Biology of human bone marrow stem cells

Clinical and Experimental Medicine

Volumn 3, Issue 3, 2003, Pages 140-149

  Bonnet, D ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

Fetal sheep; Hematopoietic stem cell; Mesenchymal stem cell; Nonobese diabetic severe combined immunodeficient mice; Plasticity; Transdifferentiation; Xenotransplantation model

Indexed keywords

CD133 ANTIGEN; CD34 ANTIGEN; CD38 ANTIGEN; CELL SURFACE MARKER; STEM CELL FACTOR; STEM CELL FACTOR RECEPTOR; THY 1 ANTIGEN;

BONE MARROW CELL; CELL COMPARTMENTALIZATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL HETEROGENEITY; CELL ISOLATION; CELL MATURATION; CELL POPULATION; CYTOLOGY; DIABETES MELLITUS; HEMATOPOIETIC STEM CELL; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; MESENCHYME CELL; MESENCHYME STEM CELL; NONHUMAN; PHENOTYPE; PLASTICITY; PRIORITY JOURNAL; REVIEW; SCID MOUSE; STEM CELL TRANSPLANTATION; STROMA CELL; XENOTRANSPLANTATION;

ANIMALS; BONE MARROW CELLS; COLONY-FORMING UNITS ASSAY; HEMATOPOIETIC STEM CELLS; HUMANS; MESODERM; MICE; MICE, SCID;

OVIS ARIES;

EID: 0344514043     PISSN: 15918890     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10238-003-0017-9     Document Type: Review

References (122)

