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 Previous Article | Table of Contents | Next Article 
Blood, Vol. 92 No. 2 (July 15), 1998:
pp. 362-367
Evidence for Circulating Bone Marrow-Derived Endothelial Cells
By
Qun Shi,
Shahin Rafii,
Moses Hong-De Wu,
Errol S. Wijelath,
Cong Yu,
Atsushi Ishida,
Yuji Fujita,
Sudesh Kothari,
Robert Mohle,
Lester R. Sauvage,
Malcom A.S. Moore,
Rainer F. Storb, and
William
P. Hammond
From the Departments of Surgery and Molecular Biology, The Hope Heart
Institute and Providence Medical Center, Seattle, WA; the
Hematology-Oncology Division, Cornell Medical College, New York, NY;
the Fred Hutchinson Cancer Research Center, Seattle, WA; the
Sloan-Kettering Cancer Research Center, New York, NY; and the
Departments of Surgery and Medicine, University of Washington School of
Medicine, Seattle, WA.
 |
ABSTRACT |
It has been proposed that hematopoietic and endothelial cells are
derived from a common cell, the hemangioblast. In this study, we
demonstrate that a subset of CD34+ cells have the
capacity to differentiate into endothelial cells in vitro in the
presence of basic fibroblast growth factor, insulin-like growth
factor-1, and vascular endothelial growth factor. These differentiated
endothelial cells are CD34+, stain for von Willebrand
factor (vWF), and incorporate acetylated low-density lipoprotein
(LDL). This suggests the possible existence of a bone
marrow-derived precursor endothelial cell. To demonstrate this
phenomenon in vivo, we used a canine bone marrow transplantation model,
in which the marrow cells from the donor and recipient are genetically
distinct. Between 6 to 8 months after transplantation, a Dacron graft,
made impervious to prevent capillary ingrowth from the surrounding
perigraft tissue, was implanted in the descending thoracic aorta. After
12 weeks, the graft was retrieved, and cells with endothelial
morphology were identified by silver nitrate staining. Using the
di(CA)n and tetranucleotide (GAAA)n repeat polymorphisms to distinguish between the donor and recipient DNA, we
observed that only donor alleles were detected in DNA from positively
stained cells on the impervious Dacron graft. These results strongly
suggest that a subset of CD34+ cells localized in the
bone marrow can be mobilized to the peripheral circulation and can
colonize endothelial flow surfaces of vascular prostheses.
| |
INTRODUCTION |
VASCULOGENESIS is the in situ
differentiation of mesodermal precursors to angioblasts that
differentiate into endothelial cells to form the primitive capillary
network. Vasculogenesis is limited to early embryogenesis and is
believed not to occur in the adult, whereas angiogenesis, the sprouting
of new capillaries from pre-existing blood vessels, occurs in both the
developing embryo and postnatal life.1,2 The basic
mechanisms underlying vasculogenesis and angiogenesis are at present
unclear. Several growth factors, in particular vascular endothelial
growth factor (VEGF) and its receptor Flk-1, have been shown to be
critical for normal development of blood vessels.3-6 In an
attempt to prove that transmural angiogenesis is responsible for
endothelialization of Dacron grafts, we implanted in the canine
descending thoracic aorta a Dacron graft made impermeable by silicone
coating. Surprisingly, we demonstrated the presence of scattered
islands of endothelial cells without any evidence of transmural
angiogenesis.7 Our results are consistent with other
reports demonstrating the presence of circulating endothelial
cells.8-11 We have also recently shown that the neointima
formed on the surface of left ventricular assist devices is colonized
by CD34+ hematopoietic progenitor cells.12
These observations suggest that vasculogenesis may not be restricted
just to early embryogenesis, but may also have a physiological role in
adults. Our study raised several interesting questions. First, are the
endothelial cells derived from cells detached from the proximal
vascular wall upstream or do they originate from the circulation?
Second, if endothelial precursors circulate, are they related to
circulating bone marrow-derived progenitor cells? Recently, evidence
for the latter was presented by Asahara et al.13 They
showed that CD34+ cells derived from the peripheral
circulation form endothelial colonies, based on the ability of these
colonies to incorporate acetylated LDL, express PECAM and
Tie-2 receptor, and produce nitric oxide by VEGF stimulation. However,
no evidence that these cells express von Willebrand factor (vWF)
antigen or form homogenous endothelial monolayers was provided.
