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Blood, Vol. 94 No. 8 (October 15), 1999:
pp. 2548-2554
Reversible Expression of CD34 by Murine Hematopoietic Stem Cells
By
Takashi Sato,
Joseph H. Laver, and
Makio Ogawa
From the Departments of Pediatrics and Medicine, Medical University
of South Carolina, and Department of Veterans Affairs Medical Center,
Charleston, SC.
 |
ABSTRACT |
We used a mouse transplantation model to address the recent
controversy about CD34 expression by hematopoietic stem cells. Cells
from Ly-5.1 C57BL/6 mice were used as donor cells and Ly-5.2 mice were
the recipients. The test cells were transplanted together with
compromised marrow cells of Ly-5.2 mice. First, we confirmed that the
majority of the stem cells with long-term engraftment capabilities of
normal adult mice are CD34 . We then observed that, after
the injection of 150 mg/kg 5-fluorouracil (5-FU), stem cells may be
found in both CD34 and CD34+ cell
populations. These results indicated that activated stem cells express
CD34. We tested this hypothesis also by using in vitro expansion with
interleukin-11 and steel factor of lineage
c-kit+ Sca-1+ CD34 bone
marrow cells of normal mice. When the cells expanded for 1 week were
separated into CD34 and CD34+ cell
populations and tested for their engraftment capabilities, only
CD34+ cells were capable of 2 to 5 months of engraftment.
Finally, we tested reversion of CD34+ stem cells to
CD34 state. We transplanted Ly-5.1 CD34+
post-5-FU marrow cells into Ly-5.2 primary recipients and, after the
marrow achieved steady state, tested the Ly-5.1 cells of the primary
recipients for their engraftment capabilities in Ly-5.2 secondary
recipients. The majority of the Ly-5.1 stem cells with long-term
engraftment capability were in the CD34 cell fraction,
indicating the reversion of CD34+ to CD34
stem cells. These observations clearly demonstrated that CD34 expression reflects the activation state of hematopoietic stem cells
and that this is reversible.
© 1999 by The American Society of Hematology.
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INTRODUCTION |
AFTER THE SUCCESSFUL hematopoietic
reconstitution of baboons with selected CD34+ baboon bone
marrow cells by Berenson et al,1 CD34 expression became the
hallmark of murine and human hematopoietic stem cells. A number of
clinical trials of transplantation of CD34+ human bone
marrow and peripheral blood stem cells have documented cases of
successful long-term engraftment.2-5 However, this dogma was recently challenged on several fronts. First, Osawa et
al6 reported that mouse marrow long-term reconstituting
cells are in the lineage (Lin) c-kit+
Ly-6A/E (Sca-1)+ CD34/low cell
population rather than CD34+ cells. Subsequently, Morel et
al7 confirmed that CD34 cells contain a
significant number of stem cells. Independently from these
observations, studies performed by Goodell et al8,9 also
raised serious questions about CD34 expression by hematopoietic stem
cells. They first reported that murine bone marrow stem cells are
highly enriched in a cell population defined by Hoechst 33342 dye as
side population (SP).8 They subsequently reported that human and rhesus bone marrow SP cells are largely
CD34/low and that, after 5 weeks of suspension
culture on bone marrow stromal cells, the rhesus and human
CD34 SP cells became CD34+.9
In our laboratory, we have shown previously that the CD34+
c-kitlow human bone marrow cells can engraft in sheep bone
marrow for more than 1.5 years.10 Subsequently, we found
that some human long-term engrafting cells reside also in the
CD34 population.11
To solve the apparent controversy, we entertained the hypothesis that
CD34 expression reflects activation and/or cycling state of stem cells
and tested this hypothesis using a murine transplantation model. We
used Lin c-kit+ Sca-1+ bone
marrow cells harvested from normal mice and mice that had been injected
with 150 mg/kg 5-fluorouracil (5-FU) 2 days before bone marrow harvest.
Stem cells in the latter model have been shown to be in active cell
division after 5-FU-induced marrow hypoplasia.12
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MATERIALS AND METHODS |
Monoclonal antibodies (MoAbs) and hybridomas.
