc. London 143, 58.
12. Bjornson, C.R., Rietze, R.L., Reynolds, B.A., Magli, M.C., and Vescovi, A.L. (1999). Turning brain into blood: A hematopoietic fate adopted by adult neural stem cells in vivo. Science 283, 534-537.
13. Bradford, G.B., Williams, B., Rossi, R., and Bertoncello, I. (1997). Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp. Hematol. 25, 445-453.
14. Brill, S., Zvibel, I., and Reid, L.M. (1999). Expansion conditions for early hepatic progenitor cells from embryonal and neonatal rat livers. Dig. Dis. Sci. 44, 364-371.
15. Buss, L. (1982). Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc. Natl. Acad. Sci. USA 79, 5337-5341.
16. Buss, L.W. (1999). Slime molds, ascidians, and the utility of evolutionary theory. Proc. Natl. Acad. Sci. USA 96, 8801-8803.
17. Butcher, E.C., and Picker, L.J. (1996). Lymphocyte homing and homeostasis. Science 272, 60-66.
18. Campbell, K.H., Ritchie, W.A., and Wilmut, I. (1993). Nuclear-cytoplasmic interactions during the first cell cycle of nuclear transfer reconstructed bovine embryos: Implications for deoxyribonucleic acid replication and development. Biol. Reprod. 49, 933-942.
19. Chadwick-Furman, N.E., and Weissman, I.L. (1995). Life history plasticity in chimaeras of the colonial ascidian botryllus schlossen. Proc. R. Soc. London B Biol. Sci. 262, 157-162.
20. Chiquoine, A.D. (1954). The identification, origin, and migration of the primordial germ cells in the mouse embryo. Anat. Rec. 118, 135-145.
21. Choi, K., Kennedy, M., Kazarov, A., Papadimitriou, J.C., and Keller, G. (1998). A common precursor for hematopoietic and endothelial cells. Development 125, 725-732.
22. Cumano, A., Garcia-Porrero, J., Dieterlen-Lievre, F., and Godin, I. (1995). Intra-embryonic hematopoiesis in mice. C R Seances Soc. Biol. Fil. 189, 617-627.
23. De Haan, G., and Van Zant, G. (1997). Intrinsic and extrinsic control of hemopoietic stem cell numbers: Mapping of a stem cell gene. J. Exp. Med. 186, 529-536.
24. Detrich, H.W., III, Kieran, M.W., Chan, F.Y., Barone, L.M., Yee, K., Rundstadler, J.A., Pratt, S., Ransom, D., and Zon, L.I. (1995). Intraembryonic hematopoietic cell migration during vertebrate development. Proc. Natl. Acad. Sci. USA 92, 10713-10717.
25. Domen, J., and Weissman, I.L. (1999). Self-renewal, differentiation or death: Regulation and manipulation of hematopoietic stem cell fate. Mol. Med. Today 5, 201-208.
26. Domen, J., Cheshier, S., and Weissman, I.L. (2000). The role of apoptosis in the regulation of hematopoietic stem cells; overexpression of Bcl-2 increases both their number and repopulation potential. J. Exp. Med. 191, 1-11.
27. Eglitis, M.A., and Mezey, E. (1997). Hematopoietic cells differentiate into both microglia and macroglia in the brains of adult mice. Proc. Natl. Acad. Sci. USA 94, 4080-4085.
28. Ezine, S., Jerabek, L., and Weissman, I. (1987). The phenotype of thymocytes derived from a single clonogenic precursor. J Immunol. 139, 2195-2199.
29. Ferrari, G., Cusella-De Angelis, G., Coletta, M., Paolucci, E., Stornaiuolo, A., Cossu, G., and Mavilio, F. (1998). Muscle regeneration by bone marrow-derived myogenic progenitors. Science 279, 1528-1530.