Circulating CD34+ myelomonocytic progenitors can
incorporate acetylated LDL and express PECAM and the VEGF receptor
(VEGFR-1, Flt-1).14-17 Therefore, it is conceivable that
nitric oxide production by these cells in response to VEGF could have
been mediated by hematopoietic Flt-1 rather than Flk-1. Nevertheless,
their study demonstrates the possibility of vasculogenesis in the
adult.
In this study, we used a canine bone marrow transplantation model in
which the donor and host DNA can clearly be distinguished by a
polymerase chain reaction (PCR)-based microsatellite assay to address
the question of whether endothelial cells lining a vascular prosthesis
can be derived from the marrow. In addition, we performed in vitro
studies in which we demonstrated that CD34+ derived from
bone marrow or the peripheral circulation could differentiate into
endothelial cells.
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MATERIALS AND METHODS |
Isolation and in vitro culture of human CD34+ cells.
Low-density mononuclear cells obtained from bone marrow, umbilical cord
blood (CB), 10- to 15-week fetal liver (FL), and granulocyte colony-stimulating factor (G-CSF)-mobilized peripheral blood (PB) were
obtained using Ficoll separation. Low-density mononuclear cells were
washed twice with 0.1% bovine serum albumin (BSA) in phosphate-buffered saline (PBS) and were resuspended to 1 × 108 cells/mL. A mouse IgG1 antihuman
CD34+ antibody developed by one of the authors (M.A.S.M.)
(11.1.6; licensed to Oncogene Science, Uniondale, NY) was added to the cells at a concentration of 50 µg/mL for 30 minutes at 4°C. The cells were washed twice with 0.1% BSA in PBS and resuspended to a
concentration of 1 × 108 cells/mL, and 30 µg/mL of
sheep antimouse IgG1 immunomagnetic beads (Dynal A.S.,
Oslo, Norway), providing a 16:1 bead-to-cell ratio, was added for 30 minutes at 4°C. The bead-positive fraction was selected with a
magnetic separator, resuspended in 20% fetal calf serum (FCS), and
kept overnight at 37°C in 100% humidified air with 5%
CO2. The following day, the cells in the bead-negative fraction were recovered. Flow cytometry of the purified cells showed
that 95% of the isolated cells were CD34+. Viability of
the cells was evaluated by Trypan Blue exclusion. Isolated
CD34+ cells were depleted of adherent cells by incubation
with fibronectin/gelatin-coated plastic dishes at 37°C for 24 hours
and removal of the nonadherent cells. This process was repeated three
times and the nonadherent CD34+ cells were then reseeded
onto fibronectin and gelatin-coated plastic dishes and cultured in 10%
fetal bovine serum (FBS) in M199 medium containing VEGF (10 ng/mL),
basic fibroblast growth factor (bFGF; 1 ng/mL), and insulin-like growth
factor-1 (IGF-1; 2 ng/mL). Colonies were stained for vWF
and acetylated LDL to identify endothelial cells.
Reverse transcriptase-PCR (RT-PCR).
First-strand cDNA was synthesized by RT of 200 ng total RNA isolated
from the purified CD34+ cells using guanidine thiocyanate
and amplified by Taq DNA polymerase dissolved in PCR buffer (KlenTaq;
CLONTECH) in a 50 µL reaction containing 0.2 mmol/L dNTPs and 40 pmol
of Flk-1 primers (sense, 5 CTGGCATGGTCTTCTGTGAAGCA-3;
antisense, 5 AATACCAGTGGATGTGATGCGG-3). The PCR profile
consisted of 1 minute of denaturing at 94°C, followed by 25 cycles
of 1 minute of denaturing at 94°C, 1 minute of annealing at
64°C, 2 minutes of extension at 72°C, and a final extension step of 10 minutes. The PCR product (20 µL) was separated by a 2%
agarose gel and stained with ethidium bromide to identify a 790-bp
product. Human umbilical vein endothelial cells and bone marrow
endothelial cells were used as positive controls.
Dogs and DLA typing.