Fluorescein isothiocyanate (FITC)-conjugated RAM34 (anti-CD34; rat
IgG2a), phycoerythrin (PE)-conjugated D7 (anti-Ly-6A/E [anti-Sca-1]; rat IgG2a), allophycocyanin (APC)-conjugated 2B8 (anti-c-kit; rat IgG2b), biotin-conjugated A20 (anti-Ly-5.1; rat IgG2a), biotin-conjugated 53-2.1 (anti-Thy-1.2; rat IgG2a),
biotin-conjugated RA3-6B2 (anti-CD45R/B220; rat IgG2a),
biotin-conjugated RB6-8C5 (anti-Gr-1; rat IgG2b), and
biotin-conjugated M1/70 (anti-Mac-1; rat IgG2b) were purchased from
Pharmingen (San Diego, CA). Some antibodies were also received as
either nonlabeled antibodies or hybridomas. Purified antibodies were
conjugated to FITC or to biotin in our laboratory. MoAb ACK4
(anti-c-kit; rat IgG2a) was provided by S.I. Nishikawa (Kyoto
University, Kyoto, Japan). Hybridoma RB6-8C5 (anti-Gr-1; rat IgG2b)
was provided by R.L. Coffman (DNAX, Palo Alto, CA). MoAb TER-119
(anti-erythrocytes; rat IgG2b) was a gift from T. Kina (Kyoto
University). Hybridomas 14.8 (anti-B220; rat IgG2b), M1/70.15.11.5
(anti-Mac-1; rat IgG2b), GK1.5 (anti-CD4; rat IgG2b), and 53-6.72 (anti-CD8; rat IgG2a) were purchased from American Type Culture
Collection (Rockville, MD). Hybridoma A20 (anti-Ly-5.1; IgG1) was
provided by H. Fleming (Emory University, Atlanta, GA).
Cell preparation.
Ten- to 12-week-old male C57BL/6-Ly-5.1 mice (Jackson Laboratories, Bar
Harbor, ME) were used as bone marrow donors. Ten- to 14-week-old female
C57BL/6-Ly-5.2 mice (Charles River Laboratories, Raleigh, NC) were used
as irradiated recipients and as the source of compromised bone marrow
cells.13 In some experiments, the donor mice were treated
with an intravenous injection of 5-FU at 150 mg/kg body weight 48 hours
before death. Bone marrow cells were flushed from femurs and tibiae,
pooled, washed twice with phosphate-buffered saline (PBS) containing
0.1% bovine serum albumin (BSA), made into single-cell suspension by
repeated pipetting, and filtered through 40-µm nylon mesh. The cells
with densities ranging from 1.063 to 1.077 g/mL were collected by
gradient separation using Nycodenz (Accurate Chemical and Scientific
Corp, Westbury, NY). Cells reacting to anti-Mac-1, anti-Gr-1,
anti-B220, anti-CD4, anti-CD8, and TER-119 were removed by using 2 depletions with immunomagnetic beads (Dynabeads M-450 coupled to sheep
antirat IgG; DYNAL, Great Neck, NY). For fluorescence-activated cell
sorting (FACS), the resulting Lin cells were stained
with FITC-conjugated anti-CD34 (RAM34), PE-conjugated anti-Sca-1, and
biotin-conjugated anti-c-kit. Cells were further stained with
streptavidin-conjugated APC (Caltag Laboratories, San Francisco, CA).
After the addition of propidium iodide (PI) at a concentration of 1 µg/mL, the cells were washed twice, resuspended in PBS containing
0.1% BSA, and kept on ice until cell sorting. In the serial
transplantation experiments, cells were stained with FITC-conjugated
anti-CD34, PE-conjugated anti-Sca-1, APC-conjugated anti-c-kit, and
biotin-conjugated anti-Ly-5.1. Subsequently, the cells were washed
twice and stained with streptavidin-conjugated Red 613 (Life
Technologies, Gaithersburg, MD). PI staining was omitted, because its
emmision wavelength is similar to that of Red 613. Cell sorting was
performed on FACS Vantage (Becton Dickinson, San Jose, CA), with
appropriate isotype-matched controls. The bone marrow cells were first
enriched for c-kit+, Sca-1+ cells and then the
cells were sorted again based on CD34 expression.
Suspension culture.
Five thousand Lin c-kit+
Sca-1+ CD34 cells were stained with
PKH26 (Sigma Immunochemicals, St Louis, MO)14,15 and
incubated in a 25-cm2 culture flask. The culture medium
contained  -modification of Eagle's medium (MEM; ICN Biomedicals,
Aurora, OH), 20% fetal calf serum, 1% deionized fraction V BSA, 1 × 104 mol/L 2-mercaptoethanol, recombinant
steel factor (SF; c-kit ligand), and interleukin-11 (IL-11). SF was
purchased from R&D Systems (Minneapolis, MN) and used at a
concentration of 100 ng/mL. Human IL-11 (a gift from P. Schendel,
Genetics Institute, Cambridge, MA) was used at a concentration of 100 ng/mL. After 1 week of incubation, the cells were washed twice and
stained with FITC-conjugated anti-CD34 and were sorted into
CD34 and CD34+ fractions.
