Experimental Hematology
Volume 37, Issue 7 , Pages 775-783 , July 2009

Problems in the promised land: Status of adult marrow stem cell biology

  • Peter J. Quesenberry

      Affiliations

    • Corresponding Author InformationOffprint requests to: Peter J. Quesenberry, M.D., Department of Medicine, Division of Hematology/Oncology, Warren Alpert Medical School of Brown University and Rhode Island Hospital, 593 Eddy Street, George 3, Providence, RI 02903
  • ,
  • Gerri J. Dooner
  • ,
  • Mark S. Dooner

Received 5 May 2009 ,Revised 5 May 2009 ,Accepted 7 May 2009.

References 

  1. Bertoncello I, Hodgson GS, Bradley TR. Multiparameter analysis of transplantable hemopoietic stem cells: the separation and enrichment of stem cells homing to marrow and spleen on the basis of rhodamine 123 fluorescence. Exp Hematol. 1985;13:999–1006
  2. Baines P, Visser JW. Analysis and separation of murine bone marrow stem cells by H33342 fluorescence-activated cell sorting. Exp Hematol. 1983;11:701–708
  3. Ploemacher RE, Brons NHC. Cells with marrow and spleen repopulating ability and forming spleen colonies on days 16, 12, and 8 are sequentially ordered on the basis of increasing rhodamine 123 retention. HJ Cell Physiol. 1988;36:531
  4. Wolf NS, Kone A, Priestley GV, Bartelmez SH. In vivo and in vitro characterization of long-term repopulating primitive hematopoietic cells isolated by sequential Hoechst 33342-rhodamine 123 FACS selection. Exp Hematol. 1993;21:614–622
  5. Forsberg EC, Prohaska SS, Katzman S, et al. Differential expression of novel potential regulators in hematopoietic stem cells. PLoS Genet. 2005;1:e28
  6. Rossi DJ, Bryder D, Zahn JM, et al. Cell intrinsic alterations underlie hematopoietic stem cell aging. Proc Natl Acad Sci U S A. 2005;102:9194–9199
  7. Arber C, BitMansour A, Sparer TE, et al. Common lymphoid progenitors rapidly engraft and protect against lethal murine cytomegalovirus infection after hematopoietic stem cell transplantation. Blood. 2003;102:421–428
  8. Manz MG, Miyamoto T, Akashi K, Weissman IL. Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci U S A. 2002;399:11872–11877
  9. Miyamoto T, Iwasaki H, Reizis B, et al. Myeloid or lymphoid promiscuity as a critical step in hematopoietic lineage commitment. Dev Cell. 2002;3:137–147
  10. Christensen JL, Weissman IL. Flk-2 is a marker in hematopoietic stem cell differentiation: a simple method to isolate long-term stem cells. Proc Natl Acad Sci U S A. 2001;498:14541–14546
  11. Kondo M, Scherer DC, King AG, et al. Lymphocyte development from hematopoietic stem cells. Curr Opin Genet Dev. 2001;11:520–526Review
  12. Kondo M, Scherer DC, Miyamoto T, et al. Cell fate conversion of lymphoid-committed progenitors by instructive actions of cytokines. Nature. 2000;407(6802):383–386
  13. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000;404(6774):193–197
  14. Cheshier SH, Morrison SJ, Liao X, Weissman IL. In vivo proliferation and cell cycle kinetics of long-term self-renewing hematopoietic stem cells. Proc Natl Acad Sci U S A. 1999;16:3120–3125
  15. Kondo M, Weissman IL, Akashi K. Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell. 1997;28:661–672
  16. Morrison SJ, Wandycz AM, Hemmati HD, Wright DE, Weissman IL. Identification of lineage of multipotent hematopoietic progenitors. Development. 1997;124:1929–1939
  17. Adolfsson J, Mansson R, Buza-Vidas N, et al. Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential: a revised road map for adult blood lineage commitment. Cell. 2005;121:295–306