30. Fricker, R.A., Carpenter, M.K., Winkler, C., Greco, C., Gates, M.A., and Bjorklund, A. (1999). Site-specific migration and neuronal differentiation of human neural progenitor cells after transplantation in the adult rat brain. J. Neurosci. 19, 5990-6005.
31. Fuchs, E., and Segre, J.A. (2000). Stem cells: A new lease on life. Cell 100, this issue, 413-155.
32. Gage, F.H. (1998). Stem cells of the central nervous system. Curr. Opin. Neurobiol. 8, 671-676.
33. Gandy, K.L., and Weissman, I.L. (1998). Tolerance of allogeneic heart grafts in mice simultaneously reconstituted with purified allogeneic hematopoietic stem cells. Transplantation 65, 295-304.
34. Gardner, R.L., and Rossant, J. (1979). Investigation of the fate of 4-5 day post-coitum mouse inner cell mass cells by blastocyst injection. J. Embryol. Exp. Morphol. 52, 141-152.
35. Gazitt, Y., Reading, C.C., Hoffman, R., Wickrema, A., Vesole, D.H., Jagannath, S., Condino, J., Lee, B., Barlogie, B., and Tricot, G. (1995). Purified CD34+ Lin- Thy+ stem cells do not contain clonal myeloma cells. Blood 86, 381-389.
36. Goodell, M.A., Brose, K., Paradis, G., Conner, A.S., and Mulligan, R.C. (1996). Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J. Exp. Med. 183, 1797-1806.
37. Grosberg, R.K. (1981). Competitive ability influences habitat choice in marine invertebrates. Nature 290, 700-702.
38. Gurdon, J.B., and Uehlinger, V. (1966). "Fertile" intestine nuclei. Nature 270, 1240-1241.
39. Gussoni, E., Soneoka, Y., Strickland, C., Buzney, E., Khan, M., Flint, A., Kunkel, L., and Mulligan, R. (1999). Dystrophin expression in the mdx mouse restored by stem cell transplantation. Nature 401, 390-393.
40. Harrison, D.E. (1980). Lifespans of immunohemopoietic stem cell lines. Adv. Pathobiol. 7, 187-199.
41. Harrison, D.E., Astle, C.M., and Lerner, C. (1988). Number and continuous proliferative pattern of transplanted primitive immunohematopoietic stem cells. Proc. Natl. Acad. Sci. USA 85, 822-826.
42. Hirsch, E., Iglesias, A., Potocnik, A.J., Hartmann, U., and Fassler, R. (1996). Impaired migration but not differentiation of haematopoietic stem cells in the absence of beta1 integrins. Nature 380, 171-175.
43. Jackson, K.A., Mi, T., and Goodell, M.A. (1999). Hematopoietic potential of stem cells isolated from murine skeletal muscle. Proc. Natl. Acad. Sci. USA 96, 14482-14486.
44. Jones, E.M., and Sarvetnick, N. (1997). Islet regeneration in IFNγ transgenic mice. Horm. Metab. Res. 29, 308-310.
45. Kay, H. (1965). Lancet ii, 418-419.
46. Kempermann, G., Kuhn, H.G., and Gage, F.H. (1997). More hippocampal neurons in adult mice living in an enriched environment. Nature 386, 493-495.
47. Kondo, M., Weissman, I.L., and Akashi, K. (1997). Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91, 661-672.
48. Lauzon, R.J., Patton, C.W., and Weissman, I.L (1993). A morphological and immunohistochemical study of programmed cell death in Botryllus schlosseri (Tunicata, Ascidiacea). Cell Tiss. Res. 272, 115-127.
49. Lemischka, I.R., Raulet, D.H., and Mulligan, R.C. (1986). Developmental potential and dynamic behavior of hematopoietic stem cells. Cell 45, 917-927.
50. Lois, C., and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148.
51. MacGregor, G.R., Zambrowicz, B.P., and Soriano, P. (1995). Tissue non-specific alkaline phosphatase is expressed in both embryonic and extraembryonic lineages during mouse embryogenesis but is not required for migration of primordial germ cells. Development 121, 1487-1496.