1. Siminovitch L, McCulloch EA, Till JE (1963) The distribution of colony-forming cells among spleen colonies. J Cell Comp Physiol 62, 327-336
2. Phillips R (1991) Hematopoietic stem cells: concepts, assays, and controversies. Semin Immunol 3:337-347
3. Hodgson GS, Bradley TR (1979) Properties of hematopoietic stem cells surviving 5-fluorouracil treatment. Nature 281:381-384
4. Spangrude GJ, Heimfield S, Weissman IL (1988) Purification and characterization of murine hematopoietic stem cells. Science 241:58-63
5. Spangrude GJ, Johnson JR (1990) Resting and activated subsets of mouse multipotent hematopoietic stem cells. Proc Natl Acad Sci U S A 87:7433-7440
6. Morrison SJ, Weissman IL (1994) The long-term repopulating subset of hematopoietic stem cells is deterministic and isolatable by phenotype. Immunity 1:661-673
7. Srour EF, Zanjani ED, Cornetta K, et al (1993) Persistence of human multilineage, self-renewing lymphohematopoietic stem cells in chimeric sheep. Blood 82:3333-3339
8. Zanjani ED, Almeida-Porada G, Ascensao JL et al (1997) Transplantation of hematopoietic stem cells in utero. Stem Cells 15:79-84
9. McCune JM (1996) Development and applications of the SCID-hu mouse model. Semin Immunol 8:187-196
10. Torbett BE, Picchio G, Mosier DE (1991) Hu-PBL-SCID mice: a model for human immune function, AIDS, and lymphomagenesis. Immunol Rev 124:139-164
11. Dick JE (1996) Normal and leukemic human stem cells assayed in SCID mice. Semin Immunol 8:197-206
12. Shultz LD, Schweitzer PA, Christianson SW et al (1995) Multiple defects in innate and adaptive immunological function in NOD/LtSz-scid mice. J Immunol 154:180-191
13. Gan O, Murdoch B, Larochelle A et al (1997) Differential maintenance of primitive human SCID-repopulating cells, clonogenic progenitors, and long-term culture marrow stromal cells. Blood 2:641-650
14. Ishikawa F, Livingston AG, Wingard J, Nishikawa S, Ogawa M (2002) An assay for long-term engrafting human stemcells based on newborn NOD/SCID/b2-microglobulin null mice. Exp Hematol 30:488-494
15. Kollet O, Peled A, Byk T et al (2000) β2 microglobulin-deficient (B2mnull) NOD/SCID mice are excellent recipients for studying human stem cell function. Blood 95:3102-3105
16. Shultz LD, Lang PA, Christianson SH et al (2000) NOD/LtSz-Rag1null mice: an immunodeficient and radioresistant model for engraftment of human hematolymphoid cells, HIV infection, and adoptive transfer of NOD mouse diabetogenic T cells. J Immunol 164:2496-2507
17. Arevalo JMG, Ertl DC, Dao MA et al (1994) A new immunodeficient mouse strain: the nude NOD/SCID for human hematopoietic cell xenotransplantation. Blood 94[Suppl 1]:129a
18. Spangrude GJ, Brooks DM, Tumas DB (1995) Long-term repopulation of irradiated mice with limiting numbers of purified hematopoietic stem cells: in vivo expansion of stem cell phenotype but not function. Blood 85:1006-1008
19. Van Der Loo JC, Ploemacher RE (1985) Marrow- and spleen seeding efficiencies of all murine hematopoietic stem cell subsets are decreased by preincubation with hematopoietic growth factors. Blood 85:2598-2606
20. Cashman JD, Eaves CJ (2000) High marrow seeding efficiency of human lymphomyeloid repopulating cells in irradiated NOD/SCID mice. Blood 96:3979-3981
21. Wang J, Kimura T, Asada R, Harada S, Yokota S, Kawamoto Y, Fujimura Y, Tsuji T, Ikehara S, Sonoda Y (2003) SCID-repopulating cell activity of human cord blood- derived CD34-cells assured by intra-bone marrow injection. Blood 101:2924-2931
22. 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
23. Mazurier F, Doedens M, Gan O, Dick JE (2003) Rapid myeloerythroid repopulation after intrafemoral transplantation of NOD-SCID mice reveals a new class of human stem cells. Nat Med 9:959-963
24. Zanjani ED, Almeida-Porada G, Falke AW (1996) The human/sheep xenograft model: a large animal model of human hematopoiesis. Int J Hematol 63:179-192
25. Zanjani ED, Pallavicini MG, Ascensao JL et al (1992) Engraftment and long term expression of human fetal hematopoietic stem cells in sheep following transplantation in utero. J Clin Invest 89:1178-1188
26. Srour EF, Zanjani ED, Brandt JE et al (1992) Sustained human hematopoiesis in sheep transplanted in utero during early gestation with fractionated adult human bone marrow cells. Blood 79:1404-1412