Hematopoietic reconstitution.
Ly-5.2 mice were administrated with a single 850-cGy dose of total body
irradiation using 4 × 106 V linear accelerator. The
FACS-sorted cells from donor (Ly-5.1) mice or cultured cells were
injected into the tail vein of the irradiated Ly-5.2 mice along with 4 × 105 compromised Ly-5.2 marrow cells. Compromised
marrow cells had been subjected to 2 previous rounds of transplantation
and regeneration.13 Peripheral blood was obtained from the
retro-orbital plexus using heparin-coated micropipets (Drummond
Scientific Co, Broomall, PA) 2, 5, and/or 8 months after
transplantation. Red blood cells were lysed by 0.15 mol/L
NH4Cl. The samples were stained with FITC-conjugated
anti-Ly-5.1 and analyzed for donor-derived cells on FACS Vantage.
Donor cells in T-cell, B-cell, granulocyte, and monocyte/macrophage
lineages at 5 months posttransplantation were analyzed by staining with
biotin-conjugated anti-Thy-1.2, biotin-conjugated anti-B220,
biotin-conjugated anti-Gr-1, and biotin-conjugated anti-Mac-1,
followed by staining with streptavidin-conjugated PE.
Retransplantation.
Mice that had been transplanted with Lin
c-kit+ Sca-1+ CD34+ cells of
5-FU-treated mice were killed 3 months after transplantation. Ly-5.1
Lin c-kit+ Sca-1+
CD34 cells and Ly-5.1 Lin
c-kit+ Sca-1+ CD34+ cells were
prepared from the marrow of these mice and were injected into secondary
Ly-5.2 recipients along with 5 × 104 Ly-5.2
compromised cells. Peripheral blood was analyzed for Ly-5.1 cells 2 and
5 months after the secondary transplantation.
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RESULTS |
Transplantation of CD34 and CD34+ cells
of normal mice.
We isolated CD34 and CD34+ cells from
the c-kit+ Sca-1+ population of both normal and
post-5-FU bone marrow using the FACS regions shown in
Fig 1. In
Fig 2, we present the result of
reanalysis of the sorted CD34+ and CD34
cells of normal mice that showed greater than 99% purity. Because the
ratio of the Lin c-kit+
Sca-1+ CD34 (R2) cells to
Lin c-kit+ Sca-1+
CD34+ (R3) cells was 1:5, we transplanted 100 CD34 cells or 500 CD34+ cells. The level
of engraftment was determined by measuring the percentage of donor
(Ly-5.1) peripheral blood nucleated cells at 2 and 5 months after
transplantation. The results are presented in
Fig 3. The average engraftment levels of
the 8 mice transplanted with 100 CD34 cells was
26.5% ± 20.4% at 2 months and 34.7% ± 33.5% at 5 months posttransplantation. Only 1 of 8 mice transplanted with 500 CD34+ (R3) cells engrafted at the levels of 2.8% and
1.8%, respectively, at 2 and 5 months. The remaining 7 mice and the 5 mice receiving only compromised marrow cells showed no Ly-5.1 cells.
Similar results were obtained in 2 additional experiments. These
results were in agreement with the premise that CD34
cells of normal mice were capable of long-term
engraftment.6,7
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| Fig 1.
FACS sorting regions used for preparation of
c-kit+ Sca-1+ CD34 and
c-kit+ Sca-1+ CD34+ cell
populations. Lin+ cells had been removed from mononuclear
marrow cells by using immunomagnetic beads before staining for FACS
sorting. The Lin cells were enriched for
c-kit+ Sca-1+ cells using the R1 and R4
windows and again sorted on the basis of CD34 expression using R2, R3,
R5, and R6 windows.
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| Fig 3.
Percentage of donor nucleated cells in the blood of
individual mice transplanted with 100 Lin
c-kit+ Sca-1+ CD34 or 500 Lin c-kit+ Sca-1+
CD34+ marrow cells of normal mice. ( ) 2 months
posttransplantation; ( ) 5 months posttransplantation.