Beagles, harriers, Walker hounds, and crossbred dogs were used in this
study. Dogs were either bred at the Fred Hutchinson Cancer Research
Center or purchased from Department of Agriculture licensed vendors
located in the states of Washington and Michigan. Dogs were immunized
against leptospirosis, distemper, hepatitis, and parvovirus; dewormed;
and observed for disease for at least 2 months before being entered on
study. Dogs weighed from 5.8 to 18.6 kg (median, 10 kg) and were 7 to
36 months old (median, 10 months old). The experimental protocols and
the facilities used were approved by the Fred Hutchinson Cancer
Research Center's Internal Animal Care and Use Committee per
guidelines stipulated in the Experimental Animal Welfare Act of 1985 administered through the National Institutes of Health. Recipients were
conditioned with 920 cGy total body irradiation from two opposing
60Co sources. Within 4 hours of irradiation, they received
an IV infusion of  4 × 108 marrow cells/kg followed on
days 1 and 2 by 6.3 to 19.6 × 108 donor nucleated
peripheral blood leukocytes/kg. To prevent graft-versus-host disease,
recipients received mycophenolate mofetil (10 mg/kg BID, SC) from day 0 to 28 and cyclosporine (10 mg/kg BID, IV) from day  1 to
35.18
Blood counts were monitored until recovery to preirradiation levels.
Six months after transplantation, the 6 dogs used for Dacron graft
implantation showed marrow and peripheral blood cells of donor origin
only as determined by standard cytogenetics and microsatellite markers.
Graft implantation.
Dacron grafts made impermeable by silicone coating were implanted into
the descending thoracic aortas of the 6 beagle dogs. The 12 cm,
3-component composite graft was constructed with 4-cm expanded
polytetrafluoroethylene at the ends to prevent host pannus migration to the central 4-cm Dacron graft, which was coated with silicone rubber to block perigraft tissue ingrowth. After 12 weeks, grafts were retrieved, rinsed with 5% dextrose, and silver nitrate stained (0.5% AgNO3) to help identify areas of endothelial
cells.9 Häutchens were then performed for
microsatellite analysis.19 Häutchens from grafts that
were not silver nitrate stained were obtained for vWF immunofluoresence
analysis (Fig 1). Additionally, to obtain
an understanding of the cellular structure underneath the endothelial
monolayer, areas close to where the Häutchens were performed on
silver nitrate stained grafts were fixed in resin and processed for
CD34 and hematoxylin and eosin staining.
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| Fig 1.
Differentiation of CD34+ hematopoietic
cells to endothelial cells. (a) Adherent endothelial colonies formed
after 15 to 20 days in culture incubation with VEGF/IGF/bFGF (original
magnification × 400). (b) Formation of endothelial monolayer after
continuous incubation with VEGF (original magnification × 600). (c)
Endothelial monolayers incorporating acetylated LDL (original
magnification × 600). (d) CD34+ differentiated cells
that stained positively for vWF antigen (original magnification × 600). (e) CD34-selected cells expressing Flk-1 mRNA. BMEC, bone marrow
endothelial cells; BM, bone marrow; CB, cord blood; PB, peripheral
blood; FL, fetal liver; HUVEC, human umbilical vein
endothelial cells.
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DNA extraction and microsatellite analysis.
We used a PCR-based microsatellite assay to detect polymorphism among
di-(CA)n and tetra-(GAAA)n to determine the
origin of the endothelial cells on the silver nitrate-stained
impervious Dacron grafts.20 DNA on Häutchens was
extracted and donor/recipient polymorphism was analyzed by PCR in a 50 µL reaction volume that contained High Fidelity Taq (3 U), 200 µmol/L dNTP, and 20 pmol of [ -32P]ATP end-labeled
primer and 20 pmol of the corresponding unlabeled primer. PCR was
performed under the following conditions: initial denaturing at
94°C for 3 minutes, followed by 35 cycles of denaturing at 92°C
for 1 minute, annealing at 55°C for 2 minutes, and extension at
72°C for 3 minutes. The final extension was performed at 72°C for 10 minutes. Five microliters of PCR reaction product was denatured in formamide buffer at 99°C for 3 minutes and loaded on a 4%
denaturing sequencing gel. The gels were exposed to Autoradiographic
films (Kodax XAR-5; Eastman Kodak, Rochester, NY)
overnight at 70°C.
| |
RESULTS |
Differentiation of hematopoietic CD34+ cells into
endothelial cells.
After 15 to 20 days in culture, adherent colonies of rapidly
proliferating endothelial cells were observed (Fig 1a). Continuous incubation of these colonies in the presence of VEGF (10 ng/mL) resulted in the proliferation of the colonies that eventually formed
cobblestone monolayers (Fig 1b). These monolayers could be passaged for
up to 30 times and, compared with freshly isolated human umbilical vein
endothelial cells, had 10 times more proliferative potential, as
measured by thymidine uptake (data not shown). These differentiated
cells had the capacity to incorporate acetylated LDL (Fig 1c) and
stained positively for vWF (Fig 1d).