27. Morris B, Miyasaka M (1985) Immunology of the sheep. Roche, Basel, Switzerland
28. Civin CI, Almeida-Porada G, Lee MJ et al (1996) Sustained, retransplantable, multilineage engraftment of highly purified adult human bone marrow stem cells in vivo. Blood 88:4102-4109
29. Civin CI, Strauss LC, Browall C et al (1985) Antigenic analysis of hematopoiesis. III. A hematopoietic progenitor cell surface antigen defined by a monoclonal antibody against KG-1a cells. J Immunol 133:157-164
30. Andrews RE, Singer JW, Bernstein ID (1989) Precursors of colony-forming cells in humans can be distinguished from colony-forming cells by expression of CD33 and CD34 antigen and light scatter. J Exp Med 169:1721-1731
31. Krause DS, Fackler MJ, Civin CI et al (1996) CD34: structure, biology, and clinical utility. Blood 87:1-13
32. Berenson RJ, Bensinger WI, Hill RS et al (1991) Engraftment after infusion of CD34+ marrow cells in patients with breast cancer or neuroblastoma. Blood 77:1717-1722
33. Siena S, Bregni M, Brando B et al (1991) Flow cytometry for clinical estimation of circulating hematopoietic progenitors for autologous transplantation in cancer patients. Blood 77:400-409
34. Fina L, Molgaard HV, Roberston D et al (1990) Expression of the CD34 gene in vascular endothelial cells. Blood 75:2417-2426
35. Baumhueter S, Dybdal N, Kyle C et al (1994) Global expression of murine CD34, a sialomucin-like endothelial ligand for l-selectin. Blood 84:2554-2565
36. Brown J, Greaves MF, Molgaard HV (1991) The gene encoding the stem cell antigen, CD34, is conserved in mouse and expressed in hematopoietic cell lines, brain, and embryonic fibroblasts. Int Immunol 3:75-84
37. Greaves MF, Brown J, Molgaard HV et al (1992) Molecular features of CD34: a hematopoietic progenitor cell-associated molecule. Leukemia 6[Suppl 1]:31-36
38. Corbeil D, Roper K, Weigmann A, Huttner WB (1998) AC133 hematopoietic stem cell antigen: human homologue of mouse kidney prominin or distinct member of a novel protein family? Blood 91:2625-2626
39. Miraglia S, Godfrey W, Yin AH, Atkins K, Wamke R, Holden JT, Bray RA, Walker EK, Buck DW (1997) A novel five-transmembrane hematopoietic stem cell antigen: isolation, characterization, and molecular cloning. Blood 90:5013-5021
40. Miraglia S, Godfrey W, Buck D (1998) A response to AC133 hematopoietic stem cell antigen: human homologue of mouse kidney prominin or distinct member of a novel protein family? Blood 91:4390-4391
41. Yin AH, Miraglia S, Zanjani EM et al (1997) AC133, a novel marker for human hematopoietic stem and progenitor cells. Blood 90:5002-5012
42. Wuchter C (2001) Impact of CD133 (AC133) and CD90 expression analysis for acute leukemia immunophenotyping. Haematologica 86:154-161
43. Majka M, Ratajack J, Machalinski B, Carter A, Pizzini D, Wasik MA, Gewirtz AM, Ratajack MZ (2000) Expression and function of AC133, a putative cell surface marker of primitive human haematopoietic cells. Folia Histochem Cytobiol 38:53-63
44. Bhatia M (2001) AC133 expression in human stem cells. Leukemia 15:1685-1688
45. Ziegler BL, Valtieri M, Almeida-Porada G et al (1999) KDR receptor: a key marker defining hematopoietic stem cells. Science 285:553-558
46. Craig W, Kay R, Cutler RB, Lansdorp PM (1993) Expression of Thy-1 on human hematopoietic progenitor cells. J Exp Med 177:1331-1342
47. Bhatia M, Wang JCY, Kapp U et al (1997) Purification of primitive human hematopoietic cells capable of repopulating immune-deficient mice. Proc Natl Acad Sci U S A 94:5320-5325
48. Goodell MA, Brose K, Paradis G et al (1996) Isolation and functional properties of murine hematopoietic stem cells that are replicating in vivo. J Exp Med 183:1797-1806
49. Yusa K, Tsuruo T (1989) Reversal mechanism of multidrug resistance by verapamil: direct binding of verapamil to P-gl ycoprotein on specific sites and transport of verapamil outward across the plasma membrane of K562/ADM cells. Cancer Res 49:5002-5006
50. Miller CL, Eaves CJ (1997) Expansion in vitro of adult murine hematopoietic stem cells with transplantable lymphomyeloid reconstitution. Proc Natl Acad Sci U S A 94:13648-13653
51. Goodell MA, Rosenzweig M, Kim H et al (1997) Dye efflux studies suggest that hematopoietic stem cells expressing low or undetectable levels of CD34 antigen exist in multiple species. Nat Med 3:1337-1345