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Transplantation of CD34 and CD34+
cells of 5-FU-treated mice.
Because the ratio of the CD34 (Fig 1, R5) to
CD34+ (Fig 1, R6) cell populations in the bone marrow cells
of 5-FU-treated mice was roughly 1:1, we transplanted 100 CD34 or 100 CD34+ cells per mouse for
measurement of engraftment capability. In contrast to the cells from
normal mice, both CD34 and CD34+ cells
engrafted (Fig 4). The average levels of
engraftment were 47% ± 16.0% (N = 10) and 62.8% ± 14.6% (N = 10) at 2 months posttransplantation, 64.4% ± 21.9% (N = 10) and
67.8% ± 13.9% (N = 10) at 5 months posttransplantation and 64.3% ± 23.7% (N = 10) and 59.7% ± 23.1% (N = 9) at 8 months
posttransplantation for CD34 cells and
CD34+ cells, respectively. All mice showed evidence for
multilineage engraftment at 8 months posttransplantation. An example of
engraftment by CD34+ post-5-FU cells is shown in
Fig 5. A similar result was obtained in an
additional experiment.
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| Fig 4.
Percentage of donor nucleated cells in the blood of
individual mice transplanted with 100 Lin
c-kit+ Sca-1+ CD34 or 100 Lin c-kit+ Sca-1+
CD34+ marrow cells of 5-FU-treated mice. () 2 months
posttransplantation; () 5 months posttransplantation; ( ) 8 months
posttransplantation.
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| Fig 5.
An example of multilineage hematopoietic engraftment at 8 months posttransplantation by Lin c-kit+
Sca-1+ CD34+ marrow cells of 5-FU-treated
mice.
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Conversion of CD34 to CD34+ stem cells
in culture.
The results listed above strongly suggested that changes in the
activation and/or cycling state of the bone marrow are the cause for
the phenotypic changes of the stem cells. We wished to further test
this premise by using cell culture. Both CD34+ and
CD34 populations of Lin
c-kit+ Sca-1+ cells of normal mice were
incubated in suspension culture for 1 week in the presence of SF and
IL-11. The CD34+ cell populations expanded 4,000-fold. The
CD34 cells expanded from 5,000 to 5 × 106 (1,000-fold) and 75% of the cultured cells became
CD34+, as shown in Fig 6.
Simultaneous staining with PKH26, which binds to membrane lipid,
confirmed the divisional history of the cultured cells. All cells that
were PKHbright before incubation became PKHdull
after the suspension culture (Fig 6), indicating that all cells divided
several times. Because the ratio of CD34 (R7) to
CD34+ (R8) cells was 1:3 after incubation, we transplanted
either 5 × 104 CD34 cells or 1.5 × 105 CD34+ cells to each recipient. The
results of transplantation are shown in Fig
7. The levels of engraftment at 2 and 5 months after transplantation of
the cultured CD34+ cells were 58.8% ± 13.3% (N = 10)
and 60.1% ± 19.2% (N = 10), respectively. In contrast, the levels
in the mice transplanted with cultured CD34 cells
were 0.4% ± 0.5% (N = 10) at 2 months and 0.3% ± 0.4% (N = 10) at 5 months. These results clearly demonstrated that
CD34 stem cells that are stimulated in culture
undergo phenotypic changes and express CD34.
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| Fig 6.
Flow cytometric analysis of CD34 expression before and
after culture. Sorted Lin c-kit+
Sca-1+ CD34 cells were stained with PKH26
and analyzed before culture (left). After 1 week of incubation with SF
and IL-11, cells were analyzed for CD34 expression and PKH26
fluorescence (right). Dotted and solid lines represent cells stained
with IgG2a-FITC and CD34-FITC, respectively.
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| Fig 7.
Percentage of donor nucleated cells in the blood of
individual mice transplanted with 5 × 104
CD34 cultured cells or 1.5 × 105
CD34+ cultured cells. () 2 months posttransplantation;
() 5 months posttransplantation.
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Reversion of CD34+ stem cells to CD34.
The results in the 2 studies of stem cell activation were concordant
and strongly indicated that CD34 expression reflects the activation
and/or cycling state of stem cells. In the next experiment, we tested
the hypothesis that activated CD34+ stem cells revert to
CD34 stem cells when the bone marrow attains a
steady state. We transplanted Lin c-kit+
Sca-1+ CD34+ cells from the bone marrow of
Ly-5.1 5-FU-treated mice into 10 Ly-5.2 primary recipients. Three
months later, 61.5% of the Lin marrow cells of the
primary recipients were of donor-origin (Ly-5.1; Fig 8A). The donor origin Ly-5.1 cells were
then isolated from the primary recipients and separated on the basis of
CD34 expression (Fig 8B). Each population was transplanted into
secondary Ly-5.2 hosts for analysis of engraftment capabilities.