  18. Randal TD, Lund FE, Howard MD, et al. Expression of murine CD38 defines a population of long-term reconstituting hematopoietic stem cells. Blood. 1996;87:4057–4067
  19. Morrison SJ, Weissman IL. The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity. 1994;1:661–673
  20. Forsberg EC, Bhattacharya D, Weissman IL. Hematopoietic stem cells: expression profiling and beyond. Stem Cell Rev. 2006;2:23–30Review
  21. Warren L, Bryder D, Weissman IL, et al. Transcription factor profiling in individual hematopoietic progenitors by digital RT-PCR. Proc Natl Acad Sci U S A. 2006;103:17807–17812
  22. Bryder D, Rossi DJ, Weissman IL. Hematopoietic stem cells: the paradigmatic tissue-specific stem cell. Am J Pathol. 2006;169:338–346Erratum in: Am J Pathol. 2006;169:1899
  23. Forsberg EC, Serwold T, Kogan S, et al. New evidence supporting megakaryocyte-erythrocyte potential of flk2/flt3+ multipotent hematopoietic progenitors. Cell. 2006;126:415–426
  24. Passegue E, Wagers AJ, Giuriato S, et al. Global analysis of proliferation and cell cycle gene expression in the regulation of hematopoietic stem and progenitor cell fates. J Exp Med. 2005;202:1599–1611
  25. Wagers AJ, Weissman IL. Differential expression of alpha2 integrin separates long-term and short-term reconstituting Lin-/loThy1.1(lo)c-kit+ Sca-1_hematopoietic stem cells. Stem Cells. 2006;24:1087–1094
  26. Cantor AB, Orkin SH. Hematopoietic development: a balancing act. Curr Opin Genet Dev. 2001;11:513–519
  27. Ivanova NB, Dimos JT, Schaniel C, et al. A stem cell molecular signature. Science. 2002;298:601–604
  28. Pritsker M, Doniger TT, Kramer LC, et al. Diversification of stem cell molecular repertoire by alternative splicing. Proc Natl Acad Sci U S A. 2005;102:14290–14295
  29. Hu M, Krause D, Greaves M, et al. Multilineage gene expression precedes commitment in the hematopoietic system. Genes Dev. 1997;15:774
  30. Orlic D, Laprise SL, Cline AP, Anderson SM, Bodine DM. Isolation of stem cell-specific cDNAs from hematopoietic stem cell populations. Ann N Y Acad Sci. 1999;872:243–254discussion 254–255
  31. Tajima F, Deguchi T, Laver JH, et al. Reciprocal expression of CD38 and CD34 by adult murine hematopoietic stem cells. Blood. 2001;97:2618–2624
  32. Li CL, Jonson GR. Rhodamine 123 reveals heterogeneity within murine Lin-, Sca-1+ hematopoietic stem cells. J Exp Med. 1992;175:1443
  33. Li CL, Johnson GR. Murine hematopoietic stem and progenitor cells: I. Enrichment and biologic characterization. Blood. 1995;85:1472–1479
  34. Zijlmans JM, Visser JW, Kleiverda K, et al. Modification of rhodamine staining allows identification of hematopoietic stem cells with preferential short-term or long-term bone marrow-repopulating ability. Proc Natl Acad Sci U S A. 1995;92:8901–8905
  35. Huttmann A, Liu SL, Boyd AW, et al. Functional heterogeneity within rhodamine 123loHoechst33342lo/sp primitive hematopoietic stem cells revealed by pryronin Y. Exp Hematol. 2001;29:1109–1116
  36. Weismann A, Phillips RL, Mojica M, et al. Expression of CD27 on murine hematopoietic stem and progenitor cells. Immunity. 2000;12:193–199
  37. Aardal N, Laerum O. Circadian variations in mouse bone marrow. Exp Hematol. 1983;9:792–801
  38. Stevold O, Laerum O, Riise T. Age-related differences and circadian and seasonal variations of myelopoietic progenitor cell (CFU-GM) numbers in mice. Eur J Haematol. 1988;40:42–49
  39. Smaaland R, Laerum O, Southern R, et al. Colony-forming units granulocyte-macrophage and DNA synthesis of human bone marrow are circadian stage dependent and show co-variation. Blood. 1992;79:2281–2287
  40. D'Hondt L, McAuliffe C, Damon J, et al. Circadian variations of bone marrow engraftability. J Cell Physiol. 2004;200:63–70