Because VEGF is critical for endothelial cell development, we
investigated whether CD34+ cells isolated from different
sources expressed Flk-1. RT-PCR of total RNA extracted from selected
nonadherent CD34+ cell populations isolated from CB, bone
marrow, FL, and G-CSF-mobilized PB demonstrated the presence of Flk-1
mRNA (Fig 1e). As shown in Table 1,
CD34+ cells, when placed in culture, formed significant
numbers of vWF-positive colonies. Although CD34+ cells
derived from FL generated large numbers of endothelial colonies, it is
remarkable that G-CSF-mobilized CD34+ cells derived from
PB also did so. The presence of VEGF was critical for endothelial
differentiation in vitro (Table 1), even though bFGF and IGF-1 enhanced
endothelial colony formation. Thus, our findings suggest that the
CD34+ cell may behave like a circulating endothelial
progenitor cell.
Endothelialization of vascular prostheses by marrow-derived cells.
Figure 2a shows the sensitivity of the
PCR-based microsatellite assay. Mixtures of cells down to 1.0% in a
total of 2,000 cells could be detected as discrete bands.
Häutchen preparations (Fig 2b and c) identified nucleated cells
that were positive for vWF, indicating that the cells were endothelial.
DNA from this Häutchen was extracted and the genotype was
determined to be of donor origin (Fig 2d).
Figure 3a represents a silver
nitrate-stained graft showing typical polygonal-shaped endothelial
cells. The endothelial monolayer was stripped from this graft using the
Häutchen technique and DNA was extracted for PCR-microsatellite
analysis. As shown in Fig 3b, only DNA alleles corresponding to
the donor were detected. Immunostaining of the endothelial monolayer
with a polyclonal antibody to CD34 was positive (Fig 3c). Hematoxylin and eosin-stained sections taken from an area where the Häutchen was performed showed a single layer of endothelial cells on the flow
surface of the silicone-coated Dacron graft with hardly any nucleated
cells below the endothelial monolayer (Fig 3d).
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| Fig 2.
Detection of bone-marrow-derived endothelial cells on
vascular prostheses. (a) Sensitivity of the microsatellite assay.
(b and c) Double labeling with Hoechst and FITC anti-vWF. (d)
PCR analysis for (CA)n repeat polymorphism of DNA extracted
from (b).
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| Fig 3.
PCR genotyping for determination of origin of
silver-nitrate-stained endothelial cells. (a) Polygonal endothelial
cells identified on Dacron grafts after silver nitrate staining. (b)
PCR genotyping of silver nitrate-stained endothelial cells
demonstrating bone marrow origin. (c) Endothelial cells stained
positive for CD34 antigen. (d) Hematoxylin and eosin staining of silver
nitrate-stained section.
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| |
DISCUSSION |
To begin to analyze the potential role of circulating endothelial
progenitor cells capable of promoting endothelialization in vivo, we
performed in vitro studies focusing on the CD34+ progenitor
as a possible candidate for several reasons. First, CD34, a marker for
hematopoietic progenitor cells that give rise to all blood
cells,21 is also found on endothelial cells in the adult
and developing embryo.22-24 Second, it is believed that a
single progenitor cell, the hemangioblast, can give rise to both the
hematopoietic and vascular systems during embryogenesis, because common
antigens are found on both endothelial and hematopoietic cells.23,25,26 Third, tyrosine kinase receptors, such as
Tie, Tek, and Flk-1, that are specifically found on endothelial
cells27-29 are also expressed on the hematopoietic
CD34+ progenitor cell.30-32 Targeted disruption
of the gene encoding Flk-1 in mice resulted in failure to develop
endothelial cells, suggesting a critical role for Flk-1 in the early
stages of endothelial differentiation.5 Furthermore,
disruption of the VEGF gene resulted in defective development of
embryonic vasculature.3,4 Also, inactivation of the Tie and
Tek gene showed a critical role for these receptors in endothelial cell
development, although their function may be related to events further
downstream to Flk-1 and VEGF during embryonic
angiogenesis.32-34 In our in vitro studies, cultured
CD34+ cells in medium containing bFGF and VEGF
differentiated into endothelial cell colonies, as judged by
vWF-positive staining. There was an absolute requirement for VEGF in
endothelial colony formation, suggesting the presence of Flk-1 on CD34
is critical for this process, consistent with previous studies
demonstrating an essential role for Flk-1 in endothelial development.