Because the ratio of CD34 (R9) to CD34+
(R10) cells was 1:5, individual mice received either 1,000 CD34 or 5,000 CD34+ cells. The results
are presented in Fig 9. The levels of
engraftment at 2 and 5 months posttransplantation by
CD34 Ly-5.1 cells were 25.0% ± 13.3% (N = 6)
and 27.3% ± 23.2% (N = 6), respectively. Those by
CD34+ Ly-5.1 cells at 2 and 5 months posttransplantation
were 0.98% ± 0.97% (N = 7) and 0.63% ± 0.65% (N = 7),
respectively. These results clearly demonstrated that, when bone marrow
recovers from the radiation-induced hypoplasia and reaches steady
state, CD34 expression of the cells is downregulated to undetectable
levels.
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| Fig 8.
Analysis of Lin marrow cells from primary
recipients transplanted with CD34+ cells. (A) Dotted and
solid lines represent cells stained with isotype-matched Ig and
Ly-5.1-specific antibody. Sixty-five percent of the Lin
marrow cells of the primary recipients were donor-derived (Ly-5.1)
cells. (B) Sorting windows of Ly-5.1+ Lin
c-kit+ Sca-1+ cells. The ratio of the cells
in R9 to R10 was 1:5.
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| Fig 9.
Percentage of donor (Ly-5.1) cells in the blood of
individual secondary recipients. Ly-5.1 Lin
c-kit+ Sca-1+ CD34+
post-5-FU marrow cells were transplanted to Ly-5.2 primary recipients.
Three months later, 1,000 Ly-5.1 CD34 bone marrow cells
or 5,000 Ly-5.1 CD34+ bone marrow cells of the primary
recipients were transplanted to individual secondary Ly-5.2 recipients.
() 2 months posttransplantation; () 5 months
posttransplantation.
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| |
DISCUSSION |
In this project, we used Lin c-kit+
Sca-1+ cells because these cells in both normal C57BL
mice6 and 5-FU-treated C57BL/6 mice12 are
highly enriched for stem cells. Injection of a single Lin c-kit+ Sca-1+
CD34 cell from normal mice produced sustained
high-level engraftment in an irradiated recipient for 10 months 21% of
the time.6 In our laboratory, we repeatedly observed that
100 Lin c-kit+ Sca-1+ marrow
cells from 5-FU-treated mice can provide high levels of long-term
engraftment of lethally irradiated mice.15-17
We observed clear-cut association between CD34 expression and the
activation state of stem cells with long-term reconstitution capabilities. The majority of stem cells in the bone marrow of normal
adult mice were CD34, as reported by Osawa et
al.6 In vivo and in vitro activation of stem cells was
associated with expression of CD34, and the activated CD34+
stem cells reverted to CD34 state as bone marrow
attained stationary phase. Because mouse hematopoiesis has been an
excellent model for human hematopoiesis, the observations presented in
this report may have important clinical implications. It is possible
that, in patients who receive chemoradiotherapy for their malignancies,
stem cell CD34 expression may vary depending on the recovery state of
the bone marrow. If so, the timing of autologous transplantation using
selected CD34+ cells needs to be carefully considered.
Yoder et al18 reported that murine hematopoietic stem cells
in the day-9 yolk sac and those in the day-12 to -14 fetal liver are
CD34+. Morel et al,7 when studying 4- to
6-week-old mice, reported that both CD34 and
CD34+ cell populations contain stem cells. It will be of
interest to study whether the developmental changes in the CD34
expression are related to the kinetic state of the stem cells. Although
we have shown association between activation state and CD34 expression of stem cells, we did not address the cause-and-result relationship between cell cycling state and CD34 expression of the stem cells. However, Randall and Weissman12 have shown an
association between post-5-FU phenotypic changes and the
activation/cell cycle state of the stem cells. In this regard, it will
be of particular interest to study granulocyte colony-stimulating
factor (G-CSF)-mobilized peripheral blood stem cells, because these
cells have been shown to reside in G0/G1 state,
despite stimulation by G-CSF.19
| |
ACKNOWLEDGMENT |
The authors thank Dr Haiqun Zeng for assistance in FACS sorting, Dr
Pamela N. Pharr and Anne G. Livingston for assistance in preparation of
this manuscript, and the staff of Radiation Oncology Department of the
Medical University of South Carolina for assistance in irradiation of mice.
| |
FOOTNOTES |
Submitted April 1, 1999; accepted June 15, 1999.