52. Uchida N, Fujisaki T, Eaves AC, Eaves CJ (2001) Transplantable hematopoietic stem cells in human fetal liver have a CD34+ side population (SP) phenotype. J Clin Invest 108:1071-1077
53. Zhou S, Schuetz JD, Bunting KD, Colapietro AM, Sampath J et al (2001) The ABC transporter Bcrp1/ABCG2 is expressed in a wide variety of stem cells and is a molecular determinant of the side-population phenotype. Nat Med 7:1028-1034
54. Zanjani ED, Almeida-Porada G, Livingston AG et al (1998) Human bone marrow CD34- cells engraft in vivo and undergo multilineage expression that includes giving rise to CD34+ cells. Exp Hematol 26:353-360
55. Bhatia M, Bonnet D, Murdoch B et al (1998) Identification of a newly discovered class of human hematopoietic cells with SCID-repopulating activity. Nat Med 94:1038-1044
56. Osawa M, Hanada K, Hamada H et al (1996) Long-term lymphohematopoietic reconstitution by a single CD34-low/negative hematopoietic stem cell. Science 273:242-245
57. Bonnet D (2001) Normal and leukemic CD34-negative human hematopoietic stem cells. Rev Clin Exp Hematol 5:42-61
58. Nakamura Y, Ando K, Chargui J et al (1999) Ex vivo generation of CD34+ fromCD34- hematopoietic cells. Blood 94:4053-4058
59. Fujisaki T, Berger MG, Rose-John S, Eaves CJ (1999) Rapid differentiation of a rare subset of adult human Lin-CD34-CD38- cells stimulated by multiple growth factors. Blood 94:1926-1932
60. Karanu FN, Yuefei L, Gallacher L, Sakano S, Bhatia M (2003) Differential response of primitive human CD34- and CD34+ hematopoietic cells to the Notch ligand Jagged.1. Leukemia 17:1366-1374
61. Dao MA, Arevalo J, Nolta JA (2003) Reversibility of CD34 expression on human hematopoietic stem cells that retain the capacity for secondary reconstitution. Blood 101:112-118
62. Zanjani ED, Almeida-Porada G, Livingston AG, Zeng H, Ogawa M (2003) Reversible expression of CD34 by adult human bone marrow long-term engrafting hematopoietic stem cells. Exp Hematol 31:406-412
63. Glimm H, Eisterer W, Lee K, Cashman J, Holyoake TL, Nicolini F, Shultz LD, Von Kalle C, Eaves CJ (2001) Previously undetected human hematopoietic cell populations with short-term repopulating activity selectively engraft NOD/SCID-β2 microglobulin-null mice. J Clin Invest 107:199-206
64. Guenechea G, Gan O, Dorrell C, Dick JE (2001) Distinct classes of human stem cells that differ in proliferate and self-renewal potential. Nat Immunol 2:75-82
65. Papayannopoulos T, Nakamoto B (1993) Peripheralization of hematopoietic progenitors in primates treated with anti-VLA4 integrin. Proc Natl Acad Sci U S A 90:9374-9378
66. Prosper F, Stroncek D, McCarthy JB, Verfaillie CM (1998) Mobilization and homing of peripheral blood is related to reversible downregulation of alpha4-beta1 integrin and function. J Clin Invest 101:2456-2467
67. Zanjani ED, Flake AW, Almeida-Porada G, Tran N, Papayannopoulou T (1999) Homing of human cells in the fetal sheep model: modulation by antibodies activating or inhibiting very late activation antigen 4 dependent function. Blood 94:2515-2522
68. Peled A, Petit I, Kollet O, Magid M, Ponomaryov T, Byk T, Nagler A et al (1999) Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4. Science 283:845-848
69. Rosu-Myles, Gallacher L, Murdoch B, Hess DA, Keeney M, Kelvin D et al (2000) The human hematopoietic stem cell compartment is heterogeneous for CXCR4 expression. Proc Natl Acad Sci U S A 97:14626-14631
70. Srour EF, Jetmore A, Wolber FM, Plett PA, Abonour R, Yoder MC, Orschell-Traycoff CM (2001) Homing, cell cycle kinetics and fate of transplanted hematopoietic stem cells. Leukemia 15:1681-1684
71. Whetton AD, Graham GJ (1999) Homing mobilization in the stem cell niche. Trends Cell Biol 9:233-238
72. Nilsson SK, Dooner MS, Tianks CY, Weier HU, Quesenberry PJ (1997) Potential and distribution of transplanted hematopoietic stem cells in a non-ablated mouse model. Blood 89:4013-4020
73. Nilsson SK, Johnston HM, Coverdale JA (2001) Spatial localization of transplanted hematopoietic stem cells: interferences for the localization of stem cell niches. Blood 97:2293-2299
74. Lichtman MA (1981) The ultrastructure of hematopoietic environment of the marrow: a review. Exp Hematol 9:391-410