52. Magor, B.G., De Tomaso, A., Rinkevich, B., and Weissman, I.L. (1999). Allorecognition in colonial tunicates: Protection against predatory cell lineages? Immunol. Rev. 167, 69-79.
53. Medvinsky, A., and Dzierzak, E. (1996). Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 86, 897-906.
54. Metcalf, D., and Moore, M.A.S. (1971). Hematopoietic Cells (Amsterdam: North-Holland).
55. Millar, R. (1971). In Advances in Marine Biol, R.H. Russell and M. Young, eds. (London: Allen and Unwin), 1-100.
56. Mintz, B., and Russell, E.S. (1957). Gene-induced embryological modifications of primordial germ cells in the mouse. J. Exp. Zool. 134, 207-237.
57. Molineux, G., Pojda, Z., Hampson, I.N., Lord, B.I., and Dexter, T.M. (1990). Transplantation potential of peripheral blood stem cells induced by granulocyte colony-stimulating factor. Blood 76, 2153-2158.
58. Moore, M., and 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.
59. Morrison, S.J., and Weissman, I.L. (1994). The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 7, 661-673.
60. Morrison, S.J., Hemmati, H.D., Wandycz, A.M., and Weissman, I.L. (1995). The purification and characterization of fetal liver hematopoietic cells. Proc. Natl. Acad. Sci. USA 92, 10302-10306.
61. Morrison, S.J., Prowse, K.R., Ho, P., and Weissman, I.L. (1996a). Telomerase activity in hematopoietic cells is associated with self-renewal potential. Immunity 5, 207-216.
62. Morrison, S.J., Wandycz, A.M., Akashi, K., Globerson, A., and WeissMan, I.L. (1996b). The aging of hematopoietic stem cells. Nat. Med. 2, 1011-1016.
63. Morrison, S.J., Wandycz, A.M., Hemmati, H.D., Wright, D.E., and Weissman, I.L. (1997a). Identification of a lineage of multipotent hematopoietic progenitors. Development 124, 1929-1939.
64. Morrison, S.J., Wright, D.E., and Weissman, I.L (1997b). Cyclophosphamide/granulocyte colony-stimulating factor induces hematopoietic stem cells to proliferate prior to mobilization. Proc. Natl. Acad. Sci. USA 94, 1908-1913.
65. Morrison, S.J., White, P.M., Zock, C., and Andersen, D.J. (1999). Prospective identification, isolation by flow cytometry, and in vivo self-renewal of multipotent mammalian neural crest stem cells. Cell 96, 737-749.
66. Muller-Sieburg, C.E., and Riblet, R. (1996). Genetic control of the frequency of hematopoietic stem cells in mice: Mapping of a candidate locus to chromosome 1. J. Exp. Med. 183, 1141-1150.
67. lo hematopoietic stem cell. Cell 44, 653-662.
68. Oka, H., and Watanabe, H. (1957). Colony-specificity in compound ascidians as tested by fusion experiments. Proc. Japan. Acad. Sci. 33, 657-664.
69. Osawa, M., Hanada, K., Hamada, H., and Nakauchi, H. (1996). Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273, 242-245.
70. Overturf, K., al-Dhalimy, M., Ou, C.N., Finegold, M., and Grompe, M. (1997). Serial transplantation reveals the stem-cell-like regenerative potential of adult mouse hepatocytes. Am. J. Pathol. 151, 1273-1280.
71. Owen, R.D. (1945). Immunogenetic consequences of vascular anastomoses between bovine twins. Science 102, 400-401.
72. Palmer, T.D., Takahashi, J., and Gage, F.H. (1997). The adult rat hippocampus contains primordial neural stem cells. Mol. Cell. Neurosci. 8, 389-404.
73. Pancer, Z., Gershon, H., and Rinkevich, B. (1995). Coexistence and possible parasitism of somatic and germ cell lines in chimeras of the colonial urochordate botryllus schlosseri. Biol. Bull. 189, 106-112.