Supported by National Institutes of Health Grants No. RO1-DK32294,
RO1-DK/HL 48714, and PO1-CA78582 and by the Office of Research and
Development, Medical Research Services, Department of Veterans Affairs.
The publication costs of this
article were defrayed in part by
page charge payment. This article
must therefore be hereby marked
"advertisement"
in accordance with 18 U.S.C. section
1734 solely to indicate this fact.
Address reprint requests to Makio Ogawa, MD, PhD, Ralph H. Johnson VA
Medical Center, 109 Bee St, Charleston, SC 29401-5799; e-mail:
ogawam{at}musc.edu.
| |
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T. Yokota, K. Oritani, S. Butz, K. Kokame, P. W. Kincade, T. Miyata, D. Vestweber, and Y. Kanakura
The endothelial antigen ESAM marks primitive hematopoietic progenitors throughout life in mice
Blood,
March 26, 2009;
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[Abstract]
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I. Roeder, K. Horn, H.-B. Sieburg, R. Cho, C. Muller-Sieburg, and M. Loeffler
Characterization and quantification of clonal heterogeneity among hematopoietic stem cells: a model-based approach
Blood,
December 15, 2008;
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S. Knaan-Shanzer, I. van der Velde-van Dijke, M. J.M. van de Watering, P. J. de Leeuw, D. Valerio, D. W. van Bekkum, and A. A.F. de Vries
Phenotypic and Functional Reversal Within the Early Human Hematopoietic Compartment
Stem Cells,
December 1, 2008;
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J. S. Nielsen and K. M. McNagny
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M. Jaksch, J. Munera, R. Bajpai, A. Terskikh, and R. G. Oshima
Cell Cycle-Dependent Variation of a CD133 Epitope in Human Embryonic Stem Cell, Colon Cancer, and Melanoma Cell Lines
Cancer Res.,
October 1, 2008;
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[Abstract]
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R. H. Cho, H. B. Sieburg, and C. E. Muller-Sieburg
A new mechanism for the aging of hematopoietic stem cells: aging changes the clonal composition of the stem cell compartment but not individual stem cells
Blood,
June 15, 2008;
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M. B. Bowie, D. G. Kent, M. R. Copley, and C. J. Eaves
Steel factor responsiveness regulates the high self-renewal phenotype of fetal hematopoietic stem cells
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[Abstract]
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R. Pelayo, K. Miyazaki, J. Huang, K. P. Garrett, D. G. Osmond, and P. W. Kincade
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[Abstract]
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D. A. Santillan, C. M. Theisler, A. S. Ryan, R. Popovic, T. Stuart, M.-M. Zhou, S. Alkan, and N. J. Zeleznik-Le
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Cancer Res.,
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[Abstract]
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J. M. Nygren, D. Bryder, and S. E. W. Jacobsen
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July 1, 2006;
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B. Dykstra, J. Ramunas, D. Kent, L. McCaffrey, E. Szumsky, L. Kelly, K. Farn, A. Blaylock, C. Eaves, and E. Jervis
High-resolution video monitoring of hematopoietic stem cells cultured in single-cell arrays identifies new features of self-renewal
PNAS,
May 23, 2006;
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S. Massberg, I. Konrad, K. Schurzinger, M. Lorenz, S. Schneider, D. Zohlnhoefer, K. Hoppe, M. Schiemann, E. Kennerknecht, S. Sauer, et al.