  41. Necas E, Znojil V. CFU-S content and cycling rate in several strains of mice. Exp Hematol. 1987;15:759–764
  42. Peters SO, Kittler EL, Ramshaw HS, et al. Murine marrow cells expanded in culture with IL-3, IL-6, IL-11, and SCF acquire an engraftment defect in normal hosts. Exp Hematol. 1995;23:461–469
  43. Peters SO, Kittler EL, Ramshaw HS, et al. Ex vivo expansion of murine marrow cells with interleukin-3 (IL-3), IL-6, IL-11, and stem cell factor leads to impaired engraftment in irradiated hosts. Blood. 1996;87:30–37
  44. Becker PS, Nilsson SK, Li Z, et al. Adhesion receptor expression by hematopoietic cell lines and murine progenitors: modulation by cytokines and cell cycle status. Exp Hematol. 1999;27:533–541
  45. Berrios VM, Dooner GJ, Nowakowski G, et al. The molecular basis for the cytokine-induced defect in homing and engraftment of hematopoietic stem cells. Exp Hematol. 2001;29:1326–1335
  46. Reddy GP, McAuliffe CI, Pang L, et al. Cytokine receptor repertoire and cytokine responsiveness of Ho dull/Rh dull stem cells with differing potentials for G1/S phase progression. Exp Hematol. 2002;30:792–800
  47. Habibian HK, Peters SO, Hsieh CC, et al. The fluctuating phenotype of the lymphohematopoietic stem cell with cell cycle transit. J Exp Med. 1998;188:393–398
  48. Cerny J, Dooner M, McAuliffe C, et al. Homing of purified murine lymphohematopoietic stem cells: a cytokine-induced defect. J. Hematother Stem Cell Res. 2002;11:913–922
  49. Colvin GA, Dooner MS, Dooner GJ, et al. Stem cell continuum: directed differentiation hotspots. Exp Hematol. 2007;35:96–107
  50. Colvin GA, Lambert JF, Carlson JE, McAuliffe CI, Abedi M, Quesenberry PJ. Rhythmicity of engraftment and altered cell cycle kinetics of cytokine-cultured murine marrow in simulated microgravity compared with static cultures. Vitro Cell Dev Biol Anim. 2002;38:343–351
  51. Colvin GA, Lambert JF, Moore BE, et al. Intrinsic hematopoietic stem cell/progenitor plasticity: inversions. J Cell Physiol. 2004;199:20–31
  52. Reddy GP, Tiarks CY, Pang L, et al. Cell cycle analysis and synchronization of pluripotent hematopoietic progenitor stem cells. Blood. 1997;90:2293–2299
  53. Pang L, Reddy PV, McAuliffe CI, et al. Studies on BrdU labeling of hematopoietic cells: stem cells and cell lines. J Cell Physiol. 2003;197:251–260
  54. Bradford GB, Williams B, Rossi R, et al. Quiescence, cycling, and turnover in the primitive hematopoietic stem cell compartment. Exp Hematol. 1997;25:445–453
  55. Fleming WH, Alpern EJ, Uchida N, et al. Functional heterogeneity is associated with the cell cycle status of murine hematopoietic stem cells. J Cell Biol. 1993;122:897–902
  56. Quesenberry PJ, Stanley K. A statistical analysis of murine stem cell suicide techniques. Blood. 1980;56:1000–1005
  57. Till JE, McCulloch EA. A direct measurement of radiation sensitivity of normal mouse marrow cells. Radiat Res. 1961;14:213–222
  58. Becker AJ, McCulloch EA, Siminovitch L, et al. The effect of differing demands for blood cell production on DNA synthesis by hemopoietic colony-forming cells of mice. Blood. 1965;26:296–308
  59. Lajtha LG, Pozzi LV, Schofield R, et al. Kinetic properties of hemopoietic stem cells. Cell Tissue Kinet. 1969;2:39
  60. Frindel E, Leuchars E, Davis AJS. Thymus dependency of bone marrow stem cell proliferation in response to certain antigens. Exp Hematol. 1976;4:275–284
  61. Lord BI. Haemopoietic stem cells. In: Potten CS, ed. Stem Cells: Their Identification and Characterization. Edinburgh: Churchill Livingston; 1983:118.