75. Weiss L (1976) The hematopoietic microenvironment of the bone marrow: an ultrastructural study of the stroma in rats. Anat Rec 186:161-184
76. Dexter TM, Allen TD, Lajtha LG (1977) Conditions controlling the proliferation of hematopoietic stem cells in vitro. J Cell Physiol 91:335-344
77. Friedenstein AJ, Chailakjan RK, Lalykina KS (1970) The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 3:393-403
78. Owen M, Fiedenstein AJ (1988) Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 136:42-60
79. Gronthos S, Simmons PJ (1996) The growth factor requirement of STRO-1 positive human bone marrow stromal precursors under serum-deprived conditions in vitro. Blood 85:929-940
80. Fernandez M, Simon V, Herrera G, Cao C, Del Favero H, Minguell JJ (1997) Detection of stromal cells in peripheral blood peripheral cell collections from breast cancer patients. Bone Marrow Transplant 20:265-271
81. Lazarus HM, Haynesworth SE, Gerson SL, Caplan AL (1997) Human bone marrow derived mesenchymal (stroaml) progenitor cells (MSC) cannot be recovered from peripheral blood progenitor cell collections. J Hematother 6:447-455
82. Erices A, Conget P, Minguell JJ (2000) Mesenchymal progenitor cells in human umbilical cord blood. Br J Hematol 109:235-242
83. Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, Hows JM (2003) Adult bone marrow is a rich source of human mesenchymal stem cells but umbilical cord blood and mobilized adult blood are not. Br J Hematol 121:368-374
84. Colter DC, Class R, DiGirolamo CM et al (2000) Rapid expansion of recycling stem cells in cultures of plastic adherent cells from human bone marrow. Proc Natl Acad Sci U S A 97:3213-3218
85. Zohar R, Sodek J, McCulloch CA (1997) Characterisation of stromal progenitor cells enriched by flow cytometry. Blood 90:3471-3481
86. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Dopuglas R, Mosca JD et al (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284:143-147
87. Tocci A, Forte L (2003) Mesenchymal stem cell: use and perspectives. Hematol J 4:92-96
88. Bianco P, Riminucci M, Gronthos S et al (2001) Bone marrow stromal stem cells: nature, biology and potential applications. Stem Cells 19:180-192
89. Sekiya I, Larson BL, Smith JR, Pochampally R, Cui JG, Prockop DJ (2002) Expansion of human adult stem cells from bone marrow: conditions that maximize these yields of early progenitors and evaluate their quality. Stem Cells 20:530-541
90. Gronthos S, Zannettino ACW, Hay SJ, Shi S, Graves SE, Kortesidi A, Simmons PJ (2003) Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 116:1827-1835
91. Azizi SA, Stokes D, Augelli BJ, DiGirolamao C, Prockop DJ (1998) Engraftment and migration of human bone marrow stromal cells implanted in the brains of albino rats-similarities to astrocytes grafts. Proc Natl Acad Sci U S A 95:3908-3913
92. Majumdar MK, Thiede MA, Haynesworth SE, Bruder SP, Gerson SL (2000) Human marrow-derived mesenchymal stem cells (MSCs) express hematopoietic cytokines and support long-term hematopoiesis when differentiated toward stromal and osteogenic lineages. J Hematother Stem Cell Res 9:841-848
93. Angelopoulou M, Novelli E, Grove JE, Rinder HM, Civin C, Cheng L, Krause DS (2003) Cotransplantation of human mesenchymal stem cells enhances human myelopoieisis and megakaryocytopoeisis in NOD/SCID mice. Exp Hematol 31:413-420
94. Jiang Y, Jahagirda BN, Reinhardt RL et al (2002) Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 418:41-49
95. Reyes M, Lund T, Lenvik T, Agular D, Koodie L, Verfaillie C (2001) Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 98:2615-2625
96. Schwartz RE, Reyes M, Koodie L, Jiang Y, Blackstad M, Lund T, Lenvik T, Johnson S, Hu WS, Verfaillie CM (2002) Multipotent adult progenitor cells from bone marrow differentiate into functional hepatocyte-like cells. J Clin Invest 109:1291-1302
97. Lemischka I (1999) The power of stem cells reconsidered? Proc Natl Acad Sci U S A 96:14193-14195
98. Orkin SH (2000) Stem cell alchemy. Nat Med 6:1212-1213
99. Blau HM, Brazelton TR, Weimann JM (2001) The evolving concept of stem cell: entity or function? Cell 105:829-841
100. Morrison SJ (2001) Stem cell potential: can anything make anything? Curr Biol 11:R7-R9
101. Anderson DJ, Gage FH, Weissman IL (2001) Can stem cells cross boundaries? Nat Med 7:393-395