74. Petersen, B.E., Bowen, W.C., Patrene, K.D., Mars, W.M., Sullivan, A.K., Murase, N., Boggs, S.S., Greenberger, J.S., and Goff, J.P. (1999). Bone marrow as a potential source of hepatic oval cells. Science 284, 1168-1170.
75. Ray, J., Peterson, D.A., Schinstine, M., and Gage, F.H. (1993). Proliferation, differentiation, and long-term culture of primary hippocampal neurons. Proc. Natl. Acad. Sci. USA 90, 3602-3606.
76. Reynolds, B.A., and Weiss, S. (1992). Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710.
77. Richman, C.M., Weiner, R.S., and Yankee, R.A. (1976). Increase in circulating stem cells following chemotherapy in man. Blood 47, 1031-1039.
78. Sabin, F.R. (1920). Studies on the origin of blood vessels and of red corpuscles as seen in the living blastoderm of the chick during the second day of incubation. Contrib. Embryol. 9, 213.
79. Scofield, V.L., Schlumpberger, J.M., West, L.A., and Weissman, I.L. (1982). Protochordate allorecognition is controlled by a MHC-like gene system. Nature 295, 499-502.
80. Shizuru, J., and Weissman, I. (1999). Isolation and characterization of hematopoietic stem cells. In Hematopoietic Cell Transplantation, E.D. Thomas, K.G. Blume, and S.J. Forman, eds. (Maiden, MA: Blackwell Science, Inc.), pp. 63-78.
81. Shizuru, J.A., Jerabek, L., Edwards, C.T., and Weissman, I.L. (1996). Transplantation of purified hematopoietic stem cells: Requirements for overcoming the barriers of allogeneic engraftment. Biol. Blood Marrow Transplant. 2, 3-14.
82. Siminovitch, L., McCulloch, E., and Till, J. (1963). The distribution of colony-forming cells among spleen colonies. J. Cell. Comp. Physiol. 62, 327-336.
83. Smith, L.G., Weissman, I.L., and Heimfeld, S. (1991). Clonal analysis of hematopoietic stem-cell differentiation in vivo. Proc. Natl. Acad. Sci. USA 88, 2788-2792.
84. Spangrude, G.J., Heimfeld, S., and Weissman, I.L. (1988). Purification and characterization of mouse hematopoietic stem cells. Science 241, 58-62.
85. Steinbeck, J. (1955). The Log from the Sea of Cortez (New York: Penguin Books).
86. Stemple, D.L., and Anderson, D.J. (1992). Isolation of a stem cell for neurons and glia from the mammalian neural crest. Cell 71, 973-985.
87. Stoner, D.S., and Weissman, I.L. (1996). Somatic and germ cell parasitism in a colonial ascidian: Possible role for a highly polymorphic allorecognition system. Proc. Natl. Acad. Sci. USA 93, 15254-15259.
88. Stoner, D.S., Rinkevich, B., and Weissman, I.L. (1999). Heritable germ and somatic cell lineage competitions in chimeric colonial protochordates. Proc. Natl. Acad. Sci. USA 96, 9148-9153.
89. Suhonen, J.O., Peterson, D.A., Ray, J., and Gage, F.H. (1996). Differentiation of adult hippocampus-derived progenitors into olfactory neurons in vivo. Nature 383, 624-627.
90. Takahashi, M., Palmer, T.D., Takahashi, J., and Gage, F.H. (1998). Widespread integration and survival of adult-derived neural progenitor cells in the developing optic retina. Mol. Cell. Neurosci. 12, 340-348.
91. Thomas, E.D. (1991). Frontiers in bone marrow transplantation. Blood Cells 17, 259-267.
92. Till, J.E., and McCulloch, E.A. (1961). A direct measurement of the radiation sensitivity of normal mouse bone marrow cells. Radiat. Res. 14, 1419-1430.