  62. Gidali J, Istvan E, Fehr I. Long-term perturbation of hemopoiesis after moderate damage to stem cells. Exp Hematol. 1985;13:647–651
  63. Croizat H, Frindel E, Tibiana M, et al. Antigenic stimulation of DNA synthesis in the haematopoietic stem cells of axenic mice. Nature. 1970;228:1187–1188
  64. Croizat H, Frindel E, Tubiana M. Proliferative activity of stem cells in the bone-marrow of mice after single and multiple irradiations (total-or partial-body exposure). Int J Radiat Biol. 1970;18:347–358
  65. Vassort F, Winterholer M, Frindel E, et al. Kinetic parameters of bone marrow stem cells using in vivo suicide by tritiated thymidine or hydroxyurea. Blood. 1973;41:789
  66. Lord BI, Lajtha LG, Gidali J. Measurement of the kinetic status of bone marrow precursor cells: three cautionary tales. Cell Tissue Kinet. 1974;7:507–515
  67. Guigon M, Sainteny F, Dumenil D, et al. Response of quiescent and cycling CFU to stimulation. Exp Hematol. 1978;6:270–272
  68. Wu AM. A method for measuring the generation time and length of DNA synthesizing phase of clonogenic cells in a heterogeneous population. Cell Tissue Kinet. 1981;14:39
  69. Monette FC, Demers ML. An alternate method for determining the proliferative status of transplantable murine stem cells. Exp Hematol. 1982;10:307–313
  70. Boersma WJA. Radiation sensitivity and cycling status of mouse bone marrow prothymocytes and day 8 colony forming units spleen (CFUs). Exp Hematol. 1983;11:922–930
  71. Monette F, Holden SA, Sheehy MJ, et al. Specificity of hemin action in vivo at early stages of hematopoietic cell differentiation. Exp Hematol. 1984;12:782–787
  72. Inoue T, Cronkite EP, Commerford SL, et al. Residual toxicity in hematopoietic cells following a single dose of methylnitrosourea. Leuk Res. 1984;8:105–116
  73. Wdzieczak-Bakala J, Pines M, Guigon M, et al. Cyclic AMP response to various haemopoietic regulators. Cell Tissue Kinet. 1985;18:297–306
  74. Goldeck H. Der 24-stoden-rytmus der erythropoese. Arztl Forsch. 1948;2:22–27
  75. Levy F, Blazsek I, Ferle-Vidovic A. Circadian and seasonal rhythms in murine bone marrow colony-forming cells affect tolerance for the anticancer agent 4-o-tetrahydropyranyladriamycin (THP). Exp Hematol. 1988;8:696–701
  76. Takahashi J, Zatz M. Regulation of circadian rhythmicity. Science. 1982;217:1104–1111
  77. Juopperi TA, Sharkis SJ. Isolation of quiescent marrow hematopoietic stem cells by homing properties. Methods Mol Biol. 2008;430:21–30
  78. Pearce DJ, Bonnet D. The combined use of Hoechst efflux ability and aldehyde dehydrogenase activity to identify murine and human hematopoietic stem cells. Exp Hematol. 2007;35:1437–1446
  79. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that reside in the low oxygenic niches. Blood. 2007;110:3056–3063
  80. Till JE, McCulloch EA, Siminovitch L. A stochastic model of stem cell proliferation, based on the growth of spleen colony-forming cells. Proc Natl Acad Sci U S A. 1964;51:29–36
  81. Stewart FM, Crittenden RB, Lowry PA, et al. Long-term engraftment of normal and post-fluorouracil murine marrow into normal nonmyeloablated mice. Blood. 1993;81:2566–2571
  82. Quesenberry PJ, Ramshaw H, Crittenden RB, et al. Engraftment of normal murine marrow into non-myeloablated host mice. Blood Cells. 1994;20:348–350
  83. Ramshaw HS, Rao SS, Crittenden RB, et al. Engraftment of bone marrow cells into normal unprepared hosts: effects of 5-fluorouracil and cell cycle status. Blood. 1995;86:924–929
  84. Ramshaw HS, Crittenden RB, Dooner M, et al. High levels of engraftment with a single infusion of bone marrow cells into normal unprepared mice. Biol Blood Marrow Transplant. 1995;1:74–80