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R. P. Visconti, Y. Ebihara, A. C. LaRue, P. A. Fleming, T. C. McQuinn, M. Masuya, H. Minamiguchi, R. R. Markwald, M. Ogawa, and C. J. Drake
An In Vivo Analysis of Hematopoietic Stem Cell Potential: Hematopoietic Origin of Cardiac Valve Interstitial Cells
Circ. Res.,
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H. B. Sieburg, R. H. Cho, B. Dykstra, N. Uchida, C. J. Eaves, and C. E. Muller-Sieburg
The hematopoietic stem compartment consists of a limited number of discrete stem cell subsets
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D. A. Hess, L. Wirthlin, T. P. Craft, P. E. Herrbrich, S. A. Hohm, R. Lahey, W. C. Eades, M. H. Creer, and J. A. Nolta
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R. Gupta, S. Karpatkin, and R. S. Basch
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H. K. Haider and M. Ashraf
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C. C. Zhang and H. F. Lodish
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The Kinetic Status of Hematopoietic Stem Cell Subpopulations Underlies a Differential Expression of Genes Involved in Self-Renewal, Commitment, and Engraftment
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D. A. Hess, T. E. Meyerrose, L. Wirthlin, T. P. Craft, P. E. Herrbrich, M. H. Creer, and J. A. Nolta
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D. C. Dooley, B. K. Oppenlander, and M. Xiao
Analysis of Primitive CD34- and CD34+ Hematopoietic Cells from Adults: Gain and Loss of CD34 Antigen by Undifferentiated Cells Are Closely Linked to Proliferative Status in Culture
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P. A. Dreyfus, F. Chretien, B. Chazaud, Y. Kirova, P. Caramelle, L. Garcia, G. Butler-Browne, and R. K. Gherardi
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S. Sergejeva, A.-K. Johansson, C. Malmhall, and J. Lotvall
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N. Forraz, R. Pettengell, and C. P. McGuckin
Characterization of a Lineage-Negative Stem-Progenitor Cell Population Optimized for Ex Vivo Expansion and Enriched for LTC-IC
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J. Larsson, U. Blank, H. Helgadottir, J. M. Bjornsson, M. Ehinger, M.-J. Goumans, X. Fan, P. Leveen, and S. Karlsson
TGF-{beta} signaling-deficient hematopoietic stem cells have normal self-renewal and regenerative ability in vivo despite increased proliferative capacity in vitro
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S. Rutella, G. Bonanno, M. Marone, D. de Ritis, A. Mariotti, M. T. Voso, G. Scambia, S. Mancuso, G. Leone, and L. Pierelli
Identification of a Novel Subpopulation of Human Cord Blood CD34-CD133-CD7-CD45+Lineage- Cells Capable of Lymphoid/NK Cell Differentiation After In Vitro Exposure to IL-15
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N. Ferrari, G. L. Palmisano, L. Paleari, G. Basso, M. Mangioni, V. Fidanza, A. Albini, C. M. Croce, G. Levi, and C. Brigati
DLX genes as targets of ALL-1: DLX 2,3,4 down-regulation in t(4;11) acute lymphoblastic leukemias
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J.-F. Lambert, M. Liu, G. A. Colvin, M. Dooner, C. I. McAuliffe, P. S. Becker, B. G. Forget, S. M. Weissman, and P. J. Quesenberry
Marrow Stem Cells Shift Gene Expression and Engraftment Phenotype with Cell Cycle Transit
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J. Wang, T. Kimura, R. Asada, S. Harada, S. Yokota, Y. Kawamoto, Y. Fujimura, T. Tsuji, S. Ikehara, and Y. Sonoda
SCID-repopulating cell activity of human cord blood-derived CD34- cells assured by intra-bone marrow injection
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M. Masuya, C. J. Drake, P. A. Fleming, C. M. Reilly, H. Zeng, W. D. Hill, A. Martin-Studdard, D. C. Hess, and M. Ogawa
Hematopoietic origin of glomerular mesangial cells
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M. T. Mitjavila-Garcia, M. Cailleret, I. Godin, M. M. Nogueira, K. Cohen-Solal, V. Schiavon, Y. Lecluse, F. Le Pesteur, A. H. Lagrue, and W. Vainchenker
Expression of CD41 on hematopoietic progenitors derived from embryonic hematopoietic cells
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K. Yasui, K. Matsumoto, F. Hirayama, Y. Tani, and T. Nakano
Differences Between Peripheral Blood and Cord Blood in the Kinetics of Lineage-Restricted Hematopoietic Cells: Implications for Delayed Platelet Recovery Following Cord Blood Transplantation
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H. K. A. Mikkola, Y. Fujiwara, T. M. Schlaeger, D. Traver, and S. H. Orkin
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Y. Guo, M. Lubbert, and M. Engelhardt
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M. A. Dao, J. Arevalo, and J. A. Nolta
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The human hematopoietic stem cell compartment is heterogeneous for CXCR4 expression
PNAS,
December 19, 2000;
97(26):
14626 - 14631.