93. Turpen, J.B., Kelley, C.M., Mead, P.E., and Zon, L.I. (1997). Bipotential primitive-definitive hematopoietic progenitors in the vertebrate embryo. Immunity 7, 325-334.
94. Uchida, N. (1992). Characterization of Mouse Hematopoietic Stem Cells. Ph.D. thesis, Stanford University, Stanford, California.
95. Uchida, N., and 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.
96. Uchida, N., Jerabek, L., and Weissman, I.L. (1996). Searching for hematopoietic stem cells. II. The heterogeneity of Thy-1.1(lo)lin (-/lo)Sca-1+ mouse hematopoietic stem cells separated by counterflow centrifugal elutriation. Exp. Hematol. 24, 649-659.
97. Uchida, N., Tsukamoto, A., He, D., Friera, A.M., Scollay, R., and Weissman, I.L. (1998). High doses of purified stem cells cause early hematopoietic recovery in syngeneic and allogeneic hosts. J. Clin. Invest. 101, 961-966.
98. Uchida, N., He, D., Reitsma, M.J., Masek, M., Weissman, I., Gage, F., Buck, D. (1999). Direct isolation of human neural stem cells from fetal brain by cell sorting. J. Neurosci. 25, 1767.
99. van Bekkum, D., van Putten, L., and de Vries, M. (1962). Anti-host reactivity and tolerance of the graft in relation to secondary disease in radiation chimeras. Ann. N Y Acad. Sci. 99, 550-568.
100. Vaziri, H., Dragowska, W., Allsopp, R.C., Thomas, T.E., Harley, C.B., and Lansdorp, P.M. (1994). Evidence for a mitotic clock in human hematopoietic stem cells: Loss of telomeric DNA with age. Proc. Natl. Acad. Sci. USA 91, 9857-9860.
101. Visser, J.W.M., Gauman, J.G.J., Mulder, A.H., Eliason, J.F., and de Leeuw, A.W. (1984). Isolation of murine pluripotent hemopoietic stem cells. J. Exp. Med. 59, 1576-1590.
102. Wakayama, T., Perry, A.C., Zuccotti, M., Johnson, K.R., and Yanagimachi, R. (1998). Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature. 394, 369-374.
103. Watkins, D.I., Chen, Z.W., Hughes, A.L., Hodi, F.S., and Letvin, N.L. (1990). Genetically distinct cell populations in naturally occurring bone marrow-chimeric primates express similar MHC class I gene products. J. Immunol. 144, 3726-3735.
104. Weissman, I.L. (1989). Some observation on the life history of lymphocytes. Harvey Lect. 85, 43-69.
105. Weissman, I.L., Papaioannou, V.E., and Gardner, R.L. (1978). Fetal hematopoietic origins of the adult hematolymphoid system. In Cold Spring Harbor Symposia on Differentiation of Normal and Neoplastic Hematopoietic Cells, B. Clarkson, P.A. Marks, and J.E. Till, eds., pp. 33-47.
106. Weissmann, A. (1892). Das Keimplasma: Eine Theorie der Verebung (Fisher-Verlag).
107. Whitlock, C.A., Tidmarsh, G.F., Muller-Sieburg, C., and 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.
108. Wilmut, I., Schnieke, A.E., McWhir, J., Kind, A.J., and Campbell, K.H. (1997). Viable offspring derived from fetal and adult mammalian cells. Nature 385, 810-813.
109. Wu, A., Till, J., Siminovitch, L., and McCulloch, E. (1968). Cytological evidence for a relationship between normal hematopoietic colony-forming cells and cells of the lymphoid system. J. Exp. Med. 127, 455-467.
110. Yandava, B.D., Billinghurst, L.L., and Snyder, E.Y. (1999). "Global" cell replacement is feasible via neural stem cell transplantation: Evidence from the dysmyelinated shiverer mouse brain. Proc. Natl. Acad. Sci. USA 96, 7029-7034.