  85. Rao SS, Peters SO, Crittenden RB, et al. Stem cell transplantation in the normal nonmyeloablated host: relationship between cell dose, schedule, and engraftment. Exp Hematol. 1997;25:114–121
  86. Blomberg M, Rao S, Reilly J, et al. Repetitive bone marrow transplantation in nonmyeloablated recipients. Exp Hematol. 1998;26:320–324
  87. Colvin GA, Lambert JF, Abedi M, et al. Murine marrow cellularity and the concept of stem cell competition: geographic and quantitative determinants in stem cell biology. Leukemia. 2004;18:575–583
  88. Nilsson SK, Dooner MS, Tiarks CY, et al. Potential and distribution of transplanted hematopoietic stem cells in a nonablated mouse model. Blood. 1997;89:4013–4020
  89. Sieburg HB, Cho RH, Dykstra B, et al. The hematopoietic stem cell compartment consists of a limited number of discrete stem cell subsets. Blood. 2006;107:2311–2316
  90. Hendrikx PJ, Martens ACM, Hagenbeek A, et al. Homing of fluorescently labeled hemopoietic stem cells. Exp Hematol. 1997;25:445
  91. Brecher G, Neben S, Yee M. Bone marrow proliferation after passage through an irradiated host. In:  Daniak N,  Cronkite EP,  McCaffrey P,  Shadduck RK editor. The Biology of Hematopoiesis. New York: Wiley-Liss; 1990;p. 449
  92. Shirota T, Tavassoli M. Alterations of bone marrow sinus endothelium induced by ionizing irradiation: implications in the homing of intravenously transplanted marrow cells. Blood Cells. 1992;18:197–214
  93. Shirota T, Tavassoli M. Cyclophosphamide induced alterations of bone marrow endothelium: implications in homing of marrow cells after transplantation. Exp Hematol. 1992;19:369–373
  94. Stohlman F, Brecher G, Schneiderman M, et al. The hemolytic effect of ionizing radiations and its relationship to the hemorrhagic phase of radiation injury. Blood. 1957;12:1061–1085
  95. Ross EAM, Anderson N, Micklem HS. Serial depletion and regeneration of the murine hematopoietic system. Implications for hematopoietic organization and the study of cellular aging. J Exp Med. 1982;155:432–444
  96. Micklem HS. Decline of colony-forming units with serial bone marrow cell passages: intrinsic or extrinsic causation? Factors affecting serially transplanted bone marrow. A commentary. Blood Cells. 1983;9:527–533
  97. Watson GE, Lorimore SA, MacDonald DA, et al. Chromosomal instability in unirradiated cells induced in vivo by a bystander effect of ionizing radiation. Cancer Res. 2000;60:5608–5611
  98. Lorimore SA, McIlrath JM, Coates PJ, et al. Chromosomal instability in unirradiated hemopoietic cells resulting from a delayed in vivo bystander effect of gamma radiation. Cancer Res. 2005;65:5668–5673
  99. Janowska-Wieczorek A, Majka M, Kijowski J, et al. Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment. Blood. 2001;3143–3149
  100. Ratajczak J, Miekus K, Kucia M, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic stem/progenitor cells: evidence for horizontal transfer of mRNA and protein delivery. Leukemia. 2006;20:847–856
  101. Deregibus MC, Cantaluppi V, Calogero R, et al. Endothelial progenitor cell-derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007;110:2440–2448
  102. Aliotta JM, Sanchez-Guijo FM, Dooner GF, et al. Alteration of marrow gene expression, protein production, and engraftment into lung by lung-derived microvesicles: a novel mechanism for phenotype modulation. Stem Cells. 2007;25:2245–2256

PII: S0301-472X(09)00158-1

doi: 10.1016/j.exphem.2009.05.003

Experimental Hematology
Volume 37, Issue 7 , Pages 775-783 , July 2009