[Abstract]
[Full Text]
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J. R. Beauchamp, L. Heslop, D. S.W. Yu, S. Tajbakhsh, R. G. Kelly, A. Wernig, M. E. Buckingham, T. A. Partridge, and P. S. Zammit
Expression of CD34 and Myf5 Defines the Majority of Quiescent Adult Skeletal Muscle Satellite Cells
J. Cell Biol.,
December 11, 2000;
151(6):
1221 - 1234.
[Abstract]
[Full Text]
[PDF]
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J. Domen and I. L. Weissman
Hematopoietic Stem Cells Need Two Signals to Prevent Apoptosis; BCL-2 Can Provide One of These, Kitl/c-Kit Signaling the Other
J. Exp. Med.,
December 11, 2000;
192(12):
1707 - 1718.
[Abstract]
[Full Text]
[PDF]
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J. H. S. Kabarowski and O. N. Witte
Consequences of BCR-ABL Expression within the Hematopoietic Stem Cell in Chronic Myeloid Leukemia
Stem Cells,
November 1, 2000;
18(6):
399 - 408.
[Abstract]
[Full Text]
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Y. Zhao, Y. Lin, Y. Zhan, G. Yang, J. Louie, D. E. Harrison, and W. F. Anderson
Murine hematopoietic stem cell characterization and its regulation in BM transplantation
Blood,
November 1, 2000;
96(9):
3016 - 3022.
[Abstract]
[Full Text]
[PDF]
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R. W. Storms, M. A. Goodell, A. Fisher, R. C. Mulligan, and C. Smith
Hoechst dye efflux reveals a novel CD7+CD34- lymphoid progenitor in human umbilical cord blood
Blood,
September 15, 2000;
96(6):
2125 - 2133.
[Abstract]
[Full Text]
[PDF]
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J. Y. Lee, Z. Qu-Petersen, B. Cao, S. Kimura, R. Jankowski, J. Cummins, A. Usas, C. Gates, P. Robbins, A. Wernig, et al.
Clonal Isolation of Muscle-derived Cells Capable of Enhancing Muscle Regeneration and Bone Healing
J. Cell Biol.,
September 5, 2000;
150(5):
1085 - 1100.
[Abstract]
[Full Text]
[PDF]
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M. Rosu-Myles, M. Khandaker, D.M. Wu, M. Keeney, S.R. Foley, K. Howson-Jan, I. C. Yee, F. Fellows, D. Kelvin, and M. Bhatia
Characterization of Chemokine Receptors Expressed in Primitive Blood Cells During Human Hematopoietic Ontogeny
Stem Cells,
September 1, 2000;
18(5):
374 - 381.
[Abstract]
[Full Text]
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F. Tajima, T. Sato, J. H. Laver, and M. Ogawa
CD34 expression by murine hematopoietic stem cells mobilized by granulocyte colony-stimulating factor
Blood,
September 1, 2000;
96(5):
1989 - 1993.
[Abstract]
[Full Text]
[PDF]
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C. M. Orschell-Traycoff, K. Hiatt, R. N. Dagher, S. Rice, M. C. Yoder, and E. F. Srour
Homing and engraftment potential of Sca-1+lin- cells fractionated on the basis of adhesion molecule expression and position in cell cycle
Blood,
August 15, 2000;
96(4):
1380 - 1387.
[Abstract]
[Full Text]
[PDF]
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K. Matsumoto, K. Yasui, N. Yamashita, Y. Horie, T. Yamada, Y. Tani, H. Shibata, and T. Nakano
In Vitro Proliferation Potential of AC133 Positive Cells in Peripheral Blood
Stem Cells,
May 1, 2000;
18(3):
196 - 203.
[Abstract]
[Full Text]
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R. Huss
Isolation of Primary and Immortalized CD34- Hematopoietic and Mesenchymal Stem Cells from Various Sources
Stem Cells,
January 1, 2000;
18(1):
1 - 9.
[Abstract]
[Full Text]
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M. A. Goodell
CD34+ or CD34-: Does it Really Matter?
Blood,
October 15, 1999;
94(8):
2545 - 2547.
[Full Text]
[PDF]
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D. S. Kaufman, E. T. Hanson, R. L. Lewis, R. Auerbach, and J. A. Thomson
Hematopoietic colony-forming cells derived from human embryonic stem cells
PNAS,
September 11, 2001;
98(19):
10716 - 10721.
[Abstract]
[Full Text]
[PDF]
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ABSTRACT
INTRODUCTION