102. Lagasse E, Shizuru JA, Uchida N, Tsukamoto A, Weissman IL (2001) Toward regenerative medicine. Immunity 14:425-436
103. Wulf GG, Jackson KA, Goodell MA (2001) Somatic stem cell plasticity: current evidence and emerging concepts. Exp Hematol 29:1361-1370
104. Theise ND, Nimmakayalu M, Gardner R et al (2000) Liver from marrow in humans. Hepatocyte 32:11-16
105. Alison MR, Poulsom R, Jeffery R et al (2000) Hepatocytes from non-hepatic adult stem cells. Nature 406:257
106. Kleeberger W, Rothamel T, Glocckner S, Flemming P, Lehmann U, Kreipe H (2002) High frequency of epithelial chimerisms in liver transplants demonstrated by microdissection and STR-analysis. Hepatology 35:110-116
107. Brittan M, Hunt T, Jefferey R et al (2001) Bone marrow derivation of pericryptal myofibroblasts in the mouse and human small intestine and colon. Gut 50:752-757
108. Caplice NM, Bunch TJ, Stalboerger PG, Wang S, Simper D, Miller DV, Russell ST, Litzow MR, Edwards WD (2003) Smooth muscle cells in human coronary artherosclerosis can originate from cells administrated at marrow transplantation. Proc Natl Acad Sci U S A 100:4754-4759
109. Poulsom R, Forbes SJ, Hodivala-Dilke K et al (2001) Bone marrow contributes to renal parenchymal turnover and regeneration. J Pathol 195:229-235
110. Grimm PC, Nickerson P, Jeffery J et al (2001) Neointimal and tubulointestitial infiltration by recipient mesenchymal cells in chronic renal-allograft rejection. N Engl J Med 345:93-97
111. Weimann JM, Charlton CA, Brazelton TR, Hackman RC, Blau HM (2003) Contribution of transplanted bone marrow to Purkinje neurons in human adult brains. Proc Natl Acad Sci U S A 100:2088-2093
112. Gussoni E, Bennett RR, Muskiewicz KR, Meyerrose T, Nolta JA, Gilgoff I, Stein J, Chan YM, Lidov HG, Bonnemann CG, Von Moers A, Morris GE, Den Dunnen JT, Chamberlain JS, Kunkel LM, Weinberg K (2002) Long-term persistence of donor nuclei in a Duchenne muscular dystrophy patient receiving bone marrow transplantation. J Clin Invest 110:807-814
113. Kopen G, Prockop DJ, Phinney D (1999) Marrow stromal cells migrate though out the forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse. Proc Natl Acad Sci U S A 96:10711-10716
114. Liechty K, MacKenzie T, Shaaban A et al (2000) Human mesenchymal stem cells engraft and demonstrate site-specific differentiation after in utero transplantation in sheep. Nat Med 6:1282-1286
115. De Bari C, Dell'Accio F, Vandenabeele F, Vermeesch JR, Raymackers JM, Lyuten FP (2003) Skeletal muscle repair by adult human mesenchymal stem cells from synovial membrane. J Cell Biol 160:909-918
116. Zhao LR, Duan WM, Reyes M, Verfaillie CM, Low WC (2003) Immunohistochemical identification of multipotent adult progenitor cells from human bone marrow after transplantation into the rat brain. Brain Res Brain Res Protoc 11:38-45
117. Zhao LR, Duan WM, Reyes M, Keene CD, Verfaillie CM, Low WC (2002) Human bone marrow stem cells exhibit neural phenotypes and ameliorate neurological deficits after grafting into the ischemic brain of rats. Exp Neurol 174:11-20
118. Danet G, Luongo JL, Butler G, Lu MM, Tenner AJ, Simon MC, Bonnet D (2002) C1qRp defines a new human stem cell population with hematopoietic and hepatic potential. Proc Natl Acad Sci U S A 99:10441-10445
119. Newsome PN, Johannsessen I, Boyle S, dalakas E, McAulay K, Samuel K, Rae F, Forrester L, Turner ML, Hayes PC, Harrisson DJ, Bickmore WA, Plevris JN (2003) Human cord-blood derived cells differentiate into hepatocytes in the mouse liver with no evidenced of cellular fusion. Gastroenterology 124:1891-1900
120. Ishkawa F, Drake CJ, Yang S, Fleming PA, Minamiguchi H, Visconti RP, Crosby CV, Argraves WS, Harada M, Lyndon Key L, Livingston AG, Wingard JR, Ogawa M (2003) Transplanted human cord blood cells give rises to hepatocytes in engrafted mice. Ann N Y Acad Sci 996:174-185
121. Wang X, Ge S, McNamara G, Hao QL, Crooks GM, Nolta JA (2003) Albumin-expressing hepatocyte-like cells develop in the livers of immune-deficient mice that received transplants of highly purified human hematopoietic stem cells. Blood 101:4201-4208
122. Krause DS, Theise ND, Collector MI et al (2001) Multi-organ, multi-lineage engraftment by a single bone marrow-derived stem cell. Cell 105:369-377