We provided the following controls to demonstrate that the
CD34+ hematopoietic cells do indeed differentiate to
endothelial cells. First, vWF staining was not detectable in freshly
isolated CD34+ cells either by immunocytochemistry or flow
cytometry (data not shown). Second, only nonadherent CD34+
cells were obtained by culturing for 3 days on
fibronectin/collagen-coated plastic dishes to remove any mature
endothelial cells that are also CD34+ before the start of
any experiments. Third, cells from this nonadherent population were
negative for vWF just before culturing, again demonstrating lack of
endothelial cells at the start of the experiments. Together, these
controls make it extremely unlikely that the endothelial colonies
observed in our studies were due to contaminating endothelial cells.
The presence of circulating endothelial cells was demonstrated
initially in the 1960s by several investigators using Dacron grafts
placed in the pig, rabbit, and dogs.8,9 In a report from
1971, endothelial cells lining the coronary arteries of a transplanted
human heart were shown to be derived from the recipient and not the
donor,35 and more recently endothelial cells
have been shown to line a ventricular assist device.10
These findings suggest what we have termed fallout endothelialization
occurs in the human. More recently, evidence for fallout
endothelialization in the dog also was demonstrated.7,11
Although in these studies the results are all consistent with the
hypothesis that circulating endothelial precursor cells can form a
monolayer on a graft surface, the origin of these cells remained
unclear. The possible sources from which these cells could have been
derived are, first, mature endothelial cells detached from other areas
of the vascular wall; second, endothelial precursor cells in
circulation; or, third, endothelial precursors derived from the marrow.
The major objectives of this study, using a combined in vitro and in
vivo approach, were to attempt to establish the genetic origin of the
endothelial cells lining the impervious Dacron grafts and to identify
endothelial progenitor cells from the marrow cell population, focusing
in particular on the CD34+ hematopoietic progenitor cell.
We used a canine marrow transplant model and a PCR-based microsatellite
assay to determine the origin of the endothelial cells on an impervious
Dacron graft. Because the sensitivity of the polymorphism assay is such
that mixtures of cells down to 1% can be detected (Fig 1), one would
assume that, if the Häutchens contained host endothelial cells,
we would have consistently detected host DNA alleles, because the
Häutchens analyzed were taken from areas shown by silver nitrate
staining to have an extensive endothelial monolayer. The finding of a
pure donor genotype strongly suggests that the endothelial cells
derived from cells coming from the bone marrow.
Our experimental approach has allowed us to address the role of bone
marrow derived endothelial cells in promoting endothelial monolayer
formation in vivo. Our data confirm predictions based on previous in
vivo studies and in vitro studies of CD34+ hematopoietic
cells described herein. These data provide evidence that vasculogenesis
is not only restricted to early embryogenesis, but may play a
physiological role as demonstrated in this study, or may contribute to
the pathology of vascular diseases in adults. Formal proof of our
hypothesis awaits the development of a double-labeling method to detect
genetic origin and endothelial phenotype in a single cell on a Dacron
graft implanted in a marrow-transplanted dog.
| |
FOOTNOTES |
Submitted November 12, 1997;
accepted April 21, 1998.
Q.S. and S.R. contributed equally to this study.
Supported in part by National Institutes of Health (NIH) Grants No.
HL36444, DK42716, and CA15704. S.R. was supported by the American Heart
Association, by a Grant-In-Aid, and by NIH RO1 HL58707-01.
Address reprint requests to William P. Hammond, MD, President and
Medical Director, The Hope Heart Institute, 528 18th Ave, Seattle, WA
98122; e-mail: bhammond{at}PMCprov.org.
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be hereby marked "advertisement" is accordance with 18 U.S.C. section 1734 solely to indicate this fact.
| |
ACKNOWLEDGMENT |
The authors thank C.R. Bard, Inc and W.L. Gore, Inc for donation of the
vascular graft material. We appreciate the assistance of Dorothy Mungin
and Karen Englehart, Histologists; Warren Berry, Medical Photographer;
Mary Ann Sedgwick Harvey, Medical Editor; and Mary-Ann Nelson, Medical
Illustrator.
| |
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Abstract
Introduction
Abstract